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American Thoracic Society Documents
An Official American Thoracic Society/European
Respiratory Society Statement: Key Concepts
and Advances in Pulmonary Rehabilitation
Martijn A. Spruit, Sally J. Singh, Chris Garvey, Richard ZuWallack, Linda Nici, Carolyn Rochester, Kylie Hill,
Anne E. Holland, Suzanne C. Lareau, William D.-C. Man, Fabio Pitta, Louise Sewell, Jonathan Raskin, Jean Bourbeau,
Rebecca Crouch, Frits M. E. Franssen, Richard Casaburi, Jan H. Vercoulen, Ioannis Vogiatzis, Rik Gosselink,
Enrico M. Clini, Tanja W. Effing, François Maltais, Job van der Palen, Thierry Troosters, Daisy J. A. Janssen, Eileen Collins,
Judith Garcia-Aymerich, Dina Brooks, Bonnie F. Fahy, Milo A. Puhan, Martine Hoogendoorn, Rachel Garrod,
Annemie M. W. J. Schols, Brian Carlin, Roberto Benzo, Paula Meek, Mike Morgan, Maureen P. M. H. Rutten-van Mölken,
Andrew L. Ries, Barry Make, Roger S. Goldstein, Claire A. Dowson, Jan L. Brozek, Claudio F. Donner,
and Emiel F. M. Wouters; on behalf of the ATS/ERS Task Force on Pulmonary Rehabilitation
THIS OFFICIAL STATEMENT OF THE AMERICAN THORACIC SOCIETY (ATS) AND THE EUROPEAN RESPIRATORY SOCIETY (ERS) WAS
APPROVED BY THE ATS BOARD OF DIRECTORS, JUNE 2013, AND BY THE ERS SCIENTIFIC AND EXECUTIVE COMMITTEES IN JANUARY
2013 AND FEBRUARY 2013, RESPECTIVELY
CONTENTS Lung Volume Reduction Surgery
Lung Transplantation
Overview
Behavior Change and Collaborative Self-Management
Introduction
Introduction
Methods
Behavior Change
Definition and Concept
Operant conditioning
Exercise Training
Changing cognitions
Introduction
Enhancement of self-efficacy
Physiology of Exercise Limitation
Addressing motivational issues
Ventilatory limitation
Collaborative Self-Management
Gas exchange limitation
Advance Care Planning
Cardiac limitation
Body Composition Abnormalities and Interventions
Limitation due to lower limb muscle dysfunction
Introduction
Exercise Training Principles
Interventions to Treat Body Composition Abnormalities
Endurance Training
Special Considerations in Obese Subjects
Interval Training
Physical Activity
Resistance/Strength Training
Timing of Pulmonary Rehabilitation
Upper Limb Training
Pulmonary Rehabilitation in Early Disease
Flexibility Training
Pulmonary Rehabilitation and Exacerbations of COPD
Neuromuscular Electrical Stimulation
Early Rehabilitation in Acute Respiratory Failure
Inspiratory Muscle Training
Physical activity and exercise in the unconscious patient
Maximizing the Effects of Exercise Training
Physical activity and exercise in the alert patient
Pharmacotherapy
Role for rehabilitation in weaning failure
Bronchodilators
Long-Term Maintenance of Benefits from Pulmonary
Anabolic hormonal supplementation
Rehabilitation
Oxygen and helium–hyperoxic gas mixtures
Maintenance exercise training programs
Noninvasive ventilation
Ongoing communication to improve adherence
Breathing strategies
Repeating pulmonary rehabilitation
Walking aids
Other methods of support
Pulmonary Rehabilitation in Conditions Other Than COPD
Patient-centered Outcomes
Interstitial Lung Disease
Quality-of-Life Measurements
Cystic Fibrosis
Symptom Evaluation
Bronchiectasis
Depression and Anxiety
Neuromuscular Disease
Functional Status
Asthma
Exercise Performance
Pulmonary Arterial Hypertension
Physical Activity
Lung Cancer
Knowledge and Self-Efficacy
Outcomes in Severe Disease
Composite Outcomes
Am J Respir Crit Care Med Vol 188, Iss. 8, pp e13–e64, Oct 15, 2013 Program Organization
Copyright ª 2013 by the American Thoracic Society Patient Selection
DOI: 10.1164/rccm.201309-1634ST
Internet address: www.atsjournals.org Comorbiditiese14 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 188 2013
Rehabilitation Setting and frequent comorbidities. Therefore, integrated care principles
Home-based and community-based exercise training are being adopted to optimize the management of these complex
Technology-assisted exercise training patients (2). Pulmonary rehabilitation is now recognized as a core
Program Duration, Structure, and Staffing component of this process (Figure 1) (3). Health behavior change
Program Enrollment is vital to optimization and maintenance of benefits from any
Program Adherence intervention in chronic care, and pulmonary rehabilitation has
Program Audit and Quality Control taken a lead in implementing strategies to achieve this goal.
Health Care Use Noteworthy advances in pulmonary rehabilitation that are
Program Costs discussed in this Statement include the following:
Impact on Health Care Use d There is increased evidence for use and efficacy of a variety
Impact on Medical Costs
of forms of exercise training as part of pulmonary rehabil-
Cost-Effectiveness itation; these include interval training, strength training,
Moving Forward upper limb training, and transcutaneous neuromuscular
electrical stimulation.
Background: Pulmonary rehabilitation is recognized as a core compo-
nent of the management of individuals with chronic respiratory disease. d Pulmonary rehabilitation provided to individuals with chronic
Since the 2006 American Thoracic Society (ATS)/European Respiratory respiratory diseases other than COPD (i.e., interstitial lung
Society (ERS) Statement on Pulmonary Rehabilitation, there has been disease, bronchiectasis, cystic fibrosis, asthma, pulmonary hy-
considerable growth in our knowledge of its efficacy and scope. pertension, lung cancer, lung volume reduction surgery, and
Purpose: The purpose of this Statement is to update the 2006 docu- lung transplantation) has demonstrated improvements in
ment, including a new definition of pulmonary rehabilitation and symptoms, exercise tolerance, and quality of life.
highlighting key concepts and major advances in the field.
Methods: A multidisciplinary committee of experts representing the
d Symptomatic individuals with COPD who have lesser
ATS Pulmonary Rehabilitation Assembly and the ERS Scientific Group
degrees of airflow limitation who participate in pulmonary
01.02, “Rehabilitation and Chronic Care,” determined the overall rehabilitation derive similar improvements in symptoms,
scope of this update through group consensus. Focused literature exercise tolerance, and quality of life as do those with
reviews in key topic areas were conducted by committee members more severe disease.
with relevant clinical and scientific expertise. The final content of this d Pulmonary rehabilitation initiated shortly after a hospital-
Statement was agreed on by all members. ization for a COPD exacerbation is clinically effective,
Results: An updated definition of pulmonary rehabilitation is pro- safe, and associated with a reduction in subsequent hospi-
posed. New data are presented on the science and application of tal admissions.
pulmonary rehabilitation, including its effectiveness in acutely ill
individuals with chronic obstructive pulmonary disease, and in indi- d Exercise rehabilitation commenced during acute or critical
viduals with other chronic respiratory diseases. The important role of illness reduces the extent of functional decline and hastens
pulmonary rehabilitation in chronic disease management is high- recovery.
lighted. In addition, the role of health behavior change in optimizing
d Appropriately resourced home-based exercise training has
and maintaining benefits is discussed.
Conclusions: The considerable growth in the science and application
proven effective in reducing dyspnea and increasing exer-
of pulmonary rehabilitation since 2006 adds further support for its
cise performance in individuals with COPD.
efficacy in a wide range of individuals with chronic respiratory d Technologies are currently being adapted and tested to
disease. support exercise training, education, exacerbation man-
agement, and physical activity in the context of pulmonary
Keywords: COPD; pulmonary rehabilitation; exacerbation; behavior;
rehabilitation.
outcomes
d The scope of outcomes assessment has broadened, allow-
ing for the evaluation of COPD-related knowledge and
self-efficacy, lower and upper limb muscle function, bal-
OVERVIEW ance, and physical activity.
Pulmonary rehabilitation has been clearly demonstrated to re- d Symptoms of anxiety and depression are prevalent in indi-
duce dyspnea, increase exercise capacity, and improve quality viduals referred to pulmonary rehabilitation, may affect
of life in individuals with chronic obstructive pulmonary disease outcomes, and can be ameliorated by this intervention.
(COPD) (1). This Statement provides a detailed review of progress
in the science and evolution of the concept of pulmonary rehabil- In the future, we see the need to increase the applicability and
itation since the 2006 Statement. It represents the consensus of 46 accessibility of pulmonary rehabilitation; to effect behavior change
international experts in the field of pulmonary rehabilitation. to optimize and maintain outcomes; and to refine this intervention
On the basis of current insights, the American Thoracic So- so that it targets the unique needs of the complex patient.
ciety (ATS) and the European Respiratory Society (ERS) have
adopted the following new definition of pulmonary rehabilita-
tion: “Pulmonary rehabilitation is a comprehensive intervention INTRODUCTION
based on a thorough patient assessment followed by patient- Since the American Thoracic Society (ATS)/European Respira-
tailored therapies that include, but are not limited to, exercise tory Society (ERS) Statement on Pulmonary Rehabilitation was
training, education, and behavior change, designed to improve published in 2006 (1), this intervention has advanced in several
the physical and psychological condition of people with chronic ways. First, our understanding of the pathophysiology underly-
respiratory disease and to promote the long-term adherence to ing chronic respiratory disease such as chronic obstructive
health-enhancing behaviors.” pulmonary disease (COPD) has grown. We now more fully
Since the previous Statement, we now more fully understand appreciate the complex nature of COPD, its multisystem man-
the complex nature of COPD, its multisystem manifestations, ifestations, and frequent comorbidities. Second, the science andAmerican Thoracic Society Documents e15
Figure 1. A spectrum of support for
chronic obstructive pulmonary dis-
ease. Reprinted by permission from
Reference 3.
application of pulmonary rehabilitation have evolved. For ex- Task Force meetings were organized during the ATS Inter-
ample, evidence now indicates that pulmonary rehabilitation is national Congress 2011 (Denver, CO) and during the ERS An-
effective when started at the time or shortly after a hospitaliza- nual Congress 2011 (Amsterdam, The Netherlands) to present
tion for COPD exacerbation. Third, as integrated care has risen and discuss the latest scientific developments within pulmonary
to be regarded as the optimal approach toward managing chronic rehabilitation. In preparation, the Statement was split up into
respiratory disease, pulmonary rehabilitation has established itself various sections and subsections. Task Force members were
as an important component of this model. Finally, with the recog- appointed to one or more sections, based on their clinical and
nition that health behavior change is vital to optimization and scientific expertise. Task Force members reviewed new scientific
maintenance of benefits from any intervention in chronic care, advances to be added to the then-current knowledge base. This
pulmonary rehabilitation has taken a lead in developing strategies was done through identifying recently updated (published be-
to promote self-efficacy and thus the adoption of a healthy lifestyle tween 2006 and 2011) systematic reviews of randomized trials
to reduce the impact of the disease. from Medline/PubMed, EMBASE, the Cochrane Central Reg-
Our purpose in updating this ATS/ERS Statement on Pulmo- ister of Controlled Trials, CINAHL, the Physical Therapy Evi-
nary Rehabilitation is to present the latest developments and dence Database (PEDro), and the Cochrane Collaboration, and
concepts in this field. By doing so, we hope to demonstrate its supplementing this with recent studies that added to the evidence
efficacy and applicability in individuals with chronic respiratory based on pulmonary rehabilitation (Table 2). The Task Force
disease. By necessity, this Statement focuses primarily on COPD, members selected the relevant papers themselves, irrespective
because individuals with COPD represent the largest proportion of of the study designs used. Finally, the Co-Chairs read all the
referrals to pulmonary rehabilitation (4), and much of the existing sections, and together with an ad hoc writing committee (the
science is in this area. However, effects of exercise-based pulmo- four Co-Chairs, Linda Nici, Carolyn Rochester, and Jonathan
nary rehabilitation in people with chronic respiratory disease Raskin) the final document was composed. Afterward, all Task
other than COPD are discussed in detail. We hope to underscore Force members had the opportunity to give written feedback. In
the pivotal role of pulmonary rehabilitation in the integrated care total, three drafts of the updated Statement were prepared by
of the patient with chronic respiratory disease. the four Co-Chairs; these were each reviewed and revised iter-
atively by the Task Force members. Redundancies within and
METHODS across sections were minimized. This document represents the
A multinational, multidisciplinary group of 46 clinical and re- consensus of these Task Force members.
search experts (Table 1) participated in an ATS/ERS Task This document was created by combining a firm evidence-
Force with the charge to update the previous Statement (1). based approach and the clinical expertise of the Task Force
Task Force members were identified by the leadership of the members. This is a Statement, not a Clinical Practice Guideline.
ATS Pulmonary Rehabilitation Assembly and the ERS Scien- The latter makes specific recommendations and formally grades
tific Group 01.02, “Rehabilitation and Chronic Care.” Members strength of the recommendation and the quality the scientific ev-
were vetted for potential conflicts of interest according to the idence. This Statement is complementary to two current docu-
policies and procedures of ATS and ERS. ments on pulmonary rehabilitation: the American College ofe16 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 188 2013
TABLE 1. MULTIDISCIPLINARY COMPOSITION OF THE AMERICAN TABLE 2. METHODS CHECKLIST
THORACIC SOCIETY/EUROPEAN RESPIRATORY SOCIETY TASK
FORCE ON PULMONARY REHABILITATION Yes No
d Chest physicians/respirologists/pulmonologists Panel assembly
d Elderly care physician d Included experts from relevant clinical and nonclinical X
d Physiotherapists disciplines
d Occupational therapist d Included individual who represents views of patients in X
d Nurses society at large
d Nutritional scientist d Included methodologist with documented expertise X
d Exercise physiologists Literature review
d Methodologists d Performed in collaboration with librarian X
d Psychologists/behavioral experts d Searched multiple electronic databases X
d Health economists d Reviewed reference lists of retrieved articles X
Evidence synthesis
d Applied prespecified inclusion and exclusion criteria X
d Evaluated included studies for sources of bias X
Chest Physicians and American Association of Cardiovascular and d Explicitly summarized benefits and harms X
Pulmonary Rehabilitation (AACVPR) evidence-based guidelines d Used PRISMA to report systematic review X
(5), which formally grade the quality of scientific evidence, and d Used GRADE to describe quality evidence X
Generation of recommendations
the AACVPR Guidelines for Pulmonary Rehabilitation Programs,
d Used GRADE to rate the strength of recommendations X
which give practical recommendations (6). This Statement has been
endorsed by both the ATS Board of Directors (June 2013) and Definition of abbreviations: GRADE ¼ Grading of Recommendations Assess-
the ERS Executive Committee (February 2013). ment, Development and Evaluation; PRISMA ¼ Preferred Reporting Items for
Systematic Reviews and Meta-Analyses.
DEFINITION AND CONCEPT
In 2006 (1), pulmonary rehabilitation was defined as “an evidence- initiated at any stage of the disease, during periods of clinical
based, multidisciplinary, and comprehensive intervention for patients stability or during or directly after an exacerbation. The goals of
with chronic respiratory diseases who are symptomatic and often pulmonary rehabilitation include minimizing symptom burden,
have decreased daily life activities. Integrated into the individualized maximizing exercise performance, promoting autonomy, increas-
treatment of the patient, pulmonary rehabilitation is designed to re- ing participation in everyday activities, enhancing (health-related)
duce symptoms, optimize functional status, increase participation, quality of life, and effecting long-term health-enhancing behavior
and reduce healthcare costs through stabilizing or reversing systemic change.
manifestations of the disease.” This document places pulmonary rehabilitation within the
Even though the 2006 definition of pulmonary rehabilitation concept of integrated care. The World Health Organization
is widely accepted and still relevant, there was consensus among defines integrated care as “a concept bringing together inputs,
the current Task Force members to make a new definition of pul- delivery, management and organization of services related to
monary rehabilitation. This decision was made on the basis of diagnosis, treatment, care, rehabilitation and health promotion”
recent advances in our understanding of the science and process (8). Integration of services improves access, quality, user satis-
of pulmonary rehabilitation. For example, some parts of a com- faction, and efficiency of medical care. As such, pulmonary reha-
prehensive pulmonary rehabilitation program are based on years bilitation provides an opportunity to coordinate care throughout
of clinical experience and expert opinion, rather than evidence- the clinical course of an individual’s disease.
based. Moreover, nowadays pulmonary rehabilitation is considered
to be an interdisciplinary intervention rather than a multidisciplinary EXERCISE TRAINING
approach (7) to the patient with chronic respiratory disease. Fi-
nally, the 2006 definition emphasized the importance of stabilizing Introduction
or reversing systemic manifestations of the disease, without specific Exercise capacity in patients with chronic respiratory disease
attention to behavior change. such as COPD is impaired, and is often limited by dyspnea.
On the basis of our current insights, the ATS and the ERS The limitation to exercise is complex and it would appear the
have adopted the following new definition of pulmonary reha- limitation to exercise is dependent on the mode of testing (9).
bilitation: “Pulmonary rehabilitation is a comprehensive inter- The exertional dyspnea in this setting is usually multifactorial in
vention based on a thorough patient assessment followed by origin, partly reflecting peripheral muscle dysfunction, the con-
patient-tailored therapies, which include, but are not limited to, sequences of dynamic hyperinflation, increased respiratory load,
exercise training, education, and behavior change, designed to or defective gas exchange (10–12). These limitations are aggra-
improve the physical and psychological condition of people with vated by the natural, age-related decline in function (13) and
chronic respiratory disease and to promote the long-term adher- the effects of physical deconditioning (detraining). In addition,
ence of health-enhancing behaviors.” they are often compounded by the presence of comorbid con-
Pulmonary rehabilitation is implemented by a dedicated, in- ditions. Some of these factors will be partially amenable to
terdisciplinary team, including physicians and other health care physical exercise training as part of a comprehensive pulmonary
professionals; the latter may include physiotherapists, respira- rehabilitation program.
tory therapists, nurses, psychologists, behavioral specialist, exer- Considered to be the cornerstone of pulmonary rehabilitation
cise physiologists, nutritionists, occupational therapists, and (1), exercise training is the best available means of improving
social workers. The intervention should be individualized to muscle function in COPD (14–18). Even those patients with
the unique needs of the patient, based on initial and ongoing severe chronic respiratory disease can often sustain the neces-
assessments, including disease severity, complexity, and comor- sary training intensity and duration for skeletal muscle adapta-
bidities. Although pulmonary rehabilitation is a defined inter- tion to occur (16, 19). Improvements in skeletal muscle function
vention, its components are integrated throughout the clinical after exercise training lead to gains in exercise capacity despite
course of a patient’s disease. Pulmonary rehabilitation may be the absence of changes in lung function (20, 21). Moreover, theAmerican Thoracic Society Documents e17
improved oxidative capacity and efficiency of the skeletal nonhypoxemic patients with COPD, allows for higher intensity
muscles leads to a reduced ventilatory requirement for a given training, probably through several mechanisms, including a de-
submaximal work rate (22); this may reduce dynamic hyperin- crease in pulmonary artery pressure, carotid body inhibition,
flation, thereby adding to the reduction in exertional dyspnea and a decrease in lactic acid production, all resulting in a
(23). Exercise training may have positive effects in other areas, dose-dependent decrease in respiratory rate, and thereby a re-
including increased motivation for exercise beyond the rehabil- duction in dynamic hyperinflation (41, 45–48).
itation environment, reduced mood disturbance (24–26), less Cardiac limitation. The cardiovascular system is affected by
symptom burden (27), and improved cardiovascular function chronic respiratory disease in a number of ways, the most impor-
(28, 29). Optimizing medical treatment before exercise training tant being an increase in right ventricular afterload. Contributing
with bronchodilator therapy, long-term oxygen therapy, and the factors include elevated pulmonary vascular resistance resulting
treatment of comorbidities may maximize the effectiveness of from combinations of hypoxic vasoconstriction (49), vascular
the exercise training intervention. injury and/or remodeling (50, 51), and increased effective pul-
Before starting an exercise training program, an exercise as- monary vascular resistance due to erythrocytosis (52). An over-
sessment is needed to individualize the exercise prescription, loaded right ventricle may lead to right ventricular hypertrophy
evaluate the potential need for supplemental oxygen, help rule and failure (53). Right ventricular hypertrophy may also com-
out some cardiovascular comorbidities, and help ensure the promise left ventricular filling by producing septal shifts; these
safety of the intervention (30–35). further reduce the ability of the heart to meet exercise demands
This patient assessment (35) may also include a maximal (54). Other cardiac complications include tachyarrythmias and
cardiopulmonary exercise test to assess the safety of exercise, elevated right atrial pressure (due to air trapping). The latter
to define the factors contributing to exercise limitation, and to may further compromise cardiac function during exercise (55,
identify a suitable exercise prescription (30). 56). Some of the substantial physiologic benefits from exercise
Identifying a single variable limiting exercise in individuals training (57–60) may be due, in part, to an improvement in
with COPD is often difficult. Indeed, many factors may contrib- cardiovascular function (28, 29).
ute directly or indirectly to exercise intolerance. Because of this, Limitation due to lower limb muscle dysfunction. Lower limb
separating the various mechanisms contributing to exercise intol- muscle dysfunction is frequent in individuals with chronic
erance is often a largely academic exercise and is not always nec- respiratory disease and is an important cause of their exercise lim-
essary or feasible. For example, deconditioning and hypoxia itation (61, 62). A summary of common skeletal muscle abnor-
contribute to excess ventilation, resulting in an earlier ventila- malities in chronic respiratory disease is given in the ATS/ERS
tory limitation. Consequently, exercise training and oxygen Statement on Skeletal Muscle Dysfunction in COPD (63). Pe-
therapy could delay a ventilatory limit to exercise without ripheral muscle dysfunction in individuals with chronic respira-
altering lung function or the maximal ventilatory capacity. An- tory disease may be attributable to single or combined effects of
alyzing the output from a cardiopulmonary exercise test may inactivity-induced deconditioning, systemic inflammation, oxida-
uncover otherwise hidden exercise-related issues, such as hyp- tive stress, smoking, blood gas disturbances, nutritional impair-
oxemia, dysrhythmias, musculoskeletal problems, or cardiac ment, low anabolic hormone levels, aging, and corticosteroid use
ischemia (30). (61, 63–70). Skeletal muscle dysfunction is frequently reported as
fatigue; in many individuals this is the main limiting symptom,
particularly during cycle-based exercise (71, 72). This could be
Physiology of Exercise Limitation related to the fact that the peripheral muscle alterations as de-
Exercise intolerance in individuals with chronic respiratory dis- scribed previously (63) render these muscles susceptible to con-
ease may result from ventilatory constraints, pulmonary gas ex- tractile fatigue (73, 74).
change abnormalities, peripheral muscle dysfunction, cardiac The lactic acidosis resulting from exercising skeletal muscles
dysfunction, or any combination of the above (10–12). Anxiety, at higher intensities is a contributory factor to exercise termina-
depression, and poor motivation may also contribute to exercise tion in healthy individuals, and may also contribute to exercise
intolerance (36); however, a direct association has not been limitation in patient with COPD (75, 76). Patients with COPD
established (37–39). often have increased lactic acid production for a given exercise
Ventilatory limitation. In COPD, ventilatory requirements work rate (57, 71), thereby increasing their ventilatory require-
during exercise are often higher than expected because of in- ment (57). The increased ventilatory requirement imposes an
creased work of breathing, increased dead space ventilation, im- additional burden on the respiratory muscles, which are already
paired gas exchange, and increased ventilatory demand as a facing increased impedance to breathing. This rise in lactic acid
consequence of deconditioning and peripheral muscle dysfunc- is exacerbated by a tendency to retain carbon dioxide during
tion. Adding to this increased demand is the limitation to max- exercise, further increasing acidosis and resultant ventilatory
imal ventilation during exercise resulting from expiratory airflow burden. Improving skeletal muscle function is therefore an im-
obstruction and dynamic hyperinflation in individuals with portant goal of exercise training programs.
COPD (40, 41). This leads to further increased work of breath- Limitations due to respiratory muscle dysfunction. The dia-
ing, increased load and mechanical constraints on the respira- phragm of individuals with COPD adapts to chronic overload
tory muscles (42, 43), with a resulting intensified sense of and has greater resistance to fatigue (77, 78). As a result, at
dyspnea. identical absolute lung volumes, the inspiratory muscles are
Gas exchange limitation. Hypoxia directly increases pulmo- capable of generating more pressure than those of healthy con-
nary ventilation through augmenting peripheral chemoreceptor trol subjects (79–81). However, patients with COPD often have
output and indirectly through stimulation of lactic acid produc- static and dynamic hyperinflation, which places their respiratory
tion. Lactic acidemia resulting from anaerobic metabolism by the muscles at a mechanical disadvantage. Thus, despite adapta-
muscles during higher intensity exercise contributes to muscle tions in the diaphragm, both functional inspiratory muscle
task failure and increases pulmonary ventilation, as lactic acid strength (82) and inspiratory muscle endurance (83) are com-
buffering results in an increase in carbon dioxide production promised in COPD. As a consequence, respiratory muscle
and acidosis stimulates the carotid bodies (44). Supplemental weakness, as assessed by measuring maximal respiratory pres-
oxygen therapy during exercise, in hypoxemic and even in sures, is often present (82–86). This contributes to hypercapniae18 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 188 2013
(87), dyspnea (88, 89), nocturnal oxygen desaturation, and re- individuals with moderate to severe COPD (100). After 3
duced exercise performance (71, 90). months of training, those in the Nordic walking group spent
more time walking and standing, had an increased intensity of
walking, and increased their 6-minute walk distance compared
Exercise Training Principles with the control group. These improvements were sustained at 6
The general principles of exercise training in individuals with and 9 months after the initial 3-month intervention. This result
chronic respiratory disease are no different from those for was reinforced by a randomized study of 36 individuals with
healthy individuals or even athletes. For physical training to COPD that compared walking with outdoor cycle training on
be effective the total training load must reflect the individual’s walking outcome, the endurance shuttle walk time (98). Both
specific requirements, it must exceed loads encountered during groups trained indoors for 30 to 45 minutes per session, three
daily life to improve aerobic capacity and muscle strength (i.e., times weekly over 8 weeks. The walk training group increased
the training threshold), and must progress as improvement their endurance shuttle walk time significantly more than did
occurs. Various modes of training will be required for improve- the cycle training group, providing evidence for ground walk-
ments in cardiorespiratory endurance, strength, and/or flexibil- ing as a preferred mode of exercise training to improve walk-
ity. The text below provides details on endurance training, ing endurance.
interval training, resistance training, neuromuscular electrical
stimulation, and respiratory muscle training.
Interval Training
Interval training may be an alternative to standard endurance
Endurance Training training for individuals with chronic respiratory disease who
Since the previous Statement new science has been reported on have difficulty in achieving their target intensity or duration
the endurance training component of pulmonary rehabilitation, of continuous exercise because of dyspnea, fatigue, or other
especially in the area of its widened scope. However, the aims of symptoms (60, 101). Interval training is a modification of endur-
the intervention and the principles of the exercise prescription ance training in which high-intensity exercise is regularly inter-
have not changed substantially. The aims are to condition the spersed with periods of rest or lower intensity exercise. This
muscles of ambulation and improve cardiorespiratory fitness may result in significantly lower symptom scores (93) despite
to allow an increase in physical activity that is associated with a re- high absolute training loads, thus maintaining the training
duction in breathlessness and fatigue. Higher intensity endurance effects of endurance training (93, 102, 103), even in cachectic
exercise training is commonly used by pulmonary rehabilitation individuals with severe COPD (104). The practical difficulty of
programs (91). However, for some individuals, it may be difficult interval training is its mode of delivery, which typically requires
to achieve the target intensity or training time, even with close a cycle-based program and continuing the regimen in unsuper-
supervision (60). In this situation, low-intensity endurance train- vised settings.
ing or interval training are alternatives (92, 93). Recently, the Since the previous Statement there has been considerable re-
number of steps per day has been suggested as an alternative search interest in interval training in COPD, with the publication
yet tangible target of exercise training (94); this may emerge as of several randomized, controlled trials (102, 105–110) and sys-
an important concept in pulmonary rehabilitation (95). tematic reviews (111, 112). Overall, these studies have found no
Endurance exercise training in the form of cycling or walking clinically important differences between interval and continu-
exercise is the most commonly applied exercise modality in pul- ous training modes in outcomes including exercise capacity,
monary rehabilitation (23, 59, 60). The framework recommen- health-related quality of life, and skeletal muscle adaptation
ded by the American College of Sports Medicine (ACSM’s immediately after training. Longer term effects of or adherence
Guidelines for Exercise Testing and Prescription on Frequency, to interval training have not been investigated.
Intensity, Time, and Type [FITT]) can be applied in pulmonary To date, most studies in COPD have matched the total work
rehabilitation (96). Endurance exercise training in individuals performed by continuous training and interval training groups,
with chronic respiratory disease is prescribed at the same fre- and found similar training adaptations (93, 109, 113). Whether
quency: three to five times per week. A high level of intensity of it might be possible to achieve greater total work using interval
continuous exercise (.60% maximal work rate) for 20 to 60 training, and therefore achieve even larger training adaptations,
minutes per session maximizes physiologic benefits (i.e., exercise remains currently unknown. In contrast, for individuals with
tolerance, muscle function, and bioenergetics) (96). A Borg chronic heart failure a high-intensity interval training program
dyspnea or fatigue score of 4 to 6 (moderate to [very] severe) was superior to moderate-intensity continuous training at
or Rating of Perceived Exertion of 12 to 14 (somewhat hard) is matched work for both exercise capacity and quality of life
often considered a target training intensity (97). (114). The reason for this difference in outcomes between pa-
Walking (either ground-based or on a treadmill) and biking tient populations is unclear. However, the high prevalence of
(using a stationary cycle ergometer) are optimal exercise modal- chronic heart failure in individuals undergoing pulmonary reha-
ities if tolerated by the individual. Walking training has the ad- bilitation suggests that high-intensity interval training may have
vantage of being a functional exercise that can readily translate a useful role for individuals with comorbid disease.
to improvement in walking capacity. If the primary goal is to in- The efficacy of interval training versus endurance training in
crease walking endurance, then walking is the training modality decreasing dyspnea during the exercise training is unclear. Evi-
of choice (98) in this situation. Biking exercise places a greater dence available at the time of the previous Statement suggested
specific load on the quadriceps muscles than walking (9) and that in COPD, interval training resulted in lower symptom scores
results in less exercise-induced oxygen desaturation (99). while allowing for higher training intensities (93, 109). Subse-
Since the previous Statement, there has been an increased quent studies have found no difference in symptoms between
awareness of the efficacy of leisure walking as a mode of exercise continuous and interval training (105, 106); however, these stud-
training in COPD. This is highlighted by a randomized con- ies have used slightly longer training intervals (1 min or more,
trolled trial of a 3-month outdoor Nordic walking exercise pro- compared with 30 s in previous studies). It is possible that dur-
gram (1 h of walking at 75% of initial maximal heart rate three ing high-intensity interval training, shorter intervals (,1 min)
times per week) versus control (no exercise) in 60 elderly are required to achieve lower symptom scores (111). Indeed, theAmerican Thoracic Society Documents e19
metabolic response during interval training seems comparable weight, increasing the repetitions per set, increasing the number
to the metabolic load during simple, self-paced domestic activ- of sets per exercise, and/or decreasing the rest period between
ities of daily life (115). sets or exercises (116, 118). Because the optimal resistance
There is no evidence regarding the role of interval training training approach for patients with chronic respiratory disease
for individuals with respiratory conditions other than COPD. is not known, clinicians often follow these recommendations.
Extrapolating from COPD studies, when continuous training Alternative models for progression in training intensity, such
is curtailed by severe dyspnea or oxyhemoglobin desaturation as daily undulating periodized resistance training (e.g., making
(as in interstitial lung disease), interval training may be a rea- alterations in training volume and intensity on a daily basis
sonable strategy to increase exercise intensity and training [138]) may be advantageous (139), but data are lacking.
adaptations. Clinical trials in COPD have compared resistance training
In summary, interval training and continuous training appear with no training and with endurance training. Lower limb resis-
to be equally effective in COPD. Interval training may be a useful tance training consistently confers gains in muscle force and mass
alternative to continuous training, especially in symptom-limited compared with no exercise training (136, 140–143). The effects
individuals who are unable to tolerate high-intensity continuous on other outcomes are less consistent. It appears that the ca-
training. Further research is necessary regarding its applications pacity for increased lower limb muscle force to translate into
in chronic respiratory diseases other than COPD. increased maximal or submaximal exercise capacity is depen-
dent, at least in part, on the magnitude of the training load.
Studies that have used loads equal to or exceeding 80% of
Resistance/Strength Training one repetition maximum throughout the training program have
Resistance (or strength) training is an exercise modality in which reported improvements in submaximal exercise capacity (21,
local muscle groups are trained by repetitive lifting of relatively 120) and peak power measured via cycle ergometry (142) as
heavy loads (116–118). Resistance training is considered impor- well as peak walk speed measured over a 30-m track (140).
tant for adults to promote healthy aging (119) and also appears Similar findings have been reported in individuals with chronic
to be indicated in individuals with chronic respiratory disease heart failure (144). In some (120, 136), but not all studies (141),
(21, 120), such as those with COPD, who have reduced muscle training loads between 50 and 80% of one repetition maximum
mass and strength of their peripheral muscles, relative to were sufficient to improve endurance exercise capacity. Training
healthy control subjects (65, 121). These systemic manifesta- programs that appear to have used more modest loads are inef-
tions of COPD are related to survival, health care use, and fective at conferring gains in exercise capacity (143).
exercise capacity (61, 122–125). Further, as falling appears to When added to a program of endurance constant-load exer-
be common among people with COPD (126, 127), and muscle cise, resistance training confers additional benefits in muscle
weakness is an important risk factor for falls in the older pop- force, but not in overall exercise capacity or health status (15,
ulation (128), optimizing muscle strength is likely to be an im- 117, 132, 133). However, gains in quadriceps muscle strength
portant goal of rehabilitation in this population. In addition to may optimize performance of tasks that specifically load these
the expected effects on muscle strength, it is possible that resis- muscles, such as stair-climbing and sit-to-stand (145). Resis-
tance training may also assist with maintaining or improving tance training for the muscles of the upper limbs has been dem-
bone mineral density (129), which has been shown to be abnor- onstrated to increase the strength of the upper limb muscles and
mal low (e.g., osteoporosis or osteopenia) in about 50% of indi- translate this into improvements in related tasks, such as the
viduals with COPD (130, 131). 6-minute peg board and ring test (146, 147).
Of note, endurance training, which is the mainstay of exercise Resistance exercise elicits a reduced cardiorespiratory re-
training in pulmonary rehabilitation programs, confers subopti- sponse compared with endurance exercise (101). That is, resis-
mal increases in muscle mass or strength compared with pro- tance exercise demands a lower level of oxygen consumption
grams that include specific resistance exercise (15, 132, 133). and minute ventilation, and evokes less dyspnea (101). In the
Resistance training has greater potential to improve muscle clinical setting, this makes resistance exercise an attractive and
mass and strength than endurance training (21, 120, 132, 134– feasible option for individuals with advanced lung disease
136), two aspects of muscle function that are only modestly or comorbidities who may be unable to complete high-intensity
improved by endurance exercises (23). Moreover, strength endurance or interval training because of intolerable dyspnea
training results in less dyspnea during the exercise period, (60, 101). It may also be an option for training during disease
thereby making this strategy easier to tolerate than endurance exacerbations (148).
constant-load training (101). In summary, the combination of constant-load/interval and
The optimal resistance training prescription for patients with strength training improves outcome (i.e., exercise capacity and
chronic respiratory disease is not determined, as evidenced by muscle strength [15]) to a greater degree than either strategy
the wide variation in its application among clinical trials alone in individuals with chronic respiratory disease, without
(117). The American College of Sports Medicine recommends unduly increasing training time (132).
that, to enhance muscle strength in adults, 1 to 3 sets of 8 to 12
repetitions should be undertaken on 2 to 3 days each week
(116). Initial loads equivalent to either 60 to 70% of the one Upper Limb Training
repetition maximum (i.e., the maximal load that can be moved Many problematic activities of daily living in individuals with
only once over the full range of motion without compensatory chronic respiratory disease involve the upper extremities, includ-
movements [137]) or one that evokes fatigue after 8 to 12 rep- ing dressing, bathing, shopping, and many household tasks (149).
etitions are appropriate. The exercise dosage must increase over Because of this, upper limb training is typically integrated into
time (the so-called overload) to facilitate improvements in mus- an exercise regimen. Examples of upper extremity exercises
cular strength and endurance. This increase occurs when an include aerobic regimens (e.g., arm cycle ergometer training)
individual can perform the current workload for 1 or 2 repeti- and resistance training (e.g., training with free weights and elas-
tions over the desired number of 6 to 12, on 2 consecutive tic bands, which provide resistance). Typical muscles targeted
training sessions (116). Overload can be achieved by modulat- are the biceps, triceps, deltoids, latissimus dorsi, and the
ing several prescriptive variables: increasing the resistance or pectorals.e20 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 188 2013
Complementing a previous review (134), a systematic review according to a specific protocol in which the intensity (ampli-
of upper limb training in COPD published since the previous tude), frequency, duration, and wave form of the stimulus are
Statement demonstrates that upper limb resistance training chosen to achieve the desired muscle response (157–159). The
improves upper limb strength (150). This review included all electrical stimulus amplitude (intensity) determines the strength
forms of upper limb training, categorizing the trials as offering of muscle contraction.
supported (cycle ergometry) and unsupported (including free Muscle contraction induced by electrical stimulation does not
weights/lifting a dowel/throwing a ball) exercise programs. lead to dyspnea, poses minimal cardiocirculatory demand (158,
The outcome measures across the trials were diverse, making 160–165), and bypasses the cognitive, motivational, and psycho-
firm conclusions challenging. However, the analysis indicated logical aspects involved in conventional exercise that may hinder
that improvements in upper limb performance were equivocal. or prevent effective exercise training (166). As such, it is suited
Furthermore, it was difficult to determine whether upper limb for deconditioned individuals with severe ventilatory and/or car-
training led to additional benefit in health-related quality of life diac limitation, including those hospitalized with acute disease
or dyspnea associated with activities of daily living. exacerbations or respiratory failure. Small, relatively inexpensive,
Since the above review two trials of unsupported resistance portable electrical stimulators are also suitable for home use, and
training (146, 147) have been published. The first was (146) therefore may benefit persons who are too disabled to leave their
a 3-week inpatient trial that compared unsupported upper ex- homes, require home mechanical ventilation, or who lack access
tremity training plus pulmonary rehabilitation with pulmonary to traditional pulmonary rehabilitation programs (167).
rehabilitation alone. The between-group comparison identified NMES improves limb muscle strength, exercise capacity, and
significant gains in the upper limb training group in the 6-minute reduces dyspnea of stable outpatients with severe COPD and
ring test, an upper limb activities test. Perhaps unsurprisingly, poor baseline exercise tolerance (159, 162, 167), and NMES can
there was no additional benefit detected in the 6-minute walk be continued during acute COPD exacerbations (167, 168). In
test (6MWT). The second trial (147) compared upper extremity a randomized, sham-controlled trial, transcutaneous nerve sti-
resistance training with a sham intervention; both groups partic- mulation applied over traditional acupuncture points led to
ipated in an endurance and strength-based lower limb exercise within- and between-group increases in multiple outcome varia-
training regimen. Compared with the control group, the interven- bles, including FEV1; 6-minute walk distance; quality of life,
tion group had improvements in upper limb performance but as measured by the St. George’s Respiratory Questionnaire
there was no change in health-related quality of life or dyspnea (SGRQ); and b-endorphin levels (169). In another study, individ-
during activities of daily living. Taken together, the evidence uals with COPD with low body mass index, severe airflow limita-
suggests that upper extremity training increases upper limb func- tion, and severe deconditioning who had been released from
tion in patients with COPD. However, the optimal approach to hospitalization for exacerbations achieved greater improve-
training remains to be determined. Furthermore, it is not clear ments in leg muscle strength and dyspnea during activities of
whether and to what extent specific gains in upper limb function daily life after a 4-week treatment with NMES plus active limb
translate into improvements in broader outcomes such as health- mobilization and slow walking as compared with the same mobi-
related quality of life. lization regimen without NMES (170). NMES added to active
limb mobilization also augments gains in mobility among bed-
bound individuals with chronic hypercapnic respiratory failure
Flexibility Training
due to COPD who are receiving mechanical ventilation (171). It
Although flexibility training is a component of many exercise also preserves muscle mass (172) and helps prevent critical illness
regimens and is commonly provided in pulmonary rehabilitation, neuromyopathy among critically ill individuals in the intensive
there are, to date, no clinical trials demonstrating its effective- care unit (173). The mechanisms by which NMES improves mus-
ness in this particular setting. Improved thoracic mobility and cle function and exercise capacity or performance are incom-
posture may increase the vital capacity in patients with chronic pletely understood. The pattern of muscle fiber activation
respiratory disease (151). Because respiration and posture have during NMES may differ from that which occurs during conven-
a coupled relationship, a thorough evaluation includes both the tional exercise (174–176). The precise electrical stimulation pro-
assessment and treatment of patients with chronic respiratory tocol chosen may also impact the rehabilitation outcomes of
disease (152). Common postural impairments include thoracic NMES. Specifically, the frequency of stimulus delivered likely
kyphosis, increased chest anterior–posterior diameter, shoulder determines the types of muscle fibers activated (177). A NMES
elevation and protraction, and trunk flexion (152–154). Postural stimulus frequency up to 10 Hz likely preferentially activates slow-
abnormalities are associated with a decline in pulmonary func- twitch fibers and may selectively improve resistance to fatigue
tion, decreased quality of life, poor bone mineral density, and (178), whereas a frequency greater than 30 Hz may activate both
increased work of breathing (155, 156). Postural deviations are types of fibers, or may selectively recruit fast-twitch fibers and
known to alter body mechanics, resulting in back pain, which in enhance power (179). Studies conducted to date in individuals
turn alters breathing mechanics (155). One approach in pulmo- with COPD who have demonstrated gains in both muscle strength
nary rehabilitation is to have patients perform both upper and and endurance have used stimulus frequencies ranging from 35 to
lower body flexibility exercises (including stretching of major 50 Hz (158, 162, 167, 171). Effects of low-frequency NMES have
muscle groups such as the calves, hamstrings, quadriceps, and not been studied in individuals with COPD (159). Some investi-
biceps, as well as range of motion exercises for the neck, should- gators advocate delivery of a combination of stimulus frequencies
ers, and trunk) at least 2–3 days/week (153). during NMES training to most closely mimic normal motor neu-
ron firing patterns and have maximal impact on muscle function
(180, 181). The duration of benefits in muscle function after a lim-
Neuromuscular Electrical Stimulation ited period (e.g., several weeks) of NMES muscle training has not,
Transcutaneous neuromuscular electrical stimulation (NMES) to date, been studied in individuals with chronic respiratory dis-
of skeletal muscle is an alternative rehabilitation technique ease. There are no formal patient candidacy guidelines for NMES.
wherein muscle contraction is elicited, and selected muscles Contraindications to NMES are primarily based on expert
can thereby be trained, without the requirement for conventional opinion. Most care providers do not perform NMES on individ-
exercise. Electrical stimulation of the muscle is delivered uals with implanted electrical devices such as pacemakers orAmerican Thoracic Society Documents e21
implanted defibrillators; or persons with seizure disorder, uncon- (188). Small gains, which may not be clinically important, have
trolled cardiac arrhythmias (particularly ventricular), unstable been shown in health-related quality of life (188, 189).
angina, recent myocardial infarction, intracranial clips, and/or IMT given as an adjunct to whole-body exercise training has
total knee or hip replacement (160, 161, 163). Individuals with an additional benefit on inspiratory muscle strength and endur-
severe osteoarthritis of the joints to be mobilized by the muscles ance, but not on dyspnea or maximal exercise capacity (188–190).
to be stimulated, or persons with severe peripheral edema or Because whole-body exercise training confers substantial improve-
other skin problems wherein desired placement of electrodes ments in exercise capacity, dyspnea, and health-related quality of
would be limited, may also be poor candidates for NMES. life (91) it seems that detecting further improvement using IMT is
NMES is safe and generally well tolerated. The adverse effect difficult.
reported most commonly is mild muscle soreness that usually It is possible that IMT as an adjunct to whole-body exercise
resolves after the first few NMES sessions (177), and that in training may benefit those individuals with COPD with marked
part relates to the stimulus amplitude and frequency chosen. inspiratory muscle weakness. Indeed, the added effect of IMT on
Pulse amplitudes greater than 100 mA may lead to intolerable functional exercise capacity just failed to reach statistical signif-
muscle discomfort. Some individuals are unable to tolerate icance in those individuals with COPD and inspiratory muscle
NMES even at lower stimulus amplitudes and gains in exercise weakness (189, 191). This finding, however, needs to be con-
tolerance may depend on the patient’s ability to tolerate incre- firmed prospectively.
mental training stimulus intensities (182). At the start of NMES Although the nature of IMT programs differs considerably
training, stimulus amplitudes that lead to nonpainful muscle among studies, the use of an interval-based program with loaded
contraction are applied, and incremental gains in the stimulus breathing, interspersed with periods of rest, has been shown to
amplitude are made over the course of the training program, optimize the training loads that can be tolerated as well as the
according to patient tolerance. rate of change in PImax (192). Gains in inspiratory muscle func-
Taken together, evidence suggests that is a promising training tion are lost 12 months after cessation of the IMT program (193).
modality within pulmonary rehabilitation, particularly for In summary, current evidence indicates that IMT used in iso-
severely disabled patients with COPD. It remains unclear lation does confer benefits across several outcome areas. How-
whether NMES is effective for individuals with COPD with ever, its added benefit as an adjunct to exercise training in COPD
a higher degree of baseline exercise tolerance (183). More- is questionable. It is conceivable that IMT might be useful when
over, the impact of NMES in clinically stable individuals with added to whole-body exercise training in individuals with marked
chronic respiratory conditions other than COPD has not been inspiratory muscle weakness or those unable to participate in
evaluated. cycling or walking because of comorbid conditions, but this idea
needs to be evaluated prospectively.
Inspiratory Muscle Training
The pressure-generating capacity of the inspiratory pump Maximizing the Effects of Exercise Training
muscles is reduced in individuals with COPD (121). This is Relatively few clinical trials have evaluated the potential role of
primarily due to the deleterious effects of pulmonary hyper- adjuncts designed to enhance the positive effects of exercise
inflation, which serves to shorten and flatten the diaphragm, training in patients with chronic respiratory disease. The follow-
placing it at a mechanical disadvantage (79). The reduced ing outlines some of the research in this area.
pressure-generating capacity of the inspiratory muscles contrib- Pharmacotherapy. BRONCHODILATORS. In individuals with chronic
utes to both exercise intolerance and the perception of dyspnea airflow limitation, pharmacologic therapy is one of the key
in individuals with COPD (61, 89). Endurance exercise training, components of disease management, used to prevent and con-
despite conferring large gains in exercise capacity and reducing trol symptoms, reduce exacerbations, and improve exercise
dyspnea, does not appear to improve the pressure-generating tolerance and health status (194). Inhaled bronchodilators primarily
capacity of the inspiratory muscles (21, 184, 185), likely because act on airway smooth muscle, and not only improve expiratory flow
the ventilatory load during whole-body exercise is of insufficient in individuals with airflow limitation but also reduce resting
magnitude to confer a training adaptation. For this reason, there (195) and dynamic hyperinflation (196). Both short-acting
has been interest in applying a specific training load to the (197) as well as long-acting bronchodilators (196) increase
inspiratory muscles in individuals with weakened inspiratory exercise capacity in COPD. Bronchodilator therapy may be
muscles, in an effort to increase exercise capacity and reduce especially effective in enhancing exercise performance in indi-
dyspnea. viduals with a ventilatory exercise limitation (74). With opti-
The most common approach to inspiratory muscle training mal bronchodilation, the primary locus of exercise limitation
(IMT) uses devices that impose a resistive or a threshold load. may change from dyspnea to leg fatigue, thereby allowing
The properties of these devices have been described elsewhere individuals to exercise their peripheral muscles to a greater
(186, 187). In individuals with COPD, IMT performed with degree. This illustrates the potential synergy between pharma-
loads equal to or exceeding 30% of an individual’s maximal cologic and nonpharmacologic treatments.
inspiratory pressure [PImax]) confers gains in inspiratory muscle Optimizing the use of maintenance bronchodilator therapy
strength and endurance (188, 189). Studies of IMT in individuals within the context of a pulmonary rehabilitation program for
with COPD have investigated the effects of IMT in isolation COPD results in augmentation of exercise tolerance benefits
and of IMT added to whole-body exercise training. (198, 199), possibly by allowing individuals to exercise at higher
Meta-analyses of IMT, compared with sham IMT or no inter- intensities. Therefore, optimization of bronchodilator therapy
vention, in individuals with COPD demonstrate significant before exercise training in patients with airflow limitation is
improvements in inspiratory muscle strength and inspiratory generally routine in pulmonary rehabilitation. Although inhaled
muscle endurance (188, 189). In addition, significant and clini- corticosteroids are indicated for individuals with severe COPD
cally meaningful reductions in dyspnea during activities of daily and recurrent exacerbations (200), no effects on exercise capac-
living and increases in peak inspiratory flow were observed ity have been shown (201).
(188). Improvements have been demonstrated in walk distance, ANABOLIC HORMONAL SUPPLEMENTATION. Exercise training
but not peak power achieved during cycle ergometry testing programs that are part of pulmonary rehabilitation have beenYou can also read
