Journal of Cardiopulmonary Rehabilitation & Prevention:
Association Between Peripheral Muscle Strength and Daily Physical Activity in Patients With COPD: A SYSTEMATIC LITERATURE REVIEW AND META-ANALYSIS
Rausch Osthoff, Anne-Kathrin MSc; Taeymans, Jan PhD; Kool, Jan PhD; Marcar, Valentine; van Gestel, Arnoldus J.R. PhD
Department of Physiotherapy, Zurich University of Applied Sciences (ZHAW), Winterthur, Switzerland (Ms Osthoff and Drs Kool, van Gestel, and Marcar); and Bern University of Applied Sciences, Bern, Switzerland (Dr Taeymans).
Correspondence: Anne-Kathrin Rausch Osthoff, MSc, Department of Physiotherapy, Zurich University of Applied Sciences, Technikumstrasse 71, 8401 Winterthur, Switzerland (firstname.lastname@example.org).
None of the authors has a conflict of interest related to the content of the manuscript.
None of the authors received any funding.
BACKGROUND: Patients with chronic obstructive pulmonary disease have skeletal muscle dysfunction and reduced daily physical activity (PA). Whether the reduction in quadriceps strength (QS) is directly linked to physical inactivity remains to be elucidated.
METHODS: A systematic review and a meta-analysis were conducted to determine the potential relationship between QS and the level of PA. The overall estimate of the correlation coefficient (r *) was calculated, and a subgroup analysis was conducted to analyze the association between QS and indices of PA separately.
RESULTS: A total of 8 studies were included in the meta-analysis. The overall association between QS and PA was low but highly significant (r * = 0.288, 95% CI = 0.180–0.389; P < .001). In the subgroup analysis, the association between QS and the number of steps per day was low (r = 0.260; 95% CI = 0.060–0.440) and the association between QS and the time spent walking was moderate (r = 0.418; 95% CI = 0.229–0.576).
CONCLUSIONS: Peripheral muscle strength is associated with PA as assessed by the number of steps per day and the time spent walking in patients with chronic obstructive pulmonary disease. The overall association between QS and PA was low to moderate and highly significant.
Physical inactivity in daily life is a prominent feature in patients with chronic obstructive pulmonary disease (COPD).1–5 The amount of physical activity (PA) gradually declines with severity of disease5–7 and may deteriorate even more over time because of factors such as acute exacerbations.2,8 Furthermore, several studies have demonstrated that the level of PA is associated with hospitalization4,8,9 and is known as the strongest predictor of all-cause mortality4,10 in patients with COPD.
Physical inactivity has become a topic of interest since the American Thoracic Society and European Respiratory Society11 underlined the importance of promoting long-term self-management and adherence to exercise in the home setting in patients with COPD. In addition, results from the PERCEIVE Study indicated that patients' perceptions of their COPD impacted the activities of daily living.12
It has been clearly demonstrated that patients with COPD have skeletal muscle dysfunction13–16 and therefore resistance training of peripheral muscles has been recommended during pulmonary rehabilitation (PR) in these patients.11,17,18 However, there is an eloquent difference between functional capacity status and daily PA as the latter may be elicited by the habitual and environmental factors of sedentary patients.19 To be meaningful for patients with COPD, improvements in peripheral muscle strength need to be translated into changes in PA and participation in everyday situations.
The impression gained from the literature is that uncertainty exists whether the reduction in muscle strength observed in patients with COPD is directly linked to physical inactivity. Therefore, we conducted a meta-analysis to summarize the current evidence on physical inactivity in patients with COPD and to determine the potential relationship between peripheral muscle strength and the level of PA in these patients. As the quadriceps muscles are the most commonly used muscles in clinical research14 and quadriceps strength (QS) is associated with both the degree of airflow limitation20 and exercise capacity,20,21 we included studies that assessed QS to reflect peripheral muscle strength in the present meta-analysis.
Study identification commenced by electronic searching, using the MEDLINE (through PubMed), CINAHL, Cochrane Library, PEDro, EMBASE databases, and Google scholar, on articles published between January 1, 1990, and December 31, 2012. Search terms used were as followed: “Pulmonary Disease, Chronic Obstructive” (MeSH) OR “chronic obstructive pulmonary disease” (Text Word) OR “COPD” (Text Word) AND “Activities of Daily Living” (MeSH) OR “Physical Activity” (Text Word) OR “Muscle” (MeSH) OR “Muscle, skeletal” (MeSH) OR “Muscle Strength” (MeSH) OR “Muscle Strength Dynamometer” (MeSH) OR “Quadriceps Muscle” (MeSH) OR “Peripheral Muscle Strength” (Text Word). An additional search for gray literature on issue-specific databases,22–24 citation tracking, and key author searches was conducted.
The following criteria were applied to determine the eligibility of each study for inclusion in the meta-analysis:
* Studies had to pertain patients with COPD (GOLD Stages I–IV),
* studies must include at least 1 measure of QS and 1 explicit measure of PA,
* studies must report the correlation coefficient reflecting the level of association between these variables, and
* studies had to be published in English, German, or Dutch.
To avoid duplication, data were not included if they had already been reported in previously published work. There was no restriction concerning sample size or study design. Two reviewers independently evaluated records for eligibility. Disagreement was resolved by discussion and consensus.
Two reviewers independently analyzed the quality of the included studies as recommended by the guideline of Meta-analysis of Observational Studies in Epidemiology (MOOSE).25 Accordingly, the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement was used to analyze both the quality of reporting and the authors' “appraisal of risk of bias.”26,27
Descriptive data for continuous variables were expressed as mean and standard deviation. To determine the potential relationship between QS and the level of PA, 2 meta-analyses with correlation coefficients were conducted. Four different indices of PA were used as proxies for PA in the individual studies: (1) the scores of PA-questionnaires, (2) the number of steps per day, (3) the PA level, and (4) the time spent walking. Three studies28–30 presented 2 different indices of PA. In multiple outcome studies, correction for the fact that groups are not independent (ie, outcomes of the same participants were assessed with more than 1 method) has been recommended by Borenstein et al.31 Accordingly, the results of these multiple outcome studies were “collapsed” and then included in the overall meta-analysis. The overall estimate of the correlation coefficient (r *coll) was calculated by using the correlation coefficients of the 8 studies.
Another way to correct for not following the assumption of independency is to include the results of the different outcomes of PA in 4 different subgroups. In this subgroup analysis, the overall estimate of the correlation coefficient (r *pool) was calculated by pooling the 4 correlation coefficients of the subgroups. Appropriate data were pooled using the DerSimonian and Laird random-effects model that accounts for both within- and between-study variation.32
Test for Publication Bias
It has been discussed elsewhere that publication bias is not very informative if fewer than 10 studies are included in a meta-analysis.33 However, for the completeness of the present meta-analysis, a publication bias analysis was conducted for the 8 studies based on their “collapsed” data.
Test for Heterogeneity
To assess heterogeneity, the Q-statistic and its P value were calculated. I2 was calculated as a mass of between-study variability (for each set of effect sizes) according to Borenstein et al31 and Higgings et al.34
All statistical analyses were conducted with CMA-235 (Biostat, Englewood, NJ) software. The level of significance was set at 5%.
Figure 1 summarizes the selection process for this systematic review and meta-analysis. A total of 1649 articles were identified using the MEDLINE (through PubMed), CINAHL, Cochrane Library, PEDro, and EMBASE databases. From these studies 1640 articles were excluded because they did not meet the inclusion criteria. Disagreements about the inclusion of 2 studies were resolved by 2 review authors. The study of Pitta et al36 did not analyze the association between QS and PA and was consequently excluded. Coronell et al37 did investigate the association between QS and PA but failed to report a correlation coefficient.
A total of 9 studies8,28–30,37–41 investigated the association between daily PA and QS in patients with COPD (GOLD I–IV) and were used for the present review. Eight studies were included for further analysis in the meta-analysis (Table 1). The quality of reporting and the authors' appraisal of risk of bias of the 9 included studies (STROBE) were of sufficient methodological quality (Table 1).26,42
Assessments of QS and PA
In all studies, the strength of the peripheral muscles was quantified by assessing the strength of the quadriceps muscle (QS). The latter was assessed by the measurement of maximal voluntary strength (maximal voluntary contraction) and reported as kilograms (kg), newtons (N), or as percentage of predicted value (QS, %pred). Different devices such as a dynamometer or oscillograph were used. Maximal voluntary contraction was measured with the patients' knee and hip both flexed at 90°,28–30,38 as described by Edwards et al.43 Pitta et al8,41 measured QS with the patients' knee in 60° flexion.8,41 The different methods used to assess daily PA were self-reported questionnaires44,45 and different accelerometers such as DynaPort (McRoberts, the Hague, the Netherlands),8,39,41Actiwatch (Cambridge Neurotechnilogy, Cambridge, UK),28SenseWear Pro (BodyMedia, Pittsburgh, PA),29,30 and RT3 (Stay Healthy Inc, Monrovia, CA).40
Overall Meta-analysis of the Association Between QS and PA
The results of the overall meta-analysis are presented in Figure 2. The overall estimate of the correlation coefficient as analyzed with the “collapsed” method (r *coll) was 0.305 (95% CI = 0.175–0.425; P < .001), while with the pooled subgroup, the estimate of the correlation coefficient (r *pool) was 0.288 (95% CI = 0.180–0.389; P < .001). Hence, the use of both methods leads to very similar, positive, low to moderate but highly significant overall correlation coefficients.
Association Between QS and Subgroups Reflecting PA
Three studies28,37,38 assessed PA by using self-reported questionnaires. Two studies37,38 used Baeck's questionnaire modified for elderly and 1 study28 applied the Nottingham Extended Activities of Daily Living questionnaire. The calculated estimate of the correlation coefficient in the first subgroup was low, positive, but not significant (r = 0.267; 95% CI =−0.101 to 0.570) (Figure 2). The result of the Q-test for heterogeneity in this subgroup was not significant (Q = 1.369; df = 1; P = .242) while I2 was 26.9%.
Two studies29,30 used the SenseWear Pro accelerometer to measure both the number of steps per day and the physical activity level (PAL). In the second subgroup, the calculated estimate of the correlation coefficient between QS and the number of steps per day was low, positive, and significant (r = 0.260; 95% CI = 0.060–0.440). In this subgroup, no between-studies heterogeneity was observed (Q = 0.427; df = 1; P = 0.514 and I2= 0.0%).
The calculated estimate of the correlation coefficient between QS and PAL of the third subgroup was low, positive, but not significant (r = 0.191; 95% CI =−0.012 to 0.380). In this subgroup, the results of the Q-test for heterogeneity were significant (Q = 7.277; df = 1; P = .007) while I2 was 86.3%.
Five studies investigated an association between time spent walking and QS. Although 3 studies8,28,39 failed to demonstrate a significant association between QS and PA, a moderate, positive, and highly significant (P < .0001) estimate of the correlation coefficient was found in the fourth subgroup analysis (r = 0.418; 95% CI = 0.229–0.576). In addition, no between-studies heterogeneity was observed (Q = 2.783; df = 4; P = .595 and I2= 0.0%).
Under random effects conditions, the funnel plot is symmetric (the trim and fill algorithm calculated no missing study) while the fail'n safe algorithm found that another 57 nonsignificant studies would be needed to bring the overall effect size to a level of P = .05 (Figure 3).
In this study, we conducted a meta-analysis to determine the potential relationship between peripheral muscle strength and the level of PA in patients with COPD. Physical activity as assessed by the number of steps per day and the time spent walking showed low to moderate associations with QS in patients with COPD. The overall estimate of the association between QS and PA was low to moderate but highly significant. The conclusion of this meta-analysis, however, should be interpreted with caution because of several methodological limitations.
It is well recognized that PA in daily life plays an important role in terms of disability and mortality in patients with COPD.4,8–10 There are strong indications that PA is reduced in patients with COPD and that the amount of PA gradually declines with severity of disease.6,7 Given the multiple health benefits of sufficient PA in daily life, it is important to determine possible factors that would be capable of increasing PA in patients with COPD.
Resistance training of peripheral muscles has been recommended during PR for increasing peripheral muscle strength in patients with COPD.11,17,46 In a review including 18 controlled trials, O'Shea47 concluded that resistance training increases muscle strength that may carry over to improved daily tasks such as stair-climbing, sit-to-stand, and arm elevation activities. However, in previous research we found that these laboratory-based tests cannot be used to accurately reflect the abilities of daily activities in patients with COPD.48 This discrepancy may be due to external factors, such as effort spent, motivation, the instructions, and encouragement given to the subjects participating in these laboratory-based tests.48 Recently, the Global Initiative for Chronic Obstructive Lung Disease49 stated that increased participation in physical and social activities of daily living should receive priority in the management of patients with COPD. To address this recommendation, it may be useful to investigate to what extent peripheral muscle strength contributes to PA in patients with COPD.
Association Between QS and Questionnaire-Based PA
Systematic review and meta-analysis of 3 studies28,37,38 demonstrated that there is no association between QS and PA as assessed by questionnaires in patients with COPD. In addition, the use of self-reported activity questionnaires has been challenged as a poor measure of actual PA in daily life.50 Self-reported activity questionnaires have limited validity and reliability51 and correlate only poorly with objectively quantified PA in patients with COPD.52,53 It has been speculated that the weak association between self-reported activity and actual PA may be due to the effect of social desirability and social approval on self-reports.54 In addition, impaired memory,55 the possibility of misreporting activity time,56 or unnoticed movements52 may also influence accurate recall of the type, intensity, frequency, and duration of daily PA.
Association Between QS and the Number of Steps Per Day
Multiaxial accelerometers are sophisticated devices that quantify the intensity of movements by detecting motion in more than 1 plane of movement.57 The accelerometer is known to be the most accurate field-based estimate of PA.58 Recently, van Remoortel et al59 compared the validity of 6 activity monitors in 39 patients with COPD (GOLD I–IV). The DynaPort MiniMod, Actigraph GT3X, and SenseWear Pro accelerometer were identified as the most valid devices during standardized physical activities like standing, sitting, and walking in different paces.
Systematic review and meta-analysis of the 2 studies that used the SenseWear Pro accelerometer29,30 demonstrated that the association between QS and the number of steps per day in patients with COPD is significant, but low. Since it has been suggested that a minimal of 10 000 steps per day is recommended for health promotion in the general population,60,61 it may be postulated that increasing QS may be useful to address this recommendation. However, it should be stressed that no causality or directionality of the findings can be inferred in this study. Therefore, improvement in QS does not necessarily cause the number of steps per day to increase in these patients. Furthermore, it has been demonstrated that using the number of steps per day may underestimate the amount of PA, particularly when the walking speed of patients is rather low.62
Association Between QS and the PAL
Although Waschki et al30 demonstrated that the PAL is independently associated with QS, the results of the overall meta-analysis did not suggest any association. During slow-to-moderate paced walking in a laboratory setting accelerometers provide valid63,64 and reliable52,64 estimates of energy expenditure (EE) in patients with COPD. However, there are limitations for using accelerometers to estimate EE in daily life in these patients.65 Because most accelerometers are unable to detect energy cost from upper body movement, load carriage, or changes in surface or terrain, EE estimation depends on the type of activity performed.66 During activities such as upper arm exercise and cycling, the use of accelerometers to estimate EE may be less accurate.67
Association Between QS and Walking Time
In this study, we found that QS was moderately correlated with the time patients with COPD spent walking in daily life. Recently, it has been demonstrated that the majority of patients with moderate to very severe COPD walk more than 30 minutes per day.68 Because most patients with COPD walk very slowly, the authors underline the fact that this does not mean that they are physically active.
Does PR Improve PA in Patients With COPD?
Research has demonstrated that PR is beneficial to patients with COPD as it improves exercise capacity and locomotor muscle strength.69,70 Although the main purpose of PR should be enhancing PA,71 few studies have investigated the impact of PR on PA in patients with COPD. Pitta et al72 assessed PA at baseline, after 3 months, and at the end of a 6-month multidisciplinary rehabilitation program in 29 patients with COPD. Although 3 months of PR improved exercise capacity and QS in patients with COPD, these improvements did not result in patients spending more time walking in daily life. After an additional 3 months of PR (ie, 6 months in total), daily PA had increased.72 However, it would be more powerful to determine whether improvements in QS during PR are associated with improvements in PA. Unfortunately, only 1 study addressed this issue and analyzed the impact of PR-induced improvements in QS on improvements in PA.40 In that study, PR-induced improvements in QS did not predict changes in PA, which suggests that improvements in QS do not translate simply into improvements in level of activity.
Since QS was found to be associated with both the number of steps per day and the time spent walking in this meta-analysis, the factor “walking speed” could be neglected on the basis of the topic of this study. Because of the highly significant association between QS and PA in this study, we wish to underline the importance of increasing peripheral muscle strength in patients with COPD. Since decreasing patient activity level is an early consequence of COPD, it may be postulated that resistance training of peripheral muscles should be implemented from the early stages of the disease. Recently it has been demonstrated that walking intensity is a significant predictor of disease severity in patients with COPD.73 Future research should focus on the impact of resistance training of peripheral muscles on the intensity of PA in these patients.
This study has certain limitations that need to be taken into account. The design of this study does not allow the establishment of a causal relationship between QS and PA. Decreased PA often clusters with established risk factors, such as older age, impaired lung function, decreased cardiopulmonary exercise capacity, less motivation, and the presence of comorbidities in patients with COPD. This makes disentangling the independent effects of reduced QS on PA a daunting task. In addition, the included studies all have a cross-sectional design. Randomized controlled interventional studies are needed to investigate the predominant role of QS on daily PA and to assess the clinical usefulness of training peripheral muscles in patients with COPD. Furthermore, it should be stressed that the methods used to quantify peripheral muscle strength were very different.
To the best of our knowledge, there is no existing gold standard to evaluate the internal and external validity of observational studies.74–76 Despite the fact that the STROBE has been challenged,26 we implemented the STROBE in this study. Because the number of studies in this meta-analysis was very small, the estimate of the between-studies variance (I2) has poor precision. Additional potential sources of bias in this review included study identification and selection, quality assessment, data synthesis, and interpretation.
The available information suggests that PA as assessed by the number of steps per day and the time spent walking showed low to moderate, but significant associations with QS in patients with COPD. The overall association between QS and PA was low to moderate and highly significant.
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accelerometer; COPD; meta-analysis; peripheral muscle strength; physical activity
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