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(Chest. 2004;126:903-914.)
© 2004 American College of Chest Physicians

Peripheral Muscle Strength Training in COPD*

A Systematic Review

Simone D. O’Shea, BPhty (Hons); Nicholas F. Taylor, PhD and Jennifer Paratz, PhD

* From Wodonga Regional Health Service (Ms. O’Shea), Wodonga; Musculoskeletal Research Centre (Dr. Taylor), La Trobe University Melbourne; and The Alfred Hospital (Dr. Paratz), Melbourne, VIC, Australia.

Correspondence to: Simone O’Shea, BPthy (Hons), Wodonga Regional Health Service, PO Box 156, Wodonga, VIC, 3689, Australia; e-mail: simoshe{at}optusnet.com.au


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Background: Skeletal muscle weakness, and the associated impact on exercise tolerance, provides a strong theoretical rationale for strength training intervention for people with COPD.

Aim: The purpose of this review was to examine systematically the current evidence for peripheral muscle strength training in people with COPD.

Method: Empirical trials and reviews relating to strength training in COPD were obtained by searching electronic databases and citation tracking, using the keywords of COPD with strength/resistance training and skeletal muscle. Two reviewers completed data extraction and quality assessment independently, using the PEDro (physiotherapy evidence database) scale and a checklist for review articles. Effect sizes and 95% confidence intervals were determined for empiric trials and metaanalysis used where appropriate.

Results: The search strategy yielded 13 articles (9 empirical trials and 4 reviews). Strength training was found to have strong evidence for improving upper body and leg strength. However, no strong evidence for strength training was found for other outcome measures.

Conclusions: Further research is required to investigate the effects of strength training on functional activities, such as balance, upper limb function, self care, and participation in daily life.

Key Words: COPD • exercise training • review • skeletal muscle


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Exercise intolerance, particularly with disease progression, is a key feature of COPD. The sequelae of exercise intolerance include increased difficulty performing daily tasks, difficulty participating in everyday events,1 and higher utilization of health-care services.2 Often these changes are described as a vicious downward spiral associated with increasing disability.3

A growing body of evidence is emerging indicating the presence of skeletal muscle dysfunction in COPD.4567 Muscle changes observed include reductions in type I fibers, atrophy of type I and II fibers, reduced capillarity, and altered metabolic enzyme levels.4 Numerous factors have been identified as contributing to skeletal muscle changes, including hypoxia, hypercapnia, inflammation, nutrition, deconditioning, and steroid-induced myopathy.4 Skeletal muscle changes highlight that muscle conditioning may play an integral role in the treatment of this population.

Muscle conditioning in COPD has predominantly focused on endurance training. Improvements in muscular endurance and exercise capacity have been shown after endurance training, without changing muscle mass or strength.8 Strength training may provide a means of ameliorating skeletal muscle atrophy and weakness in COPD. The purpose of this review was to examine systematically the current evidence for peripheral muscle strength training in COPD, with regard to changes in impairments, activity limitation, and participation restrictions.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusions
 References
 
An overview of the systematic review process is seen in the flow chart (Fig 1 ).



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  		Figure 1.. Overview of systematic review process.

 
Search Strategy
Study identification commenced by electronic searching, from the earliest available time until the present, using the following databases: MEDLINE, preMEDLINE, PubMed, EMBASE, CINAHL, AMED, AMI, Expanded Academic Index, Sports Discus, Ausport Medical, DARE, and Cochrane. Search terms used were as follows: obstructive lung disease, COPD, chronic obstructive lung disease, chronic obstructive airway disease, chronic airways limitation, chronic airways obstruction, chronic bronchitis, and pulmonary emphysema. These terms were combined with strength training, strength exercise, weight training, weight lifting, resistance exercise, resistance training, progressive resistance exercise, and progressive resistance training, as well as peripheral muscle and skeletal muscle. Citation tracking and key author searches were also completed.

Inclusion Criteria
Identified articles (title and abstract) were assessed by two independent reviewers using the outlined criteria (Table 1 ). Full articles were obtained where inclusion could not be determined from title or abstract. Once each reviewer completed the assessment, any differences were discussed and resolved by consensus.


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  		Table 1.. Criteria for Inclusion or Exclusion of Articles in Systematic Review

 
Quality Assessment
Two independent reviewers assessed the quality of included articles, rating empirical trials out of 10 on the PEDro (physiotherapy evidence database) scale9 and review articles using the guidelines of Oxman.10 Standardized forms were developed in order to extract information from each study included in the review.

Data Analysis
To compare results between studies, effect sizes and 95% confidence intervals (CIs) were calculated using Web-based metaanalysis software.11 Where no baseline differences existed between groups, the unbiased effect size estimator (d) was calculated.12 For single-group pre/post intervention studies, effect sizes were calculated according to the method described by Howell.13 Overall effects were calculated for muscle strength using the random effects model for metaanalysis.12 Due to differing study designs, metaanalysis was deemed inappropriate for other measures, as effects may not have been only attributable to strength training. The strength of an effect size was interpreted descriptively using the terms described by Cohen,14 whereby effect sizes are labeled as either small (d = 0.2), medium (d = 0.5), or large (d = 0.8). Results were described using the International Classification of Functioning (ICF),15 developed by the World Health Organization to measure how people live within a particular health condition, in this case COPD (Fig 2 ).



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  		Figure 2.. Classification of outcome measures using ICF guidelines. *Health Status Questionnaire 2.0 (SF-36).

 

   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusions
 References
 
Eighty-three articles were identified during electronic searching, of which 64 were excluded after application of inclusion criteria. Detailed assessment of the 19 remaining articles resulted in the exclusion of a further 6 articles. A final library of 13 articles remained: 9 empirical studies161718192021222324 and 4 reviews.25262728

Study Quality and Design
Review Articles: None of the included reviews were systematic reviews. Information was not provided about literature searching or inclusion criteria, and methodologic validity of studies was described, rather than using specified criteria. One review28 attempted study comparison via a Table.

Empiric Studies: A median score of 5 out of 10 (range, 2 to 6; mode = 5) on the PEDro scale9 was found. Six studies171819202124 reported random allocation of subjects to groups, with three studies161924 also reporting concealment of treatment allocation. Blinding of assessors to group allocation, for at least one key outcome measure, was undertaken in three of the included studies,181920 and intention-to-treat analysis occurred in four studies.16172123

Study design was variable. Four studies16182122 compared strength training with a no-treatment control group. One study23 used a single-group pre/post design of combined interval and strength training, while others compared resistance training with endurance training19; or standard medical treatment with mixed training24; or aerobic training with combined strength and aerobic exercise20; or three different training protocols (strength, aerobic, combined strength and aerobic training) with a no-treatment control group.17 Ortega and colleagues17 did not report control group data; therefore, strength training data were compared with endurance training in this review.

Program Content and Environmental Factors
Key features of empirical studies are summarized in Table 2 . Training sessions generally included two to four sets of 6 to 12 repetitions of each exercise at intensities ranging from 50 to 85% of one repetition maximum (1RM). Three studies162223 did not define the load with reference to the 1RM. Eight of nine programs were conducted in outpatient clinics, and weight machines were typically used. Free weights were used exclusively in two studies,1623 and in a third study18 were used in conjunction with machines. On average, subjects performed six exercises (range, three to nine exercises) in a session, focusing on trunk, upper limb, and lower limb strengthening. Training durations were typically 12 weeks (range, 6 to 26 weeks), and training frequency was three times per week, except in one program where frequency was not stated16 and in another program where training occurred twice per week.21


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  		Table 2.. Comparison of Included Empirical Studies on Strength Training in COPD*

 
Personal Factors
The average age of participants included in studies was 62 years (SD 6.8; mean age range, 48.5 to 71.5 years). In general, more men were included, representing > 70% of the total study population. The mean FEV1 percentage of predicted across studies was 46.1% (SD 13.1; range, 38 to 77.5% predicted), representing moderate airflow limitation. Most studies excluded participants with comorbidities such as cardiovascular disease, pulmonary hypertension, and neurologic or orthopedic problems limiting exercise.

Four studies18192022 reported ≥ 90% attendance at exercise sessions, and another study24 reported 77% attendance over a 6-month period. Participant attrition rates were reported in six studies171820222324 and were generally < 20% (Table 3 ). The main reasons reported for participants failing to complete studies were as follows: hospitalization, lack of motivation, death, surgery, changes in treatment, other medical conditions, and injury unrelated to training. No studies reported any adverse events or participants failing to complete as a direct result of strength training regimes.


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  		Table 3.. ICF Factors Across Studies*

 
Impairments
The ICF describes impairments as significant deviations or loss with regard to body structure or function.15

Changes in Muscle Strength: Effect sizes and 95% CIs for upper body strength were determined from three studies (Fig 3 ).171820 Figure 3 clearly indicates a positive effect favoring treatment, supported by metaanalysis ({delta} = 0.70; 95% CI, 0.28 to 1.11; z = 3.30, p < 0.001). Knee extensor strength was commonly reported, with five studies1718202124 providing sufficient data to calculate effect sizes (Fig 4 ). Resistance training showed a positive effect on knee extensor strength ({delta} = 0.90; 95% CI, 0.42 to 1.38; z = 3.65, p < 0.001).



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  		Figure 3.. Effect sizes and 95% CIs: upper body strength. lat dorsi = latissmus dorsi; pec = pectoralis.

 
Changes in Muscle Cross-sectional Area: A significant 8% increase in bilateral quadriceps cross-sectional area was reported in the one study20 reporting this measure. However, this difference translated into a small effect size (d = 0.2; 95% CI, – 0.02 to 0.43).

Respiratory Function: A number of measures of respiratory function were reported across studies, with calculation of effect sizes limited to four studies.16181924 Significant baseline differences excluded one study18 from analysis. Overall, respiratory function did not appear to change after strength training, as represented by effect sizes and CIs traversing zero (Table 4 ).


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  		Table 4.. Effect Sizes (95% CIs) for Other Outcome Measures*

 
Maximal Exercise Capacity: Six studies provided measures including aerobic capacity (maximal oxygen consumption [O2]), minute ventilation (E), and peak watts during incremental ergometry cycle testing. Two studies1720 were excluded from analysis because of baseline differences during ergometry cycle testing. In general, most studies found strength training did not change maximal exercise capacity (Table 4).

Changes in Psychological Function: Four studies17192024 using the chronic respiratory disease questionnaire (CRDQ)29 provided sufficient data to calculate effect sizes. Overall, effect sizes and CIs did not reflect changes after strength training (Table 4). The Health Status Questionnaire 2.0 (Short Form-36 Health Status Questionnaire [SF-36])30 has eight domains, of which five can be thought to represent measures of psychological function (health perception, health role limitations, emotional role limitations, mental health, and vitality). Four of these domains, not health perception, demonstrated large effect sizes, supporting treatment.23

Changes in Activity
Activity refers to performance of a particular task or action by an individual.15

Walking Endurance: Walking performance was assessed in seven studies using one of three measures: 6-min walk test (6MWT),181920232431 12-min walk test (12MWT),1632 and shuttle walk test.1733 Data were excluded from one study.18 The evidence for improved walking performance after strength training is weak, with four of six studies16171924 demonstrating small effect sizes and CIs traversing zero (Table 4).

Cycling Endurance: Submaximal cycling endurance was measured in three studies.171819 A large effect size (d = 4.42; 95% CI, 3.46 to 5.38) was found when strength training was compared with a no-treatment control group.18 In two other studies,1719 where strength training was compared against endurance training, an effect favoring the control condition (endurance training) was found (d = – 1.09; 95% CI, – 1.02 to – 0.46; and d = – 0.74, 95% CI, – 1.36 to – 0.81, respectively).

Health Status (Physical Function Domain): A large effect favoring treatment was found for one study23 reporting this measure, as assessed by the SF-3630 (d = 1.64; 95% CI, 1.23 to 2.05).

Changes in Participation
Participation is defined by the ICF as involvement in life situations.15 The societal function domain of the SF-3630 was used in one study,23 and a positive effect favoring treatment is indicated by the large effect size (d = 1.41; 95% CI, 1.00 to 1.82). However, another study22 found no effect for participation after strength training when assessed with the St. George Respiratory Questionnaire (SGRQ) [d = – 0.37; 95% CI, – 0.75 to 0.01).34 For the purposes of this review, the SGRQ was considered a participation measure, as greatest weighting during scoring is given to items relating to the impact of COPD on daily life, for example the effect on the ability to work.

Long-term Outcomes
Two studies examined the longer term effects of strength training, assessing subjects 12 weeks17 and 12 months after completion of program24; in both studies, effect sizes were similar to those at program completion (Table 4).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusions
 References
 
The typical program structure used in the empirical studies reviewed was similar to strength training guidelines for healthy young adults35 and protocols applied to healthy older adults.36 However, training intensity was somewhat greater than American College of Sports Medicine strength training guidelines for older adults.35 Despite variation from the guidelines, adverse events for people with COPD were not reported in any of the studies reviewed. Therefore, strength training appears to be safe and appropriate for use in pulmonary rehabilitation. However, given subjects in most studies were thoroughly screened for other health conditions, careful consideration is required when prescribing progressive resistance programs for people with COPD where comorbidities exist.

Pulmonary rehabilitation programs teach participants how to exercise, with the hope exercise will be maintained as part of long-term disease management. One possible barrier to ongoing exercise is access to equipment. In most studies, preferential use of machine weights in outpatient clinics may preclude participants from continuing with training after the program. Use of free weights or resistance bands in the home setting may provide a simple, inexpensive, and practical means by which strength training programs can be maintained. As only one study16 investigated the feasibility and effectiveness of home-based strength training, further investigation is required comparing program setting on effectiveness, cost, and maintenance of strength training for people with COPD.

Changes in Impairment
Similar to studies3738 of other types of exercise training in COPD, respiratory function does not appear to be modified or changed by strength training. Therefore, it is likely improvements in exercise tolerance following training in COPD are related to other factors, such as changes in muscle structure and function. Despite evidence indicating strength training can induce skeletal muscle hypertrophy in healthy older adults,36 only minor changes were detected for people with COPD,20 which could reflect differences in training type and intensity, sample size, or disease-related factors. In contrast, changes in muscle function were more positive, with appreciable increases in muscle strength providing evidence that resistance training is a means of tackling muscle weakness in this population.

When compared with American College of Sports Medicine guidelines for improving cardiovascular fitness,39 strength training in isolation would appear unlikely to cause changes in aerobic capacity.40 A recent metaanalysis36 of strength training in healthy older adults indicated weak evidence for improved aerobic capacity after strength training. In the current review, examination of changes in cardiovascular fitness, after strength training, were hampered by differences in study design. Two studies2022 favored strength training. However, in one study,20 strength exercises were combined with aerobic training; in the other study,22 the large effect size may have been overestimated due to lack of blinding and a large attrition rate in the control group. Another two studies1719 compared strength training against endurance training, possibly masking an effect for strength training if it were present. It appears unlikely that isolated strength training would lead to changes in cardiovascular fitness for people with COPD; however, more conclusive evidence is required.

A large affective component has been attributed to impaired exercise tolerance and functional status in COPD.374142 Therefore, psychological benefits gained through exercise training may be just as important as any physiologic changes. For the included studies, psychological changes were generally examined as part of health-related quality of life (HRQL) measures. Despite extraction of psychological domains during analysis, the use of different HRQL measures, different reporting methods, and the broad-based nature of HRQL scales,43 the effect of strength training on psychological variables was unclear. While it has been shown that HRQL measures correlate well with exercise tolerance for people with COPD,44 it is not indicative of the contribution of psychological factors. Greater understanding of the effects of exercise training on psychological factors, and indeed HRQL, may occur by improved definition and delineation of these factors prior to selection of outcome measures.

An area not examined by any of the included studies was the effect of strength training on bone mineral density. Long-term oral steroid use in patients with COPD can affect bone health, leading to osteoporosis. Positive trends for improved bone mineral density after strength training in healthy older adults have been found,36 warranting further consideration for people with COPD.

Changes in Activity
Overall, the findings of this review provide no clear evidence that strength training leads to changes in activity. However, study design features, such as comparison with endurance training,19 and combined programs of strength and aerobic training,202324 made it difficult to determine the impact of resistance training on measures of activity. Also, the majority of studies examined activity using two measures, walking and cycling endurance. It could be argued these measures examine exercise performance, and may not accurately reflect activity limitations. However, a positive effect for activity was seen when a more generalized measure of physical function (SF-36) was used in one study.23 Therefore, a broader range of measures, reflecting activities of daily living and functional performance need to be examined.

Walking remains an important measure; however, current field walking tests may not adequately reflect walking needs or abilities in daily life.45 Muscle weakness has been correlated with increased risk of falls and fractures,4647 which have the potential to increase morbidity, dependence, and health system burden. Positive effects for strength training on dynamic balance have been shown in healthy older adults36 and need to be examined in COPD. Another area that may reflect activity limitation in COPD is upper limb function. Limitations in upper limb activities have the potential to impair self care and independence, and should be examined as part of the strength training literature.

Changes in Participation
Whether strength training improves the ability of people with COPD to participate in normal everyday life situations is not known. Variability in the findings of studies in this review may reflect design features such as no control group,23 a measurement scale not limited to participation measures,2234 and lack of blinding. For improvements after strength training to be meaningful for people with COPD, they need to translate into changes in activity and participation.

Long-term Outcomes
The long-term benefits of strength training require further investigation, as preliminary examination reveals training gains may be maintained to an extent.1724 What was not examined during follow-up in these studies was whether participants performed exercise between testing. It could be argued participants guided through a training program were more likely to continue with some form of exercise because of experience and increased motivation, compared with a control group lacking training experience. Understanding how well changes after training are maintained or what level of exercise is required to sustain them is important in the development of pulmonary rehabilitation programs.

Review Articles
One of the problems associated with all reviews is the potential for the author’s subjective judgements to influence the review outcome. Potential sources of bias in a review include study identification and selection, quality assessment, data synthesis, and interpretation. Systematic reviews aim to reduce bias by making each part of the process explicit and reproducible.10 All review articles examined had an increased potential for bias as traditional, descriptive review formats were used. Despite this, the general consensus from these reviews was that evidence for strength training for people with COPD exists, with a need for more controlled clinical trials. The findings of the current review support this consensus.


   Conclusions
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
References
 
This review found evidence resistance training in people with COPD can produce increases in upper and lower limb strength. Furthermore, strength training protocols appeared feasible for people with COPD. High levels of adherence were reported, and few (if any) adverse events were associated with the intervention. The findings were inconclusive for other outcome measures such as aerobic capacity, walking endurance, and psychological and respiratory function. A key area requiring further investigation is the impact of strength training programs on the functional performance of people with COPD in everyday situations, as increasing strength will be more meaningful if it is associated with increased activity and societal participation. Broadening the examination of activity limitations to include measures such as balance, upper-limb function, and self care may facilitate greater understanding of the role of strength training for people with COPD.



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  		Figure 4.. Effect sizes and 95% CIs: knee extensor strength.

 

   Footnotes
 
Abbreviations: CI = confidence interval; CRDQ = chronic respiratory disease questionnaire; HRQL = health-related quality of life; ICF = International Classification of Functioning; PEDro = physiotherapy evidence database; SF-36 = Short Form-36 Health Status Questionnaire; SGRQ = St. George Respiratory Questionnaire; E = minute ventilation; O2 = oxygen consumption; 1RM = one repetition maximum; 6MWT = 6-min walk test; 12MWT = 12-min walk test

Received for publication July 30, 2003. Accepted for publication November 20, 2003.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 

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M D L Morgan
Peripheral muscle training in COPD: still much to learn
Thorax, May 1, 2005; 60(5): 359 - 360.
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