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Women and Exercise:

Physiology and Sports Medicine


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Women and Exercise:
Physiology and Sports Medicine
2nd Edition

MONA M. SHANGOLD, M.D.


Professor of Obstetrics and Gynecology
Director, Division of Reproductive Endocrinology
Director of the Sports Gynecology and Women's Life Cycle Center
Hahnemann University
Philadelphia, Pennsylvania

GABE MIRKIN, M.D.


Associate Clinical Professor
Georgetown University School of Medicine
Washington, D.C.

F. A. DAVIS COMPANY • Philadelphia


F. A. Davis Company
1915 Arch Street
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Copyright © 1994 by F. A. Davis Company

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As new scientific information becomes available through basic and clinical research, recommended treatments and
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Library of Congress Cataloging-in-Publication Data

Women and exercise : physiology and sports medicine / [edited by] Mona
M. Shangold, Gabe Mirkin.—Ed. 2.
p. cm.
Includes bibliographical references and index.
ISBN 0-8036-7817-7
1. Women athletes—Physiology. 2. Exercise for women-
-Physiological aspects. 3. Sports for women—Physiological aspects.
4. Sports medicine. I. Shangold, Mona M. II. Mirkin, Gabe.
[DNLM: 1. Physical Fitness. 2. Sports. 3. Sports Medicine.
4. Women. 5. Exercise. QT260 W8715 1993]
RC1218.W65W65 1993
613.7'11'082—dc20
DNLM/DLC 93-17937
for Library of Congress CIP

Authorization to photocopy items for internal and personal use, or the internal or personal use of specific clients,
is granted by F.A. Davis Company for users registered with the Copyright Clearance Center (CCC) Transactional
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For those organizations that have been granted a photocopy license by CCC, a separate system of payment has
been arranged. The fee code for users of the Transactional Reporting Service is: 8036-7817/7 0 + $.10.
To Kenneth,
Our greatest treasure
and
Our greatest joy
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Preface to the Second Edition

The success and warm reception of the first edition and the many advances
in this field have led to the development of this second edition, in which all ma-
terial has been updated and expanded. Much has happened since the publication
of the first edition: Women athletes have set many new records; researchers have
devoted increased attention to the consequences of exercise for women; clini-
cians have devoted greater attention to the needs and concerns of exercising
women; and increasing numbers of female couch potatoes have acknowledged
that exercise is beneficial and desirable.
The contributors remain accepted authorities and leaders in their fields. The
same blend of basic and clinical science is presented, providing comprehensive
coverage for both researchers and clinicians. Those caring for athletic women
have shared their vast experience in a valuable composite of science and art. We
believe this edition is even better than the first, and we hope it will surpass the
first edition in providing satisfaction and inspiration.

Mona Shangold, M.D.


Gabe Mirkin, M.D.

vii
Preface to the First Edition

We have prepared this book to assist physicians and other health care pro-
fessionals in caring for women who exercise. Included are chapters covering the
many fields necessary to provide comprehensive care to women who range from
novice exercisers to elite athletes and who may require information about train-
ing, health maintenance, treatment of disease or injury, and rehabilitation. Chap-
ters have been written by leading authorities in each of these fields to supply the
necessary depth of scientific background and clinical experience. In each case,
relevant basic science is explained, and pertinent literature is reviewed and in-
terpreted. When sufficient data are present, most authors have outlined and jus-
tified their personal recommendations, based on these data. Because clinical
medicine often requires action even when sufficient data are lacking or inconclu-
sive, many contributors have outlined their advice for these situations, based on
their own expertise and clinical experience. We believe readers will find these
recommendations invaluable.
Contributors to this volume include both basic scientists and practicing
physicians. We purposely have encouraged some basic scientists and clinicians
to cover the same topics from their different perspectives. We feel that this ap-
proach adds greatly to the value of this book.
Although elementary textbooks must oversimplify in order to teach stu-
dents, this book is aimed at scientists and educators, who appreciate that re-
search may, at times, lead to conflicting conclusions and different recommen-
dations based upon these conclusions. We are confident that the sophisticated
reader will find the controversy generated by these different perspectives re-
freshing, stimulating, and representative of the state of the art in this field.
No other book to date has covered so many relevant topics dealing with ex-
ercise and sports medicine for women in the depth that is provided in this vol-
ume. We hope this volume meets the needs of generalists caring for women ath-
letes and specialists wanting information outside of their own specialty. Above
all, we hope it will enable exercising women to receive the best care possible.

Mona Shangold, M.D.


Gabe Mirkin, M.D.

viii
Contributors

Oded Bar-Or, M.D


Professor of Pediatrics Associate Professor of Medicine
Director, Children's Exercise and Nutrition Harvard Medical School
Centre Boston, Massachusetts
McMaster University
Hamilton, Ontario, Canada Thomas D. Fahey, Ed.D.
Professor of Physical Education
Kelly D. Brownell, Ph.D. California State University
Professor of Psychology Chico, California
Professor of Epidemiology and Public
Health Catherine Gilligan, B.A.
Co-Director, Yale Center for Eating and Associate Researcher
Weight Disorders Biogerontology Laboratory
Yale University University of Wisconsin
New Haven, Connecticut Madison, Wisconsin
LethaY. Griffin, M.D., Ph.D.
Marshall W. Carpenter, M.D. Staff Physician,
Associate Professor, Obstetrics and Peachtree Orthopaedic Clinic
Gynecology Team Physician,
Brown University Georgie State University
Director of Maternal-Fetal Medicine Atlanta, Georgia
Department of Obstetrics and Gynecology
Women and Infants Hospital of Rhode Carlos M. Grilo, Ph.D.
Island Director of Psychology
Providence, Rhode Island Yale Psychiatric Institute
Assistant Professor in
David H. Clarke, Ph.D. Psychiatry
Chair, Department of Kinesiology Yale University School of Medicine
University of Maryland New Haven, Connecticut
College Park, Maryland
Christine Haycock, M.D.
Pamela S. Douglas, M.D. Professor Emeritus
Director of Nonlnvasive Cardiology UMDNJ, New Jersey Medical School
Beth Israel Hospital Newark, New Jersey
Ix
X Contributors

Jack L. Katz, M.D. Department of Orthopaedic Surgery


Professor of Clinical Psychiatry Memphis, Tennessee
Cornell University Medical College
New York, New York Mona M. Shangold, M.D.
Chairman, Department of Psychiatry Professor of Obstetrics and Gynecology
North Shore University Hospital Director, Division of Reproductive
Manhasset, New York Endocrinology
Director of the Sports Gynecology and
Robert M. Malina, Ph.D. Women's Life Cycle Center
Professor Hahnemann University
Departments of Kinesiology and Health Philadelphia, Pennsylvania
Education and of Anthropology
University of Texas Arthur J. Siegel, M.D.
Austin, Texas Assistant Professor of Medicine
Harvard Medical School
Gabe Mirkin, M.D. Chief, Internal Medicine Department
Associate Clinical Professor McLean Hospital
Georgetown University School of Medicine Belmont, Massachusetts
Washington, D.C.
Everett L. Smith, Ph.D.
Director, Biogerontology Laboratory
Morris Notelovitz, M.D., Ph.D.
Department of Preventive Medicine
President and Medical Director University of Wisconsin
Women's Medical and Diagnostic Center Madison, Wisconsin
The Climacteric Clinic, Inc. and
Midlife Centers of America, Inc. Denise E. Wilfley, Ph.D.
Gainesville, Florida
Research Scientist and Lecturer
Clinical Director Department of Psychology
Mary L. OToole, Ph.D. Yale Center for Eating and Weight
Associate Professor Disorders
Director, Human Performance Laboratory Yale University
University of Tennessee-Campbell Clinic New Haven, Connecticut
Contents

PARTI
BASIC CONCEPTS OF EXERCISE PHYSIOLOGY 1

1. Fitness: Definition and Development 3


Mary L. O'Toole, Ph.D., and Pamela S. Douglas, M.D.
Components of Fitness 4
Muscular Strength and Endurance 4
Body Composition 4
Flexibility 4
Cardiovascular-Respiratory Capacity 4
Benefits of Fitness 5
For Healthy Individuals 5
Medical Implications 6
Fitness Evaluation 8
Muscular Strength and Endurance 8
Body Composition 9
Flexibility 9
Functional Capacity 9
Fitness Development and Maintenance 14
Fitness Development 14
Fitness Maintenance 16
Factors Affecting Fitness Development and Maintenance 17
Training for Competition 19
Interval Training 19
Cross Training 20

2. Exercise and Regulation of Body Weight 27


Denise E. Wilfley, Ph.D., Carlos M. Grilo, Ph.D., and Kelly D. Brownell, Ph.D.
The Nature and Severity of Weight Disorders 28
The Association Between Physical Activity and Weight 31
Exercise and Weight Control 32
Likely Mechanisms Linking Exercise and Weight Control 33
Energy Expenditure 34
xi
Xll Contents

Appetite and Hunger 36


Body Composition 37
Physical Activity and Health 37
Psychologic Changes 38
The Challenge of Adherence 39
Adherence and the Demographics of Obesity 39
Obstacles to Exercise for the Overweight Individual 39
Adherence Studies 40
Program Recommendations 43
Avoid a Threshold Mentality 43
Consistency May be More Important than the Type or Amount of Exercise ... 44
Provide Thorough Education 45
Be Sensitive to the Special Needs of Overweight Persons 45
Special Issues 45
The Role of Exercise in the Search for the Perfect Body 45
Ideal Versus Healthy Versus Reasonable Weight 45
Exercise Overuse (Abuse) 47

3. Training for Strength 60


David H. Clarke, Ph.D.
Definition of Strength 60
Isotonic Training 61
Isometric Training 63
Isotonic Versus Isometric Traning 64
Eccentric Training 65
Isokinetic Exercise 67
Hypertrophy of Skeletal Muscle 68
Aging and Strength Development 69

4. Endurance Training 73
Thomas D. Fahey, Ed.D.
Factors that Determine Success in Endurance Events 73
Maximal Oxygen Consumption 74
Mitochondrial Density 77
Performance Efficiency 78
Body Composition 79
Sex Differences in Endurance Performance 80
Training for Endurance 82
Components of Overload 83
Principles of Training 84

5. Bone Concerns 89
Everett L. Smith, Ph.D.
Catherine Gilligan, B.A.
Incidence and Cost of Osteoporosis 90
Effects of Calcium Intake 91
Mechanism of Exercise Benefits 93
Effects of Inactivity 94
Effects of Exercise 96
Athletic Amenorrhea and Bone 97
Problems in Studying Exercise Effects 98
Contents Xiii

6. Nutrition for Sports 102


Gabe Mirkin, M.D.
Nutrients 103
Carbohydrates 103
Proteins 103
Fats 105
Energy Storage 105
Comparing Women and Men 106
Endurance 106
"Hitting the Wall": Depletion of Muscle Glycogen 106
"Bonking": Depletion of Liver Glycogen 107
Increasing Endurance 107
Training to Increase Endurance 107
Utilizing Fat Instead of Glycogen 107
Diet and Endurance 108
Food Intake During the Week Before Competition 108
Eating the Night Before Competition 109
Eating the Meal Before Competition 109
Eating Before Exercising 110
Eating During Competition 110
Drinking Before Competition 1ll
Drinking During Competition Ill
Dehydration and "Heat Cramps" Ill
Women May Need Less Fluid Than Men 112
When to Drink 112
What to Drink 112
Cold or Warm? 113
Eating and Drinking After Competition 113
Protein Requirements 113
Vitamins 114
Mechanism of Function 114
Vitamin Needs of Female Athletes 115
Vitamin C and Colds 115
Vitamins and Birth Control Pills 115
Vitamins and Premenstrual Syndrome 116
Minerals 116
Iron 116
Calcium 117
Sodium 118
Potassium 118
Trace Minerals 119
The Athlete's Diet 119

PART II
DEVELOPMENTAL PHASES 127

7. The Prepubescent Female 129


Oded Bar-Or, M.D.
Physiologic Response to Short-Term Exercise 130
Submaximal Oxygen Uptake 130
Maximal Aerobic Power 131
XlV Contents

Anaerobic Power and Muscle Endurance 131


Muscle Strength 132
Trainability 132
Thermoregulatory Capacity 133
Response to Hot Climate 133
Response to Cold Climate 134
High-Risk Groups for Heat- or Cold-Related Disorders 135
Growth, Pubertal Changes, and Athletic Training 135
Coeducational Participation in Contact and Collision Sports 137

8. Growth, Performance, Activity, and Training During Adolescence 141


Robert M. Molina, Ph.D.
The Adolescent Growth Spurt 142
Body Size 142
Body Composition 142
Menarche 142
Physical Performance and Activity During Adolescence 143
Strength 143
Motor Performance 144
Maximal Aerobic Power 144
Physical Activity Habits 145
Significance of the Adolescent Plateau in Performance 145
Influence of Training on the Tempo of Growth and Maturation During
Adolescence 146
Stature and Body Composition 146
Sexual Maturation 147
Hormonal Responses 148
Fatness and Menarche 149
Other Maturity Indicators 149
Overtraining 149

9. Menstruation and Menstrual Disorders 152


Mono M. Shangold, M.D.
Prevalence of Menstrual Dysfunction Among Athletes 152
Review of Menstrual Physiology 154
Types of Menstrual Dysfunction 154
Menstrual Cycle Changes with Exercise and Training 156
Weight Loss and Thinness 156
Physical and Emotional Stress 157
Dietary Factors 157
Hormonal Changes with Exercise and Training 159
Acute Hormone Alterations with Exercise 159
Chronic Hormone Alterations with Training 159
Consequences of Menstrual Dysfunction 162
Luteal Phase Deficiency 162
Anovulatory Oligomenorrhea 162
Hypoestrogenic Amenorrhea 163
Diagnostic Evaluation of Menstrual Dysfunction in Athletes 165
Treatment of Menstrual Dysfunction in Athletes 166
Evaluation and Treatment of Primary Amenorrhea 168
Contents XV

10. Pregnancy 172


Marshall W. Carpenter, M.D.
Physiologic Changes of Pregnancy 173
Acute Physiologic Response to Exertion in the Nonpregnant State 173
Acute Metabolic Response to Exertion 174
Effect of Pregnancy on the Acute Physiologic Response to Exertion 175
Effect of Pregnancy on the Acute Metabolic Response to Exertion 176
Maternal Thermoregulation During Exercise 177
Acute Effects of Maternal Exertion on the Fetus 178
Maternal Exercise Training Effects on Fetal Growth and Perinatal Outcome . . . . 179
Recommendations About Recreational Exercise 180

11. Menopause 187


Morris Notelovitz, M.D., Ph.D., and Mono M. Shangold, M.D.
Menopause in Perspective 187
Osteoporosis and Bone Health 189
Osteogenesis: A Brief Overview 189
Exercise and Osteogenesis: Clinical Research 192
Atherogenic Disease and Cardiorespiratory Fitness 196
Lipids, Lipoproteins, and Exercise 196
Aerobic Power 198
Muscle Tissue and Strength 202
Age-Related Loss of Muscle Tissue and Strength 202
Strength Training 205
Other Menopausal Problems: Vasomotor Symptoms 205
Other Age-Related Changes 205
Exercise and Adipose Tissue 205
Exercise and Osteoarthrosis 206
Exercise and Well-Being 206

PART III
SPECIAL ISSUES AND CONCERNS 215
12. The Breast 217
Christine E. Haycock, M.D.
Breast Support 217
Nipple Injury 219
Trauma 219
Breast Augmentation and Reduction 219
Pregnancy and Lactation 220
Premenstrual Changes and Fibrocystic Breasts 220
Exercise Following Trauma or Surgery 221

13. Gynecologic Concerns in Exercise and Training 223


Mono M. Shangold, M.D.
Contraception 223
Oral Contraceptives 224
Intrauterine Devices (lUDs) 225
Mechanical (Barrier) Methods 225
XVi Contents

Norplant 225
Choosing a Contraceptive 226
Dysmenorrhea 226
Endometriosis 227
Premenstrual Syndrome 227
Fertility 229
Stress Urinary Incontinence 229
Postoperative Training and Recovery 230
Effect of Menstrual Cycle on Performance 231

14. Orthopedic Concerns 234


Letha Y. Griffin, M.D., Ph.D.
Patella Pain 235
Anatomy of the Patella 235
Sources of Pain 236
Evaluating Patella Pain 238
Acute Traumatic Patella Dislocation 242
Patella Subluxation 245
Patellofemoral Stress Syndrome 247
Patella Plica 249
Patella Pain: Summary 249
Impingement Syndromes 249
Ankle Impingement 250
Wrist Impingement 250
Shoulder Impingement 251
Other Common Conditions 253
Achilles Tendinitis 253
Shin Splints 254
Stress Fractures 255
Low Back Pain 256
Bunions 257
Morton's Neuroma 258

15. Medical Conditions Arising During Sports 261


Arthur J. Siegel, M.D.
The Physiology of Athletes 262
Cardiac Changes with Exercise and Training: Risks and Benefits 263
Primary and Secondary Prevention of Heart Disease Through Exercise 263
Exercise and Cancer Risk 264
Hazards of Exercise 264
Heat Stress 264
Hematologic Effects: Iron Status and Anemia 267
"Runner's Diarrhea" 269
Effects on the Urinary Tract 269
Exercise-Induced Asthma 270
Exercise-Induced Anaphylaxis 272
Exercise-Induced Urticaria 273
Pseudosyndromes in Athletes 273
Pseudoanemia ("Runner's Anemia") 273
"Athletic Pseudonephritis" 273
Contents xvii

Serum Enzyme Abnormalities: Muscle Injury and Pseudohepatitis 274


Pseudomyocarditis 274
Screening the Athlete for Medical Clearance 275
Caution: When Not to Exercise 275

16. Cardiovascular Issues 282


Pamela S. Douglas, M.D.
Aerobic Capacity 282
Cardiac Function in Response to Exercise 283
Exercise Electrocardiographic Testing 286
Exercise Limitations in Heart Disease 287
Mitral Valve Prolapse 287
Anorexia Nervosa 288
Sudden Death 288
Other Forms of Heart Disease 289

17. Eating Disorders 292


Jack L Katz, M.D.
Epidemiology 293
Setting and Onset 293
Anorexia Nervosa 293
Bulimia Nervosa 294
Clinical Features 295
Anorexia Nervosa 295
Bulimia Nervosa 297
Biology of Eating Disorders 298
Physical Sequelae 298
Laboratory Findings 299
Endocrine Abnormalities: Hypothalamic Implications 300
Diagnosis, Course, and Prognosis of the Eating Disorders 301
Co-Morbidity 302
Theories of Etiology 303
Treatment 305
Exercise and Eating Disorders 307
Eating Disorders and Other Special Subcultures 309

APPENDIX A 313

Exercise Following Injury, Surgery, or Infection 313

INDEX 319
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I

Basic Concepts
of Exercise
Physiology
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CHAPTER 1

Fitness: Definition
and Development
MARY L. OTOOLE, Ph.D., and PAMELA S. DOUGLAS, M.D.

COMPONENTS OF FITNESS Flexibility


Muscular Strength and Endurance Functional Capacity
Body Composition
FITNESS DEVELOPMENT AND
Flexibility
MAINTENANCE
Cardiovascular-Respiratory Capacity
Fitness Development
BENEFITS OF FITNESS Fitness Maintenance
For Healthy Individuals Factors Affecting Fitness
Medical Implications Development and Maintenance
FITNESS EVALUATION TRAINING FOR COMPETITION
Muscular Strength and Endurance Interval Training
Body Composition Cross Training

T he term "physical fitness" connotes a state of optimal physical well-being.


However, a universally accepted definition of physical fitness is difficult to find.
Cureton,1 a pioneer in the fitness movement, defined it as "the ability to handle
the body well and the capacity to work hard over a long period of time without
diminished efficiency." Others have used physical fitness to describe a quality of
life rather than a precise set of conditions. For example, in monographs pub-
lished by the President's Council on Physical Fitness2,3 to offer guidance to those
interested in improving their physical fitness, a physically fit individual is
described as one able to perform vigorous work without undue fatigue and still
have enough energy left for enjoying hobbies and recreational activities, as well
as for meeting emergencies. Exercise physiology texts4-8 have similar descrip-
tive rather than quantitative definitions of physical fitness. For example, Lamb6
defines it as "the capacity to meet successfully the present and potential physical
challenges of life." So, despite all the interest generated by physical fitness, a
need remains for a clear definition of fitness to allow accurate assessment of an
individual's level of fitness.
The most successful definitions used to quantify "fitness" have been based
on its measurable components. Muscular strength and endurance, body com-
3
4 Basic Concepts of Exercise Physiology

position, flexibility, and cardiovascular-res- their muscles for strength and endurance
piratory capacity are generally agreed upon performance is similar to that of men. The
as the major components of physical fit- topics of muscular strength and endurance
ness.9 Therefore, for the purposes of this are covered in detail in Chapters 3 and 4.
text, an operational measure of fitness based
on combined capabilities in these four com-
ponents will be assumed to quantify an indi- Body Composition
vidual's level of physical fitness. Body composition makes an important
A further problem in evaluating fitness contribution to an individual's level of phys-
is the wide variation in individual need for ical fitness. Performance, particularly in ac-
physical work capacity. For example, an tivities that require one to carry one's body
adult who wishes to enjoy optimal health weight over distance, will be facilitated by a
must maintain a certain degree of physical large proportion of active tissue (muscle) in
fitness, while a competitive ultraendurance relation to a small proportion of inactive tis-
athlete needs to maintain a greater capacity sue (fat).14 In general, women have a greater
for physical work. Therefore, the adequacy percentage of fat than do men, whether
of one's physical fitness cannot be judged trained or untrained. Therefore, when per-
simply by the attainment of some magic forming a weight-bearing activity such as
number. However, normative values for the distance running, women tend to be at a dis-
parameters of muscular strength and endur-
advantage compared with their male coun-
ance, body composition, flexibility, and car- terparts. The role of exercise in reaching
diovascular-respiratory capacity have been and maintaining a desirable weight and per-
developed based on age, gender, and habit- centage of body fat is discussed at length in
ual activity level.10-12 An interested individ- Chapter 2.
ual can compare her own values to the
appropriate (based on desired activity
level) normative values to assess the ade- Flexibility
quacy of her "fitness level."
Flexibility is the degree to which body
segments can move or be moved around a
COMPONENTS OF FITNESS joint. 56 The flexibility, or range of motion
around a particular joint, is determined by
Muscular Strength and the configuration of bony structures and the
Endurance length and elasticity of ligaments, tendons,
Muscular strength refers to the force or and muscles surrounding the joint.5,6 Al-
tension that can be generated by a muscle or though there are no research data to sup-
muscle group during one maximal effort.5,6,9 port the concept that flexibility aids in co-
Muscular endurance is the ability to perform ordinated movements, it certainly makes
many repetitions at submaximal loads.5,6,13 sense that by allowing free movement with-
For example, it takes a certain amount of out unnecessary restriction, the body's effi-
strength to lift and swing a tennis racquet, ciency and grace would be increased and
but it takes muscular endurance to repeat the potential for injury reduced.15
that swing hundreds of times during the
course of a 2-hour match. An individual may Cardiovascular- Respiratory
have a great deal of strength but little endur- Capacity
ance, or may have extraordinary strength in
one muscle group but not in others. Al- The cardiovascular-respiratory compo-
though women usually have a smaller mus- nent of fitness reflects the integrity of the
cle fiber area and, therefore, lower absolute heart and lungs as well as the ability of the
strength levels than men, the trainability of muscle cells to use oxygen as fuel. It there-
Fitness: Definition and Development 5

fore reflects the degree to which an individ- aged women and men responded to the ex-
ual can increase metabolism above resting ercise training program in a similar fashion,
levels.4 6,8,9 Incremental tests up to maximal with a 21% increase in aerobic capacity and
oxygen uptake (Vo2 max) are used to mea- a 6% decrease in submaximal heart rates
sure this component and to define the limits during posttraining exercise tests.
of physical work capacity. This measure- There have also been suggestions that ex-
ment is considered to be the best single ercise may affect longevity, or that a "rever-
measure of an individual's overall functional sal of aging" may occur. A number of epide-
capacity.16 This and other measures of fit- miologic studies have attempted to examine
ness will be discussed below. the long-term effects of exercise upon lon-
gevity. Although no study has yet demon-
strated a negative effect, in general such
studies may have limited applicability be-
BENEFITS OF FITNESS cause of the many methodologic problems
inherent in choosing subject populations for
this type of study. From the viewpoint of this
Regular physical activity, resulting in fit- text, of primary importance is the fact that
ness, has benefits to disease-free individu- few have examined female populations.
als as well as implications for the medical Other limitations include the inclusion of
care of individuals with certain dis- ex-athletes who may have had intense ex-
eases.4'1"82°-23,25-28 There is general agree- ercise training for short periods of time;
ment that exercise performed by healthy in- classification of activity level based on
dividuals has both physical and psychologic workplace activity; and the interaction of a
benefits, including improved physical per- number of covariables such as obesity,
formance and enhanced quality of life. In smoking, environment, other life habits, and
contrast, although exercise clearly does not importantly, concomitant medical diseases.
change the course of most diseases, there Exercise training, however, has been well
are certain medical implications that are im- documented to modify or retard aspects of
portant. the aging process.20,21 Exercise training
slows the normal age-related declines in
For Healthy Individuals peak performance and maximal aerobic ca-
pacity, and it retards the loss of muscle and
Physical Benefits
bone mass and the increase in body fat. The
In reviewing the physiologic aspects of ex- exercising older woman has an aerobic
ercise in women, Drinkwater17 cites numer- capacity and body composition similar
ous studies that support the hypothesis that to those of much younger, sedentary
women of all ages benefit from programs women.22,23 It has been suggested that the
of physical conditioning. The observed rate of decline in many physiologic param-
changes in the women are similar to those in eters may be reduced by approximately 50%
men and include increases in maximal aer- in physically fit as compared with sedentary
obic capacity, maximal minute ventilation, women.24
02 pulse, and increases in submaximal work
performance.18,19 With training, one can per-
form the same amount of work with lower Psychologic Benefits
heart and respiratory rates and with a lower Although subjective parameters are ex-
systolic blood pressure. Some studies show traordinarily difficult to measure, and a
that beneficial effects occur after as little as small number of participants may note a
4 weeks of training.17 Improvements re- negative effect of exercise, it is generally
ported by Getchell and Moore27 are typical thought that fitness leads to an improved
of the expected responses; that is, middle- quality of life. In several studies, the major-
6 Basic Concepts of Exercise Physiology

ity of participants in an exercise program duced or, less often, an unchanged risk
noted an enhancement of mood, self-confi- associated with higher levels of physical ac-
dence, and feelings of satisfaction, achieve- tivity.29,31-36 Unfortunately, methodologic
ment, and self-sufficiency.25-28 Interestingly, problems similar to those inherent in stud-
in one study, those with the greatest im- ies of longevity also limit the applicability of
provement in endurance also had a more many of these studies to women. One pro-
marked improvement on psychologic test- spective study that did include 3120 women
ing.25 In general, women who exercise regu- reported a decrease in both all-cause and
larly are more likely to be more comfortable cardiovascular disease mortality rates in
with day-to-day physical exertion and to physically fit versus inactive women.30
have reduced anxiety and an improved body The amount of activity necessary to re-
image.26-28 duce cardiovascular risk is similarly un-
clear. It appears that no amount of exercise
will lower the incidence of cardiovascular
Medical Implications disease in those at especially high risk.
Women with medical illnesses may have a However, in women at "usual" risk, it is
lower level of fitness than their counterparts likely that, as with men, moderate amounts
in a comparable but healthy, sedentary pop- of exercise are protective, with benefit ac-
ulation. Although this may be due to limita- cruing to those expending 200 to 500 kcal/d
tions imposed by either the primary or an or 2000 kcal/wk pursuing vigorous activity.
associated illness, it may also be related to No studies have yet been performed to doc-
the adoption of a less active lifestyle. In the ument this effect in women.37-39 Although
latter case, increased fitness through partic- most studies have examined the effects of
ipation in regular exercise programs en- aerobic exercise, studies have shown that
courages the patient to increase her level of cardiovascular endurance may be increased
activity in daily life and in recreation, thus by resistive exercise as well.40
yielding at least a subjective improvement in The mechanisms by which exercise may
health. improve cardiovascular health are unclear.
Fitness or exercise training may have sal- Certainly, training enhances cardiac effi-
utary effects upon specific medical disease ciency, allowing a given work rate to be
in three ways: (1) as primary prevention achieved at a lower heart rate and blood
(e.g., in modifying factors known to increase pressure level. This is equally true in the
the risk of acquiring heart disease); (2) as healthy individual and in a patient with
secondary prevention or modification of the known coronary disease. Table 1-1 groups
natural history of a disorder (e.g., decreases these and other physiologic changes occur-
in both systolic and diastolic resting blood ring in the cardiovascular system with ex-
pressures); and (3) for rehabilitation or pal- ercise according to the method by which
liation of a specific disorder. The last is they might prevent coronary heart disease,
more closely related to task-specific exer- additionally noting the likelihood of each
cise and is beyond our consideration of the adaptation of being an important factor in
benefits of overall fitness. prevention.41 The beneficial effects of exer-
cise are likely multifactorial, and the mech-
Cardiovascular Disease
anisms are still unclear.
Exercise may also affect cardiovascular
Coronary Artery Disease. Although cor- disease by altering risk factors for its devel-
onary artery disease is more common in opment. In healthy women, higher levels of
men, it is the leading cause of death in fitness, as determined by exercise duration
women as well. Studies examining the ef- on treadmill testing, have been associated
fects of fitness upon the risk of developing with lower body weight, a lower percentage
coronary artery disease find either a re- of body fat, lower incidence of cigarette
Fitness: Definition and Development 7

Table 1-1. BIOLOGIC MECHANISMS BY WHICH EXERCISE MAY CONTRIBUTE TO THE


PRIMARY OR SECONDARY PREVENTION OF CORONARY HEART DISEASE*

Maintain or increase myocardial oxygen supply


Delay progression of coronary atherosclerosis (possible).
Improve lipoprotein profile (increase HDL-C/LDL-C ratio) (probable).
Improve carbohydrate metabolism (increase insulin sensitivity) (probable).
Decrease platelet aggregation and increase fibrinolysis (probable).
Decrease adiposity (usually).
Increase coronary collateral vascularization (unlikely).
Increase coronary blood flow (myocardial perfusion) or distribution (unlikely).
Decrease myocardial work and oxygen demand
Decrease heart rate at rest and submaximal exercise (usually).
Decrease systolic and mean systemic arterial pressure during submaximal exercise (usually) and at rest
(possible).
Decrease cardiac output during submaximal exercise (probable).
Decrease circulating plasma catecholamine levels (decrease sympathetic tone) at rest (probable) and at
submaximal exercise (usually).
Increase myocardial function
Increase stroke volume at rest and in submaximal and maximal exercise (likely).
Increase ejection fraction at rest and in exercise (possible).
Increase intrinsic myocardial contractility (unlikely).
Increase myocardial function resulting from decreased "afterload" (probable).
Increase myocardial hypertrophy (probable); but this may not reduce CHD risk.
Increase electrical stability of myocardium
Decrease regional ischemia at rest or at submaximal exercise (possible).
Decrease catecholamines in myocardium at rest and at submaximal exercise (probable).
Increase ventricular fibrillation threshold due to reduction in cyclic AMP (possible).
'Expression of likelihood that effect will occur for an individual participating in endurance-type training program
for 16 wk or longer at 65-80% of functional capacity for 25 min or longer per session (300 kcal) for 3 or more
sessions per week ranges from unlikely, possible, likely, probable, to usually.
Abbreviations: HDL-C = high-density lipoprotein cholesterol; LDL-C = low-density lipoprotein cholesterol; CHD =
coronary heart disease; AMP = adenosine monophosphate.
Source: Haskell,41 p. 65, with permission.

smoking, lower systolic and diastolic blood tion of preexisting coronary disease are
pressures, lower total cholesterol with a much less clear. At least one well-controlled
higher high-density lipoprotein (HDL) study in men with heart disease showed a
subtraction, lower triglycerides, and, most modest decrease in deaths due to myocar-
importantly, a lower incidence of cardiovas- dial infarction, with a trend toward a reduc-
cular disease and lower mortality rate.42 tion in deaths from all causes in individuals
Using multiple regression analysis, Gibbons pursuing exercise programs.45 Although car-
and colleagues42 demonstrated independent diac patients are generally encouraged to
associations between fitness level and lipid avoid resistive exercise because of the re-
profiles, blood pressure, and smoking, sug- sultant unfavorable cardiac-loading condi-
gesting that risk factors for coronary heart tions, some successfully used forms of
disease may be modified by fitness level. exercise (e.g., rowing, bicycling) have sig-
Other studies have partly confirmed these nificant resistive as well as aerobic compo-
results, finding more favorable lipid profiles nents. No study has demonstrated a harmful
in active women;43 however, an exercise- effect of carefully performed exercise in se-
related increase in HDL cholesterol has lected cardiac patients.
been demonstrated only in men, not in Hypertension. Appropriately tailored ex-
women.44 ercise programs have been shown to result
The benefits of exercise in the modifica- in 5- to 10-mm decreases in both systolic
8 Basic Concepts of Exercise Physiology

and diastolic resting blood pressures.46 48 ity or disuse. Further, most studies of ath-
Although the mechanisms of these changes letes engaged in weight-bearing exercise
are unknown, exercise may be a useful ad- (e.g., not swimmers) have shown up to a 40%
junct to more conventional therapy. Care increase in bone mass over more sedentary
must be taken in the exercise prescription, control subjects.52,53 Controlled trials, with
however, because the normal increases in or without calcium supplementation, have
systolic and diastolic blood pressure levels demonstrated that exercise may retard or
with exercise are enhanced in patients with even reverse the normal loss of bone min-
hypertension. Further, exercise blood pres- eral content.54-56 Thus, stresses imposed by
sure has been correlated with left ventricu- exercise may be beneficial in preventing os-
lar mass, an independent risk factor for car- teoporosis. However, exercise is more effec-
diovascular mortality.49 Thus, it is important tive when estrogen and calcium supple-
for the hypertensive individual to pursue ments are also given.
dynamic or aerobic types of exercise that
have less marked increases in blood pres-
Selected Other Diseases
sure than those requiring resistive activity.
Associated with hypertensive disease are Exercise training has been found to be of
cerebrovascular accidents. Exercise has benefit in a variety of other chronic dis-
been shown to enhance fibrinolysis and may eases. In general, it improves cardiovascular
therefore reduce the incidence of or mor- function, muscle strength, endurance, flexi-
bidity from stroke.50 bility, adjustment to disease, activity level,
and overall well-being. Additional benefits
may be specific to the underlying disease.
Obesity
For example, in patients with chronic ob-
The benefits of exercise with regard to structive airways disease, exercise is useful
obesity are discussed in detail in Chapter 2. for ventilatory muscle training, increased
Obesity is probably an independent risk fac- tolerance of dyspnea, and reduction in as-
tor for cardiovascular disease in both sexes; sociated anxiety.57 In those with end-stage
its reduction would therefore be expected to renal disease, exercise may lower blood
contribute to cardiac health.51 Exercise pressure and otherwise modify cardiovas-
clearly increases caloric expenditure cular risk.58 Additionally, in patients with
through the effort necessary to maintain ac- both insulin-dependent and insulin-inde-
tivity, favorably alters metabolic rate and pendent diabetes mellitus, a regularly fol-
heat production, and is useful in preserving lowed exercise regimen may decrease insu-
muscle mass during dieting. In addition to lin resistance, requirements, and circulating
the subjective enhancement of perceived levels and improve glucose tolerance,
health, the toning effects of exercise may thereby decreasing all diabetic "complica-
have a positive effect on self-image and may tions," especially cardiovascular disease. In
therefore encourage the dieter to adhere to patients with depression, exercise seems to
both exercise and dietary programs. improve mood or at least provide a physical
vigor important in counteracting affective
illness.59
Osteoporosis
With aging, the mineral content of bone
decreases much more rapidly in women FITNESS EVALUATION
than in men, such that, after menopause, up
to 8% of bone mass may be lost per decade. Muscular Strength and
Although this has been regarded as an in- Endurance
evitable effect of aging and hormonal The strength of a particular muscle group
changes, it is clearly accelerated by inactiv- can be quantified in several ways. Maximal
Fitness: Definition and Development 9

isometric strength is the force generated digitizing of video, high-speed film analysis,
during a maximal contraction against im- or electrogoniometers. For a complete as-
movable resistance. Strain gauge tensiome- sessment of movement during activity,
ters have long been used to measure iso- range of motion must be measured simulta-
metric strength. Maximal isotonic strength neously in several planes. A less precise as-
is the greatest amount of weight that can be sessment of flexibility can be obtained using
moved through the full range of motion only field tests such as the sit-and-reach test of
once (one repetition maximum, or 1 RM). Wells and Dillon60 or the trunk flexion/exten-
Free weights or various pulley devices can sion tests of Cureton.1
be used to measure isotonic strength. Isoki- As with the other components of fitness,
netic strength is a measure of the maximal each individual's need for flexibility may dif-
force that can be generated throughout the fer. However, the prevailing clinical opinion
range of motion at a constant speed. Sophis- is that a normal range of motion for each
ticated isokinetic dynamometers can mea- joint is necessary for pain-free movement.
sure both concentric and eccentric muscle These normal values can be found in texts
performance at varying speeds. Muscular on athletic training61 or physical therapy.62
endurance can be assessed by multiple rep- The need for any additional flexibility varies
etitions (e.g., 20 to 30 RM) either isotoni- among individuals and with activity inter-
cally or isokinetically. As with the other ests.61
components of physical fitness, individual
needs or desire for muscular strength and
endurance will vary. The choice of methods Functional Capacity
to evaluate muscle performance will de- Terminology
pend, in part, on the importance that the ex-
erciser places on this component of physical Oxygen uptake measurements or estima-
fitness. See Chapter 3 for a complete discus- tions used to quantify activity or exercise
sion of muscular strength and endurance. can be reported in several different ways. In
absolute terms, it is simply liters of oxygen
used per minute. Because 1 L of oxygen is
Body Composition
roughly equivalent to 5 kcal,9 the approxi-
Evaluation of body composition is based mate energy cost for any particular activity
on the classification of body components as level can be calculated. One disadvantage of
either lean body mass or body fat. Com- using liters per minute is the discrepancy
monly used methods for assessing body between energy costs for individuals of
composition are hydrostatic weighing, an- varying weights.9 For example, a 200-lb man
thropometric and skinfold thickness mea- will consume more oxygen during activity
surements, and bioelectric impedance mea- (or even sitting at rest) than will a 100-lb
surements. A further discussion of body woman. For this reason, oxygen uptake is
weight and body composition can be found more often reported as milliliters of oxygen
in Chapter 2. consumed per kilogram of body weight per
minute (mL.kg - 1 -min - 1 ). This allows the
Flexibility energy cost of various tasks to be compared
among individuals without the bias of body
Flexibility can be measured directly or as- weight. It is in these terms that Vo2 max is
sessed indirectly during movement tasks.5 most often reported for athletes. Although a
Direct measurement of resting or static high Vo2 max may be taken as a "badge of
range of motion around a specific joint can honor" by endurance athletes, it actually
be obtained with a goniometer. Dynamic has poor predictive ability for sports perfor-
flexibility or movement around a particular mance.4 Nonetheless, a high Vo2 max is in-
joint during an activity can be measured by dicative of a large aerobic capacity. The
1O Basic Concepts of Exercise Phvsioloav

highest Vo2 max reported in the literature Measurement


for men is 14 mL-kg - 1 -min - 1 higher than
that reported for women.63,64 (This apparent Maximal oxygen uptake (Vo2 max) is the
gender discrepancy will be discussed later.) best single measure of the overall functional
With the advent of large-scale exercise capacity of an individual. Since human me-
testing and prescription at hospitals, univer- tabolism depends on oxygen utilization, an
sities, and health clubs, energy expenditure indirect estimate of energy metabolism can
has been classified in metabolic equivalents be made by measuring the amount of oxygen
(METs). One MET is the equivalent of rest- required to perform a given task. Oxygen up-
ing oxygen consumption taken in a sitting take is frequently used to quantify an indi-
position. For an average man, that is approx- vidual's maximal exercise capacity.
imately 250 mL/min, and for an average Vo2 max can be calculated from the actual
woman, 200 mL/min.9 METs can also be ex- measurement of expired oxygen and carbon
pressed in terms of oxygen consumption per dioxide during any exercise task of sufficient
unit of body weight, in which case, 1 MET is intensity and duration to require maximal
equivalent to 3.5 mL/kg per minute (mL- use of aerobic energy systems.4,6,9 The most
kg - 1 -min - 1 ). One MET is also equal to 1 commonly used exercise tests make use of a
kcal/kg per hour (kcal-kg -1 -hr -1 ). 70 The treadmill, cycle ergometer, or rowing er-
MET cost of a particular exercise can be cal- gometer. Any other device, such as bench
culated by dividing the metabolic rate (Vo2) stepping or simulated stair-climbing ma-
during exercise by the resting metabolic chines, that can be calibrated to allow the
rate. The American College of Sports Medi- quantification of the exercise work, can also
cine (ACSM) has constructed tables listing be used.66 The volume and concentration of
the energy cost in METs for walking, jogging, respiratory gases is measured either breath
and running during a range of speeds and by breath or averaged for a certain time pe-
grades of the treadmill (Tables 1-2 and 1- riod (e.g., 15 seconds), using some kind of
3).65 Similar tables have been constructed volume-metering device such as a Tissot
for MET levels during bicycle ergometry and spirometer or volume transducer, along
bench-stepping (Tables 1-4 and 1-5).65 with oxygen and carbon dioxide analyzers.
These tables are equally applicable to men Commercial metabolic carts with these com-
and women. ponents are available.

Table 1-2. APPROXIMATE ENERGY REQUIREMENTS IN METS FOR HORIZONTAL AND


GRADE WALKING
mph 1.7 2.0 2.5 3.0 3.4 3.75
% Grade m/min 45.6 53.7 67.0 80.5 91.2 100.5
0 2.3 2.5 2.9 3.3 3.6 3.9
2.5 2.9 3.2 3.8 4.3 4.8 5.2
5.0 3.5 3.9 4.6 5.4 5.9 6.5
7.5 4.1 4.6 5.5 6.4 7.1 7.8
10.0 4.6 5.3 6.3 7.4 8.3 9.1
12.5 5.2 6.0 7.2 8.5 9.5 10.4
15.0 5.8 6.6 8.1 9.5 10.6 11.7
17.5 6.4 7.3 8.9 10.5 11.8 12.9
20.0 7.0 8.0 9.8 11.6 13.0 14.2
22.5 7.6 8.7 10.6 12.6 14.2 15.5
25.0 8.2 9.4 11.5 13.6 15.3 16.8
Source: American College of Sports Medicine,65 with permission.
Fitness: Definition and Development 11

Table 1-3. ENERGY REQUIREMENTS IN METS FOR HORIZONTAL AND UPHILL JOGGING/
RUNNING*
a. Outdoors on Solid Surface
mph 5 6 7 7.5 8 9 10
% Grade m/min 134 161 188 201 215 241 268

0 8.6 10.2 11.7 12.5 13.3 14.8 16.3


2.5 10.3 12.3 14.1 15.1 16.1 17.9 19.7
5.0 12.0 14.3 16.5 17.7 18.8 21.0 23.2
7.5 13.8 16.4 18.9 20.2 21.6 24.1 26.6
10.0 15.5 18.5 21.4 22.8 24.3 27.2
12.5 17.2 20.6 23.8 25.4 27.1
b. On the Treadmill
mph 5 6 7 7.5 8 9 10
% Grade m/min 134 161 188 201 215 241 268

0 8.6 10.2 11.7 12.5 13.3 14.8 16.3


2.5 9.5 11.2 12.9 13.8 14.7 16.3 18.0
5.0 10.3 12.3 14.1 15.1 16.1 17.9 19.7
7.5 11.2 13.3 15.3 16.4 17.4 19.4 21.4
10.0 12.0 14.3 16.5 17.7 18.8 21.0 23.2
12.5 12.9 15.4 17.7 19.0 20.2 22.5 24.9
15.0 13.8 16.4 18.9 20.3 21.6 24.1 26.6
*Differences in energy expenditures are accounted for by the effects of wind resistance.
Source: American College of Sports Medicine,65 with permission.

Most often the test is incremental, with quires an oxygen uptake of approximately 24
the work rate increased at the beginning of m L - k g - 1 - m i n - 1 . Work increments should
each of several stages.4,6,9 During an incre- require 3 to 7 m L - k g - 1 - m i n - 1 increases in
mental test, oxygen uptake will increase in a oxygen uptake. Because of expected higher
linear relationship with the increasing work maximal capacities, endurance athletes can
rate. The test protocol ideally should reflect be started at work rates greater than 30 mL-
the exercise capabilities of the subject pop- kg~'-min - 1 with increments of 3 to 7 mL-
ulation being tested. Healthy individuals kg - 1 -min - 1 . Elderly women or those with
can usually begin with a work rate that re- known or suspected limitations should

Table 1-4. ENERGY EXPENDITURE IN METS DURING BICYCLE ERGOMETRY


Exercise Rate (kg/mln and watts)
Body Weight
300 450 600 750 900 1050 1200 (kg/min)
kg Ib 50 75 100 125 150 175 200 (watts)
50 110 5.1 6.9 8.6 10.3 12.0 13.7 15.4
60 132 4.3 5.7 7.1 8.6 10.0 11.4 12.9
70 154 3.7 4.9 6.1 7.3 8.6 9.8 11.0
80 176 3.2 4.3 5.4 6.4 7.5 8.6 9.6
90 198 2.9 3.8 4.8 5.7 6.7 7.6 8.6
100 220 2.6 3.4 4.3 5.1 6.0 6.9 7.7
Note: Vo2 for zero-load pedaling is approximately 550 mL/min for 70- to 80-kg subjects.
Source: American College of Sports Medicine,65 with permission.
12 Basic Concepts of Exercise Physiology

Table 1-5. ENERGY EXPENDITURE IN work rate will not be accompanied by an in-
METS DURING STEPPING AT DIFFERENT crease in oxygen uptake.6
RATES ON STEPS OF DIFFERENT HEIGHTS
Because the direct measurement of maxi-
Step Height Step is/mill mal oxygen uptake depends on subject mo-
tivation and the use of rather elaborate lab-
cm in 12 IS 24 30 oratory equipment, various submaximal
0 0 1.2 1.8 2.4 3.0 laboratory tests and field tests have been de-
4 1.6 1.5 2.3 3.1 3.8 vised to estimate maximal aerobic capacity.
8 3.2 1.9 2.8 3.7 4.6 Many of the submaximal predictive tests are
12 4.7 2.2 3.3 4.4 5.5
16 6.3 2.5 3.8 5.0 6.3
based on a linear relationship between heart
20 7.9 2.8 4.3 5.7 7.1 rate and oxygen uptake.4'6'9 The slope of this
24 9.4 3.2 4.8 6.3 7.9 line is unique to each individual and de-
28 11.0 3.5 5.2 7.0 8.7 pends on state of training but not on gender
32 12.6 3.8 5.7 7.7 9.6 (Fig. 1-1). A widely used predictive test is
36 14.2 4.1 6.2 8.3 10.4
40 15.8 4.5 6.7 9.0 11.2
the Astrand-Rhyming Nomogram.4 This no-
mogram allows the prediction of Vo2 max
Source: American College of Sports Medicine,65 with from the heart rate attained during one 6-
permission.
minute work bout on a cycle ergometer, but
can also be used with a step-test protocol.
Alternately, if oxygen uptake and heart rate
begin much lower and increase the work are measured at two submaximal exercise
rate more gradually. Duration of the early intensities, the line representing the rela-
stages should be at least 2 minutes to ensure tionship between heart rate and oxygen up-
gradual physiologic adjustments. The later take can then be extrapolated to the age-pre-
stages can be 1 minute in duration. When the dicted maximal heart rate (200 — age) and
maximal capacity for aerobic energy trans- Vo2 max estimated (Fig. 1-2). McArdle and
fer has been reached, a further increase in associates9 have also developed a set of

Figure 1-1. HR-Vo2 line for a 20-year-old woman before and after a 10-week aerobic conditioning
program. (From McArdle, Katch, and Katch,9 with permission.)
Fitness: Definition and Development 13

Figure 1-2. Application of the linear relation-


ship between submaximal heart rate and ox-
ygen consumption to predict Vo2 max. (From
McArdle, Katch, and Katch,9 with permis-
sion.)

norms for the estimation of Vo2 max from relation (r = 0.67) between these two mea-
measurement of recovery heart rate follow- surements in 36 untrained female subjects.
ing a bench-stepping protocol. Since one of Because factors such as body weight, body
the more practical uses of Vo2 max test data fatness, and movement efficiency contribute
is for monitoring an individual's progress in to distance covered, these tests have error
fitness programs over a period of time, it is ranges of from 10% to 20% of actual maximal
unimportant which protocol is used as long oxygen uptake.9 They can be used only as a
as the same one is used in follow-up tests. rough estimate of aerobic capacity.
Several tests of distance covered in a
given time period (walking, running, or a
Anaerobic Threshold
combination of the two) have also been used
to predict aerobic capacity. The most widely Traditionally, the term "anaerobic
known is the 12-minute walk/run test first threshold" has been used to describe the
suggested by Cooper in Aerobics.61 Cooper68 level of exercise at which aerobic metabo-
reported a correlation (based on tests of 47 lism becomes insufficient to meet the re-
male military personnel) of 0.90 between quired energy demands. This is assumed to
distance covered and maximal oxygen up- be the point at which the resultant increase
take actually measured in the laboratory. in anaerobic glycolysis causes lactate to ac-
However, Maksud and colleagues,69 repeat- cumulate in the muscles and blood.6 Be-
ing this correlation for women, reported a cause this explanation is no doubt an over-
correlation of only 0.70 between actually simplification of the physiologic changes
measured oxygen uptake and distance cov- occurring, many investigators now avoid the
ered, in a group of 26 female athletes. Katch term "anaerobic threshold" and prefer ei-
and co-workers70 noted a similarly low cor- ther "lactate breaking point" or "ventilation
14 Basic Concepts of Exercise Physiology

breaking point" to describe this alteration in FITNESS DEVELOPMENT AND


metabolism.71 MAINTENANCE
During light and moderate exercise, min-
ute ventilation increases in a linear manner Fitness Development
with increasing exercise intensity (oxygen
Flexibility
uptake). However, at some point during the
increasing exercise, the ventilation in- Flexibility can best be improved through
creases out of proportion to the increase in the use of sustained static stretches.5,6,13 The
oxygen consumption. This point has been muscles and connective tissue to be
designated as the "ventilation breaking stretched should be slowly elongated to the
point." In an untrained individual, this point point at which the exerciser feels a mild ten-
generally falls between 40% and 60% of Vo2 sion.5'13 Usually, this position is then held for
max and is associated with a more rapid rise between 10 and 30 seconds.13 During this
in blood lactate to a concentration of 2 mil- time period, the exerciser should feel a
limoles (mmol) per liter (20 mg/dL blood). gradual release of this feeling of tension as
A second upswing in both ventilation and the stretch or myotatic reflex is overcome.
blood lactate can be seen at between 65% As the tension is released, the exerciser
and 90% Vo2 max and a lactate concentration should slowly move a fraction further, again
of 4 mmol/L (36 mg/dL).72 In highly trained to the point of tension, and continue to hold
athletes, these ventilation breaking points for approximately 30 seconds.13 Stretching
occur at higher percentages of Vo2 max. following an exercise session, when the
The mechanism of the ventilation break- muscle and connective tissues are warm,
ing point has not been satisfactorily ex- has been found to be the best time for im-
plained but is usually associated with the ac- proving flexibility.6
cumulation of lactic acid in the blood
(hence, the appearance and rise of blood
Cardiovascular Fitness
lactate).6 The need to dispose of excess car-
bon dioxide produced from the buffering of The ACSM has developed guidelines for
excess hydrogen ions (from the lactic acid) building and maintaining fitness in healthy
drives the peripheral chemoreceptors that adults.65,73 In recommending the quantity
stimulate increased ventilation. Ventilation and quality of exercise, the ACSM cites five
breaking points can be found during gas ex- components that are applicable to the de-
change measurements, whereas lactate sign of exercise programs for adults regard-
breaking points can be found through fre- less of age, gender, or initial level of fitness:
quent analysis of a small amount of blood, (1) type of activity, (2) intensity, (3) dura-
usually taken by a fingerstick. Most experi- tion, (4) frequency, and (5) progression.
ments with highly trained athletes use the 4- Type of Activity. The exercise program
mmol value rather than the more reproduc- should include activities that use large mus-
ible 2-mmol value, since athletes can exer- cle groups in a continuous rhythmic man-
cise for several hours with lactate values ner. Activities such as walking, hiking, jog-
greater than 2 mmol but less than 4 mmol. As ging/running, swimming, bicycling, rowing,
with the ventilation breaking point, there is cross-country skiing, skating, dancing, and
no universally accepted explanation for the rope skipping are ideal. Because control of
lactate breaking point. Among the explana- exercise intensity within rather precise lim-
tions offered are increased production of its is often desirable at the beginning of an
lactate, decreased clearance of lactate, a exercise program, the most easily quantified
combination of these two, and increased re- activities, such as walking or stationary cy-
cruitment of fast-twitch (glycolytic) motor cling, are particularly useful. Various endur-
units. ance game activities such as field hockey,
Fitness: Definition and Development 15

soccer, and lacrosse may also be suitable translated into MET levels. The intensity of
but may have high-intensity components, training sessions comprised of most activi-
and therefore should not be used in the ex- ties can be monitored through the use of tar-
ercise prescription until participants are get heart rates (Fig. 1-3) or through MET
able to exercise comfortably at a minimum levels. The energy cost in METs of various
level of 5 METs.65 If intensity, duration, and activities can be found in the ACSM Guide-
frequency are similar, the training result ap- lines for Exercise Testing and Exercise Pre-
pears to be independent of the mode of aer- scription (see Tables 1-2 through 1-5).65 Ac-
obic activity. Therefore, a similar training ef- curate quantification of some activities may
fect on functional capacity can be expected, be difficult. For example, target heart rates
regardless of which endurance activity is derived from treadmill exercise tests may
used. not adequately quantify swimming or vari-
Intensity. The conditioning intensity of ous other activities with a large upper-body
the aerobic portion of the exercise session is component, such as aerobic dance.75
best expressed as a percentage of the indi- Duration. Each training session should
vidual's maximal or functional capacity. Ef- last between 15 and 60 minutes, with an aer-
fective training intensities are from 50% to obic component of at least 15 minutes. Typ-
85% of Vo2 max or 60% to 90% of the maxi- ically, an exercise session should include a
mum heart rate achieved during a graded 5- to 10-minute warm-up, 15 to 60 minutes of
exercise test.65'73'74 These intensities can be aerobic exercise at the appropriate training

Figure 1-3. Maximal heart rates and training-sensitive zones for use in aerobic training programs for
people of different ages. (From McArdle, Katch, and Katch,9 with permission.)
16 Basic Concepts of Exercise Physiology

level, and a cool-down of 5 to 10 min- the largest changes usually seen in the in-
utes.65,73,74 The function of the warm-up is dividuals who have the lowest initial fitness
gradually to increase the metabolic rate levels.76 Both men and women respond to
from the 1-MET level to the MET level re- aerobic training with similar increments in
quired for conditioning. In planning the aer- maximal oxygen uptake.73 An individual
obic portion of the workout, one must con- starting a fitness program can expect a sig-
sider that duration and intensity are nificant improvement in functional capacity
inversely related. That is, the lower the ex- to occur during the first 6 to 8 weeks.4,6,9 The
ercise intensity, the longer the workout length of time necessary to reach one's true
needs to be. Although significant cardiovas- Vo2 max depends on the initial fitness level
cular improvements can be made with very and intensity of training. As conditioning
intense (more than 90% Vo2 max) exercise takes place, the exercise intensity will need
done for short periods of time (5 to 10 min- adjustment in order to keep the participant
utes), high-intensity, short-duration ses- exercising in the training range. During the
sions are not appropriate for individuals initial phases of a program, this is best done
starting a fitness program.65 Because of po- by changing the MET level to correspond to
tential hazards (including an unnecessary the desired exercise heart rate. Since with
risk of injury) for untrained individuals em- conditioning the heart rate will drop for any
barking on a high-intensity program, low to given submaxirnal work rate, intensity ad-
moderate intensity for longer durations is justments will result in more actual work
recommended for those beginning a fitness being done during each exercise session.65
program. Although the recommended dura- Follow-up graded exercise tests should be
tion of the aerobic or conditioning part of done during the first year of the program to
the workout is 15 to 60 minutes, an adequate help in the intensity adjustment and in mo-
training response can be elicited by main- tivating the participant. The goals of the par-
taining the prescribed exercise intensity for ticipant need to be taken into account to de-
a period of approximately 15 minutes.65 With termine when the exercise program can be
the warm-up and cool-down, a reasonable changed from one with a goal of increasing
amount of total workout time for a person fitness level to one with the goal of maintain-
beginning an exercise program would be 30 ing the newly acquired level. Sample exer-
minutes. The cool-down phase should in- cise programs for sedentary, active, and
clude exercise of diminishing intensity to re- competing women are shown in Appendix
turn the physiologic systems of the body to 1-1. It must be stressed that no program
their resting states. should be undertaken lightly and that, for
Frequency. The frequency of exercise many women, the ideal program may be a
sessions is somewhat dependent on the in- highly individualized "exercise prescrip-
tensity and duration of the exercise. For ex- tion" developed in conjunction with a phy-
ample, exercise programs for individuals sician and exercise physiologist.
with very low functional capacities (less
than 5 METs) may start out with several Fitness Maintenance
short (5-minute) sessions per day. For most
individuals, exercise programs for improv- Activity Level
ing one's fitness level should be done three Exercise must be continued on a regular
to five times per week.65 basis in order to maintain a given fitness
Progression. The degree of improvement level. Hickson and colleagues28,77,78 have
in Vo2 max (the best measure of functional shown that the duration and frequency of
capacity) is directly related to the intensity, exercise may be reduced by as much as two
duration, and frequency of the training. Re- thirds without affecting the training-induced
search has documented improvements in Vo2 max, but intensity plays a critical role in
Vo2 max ranging between 5% and 25%, with maintaining the training-induced changes.
Fitness: Definition and Development 17

When the duration of exercise sessions fol- developing and maintaining fitness can be
lowing 10 weeks of training was reduced used for training.65,73 Many recreational ac-
from 40 minutes per day to 26 or 13 minutes tivities, however, are intermittent in nature
per day for the next 5 weeks, no reduction in and their energy expenditure is difficult to
the exercise-induced Vo2 max was seen.77 quantify. Although there are tables listing
Similarly, when sessions were reduced from average energy expenditures,9,73 the amount
6 days/wk to 4 or 2 days/wk, there again was of energy expended often depends on the
no reduction in Vo2 max.78 However, data skill of the participants. For example, it is dif-
suggest that in order to maintain training- ficult to imagine that the energy expended
induced gains, an individual must continue by a professional tennis player such as Mon-
to exercise at an intensity of at least 70% of ica Seles is in any way similar to that ex-
the training intensity.28 Therefore, after pended by some weekend players. Recrea-
achieving a desired level of fitness, an indi- tional activities, then, are best used to
vidual can theoretically be expected to supplement a planned program for the de-
maintain this level by exercising at least velopment and maintenance of physical fit-
twice a week at 70% or more of her training ness.
intensity for a minimum of 13 minutes per
session. Factors Affecting Fitness
Caution is advised, however, in the inter- Development and Maintenance
pretation of these data, since the subjects
from whom these conclusions were reached Age
were highly conditioned men and women, Increased age alone is not a contraindi-
and the results may not be applicable to in- cation to participation in a fitness program.
dividuals training at lower intensities. It Regular training will result in positive phys-
should also be kept in mind that body com- iologic adaptations, regardless of age.6,73,79
position is one of the components of "phys- Some studies have shown that older individ-
ical fitness." Thus, if the participant is using uals may require longer to adjust to physical
the exercise program to maintain caloric training programs and may not make as
balance and to keep body fat at a reasonable large an absolute improvement in fitness
level, a maintenance program of 4 to 5 days/ level as a younger person.73 However, a com-
wk would be a better choice. parison of improvements is often difficult
When an individual stops training, a sig- because younger individuals tend to train at
nificant detraining effect occurs within 2 higher intensities than do older individuals.
weeks, as measured by a decrease in physi- As an individual ages, there will be some de-
cal work capacity.9 A 50% reduction of the crease in Vo2 max regardless of training,
newly acquired gain in fitness has been since there is an age-related drop in maxi-
shown to occur by 4 to 12 weeks after ces- mal heart rate, which, in turn, reduces max-
sation of training, while a return to pretrain- imal cardiac output.4 An age-related de-
ing fitness level can be expected after ces- crease in Vo2 max does not imply that an
sation of training between 4 weeks and 8 older individual cannot or should not partic-
months.73 Although much of this research is ipate in activities requiring a great deal of fit-
based on information from male subjects, ness. For example, each year there are sev-
the deconditioning pattern and time-course eral contestants and finishers over age 70
are expected to be similar in women.76 years in the Hawaiian Ironman Triathlon, a
contest that takes 9 to 17 hours to complete.
Role of Recreational Sports
Gender
Recreational sports that require an en-
ergy expenditure of sufficient intensity and Although most of the research supporting
duration to fall within ACSM guidelines for the quantity and quality of exercise neces-
18 Basic Concepts of Exercise Physiology

sary to develop and maintain fitness was ini- excluded from exercise, many patients will
tially derived from male subject data, it ap- need special considerations in the design
pears to be equally applicable to women. and implementation of appropriate exercise
Numerous recent studies have documented training. Any aspect of an exercise program
similar training responses for men and may be changed to adapt to the individual's
women.73 Before puberty, there is no differ- needs, as long as the core features of exer-
ence in maximal aerobic power between cise mode, intensity, duration, and fre-
boys and girls.4 After that, however, the po- quency are preserved. Although reductions
tential for absolute magnitude of aerobic ca- in intensity are most common, exercise mo-
pacity is higher for men. There seem to be at dality may be altered (e.g., using non-
least three basic physiologic differences be- weight-bearing or low-impact activities for
tween men and women that affect the capac- the patient with arthritis, extreme obesity,
ity for aerobic power.17'19 Women usually or musculoskeletal abnormalities). Regard-
have a higher percentage of body fat, a less of initial fitness level or absolute level of
smaller oxygen-carrying capacity, and a achievement, the positive effects of en-
smaller muscle-fiber area than do men. hanced well-being, muscular strength, and
When the effects of body weight and per- activity tolerance may be expected. Moni-
centage of body fat are corrected mathemat- toring methods may also need to be adapted
ically, the differences in Vo2 max are to the individual situation (e.g., use of res-
lessened. Studies have averaged these dif- piratory rate rather than heart rate for ex-
ferences to be approximately 50%, 20%, and ercise intensity in the patient with a pace-
9% when Vo2 max is expressed as liters per maker). Detailed discussion of exercise
minute, milliliters per kilogram per minute, prescription is beyond the scope of this
and milliliters per kilogram fat-free mass, re- chapter.
spectively. The remaining difference (ap-
proximately 9%) is either still a difference in
Sudden Death
conditioning or more probably a gender-
linked difference in the ability to transport Sudden death during exercise has been
and utilize oxygen. Since women usually well publicized, yet is extremely rare and
have a lower hemoglobin concentration most unlikely in an otherwise healthy indi-
than men (normal range equals 12 to 16 g/dL vidual without known cardiac disease.80-85
for women; 14 to 18 g/dL for men) and a Although sudden death may occur more
smaller blood volume, they have a smaller often during activity than during rest, most
maximal oxygen-carrying capacity than occurrences are related to usual daily activ-
men. In addition, endurance-trained women ities and not to exercise programs.
have approximately 85% of the muscle-fiber The causes of sudden death during exer-
areas of endurance-trained men. Although cise have been examined in male athletes.83
the fiber area is different, the muscle com- In the young, nearly 65% have some form of
position is much the same for male and fe- hypertrophic cardiomyopathy, 14% have
male endurance athletes.17 congenital coronary artery anomalies, 10%
have coronary heart disease, and 7% have
ruptured aorta or Marfan's syndrome. In
Underlying Disease
contrast, of those dying suddenly after age
For any woman with known or suspected 35, more than 80% have coronary heart dis-
medical illness, embarking upon a fitness ease. Other associated diseases include hy-
program should be preceded by consulta- pertrophic cardiomyopathy, mitral valve
tion with a physician with special training in prolapse, and acquired valvular disease. For
the patient's disease and, when indicated, this reason, women with known or sus-
by continued close medical supervision. Al- pected cardiovascular disease and previ-
though it is rare that an individual should be ously sedentary individuals over 50 years of
Fitness: Definition and Development 19

age should seek the advice of an internist or exercise clothing, or much more. Costs for
cardiologist before pursuing a vigorous ex- the use of facilities can be from less than
ercise program. While most cardiovascular $100 per year for a YMCA/YWCA or local
illnesses do not preclude the achievement university-based program to $500 or $600
of fitness, the exercise program should be per year for a health club membership. In-
individually tailored to meet the needs and dividuals can join exercise classes, such as
limitations of the participant. Further, there one in aerobic dance, or they may choose to
are a small number of illnesses in which any carry out their prescription on their own
form of vigorous activity should be strictly Equipment for walking or jogging programs
limited. is minimal, but that for a bicycling program
is more.
Injury
Most of the injuries resulting from partic- TRAINING FOR COMPETITION
ipation in fitness programs are musculoskel-
etal injuries. Although occasionally there Training for competition differs from
are traumatic injuries, such as fractures and training for fitness in that its main objective
torn ligaments, more frequently the injuries is improvement of performance rather than
are the result of chronic microtrauma or improvement of health. Training for com-
overuse. These injuries include muscle petition should begin by using the same
strains, tendinitis, synovitis, bursitis, and ACSM guidelines for intensity, frequency,
stress fractures. In most cases, these inju- and duration. A period of approximately 8
ries are not serious enough to prevent train- weeks is necessary to lay the groundwork
ing but often require alterations in training for a more intense training program.6 Phys-
patterns. Overuse injuries have been attrib- iologic adaptations occurring in ligaments
uted mainly to errors in training, such as and muscles during that time make them
progressing too fast and not allowing less susceptible to overuse injuries, which
enough time for recovery and adaptation.84 otherwise might occur as a result of high-in-
tensity training. Once the fitness base is laid,
the competitive athlete must overload her
Practical Considerations
system further to continue improving. The
Practical considerations are often critical overload should be progressive and individ-
to whether or not an individual participates ualized to the specific goals of the athlete. At
in a fitness program. The most important of this point, training should be as specific to
these considerations for most people is the competition as possible. That is, the ex-
time. Everyone has certain constraints on erciser needs to train the specific muscles to
her time, whether they be job-related or be involved in the desired performance in a
home-related. An individual wishing to par- manner specific to the competition.
ticipate in an exercise program to improve
fitness must make a time commitment. A Interval Training
minimum of at least 1 hour three times per
week is necessary. This could comprise a Because most competition involves an el-
bare minimum of 30-minute exercise ses- ement of speed, the exerciser may benefit
sions plus time to change clothes, travel, from interval as well as continuous training.6
and so forth. Cost is another factor to be con- Interval training is a means of accomplish-
sidered. Most exercise test evaluations with ing a great deal of work in a short period of
an exercise prescription cost between $100 time by interspersing work intervals with
and $400. Following this initialfinancialou rest intervals. The work intervals may be of
lay, each individual can spend as little as the any desired length, from just a few seconds
cost of a good pair of shoes and comfortable to several minutes. The length of the work
20 Basic Concepts of Exercise Physiology

interval is determined by the specific de- for general well-being and protection
mands of the competition and by the energy against some disease states. A greater de-
system the athlete wishes to train. Intervals gree of fitness is beneficial for certain rec-
of less than 4 seconds can be used to de- reational and competitive sport activities.
velop strength and power for activities such Cardiovascular fitness can be developed ac-
as a high jump, shot put, golf swing, or tennis cording to the guidelines of the ACSM. Rate
stroke. Intervals of up to 10 seconds are and degree of improvement for women can
used to develop sustained power for activi- be expected to be similar to that for men and
ties such as sprints, fast breaks, and so on. depends on intensity, duration, and fre-
The length of these intervals forces the body quency of exercise sessions.
to use immediate, short-term energy sys-
tems. Intervals of up to 11/2minutes are used
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1982.

APPENDIX 1-1

Sample Training Programs


The following are sample training schedules for women starting a fitness
program. They are, however, only examples of types of activities that would be
appropriate for women in these categories and should not be undertaken without
proper medical and fitness evaluation. Also included are general guidelines to be
followed by an athlete training for competition. Since a competitive athlete must
train specifically for the requirements of her sport, a program appropriate for one
athlete may be of little benefit to someone in another sport.

SAMPLE 8-WEEK PROGRAM FOR A SEDENTARY


30-YEAR-OLD WOMAN

Weeks 1-4. (Initial Stage—The energy cost of the exercise in this stage should
be approximately 200 kcal per session. Exercise sessions should be three
times per week or every other day.)
Warm-up. 5 min walking (heart rate [HR] = 110 beats per minute [bpm]; 5
min stretching (areas to stretch: Achilles tendon, hamstrings, lower
back, and shoulders).
Aerobic Phase. 15 min vigorous walking, jogging, stationary cycling, or any
combination of these (HR = 135-145 bpm). After the second week, the
time for this phase should be gradually increased (by 1 min every other
day) to 20 min.
Cool-down. 5 min walking (HR = 100-110 bpm); 5 min stretching (same as
in warm-up).
Weeks 4-8. (Improvement Stage—The energy cost of exercise in this stage
should be approximately 300 kcal per session. Exercise sessions should be
three to five times per week.)
Warm-up. 5 min walking (HR =115 bpm); 5 min stretching, as previously.
Aerobic Phase. 20 min initially; gradually increase to 25 min, as above. Aer-
obic activities can include walking, jogging, cycling, or any other con-
tinuous, rhythmic exercise. (HR = 140-150 bpm.)
24 Basic Concepts of Exercise Physiology

Cool-down. 5 min walking (HR = 100-110 bpm); 5 min stretching, as


previously.
Week 8 and Afterward. (Maintenance Stage—The energy cost should still be
approximately 300 kcal per session.)
Warm-up. Same as above.
Aerobic Phase. Intensity and duration of sessions should be the same as in
Improvement Stage. Exercise should be done at least 3 times per week.
Recreational sport activities of approximately the same intensity may
be substituted 1 day per week.
Cool-down. Same as above.

SAMPLE 8-WEEK PROGRAM FOR SEDENTARY 60-


YEAR-OLD WOMAN

Weeks 1-4. (Initial Stage—200 kcal per session; three times per week.)
Warm-up. 5 min walking (HR = 100 bpm); 5 min stretching (areas to stretch:
Achilles tendon, hamstrings, lower back, and shoulders).
Aerobic Phase. 12-15 min vigorous walking or stationary cycling (HR = 110-
120 bpm).
Cool-down. 5 min walking (HR = 95-105 bpm); 5 min stretching, as
previously.
Weeks 4-8. (Improvement Stage—300 kcal per session, three to five times per
week.)
Warm-up. 5 min walking (HR =110 bpm); 5 min stretching, as previously.
Aerobic Phase. 15 min initially; gradually increase to 25 min of walking, jog-
ging, stationary cycling, or any combination of these (HR = 120-130
bpm).
Cool-down. 5 min walking (HR = 100-105 bpm); 5 min stretching, as
previously.
Week 8 and Afterward. (Maintenance Stage—The energy cost per session
should remain at 300 kcal. Exercise should be done at least three times per
week.) Exercise program can remain the same as in the Improvement Stage
with recreational sport activities substituted once a week if desired.

SAMPLE 8-WEEK PROGRAM FOR A MODERATELY


ACTIVE 45-YEAR-OLD WOMAN

Weeks 1-2. (Initial Stage—Energy cost approximately 300 kcal per session. The
purpose of this stage in a moderately active woman is to allow adaptation
[particularly musculoskeletal] to occur in response to specific aerobic activ-
ity, such as jogging.)
Warm-up. 5 min walking or slow jogging (HR = 120-125 bpm); 5 min stretch-
ing (Achilles tendon, hamstrings, lower back, shoulders).
Fitness: Definition and Development 25

Aerobic Phase. 25 min of vigorous walking, jogging, stationary cycling, row-


ing, or any other continuous, rhythmic activity of choice. (HR = 135-
140 bpm.)
Cool-down. 5 min slow jogging and/or walking (HR =110 bpm); 5 min of
stretching, as previously.
Weeks 3-8. (Improvement Stage—300-500 kcal per session.)
Warm-up. 10 min (same as previously).
Aerobic Phase. 25 min initially; gradually increase to 45 min per session. Any
activity that will keep the heart rate 140-145 bpm for this length of time
may be used.
Cool-down. 10 min (same as previously).
Week 8 and Afterward. (Maintenance Stage—Exercise sessions should be sim-
ilar to those in the Improvement Stage and should be done at least three
times per week with an energy cost of 500 kcal per session.)

GUIDELINES FOR THE COMPETITIVE ATHLETE

1 Training should be in three stages, comparable to those shown earlier but


on a higher level—laying a base, increasing intensity, and fine tuning.
2 When adding sport-specific activities, training should be under conditions
as similar to competitive conditions as possible.
3 Set reasonable goals in a reasonable time frame.
4 Keep a training diary to discover your own personal pattern of optimal
training and to discover practices that lead to injury for you.
5 Use an overload/adaptation/progression system. That is, allow enough
time for adaptation to occur after a hard workout, by following the hard
workout with several easy or moderate ones. For example, after a race,
some running coaches suggest waiting one day for each mile that was run
before beginning the next hard workout.
6 Balance the high energy output of training with a high caloric intake.

SAMPLE PROGRAM FOR A USTS DISTANCE


TRIATHLETE

(0.9-mile swim, 25-mile bike, 6.2-mile run)


Weeks 1-4. (Initial Stage—Goals are gradually to increase weekly mileage to 3
miles of swimming, 45 miles of bicycling, and 20 miles of running.)
Each workout should follow the format given previously (that is, warm-up,
aerobic phase, and cool-down). The warm-up and cool-down phases
should include gradual transition from rest to swimming, cycling, or
running, as well as stretching of the muscles specific to that activity.
Each activity should be done three times per week, or nine total workouts
for the week. Since there are a variety of muscle groups being used, each
with its own stresses, the triathlete can safely exercise every day. In
26 Basic Concepts of Exercise Physiology

order to complete the nine workouts, single workouts can be done on 5


days, and double workouts on 2 other days. Workouts in the same sport
should not be done on 2 consecutive days.
Training mileages per workout should be up to 1500 meters swimming, 25
miles cycling, and 6 miles running. No interval training should be done.
All training mileages should be accomplished aerobically; that is, at the
end of the workout, the triathlete should feel that she could repeat the
workout immediately.
Weeks 4-12. (Improvement Stage—The time to increase the intensity of the
workouts.)
Mileages should be increased to 5 miles of swimming, 75 miles of bicycling,
and 25 miles of running per week.
During this stage, the emphasis should be on increasing the mileages so that
some workouts are done slower than race pace at distances longer than
race distances. Other workouts should be done using interval training.
One interval training workout per week per sport is sufficient, and inter-
val training should probably not be done on consecutive days. Time tri-
als at race distances can be added during this phase.
Each activity should be done four or five times per week for a total of no more
than 15 workouts per week. Hard workouts should be followed by easy
workouts in each activity so that hard workouts are not done on two
consecutive days. Occasionally, a swim workout should be immediately
followed by a bike workout and a bike workout immediately followed by
a run.
Weeks 12 Through the Competitive Season. The emphasis during this time
should be on race performance. The total amount of training should be cut
down, particularly on weeks when the triathlete is competing. The emphasis
in workouts should be on quality rather than quantity. Short intervals con-
centrating on speed rather than endurance should be done once a week for
each activity. Other days can either be at race pace for distances shorter
than the race, or slower for longer distances. One day a week can be com-
plete rest or a very easy workout.
CHAPTER 2

Exercise and Regulation


of Body Weight*
DENISE E. WILFLEY, Ph.D., CARLOS M. GRILO, Ph.D., and
KELLY D. BROWNELL, Ph.D.

THE NATURE AND SEVERITY OF Obstacles to Exercise for the


WEIGHT DISORDERS Overweight Individual
Adherence Studies
THE ASSOCIATION BETWEEN
PHYSICAL ACTIVITY AND PROGRAM RECOMMENDATIONS
WEIGHT Avoid a Threshold Mentality
Consistency May Be More Important
EXERCISE AND WEIGHT
than the Type or Amount of
CONTROL
Exercise
LIKELY MECHANISMS LINKING Provide Thorough Education
EXERCISE AND WEIGHT Be Sensitive to the Special Needs of
CONTROL Overweight Persons
Energy Expenditure
SPECIAL ISSUES
Appetite and Hunger
The Role of Exercise in the Search for
Body Composition
the Perfect Body
Physical Activity and Health
Ideal Versus Healthy Versus
Psychologic Changes
Reasonable Weight
THE CHALLENGE OF ADHERENCE Exercise Overuse (Abuse)
Adherence and the Demographics of
Obesity

p
1 eople are searching frantically for the ideal body. In 1989, U.S. consumers
spent an estimated $32 billion on weight control programs and products.1 This
drive for thinness has created a burgeoning marketplace for physical fitness
equipment, attire, and health clubs. This stems from a clear belief that exercise
aids in weight maintenance in persons at normal weight and in weight loss in
overweight individuals. In fact, women often state that exercise is one of their
primary methods of weight control.
The concern for thinness and dieting behavior is especially prevalent among

* Preparation of this chapter was supported in Jenny Craig Foundation for the Fellowship Pro-
part by a MacArthur Foundation Fellowship to gram of the Yale Center for Eating and Weight
Carlos M. Grilo and in part by a grant from the Disorders.
27
28 Basic Concepts of Exercise Physiology

women. The eating disorders of anorexia and 50% of men reported they were cur-
and bulimia, both of which involve preoc- rently either trying to lose weight or to
cupation with weight, are seen almost exclu- maintain their current weight.4
sively in women. Obesity occurs equally in There are countless variations among
women and men, yet women are more fre- women in the combinations of diet and ex-
quently the consumers of weight control ercise programs they follow. It is important,
products and are more likely to attend clin- therefore, to understand the physiologic
ical programs. and psychologic effects of such programs
In our culture, the search for the perfect and to identify approaches that are safe and
body begins at a young age and is especially effective. Exercise physiology and sports
pronounced among women. A recent sur- medicine are central to this endeavor. In
vey, the Youth Risk Behavior Surveillance spite of the fitness boom, many women and
System (YRBSS), revealed interesting find- men are too inactive to attain the psycho-
ings regarding weight control practices logic and health benefits of exercise, and
among adolescents. Using self-administered many of those who begin exercise programs
questionnaires in comparable national, do not continue exercising long enough to
state, and local surveys, the YRBSS mea- achieve their health and fitness goals.5
sures the prevalence of health-risk behav- In this chapter, we discuss the prevalence,
iors of adolescents.2,3,4 The 1990 YRBSS severity, and refractory nature of weight
included 11,631 students from grades 9 problems. The effects of exercise on food in-
through 12. take, metabolism, and regulation of body
Substantial differences were found in the weight are outlined, with specific focus on
weight perceptions of boys and girls. Female the effects of exercise on women. We discuss
students were twice as likely as male stu- mechanisms by which exercise facilitates
dents to consider themselves "too fat" (34% long-term weight loss, because there appear
versus 15%, respectively). Moreover, many to be multiple pathways linking exercise to
more female students were engaging in weight change. We then discuss ways to in-
weight control strategies. Among female stu- crease adherence, with particular focus on
dents, 44% reported that they were cur- the importance of tailoring exercise inter-
rently trying to lose weight, 26% were trying ventions to the special physical and psycho-
to keep from gaining weight, 7% were try- social needs of overweight persons. We also
ing to gain weight, and only 23% were not examine special issues such as how our cul-
trying to do anything about their weight. ture's preoccupation with shape and weight
Among male students, 15% reported that may perpetuate unhealthy attitudes toward
they were trying to lose weight, 15% were dieting and exercise, how to establish crite-
trying to keep from gaining weight, 26% were ria for a "reasonable weight" for an individ-
trying to gain weight, and 44% were not try- ual, and when exercise can be psychologi-
ing to do anything about their weight. Fe- cally and/or physically harmful. We end by
male students reported using exercise describing the role exercise can play in
(51%) and skipping meals (49%) as the two weight regulation and by outlining an ap-
most common means of weight control. proach to exercise that accounts for meta-
In sum, weight control is widely sought bolic variables, cultural factors, psychologic
after by both female adolescents and adults issues, and the challenge of long-term ad-
in the United States.4 Among high school herence.
girls in 1990, 70% of girls versus 30% of boys
reported that they were either trying to lose
weight or maintain their current weight. THE NATURE AND SEVERITY
Data collected on adults looks very similar. OF WEIGHT DISORDERS
Among 60,912 adults in the 1989 Behavior
Survey and Behavioral Risk Factor Surveil- Overweight is a prevalent problem with
lance System (BRFSS), about 70% of women serious adverse effects on health and Ion-
Exercise and Regulation of Body Weight 29

gevity. Approximately 27% of women and ronmental, cultural, socioeconomic, and


24% of men are overweight, using a criterion psychologic factors.
of 20% or more above desirable weight.6 Careful measurement of height and weight
Overweight is associated with elevated is currently the first step in the clinical as-
serum cholesterol, elevated blood pressure, sessment of the overweight.10 The body
cardiovascular disease, and noninsulin-de- mass index (BMI), the weight in kilograms
pendent diabetes.7'8 It also increases the risk divided by the square of the height in me-
for gallbladder disease and some types of ters, a measure of relative weight, is a more
cancer, and it has been implicated in the de- useful measurement of degree of overweight
velopment of osteoarthritis of the weight- than weight tables, since it correlates highly
bearing joints.9 (0.8) with more precise laboratory assess-
Overweight clearly affects a large propor- ments of body composition and is adjusted
tion of the U.S. population. The burdens of for height in order to compare body weight
overweight are shouldered disproportion- across individuals or groups.7 For persons of
ately by the poor and members of certain average weight, one BMI unit is equivalent
ethnic groups. Overweight is multideter- to approximately 6.8 Ib in men and 5.8 Ib in
mined in nature, reflecting biologic, envi- women (Fig. 2-1). Since risk is approxi-

Figure 2-1. Nomogram for body


mass index (BMI). To determine
BMI, place a ruler or other
straightedge between the body
weight column on the left and the
height column on the right and
read the BMI from the point
where it crosses the center.
(®George A. Bray, M.D., 1978, re-
printed with permission.)
30 Basic Concepts of Exercise Physiology

ing and physical activity to the point where


body weight drops low enough to be life-
threatening. It occurs primarily in adoles-
cents and young adults in their early 20s,
and with few exceptions is confined to fe-
males. It is not the "flip side" of obesity. An-
orexics have characteristic family back-
grounds and patterns that are not common
among the overweight. There are also few
overweight persons who develop anorexia
nervosa.
Another eating disorder characterized by
excessive weight preoccupation and con-
cerns is bulimia nervosa. It involves fluctu-
ations between extreme dietary restriction
and out-of-control eating (binge eating).
Most women with bulimia nervosa report
the onset of binge eating following a severe
diet.12 The binge eating is followed by some
compensatory behavior such as self-in-
duced vomiting, use of diuretics or laxatives,
strict dieting or fasting, or vigorous exercise
in order to prevent weight gain. As with an-
orexia nervosa, bulimia nervosa is most
common among females. Among the con-
tributing factors are cultural pressures to be
thin, mothers' criticism of daughters' weight
and appearance, dysfunctional family pat-
Figure 2-2. Risk classification algorithm. After measur-
ing the BMI, the individual risk is increased or de- terns, low self-esteem, social self-conscious-
creased based on the presence of complicating factors. ness, and dieting itself. 13-15
(George A. Bray, M.D., 1988, reprinted with permis- Both anorexia nervosa and bulimia ner-
sion.)
vosa are most common in the populations
who are most invested in dieting and weight
loss—predominately white, middle to upper
mately proportional to degree of over- class females.16 In contrast, obesity is nega-
weight, Bray10 classifies the degree of risk on tively correlated with socioeconomic sta-
a scale from Class 0, very low risk, to Class tus.17 There is an overall correlation be-
IV, very high risk (Fig. 2-2). tween the cultural pressure to be thin and
Weight loss programs have shown dra- prevalence of eating disorders, both across
matically improved short-term results over and within ethnic groups.18 It is also well
the past two decades, but long-term results documented that eating disorders are more
are still discouraging. This resistance to prevalent in occupations (e.g., modeling)
treatment, combined with the high preva- and other life activities (e.g., gymnastics)
lence and striking severity noted earlier, that place pressure on females to be thin.19
make obesity a public health problem of In each of these disorders, complex inter-
considerable magnitude.11 actions exist among food intake, physical ac-
At the other end of the continuum of tivity, metabolism, psychology, and culture.
weight concerns lies anorexia nervosa (see The remainder of this chapter will discuss
Chapter 17). This involves a morbid and the interplay of these factors in the lives and
persistent dread of fat, with pathologic diet- health of women.
Exercise and Regulation of Body Weight 31

THE ASSOCIATION BETWEEN cert with the significant decline in physical


PHYSICAL ACTIVITY AND activity. Given the effects of changes in di-
WEIGHT etary composition and exercise on metabo-
lism and body composition, it is not difficult
During the last century, overweight has to posit a relationship between these factors
become increasingly common despite an and increased obesity.
overall decrease in the average daily caloric Research generally shows that over-
intake of the population.11,'20,21 Several impor- weight individuals are less active than their
tant changes have occurred during this pe- average-weight peers.26 Physical activity is
riod of time that may help explain this phe- inversely related to body weight, body com-
nomenon. Daily energy expenditure has position,27'28 and waist-to-hip ratio, although
decreased as society has progressed from its relation to different degrees of obesity is
an agricultural, to an industrial, to an infor- less clear. There are factors, however, that
mation-based economy, with fewer and must be considered when interpreting these
fewer jobs requiring physical exertion. Our results. First, many studies with both chil-
culture has also adopted a technology-ori- dren and adults have failed to find meaning-
ented philosophy of saving energy and in- ful differences in activity levels between
creasing comfort. As a result, daily energy overweight and average-weight persons.26
expenditure has dropped dramatically dur- Studies with those who are extremely over-
ing this century. weight, however, have found significantly
In 1984, the U.S. Department of Agricul- lower activity levels than for average-weight
ture estimated that between the years of persons. A second factor is that lower levels
1965 and 1977 the average daily energy ex- of activity may not necessarily represent a
penditure dropped by 200 calories per day lower energy expenditure. For example, an
(the equivalent of almost 21 lb/y).22 A report overweight person will require more energy
issued by the Centers for Disease Control to perform the same activity than a normal-
(CDC) in 1992, based on the national school- weight person because of additional energy
based Youth Risk Behavior Survey, esti- required to carry the excess weight. There-
mated that only 37% of students in grades 9 fore, an overweight person may actually ex-
to 12 were vigorously active three or more pend more calories than a lighter-weight
times per week. A comparison of these 1992 person who exercises more. A third factor
CDC findings with the 1984 report issued by may be the most important. Although over-
the National Children and Youth Fitness weight individuals may be less active than
Study, suggests that participation in vigor- average-weight persons, it is possible that
ous activity in adolescents is decreas- physical inactivity is a consequence—not a
ing.2,23,24 Another report issued by the CDC in cause—of being overweight. We speculate
1987 revealed that fewer than 20% of U.S. that since physical activity becomes in-
adults engage in regular vigorous activity, creasingly difficult with increased weight,
while approximately 50% lead sedentary this may lead to marked declines in exer-
lives.24,25 These declines in physical activity cise.
among adolescents and adults are unques- We have addressed the underuse of activ-
tionably related to the increased prevalence ity and its association with increased
of obesity in the United States. weight. Later we will address the overuse
During this century, more has changed (abuse) of activity. Discussing both the un-
than physical activity. Despite lower caloric deruse and overuse of exercise is important
intake, changes in dietary habits may play a for understanding the relationship between
role in increased weight. These changes in- exercise and weight regulation. We will now
clude increased fat consumption and meal discuss the role that exercise plays in weight
irregularity (fewer meals are consumed). loss and maintenance and outline possible
These changes must be considered in con- links between them.
32 Basic Concepts of Exercise Physiology

EXERCISE AND WEIGHT have found that combining exercise and di-
CONTROL etary change produces greater weight loss
than diet change alone.
Data reveal a pattern of weight regain It appears, however, that exercise exerts a
when dietary interventions are used alone special impact on weight maintenance. Be-
to control weight, whereas diet combined havior modification dietary programs, ex-
with exercise leads to better maintenance.29 ercise, and combinations of diet and exer-
The importance of exercise for weight con- cise have about the same short-term effect
trol is clear: regular exercise is a central on weight loss.26 Thus, physical activity has
component of losing weight and is the single a modest effect on initial weight loss, per-
best predictor of long-term weight mainte- haps because dietary compliance is good
nance.11'29-37 early in a program and there is little room
Correlational studies reveal consistently for additional weight loss. However, long-
that exercise is associated with successful term effects are clear: exercise is critical for
weight loss and maintenance.35,38-41 Kayman weight maintenance. When the participants
and associates35 studied formerly obese in experimental studies are followed for 1 or
women who lost weight and kept it off and 2 years, striking effects of exercise emerge.
compared them with obese women who had A study by Pavlou and colleagues29 provides
lost weight and regained. Of the maintain- persuasive evidence for the benefit of exer-
ers, 90% were exercising regularly (mini- cise in weight maintenance—regardless of
mum of three times a week for >30 min- the type of dietary intervention. In this
utes), compared to only 34% of the regainers study, 160 male members of the Boston Po-
(Fig. 2-3). lice Department and the Metropolitan Dis-
Experimental weight loss treatment stud- trict Commission were randomly assigned
ies with random assignment and control to one of four 12-week programs (balanced
groups comparing exercise to no exercise caloric-deficit diet [BCDD] of 100 kcal; a
provide the strongest scientific support for ketogenic protein-sparing modified fast
the role of exercise in weight control. Many [PSMF]; and two liquid forms of these bal-
of these studies,29,34,37,42-46 but not all, 47-49 anced and ketogenic diets [DPC-70 and DPC-

Figure 2-3. Maintenance and re-


lapse after weight loss in women.
(Adapted from Kayman et al,35 p
803, with permission.)
Exercise and Regulation of Body Weight 33

800]) and to either an exercise or nonexer- which bolster energy expenditure by as lit-
cise group. Figure 2-4 displays 8- and 18- tle as 200 to 400 calories per day, result in
month follow-up data,29 showing no differ- enhanced maintenance in children.51,52 We
ence between the initial and the 18-month would like to underscore the connection be-
follow-up weight for those who did not ex- tween exercise and weight maintenance, be-
ercise, regardless of the four types of diets cause for many people, keeping the weight
used for weight loss. In sharp contrast, the off is a greater challenge than losing weight
exercise group maintained weight loss. Fur- initially.
thermore, whether one added or stopped
exercise following treatment predicted
weight maintenance. As shown in Fig. 2-5, LIKELY MECHANISMS LINKING
participants who ceased exercise at the end EXERCISE AND WEIGHT
of treatment regained weight, whereas those CONTROL
who started exercise at the end of treatment
maintained their weight loss at an 18-month Conventional wisdom suggests that over-
follow-up. In sum, exercisers were much less weight persons should exercise more, pre-
likely to regain their weight during follow- sumably because "it burns calories." It is
up. No comparable studies have been per- unlikely, however, that exercise exerts its
formed using women, but we may tentatively powerful effects on weight control simply
assume that the findings would be similar. because it burns calories. Exercise can alter
Exercise facilitates maintenance with body weight, body composition, appetite,
both balanced diets29,50 and very low calorie and basal metabolism, and can affect health,
diets.29,37 Furthermore, even minimal in- independent of weight loss. Moreover, ex-
creases in lifestyle activities (e.g., walking ercise can enhance psychologic well-being,
instead of riding, doing errands by walking), improve self-esteem, and increase motiva-

Figure 2-4. Exercise as an adjunct to weight-loss maintenance in moderately obese subjects. Follow-up data after
18 months confirm the long-term effectiveness of exercise intervention for as short a period as 8 weeks. There is no
difference between initial and 18-month follow-up weight for those who did not exercise, 29regardless of the diet used
for weight loss. In contrast, the exercise group maintained weight loss. (From Pavlou et al, p 1121, with permission.)
34 Basic Concepts of Exercise Physiology

Figure 2-5. The addition or removal of learned exercise would appear to be a major contributing factor relative to
weight maintenance. Subjects who ceased exercise regained or demonstrated a strong tendency to return to pre-
study weights. Poststudy introduction of exercise (learned but nonsupervised) creates a positive effect. (Number of
subjects given in parentheses.) (From Pavlou et al,29 p 1122, with permission.)

tion. Although the exact links are not fully for individuals. For example, if metabolic
understood, there are multiple pathways by variables emerge as important, the types
which exercise may aid in weight control and amount of exercise needed to boost
(Table 2-1). metabolic rate should be prescribed. If psy-
Understanding the potential mechanisms chologic mechanisms are important, consis-
is crucial for prescribing exercise programs tency, rather than type or amount, may be
the central feature of a program. As a result,
Table 2-1. POSSIBLE LINKS BETWEEN different programs might be prescribed de-
EXERCISE AND WEIGHT CONTROL pending on the nature of the links between
1. Exercise expends energy.
exercise and weight control.
2. Exercise may decrease appetite.
3. Exercise may enhance metabolic rate.
4. Exercise may preserve lean body tissue. Energy Expenditure
5. Exercise may limit preference for dietary fat.
6. Exercise enhances health. Exercise Expends Energy
7. Exercise improves risk factors associated with
overweight. Any activity uses energy, so any increase
8. Exercise has positive psychologic effects: in activity can aid in weight control. Table 2-
Improves self-esteem and psychologic well-
being, 2 provides values for caloric expenditure of
Decreases mild stress and anxiety, various physical activities. Several impor-
Increases confidence, tant points are highlighted by this chart.
May enhance dietary adherence. First, routine activities like using stairs and
Source: Adapted from Grilo et al.,26 p 257, with walking are useful ways of expending en-
permission. ergy. For example, walking up and down two
Exercise and Regulation of Body Weight 35

Table 2-2. CALORIC VALUES FOR 10


MINUTES OF ACTIVITY
Body Weight Body Weight
125 175 250 125 175 250

Personal Necessities Light Work


Sleeping 10 14 20 Assembly line 20 28 40
Sitting (watching TV) 10 14 18 Auto repair 35 48 69
Sitting (talking) 15 21 30 Carpentry 32 44 64
Dressing or washing 26 37 53 Bricklaying 28 40 57
Standing 12 16 24 Farming chores 32 44 64
House painting 29 40 58
Locomotion
Walking downstairs 56 78 111 Heavy Work
Walking upstairs 146 202 288 Pick and shovel work 56 78 110
Walking at 2 mph 29 40 58 Chopping wood 60 84 121
Walking at 4 mph 52 72 102 Dragging logs 158 220 315
Running at 5.5 mph 90 125 178 Drilling coal 79 111 159
Running at 7 mph 118 164 232
Running at 12 mph 164 228 326 Recreation
Cycling at 5.5 mph 42 58 83 Badminton 43 65 94
Cycling at 13 mph 89 124 178 Baseball 39 54 78
Basketball 58 82 117
Housework Bowling (nonstop) 56 78 111
Making beds 32 46 65 Canoeing (4 mph) 90 128 182
Washing floors 38 53 75 Dancing (moderate) 35 48 69
Washing windows 35 48 69 Dancing (vigorous) 48 66 94
Dusting 22 31 44 Football 69 96 137
Preparing a meal 32 46 65 Golfing 33 48 68
Shoveling snow 65 89 130 Horseback riding 56 78 112
Light gardening 30 42 59 Ping-pong 32 45 64
Weeding garden 49 68 98 Racquetball 75 104 144
Mowing grass (power) 34 47 67 Skiing (alpine) 80 112 160
Mowing grass (manual) 38 52 74 Skiing (water) 60 88 130
Skiing (cross-country) 98 138 194
Sedentary Occupation
Squash 75 104 144
Silting writing 15 21 30 Swimming (backstroke) 32 45 64
Light office work 25 34 50 Swimming (crawl) 40 56 80
Standing, light activity 20 28 40 Tennis 56 80 115
Typing (electric) 19 27 39 Volleyball 43 65 94
Source: From Brownell,135 pp 66-67, with permission.

flights of stairs per day, in place of using an typical fast-food meal consisting of a quar-
elevator, would account for approximately 6 ter-pound cheeseburger, a small order of
Ib of weight loss per year for an average- french fries, and a chocolate shake contains
weight man.53 Second, heavier people burn about 1100 calories. To expend 1100 calories
more calories than normal-weight people through exercise would require running 11
while doing the same activity, because more miles or playing tennis for 3 hours.
energy is required to move the extra mass. However, Bray55 and others have ob-
Despite these facts, many people are dis- served that weight loss in people who exer-
appointed when they learn that even very cise tends to be greater than would be ex-
rigorous physical activities produce rela- pected through the direct expenditure of
tively small energy deficits.54 For example, a energy. Consequently, other physiologic or
36 Basic Concepts of Exercise Physiology

psychologic mechanisms are likely to be im- ventions with weight-cyclers, as they may
portant. bolster RMR.46

Exercise May Enhance Metabolic Rate Appetite and Hunger


Resting metabolic rate (RMR) accounts Exercise May Decrease Appetite
for approximately 60% to 75% of a person's
total daily energy needs.55–57 Thus, small A number of studies with both humans
changes that either decrease or increase and animals have examined the association
RMR can have a dramatic effect on a per- between exercise and appetite.26 A frequent
son's total daily energy expenditure. For in- misconception is that increased activity will
stance, dieting can lead to a rapid and sig- be met with increased food intake, so there
nificant reduction in RMR.55,57–62 Since is no net benefit of the exercise. Although
dieting and weight loss often lower RMR, it the effects of exercise on appetite are com-
is important to find ways to help offset this plex, this regulatory mechanism tends to be
metabolic slowdown.57,63 in effect for only certain levels of activity.26
Exercise may prevent or at least reduce Studies with humans suggest that exercise
the decline in the body's metabolic rate pro- can be effective in regulating appetite. In-
duced by dieting.57,60,64,65 Tremblay and creasing physical activity moderately tends
colleagues65 found a significant increase in to decrease appetite, food intake, and body
RMR (8% of pretraining value) in obese in- weight, whereas increasing exercise to vig-
dividuals who engaged in an 11-week train- orous levels leads to increased appetite but
ing program, despite significant reductions stable body weight.67–70 However, women
in body weight and body fat mass. Broeder may benefit less from the suppression ef-
and colleagues66 observed that 12 weeks of fects of exercise on appetite than do men.67
either high-intensity endurance or resist- Some studies have found that increased
ance training helped to prevent an attenua- physical activity does not decrease appetite
tion in RMR normally observed during ex- in lean women, and that they may in fact eat
tended periods of negative energy balance, more,67,70,71 although their appetite does not
by either preserving the person's fat-free appear to increase beyond the level needed
mass via endurance training, or increasing it to maintain weight.
via resistance training. In contrast, Phinney In sum, exercise is unlikely to increase ap-
and colleagues49 found that when physical petite beyond the level to keep body weight
activity was added while on a very low cal- stable, and often may lead to decreased food
orie diet, it further depressed the metabolic intake. However, a potential problem exists,
rate rather than raised it. These conflicting since people may "believe" they will be hun-
findings underscore the need for more re- grier after they exercise. Monitoring one's
search to define the amount and types of ex- feelings of hunger before and after exercise
ercise that have the most beneficial meta- may help dispel this myth. In fact, some in-
bolic effects. dividuals find it useful to exercise at times
Another dilemma confronting dieters is when they are tempted to overeat.
the potential metabolic consequences of
successive episodes of weight loss followed
Exercise May Limit Preference for
by regain (i.e., weight cycling or yo-yo diet-
ing). There is inconclusive evidence about Dietary Fat
whether weight cycling produces greater Another potential benefit of exercise may
drops in RMR with repeated dieting efforts.26 be its influence on the intake of fat in the
To the extent that this does occur, it may be diet. Several animal studies have found that
particularly important to use exercise inter- weight cycling (repeated cycles of weight
Exercise and Regulation of Body Weight 37

loss and regain) results in a higher con- exists that regular physical activity is asso-
sumption of dietary fat,72,73 accompanied by ciated with good health.82–84 Moreover, even
larger adipose tissue depots.72 Exercise, modest levels of exercise are sufficient for
however, seems to limit this increased di- significant health benefits.79,85,86 Lee87 re-
etary fat selection in weight-cycled female viewed the literature pertaining to women
rats, and reduces the amount of body fat re- and aerobic exercise and concluded that
gained during refeeding periods.73 These middle-aged and older women incur the
findings may have important implications same physiologic and health benefits from
for the treatment of overweight in humans, exercise as do men (see Appendices 2-1 and
since weight cycling is common. 2-2).
One study provides convincing evidence
that even low levels of activity can have
Body Composition a substantial health impact. Blair and
Exercise May Preserve Lean (Muscle) colleagues79 calculated the age-adjusted all-
Tissue cause death rates over an 8-year period in
10,224 men and 3120 women who were ap-
Unfortunately, weight loss is not due parently healthy at baseline. Each person
solely to the loss of body fat. Weight loss is was assigned to a fitness category (based on
accounted for by several changes, including entry maximal treadmill testing), ranging
the loss of both lean and fat body tissue. As from the very unfit (Fitness Level 1) to the
much as 25% of the weight lost by dieting very fit (Fitness Level 5). In all BMI strata,
alone can be lean body mass (LBM).57 In the low-fit men and women had higher death
fact, the often observed slowing of weight rates than moderate- and high-fit subjects.
loss despite continued dieting (reaching a Therefore, physically fit individuals had
plateau) may be due partly to the loss of lean much lower mortality rates (Fig. 2-6). The
tissue, since lean tissue requires more en- largest reductions in risk, however, came
ergy to sustain itself. from moving from very low to moderate lev-
The loss of LBM decreases when exercise els of fitness, not from being extremely ac-
(even low to moderate) is combined with tive. This study and others have helped
diet.74 Several studies have found that regu- counter the notion that one must exercise
lar aerobic exercise, even in the absence of vigorously to obtain the health benefits of
dietary restriction, can produce significant exercise,83,85 and is critically important for
body fat loss with minimal loss of lean tis- overweight persons, in whom adherence is
sue.75–77 More recently, resistance training
has been used to improve the ratio of lean to
fat tissue, which may have the added benefit
of increasing energy expenditure.78 Since in-
creasing LBM and decreasing body fat may
increase metabolic rate (because muscle re-
quires more calories than does fat), exercise
prescriptions with this goal in mind may be
especially useful.

Physical Activity and Health


Prospective studies reveal an inverse re-
lationship between exercise or fitness level
Figure 2-6. The relationship between fitness level and
and morbidity and mortality in overweight death rate in women. (From Brownell,135 p 178, with
men and women.79–82 Substantial evidence permission, based on findings of Blair et al.79)
38 Basic Concepts of Exercise Physiology

greatest in the low to moderate intensity diet was related to adherence to exercise,
range.5,33,51 and that adherence was better in programs
with lower rather than higher caloric expen-
diture.
Exercise Improves Medical Conditions In these studies,51,96 low calorie expendi-
Often Associated with Overweight ture was related to increased dietary adher-
Exercise helps offset medical conditions ence and weight loss. Physiologic factors
prevalent in the overweight. Conditions (e.g., increased metabolic rate) alone can-
such as high blood pressure, elevated cho- not account for the weight loss when the
lesterol, and diabetes improve with exer- amount of exercise is so minimal. These
cise.83 Exercise can provide these benefits findings raise the important issue of
independent of weight loss.53,54,83,88,89 Several whether perceived or actual fitness is the
studies have now shown an association be- key factor in linking exercise to weight con-
tween distribution of body fat (abdomi- trol. Since adherence is better for low- to
nal fat) and increased health risk (e.g., moderate-intensity exercise, low levels may
higher incidence of myocardial infarctions evoke feelings of mastery. Improved self-
and strokes).90 Recent population-based concept due to exercising may then gener-
studies show that physically active men and alize to other aspects of functioning, thereby
women have lower (more favorable) waist- increasing confidence for controlling di-
to-hip ratios.91–94 Therefore, in the absence etary practices. One's perception of being
of clinical intervention data, it seems rea- physically fit thus may be more important
sonable to recommend exercise for over- than physical fitness per se.95 Developing
weight persons with a high waist-to-hip the self-image of an exerciser should en-
ratio, although research is needed to docu- hance self-efficacy, which could lead to in-
ment whether exercise reduces abdominal creased self-determination.
fat. Collectively, these studies show that ex-
ercise of low to moderate intensity is asso-
ciated with improved dietary patterns and
weight loss. These results parallel others
Psychologic Changes
that suggest that exercise may not need to
Exercise has important psychologic ef- be aerobic or of high intensity to engender
fects and is associated with positive psycho- positive psychologic correlates.98–101 In-
logic health. Physical activity improves deed, high-intensity exercise can increase
mood, psychologic well-being (especially negative mood states such as tension, anxi-
immediately following exercise), and self- ety, and fatigue.102 Such negative conse-
concept, and also decreases mild anxiety, quences are important to avoid, since they
depression, and stress.95,96 In persons at- represent potential barriers to exercise ad-
tempting to lose or maintain weight, exer- herence.
cise may relieve stress or other negative In sum, exercise is an important predictor
feelings that precede dietary lapses.97 of success at weight reduction and mainte-
Surprisingly low levels of exercise seem to nance and has numerous health and
complement dieting by increasing dietary psychologic benefits. The link between ex-
adherence.51,96 Rodin and Plante96 reported ercise, weight control, and positive psycho-
that findings from their weight control stud- logic functioning dictates the importance of
ies suggest that people who engage in mod- finding strategies to help individuals be-
est exercise (i.e., jumping jacks for 10 min- come more active. In the next section, we
utes a day, three times a week) are will discuss the challenge of adherence and
substantially more successful at weight con- suggest ways to maximize an overweight
trol than nonexercisers. Similarly, Epstein person's ability to comply with exercise reg-
and colleagues51 found that adherence to imens.
Exercise and Regulation of Body Weight 39

THE CHALLENGE OF Table 2-3. POTENTIAL PHYSICAL AND


ADHERENCE PSYCHOLOGIC BARRIERS TO EXERCISE IN
OVERWEIGHT PERSONS
Poor adherence has long been considered
a challenge in exercise programs. Although Physical Barriers
there have been over 200 studies conducted Poor fitness
Excess weight
in the past 20 years on various determinants
of exercise behavior,103 little systematic in- Psychologic Barriers
vestigation has been conducted on over- Negative experiences
weight persons. We will draw from the exist- Teased by peers
ing studies on adherence relevant for Picked last for teams
Social Anxiety
overweight persons and suggest ways to de- Shame of being observed
velop a program. The reader is referred to Body image dissatisfaction
prior reviews for a more general overview of Lack of confidence
exercise adherence, since they provide Lack of knowledge or experience
a framework from which a program for Source: Adapted from Grilo et al,26 p 264, with
the overweight individual can be estab- permission.
lished.5,26,83,103
physical and psychologic barriers to exer-
Adherence and the cise among overweight individuals is criti-
Demographics of Obesity cal. Table 2-3 summarizes potential barriers
to exercise.
Although most people who are over-
weight know that increased exercise may
help them lose weight, many are unable to Physical Burden
establish and maintain a personal exercise For many overweight persons, exercise is
program. Professionals are confronted with unpleasant due to poor physical condition-
the challenge of helping these individuals ing and excess weight. Weight becomes a
increase their level of physical activity. burden that must be overcome. Increasing
One reason that exercise adherence is a physical activity may be difficult, painful,
special challenge in overweight persons is and fatiguing. Starting a program too quickly
that groups most likely to be overweight are or vigorously may lead to excess fatigue,
also least likely to exercise. Overweight oc- physical discomfort, and injuries, each of
curs with especially high prevalence in mi- which can deter a person from future efforts.
nority populations104,105and in persons with Starting overweight people with a low- to
lower socioeconomic status (SES).21,106 In ad- moderate-paced program is crucial for pre-
dition, the incidence of obesity increases venting injuries, enhancing exercise self-
with age, particularly in women.21,107 For Af- efficacy, and sustaining adherence.
rican-American women ages 45 to 75 years,
obesity rates are as high as 60%.21 Exercise
rates for obese persons, the elderly, minor- Negative Associations
ity groups, and those with low SES, however, Psychologic barriers are sometimes for-
are very low.103,108 midable obstacles for overweight people to
overcome in order to exercise regularly. For
Obstacles to Exercise for the people who have been overweight since
Overweight Individual childhood, early memories such as being
teased, being picked last for teams, and suf-
Several obstacles can impede the transi- fering from poor athletic performance leave
tion from the desire to exercise to the act of many obese persons ashamed and self-con-
exercising. Careful attention to potential scious about their bodies.109,110 Overweight is
40 Basic Concepts of Exercise Physiology

often associated with social rejection.111,112 diet for weight control. It will be important
Consequently, many overweight persons to keep this inexperience in mind when de-
manifest disturbances in areas of life af- veloping exercise programs for these indi-
fected by weight, such as body image, social viduals.
interactions, and self-esteem.112
It is not surprising that thoughts of exer-
cise may evoke unpleasant memories, feel- Adherence Studies
ings of inadequacy, and shame at the pros- Exercise adherence has been understud-
pect of being observed. Not only does the ied with overweight persons. This is unfor-
excess weight add a physical burden, but a tunate, since overweight persons have low
persistent negative body image may dis- exercise participation rates and are at a high
courage a person from exercising with oth- risk for health problems that can be im-
ers, and the lack of self-confidence may pre- proved with exercise.103 For instance,
vent a person from starting an exercise Gwinup115 found that only 32% of overweight
program. It is important to be sensitive to women enrolled in a walking exercise pro-
such experiences and to create a supportive gram remained in the program for 1 year. In
atmosphere so that overweight persons can a prospective study with a large community
identify and initiate activities they enjoy in a sample, Sallis and co-workers116 found that
positive way. Helping overweight persons overweight subjects were less likely to adopt
identify clothing that they feel comfortable exercise than were normal-weight subjects.
wearing, from shoes to workout apparel, and
explaining where to obtain exercise clothing
Intensity
in large sizes is useful and appreciated. It is
essential to encourage patients to experi- Less intense, "lifestyle" activity or mod-
ment with different activities until they ex- erate-intensity activities (those that require
perience pleasure and satisfaction. This less than 60% of maximal capacity, such as
may include exploring community options walking) generally have superior initiation
that provide opportunities to exercise with and adherence rates and lower drop-out
other overweight individuals. rates than do vigorous activities.51,83,87,116,117
This seems to hold true among widely di-
verse groups of people. A large community
Developmental and Gender Issues
study in California116 found that both men
Exercise initiation and maintenance may and women were more likely to adopt mod-
be enhanced by tailoring interventions to erate activity than a vigorous fitness regi-
specific developmental milestones.113 An ex- men. Moderate activity programs showed a
ecutive woman with an ill mother will have dropout rate (25% to 35%) roughly one half
different developmental and practical issues of that seen for vigorous exercise (50%). Ad-
than a teenager with minimal responsibili- ditionally, moderate activity appears to be
ties. Table 2-4 presents features and exam- more readily maintained over the life span,
ples of physical activity programs for sev- whereas participation in vigorous activity
eral important periods. It is also important declines dramatically with age.118 This is es-
to tailor interventions specifically for pecially important to consider with over-
women. For example, many women have not weight persons, since overweight increases
been involved in physical activity programs. with age. In fact, low-intensity exercise (30%
The fact that inactivity is considered a prob- to 45% MHR) has produced significant in-
lem for women reflects a substantial shift in creases in fitness for women in their 60s and
attitudes in the past 25 years.114 Many 70s.119 Overweight children also do better
women over 30 were never encouraged to when low-intensity, lifestyle exercise regi-
participate in team sports or recreational mens are prescribed, versus high-intensity
physical activity; instead, many learned to activities; Epstein and colleagues52,120 found
Exercise and Regulation of Body Weight 41

Table 2-4. PHYSICAL ACTIVITY PROGRAMS FOR SEVERAL MAJOR DEVELOPMENTAL


MILESTONES

Milestone
(Critical Period) Specific Features Goals/Strategies

Adolescence Rapid physical and emotional changes Exercise as part of a program of healthy weight
Increased concern with appearance regulation (both sexes)
and weight Noncompetitive activities that are fun, varied
Need for independence Emphasis on independence, choice
Short-term perspective Focus on proximal outcomes (e.g., body image,
Increased peer influence stress management)
Peer involvement, support
Initial work entry Increased time and scheduling Choice of activities that are convenient, enjoyable
constraints Focus on proximal outcomes
Short-term perspective Involvement of worksite (environmental
Employer demands prompts, incentives)
Realistic goal setting, injury prevention
Coeducational, noncompetitive activities
Parenting Increased family demands and time Emphasis on benefits to self and family (e.g.,
constraints stress management, weight control, well-being)
Family-directed focus Activities appropriate with children (e.g.,
Postpartum effects on weight, mood walking)
Flexible, convenient, personalized regimen
Inclusion of activities of daily living
Neighborhood involvement, focus
Family-based public monitoring, goal-setting
Availability of child-related services (child care)
Retirement age Increased time availability and Identification of current and previous enjoyable
flexibility activities
Longer-term perspective on health; Matching of activities to current health status
increased health concerns, Emphasis on mild- and moderate-intensity
"readiness" activities, including activities of daily living
Caregiving duties, responsibilities Use of "life path point" information and prompts
(parents, spouse, children, or Emphasis on activities engendering
grandchildren) independence
Garnering support of family members, peers
Availability of necessary services (e.g.,
caretaking services for significant other)
Source: From King,113 p 250, with permission.

that lifestyle exercise was superior to pro- extreme effort. Adherence is increased
grammed aerobic exercise for long-term when the activity can be readily incorpo-
weight maintenance (Fig. 2-7). It may be rated into daily life; this, in turn, may en-
that since lifestyle programs are more flexi- hance one's confidence in the ability to per-
ble and easily incorporated into one's daily form physical activity (self-efficacy), which
routine, fewer barriers emerge to preclude may improve adherence. Moderate-inten-
continued participation.51,121 sity activity has many of the health benefits
In sum, prescription of lifestyle activity of vigorous exercise,79,116,122 with the added
over vigorous, programmed exercise may benefit of easier maintenance.83
represent one key to adherence for over-
weight persons. Beginning individuals with
Relapse Prevention Strategies
modest activity goals that are readily incor-
porated into their daily life is preferable to Cognitive behavioral therapy (CBT) pro-
approaches that promote sweat, pain, and grams for exercise adherence that have in-
42 Basic Concepts of Exercise Physiology

Figure 2-7. Percent overweight for


children in three groups (calis-
thenics, programmed aerobic ex-
ercise, and lifestyle exercise) at 0,
2, 6, 12, and 24 months. (From Ep-
stein et al,120 p 351, with permis-
sion.)

corporated components of Marlatt and nance of exercise and proposed that indi-
Gordon's123 relapse prevention model result viduals in the different stages may require
in better physical activity rates at follow- different cognitive and behavioral ap-
up.124–128 Although originally developed for proaches.5,129,130 This model proposes that
other areas such as smoking and alcohol, people proceed through five stages: precon-
this model offers several important sugges- templation, contemplation, preparation, ac-
tions to persons trying to maintain any be- tion, and maintenance, as follows:131
havior change. Three elements are particu-
larly useful for increasing adherence: (1) Precontemplation. Precontemplators do
flexible rather than rigid exercise goals,128 not intend to change their behavior in
(2) training individuals in specific tech- the foreseeable future. These individu-
niques to cope with missed exercise ses- als are unaware of the benefits of exer-
sions,126 and (3) identifying potential situa- cise or are uncertain about whether the
tions that might interfere with exercise or benefits are greater than the negative
lifestyle changes and developing plans for aspects. Movement to the next stage
coping with those high-risk situations and would require acknowledging and be-
setbacks.124 Moreover, relapse training, in coming more aware of the negative as-
comparison to a treatment with no relapse pects of their lack of exercise.
training, results in significantly greater Contemplation. Contemplators are aware
weight maintenance.124 Even minimal inter- of the negative aspects of their lack of
vention strategies such as telephone con- exercise and are seriously considering
tacts or mailings, however, may enhance ad- taking action. Both the positive and
herence and maintenance of weight loss.31,36 negative aspects are considered. Con-
templators have not, however, commit-
ted themselves to the necessary steps
Stages of Change in Exercise Adoption
for change. Exercisers will progress to
and Maintenance
the next stage only after a decision to
Recently, several researchers have sug- change their lack of exercise.
gested that individuals proceed through Preparation. Exercisers in the prepara-
specific stages in the initiation and mainte- tion stage are characterized by a readi-
Exercise and Regulation of Body Weight 43

ness and intention to begin exercise or study134 found a significant interaction be-
change their behavior in the foreseea- tween weight loss treatment and gender:
ble future. These individuals have eval- women did better when treated with their
uated past successes and failures and spouses, whereas men did better when
are on the verge of taking action. Move- treated alone. This study is an example of
ment to the next stage requires setting the potential need to match particular sup-
attainable goals and steps for action. port interventions to the individual's needs
Action. Persons in the action stage begin and characteristics.
to make changes in their behavior. A Equivalent studies looking at social sup-
central focus is setting appropriate port and exercise adherence in overweight
goals and taking action to implement persons have not been done. Our clinical ex-
them. They are aware of the cognitive, perience suggests, however, that there tend
behavioral, and/or environmental fac- to be "solo" versus "social" exercisers. The
tors that may interfere with continued "solo" type individual typically does not de-
progress. sire the company of others and tends to se-
Maintenance. Persons in the mainte- lect activities such as walking or jogging
nance stage focus their attention on alone. A "social" exerciser may prefer an
preventing relapse to former behaviors aerobics class or jogging with a partner. Our
as well as continuing the exercise pat- experience is that a better match between
terns begun in the action stage. Exercis- personality type and type of exercise results
ers in the maintenance stage are con- in a better fit.135
centrating on identifying potential Further research is needed to identify the
situations that may interfere with their factors that predict success with spouse,
continued success. family, or peer interventions for exercise
and dietary adherence with obese persons.
A potential major contribution of this Brownell135 and Brownell and Rodin136 pro-
model for increasing and maintaining exer- vide specific strategies and techniques to
cise lies in its consideration of the readiness aid overweight individuals in identifying
of individuals for change.5 Awareness of and pursuing the type of social support they
variables such as readiness can facilitate pa- need.
tient-treatment matching, thus improving
outcome.132 In fact, a recent study129 found
that exercise programs must accommodate PROGRAM
the large percentage of individuals who are RECOMMENDATIONS
not ready to change their exercise habits.
Research is needed on how to best match Three basic issues confront the clinician:
exercise interventions to patient's stages of (1) the type of exercise to prescribe, (2)
change. The concepts of readiness and ways to maximize adherence, and (3) re-
patient-treatment matching apply not only lapse prevention. Table 2-5 outlines our rec-
to exercise in overweight persons, but also ommendations for exercise programs for
to dieting itself.11 overweight persons. Important elements are
discussed below.
Social Support
Avoid a Threshold Mentality
All health behaviors, including exercise,
are Influenced by social context. Attempts to Any activity, even those not normally la-
improve weight loss by involving significant beled as exercise, can provide substantial
others have met with mixed results,133 per- benefit. It is important to avoid the trap of
haps because of a failure to assess the needs defining physical activity in traditional
and characteristics of the target groups. One terms (70% of maximal heart rate, three
44 Basic Concepts of Exercise Physiology

Table 2-5. RECOMMENDATIONS FOR d. Use exercise following dietary lapses to


MAXIMIZING EXERCISE ADHERENCE IN psychologically regain a sense of control,
OBESE PERSONS mastery, and commitment.
e. Convey philosophy that a lapse can be used as a
General Principles signal to re-initiate small amounts of physical
1. Be sensitive to psychologic barriers. activity (e.g., a 2-minute walk). Encourage
2. Be sensitive to physical barriers. notion that all exercise has a cumulative effect
3. Decrease focus on exercise threshold. on a number of domains (health, mood, sense of
4. Increase focus on enhanced self-efficacy. mastery).
5. Emphasize consistency and enjoyment, not f. Use of minimal intervention strategies, including
amount and type. phone contacts, may foster exercise
6. Begin at a person's level of fitness. maintenance.
7. Encourage people to define routine activities as
Source: Adapted from Grilo et al,26 p 266, with
"exercise."
permission.
8. Focus on compliance and avoid emphasis on
minor metabolic issues (e.g., whether to exercise
before or after a meal).
9. Consider life-span developmental context. times per week, for at least 15 minutes). This
10. Consider sociocultural issues and gender three-part equation (frequency, intensity,
influences. and duration) has been defined as essential
11. Evaluate social support network. for cardiorespiratory conditioning,57 but it
12. Evaluate stage of change and intervene implies an exercise "threshold"—that is,
accordingly.
that exercise must occur in a specific
Specific Interventions amount to be beneficial. This threshold may
1. Prescription motivate physically active or athletic per-
a. Provide clear information about importance of sons, but it may deter others, including the
activity, including the psychologic benefits. overweight. Since any exercise is worth-
b. Maximize routine activity. Define daily activities while, the threshold mentality may hinder
as exercise. more than help. As a professional working
c. Maximize walking (e.g., walk while doing
errands). with overweight people, it is important for
d. Increase use of stairs in lieu of escalators and you to stress that low to moderate levels of
elevators. exercise provide many health,79 psycho-
e. Incorporate a programmed activity that is logic,96 and weight-loss benefits.52,120 Show-
enjoyable, fits with lifestyle, and is feasible as ing overweight persons data such as Figure
client's fitness improves.
2. Behavioral 2-6 can help make this point.
a. Introduce self-monitoring, feedback, and goal-
setting techniques.
b. Identify important targets other than weight Consistency May Be More
loss, including physical changes, increased Important than the Type or
mobility (flexibility, endurance, ease), and Amount of Exercise
lowered heart rate.
c. Suggest that exercise may help soothe emotional We believe the most important question to
distress when risk for overeating is high. ask about exercise is, "Will 1 be doing this a
d. Stimulus control: increase exercise cues (e.g., year from now?" It is important to help pa-
reminders for increasing activity) and decrease tients choose activities that will be enjoya-
competing cues (e.g., do not schedule exercise
when it might conflict with work or social
ble in the long run. Developing a consistent
obligations). form of activity, or a consistent set of activ-
3. Maintenance and relapse prevention ities, is the primary focus. It is preferable to
a. Use flexible guidelines and goal-setting, but have a person regularly play tennis twice a
avoid rigid rules. week and walk for one additional day than to
b. Identify potential high-risk situations for
skipping exercise (e.g., stressful times, busy
run 4 miles/d for a week and then stop en-
schedule). tirely. Lifestyle change, consistency, and
c. Develop plans to cope with high-risk situations. moderation are the key goals.
Exercise and Regulation of Body Weight 45

Provide Thorough Education for the increase in dieting and exercise be-
havior.137 Consumers are frantically search-
It is important to emphasize that even ing for information to achieve the perfect
low-intensity exercise leads to enhanced di-
body. One need only look at the multibillion
etary adherence and weight control. Other- dollar industry to help people look more at-
wise, people will feel they are always exer-
cising "less than they should." Education tractive—diets, exercise paraphernalia,
regarding the physical and psychologic ben- cosmetics, fashions, and various forms of
efits of exercise can expand the patient's un- cosmetic surgery—to realize the extent to
derstanding of the potential benefits. Dis- which there is societal pressure to "look
pelling erroneous notions such as "no pain, good."141
Two beliefs fuel this search for the "ideal"
no gain" is an essential component. Poor
health behaviors can result from inadequate body. The first belief is that the body is infi-
information as well as nonadherence. nitely malleable, and that with the right diet,
exercise program, and personal effort, an in-
dividual can achieve the aesthetic ideal. The
Be Sensitive to the Special second belief is that once the ideal is
Needs of Overweight Persons achieved, there will be considerable re-
Since obese persons have special psycho- wards, such as career advancement, wealth,
interpersonal attraction, and happiness.137
logic and physical barriers to exercise, help-
ing them feel comfortable with exercise and
helping them define even low levels of activ- Ideal Versus Healthy Versus
ity as exercise is an important step toward Reasonable Weight
adherence. Simply conveying understand- The body cannot be shaped at will. Ge-
ing and sensitivity can be helpful. netic factors play a substantial role in limit-
ing our ability to change body weight142,143
and body shape.144 Certain individuals may
SPECIAL ISSUES be prone to gain weight or to have specific
body shapes and these factors may resist at-
It is important to develop "reasonable" tempts to lose weight.11 This creates a mis-
weight-loss goals and healthy attitudes re- match between cultural pressures and bio-
garding exercise and diet. Our culture's pre- logic realities.137
occupation with shape and weight may This collision between cultural pressures
foster unhealthy attitudes. Health care pro- and biologic realities leads to the critical
fessionals should be aware of methods to question of how much control a person has
encourage the pursuit of "reasonable" over weight and shape.145 Scientists have es-
weight-loss goals. timated that current aesthetic ideals (popu-
lar models and actresses) have 10% to 15%
body fat, compared with 22% to 26% for
The Role of Exercise In the
healthy, normal-weight women.137,140,146 For
Search for the Perfect Body instance, a study by Wiseman and
Today's aesthetic ideal is becoming in- colleagues140 found that the majority of Play-
creasingly lean, coupled with an added pres- boy centerfolds and Miss America contes-
sure to be physicallyfit.137–140The symbolic tants were 15% or more below their ex-
connotations of having the ideal body (suc- pected weight, one of the criteria for
cess, self-control, acceptance), current stan- anorexia nervosa. One may speculate that
dards about ideal body weight and shape, many of our "ideals" have eating disorders.
and the overstated health benefits of slen- Miss America contestants work out an aver-
derness are important factors responsible age of 14 hours per week, with some ap-
46 Basic Concepts of Exercise Physiology

preaching 35 hours.147 Although the current weight, but a reasonable weight. Table 2-6
societal ideal is unattainable and/or unreal- lists questions to formulate a reasonable
istic for most people, those who do not meet weight for an individual patient. The calcu-
the ideal are often judged to be lazy, indul- lation of reasonable weight would take into
gent, and lacking willpower. The exercise account the individual's weight history, de-
and weight loss needed to pursue the aes- velopmental stage, social circumstances,
thetic ideal, however, is far in excess of what metabolic profile, and other factors. For in-
is necessary (or recommended) for healthy stance, specific milestones, transitions, and
living.146 life periods affect how women feel toward
Weight-loss programs typically identify their bodies. Females begin life with more
some "goal weight" or "ideal weight" as the body fat than males, and this difference con-
desired outcome. Moreover, whether or not tinues to increase during specific develop-
there are formal goals developed by pro- mental stages over the life span (at puberty,
gram staff, patients often have self-imposed pregnancy, and menopause). These physi-
goals influenced by visualizations of an aes- ologic changes promote weight gain.148 Dis-
thetic ideal. The notion of ideal weight may cussing these developmental transitions
be useful for people who are only mildly can help women develop an acceptance and
overweight (because the ideal is potentially understanding of the physiologic changes
attainable), or for prevention efforts in while also using this information to formu-
which excess weight beyond the standard late a reasonable weight goal.
signals the need for intervention. For many In some cases, reasonable weight and
people, however, the ideal generates a health ideals may be the same (e.g., the in-
search for an elusive goal, which often leads dividual can sustain the effort, calorie re-
to poor long-term results. striction, and exercise necessary to main-
Brownell and Wadden11 suggest that it is tain that weight). On the other hand, the
important to think not only of an ideal reasonable weight might exceed the ideal
weight if biologic, psychologic, develop-
mental, or cultural variables interfere.
Nonetheless, any weight loss is likely to
Table 2-6. QUESTIONS USED AS CLINICAL
CRITERIA TO HELP ESTABLISH A be beneficial, particularly if it can be main-
"REASONABLE WEIGHT" FOR AN tained. For some individuals, a small weight
INDIVIDUAL* loss can lead to significant improvements in
medical conditions149,150 and may have a
1 . Is there a history of excess weight in your parents
or grandparents? number of positive outcomes, such as feel-
2. What is the lowest weight you have maintained as ing more energetic, improved mobility, or
an adult for at least one year? less dependence on others for basic needs.
3. What is the largest size of clothes that you feel Thus, patients should be encouraged to set
comfortable in, at the point you say "I look pretty goals according to several parameters, since
good considering where I have been"? At what
weight would you wear these clothes? this may help to prevent the common trap of
4. Think of a friend or family member (with your age viewing anything but goal weight as failure.
and body frame) who looks "normal" to you. What Tracking changes in physiologic factors that
does the person weigh? are likely to change with increased physical
5. At what weight do you believe you can live with the activity and weight loss (e.g., blood sugar,
required changes in eating and/or exercise?
blood pressure, serum cholesterol); anthro-
*Thesequestions are based in part on criteria proposed pometric measures (e.g., skinfold thickness
by Brownell and Rodin136 and represent clinical im- and circumferences); and psychologic
pression. Research-based criteria have not been
established. changes may provide clear evidence of ac-
Source: Reprinted from Brownell and Wadden,11 p 509, complishment to both patients and health
with permission. professionals. Maintaining these benefits
Exercise and Regulation of Body Weight 47

can be one central goal of treatment, even if males said that they were often, usually, or
more weight is to be lost. always "terrified of being fat."
This "terror of being fat" can cause some
individuals to fall into the trap of excessively
Exercise Overuse (Abuse) exercising while still falling short of the
"perfect body." Many studies evaluate
As we have noted, exercise is an impor- whether people diet or exercise, but mini-
tant aspect of weight control and is gener- mal attention has been paid to why they do
ally viewed as a healthy and positive en- so. A substantial subset of runners may be
deavor. Unfortunately, exercise can become motivated by the fear of being fat and may be
compulsive when done in pursuit of exces- running away from a vision of being fat. Be-
sive thinness. An enduring fear of being fat cause both diet and exercise are excessive
is a hallmark of anorexia nervosa and bu- in some individuals, knowing the motivation
limia nervosa.14,151–153 Vigorous exercise can may be helpful in detecting unhealthy exer-
be a means of weight loss or one of several cise and dietary behaviors. Table 2-7 pre-
tactics used by the individual to counteract sents questions that might aid health profes-
the ingestion of excess calories or deal with sionals in determining whether exercise is
body image concerns. Intense fears of be- excessive or potentially problematic.158
coming fat may exist in people across all These questions are based on our clinical
weight groups and body shapes. experience and may not predict exercise
Even exceptionally lean persons may abuse. Rather, affirmative responses sug-
have body image disparagement. In fact, a gest the need for further evaluation and un-
growing body of research with athletes sug- derstanding of that individual's use (or po-
gests that a disproportionately high rate of tential abuse) of exercise. It is critically
fear of fatness and extreme dieting measures
may exist in these lean and fit individuals.19
One group of researchers investigated the
functional role of exercise in a group of 112 Table 2-7. ASSESSMENT QUESTIONS TO
women who were regular exercise partici- SCREEN FOR POTENTIAL EXERCISE
ABUSE
pants.154 While only a handful were over-
weight, 77% of these relatively slender and 1 . Are there times during the day when you feel
active women wanted to lose weight, and unable to stop thinking about exercise, even if you
most of them were dieting (57%). Another want to?
2. Do you feel anxious, irritable, or uncomfortable
study revealed that 19% of a group of female when you miss an exercise session?
runners met diagnostic criteria for bulimia 3. If you miss an exercise session, do you feel that you
nervosa,155 which is a much higher preva- need to make up for it (e.g., by staying up later or
lence than expected in this group.156 Of the getting up earlier to do it, by increasing the amount
bulimic women, most cited exercise as their of exercise you do the next day)?
4. Have you sometimes exercised despite being
most common compensation tactic for advised against it (i.e., by a doctor, friend, family
binge-eating episodes. Results did not indi- member)? What advice was given? Why did you
cate a particular weight or running profile exercise?
(that is, the bulimics were not significantly 5. Do you try to increase your exercise session (or
different on mileage per week or fastest time add an additional exercise) when you feel you have
overeaten or when you eat "junk foods"?
for a 10-K race than nonbulimics), but did 6. Do you worry about putting on weight or becoming
reveal associated psychologic factors (di- fat if you miss an exercise session?
etary restraint and depression). A survey 7. When you exercise, do you think about the calories
conducted in Runner's World magazine157 re- or the amount of fat you are burning off?
vealed that among the 4000 runners who re- Source: From Grilo and Wilfley,158 p 163, with
sponded, 48% of the females and 21% of the permission.
48 Basic Concepts of Exercise Physiology

important for health professionals to rec- adolescents and adults: Youth risk behavior
ognize possible signs and symptoms of ex- survey and behavioral risk factor surveil-
ercise abuse. lance system. In Methods for Voluntary
Weight Loss and Control. NIH Technology
Assessment Conference, 1992, p 46.
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135. Brownell KD: The LEARN program for vosa: A multidimensional perspective.
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Ahrens AH: Cultural expectations of thin- D: Anorexia nervosa and bulimia among 300
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143. Stunkard AJ, Harris JR, Pedersen NL, effects of an exercise training regimen upon
McClearn GE: The body mass index of women aged 52 to 79. J Gerontol 28:50,
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JMed 322:1483,1990. 160. Badenhop DT, Cleary PA, et al: Physiologi-
144. Bouchard C, and Johnson FE (eds): Fat dis- cal adjustments to higher- or lower-inten-
tribution during growth and later health sity exercise in elders. Med Sci Sports Exerc
outcomes. Alan Liss, New York, 1988. 15:496, 1983.
145. Brownell KD: Personal responsibility and 161. Bassey EJ, Patrick JM, Irving JM, Blecher A,
control over our health: When expectation and Fenten PH: An unsupervised "aerobics"
exceeds reality. Health Psychol 10:303, physical training programme in middle-
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146. Katch FI, and McArdle WD: Nutrition, and responses. Eur J Appl Physiol 52:120,
Weight Control and Exercise, ed 3. Lea and 1983.
Febiger, Philadelphia, 1988. 162. Blumenthal JA, Schocker DD, Needels TL,
147. Trebbe A: Ideal is body beautiful and clean and Hindle P: Psychological and physiolog-
cut. USA Today, September 15, 1979, p 1. ical effects of physical conditioning on the
148. Rodin J, and Larson L: Social factors and the elderly. J Psychosom Res 26:505, 1982.
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and Wilmore JH (eds): Eating, Body Weight Cardiovascular and behavioral effects of
and Performance in Athletes. Lea and Febi- aerobic exercise training in healthy older
ger, Philadelphia, 1992, p 146. men and women. J Gerontol 44:M147, 1989.
149. Blackburn GL, and Kanders BS: Medical 164. Cavanaugh DJ, and Cann CE: Brisk walking
evaluation and treatment of the obese pa- does not stop bone loss in postmenopausal
tient with cardiovascular disease. Am J Car- women. Bone 9:201,1988.
diol 60:55g, 1987. 165. Cowan MM, and Gregory LW: Responses of
150. Wassertheil-Smoller SW, Blaufox MD, pre- and post-menopausal females to aero-
Oberman A, Langford HG, and Davis BR: bic conditioning. Med Sci Sports Exerc
TAIM Study: Adequate weight loss as effec- 17:138, 1985.
tive as drug therapy for mild hypertension. 166. Franklin B, Buskirk E, Hodgson J, et al: Ef-
Paper presented at American Heart Asso- fects of physical conditioning on cardiore-
ciation Conference on Cardiovascular Dis- spiratory function, body composition and
ease Epidemiology, San Diego, 1990. serum lipids in relatively normal-weight
151. Fairburn CG, and Cooper, PJ: The clinical and obese middle-aged women. Int J Obes
features of bulimia nervosa. Br J Psychiatry 3:97, 1979.
144:238, 1984. 167. Getchell LH, and Moore JC: Physical train-
152. Garfinkel PE, and Garner DM: Anorexia ner- ing: Comparative response of middle-aged
54 Basic Concepts of Exercise Physiology

adults. Arch Physical Med Rehab 56:250, 175. Netz Y, Tenenbaum G, and Sagir M: Patterns
1975. of psychological fitness as related to pat-
168. Haber P, Honiger B, Kilicpera M, and Nied- terns of physical fitness among older adults.
erberger M: Effects on elderly people 67-76 Percept Motor Skills 67:647, 1988.
years of age of three-month endurance 176. Seals DR, Hagberg JM, Hurley BF, Ehsani
training on bicycle ergometer. Eur Heart J AA, and Holloszy JO: Endurance training in
5:37,1984. older men and women I. Cardiovascular re-
169. Jarvie GJ, and Thompson, JK: Appropriate sponse to exercise. J Appl Physiol 57:1024,
use of stationary exercycles in the natural 1984.
environment: The failure of instructions and 177. White MK, Yeater RA, Martin RB, et al: Ef-
goal setting to appreciably modify exercise fects of aerobic dancing and walking on car-
patterns. Behav Ther 8:187,1985. diovascular function and muscular strength
170. Jette M, Sidney K, and Campbell J: Effects of in post-menopausal women. J Sports Med
a twelve-week program on maximal and 24:159, 1984.
submaximal work output indices in seden- 178. MacKeen PC, Franklin BA, Nicholas C, and
tary middle-aged men and women. J Sports Buskirk ER: Body composition, physical
Med Physical Fitness 28:59,1988. work capacity and physical activity habits at
171. Juneau M, Rogers F, DeSantos V, et al: Effec- 18-months follow-up of middle-aged women
tiveness of self-monitored, home-based, participating in an exercise intervention
moderate-intensity exercise training in mid- program. Int J Obes 7:61, 1983.
dle-aged men and women. Am J Cardiol 179. Blumenthal JA, Emery CF, Madden DJ, et al:
60:66,1987. Long-term effects of exercise on psycholog-
172. Kukkonen K, Rauramaa R, Siitonen U, and ical functioning in older men and women. J
Hanninen O: Physical training of obese mid- Gerontol, in press.
dle-aged persons. Ann Clin Res 14:80,1982.
173. Lewis S, Haskell WL, Wood PD, et al: Effects
of physical activity on weight reduction in
obese middle-aged women. Am J Clin Nutr ACKNOWLEDGMENTS
29:151,1976.
174. Morrison DA, Boyden TW, Pamenter RW, et We are grateful to Adele Jones for her as-
al: Effects of aerobic training on exercise tol- sistance with the preparation of this manu-
erance and echocardiographic dimensions script.
in untrained postmenopausal women. Am
Heart J 112:561,1986.
APPENDIX 2-1

Research Examining Physiologic Effects of Exercise in Adult Women:


Subject and Program Characteristics
Subjects Program

Session
Time Freq/ Weeks'
Authors N Age Notes (min) Week Intensity Duration Control Group

Adams and DeVries159 23 52-79 17 ex 40 3 60% MHR 13 Last six to volunteer


Badenhop et al.160 32 >60 6 control 50 3 60%-75% MHR 9 Those unable to commit time
26 F, 8 M 30%-45% MHR
14 mod ex
14 low ex
4 control
Bassey et al.161 108 55-60 53 F 20-40 5 ? 12 Randomly assigned to
55 M successive programs
Blumenthal et al.162 24 65-85 18 F 30 3 70%-85% MHR 11 None
6M
Blumenthal et al.163 101 60-83 51 F, 50 M 60 3 70% MHR 16 Random
33 aerobic
34 yoga control
34 wait list control
Cavanaugh and Cann164 17 m = 56 8 ex 25-50 3 60% MHR 52 Those unable to commit time
9 control
Cowan and Gregory165 38 35-66 20 pre-menopause 50 4 80% MHR 9 Randomly assigned to ex or
18 post-menopause control
Franklin et al.166 36 29-47 23 obese 45 4 75% Vo2max 12 None
13 normal
Foster et al.119 16 67-89 9 mod ex 17-42 5 60% MHR 10 None
9 low ex 40% MHR
Getchell and Moore167 23 28-57 11 F 30 3-4 75%-85% MHR 10 None
12 M
APPENDIX 2-1

Research Examining Physiologic Effects of Exercise in AdultWomen:


Subject and Program Characteristics (Continued)
Subjects Program

Session
Time Freq/ Weeks'
Authors N Age Notes (min) Week Intensity Duration Control Group

Haber et al.168 12 67-76 8F 20-40 3 60% MHR 12 None


4M
169
Jarvie and Thompson 16 26-52 12 F 25 7 pulse? 17 Wait list
4M
170
Jette et al. 26 35-53 12 F 30 3 60% Vo2max 12 Random 50% in no-ex gp
14 M
171
Juneau et al. 120 40-60 60 F 50 5 65%-77% MHR 24 Random 50% in no-ex gp
60 M
172
Kukkonen et al. 169 35-50 97 F 30-60 3-6 60%-70% MHR 68 None
72 M
173
Lewis et al. 22 30-52 25 and 60 2 and 2 80% MHR and low 17 None
Morrison et al.174 32 m = 51 22 ex 40 3 65%-75% MHR 32 Random
10 control
Netz et al.175 24 50-64 13 F 60 3 70% MHR 12 None
11 M
176
Seals et al. 24 60-69 14 ex 30 and 60 3 40% MHR and 48* Assignment method not
10 control 85% MHR specified
177
White et al. 72 50-63 36 walk 33 4 70% MHR 24 None
36 dance
*Subjects spent 24 weeks in low-intensity activity and then 24 weeks in higher-intensity.
MHR = age-adjusted maximal heart rate; Vo2max = maximal oxygen capacity.
Source: Adapted from Lee,87 p 134, with permission.
APPENDIX 2-2

Outcomes of Studies Listed in Appendix 2-1


% Physical Outcomes
Drop
Authors Program Type Out Improved No Change Follow-up
159
Adams and DeVries Supervised 0 PWC RSBP None
Vo2max RDBP
O2 pulse Skinfolds
RHR
Weight
Badenhop et al.160 Supervised 0 PWC, EHR None
Vo2max
Bassey et al.161 Home-based 53 EHR 12-week follow-up of 29
phys. activity Ss—some
maintenance
Blumenthal et al.162 Supervised 8 PWC RSBP, RDBP None
Endurance RHR, EHR
Weight
Blumenthaletal. 163 Supervised 4 Vo2max Bone density Blumenthal et al.179
RHR Grip strength
Endurance
Anaerobic threshold
Total cholesterol, LDL
Cavanaugh and Cann164 Supervised 0 RHR Bone density None
Phys. activity %fat
Cowan and Gregory165 Supervised? (not 0 %fat Weight None
specifically stated) V"o2max Lean mass
Endurance
Foster et al.119 Supervised 24 Vo2max Weight None
PWC Blood lactate
EHR
Total cholesterol
HDL
APPENDIX 2-2

Outcomes of Studies Listed in Appendix 2-1 (Continued)


% Physical Outcomes
Drop
Authors Program Type Out Improved No Change Follow-up

Rate-pressure prod
Franklin etal.166 Supervised 0 EHR Lean mass See MacKeen et al.178
Weight
Skinfolds
%fat
ESBP
RSBP, RDBP, EDBP
(obese only)
Getchell and Moore167 Supervised? (not EHR Weight None
specifically stated) Skinfolds
Vo2max
Lactic acid
Haber et al.168 Supervised 0 PWC EHR None
Max work load
Vo2max
Jarvie and Thompson169 Home-based 75 Vo2max None
Skinfolds
Weight
Jette et al. (1970) Supervised 0 Vo2max Blood lactate None
171
EHR
Juneau et al. Home-based 6 Vo2max RHR None
Weight (M only) EHR
%fat
Lean mass
Kukkonen et al.172 Home-based 44 Weight Total cholesterol Program continued for
BMI 17 months; tested at
Vo2max 2, 5, 11, and 17
RSBP, RDBP (M only)
Serum triglyceride (F
only)
Lewis et al.173 Supervised 9 %fat Serum triglyceride None
Weight Total cholesterol
RHR, EHR
ESBP
HDL:LDL ratio
Endurance
MacKeen et al.178 18-month follow-up of 64 Physical activity Yes
Franklin et al.166 Vo2max
%fat
Morrison et al.174 Supervised 22 Vo2max None
Endurance
Cardiac efficiency
Netz et al.175 Supervised ?high EHR
Weight
Seals et al.176 Home-based then 22 Vo2max EHR None
supervised Weight Cardiac output
RHR Blood lactate
ESBP
Blood lactate
Cardiac efficiency
White et al.177 One class/wk supervised 29 RHR
plus home-based Weight
RSBP (down)
RDBP (up)
Muscle strength
Endurance
Endurance = time spent in standard exercise task; EDBP = exercising diastolic blood pressure; HDL = high-density lipoprotein level; RDBP = resting diastolic
blood pressure; RHR = resting heart rate; Vo2max = maximal oxygen capacity; EHR = exercising heart rate; ESBP = exercising systolic blood pressure; LDL
= low-density lipoprotein level; RSBP = resting systolic blood pressure; PWC = physical work capacity.
Source: Adapted from Lee,87 pp 136-137, with permission.
CHAPTER 3 3

Training for Strength


DAVID H. CLARKE, Ph.D.

DEFINITION OF STRENGTH ISOKINETIC EXERCISE


ISOTONIC TRAINING HYPERTROPHY OF SKELETAL
ISOMETRIC TRAINING MUSCLE
ISOTONIC VERSUS ISOMETRIC AGING AND STRENGTH
TRAINING DEVELOPMENT

ECCENTRIC TRAINING

w ith proper training, women can become very strong. However, even with
the same strength-training program, their muscles will not enlarge as much as
those of men. The data-based studies regarding the adaptations resulting from
strength training have come predominantly from research conducted on male
subjects, but, aside from questions raised concerning muscle hypertrophy, it
seems tenable to conclude that principles that apply to men also apply to women.

DEFINITION OF STRENGTH

The first concept that needs to be defined is that of strength. A dictionary


definition is unacceptable, as the terms "tough," "powerful," and "muscular" do
very little to describe what is actually a functional concept. Attempts at obtaining
a true measure of muscle force show that maximum tension varies from 1.5 to 2.5
kg • cm– 2 in vertebrate nonhuman muscles and perhaps slightly higher in the nor-
mal human.1 Thus, if one assumes a value of 3 kg • cm –2 and that large muscles of
the thigh may have 100 cm2 of cross section, the resulting internal force that
could be developed would be 300 kg. Obviously, the amount of useful torque that
can be marshaled during normal activities must be expressed somewhat differ-
ently, since it is not feasible to determine true internal tensions. Thus, it is cus-
tomary to employ the concept of the maximal voluntary contraction (MVC),
which implies that the effort is not submaximal or created by some external stim-
ulus, such as a tetanic shock. Yet one does not know whether the contraction
resulted in any movement, whether it caused any muscle shortening or length-
ening, and, if movement did occur, whether it was at a fixed speed or whether
6O
Training for Strength 61

the tension on the muscle was constant or 10 RM. When an appropriate number of ad-
variable. ditional repetitions of the 10 RM could be
Mastering the terminology helps one not performed, more weight was added and the
only to understand the literature on process continued at this new 10-RM weight.
strength training but also to comprehend It is generally thought that keeping the total
the difficulty faced by investigators in quan- number of repetitions for the three sets
tifying the results of various training regi- somewhere in the range of 30 to 35 enhances
mens. There are few absolute standards the development of muscular strength.
available for the assessment of strength, so Using a program with reduced resistance
a wide variety of procedures has been em- and increased repetitions is thought to em-
ployed. Thus, there has been great difficulty phasize muscular endurance. Houtz, Par-
in making clear comparisons among various rish, and Hellebrandt3 applied the PRE prin-
studies. In the present context, isotonic ciple to female subjects, exercising the
strength (or dynamic strength) of a muscle is quadriceps and forearm muscles, and found
defined as the maximum force that can be that strength more than doubled in 4 weeks.
exerted by that muscle during contraction Thus, it seems probable that the principles
as it moves through its full range of motion. of strength development can be successfully
This can be further delineated into concen- applied to women as well as men.
tric (i.e., shortening) and eccentric (i.e., Interest in refining the procedures for PRE
lengthening) forms. Isometric strength (or for effective strength gains has been the sub-
static strength) is a single MVC performed ject of fairly intense investigation in the
by a muscle group in a static position, in subsequent years. Berger4 has provided
which no shortening or lengthening of the considerable insight into the strength
muscle occurs; isokinetic strength resembles development process, using various combi-
the isotonic contraction, since the joint nations of repetitions, sets (number of re-
moves through a range of motion, but the peated sequences the exercise is performed
speed of movement is held constant. This during a given session), and number of
latter system requires specialized equip- training sessions per week. The criterion
ment to control for a variety of movement measure of muscular strength was the 1 RM,
speeds. defined as the maximum amount of weight
that could be successfully moved through a
complete range of motion for one repetition.
ISOTONIC TRAINING In one study,4 Berger trained six groups for
12 weeks employing the bench press exer-
The usual method of training has been to cise. The groups used resistances of 2, 4, 6,
follow a routine of isotonic exercises. A sys- 8, 10, and 12 RM as their training modalities
tem described by DeLorme and Watkins2 and performed only one set of repetitions
during the period immediately following per training session. At the end of this time
World War II became known as progressive it was found that those training at four, six,
resistance exercise (PRE) and was based on and eight repetitions gained significantly
a set of 10 repetitions maximum (10 RM), greater amounts of strength than any of the
which is the heaviest weight that can be other groups, suggesting that an optimum
lifted and lowered 10 times in succession. target for training would be to perform be-
The manner in which these exercises were tween three and nine repetitions. Using one,
to be employed was first to perform a set of two, and three sets of repetitions and em-
10 repetitions of one half of the weight of the ploying 2, 6, and 10 RM as the weights and
10 RM, then to perform a second set of 10 numbers of repetitions in each set, he found
repetitions at three fourths of the weight of that no advantage was gained by exercising
the 10 RM, and finally to perform as many with heavier loads for 2 RM than with lighter
repetitions as possible at the weight of the loads at 10 RM.5 All combinations resulted in
62 Basic Concepts of Exercise Physiology

significant strength increases, but strength each other. Thus, it appears that strength
gains were maximal when the number of gains are greatest when resistance is high.
repetitions per set was 6 RM for three sets. Since few repetitions can be done using high
To determine whether increasing the num- resistance, a smaller time expenditure is re-
ber of sets beyond three would lead to quired for this training.
greater gains in strength, Berger6 compared The question of whether an effective train-
the strength achieved by performing 2 RM ing response can be elicited for women may
for six sets, 6 RM for three sets, and 10 RM be answered in the affirmative, at least if the
for three sets. He found that all three groups intensity of the training program is high
gained significantly and similarly in enough, and if the program lasts long
strength. This suggests that there is a point enough. Staron et al.9 submitted adult
beyond which gains in muscular strength women to such a program of high-intensity,
should not be anticipated. heavy-resistance exercises of the lower ex-
Berger and Hardage7 studied an alternate, tremity for 20 weeks. A significant increase
somewhat unique modification of the 10-RM in the 1 RM was found for each exercise,
training technique. One group performed 10 even though the subjects trained only twice
repetitions for one set, but each repetition a week.
was adjusted so that it required maximum ef- A consideration for most individuals en-
fort, that is, a 1 RM. Subsequent repetitions gaging in weight training exercise has to do
were performed by gradually reducing the with how long the results of training will per-
load, so that at the 10th repetition the sub- sist if the training frequency is reduced.
jects were still exerting maximum tension. Graves et al.10 recruited both male and fe-
When compared with the regular 10-RM male subjects who trained for either 10 or 18
group, it was found that both groups im- weeks on knee extension, using a 7- to 10-
proved significantly in the 1-RM bench RM regimen. Following this 10-week period,
press after 8 weeks of training. However, the the subjects reduced their training fequency
1-RM group improved significantly more from a minimum of three times per week to
than the regular 10-RM group, indicating the less. Subjects who stopped training alto-
relative importance of intensity of effort in gether lost 68% of the previously gained
training. It should be noted that almost all strength, but those who reduced to 2 and
studies have shown the importance of at- even 1 day per week did not change signifi-
taining maximal tension of the muscles dur- cantly in strength. Thus, a maintenance rou-
ing the course of the exercise. tine would seem to be possible when train-
To compare the strength achieved by per- ing only once per week.
forming many repetitions using light weight It has generally been found that men have
with that gained by performing few repeti- greater absolute amounts of strength than
tions using heavy weight, Anderson and women under most conditions.11–14 Even un-
Kearney8 trained 43 male subjects using trained men who have not been specifically
three sets of 6 to 8 RM for one group, 30 to weight training15 exhibit greater upper and
40 RM for a second group, and 100 to 150 RM lower body strength than female athletes
for a third group, all subjects employing the trained in such sports as basketball and vol-
bench press three times per week for 9 leyball but not weight training. The ratios
weeks. Strength was assessed with the 1-RM comparing the strength of women to that of
bench press, administered before and after men are on the order of 0.46 to 0.73 when
the training. Gains in strength were compared on maximal strength of elbow
achieved by all three groups, but only the flexion, shoulder flexion, back extension,
high-resistance, low-repetition (6- to 8-RM) and hand grip.16 Even though this is the case,
group was significantly stronger than the the established principles of strength train-
other two groups, which did not differ from ing are applicable to both men and women.
Training for Strength 63

ISOMETRIC TRAINING These principles were applied to postpu-


bescent young men who were trained in
The systematic use of isometric training wrist flexion employing the Hettinger and
principles can probably be traced to the Muller strategy17 of two-thirds maximum
1953 report of Hettinger and Muller,17 who tension for one 6-second period each day.
found an average strength increase of 5% This was compared with a technique in
per week when the muscle tension was held which 80% of maximum strength was em-
for 6 seconds at two thirds of maximum ployed in five 6-second periods.23 Both
strength. Even when the tension was in- groups of subjects improved significantly
creased to 100%, or when the length of time after 4 weeks of training, although no signif-
was increased, very little additional im- icant difference resulted between the two
provement was noted. Isometric exercises groups. This suggests that a single 6-second
are normally performed by establishing a bout of isometric exercise on a daily basis is
given joint angle and exerting isometric ten- about as effective for developing muscular
sion at that point in the range of motion strength as bouts practiced more frequently
(e.g., pushing against a stationary wall). As and at higher tensions. Furthermore, high
with isotonic exercises, more than one set school boys and girls training for one con-
may be performed and the length of time for traction per day at 25%, 50%, 75%, and 100%
which the tension is exerted may vary. How- of maximum isometric elbow flexion
ever, the amount of the strength gain sug- strength were compared after training.24
gested by Muller18 has not been confirmed in With the exception of the 25% resistance
subsequent experimentation. It seems more group, all groups became stronger. Thus,
likely that the amount of strength gain would the age of subjects seems to be of little con-
depend on the relative state of training of a sequence for achieving strength-training re-
given muscle group. Thus, the closer one is sults.
to a theoretic maximum, the more likely the Increasing the number of isometric con-
gains are to be small.19 tractions appears to increase the strength
Isometric exercise does increase muscu- gain over a greater range of motion.25 One
lar strength. Josenhans20 employed isomet- group of subjects held three maximum iso-
ric exercises for the grip and the flexor and metric contractions at an elbow joint angle
extensor muscles of the finger, the elbow, of 170 degrees' flexion, each for 6 seconds,
and the knee and found a 40% increase in in a program that was of 6 weeks' duration.
muscular force at the end of the training pe- Another group performed twenty 6-second
riod. When 5-second maximal isometric maximum contractions at the same joint
contractions of the quadriceps muscles angle. Maximum strength was assessed be-
were employed, it was found that strength fore and after the experiment at angles of
increases vary between 80% and 400%.21 both 90 and 170 degrees. All tests used iso-
Morehouse22 separated some trained sub- metric maximum contractions. The subjects
jects into high- and low-strength groups and who performed more contractions gained
employed either 1, 3, 5, or 10 maximum iso- strength significantly at both joint angles,
metric contractions each session. Subjects while those who performed fewer contrac-
increased significantly in strength after 5 tions became stronger only at the angle of
weeks, with similar improvements found re- 170 degrees, the training angle. Thus, the
gardless of level of initial strength. Appar- longer duration of work seems to be more
ently, most individuals can anticipate in- beneficial for strength development, but the
creases in strength regardless of how strong difference is small compared with the
they are at the outset, unless they are al- amount of effort required. The evidence for
ready in an advanced state of muscular joint-angle-specific effects of isometric
training. training is fairly strong, especially when the
64 Basic Concepts of Exercise Physiology

muscles are placed at a relatively short ing of six maximal voluntary contractions at
length. This can be accomplished by manip- a predetermined "sticking point" in the
ulating the joint angle. This specificity of bench press. Analysis of the 1-RM bench
training response is difficult to justify if the press before and after the training program
training adaptation results in changes in revealed significant improvements for both
muscle size. An alternate explanation would groups. However, the experimental group
involve some sort of neural adaptation. was significantly stronger than the control
Thus, Kitai and Sale26 trained the ankle plan- group, providing evidence that isometric
tar flexor muscles of women at a joint angle training enhances the standard isotonic
of 90 degrees employing two sets of five training routine in the achievement of max-
maximal voluntary isometric contractions imum strength.
each held for 5 seconds. The training pro-
gram was 6 weeks in duration and result-
ed in significant increases in voluntary ISOTONIC VERSUS ISOMETRIC
strength at the training angle and the two TRAINING
adjacent angles at 5 and 10 degrees in either
direction only. Examination of peak It has been difficult to compare the im-
strength of maximum twitch of the involved provements in strength resulting from iso-
muscles would point to a neural mechanism tonic and isometric training methods, be-
as being responsible for this joint specificity cause the intensities of training in the two
in isometric training. This point has been re- methods cannot be equated. The ideal
inforced by the finding of an increase in method of comparison would employ two
maximal integrated electrical activity at the exercise regimens, both of equal workloads.
specific training angle.27 However, this has been difficult to accom-
Whereas most investigations have em- plish because isometric exercises involve
ployed either male subjects or a combina- no movement and, thus, are difficult to quan-
tion of male and female subjects, Hansen28'29 tify in physical terms.
used female subjects, employing sustained Despite the problems inherent in compar-
and repeated isometric contractions. The ing isotonic and isometric training effects,
gains in isometric strength in this study Rasch and Morehouse,31 in one of the earlier
ranged from approximately 4% to 11% over studies, compared these two methods by
a 5-week training program. having one group (isotonic) perform a 5-RM
A more recent development has been the procedure involving three sets of arm
incorporation of functional isometrics into presses and curls, taking a total of 15 sec-
an isotonic strength training program. In a onds to perform, and having the other group
given range of motion, it is common to locate (isometric) employ a 15-second exercise pe-
a given point at which the muscle is most in- riod contracting the muscles isometrically
efficient. Weight lifters refer to this as the at two-thirds maximum. Following 6 weeks
"sticking point" of exercise. It represents of training, substantial increases were found
the point at which the force available is for the isotonic exercise group in elbow flex-
equal to the resistance of the weight. To de- ion and arm elevation and for the isometric
termine whether the incorporation of maxi- exercise group in arm elevation alone. No
mum isometric contractions at this point significant gain was made in elbow flexion
would permit the development of strength for the isometric training group. Thus, sub-
beyond that provided by the isotonic exer- jects employing isotonic exercise gained a
cise alone, subjects30 in a control group greater amount of strength than did those
trained on the bench press exercise using an subjects employing isometric exercises. It
isotonic training procedure employing 6 to 8 was suggested by the investigators that
RM, while the experimental group added to some of the strength development may have
this routine an isometric program consist- come from the acquisition of skill, since sub-
Training for Strength 65

jects tended to do better when performing ually increased force to maximum over ap-
familiar procedures. This may help explain proximately 4 seconds. The isotonic group
sudden early increases in strength; they lifted a load equivalent to 75% of maximum
may be attributable more to neuromuscular as far as possible, also over a duration of 4
coordination than to true muscle hypertro- seconds. The exercise involved supination
phy. of the left hand and included 12 male and 8
Isometric and isotonic training proce- female subjects. All training procedures re-
dures were applied to subjects engaging in sulted in a significant improvement in
exercise over a 12-week training period, ex- strength. However, no significant differ-
ercising three times per week and employ- ences were found between the different pro-
ing the larger muscles of the back.32 The iso- cedures. Chui36 noted similar findings. Two
metric group trained with a back pull groups trained with rapid and slow isotonic
machine, contracting the muscles for 6 sec- contractions and were compared with a
onds maximally, three sets per exercise ses- group employing isometric contractions.
sion, and the isotonic group employed back The slow isotonic contractions required a
hyperextension exercises based on an 8- to cadence of 4 seconds for movement and re-
12-RM regimen. Both groups improved sig- covery, and the isometric contractions were
nificantly in muscular strength, but the iso- held for 6 seconds. All groups employed a
metric group gained significantly more weight equal to a 10-RM resistance. No ad-
when an isometric test was employed, and vantage was found for either procedure over
the isotonic group performed better when a the other, although each group gained sig-
test of isotonic strength, such as the 1-RM nificantly in muscular strength. When iso-
procedure, was used. This finding suggests metric contractions were lengthened to 30
that training is specific, a concept that has seconds,37 the development of strength was
received additional support from some found to be less than by isotonic methods by
studies. some 14%, even though both isotonic and
This is in contrast, however, to the work of isometric methods caused increases in mus-
many other investigators who have reported cular strength.
similar gains in strength from these two dif- Thus, it would seem desirable to employ
ferent training methods. For example, isotonic procedures whenever possible.
Berger33 trained subjects for 12 weeks both Gains in strength with isometric exercise
isometrically and isotonically and used the tend to be less consistent than those with
criterion of the 1-RM test. The final strength isotonic exercise, when many training tech-
of the isometrically trained group was not niques and strength tests are employed.
significantly different from seven of the nine
groups that trained isotonically. Coleman34
employed the elbow flexor muscle in a pro- ECCENTRIC TRAINING
gram of 12 weeks' duration, using an isomet-
ric regimen consisting of two 10-second con- As pointed out earlier, isotonic movement
tractions and an isotonic training program can be divided into a concentric (shorten-
consisting of a 5-RM regimen. In this in- ing) and an eccentric (lengthening) phase.
stance, there was an attempt to equate the It is generally concluded that in isotonic
load, duration, and range of motion of the training the greatest force is exerted con-
exercise. No significant difference was found centrically, and this usually means that the
between the two methods, although both muscle is shortening and the load is being
produced significant strength gains. lifted against gravity. Thus, loads are ad-
Salter35 investigated the effect on muscu- justed so that the greatest tension is pro-
lar strength of maximum isometric and iso- vided during this phase. The eccentric
tonic contractions, performed at different phase is ordinarily employed to complete
repetition rates. The isometric group grad- the movement so that the muscle returns to
66 Basic Concepts of Exercise Physiology

its original length. The weight is simply low- 31%. This suggests that during maximum
ered slowly with gravity assistance. It is gen- contractions in eccentric movement, the an-
erally accepted that the amount of weight tagonistic muscles are also contracted. By
that can be lowered maximally is about 20% palpation and by examination of the electro-
greater than that which can be lifted against myographic activity emanating from the an-
gravity. Logically, one would expect the tagonistic muscle, the investigators verified
added force that can be resisted with an ec- that this occurs. This finding illustrates the
centric contraction to be a greater stimulus fact that it is very difficult to isolate muscle
to strength gain. However, scientific studies activity in the human body.
have failed to show any advantage of eccen- More recently, Johnson and co-workers40
tric over concentric training. trained subjects with eccentric movements
Bonde Petersen38 studied isometric, iso- on one arm and leg and concentric move-
tonic, and eccentric contractions in female ments on the opposite arm and leg, three
and male subjects for a period lasting from times weekly for a period of 6 weeks. The
20 to 36 days. Training for each subject con- specific exercises included the arm curl, arm
sisted of one of the following protocols: 1 press, knee flexion, and knee extension.
maximum isometric contraction daily, 10 Each exercise lasted for 3 seconds. The con-
maximum isometric contractions daily, or centric movement was performed against a
10 eccentric contractions daily. It was found resistance of 80% of the subject's 1-RM
that performance of one maximum isometric strength, and the eccentric movement was
contraction daily had no effect on the iso- against 120% of 1 RM. Both exercise pro-
metric strength of the subjects; performance grams resulted in significant gains in
of 10 isometric contractions daily caused no strength in all subjects, but neither training
change in the strength of the female subjects procedure produced gains that were signifi-
but led to a significant increase (13%) for the cantly different from the other. Interest-
male subjects. Subjects who trained with the ingly, the subjects felt that the eccentric
10 daily eccentric contractions failed to training movements were easier to perform
demonstrate any significant increase in than the concentric movements.
strength. This lack of significant strength Jones and Rutherford 41 included a group
gain may have been due to training every of subjects who trained by eccentric and iso-
day rather than every other day. It is possi- metric procedures as well. In each case sub-
ble that insufficient time was allowed be- jects trained knee extensor muscles three
tween training sessions to recover com- times per week for 12 weeks. The isometric
pletely from the previous training session. group held a contraction of 80% of maximum
Singh and Karpovich39 designed a study to for 4 seconds, the concentric group trained
determine the effect of eccentric training on at an intensity of 6 RM, and the eccentric
a muscle group as well as on its antagonist subjects employed a resistance of 145% of
(the opposing muscle complex). In this in- the concentric strength. A large and signifi-
stance, the forearm extensors were given 20 cant increase in isometric force occurred,
maximum eccentric contractions four times and these gains were significantly greater
per week for 8 weeks, and the extensors as than found for both concentric and eccen-
well as the forearm flexors were tested for tric training. Even though there was no sig-
maximum strength before and after training. nificant difference between concentric and
Concentric and isometric strength of the ex- eccentric training regimens, both programs
ercised muscles increased approximately resulted in significant increases in strength,
40%, but the eccentric strength increased approximately 15% for the concentric train-
only 23%. When the antagonistic muscles ing and 11% for eccentric.
were examined, it was found that they also The perception that eccentric exercise is
increased in strength, ranging from 17% to easier to perform would seem to lead sub-
Training for Strength 67

jects to greater compliance and acceptabil- studied groups that exercised isometrically,
ity of such training. However, present equip- isotonically, and isokinetically for a 4-week
ment and common training habits do not period. Significant increases in isometric
permit isolation of eccentric contractions. strength occurred for all groups, with one
Moreover, since a muscle can resist greater exception: when the isotonic group was
force in an eccentric contraction than in a tested at 90 degrees rather than 45 degrees,
concentric contraction, considerably no significant improvement was noted.
greater tension is required in the eccentric None of the groups improved significantly in
movement in order to promote strength the quadriceps muscles when tested for iso-
gains. Thus, in a regular isotonic exercise kinetic work, but all were significantly better
encompassing both concentric and eccen- when the hamstring muscles were tested.
tric contractions, the eccentric phase con- Lesmes and colleagues44 trained male sub-
tributes relatively little to strength devel- jects isokinetically on knee extensors and
opment, since the amount of force is flexors four times per week for 7 weeks, at
undoubtedly well below the training stimu- maximal intensity and at a constant velocity
lus during that phase of the exercise. of 180 degrees/sec. One leg was trained at 6-
second work bouts and the other leg at 30-
ISOKINETIC EXERCISE second work bouts, the ratio of work to rest
providing a method of keeping workloads
The newest form of exercise used for equal. Isokinetic testing was accomplished
training is isokinetic exercise. It is often re- at various intervals between 60 and 300 de-
ferred to as "accommodating resistance ex- grees/sec. Increased peak torque occurred
ercise," because, as explained earlier, it has at both 6 and 30 seconds at all intensities ex-
the unique feature of adjusting to the ability cept those between approximately 180 and
of the muscles throughout the range of mo- 300 degrees/sec. It apparently makes some
tion, so that weak spots are eliminated and difference to train isokinetically, but it de-
the muscles remain under constant tension pends upon the velocity at which one trains
throughout the movement. Actually, few ac- and the speed at which testing occurs.45 In
tivities produce and maintain isokinetic ten- general, training at slow speed (60 degrees/
sion, the arm strokes in swimming and oar sec) does not cause significant peak torque
strokes in rowing being the major excep- increases, and training at fast speed (240 de-
tions. Properly designed equipment offers grees/sec) does not enhance peak torque at
exercise at any one of a range of fixed slow speeds. This is another example of the
speeds; the subject determines the resist- specificity of strength training.
ance by the applied force. Thus, it is possi- Thus, isokinetic exercises are effective in
ble to exercise maximally throughout a full increasing muscular strength but probably
range of motion using any one of several not more so than isotonic training. The abil-
speeds. In isokinetic exercise, increased ity of isokinetic movements to create maxi-
force does not produce increased accelera- mum tension throughout the range of mo-
tion but simply increased resistance. tion is clearly desirable, but methods of
One of the earlier studies42 compared iso- measuring strength may not illustrate this
kinetic training with isotonic and isometric advantage. Perhaps future studies using
training over an 8-week period. The isoki- more refined methods to measure gains in
netic group increased in total muscular abil- strength may show increased gains in
ity by 35%, the isotonic group increased strength with isokinetic training compared
28%, and the isometric group increased ap- with isotonic and isometric training. How-
proximately 9%. Employing quadriceps and ever, the specificity of training and the bias
hamstring muscle exercises on 12 male and inherent in that situation make it difficult to
48 female subjects, Moffroid and associates43 compare results.
68 Basic Concepts of Exercise Physiology

HYPERTROPHY OF SKELETAL ence and muscle cross-sectional area. How-


MUSCLE ever, male subjects had higher absolute val-
ues in strength and hypertrophy than did
Based on the evidence presented so far, females. No significant differences occurred
heavy resistance exercise unquestionably in thigh muscle size. Thus, even though men
results in increases in muscular strength for have larger muscles than women, and
men. While some of the experimentation has women normally have low blood concentra-
included women, the extent of strength de- tions of testosterone, which might be ex-
velopment and muscle hypertrophy for pected to limit the development of muscle
women has not been studied as extensively. size, percentage changes in muscle hyper-
One of the most striking occurrences for trophy resulting from heavy-resistance
men engaged in weight training over an ex- training are similar in men and women. It is
tended period of time is the obvious evi- also true that anabolic steroid administra-
dence of hypertrophy, as shown by changes tion during training will promote muscle hy-
in muscle size accompanying increases in pertrophy in women. However, the adverse
strength. The extent of these changes de- metabolic effects of anabolic steroid use out-
pends on a number of factors surrounding weigh their potential desirability for en-
the strengthening regimen. However, for hancing muscle size.
men, high blood levels of androgens ac- One of the major issues examined over the
count for the increased muscle size. years has been to clarify the nature of hy-
One of the reasons for the reluctance of pertrophy itself. It is clear that size in-
women to engage in serious weight training creases with strength development, and ex-
in the past has been a fear that they would amining the structural changes that take
develop the same hypertrophy that men do place within the muscle has been of interest
and would look "masculine." Wilmore12 ex- to exercise physiologists and biologists. The
amined the strength and body composition term "hypertrophy" denotes an increase in
of 47 women and 26 men before and after a the size or bulk of the muscle fibers, rather
10-week intensive weight-training program. than an increase in the number of muscle fi-
Men were found to be stronger than women bers (called hyperplasia). The question of
in most measures of strength, but women whether the latter actually occurs as a result
were stronger in leg strength per unit of lean of systematic weight training has been the
body weight. Both groups made similar rel- subject of a number of investigations. Early
ative gains in strength, but the degree of studies concentrated on laboratory animals
muscular hypertrophy for women was con- as subjects. Goldspink47 trained mice by
siderably less than that noted for men. means of an exercise requiring the pulling of
However, when hypertrophy is assessed a weight to retrieve food. He reported a 30%
in a more direct manner, such as by com- increase in cross-sectional area of the aver-
puted axial tomography (CAT) scan rather age fiber. He also reported a threefold or
than by a more indirect procedure of deter- fourfold increase in the number of myofi-
mining lean body mass, sex differences in brils per fiber. In working with guinea pigs,
muscle hypertrophy apparently disappear Helander48 found an increase of some 15% in
or become minimal.46 Male and female sub- actomyosin as a result of training. The stud-
jects participated in a 16-week training pro- ies suggest that both hypertrophy and hy-
gram in which significant strength increases perplasia take place.
in elbow flexion, elbow extension, knee flex- One of the earliest studies to report the
ion, and knee extension occurred. Percent- formation of new muscle fibers (hyperpla-
age changes in strength were not signifi- sia) was published by van Linge,49 who sur-
cantly different between males and females, gically implanted the plantaris muscle of fe-
nor was any significant sex difference found male rats into the calcaneus. He cut the
in relative increases in upper arm circumfer- nerve of the other plantar flexors so that the
Training for Strength 69

plantaris muscle would provide plantar flex- occur in skeletal muscle. Many of these en-
ion. The formation of new muscle fibers was zymatic changes are important for the at-
observed at the end of a prolonged heavy tainment of muscle endurance, and many
training period. Several studies have per- occur during weight training. The biochem-
formed muscle tenotomy (severing the mus- ical changes that take place for the weight-
cle tendon at its insertion) to observe the ef- lifting individual are those that are involved
fect of training on the muscle that must take primarily in anaerobic metabolism.
over the function of the cut muscle. A very
rapid hypertrophy takes place after this pro-
cedure, and fiber splitting and branching AGING AND STRENGTH
have been reported, as well as increases in DEVELOPMENT
strength and fiber diameter.
If a muscle is examined repeatedly for sev- It is agreed that aging results in a decrease
eral months after removal of its synergists, in muscular strength. The greatest decline,
hyperplasia is noted.50 Gonyea51 subjected however, usually does not take place until
20 cats to a conditioning program involving after the age of 50. On the other hand,
lifting of weights with the right forelimb strength increases markedly during the ad-
against increasing resistance to receive a olescent years and reaches its highest value
food reward. The program lasted for 34 in the early 20s.53 Klein and colleagues54
weeks, and the flexor carpi radialis muscle compared physically active subjects of ages
was examined to determine any increase in 25 and 66 and found the maximal voluntary
fiber number as a result of low-resistance isometric contraction to be 31% greater in
and high-resistance training. The control the young subjects. Similar results are found
group experienced no difference in the num- with isokinetic torque. A study of young and
ber of fibers in either the left or right limb, old tennis players55 found that at all speeds,
and no difference in the number of fibers ranging from 30 to 240 degrees/sec, the
was found in those that lifted a "light-resist- young subjects generated significantly more
ance" weight. There was a significant in- torque than the older subjects. When com-
crease in fiber number (20.5%) for those lift- pared with inactive subjects, those who
ing the heavy load. This was attributed to were active were significantly stronger, and
muscle fiber splitting. men were stronger than women at all
Male albino rats were trained by Ho and speeds. When the data were presented as a
co-workers52 in a progressive training pro- percentage of maximum rather than as ab-
gram against high resistance for 8 weeks. solute values, women exhibited a larger rel-
The number of fibers per unit of cross-sec- ative decline in torque at high speeds than
tional area increased significantly in the men. It should also be noted that when iso-
weight-lifting animals. The authors sug- kinetic torque is adjusted for fat-free muscle
gested that the fiber splitting appeared to be mass or muscle mass itself, age-related dif-
due to some sort of "pinching off" of a small ferences between men and women are no
segment from the parent fiber or to an invag- longer significant.56
ination of the sarcolemma deep into the Strength increases for older men as a re-
muscle fiber in a plane parallel to the sar- sult of resistance training have been clearly
comeres. identified within 12 weeks.57–59 The same
Under certain conditions, fiber splitting holds true for older women. Charette and
seems to occur, but hypertrophy still re- co-workers60 trained women aged 64 to 86
mains the major mechanism for the size in- years on lower extremity exercises for 12
crease that results from intense weight weeks, exercising three times a week, per-
training. In addition to the structural forming three sets of each exercise at 6-RM
changes evident from hypertrophy and hy- intensity. All seven of the exercises resulted
perplasia, a number of enzymatic changes in significantly greater increases in strength
70 Basic Concepts of Exercise Physiology

than control subjects who did not train. The timal regimen of exercises seems to be six to
average gain was 11.5%. When combined nine repetitions maximum undertaken for
aerobic and anaerobic training was exam- three sets at least three times a week. Most
ined over 50 weeks, Cress and associates61 individuals will be working with a system
found that the exercise subjects, aged 72 that is at the very least an isotonic one. How-
years, responded to regular exercise train- ever, because some of the equipment cur-
ing of the leg muscles some 12% more than rently available is specifically designed to
nontraining control subjects. It is significant maximize the tension throughout the full
to note that the control subjects curtailed range of motion, many people now use what
their normal independent activities by some are called variable-resistance machines (for
34% over the winter months, ostensibly be- example, Universal, Keiser, Nautilus). It
cause of a fear of falling in inclement seems reasonably clear that both isotonic
weather. and isokinetic exercises can be used suc-
Further examination of the relative distri- cessfully for developing muscle strength.
bution and size of fiber types of muscles that Less effective are isometric exercises and
have undergone such training reveals im- eccentric contractions. Gains are greater for
portant clues regarding muscle hypertro- untrained than for trained individuals. Most
phy. If one considers that human muscle is athletes, male or female, find increases in
composed of a combination of essentially strength to come more slowly near the peak
two types of fibers, it helps to understand of training.
the response to a functional overload. One Many of the changes associated with mus-
type responds rapidly to stimulation, and cle hypertrophy are cellular and thus are not
one responds more slowly. The fast type are associated with noticeable enlargement.
called fast-twitch fibers (FT) and fatigue With training, men develop greater muscle
fairly quickly. On the other hand, the slow- hypertrophy than women, because they
twitch fibers (ST) are better adapted to en- have much higher levels of androgenic hor-
durance activities, and thus fatigue less mones, but women can become very strong
quickly. Age-related changes in men reveal through weight training and still not de-
the atrophy of FT fibers,53 but during velop markedly enlarged muscles. The av-
strength training the relative area of the FT erage woman should find a number of ad-
fibers has been shown to increase signifi- vantages in being physically strong as she
cantly.57 The same phenomenon occurs carries out normal activities and engages in
with women. Charette's 12-week training other fitness exercise. This may have special
program60 caused a 20.1% increase in FT significance with increasing age.
fiber area, and Cress's 50-week program61 re- The principles outlined, not the type of
vealed an increase of 46%. No evidence in- equipment available, should form the basis
dicates any change in the percentage of the for exercise selection. Selecting appropriate
fiber types as a result of training, so the con- exercises and establishing an acceptable
clusion can be reached that not only can el- routine are more important to strength de-
derly women safely engage in a resistance velopment than the use of certain commer-
training program, but they can expect cial fitness machines. Training with free
changes to occur as a result of muscle hy- weights can accomplish the same gains in
pertrophy. strength as training with machines. How-
ever, free weights are more likely to cause
injury, since the weights are unsupported
SUMMARY and require somewhat greater skill to use.
The individual should choose the appropri-
The unmistakable conclusion to be drawn ate exercises and engage in a systematic and
is that training for strength is a goal that can progressive program. Early gains are due to
be pursued by both men and women. An op- an increase in motor coordination. Those
Training for Strength 71

gains that occur after several months of parisons in untrained men and women ath-
training are due to greater muscle strength. letes, age 10 to 69. Med Sci Sports 13:194,
Expecting great gains in strength after a few 1981.
16. Yates JW, et al: Static lifting strength and
weeks of training is unrealistic, since the ac- maximal isometric voluntary contractions of
quisition of strength is a slow and progres- back, arm and shoulder muscles. Ergonomics
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about improvement are a common cause of 17. Hettinger TL, and Muller EA: Muskelleistung
attrition among novices. Qualified instruc- und muskeltrainung. Arbeitsphysiol 15:111,
1953.
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19. Muller EA, and Rohmert W: Die geschwindig-
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42. Thistle HG, et al: Isokinetic contraction: A to quadriceps muscle strength and morphol-
new concept of resistive exercise. Arch Phys ogy. Clin Physiol 1:87, 1981.
Med Rehabil 48:279, 1966. 58. Brown AB, McCartney N, and Sale DG: Posi-
43. Moffroid M, et al: A study of isokinetic exer- tive adaptations to weight-lifting in the el-
cise. Phys Ther 49:735, 1969. derly. J Appl Physiol 69:1725, 1990.
44. Lesmes GR, et al: Muscle strength and power 59. Frontera WR, et al: Strength conditioning in
changes during maximal isokinetic training. older men: Skeletal muscle hypertrophy and
Med Sci Sports 10:266, 1978. improved function. J Appl Physiol 64:1038,
45. Ewing JL, et al: Effects of velocity of isokinetic 1988.
training on strength, power, and quadriceps 60. Charette SL, et al: Muscle hypertrophy re-
muscle fibre characteristics. Eur J Appl Phys- sponse to resistance training in older
iol 61:159, 1990. women. J Appl Physiol 70:1912,1991.
46. Cureton KJ, et al: Muscle hypertrophy in men 61. Cress ME, et al: Effect of training on VO2max,
and women. Med Sci Sports Exerc 20:338, thigh strength, and muscle morphology in
1988. septuagenarian women. Med Sci Sports Exerc
47. Goldspink G: The combined effects of exer- 23:752,1991.
cise and reduced food intake on skeletal mus-
cle fibers. J Cell Comp Physiol 63:209,1964.
CHAPTER 4

Endurance Training
THOMAS D. FAHEY, Ed.D.

FACTORS THAT DETERMINE SEX DIFFERENCES IN ENDURANCE


SUCCESS IN ENDURANCE PERFORMANCE
EVENTS
Maximal Oxygen Consumption
Mitochondrial Density TRAINING FOR ENDURANCE
Performance Efficiency Components of Overload
Body Composition Principles of Training

u ntil recently, systematic studies of female endurance athletes were limited.


This is understandable because, before passage of Title IX of the Civil Rights Act
in 1972, the number of women competing in endurance sports was small.1 This
legislation mandated equal opportunity for sports participation in the schools.
The American College of Sports Medicine is perhaps the premier organiza-
tion for the study of sports medicine in the world. In 1971 it published the Ency-
clopedia of Sport Sciences and Medicine.2 This monumental work consisted of over
1700 pages, but fewer than 10 pages were devoted to women and sports medicine.
Until 1958, the longest event in women's track and field in competitions hosted
by the Amateur Athletic Union of the United States was 440 yards. In 1965, top
female runners were threatened with banishment from international competi-
tion if they ran in a race longer than 1.5 miles. In 1984, the first Olympic marathon
for women was held in Los Angeles. Now, it is common for women to compete in
endurance events such as ultramarathons, triathlons, and long-distance swim-
ming and cycling.

FACTORS THAT DETERMINE SUCCESS IN


ENDURANCE EVENTS

Important factors in endurance performance include maximal oxygen con-


sumption (Vo2max), mitochondrial density, performance efficiency, and body
composition.3 Sex differences exist in endurance performance. However, the rel-
ative changes that occur with training and the basic underlying mechanisms that
determine performance are the same in men and women.
73
74 Basic Concepts of Exercise Physiology

Maximal Oxygen Consumption Stroke volume is affected by hemody-


Maximal oxygen consumption (Vo2max) namic and myocardial factors. It is closely
is considered to be the best measure of car- linked to venous return of blood to the heart.
The ability of the heart to contract with in-
diovascular capacity. Many sports medicine
creased force as its chambers are stretched
experts think of it as the single most impor-
(a phenomenon known as preload) is de-
tant measure of physical fitness. It is defined
as the point at which O2 consumption fails to scribed by the Frank-Starling principle.4
Many factors affect preload. These include
rise despite an increased exercise intensity
total blood volume, body position, intratho-
or power output. The greater ability of racic pressure, atrial contribution to ven-
trained people to sustain a high exercise in-
tricular filling, pumping action of skeletal
tensity is largely due to a greater Vo2max.
muscle, venous tone, and intrapericardial
Vo2max is equal to the product of maxi- pressure.4 These hemodynamic factors can
mum cardiac output and maximum arterio- have acute and chronic effects on stroke vol-
venous oxygen difference (Eq. 5-1): ume, oxygen transport capacity, and per-
Vo2max = Qmax (a — v)O2max ception of fatigue. An example is during en-
where Vo2max is the maximal rate of O2 con- durance exercise where there is a decrease
sumption (in L.min –1 ), Qmax is the maxi- in blood volume due to dehydration or a de-
mum cardiac output (L.min –1 ), and (a — crease in venous tone. There is a compen-
v)O2max is the maximum arterial-venous O2 satory increase in heart rate and an increase
difference (mL O2.100 mL – 1 ). Thus, Vo2max in perceived exertion. Increased blood vol-
is a function of the maximum rate of oxygen ume resulting from endurance training also
transport and oxygen utilization. causes an increase in stroke volume.
During the transition from rest to maximal Stroke volume is also affected by myocar-
exercise, there is a linear increase in (a — dial contractility. The contractile force of
v)O2. Arterial oxygen partial pressure (Pao2) the myocardium changes in response to cir-
is well maintained in most athletes during culating catecholamines, the force-fre-
exercise. The increase is due to the decrease quency relationship of the muscle, sympa-
in venous oxygen partial pressure (Pvo2). thetic nerve impulses, intrinsic depression,
There is only a limited capacity to increase loss of myocardium, pharmacologic depres-
oxygen extraction through endurance train- sants, and inotropic agents. Positive inotro-
ing. The venous blood draining the active pic agents include digitalis, and negative
muscles of both trained and untrained peo- inotropic agents include hypoxemia, hyper-
ple during maximal exercise contains rela- capnia, and acidosis.4 Endurance training
tively little oxygen. increases myocardial contractility by in-
To be successful in competition, athletes creasing Ca++-myosin ATPase activity.5.6
in sports that require endurance must have The combination of increased preload and
a large cardiac output capacity. Maximum contractility is responsible for the increase
cardiac output is the product of maximum in stroke volume that occurs with endurance
heart rate (HR) and maximum stroke vol- training. Both of these factors are limited by
ume (SV) (Eq. 5-2): ventricular volume, which is affected by ge-
netic and environmental factors during
Qmax = (HRmax)(SVmax) growth and development. It can be changed
Maximum heart rate is largely determined to some extent through endurance train-
by heredity and age. It is not appreciably af- ing.7,8
fected by training. Because HRmax and (a — The relative importance of genetics and
v)O2max are stable, changes in Vo2max with environment for success in endurance ex-
training are mostly due to changes in stroke ercise is not known. Roost9 examined car-
volume. diac dimensions in trained and untrained
Endurance Training 75

school children. All of the trained children ular wall thickness increases, with no in-
were classified as talented, with potential for crease in left ventricular volume.24,25
eventual success in endurance events. He Changes in Vo2max and in endurance capac-
could find no children with congenitally en- ity are not the same. Endurance perfor-
larged hearts. Thus, considering left ventric- mance can be improved by much more than
ular diameter and wall size, the importance 20%. This is possible by improving mito-
of genetic predisposition for success may chondrial density, speed, running economy,
have been overstated. and body composition.
The oxygen consumption capacity of a
muscle varies according to fiber type.10 The Factors Limiting Vo2max
ability of the mitochondria to extract oxygen
from blood is approximately three to five The limiting factor of Vo2max has been a
times greater in slow-twitch red than in fast- source of debate for many years. Proposed
twitch white fibers. Training can double the limiting factors include cardiac output, pul-
mitochondrial mass.11 It is possible for elite monary ventilation, lung diffusion, and oxy-
endurance athletes to have 10 times the gen utilization.
muscle oxygen-extracting capacity in their A basic experimental design for determin-
trained muscles as sedentary people. Sev- ing if oxygen supply or utilization is the lim-
eral studies have demonstrated a high cor- iting factor involves artificially increasing
relation (r 0.80) between Vo2max and leg the supply of oxygen to the working muscle.
muscle mitochondrial activity.12,13 Cardiac If maximal oxygen consumption does not
output and muscle mitochondrial capacities change, it implies that the ability of the tis-
are important determinants of the upper sues to utilize oxygen is the limiting factor.
limits of Vo2max. On the other hand, if Vo2max increases with
There is a strong genetic component for an artificial increase in O2 to the muscles,
Vo2max.14–17 The well-known exercise phys- cardiac output probably is the limiting fac-
iologist Per-Olaf Åstrand has stated that to tor. Considerable evidence suggests that
become an Olympic-level endurance athlete cardiac output is the limiting factor for max-
requires choosing one's parents carefully! imal aerobic capacity. Vo2max is increased if
Genetic studies typically show less variance the rate of oxygen supply to the muscle is in-
in Vo2max and muscle fiber type between creased through induced erythrocythemia
monozygous twins than between dizygous (blood doping) or breathing 100% oxygen
twins. However, these studies also show during exercise.26–28
that training is critical for success, but the Another technique for investigating this
ability to improve performance in response question is to vary the amount of active tis-
to an endurance training program depends sue requiring increased oxygen during ex-
on genetic factors. ercise.29–31 Adding active arm work during
Intense endurance training results in a maximal treadmill exercise does not in-
maximum increase in Vo2max of approxi- crease Vo2max. This type of exercise in-
mately 20%.18–21 However, greater increases creases the amount of tissue that requires
are possible if the initial physical fitness of oxygen. Several studies have found that
the subject is low.22,23 Only certain types of Vo2peak in isolated quadriceps muscle was
exercise promote the cardiac alterations much higher than when the muscle was ex-
necessary for increased Vo2max. Maximal ercised as part of a whole body maximum ef-
stroke volume can be increased in response fort. 29–31
to a volume overload induced by participa- Many exercisers use expressions such as
tion in sports such as running, cycling, and "I was winded" or "my wind gave out on
swimming. In pressure-overload sports me." There is little evidence that pulmonary
such as weight lifting, however, left ventric- function limits aerobic capacity at sea level
76 Basic Concepts of Exercise Physiology

in healthy people. The lungs have a very The critical mitochondrial Po2 is thought
large reserve that enables them to meet to be 1 mm Hg.37 Indirect estimates of mito-
most of the body's requirements for gas ex- chondrial Po2 during maximal exercise sug-
change and acid-base balance during heavy gest that it is above the critical level.33–35
exercise. Considerable direct and indirect
evidence exists for this:
Vo2max as Predictor of Endurance
• The alveolar and capillary surface areas of Performance
the system are approximately 140 and 125
m2, respectively. The alveolar-capillary If Vo2max were the only predictor of en-
diffusion distance is no more than a few durance performance, then endurance con-
microns thick. Thus, the lung has an ex- tests could be decided in the laboratory. Re-
tremely large diffusion capacity. search scientists could administer treadmill
• Low pulmonary resistance to blood flow tests. The person with the highest Vo2max
allows pulmonary blood volume to in- would be the winner. This might be easier
crease during heavy exercise by three and more precise than conducting athletic
times the value at rest. contests on the track, road, or swimming
• During exercise, the ventilation-perfusion pool. However, Vo2max is only one factor
ratio increases four to five times above that determines success in endurance
rest. events.
• The sigmoid shape of the oxyhemoglobin In a heterogeneous sample, women with a
dissociation curve allows the mainte- high Vo2max tend to run faster in the mara-
nance of resting values of hemoglobin ox- thon.38 This relationship does not exist
ygen saturation even when Pao2 drops when the sample is homogeneous (i.e., the
slightly. runners are of the same ability level).39 For
• Pao2 changes very little during heavy ex- example, Grete Waitz and Derek Clayton had
ercise. A constant Pao2 suggests that the Vo2max values of 73 and 69 mL.kg –1 • min –1 ,
lungs do not limit Vo2max, because Pao2 is respectively. These values were measured
an important indicator of lung function.3,32 shortly after they set world records for the
women's and men's marathons. Yet, Clay-
Dempsy and Fregosi32 presented evidence
ton's time was over 15 minutes faster than
that the lungs may be limiting in some elite
Waitz's. Other factors important for success
male endurance athletes. No such evidence
include speed, the ability to continue exer-
has been presented for elite female athletes.
cising at a high percentage of Vo2max, lactic
In their subjects, Pao2 dropped as low as 65
acid clearance capacity, maximal muscle
mm Hg. There was a significant widening in
blood flow, and performance economy.
the difference between alveolar oxygen par-
A high Vo2max is a prerequisite to per-
tial pressure (PAo2) and Pao2. They hypoth-
forming at elite levels in endurance events.
esized that there was a diffusion limitation
The minimum values for elite female endur-
as well as increased airway impedance at
ance athletes are approximately 65 mL-
high levels of ventilation in these athletes.
kg–1 • min – 1 for runners and cross-country
Others have argued that oxygen supply
skiers. Appropriate values for swimmers are
does not limit either Vo2max or endur-
55 to 60 mL.kg –1 . Cyclists require approxi-
ance.33–36 Rather, the limiting factors are
mately 60 mL.kg – 1 . The evidence for a min-
biochemical. Suggested limiting factors in-
imum aerobic capacity requirement is cir-
clude decreases in the rate and force of myo-
cumstantial:
fibrillar cross-bridge cycle activity. Contrib-
uting factors may be failure of calcium • All elite endurance athletes have high aer-
transport mechanisms or decreased myofi- obic capacities. Even though Vo2max is a
brillar ATPase activity. poor predictor of performance among ath-
Endurance Training 77

letes at the same level of competition, the • Changes in running performance with
variance in maximal aerobic power be- training occur without equivalent changes
tween them is small. in Vo2max.
• Oxygen consumption increases as a func-
Noakes's data suggest that a good predic-
tion of velocity in all endurance events. tor of endurance performance is peak tread-
Although athletes vary somewhat in their
mill velocity. He hypothesized that maxi-
efficiencies, the variance between them is
mum speed may be related to the muscles'
small. capacity for high cross-bridge cycling and
Even though a high Vo2max is important for respiratory adaptations. Respiratory adap-
achieving superior levels of endurance, it is tations may make it possible to prevent the
not the only requirement for success. onset of exercise-induced dyspnea.
Noakes36 has questioned the validity of
Vo2max as a predictor of endurance perfor-
mance. His reservations are based on these Mltochondrial Density
observations: Mitochondrial density is a better predic-
• Much of the evidence of an oxygen limi- tor of endurance capacity than Vo2max. En-
tation during exercise is circumstantial. durance is the ability to sustain a particular
Noakes analyzed the data of the classic submaximal level of physical effort. Davies
studies that established Vo2max as a lab- and co-workers43 showed that cytochrome
oratory benchmark for cardiovascular oxidase activity (which is directly depen-
performance.40–42 He found that most sub- dent upon mitochondrial mass) had a cor-
jects did not show that Vo2 leveled off with relation coefficient of 0.92 with running en-
increasing intensity of exercise at maxi- durance but only 0.70 with Vo2max. With
mum. training, Vo2max increases by less than 20%
• Studies have used transfusion or O2 in most people, but the ability to sustain a
breathing in an attempt to show that O2 given submaximal exercise intensity may in-
transport is limiting. None of these stud- crease by much more. Endurance perfor-
ies have demonstrated that their subjects mance by athletes in sports such as cycling,
reached a plateau in Vo2 during normal ex- running, swimming, and cross-country ski-
ercise. There was no evidence of an O2 ing requires intense effort and maintenance
transport limitation before the experi- of that intensity for a long time. Increased
mental intervention. mitochondrial density may be the key factor
• In blood doping studies, there is a disso- in endurance. It may allow some athletes to
ciation between changes in Vo2max and run, cycle, or swim at high velocities for
performance. Performance changes last longer than others, even though their maxi-
only a few days, while changes in Vo2max mal oxygen uptakes are similar to those of
last longer. slower athletes.
• Exercise at extreme altitudes is not lim- Endurance training results in an in-
ited by high blood lactate levels or by in- creased mitochondrial density in both fast-
dications of central limitations in cardiac twitch and slow-twitch muscle fibers.44 This
or respiratory function. probably plays a major role in improving en-
• Exhaustion during maximal exercise oc- durance. There are several possible mecha-
curs at a lower oxygen consumption dur- nisms. Increased mitochondrial mass may
ing cycling than during running in the increase fat utilization during exercise and
same subjects. thus spare muscle glycogen. It also may im-
• Blood lactate levels at exhaustion during prove muscle lactic acid clearance capacity,
progressive treadmill exercise testing are allowing exercise at a higher intensity.44,45
lowest in elite athletes. A fundamental purpose of energy metab-
78 Basic Concepts of Exercise Physiology

olism during exercise is to generate ATP to • During sustained exercise, lactate produc-
meet the demands of the exercise intensity. tion and removal occur simultaneously
A deficit in ATP causes the athlete to fatigue within active muscle.
quickly. The rate of ATP formation is critical. • Most lactic acid produced during exercise
Fat provides the most energy per gram. Car- is oxidized.
bohydrate is the most important fuel for • During endurance exercise, the turnover
high-intensity endurance exercise, how- and oxidation rates of lactate exceed
ever, because it provides the most ATP per those of glucose.
liter of oxygen. Thus, carbohydrate pro- • Lactate production during both rest and
vides ATP more quickly than does fat.46 exercise is not necessarily associated
At least two problems are associated with with muscle anaerobiosis.
the use of carbohydrates during endurance • Training mainly affects the rate of lactate
exercise: removal rather than its production.

• The supply of carbohydrates is limited. The effects of the increased mitochon-


• The rapid use of carbohydrates during drial mass with training are complex but el-
high-intensity exercise results in a rate of egant. Glycogen is the critical fuel for endur-
lactic acid production greater than its rate ance exercise. However, its use increases
of clearance. Accumulation of lactic acid the risk of its own depletion and lactic acid
may interfere with muscle contraction accumulation due to an excess of lactic acid
and energy metabolism.47,48 production over clearance. The increased
mitochondrial mass that results from train-
Increasing muscle mitochondrial mass may ing prevents lactic acid accumulation. It
help the body to cope with both of these does this by providing the muscles with an
problems. increased capacity for lactic acid oxidation.
The glycogen content of muscle is impor- It also prevents glycogen depletion by al-
tant in endurance capacity. When glycogen lowing an increased use of fats as fuel.
is depleted, fatigue results. During sustained Nevertheless, training is probably not as
exercise, muscle glycogen is the muscle's important as genetics for obtaining a high
principal source of carbohydrate.45 In addi- mitochondrial mass in the muscles required
tion, the rate of glycogen utilization in- for endurance exercise.50 Studies of success-
creases as a function of exercise intensity. It ful male endurance athletes have shown that
is very important, then, for the athlete to they often have a high percentage of slow-
conserve glycogen to maintain the intensity twitch muscle fibers. A high mitochondrial
of exercise at the desired level. Endurance density is a characteristic of these fibers.
training, which results in an increased mi- Tesch and Karlsson51 suggest, however, that
tochondrial mass, increases the capacity of the greater percentage of slow-twitch fibers
the muscle to oxidize fat.49 This slows the in the active muscles of endurance athletes
rate of glycolysis and the catabolism of glu- may be an adaptive response. As discussed,
cose and glycogen. Thus, glycogen is spared Vo2max and mitochondrial density are
and fatigue delayed. highly related. Athletes whose muscles have
The increased mitochondrial mass ac- a high mitochondrial mass also have high
companying training may also increase the Vo2max values.
muscle's ability to remove lactate through
oxidation. For more than 50 years, lactic
acid has been thought of by many as a met- Performance Efficiency
abolic pariah. However, research using ra- Although exercise intensity is the most
dioactive tracer methodology has demon- important determinant of metabolic rate, in-
strated that lactate is an important substrate dividual differences in performance effi-
during exercise:45,50 ciency can be responsible for the difference
Endurance Training 79

between winning and losing. When power ulating ventilation, changing body compo-
output can be measured accurately, effi- sition, improving training status, and im-
ciency can be calculated with the following proving running style.55
equation (Eq. 5-3):52 Other than metabolic considerations,
Change in power output
Efficiency =
Change in caloric equivalent of O2 consumption (100)
Efficiency is decreased by energy lost as technique is probably the most important
heat, by wasted movement, and by mechan- factor affecting performance efficiency. In
ical factors such as wind resistance, friction, swimming, athletes should develop good
and drag. The efficiency of walking and cycle hydrodynamics, using strokes that employ
ergometry is slightly less than 30%.52,53 It is efficient propulsive force and minimize
probable that the efficiency of running, cy- drag. This may contribute almost as much to
cling, swimming, and cross-country skiing at success as improving the physiologic as-
competitive exercise intensities is less than pects of endurance. Likewise, the frequent
that. use of "skating" in cross-country skiing has
High-intensity exercise is not performed revolutionized the sport. Efficient runners
at a steady rate. Vo2 does not account for all are thought to have a lower vertical compo-
of the ATP supplied during exercise; a por- nent in their technique. Efficient cyclists
tion is supplied through anaerobic glycoly- pedal smoothly at high revolutions per min-
sis. Consequently, efficiency cannot be ac- ute without engaging muscle groups that do
curately calculated even when power output not contribute to pedaling speed.57,58 Wind
can be measured. resistance is also a factor in running and cy-
The relative change in efficiency can be cling. It is reduced by wearing clothing that
estimated by measuring changes in oxygen enhances aerodynamics.
consumption under different conditions. Vo2
measurements can measure the effects of Body Composition
wind resistance, mechanical aids (e.g., toe
clips in cycling and wax in cross-country ski- The importance of body composition for
ing), and technique. A fundamental problem endurance varies with the sport. In distance
is determining how much of the efficiency is running, gravity places a greater load on the
due to mechanical factors (i.e., technique athlete than in swimming or cycling. Run-
and equipment) and how much to physio- ners are usually leaner than other endur-
logic factors (i.e., mitochondrial density). ance athletes, and there is less variance in
For example, if one runner seems more effi- body fat among elite performers.59–62 Typi-
cient than another, it is difficult to identify cal fat percentages for female endurance
whether the greater efficiency is due to a athletes are shown in Table 4-1. Although
more efficient running style or to a superior the data are limited, all categories of female
lactic acid clearance capacity. endurance athletes are leaner than seden-
In women, running economy (the oxygen tary women of the same age. Swimmers have
cost of running at a specific speed) has not more body fat than runners, cyclists, and
been shown to be a good predictor of per- cross-country skiers. In long-distance swim-
formance.54 However, when the subject pop- mers, a slightly higher fat percentage de-
ulation is homogeneous, running economy creases drag in the water and provides in-
aids in the prediction of running perfor- sulation against the cold.
mance.55,56 At present, the effect of running Tanaka and Matsuura60 reported that an-
economy on performance is not well under- thropometric factors accounted for 20% to
stood. The most promising methods for 40% of the variance in male distance run-
improving running economy may be manip- ners. This is comparable to the importance
80 Basic Concepts of Exercise Physiology

Table 4-1. BODY COMPOSITION OF ELITE fects may include endocrine and reproduc-
FEMALE ENDURANCE ATHLETES tive function and bone metabolism. These
Sport Percent Fat problems are discussed elsewhere in this
volume.
Distance running65 15.2 It is possible that the higher percentage of
Distance running 62 16.9 body fat found in female swimmers com-
Distance running38 15.3
Distance running54 15.4 pared with that of other endurance athletes
Cross-country skiing66 21.8 may be an advantage. When swimming at
Cross-country skiing67 16.1 comparable velocities, women demonstrate
Cycling20 15.4 a lower body drag than men, probably due to
Swimming68 18.1 more subcutaneous fat. This makes women
Swimming69 17.8
Swimming70 13.7 more efficient at the sport. The ideal fat per-
Swimming71 15.6 centage of the female swimmer is also af-
Swimming59 16.6 fected by fitness and stroke mechanics,
Swimming72 21.7 however. Rennie and co-workers64 have hy-
pothesized that women could swim faster
than men if they could develop comparable
of maximal oxygen consumption. However, physical capacities. The difference between
remember that correlation coefficients de- the sexes in the world record in the 1500-
scribe relationships. They do not mean that meter run is 10%, but there is only a 6% dif-
one factor causes another. These investiga- ference between them in the 400-meter
tors did not study female athletes. Most swim. The lower drag among women swim-
studies have found that female distance run- mers may account for the reduced sex dif-
ners average 16% fat. Levels as low as 6% ference. Top women swimmers today are
have been reported. Christensen and swimming faster than did 1972 Olympic
Ruhling38 have found that female marathon champion Mark Spitz.
runners continue to become leaner the
longer they participate in the sport. Novice
marathon runners were found to have 18% SEX DIFFERENCES IN
fat, experienced marathoners had 16.3%, ENDURANCE PERFORMANCE
and elite marathoners had 15.3%. The aver-
age body fat percentage of a young adult Women's performance times are 6% to
woman in the United States is 25%. 15% slower than men's in most endurance
In running, cycling, and cross-country ski- sports73,74 (Table 4-2). However, there is
ing, excess fat increases the energy cost of considerable variance in performance in
exercise. The ideal lower limit of body fat is specific events. As mentioned, in the 400-
not known. There is a 40% to 60% difference meter swim, the difference between the
between men and women in Vo2max ex- men's and women's world record is slightly
pressed in liters per minute, but these sex more than 6%. The difference in the 80-km
differences are reduced to less than 10% run is almost 44%. Men rode longer dis-
when Vo2max is expressed per kilogram lean tances in the 1988 Olympic cycling road race
body mass.63 Although it appears that low competition (82 km for women and 196.8 km
levels of body fat are desirable for peak en- for men). Yet the average velocity of the win-
durance performance in women, world dis- ning man was only 5% faster than that of the
tance running records have been set by winning woman. There are slightly larger dif-
women with greater than 15% fat. Extremely ferences between the sexes in upper-body
low levels of body fat in female endurance endurance events, such as canoeing.75 Men
athletes may affect other aspects of physi- have relatively more muscle in the upper
ology. Related are the training and dietary body, which allows them to generate more
habits necessary to achieve low body fat. Ef- power.
Endurance Training 81

Table 4-2. COMPARISON BETWEEN MALE same training stimuli.79,80 At elite levels, the
AND FEMALE GOLD MEDAL ENDURANCE training programs of men and women may
PERFORMANCE TIMES IN THE 1992 be closer to each other in intensity than
OLYMPICS
those of lower-level athletes. With years of
Performance Time training, men and women get closer to their
absolute potential. As they approach abso-
Event Male Female
lute potential, it becomes possible to make
Track realistic comparisons of true sex differ-
800-m run 1:43.66 1:55.54 ences.
1500-m run 3:40.12 3:55.30 Absolute maximal oxygen consumption
10,000-mrun 27:46.70 31:06.02 (L.min – 1 ) is typically more than 40%
Marathon 2:13.23 2:32.41
greater in men than in women. This differ-
Swimming ence is reduced to approximately 20% when
200-m freestyle 1:46.70 1:57.90 Vo2max is expressed per kilogram body
400-m freestyle 3:45.00 4:07.18 weight.77 It decreases further to less than
200-m butterfly stroke 1:56.26 2:08.67 10% when expressed per kilogram of lean
200-m breaststroke 2:10.16 2:26.65
200-m backstroke 1:58.47 2:07.06
body weight. Although excess fat is a hand-
icap to women endurance athletes, it does
not appear to account for all sex differences
in performance. Cureton and Sparling78
Some events, such as the 80-km run, are added extra weight to men in an attempt ex-
not contested very often by women. This perimentally to equalize fat masses. They
makes it difficult to determine true sex dif- were able to completely abolish the differ-
ferences from performance comparisons. ences between men and women in relative
Sex differences in the physiologic responses Vo2max, but the following sex differences re-
to exercise are often unclear from the liter- mained: 30% in distance run in 12 minutes,
ature, since many studies have compared 31% in maximum treadmill run time, and
physically fit male subjects with sedentary 20% in running efficiency after the experi-
female subjects. mental intervention. They estimated that fat
Organ size and body mass are probably percentage accounts for 74% of the sex dif-
the most important factors determining the ferences in running performance. The
sex differences in endurance performance. higher Vo2max of men (mL•kg LBM –1 ) ac-
Greater size provides a greater power-out- counted for 20%.
put capacity. Men have more muscle mass, The average man has a larger heart size
both in relative and absolute terms, while and heart volume than the average woman
women have more fat. Greater lean body (in both absolute and relative terms). This
mass is an asset, while more fat weight is a results in a greater stroke volume during
hindrance. Although muscle fiber composi- maximal exercise and contributes to the sex
tion is similar between the sexes, both fast- differences in Vo2max. Even though women
twitch and slow-twitch muscle fibers are have a higher relative heart rate during ex-
usually larger in men.76 ercise, it is not enough to compensate for
Sex differences in endurance performance their lower stroke volume. The resultant
increase as sport levels decrease.75 Thus, smaller cardiac output of women contrib-
there are fewer sex differences between utes to their lower aerobic capacity. The
male and female elite athletes than between amount and concentration of hemoglobin
those of lesser standing. Strength and power also are higher in men, giving male blood
differences are major reasons for sexual di- greater oxygen-carrying capacity. Women
morphism in performance. Males and fe- average about 13.7 g Hb.100 mL –1 , whereas
males make the same relative gains in men average 15.8 g Hb.100 m L – 1 . The differ-
strength when they are subjected to the ence is attributed to the stimulating effect of.
82 Basic Concepts of Exercise Physiology

androgens on hemoglobin production and extreme fatigue that occurs late in the race
to the effects of menstrual blood loss and dif- and is probably related to glycogen deple-
ferences in dietary intake3 (see Chapter 6). tion.
There are few sex differences among the Costill and co-workers89 did not support
factors that account for individual differ- this hypothesis. They used equally trained
ences in endurance performance. In com- male and female subjects who ran for 1 hour
paratively trained men and women, the en- on a treadmill and found that the capacity to
ergy cost of running is similar.8 Bosco and use fat as fuel during exercise was similar in
colleagues82 have shown that the energy men and women. Muscle succinate dehy-
cost of running is related to the percentage drogenase and carnitine palmitoyl transfer-
of fast-twitch fibers. They have hypothe- ase activities were higher in the men, sug-
sized that many women runners have a gesting that the muscle mitochondrial
higher proportion of slow-twitch fibers than density in the male subjects may have been
most men. Women thus may have a predis- greater.
position for a higher running economy dur-
ing submaximal exercise.83 As discussed,
other investigators have found no difference TRAINING FOR ENDURANCE
between men and women in the distribution
of muscle fiber types. Training is an adaptive process. Unfortu-
There are differences in running economy nately, athletes often forget this simple fact.
in different subject populations. This may They attempt overzealous training pro-
partially explain some of the variability in grams with no real thought as to how their
running performance not explained by bodies will respond to them. Consequently,
Vo2max. Most studies show no sex differ- they often become overtrained. They fail to
ences in the percentage of Vo2max sustained improve at a desirable rate, or they become
during exercise.84,85 Although there is some injured.
disagreement among researchers, there do Selye90 formulated a theory of stress ad-
not seem to be any appreciable sex differ- aptation, which has implications for condi-
ences in performance efficiency in running tioning endurance athletes. Selye called his
or cycling.86 theory the general adaptation syndrome
To date, there are no definitive studies on (GAS). He described three processes in-
sex differences in lactate production and volved in the response to a stressor: (1)
clearance rates. No large sex differences in alarm reaction, (2) resistance development,
temperature regulation capacity have been and (3) exhaustion.
found when researchers have made a seri- In the alarm reaction, the body mobilizes
ous attempt to use subjects of equal fitness. its resources. During exercise, cardiac out-
Finally, there are no sex differences in the put increases, blood is directed to active
ability to improve Vo2max through training muscle, and metabolic rate increases. Body
or in the ability to improve endurance per- balance is upset.
formance through interval and continuous The resistance development stage can
exercise programs.87 also be called the adaptive stage. It occurs
Ullyot88 hypothesized that the higher when fitness is increased. It is the goal and
body fat of women could be an advantage purpose of the endurance training program.
during marathon and ultramarathon endur- The athlete must exercise at a threshold in-
ance events, because they may have a tensity to get an adaptive response. This
greater capacity for fat metabolism. Ullyot threshold is individual and is much higher
observed that, unlike male runners, many in elite athletes than in sedentary people.
women runners do not "hit the wall" during When a stress cannot be tolerated, the
the marathon. "Hitting the wall" is sudden, athlete enters the stage of exhaustion. This
Endurance Training 83

stress can be either acute or chronic. Symp- will probably have to be decreased and rest,
toms of acute exhaustion include fractures, increased. The application of each factor de-
sprains, and strains. Chronic exhaustion is pends on variables such as experience, time
characterized by stress fractures, staleness, of year, health, goals, and environment.
and emotional stress. The basic purpose of Intensity is perhaps the most critical of
the training program is to train hard enough the basic overload factors. As discussed, the
to get an adaptive response and improve fit- optimum intensity during endurance exer-
ness, but not so hard as to become injured. cise is tied to carbohydrate metabolism. If
The body adapts specifically to the stress the intensity is too high, lactic acid produc-
of exercise.91 Athletes should develop the tion exceeds clearance capacity. The athlete
type of fitness required in their sport; run- fatigues very quickly, and recovery is more
ners should run and weight lifters should lift difficult. In addition, valuable glycogen
weights. The training program should also stores are rapidly depleted. However, if the
reflect the various components of the activ- pace is too slow, then the athlete does not
ity. For example, if a runner or cyclist must perform up to potential. She will probably
go up hills in competition, then she should lose the race or will not reach the desired
include hill-running or hill-cycling in her level of physical conditioning.
program. There have been many attempts by re-
The varying force requirements encoun- searchers to identify physiologic markers of
tered during exercise are met by recruiting the ideal exercise intensity. Markers include
the number of motor units needed to per- blood lactate, heart rate, ventilation, per-
form the task. Because a motor unit is ceived exertion, and percentage of maxi-
trained in proportion to its recruitment,92 it mum effort. Esoteric physiologic measures
is critical that the motor units that will be such as lactate inflection point have not
used in competition be trained regularly. been very useful. Good measures of training
Therefore, a runner who hopes to run re- load are exercise heart rate, percentages of
peated 6-minute miles in competition must race pace, and perceived exertion. Exercise
include a portion of her training at race pace heart rate helps select a pace that is propor-
or faster. This will condition the motor units tional to oxygen consumption. Training at
that will be recruited during the race. The different speeds helps to train more motor
frequency of different types of training de- units, since different motor units are re-
pends upon the relative importance of their cruited when running fast or slow. Perceived
target motor units. So, while repeated short exertion helps the athlete to adjust the train-
sprints may be the central component for a ing program. She can better respond to in-
100-meter runner, they would be much less jury, illness, glycogen depletion, overtrain-
valuable for a distance runner. ing, and environmental stress. The most
effective programs are those that work the
athlete through a range of distances and in-
Components of Overload tensities according to the requirements of
The amount of overload (training stimu- the sport.
lus) in the training program can be varied by The program should consist of over-dis-
manipulating intensity, volume, duration, tance training and interval training. The pur-
and rest. Intensity is the speed at which the pose of over-distance training (long, slow
activity is carried out. Volume is the number distance) is to increase or maintain Vo2max.
of repetitions. Duration is the distance of It also increases tissue respiratory capacity
each repetition. Rest is the amount of time by increasing muscle mitochondrial den-
between repetitions; each factor is affected sity. As discussed, mitochondrial density is
by the others. For example, if the intensity better correlated with endurance capacity
(speed) is increased, volume and duration than is Vo2max. It is probably the major ben-
84 Basic Concepts of Exercise Physiology

eficiary of over-distance conditioning. Be- "Listen to your body," the third principle,
cause of the principle of specificity, how- is familiar to anyone who has ever read a
ever, a segment of this distance training book or article on exercise. While the ex-
should be conducted close to race pace. pression is a bit weathered, it is true never-
Interval training involves periods of in- theless. The athlete should not adhere to
tense exercise interspersed with rest (see her planned program too dogmatically.
Chapter 1). The nature of the interval train- Sometimes her body needs rest more than
ing program varies with the distance of com- exercise. Most studies show that the abso-
petition. Athletes who run shorter races will lute intensity is perhaps the most important
run shorter, faster distances in training than factor in improving fitness. An overtrained
those who run longer, slower races. Interval athlete is typically not recovered enough to
training increases Vo2max. It does this by in- train at the optimal intensity. A few days'
creasing maximal cardiac output and speed. rest sometimes will allow her to recover
Interval training also teaches pace, builds enough to train more intensely. On the other
speed, and improves lactate removal. It also hand, she should still try to follow a struc-
increases mitochondrial density but is less tured program.
effective than over-distance training. Endurance athletes should train first for
distance and only later for speed. Soft tis-
sues need time to adjust to the rigors of
Principles of Training
training. Ligaments and tendons adjust very
Nine principles of endurance training are slowly to the stresses of exercise.93 The ath-
listed in Table 4-3. They are explicit instruc- lete must prepare her body for heavy train-
tions for applying the general adaptation ing, or injury may result.
syndrome to the training of endurance ath- The fifth training principle suggests that
letes and will result in improved perfor- athletes should cycle the volume and inten-
mance with a minimum risk of injury. sity of their workouts. The practice of alter-
The first principle is to train all year nating between hard and easy training days
round. Athletes lose much fitness through is an application of cycle training (also
deconditioning. They are much more sus- called periodization of training).3 Cycle
ceptible to injury if they try to get in shape training allows the body to recover more
rapidly during the competitive season. The fully and to train hard when hard training is
next principle is related to the first: Get in required.
shape gradually. The athlete should give her Athletes should incorporate base and
body time to adapt to the stress of exercise. peak cycles (workouts) into the competitive
Overzealous training leads to injury and strategy. These cycles are groups of work-
overtraining. outs practiced to improve fitness gradually
(base) or to increase sharpness for compe-
tition (peak). Base or load cycles are char-
Table 4-3. PRINCIPLES OF ENDURANCE acterized by high volume with varying in-
TRAINING tensity. Peak cycles employ low volume and
• Train all year round. high-intensity workouts with plenty of rest.
• Get in shape gradually. Peak cycles are designed to produce maxi-
• Listen to your body. mum performance. The base or load cycle is
• Begin with over-distance training before the foundation for peak performance. How-
progressing to interval training.
• Cycle your training: Incorporate load, peak, and ever, peak fitness can be maintained for only
recovery cycles. a short time, and every peak is gained at the
• Do not overtrain; rest the day before competition. price of deconditioning. Both cycles are
• Train systematically. thus important. The successes of the peaks
• Train the mind. make the hard work of the base period
• Put sport in its proper perspective.
worthwhile.
Endurance Training 85

A difficult training principle to adhere to must also have time for her family and other
is the sixth, "do not overtrain." It contra- aspects of life that are important to her.
dicts the work ethic that is ingrained in so
many athletes. The athlete should think of
conditioning for endurance events as a mul- SUMMARY
tiyear process. Adaptations to training take
place very gradually. Excessive training The determining factors of endurance
tends to lead to overtraining and overuse in- performance include maximal oxygen con-
juries rather than to accelerated develop- sumption, mitochondrial density, perfor-
ment of fitness. Similarly, athletes should mance efficiency, and body composition.
avoid excessive competition because nu- Maximal oxygen consumption is the body's
merous studies have shown that consider- maximum ability to transport and use oxy-
able muscle damage occurs during long-dis- gen and is largely determined by the cardiac
tance races.74 Competing too frequently output capacity. It is improved by about 20%
results in an inability to recover, which de- through training. A high initial value is im-
creases the overall level of conditioning. portant for success in endurance events. Mi-
The seventh training principle tells the tochondrial density is highly related to en-
athlete to train systematically. The athlete durance capacity. It provides a high
should plan an approximate workout sched- oxidative capacity and the ability to use fats
ule for the coming year (or even the next 4 as fuel during exercise. Efficiency is deter-
years), month, and week. Of course, she mined by physiologic factors such as mito-
should not be so rigid that she cannot chondrial density. Mechanical factors, such
change the program owing to unforeseen as technique and wind resistance, are also
circumstances. She should train in a manner important. The importance of body compo-
that will produce a consistent increase in fit- sition for endurance varies with the sport. In
ness. Coaching, training partners, and a sports such as running, cycling, and cross-
training diary will help her workouts be- country skiing, additional fat increases the
come more systematic. Coaching helps the energy cost of exercise. The ideal lower limit
athlete meet her competitive goals. A good of body fat is not known. In long-distance
coach, who is knowledgeable and experi- swimmers, a slightly higher fat percentage
enced, can keep her from repeating common decreases drag in the water and provides in-
training mistakes made by others. The sulation against the cold.
coach will also help motivate the athlete. Sex differences exist in endurance perfor-
Training partners are important for motiva- mance. The relative changes that occur with
tion and competition. The training diary will training and the basic underlying mecha-
help the athlete to formulate her goals and nisms that determine performance are the
to identify effective training techniques. same in men and women. Women trail men
Training the mind is as important as train- by 6% to 15% in most endurance sports, but
ing the body. Successful athletes believe in there is considerable variance in perfor-
themselves and their potential; they have mance in specific events. It is difficult to
goals and know how to achieve them. In en- summarize and quantify physiologic sex dif-
durance training in particular, the athlete ferences reported in the literature; physi-
must be patient and be content with contin- cally fit male subjects were often compared
uous small improvements over many years. with sedentary female subjects.
Finally, sports should be put in their Training is an adaptive process. Athletes
proper perspective. Too often, athletes should not become involved in overzealous
think of themselves solely as runners, cy- training programs that often lead to injury.
clists, or swimmers rather than as human Because the body adapts specifically to the
beings who participate in those activities. stress of exercise, the training program
Although sports are important, the athlete should reflect the various components of
86 Basic Concepts of Exercise Physiology

the activity. Training overload can be varied cytochrome oxidase activity and its relation-
by manipulating intensity, volume, duration, ship to maximal oxygen consumption in man.
and rest. Intensity is most important for Pflugers Arch 349:319,1974.
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CHAPTER 5

Bone Concerns
EVERETT L. SMITH, Ph.D., and CATHERINE GILLIGAN, B.A.

INCIDENCE AND COST OF EFFECTS OF EXERCISE


OSTEOPOROSIS
EFFECTS OF CALCIUM INTAKE ATHLETIC AMENORRHEA AND
BONE
MECHANISM OF EXERCISE
BENEFITS PROBLEMS IN STUDYING EXERCISE
EFFECTS OF INACTIVITY EFFECTS

T tie skeleton is a dynamic tissue, constantly responding to conditions relative


to its two major functions: providing structural support and acting as a mineral
reservoir. Two interacting homeostatic mechanisms control plasma calcium and
skeletal mineral: hormones and mechanical stress. The structural support func-
tion of the skeleton permits movement and protects vital organs. As a reservoir,
the skeleton responds to changes in hormone levels and helps to maintain blood
calcium at about 9.8 mg/dL (Table 5-1).1 Because of the skeleton's dual role,
structural integrity is jeopardized when the demands on the reservoir to main-
tain serum homeostasis are too high. When dietary calcium is inadequate, cal-
cium is mobilized from the bone to maintain serum calcium. If the dietary inad-
equacy is chronic, calcium will be pulled continually from the bone reservoir,
resulting in a negative calcium balance and a net loss of calcium and phosphorus.
Mechanical strain through weight bearing and muscle contraction play a signif-
icant role in maintaining skeletal structural integrity, as bone mineral content
(BMC) changes in response to the mechanical stressors applied. Under balanced
conditions, the hormonal and mechanical homeostatic mechanisms maintain
both skeletal integrity and serum calcium. With aging, however, multiple factors
decline (involving diet, hormonal levels, and mechanical strain), precipitating
bone involution that results in bone more susceptible to fracture and
osteoporosis.
Hormones and mechanical strain interact in maintaining body and skeletal
functions. If stress to specific skeletal segments or to the skeleton as a whole is
significantly reduced, bone mass declines. In severe disuse, such as in bed rest
or spinal cord injury, the mobilization of calcium from bone increases serum lev-
els, decreases parathyroid levels and 1,25-(OH)2 vitamin D, and thus decreases
calcium absorption in the intestinal tract and increases calcium elimination from
89
90 Basic Concepts of Exercise Physiology

Table 5-1. SERUM CALCIUM HOMEOSTASIS


Condition Hormonal Response Metabolic Adaptation to Condition
Low serum calcium Increased PTH Increased fractional calcium absorption
Decreased renal excretion of calcium
Increased active form of vitamin D
Increased bone resorption

High serum calcium Decreased PTH Decreased fractional calcium absorption


Increased calcitonin Increased renal excretion of calcium
Decreased active form of vitamin D
Decreased bone resorption

Decreased gonadal function Decreased gonadal hormones Decreased fractional calcium absorption
Increased sensitivity of bone to PTH
PTH = parathyroid.
Source: Adapted from Smith and Raab,1 with permission.

the kidneys. Generally, the decline in activ- causes 1.3 million fractures at a cost of 3.8
ity with age and the resultant bone and bio- billion dollars each year.2 A major cause of
chemical changes are subtle. Over a long osteoporosis is age-related bone loss. Peak
term, however, inactivity can significantly bone mass is reached at about age 35 in both
reduce bone mass and threaten the integrity men and women. After age 35, women lose
of skeletal structure. up to 1% per year, and they may lose as
much as 4% to 6% per year during the first 4
to 5 years after menopause (Fig. 5-1). Men
INCIDENCE AND COST OF maintain bone mass until about age 50, after
OSTEOPOROSIS which they lose approximately 0.4% to 0.5%
per year. Both peak bone mass and rate of
Osteoporosis is a major public health loss are involved in the likelihood of devel-
problem, affecting more than 20 million peo- oping osteoporosis. In cortical bone, loss
ple in the United States. Osteoporosis occurs primarily on the endosteal surface,

Figure 5-1. Cross-sections of long bones of women aged 30 and 70 years. Note the enlarged medul-
lary cavity and increased porosity of the cortical bone at age 70.
Bone Concerns 91

EFFECTS OF CALCIUM INTAKE

Both cross-sectional and longitudinal


studies of the effect of calcium intake on
bone density or bone loss have produced
mixed results. In a cross-sectional study,
Matkovic and colleagues3 compared bone
mass and fracture incidence in two Yugosla-
vian populations, one with high (947 mg/d)
and one with low (424 mg/d) calcium intake
based on dietary histories. The two groups
were otherwise similar in heredity and en-
vironment. The high-calcium group had a
significantly greater skeletal mass at matu-
rity and a lower fracture incidence in old
age. The loss of bone mass with age was sim-
ilar in the two groups; therefore, the greater
incidence of fractures in the low-calcium
group was attributed to lower peak bone
mass. Other cross-sectional studies have re-
ported slight or nonsignificant correlations
Figure 5-2. A longitudinal section of the proximal end of habitual calcium intake with bone mass or
of a fernur, showing the trabecular structure within the
bone that provides maximum strength in the direction fracture incidence.4,5
of greatest applied pressure. The periosteum is a highly Studies of the effects of calcium supple-
vascular layer covering the surface of the bone; the end- mentation on bone loss have not consis-
osteum lines all interbone surfaces. (Adapted from Van
De Graff, KM: Human Anatomy, ed 2. Dubuque IA, Wil- tently demonstrated a positive effect. In 3-
liam C. Brown Publishers, 1988, p 158.) and 4-year studies, we found that calcium
supplementation reduced cortical bone loss
in the arm (radius, ulna, and humerus) of el-
derly and middle-aged postmenopausal
with some loss on the periosteal surface women, but did not affect bone loss in
(Fig. 5-2). In trabecular bone, the trabeculae premenopausal women.6,7 Horsman and
are thinned and may be entirely resorbed colleagues8 also reported that calcium sup-
(see Fig. 11-2). In the spine, horizontal sup- plementation reduced bone loss over 2 to 3
port trabeculae are lost preferentially, years at cortical forearm sites. In a 2-year
which reduces bone strength more than in- study, Prince and associates9 found that cal-
dicated by the density alone (Fig. 5-3). In cium supplementation combined with exer-
conjunction with this decreased bone mass, cise decreased forearm bone loss signifi-
the internal structure of bone also changes. cantly compared to exercise alone. Other
Osteons are decreased in size and increased 2-year studies, however, failed to detect a
in number. Micropetrosis increases with la- significant difference in radius bone loss be-
cunae filled by calcium depositions. These tween calcium-supplemented and control
qualitative bone changes, in addition to the groups.10-12 Riis13 reported that calcium sup-
decreased BMC, contribute to a greater frac- plementation reduced cortical bone loss in
ture potential. the proximal forearm but did not retard tra-
Although bone mass plays a significant becular bone loss in the distal radius or
role in determining bone strength, it is not spine in women who were recently post-
the sole determinant. The geometric struc- menopausal. Similarly, Ettinger and co-
ture of the tissue, determined by habitual workers14 found no effect of calcium supple-
stresses, collagen orientation, ligaments, mentation for 1 year on spine bone loss in
and muscle tone, is also important. early postmenopausal women.
92 Basic Concepts of Exercise Physiology

Figure 5-3. Varying degrees of osteoporosis in lumbar vertebrae. Upper left: Normal structure in a 63-year-old man.
Lower left: The longitudinal trabeculae are narrowed and some broken ones are seen in the center of this vertebra,
showing mild osteoporosis in a 65-year-old woman; the horizontal trabeculae are conspicuously reduced. Upper right:
Pronounced osteoporosis in a 70-year-old woman. There is clear-cut breaking off of numerous longitudinal trabeculae
on the right and the left. Lower right: High-grade osteoporosis in a 71-year-old woman. The vertebral body has almost
completely collapsed; there are several gaps in the trabecular structure, and the restraining bone is transformed, with
formation of new longitudinal trajectories. (From Remagen, W: Osteoporosis. Sandoz Ltd., Basle, Switzerland, 1989,
Fig. 31, with permission.)

Recent studies have investigated the ef- dius. In late postmenopausal women (>5
fects of calcium supplementation on bone years since menopause), however, the CCM
loss in premenopausal and early and late group did not change significantly at any site
postmenopausal women. Premenopausal measured; those taking CC declined signifi-
women who increased their dietary calcium cantly in spine BMD; and the placebo group
by an average of 610 mg/d (n = 20) did not declined significantly in spine and femur
change significantly in spine bone mineral BMD. Radius BMD declined significantly
density (BMD), while control subjects de- less in the CCM than in the placebo group.
creased significantly (n = 17). Calcium sub- When subgroups of the late postmenopausal
jects thus had significantly greater spine groups were formed on the basis of calcium
BMD after 30 and 36 months than did control intake (<400 mg or 400 to 650 mg), differ-
subjects.15 Dawson-Hughes and colleagues16 ences in change between groups were ap-
studied 301 women with self-selected diets parent only for the lower-calcium subgroup.
low in calcium (<650 mg/d), who were di- After 2 years, CCM had significantly reduced
vided into placebo, calcium citrate malate loss in spine, femur, and radius BMD com-
(CCM) supplement, and calcium carbonate pared to the placebo group, and CC had sig-
(CC) supplement groups and followed for 2 nificantly reduced loss in radius BMD com-
years. In early postmenopausal women (<5 pared to the placebo group. Elders and
years since menopause), the groups did not associates17 found that calcium supplemen-
differ in BMD loss in the spine, femur, or ra- tation retarded spine bone loss in early
Bone Concerns 93

postmenopausal women during the first ness. The degree of bone hypertrophy or at-
year, but not the second year, of their trial. rophy is proportional to the difference in
Finally, a team led by Nelson18 randomly as- magnitude and frequency of the mechanical
signed postmenopausal women (mean age stimulus from normal. The habitual stimulus
60, mean years since menopause 11) to a to weight-bearing segments (legs and spine)
high-calcium (831 mg) or placebo (41 mg is much greater than that to the non-weight-
calcium) drink over a 1-year period. Half of bearing areas (ribs, arms, and skull). For ex-
the subjects in each group participated in a ample, the impact of the heel during walking
1-year walking program. Calcium supple- (1.2 to 1.5 times body weight) is much
mentation significantly reduced loss in greater than the stress applied by muscle
femur BMD but did not affect loss in the contractions in the arm during activities of
spine, radius, or total body calcium. daily living. Therefore, the calcaneus is nor-
Some of the differences among calcium in- mally under greater stress than the radius,
tervention studies may be due to the wide so when both bones are free of stress (as in
variety of forms and doses of calcium used, the case of the astronauts in space), more
along with differences in study length, sub- bone is lost from the calcaneus than from
ject selection criteria, menopausal age, self- the radius.22,23
selected dietary intake, sites measured, and Numerous models of the mechanism by
sample sizes. It is reasonable to hypothesize which bone responds to mechanical forces
that calcium supplementation affects mainly have been proposed. Bassett24 indicated
cortical bone in the early postmenopause19 that bone functions as a piezoelectric crys-
but may affect other sites in premenopausal tal, generating an electric charge in propor-
and late postmenopausal women. Calcium tion to the forces applied to the bone.
supplementation may be most beneficial for Carter25 hypothesized that mechanical
women with a self-selected diet low in cal- forces produce microfractures, which stim-
cium and can be expected to avert only that ulate osteoclastic remodeling coupled with
portion of bone loss due to inadequate cal- osteoblastic activity. A recent study, how-
cium intake.20 ever, did not detect evidence of microfrac-
ture in rats subjected to 20,000 loading cy-
MECHANISM OF EXERCISE cles per day for 5 or 6 days.26 Other ways in
BENEFITS which exercise may stimulate osteoclastic
and osteoblastic activity include increased
While evidence is accumulating that phys- hydrostatic pressure and streaming poten-
ical activity increases bone mass, research tials.
on the mechanisms by which bone is af- Whereas dynamic loading produces hy-
fected by mechanical stress is still in its pertrophy, static loading of bone produces
early stages. little or no hypertrophy.27 For a bone to hy-
In 1892, Wolff21 hypothesized that in- pertrophy, dynamic stimuli must exceed
creased weight bearing compresses and a threshold magnitude and frequency.
bends the long bones, increases mineral Lanyon28 demonstrated that both the rate
content, and consequently strengthens and magnitude of strain influenced bone re-
bones, making them less liable to fracture modeling. He monitored BMC in the radii of
under similar loads. Weight bearing (grav- sheep under artificial stimulation. No
ity) and muscle contraction are the two change occurred with a strain magnitude
major mechanical forces applied to bone. less than that of the animal's normal walking
Both hypodynamic and hyperdynamic load. With higher strain magnitude and nor-
states affect bone balance. Bone mass in- mal strain rates, periosteal bone deposition
creases with greater weight-bearing activity increased slightly on both convex and con-
or muscle contraction or both and de- cave surfaces. When both magnitude and
creases with immobilization or weightless- rate were higher than in normal walking,
94 Basic Concepts of Exercise Physiology

periosteal bone increased substantially. osteal surface than did untrained sows. Min-
Other studies have applied more precisely eral apposition rate was also higher, at both
quantified stress to bone. Rubin and the periosteal (76%) and intracortical oste-
Lanyon29 applied controlled mechanical onal (23%) levels. Similarly, evidence of al-
loads, using a pneumatically operated de- tered cellular activity was found in trained
vice, to rooster ulnae isolated from muscular adult rats.34 Bone density and trabecular
stress. Bone mass decreased if no load was number, thickness, and density were signif-
applied, remained fairly constant at 4 cycles icantly higher in trained animals than in
per day of normal (2000 microstrain) mag- controls after 18 and 26 weeks of exercise.
nitude, and hypertrophied at a normal mag- The mineral apposition rate and bone for-
nitude loading for 36 cycles per day (each mation rate were significantly higher in
cycle about 2 seconds). The hypertrophy trained animals, while the percentage of
from 3600 cycles per day and 36 cycles per eroded and labeled perimeter tended to be
day did not differ. In a similar study, the lower in the trained animals. This study sup-
number of loading cycles was held constant, ports the concept of Frost35 that increased
and the magnitude of the strain varied.30 activity stimulates modeling and depresses
Bone change was directly proportional to remodeling.
the strain. Bone atrophied at strains below Bone requires a specific magnitude and
1000 microstrain, and cross-sectional area rate of stimulus in order to hypertrophy.
increased with strains over 1000 micro- Within a normal range of stimulus specific to
strain. It appears that the magnitude of the the individual's activities and genotype,
strain is more important than the frequency bone neither atrophies nor hypertrophies.
of application. Beyond or below this range, bone will
Recent studies have investigated the bio- change, as shown in Figure 5-4. Increased
chemical and histologic sequelae of bone hypertrophy with increased stress will
loading. The mechanism by which strain occur only to a point, however. Severe, re-
produces an osteogenic cellular response petitive loading may result in fatigue dam-
has not been delineated. Histomorphome- age such as that seen in the metatarsals, cal-
tric data show increased osteoclastic func- caneus, tibia, and femur of some soldiers
tion with disuse and increased osteoblastic and distance runners. Fatigue damage may
function with increased activity. Neither also occur in untrained persons who in-
mature osteoclasts nor osteoblasts, how- crease their activity levels more rapidly
ever, seem to respond directly to changes in than the bone can adapt. At the other end of
skeletal strain. Osteocytes (that number up the spectrum, bone atrophies with lessened
to 20,000 per cubic millimeter), however, mechanical stress due to bed rest and
may respond to changes in skeletal strain by weightlessness.
the production of chemical transmitters act-
ing on bone precursor cells. Using an in
vitro core biopsy model in the presence of EFFECTS OF INACTIVITY
[3H]uridine, El Haj and colleagues31 ob-
served an increase in radioactive osteocyte Donaldson and associates36 observed
RNA compared to nonloaded specimens. three men for 30 to 36 weeks of bed rest, and
Pead and Lanyon32 reported that within 5 Hulley and colleagues37 observed five men
days after a single period of skeletal loading, for 24 to 30 weeks of bed rest. Calcium bal-
quiescent surface-lining cells were trans- ance was negative throughout bed rest, with
formed into active, bone-forming osteo- 0.5% to 0.7% of total body calcium lost per
blasts. month. In the weight-bearing calcaneus,
Cellular activity at the femur midshaft in- bone loss was magnified; 25% to 45% was
creased significantly in sows training on a lost after 36 weeks. After remobilization, cal-
motor-driven treadmill for 20 weeks.33 cium balance became positive within a
Trained sows had a 27% greater active peri- month, and BMC was regained at a rate sim-
Bone Concerns 95

Figure 5-4. Effect of mechanical loading on bone mineral content. (Adapted from Carter.25)

ilar to the rate of loss, reaching baseline lev- less severe than that of a patient at bed rest,
els in about 36 weeks. Krolner and Toft38 ob- but extended over 10 to 20 years, the resul-
served a 0.9% per week loss from the lumbar tant bone loss can be a major contributor to
spine in individuals at bed rest for an aver- the development of osteoporosis.
age of 27 days because of a disk protrusion. Human studies of immobilization are rare,
LeBlanc and co-workers39 recently reported but a number of animal studies have been
the effects of 17 weeks of bed rest and 6 performed. Kazarian and Von Gierke40 im-
months of recovery at various skeletal sites. mobilized 16 rhesus monkeys in full body
During bed rest, subjects lost significantly in casts for 60 days. Bone from the immobi-
BMD at the calcaneus (10%), femur trochan- lized animals had fewer and thinner trabec-
ter (5%), lumbar spine (4%), femur neck ulae, smaller trabecular plates, reduced tra-
(4%), tibia (2%), and total body (1.4%). The becular surfaces, and reduced cortical
lumbar spine, femur trochanter, and tibia thickness compared with bones of control
BMD tended to increase during the recovery animals. Remodeling occurred in the trabec-
period, but only calcaneus BMD increased ulae of the femoral neck, which "corre-
significantly. The distal and proximal radius sponded in position and curvature to the
and ulna BMD did not decrease significantly lines of maximum compressive stress," so
during bed rest or increase significantly dur- that only those trabeculae necessary for
ing recovery. Regional analysis of total body structural integrity were retained. The com-
scans showed significant decreases in lum- pressive strength of the immobilized bones
bar spine, total spine, pelvis, trunk, and legs was two to three times less than that in con-
during bed rest, with a significant increase trol animals. Cortical bone at the sites of
in head BMD during bed rest. Pelvis and muscle and tendon attachments also was
trunk BMD increased significantly in the re- significantly weaker than in control animals.
covery period. In the average woman, the Young41 and Niklowitz42 and their co-
usual decline in activity is more gradual and workers investigated changes in the tibias of
96 Basic Concepts of Exercise Physiology

monkeys during 7 months of immobilization of the studies in which it was measured. Aer-
and up to 40 months of recovery and remo- obic weight-bearing activities increased
bilization. Remodeling was obvious within 1 spine bone density in middle-aged post-
month of immobilization. After 10 weeks, menopausal women18,52 and women with os-
they observed endosteal resorption, sub- teoporosis.53 In two of these studies,52,53 the
periosteal loss, striations in the cortex (in- total BMD of L2 to L4 was increased signifi-
dicative of resorptive cavities), surface ero- cantly compared to controls, while in the
sion in the juxta-articular areas (patella and third study,18 trabecular (LI to L3) but not
femoral condyles), and thin, irregular exter- total BMD was affected. Physical activity
nal lamellar bone. During 6 months of im- programs incorporating arm exercises in-
mobilization, BMC decreased 23% to 31% creased BMD or decreased bone loss in the
and bending stiffness, 36% to 40%. Normal radius and ulna.6,54-56 In our study56 of mid-
bending properties of the bone were re- dle-aged women, the response to exercise
stored within 8V2 months of recovery and re- appeared to be independent of menopausal
mobilization, but BMC did not return to nor- status. A few studies that used primarily aer-
mal even after 15 months. New primary obic weight-bearing training reported no ef-
haversian systems were generated during fects on radius9,57,58or spine59 bone density.
that time, and by 40 months the cortex con- The bone hypertrophy observed in
tained many secondary and tertiary osteons weightlifters, along with animal studies
and approached normal BMC. showing a linear relationship between strain
and bone hypertrophy, have led to several
studies utilizing resistance training to pro-
EFFECTS OF EXERCISE mote BMD. In studies comparing general
aerobic training with and without additional
Numerous studies indicate that bone den- resistance training, groups performing the
sity is responsive to mechanical loading. strength training tended nonsignificantly to
The effect appears to be primarily local and increase more in calcium bone index (bone
proportional to the level of strain placed on mass of the central third of the skeleton ad-
the bone. The most convincing evidence justed for body size) and radius BMD than
that bone hypertrophy is localized appears those in aerobic training alone.54,60 Resist-
in studies of both young and old tennis play- ance training alone, however, has not con-
ers, whose dominant humerus was up to 35% sistently altered BMD. In studies of pre-
higher in BMD than was the nondominant menopausal and early postmenopausal
arm.43- 45 In studies of athletes, the amount of women, exercise subjects increased in ver-
hypertrophy was related to the loading ap- tebral BMD relative to controls.61,62 Calca-
plied by the sports activity. For example, neus, femur, and distal forearm BMD, how-
weightlifters had higher bone density in the ever, were not significantly affected in these
spine and femur than aerobic athletes,46-49 studies. Postmenopausal women receiving
whereas swimmers did not have signifi- estrogen replacement therapy (ERT) and
cantly higher spine density than did seden- assigned to a resistance-training group in-
tary subjects.48-50 In one study, male swim- creased significantly in spine, total body,
mers had significantly higher vertebral BMD and radius BMD; only in the radius, how-
than sedentary subjects, but no difference ever, did the change differ significantly from
could be detected between swimming and that in the women receiving ERT alone.63 In
sedentary women.51 contrast to these positive findings, pre-
Intervention studies have confirmed the menopausal women in a resistance-training
beneficial effect of exercise at various skel- program lost significantly more vertebral
etal sites, including the spine, radius, calca- BMD than did controls.64 Postmenopausal
neus, and tibia. Femur BMD, however, was women who performed back extensions
not significantly affected by exercise in any with light weights for 2 years did not differ
Bone Concerns 97

significantly in vertebral BMD change from rheic controls; in fact, oarswomen tended to
controls.65 be higher in vertebral BMC. Regular, oligo-
menorrheic and amenorrheic oarswomen
did not differ significantly. This may have
ATHLETIC AMENORRHEA AND been the result of small sample sizes, how-
BONE ever, since a nonsignificant trend toward
lower density in groups with menstrual dis-
Whereas exercise is associated with an in- turbances was apparent. The authors spec-
crease in bone density, excessive exercise ulated that the increased muscular work of
leading to amenorrhea is associated with a the back involved in rowing and weightlift-
decrease in bone density. Investigators have ing exerted a protective effect on vertebral
found that unlike hyperprolactinemic, ano- bone. Wolman and colleagues,85 however,
rexic, and premature menopausal women, did not confirm this protective effect on ver-
amenorrheic athletes do not have signifi- tebral trabecular bone density. A two-way
cantly lower cortical (radius) BMD, 66-74 but analysis of variance incorporating men-
they are significantly lower than eumenor- strual status and sports activity showed a
rheic athletes in vertebral HMD67-69,73,75 and significant (negative) factor for amenorrhea
vertebral trabecular density.72,75-79 Men- and a significant (positive) factor for rowers
strual history is an important determinant of but no significant interactive effect.
vertebral density even among currently eu- The apparent immunity of the radius and
menorrheic athletes.68,77 Athletes with men- susceptibility of the spine to menstrual dis-
strual disorders also appear more prone to orders indicates that there may be a differ-
injury and stress fractures.68,80-82 ential responsiveness of cortical and trabec-
A few longitudinal studies have demon- ular bone. A recent study included
strated that subjects with menstrual distur- additional sites of varying trabecular com-
bances lose more vertebral bone. Prior and position.68 Ninety-seven athletes were
colleagues83 studied 66 women without overt graded for menstrual history, and BMD was
menstrual irregularities, who varied widely measured at the spine (LI to L4), femur neck
in their exercise patterns. They found that and shaft, radius (10% and 20% distal), tibia,
ovulatory disturbances accounted for 24% of and fibula. Spine and femur shaft BMD were
the variance in vertebral bone loss: spinal higher in subjects who had always been reg-
bone density tended to increase in women ular than in subjects with some history of
with normal cycles but decreased signifi- menstrual irregularity. Currently amenor-
cantly in women with two or more short lu- rheic subjects with a history of oligomenor-
teal phases and in those with anovulatory rhea or amenorrhea were significantly lower
cycles. Cann and associates84 reported that in vertebral BMD than subjects with other
loss of vertebral bone with amenorrhea was patterns of irregularity. No differences were
biphasic. In one year, women who had been detected at other sites. The authors con-
amenorrheic 3 years or less lost 4.2% in ver- cluded that deficits in bone density from
tebral trabecular mineral content, while previous menstrual irregularity appeared to
those who had been amenorrheic for longer be confined to the vertebrae. Weight was sig-
periods did not change significantly. nificantly correlated with BMD at all sites,
In most of these studies of bone density, and the association became stronger as the
the athletes were runners or involved in severity of menstrual disorder increased.
other aerobic sports that did not particu- An important question is whether bone
larly stress the back musculature. On the deficits due to amenorrhea can be corrected
other hand, Snyder and co-workers74 re- or averted. Seven subjects who regained
ported that oarswomen, regardless of men- menses following a reduction in training in-
strual status, did not differ significantly in creased significantly (6.3%) in vertebral
vertebral BMC from sedentary eumenor- BMD, while matched eumenorrheic subjects
98 Basic Concepts of Exercise Physiology

did not change significantly over 1 year.86 tempting to delineate the exercise programs
Bone density increased more slowly the fol- most effective in stimulating bone hypertro-
lowing year, and then plateaued. After 4 phy.
years of normal menses, vertebral density
remained well below normal. Further evi-
SUMMARY
dence of the persistence of vertebral loss
was provided by a study of 208 runners. Sub- Bone is a dynamic tissue performing two
jects with past or current untreated amen- functions: providing structural support and
orrhea had significantly lower spinal den- acting as a mineral reservoir. Two homeo-
sity than subjects who had always been static mechanisms act on bone at the same
regular. Women with current or past oligo- time: hormones and mechanical stress.
menorrhea but no amenorrhea, and women Researchers have evaluated the relation-
with treated (by estrogen or oral contracep- ship of weight-bearing and non-weight-
tives) amenorrhea for less than 3 years were bearing forces on bone to bone mass and
similar in bone density to the always-regular bone strength. Bone adjusts locally to sup-
subjects. port the structural demands of weight-bear-
ing and muscular activity. Inactivity results
PROBLEMS IN STUDYING in bone involution, whereas increased activ-
EXERCISE EFFECTS ity induces bone hypertrophy. Subjects at
bed rest or in weightless conditions lose
In animal studies, exercise and mechani- bone rapidly. Conversely, athletes have
cal loading have consistently benefitted greater bone mass than their sedentary
bone density. Although the mechanisms counterparts. Exercise intervention slows or
have not been fully elucidated, loading pro- reverses bone loss in middle-aged and el-
duces increased cellular activity and bone derly women. Bone response is specific to
formation rates. In humans, athletes had the area stressed, as seen in the selective
greater bone density than sedentary sub- hypertrophy of the dominant arm in tennis
jects, but few cross-sectional studies of non- players. Very intense levels of exercise cou-
athletes have been able to detect a differ- pled with amenorrhea may reduce skeletal
ence in bone density between moderately mass, especially in the spine.
active and sedentary subjects. It could be More research is needed to understand
that many moderately active subjects do not the precise mechanisms by which exercise
exceed the threshold for stimulating bone affects bone, and the optimum type and in-
hypertrophy. Intervention studies gener- tensity of physical activity for preventing os-
ally, but not always, increased bone density teoporosis.
or reduced bone loss. A confusing aspect of
bone research is the failure of intervention
with weight training to increase bone mass REFERENCES
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exercise programs of insufficient intensity, Proceedings, Second Acta Medica Scandinav-
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eral difference between human and animal sell Trycheri, Uppsala, Sweden, 1986, p 149.
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no 421-132:46, Washington, DC, 1984.
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Bone Concerns 99

4. Freudenheim JL, Johnson NE, and Smith EL: 18. Nelson ME, Fisher EC, Dilmanian FA, et al: A
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Clin Endocrinol Metab 70:264,1989. ulation of load-related stimulation of new
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4(Suppl):1128, 1989 (abstr). bone to overloading in the adult rat: A single
100 Basic Concepts of Exercise Physiology

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35. Frost, HM: A new direction for osteoporosis bone mineral content in postmenopausal
research: A review and proposal. Bone women. Ann Intern Med 108:824,1988.
12:429,1991. 53. Krolner B, Toft B, Nielson SP, et al: Physical
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Metabolism 19:1071, 1970. Sci 64:541,1983.
37. Hulley SB, Vogel JM, and Donaldson CL: Ef- 54. Rikli RE, and McManis BG: Effects of exercise
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Clin Invest 50:2506, 1971. 55. Simkin A, Ayalon J, and Leichter I: Increased
38. Krolner B, and Toft B: Vertebral bone loss: An trabecular bone density due to bone-loading
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Clin Sci 64:537,1983. women. Calcif Tissue Int 40:59, 1986.
39. LeBlanc AD, Schneider VS, Evans HFJ, et al: 56. Smith EL, Smith PE, Ensign CJ, et al: Bone in-
Bone mineral loss and recovery after 17 volution decrease in exercising middle-aged
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40. Kazarian LE, and Von Gierke HE: Bone loss as 57. Aloia JF, Cohn SH, Ostuni JA, et al: Preven-
a result of immobilization and chelation: Pre- tion of involutional bone loss by exercise.
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1983. 59. Cavanaugh DJ, and Cann CE: Brisk walking
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effects of immobilization on cortical bone in women. Bone 9:201,1988.
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26(Suppl):S115, 1983. of two randomised exercise programmes on
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Bone mass in lifetime tennis athletes. JAMA women. Br Med J 292:607,1987.
44:1107,1980. 61. Gleeson PB, Protas EJ, LeBlanc AD, et al: Ef-
44. Jones HH, Priest JS, Hayes WC, et al: Humeral fects of weight lifting on bone mineral density
hypertrophy in response to exercise. J Bone in premenopausal women. J Bone Min Res
Joint Surg 59A.-204, 1977. 5:153, 1990.
45. Montoye HJ, Smith EL, Pardon DF, et al: Bone 62. Pruitt LA, Jackson RD, Bartels RL, et al:
mineral in senior tennis players. Scandina- Weight-training effects on bone mineral den-
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46. Block J, Genant HK, Black D, et al: Greater Min Res 7:179,1992.
vertebral bone mineral in exercising young 63. Notelovitz M, Martin D, Tesar R, et al: Estro-
men. Western J Med 145:39, 1986. gen therapy and variable-resistance weight
47. Davee AM, Rosen CJ, and Adler RA: Exercise training increase bone mineral in surgically
patterns and trabecular bone density in col- menopausal women. J Bone Min Res 6:583,
lege women. J Bone Min Res 5:245, 1990. 1991.
48. Heinrich CH, Going SB, Pamenter RW, et al: 64. Rockwell JC, Sorenson AM, Baker S, et al:
Bone mineral content of cyclically menstru- Weight training decreases vertebral bone
ating female resistance and endurance density in premenopausal women: A pro-
trained athletes. Med Sci Sports Exerc 22:558, spective study. J Clin Endocrinol Metab
1990. 71:988, 1990.
49. Nilsson BE, and Westlin NE: Bone density in 65. Sinaki M, Wahner HW, Offord KP, et al: Effi-
athletes. Clin Orthop Rel Res 77:179, 1971. cacy of nonloading exercises in prevention of
50. Jacobson PC, Beaver W, Grubb SA, et al: Bone vertebral bone loss in postmenopausal
density in women: College athletes and older women: A controlled trial. Clin Proc 64:762,
athletic women. J Orthop Res 2:328,1984. 1989.
51. Orwoll ES, Ferrant J, and Owatt SK: The re- 66. Cann CE, Martin MC, Genant HK, et al: De-
lationship of swimming exercise to bone creased spinal mineral content in amenor-
mass in men and women. Arch Intern Med rheic women. JAMA 251:626,1984.
149:2197, 1989. 67. Drinkwater BL, Nilson K, Chesnut CH, et al:
Bone Concerns 101

Bone mineral content of amenorrheic and eu- 77. Cann CE, Cavanaugh DJ, Schnurpfiel K, et al:
monorrheic athletes. N Engl J Med 311:277, Menstrual history is the primary determinant
1984. of trabecular bone density in women. Med Sci
68. Drinkwater BL, Bruemner B, and Chesnut, Sports Exerc 20:S59,1988 (abstr).
CH: Menstrual history as a determinant of 78. Lloyd T, Buchanan JR, Bitzer S, et al: Inter-
current bone density in young athletes. relationships of diet, athletic activity, men-
JAM A 263:545,1990. strual status and bone density in collegiate
69. Fisher EC, Nelson ME, Frontera WR, et al: women. Am J Clin Nutr 46:681,1987.
Bone mineral content and levels of gonado- 79. Louis O, Demeirlier K, Kalender W, et al: Low
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ning women. J Clin Endocrinol Metab elite female runners. Int J Sports Med 12:214,
62:1232, 1986. 1991.
70. Jones KP, Ravnikar VA, Tulchinsky D, et al: 80. Myburgh KH, Hutchins J, Fataar AB, et al:
Comparison of bone density in amenorrheic Low bone density is an etiologic factor for
women due to athletics, weight loss, and pre- stress fractures in athletes. Ann Intern Med
mature menopause. Obstet Gynecol 66:5, 113:754, 1990.
1985. 81. Lloyd T, Triantafyllou J, Baker ER, et al:
71. Linnell SL, Stagger JM, Blue PW, et al: Bone Women athletes with menstrual irregularity
mineral content and menstrual regularity in have increased musculoskeletal injuries.
female runners. Med Sci Sports Exerc 16:343, Med Sci Sports Exerc 18:374,1986.
1984. 82. Warren MP, Brooks-Gunn J, Hamilton LH, et
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73. Nelson ME, Fisher EC, Catsos PD, et al: Diet nal bone loss and ovulatory disturbances. N
and bone status in amenorrheic runners. Am Engl J Med 323:1221,1990.
J Clin Nutr 43:910, 1986. 84. Cann CE, Martin MC, and Jaffe RB: Duration
74. Snyder AC, Wenderoth MP, Johnston CC, et of amenorrhea affects rate of bone loss in
al: Bone mineral content of elite lightweight women runners: Implications for therapy.
amenorrheic oarswomen. Hum Biol 58:863, Med Sci Sports Exerc 17:214,1985 (abstr).
1986. 85. Wolman RL, Clark P, McNally E, et al: Men-
75. Cook SD, Harding AF, Thomas KA, et al: Tra- strual state and exercise as determinants of
becular bone density and menstrual function spinal trabecular bone density in female ath-
in women runners. Am J Sports Med 15:503, letes. Br Med J 301:516,1990.
1987. 86. Drinkwater BL, Nilson K, Ott S, et al: Bone
76. Buchanan JR, Myers C, Lloyd T, et al: Deter- mineral density after resumption of menses
minants of peak trabecular bone density in in amenorrheic athletes. JAMA 256:380,1986.
women: The role of androgens, estrogen and
exercise. J Bone Min Res 3:673, 1988.
CHAPTER 6

Nutrition for Sports


GABE MIRKIN, M.D.

NUTRIENTS DRINKING DURING COMPETITION


Carbohydrates Dehydration and "Heat Cramps"
Proteins Women May Need Less Fluid Than
Fats Men
When to Drink
ENERGY STORAGE
What to Drink
Comparing Women and Men
Cold or Warm?
ENDURANCE EATING AND DRINKING AFTER
"Hitting the Wall": Depletion of COMPETITION
Muscle Glycogen
"Bonking": Depletion of Liver PROTEIN REQUIREMENTS
Glycogen VITAMINS
INCREASING ENDURANCE Mechanism of Function
Training to Increase Endurance Vitamin Needs of Female Athletes
Vitamin C and Colds
UTILIZING FAT INSTEAD OF Vitamins and Birth Control Pills
GLYCOGEN Vitamins and Premenstrual
DIET AND ENDURANCE Syndrome
Food Intake during the Week before MINERALS
Competition Iron
Eating the Night before Competition Calcium
Eating the Meal before Competition Sodium
Eating before Exercising Potassium
Eating during Competition Trace Minerals
DRINKING BEFORE COMPETITION THE ATHLETE'S DIET

w, ith the exception of iron and calcium, nutrient requirements for female ath-
letes are the same as those for their male counterparts. Women suffer far more
frequently than men from deficiencies of iron and calcium. Ten percent of
healthy, white, middle-class female adolescents are iron deficient, while 5% have
iron-deficiency anemia.1 Athletes are at greater risk than nonathletes for devel-
oping iron deficiency,2 which, even in the absence of anemia, can limit athletic
endurance.
Hypoestrogenic female athletes are at increased risk of developing osteo-
porotic bone fractures.3 In addition to hormone replacement, the prevention and
1O2
Nutrition for Sports 103

treatment of this condition should include Table 6-1. ESSENTIAL NUTRIENTS


ingestion of adequate amounts of calcium.
Water
A proper diet can help female athletes to Linoleic acid
maximize performance. However, many ath- 8 or 9 amino acids
letes have nutritional misconceptions that 13 vitamins
hinder performance rather than help it. For Approximately 21 minerals
example, many athletes incorrectly believe Glucose (for energy)
that a high-protein diet improves perfor-
mance and increases muscle size and
strength, that vitamin requirements are sig- in competition by following sound scientific
nificantly greater for athletes, that fluid re- nutritional practices. A brief discussion of
quirements during exercise should be dic- basic principles of nutrition will precede the
tated by thirst, and that salt tablets should sections on the application of such princi-
be taken in hot weather.4,5 All of these myths ples to athletic competition.
will be refuted in this chapter.
In 1967, the women's world record for the
marathon was 3:15:22, set by Maureen Wil- Carbohydrates
ton of Toronto, Canada. By 1985, the world Carbohydrates are composed of sugars.
record was lowered to 2:21:06 by Ingrid They can be monosaccharides, such as glu-
Kristiansen of Norway. The fantastic im- cose and fructose in fruit; disaccharides,
provement in world records in all sporting such as lactose in milk or sucrose in candy;
events is due primarily to superior training and polysaccharides, such as starch in a po-
methods, but it is also due to improved tato or fiber in celery.
knowledge about nutrition. In the late 1960s, Before carbohydrates can be absorbed,
it was common for athletes to eat high-pro- they must first be hydrolyzed into one or
tein diets, to reduce their intake of food on more of the following four sugars: glucose,
the days before competition, to ingest no fructose, galactose, and mannose. Of these
food or liquids during competition, and to sugars, only glucose circulates beyond the
eat only a limited amount of food after com- portal system. The other three are con-
petition. Today knowledgeable athletes fol- verted to glucose by hepatocytes before
low none of these old regimens.6 they can re-enter the circulation (Fig. 6-1).
This chapter reviews some of the basic Circulating glucose can be used by all
physiologic principles that serve as the cells as a source of energy. Glucose that is
foundation for advising athletes how to use not used immediately can be stored as gly-
nutrition to improve sports performance. cogen only in the liver and muscles. When
these tissues are saturated with glycogen,
excess glucose is then converted to fat. Liver
glycogen can yield glucose to the circula-
NUTRIENTS tion, where it subsequently can be used by
other tissues. On the other hand, the glu-
Humans require approximately 46 nutri- cose from muscle glycogen can be utilized
ents to be healthy. An essential nutrient is only by that particular muscle.
one that cannot be produced by the body in
adequate amounts and, therefore, must be
supplied by the diet (Table 6-1). Lack of an Proteins
essential nutrient can impair performance, Fifteen percent of ingested protein is hy-
but taking large amounts of any specific nu- drolyzed to amino acids and polypeptides in
trient has not been shown to improve per- the stomach, while the remaining protein
formance. undergoes hydrolysis in the small intestine.
Athletes can improve their performances These metabolites are actively transported
104 Basic Concepts of Exercise Physiology

Figure 6-1. Sugar circulation. All carbohydrates are sugars bound together. They can be single sug-
ars, as in fruit and honey; two sugars bound together, as in milk and table sugar; and hundreds and
thousands of sugars bound together, as in corn and beans.
Nutrition for Sports 105

into intestinal epithelial cells. Once there, creatic lipase into monoglycerides, free fatty
most of the polypeptides are hydrolyzed to acids, and glycerol (Table 6-2), which enter
form amino acids, which are then absorbed the epithelial cells lining the intestines.
into the general circulation. Once there, the monoglycerides are hydro-
The main functions of proteins are to lyzed to form glycerol and fatty acids. Then,
form structural components, enzymes, triglycerides are formed again, are com-
hormones, neurotransmitters, antibodies, bined with cholesterol and phospholipids,
transport molecules, and clotting factors. and are covered with a lipoprotein coating
Protein also can be a source of energy. As to form chylomicron particles, which pass
much as 10% of energy during exercise can through the lymphatic system into the gen-
come from protein, with more than half eral circulation. Short-chain fatty acids can
coming from one amino acid, leucine. Since be absorbed directly into the circulation.
leucine represents only a small fraction of Excess fat is stored primarily in fat cells and
the amino acids in ingested protein, the leu- muscles.
cine that is used for energy must come from
a source other than ingested protein. It also
does not come from muscle sources of leu- ENERGY STORAGE
cine. Most of the leucine that is used for en-
ergy is formed de novo. The nitrogen for the Only fats and carbohydrates are stored
newly formed leucine comes from other for future use as an energy source. The
branched-chain amino acids (isoleucine human body cannot store extra protein. Fat
and valine), and most of the carbon comes stores energy in the most economic way, as
from glucose and other amino acids. it provides 14 times as much energy per
Before amino acids can be used for en- given weight as stored liver glycogen, which
ergy, deamination or transamination must must be stored with other liver tissue. One
occur to remove the nitrogen. Athletic train- pound of stored fat will yield 3500 kcal,
ing can double the levels of important trans- whereas 1 Ib of liver contains only enough
aminases, such as SCOT and SGPT, and this glycogen to yield 250 kcal. This great dispar-
increases significantly the body's ability to ity in energy storage is explained by the fact
utilize leucine and other amino acids for en- that fat occupies 85% of the space in fat cells,
ergy. while liver glycogen is diluted by other cel-
lular elements and occupies less than 15% of
the space in liver cells.
Fats The body of the average athlete contains
More than 95% of the fat in foods is in the only enough stored fat to support exercise
form of triglycerides. Fat is separated from for 119 hours, enough stored muscle glyco-
other foodstuffs in the stomach, but it is not gen for11/2hours, and enough stored liver
degraded until it is emulsified (dispersed in glycogen for 6 minutes. Table 6-3 shows
water) by bile salts in the small intestine. how limited the stores of carbohydrates are
The fat globules are then hydrolyzed by pan- and how extensive the fat stores are.

Table 6-2. GLYCEROL AND FATTY ACIDS


C-C-C-C • • • C-C-COOH C-OH C-C-C • • • C-C-COOH
| |
C-C-C-C • • • C-C-COOH * C-OH + C-C-C • • • C-C-COOH
i1 i
C-C-C-C • • • C-C-COOH C-OH C-C-C • • • C-C-COOH
TRIGLYCERIDE , GLYCEROL + FATTY ACIDS
106 Basic Concepts of Exercise Physiology

Table 6-3. MAXIMAL BODY STORAGE swimming performances. It is likely that the
CAPACITY FOR CARBOHYDRATES AND insulating properties of fat, rather than the
FATS7 glycogen-sparing effect, gave them an ad-
Weight of Available vantage. Loss of body heat is a major prob-
Storage Site Tissue (g) Energy (kcal) lem in distance swimming. Furthermore,
having extra fat raises a swimmer higher out
Muscle glycogen 125-300 500-1200
Liver glycogen 50-100 200-400
of the water and reduces drag (see Chapter
Body fat 6000-15,000 50,000-140,000 4).

ENDURANCE
Comparing Women and Men
At the same level of fitness, the average Endurance is the ability to continue exer-
woman has 7% to 10% more body fat than the cising muscles for an extended period of
average man. For example, top female mar- time. To continue exercising, muscles re-
athon runners have 12% to 20% body fat, quire energy, the major sources of which are
compared with 5% to 10% for their male triglycerides and glycogen in muscles and
counterparts. triglycerides and glucose in blood.
Muscles use primarily fats and carbohy- The main advantage of fats is that the
drates as their energy sources. At rest, mus- body can store vast amounts. The main ad-
cles use mostly fats for energy. During ex- vantage of carbohydrates is that they can be
ercise, muscles use more carbohydrates, utilized under anaerobic conditions. Fat me-
with a higher percentage of carbohydrates tabolism always requires oxygen. As exer-
and a lower percentage of fat being used as cise intensity increases, the percentage of
the intensity of the exercise is increased. In energy derived from muscle glycogen also
spite of their increased percentage of body increases. Much of the exercise during most
fat, women use the same percentage of fat as competition events is done at maximum or
men through all intensities of exercise. For near-maximum intensity. The limiting factor
example, at race pace for the marathon, top for exercising at an intensity greater than
male and female runners have been shown 70% of Vo2max is the amount of glycogen
to derive the same 50% of their energy from that muscles can store.12
fat,8 and top female athletes have not dem-
onstrated greater endurance than male ath- "Hitting the Wall": Depletion of
letes. Muscle Glycogen
In running events from 100 to 1500 meters,
world records for women are 7% to 10% Muscle endurance depends on the ade-
slower than those for men.9,10 In running quacy of muscle glycogen stores. Depletion
events from 1500 meters to the marathon, of muscle glycogen causes pain and fatigue
world records for women are 13% to 15% and causes an athlete to lose much of her
slower than those for men.11 The extra fat strength and to have difficulty coordinating
that most women carry slows them down muscle movements. Athletes refer to this as
during running. However, having extra fat is hitting the wall, a common occurrence in
an advantage during swimming. Penny Dean marathon runners after they have raced
of California set the world's record for men more than 18 miles. The more glycogen that
and women for a single crossing of the En- can be stored in a muscle, the longer it can
glish Channel in 7 hours and 40 minutes (in be exercised. Recent research has called
1978), and Cynthia Nichols of Canada set the into question this explanation. Since bicycle
record for a double crossing at 19 hours and racers run out of their muscle glycogen after
12 minutes (in 1977). Their extra fat may 2 hours of racing and do not "hit the wall,"
well be the reason for their great endurance another explanation would be more feasible.
Nutrition for Sports 107

The most likely cause is that hard running After the athlete eats, her muscles fill with
damages the fibrous connective tissue in glycogen, and this reduces production of
muscles, while the smooth rotary motion of glycogen synthetase. Therefore, the effects
pedalling does not. of depletion training are short-lived, and de-
pletion training should be repeated at fre-
"Bonking": Depletion of Liver quent intervals. However, athletes usually
do not perform depletion training more fre-
Glycogen
quently than once a week, because depletion
Brain endurance depends on circulating of muscle glycogen leads to increased utili-
glucose. More than 98% of the energy for the zation of muscle protein for energy. This
brain is derived from blood glucose, which damages the muscle, delays recovery, and
depends on hepatic glycogen stores for limits the amount of intense training the ath-
maintenance. When the blood concentra- lete can accomplish.
tion of glucose falls to low levels, the athlete Many recreational athletes do not appre-
may feel very tired and can suffer from a syn- ciate the importance of depletion training
copal episode or seizures or both. Athletes and enter marathons before they have put
refer to this as "bonking." Bicyclists who do this training technique to adequate use. As a
not eat during endurance races may experi- result, they have inadequate muscle glyco-
ence this after 4 or more hours of cycling. gen stores to enable them to run the neces-
sary distance.

INCREASING ENDURANCE
UTILIZING FAT INSTEAD OF
An athlete can improve endurance by GLYCOGEN
using training methods and dietary manip-
ulations that increase muscle glycogen stor- In addition to depletion training, other
age and decrease muscle glycogen utiliza- techniques that have been promoted to de-
tion by increasing fat utilization.13 crease glycogen utilization by muscles dur-
ing exercise include eating a high-fat diet for
Training to Increase Endurance several days prior to competition, taking nu-
tritional supplements, and taking sympatho-
To improve the ability of muscles to store mimetic agents.
increased amounts of glycogen13 and utilize At least one study showed that eating a
increased amounts of fat (and less glyco- high-fat diet for several days prior to com-
gen),14 athletes use a training technique petition will increase muscle utilization of
called depletion. They exercise until muscle fat. However, endurance was not improved
glycogen has been nearly depleted (Table by this technique.16,17 It is not unusual for
6-4). This causes muscle cells to increase blood glucose concentrations to fall as low
production of glycogen synthetase, which as 30 mg/dL during vigorous exercise. Eat-
increases glycogen synthesis and, in turn, ing a high-fat diet does not reduce muscle
glycogen storage.15 glycogen utilization or prevent the devel-
opment of hypoglycemia (with or without
symptoms) during exercise.17
There is no evidence that taking large
Table 6-4. AVERAGE TIMES FOR MUSCLE amounts of any vitamin, mineral, protein, or
GLYCOGEN DEPLETION IN ELITE.
ATHLETES carbohydrate will cause muscles to increase
l
their utilization of fat.18
Marathon runner A-2Vih Claims have been made that carnitine
Bicycle racer 4-6 h
Cross-country skier 10-12 h
supplements enhance endurance. Carnitine
is a protein that transports fat into mito-
108 Basic Concepts of Exercise Physiology

chondria, where fat is catabolized for en- bodies process foods in the same ways. An
ergy. However, there is no evidence that any athlete can increase her endurance by eat-
supplement will increase mitochondria! fat ing the right meals 3 days before, the night
content enough to increase fat utilization. before, or several hours before competition.
Myocytes and hepatocytes synthesize large
amounts of carnitine from lysine and methi-
onine, and human myocytes contain enough
Food Intake during the Week
carnitine to support fat metabolism even
before Competition
under extreme exercise conditions.19 The In 1939, Scandinavian researchers
fact that most athletes include meat, fish, or showed that eating a high-carbohydrate diet
chicken—rich sources of carnitine—in their for several days before a competitive event
diets provides another reason why athletes increases muscle glycogen stores and en-
do not need carnitine supplements. durance, while a low-carbohydrate diet de-
Caffeine raises blood triglyceride levels creases muscle glycogen stores and endur-
by increasing catecholamine production ance.22 In the mid-1960s, other investigators
and sensitivity. Catecholamines increase proposed a method of "carbohydrate load-
triglyceride utilization by promoting free ing" that was practiced by many endurance
fatty acid release from adipocytes and up- athletes throughout the world.23,24
take by myocytes. Taking caffeine prior to
1 Seven days prior to competition, the
workouts has been shown to increase en-
athlete performs a long depletion work-
durance in training sessions by increasing
out.
muscle utilization of fat,20 but it has not been
2 For the next 3 days, she keeps the gly-
shown to increase endurance in competi-
cogen content of her exercised muscles
tion. A possible explanation for this differ-
low by eating a low-carbohydrate diet.
ence in responses is that caffeine may be ef-
3 For the next 3 days, she eats her regular
fective in prolonging endurance only when
diet plus extra carbohydrate-rich foods.
endogenous catecholamine levels are low.
In a laboratory setting, athletes may be re- Athletes should not ingest extra carbohy-
drate for more than 3 consecutive days. In
laxed and have low circulating levels of cat-
echolamines. Raising catecholamines in thisthat time, muscles and liver will be at their
situation may enhance performance. How- maximum capacity for storing glycogen, so
ever, prior to competition most athletes no additional glycogen can be stored. In ad-
have very high levels of catecholamines. dition, carbohydrate packing should not be
Raising their levels further may not help used in events lasting less than 60 minutes,
them and, indeed, may harm them. Large because it will not be helpful and may even
amounts of catecholamines can cause trem- be harmful. 25 The muscles of trained athletes
ors and irritability. are not depleted of glycogen in so short a
Seven days of supplementation of a high-time. Carbohydrate packing may reduce per-
carbohydrate diet with dihydroxyacetone formance in events requiring great speed
and pyruvate has been shown in one study over short distances, since each gram of gly-
to increase endurance.21 Further studies are
cogen is stored with almost three additional
needed before this practice can be acceptedgrams of water, making the muscles much
as an effective means of increasing endur- heavier than usual.
ance. Few top athletes practice this 7-day regi-
men today because it can hinder perfor-
mance. During the depletion phase, the ath-
DIET AND ENDURANCE lete cannot train properly and usually is
irritable and unable to perform mental tasks
Female athletes should follow the same effectively. During the high-carbohydrate
nutritional principles as men, since their phase, the ingestion of vast amounts of car-
Nutrition for Sports 109

bohydrates has been reported to cause evening prior to competition does not seem
chest pain,26 myoglobinuria, and nephritis.27 to hinder performance and may actually
However, these side effects are rare. Marked help it. However, more research is needed
overeating raises blood lipid levels, and this to resolve this question.
can lead to occlusion of the coronary arter-
ies in exercisers who already have signifi- Eating the Meal before
cant arteriosclerosis. Furthermore, this reg- Competition
imen has not been shown to be more
effective than simply reducing the workload The major function of the precompetition
and ingesting some extra carbohydrates.28 meal is to maximize hepatic glycogen (see
As a result of all of these concerns, most Table 6-5). Serum glucose is sufficient to
top athletes in endurance sports avoid the support brain function for only 3 minutes.
low-carbohydrate phase and modify the To prevent hypoglycemia, hepatocytes must
high-carbohydrate phase. The runner can release glucose constantly. However, there
maximize muscle glycogen by a combina- is enough glycogen in hepatocytes to last
tion of reducing her workload and eating a only 12 hours when the athlete is at rest.32
regular diet that contains at least 55% of its Obviously, during exercise, liver glycogen is
calories from carbohydrates.29 The 7-day depleted much faster than that.
carbohydrate-packing regimen thus is
changed to eating a high-carbohydrate diet Timing of Meal
and stopping intense exercise 4 days prior
to competition. To maximize hepatic glycogen stores, the
precompetition meal should be ingested 5
or fewer hours before competition. If the
Eating the Night before meal is eaten more than 5 hours before com-
Competition petition, the hepatocytes will be depleted of
On the night before a competitive event, a considerable amount of stored glycogen
many athletes eat a high-carbohydrate and will have less than maximal glycogen
meal. The primary purpose of this meal is to stores when the athlete starts competition.
increase muscle glycogen stores (Table 6- Several previous studies showed that eating
5). The pregame meal cannot serve this sugared food just before competition in-
function, since it takes at least 10 hours to creased an athlete's chances of developing
replenish muscle glycogen stores.30 postprandial hyperinsulinemia, which can
It is controversial whether muscle glyco- cause hypoglycemia.33 However, the vast
gen storage is promoted more by ingestion majority of recent reports conclude that pre-
of starch or monosaccharides and disaccha- event glucose consumption can cause re-
rides. One recent study showed that a high- duced blood glucose levels during exercise,
monosaccharide and high-disaccharide diet but it has no effect on endurance.34,35 The
caused more muscle glycogen to be stored brains of well-conditioned athletes can con-
than did a high-starch diet.31 Based on these tinue to function at lower blood sugar levels
findings, ingestion of simple sugars on the than those of unfit individuals.
At rest, blood glucose levels as low as 25
mg/dL usually cause a deterioration in brain
function and loss of consciousness. How-
Table 6-5. PRIMARY FUNCTION OF ever, physically fit individuals can usually
MEALS BEFORE AN AFTERNOON
COMPETITION tolerate such levels during exercise without
developing any symptoms at all,36 even
Supper (the day before): To increase muscle glycogen though they are using up their muscle gly-
stores
Breakfast: To increase hepatic glycogen stores
cogen stores at an accelerated rate37 and will
feel fatigue sooner than usual.38
110 Basic Concepts of Exercise Physiology

Composition of Meal just prior to exercising. It is speculated that,


when pain does occur, it is due to stomach
Precompetition meals should be high in muscle spasms, which result from ischemia
carbohydrates. It does not make any differ- caused by the shunting of blood from the
ence whether the meal is also high in fat. A stomach muscles to the exercising mus-
combination of a high-carbohydrate meal 4 cles.40 During exercise, gastric motility in-
hours before exercise and around 50 g of creases,41-43 and splanchnic blood flow de-
carbohydrate 5 minutes before exercise can creases.44
increase glycogen stores and maximize en- A drug company has advertised that tak-
durance.39 The athlete can eat any foods she ing fructose before exercise, compared to
likes, as long as she suffers no discomfort glucose, results in a much lower rate of mus-
and has an empty stomach by the time she cle glycogen depletion, because fructose
starts to exercise (Table 6-6). does not cause a rapid rise in either blood
Theoretically, fat and protein are poor sugar or insulin.45 However, there is no evi-
choices for the precompetition meal. Fat de- dence that eating fructose prior to exercis-
lays stomach emptying, and the urea and ke- ing offers any advantage over eating nothing
tones released by the catabolism of protein at all, and there is evidence that eating fruc-
can promote diuresis. However, no con- tose is less advantageous than eating noth-
trolled studies have demonstrated adverse ing at all. It is true that fructose ingestion
effects from fat or protein in precompetition may cause a lower rise than glucose in blood
meals, and many athletes can tolerate high- glucose and insulin levels,46,47 but eating
fat and high-protein precompetition meals fructose does cause an increase in circulat-
without having their performances hin- ing glucose and insulin levels, whereas eat-
dered. ing nothing does not. Fructose ingestion
also causes a greater rate of muscle glycogen
Eating Before Exercising utilization, compared with eating noth-
ing.48,49 The fact that fructose costs 15 times
Provided that the exercise is not too in- as much as glucose offers an added disad-
tense and the amount of food eaten is not too vantage.
great, most exercisers will not suffer from
abdominal pain or discomfort when they eat
Eating During Competition

Table 6-6. EXAMPLES OF


It is not necessary for most conditioned
PRECOMPETITION MEALS THAT PASS athletes to eat during events that last less
RAPIDLY FROM THE STOMACH than 2 hours. However, athletes can benefit
from eating during events lasting longer
Break fast #1
than that. The abilitity of exercising muscles
Breakfast cereal with milk to utilize ingested carbohydrates in place of
A few small pieces of fruit
Toast with butter muscle glycogen is dependent on condition-
1 cup of coffee ing. The higher the level of fitness, the better
1 glass of milk able the athlete is to utilize ingested carbo-
No more than 1A glass of orange juice hydrates during exercise.50
Break fast #2 In contrast to ingestion of food before ex-
Pancakes ercising, ingestion of food during exercise
A small pat of jelly does not cause significant pancreatic output
Breakfast cereal of insulin. At rest, eating causes hypergly-
Milk or coffee cemia, which promotes insulin release.
Glass of water However, during exercise, muscles remove
1/2 glass of fruit juice or a small piece of fruit
glucose so rapidly from the circulation that
Nutrition for Sports Ill
blood levels of glucose rarely rise high the week prior to competition by doubling
enough to induce significant insulin release her daily intake of fluid for 1 week. An in-
from the pancreas.51 Insulin-induced hypo- crease from 1 L to 2 L can increase blood vol-
glycemia caused by eating during intense ume by 10%.60 The extra fluid is not lost com-
exercise does not occur.52 pletely as urine.
Almost any food can be used for energy. She can also increase her intake of fluids
When taken during exercise, glucose has not during exercise by distending her stomach
been shown to be more effective than table with a large amount of fluid just before she
food in prolonging endurance. Studies com- competes. If she drinks 600 mL of water just
paring glucose with fructose offer conflicting before competition, almost 400 mL will pass
results. One study showed that neither glu- into the intestines in 20 minutes.61 Then she
cose nor fructose is better than placebo in should try to ingest 3 oz (about 90 mL) of
reducing muscle glycogen utilization.43 An- water every 10 minutes.
other study showed that fructose has a
greater muscle-glycogen-sparing effect,53
while a third study showed that glucose has DRINKING DURING
a greater glycogen-sparing effect.54 COMPETITION
Any maneuver that causes muscles to in-
crease the rate at which they utilize fat for Although most fit athletes do not gain any
energy theoretically should help to con- advantage from eating during competition in
serve muscle glycogen and prolong endur- events lasting less than 2 hours, they can al-
ance. A high-fat diet has been shown to in- ways benefit from keeping themselves ade-
crease endurance in rats,55 but neither a fatty quately hydrated. Competitive runners and
meal nor glycerol has been shown to pro- swimmers can lose approximately \1A L of
long endurance in humans.56,57 fluid during an intense 1-hour workout. Al-
Ten years ago, maltodextrin glucose poly- though athletes exercising in warm, humid
mer solutions, Exceed (Ross Laboratories, environments can see their sweat and ap-
Columbus, Ohio) and MAX (Coca-Cola), ap- preciate their obvious fluid loss, those ex-
peared to enhance endurance in events last- ercising in water sports may not be able to
ing longer than 2 hours.58 The polymers in perceive that this loss has occurred.
these drinks are composed of five glucose
molecules and seemed to supply calories at
a low osmotic pressure, thereby not delay- Dehydration and "Heat
ing absorption and resultant glucose utili- Cramps"
zation. However, recent data show that they
are not superior to free glucose for maintain- As the athlete becomes progressively
ing hydration and blood glucose levels, and more dehydrated, her blood volume de-
they have not been shown to increase en- creases. There may not be an adequate vol-
durance.59 ume of circulating blood to carry heat from
exercising muscles to the skin, where the
heat can be dissipated, and, at the same
DRINKING BEFORE time, to carry oxygen to heavily exercising
COMPETITION muscles. Reduced cutaneous blood flow will
raise body temperature, and this will impair
The maximal amount of fluid that can be performance. The decreased blood volume
absorbed during exercise is 600 to 800 can also limit the amount of blood that flows
mL/h. No matter how much fluid an athlete to the most heavily exercising muscles. The
ingests during competition, she will not be resultant hypoxia can cause sustained pain-
able to absorb enough to keep up with her ful muscle contractions, known as heat
losses. She can increase hydration during cramps.62
112 Basic Concepts of Exercise Physiology

Women May Need Less Fluid What to Drink


than Men Adequate hydration will usually prevent
Earlier studies showed that men have bet- heat cramps and hyperthermia. Water is the
ter tolerance than women for exercising in preferred drink to be taken during exercise
the heat. However, these studies did not lasting less than 1 hour. Extra calories64 and
compare men and women exercising at com- minerals65 are usually not needed. With ad-
parable percentages of their Vo2max. More equate dietary intake, the athlete will store
recent studies have shown that women are enough hepatic and muscle glycogen to last
able to tolerate exercise in the heat as well 1 hour.64,65 Athletes who exercise longer than
as men, provided that they both have the that need energy sources and minerals also.
same Vo2max.63 The rules for energy-containing fluids have
During exercise, women perspire less changed dramatically in the last few years.
than men of the same fitness level,63 but In 1968, studies showed that 2.5% was the
there is no evidence that women tolerate ex- highest concentration of sugar that could be
ercise in the heat better than men. There- contained in an exercise drink and still be
fore, female athletes should take the same absorbed.66,67 This posed a problem because
precautions as men to ensure that they are drinks taste best when they contain a 7% to
adequately hydrated during hot-weather ex- 10% concentration of sugar. Soft drinks and
ercise. fruit juices contain 7% to 10% sugar. Soon
after these studies, many exercise drinks
containing 2.5% sugar appeared on the mar-
ket. They did not taste good because the
When to Drink
concentration of sugar was too low, so some
The athlete should drink before she feels of the manufacturers added saccharin to
thirsty. By the time that she perceives thirst, sweeten the taste.
she already will have lost 1 to 2 L of fluid and Twenty years later, new studies refuted
will not be able to replace that deficit while the 1968 report. The 1968 data were col-
she exercises. During intense exercise, it is lected on resting subjects. Exercise in-
impossible to absorb fluids as fast as they creases gastric emptying for both solid
are lost. The maximum rate of gastric emp- meals and liquids.68 When the same studies
tying is about 800 mL/h. It is common for were repeated using people who were exer-
competing athletes to perspire as much as cising, 7% to 10% sugared drinks were ab-
2000 mL/h. sorbed rapidly. Based on the most recent
Thirst is a late sign of dehydration during evidence, special exercise drinks are not
exercise because osmoreceptors in the necessary, although many athletes prefer
brain will not signal a thirst sensation until them. All 10% drinks are equally effective in
the blood sodium concentration rises con- supplying energy. A basic 10% sugared drink
siderably. The primary mode of fluid loss may be prepared by dissolving 8 table-
during exercise is sweating. Sweat contains spoons of sugar in 1 L of water. Each table-
some sodium, although it is hypotonic in spoon of sugar contains 12 g of sucrose.
comparison to blood. As sodium is secreted Drinks with low levels of minerals are ab-
into sweat, the serum sodium level rises sorbed slightly more quickly than pure
more slowly than if water alone were lost. As water, but the difference is not significant.
a result, significant amounts of fluid are lost Mineral loss through sweat occurs so slowly
before hypernatremia develops enough to that conditioned athletes rarely develop hy-
cause thirst. Therefore, on a warm day, the ponatremia, hypokalemia, or hypocalcemia
athlete should drink a cup of cool water just during exercise.65 In fact, the opposite is
before she starts to exercise and every 15 more likely to occur. Serum sodium and po-
minutes during exercise. tassium levels rise during exercise and do
Nutrition for Sports 113

not fall unless the exercise is intense and Table 6-7. IMMEDIATE
prolonged. Increased serum sodium levels POSTCOMPETITION MEAL TO PREPARE
are due to the loss of sweat, which is hypo- FOR ANOTHER COMPETITION WITHIN A
FEW HOURS*
tonic in relation to blood. Increased serum
potassium levels are due to release of potas- Food Carbohydrate
sium from myocytes, preventing overheat-
1 orange 10 g
ing of muscles during exercise. Blood cal- 1 slice of bread 13 g
cium levels usually are not altered during 2 chocolate chip cookies 12 g
exercise. Magnesium levels in blood de- 1 banana 30 g
crease slightly during exercise, but this is 1 12-ounce soft drink 35 g
due primarily to cellular uptake of magne- No fluid restriction
sium and not to a significant loss of magne- *A 50-kg woman needs 75 to lOOgofCHO.
sium from the body.69,70

In events such as gymnastics, track and


Cold or Warm? field, wrestling, and swimming, athletes may
In the 1960s, studies showed that cold be scheduled to compete in several events
drinks (4°C) are absorbed faster and are less on the same day. It is very important for
likely to cause abdominal cramps than warm them to drink and eat immediately after they
ones.67 The theory was that cold water finish each event. Even if they rehydrate
causes the stomach to contract and push flu- completely (as evidenced by a return to nor-
ids rapidly into the intestines. However, mal weight), it will still take 4 to 5 hours for
more recent studies show that temperature the water to redistribute among the body
does not make much difference.71,72 Further- fluid compartments.79 Delaying carbohy-
more, carbonated drinks are absorbed as drate ingestion % hour markedly delays
rapidly as noncarbonated ones.73 muscle glycogen replenishment.80 The rec-
ommended amount of carbohydrate inges-
tion for immediate maximal rate of replen-
EATING AND DRINKING AFTER ishment is 1.5 g/kg of body weight81 (Table
COMPETITION 6-7). Doubling that amount does not in-
crease glycogen replenishment further.
Much of postcompetition tiredness is due
to depletion of muscle glycogen stores and
dehydration. Recovery from vigorous exer- PROTEIN REQUIREMENTS
cise depends on muscle glycogen replenish-
ment and rehydration.74 It makes no differ- When adjusted for weight, protein re-
ence whether such replacement is quirements are the same for men and
accomplished by eating simple sugars or women. The protein requirement of 0.8 g/kg
complex carbohydrates.75,76 Fructose offers body weight per day is based on body mass.
no advantage over other carbohydrates, as It is increased significantly by reduced ca-
glucose causes more rapid muscle glycogen loric intake, but had previously been felt to
restoration than fructose does.77 Carbohy- be increased only slightly during exer-
drate intake in athletes averages around 250 cise.82-84 However, several recent studies
g/d. This is far too little to afford maximal using leucine turnover measurements seem
glycogen replacement. It takes at least 600 to show an increase of up to 20% in protein
g/d of carbohydrate for maximum compen- turnover during aerobic exercise.85,86 The
sation. Therefore, it is important for athletes case for increased protein needs during ex-
to eat carbohydrate-rich meals after com- ercise is supported further by other studies
petition.78 showing increased excretion of 3-methyl
114 Basic Concepts of Exercise Physiology

histidine,87 increased urea nitrogen losses,87 tein (1.3 X 100) or 160 g of lower-quality
and depression of protein synthesis.88 protein in a week. This is accomplished by
Further research is necessary before pro- eating the equivalent of only 2 cups of corn
tein can be considered a significant source and beans per day.
of energy during exercise.89 Studies show an Since the body cannot store extra protein,
increased utilization of only the branched- the excess is catabolized into ammonia and
chain amino acids, leucine, isoleucine, and organic acids, much of which is excreted in
valine. This does not make a strong case for the urine. These compounds act as diuretics
increased protein utilization during exer- and, during exercise in hot weather, can
cise. The branched-chain amino acids are cause dehydration and increase the risk of
degraded by active skeletal muscles to re- heat stroke.94 Ingesting excessive amounts
lease nitrogen, which is combined with py- of protein can also increase calcium require-
ruvate in muscles to form alanine. The liver ments by increasing urinary loss.95 While
removes nitrogen from alanine to form glu- this is probably of little significance to most
cose, as a source of energy. However, turn- women, it may accelerate bone loss in hy-
over rates for amino acids that are not poestrogenic female athletes. Taking more
branched chain, such as lysine, are unaf- than 4 g of extra protein per kilogram per
fected by exercise,90 nitrogen losses are not day can also cause loss of appetite and di-
consistently elevated during and after exer- arrhea.
cise,90 and no loss of muscle mass can be de-
tected during exercise.90 VITAMINS
Taking extra protein does not increase
protein turnover rates in exercisers,91 but Sixty million Americans, or 37% of the
when combined with a heavy resistance adult population, take vitamin supple-
program, it was shown to increase protein ments.96 More women (42%) than men
retention slightly.92 In that study, an extra 2 (31%) take vitamins, presumably because
g of protein supplements per kilogram per they are more health conscious than men.
day was added to the subjects' usual intake Three out of four Americans think that tak-
of 1.3 g. The vast majority of the extra pro- ing extra vitamins will give them more en-
tein was oxidized for energy, with only a ergy.97 One out of five believes that lack of vi-
small amount retained in lean tissue. tamins causes arthritis and cancer,98 and
The sole stimulus to make a muscle one out of 10 does not know that vitamin re-
stronger is to exercise that muscle against quirements can be met without taking sup-
resistance. This stimulus is so strong that plements.99 Although 10% may seem like a
muscles can be enlarged and strengthened small part of the population, this figure sig-
by proper resistance training, even if a sub- nifies that 25 million Americans believe that
ject is fasting or losing weight and if all of her they have to take vitamin supplements to be
other muscles are becoming smaller.93 healthy.
It does not take much extra protein to sup-
ply amino acids for enlarging muscles. An
Mechanism of Function
athlete with an excellent strength-training
program may gain 1 Ib of muscle in a week. A vitamin is an organic compound that the
Since muscle is 72% water, 1 Ib of muscle body requires in small amounts for health.
contains only about 100 g of protein. How- While the exact mechanisms of function for
ever, the loss of efficiency in high-quality several vitamins are not completely under-
protein utilization is around 30% and in stood, much is known about the function of
poorer-quality protein, around 60%. There- the B vitamins, which are parts of enzymes.
fore, to build 100 g of extra protein, the ath- Because the enzymes containing these vita-
lete must consume 130 g of high-quality pro- mins are required in only small amounts,
Nutrition for Sports 115

they catalyze reactions without being de- These four vitamins catalyze the reactions
pleted. that convert carbohydrates and protein to
The B vitamins enter the cells that are to energy.105 For example, heavy exercise can
use them. Such cells produce apoenzymes, increase riboflavin requirements by as
which combine with the vitamins to form much as 17%,105 but the total daily needs for
holoenzymes. Cells produce only limited riboflavin can be met by drinking three
amounts of apoenzymes, leaving unbound B glasses of milk. The total needs for all four
vitamins in excess. The Recommended Di- "energy" vitamins can be met by eating a
etary Allowances (RDAs) for B vitamins, de- varied diet that contains more than 2000 cal-
termined by the Food and Nutrition Board ories per day, because all four of these vita-
(FNB) of the National Research Council of mins are found in meat, fish, chicken, milk,
the National Academy of Sciences, "are the and whole grains.
levels of intake ... adequate to meet the Although the refining process removes
known nutritional needs of practically all thiamine, niacin, riboflavin, and panto-
healthy persons."100 It also represents the thenic acid from flour, most manufacturers
amount of B vitamins that will saturate the routinely add these vitamins in order to
apoenzymes of the target cells.100 Ingesting comply with interstate shipping laws. Thus,
more vitamins does not increase the rate of athletes who eat breads made from refined
reactions, because cellular apoenzymes are flour rarely need supplements containing
the limiting factor. these "energy vitamins."
To help your patients understand why ex-
cess dosages of B vitamins are not needed,
you can use the following analogy offered by Vitamin C and Colds
Herbert and Barrett.101 Consider the human Some athletes take large doses of vitamin
body to be like a traffic intersection. Many C in the hope that it will help to protect them
cars (chemical reactions) pass through the from developing upper respiratory infec-
intersection, but only one police officer (vi- tions. However, virtually all double-blind
tamin) is necessary to direct traffic. Bringing studies on the subject show that vitamin C
in many police officers (excess vitamins) does not prevent colds.106
will not cause more cars (chemical reac-
tions) to pass through the intersection.
Vitamins and Birth Control Pills
Vitamin Needs of Female Whether women who take oral contracep-
Athletes tives require vitamin supplementation re-
mains controversial.107-109A review of the lit-
The diets of athletes who take in more erature shows that, on the average, women
than 2000 calories per day usually supply vi- who take birth control pills have lower
tamins in amounts greater than their serum levels of riboflavin, pyridoxine, fola-
RDAs.102 People who try to control their cin, cyanocobalamin, and ascorbic acid and
weight usually restrict their intake of food, higher body levels of vitamin K.109 However,
and this can lead to an intake of vitamins their tissue levels110 and blood levels111 are
that is less than the RDA. However, the still within the normal range. There is no ev-
RDAs are set so far above minimum require- idence that such women are more likely to
ments that dieters rarely develop signs or develop clinical symptoms of vitamin defi-
symptoms of vitamin deficiency, even if they ciency. Since birth control pills increase the
do not meet the RDAs.103 need for these vitamins only a small per-
Prolonged exercise can increase require- centage, if at all, it seems unlikely that vita-
ments for thiamine, niacin, riboflavin, and min requirements change appreciably be-
pantothenic acid beyond their RDAs.104 cause of oral contraceptive use.
116 Basic Concepts of Exercise Physiology

Vitamins and Premenstrual Table 6-8. Minerals


Syndrome
Major Trace
Strength, speed, endurance, and coordi-
Calcium Fluorine
nation have not been shown to vary consis- Phosphorus Silicon
tently throughout the menstrual cycle. Fe- Chlorine Vanadium
male athletes report greater perceived Potassium Chromium
exertion premenstrually. Premenstrual syn- Sulfur Manganese
drome (PMS) is discussed more thoroughly Sodium Iron
Magnesium Cobalt
in Chapter 13. Nickel
Several investigators have suggested that Copper
nutritional factors play a role in PMS and Zinc
have proposed dietary therapy for this syn- Selenium
drome. Pyridoxine has been touted as a Molybdenum
Tin
treatment for PMS, because it is claimed to Iodine
raise serotonin levels in the brain. Pyridox-
ine is a coenzyme for 5-hydroxy-tryptophan
decarboxylase, which catalyzes trypto-
phan's conversion to serotonin. High levels ments which contain iron. Most healthy
of serotonin are associated with mood ele- people can take iron supplements without
developing obvious toxicity.124 However, a
vation; low levels are associated with de-
pression. There is no evidence, however, recent study from Finland124a showed that
that PMS sufferers have low brain levels of high stored iron levels may increase a per-
serotonin or that giving extra pyridoxine son's chances of developing a myocardial
will raise brain levels. Two studies showed infarction. It is proposed that free iron cat-
alyzes free radical production which con-
that taking pyridoxine improves PMS symp-
toms,112,113 while another showed no im- verts LDL cholesterol to oxidized LDL to
provement.114 Although many women con- form arteriosclerotic plaques in arteries.
Iron supplements can harm people who
sider pyridoxine, in any dosage, to be
have hereditary disorders of iron metabo-
harmless, large doses of pyridoxine have
been reported to cause neural toxicity.115,116 lism, such as hemochromatosis and por-
phyria.
As many as one out of every four female
MINERALS athletes is iron deficient.117 Men and non-
menstruating women need about 12 mg of
The major minerals are listed in Table 6- iron per day. The average man ingests ade-
8. Iron and calcium are the only supple- quate iron from dietary sources alone. The
ments that healthy female athletes may average woman ingests around 12 mg of iron
need to take. An adequate diet can provide per day, but menstruating women need 18
adequate amounts of all minerals, but many mg of iron per day, the extra 6 mg needed to
diets are deficient in these two. replace the iron that is lost through men-
strual bleeding. Birth control pills reduce
iron requirements by decreasing menstrual
Iron blood loss and increasing iron absorption.118
Because of the high prevalence of iron de- Iron deficiency, even in the absence of
ficiency among female athletes and because anemia, can impair endurance.119 Approxi-
of its detrimental effect upon performance, I mately 40% of the iron in the body is in the
recommend that female athletes who have iron reserves, such as the liver, bone mar-
ferritin levels below 25 take daily supple- row, and spleen. The rest is contained in he-
ments containing 30 to 60 mg of elemental moglobin. Iron-deficiency anemia does not
iron. All others should avoid all supple- occur until almost all of the iron reserves are
Nutrition for Sports 117

depleted. Iron deficiency reduces the con- and vitamin D all help to prevent osteopo-
centration of a-glycerophosphate oxidase in rosis. Estrogen appears to be the most im-
muscle, and this impairs glycolysis and portant. With adequate calcium intake, es-
leads to lactic acid accumulation in muscle trogen replacement, and exercise, even
and blood.120 An increase in lactate causes a osteoporotic bones can increase in den-
lowering of pH, and this reduces muscular sity.125 Low bone density of any cause in-
endurance.121 People who have iron defi- creases a woman's chances of developing
ciency, even without anemia, have a re- stress fractures during exercise.126
duced rate of lactic acid clearance from the Exercise can enlarge bones and increase
blood, and they tire earlier during exercise. bone density.127,128The bones in the racquet-
Restoring their iron reserves to normal in- holding arm of a tennis player are larger and
creases their endurance.122 denser than those in the other arm. Runners
The most accurate test for detecting iron have denser femoral shafts than rowers,
deficiency is a microscopic examination of dancers, and sedentary controls.129 How-
bone marrow for stained iron. However, ob- ever, exercise will not maintain bone den-
taining marrow is painful, invasive, and ex- sity effectively in women who lack estro-
pensive. A simple, noninvasive screening gen.130 For example, exercise-associated
test for iron deficiency is the measurement amenorrhea is associated with decreased
of serum ferritin. Caution must be used in in- bone density,131 and estrogen replacement
terpreting the results, since inflammation helps to maintain bone density in hypoes-
anywhere in the body can raise ferritin lev- trogenic women.132 Birth control pills do not
els. A person who has an inflammatory pro- affect bone density in women whose bodies
cess may have normal serum ferritin levels produce estrogen.133 Women who have
despite having iron deficiency. Further- higher-than-normal levels of androgens
more, exercise raises serum ferritin levels. have denser bones.134
Patients who have a microcytic, hypochro- Nevertheless, adequate calcium intake is
mic anemia with normal ferritin levels with- essential for maintenance of bone density.
out elevated fetal hemoglobin should have Children who do not ingest adequate
their serum ferritin levels repeated after amounts of calcium during growth have
they stop exercising for a week.123 smaller bones with reduced amounts of cal-
Up to 30% of heme iron, found in meat, cium, and develop osteoporosis at an in-
fish, and chicken, is absorbed, while less creased rate as adults.135,136 Increasing di-
than 10% is absorbed from nonheme iron etary calcium can improve calcium balance
sources. Acidity enhances iron absorption in women who lack estrogen.137 Hypoestro-
from nonheme sources but not from heme genic women require 1500 mg of calcium per
sources. Thus, eating an orange with spin- day to maintain zero calcium balance,
ach enhances iron absorption from the spin- whereas euestrogenic women require 1000
ach, but taking vitamin C with meat does not mg to do so.138 However, estrogen is far more
increase absorption of iron from meat. On effective than dietary calcium in maintaining
the other hand, alkalinity, fiber, and tannins bone density.139 Hypoestrogenic, amenor-
reduce iron absorption from both heme and rheic women who do not have a contraindi-
nonheme sources. For example, taking ant- cation to estrogen replacement therapy
acids, eating fibrous vegetables, or drinking should be treated with estrogen and, if di-
tea or coffee decreases iron absorption from etary calcium is inadequate, calcium supple-
all sources. ments.
The best dietary sources of calcium are
dairy products and soft-boned fish, such as
Calcium
canned salmon and sardines (Table 6-9).
Estrogen, androgenic hormones, exer- Dairy products provide 72% of dietary cal-
cise, dietary calcium, etidronate, calcitonin, cium for the average American.140 Those who
118 Basic Concepts of Exercise Physiology

Table 6-9. FOODS THAT CONTAIN Sodium


APPROXIMATELY 250 MG CALCIUM
Most people do not need to consume extra
1 glass milk sodium when they exercise. The require-
1 cup yogurt ment for sodium for people at rest is 0.2 g/d.
1% cups cottage cheese
IHcups icecream With prolonged exercise in very hot
IHozhard cheese weather, the maximal requirement for so-
2 oz sardines with bones dium is approximately 3 g/d. The average
4 oz canned salmon with bones American diet contains between 6 and 18 g
of sodium chloride per day, of which 40% is
sodium (2.4 to 7.2 g). Manufacturers add so-
dium chloride to foods as a preservative,
do not meet their calcium requirements
and some people add sodium chloride to
from diet alone should take calcium supple-
foods to improve the taste. Athletes who try
ments (Table 6-10), unless they are predis-
to limit sodium intake by avoiding salty-tast-
posed to nephrolithiasis. ing foods and by adding no sodium to foods
The Food and Drug Administration has still take in about 3 g of sodium each day.
found significant amounts of lead in some Sodium chloride tablets should not be
samples of bone meal and dolomite.141 Do- given routinely to exercising athletes. Be-
lomite is most frequently harvested from the sides being unnecessary, they can cause
shells of shellfish at the bottom of harbors. gastric irritation, nausea, and, in very large
Dolomite taken from polluted harbors can doses, potassium deficiency.
contain toxic amounts of lead, mercury, ar- Sodium deficiency can occur in healthy
senic, and other heavy metals. Bone meal people because of an inadequate intake of
also may contain significant amounts of sodium or excessive use of diuretics. It can
toxic metals, since it usually comes from the also occur in people with hormonal or renal
bones of older animals.142 With aging, toxic defects. Any exerciser who feels tired and
metals accumulate in the bones of all ani- weak or develops painful muscle cramps
mals, including humans. Because dolomite should have serum levels of sodium mea-
and bone meal are usually sold as food sup- sured. If present, hyponatremia requires a
plements rather than drugs, manufacturers thorough evaluation to determine the cause
are not required by the government to list (e.g., diabetes insipidus, diabetes mellitus,
the heavy metal content of their products. water intoxication, and so on).
Therefore, labels on packages containing Many women who experience premen-
these products do not list their heavy metal strual fluid retention as part of PMS may
content. benefit from dietary sodium restriction at
the times of symptoms during each cycle.
Despite anecdotal reports of the success of
Table 6-10. CALCIUM CONTENT IN 600- this regimen, no scientific studies have as-
MG SUPPLEMENT
sessed its effectiveness.
Number of Pills
% Required to
Content of Pill Mg Calcium Ingest 1 G Potassium
Calcium 240 40 4 Potassium deficiency is an extremely rare
carbonate
Calcium lactate 78 13 12 condition in trained athletes. The kidney
Calcium 54 9 18.5 and sweat glands are highly efficient in con-
gluconate serving potassium in response to low body
Calcium 171 28 6 levels. Even with prolonged exercise in very
phosphate hot weather, potassium needs can be met by
(dibasic)
an intake of only 3 to 4 g/d.143 However, po-
Nutrition for Sports 119

tassium deficiency can occur as the result of They argue that repeated harvesting of
potassium restriction and sodium loading.144 crops depletes the soil of essential minerals.
The only way that one researcher could When the soil in a certain region is deficient
create a low-potassium diet for athletes and in a mineral, the plants and animals that
still provide enough calories for exercise grow in that region will suffer from a defi-
was to feed them candy and little else ciency of that mineral also. That may have
throughout the day. Even then, the athletes been possible in the past, but it is extremely
did not develop potassium deficiency.145 Al- unlikely to occur now. Although it is possi-
most all foods are rich in potassium. Since ble that some soils lack certain minerals, our
potassium is found primarily within cells, transportation system is so extensive and ef-
any food that contains cells also contains ficient that very few Americans eat foods
potassium. grown only in a single locality. It is impos-
Hypokalemia always requires a thorough sible for all soils to be deficient in the same
evaluation to determine the cause. Potas- single mineral.
sium deficiency can be caused by drugs, Oral contraceptive agents may reduce re-
such as diuretics and corticosteroids, and quirements for copper slightly and raise
certain foods, such as licorice. Prolonged di- those for zinc, but there is no evidence that
arrhea and vomiting also can cause potas- the latter is enough to require supplemen-
sium deficiency (Table 6-11). With diarrhea, tation. Women who take birth control pills
potassium is lost in the stool. With vomiting, have higher serum levels of copper and
loss of hydrogen ions causes a metabolic al- lower levels of zinc than those who do not
kalosis, which increases potassium loss in take such pills.146,147 Estrogen is thought to
the urine to conserve renal hydrogen ions. raise serum copper levels by increasing
Bulimia can present in athletes as weak- serum ceruloplasmin levels.148 The mecha-
ness and tiredness with laboratory evidence nism by which oral contraceptives lower
of potassium deficiency. If blood samples serum zinc levels is not known.149
show reduced potassium levels, and 24-hour
urine collections contain increased amounts
of potassium, suspect vomiting as the cause. THE ATHLETE'S DIET

Of course, your patients cannot become


Trace Minerals
great athletes just by altering their diets.
Humans require approximately 14 trace They have to choose their parents wisely
minerals in small amounts. There is no evi- and train harder than their competitors.
dence that athletes need trace mineral sup- From the foregoing discussion, it is obvious
plements, with the exception of iron, be- that they can get all the nutrients their bod-
cause trace mineral deficiencies are ies need from the foods they eat. With the
extremely rare in healthy athletes. possible exceptions of iron and calcium, a
Some lay publications for athletes claim female athlete's requirement for nutrients is
incorrectly that trace mineral deficiencies the same as it is for male athletes. The only
are common causes of fatigue in athletes. supplements that are required commonly
are iron and calcium. Taking large doses of
vitamin and mineral supplements can be
toxic. Adverse side effects have been re-
Table 6-11. MECHANISM BY WHICH ported from large doses of even the rela-
VOMITING CAUSES HYPOKALEMIA
tively harmless water-soluble vitamins,
Loss of hydrogen ions such as niacin, pyridoxine, and folic acid. To
Raised blood pH help your patients perform sports more ef-
Renal hydrogen retention fectively, you should recommend that they
Renal potassium loss
eat a varied diet that is rich is carbohydrates
120 Basic Concepts of Exercise Physiology

and that they follow the rules for eating and meal on the night before competition, and
timing foods and drinks that are outlined in by eating an easily absorbed meal 5 or fewer
this chapter. hours prior to competition. Maintaining ad-
Several lay books claim that a high-fiber, equate hydration, even before experiencing
low-fat diet will improve athletic perfor- thirst, will also improve endurance. The rate
mance. There is no evidence to support this. of recovery following intense exercise can
In fact, one study showed that exercisers be hastened by eating extra carbohydrates
who ate a diet that contained 10% fat had the and drinking large amounts of fluids soon
same improvement in Vo2max as those who after exercising.
obtained 45% of their calories from fat.150 Vitamin supplementation is not neces-
Nevertheless, you may want to recommend sary, since requirements can be met through
restricting dietary fat, saturated fat, and diet. Healthy athletes do not need to in-
cholesterol because it may help to reduce a crease their intake of sodium, potassium, or
woman's chances of developing coronary trace minerals because the body can usually
artery disease and certain types of cancers compensate for increased loss or decreased
in the future. intake by increasing retention.
Taking into account that foods have nutri-
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syndrome. Curr Med Res Opin 6(Suppl termining bone loss by exercise interven-
5):40, 1979. tion in premenopausal and postmenopausal
113. Abraham GE, and Hargrove JT: Effect of vi- women. Calcif Tissue Int 44:312,1989.
tamin B6 on premenstrual symptomatology 129. Wolman RL, Faulman L, Clark P, et al: Differ-
in women with premenstrual tension syn- ent training patterns and bone mineral den-
drome: A double-blind cross-over study. In- sity of the femoral shaft in elite, female ath-
fertility 3:155, 1980. letes. Ann Rheum Dis 50:487, 1991.
114. Stokes J, and Mendels J: Pyridoxine and 130. Dhuper S, Warren M, Brooks-Gunn J, and
premenstrual tension. Lancet 1:1177, 1972. Fox R: Effect of hormonal status on bone
115. Schaumberg H, et al: Sensory neuropathy density in adolescent girls. J Clin Endocri-
from pyridoxine abuse: A new megavitamin nol Metab 71:1083-1088,1991.
syndrome. N Engl J Med 309:445,1983. 131. Drinkwater E, Nilson K, Chesnut CH, et al:
116. Vasile A, Goldberg R, and Kornberg E: Pyri- Bone mineral content of amenorrheic and
doxine toxicity: Report of a case. J AOA eumenorrheic athletes. N Engl J Med
83:790,1984. 311:277,1984.
117. Margen S, and King J: Effect of oral contra- 132. Shangold MM: Causes, evaluation, and man-
ceptive agents on the metabolism of some agement of athletic oligo/amenorrhea. Med
trace minerals. Am J Clin Nutr 28:392,1975. Clin North Am 69:83, 1985.
118. de Wijn JF, De Jongste JL, Mosterd W, et al: 133. Lloyd T, Buchanan JR, Ursino GR, et al:
Hemoglobin, packed cell volume, serum Long-term oral contraceptive use does not
iron and iron-binding capacity of selected affect trabecular bone density. Am J Obstet
athletes during training. Nutr Metab 13:129, Gynecol 160:402,1989.
1971. 134. Dixon JE, Rodin A, Murby B, et al: Bone
119. Lukkaski HC, Hall CB, and Siders WA: Al- mass with androgen excess. Clin Endocrinol
tered metabolic response of iron-deficient 30:271, 1989.
women during graded, maximal exercise. 135. Matkovic V: Calcium metabolism and cal-
Eur J Appl Physiol 63:140,1991. cium requirements during skeletal remod-
120. Finch CA, Miller LR, Inamdar AR, et al: Iron eling and consolidation of bone mass. Am J
deficiency in the rat, physiological and bio- Clin Nutr 54:2455,1991.
chemical studies on muscle dysfunction. J 136. Sentipal JM, Wardlaw GM, Mahan J, and
Clin Invest 58:447, 1976. Matkovic V: Influence of calcium intake and
121. Finch CA, Gollnick PD, Hlastala MP, et al: growth indexes on vertebral bone mineral
Lactic acidosis as a result of iron deficiency. density in young females. Am J Clin Nutr
J Clin Invest 64:129, 1979. 54:425, 1991.
122. Nilson K, Schoene RE, Robertson HT, et al: 137. Recker RR, Saville PD, and Heaney RP: Ef-
The effects of iron repletion on exercise-in- fect of estrogen and calcium carbonate on
duced lactate production in minimally iron- bone loss in postmenopausal women. Ann
deficient subjects. Med Sci Sports Exerc Intern Med 87:649, 1977.
13:92, 1981. 138. Heaney RP, Recker RR, and Saville PD:
123. Pattini A, Schena F, and Guidi GC: Serum fer- Menopausal changes in calcium balance
ritin and serum iron changes after cross- performance. J Lab Clin Med 92:953, 1978.
country and roller ski endurance races. Eur 139. Riis B, Thomsen K, and Christiansen C: Does
J Appl Physiol 61:55, 1990. calcium supplementation prevent post-
Nutrition for Sports 125

menopausal bone loss? A double-blind, con- 146. Prasad AS, Oberleas D, Lei KY, et al: Effect of
trolled clinical study. N Engl J Med 316:173, oral contraceptive agents on nutrients: I.
1987. Minerals. Am J Clin Nutr 28:377,1975.
140. Marston RM, and Welsh SO: Nutrient con- 147. Schenker JG, Hellerstein S, Jungreis E, et al:
tent of the U.S. food supply. Nat Food Rev Serum copper and zinc levels in patients
25:7, 1984. taking oral contraceptives. Fertil Steril
141. Advice on limiting intake of bonemeal. FDA 22:229, 1971.
Drug Bull 12:5, 1982. 148. Carruthers ME, Hobbs CE, and Warren RL:
142. Roberts NJ: Potential toxicity due to dolo- Raised serum copper and caeruloplasmin
mite and bonemeal. South Med J 76:556, levels in subjects taking oral contraceptives.
1983. J Clin Pathol 19:498,1966.
143. Lane HW, Roessler GS, Nelson EW, et al: Ef- 149. Prasad AS, Moghissi KS, Lei KY, et al: Effect
fect of physical activity on human potas- of oral contraceptives on micronutrients
sium metabolism in a hot and humid envi- and changes in trace elements due to preg-
ronment. Am J Clin Nutr 31:838, 1978. nancy. In Moghissi KS, and Evans TN (eds):
144. Talbot NB, Richie RH, and Crawford JD: Nutritional Impacts on Women Throughout
Metabolic Homeostasis: A Syllabus for Life with Emphasis on Reproduction.
Those Concerned with the Care of Patients. Harper and Row, New York, 1977, p 160.
Harvard University Press, Cambridge, 1959, 150. Kosich D, Conlee R, Fisher AG, et al: The ef-
p32. fects of exercise and a low-fat diet or a mod-
145. Costill D: Muscle water and electrolytes dur- erate-fat diet on selected coronary risk fac-
ing acute and repeated bouts of dehydra- tors. In Dotson C, and Humphrey J (eds):
tion. In Panzkova J, and Rogozkin VA (eds): Exercise Physiology: Current Selected Re-
Nutrition, Physical Fitness and Health. Uni- search, Vol 2. AMS Press, New York, 1986, p
versity Park Press, Baltimore, 1978, p 106. 173.
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II
Developmental
Phases
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CHAPTER 7

The Prepubescent Female


ODED BAR-OR, M.D.

PHYSIOLOGIC RESPONSE TO Response to Cold Climate


SHORT-TERM EXERCISE High-Risk Groups for Heat- or Cold-
Submaximal Oxygen Uptake Related Disorders
Maximal Aerobic Power
Anaerobic Power and Muscle
GROWTH, PUBERTAL CHANGES,
Endurance
AND ATHLETIC TRAINING
Muscle Strength
TRAINABILITY
COEDUCATIONAL PARTICIPATION
THERMOREGULATORY CAPACITY IN CONTACT AND COLLISION
Response to Hot Climate SPORTS

r ReLecent years have seen an increasing interest in the physiologic response


children to exercise. Such interest reflects the greater participation and success
of prepubescents and adolescents in elite sports, as well as the recognition that
physical exercise is relevant to the health of the nonathletic child.
Although prepubescent athletes of both sexes engage in elite sports, it is pri-
marily the females who have become extremely successful at the national and
international levels. Such success is particularly apparent in gymnastics, figure
skating, and swimming, in which prepubescents have been performing at levels
that, a decade or two ago, were not considered feasible even for adults.
To achieve such excellence, many female athletes have to practice as much
as 4 to 6 hours per day and at high intensity. Such involvement and dedication
has educational, psychosocial, medical, gynecologic, orthopedic, and physio-
logic consequences. These have become a focus of research for sports scientists
of various disciplines.
Exercise-related research is oriented also toward the young nonathlete,
healthy or ill. Study of the healthy child has been of interest, for example, to kin-
anthropometrists, who are interested in growth patterns and the interrelation-
ships between morphologic and functional changes; to epidemiologists, who
assess the possible relationships between habitual activity during childhood
and the risk of chronic disease in later years; to motor behaviorists, who study
motor learning and skill acquisition; and to physiologists, who seek answers to
such maturation-related issues as strength development, energy expenditure of
locomotion, trainability, and thermoregulation.
The relevance of exercise to the ill child has also generated growing interest.
129
130 Developmental Phases

Pediatric cardiologists and respirologists, ysis of relationships between fitness and


for example, are using exercise for the as- growth in girls.
sessment of children with such diseases as
congenital heart defects, bronchial asthma,
and cystic fibrosis; an exercise prescription PHYSIOLOGIC RESPONSE TO
is incorporated into the management of the SHORT-TERM EXERCISE
child with diabetes mellitus, obesity, mus-
cular dystrophy, cerebral palsy, and cystic Differences in the response to short-term
fibrosis; and detrimental effects of exercise exercise (less than a 15-minute duration) of
are studied in such conditions as aortic ste- prepubescent and older females are sum-
nosis, dysrhythmia, primary amenorrhea, marized in Table 7-1. Table 7-2 is a sum-
and epilepsy. mary of gender-related differences in the re-
This chapter is meant to focus on the sponse of prepubescents to short-term
physiologic responses to exercise of the exercise. The following discussion will high-
healthy prepubescent girl. Emphasis will be light those characteristics of the prepubes-
given to differences among prepubescents, cent girl that have a direct relevance to her
adolescents, and young adults. Differences physical performance.
will also be pointed out between the re-
sponses to exercise of girls and boys. When-
Submaximal Oxygen Uptake
ever relevant, the implications to health of
such differences will be pointed out. Typically for young girls, oxygen uptake
It is assumed that the reader has some (calculated per body mass unit) while run-
basic knowledge of exercise physiology. Ad- ning or walking at any given speed is higher
ditional information on pediatric exercise than in adolescent or adult females.1,22-24 A
physiology can be found in monographs, 1-6 5.5-year-old girl, for example, who runs at 10
edited books,7-10 and proceedings of the Pe- km/h, consumes about 46 mL of oxygen per
diatric Work Physiology Group. 11-20 Further- kilogram of body weight per minute, com-
more, a journal (Pediatric Exercise Sciences, pared with 37 m L - k g - 1 - m i n - 1 in a 16-year-
Human Kinetics, Champaign, IL) is available old adolescent. Calculated per body surface
which is fully dedicated to the effects of ex- area, however, such differences disappear.25
ercise in children. A recent monograph21 in- The implication of such a high metabolic
cludes a comprehensive, longitudinal anal- cost is that, at any walking or running speed,

Table 7-1. SOME PHYSIOLOGIC RESPONSES TO ACUTE EXERCISE:COMPARISON


BETWEEN PREPUBESCENT GIRLS AND OLDER FEMALES
Typical for Girls
(Compared with
Physiologic Function Older Females)
O2 cost of walking/running Higher
O2 uptake max, L • m i n - 1 Lower
O2 uptake max, mL • k g - 1 • min -1 Higher
Heart rate submax Higher
Stroke volume submax Lower
Cardiac output submax Lower
Minute ventilation submax Higher
Ventilatory equivalent submax and max Higher
Peak anerobic power, watt Lower
Peak anaerobic power, watt • kg - 1 Lower
Mean anaerobic power, watt Lower
Mean anaerobic power, watt • k g - 1 Lower
The Prepubescent Female 131

Table 7-2. GENDER-RELATED however, there is little change in the Vo2max


COMPARISON OF THE RESPONSE OF of girls up to the age of 10 to 11 years. During
PREPUBESCENTS TO ACUTE EXERCISE the second decade of life, Vo2max per kilo-
Girls' Response gram decreases with age, such that it is ap-
(Compared proximately 4 to 6 mL-kg~'-min - 1 lower at
Physiologic Function with Boys) age 17 to 18 than at age 10 to n.1,2,29'30 It has
O2 cost of walking/running Similar been suggested that the lower Vo2max per
O2 uptake max, L • min~' Somewhat lower kilogram in the pubertal girl is due to the de-
O2 uptake max per kg body weight Somewhat lower crease in blood hemoglobin concentration,
O2 uptake max per kg lean mass Similar secondary to menstrual blood loss. This,
Heart rate submax Higher however, does not explain the drop in
Heart rate max Similar
Stroke volume submax and max Lower Vo 2max per kilogram of body weight even
Minute ventilation submax Similar before menarche. One reason could be the
Minute ventilation max Somewhat lower increasing adiposity of many girls who ap-
Peak anaerobic power, watt Somewhat lower proach puberty.31-33 Decreasing aerobic
Peak anaerobic power, watt • kg - 1 Lower power could also result from an age-related
Mean anaerobic power, watt Somewhat lower
Mean anaerobic power, watt • kg -1
Lower decrease in spontaneous habitual activity in
the second decade of life. 33-37
Although gender-related differences in
maximal aerobic power are apparent pri-
a young girl operates at a higher percentage marily after age 12 to 13 years, boys seem to
of her maximal aerobic power and will fa- have a somewhat 1,2, 33,38- 40
higher Vo2max even at ear-
tigue earlier than an older girl or a woman. lier ages. In a study comparing the
This may be the main reason why young maximal aerobic power of 6- to 16-year-old
girls cannot compete on a par with their girls and boys who were tested on the cycle
older counterparts in middle- and long-dis- ergometer, such gender-related differences
tance running. Such a difference is virtually were eliminated when Vo2max (L-min - 1 )
nonexistent during cycling.26-28 This sug- was plotted against lean leg volume rather
gests that the biochemical-to-mechanical than against age.39 A similar pattern was ap-
energy transfer efficiency in muscles is not parent among 8- to 16-year-old girls and
lower at a young age, but young girls have a boys when W170 (i.e., the mechanical power
more "wasteful" gait, which increases their at which they cycle when their heart rate is
mechanical output and metabolic demands 170 beats per minute) was plotted against
during the gait cycle. No data are available body cell mass.41 It should be realized, how-
on the age-related differences in the meta- ever, that when Vo2max is divided by lean
bolic cost of swimming. The success of leg volume or lean body mass, preadoles-
young girls in elite swimming would suggest, cent boys still have higher values than pre-
however, that a proficient young swimmer is adolescent girls.33 A more precise determi-
not less economical in her style than her nation of body composition is needed to tell
older counterpart. whether gender-related differences in max-
imal aerobic power of prepubescents are
Maximal Aerobic Power fully explained by the mass of their exercis-
ing muscles.
Throughout childhood and adolescence,
maximal aerobic power, as reflected by max-
imal oxygen uptake (Vo2max), increases Anaerobic Power and Muscle
with age. The Vo2max of 5-year-old pre- Endurance
schoolers is 0.80 to 0.90 L-min - 1 compared High-intensity muscle contractions that
with 1.1 to l.5L-min - 1 and 1.6 to 2.2L-min - 1 cannot be sustained for more than 20 to 30
for 10- and 16-year-old girls, respectively.1,2 seconds are dependent primarily on anaer-
Calculated per kilogram of body weight, obic energy pathways. Examples of "anaer-
132 Developmental Phases

obic" activities are short and long sprints in tive deficiency of anaerobic power in the
running, skating, and cycling, as well as prepubescent. Children of both sexes have
short slalom in downhill skiing. Until recent lower maximal blood lactate concentration
years, this component of fitness received lit- than do adolescents and adults. It has been
tle attention, compared with maximal aero- reported for boys, but not for girls, that cre-
bic power and muscle strength. This re- atine phosphate and glycogen concentra-
flected the paucity of reliable and valid tions in the resting muscle and, in particular,
laboratory tests for peak muscle power and the rate of glycolysis in the contracting mus-
local muscle endurance. Such tests are cur- cle are low before puberty. (For more de-
rently available, using cycle ergometers or tails, see reference 2.) Based on animal stud-
isokinetic machines. These have been ies, a relationship has been suggested
added to the Margaria step-running test,42 between muscle lactate production and cir-
which assesses peak muscle power but not culating testosterone. Whether this applies
muscle endurance. The following informa- also to humans—females or males—has yet
tion has been obtained using the Margaria to be shown. It can be assumed, however,
test and the Wingate anaerobic test.43 that a low glycolytic capacity in prepubes-
The ability of prepubertal girls and boys cents of both sexes is the main cause of their
to perform anaerobic tasks is distinctly low anaerobic performance.
lower than that of adolescents and young
adults. This was first shown for 8- to 73-year- Muscle Strength
old sedentary Italians: even when divided
by body weight, the peak muscle power of Muscle strength, defined as the maximal
the 8- to 10-year-old girls was only about force that can be exerted by a muscle or a
60% that of the 20-year-old women.42 Similar group of muscles, is similar in girls and boys
results have been shown for Nilo-Hamitic during their first decade of life.33,47 Strength
and Bantu African,44 British,39 American,45 is growth-dependent.33,47-49However, it does
and Israeli2 populations. In the last, peak not increase linearly with the growth in
muscle power and muscle endurance of the body mass or stature. In girls, the main in-
arms and the legs were both lower in the crease in strength occurs during, a few
young girls, even when corrected for differ- months following, or even just before the
ences in body weight. "growth spurt" (i.e., the year during which
The aforementioned pattern is in contrast body height velocity is at its peak). In con-
to maximal aerobic power which, when cal- trast, the increase of strength in boys
culated per kilogram body weight, is higher reaches its peak about 1 year after the
in the prepubescent girl than in the adoles- growth spurt.50,51 This difference, coupled
cent or adult female. with the earlier growth spurt in girls (about
The mechanism for the low anaerobic per- a 2-year difference), may explain why the
formance of prepubescent girls is not greater muscle strength of boys is usually
known. In a recent study performed in my not evident before age 11 or 12 years.
laboratory on adolescent girls and boys,46
lean muscle mass of the upper limb ex- TRAINABILITY
plained much of the variance in arm peak
power and muscle endurance of the boys but Does a prepubescent girl respond to train-
not of the girls. Performance of both prepu- ing in the same manner as an adolescent or
bescent girls and boys in the Margaria test, an adult female? This question is of utmost
even when corrected for fat-free mass, is relevance to the theory and practice of
lower than that of adolescents and adults.44 coaching, but should be of interest also to
It is quite likely, therefore, that qualitative the pediatric physiotherapist and the phys-
characteristics of the muscles, and possibly iatrist who wish to apply physiologic prin-
their neural control, would explain the rela- ciples to rehabilitation.
The Prepubescent Female 133

To obtain definitive answers about train- Few studies are available on the trainabil-
ability (i.e., the ability of body systems to ity of muscle strength at different ages. Niel-
adapt to repeated exercise stimuli) of differ- sen and co-workers49 trained 249 Danish
ent age groups, one must conduct a longitu- girls aged 7 to 19 years for 5 weeks. One sub-
dinal training study on these groups. Such a group did isometric knee extension, another
design must satisfy two conditions: (1) the the "vertical jump," and the third practiced
initial fitness level of all groups must be sim- acceleration in sprints. As in adults, there
ilar and (2) the training dosage must be was specificity in the responses: each sub-
equated among the groups. group improved most in the specific
Unfortunately, neither condition can be strength (but not sprinting) task at which it
adequately satisfied. First, one cannot as- had been training. While the authors did not
sume that a 6-year-old girl who, for example, report the pubertal stage of the subjects, the
sprints 50 m in 11.0 seconds has the same younger girls (less than 13.5 years) im-
sprinting ability as a 16-year-old adolescent proved more than the older ones. Likewise,
who runs at the same speed. A better ap- 8-year-old German girls improved their iso-
proach might be to use a physiologic crite- metric arm strength more than did adults
rion for equating the initial fitness level. One when given a similar training stimulus.57
cannot be sure, however, that a maximal aer- Whether trainability of strength is related to
obic power of 40 m L - k g - 1 m i n - 1 in a 6-year- the pubertal stage has yet to be shown. Most
old girl denotes the same aerobic fitness as research on muscle trainability of children
an identical value in a 20-year-old woman. It is limited to boys. There are indications,
is also fairly difficult to equate training dos- however, that trainability during prepuberty
ages. Can one assume, for example, that is similar in boys and girls.58 This is indirect
weight training at 70% of their maximal vol- evidence that training-induced strength
untary contraction represents the same gains can be achieved without the effect of
physiologic strain in a girl and a woman? androgens.
Because of such methodologic con-
straints, conclusions about the trainability
of young girls are not definitive. Some pat- THERMOREGULATORY
terns, however, seem to emerge. According CAPACITY
to several reports, when prepubescent girls
Most research on the thermoregulatory
take part in aerobic training, they respond characteristics of the exercising child is
with little or no increase in maximal oxygen
uptake, even though their athletic ability based on studies in boys. (For a review, see
may improve.52-55 This is unlike the re- reference 59.) Data are available, however,
to suggest that girls are at a disadvantage,
sponse to aerobic training of women, who
increase their maximal oxygen uptake and compared with women, when exposed to ei-
improve their athletic performance. Only a ther hot or cold climates. Very few data are
few studies have suggested that prepubes- available to compare the responses to heat
cent females do improve their maximal ox- and cold of prepubertal girls and boys.
ygen uptake in response to aerobic train-
ing.56 Response to Hot Climate
A major reason for the improvement of Table 7-3 is a summary of the morpho-
running performance in the absence of in- logic and physiologic characteristics of pre-
creased Vo2max is the training-induced im- pubescent females, as related to their ther-
provement in running economy, which is moregulatory capability. As discussed
manifested by a decrease in the O2 cost of earlier, the smaller the girl, the higher her
running. During adolescence, both aerobic Vo2 per kilogram of body weight at any given
power and running economy may improve walking or running speed. Because 75% to
with training. 80% or more of the chemical energy during
134 Developmental Phases

Table 7-3. MORPHOLOGIC AND PHYSIOLOGIC CHARACTERISTICS OF PREPUBESCENT GIRLS


AS RELATED TO THERMOREGULATION
Typical for Girls
Characteristic or Function (Compared with Women) Implication for Thermoregulation
O2 cost of running/walking Higher High metabolic heat
Surface-to-mass ratio Larger Greater heat exchange with environment
Onset of sweating Later Greater reliance on convective heat loss
Sweating rate Somewhat lower Lower evaporative capacity
Blood flow, peripheral vs. central Higher 1. Higher heat convection
2. Lower venous return

muscle contraction is converted into heat, low sweating capacity), it also decreases the
the metabolic heat load of the prepubescent venous return and stroke volume.60 The re-
girl is higher (by as much as 5% to 20%) than sulting decrease in maximal cardiac output
that of the adolescent or the adult, at equiv- is another explanation for the low ability of
alent walking or running tasks. Such a differ- prepubertal girls to exercise intensively in
ence imposes a greater strain on the young, hot climates. It should be added that, at any
small girl's thermodissipatory system. given exercise level, even when performed
Another size-related difference is the in neutral environments, cardiac output in
larger skin surface-area-per-mass ratio in young girls is somewhat lower than that of
the smaller individual. The rate of heat ex- women.61
change between the body and the environ- In summary, these geometric and physio-
ment depends on this surface area. There- logic characteristics suggest that a priori
fore, when the environment is warmer than young girls would tolerate exercise in hot
the skin, the smaller the girl, the greater the climates less effectively than adolescent or
heat gain (through conduction, convection, adult females. It has indeed been shown
and radiation) per unit body mass. This dif- that, during extreme climatic heat, prepu-
ference in heat gain becomes particularly bescent girls had to terminate their pre-
important in extreme climatic heat. scribed walking task earlier than did young
Evaporation of sweat is the main avenue women.60'62 In thermoneutral environments,
for heat dissipation during exercise, espe- on the other hand, there is no evidence that
cially in hot climates. When ambient tem- young age or small body size is detrimental
perature exceeds skin temperature, evapo- to thermoregulation.63
ration is the only available means of heat As recently shown,64 the sweat of prepu-
dissipation. Compared with women, prepu- bescent girls has a lower concentration of
bertal girls have a slow onset of sweating sodium and chloride, and a higher concen-
and a somewhat lower sweating rate while tration of potassium, than the sweat of ado-
exercising in the heat,60 which limit their ca- lescent females or of women. One possible
pacity for evaporative cooling. This differ- implication of this difference is that the op-
ence between prepubescents and adults timal electrolyte concentration of sports
seems to be even more apparent among beverages may be different for prepubes-
males. cent girls and for more mature females.
Girls were found to respond to exercise in
the heat with a marked shift of blood from
Response to Cold Climate
the central to the cutaneous vascular bed.
Although greater skin blood flow facilitates In most land-based sports, the rate of met-
greater convection of heat from the body abolic heat production exceeds heat loss,
core to the periphery (which, under certain even when the environmental temperature
climatic conditions, may compensate for a is low. Such is the case, for example, in skat-
The Pre:pubescent Female 135

ing and cross-country skiing. In other winter mented for college-age women, although the
sports, such as downhill skiing or curling, findings for prepubertal girls were inconclu-
the rate of heat production may not be high, sive.62
but clothing usually prevents excessive heat Hypohydration may often lead to heat-re-
loss. Hypothermia occurs not infrequently lated disorders. While data are not available
in such sports as mountain climbing, regarding the effects of hypohydration on
snowshoeing, and even long-distance run- the thermoregulation and health of prepu-
ning at low intensity. There is, however, no bescent girls, data on boys suggest that, for
epidemiologic evidence that prepubescent a given level of hypohydration, children
girls are more prone to hypothermia in have a greater rise in core temperature than
these events than are older females. do young adults.™ Conditions in which ex-
In contrast, small individuals are at a dis- ertion may induce heat-related disorders
tinct disadvantage during water-based ac- through hypohydration are diabetes melli-
tivities. When swimming at a speed of 30 tus, diabetes insipidus, diarrhea, and vomit-
m/rnin in 20.3°C water, 8-year-old girls (club ing. Prepubescent boys70 and girls (unpub-
swimmers) had a drop in core temperature lished data from my laboratory), like adults,
of as much as 2.5 to 3.0°C and had to be taken undergo "voluntary hypohydration" when
out of the water within 18 to 20 minutes they exercise for long periods (e.g., 1 to 2
owing to marked thermal discomfort. Their hours), even when fluids are available to
16- to 19-year-old clubmates swam for some them ad libitum. One group of young girls
30 minutes, with hardly any drop in core who are prone to hypohydration is those
temperature and with little or no thermal who compete in judo and "make weight"
discomfort.65 The reason for the cold intol- prior to competition. In some states where
erance of the younger girls was their large elementary school girls compete in wres-
surface area per mass, which facilitated con- tling, the same practice is probably fol-
ductive heat loss (water having a heat con- lowed.
ductivity at least 25 times that of air). The Lack of acclimatization to exercise in the
authors also found that the leaner girls had heat is perhaps the most important factor
a greater heat loss than those who had a that predisposes an individual to heat-re-
thicker insulative subcutaneous fat layer. lated disorders. Data suggest that 8- to 10-
year-old boys take longer than adults to ac-
climatize to the heat.71 No similar studies are
High-Risk Groups for Heat- or
available for girls, but it makes good sense to
Cold-Related Disorders
ensure that young female athletes are well
Some girls are at a potentially high risk for acclimatized to the heat before they are ex-
such heat-related disorders as heat exhaus- pected to train hard and perform well in
tion or heat stroke, while others may be warm or humid climates.
prone to hypothermia. As for hypothermia, a small, lean girl who
Evidence is available that girls with an- is immersed in water is at a greater risk than
orexia nervosa have a deficient thermoreg- a larger girl or one with thicker subcutane-
ulatory capability, both in the heat and in ous adipose tissue.
the cold.66,67 Patients with cystic fibrosis are
prone to heat-related disorders,68 possibly
because of their abnormal sweating pattern. GROWTH, PUBERTAL
Undernourished children are prone to both CHANGES, AND ATHLETIC
hypothermia and hyperthermia.69 Obese in- TRAINING
dividuals perform well and feel comfortable
in cold climates but are less tolerant to ex- Trained prepubescent and adolescent
ercise in the heat than their leaner counter- girls often have different morphologic and
parts. Such intolerance has been docu- maturational characteristics from those of
136 Developmental Phases

their untrained counterparts. A question short legs, and higher body adiposity—drop
often asked by coaches, physicians, and par- out because of unfavorable changes in body
ents is whether training per se affects mechanics.
growth, development, and maturation. To Based on reports from the late 1970s and
obtain a definitive answer, one would need early 1980s, delayed menarche (defined as
to launch a prospective study in which non- occurring after age 15 years) was particu-
athletic prepubescent girls are randomly as- larly common among divers, figure skaters,
signed to training and control groups and gymnasts, and volleyball players.73 Menar-
then followed until after puberty. Such a che is particularly delayed in those athletes
project has yet to be launched. Data avail- who are engaged in high-dosage training.
able at present are based on cross-sectional Delayed menarche in athletes seems also to
comparisons between athletes and nonath- correspond to delayed skeletal maturity.73
letes and among athletes of various special- Several factors, singly or in combination,
ties, or on retrospective analyses. The few have been suggested to link delayed men-
longitudinal studies lack proper controls.72 arche to physical training. Among these are
The conclusions derived from such studies a low percentage of body fat,80,81 insufficient
therefore are tentative at best and cannot calorie intake in conjunction with "energy
prove causality between training and drain,"72 onset of training prior to menar-
changes in growth, development, and mat- che,76 large sibship,82 and emotional stress of
uration. training and competition. It has also been
The following are general comments, suggested,83 but has yet to be confirmed, that
based on such studies. (For detailed re- hormonal changes which are associated
views, see Malina,73 Malina and co-work- with chronic exercise may be a cause for
ers,74 and Wells.75) Various female athletes, delayed menarche. In one study,72 low
primarily gymnasts, figure skaters, and bal- serum gonadotropins—LH, particularly—
let dancers, mature later and are shorter were found in premenarcheal ballet danc-
than the nonathletic female population. Oth- ers. Other endocrinologic studies are based
ers, notably swimmers, have little or no on postmenarcheal athletes (see reference
delay in maturation and are often taller than 84 for details).
nonathletes. 72-74,76-78 These data might sug- In a comprehensive review on menarche
gest that the above morphologic and matu- in athletes, Malina73 presented a two-part
rational differences are caused by training. hypothesis on the possible relationship be-
Such conclusions, however, ignore prese- tween physical activity and delayed menar-
lection and a possible bias in the drop-out che. First is the preselection by body char-
pattern. It is likely, for example, that those acteristics, in which the girl with a linear
girls with delayed puberty and short stature physique, long legs, and narrow hips (who is
become preferentially attracted to such often also a late maturer) is attracted to
sports as gymnastics and figure skating, sports and eventually is successful in them.
while the taller ones are more attracted to Second is the "socialization" process, in
competitive swimming. A recent retrospec- which early-maturing girls tend to interact
tive study79 has shown that 8- to 14-year-old socially in a nonsport environment with the
female gymnasts who were shorter than the appearance of pubertal changes. Con-
nonathletic population had been shorter versely, the late maturers are more likely to
even prior to having joined the gymnastics find sports participation socially gratifying.
program. Similarly, swimmers, who, as a Indeed, preselection and the bias in drop-
group, were taller than their nonathletic ping out from athletics may explain the late
counterparts, had been taller before train- menarche of athletes as found in cross-sec-
ing. It is also possible that, within a group of tional and retrospective analyses. One can-
gymnasts, those females who mature not ignore, however, the accumulating data
early—and thus attain broad hips, relatively on a more direct, possibly cause-and-effect,
The Prepubescent Female 137

relationship between intense sports partic- chronologic age around puberty, differences
ipation and secondary amenorrhea. in body size and strength of early and late
Although primary amenorrhea is a "nor- maturers within a gender group far surpass
mal" and common occurrence among ath- the intergender differences. Nor is there any
letes, one should not overlook the possibil- evidence to suggest that prepubescent girls
ity that it might reflect gynecologic or other are less capable of learning sport skills, are
hormonal abnormalities. (For details of rec- less agile, or have less stamina than boys.87,88
ommended investigations and of therapeu- While not addressing specifically the pre-
tic approach, see Shangold in reference 85, pubescent girl, a recent review on orthope-
as well as Chapter 8.) dic issues in the young female athlete89
points out the emergence of "overuse inju-
ries" during the teens. It rejects, however,
COEDUCATIONAL the notion that girls are more prone to injury
PARTICIPATION IN CONTACT than boys.
AMD COLLISION SPORTS Based on anthropometric and fitness-re-
lated considerations alone, therefore, pre-
Should prepubescent girls compete with pubescent girls can compete successfully
boys in contact (e.g., wrestling, basketball, with boys in contact and collision sports,
soccer) and collision (e.g., football, ice and with no undue risk to health. An early
hockey) sports? This issue has become maturing girl, in point of fact, may have an
highly controversial, attracting media atten- edge over boys who are average maturers. It
tion, because of its medical, educational, seems as though matching of prepubescent
and cultural implications. The following and circumpubescent opponents by body
comments are not meant to address the psy- size and maturation level has more rele-
chologic, sociologic, or ethical aspects of vance to health than the separation into gen-
this controversy but only some of the phys- der groups.
iologic and medical aspects.
A major issue is the added risk to health
that participants of either sex group may SUMMARY
incur owing to mixed participation. The
main potential cause for such added risk is a The physiologic responses to exercise in
marked difference in body mass, strength, the prepubescent girl are of a similar pattern
or skill among the participants. At age 9 to 12 to those of the more mature female. There
years, body mass of girls is similar to, or are, however, some age- or development-re-
even slightly greater than, that of boys. Body lated differences in these responses. The
height at that age range is quite similar in submaximal 02 cost during walking or run-
boys and girls, and the difference in the ning is higher in the young girl, which
strength of various muscle groups is only causes a lower "metabolic reserve" and
about 1 to 2 kg in favor of the boys.51 This is early fatigability in endurance events. Like-
to be contrasted with the increasingly wise, anaerobic muscle power and local
greater muscle strength of males—particu- muscle endurance are markedly lower in
larly in the upper body—after puberty.86 The prepubescents, who are therefore unlikely
attainment of such motor skills as throwing, to compete successfully with their older
kicking, catching, jumping, hopping, and counterparts in events such as jumping and
skipping during the first years of life is sim- sprinting. Girls are less-effective thermore-
ilar in boys and girls. Throughout the pre- gulators when exercising in the heat and in
pubertal years, these and other motor skills the cold. This has implications both to their
seem to develop and improve at a similar performance and to their health. Girls with
pace in both sex groups.87 obesity and anorexia nervosa are at special
It should be realized that, at any given risk for heat-related illness. Although more
138 Developmental Phases

research is needed, it appears that the train- and Exercise. Acta Paediatr Belg (Suppl
ing-induced improvement in maximal aero- 28):1, 1974.
bic power is low before puberty. 15. Borms J, and Hebbelinck M (eds): Pediatric
Work Physiology. Karger, Basel, 1978.
A causal relationship among training, 16. Ilmarinen J, and Valimaki I: Pediatric Work
growth, and maturation has yet to be estab- Physiology X. Springer Verlag, Berlin, 1983.
lished. It seems, however, that the delayed 17. Lavallee H, and Shephard RJ (eds): Frontiers
menarche in athletes may be in part a result of Activity and Child Health. Pelican, Quebec,
of intense training. 1977.
18. Rutenfranz J (ed): Pediatric Work Physiology
While coeducational participation in con- XII. Human Kinetics, Champaign, IL, 1986.
tact and collision sports may be objected to 19. Thoren C (ed): Pediatric Work Physiology.
on psychologic and societal grounds, there Acta Paediatr Scand (Suppl 213): 1, 1971.
are no physiologic or medical reasons to 20. Frenkel R, and Szmodis I (eds): Children and
ban such activities before puberty. Exercise. Pediatric Work Physiology XV. Sig-
net, Budapest, Hungary, 1991.
21. Simons J, Beunen GP, Renson R, et al (eds):
Growth and Fitness of Flemish Girls: The Leu-
ven Growth Study. Human Kinetics, Cham-
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Med Sci Sports 5:11, 1973.
CHAPTER 8

Growth, Performance, Activity,


and Training during Adolescence
ROBERT M. MALINA, Ph.D.

THE ADOLESCENT GROWTH Significance of the Adolescent


SPURT Plateau in Performance
Body Size
Body Composition INFLUENCE OF TRAINING ON THE
TEMPO OF GROWTH AND
MENARCHE
MATURATION DURING
PHYSICAL PERFORMANCE AND ADOLESCENCE
ACTIVITY DURING Stature and Body Composition
ADOLESCENCE Sexual Maturation
Strength Hormonal Responses
Motor Performance Fatness and Menarche
Maximal Aerobic Power Other Maturity Indicators
Physical Activity Habits Overtraining

AAdolescenceis a period of transition from childhood to adulthood. It includes


changes in the biologic, personal, and social domains that prepare the young girl
for adulthood in her particular culture. Thus, the biologic changes that occur
during puberty, or sexual maturation, do not occur in isolation; rather, they are
related to other developmental events so that any consideration of this period
of life must be done in a biosocial or biocultural context.
Biologically, adolescence may be viewed as beginning with an acceleration
in the rate of growth (i.e., an increase in size) prior to the attainment of sexual
maturity, then merging into a decelerative phase, and eventually terminating
with the cessation of growth. The latter is most often viewed as the attainment of
adult stature. Sexual maturity and growth are thus closely related.
The events that constitute this phase of the life cycle include changes in the
nervous and endocrine systems that initiate and coordinate the sexual, physio-
logic, and somatic changes; growth and maturation of the primary (ovaries,
vagina, and uterus) and secondary (breasts and pubic hair) sex characteristics,
leading to menarche and reproductive function; changes in size (i.e., the adoles-
cent growth spurt); changes in proportions, physique, and body composition;
and changes in the cardiorespiratory system, among others. The two most prom-
141
142 Developmental Phases

inent outward features of adolescence (ex- starts in some girls as early as 7 or 8 years of
cluding behavior) are accelerated growth age and in others as late as 12 or 13 years,
and appearance of secondary sex character- while the age at maximum rate of growth in
istics, which appear, on the average, during stature (PHV) occurs in some girls as early
the second decade of life. However, the neu- as 9 or 10 years of age and in others as late
roendocrine and other physiologic events as 13 to 15 years.1
underlying growth and pubertal change
have been in progress for some time prior to
the appearance of physical changes. The Body Composition
time span accommodating the growth spurt The fat-free mass (FFM) of girls, esti-
and puberty is thus wide. It can vary from 8 mated from body density, increases from
or 9 years through 17 or 18 years of age in about 25 kg at 10 years to about 45 kg at 18
girls, and in some cases may continue into years of age, whereas muscle mass, esti-
the early 20s. There is variation between in- mated from creatinine excretion, increases
dividuals in the time and rate at which the from about 12 kg at 10 years to 23 kg at 18
structural and functional changes occur; years.1 However, the major portion of
that is, the changes do not begin at the change in FFM and muscle mass between 10
same time and do not proceed at the same and 18 years occurs during the interval of
rate. maximal growth (about 11 to 13 years in
girls). This interval includes PHV, which oc-
curs, on average, at about 12 years of age in
THE ADOLESCENT GROWTH girls. The adolescent gain in FFM and mus-
SPURT cle mass during female adolescence is not,
however, as intense as that in males, so that
Body Size by late adolescence, females attain only
From birth to adulthood, both height and about two thirds of the estimated mean val-
weight follow a four-phased or double-sig- ues reported for males. Peak velocities of
moid growth pattern: rapid gain in infancy growth in arm and calf musculature occur,
and early childhood; slower, relatively con- on average, after PHV.
stant gain in middle childhood; rapid gain Fatness also increases during adoles-
during adolescence; and slow increase and cence, but estimates are highly variable.
eventual cessation of growth at the attain- Densitometric estimates increase from 18%
ment of adult size. Most dimensions of the body fat at about 10 years of age to 23% at 18
body—sitting height, leg length, shoulder years.1 These estimates are adjusted for
and hip breadths, limb circumferences, changes in the estimated chemical compo-
muscle mass, and so on—follow a similar sition of FFM (i.e., density of FFM, potas-
growth pattern. What varies is the timing, sium and water content of FFM) that occur
tempo, and intensity of the adolescent during growth and are lower than those
growth spurt in each. For example, maxi- based on adult chemical composition fig-
mum growth (peak velocity) in leg length ures. At the time of the growth spurt, how-
occurs early in the growth spurt, prior to ever, the rate of fat accumulation slows
that for sitting height or trunk length, while down in girls. This is especially apparent on
maximum growth in body weight occurs the extremities during the interval of PHV in
after peak height velocity (PHV). girls.
The timing of the growth spurt varies con-
siderably among children. Most data are
available for stature. According to data from MENARCHE
several longitudinal studies, the adolescent
growth spurt (i.e., the acceleration in rate of The age at menarche is perhaps the most
growth that marks the take-off of the spurt) commonly reported developmental mile-
Growth, Performance, Activity, and Training during Adolescence 143

stone of female adolescence. It is, however, improves more slowly.1 This pattern is in
a rather late maturational event. Menarche contrast to the marked acceleration of
occurs after maximum growth in stature; the strength development during male adoles-
average difference between menarche and cence, so that sex differences in muscular
PHV in a number of studies is about 1.2 to 1.3 strength are considerable.
years.1 The relationship between strength devel-
Menarche in American girls occurs, on av- opment and the growth spurt and sexual
erage, just before the 13th birthday. How- maturation in girls is not as clear as in boys.
ever, there is variability within the U.S. pop- Maximum strength development occurs, on
ulation. In the National Health Examination the average, after peak height and weight ve-
Survey in the 1960s, the median ages at men- locity in boys, the relationship being better
arche were 12.5 years for black girls and 12.8 with weight than with height.1,5 In girls, the
years for white girls.2 The median age at available longitudinal data vary. In the Oak-
menarche in American girls has not land (California) Growth Study, the time of
changed, on average, since the 1950s.3 Esti- maximum strength development (a compos-
mates for a number of European samples ite strength score of right and left grip and
vary between 12.5 and 13.4 years.1,4 pushing and pulling tests) does not closely
In contrast to population surveys of men- correspond to the growth spurt in stature,
arche, in which the average age for the pop- and a significant percentage of girls experi-
ulation is estimated mathematically on the ence peak strength gains prior to PHV.6 Peak
basis of the number of girls in each age strength gain precedes peak weight gain in
group who have attained menarche, many more than half of the girls, and follows peak
studies of athletes and of the influence of weight gain in only about one fourth. On the
training on the age at menarche use the ret- other hand, in the study of Dutch girls
rospective method. This approach relies on (Growth and Health of Teenagers), peak de-
the memory of the individual and thus has velopment of strength (arm pull test) oc-
the limitation of error in recall. curs, on average, one-half year after PHV
(the same time as it occurs in Dutch boys).7
The maximum gain in strength at this time is
PHYSICAL PERFORMANCE AND about 6.0 kg/y in girls, which contrasts with
ACTIVITY DURING a maximum gain of 12.0 kg/y in Dutch boys.7
ADOLESCENCE The data for Dutch girls are not expressed
relative to peak gain in body weight.
Characteristics of the adolescent growth Early-maturing girls are slightly stronger
spurt and sexual maturation, and of interre- than late-maturing girls of the same chron-
lationships among indices of sexual, skele- ologic age during early adolescence, about
tal, and somatic maturity, are reasonably 11 through 13 years.1 The differences be-
well documented. Changes in physical per- tween girls of contrasting maturity status,
formance and activity during female adoles- however, do not persist and are no longer
cence are less well documented. The data evident by 14 to 15 years of age. Further, the
are largely cross-sectional, with but few lon- differences in muscular strength between
gitudinal observations spanning the imme- girls of contrasting maturity status during
diate prepubertal and pubertal years. adolescence are not as marked as those be-
tween early- and late-maturing boys. The
strength advantage of girls advanced in ma-
Strength
turity status between 11 and 13 years re-
Muscular strength improves linearly with flects the larger body size of early maturers,
age from early childhood through about 15 since strength is positively related to body
years of age in girls, with no clear evidence mass. When strength is expressed per unit
of an adolescent spurt. After age 15, strength body weight, early maturers have less
144 Developmental Phases

strength per unit body weight than late-ma- of high- and low-performing girls indicated
turing girls; this difference persists through that the superior performers were about 0.5
adolescence.1 year less mature skeletally and 0.4 year later
in menarche.12 This trend is apparent in elite
female athletes (i.e., skilled performers),
Motor Performance
who tend to be later in age at menarche and
Average performances of girls in a variety delayed in skeletal maturation.13,14
of motor tasks (dash, standing long jump,
jump and reach, distance throw, and others)
improve more or less linearly from child- Maximal Aerobic Power
hood through about 13 or 14 years of age, Absolute maximal oxygen uptake (mL/
followed by a plateau in the ability to per- min) has a growth pattern in girls similar to
form some tasks and a decline in others.1,8,9 that for motor performance: it increases lin-
In most tasks, the average performances of early with age from 7 years through 13 to 14
girls fall within one standard deviation of years in untrained girls, and then declines
the boys' averages in early adolescence. slightly.15 In contrast, in untrained boys, it
After 13 to 14 years of age, however, the av- increases linearly with age through adoles-
erage performances of girls are often out- cence, so that by 16 years of age the differ-
side the limits defined by one standard de- ence between maximal oxygen uptake in un-
viation below the boys' mean performance. trained boys and girls is about 56%. When
Overhand throwing performance is an ex- expressed relative to body weight (mL-
ception; few girls approximate the throwing kg-1 • min -1 ), aerobic power declines with
performances of boys at all ages from late age from 6 through 16 years in untrained
childhood on. girls, but is more or less constant in un-
Longitudinal data relating the motor per- trained boys. The slope of the regression in
formance of girls to the timing of the adoles- girls declines from a value of 52.0 mL-kg -1
cent growth spurt are not available. Cross- min-1 at 6 years of age to 40.5 mL-kg -1
sectional analysis of longitudinal data does min -1 at 16 years. Values for untrained boys
not suggest adolescent spurts in the motor at corresponding ages are 52.8 and 53.5 mL-
performances of girls. Performances in a va- kg-1 • min - 1 , respectively, yielding a negligi-
riety of motor tasks show no tendency to ble sex difference of 1.5% at 6 years, but a
peak before, at, or after menarche (which considerable difference of 32% at 16 years.15
occurs, on average, about 1 year after PHV); The sex difference in aerobic power per
rather, performances are generally stable unit of body weight at 16 years of age is prob-
across time.5 Among boys, on the other ably related to sex differences in body com-
hand, motor performances show rather position. The aerobic power of girls per unit
clear adolescent spurts. Maximal gains in of body weight is approximately 77% of the
functional strength and power tests (flexed value for boys. This percentage is not too dif-
arm hang and vertical jump) occur, on av- ferent from estimates of lean body and mus-
erage, after PHV, whereas maximal gains in cle mass in late adolescence; that is, girls at-
speed tests (shuttle run, speed of hand tain, on the average, only about two thirds of
movement) and flexibility (sit and reach) the values for boys. The increase in relative
occur before PHV.10 fatness associated with the sexual matura-
Correlations between skeletal and sexual tion of girls probably contributes to the sex
maturity and motor performance in girls are difference in aerobic power per unit of body
low and, for many tasks, negative. The latter weight.
suggests that later maturation is more often Absolute aerobic power (mL/min) shows
associated with better motor performance a clear adolescent spurt in both girls and
in girls, whereas the opposite is more often boys, which on average occurs close to that
true in boys.1,11,12 For example, a comparison for stature.16 This reflects the growth of
Growth, Performance, Activity, and Training during Adolescence 145

heart and lung functions in proportion to through 9 (12 to 14 years), and 11.8 hours in
overall body size.1 Given the size differences grades 11 and 12 (15 to 17 years). Although
between early- and late-maturing girls, the the data suggest a trend, more specific
former have a slightly larger absolute aero- changes with age cannot be examined. In a
bic power, especially during early adoles- mixed-longitudinal sample of Dutch girls,20
cence. When expressed per unit of body the average number of hours per week spent
weight, however, relative aerobic power is in physical activity with an average energy
higher in late maturers.17 expenditure of 4 metabolic equivalents
Aerobic power responds positively to (METs) or more declined from 9.6 hours at
training, so that absolute and relative maxi- 12 to 13 years to 8.1 hours at 17 to 18 years.
mal oxygen uptakes are greater in trained The earlier adolescent years were not con-
than in untrained girls at all ages. The differ- sidered.
ences between trained and untrained girls Intensity is a critical variable when con-
are greatest during adolescence. It is also in- sidering physical activity. In the mixed-lon-
teresting to note that trained girls and boys gitudinal Dutch study, girls aged 12 to 13
differ by only 24% for absolute and 18% for participated, on the average, in only 4.0 h/
relative oxygen uptake at age 16, in contrast wk of activities of medium intensity (7 to 10
to comparable differences of 56% and 32% in METs), and 0.5/h/wk in activities of heavy
untrained boys and girls of the same age.15 intensity (10+ METs). By 17 to 18 years, the
Studies of aerobic power seldom control corresponding hours per week were 1.5 and
for the maturity status of the subjects, and O.3.20 Clearly, the majority of the activities of
the few studies that do are largely limited to these girls were of light intensity.
boys. Correlations between skeletal age and Given the type of data available, it is diffi-
aerobic power are generally low,15 but the cult to make inferences about activity habits
association between body mass and skeletal during the adolescent growth spurt and sex-
maturity confounds the relationship.1 ual maturation, as well as about possible ef-
fects of rapid growth and maturation on
activity habits. The figures do suggest, how-
Physical Activity Habits ever, that most adolescent girls are not get-
Physical activity is a major component of ting sufficient regular physical activity to
the daily energy expenditure. Energy expen- maintain a high level of aerobic fitness.
diture in free-living children and youth is dif-
ficult to measure, and the few available stud-
ies are limited to rather small samples with Significance of the Adolescent
Plateau in Performance
narrow age ranges, and largely to boys.18
Standardized questionnaires, interviews, Data relating the physical performance of
and diaries are often used to estimate phys- girls to the timing of the growth spurt and
ical activity habits in large samples of sexual maturation are not extensive. A ques-
youngsters, usually 10 years of age and tion that merits more detailed study is the
older. The data, however, are largely de- relative flatness of the performance curves
scriptive and do not consider growth and of girls during adolescence. That is, their
maturity characteristics. Results of several level of performance shows little improve-
surveys of European, Canadian, and Ameri- ment in many tasks after 13 to 14 years of
can youth indicate a slight decline in time age, and in some tasks it actually declines. Is
spent in physical activity by girls during ad- this trend related primarily to biologic
olescence.18 In the United States survey,19 for changes in female adolescence (e.g., sexual
example, the average weekly time engaged maturation, fat accumulation, physique
in physical activity outside of school physi- changes), or is it related to cultural factors
cal education was 11.5 hours in grades 5 and (e.g., changing social interests and expec-
6 (10 to 11 years), 12.5 hours in grades 7 tations, pressure from peers, lack of moti-
146 Developmental Phases

vation, limited opportunities to participate of this maturational event may be pro-


in performance-related physical activities)? grammed by conditions early in life and
Most likely both biologic and cultural fac- not necessarily by those conditions that
tors are reflected in the trend. Thus, the may be operating at or about the time of pu-
overall age-related pattern of physical per- berty.24-25
formance during female adolescence may A question of concern, therefore, is the
change with the recent emphasis on and op- role of intensive training for sport and per-
portunity for athletic competition for young haps of the stress of competition on the tim-
girls, and the wider acceptability of women ing and tempo of growth and sexual matu-
in the role of athlete. ration during adolescence. It should be
obvious that physical activity is only one of the
many factors that may influence growth and
maturation.
INFLUENCE OF TRAINING ON
THE TEMPO OF GROWTH AND
MATURATION DURING Stature and Body Composition
ADOLESCENCE Regular physical training has no apparent
effect on statural growth. It is, however, a
Under adequate environmental condi- significant factor in the regulation of body
tions, the timing of the adolescent growth weight and composition, specifically fat-
spurt and sexual maturation is genetically ness. Changes in response to short- or long-
determined. However, these processes can term training programs largely reflect fluc-
be influenced by environmental factors. The tuating levels of fatness, with minimal or no
delaying effects of chronic undernutrition change in FFM. The role of regular activity in
are well documented. Socioeconomic varia- the development of adipose tissue cellular-
tion in growth and maturation is evident in ity and subcutaneous fat distribution is not
some societies but not in others.1 Criteria of clearly established.26
socioeconomic status, of course, vary from Regular training is a significant factor in
country to country, but data from industri- the growth and integrity of skeletal and mus-
alized countries indicate inconsistent cle tissues. Changes in bone tissue include
trends in ages at PHV and menarche relative greater mineralization, density, and mass.
to indices of socioeconomic status. Another Training-associated changes in muscle tis-
factor related to age at menarche is the num- sue are generally specific to the type of pro-
ber of children in the family. Girls from gram followed. Strength or resistance train-
larger families tend to experience menarche ing is associated with hypertrophy, whereas
later than those from smaller families, and endurance training is associated with in-
this applies to athletes as well as nonath- creases in oxidative enzymes. The direction
letes. The estimated effect of each additional of responses to training in growing individ-
sibling on the age at menarche ranges from uals is similar to those observed in adults,
0.11 to 0.22 years in several samples of ath- but the magnitude of the responses varies.26
letes and nonathletes.21 The persistence of beneficial training ef-
Stressful life events are also significant. fects on adipose and muscular tissues de-
They are especially evident in the growth pends upon continued activity. In contrast,
and maturation of youngsters experiencing evidence is accumulating that excessive
disturbed home environments,22 and in the training associated with altered menstrual
"unusually 'fractured' curves of growth and function (see below and Chapter 9) and diet
pubertal development in girls translated to contributes to bone loss in some athletes.27,28
unfamiliar boarding schools at various Thus, there may be a threshold for some ad-
times in puberty."23 Studies of secular olescent athletes: regular training has a ben-
change in menarche suggest that the timing eficial effect on the integrity of skeletal tis-
Growth, Performance, Activity, and Training during Adolescence 147

sue up to a point, but excessive activity may between years of training before menarche
alter menstrual function and have a negative and age at menarche, a moderate correla-
influence on bone mass. tion that accounts for only about 28% of the
sample variance. Correlation does not imply
a cause-and-effect sequence, however; the
Sexual Maturation
association is more likely an artifact. The
Longitudinal data on the effects of training older a girl is at menarche, the more likely
on sexual maturation of girls (and boys too) she would have begun her training prior to
are lacking, and the available cross-sec- menarche, and conversely, the younger a
tional data do not indicate a significant effect girl is at menarche, the more likely she
of training on sexual maturation. Much of would have begun training after menarche
the discussion of training and sexual matu- or would have a shorter period of training
ration is based on comparisons of later prior to menarche.29 It could also be that
mean ages at menarche of athletes with later maturation is a factor in a girl's deci-
those of the general population, with the in- sion to take up sport, rather than the train-
ference that intensive training for sport "de- ing causing the lateness.13 Further, athletes
lays" menarche.13 The menarcheal data are as a group tend to be rather select, and other
generally consistent with observations of factors known to influence menarche are not
breast and pubic-hair development and considered in the analysis.
skeletal maturity of young athletes engaged It has also been suggested that menarche
in figure skating, ballet, gymnastics, and occurs later specifically in those disciplines
track—that is, they develop later.14 How- that emphasize low body weight, such as
ever, girls training for sport at prepubertal ballet and gymnastics.31 Emphasis on low
ages are not necessarily representative of body weight may involve dietary practices
those who are successful at later ages, who that adversely influence maturation, so that
in turn constitute the samples of athletes it would be difficult to partition dietary from
upon whom most menarcheal data are training effects. In addition, such sports
based. Also, Title IX legislation has influ- tend to have rather rigorous selection cri-
enced sport opportunity for girls and teria, which are often applied early in child-
women, so that many now continue to train hood and which favor the morphologic
and compete through the college years. In characteristics of the late-maturing girl. Fi-
the not-too-distant past, on the other hand, nally, data for elite university-level athletes
many young girls stopped training and com- indicate later mean ages at menarche in ath-
peting at 16 or 17 years of age. The oppor- letes across several sports that differ con-
tunity provided by Title IX most likely has siderably in training load and emphasis on
influenced the composition of the female body weight: diving, track and field, swim-
athlete population at the college level, par- ming, tennis, golf, basketball, and volley-
ticularly in swimming. The age at menar- ball.21
che in college-age swimmers in recent Nevertheless, two questions merit consid-
estimates21-29 is considerably older than that eration. First, are regular, intensive, prepu-
of elite swimmers about 20 years ago,13 and bertal training for sport and regular compe-
this is in contrast to the advanced pubertal tition sufficiently stressful to prolong the
status and skeletal maturity often observed prepubertal state and in turn delay the ado-
in age group swimmers.14 lescent growth spurt and sexual maturation?
Although not the first to suggest that train- Second, do intensive training for sport and
ing may delay menarche, Frisch and the stress of competition during the adoles-
colleagues30 concluded that for every year a cent growth spurt and sexual maturation
girl trains before menarche, her menarche produce conditions that are sufficiently ad-
will be delayed by up to 5 months. This con- verse to influence the progress and thus the
clusion is based on a correlation of +0.53 timing of these maturational events?
148 Developmental Phases

Hormonal Responses association with only "mild" growth stunt-


ing, for example, has been reported in pre-
The suggested mechanism for the associ- menarcheal ballet dancers.34 The dancers
ation between training and later menarche were delayed in breast development, men-
is hormonal. It is suggested that intensive arche, and skeletal maturation, which would
training and perhaps the associated energy suggest a prolonged prepubertal state. How-
drain influence circulating levels of gonad- ever, they were not delayed in pubic hair de-
otropic and ovarian hormones, and in turn, velopment.
menarche. Lower plasma levels of estrone, testoster-
Exercise is an effective means of stressing one, and androstenedione have been ob-
the hypothalamic-pituitary-ovarian axis, served in 11-year-old prepubertal gymnasts
producing short-term increases in serum than in swimmers of the same age and ma-
levels of all gonadotropic and sex steroid turity status, but plasma gonadotropin and
hormones.32,33 Other factors also influence dehydroepiandrosterone-sulfate (DHEAS)
hormonal levels, including diurnal varia- levels did not differ in the two samples. On
tion, state of feeding or fasting, emotional the other hand, plasma levels of the seven
states, and so on, and these need to be con- hormones assayed did not differ between
sidered. Further, virtually all hormones are early pubertal (stage 2 of breast develop-
episodically secreted, so that studies of hor- ment) gymnasts and swimmers, although
monal responses based on single serum the latter were an average of 0.5 year older.35
samples may not reflect the overall pattern. Both the prepubertal and early pubertal
What is needed are studies in which 24-hour gymnasts had been training regularly for a
levels of hormones are monitored or in longer period than the swimmers. The two
which actual pulses are sampled every 20 groups of gymnasts had been training since
minutes or so in response to exercise. Oth- 4.8 and 5.0 years of age, respectively,
erwise, the evidence from the available whereas the two groups of swimmers had
studies on the hormonal response to exer- been training since 7.2 and 8.0 years of age.
cise is inconclusive. The similar levels of DHEAS in the prepu-
It should be noted that the majority of hor- bertal gymnasts and swimmers suggests a
monal data do not deal with chronic similar stage of adrenarche, although the
changes associated with regular, intensive gymnasts had been training for a signifi-
training. Further, the data are largely de- cantly longer period. This observation thus
rived from samples of postmenarcheal does not support the suggestion that train-
women, both athletes and nonathletes, who ing delays adrenarche and prolongs the pre-
are physiologically quite different from the pubertal state.36 Moreover, recent evidence
maturing girl. What is specifically relevant does not support the view that secretion of
for the prepubertal or pubertal girl is the adrenal androgens triggers sexual matura-
possible cumulative effects of hormonal re- tion.37 Early childhood growth data for the
sponses to regular training. The hormonal two groups of athletes suggest physique dif-
responses are apparently essential to meet ferences. Since 3 years of age, the gymnasts
the stress that intensive activity imposes on had been shorter and lighter than Dutch ref-
the body. Do they have an effect on the hy- erence data, whereas the swimmers had
pothalamic center, which apparently trig- been taller and heavier. Midparental heights
gers and coordinates the changes that initi- (height of mother and height of father, di-
ate sexual maturation and eventually vided by 2) and weights were also less in the
menarche? Such data are now lacking. gymnasts than in the swimmers, and the
Hormonal data for prepubertal or puber- groups did not differ in socioeconomic sta-
tal girls involved in regular training are lim- tus.35
ited, and the results are variable and incon- Changes in basal levels of hormones in as-
clusive. Low gonadotropin secretion in sociation with training in young athletes
Growth, Performance, Activity, and Training during Adolescence 149

may be significant. Similar basal levels of occur.41 Accordingly, intensive, regular


ACTH, cortisol, prolactin, and testosterone training functions to reduce and maintain
have been reported during a 24-week train- fatness below the hypothesized minimal
ing season in small samples of premenar- level, thereby delaying menarche. The crit-
cheal and postmenarcheal competitive ical weight or fatness hypothesis has been
swimmers 13 to 18 years of age.38 During the discussed at length by many authors,21-42 and
season, ACTH levels gradually increased, the evidence does not support the specific-
prolactin levels tended to increase, and tes- ity of weight or fatness, or of a threshold
tosterone levels decreased, whereas corti- level, as the critical variable for menarche to
sol levels showed a variable pattern in the occur.
combined sample. As expected, basal estra-
diol levels differed between the premenar-
cheal and postmenarcheal swimmers, but Other Maturity Indicators
both groups experienced a decrease in basal Since indicators of sexual maturity are
levels during the first 12 weeks of training, reasonably well related to indicators of skel-
followed by a rise at 24 weeks. Basal levels etal and somatic maturity during adoles-
of estradiol at the start of training and after cence,1 it seems logical to consider the
24 weeks of training did not differ in the pre- effects of training on other maturity indica-
menarcheal swimmers, whereas the basal tors. If the hormonal responses to regular
level after 24 weeks was lower than at the training are viewed as important influences
start of training in the postmenarcheal on sexual maturation, one might expect
swimmers.38 them to influence the growth spurt, which
A role for B-endorphins in the amenor- occurs a year or so before menarche, and
rhea of runners and, in turn, in later menar- skeletal maturation around the time of men-
che in athletes has been postulated. Admin- arche. (For example, epiphyseal capping
istration of naloxone, an opiate receptor and fusion are influenced by gonadal hor-
antagonist, to amenorrheic athletes, for ex- mones, among others.)
ample, results in a marked increase in lu- Regular physical activity, including train-
teinizing hormone (LH).39 Responses of nor- ing for sport, has no apparent effect on other
mal prepubertal girls and boys to naloxone indices of biologic maturation used in
under basal conditions are different from growth studies. Age at PHV is not affected by
those of adults, however.40 Naloxone appar- training, while skeletal maturation is neither
ently does not have an effect on LH secretion accelerated nor delayed by regular training
in children. A study of the effects of nalox- for sport during childhood and adoles-
one during exercise conditions in children cence.1,2,26
might be enlightening, but ethical concerns
make collection of such data difficult.
Overtraining
Fatness and Menarche The issue of overtraining—that is, exces-
sive training without adequate time for re-
A corollary of the suggestion that training covery—must be considered, since a signif-
delays menarche is that changes in weight icant number of adolescent girls (and boys)
or body composition associated with inten- are involved in intensive training for sport.
sive training may function to delay menar- Overtraining can be short-term or chronic,
che; that is, training may delay maturation in and when it is chronic, it results in an array
young girls by keeping them lean. This idea of behavioral, emotional, and physiologic
is related to the critical weight or critical fat- symptoms.43 Data for adults indicate weight
ness hypothesis, which suggests that a cer- loss, decreased performance, and slow re-
tain level of weight (about 48 kg) or fatness covery after training. Reduction in both FFM
(about 17%) is necessary for menarche to and fat mass probably accompany weight
150 Developmental Phases

loss, and a reduction in efficiency and max- needed in which youngsters of both sexes
imal working capacity accompany the de- are followed from prepubescence through
crease in performance. Implications for puberty, in which several indicators of
growing girls should be obvious. The behav- growth and maturity are observed, and in
ioral, emotional, and physiologic complica- which both training and other factors known
tions of overtraining have the potential to to influence growth and maturation are
negatively influence growth and maturation. monitored.

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sults of a Dutch study. Int J Sports Med 4:202, athletes. Eur J Appl Physiol 52:385,1984.
1983. 36. Brisson GR, Dulac S, Peronnet F, et al: The
21. Malina RM: Darwinian fitness, physical fit- onset of menarche: A late event in pubertal
ness and physical activity. In Mascie-Taylor progression to be affected by physical train-
CGN, and Lasker GW (eds): Applications of ing. Can J Appl Sport Sci 7:61,1982.
Biological Anthropology to Human Affairs. 37. Wierman ME, and Crowley WR Jr: Neuroen-
Cambridge University Press, Cambridge, docrine control of the onset of puberty. In
1991, p 143. Falkner F, and Tanner JM (eds): Human
22. Patton RG: Growth and psychological factors. Growth, Vol 2. Plenum, New York, 1986, p 225.
In Mechanisms of Regulation of Growth, Re- 38. Carli G, Martelli G, Viti A, et al: The effect of
port of the 40th Ross Conference on Pediatric swimming training on hormone levels in
Research. Ross Laboratories, Columbus, OH, girls. J Sports Med Phys Fit 23:45,1983.
1962, p 58. 39. McArthur JW, Bullen BA, Beitins IZ, et al: Hy-
23. Tanner JM: Fetus into Man. Harvard Univer- pothalamic amenorrhea in runners of normal
sity Press, Cambridge, MA, 1989. body composition. Endocr Res Commun 7:13,
24. Ellison PT: Morbidity, mortality, and menar- 1980.
che. Hum Biol 53:635, 1982. 40. Fraioli F, Cappa M, Fabbri A, et al: Lack of en-
25. Leistol K: Social conditions and menarcheal dogenous opioid inhibitory tone on LH secre-
age: The importance of early years of life. Ann tion in early puberty. Clin Endocrinol 20:299,
Hum Biol 9:521, 1982. 1984.
26. Malina RM: Growth and maturation: Normal 41. Frisch RE: Fatness of girls from menarche to
variation and effect of training. In Gisolfi CV age 18 years, with a nomogram. Hum Biol
and Lamb DR (eds): Perspectives in Exercise 48:353, 1976.
Science and Sports Medicine, Vol 2. Youth, 42. Bronson FH, and Manning JM: The energetic
Exercise, and Sport. Benchmark Press, Indi- regulation of ovulation: a realistic role for
anapolis, IN, 1989, p 223. body fat. Biol Reprod 44:945, 1991.
27. Drinkwater BL, Nilson K, Chestnut CH, et al: 43. Kuipers H, and Keizer HA: Overtraining in
Bone mineral of amenorrheic and eumenor- elite athletes: Review and directions for the
rheic athletes. N Engçl J Med 311:277, 1984. future. Sports Med 6:79, 1988.
CHAPTER 9

Menstruation and
Menstrual Disorders
MONA M. SHANGOLD, M.D.

PREVALENCE OF MENSTRUAL Chronic Hormone Alterations with


DYSFUNCTION AMONG Training
ATHLETES
CONSEQUENCES OF MENSTRUAL
REVIEW OF MENSTRUAL
DYSFUNCTION
PHYSIOLOGY
Luteal Phase Deficiency
TYPES OF MENSTRUAL Anovulatory Oligomenorrhea
DYSFUNCTION Hypoestrogenic Amenorrhea
MENSTRUAL CYCLE CHANGES
DIAGNOSTIC EVALUATION OF
WITH EXERCISE AND TRAINING
MENSTRUAL DYSFUNCTION IN
Weight Loss and Thinness
ATHLETES
Physical and Emotional Stress
Dietary Factors
TREATMENT OF MENSTRUAL
HORMONAL CHANGES WITH DYSFUNCTION IN ATHLETES
EXERCISE AND TRAINING
Acute Hormone Alterations with EVALUATION AND TREATMENT
Exercise OF PRIMARY AMENORRHEA

I ncreased participation of women in sports has led to greater awareness of the


menstrual cycle alterations that frequently accompany exercise and training.
This raised consciousness has inspired more scientists to investigate the etio-
logic mechanisms responsible for such changes and has led many athletes to
seek medical attention. Unfortunately, many other athletes still avoid physician
consultation, usually because they fear they will be told to stop exercising. It is
the responsibility of all physicians and other health professionals to advise exer-
cising women about what is known regarding reproductive effects of exercise and
to assist them in formulating therapeutic plans.

PREVALENCE OF MENSTRUAL DYSFUNCTION


AMONG ATHLETES

Oligomenorrhea (infrequent menses) and amenorrhea (absent menses) are


more prevalent among athletes (10% to 20%)1,2 than among the general popula-
tion (5%) and are found more often in runners than in swimmers or cyclists3 (Fig.
152
Menstruation and Menstrual Disorders 153

or number of years of training.2, 4 Bachmann


and Kemmann5 have reported that the prev-
alences of oligomenorrhea and amenorrhea
among college students are 11% and 3%, re-
spectively. However, this population in-
cludes some athletes, for whom exercise
and training contribute to the problem. The
prevalence of menstrual dysfunction among
college students is higher than that among
the rest of the population because college
students tend to experience more emotional
stress than the general population and be-
Figure 9-1. The prevalence of amenorrhea in runners, cause many college students have not un-
swimmers, and cyclists, relative to training mileage.
(From Sanborn,3 with permission.) dergone full maturation of the hypotha-
lamic-pituitary-ovarian axis, making them
more susceptible to menstrual disorders. It
9-1), Among competitive athletes, the prev- is worth mentioning that the general popu-
alence of amenorrhea has been reported to lation has previously been considered to be
be as high as 50%.3 However, the prevalence sedentary, but the rising numbers of exer-
of menstrual dysfunction does not correlate cising women will undoubtedly increase the
with average weekly mileage, running pace, percentage of exercising women in the gen-

Figure 9-2. Percent menstrual change during training for women with regular menses before train-
ing, irregular menses before training, and amenorrhea before training. Of those women who had reg-
ular menses before training, 93% continued to have regular menses during training. (From Shangold,2
with permission.)
154 Developmental Phases

eral population and may raise the preva- result from variations in the length of the fol-
lence of menstrual dysfunction in this licular phase, or the time required for a fol-
group. licle to enlarge and mature enough to un-
Although it is tempting to presume that dergo ovulation.
exercise itself is responsible for the higher Throughout the menstrual cycle, the hy-
prevalence of amenorrhea associated with pothalamus secretes gonadotropin-releas-
it, many factors change simultaneously dur- ing hormone (GnRH), which is also re-
ing the course of an athletic training pro- ferred to as luteinizing hormone-releasing
gram, making it difficult to isolate causal fac- hormone (LH-RH) or luteinizing hormone-
tors. The fact that amenorrheic runners releasing factor (LRF). This decapeptide is
have a higher incidence of prior menstrual produced by cells in the arcuate nucleus of
irregularity1'2 suggests that exercise alone the hypothalamus; it promotes synthesis,
may not be responsible for menstrual dys- storage, releasability, and secretion of both
function in many cases (Fig. 9-2). pituitary gonadotropins: follicle-stimulat-
ing hormone (FSH) and luteinizing hor-
mone (LH). FSH promotes growth of the
ovarian follicle and synthesis of estrogen
REVIEW OF MENSTRUAL from androgen precursors. LH stimulates
PHYSIOLOGY ovarian androgen production, maintaining a
supply of androgens available for conver-
A brief review of menstrual physiology sion to estrogens.
follows, to facilitate the understanding of In a normal menstrual cycle, a woman pro-
readers from diverse backgrounds. It is nec- duces estrogen all the time and produces
essary to be familiar with the basic hor- significant progesterone only after ovula-
monal events of the menstrual cycle, in tion. Blood estrogen levels vary greatly
order to appreciate both the hormonal and throughout the cycle, being quite low during
menstrual alterations that accompany exer- the early follicular phase and quite high dur-
cise and training. For more comprehensive ing the late follicular phase. It is the high es-
reviews, the reader is referred to other pub- trogen level in the late follicular phase that
lications. 6-8 triggers ovulation. During the luteal phase,
A normal menstrual cycle (counting from levels of both estrogen and progesterone
the beginning of one period to the beginning are high.
of the next period) lasts from 23 to 35 days. Estrogen stimulates the endometrium
An ovarian follicle is the structure that con- (the inner lining of the uterus) to proliferate;
tains an egg; a corpus luteum is what devel- progesterone promotes maturation and sta-
ops from a follicle after the egg has been ex- bilization of an estrogen-stimulated endo-
pelled. The follicular phase is the portion of metrium. It is the decline in the concentra-
the ovarian cycle that extends from the first tions of estrogen and progesterone near the
day of menstruation until ovulation; this end of the menstrual cycle that results in
corresponds temporally with the prolifera- menstruation, which is the desquamation of
tive phase of the endometrial cycle. The lu- the endometrium (Fig. 9-3).
teal phase of the ovarian cycle extends from
ovulation until the onset of the next men-
strual period; this corresponds temporally
with the secretory phase of the endometrial TYPES OF MENSTRUAL
cycle. A normal luteal phase should ap- DYSFUNCTION
proach 14 days, while a normal follicular
phase may vary considerably in length. With any insult to a woman's reproductive
Thus, fluctuations in the length of the men- system, menstrual disturbance probably fol-
strual cycle of a woman who ovulates usually lows an orderly sequence of increasing
Menstruation and Menstrual Disorders 155

Figure 9-3. Hormonal events of the menstrual cycle, phases of the ovarian and endometrial cycles,
and endometrial height throughout the menstrual cycle.

severity: (1) luteal phase deficiency, (2) amenorrhea is likely to ensue. Many women
euestrogenic anovulation, and (3) hypo- do not seek attention when menstrual dys-
estrogenic amenorrhea. Thus, any condition function is mild or of recent onset and may
that disturbs the delicate balance of care- have hypoestrogenic amenorrhea by the
fully timed hormonal events needed for reg- time they first seek attention. Although pro-
ular ovulation and menstruation usually gression of this sequence has not been doc-
produces luteal phase deficiency first. If the umented in prospective studies, it is likely,
condition continues, euestrogenic anovula- nevertheless, and provides a useful model
tion will probably follow. If the condition for understanding menstrual dysfunction.
continues even longer, hypoestrogenic
156 Developmental Phases

MENSTRUAL CYCLE CHANGES Table 9-1. FACTORS TO WHICH AN


WITH EXERCISE AND TRAINING ATHLETE IS OFTEN SUBJECTED DURING
TRAINING
The data collected from the surveys re- 1. Weight loss
ported are derived from records of women 2. Low weight
who recorded only their menstrual patterns. 3. Low body fat
Most, but not all, women who bleed at reg- 4. Dietary alterations
5. Nutritional inadequacy
ular intervals have normal ovulatory and lu- 6. Physical stress
teal function. More accurate information 7. Emotional stress
about menstrual cyclicity can be derived 8. Acute hormone alterations
from basal body temperature records and 9. Chronic hormone alterations
hormonal measurements. By having 14 sub-
jects record their basal body temperatures
to indicate that and when ovulation had oc- have demonstrated that amenorrheic run-
curred, Prior and co-workers9 have shown in ners were thinner and had lost more weight
48 menstrual cycles that even among ath- after initiating regular running.
letic women with apparently regular men- Despite claims that women need a mini-
ses, approximately one third have anovula- mum amount of body fat in order to maintain
tion, one third have luteal phase deficiency, regular menstrual cyclicity, this hypothesis
and one third have normal luteal function. remains unproven and suspect. If such a
This suggests that menstrual disturbance minimum amount of fat must be exceeded,
among exercising women may be more per- the mechanism by which this functions also
vasive than has been appreciated. remains unproven. Adipose tissue produces
In addition to the epidemiologic studies and retains estrogen, but the amount of es-
that demonstrate a higher prevalence of oli- trogen contributed by adipose tissue is neg-
gomenorrhea/amenorrhea among athletes ligible compared with the very large quan-
than among sedentary women, several pro- tity produced by normal ovaries. Since
spective investigations have demonstrated muscle tissue contains aromatizing enzymes
changes in menstrual cyclicity in individual too, and since athletic women tend to have
women who trained. Each of these has stud- more muscle and less fat than sedentary
ied a number of factors that vary during women, aromatizing capability should be
training, any of which may contribute to comparable in both groups. Thus, the mech-
menstrual cycle alteration. It is usually very anism by which thinness promotes men-
difficult to separate the many contributory strual dysfunction remains to be shown.
variables that change simultaneously during Following the original suggestion by
training, including body composition, phys- Frisch and McArthur10 that thinness caused
ical and emotional stress, diet, and certain amenorrhea, many investigators have
hormone levels (Table 9-1). probed the relationships between thinness
and hormone production and metabolism.
Previously it was shown that thin women
Weight Loss and Thinness
metabolize most of their estradiol by 2-hy-
Many women lose both weight and body droxylation, while obese women excrete
fat when they begin to exercise regularly. most estradiol after 16-hydroxylation.11 Re-
Some attain and maintain very low levels of cently, Snow and her associates12 have
weight and fat. Simple weight loss and thin- shown that elite oarswomen who develop
ness may lead to amenorrhea, even in the menstrual dysfunction during training me-
absence of exercise. Shangold and Levine2 tabolize a greater fraction of administered
have reported that amenorrheic runners are [2-3H]estradiol by 2-hydroxylation than do
lighter than eumenorrheic (regularly men- sedentary controls or elite oarswomen who
struating) runners. Schwartz and associates1 remain eumenorrheic during training. How
Menstruation and Menstrual Disorders 157

the resultant catecholestrogens affect men- percentage of the total caloric intake of
strual function remains to be shown. amenorrheic runners compared with that of
eumenorrheic runners and eumenorrheic
nonrunners. These amenorrheic runners
Physical and Emotional Stress consumed more total calories than the other
Schwartz and colleagues1 have shown that groups, however, so that equal quantities of
amenorrheic runners associate more stress protein were consumed by all three groups.
with their exercise than do eumenorrheic Calabrese and colleagues14 have demon-
runners. This supports the concept that the strated that professional and student ballet
physical and emotional stress of both train- dancers consume fewer calories (1358 calo-
ing and competition may be substantially ries) than the recommended dietary allow-
greater than appreciated. Although regular ance (RDA) (2030 calories) established by
exercise tends to relieve stress and anxiety, the National Research Council,15 a figure in-
this action may be outweighed in busy tended for an "average" woman, weighing
women who are determined to incorporate 58 kg and exercising very little or not at all.
a specific quantity of exercise into their Although the mean daily protein intake by
daily schedules. these dancers (47.4 g) fell slightly below the
Warren13 has demonstrated the complex- RDA for "average-sized women" (50 g), this
ity and interrelationship of the factors con- protein intake was adequate when based on
tributing to the development of menstrual the RDA of 0.8 g/kg15 and the subjects' mean
dysfunction in two ballet dancers (Fig. 9-4). weight of 53.1 kg. Frisch and associates16
The dancer in the upper graph experienced have reported that a group of collegiate
no change in weight or body composition women who began athletic training prior to
throughout the year in which she had three menarche consumed less fat (65 g) and pro-
menstrual periods, each during an interval tein (71 g) than a group who began training
of inactivity. The dancer in the lower graph after menarche (95 g of fat and 92 g of pro-
developed regular menses when she gained tein), and that the former group also had
both weight and body fat, although she higher incidences of oligomenorrhea and
maintained her customary level of activity. amenorrhea. Very low levels of fat intake are
She continued menstruating regularly, de- difficult to attain, and such diets have been
spite a loss of both weight and body fat that associated with insidious negative calcium
occurred during an inactive vacation inter- balance.17 Deficiencies of the fat-soluble vi-
val. With no further loss of weight, she tamins, which require fat for absorption,
ceased menstruating altogether when she have never been reported in people con-
resumed her customary level of activity. It is suming low-fat diets, but such deficiencies
likely that stress levels are higher during in- remain a theoretical hazard. Deuster and
tervals of intensive dancing, compared with her co-workers18 have described differences
vacation intervals. Thus, activity, fat, between the dietary intakes of eumenor-
weight, and stress must be considered vari- rheic and amenorrheic runners, and they
ables in the changes observed. have reported that many amenorrheic run-
ners consume less than the recommended
Dietary Factors dietary allowances of some nutrients. Pirke
and associates19 have described menstrual
Many women who begin to exercise regu- dysfunction that developed in association
larly alter their dietary patterns because with caloric restriction, especially in asso-
they become more concerned about health- ciation with a vegetarian diet. These inves-
ful living. Those who have been exercising tigators have demonstrated impairment of
regularly for a long time often eat differently episodic LH secretion during dieting.20
from nonathletes. Schwartz and co-workers1 Despite the suggestion that amenorrheic
reported that protein constituted a smaller runners may consume inadequate choles-
158 Developmental Phases

Figure 9-4. Relationships among menses, exercise, weights, and calculated body fat values in two
young ballet dancers. (From Warren,13 with permission.)

terol to produce sufficient estrogen, there progesterone during a normal luteal phase,
remains no evidence that dietary choles- but the rest of the body can provide enough
terol is necessary for hormone synthesis. cholesterol to serve as precursor for ade-
The corpus luteum cannot make enough quate luteal progesterone production.
cholesterol de novo to synthesize adequate Although there is little to prove that estro-
Menstruation and Menstrual Disorders 159

gen production is affected by these dietary tradiol,24 progesterone,24 and testosterone23


differences, there is evidence that estrogen rise during exercise and return to normal
metabolism is altered. Longcope and co- within an hour or two after cessation of ex-
workers21 have shown that the ingestion of a ercise. Exercise-associated increments in
low-fat diet promotes the same pattern of es- ACTH, opioid peptides, melatonin, and cor-
trogen metabolism observed in thin women: tisol are facilitated by training.25,26 Since
increased production of catecholestrogens testosterone27 and cortisol28 increase also in
(the result of 2-hydroxylation) and reduced anticipation of exercise, it is probable that
production of estriol (the result of 16-hy- psychologic factors contribute to the re-
droxylation). ported changes as well. Rebar and co-
Myerson and her associates22 have shown workers29 have shown that dexamethasone
that the resting metabolic rate (RMR) of suppression abolishes all effects of exercise
amenorrheic runners is significantly less on adrenal and gonadal hormones, includ-
than that of eumenorrheic runners, which is ing those in anticipation of exercise. De-
significantly less than that of eumenorrheic tailed review of the many studies of hor-
sedentary controls. The RMR of the amen- monal changes during exercise sessions,
orrheic runners remained lower than that of ranging in duration from a few minutes to
each of the other two groups after adjust- the time required to complete a marathon, is
ment for body weight or for fat-free mass. Al- beyond the scope of this chapter. For a more
though the absolute caloric intake of the comprehensive review, readers are referred
amenorrheic runners was less than that of elsewhere.30-32
the eumenorrheic runners and was similar
to that of the sedentary controls, the differ-
Factors Influencing Hormone Levels
ences were not significant, probably due to
large intragroup variability and small sam- Plasma hormone levels represent a bal-
ple size. The amenorrheic runners also had ance among production, metabolism, utili-
higher scores on the eating attitudes test zation, clearance, and plasma volume, all of
(EAT-26, modified), including two subscales which may change simultaneously during
and total score; this reflected a higher level exercise. Levels of many hormones also are
of aberrant dietary patterns in the amenor- affected by episodic secretion, diurnal vari-
rheic group. Thus, a growing body of infor- ation, state of sleep or wakefulness, state of
mation has brought our attention to the role feeding or fasting, dietary composition and
of dietary intake as a contributing cause of caloric adequacy, temperature, body weight
menstrual dysfunction among athletes. and composition, emotional factors, and
body position. The hormonal response to
exercise in any person is often influenced by
HORMONAL CHANGES WITH the person's fitness, which affects the rela-
EXERCISE AND TRAINING tive workload of any given activity and, in
some cases, alters hormonal responsive-
Acute Hormone Alterations ness during exercise. Difficulty in control-
with Exercise ling these many variables during any spe-
cific investigation makes it even harder to
Blood levels of several protein and steroid interpret the observed exercise-induced
hormones increase transiently during con- changes in hormone levels.
tinuous, aerobic exercise. The long-term ef-
fects of such repetitive, but brief, alterations
remains unknown. Reported exercise-in- Chronic Hormone Alterations
duced changes in gonadotropin levels are with Training
inconsistent and have been confused by the Shangold and associates33 have observed
pulsatile nature of gonadotropin release. one runner during 18 menstrual cycles in
Circulating concentrations of prolactin,23 es- which she varied her weekly mileage. This
160 Developmental Phases

woman had shortening of the luteal phase


and lower progesterone levels in cycles of
greater mileage (Figs. 9-5 and 9-6). Prior
and colleagues34 have also reported luteal
phase deficiency in two runners during sev-
eral menstrual cycles of varying mileage.
One of these two runners had a normal preg-
nancy when she stopped running, suggest-
ing that exercise-induced luteal phase defi-
ciency is a reversible phenomenon.
Similarly, Frisch and associates35 ob-
served a long-distance swimmer prior to,
during, and after intensive training, with
monitoring of basal body temperature rec- Figure 9-6. Midluteal phase plasma progesterone con-
ords, as well as blood and urine hormone centrations obtained 3 to 7 days after change in cervical
mucus (presumptive evidence of ovulation), comparing
measurements. She developed a luteal seven samples from three control cycles and seven
phase defect, followed by an anovulatory samples from three training cycles. Bars indicate
cycle, during intensive training. Three means plus or minus standard errors (p < 0.001).
(From Shangold,33 reproduced with permission of The
months after completion of a long-distance American Fertility Society.)
swim (the English Channel), she regained a
normal, biphasic basal body temperature
pattern. This confirms that the menstrual alence of menstrual dysfunction was high in
cycle alterations associated with intensive both groups during intensive training, but
training occur in swimming as well as in run- was much higher in the weight-loss group;
ning. 94% of them experienced menstrual distur-
Menstrual and hormonal changes in two bances, compared with 75% of the weight-
groups of untrained women have been stud- maintenance group. Of those who lost
ied prospectively.36 One group lost weight weight, 63% experienced abnormal luteal
during a running program of increasing function, as did 66% of the weight-mainte-
mileage, and the other group maintained nance group. All subjects regained normal
weight during the same program. The prev- menstrual cyclicity within 6 months of ter-
mination of the study (and presumably of
training). As has been shown by Warren,13
weight loss and exercise act synergistically
in promoting menstrual dysfunction. How-
ever, these data36 suggest that a compensa-
tory increase in caloric intake cannot
prevent exercise-induced menstrual dys-
function in most cases.
In the same investigation of training-in-
duced menstrual dysfunction,37 two types of
luteal dysfunction were described: a short
luteal phase and an inadequate luteal phase.
The short luteal phase was marked by de-
Figure 9-5. Relationship between mileage run during creased luteal phase length, while the inad-
the first 6 days of the follicular phase and the length of
the luteal phase, defined as the interval between the equate luteal phase was characterized by in-
day of change in cervical mucus and onset of the next sufficient progesterone secretion, measured
menses, in 18 cycles, (y = 13.3 - 0.1 Ix; r = -0.81; p by the concentration in overnight urine
< 0.001). Point (1,13) represents three values. (From
Shangold,33 reproduced with permission of The Ameri- collections. The significance of these
can Fertility Society.) differences remains to be shown, but these
Menstruation and Menstrual Disorders 161

investigators have shown that menstrual serum cortisol to bolus administration of


dysfunction can be induced in normal human corticotropin-releasing hormone
women with intense training. It remains to (CRH), and to meals, among both eumenor-
be shown, however, whether a critical level rheic and amenorrheic athletes compared
of exertion must be exceeded, and why some to eumenorrheic sedentary controls. These
women are predisposed to this type of dys- data suggest that the hypothalamic-pitu-
function in response to training. If a critical itary-adrenal axes of athletic women are
level exists, the level undoubtedly differs characterized by increased CRH stimula-
among various women. tion, increased cortisol negative feedback,
Russell and associates38,39 found similar normal ACTH secretion, normal cortico-
weights and body fat levels among athletic troph responsiveness to cortisol-induced
and inactive women, but found a correlation negative feedback, and decreased respon-
among strenuous exercise, anovulatory oli- siveness to ACTH. In an excellent review,
gomenorrhea, and elevated levels of /3-en- DeSouza and Metzger44 have suggested that
dorphins and catechol estrogens. Although the adrenal response may be blunted be-
endogenous opiates are known to modulate cause the adrenal is functioning near capac-
pulsatile luteinizing hormone release in hu- ity at rest, unable to mount a greater re-
mans,40 it is unlikely that circulating levels of sponse to stimulation.
these peptides correspond to the brain lev- Boyden and associates45 have provided an
els influencing hypothalamic secretion. important clue toward understanding the al-
The fact that a generalized increase in terations in menstrual function associated
"stress" hormones occurs with exercise and with intensive exercise. They have shown
endurance training has been confirmed by that GnRH-stimulated LH levels in eumenor-
Villanueva and colleagues,41 who demon- rheic women decrease with endurance
strated increased cortisol production in training (distance running).
both eumenorrheic and amenorrheic run- Gumming and co-workers46 further en-
ners. Although the amenorrheic runners hanced our understanding of these changes
had higher levels of both serum cortisol and when they reported that eumenorrheic run-
urinary cortisol, the differences between ners (at rest) have lower LH pulse fre-
these two groups of runners were not statis- quency, LH pulse amplitude, and area under
tically significant. the LH curve over 6 hours, compared with
Loucks and her associates42 have demon- eumenorrheic sedentary women (Figs. 9-7
strated that both eumenorrheic and amen- and 9-8). These investigators47 then found
orrheic athletes have higher morning serum that acute exercise reduces LH pulse fre-
cortisol levels than do eumenorrheic sed- quency but does not change pulse amplitude
entary women, and that the serum cortisol or area under the 6-hour curve. These im-
levels in the amenorrheic athletes remained portant findings suggest that acute exercise
higher throughout the day compared to has an inhibitory effect on LH pulsatile re-
those in the eumenorrheic sedentary lease at the hypothalamic level in eumenor-
women. However, these three groups did rheic runners, perhaps contributing to the
not differ in plasma ACTH pulse frequency, observed alterations with training.
pulse amplitude, or mean level during any Several recent studies have provided
time interval, and also did not differ in even more information about LH pulsatile
serum cortisol pulse frequency. The eume- patterns in athletes. Veldhuis and co-
norrheic athletes had reduced serum corti- workers48 demonstrated reduced LH pulse
sol pulse amplitude during the day. Other frequency and normal LH pulse am-
investigators have also described mild hy- plitude in amenorrheic or severely oligo-
percortisolism in amenorrheic runners.43 menorrheic runners compared to eu-
Loucks and co-workers42 have also shown a menorrheic sedentary controls. These
blunted response of plasma ACTH and investigators also reported normal or accen-
162 Developmental Phases

in the amenorrheic athletes, compared to


the eumenorrheic sedentary controls.
These data suggest that exercise-induced
menstrual dysfunction results from inhibi-
tion of hypothalamic release of GnRH at the
level of the hypothalamus or higher brain
centers influencing hypothalamic function.

CONSEQUENCES OF
MENSTRUAL DYSFUNCTION

Luteal Phase Deficiency


The major adverse condition associated
with luteal phase deficiency is infertility,
and this association remains controversial.
Preliminary findings suggesting that proges-
terone deficiency may be linked to an in-
creased breast cancer risk49 have not been
confirmed. Prior and her associates50 have
recently demonstrated that shortening the
luteal phase correlates with loss of bone
density.

Anovulatory Oligomenorrhea
Chronic anovulation is associated with
chronic, unopposed estrogen production,
which leads to continuous endometrial
Figure 9-7. Serum LH levels in samples obtained at 15- stimulation and, as a consequence, an in-
minute intervals over 6 hours in six eumenorrheic run- creased risk of endometrial hyperplasia and
ners (upper) and four sedentary controls (lower). The
studies were performed in the early follicular phase of adenocarcinoma. Although this association
the menstrual cycle (days 3 to 6). (From Cumming,46 has been documented in women with poly-
with permission.) cystic ovary syndrome, 51-54 it has never
been reported in athletes. It remains un-
known whether anovulatory athletes carry
tuated LH release and normal estradiol re- the same, increased risk of developing en-
lease in response to exogenous GnRH dometrial hyperplasia and adenocarcinoma
pulses. as nonathletes with chronic anovulation.
Loucks and co-workers42 have shown re- Perhaps inadequate reporting or history-
duced LH pulse frequency and increased LH taking, or both, has led to the absence of
pulse amplitude in eumenorrheic athletes such reports (i.e., gynecologists may not
compared to eumenorrheic sedentary con- routinely elicit athletic histories, particu-
trols; both the LH pulse frequency and am- larly when diagnosing cancer), or perhaps
plitude of the amenorrheic athletes were anovulatory athletic women do not maintain
lower than those of the eumenorrheic ath- high enough estrogen levels long enough to
letes. An exogenous GnRH bolus caused induce hyperplasia or cancer. Until this
blunted FSH release in the eumenorrheic question is answered, it seems reasonable to
athletes and augmented FSH and LH release assume that the endometrium of the athlete
Menstruation and Menstrual Disorders 163

Figure 9-8. LH pulse frequency,


pulse amplitude, and the area
under the LH curve in eumenor-
rheic runners and sedentary con-
trols in the early follicular phase
of the menstrual cycle. (*p <
0.05, **p < 0.01 on Mann-Whitney
U test.) (From Cumming, 46 with
permission.)

responds the same as that of the nonathlete production may be iron-deficient or anemic.
to estrogen stimulation. Thus, an increased Either of these conditions can impair ath-
risk of endometrial hyperplasia and adeno- letic performance, as can heavy bleeding
carcinoma should be presumed until it is during training or competition. The preva-
disproved. lence of heavy bleeding among athletes re-
Recent studies have suggested that an- mains to be shown. As suggested earlier, it
ovulatory women may also be at increased is possible that anovulatory athletic women
risk of developing breast cancer.55 This pre- do not maintain high enough estrogen levels
liminary report requires further confirma- long enough to induce sufficient thickening
tion. This suggestion, too, has not described of the endometrial lining and consequent
the athletic habits of subjects. Thus, if profuse bleeding. However, heavy, infre-
chronic anovulation leads to an increased quent bleeding episodes are common
risk of breast carcinoma, it remains to be among adolescents, even those who are ath-
shown whether this increased risk includes letes; it is probable that more mature ath-
anovulatory athletes. letes are subject to the same risk.
Although Frisch and associates56 have re-
ported a lower prevalence of breast cancer
among former college athletes compared Hypoestrogenic Amenorrhea
with former college nonathletes, this report Estrogen promotes beneficial effects on
did not relate breast cancer prevalence to calcium metabolism, lipid metabolism, and
recent athletic participation. Thus, it re- urogenital epithelial maturation. Hypoestro-
mains to be demonstrated whether regular genic women lack these favorable effects.
exercise has any effect on breast cancer risk. Many reports have demonstrated that ath-
Prior and her colleagues50 have shown that letes with hypoestrogenic amenorrhea have
anovulatory cycles are also associated with reduced bone density and increased risk of
loss of bone density. musculoskeletal injury, compared with eu-
Chronic anovulation usually leads to in- menorrheic athletes.57-63
frequent, heavy bleeding at unpredictable Cann and co-workers57 were the first to
times. At best, this is an inconvenience, par- bring this finding to our attention. They re-
ticularly to competitive athletes, and at ported that women with hypothalamic
worst, it may require hospitalization to con- amenorrhea, in many cases associated with
trol blood loss. Between these extremes, exercise, had lower vertebral bone density
women with chronic, unopposed estrogen than several other groups of eumenorrheic
164 Developmental Phases

and amenorrheic women, including those entary women. This suggested that exercise
with hyperprolactinemia and premature is beneficial in increasing bone density, but
ovarian failure. This surprising, incidental not as beneficial as a normal estrogen level.
finding led several other investigators to the Unfortunately, differences in calcium intake
same issue. It had been shown by others that between some of these groups introduced
exercise has a beneficial effect on bone den- another variable, as occurred in the Drink-
sity, as discussed in Chapter 5. In view of the water study.59 It remains difficult to separate
higher prevalence of hypoestrogenic amen- estrogen, exercise, and calcium intake as
orrhea among athletes, it became important variables in pinpointing causality in such
to resolve whether exercise is beneficial studies.
enough to compensate for an estrogen defi- It was demonstrated by Jones and
ciency. associates61 that radial bone density re-
Rigotti and colleagues58 reported that gresses in a linear fashion with increasing
amenorrheic women with anorexia nervosa duration of amenorrhea, regardless of etiol-
had lower radial bone density than eume- ogy, confirming that hypoestrogenic young
norrheic controls and that those anorectics women lose bone density in the same pat-
who reported a high physical activity level tern as that observed for postmenopausal
had a greater bone density than those who women.65
were less active. This suggested that physi- Warren and co-workers62 have reported
cal activity offers some protection against that ballet dancers have a higher prevalence
bone loss induced by estrogen deficiency. of scoliosis and a greater incidence of frac-
In a study by Drinkwater and co-work- tures with increasing menarcheal age. They
ers,59 lower vertebral bone density was also found a higher incidence and longer du-
found in amenorrheic athletes than in eu- ration of secondary amenorrhea among
menorrheic athletes. However, these groups dancers with stress fractures. These find-
differed not only in their estrogen status but ings suggest that menarcheal delay and pro-
also in their calcium intake. Although the longed intervals of hypoestrogenic amen-
absolute values of calcium ingested by orrhea may predispose ballerinas to
the groups were not significantly different, scoliosis and stress fractures.
the amenorrheic group, but not the eume- The suggestion of increased susceptibility
norrheic group, consumed much less cal- to musculoskeletal injuries among amenor-
cium than the amount recommended for rheic athletes has been supported by the
hypoestrogenic women. Since estrogen en- work of Lloyd and colleagues.63 These au-
hances calcium absorption, hypoestrogenic thors reported that women who were in-
women require an additional 500 mg of cal- jured during their running program were
cium daily, compared with that required by more likely to have had absent or irregular
euestrogenic women. (It is recommended menses, were less likely to have used oral
that euestrogenic women consume 1000 mg contraceptives, and had been running for
of calcium daily and that hypoestrogenic more years than those running women who
women consume 1500 mg daily.64) Thus, it is were not injured.
unclear whether the lower bone density of The increased risk of cardiovascular dis-
these amenorrheic athletes was caused by ease that occurs after menopause results
estrogen deficiency, calcium deficiency, or mostly from adverse changes in lipids, in-
both. duced by estrogen deficiency. Most of the
Marcus and colleagues60 also reported adverse effects of the hypoestrogenic state
that eumenorrheic runners had greater ver- on low-density lipoprotein cholesterol con-
tebral bone density than eumenorrheic sed- centrations tend to be offset by endurance
entary women, who had greater bone den- training. In addition, most athletes have a
sity than amenorrheic runners, who had reduced risk of cardiovascular disease, com-
greater bone density than amenorrheic sed- pared with the general population. On the
Menstruation and Menstrual Disorders 165

other hand, exercise-induced hypoestro- population. However, because these tests


genic amenorrhea can reverse the beneficial have not proved cost-effective for patients
effects of strenuous exercise on plasma apo- in my practice who have only menstrual dys-
lipoprotein concentrations.66 function, I no longer perform these tests
Because estrogen leads to maturation of routinely.
the urogenital epithelium, a deficiency Menstrual disturbances may be caused by
causes thinning of the vaginal epithelium hyperprolactinemia, hypothyroidism, ovar-
and increased susceptibility to atrophic ure- ian failure, hyperandrogenism, and preg-
thritis and vaginitis. These uncomfortable nancy. To detect these conditions, it is nec-
conditions are most common after meno- essary to measure the following: serum
pause, probably because development of prolactin, thyrotropin (TSH), free thyrox-
urogenital atrophy requires several years ine, follicle-stimulating hormone (FSH), lu-
in the hypoestrogenic state. Since few ath- teinizing hormone (LH), dehydroepian-
letes remain severely hypoestrogenic long drosterone sulfate (DHEAS), testosterone,
enough to develop atrophic vaginitis, this and B-human chorionic gonadotropin (B-
condition is relatively uncommon among HCG). I also measure serum estradiol, in
athletes and can usually be treated easily order to determine whether the patient is
when it occurs. hypoestrogenic. Hyperprolactinemia may
result from a pituitary adenoma or micro-
adenoma; it requires further evaluation and
DIAGNOSTIC EVALUATION OF specific treatment. If both FSH and LH are
MENSTRUAL DYSFUNCTION IN very low, the sella turcica should be as-
ATHLETES sessed (probably by a lateral cone-down
film), to detect a large hypothalamic or pi-
I believe that all oligomenorrheic and tuitary lesion. An elevated TSH level or a low
amenorrheic athletes deserve the following: free-thyroxine level indicates hypothyroid-
(1) a thorough history, including detailed ism, which also requires further evaluation
dietary intake; (2) a physical examination, and specific treatment. Hyperandrogenism
including a pelvic examination; and (3) may result from any of several etiologies,
some blood tests (Table 9-2). The dietary including polycystic ovarian syndrome, ad-
record should be reviewed by a trained nu- renal hyperplasia, an ovarian tumor, an
tritionist. Although most athletes with men- adrenal tumor, or drug abuse; hyperandro-
strual disturbances will be found to have no genism requires further evaluation and
serious conditions, it is impossible to deter- treatment. Although many women with hy-
mine, without this assessment, whether the perandrogenism will also have peripheral
menstrual dysfunction is related to exercise signs of androgen excess, not all women do.
or to some serious pathologic condition. A Some hyperandrogenic women develop
complete blood count, measurement of elec- menstrual dysfunction before acne, hirsut-
trolytes and liver enzymes, and urinalysis ism, or other symptoms of androgen excess.
are useful screening tests for the general Therefore, I believe it is worthwhile to mea-
sure DHEAS and testosterone in all women
with menstrual dysfunction, regardless of
Table 9-2. INITIAL DIAGNOSTIC whether other symptoms are present. Preg-
EVALUATION OF OLIGOMENORRHEA OR nancy, of course, requires further care.
AMENORRHEA Ovarian failure requires at least counseling
1. History, including dietary intake and possibly also further evaluation and
2. Physical examination, including pelvic examination treatment. In a patient younger than age 30,
3. Prolactin, free thyroxine, TSH, FSH, LH, DHEAS, ovarian failure warrants a blood karyotype
testosterone, B-HCG, estradiol to detect the presence of a Y chromosome,
4. Progestin challenge test
which confers an increased risk of gonadal
166 Developmental Phases

malignancy. In a patient older than age 30, tion to protect the endometrium adequately.
no further evaluation is required. At the time This can be effected by one of the following
of the initial evaluation, and after blood has regimens: (1) medroxyprogesterone acetate
been drawn for the above determinations, 5 to 10 mg daily for 10 to 14 consecutive days
the patient may be given a prescription for a of every month; (2) oral contraceptive pills,
5- or 10-day course of medroxyprogesterone each containing 30 to 35 mg of ethinyl estra-
acetate, to assess whether her endometrium diol and 0.15 to 1.0 mg of progestin; or (3)
has been stimulated by endogenous estro- clomiphene citrate to induce ovulation
gen. If she has no withdrawal bleeding, her (Table 9-3). Ovulation induction should be
endometrium had not been stimulated and reserved for those women desiring preg-
the rest of her body probably also lacks suf- nancy at the time of evaluation. The first two
ficient estrogen. Direct measurement of choices are acceptable for women who do
serum estradiol gives more accurate infor- not seek pregnancy now, regardless of
mation, however, and is more useful in plan- whether they are sexually active. Although
ning treatment. oral contraceptive pills obviously provide
After evaluating an athlete with oligomen- contraception, medroxyprogesterone ace-
orrhea or amenorrhea in this manner, and tate does not, and this regimen requires in-
upon finding that all of these tests except the dividuals to use barrier contraceptive meth-
estradiol concentration are within normal ods if they are sexually active.
limits, the athlete can be reassured that se- Hypoestrogenic amenorrheic women re-
rious causes of menstrual dysfunction have quire hormone replacement, primarily for
been ruled out. She should be counseled skeletal protection, but also for urogenital
about potential risks that may result from protection. Such athletes should be treated
the condition. Her serum estradiol concen- with one of the following treatment proto-
tration may be helpful in planning treat- cols: (1) conjugated estrogens 0.625 to 0.9
ment. mg daily and medroxyprogesterone acetate
5 to 10 mg daily on days 1 to 12 of every cal-
endar month; (2) transdermal estradiol 0.05
TREATMENT OF MENSTRUAL to 0.10 mg daily and medroxyprogesterone
DYSFUNCTION IN ATHLETES acetate 5 to 10 mg daily on days 1 to 12 of
every calendar month; (3) oral contracep-
Even if no serious causative pathology is tive pills, each containing 30 to 35 g of ethi-
detected during the hormonal evaluation for nyl estradiol and 0.15 to 1.0 mg of progestin;
menstrual dysfunction, treatment usually is or (4) clomiphene citrate or human meno-
indicated to prevent serious resultant pa- pausal gonadotropins to induce ovulation
thology. (Table 9-4). Ovulation induction should be
The association between luteal phase de- reserved for women desiring pregnancy at
ficiency and infertility is generally accepted, the time of evaluation.
but the links between luteal phase inade- Oral contraceptive pills may be recom-
quacy and breast cancer and bone loss seem mended to any hypoestrogenic amenor-
preliminary at the present time. Until con- rheic athlete who does not desire pregnancy
firming studies for the latter two conditions
are available, treatment for only infertility is
recommended. Thus, at the present time, lu- Table 9-3. TREATMENT OF
teal phase deficiency requires no treatment EUESTROGENIC OLIGOMENORRHEA
unless and until pregnancy is desired. 1. If not sexually active or using barrier contraception:
As discussed, euestrogenic anovulatory monthly progestin therapy
women are at increased risk of developing 2. If contraception needed or preferred: oral
endometrial hyperplasia and should be contraceptives
3. If fertility desired: clomiphene citrate
treated with monthly progestin administra-
Menstruation and Menstrual Disorders 167

Table 9-4. TREATMENT OF Table 9-5. ABSOLUTE


HYPOESTROGENIC AMENORRHEA CONTRAINDICATIONS TO ESTROGEN
THERAPY
1. If fertility desired: clomiphene citrate
2. If contraception needed or preferred: oral 1. Abnormal liver function
contraceptives 2. History of thromboembolic or vascular disease
3. If contraception and fertility not of concern: cyclic 3. Breast or endometrial carcinoma
estrogen and progestin therapy 4. Undiagnosed vaginal bleeding
4. If diet inadequate: correct deficiencies
5. If very thin: weight gain?
6. If exercising very heavily: less exercise?
fluctuations in their observed responses,
and many experience psychologic benefit
from the regularity and predictability of oral
at the time of evaluation, regardless of
contraceptive therapy.
whether she is sexually active; no additional
The major advantages of taking either
contraceptive method is needed by athletes
progestin alone or estrogen and progestin as
selecting this form of hormone replacement
separate pills are the ingestion of more
therapy. Those who select the more physi-
physiologic doses of medication and the
ologic regimen of conjugated estrogens or
likelihood of having predictable bleeding.
transdermal estradiol and medroxyproges-
Although the risks of exogenous hormone
terone acetate, separately, should be ad-
administration are much less than the risks
vised to use mechanical methods of contra-
of hormone deficiency, in my view, certain
ception if they are sexually active. The major
women should probably avoid estrogen and
advantages of taking oral contraceptive
others should definitely avoid it. Absolute
agents are convenience and contraception;
contraindications to estrogen therapy are
the major disadvantages are their two most
listed in Table 9-5; relative contraindica-
common side effects: breakthrough bleed-
tions are listed in Table 9-6.
ing (bleeding on the days of pill ingestion)
Many athletes have an aversion to exoge-
and amenorrhea (lack of withdrawal bleed-
nous hormone ingestion and do not compre-
ing at the end of the hormone-containing
hend the difference between physiologic re-
pills in each package). These side effects are
placement and pharmacologic therapy. It
inconvenient but not serious; both can be al-
requires careful and concerned counseling
leviated by hormone manipulation. The low-
to convince many of these women that hor-
dose oral contraceptive pills recommended
mone replacement therapy is advisable.
are associated with much lesser side effects
If the dietary intake record reveals caloric
and complications than the higher doses
or other nutritional inadequacy, the athlete
prescribed commonly more than a decade
should be evaluated and counseled by a nu-
ago; the low-dose preparations are also as-
tritionist and possibly a psychologist or psy-
sociated with a reduction in many disease
chiatrist, if an eating disorder is suspected
risks, compared with the risk to the general
population.
Another advantage of oral contraceptives Table 9-6. RELATIVE
for athletes with menstrual dysfunction is CONTRAINDICATIONS TO ESTROGEN
predictable bleeding and continued endo- THERAPY
metrial and skeletal protection. Many ath-
1. Hypertension
letes may produce enough endogenous 2. Diabetes mellitus
estrogen to have withdrawal bleeding fol- 3. Fibrocystic disease of the breast
lowing progestin administration for several 4. Uterine leiomyomata
months and then produce too little estrogen 5. Familial hyperlipidemia
to do so during the next few months. It is dis- 6. Migraine headaches
7. Gallbladder disease
turbing to many athletes to experience such
168 Developmental Phases

(see Chapter 17). Many athletes will be will- Table 9-7. RECOMMENDATIONS FOR
ing to increase their food intake when they FOLLOW-UP OF ATHLETES WITH
understand that dietary inadequacy may be OLIGOMENORRHEA OR AMENORRHEA
contributing to the problem. Those who are 1. Annual history and physical examination
unwilling to change their diets should be re- 2. Annual prolactin, TSH, free thyroxine, FSH, LH,
ferred for such counseling by a specialist. DHEAS, testosterone, B-HCG, estradiol
Although some of them may prefer to gain 3. Annual progestin challenge test
4. Hormone replacement therapy
weight or to reduce training intensity or
quantity, to see if menses return without
hormone therapy, it is not recommended
that these measures postpone for longer ate on the day of an important competitive
than 6 months the initiation of hormone re- event and neverwantingto menstruate at all.
placement. A shorter trial is reasonable, It is likely that most would prefer to have
particularly if the athlete herself makes this normal reproductive function, rather than
suggestion. I believe that the benefits of reg- amenorrhea, even if many are unwilling to
ular exercise far outweigh these potential re- admit this to themselves.
productive hazards, which can and should
be evaluated and treated if they develop.
Despite the demonstration by several in- EVALUATION AND
vestigators that exercise-associated men- TREATMENT OF PRIMARY
strual dysfunction is often a reversible phe- AMENORRHEA
nomenon, there is no evidence that it is
reversible in all cases, nor is there any Primary amenorrhea refers to the condi-
method of predicting when normal function tion in which menstruation has never oc-
will return, if ever. It seems unlikely that curred. Secondary amenorrhea, to which we
chronic, unopposed estrogen stimulation of have referred until now, refers to the con-
the uterus will cause hyperplasia or adeno- dition in which menstruation had occurred
carcinoma in an athlete in less than one in the past but subsequently has ceased. Be-
year. However, endometrial hyperplasia can cause menarche is often delayed in athletic
develop within 6 months in postmenopausal girls, as discussed thoroughly in Chapters 7
women being treated with unopposed estro- and 8, it is tempting to assume that menar-
gen.67,68 This raises my concerns about cheal delay is related to exercise. However,
permitting any women with euestrogenic, this assumption is as dangerous as that for
anovulatory oligomenorrhea to remain un- secondary amenorrhea. Serious pathologic
treated. Similarly, bone loss takes place at conditions can easily be missed if they are
an accelerated rate as soon as a woman be- not sought.
comes hypoestrogenic, and a significant Any girl who has not developed any sec-
amount of bone will be lost within the first 3 ondary sexual characteristics by the age of
years of hypoestrogenism. I believe that it is 13 should be examined and possibly evalu-
best to initiate hormone replacement ther- ated further. The same should be done for
apy by the time 6 months have passed, for any girl who has not begun to menstruate by
both oligomenorrheic and amenorrheic ath- age 16. Physical findings will direct appro-
letes. I also believe that pelvic examination priate testing for these problems. As shown
and blood evaluation should be repeated an- in Table 9-8, the diagnostic evaluation of
nually in all athletes with menstrual dys- primary amenorrhea is similar to that for
function, regardless of whether they are re- secondary amenorrhea, except for the
ceiving hormone replacement (Table 9-7). greater emphasis in primary amenorrhea
Many athletes claim that they prefer to be upon detection of a uterus.
amenorrheic. However, there is an obvious Müllerian agenesis (which includes the
difference between not wanting to menstru- absence of the uterus) is the second most
Menstruation and Menstrual Disorders 169

Table 9-8. DIAGNOSTIC EVALUATION OF loss, and exercise act synergistically to pro-
ATHLETES WITH PRIMARY AMENORRHEA mote hormone alterations in both women
1. History, including dietary intake with regular menses and those without.
2. Physical examination, including pelvic examination Athletes are more likely than sedentary
3. Prolactin, free thyroxine, TSH, FSH, LH, DHEAS, women and girls to experience menstrual
testosterone, B-HCG, estradiol dysfunction and menarcheal delay. How-
4. Progestin challenge test ever, this greater susceptibility should not
5. If uterus not palpable on pelvic examination:
sonogram discourage any athletes from exercising in-
6. If uterus absent: testosterone, karyotype tensely or frequently. The benefits of regular
7. If FSH high: karyotype exercise far outweigh this potential hazard.
The increased susceptibility of athletes to
menstrual dysfunction also should not lead
common pathologic cause of primary amen- to the presumptive diagnosis of "exercise-
orrhea, second only to gonadal dysgenesis. induced" until completion of a comprehen-
If the presence of a uterus cannot be deter- sive hormonal evaluation to rule out all
mined with certainty by pelvic examination, other pathologic causes. It must be empha-
a pelvic sonogram should be performed. sized that the diagnosis of "exercise-related
The third most common pathologic cause of menstrual dysfunction" can be made only
primary amenorrhea is androgen insensitiv- by excluding all other etiologies. Any
ity syndrome (testicular feminization). woman or girl experiencing one of these
Thus, the absence of a uterus requires fur- problems should be evaluated and treated.
ther testing to distinguish between these
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hormone release in humans. J Clin Endocri- Scand 64:387,1985.
nolMetab 52:583,1981. 55. Gonzales ER: Chronic anovulation may in-
41. Villanueva AL, Schlosser C, Hopper B, et al: crease post-menopausal breast cancer risk.
Increased cortisol production in women run- (Medical News), JAMA 249:445, 1983.
ners. J Clin Endocrinol Metab 63:133, 1986. 56. Frisch RE, Wyshak G, Albright NL, et al:
42. Loucks AB, Mortola JF, Girton L, and Yen SSC: Lower prevalence of breast cancer and can-
Alterations in the hypothalamic-pituitary- cers of the reproductive system among for-
ovarian and the hypothalamic-pituitary-ad- mer college athletes compared to nonath-
renal axes in athletic women. J Clin Endocri- letes. Br J Cancer 52:885,1985.
nol Metab 68:402, 1989. 57. Cann CE, Martin MC, Genant HK, and Jaffe
43. Ding J-H, Sheckter CB, Drinkwater BL, et al: RB: Decreased spinal mineral content in
High serum cortisol levels in exercise-asso- amenorrheic women. JAMA 251:626,1984.
ciated amenorrhea. Ann Int Med 108:530, 58. Rigotti NA, Nussbaum SR, Herzog DB, and
1988. Neer RM: Osteoporosis in women with an-
44. DeSouza MJ, and Metzger DA: Reproductive orexia nervosa. N Engl J Med 311:1601,1984.
dysfunction in amenorrheic athletes and 59. Drinkwater BL, Nilson K, Chesnut CH, et al:
anorexic patients: A review. Med Sci Sports Bone mineral content of amenorrheic and eu-
Exerc 23:995,1991. menorrheic athletes. N Engl J Med 311:277,
45. Boyden TW, Pamenter RW, Stanforth PR, et 1984.
al: Impaired gonadotropin responses to go- 60. Marcus R, Cann C, Madvig P, et al: Menstrual
nadotropin-releasing hormone stimulation function and bone mass in elite women dis-
in endurance-trained women. Fertil Steril tance runners. Ann Int Med 102:158,1985.
41:359, 1984. 61. Jones KP, Ravnikar VA, Tulchinsky D, and
46. Cumming DC, Vickovic MM, Wall SR, and Flu- Schiff I: Comparison of bone density in amen-
ker MR: Defects in pulsatile LH release in nor- orrheic women due to athletics, weight loss,
mally menstruating runners. J Clin Endocri- and premature menopause. Obstet Gynecol
nol Metabol 60:810,1985. 66:5,1985.
47. Cumming DC, Vickovic MM, Wall SR, et al: 62. Warren MP, Brooks-Gunn J, Hamilton LH, et
The effect of acute exercise on pulsatile re- al: Scoliosis and fractures in young ballet
lease of luteinizing hormone in women run- dancers. N Engl J Med 314:1348, 1986.
ners. Am J Obstet Gynecol 153:482,1985. 63. Lloyd T, Triantafyllou SJ, Baker ER, et al:
48. Veldhuis JD, Evans WS, Demers LM, et al: Al- Women athletes with menstrual irregularity
tered neuroendocrine regulation of gonado- have increased musculoskeletal injuries.
tropin secretion in women distance runners. Med Sci Sports Exerc 18:374,1986.
J Clin Endocrinol Metab 61:557, 1985. 64. Heaney RP, Recker RR, and Saville PD: Meno-
49. Cowan LD, Gordis L, Tonascia JA, and Jones pausal changes in calcium balance perfor-
GS: Breast cancer incidence in women with mance. J Lab Clin Med 92:953, 1978.
history of progesterone deficiency. Am J Ep- 65. Meema S and Meema HE: Menopausal bone
idemiol 114:209, 1981. loss and estrogen replacement. Isr J Med Sci
50. Prior JC, Vigna YM, Schechter MT, and Bur- 12:601, 1976.
gess AE: Spinal bone loss and ovulatory dis- 66. Lamon-Fava S, Fisher EC, Nelson ME, et al: Ef-
turbances. N Engl J Med 323:1221, 1990. fect of exercise and menstrual cycle status on
51. Fechner RE and Kaufman RH: Endometrial plasma lipids, low density lipoprotein parti-
adenocarcinoma in Stein-Leventhal syn- cle size, and apolipoproteins. J Clin Endocri-
drome. Cancer 34:444,1974. nol Metab 68:17,1989.
52. Jafari K, Ghodratollah I, and Ruiz G: Endo- 67. Schiff I, Sela HK, Cramer D, et al: Endometrial
metrial adenocarcinoma and the Stein-Lev- hyperplasia in women on cyclic or continu-
enthal syndrome. Obstet Gynecol 51:97, ous estrogen regimens. Fertil Steril 39:79,
1978. 1982.
53. Coulam CB, Annegers JF, and Kranz JS: 68. Gelfand M, and Ferenczy A: A prospective 1-
Chronic anovulation syndrome and associ- year study of estrogen and progestin in post-
ated neoplasia. Obstet Gynecol 61:403, 1983. menopausal women: Effects on the endome-
54. Dennefors BL, Knutson F, Janson PO, et al: trium. Obstet Gynecol 74:398,1989.
Ovarian steroid production in a woman with
CHAPTER 10

Pregnancy
MARSHALL W. CARPENTER, M.D.

PHYSIOLOGIC CHANGES OF ACUTE METABOLIC RESPONSE


PREGNANCY TO EXERTION
ACUTE PHYSIOLOGIC RESPONSE MATERNAL THERMOREGULATION
TO EXERTION IN THE DURING EXERCISE
NONPREGNANT STATE
ACUTE EFFECTS OF MATERNAL
ACUTE METABOLIC RESPONSE TO EXERTION ON THE FETUS
EXERTION
MATERNAL EXERCISE TRAINING
EFFECT OF PREGNANCY ON THE EFFECTS ON FETAL GROWTH
ACUTE PHYSIOLOGIC AND PERINATAL OUTCOME
RESPONSE TO EXERTION
RECOMMENDATIONS ABOUT
EFFECT OF PREGNANCY ON THE RECREATIONAL EXERCISE

Exertion and pregnancy are the two most profound normal alterations in
mammalian physiology. Exertion causes acute changes in cardiac output, blood
flow distribution, oxygen uptake, fuel mobilization, and the endocrine responses
that facilitate these changes. Chronic exercise stress (exertional training) alters
resting cardiovascular and metabolic homeostasis, the circulatory response to
exertion, and aerobic capacity. Pregnancy appears to induce a primary vasodi-
latation with associated increases in cardiac output, oxygen carrying capacity,
oxygen uptake, and pulmonary changes. Whereas many of the cardiovascular
changes that characterize pregnancy at rest are similar to those seen in acute
exertion, the endocrine and metabolic changes of pregnancy differ considerably
from those seen with acute exertion. Acute maternal adaptation to exertion and
to exercise training has recently received increased investigational attention.
The effect of maternal acute and chronic exercise stress on fetal homeostasis and
growth and the role of maternal nutrition remain only superficially understood
in humans, based primarily on animal investigation. The limited physiologic and
epidemiologic investigation available, however, form the foundation for the
guidelines and counsel that can be offered to pregnant women.
This chapter examines the effects of pregnancy on resting physiology, and
its interaction with the effects of acute exertion. The impact of acute exertion on
172
Pregnancy 173

fetal homeostasis and the effect of exercise in a 17% increase in minute ventilation rel-
training on pregnancy outcome are also ex- ative to oxygen uptake (the ventilatory
plored. These observations will be related equivalent).14 This results in a fall in arterial
to recommendations which may be offered Pco2 from 39 to 31 torr, which produces a
to pregnant women in clinical circum- mild respiratory alkalosis, increasing pH to
stances. 7.44. Increased total lung capacity and in-
creased tidal volume account for most of the
increase in minute ventilation, rather than
PHYSIOLOGIC CHANGES OF changes in respiratory frequency. The in-
PREGNANCY creased resting oxygen uptake observed in
pregnancy is an early phenomenon, half of
Cardiovascular changes begin early in which occurs by 8 weeks and three quarters
pregnancy and are well established by the by 15 weeks' gestation. However, resting ox-
midtrimester, thereby anticipating later ygen uptake remains proportional to body
fetal/placental requirements for oxygen and weight, not changing from the antepartum to
nutrition. Plasma volume increases 45% by postpartum state.15'16
30 to 34 weeks,1,2 with measurable changes
by 8 weeks. Despite a dilutional anemia, red
cell volume increases by 20% to 30% by mid- ACUTE PHYSIOLOGIC
pregnancy.2 RESPONSE TO EXERTION IN
Cardiac output may increase secondary to THE NONPREGNANCY STATE
a primary increase in circulating plasma vol-
ume or decreased systemic vascular resist- The cardiovascular and respiratory sys-
ance,3 though the relationship of these fac- tems act in concert during acute exertion to
tors remains speculative.4 By 8 weeks, ensure adequate oxygen delivery to exercis-
cardiac output increases by 23% and stroke ing muscle while maintaining function in
volume by 20%.5-7 The maximal increment other tissues. Oxygen consumption is the
in cardiac output (34%) exceeds the 13% in- product of oxygen delivery (heart rate,
crease in body weight during pregnancy. stroke volume) and oxygen extraction (ar-
This is due, partly, to the 13% to 30% in- teriovenous 02 difference), as expressed in
crease in resting oxygen uptake observed in the modified Fick equation:17
pregnancy8-10 and also to the decreased ar-
teriovenous oxygen difference in preg- Vo2 = HR-SV-avD 02
nancy. During incremental exercise to maximal
End diastolic volume6,7 and stroke intensity, Vo2 increases linearly to values
volume11 appear to increase through mid- typically 10 to 20 times that at rest. Near the
pregnancy. Venous compliance increases by peak intensity of exertion, a plateau of oxy-
the second trimester and is greater in gen uptake (Vo2) occurs, which persists de-
the lower extremities.12,13 These vascular spite greater exercise intensity. This upper
changes and the expanding uterus may im- limit of oxygen uptake (Vo2max) occurs as
pede vena caval blood flow, so that maternal maximal aerobic power is reached and is the
position increasingly alters measurements most important indicator of cardiovascular
of hemodynamic function as pregnancy pro- fitness. The percentage of Vo2max may be
gresses. The further increase in resting car- used, therefore, to describe relative inten-
diac output later in pregnancy seems to be sity of exertion among individuals with dif-
heart- rate dependent butvariable, due to dif- ferent aerobic capacities when comparing
ferences in maternal stature and position. physiologic responses that are related to ex-
Respiratory changes in pregnancy involve ertional intensity. Vo2max is usually limited
respiratory control and pulmonary function. by cardiac output. (See Chapters 1 and 4.)
Changes in respiratory control are reflected Cardiac output typically increases four-to-
174 Developmental Phases

fivefold from rest to maximum exertion. Car- oxygen uptake, approaching a ratio of 40 L of
diac output increases with Vo2 in normal in- air per liter of O2 uptake. This change in ven-
dividuals in a ratio ranging from 5:1 to 6:1. tilatory pattern has been referred to as the
Heart rate increases linearly with Vo2. Ini- "ventilatory threshold"21,22 but has uncer-
tial increases during mild exertion result tain physiologic significance. It is loosely as-
from release from vagal tone, and increases sociated with elevated levels of plasma lac-
at higher exercise intensities are caused by tate, found at high exertional intensity.
increases in sympathetic tone. Up to 40% Exercise training results in a greater in-
Vo2 max, stroke volume increases with in- crease in Vo2 at ventilatory threshold than in
creased venous return to 1.5 to 2.0 times that Vo2max. Maximal voluntary ventilation does
at rest. Above a heart rate of 100, however, not limit Vo2max in normal individuals.
further increases in cardiac output are
pulse-dependent.18
Peripheral as well as central hemody- ACUTE METABOLIC RESPONSE
namic changes are necessary to effectively TO EXERTION
deliver required oxygen and fuel to exercis-
ing muscle. Blood flow is redistributed by The profound increase in the energy re-
sympathetic nerve activity, which is re- quirements of muscle during exercise neces-
flected in increased plasma norepinephrine sitates the mobilization and distribution of
concentrations.19 Norepinephrine concen- fuel from other tissues to sustain exertion
tration is closely related to intensity of ex- beyond the first seconds of movement. En-
ertion and to heart rate above 100.17 This ergy consumption may increase over 10-fold
redistribution results in an early and sus- above resting values during intense exer-
tained linear reduction in splanchnic and tion.21,23,24 Muscle can oxidize glucose, free
renal blood flow and, at high exertional in- fatty acids, glycerol and ketones to produce
tensity, causes decreased cutaneous perfu- energy. The proportion of fuel types avail-
sion. able to muscle is a function of exercise inten-
The proportion of total cardiac output sity, duration, nutritional state, and the
perfusing exercising muscle increases with physical fitness of the individual, and is de-
the relative intensity of exertion regardless termined largely by the acute hormonal re-
of individual aerobic fitness. However, this sponse to exertion.
proportion is higher at maximal aerobic Carbohydrate stores in the body are
power among individuals with high levels of found in muscle glycogen (300 to 400 g, 5 • 103
aerobic fitness. Therefore, the increment in kJ), hepatic glycogen (80 to 90 g, 1.5 • 103 kJ),
Vo2max obtained with exercise training is at- and blood glucose (20 g, 30 kJ). This is
tributable to increased oxygen uptake of ex- dwarfed by the energy stored as fat (about
ercising muscle, while nonexercising vas- 15 kg, 6-10 5 kJ). Protein is not significantly
cular beds receive the same low absolute available as fuel during acute exercise. At
blood flow. rest, free fatty acids provide the primary fuel
Oxygen uptake during exertion is also en- for muscle in the fasting state.
hanced by increased oxygen extraction from As exertional intensity increases beyond
each volume of blood perfusing exercising 60% Vo2max, carbohydrate is oxidized in
muscle. This is reflected in a three- or four- higher proportions, so that at Vo2max, all the
fold increase in arteriovenous oxygen differ- energy expended by muscle is derived from
ence at maximal exertion compared to carbohydrate oxidation. At this intense level
rest.17'20 of exertion, adenosine triphosphate (ATP)
Ventilation increases linearly with oxygen is provided increasingly by anaerobic gly-
uptake (at 20 to 25 L per liter of O2 uptake) colysis, which is reflected in rising plasma
to about 50% Vo2max, above which the in- lactate concentrations above 60% Vo2max.
crease in ventilation is greater, relative to Elevated plasma lactate may act to suppress
Pregnancy 175

lipolysis,25 thereby increasing demands on stimulate glucagon release, which, in turn,


carbohydrate as fuel. Consequently, exer- augment hepatic glycogenolysis and periph-
cise at Vo2max can only be sustained for a eral lipolysis.28,29 Both norepinephrine and
short duration, being limited by the modest epinephrine increase with percent Vo2max
stores of carbohydrate available to sustain and pulmonary artery oxygen saturation.
exertion at this intensity. Most investigators Epinephrine concentration is increased
employ some criterion for a "plateau" of ox- with intense exertion, is produced by the ad-
ygen uptake with increasing workload to es- renal medulla, and correlates positively
tablish that Vo2max has been achieved. The with norepinephrine and negatively with
uncertainty about criteria to establish a glucose concentrations.30,31 Therefore, the
maximum Vo2 plateau and the subject's dif- net effect of these changes is to augment and
ficulty in maintenance of this level of exer- sustain the release of glucose.
tion make observations under this condition Exertion also alters the metabolic effects
problematic, especially in pregnancy. Data of insulin. The drop in insulin concentration
from such studies thereby require some during acute exertion does not impede the
judgment in their interpretation. marked rise in peripheral glucose uptake
Exercise duration also influences fuel me- during exercise.32 Under these conditions,
tabolism. The immediate, local sources of only an absolute lack of insulin causes a re-
energy (ATP and phosphocreatine) provide duction in glucose uptake (in the pancre-
energy for the first 6 to 8 seconds of muscle atectomized dog), suggesting that insulin
contraction. Glycogenolysis and local lac- may only have a permissive role in periph-
tate production provide carbohydrate for 1 eral uptake during intense exertion.32 Iso-
to 3 minutes of exertion at maximal aerobic lated exertion increases insulin-mediated
exertion. Exercise beyond 5 to 10 minutes glucose uptake (insulin sensitivity) and glu-
becomes increasingly dependent on free cose uptake at maximal effective insulin con-
fatty acids. Moderate-intensity exertion for centration (insulin responsiveness) up to 48
40 minutes results in a fourfold rise in glu- hours after exercise.33
cose production by glycogenolysis and glu- Intense or prolonged moderate exertion is
coneogenesis to maintain plasma glucose required to produce a rise in circulating lev-
concentration for tissue with obligate glu- els of glucagon,29,34 growth hormone,35 and
cose needs. This response is reduced 15% to cortisol. Growth hormone response corre-
60% by glucose infusion, and 67% by glucose lates with Vo2 and plasma lactate concentra-
and insulin infusion.26 tion.35
Diet antecedent to exercise may alter ex-
ercise capacity at Vo2max. A high carbohy-
drate diet following intense exercise EFFECT OF PREGNANCY ON
increases muscle glycogen stores. Low car- THE ACUTE PHYSIOLOGIC
bohydrate diets decrease muscle and he- RESPONSE TO EXERTION
patic glycogen. Exercise capacity is in-
creased when muscle glycogen stores are The impact of pregnancy on exercise re-
augmented.21'23,2427 Carbohydrate ingestion sponse to submaximal and maximal exer-
during exertion increases exercise endur- cise differs. During pregnancy, we found that
ance.21'23,24.27 absolute oxygen consumption (L-min^ 1 )
The neuroendocrine response to exertion was 14% higher at rest, 9% higher during
facilitates the mobilization of fuels for mus- identical workloads during submaximal,
cle contraction. Norepinephrine, released weight-supported cycle ergometry, and 12%
from synaptic nerve endings, stimulates he- higher during identical submaximal tread-
patic glycogenolysis and peripheral lipoly- mill exertion16 compared to postpartum val-
sis. It also stimulates islet -adrenergic re- ues. Similar investigations by others have
ceptors to inhibit insulin release and not consistently shown an increased oxygen
176 Developmental Phases

uptake during submaximal cycle exercise in Likewise, peak age-specific heart rate ap-
pregnancy compared to nonpregnant con- pears to be unchanged by pregnancy at max-
trols.8-11,37,38 However, identical submaximal imal aerobic exertion. Also, we and others
treadmill exertion has been found to result have found no difference in maximal aerobic
in increased Vo2 during pregnancy.8,16 When power in pregnancy when compared with
oxygen consumption is expressed relative postpartum values.10
to body weight (mL-kg - 2 -min - 1 ), however, Recovery from exertion in the upright po-
there are no differences in submaximal ox- sition may differ in pregnancy. Stroke vol-
ygen uptake with either mode of exercise. Of ume recorded within 3 minutes of exercise
the increased oxygen uptake of submaximal cessation has been observed to fall 26% dur-
exertion, 75% can be accounted for when the ing the third trimester, compared to only
contribution of increased maternal weight is 11% postpartum.40 Cardiac output did not dif-
controlled for experimentally during preg- fer, being maintained by a compensatory
nancy. This was accomplished by compar- increase in heart rate. This change in post-
ing non-weight-bearing and weight-bearing exertional recovery may be related to in-
exercise during pregnancy and postpartum, creased venous compliance and capacity
and by using weight belts during postpar- and possible vena caval obstruction that
tum weight-bearing exertion to mimic preg- may characterize late pregnancy, though
nancy weight.16 These data suggest that this remains to be documented.
gravid women have an increased resting and
exertional percent Vo2max due, largely, to
the increased metabolic demands of the EFFECT OF PREGNANCY ON
conceptus as well as the increased work of THE ACUTE METABOLIC
moving a heavier body. RESPONSE TO EXERTION
Pregnancy may alter the relative contri-
bution of stroke volume and heart rate to in- Pregnancy produces alterations in hor-
creased cardiac output during incremental monal and metabolic homeostasis, which
workloads at high levels of exercise inten- distinguish it from the nonpregnant resting
sity. In the nonpregnant state, stroke vol- and exercising state. Pregnancy produces
ume does not increase with incremental ex- insulin resistance, which is reflected in an
ertion above 60% Vo2max; further increases elevated fasting insulin-glucose ratio. This
in cardiac output are due to increased heart may be observed more quantitatively by in-
rate. In contrast, limited data in pregnancy ducing hyperinsulinemia by intravenous
suggest that further increases in stroke vol- infusion and measuring the rate of glucose
ume are still possible above this level of ex- infusion required to maintain steady-state
ertional intensity.10 This change in the rela- euglycemia. This euglycemia, hyperinsulin-
tive contribution of stroke volume to emic clamp technique demonstrates a
incremental cardiac output with increased reduced requirement for infused glucose
workload alters the regression equation of during pregnancy in order to maintain eu-
Vo2 on heart rate during pregnancy. Conse- glycemia compared to that required in the
quently, the mathematic model for predict- nonpregnant state under the same hyperin-
ing Vo2max from submaximal Vo2/heart-rate sulinemic conditions.41 Insulin binding on
data in pregnant women is altered.39 red cells is unaffected by pregnancy, but
In contrast to submaximal exertion, the binding is reduced on adipocytes during
limited studies performed on pregnant pregnancy.42 Pregnancy is characterized by
women at maximal aerobic exertion show postprandial hyperglycemia and by fasting
little, if any, change in maternal cardiovas- hypoglycemia. Free fatty acid and triglycer-
cular response under this condition. Preg- ide concentrations are increased in preg-
nancy is not associated with any change in nancy.
the usual coupling of Vo2 to cardiac output.10 Acute hormonal responses to exercise
Pregnancy 177

stress support internal homeostasis in two on glucagon, growth hormone, and cortisol
ways. First, release of catecholamines by pe- response to moderate or intense exertion
ripheral nerves serves to increase and redi- has not been examined.
rect cardiac output to exercising muscle Consequently, the nature and degree of
while maintaining "adequate" perfusion to pregnancy-induced alterations of acute hor-
nonexercising vascular beds. Second, the monal response to exertion are largely
medullary release of catecholamines, and unexamined. Possible direct or indirect ef-
the release of glucagon, cortisol, and growth fects of these changes on fetal homeostasis
hormone result in providing the peripheral during maternal exertion are likewise un-
circulation with fuel to maintain both in- known.
tense and sustained exertion.
Little has been published about altera-
tions in the hormonal response to exertion MATERNAL
induced by pregnancy. Resting plasma nor- THERMOREGULATION DURING
epinephrine and epinephrine levels are un- EXERCISE
changed in pregnancy, though standing is
associated with a reduced rise in norepi- Published studies of maternal thermoreg-
nephrine concentration in pregnancy.43 Ex- ulation have examined gravidae only, during
ertion appears to produce a similar norepi- submaximal exertion lasting 20 to 30 min-
nephrine response in pregnancy as in the utes in a controlled laboratory environment
nonpregnant state.44,45 Insulin concentration of 19 to 21 °C with a relative humidity of 30%
does not appear to fall during mild exertion to 55%. Two studies examined stationary
during pregnancy46 but has not been exam- cycle exercise at approximately 60%
ined at more vigorous exercise. Glucagon, Vo2max,47,48 and one49 had subjects perform
which is increased in pregnancy, has been treadmill exercise at a maternal heart rate of
observed to rise twofold with materal exer- approximately 158 beats per minute (bpm)
tion to a pulse of only 104,46 but this was not (approximately 60% Vo2max). Under these
confirmed in later studies.44 In the nonpreg- conditions, the range of mean rectal temper-
nant state, increased glucagon concentra- ature rise was 0.3 to 0.8°C during exercise,
tions are observed after only intense or pro- inversely related to gestational age (Fig. 10-
longed exertion.29 The effect of pregnancy 1). Pregnant women appear to maintain

Figure 10-1. Resting and maximal rectal temperatures (at the bottom and top of each column, re-
spectively) during, and 10 minutes48after, a 20-minute cycle exercise period at 61%-64% maximal ox-
ygen uptake. (Adapted from Clapp ).
178 Developmental Phases

their core temperature within narrow limits, Early studies in human pregnancy exam-
though maternal thermoregulatory capacity ined fetal heart-rate response to maternal
during exertion under more stressful ambi- exertion using the same Doppler fetal mon-
ent conditions has not been examined. As- itors used clinically on quiet, recumbent
sociated fetal effects also have not been ex- women during labor. These reports de-
amined. scribed frequent fetal bradycardia with only
brief and mild maternal exertion,57,58 but the
findings may have been confounded by mo-
ACUTE EFFECTS OF MATERAL tion artifact during maternal activity.
EXERTION ON THE FETUS Subsequent investigation has employed
two-dimensional sonographic fetal heart-
Splanchnic perfusion falls linearly with rate documentation. In one such study, 85
the percentage of Vo2max, as blood flow is submaximal and 79 maximal exercise
redistributed to exercising muscle. A similar bouts59 produced no unexplained fetal bra-
reduction in uterine blood flow with mod- dycardia (< 110 bpm) during exertion. How-
erate and extreme maternal exertion during ever, postexertional fetal bradycardia was
pregnancy has been demonstrated in noted within 3 minutes of cessation of max-
sheep50-52 and goats53 and suggested in hu- imal aerobic effort in 19% (15 out of 79) of
mans (Fig. 10-2).54-56 In sheep, this exer- cases (Fig. 10-3). This bradycardia was not
cise-induced reduction of uterine perfusion associated with the duration of maximal aer-
was found to be associated with a fall in fetal obic exertion, changes in maternal blood
Po2 of 11% with moderate maternal exertion, pressure during and after exertion, or with
and 30% with exhausting exertion.51 How- gestational age. It was more likely to occur
ever, no measurable net lactate production in women with higher Vo2max values, sug-
by the conceptus has been observed under gesting that maternal cardiovascular fitness
these conditions. This suggests that oxygen does not protect against this event. All fe-
delivery is, in most fetal tissues, adequate tuses had normal fetal heart-rate patterns
for aerobic metabolism during these short- and fetal activity within 30 minutes of mater-
term experiments. nal exercise, and the birth outcome in the
pregnancies with fetal bradycardia was un-
complicated.
These data suggest that fetal homeostatic
reserve is not compromised by even ex-
treme levels of maternal exertion in the
human. The possible adverse impact of ma-
ternal upright posture on fetal homeostasis
during maternal recovery remains to be ex-
plored. The observed postexertional fall in
stroke volume in exercising gravid women
may indicate that visceral perfusion may be
compromised in pregnancy under these
conditions.
Observations of baseline fetal heart rate
before, during, and after maternal exertion
has generally shown a 10 to 15 bpm increase
Figure 10-2. Relationship between heart rate and uter- in fetal heart rate with moderate exertion
ine blood flow as percent of control in near-terra preg- lasting 30 minutes or more. Generally mater-
nant sheep: o = rest, a = 10-minute exercise at 70% nal exertion at 60% Vo2max which lasts less
Vo2max; • = 10-minute exercise at 100% Vo2max; A =
40-minute exercise at 70% Vo2max. (From Lotgering,51 than 20 minutes will not produce fetal tachy-
with permission). cardia. Exertion at this level which lasts 20
Pregnancy 179

to 30 minutes will produce a rise in fetal


heart rate which correlates with gestational
age over 20 to 36 weeks. This response does
not correlate with the minor changes in ma-
ternal core temperature (0.3°C) observed in
these subjects, however.47

MATERNAL EXERCISE
TRAINING EFFECTS ON FETAL
GROWTH AND PERINATAL
OUTCOME

The epidemiology of the workplace envi-


ronment and activity and maternal and peri-
natal outcome occupies a large body of lit-
erature. Discussion here will be limited to
studies examining the association of recre-
ational exercise with maternal and perinatal
outcome. Prospective studies of recrea-
tional exertion can be divided into nonran-
domized and randomized, controlled com-
parisons of exercising and sedentary
pregnant women. Nonrandomized studies
have shown both no effect on maternal
weight gain60 and significantly reduced ma-
teral weight gain caused by chronic mater-
nal exercise.61 Likewise, nonrandomized ob-
servations have documented either no effect
of chronic maternal exercise on birth weight
and duration of pregnancy60,62 or a significant
reduction in birth weight, percentile birth
weight, percentage body fat,63 and earlier
gestational age at birth.61,64 Exercising moth-
ers were found to have either a lower rate of
labor complications60,64 or no significant dif-
ference from their nonrandomized con-
trols.62 It should be noted that most of these
nonrandomized studies63-65 examine the ef-
fect of the cessation of maternal recreational
exertion before or early in pregnancy among
women who are exercise enthusiasts. The
remainder are simply comparisons of

onds during the postexercise period, using videotaped


recordings of two-dimensional fetal imaging. Predece-
leration baseline fetal heart rate and nadir fetal heart
Figure 10-3. Fetal heart rate following maximal exer- rate are noted for each deceleration. Zero time is time
tion during 14 episodes of fetal bradycardia. Fetal heart of cessation of maximal effort. (From Carpenter,59 with
rate was averaged over 10 cardiac cycles every 30 sec- permission).
180 Developmental Phases

women who have self-selected exercise pro- Available data suggest that maternal exer-
grams or sedentary activity. tion does not predispose to preterm labor.
Two randomized, controlled trials66,67 ex-
amined the effect of instituting exercise
training during pregnancy in sedentary RECOMMENDATIONS ABOUT
pregnant women. Only one provided ob- RECREATIONAL EXERCISE
served exercise training in a laboratory en-
vironment.67 Both studies documented ob- The limited scope of applied research re-
jective signs of cardiovascular training effect garding the effects of pregnancy on acute ex-
in the groups randomized to exercise train- ercise and training and the effects of exer-
ing; however, in contrast to the nonrandom- tion on pregnancy limit the advice that can
ized investigations, neither randomized trial be confidently given to the pregnant patient.
showed any effect of maternal exercise In 1985, the American College of Obstetri-
training on maternal weight gain, length of cians and Gynecologists published two pre-
gestation, birth weight, Apgar scores, or scriptive articles,70,71 which commented on
mode of delivery. One study66 suggested that exercise during pregnancy. These recom-
primigravid trainers had a shorter second mendations preceded much of the clinical
stage of labor. research performed in this area. As such,
Differences between the results of non- they were an attempt to form a consensus
randomized and randomized prospective opinion about principles of maternal and
studies suggest that self-selected women fetal safety during maternal exertion, and
may differ in daily activity, percentage body they reflected a necessarily conservative ap-
fat, caloric intake or food type, or other fac- proach to exercise in pregnancy that could
tors that affect fetal growth, medical treat- be used, practically, in a clinical setting.
ment during labor, and maternal and peri- Some later studies have addressed some of
natal outcome. Some of the nonrandomized these issues.
studies are detraining studies rather than The principles documented in these pub-
investigations of training effects in seden- lished guidelines are listed below. In italics,
tary women, and thereby present problems the uncertainty attending these guidelines
in applying findings in atheletes to the more or modifying data available from subse-
common, inactive pregnant woman. Women quently published research are discussed.
who enter pregnancy with a history of fre-
quent vigorous exertion may differ metabol- 1 Maternal joints become more unstable
ically from those who are relatively seden- during pregnancy and may be more
tary. prone to injury during exertion. Exer-
Transabdominal pressure transducer cises should avoid "ballistic" move-
monitoring of pregnant women during ex- ment and extreme extension and flexion
ercise has shown, in one study,68 that uterine of joints. No observational or experimen-
contractions are associated with nonrecum- tal studies have quantified the risk of joint
bent types of exercise. Another investiga- injury during pregnancy. These proscrip-
tion,69 however, examined uterine contrac- tions may reduce injury, however.
tions by the same method immediately after 2 More physically fit individuals will per-
the cessation of maternal exertion and form a given task at a relatively lower
found no increased uterine activity. These percentage of maximal aerobic capac-
studies and practical experience in the use ity. It is therefore desirable for women
of these transducers in laboring women sug- to become aerobically trained before
gest that the uterine activity detected in up pregnancy and thereby reduce fetal risk
to 50% of gravidae during exercise is likely of asphyxia and bradycardia during ma-
to represent artifact due to maternal motion. ternal exertion during pregnancy. Di-
Pregnancy 181

rect observation of fetal heart-rate re- carbohydrates during exertion if exercise


sponse during maternal exertion has is carried out at a higher percentage of
shown no fetal heart rate decelerations aerobic capacity, so it may be desirable
during exertion of any relative intensity, during pregnancy to exercise at levels that
and none following maternal exertion up elicit maternal heart rates of less than 150
to a maternal pulse of 150 bpm in the ma- bpm.
ternal age range of 21 to 37 years of age. 5 Exercise during pregnancy may result
The occasional fetal bradycardia that fol- in premature labor due to release
lows maximal maternal exertion is more of norepinephrine. Experimental data
common in the more aerobically fit show no consistent evidence of increased
mother. Maternal exertion may increase uterine contractions immediately follow-
the baseline fetal heart rate.72 However, ing exertion. Preterm labor among exer-
exercise-associated fetal tachycardia and cisers does not appear to be increased in
episodic bradycardia are unassociated either detraining or training studies.
with any measurable fetal or neonatal 6 Previously sedentary women should
morbidity.59 The usually recommended engage in activity of very low intensity
warm-up and slow cool-down periods and avoid exertional intensity known to
with exercise should probably be used increase exertional cardiovascular fit-
during pregnancy. ness. Limited human experimental data
3 Pregnant women may develop a high show no increased maternal or fetal com-
maternal core temperature during ex- promise during and after acute exertion.
ercise exceeding 15 minutes, especially Pregnant women with lower Vo2max val-
in hot and humid environments. High ues had a lower rate of fetal bradycardia
maternal core temperature may be as- after maximal exertion,59 suggesting that
sociated with teratogenesis or respira- prior sedentary lifestyle is not a contrain-
tory compromise in animals, suggesting dication to vigorous exertion during preg-
risk in the exercising mother. Human nancy.
experiments describe only a 0.3 to 0.8°C 7 Pregnant women should practice good
rise in maternal core temperature with nutritional principles (see below) and
moderate to severe maternal exertion of avoid cigarettes and alcohol. The vaso-
30 minutes' duration,47,48,73 an increase of dilatory effects of alcohol and vasocon-
little physiologic consequence. The effect strictive and hypoxemic effects of ciga-
of maternal exertion under conditions of rette smoking may compromise the
high ambient temperature and humidity homeostatic reserve of the mother and the
on fetal homeostasis and core tempera- fetoplacental unit during maternal exer-
ture has not been examined. tion. Women who smoke and drink during
4 Maternal fasting glucose levels are sig- pregnancy should probably avoid exer-
nificantly lower than in the nonpreg- tion at times when exposed to these drugs.
nant state. Since pregnant women use No human observational studies or exper-
more carbohydrate during exertion, hy- iments have been performed examining
poglycemia may occur during exertion. these interactions directly.
Little human experimental evidence is 8 Women whose pregnancies are com-
available about maternal glycemic re- promised by any maternal diseases or
sponse to exertion. Animal experiments any untoward symptoms should con-
performed in the nonpregnant state indi- tact their physician for consultation.
cate that both sympathetic and glucagon The importance of consultation of a
response to exertion must be ablated to patient with her physician should be em-
cause exertional hypoglycemia. Gravidae phasized. Though data are not available,
consume a relatively higher proportion of caution regarding exertion in many con-
182 Developmental Phases

ditions complicating pregnancy should be affected by maternal exercise. The sig-


counseled by physicians. nificance of these interactions is impos-
sible to estimate; thus, we remain cau-
We use several principles when counsel-
tious in our counseling of potentially
ing pregnant women regarding exercise:
affected pregnant patients.
1 We recognize the value of continued 6 Patients with a history of poor preg-
recreation during pregnancy, which for nancy outcome due to repeated abor-
many women includes vigorous exer- tion, abruptio placenta, preterm labor,
tion. Unless prior observational or ex- or preterm rupture of membranes are
perimental data or the individual cir- probably not compromised by exercise
cumstances of the patient's pregnancy in pregnancy, based on limited studies
appear to contradict a proposed exer- in normal women. Appropriate investi-
cise activity during pregnancy, we do gation of exercise effects on patients
not proscribe exertion for the patient. with these histories have not been per-
2 Relative exertional intensity, as de- formed, however. We counsel patients
scribed in terms of percentage of with such histories who desire to exer-
Vo2max, produces similar cardiovascu- cise about our lack of knowledge, and
lar, respiratory, and hormonal re- about their potential sense of responsi-
sponses. Likewise, fetal homeostasis is bility should another mishap occur in
similarly maintained at a given relative the present pregnancy. In this circum-
exertional intensity, regardless of the stance, however, we are nondirective in
exertional fitness of the experimental our counseling. Patients with histories
animal. We infer that this is also true for of incompetent cervix, DES exposure, or
pregnant patients and allow physical with uterocervical abnormalities are
exertion in all healthy patients up to a counseled to avoid exertion during
heart rate of 150 bpm. Since heart rate pregnancy.
is difficult to monitor during competi-
tive sports and levels of peak exertion
tend to be high, we discourage compet- NUTRITIONAL REQUIREMENTS
itive exertion for pregnant women. OF PREGNANT EXERCISERS
3 Exercise studies during pregnancy have
been limited to short bouts of exertion It seems appropriate to advise pregnant
under "comfortable" ambient condi- exercisers also about possible changes in
tions. Since exertion for prolonged pe- nutritional requirements to support the en-
riods or with high heat and humidity ergy demands of exercise and the increased
has not been examined in human preg- caloric costs of accretion of maternal and
nancy, we discourage exercise under fetal tissues. Pregnancy, but not exercise,
these conditions in pregnant patients. substantially increases dietary protein re-
4 Pregnant patients are probably more quirements. Other than fetal demands for
prone to trauma because of changes essential free fatty acids, neither exercise
in weight distribution and resulting nor pregnancy requires a net increase in di-
"clumsiness." Consequently, we cau- etary fat.
tion patients about potentially trau- Estimates of increased caloric needs of
matic sports, especially in the last half pregnancy were originally based on cross-
of pregnancy, when the uterus is more sectional data of increased maternal and
exposed to frontal trauma. fetal mass in pregnancy.73, 74 The fetal mass of
5 Fetal homeostasis during pregnancy 3.5 kg, the placental mass of 0.6 kg, the in-
compromised by uteroplacental insuf- crease in uterine and breast mass of 5 kg, of
ficiency, cardiac or respiratory disease, maternal fat of 4 kg, and the estimated in-
or significant anemia may be adversely crease in metabolic rate were used to esti-
Pregnancy 183

mate the total caloric cost of pregnancy to amounts will be provided by a balanced diet
be approximately 83,000 kcal. This estimate with sufficient increased calories. The exer-
suggests that an increase of ~250 kcal in cise-related requirements for thiamine, nia-
daily caloric intake is needed in pregnancy, cin, riboflavin, and pantothenic acid like-
consistent with the FAO/WHO/UNU,75 the wise are probably supported by a calorically
United Kingdom Department of Health and adequate diet.
Social Security,76 and the National Research Mineral needs, in the form of iron and cal-
Council.77 Longitudinal investigations of cium, are probably not increased in exercis-
pregnancy begun prior to conception pro- ing individuals. Pregnancy results in a fetal
vide different data, however. A cohort of 162 accretion of 300 mg of elemental iron and a
women from Scotland and the Netherlands maternal erythropoietic requirement of 500
underwent prospective measurements of mg. Exercise training will produce an in-
weight, body fat, dietary intake, metabolic crease in plasma volume and erythrocyte
rate at rest, and daily activity pattern.78 The mass which requires a transient increase in
estimated increased energy cost of preg- iron utilization. Recommendations for the
nancy was ~69,000 kcal. The increase in daily intake of iron (30 to 60 mg of elemental
dietary intake during pregnancy was esti- iron) and calcium (1200 to 1500 mg of ele-
mated based on fairly rigorous weighed-in- mental calcium) during pregnancy will meet
ventory 5-day measurements performed the needs of exercising as well as sedentary
every 2 to 4 weeks during pregnancy. These pregnant women.
estimates suggested that the average incre-
ment in dietary intake during pregnancy was
only ~22,000 kcal. The 47,000-kcal discrep- SUMMARY
ancy suggests either that the estimates of ca-
loric intake are in error or that there is a re- Both pregnancy and exercise produce
duction in physical activity and an increase profound adaptive cardiovascular and en-
in mechanical efficiency during pregnancy. docrine responses which affect fetal homeo-
Nevertheless, during normal pregnancy stasis. The early cardiovascular and hema-
with documented sedentary lifestyle, daily tologic changes of pregnancy include
incremental caloric intake appears to be 80 increased stroke volume, increased cardiac
to 100 kcal/d in the first half of pregnancy, output, decreased peripheral vascular re-
and approximately 150 to 200 kcal/d during sistance, increased venous compliance, in-
the second half. Since chronic exercise may creased minute respiration, and increased
increase basal metabolic rate and the char- plasma and red cell volume. These "adap-
acter, duration, frequency, and intensity of tations" occur well before the fetoplacental
exercise will otherwise affect the increased unit develops the increased gas and nutrient
caloric cost of exertion, these estimates are transport that is supported by these
complex and need to be individualized. changes.
Since maternal weight gain probably offers a Exercise in pregnancy is associated with
reproducible correlate with fetal growth in many of the same physiologic responses as-
the second half of uncomplicated, sedentary sociated with exertion in the nonpregnant
pregnancy, weekly weight gain may provide state. Vasoconstriction occurs in vascular
a practical measure of the adequacy of ca- beds, except those serving exercising mus-
loric support in exercising women. The util- cle. Mild exertion induces increases in pulse
ity of maternal weight gain as a measure of and stroke volume, which both contribute to
fetal nutritional adequacy in pregnancy in increased cardiac output. Limited data sug-
exercising women has not been adequately gest that the neuroendocrine response and
tested, however. insulin and glucagon response to exertion
Requirements for most vitamins are in- during pregnancy are similar to those found
creased during pregnancy, but adequate in the nonpregnant state. However, preg-
184 Developmental Phases

nancy is associated with a decreased arte- training by athletes after conception may re-
riovenous O2 difference and an increased duce fetal birth weight, though this thesis
stroke volume, which may impact on re- requires further investigation.
sponse to intense physical exertion. For ex- Clinical recommendations for patients de-
ample, during cycle exercise, increases in sirous of engaging in recreational exercise
stroke volume appear to contribute to incre- are limited by the small number of clinical
mental cardiac output at extreme exertional studies available. Consequently, current
intensity, which does not occur in nonpreg- published recommendations are conserva-
nant humans. tive, recognizing that the benefits of mater-
The increased weight in pregnancy and nal recreational exercise for the fetus are
the increase in metabolically active fetopla- probably miminal and the potential risks un-
cental tissue results in higher pulse, cardiac known.
output, and oxygen uptake at rest and at sim-
ilar external workloads during pregnancy,
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CHAPTER 11

Menopause*
MORRIS NOTELOV1TZ, M.D., Ph.D., and MONA M. SHANGOLD, M.D.

MENOPAUSE IN PERSPECTIVE MUSCLE TISSUE AND STRENGTH


Age-Related Loss of Muscle Tissue
OSTEOPOROSIS AND BONE and Strength
HEALTH Strength Training
Osteogenesis: A Brief Overview
Exercise and Osteogenesis: Clinical OTHER MENOPAUSAL PROBLEMS:
Research VASOMOTOR SYMPTOMS
OTHER AGE-RELATED CHANGES
ATHEROGENIC DISEASE AND
Exercise and Adipose Tissue
CARDIORESPIRATORY FITNESS
Exercise and Osteoarthrosis
Lipids, Lipoproteins, and Exercise
Aerobic Power EXERCISE AND WELL-BEING

MENOPAUSE IN PERSPECTIVE

Menopause is a natural phenomenon that usually lasts about 1 week—the dura-


tion of the last menstrual period. It is the biologic marker of the gradual but per-
sistent decrease in ovarian steroidogenesis that precedes the cessation of men-
struation by about 15 years and that postdates that event by a similar duration.
This period of reproductive senescence is known as the climacteric. The differ-
entiation between "menopause" and the "climacteric" involves more than
semantics, since it serves to illustrate that the midlife physical and psychologic
needs of women extend over a 30-year continuum. There are two additional fea-
tures of note: (1) the attenuation in endocrine function of the ovarian follicle
affects many systems remote from the reproductive tract; and (2) the climacteric
occurs at a time when certain age-related changes become apparent, so that one
must differentiate between biologically induced and chronologically induced
pathophysiology.

*Supported by grants from the National Insti- this chapter, the period is more properly called
tute on Aging R01 AG 00976, Nautilus Sports/ the "climacteric," "menopause" is certainly the
Medical Industries, Inc. more commonly used term.
tAlthough, as discussed at the beginning of
187
188 Developmental Phases

The date of menopause can be accurately terns. The late climacteric is often associ-
pinpointed, but it is a retrospective diagno- ated with conditions resulting from chronic
sis: a year of amenorrhea has to pass before estrogen deprivation—chronic atrophic
the clinical diagnosis can be confirmed. The vaginitis, the urethral syndrome, and uri-
mean age of onset of menopause in western nary incontinence.
societies is 51 years.1 The climacteric may Although the conditions just listed have
be empirically but pragmatically catego- an impact on an individual's quality of life,
rized into three decades of clinical presen- none is life-threatening. There are, however,
tation and need (Fig. 11-1): the early climac- two asymptomatic potential complications
teric (age 35 to 45), premenopausal and of the late climacteric that may have a seri-
postmenopausal periods (age 46 to 55), and ous adverse effect and that are responsible
the late climacteric (56 to 65) .2 Contrary to for much of the morbidity and mortality as-
the theory that follicular depletion is the sociated with older age in women: osteopo-
cause of menopause, primordial follicles are rosis and atherogenic disease. In the United
frequently found in the ovaries of postmeno- States, the total number of hip fractures
pausal women, but they are unable to re- among white women was 158,000 in 1986,
spond to stimulation of the pituitary gonad- and this number is expected to increase to
otropins—FSH and LH. The resultant 252,000 in the year 2020 and to 367,000 by
alteration in ovarian function brings about the year 2040.3 Of this figure, approximately
the dysfunctional uterine bleeding patterns 12% to 20% will die as a result of factors di-
that characterize this phase. As the climac- rectly attributable to their hip fracture.4
teric progresses, the decrease in estradiol Only a third of the survivors will regain nor-
production results in menopause and in a mal activity.5 Of all hip fractures, 70% to 80%
number of so-called hormone-dependent affect women. The total annual cost of hip
symptoms such as hot flushes and changes fractures was approximately $7.2 billion in
in temperament, mood, and sleeping pat- 1984, and this cost, adjusted for 5% inflation,

Figure 11-1. Diagrammatic representation of the menopause as a single event in the larger context
of the climacteric. (From Notelovitz2 with permission.)
Menopause 189

is expected to increase to $240 billion by issue is the fact that bone is a living tissue
2040.3 This cost, of course, does not take into and needs to be treated as such.
account the physical and psychologic pain
suffered by these women.
Osteogenesls: A Brief Overview
In 1989, approximately 500,000 persons
died from ischemic heart disease, the lead- Bone formation depends upon a five-stage
ing cause of death in the United States.6 An- cycle that results in "old" bone being re-
nual health-care costs for cardiovascular moved and replaced with "new" bone. Nor-
disease alone exceed $135 billion, while the mally, this process is coupled; the amount of
added costs of related injury and disability old bone removed is replaced with an equal
exceed $170 billion.7 Cardiovascular disease amount of freshly formed bone. Initiation of
has a significant influence on the well-being the cycle is dependent upon the recruitment
of the fastest-growing age group in the and activation of osteoclasts. This activity
United States: an estimated 1000 individuals usually takes place on the inner aspect of the
join the ranks of the elderly every day.8 A bone's surface—the endosteal layer—and
woman aged 65 can now expect to live an ad- results in the dissolution of bone mineral
ditional 18.8 years (14.5 years for men).9 and collagen, and the formation of a cavity.
Exercise can play an important role in en- Resorption ceases when the mean depth of
suring an appropriate quality of life in mid- the cavity reaches 60 um (trabecular bone)
dle age and later, but to be maximally effec- and 100 urn (cortical bone) from the sur-
tive, it needs to be introduced as a face.11 At this point, mononuclear cells lay
premenopausal lifestyle—hence the em- down a highly mineralized, collagen-poor
phasis on recognizing the climacteric as an bone matrix known as cement substance. It
important transitional phase in the patho- is from this surface that new bone is laid
genesis of potentially preventable disease. down by osteoblasts. These cells probably
originate from bone marrow stromal cells
(preosteoblasts), thereby sharing the abil-
ity of another cell type, the fibroblasts, to
OSTEOPOROSIS AND BONE synthesize collagen.11 The stimulus for os-
HEALTH teoblast recruitment may be mechanical
owing to humoral and/or locally produced
Osteoporosis is preventable. It is a con- substances (for example, human skeletal
dition that is relatively uncommon in men growth and other bone growth factors).12
and in black women, owing in part to their The osteoblasts are responsible for the
having a greater bone mass. Cohn and co- synthesis of collagen, which is the main
workers10 examined the skeletal and muscle component of newly formed bone matrix, or
mass of normal black women and found that osteoid. The latter matures and is later min-
their total body calcium was 16.7% higher eralized by a process that largely depends
than that of age-matched white women. on an adequate supply of calcium and phos-
More than half of this difference (9.7%) was phate and the formation of hydroxyapatite
calculated to be due to a greater muscle crystals.10 At a microstructural level, numer-
mass in the black women. Thus, despite the ous small crystallites of hydroxyapatite may
complexity of bone physiology, two practi- be seen in intimate juxtaposition and in
cal issues need to be addressed: (1) women' highly organized geometric arrangements
need to acquire as much bone as possible with collagen fibrils.11
before menopause, and (2) the rate at which The elastic and tensile strength of bone
bone is lost thereafter needs to be modu- depends in large measure on this interrela-
lated. Exercise plays a pivotal role, in that it tionship. Another very important determi-
is one of the few known means of stimulating nant of the mechanical strength of bone is
new bone formation. Central to the entire the orientation of the collagen fibrils in the
190 Developmental Phases

bone matrix and the three-dimensional net- rangement of vertical and horizontal trabec-
work of plates and bars found especially in ulae (Fig. 11-2). Interruption of this support
trabecular bone (such as vertebrae), and to system—for example, loss of horizontal tra-
a lesser extent in cortical bone (for example, beculae as a result of aging—can impair the
the radius), resulting in a scaffoldlike ar- structural integrity of the bone and result in

Figure 11-2. Scanning electron micrograph of an iliac crest biopsy from (A) a normal subject auu
(fi) a woman with osteoporosis. Contrast the normal contiguous vertical and horizontal trabeculae
with the thinning decreased number and loss of continuity of the trabecular plates in osteoporosis.
(From Dempster DW, et al: A simple method for correlative light and scanning electron microscopy
of human iliac crest bone biopsies: Qualitative observations in normal and osteoporotic subjects. J
Bone Min Res 1(1):15, 1986, with permission.)
Menopause 191

fracture, even in the presence of a relatively 30 years from age 50 to age 80.13 Trabecular
normal amount of bone mineral.13 This is an bone accrual reaches its maximum during
important consideration when prescribing the mid to late 20s and is followed thereafter
exercise for older women. by a linear loss of bone.15 Others maintain
that the trabecular bone loss pattern equals
that of cortical bone, with a loss of at least
Types and Rates of Bone Loss
0.19% per year before menopause and at
As mentioned above, there are two types least 1.1% thereafter. Thus an estimated
of bone: cortical and trabecular. Cortical 31.7% of trabecular bone is lost during the
(compact) bone is found primarily in the ap- 50-year span between 30 and 80 years of
pendicular skeleton (for example, in the age.13 The greater the bone mineral content
femur, tibia, and fibula of the lower limbs, at bone mass maturity (maximum), of
and in the humerus, ulna, and radius of the course, the more an individual can afford to
arms). Cortical bone constitutes 80% of the lose, so there is a need to focus on the ac-
total skeleton but is metabolically less ac- crual of bone during youth rather than on
tive than trabecular bone. About 10% of the the treatment of a reduced bone mass in the
cortical bone is remodeled each year. postmenopausal period.
Trabecular (cancellous) bone is found in
the axial skeleton, primarily in the vertebral
How to Acquire More Bone
bodies (70% to 95%), with lesser concentra-
tions in areas such as the neck of the femur Mechanical force plays an important role
(25% to 35%) and the distal radius (5% to in bone formation and function, but it is not
20%). The remodeling process is far more known how much exercise is needed and
active in trabecular bone, in part because whether there is an optimal form of exercise
the architectural arrangement of the bone for bone accrual. It has been postulated16
plates provides a larger exposed surface that there is a physiologic "band" of activity
area for exchange with the extracellular that is site-specific: immobilization can lead
compartment. Approximately 40% of trabec- to severe bone loss at some sites, whereas
ular bone is remodeled each year. Because repeated loading at appropriate strain mag-
of this greater activity, vertebral osteopo- nitudes can result in bone hypertrophy. The
rosis occurs more frequently than hip (cor- frequency and degree of activity is impor-
tical-related) fractures. It may also account tant: repeated and prolonged exercise
for the increased susceptibility of the ver- causes bone fatigue and microscopic frac-
tebrae to the bone mineral loss noted in fe- tures.16 Given appropriate intervals between
male long-distance runners.14 periods of exercise, however, normal bone
After longitudinal bone growth has been turnover will repair these microfractures
completed, the bone mineral content and and even strengthen the bone.16 Excessive
mass of bone further increase until about activity is known to have an adverse effect,
the age of 35 years, at which point the indi- with stress fractures a common reality in
vidual is said to have achieved her maximal long-distance runners.16
cortical bone mass. From this age until the Gravity. Bone mineral is lost with the in-
onset of menopause, it is considered normal activity of simple bed rest. The average rate
for women to lose