|Year : 2018 | Volume
| Issue : 3 | Page : 150-156
The effect of body mass index on pulmonary rehabilitation outcomes in patients with chronic obstructive pulmonary disease
Esra Pehlivan1, Arif Balci2, Esra Yazar2, Elif Yelda Niksarlioglu2, Lütfiye Kiliç2
1 Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, University of Health Sciences, Istanbul, Turkey
2 Department of Pulmonary Rehabilitation, Yedikule Chest Diseases and Thoracic Surgery Training and Research Hospital, University of Health Sciences, Istanbul, Turkey
|Date of Submission||21-May-2018|
|Date of Decision||30-Jun-2018|
|Date of Acceptance||29-Aug-2018|
|Date of Web Publication||31-Dec-2018|
Dr. Esra Pehlivan
Hürriyet Mh, Rüya Sk, No. 12 D: 12 Bahçelievler, Istanbul
Source of Support: None, Conflict of Interest: None
CONTEXT: Although pulmonary rehabilitation (PR) is increasingly used in patients with chronic obstructive pulmonary disease (COPD), the factors affecting the gains obtained from PR are still not clear.
AIMS: We aimed to investigate the effect of body mass index (BMI) on PR outcomes in COPD.
SETTINGS AND DESIGN: The study was a retrospective–descriptive study.
SUBJECTS AND METHODS: Patients with BMI of 18.5–25 kg/m2 were referred to as Group 1 (n = 15) and patients with BMI ≥25 kg/m2 as Group 2 (n = 17). All patients received PR for 8 weeks. Six-min walking distance (6MWD), forced expiratory volume in 1-s, forced vital capacity (FVC), carbon monoxide diffusing capacity (DLCO), maximal inspiratory pressure (MIP), modified Medical Research Council dyspnea scale (mMRC), and COPD assessment test (CAT) scores were compared.
STATISTICAL ANALYSIS USED: Paired t-test, Wilcoxon rank, and Mann–Whitney-U test were used for statistical analysis.
RESULTS: Thirty-two patients were included in the study. Baseline parameters were similar except 6MWD. Following PR, 6MWD, mMRC, and CAT scores were significantly improved in both the groups (P < 0.05). A significant difference was found in favor of Group 1 for FVC (P = 0.039) and MIP (P = 0.018), while no difference was detected in DLCO.
CONCLUSIONS: In this study, PR yielded similar gains between COPD patients with high BMI and those with normal BMI in terms of exercise capacity, dyspnea, and disease symptom severity. The only additional gains were achieved in the respiratory functions of patients with normal weight. All COPD patients should be referred to PR, regardless of the BMI, taking into account the resulting PR gains.
Keywords: Body mass index, chronic obstructive pulmonary disease, obesity, pulmonary rehabilitation
|How to cite this article:|
Pehlivan E, Balci A, Yazar E, Niksarlioglu EY, Kiliç L. The effect of body mass index on pulmonary rehabilitation outcomes in patients with chronic obstructive pulmonary disease. Eurasian J Pulmonol 2018;20:150-6
|How to cite this URL:|
Pehlivan E, Balci A, Yazar E, Niksarlioglu EY, Kiliç L. The effect of body mass index on pulmonary rehabilitation outcomes in patients with chronic obstructive pulmonary disease. Eurasian J Pulmonol [serial online] 2018 [cited 2020 Apr 3];20:150-6. Available from: http://www.eurasianjpulmonol.com/text.asp?2018/20/3/150/245973
| Introduction|| |
Pulmonary rehabilitation (PR) is a valid and reliable treatment modality for many patients with respiratory conditions, especially chronic obstructive pulmonary disease (COPD). The effect of obesity on exercise tolerance and dyspnea in COPD patients is still unclear. Although there are some views that clinical and functional findings will not affect PR outcomes, it is suggested that PR may be more effective in obese patients, especially weight loss reduces airway obstruction in COPD patients and increases static lung volumes. In our study, we aimed to investigate the effect of body mass index (BMI) on PR gains in COPD patients.
| Subjects and Methods|| |
The records of 32 COPD patients enrolled in the exercise program of PR center between 2014 and 2017 were retrospectively reviewed. The study was approved by the Local Ethics Committee (Protocol no: 10840098-604.01.01-E.4229). Signed informed consent was obtained from each patient before commencing the PR program for routine clinical procedure. Data from fifty patients were retrospectively analyzed. Sixteen with missing data and two cachectic patients were excluded from the study. The remaining patients were divided into two groups by BMI. Patients with BMI of 18.5–25 kg/m2 were referred to as Group 1 (n = 15) and patients with BMI ≥25 kg/m2(25.3–38.4) as Group 2 (n = 17) [Figure 1].
Six-min walking test
The test was conducted in a 30-m corridor in line with the American Thoracic Society (ATS) guidelines. Patients were informed that they should walk as fast as they can walk. Before and after the test, oxygen saturation, heart rate, Borg fatigue rating, and walking distance were recorded.,
Pulmonary function test
It was conducted using the SensorMedics model 2400 (Yorba Linda, CA, USA), according to the ATS guidelines.
Carbon monoxide diffusion test
It was performed in the pulmonary function test laboratory using Cosmed Quark PFT (USA) with single-breath technique.
Maximum inspiratory pressure-maximum expiratory pressure
The mouth pressure measurement was performed with the Micro-RPM ® instrument from SensorMedic. Patient placed a rubber mouthpiece with flanges, on the device, sealed their lips firmly around the mouthpiece, exhaled/inhaled slowly and completely, and then tried to breath in as hard as possible. The patient was allowed to rest for about a minute and the maneuver was repeated five times. Verbal or visual feedback was provided after each maneuver. The aim is that the variability between measurements is <10 cmH2O. The maximum value was obtained.
Modified medical research council dyspnea scale
Dyspnea perceptions during the activities of daily living were assessed with the modified Medical Research Council (mMRC) scale.
Chronic obstructive pulmonary disease sment assessment test
COPD Assessment Test (CAT) scale was employed to determine the severity of COPD.
All patients received an 8-week PR for a total of 5 days consisting of 2 days a week at hospital setting and 3 days a week at home setting without supervision. The exercise program included breathing exercises, aerobic exercises, and upper and lower extremity strengthening exercises. Chest breathing, diaphragmatic breathing, and lateral basal breathing exercises were taught as a part of respiratory exercises. Methods of breath control and coping with dyspnea were explained. Treadmill (15 min/day), cycling (15 min/day), and arm ergometer workouts (15 min/day) were used for aerobic exercises, while free-weight lifting was used for strengthening exercises. The aerobic exercise workload was calculated by target heart rate method with the maximum heart rate being at least 60%. One-repetation maximum which was calculated in the strengthening exercises started at 20% of the weight which was progressively increased depending on the tolerance.
Normalities of the test data were examined using “Shapiro–Wilk” test. With regard to normally distributed data, intragroup variances were compared using “paired t-test,” while intergroup comparisons were made using “Independent student's t-test.” With regard to nonnormally distributed data, intragroup comparisons were made using “Wilcoxon rank test,” while intergroup variances were compared using “Mann–Whitney U-test.” Statistical significance level was accepted at P < 0.05. We estimated that a sample size of 15 patients for each group to have 80% power with 5% Type 1 error level to detect a minimum clinically significant difference of 54 m  of the 6-min walking distance (6MWD) with the highest standard deviation of the study parameters.
| Results|| |
The records of 32 COPD patients with a mean age of 58.81 ± 11.58 years, of whom 24 (75%) were male and 8 (25%) were female, and who were included in the PR program, while they were in stable period, were retrospectively reviewed. The patients' disease severity stages according to The Global Initiative for Chronic Obstructive Lung Disease were 12.5% (n = 4) Stage 1; 21.9% (n = 7) Stage 2; 13% (n = 40.6) Stage 3; and 25% (n = 8) Stage 4, respectively. Patients with BMI of 18.5–25 kg/m 2 were referred to as Group 1 (n = 15) and patients with BMI >25 kg/m 2(25.3–38.4) as Group 2 (n = 17). When additional disease profiles were examined, two hypertensive patients and one patient with ischemic heart disease in Group 1 and three hypertensive patients and one diabetic patient in Group 2 were detected. Baseline parameters were similar in groups except for 6MWD. In Group 2 patients, baseline 6MWDs were lower than in Group 1 patients (P = 0.039). Patients' baseline clinical and demographic characteristics are presented in [Table 1].
|Table 1: Comparison of prepulmonary rehabilitation clinical and functional parameters by groups|
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Statistically significant improvement was observed in both the groups for 6MWD (m), CAT, and mMRC scores at the end of the PR exercise program. However, there was no difference between the groups; the gains were similar. When the changes in the parameters of respiratory function test were examined, there were positive but nonstatistical improvements in Group 1, while there were nonstatistically significant decreases in Group 2. Intergroup comparisons showed a significant difference in forced vital capacity (FVC) (% predicted) value in favor of Group 1 (P = 0.039). The changes in the pre- and post-PR clinical and functional parameters of the groups were presented in [Table 2].
|Table 2: Pre- and post-pulmonary rehabilitation clinical and functional parameters of Group 1 vs. Group 2|
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Maximal inspiratory pressure (MIP) and MEP values of the subgroup with available mouth pressure measurements (Group 1, n = 7; Group 2, n = 5) showed increased MIP value in Group 1 (P = 0.018), whereas no difference in Group 2 (P = 0,176). There was no statistically significant difference between the groups for delta MIP versus MEP values [Table 2]. In the subgroup (Group 1, n = 12; Group 2, n = 16) consisting of patients who were eligible for testing and compatible with the measurement of carbon monoxide diffusing capacity (DLCO), no statistically significant difference was found between the groups in terms of diffusion capacity [Table 2].
| Discussion|| |
The study results showed that PR yielded similar gains between COPD patients with high BMI and those with normal BMI in terms of exercise capacity, dyspnea, and disease symptom severity. The only additional gains were achieved in respiratory functions of patients with normal weight. After rehabilitation, no statistically significant difference was found between the groups in terms of respiratory muscle strength and diffusion capacity.
Excess weight and obesity is a health problem seen worldwide. Based on the Global Burden of Disease Study, as per 2013 data, 2.1 million people were reported to be overweight or obese, whereas as per 2016 data, 120.1 million people were reported to be overweight or obese and the prevalence of obesity in COPD was known to be 18%.
In obese patients with COPD, dyspnea increases, quality of life impairs, and depression, sleep disturbances, and cardiac and metabolic comorbidity risks are also increased. On the other hand, physical inactivity and obesity are interchangeable risk factors of chronic diseases and PR is the most important nonpharmacological treatment approach that can reverse this. A study examining the effect of body composition on PR gains in COPD setting demonstrated that gains increased exercise tolerance, irrespective of muscle mass or obesity. A similar study including 155 patients achieved similar gains of exercise capacity and self-report disease impact of individuals regardless of BMI. In parallel with our literature, it was also found that the PR program is effective in controlling exercise capacity, dyspnea, and disease symptom severity both in overweight and obese COPD patients and COPD patients with normal weight.
Obese patients often experience the vicious cycle of low exercise capacity, physical disability, and breathlessness leading to physical inactivity. Excess weight is associated with low exercise capacity. Exercise capacity of obese and nonobese COPD patients is affected by many factors both pulmonary and nonpulmonary. A study reported that obese individuals had similar features in terms of many parameters such as oxygen consumption and minute ventilation while having a lower 6MWD. In our study, the 6MWD of high BMI group was shorter. Moreover, we showed that although the COPD patients with high BMI had a shorter initial 6MWD, similar exercise capacity improvement was observed in both the groups.
PR protocols applied in obese patients are similar to those applied in patients with other chronic respiratory diseases. In a study, obese patients on CPAP with sleep apnea syndrome were randomly allocated to exercise training on a cycle ergometer, either alone or with respiratory muscle training or noninvasive ventilation (NIV). It was emphasized that NIV may be preferred for its ability to reduce cardiometabolic risk, while no additional benefit was observed in groups whose program was supplemented with respiratory muscle training and NIV. Another approach in the literature is land-based and water-based exercise programs. Water-based exercise programs have long been on the agenda in obese patients. In a study examining water-based exercise in COPD setting, water-based exercise training was found to increase endurance exercise capacity more than land-based exercise. Same investigators reported that water-based training in obese patients with COPD improved exercise capacity and health-related quality of life more than a similar land-based exercise training program. In our study, a standard PR program boosted with aerobic and strengthening exercises applied to all chronic respiratory patients was used. There is a need for studies designed with different exercise modalities.
In a parallel design study, compared obese and nonobese COPD patients, researchers reported that obese patients had higher static recoils and intraabdominal pressures, while there was no difference in resting respiratory muscle strength. In our study, an increase in postrehabilitation inspiratory muscle strength was found only in individuals with a low BMI. Obesity may be a clinical parameter that prevents the positive effect of PR on respiratory muscle strength.
A study where dietary energy restriction coupled with resistance exercise training is applied together in obese patients with COPD showed improved BMI, increased exercise capacity, and improved health status. In another study on obese women, dyspnea on exertion was reduced by only aerobic exercise with no weight loss. All of our patients have consulted to a dietician for our routine clinic operation. One of the weaknesses of our study is that the reflections of dietary programs applied to the patients on PR gains have not been documented. Given the literature, we believe that the combination of healthy nutrition and exercise is the ideal approach.
Dyspnea is one of the most important symptoms affecting the quality of life in patients with COPD and moderate or severe dyspnea is defined in more than 40% of the COPD patients. In a population-based study, it was reported that obese patients with COPD had more dyspnea complaints and poorer quality of life compared to patients with normal weight. Compared with COPD patients with different weights and similar forced expiratory volume in 1-s values, obese patients with COPD have been shown to have less hyperinflation and greater inspiratory capacity. One study showed that the post-PR dyspnea score decreased in patients with a mMRC dyspnea score of 3 and higher. In another study, PR was shown to improve dyspnea score in all patients having different mMRC dyspnea scores. In our study, baseline dyspnea scores were similar among groups and similarly to the literature; a significant improvement in the dyspnea score was observed in both groups following PR. However, there was no difference in the level of improvement among groups.
In a study  on a patient population consisting of obese asthma and COPD patients, it was found that weight loss decreased airway obstruction and increased expiratory reserve volume (ERV), RV, functional residual capacity, and DLCO parameters. Another study  showed that exercise capacity is low even in obese patients with COPD with early-stage spirometric changes. The same study emphasized that obesity had no effect on PR outcomes. In our study, we found that baseline respiratory function parameters were similar in both groups and that the spirometric values of COPD patients with normal weight were either maintained or had a tendency to increase after the exercise program, and that the spirometric parameters of the obese group tended to decrease in a nonstatistically significant manner. We also found that there was a significant difference in FVC values in favor of patients with normal weight. This can be interpreted as reduced positive effect on respiratory functions in obese patients with COPD, resulting from PR.
The CAT is an easy-to-use questionnaire that has become increasingly common in clinical practice to determine the control status and quality of life of the disease. It correlates strongly with dyspnea and exercise tolerance. It has also been reported that CAT test can be used to follow the changing health situation and determine the PR gains. A study involving 544 patients with severe COPD found significant improvement in CAT and mMRC scores after PR applied at home setting. Another study conducted on obese patients with COPD reported that PR significantly improved CAT scores, irrespective of BMI. Similarly, in our study, we observed a significant post-PR improvement in CAT score in both groups, with no difference in terms of improvement level.
A study investigating what clinical predictors might be in predicting PR activity in COPD, it has been reported that baseline clinical and functional findings may not be predictive of PR gains. However, it has been suggested that overweight and obese hypoxemic patients with BMI >25 kg/m 2 may benefit more from exercises due to their low conditions. Although, in our study, there were groups that were not similar in terms of 6MWD among groups that were formed by their BMI, PR gains for exercise capacity, dyspnea score, and self-report disease impact of individuals were similar at the end of the program. The results were not affected by basal exercise capacity. In addition, PR gains for respiratory muscle strength and spirometric values were lower in the group with higher BMI.
The study design was retrospective and the number of cases was relatively small.
| Conclusions|| |
PR yielded similar benefits between COPD patients with high and normal BMI in terms of exercise capacity, dyspnea, and disease control status in this study. Additional gains were achieved in respiratory functions of COPD patients with normal BMI. In the literature, although different effects of obesity on PR outcomes are reported, we can say that PR improves exercise capacity, dyspnea, and disease severity control independently of BMI and that every COPD patient should be referred to PR. However, the future studies are warranted on the development of new exercise programs and dietary recommendations to increase the gains of obese patients with COPD from PR.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Spruit MA, Singh SJ, Garvey C, ZuWallack R, Nici L, Rochester C, et al.
An official American Thoracic Society/European Respiratory Society Statement: Key concepts and advances in pulmonary rehabilitation. Am J Respir Crit Care Med 2013;188:e13-64.
Sava F, Laviolette L, Bernard S, Breton MJ, Bourbeau J, Maltais F, et al.
The impact of obesity on walking and cycling performance and response to pulmonary rehabilitation in COPD. BMC Pulm Med 2010;10:55.
Ramachandran K, McCusker C, Connors M, Zuwallack R, Lahiri B. The influence of obesity on pulmonary rehabilitation outcomes in patients with COPD. Chron Respir Dis 2008;5:205-9.
Shafey B, El-Deib A. Effect of weight reduction on obese patients with COPD and bronchial asthma. Egyptian Journal of Chest Diseases and Tuberculosis 2015;64:773-8.
Brooks D, Solway S, Gibbons WJ. ATS statement on six-minute walk test. Am J Respir Crit Care Med 2003;167:1287.
Holland AE, Spruit MA, Troosters T, Puhan MA, Pepin V, Saey D, et al.
An official European Respiratory Society/American Thoracic Society technical standard: Field walking tests in chronic respiratory disease. Eur Respir J 2014;44:1428-46.
Miller MR, Crapo R, Hankinson J, Brusasco V, Burgos F, Casaburi R, et al.
General considerations for lung function testing. Eur Respir J 2005;26:153-61.
Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CP, Brusasco V, et al.
Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J 2005;26:720-35.
American Thoracic Society/European Respiratory Society. ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med 2002;166:518-624.
Wen AS, Woo MS, Keens TG. How many maneuvers are required to measure maximal inspiratory pressure accurately. Chest 1997;111:802-7.
Fletcher CM, Elmes PC, Fairbairn AS, Wood CH. The significance of respiratory symptoms and the diagnosis of chronic bronchitis in a working population. Br Med J 1959;2:257-66.
Yorgancıoğlu A, Polatlı M, Aydemir Ö, Yılmaz Demirci N, Kırkıl G, Naycı Atış S, et al.
Reliability and validity of Turkish version of COPD assessment test. Tuberk Toraks 2012;60:314-20.
Redelmeier DA, Bayoumi AM, Goldstein RS, Guyatt GH. Interpreting small differences in functional status: The six minute walk test in chronic lung disease patients. Am J Respir Crit Care Med 1997;155:1278-82.
Gomes-Neto M, Araujo AD, Junqueira ID, Oliveira D, Brasileiro A, Arcanjo FL. Comparative study of functional capacity and quality of life among obese and non-obese elderly people with knee osteoarthritis. Rev Bras Reumatol Engl Ed 2016;56:126-30.
GBD 2015 Risk Factors Collaborators. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990-2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016;388:1659-724.
O'Donnell DE, Ciavaglia CE, Neder JA. When obesity and chronic obstructive pulmonary disease collide. Physiological and clinical consequences. Ann Am Thorac Soc 2014;11:635-44.
ten Hacken NH. Physical inactivity and obesity: Relation to asthma and chronic obstructive pulmonary disease? Proc Am Thorac Soc 2009;6:663-7.
Tunsupon P, Mador MJ. The influence of body composition on pulmonary rehabilitation outcomes in chronic obstructive pulmonary disease patients. Lung 2017;195:729-38.
Broderick J, Mc Grath C, Cullen K, Talbot D, Gilmor J, Baily-Scanlan M, et al.
Effects of pulmonary rehabilitation on exercise capacity and disease impact in patients with chronic obstructive pulmonary disease and obesity. Physiotherapy 2018;104:248-50.
Jebb SA, Moore MS. Contribution of a sedentary lifestyle and inactivity to the etiology of overweight and obesity: Current evidence and research issues. Med Sci Sports Exerc 1999;31:S534-41.
Greening NJ, Evans RA, Williams JE, Green RH, Singh SJ, Steiner MC, et al.
Does body mass index influence the outcomes of a waking-based pulmonary rehabilitation programme in COPD? Chron Respir Dis 2012;9:99-106.
Rodríguez DA, Garcia-Aymerich J, Valera JL, Sauleda J, Togores B, Galdiz JB, et al.
Determinants of exercise capacity in obese and non-obese COPD patients. Respir Med 2014;108:745-51.
Bautista J, Ehsan M, Normandin E, Zuwallack R, Lahiri B. Physiologic responses during the six minute walk test in obese and non-obese COPD patients. Respir Med 2011;105:1189-94.
Vivodtzev I, Tamisier R, Croteau M, Borel JC, Grangier A, Wuyam B, et al.
Ventilatory support or respiratory muscle training as adjuncts to exercise in obese CPAP-treated patients with obstructive sleep apnoea: A randomised controlled trial. Thorax 2018. pii: thoraxjnl-2017-211152.
Gappmaier E, Lake W, Nelson AG, Fisher AG. Aerobic exercise in water versus walking on land: Effects on indices of fat reduction and weight loss of obese women. J Sports Med Phys Fitness 2006;46:564-9.
McNamara RJ, McKeough ZJ, McKenzie DK, Alison JA. Water-based exercise in COPD with physical comorbidities: A randomised controlled trial. Eur Respir J 2013;41:1284-91.
McNamara RJ, McKeough ZJ, McKenzie DK, Alison JA. Obesity in COPD: The effect of water-based exercise. Eur Respir J 2013;42:1737-9.
Ora J, Laveneziana P, Wadell K, Preston M, Webb KA, O'Donnell DE, et al.
Effect of obesity on respiratory mechanics during rest and exercise in COPD. J Appl Physiol (1985) 2011;111:10-9.
McDonald VM, Gibson PG, Scott HA, Baines PJ, Hensley MJ, Pretto JJ, et al.
Should we treat obesity in COPD? The effects of diet and resistance exercise training. Respirology 2016;21:875-82.
Bernhardt V, Stickford JL, Bhammar DM, Babb TG. Aerobic exercise training without weight loss reduces dyspnea on exertion in obese women. Respir Physiol Neurobiol 2016;221:64-70.
Müllerová H, Lu C, Li H, Tabberer M. Prevalence and burden of breathlessness in patients with chronic obstructive pulmonary disease managed in primary care. PLoS One 2014;9:e85540.
García-Rio F, Soriano JB, Miravitlles M, Muñoz L, Duran-Tauleria E, Sánchez G, et al.
Impact of obesity on the clinical profile of a population-based sample with chronic obstructive pulmonary disease. PLoS One 2014;9:e105220.
Guenette JA, Jensen D, O'Donnell DE. Respiratory function and the obesity paradox. Curr Opin Clin Nutr Metab Care 2010;13:618-24.
Croitoru A, Ioniţă D, Stroescu C, Pele I, Gologanu D, Dumitrescu A, et al.
Benefits of a 7-week outpatient pulmonary rehabilitation program in COPD patients. Pneumologia 2013;62:94-8, 101.
Evans RA, Singh SJ, Collier R, Williams JE, Morgan MD. Pulmonary rehabilitation is successful for COPD irrespective of MRC dyspnoea grade. Respir Med 2009;103:1070-5.
El-Shafey BI, El-Deib AE. Effect of weight reduction on obese patients with COPD and bronchial asthma. Egypt J Chest Dis Tuberc 2015;64:773-8.
Ringbaek T, Martinez G, Lange P. A comparison of the assessment of quality of life with CAT, CCQ, and SGRQ in COPD patients participating in pulmonary rehabilitation. COPD 2012;9:12-5.
Horita N, Yomota M, Sasaki M, Morita S, Shinkai M, Ishigatsubo Y, et al.
Evaluation of the chronic obstructive pulmonary disease assessment test in Japanese outpatients. Clin Respir J 2014;8:213-9.
Jones PW, Harding G, Wiklund I, Berry P, Tabberer M, Yu R, et al.
Tests of the responsiveness of the COPD assessment test following acute exacerbation and pulmonary rehabilitation. Chest 2012;142:134-40.
Greulich T, Koczulla AR, Nell C, Kehr K, Vogelmeier CF, Stojanovic D, et al.
Effect of a three-week inpatient rehabilitation program on 544 consecutive patients with very severe COPD: A retrospective analysis. Respiration 2015;90:287-92.
Vagaggini B, Costa F, Antonelli S, De Simone C, De Cusatis G, Martino F, et al.
Clinical predictors of the efficacy of a pulmonary rehabilitation programme in patients with COPD. Respir Med 2009;103:1224-30.
[Table 1], [Table 2]