Prova Decon He C I Mentos

A long-term pulmonary rehabilitation program
progressively improves exercise tolerance, quality of life

and cardiovascular risk factors in patients with COPD
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L. F. F. REIS 1, 2, F. S. GUIMARES 3, 4, S. J. FERNANDES 2

L. A. CANTANHEDE 2, C. M. DIAS 3, 5, A. J. LOPES 3, 6, S. L. S. DE MENEZES 3, 4
Background. Support and treatment options have

been widely discussed in recent decades with the
aim of improving morbidity, mortality and quality of
life of chronic respiratory disease (COPD) patients.
Although it is believed that longer pulmonary rehabilitation programs can provide better results, most of
the evidence comes from short-term programs.
Aim. To determine the effects of an outpatient pulmonary rehabilitation program on exercise tolerance,
dyspnoea, hemodynamic variables and quality of life.
Design. Case series study.
Setting. Rehabilitation Centre.
Population and Methods. A convenience sample of
COPD patients was enrolled in this study. The intervention consisted of a 96-wk exercise training program, including aerobic training, upper-limb exercises
and inspiratory muscle training. Pulmonary function
tests, blood biochemistry, six-minute walking distance
test and health-related quality of life were recorded at
baseline and after completion of the 6th, 12th, 18th,
24th months.
Results. Forty one consecutive COPD patients were recruited and thirty six completed the study. There was
a significant improvement in hemodynamics, demonstrated by the gradual reduction in heart rate, blood
pressure and MvO2 (double product) starting from the
12th month. Lipid profile showed a reduction of low
density lipids and an increase of the high density lipids levels starting from the 6th month. Exercise tolerance, dyspnoea, respiratory muscle strength and quality of life also improved starting from the 6th month.
Conclusion. A 24-month pulmonary rehabilitation
program leads to a progressive improvement in quality of life, dyspnoea and exercise tolerance, and reduc-
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EUR J PHYS REHABIL MED 2013;49:491-7
Corresponding author: S. Lcia Silveira de Menezes, Programa de

Ps-Graduao em Cincias da Reabilitao, Praa das Naes 34,
Bonsucesso, Rio de Janeiro, 21041-021, Brazil.
E-mail: smenezes@unisuam.edu.br
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1Physical
Therapy School, Augusto Motta University Centre

(UNISUAM), Rio de Janeiro, Brazil
2Rehabilitation Centre of Rio de Janeiro Military Police
Rio de Janeiro, Brazil
3Rehabilitation Science Graduate Program, Augusto Motta
University Center (UNISUAM), Rio de Janeiro, Brazil
4Physical Therapy School, Federal University of Rio de
Janeiro, Rio de Janeiro, Brazil
5Physical Therapy Service, Brazilian Air Force Hospital
(HFAG), Rio de Janeiro, Brazil
6Laboratory of Respiratory Physiology, University of the
State of Rio de Janeiro, Rio de Janeiro, Brazil
es cardiovascular risk factors in patients with chronic

obstructive pulmonary disease.
Impact. Our study suggests that long-term pulmonary
rehabilitation programs can result in further improvements in the aforementioned cardiorespiratory variables.
Key words: Pulmonary disease, chronic obstructive - Exercise - Cardiovascular system - Quality of life.
hronic obstructive pulmonary disease (COPD)

is characterized by airflow limitation that is not
fully reversible and a range of pathological changes
in the lung, some significant extrapulmonary effects and important chronic comorbidities (e.g., cardiovascular disease, musculoskeletal impairment,
diabetes mellitus and metabolic syndrome).1 The
chronic airflow limitation is caused by a combination of small airways disease and parenchymal destruction, usually both progressive and associated
with an abnormal inflammatory response of the
lungs to noxious particles or gases.1 This disease
EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE
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Long-term pulmonary rehabilitation on COPD
is the fifth leading cause of global morbidity 1, 2

and a major public health problem. Support and
treatment options have been widely discussed in
recent decades with the aim of improving morbidity, mortality and quality of life of COPD patients.
Currently, the clinical management of these patients
includes the use of long-term beta2 agonists and
anticholinergics, the continuous use of inhaled corticosteroids, as well as the participation in pulmonary rehabilitation programs. These procedures are
evidence-based, showing that the clinical guidelines represent a valuable advance in comprehensive care of patients with COPD.1, 3
In this way, pulmonary rehabilitation has been advocated as a way to improve the functional status of
patients with chronic respiratory diseases.4 Patients
who are candidates for pulmonary rehabilitation
have respiratory impairment, defined as an underlying pathophysiologic defect that gives rise to a disability. Therefore, the goals of pulmonary rehabilitation are to alleviate symptoms, restore functional
capabilities as much as possible, and the
improvement in participation restriction, thus enhancing
overall quality of life.5, 6 The essential components
include exercise training, respiratory muscle training, education, other possible interventions, and
outcomes assessment.5
Many patients with COPD are limited in their
physical activity by dyspnoea. Lung hyperinflation,
increased dead space ventilation, and increased energy consumption during hyperpnoea lead to decreased ventilatory reserve and dyspnea on exertion.7, 8 Some subjects with COPD have decreased
maximal respiratory pressures 9-11 which indicate
respiratory muscle weakness and may contribute to
the perception of dyspnoea. If an adequate training
stimulus is applied, it is possible to improve the respiratory and peripheral muscle function, and, thus,
the exercise performance,12, 13 dyspnoea 13, 14 and
quality of life.5, 15-17
Although it is believed that longer pulmonary
rehabilitation programs can provide better results,18 most of the evidence comes from shortterm programs. Since there are few studies addressing the impact of long-duration programs in
clinically relevant outcomes, the purpose of this
study was to determine the effects of an outpatient pulmonary rehabilitation program on exercise tolerance, dyspnoea, hemodynamic variables
and quality of life.
Materials and methods

Patients
This was a case series study, using a convenience
sample of patients diagnosed with COPD who were
referred to the Military Police Rehabilitation Centre
in Rio de Janeiro, Brazil. All patients classified as
severe or very severe 1 were eligible to participate in
this study. According to the Helsinki declaration, the
protocol was approved by the 40th Ethics Committee
(process: CAAE 0003.0.307.000-10) and written informed consent was obtained from all participants.
Patients were not included if any of the following
criteria was present: informed consent could not be
obtained, history of respiratory infection in the last
four weeks preceding the study, diagnosis of other diseases contributing to dyspnoea and exercise
limitation, history of coronary artery disease (CAD),
disorders of the musculoskeletal system incompatible with exercise program, cognitive impairment
or inability to perform the tests and the exercise
program. Patients who did not show adherence to
the program and/or presented any acute episode of
disease exacerbation were excluded from the study.
At the beginning of the study, none of the subjects
were current smokers and only six patients had total
cholesterol levels above 239 mg/dL. These patients
maintained their current dietary counselling during
the period of the study, without using lipid-lowering
drugs. No patients presented with low-density lipoprotein cholesterol higher than 159 mg/dL.
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Intervention
The intervention consisted of a 96-week exercise

training program, including aerobic training, upperlimb exercises and inspiratory muscle training. Airway clearance techniques were applied prior to the
exercises sessions when needed, and consisted of
positive expiratory pressure therapy (PEP) or oscillating positive pressure (Flutter VRP1 - Scandipharm
International, Powys, UK). A specialized and experienced physiotherapist closely supervised all exercise sessions, which were conducted three times
a week. Aerobic training consisted of 30 min in a
cycle ergometer (Movement, magnetic 2500 electronic model, So Paulo, Brazil) or treadmill (Movement RT 250 GII, So Paulo, Brazil). Initial training
intensity was set at 50-65% of the baseline maximal
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The domains Social Functioning, Health Perceptions, and Life Satisfaction were assessed using
questions from the Medical Outcomes Study 36-item
short-form healthy survey (SF-36).29 Disease-specific
health-related quality of life was assessed by means
of the Airways Questionnaire 20 (AQ-20) 30-32 in nine
patients. The respective validated Brazilian versions
were administered by a trained physiotherapist.
Statistical analysis
Statistical analysis was performed on SigmaStat
Program for Windows (version 3.0, Jandel Scientific,
CA, USA). The normality of the data (KolmogorovSmirnov test with Lilliefors correction) and the homogeneity of variances (Levene median test) were
tested. Then, the data were compared using One
Way Repeated Measures ANOVA or Friedmans
ANOVA on Ranks, followed by Tukeys test. The results were expressed as mean standard deviation
(SD) and the level of significance was set at 5%.
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workload for ergometer cycling and at 70% of the

average walking speed during the baseline 6MWT
for treadmill walking. Moreover, during the exercise
sessions the degree of perceived exertion was assessed using a modified Borg Scale, and the load
was adjusted according to a 3-4 (moderatesomewhat hard) score.19 Upper-limb exercises were performed using lifting of weights that allowed three
sets of twelve repetitions of biceps curls, triceps extension, shoulder flexion, shoulder abduction, and
shoulder elevations. There was a 20-s rest period
between the exercise sets. After upper limb exercises the patients trained with a threshold loaded
breathing device (ThresholdTM IMT; Respironics
HealthScan, NJ, USA) during 30 min. The load was
adjusted according to 25% of maximal inspiratory
pressure (MIP), with progressive increases as tolerated up to 40% of the initially measured MIP. The
goal was to have all patients training at 40% of MIP
during the second month of training. The intensity
was reviewed monthly for aerobic, upper-limb and
inspiratory muscle training.
Results
Outcome measurements
Pulmonary function tests, blood biochemistry,

six-minute walking distance test and health-related quality of life were recorded in a standardized
manner and sequence before starting the training
and after completion of the 6th, 12th, 18th, 24th
months.
Blood samples were collected and analysed at our
institutional clinical laboratory. Forced spirometry,
body plethysmography, and single-breath diffusing
capacity were performed according to the American
Thoracic Society (ATS) recommendations 20-22 using
a Collins Plus pulmonary function testing system
(Warren E Collins, Braintree, MA, USA). Maximal inspiratory and expiratory pressures (MIP and MEP)
were measured with an analogical manometer (Instrumentation Industries, PA, USA) according to the
method previously described.23 Exercise tolerance
and work rate were assessed by the six-minute walking distance test following international standards.22,
24-28 The variables heart rate, arterial blood pressure,
MVO2 (heart rate X systolic arterial pressure) and
peripheral oxygen saturation were also measured at
rest. A digital oximeter (Onyx 9500, Nonin Medical,
MN, USA) was used to measure heart rate (HR) and
peripheral oxygen saturation (SpO2).
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From June 2002 to September 2010, 41 consecutive COPD patients who were admitted in our pulmonary rehabilitation program agreed to participate
in the study. Five patients were excluded because
of low-adherence (N.=3) and disease exacerbation
(N.=2). Thirty-six patients (14 females and 22 males)
completed the study and all were receiving inhaled
beta 2-agonist agents, 21 patients were receiving inhaled steroids, and 10 patients were receiving tiotropium therapy. Five patients were using continuous
supplemental oxygen during exercise. The pharmacologic treatment during the period of the study was
standardized and followed the GOLD recommendations for all patients.1 Patients were stable at the time
of entry into the exercise program, and none had
clinical evidence of cardiovascular or neuromuscular diseases limiting their exercise capacity. Baseline
characteristics of the patients are presented in Table
I. There were no significant differences in these variables over the time-points of the study.
There was a significant improvement in hemodynamics, demonstrated by the gradual reduction
in heart rate, blood pressure and MvO2 (double
product) starting from the 12th month. Lipid profile
showed reduction of low density lipids and increase
493
Table I.Demographic and baseline functional data.

Variables
N.=36
Age (y)
Female (N. %)
Body mass index (kg/m2)
FEV1 (% predicted)
FEV1/FVC (%)
PEF (Lpm)
SpO2 (%)
RV (% predicted)
TLC (% predicted)
DLCO (% predicted)
61.727.62
14 (39)
23.104.56
35.699.58
64.065.19
196.3961.64
932
15646
11525
7515
of the high density lipids levels starting from the 6th

month (Table II).
Exercise tolerance, dyspnoea, respiratory muscle
strength and quality of life also improved starting
from the 6th month (Tables III, IV).
Discussion
This study demonstrated that a long-term rehabilitation program progressively improves the hemodynamic and lipid profile of COPD patients,
with reduction in heart rate, blood pressure and
MvO2, decrease of low-density lipoprotein cholesterol and increase of high-density levels. Ad-
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Values are meanSD unless otherwise stated, of thirty six patients. BMI:
body mass index; FEV1: forced expiratory volume at one second; FVC:
forced vital capacity; PEF: peak expiratory flow; SpO2: peripheral arterial
oxygen saturation; RV: residual volume; TLC: Total lung capacity; DLCO: diffusing capacity of the lung for carbon monoxide.
Table II.Hemodynamics and blood biochemistry data.

Variables
Pre-training
HR (bpm)
SP (mmHg)
DP (bpm x mmHg)
TOT-CHOL(mg/dL)
HDL-CHOL(mg/dL)
LDL-CHOL(mg/dL)
CASTELLI I
CASTELLI II
TRIGLYCERIDES (mg/dL)
GLYCEMIA(mg/dL)
96.510.4
144.910.6
14027.782127.12
216.723.9
45.714.3
115.917.8
5.11.2
2.70.7
97.810.7
96.48.8
Post-training
6th month
12th month
80.76.5*
131.57.5*
1624.031202.62*
187.217.2*
54.714.0*
104.410.9*
3.60.8*
2.00.5*
84.4 14.2*
85.36.8*
76.17.5*
124.98.8*
9543.751403.81*
170.614.9*
58.913.5*
100.18.5*
3.20.7*
1.80.4*
82.813.1*
84.27.1*
18th month
71.54.4*
117.36.5*
8397.08794.98*
174.116.2*
62.411.2*
93.88.3*
2.90.5*
1.50.3*
80.013.0*
81.27.0*
24th month
68.6 3.1*
112.44.7*
7713.89595.25*
169.919.5*
65.410.4*
91.46.5*
2.70.5*
1.40.3*
75.29.7*
78.56.7*
Values are meansSD of thirty six patients. HR: heart rate; SP: systolic pressure; DP: double product; TOT-CHOL: total cholesterol; HDL-CHOL: high-density
lipoprotein cholesterol; LDL-CHOL: low-density lipoprotein cholesterol. *Statistically different from pre-training; statistically different from 6 months; statistically different from 12 months.
Table III.Exercise tolerance, dyspnea, body mass index and respiratory muscle strength.
Pre-training
6-MINWD (m)
BODE
BMI
BORG SCALE
MIP (cmH2O)
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321.977.1
5.61.6
23.14.6
4.31.0
75.06.6
Post-training
6th month
12th month
18th month
422.678.9*
4.61.3*
21.83.3
2.90.7*
85.08.2*
459.575.1*
483.367.7*
4.11.5*
22.42.7
2.40.5*
90.48.6*
3.31.0*
22.72.3
1.90.7*
93.88.1*
24th month
516.973.9*
3.10.9*
232.1
1.50.6*
105.48.6*
Values are meansSD of thirty six patients. 6-MINWD: distance in the six-minute walk distance test; BODE: multidimensional grading system; BMI: body
mass index; MIP: maximal inspiratory pressure. *Statistically different from pre-training; Statistically different from 6 months; Statistically different from 12
months. Statistically different from 18 months.
Table IV.Outcomes of general health-related (SF-36) and disease-specific quality of life (AQ-20) questionnaires after the exercise
training program.
Pre-training
SF-36
AQ-20
31.09.6
87.85.9
Post-training
6th month
52.611.3*
74.64.5
12th month
18th month
24th month
56.910.4*
69.06.2
62.27.9*
66.87.3*
64.43.9*
74.43.9
SF-36 values are meansSD of 36 patients. AQ-20 values are meanSD of nine patients. *Statistically different from pretraining. Statistically different from 6
months; Statistically different from 12 months.
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cardiovascular diseases.38 Smoking is a major cause

of COPD and cardiovascular disorders, including
coronary heart disease (CHD) and peripheral arterial disease. Smoking-induced inflammation and
other risk factors like dyslipidaemia cause vascular
endothelial damage via oxidative stress, then, a vicious cycle with the characteristics of atherosclerosis ensues.39 Low-density lipids cholesterol (LDLCHOL) reduction is associated with a reduced risk
of cardiovascular disease (CVD), death, myocardial
infarction, revascularization indication, hospitalization for unstable angina, and stroke. The prevalence
of both, CVD and COPD, increases with age and
the likelihood of detecting CVD or modifiable risk
factors for CVD in patients with COPD is high.40,
41 Some authors previously reported that low and
moderate intensity endurance training in sedentary patients suffering from metabolic syndrome
simultaneously improved blood rheology, body
composition and lipid oxidation at exercise.42-44 It
has been demonstrated that, in obese and diabetic
patients, endurance training reduce the levels of
glycemia, heart rate and arterial pressure at rest,
although these variations did not alter the course
of disease.45, 46 In our study, we observed a significant reduction in LDL-C, triglycerides and glycemia
levels associated to the gradual reductions in blood
pressure and heart rate. Although the benefits of
exercise programs for hypertensive, diabetic and
obese patients are well-known,43, 45, 46 the present
study demonstrated that a long-term supervised
program contributes for the decrease in the risk
of cardiovascular disease in COPD patients. Along
to appropriate pharmacological therapy, pulmonary rehabilitation is the only treatment that has
proven to significantly reduce dyspnoea.5, 47 This
reduction is thought to be mediated via decreased
levels of ventilation during submaximal exercise
resulting from training-induced improvements in
aerobic capacity of the skeletal muscles lowering
blood lactate concentration and increased mechanical efficiency of these muscles.48 As in most pulmonary rehabilitation programs, not all patients in
our sample underwent a cardiopulmonary exercise
testing.49 Indeed, measurements of maximal oxygen consumption, anaerobic threshold, heart rate
and ventilatory reserve, oxygen pulse and other
cardiopulmonary variables would be valuable to
identify the factors associated to exercise limitation, and corroborate the cardiovascular and res-
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ditionally, this long-term rehabilitation program

improved exercise tolerance, dyspnoea, respiratory muscle strength and quality of life. Ochmann
et al.(2012) 31 recently published a review on the
benefits of long-term pulmonary rehabilitation programs, including its maintenance, and suggesting,
even with a small degree of evidence, the reduction in morbidity and mortality. Our results are
in agreement with the above study and with the
work of Berry et al.(2003),33 which showed that an
18-month exercise program results in greater improvements in self-reported disability and physical function when compared with a three-month
exercise program. These authors suggested that
long-term exercise programs should be recommended for all patients with COPD. Additionally,
in a recent ATS/ERS Statement, longer programs
were recommended because of its larger and more
endurable training effects.18 Although this recommendation, there are few evidences on the longterm effects of pulmonary rehabilitation, and most
of the programs are based on study results from
short-term programs (4 to 12 weeks). Actually, this
short period has proven to be enough to generate
clinically relevant effects, but from the premise that
exercise programs should be maintained because
benefits disappeared if exercise is discontinued,8
some studies has addressed different post-program
follow-up strategies.6, 34 Many of these studies have
demonstrated that despite different follow-up strategies an expressive number of patients stop doing
exercises after discharge, but longer lasting programs seem to enhance long-term effects.34-38
In our study the exercise program consisted
of aerobic training, upper limb exercises and inspiratory muscle training. A previous study demonstrated that a combination of aerobic training
and strength exercises was safe and well tolerated
despite the severity of lung disease.15 According
to these authors, it is possible that a strength and
aerobic long duration training instead of aerobic
training alone could produce a greater improvement in exercise capacity. Additionally, strength
training results in less dyspnoea during exercise,
being easier to tolerate than aerobic training.15,
18 The prevalence of metabolic syndrome is high
among COPD patients, and is characterized by abdominal obesity, atherogenic dyslipidaemia, raised
blood pressure, insulin resistance, and prothrombotic and inflammatory states that predispose to
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Conclusions
A 24-month pulmonary rehabilitation program
leads to a progressive improvement in quality of
life, dyspnea and exercise tolerance, and reduces
cardiovascular risk factors in patients with chronic
obstructive pulmonary disease.
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piratory functional improvement throughout the

period of the study.
According to Ltters et al., inspiratory muscle
training associated with general exercise reconditioning can generate significant training effects on
inspiratory muscle strength and endurance, mainly
in patients with muscle weakness.49 Additionally,
when the load placed on the respiratory muscles is
sufficient to augment inspiratory muscle strength,
it improves the exercise capacity, quality of life and
dyspnoea.49, 50 There is a significant positive association between the percentage increase in maximum inspiratory pressure (MIP) and the relative
magnitude of the inspiratory muscle training (IMT)
load.51 In this context, it has been described that
to achieve a 20% increase in MIP it is necessary a
load of 30% MIP.49 In our study, the IMT load was
adjusted to 40% of patients MIP, however, as our
protocol included other procedures, even with the
increment observed in inspiratory muscle strength
we cannot attribute the reduction of dyspnoea to
the inspiratory muscle training.16
Since COPD is considered a complex disease
with systemic manifestations (which depend on
the disease phenotype), during the treatment of
these patients it is important to consider different
outcomes to reflect the symptoms relief, functional
status and overall health-related quality of life.6
The American Thoracic Society provided the highest grade of evidence for the health-related quality of life benefits related to pulmonary rehabilitation.18 Our study showed progressive improvement
in quality of life, however, as previously described
6, 32, 35 it is not possible to determine which components of pulmonary rehabilitation are essential,
its ideal length, the required degree of supervision
and intensity of training, and how long the treatment effects persist.
The foremost outcome of our study was the progressive improvement in hemodynamic, biochemical, functional and quality of life related variables
up to a two-year period of treatment. This result
suggests that longer pulmonary rehabilitation programs may be necessary to achieve maximal benefits for COPD patients. Further studies, with longer
follow-up periods and other clinically relevant outcomes, as need for hospitalization and mortality,
are necessary in order to determine the ideal duration, the maintenance of effects and the costs of
long-term pulmonary rehabilitation programs.
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Microcirc 2006;35:333-9.
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Vol. 49 - No. 4
Received on July 30, 2012.

Accepted for publication on January 9, 2013.
Epub ahead of print on March 13, 2013.
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A long-term pulmonary rehabilitation program

progressively improves exercise tolerance, quality of life

L. F. F. REIS 1, 2, F. S. GUIMARES 3, 4, S. J. FERNANDES 2

Background. Support and treatment options have

EUR J PHYS REHABIL MED 2013;49:491-7

Corresponding author: S. Lcia Silveira de Menezes, Programa de

Therapy School, Augusto Motta University Centre

es cardiovascular risk factors in patients with chronic

hronic obstructive pulmonary disease (COPD)

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

Long-term pulmonary rehabilitation on COPD

is the fifth leading cause of global morbidity 1, 2

Materials and methods

The intervention consisted of a 96-week exercise

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

workload for ergometer cycling and at 70% of the

Pulmonary function tests, blood biochemistry,

Long-term pulmonary rehabilitation on COPD

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

Long-term pulmonary rehabilitation on COPD

Table I.Demographic and baseline functional data.

of the high density lipids levels starting from the 6th

Table II.Hemodynamics and blood biochemistry data.

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

cardiovascular diseases.38 Smoking is a major cause

ditionally, this long-term rehabilitation program

Long-term pulmonary rehabilitation on COPD

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

Long-term pulmonary rehabilitation on COPD

piratory functional improvement throughout the

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

Long-term pulmonary rehabilitation on COPD

Received on July 30, 2012.

EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE

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