Abstract
BACKGROUND: The goal of this study was to evaluate the effects of resistance training on subjects with COPD.
METHODS: We performed a systematic search in MEDLINE, PubMed, Embase, CINAHL, Elsevier ScienceDirect, EBM Reviews, Cochrane Central Register of Controlled Trials, and ClinicalTrials.gov and also of leading respiratory journals for randomized controlled trials on COPD treatment for ≥ 4 weeks with resistance training compared with non-exercise control or with combined resistance and endurance training compared with endurance training alone. Data from these studies were pooled to calculate odds ratio and weighted mean differences (WMDs) with 95% CI.
RESULTS: Eighteen trials with 750 subjects with advanced COPD met the inclusion criteria. There were 2 primary and 5 secondary outcomes. Compared with non-exercise control, resistance training led to significant improvements in the dyspnea domain of the Chronic Respiratory Disease Questionnaire (WMD of 0.59, 95% CI 0.26–0.93, I2 = 0%, P < .001), skeletal muscle strength, and percent-of-predicted FEV1 (WMD of 6.88%, 95% CI 0.41–13.35%, I2 = 0%, P = .04). The combination of resistance and endurance training significantly improved the St George Respiratory Questionnaire total score (WMD of −7.44, 95% CI −12.62 to −2.25, I2 = 0%, P = .005), each domain score, and skeletal muscle strength. There were no significant differences in 6-min walk distance, 6-min pegboard and ring test, maximum exercise work load, and maximum oxygen consumption between the 2 groups. There were no reports of adverse events related to resistance-training intervention.
CONCLUSIONS: Resistance training can be successfully performed alone or in conjunction with endurance training without increased adverse events during pulmonary rehabilitation in COPD.
Introduction
COPD is a major cause of chronic morbidity and mortality throughout the world and is projected to be the third most common cause of death by 2020.1 Exercise intolerance is a cardinal complaint of patients with COPD. Skeletal muscle dysfunction is a common extrapulmonary manifestation of COPD.2 Studies suggest that skeletal muscle dysfunction is associated with exercise limitation and health-care utilization.3,4 Skeletal muscle dysfunction is also an independent predictor of morbidity and mortality in COPD,5 irrespective of the degree of air-flow limitation. Muscle changes observed in patients with COPD include reductions in type I fibers, atrophy of type I and II fibers, reduced capillarity, and altered metabolic enzyme levels.6 The pathogenic mechanisms of skeletal muscle dysfunction are considered to be related to multiple factors, including nutritional abnormalities, muscle disuse, systemic inflammation, medical use of corticosteroids, tissue hypoxia, and hypercapnia.6,7
Progressive resistance training provides a training modality for increasing peripheral muscle strength in COPD. Ortega et al8 reported that the increase in muscle strength obtained after resistance training is higher than that obtained after endurance training. In addition, resistance training evokes less dyspnea during exercise,9 thereby making this strategy easier to tolerate than endurance training.10,11 A combination of resistance and endurance training in COPD has demonstrated a greater improvement in peripheral muscle function compared with endurance training alone.12
In the past few years, there have been several systematic reviews on the efficacy of resistance training.13–16 However, previous meta-analyses focused on whether resistance training is effective in improving skeletal muscle strength and lung function, whereas little data are so far available on other clinically relevant outcomes, such as quality of life, dyspnea, and exercise capacity. Moreover, previous analyses13–15 included both randomized controlled trials (RCTs) and case-control trials, which potentially introduced bias because the real-world outcomes of pulmonary rehabilitation can be affected by a number of social and cultural factors. Finally, many RCTs have been published since the previous meta-analysis conducted by O'Shea et al14, offering input for more extensive analysis.17–23 The aim of this meta-analysis was to investigate the effects of resistance training alone or combined with endurance training on clinically relevant rehabilitation outcomes in advanced COPD, including quality of life, dyspnea, functional exercise capacity, maximum exercise capacity, skeletal muscle function, lung function, and adverse events.
QUICK LOOK
Current knowledge
COPD is a major cause of chronic morbidity and mortality throughout the world and is projected to be the third most common cause of death by 2020. Skeletal muscle dysfunction is associated with exercise limitation and increased health-care utilization. The impact of respiratory muscle training in COPD has met with conflicting results.
What this paper contributes to our knowledge
A meta-analysis showed that dyspnea scale scores, skeletal muscle strength, and lung function improved following resistance training. Although skeletal muscle strength and quality of life improved following combined resistance and endurance training, this failed to translate into improved exercise capacity. The data suggest that resistance training can be successfully performed alone or in conjunction with endurance training without increasing adverse events during pulmonary rehabilitation.
Methods
Data Sources
We searched MEDLINE, PubMed, Embase, CINAHL, Elsevier ScienceDirect, EBM Reviews, Cochrane Central Register of Controlled Trials, ClinicalTrials.gov and leading respiratory journals and conference abstracts from January 1980 to October 2013 to identify related articles. We also searched the Science Citation Index database (Web of Science) and PubMed using the related-articles function by entering all included studies. Reference lists from original and review articles were also reviewed to identify additional relevant studies. All publications and abstracts in English were considered. Moreover, an additional search in May 2014 was performed to identify additional trials that fulfilled our search criteria.
The search terms were as follows: COPD, chronic obstructive pulmonary disease, chronic obstructive lung disease, chronic airways limitation, chronic airways obstruction, chronic bronchitis, and pulmonary emphysema. These terms were used in various combinations with strength training, strength exercise, resistance training, resistance exercise, weight training, weight lifting, aerobic training, aerobic exercise, endurance training, endurance exercise, exercise training, and pulmonary rehabilitation.
Study Selection
The inclusion criteria were: (1) subjects with stable moderate-to-very-severe COPD without other lung diseases; (2) RCTs comparing resistance training with non-exercise control or combined resistance and endurance training with endurance training alone; (3) exercise duration of at least 4 weeks; (4) outcomes including health-related quality of life, dyspnea scale, functional exercise capacity, maximum exercise capacity, skeletal muscle function, and pulmonary function; (5) human studies; and (6) English language.
Quality Assessment
The methodological quality of each study was assessed by the modified Jadad scale,24 which scores trials according to randomization, concealment of allocation, double blinding, withdrawals, and dropouts.
Data Extraction
Data extraction was based on reported statistics (means, SD, and SE). Two reviewers (WL and JC) independently extracted data from the selected studies. If a disagreement arose, all authors conferred until a consensus was achieved. Authors of a publication were contacted if only the abstract was available or data were missing. Supplemental data for included studies were reviewed to minimize selective reporting of secondary end points in published manuscripts. Primary outcomes were changes from baseline in health-related quality of life and dyspnea scale. Secondary outcomes included changes from baseline in skeletal muscle function, functional exercise capacity, maximum exercise capacity, FEV1, and adverse events.
Statistical Analysis
RevMan 5.2 (The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark) was used to analyze all collected data. Fixed-effects odds ratios for dichotomous outcomes and weighted mean differences (WMDs) for continuous outcomes, with corresponding 95% CI, were calculated for individual trials. The trials were pooled using fixed-effects odds ratios or WMDs as appropriate. I2 was calculated to efficiently test heterogeneity, with values of 25, 50 and 75% considered to represent low, moderate, and high heterogeneity, respectively. The differences between resistance-training groups and non-exercise control groups or resistance-and-endurance-training groups and endurance-training-alone groups were pooled using a fixed-effects model when there was no evidence of significant heterogeneity in the analysis. If significant heterogeneity was found, a random-effects model was used.25
Results
Search Results
The process used for searching and selecting trials is presented in Figure 1. Of the 3,562 English articles screened, we excluded 3,544 that were not relevant, had incomplete or duplicate data, or were not RCTs. Eighteen parallel RCTs involving 750 subjects met the inclusion criteria and were selected for analysis. Thirteen of the 18 included trials compared resistance training with non-exercise control, and 4 trials compared combined resistance and endurance training with endurance training alone. One trial compared resistance training, endurance training, combined resistance and endurance training, and non-exercise control. The main characteristics of these trials are listed in Tables 1 and 2. All data adopted in this study were published openly in various journals.
Flow chart. RCT = randomized controlled trial.
Subject Characteristics
Included Studies
Quality Assessment
The methodological quality of the included studies is provided in Table 2. There were 8 studies with Jadad scores of ≥ 3 points. Ten trials scored poorly according to the modified Jadad scale. Eight trials reported blinding methods. Of these, 6 trials reported blinding of the investigators or outcome assessors, and 2 trials reported blinding of both outcome assessors and subjects with COPD. Per-protocol analysis was used in 16 trials, and intention-to-treat analysis was used in 2 trials.
Primary Outcomes
Chronic Respiratory Disease Questionnaire Score
Resistance-Training Group Versus Non-Exercise Control Group.
Three studies reported dyspnea domain scores using the Chronic Respiratory Disease Questionnaire (CRQ).18,19,32 The results of each study showed significant improvements in CRQ dyspnea domain scores in the resistance-training groups. The overall analysis showed statistically significant improvements in CRQ dyspnea domain scores in the resistance-training groups (WMD of 0.59, 95% CI 0.26–0.93, I2 = 0%, P < .001). The improvement in dyspnea domain scores achieved a minimum clinically important difference of 0.5 units.37 Two included trials reported CRQ fatigue domain scores, whereas the pooled analysis showed no significant improvements in fatigue domain scores (WMD of 0.26, 95% CI −0.11 to 0.64, I2 = 5%, P = .17).18,32 Only one study reported CRQ emotion and mastery domain scores.32 The results showed no significant difference in CRQ emotion domain scores (d = 0.20, 95% CI −0.20 to 0.60) and mastery domain scores (d = 0.10, 95% CI −0.33 to 0.53) between the 2 groups (Fig. 2).
Effects of resistance training vs non-exercise control on Chronic Respiratory Disease Questionnaire scores. IV = inverse variance weighting.
Resistance-and-Endurance-Training Group Versus Endurance-Training-Alone Group.
Only one trial reported each CRQ domain score.35 There were no significant differences in dyspnea domain scores (d = −0.60, 95% CI −1.23 to 0.03), fatigue domain scores (d = −0.30, 95% CI −1.18 to 0.58), emotion domain scores (d = 0.00, 95% CI −0.74 to 0.74), and mastery domain scores (d = 0.10, 95% CI −0.89 to 1.09) between the 2 groups.
St George Respiratory Questionnaire
Resistance-Training Group Versus Non-Exercise Control Group.
Only one included trial reported St George Respiratory Questionnaire (SGRQ) total scores and each domain score.20 The results showed no statistically significant improvements in SGRQ total scores (d = −3, 95% CI −14 to 8), symptom domain scores (d = −7, 95% CI −23 to 9), activity domain scores (d = −0.1, 95% CI −15 to 15), and impact domain scores (d = −3, 95% CI −16 to 10) in the resistance-training group.
Resistance-and-Endurance-Training Group Versus Endurance-Training-Alone Group.
Three studies reported SGRQ total scores,20,22,23 and 2 studies reported each SGRQ domain score.22,23 The results of 2 included studies showed significant improvements in SGRQ total scores, symptom domain scores, activity domain scores, and impact domain scores in the resistance-and-endurance-training group. The overall analysis showed statistically significant improvements in SGRQ total scores (WMD of −7.44, 95% CI −12.62 to −2.25, I2 = 0%, P = .005), symptom domain scores (WMD of −14.81, 95% CI −21.23 to −8.39, I2 = 0%, P < .001), activity domain scores (WMD of −25.27, 95% CI −31.46 to −19.08, I2 = 11%, P < .001), and impact domain scores (WMD of −8.23, 95% CI −15.31 to −1.15, I2 = 0%, P = .02), favoring the combination training (Fig. 3).
Effects of combined resistance and endurance training vs endurance training alone on St George Respiratory Questionnaire scores. IV = inverse variance weighting.
Secondary Outcomes
Skeletal Muscle Function
Resistance-Training Group Versus Non-Exercise Control Group.
The cumulative analysis showed significant improvements in knee extension strength (WMD of 7.78 kg, 95% CI 5.18–10.38 kg, I2 = 0%, P < .001),28,32,34 leg press strength (WMD of 16.67 kg, 95% CI 2.87–30.47 kg, I2 = 0%, P = .02),17,26,27,29,34 and shoulder flexion strength (WMD of 2.88 kg, 95% CI 0.56–5.20 kg, I2 = 0%, P = .01)19,32 in the resistance-training groups. However, the difference was not statistically significant in pectoral muscle strength (WMD of 2.29 kg, 95% CI −0.41 to 4.99 kg, I2 = 0%, P = .10) after resistance training (Fig. 4).17,26,32 Only one study measured latissimus dorsi strength, which showed a significant improvement (d = 2.50 kg, 95% CI −0.70 to 5.70 kg) in the resistance-training group.19
Effects of resistance training vs non-exercise control on skeletal muscle strength. IV = inverse variance weighting.
Resistance-and-Endurance-Training Group Versus Endurance-Training-Alone Group.
The cumulative analysis showed significant improvements in leg press strength (WMD of 12.34 kg, 95% CI 5.96–18.72 kg, I2 = 0%, P < .001)23,36 and pectoral muscle strength (WMD of 4.48 kg, 95% CI 2.53–6.43 kg, I2 = 0%, P < .001)23,35,36 in the resistance-and-endurance-training group compared with the endurance-training-along group. No significant difference in latissimus dorsi strength (WMD of 6.07 kg, 95% CI −3.22 to 15.37 kg, I2 = 0%, P = .20) was observed after the addition of resistance training to endurance training (Fig. 5).23,35 Only one study measured knee extension strength (d = 10.00 kg, 95% CI −1.53 to 21.53 kg, P < .002).35
Effects of combined resistance and endurance training vs endurance training alone on skeletal muscle strength. IV = inverse variance weighting.
6-min Walk Distance
Resistance-Training Group Versus Non-Exercise Control Group.
Five studies included the 6-min walk distance (6MWD) as an end point.17,21,26,32,34 The results of each study and of our pooled analysis showed no significant difference in 6MWD (WMD of 1.83 m, 95% CI −15.32 to 18.97 m, I2 = 0%, P = .83) between the 2 groups.
Resistance-and-Endurance-Training Group Versus Endurance-Training-Alone Group.
Two included trials reported 6MWD.35,36 The results of each study showed no significant improvements in 6MWD in the resistance-and-endurance-training group. The pooled analysis showed no obvious changes in 6MWD between the 2 groups (WMD of −1.94 m, 95% CI −49.55 to 45.67 m, I2 = 0%, P = .94).
6-min Pegboard and Ring Test
Maximum Exercise Work Load
Resistance-Training Group Versus Non-Exercise Control Group.
Two included trials reported the maximum exercise work load.27,29 The results of each study showed no significant difference, and the overall analysis also showed no significant difference between the 2 groups (WMD of 3.46 W, 95% CI −16.75 to 23.67 W, I2 = 0%, P = .74).
Resistance-and-Endurance-Training Group Versus Endurance-Training-Alone Group.
Two included trials reported the maximum exercise work load.23,35 The results of each study showed no significant difference, and the overall analysis also showed no significant difference between the 2 groups (WMD of 2.91 W, 95% CI −18.03 to 23.85 W, I2 = 0%, P = .79).
Maximum Oxygen Consumption
Resistance-Training Group Versus Non-Exercise Control Group.
Three included trials reported maximum oxygen consumption.20,27,29 The results of each study showed no significant difference, and the pooled analysis also showed no significant difference between the 2 groups (WMD of 0.04 L/min, 95% CI −0.13 to 0.21 L/min, I2 = 0%, P = .61).
Resistance-and-Endurance-Training Group Versus Endurance-Training-Alone Group.
Two studies reported maximum oxygen consumption.20,35 The results of each study showed no significant difference, and the pooled analysis also showed no significant difference between the 2 groups (WMD of 0.02 L/min, 95% CI −0.16 to 0.21 L/min, I2 = 0%, P = .79).
Pulmonary Function
Change in FEV1
Resistance-Training Group Versus Non-Exercise Control Group.
Three trials reported percent-of-predicted FEV1,27,33,34 and 4 trials reported absolute FEV1.27,30,33,34 The pooled analysis showed significant improvements in percent-of-predicted FEV1 (WMD of 6.88%, 95% CI 0.41–13.35%, I2 = 0%, P = .04) in the resistance-training groups compared with the non-exercise control groups. For absolute FEV1, the difference between the 2 groups was not statistically significant (WMD of 0.17 L, 95% CI −0.01 to 0.35 L, I2 = 0%, P = .07) (Fig. 6).
Effects of resistance training vs non-exercise control on FEV1. A: Percent-of-predicted FEV1. B: Absolute FEV1. IV = inverse variance weighting.
Only one trial reported absolute FVC.33 The results showed significant improvements in the resistance-training group (d = 0.11 L, 95% CI −0.62 to 0.84 L, P < .05).
Attrition Rate and Adverse Events
The attrition rate was reported in 17 included studies. The mean attrition rate was 16.9%, ranging from 0 to 38.0%. The main reasons for withdrawal included COPD exacerbations (17/119), failure to complete the program (21/119), non-protocol-related or non-COPD-related health problems (34/119), personal reasons (34/119), refusal of post-rehabilitation measurements (5/119), musculoskeletal problems (4/119), treatment changes (3/119), and generalized weakness (1/119). The pooled analysis showed that the attrition rate was higher in the resistance-training group compared with the non-exercise control group (odds ratio of 1.79, 95% CI 1.04–3.08, I2 = 0%, P = .03) (Fig. 7). No significant difference in the attrition rate between the resistance-and-endurance-training and endurance-training-alone groups (odds ratio of 1.15, 95% CI 0.32–4.15, I2 = 0%, P = .83) was observed (Fig. 8). No significant changes were observed in reasons for withdrawal between the resistance-training and non-exercise control groups (Fig. 9). There were no reports of adverse events related to resistance-training intervention. The overall analysis showed no obvious difference in reasons for withdrawal between the resistance-and-endurance-training and endurance-training-alone groups (Fig. 10).
Effects of resistance training vs non-exercise control on attrition rates. M-H = Mantal-Haenszel statistics.
Effects of combined resistance and endurance training vs endurance training alone on attrition rates. M-H = Mantal-Haenszel statistics.
Effects of resistance training vs non-exercise control on reasons for withdrawal. M-H = Mantal-Haenszel statistics.
Effects of combined resistance and endurance training vs endurance training alone on reasons for withdrawal. M-H = Mantal-Haenszel statistics.
Discussion
Exercise training provides an effective therapy for exercise limitation in patients with COPD. The conventional modalities of exercise training include mainly endurance and resistance training. Endurance training is recommended by various guidelines as the cornerstone of successful pulmonary rehabilitation.38–40 Although increases in muscle strength after resistance training were demonstrated in subjects with COPD,41 the effect of resistance training and combined resistance and endurance training on clinically relevant outcomes in patients with COPD remains controversial. This meta-analysis incorporated 18 RCTs and included data from 750 subjects with advanced COPD. The effects of resistance training and combined resistance and endurance training were evaluated by their impact on quality of life, dyspnea, functional exercise capacity, maximum exercise capacity, skeletal muscle function, lung function, and adverse events. To our knowledge, this is the largest analysis to date of the efficacy of resistance training on clinically relevant outcomes in subjects with COPD.
This meta-analysis clearly showed the beneficial effects of resistance training on skeletal muscle strength in subjects with COPD. The results support previous findings.13,14,16 O'Shea et al14 reported that there were obvious increases in knee extension strength, leg press strength, and latissimus dorsi strength following resistance training versus no exercise (control). We did not perform cumulative analysis of latissimus dorsi strength because there was only one suitable study. O'Shea et al14 included some non-RCTs. In addition, they included all studies with resistance training, including resistance training versus non-exercise control, resistance training versus endurance training, resistance training versus resistance plus endurance training, resistance plus endurance training versus non-exercise control, and resistance plus endurance training versus endurance training. Thus, there may be a higher risk of heterogeneity in their analysis. Actually, O'Shea et al14 did not report the effect of resistance training on pectoral muscle strength because statistical heterogeneity between trials prevented the use of meta-analysis. More importantly, they reported the percentage increase in skeletal muscle strength, and we reported the absolute value of skeletal muscle strength. Other important findings of our study include the beneficial effects of resistance training on shoulder flexion strength and CRQ dyspnea domain scores. The improvement in CRQ dyspnea domain scores achieved a minimum clinically important difference of 0.5 units. Despite the positive effects of resistance training on skeletal muscle strength and CRQ dyspnea domain scores, there were no significant differences between the 2 groups in functional exercise capacity (including 6MWD and 6-min pegboard and ring test scores) and maximum exercise capacity (including maximum exercise work load and maximum oxygen consumption). Our results support resistance training performed in conjunction with endurance training because the combination may improve skeletal muscle strength and quality of life to a greater degree than endurance training alone in patients with COPD. However, gains in skeletal muscle strength and quality of life failed to translate into improvements in exercise capacity. The mechanisms of intrinsic muscle changes after resistance training have been scarcely studied in COPD.41 Some authors speculated that the changes were related to the expression of muscle insulin-like growth factor-1 and myogenic regulatory factors.42 Additional studies are required to examine the mechanisms of intrinsic muscle changes after resistance training, which should greatly improve the clinical outcomes in patients with COPD.
It has been generally accepted that pulmonary rehabilitation by itself does not improve lung function.43,44 A meta-analysis conducted by Strasser et al15 showed that resistance training did not increase FEV1 but may carry potential benefits for FVC. Because of the inclusion of all studies with resistance training, there was a high heterogeneity with regard to percent-of-predicted FEV1 (I2 = 68.1%). Our results showed that there was an obvious improvement in percent-of-predicted FEV1 and an increasing trend of absolute FEV1 in the resistance-training group. Although this phenomenon had been reported previously,15,45,46 we did not consider it to be a direct consequence of resistance training per se. We believe that it could be a result of better maintenance of lung function in a more consistent way during pulmonary rehabilitation. We did not perform a cumulative analysis of FVC due to a lack of suitable studies.
We found that the attrition rate was higher in the resistance-training group. However, there were no obvious differences between the 2 groups regarding the reasons for withdrawal. Moreover, there were no reports of adverse events related to resistance-training intervention. Our results indicate that resistance training is a safe and tolerable modality of exercise training for patients with COPD.
The main strength of our study was inclusion of a large pool of subjects with COPD, allowing us to perform robust analysis of clinically relevant outcomes following resistance training versus no-exercise control or combined resistance and endurance training versus endurance training alone. The trials included in this analysis used almost identical designs with regard to inclusion and exclusion criteria, and the clinical characteristics of study populations were homogeneous. However, the results should be interpreted with caution because they might have been influenced by other factors. First, the duration of the resistance-training intervention in most of included trials was too short to allow adequate evaluation of the long-term efficacy and exacerbations. Additional long-term studies are anticipated to answer this question.41 Second, the availability of outcome data suitable for meta-analysis was limited. For comparisons of resistance training versus non-exercise control or combined resistance and endurance training versus endurance training alone, there was a lack of sufficient number of studies reporting SGRQ and CRQ scores and lung function. Third, there is a potential risk of publication bias47 because negative findings are less likely to be published. We have not analyzed this aspect here. Fourth, none of the included studies reported the sample size calculation, although we were very rigorous in a thorough search of related publications. Based on the results of the sample size calculation, many of the included trials may have lacked sufficient sample size, which might be associated with bias. Fifth, the methodological quality of the 10 included RCTs was low to moderate. The reason may be explained by the fact that a double-blind design in studies on this topic may not be achievable. Despite this, we avoided including case-control studies, unlike several other related meta-analyses. Hence, our conclusions need further validation in large-sample studies. Finally, only 2 included trials performed intention-to-treat analysis. This suggested that most subjects included in our analysis were those who were able to or wanted to complete resistance-training programs, which inevitably induced bias. The current limitations noted in many studies on the use of resistance training in patients with COPD, including ours, may encourage future improvements in the quality of related research.
Nevertheless, in our study, the clinical homogeneity of the trials resulted in statistical homogeneity for all outcome measures across the trials. Selection bias was minimized using a systematic search strategy, and we specified the inclusion and exclusion criteria. Furthermore, 2 reviewers independently evaluated the selected studies, and all authors consulted to reach consensus if necessary. Double counting of subjects from overlapping publications was avoided. Selective reporting of secondary end points in published manuscripts may also bias results. We minimized this bias by obtaining supplemental data for included studies.
Conclusions
In summary, this meta-analysis showed that dyspnea scale scores, skeletal muscle strength, and lung function improved following resistance training. Although skeletal muscle strength and quality of life improved following combined resistance and endurance training, they failed to translate into improved exercise capacity. Our results indicate that resistance training can be successfully performed alone or in conjunction with endurance training without increasing adverse events during pulmonary rehabilitation. Because of the limitations of this meta-analysis, we suggest further work to compare resistance training versus non-exercise control or combined resistance and endurance training versus endurance training alone. Larger, longer, multi-center, double-blind, parallel RCTs are needed to validate the long-term outcomes and safety of resistance-training programs for patients with COPD.
Acknowledgments
We thank Guang-qiao Zeng MD (State Key Laboratory of Respiratory Disease, Guangzhou Medical University, Guangzhou, China) for writing assistance.
Footnotes
- Correspondence: Rui Chen MD, Department of Respiratory Diseases, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, 107 Yan Jiang Road, Guangzhou 510120, China. E-mail: gzchenrui{at}163.com. Yu-qi Zhou MD, Department of Respiratory Diseases, The Third Affiliated Hospital, Sun Yat-sen University, 600 Tian He Road, Guangzhou 510630, China. E-mail: zzyyqqcj7605{at}163.com.
Ms Liao, Mr Chen, and Dr X Chen are co-first authors.
This study was supported by Guangdong Provincial Science and Technology Project grant 2011B080701062 and Guangdong Natural Science Foundation grant S2012010008623. The authors have disclosed no conflicts of interest.
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