ARTICLE
Sympathetic
such as increase of venous return and myocardial contrac-
tility44. Furthermore, maximum O2 uptake, both absolute,
and gender and age-related, is an important longevity fac-
tor, i.e., the higher the aerobic conditions of an individual,
the smaller his/her mortality risk3,45,46 (table 1). These ad-
justments of HR behavior from aerobic training may also
Rest Submaximal Maximal be due to changes in the sympathetic-vagal balance or in-
Exercise Exercise
trinsic adaptations, such as improvement in the atrioven-
Fig. 1 Heart rate autonomic control at rest and at exercise. Parasym- tricular conduction system47. Some studies suggest that the
pathetic role decreases when intensity of exercise is increased, and the mere practice of physical exercises is not enough to effec-
opposite happens with the sympathetic role. tively decrease mortality risk, being necessary that the train-
ing program be capable of promoting adjustments in both,
the individuals aerobic condition3,45,46 and the autonomic
the effect of pharmacological block20-22, and is almost ex- function48.
clusively mediated by vagal inhibition, with no significant It remains unclear if the improvement of the aerobic con-
sympathetic role20, partly from different times of latency dition from training enhances cardiac vagal tone, thus rest-
from the two branches to this physiological stress. ing-HR variability. Therefore, the purpose of this review is
HR variability was originally studied by Hon and Lee23 to discuss the effects of aerobic training on the autonomic
in newborns, and has been the target of many researches nervous system to control resting HR, and in the initial and
over the past few years. At a search with the key word heart
rate variability on MedLine, there were over 6,000 refer-
ences, 32% between the years 1999 and 2002, showing a
TABLE 1
raising interest on the theme within the academic/scientif-
Mortality relative risk according to aerobic condition
ic fields. HR variations or variability can be measured within
the time and frequency domains, with specific protocols Aerobic RR
for each domain24-30, even with specificity enough for an condition* (CI 95%)
isolated assessment of cardiac vagal tone (parasympathet-
ic branch) in the transition from rest to dynamic exercise20. Laukkanen et al., 2001 > 10.6 1.0 (ref)
(asymptomatic individuals) 9.3-10.6 0.71-3.01
A reduction of the cardiac vagal tone, thus of HR vari-
7.9-9.2 1.44-5.39
ability, regardless of the measuring protocol, is related to < 7.9 2.02-7.32
autonomic dysfunction, chronic-degenerative diseases, and
increased mortality risk31-37, thus representing an impor- Kavanagh et al., 2002 < 4.2 1.0 (ref)
(individual with 4.2-6.3 0.54-0.71
tant indicator of health status38,39. An isolated decrease of cardiovascular disease) > 6.3 0.33-0.47
HR variability reflects a two- to five-fold increase in the
relative mortality risk due to a cardiac event33,40; when as- Myers et al., 2002 1.0-5.9 3.0-6.8
(asymptomatic individuals) 6.0-7.9 1.5-3.8
sociated to a significant decrease of baroreflex sensitivity 8.0-9.9 1.1-2.8
(< 3 ms/mmHg), this relative risk may reach a 7-fold in- 10.0-12.9 0.7-2.2
crease33. On the other hand, in individuals with congestive > 13.0 1.0 (ref)
heart failure, even small increases in HR variability indi-
Myers et al., 2002 1.0-4.9 3.3-5.2
ces, such as standard-deviation of normal RR intervals (time (individuals with 5.0-6.4 2.4-3.7
domain), may decrease mortality risk in up to 20%32. For cardiovascular conditions) 6.5-8.2 1.7-2.8
this reason, and for its predominance on resting, cardiac 8.3-10.6 1.4-2.2
vagal activity has been addressed in a number of trials, > 10.7 1.0 (ref)
especially when it relates to physical activity. * Aerobic condition measured in METs.
Today, at the light of science, one cannot deny that aero- RR: Relative risk for cardiovascular mortality.
ref.: Value of reference.
bic training leads to improvement in the maximum oxygen
114 Rev Bras Med Esporte _ Vol. 9, N 2 Mar/Abr, 2003
final exercise transients, i.e., the potential of aerobic train- EFFECTS ON EXERCISE-HR
ing in inducing physiological changes of the cardiac vagal As previously discussed, HR behavior during the exer-
tone. cise is mediated by ANS. HR variability is the oscillation in
This review was based primarily on original studies in time between consecutive myocardial contractions (systo-
humans of different medical and physical conditions (lev- les)23.
els of physical activity) ranging from individuals with se- Studies with selective pharmacological block22 showed
vere heart conditions, even heart-transplanted subjects, to the exclusive role of the vagus nerve in HR response at the
healthy, but sedentary individuals to high-performance ath- initial transient of the exercise20,21, with predominance of
letes. the vagal activity at rest that is gradually inhibited at sub-
maximal exercise63 both active and passive64-66, up to the
EFFECTS ON RESTING-HR maximum level of exercise, when parasympathetic activi-
A low resting HR reflects a good health condition, where- ty is apparently totally inhibited67, causing smaller or ab-
as higher values are apparently related to a higher mortal- sence of HR variability.
ity risk49. A mistake often made in sports area is to use In the initial seconds of the exercise, HR increases due to
resting-HR as an indicator of the degree of aerobic condi- inhibition of vagal activity, which not only increases atria
tioning, since the association between low resting-HR and contractility, but also conduction velocity of the ventricle
maximal aerobic power is quite modest, and may be due to depolarization wave from AV node62, regardless of the lev-
higher resting vagal activity50, reducing diastolic depolar- el of intensity of the exercise68,69 and aerobic conditioning
ization rate and prolonging duration of the cardiac cycle, of healthy individuals70,71. On other hand, an individual who
primarily on account of a proportionally longer diastole13. does not elevate significantly his/her HR in the beginning
However, can training induce higher resting vagal activity, of the exercise, may be signalizing an impaired vagal ac-
and therefore be accountable for lower resting-HR? tivity72. After this initial stage, as one goes on exercising,
Studies suggest that well-trained or physically well-fit HR increases again, due to adrenergic overstimulation on
(aerobically) individuals present a lower resting-HR, sug- sinus node, or due to increase of serum norepinephrine, or
gestive of higher parasympathetic activity51-55 or lower sym- atrial mechanics distention and therefore, sinus node dis-
pathetic activity56. However, except for the later, a cross- tention due to a higher venous return, and the increase in
sectional analysis does not allow us to conclude that training bodys temperature and bloods acidity73.
was responsible for such adjustment on the ANS. These stud- While Tulppo et al.74 and Goldsmith et al.75 relate de-
ies did not take into consideration the level of aerobic con- crease of HR variability to age, in face of decreased physi-
ditioning and the autonomic function of athletes prior to cal fitness from aging, and that this could be reverted by
training; by knowing that there is an important genetic in- maintaining or improving aerobic physical condition, re-
fluence in determining HR variability57, one could specu- sults from Migliaro et al.76 and Byrne et al.77 suggest that
late that those individuals could have better cardiovascular age alone could be the main factor to decrease autonomic
adjustment upon training for having a better prior cardiac modulation, regardless of aerobic fitness.
vagal tone58. Uusitalo et al.59 and Bonaduce et al.60, after The increase in maximal O2 uptake through aerobic train-
longitudinal studies, noted a reduction of resting-HR, even ing can lessen the age-related decrease of baroreflex sensi-
though significant changes in autonomic indicators were tivity78,79. A program of mild-intensity exercises would be
not seen. Exercise-induced bradycardia can also be due to enough to show some improvement in the autonomic func-
intrinsic adaptation of the sinus node61. tion of healthy adults80 or those with chronic heart fail-
A lower resting-HR can also be consequence of other ure81, even without direct training supervision82; changes
factors derived from a training program60, such as the in- on vagal activity caused by physical training would be cen-
crease of venous return and systolic volume. With the im- tral, possibly directly on baroreflex, whereas the sympa-
provement of the venous return, there is an increase in the thetic activity would be primarily related to peripheral
systolic volume, and according to Frank-Starling law, when changes (vasoconstriction)82. These changes can be seen
there is an increase in the volume of blood in its cavities, already in the first weeks of training in individuals with
there is an increase in heart contractility62. To keep resting- coronary heart disease83 and post-myocardial infarction
heart output constant, there is a decrease of HR in response (MI)84,85. Even though Seals et al.86 have suggested that such
to a higher systolic volume, and these adaptations are ex- improvements should be further evidenced in individuals
pected in individuals with better aerobic conditioning62, re- with abnormal cardiac function, believing that aerobic train-
gardless of their autonomic function. However, will train- ing would have a smaller impact on HR variability of healthy
ing effects on cardiorespiratory variables also modify ANS? individuals, Melanson and Freedson87, Stein et al.88, Al-
Rev Bras Med Esporte _ Vol. 9, N 2 Mar/Abr, 2003 115
Ani et al.89, and Gallo Jr et al.90 reached significant out- EFFECTS ON HR POST-EXERCISE RECOVERY
comes with training on autonomic markers of healthy in-
Another very important aspect addressed by the litera-
dividuals, and Levy et al.91 further suggest that these gains
ture over the last few years is post-exercise, maximal95-97
would not be age-dependent. In spite of the different meth-
and submaximal98-100 HR recovery. HR behavior at the final
odologies used, and the fact that time of effective training
transient of the exercise is another indicator of vagus nerve
had ranged from six weeks to 12 months, the results were
integrity. HR fall at the end of the exercise does not replace
consonant, showing an increase in vagal activity due to an
other measurements of cardiac autonomic activity, but it is
exercise program, or even a decrease in resting sympathet-
a remarkable complement to a medical and/or physical as-
ic activity, which aid to hemodynamic improvements56,92.
sessment of an individual101.
Duru et al.93 were not successful in investigating posi-
tive effects of the regular physical exercises in the auto- At the end of the exercise, special attention should be
nomic function of post-MI individuals when compared to paid to HR behavior, as its lowering less than 12 beats per
sedentary matches, as, although resting-HR being lower after minute (bpm) if return to rest is active97 or 18 bpm if pas-
training, variability indices (in frequency domain) are not sive, in the supine position102, at the first recovery minute
significantly altered. On the other hand, in the control group, after a maximum-exercise test, represents an unfavorable
there was a significant decrease of these indices, showing prognosis for relative-risk of cardiovascular mortality in
an advanced stage of autonomic imbalance in favor of a asymptomatic individuals and cardiopaths95,97,102, i.e., for
sympathetic preponderance in individuals with post-MI left both initial and final transient, the smaller the HR varia-
ventricular dysfunction. These results can be interpreted tion, the higher the relative risk.
in another way: the regular practice of physical exercises This stage of the exercise has been intensively investi-
can, at least, maintain sympatho-vagal balance under para- gated over the last few years, but results still differ as to
sympathetic predominance in post-MI individuals, where- the necessary time for total restore to post-exercise ANS
as sedentarism tends to increase sympathetic influence, even resting levels. The time for HR to fall to resting levels de-
at rest. Other studies also failed in finding differentiated pends on the interaction among autonomic functions, the
adaptations of ANS to a program of exercises. Loimaala et level of physical fitness103,104, and also on the intensity of
al.94 did not find differences on variability indices of ap- the exercise68,105. Recovery can take one hour after light or
parently healthy sedentary individuals with age ranging moderate exercise105, four hours after long-duration aero-
from 35 to 55 years, after 5 months of training, even at bic exercise106, and even up to 24 hours after intense or
night, when sympathetic activity is quite decreased and maximal exercise107. The mechanisms responsible for such
there is less interference of other variables, with improve- discrepancies as to the time needed for total HR post-exer-
ment on resting-HR only, probably due to intrinsic adapta- cise recovery are not fully clear, and the following expla-
tions. nations are currently considered as the most plausible: de-
On the other hand, another interesting aspect is that creased vagal activity105,108-110, sympathetic overactivity107,111
Boutcher and Stein58 have observed that individuals with or even increase in the activity of both ANS branches, re-
better cardiac vagal tone respond better to an aerobic train- covering balance with slight vagal predominance25. Five
ing, with higher gains in maximum oxygen uptake, and minutes after a moderate to intense exercise session, se-
further decreasing resting-HR. Confirming the last studies, rum norepinephrine is still higher than when in rest 110, sug-
Uusitalo et al.59 e Bonaduce et al.60, after investigating ef- gesting higher sympathetic activity at this stage. However,
fects of high aerobic performance training on autonomic one must take into account a latency time of about 2.5 min-
modulations of young athletes, did not find differences, utes for serum norepinephrine to reach its peak112, leading
neither for males nor females. It is possible that some chang- us to wonder that the five-minute recovery time of this study
es in ANS activity, due to training, are observed only as a could be too short. It seems that with aging, the time to
response to a stimulus, such as changes in posture or dur- norepinephrine be removed from the blood is slower, and
ing exercise, but not in rest85,90, as in most protocols. One cardiac rhythm remains faster for a longer time after the
cannot state that failure in finding differences in autonom- exercise. The decrease of post-exercise norepinephrine con-
ic functions due to training is due to measuring in rest, centration comes along HR decrease, but there is indica-
without taking into account the possibility of a ceiling-ef- tion that at the beginning of recovery, vagal modulation is
fect of ANS activities, which could justify the mere main- primarily responsible for HR fall69,110.
taining of the magnitude of sympathetic and parasympa- Heart-transplanted individuals have a significantly slower
thetic influences on HR variability after training period in HR recovery at the first minute post-exercise when com-
athletes or physically very well-fit individuals. pared to apparently healthy individuals113, endorsing the
116 Rev Bras Med Esporte _ Vol. 9, N 2 Mar/Abr, 2003
idea from Perini et al.110. Physical training can increase the Apparently, aerobically well-fit individuals present a
delta between HR at the end of the exercise and at the be- more effective autonomic activity than sedentary ones, and
ginning of recovery, and eight weeks of training would be there is indication that individuals with better cardiac va-
enough to augment this difference within the first 30 sec- gal tone have a better response to aerobic training, which
onds post-exercise114, with no differences in outcome for lead us to question whether aerobically well-fit athletes have
gender or age group115; however, such adaptation may be a higher cardiac vagal tone due to training or those indi-
lost in few weeks without training79,114. In children, recov- viduals with genetically higher cardiac vagal tone have a
ery may be faster than in young adults due to their higher higher potential to become elite athletes if properly trained.
central cholinergic modulation116; there are differences for Certainly, the large variety of HR measuring methods,
elders as well, in whom decrease of post-exercise serum and the features and peculiarities of the samples and the
norepinephrine takes longer117. Apparently, the time for total outlines used in each trial, have added to differences among
restoration of ANS activities is inversely related to the max- the results and their interpretations as to the effects of ex-
imum level of O2 uptake55,106, in spite of Arai et al.63 not ercise and training on parasympathetic ANS and HR con-
having found evidences in their results that indicated dif- trol.
ferences in variables such as: gender63,118, position of sub- In spite of the need of other studies on immediate and
ject on recovery (seated or supine), and level of physical late acute effects, and chronic effects of physical exercise
activity among healthy individuals63. When healthy indi- on the autonomic nervous system, especially of the para-
viduals were compared to heart-failure or heart-transplanted sympathetic component, identifying possible changes on
individuals, the former required shorter time for post-max- the cardiac vagal tone, some conclusions could be reached.
imal exercise HR recovery; notwithstanding, HR variability
measured under frequency domain at the peak of the exer- REFERENCES
cise did not show differences among the groups, probably
a sign of complete inhibition of vagal activity at this stage67. 1. Blair SN, Kohl 3rd HW, Barlow CE, Paffenbarger RS, Gibbons LW, Mac-
era CA. Changes in physical fitness and all-cause mortality. A prospec-
The groups of heart-failure and heart-transplanted individ- tive study of healthy and unhealthy men. JAMA 1995;273:1093-8.
uals had reduced their HR less than 10 bpm at the begin-
2. Centers for Disease Control. Coronary heart disease attributable to sed-
ning of the recovery stage, which is compatible to a prob- entary life-style selected states, 1988. JAMA 1990;264:1390-2.
able autonomic dysfunction and related to a high mortality 3. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Ex-
risk95-97. ercise capacity and mortality among men referred for exercise testing. N
Engl J Med 2002;346:793-801.
CONCLUSIONS 4. Willians PT. Physical fitness and activity as separate heart disease risk
factors: a meta-analysis. Med Sci Sports Exerc 2001;5:754-61.
As discussed in this review, HR variability has been stud- 5. Erikssen G, Liestol K, Bjornholt J, Thaulow E, Sandvik L, Erikssen J.
ied at a number of trials over the last few years, especially Changes in physical fitness and changes in mortality. Lancet 1998;352:
759-62.
its relation to a higher risk of cardiovascular mortality, a
6. McGinnis JM, Foege WH. Actual causes of death in the United States.
common finding in many of these trials. Vagal nerve activ- JAMA 1993;270:2207-12.
ity (parasympathetic branch) is considered to be a cardio- 7. Pearson TA, Blair SN, Daniels SR, Eckel RH, Fair JM, Fortmann SP, et
vascular protection factor; therefore, ANS dysfunction, par- al. AHA guidelines for primary prevention of cardiovascular disease and
ticularly reduction of the cardiac vagal tone, translates in a stroke: 2002 update. Consensus panel guide to comprehensive risk re-
significant increase of cardiovascular mortality risk. It is duction for adult patients without coronary or other atherosclerotic vas-
cular diseases. Circulation 2002;106:388-91.
not clear if the regular practice of physical exercise can
8. Kraus WE, Houmard JA, Duscha BD, Knetzger KJ, Wharton MB, Mc-
significantly increase ANS function, as shown by some ev-
Cartney JS, et al. Effects of the amount and intensity of exercise on
idences. Perhaps some of the changes that take place in plasma lipoproteins. N Engl J Med 2002;347:1483-92.
HR control at rest and at exercise submaximal levels are 9. Paffenbarger RS, Lee IM. Physical activity and fitness for health and
consequence of intrinsic adaptations of the sinus node, or longevity. Res Q Exerc Sport 1996;67:11-28.
derived from other physiological changes, such as the in- 10. Manson JE, Hu FB, Rich-Edwards JW, Colditz GA, Stampfer MJ, Wil-
crease of venous return and systolic volume, and improved lett WC, et al. A prospective study of walking as compared with vigor-
myocardial contractility; or peripheral, such as improved ous exercise in the prevention of coronary heart disease in women. N
Engl J Med 1999;341:650-8.
oxygen extraction (oxygen arteriovenous difference) or en-
11. Manson JE, Greenland P, LaCroix AZ, Stefanick ML, Mouton CP, Ober-
hanced O2 use to generate more work (mechanical efficien-
man A, et al. Walking compared with vigorous exercise for the preven-
cy), causing HR to reduce to those (submaximal) required tion of cardiovascular events in women. N Engl J Med 2002;347:716-
levels. 25.