Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 13  |  Issue : 5  |  Page : 616-622

Pulmonary rehabilitation outcome in chronic obstructive pulmonary disease patients with a different body composition


Department of Chest, Faculty of Medicine, Beni-Suef University, Beni-Suef, Egypt

Date of Submission01-Apr-2019
Date of Acceptance01-Aug-2019
Date of Web Publication21-Jan-2020

Correspondence Address:
MD Laila A Alsharaway
MD in Chest Diseases, Elramed Street, Beni-Suef, 62521
Egypt
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ejb.ejb_33_19

Rights and Permissions
  Abstract 

Context Change in body composition is commonly present in chronic obstructive pulmonary disease (COPD) patients.
Aim The aim of this study was to investigate the effects of pulmonary rehabilitation program (PRP) on COPD patients who have a different body composition.
Materials and methods In this study, we measure;Deg;BM;Deg;I and fat-free mass index (FFMI) using a single-frequency bioelectrical impedance analysis apparatus to classify patients into three categories: Group 1 nonmuscle depleted;Deg;BM;Deg;I greater than or equal to 21 kg/m2 and FFMI greater than or equal to 16. Group 2 muscle depleted;Deg;BM;Deg;I greater than or equal to 21 kg/m2 and FFMI less than 16 in men or FFMI less than 15 in women. Group 3 muscle depleted with cachexia;Deg;BM;Deg;I less than 21 kg/m2 and FFMI less than 16 in men or FFMI less than 15 in women. PRP outcomes were assessed by the improvement in pulmonary function severity, exercise capacity by 6-min walk test, dyspnea score by modified-British Medical Research Council, and health status by combined assessment test score and arterial blood gas improvements.
Results Forty-four patients with FFMI were measured by bioelectrical impedance analysis. The patients were mainly elderly men (N=35; 79%), who have a mean age of 65 years with different global initiative obstructive lung disease stage I–IV. In the nonmuscle depleted group, there were statistically significant improvements in the mean values of FFMI (kg/m2) while in the muscle depleted group there were improvements as regards the mean values of dyspnea score by modified-British Medical Research Council; in the cachectic group there were statistically significant improvements in the mean values of BMI (kg/m2), forced expiratory volume in the first second (FEV1), forced expiratory volume in first second divided by forced vital capacity ratio, combined assessment test score after PRP.
Conclusions A comprehensive PRP outcome change in COPD patients with different body compositions.

Keywords: body composition, chronic obstructive pulmonary disease, pulmonary rehabilitation


How to cite this article:
Alsharaway LA. Pulmonary rehabilitation outcome in chronic obstructive pulmonary disease patients with a different body composition. Egypt J Bronchol 2019;13, Suppl S1:616-22

How to cite this URL:
Alsharaway LA. Pulmonary rehabilitation outcome in chronic obstructive pulmonary disease patients with a different body composition. Egypt J Bronchol [serial online] 2019 [cited 2020 Jul 15];13, Suppl S1:616-22. Available from: http://www.ejbronchology.eg.net/text.asp?2019/13/5/616/276281


  Introduction Top


Chronic obstructive pulmonary disease (COPD) is a common, preventable, and treatable disease that is characterized by respiratory symptoms and airflow limitation that is due to airway and/or alveolar abnormalities usually caused by significant exposure to noxious particles or gases [1].

Measurement of BMI may not accurately reflect changes in body composition in COPD. Body weight consists of fat mass and fat-free mass (FFM), which includes water and body cell mass (bones, internal organs, muscle). Measurement of body cell mass can be performed by measurement of fat-free mass index (FFMI) [2]. COPD patients have concomitant chronic diseases linked to the same risk factors, that is, aging, smoking, and inactivity, which may have a great impact on health status and survival in those patients. Skeletal muscle dysfunction is characterized by sarcopenia (loss of muscle cells) and abnormal function of the cells [3]. Inflammatory mediators may contribute to skeletal muscle wasting and cachexia. The association between low body cell mass and worsening prognosis is a common observation in COPD patients [4].

Cachexia and muscle depletion are characterized by FFM depletion, which can be estimated using skinfold anthropometric measurement and bioelectrical impedance analysis (BIA) [5]. FFM measurement by BIA is easy to perform and has shown significant correlations to reference measurements methods such as magnetic resonance imaging [6].

Pulmonary rehabilitation is a comprehensive intervention including exercise, nutritional counselling, psychological counselling, and education about the disease nature, progression, prevention of exacerbation, and breathing exercises, which lead to improvement in clinical outcomes such as quality of life, dyspnea score, and exercise capacity [7].

Thus, the aim of this study was to assess pulmonary rehabilitation outcome on COPD patients with different body compositions.


  Materials and methods Top


Materials

A retrospective, randomized, controlled study in the period from June 2016 to October 2018 .The study protocol was reviewed by the appropriate Ethics Committee, from Faculty of Medicine, Beni Suef University. All patients gave their informed, written consent before study inclusion.

The study population consists of 44 patients with a clinical diagnosis of COPD and confirmed by doing pulmonary function tests they were chosen from the Outpatient Clinic of Chest Diseases Department, at Faculty of Medicine, Beni-Suef University

Inclusion criteria

Diagnosis of COPD patients was established by full clinical history and examination, history of cigarette or shisha smoking or history of indoor biomass fuel exposure, and spirometric measurements that demonstrated irreversible airflow obstruction. All patients were required to fulfill the criteria of COPD according to latest global initiative obstructive lung disease (GOLD) 2019 classification. Patients must have had at least 3 months of smoking cessation.

Exclusion criteria

Patients with acute exacerbation; patients with acute respiratory failure; and patients with joint, muscle, and neurological disorders unable to do pulmonary rehabilitation exercises; patients with cardiac failure class III or IV NYHA, neoplastic disease, and hyperthyroidism were excluded, as these can be causes of weight loss. Patients who had contraindications for BIA measurement, such as those with defibrillator placement or pacemakers, were excluded from the study.

Study design

Patients were classified by body composition into three different groups based on BMI and FFM depletion:
  1. Group 1: nonmuscle depleted BMI greater than or equal to 21 kg/m2 and FFMI greater than or equal to 16.
  2. Group 2: muscle depleted BMI greater than or equal to 21 kg/m2 and FFMI less than 16 in men or FFMI less than 15 in women.
  3. Group 3: muscle depleted with cachexia BMI less than 21 kg/m2 and FFMI less than 16 in men or FFMI less than 15 in women.


Study outcome

All tests were performed before and after pulmonary rehabilitation program:
  1. Assessment of exercise capacity by 6-min walk test (6MWT) [8].
  2. Assessment of symptoms by the Modified British Medical Research Council Questionnaire (mMRC) [9].
  3. Assessment of health status impairment in COPD by combined assessment test (CAT) score. which is an eight-item test [10].
  4. Arterial blood gas measurements where PO2, PCO2, and SpO2 were measured [11].


Assessment of functional severity by spirometry [12].

This was performed by MasterScreen PFT. No.781040, where forced expiratory volume in the first second (FEV1), forced vital capacity (FVC), and FEV1–FVC were measured:
  1. Stage I: mild FEV1/FVC less than 0.70 FEV1 greater than or equal to 80% predicted.
  2. Stage II: moderate FEV1/FVC less than 0.70 50% less than or equal to FEV1 less than 80% predicted.
  3. Stage III: severe FEV1/FVC less than 0.70 30% less than or equal to FEV1 less than 50% predicted.
  4. Stage IV: very severe FEV1/FVC less than 0.70 FEV1 less than 30% predicted or FEV1 less than 50% predicted plus chronic respiratory failure.


Methods

Pulmonary rehabilitation program

The pulmonary rehabilitation program (PRP) consists of a 1 h session three times a week for a 8-week period. Patients underwent strengthening, endurance exercise, and respiratory muscle exercises. They exercised on a treadmill and on a cycle ergometer. They also performed light floor exercises with and without weights and stretching exercises as per ATS guidelines for pulmonary rehabilitation [2].

BMI measurement is calculated by dividing the weight in kilograms by height in meters squared. FFMI measurement: The bioelectrical impedance technique is a reliable and valid approach for estimation of human body composition. This method is safe, noninvasive, and provides rapid measurements. The procedure involves sending a very small current of 800 µA at an alternating frequency of 50 kHz through the body and measuring its resistance. We used Body Fat Analyzer BT 905 (BIA BT-905) (Skylark Device Co., Taipei, Taiwan). Both instruments required electrode placements at specific sites on the wrist, distal second metacarpal, ankle, and distal second metatarsal. Therefore, ‘whole-body’ BIA was measured. FFMI is measured by dividing the FFM in kilograms by height in meters squared.

Statistical analysis

The statistical analysis was performed using SPSS 19 (SPSS, Chicago, IL, USA). Results are presented as the mean±SD, and proportional data are presented as percentages. Groups were compared using one-way analysis of variance. Two groups were compared using the independent samples t-test. Relevant indicators of COPD were correlated using Spearman’s correlation or Pearson’s correlation analysis.

A P value of less than 0.05 was considered statistically significant.


  Results Top


This study was done on 44 COPD patients. The age of the patients ranged from 52 to 78 years with a mean age of 65 years. Of the patients 35 (79%) were men and nine (20%) were women. Clinical characteristics of the studied patients with different stages of COPD according to GOLD classification and 11 patients were nonmuscle depleted with a BMI more than or equal to 21 kg/m2 and FFMI greater than or equal to 16 and 16 patients with muscle depleted BMI greater than or equal to 21 kg/m2 and FFMI less than 16 and 17 patients with cachexia BMI less than 21 kg/m2 and FFMI less than 16. The groups were well balanced in terms of comorbidities and age as in [Table 1]. Also, the sample size was determined according to the duration of the study.
Table 1 Clinical characteristic of the patients

Click here to view


In the nonmuscle depleted group, there were statistically significant differences as regards the mean values of FFMI (kg/m2) mean±SD (64±22) to be mean±SD (68.10±15.10) after PRP but there were improvements regarding other variables but nonstatistically significant differences as shown in [Table 2]. In the muscle depleted group, there were statistically significant differences as regards the mean values of dyspnea score by mMRC mean±SD (2.93±1.1) to be mean±SD (2.37±0.78), but there were improvements regarding other variables but nonstatistically significant differences as given in [Table 3]. In the cachectic group, there were statistically significant differences as regards the mean values of BMI (kg/m2) mean±SD (19.06±2.6) to be mean±SD (24.67±5.06), FEV1 mean±SD (28.10±10.52) to be mean±SD (40.39±13.8), FEV1/FVC mean±SD (42.56±15.97) to be mean±SD (48.85±14.63), CAT score mean±SD (12.56±5.28) to be mean±SD (18.31±6.63), but there were improvements regarding other variables but nonstatistically significant differences as in [Table 4].
Table 2 Statistical comparison between different variables in the nonmuscle depleted group before and after pulmonary rehabilitation program

Click here to view
Table 3 Statistical comparison between different variables in the muscle-depleted group before and after pulmonary rehabilitation program

Click here to view
Table 4 Statistical Comparison between different variables in the muscle depleted group with cachexia before and after pulmonary rehabilitation program

Click here to view


Comparison between nonmuscle depleted, muscle depleted, and cachectic group before PRP showed statistically significant difference as regards the mean values of BMI (kg/m2), FFMI (kg/m2), SpO2, FEV1, dyspnea (mMRC), CAT score as in [Table 5], while after PRP there were statistically significant differences as regards the mean values of PCO2, FEV1, dyspnea (mMRC), and CAT score as in [Table 6].
Table 5 Statistical comparison between non-muscle depleted, muscle depleted, and cachectic group before pulmonary rehabilitation program

Click here to view
Table 6 Statistical comparison between non-muscle depleted, muscle depleted, and cachectic groups after pulmonary rehabilitation program

Click here to view


Regarding FFMI as the lowest mean values in the cachectic group 28±10 to be 40.39±13.81 after PRP, followed by the muscle depleted group 38±14 to be 47.87±13.60 after PRP and the highest value was in the nonmuscle depleted group 64±22 which was also found to be 68.10±15.10 after PRP, with statistically significant difference between them before PRP but nonsignificant after PRP.

In this study, the lowest mean values of FEV1 found in the cachectic group 28±10 to be 40.39±13.81 after PRP, followed by the muscle depleted group 38±14 to be 47.87±13.60 after PRP, and the highest value was in the nonmuscle depleted group 64±22 which was also found to be 68.10±15.10 after PRP. Regarding FEV1/FVC the lowest mean values in the cachectic group 42.56±15.97 to be 48.85±14.63 after PRP followed by the muscle depleted group 45.54±14.71 to be 51.07±12.90 after PRP and the highest value was in the nonmuscle depleted group 49.04±15.93 and then 53.28±13.49 after PRP.

In the current study, the lowest mean values of PO2 were found in the cachectic group 44.92±10.1 to be 56.93±10.4 after PRP followed by the muscle depleted group 48.68±10 and 63.9±11.1 after PRP and the highest value was in the nonmuscle depleted group 51.94±11.5 which was also found to be 64.68±7.3 after PRP. The highest mean values of PCO2 found in the cachectic group were 47.85±6.1 and 46.45±5.02 after PRP, followed by the muscle depleted group 44.72±4.5 and 42.68±5.85 after PRP and the highest value was in the nonmuscle depleted group 44.32±7.5 to be 40.82±5.27 after PRP.

The lowest mean values of SpO2 was found in the cachectic group 92.56±2.9 to be 93.86±3.2 after PRP, followed by the muscle depleted group 94.87±2.4 to be 93.25±3.3 after PRP and the highest value was in the nonmuscle depleted group 96.27±1.6 which was also found to be 92.93±2.0 after PRP; the lowest mean values of 6MWT found in the cachectic group were 223.83±74.2 and 270.25±89.9 after PRP, followed by the muscle depleted group 229.13±70.9 and 291.50±68.9 after PRP and the highest value was in the nonmuscle depleted group 291.82±88.6 to be 326.82±58.1 after PRP. The highest mean values of dyspnea (mMRC) was found in the cachectic group 3.44±.6 and 2.37±1 after PRP, followed by the muscle depleted group 2.93±1 to be 2.37±0.7 after PRP and the highest value was in the nonmuscle depleted group 2.18±1 to be 1.54±0.5 after PRP. The lowest mean values of CAT score found in the muscle depleted group were 11.93±6 and 17.12±6.9 after PRP, followed by the cachectic group to be 12.56±5.2 and 18.3±6.6 after PRP and the highest value was in the nonmuscle depleted group 24.45±8.8 and 27.09±5.5 after PRP.


  Discussion Top


PRP improves the health status and exercise capacity in COPD patients with different body compositions, but there was significant improvement in functional severity and health status in COPD patients with muscle depleted with cachexia while dyspnea score improved significantly in patients with muscle depleted without cachexia but FFMI significantly increased in the non-muscle depleted COPD patients. FFMI significantly correlated with dyspnea, exercise capacity, pulmonary function, and respiratory muscle function and may be a predictor of COPD severity due to enhanced protein catabolism in COPD patients with muscle mass depletion [13]. Previous studies have reported that the muscle mass depletion subgroup, defined as BMI less than 21 kg/m2 and FFMI less than 16 in men or FFMI less than 15 in women, was more prevalent in COPD GOLD stage IV more than patients in GOLD stages II and III [14]. So our results agree with the previous work as muscle depleted with cachexia group with BMI less than 21 kg/m2 and FFMI less than 16 with a mean FEV1 of 28.1±10.52 which means that most of them are in stage IV but there was statistically significant increase after PRP as the mean FEV1 reaches 40.39±13.81 [15].

Weight loss was particularly prevalent in COPD patients and was closely correlated with exercise capacity limitation, increased frequency of exacerbations, and decreased quality of life and mortality. Improvements in exercise performance, and quality of life and skeletal muscle function after exercise training in COPD patients are well reported. However, the effect of PRP on COPD patients with different body compositions has rarely been studied.

Previous studies hypothesized that FFM-depleted COPD patients are less likely to improve after pulmonary rehabilitation since exercise training can induce systemic inflammation and oxidative stress in COPD patients with muscle depletion [16].

Regarding FFMI the lowest mean values were in the cachectic group followed by the muscle depleted group and the highest value was in the nonmuscle depleted group with statistically significant difference between them before PRP but nonsignificant after PRP. So, these results agree with Jones et al. [15] as they found that patients who had sarcopenia had the same responses to pulmonary rehabilitation as those without muscle sarcopenia in terms of exercise performance (incremental shuttle walk) and quality of life (St. George’s questionnaire). Tunsupon and Mador [17] found that body weight muscle depletion and muscle depletion had no effect on patients achieving the minimal clinically important difference for quality of life and exercise tolerance measures after PRP which is not in agreement with our results. Maltais et al. [18] performed aerobic exercise on patients with COPD and he found that COPD patients who had muscle depletion have weaker muscles than those who had not have muscle depletion.

In this study the lowest mean values of FEV1 was found in the cachectic group, followed by the muscle depleted group and the highest value was in the non-muscle depleted group, regarding FEV1/FVC the lowest mean values were in the cachectic group, followed by the muscle depleted group and the highest value was in the nonmuscle depleted group. Criner et al. [19] found that there were statistically significant improvements of the mean values of FEV1, FEV1/FVC but there were improvements in 6MWT but not significant after 8 weeks of pulmonary rehabilitation.In our study, the lowest mean values of 6 MWT were found in the cachectic group followed by the muscle depleted group and the highest value was in the non-muscle depleted group. The highest mean values of dyspnea (mMRC) was found in the cachectic group, followed by the muscle depleted group and the highest value was in the nonmuscle depleted group. The lowest mean values of CAT score was found in the muscle depleted group followed by the cachectic group and the highest value was in the nonmuscle depleted group.

In the study of Troosters et al. [20], 100 patients were assigned to receive the full exercise training program. Patients who completed the 6-month duration program of outpatient training resulted in significant and clinically relevant improvement in exercise performance, 6-minute walk distance, quality of life, and respiratory and peripheral muscle strength. In the study of Griffiths et al. [21] on 200 disabling chronic lung disease patients (the majority with COPD) who were assigned for a 6-week rehabilitation program also showed greater improvements in general and disease-specific health status and walking ability.

In the study by Ali et al. [22] nine sessions of PR exercises in COPD patients with acute exacerbation produced statistically significant improvement in FEV1, 6MWT, exercise capacity, general well-being, and peak oxygen uptake.

In a study of Ries et al. [23] on 119 outpatients COPD with moderate to severe airflow obstruction were randomly assigned to an 8-week comprehensive pulmonary rehabilitation; there were significant improvement in clinical symptoms and exercise performance. Pulmonary rehabilitation improves COPD systemic manifestations and relieves dyspnea. These improvements are clinically important.

Study limitation

BIA is not a gold standard method for assessing body composition, but is safe and relatively available. The small number of patients is another important limitation of this study, which did not allow statistical analysis in some groups. Also, female participants were fewer due to the relatively low morbidity of COPD in women.


  Conclusion Top


PRP improves different functional parameters, health status, and exercise capacity in COPD patients with a different body composition but there is significant improvement in functional severity and health status in COPD patients with muscle depleted with cachexia.

Acknowledgements

This manuscript has been read and approved by all the authors and each author believes that the manuscript represents honest work.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Global Initiative for Chronic Obstructive Lung Disease. Global strategy for diagnosis, management and prevention of chronic obstructive lung disease2019 Global Initiative for Chronic Obstructive Lung Disease  Back to cited text no. 1
    
2.
Nici L, Donner C, Wouters E, Zuwallack R, Ambrosino N, Bourbeau J et al. American Thoracic Society/European Respiratory Society statement on pulmonary rehabilitation. Am J Respir Crit Care Med 2006; 173:1390–1413.  Back to cited text no. 2
    
3.
Wagner PD. Possible mechanisms underlying the development of cachexia in COPD. Eur Respir J 2008; 31:492–501.  Back to cited text no. 3
    
4.
Landbo C, Prescott E, Lange P, Vestbo J, Almdal TP. Prognostic value of nutritional status in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999; 160:1856–1861.  Back to cited text no. 4
    
5.
Schols AM, Fredrix EW, Soeters PB, Westerterp KR, Wouters EF. Resting energy expenditure in patients with chronicobstructive pulmonary disease. Am J Clin Nutr 1999; 54:983–987.  Back to cited text no. 5
    
6.
Janssen I, Heymsfield SB, Baumgartner RN, Ross R. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol 2000; 89:465–471.  Back to cited text no. 6
    
7.
Ries AL, Bauldoff GS, Carlin BW, Casaburi R, Emery CF, Mahler DA et al. Pulmonary rehabilitation: joint ACCP/AACVPR evidence-based clinical practice guidelines. Chest 2007; 131:4s–42s.  Back to cited text no. 7
    
8.
Puente-Maestu L, Palange P, Casaburi R, Laveneziana P, Maltais F, Neder JA et al. Use of exercise testing in the evaluation of interventional efficacy: an official ERS statement. Eur Respir J 2016; 47:429–460.  Back to cited text no. 8
    
9.
Fletcher CM. Standardised questionnaire on respiratory symptoms: a statement prepared and approved by the MRC Committee on the Aetiology of Chronic Bronchitis (MRC breathlessness score). BMJ 1960; 2:1662.  Back to cited text no. 9
    
10.
Jones PW, Harding G, Berry P, Wiklund I, Chen WH, Kline Leidy N. Development and first validation of the COPD Assessment Test. Eur Respir J 2009; 34:648–654.  Back to cited text no. 10
    
11.
Kelly AM, McAlpine R, Kyle E. How accurate are pulse oximeters in patients with acute exacerbations of chronic obstructive airways disease?. Respir Med 2001; 95:336–340.  Back to cited text no. 11
    
12.
Pellegrino R, Viegi G, Brusasco V, Crapo RO, Burgos F, Casaburi R et al. Interpretative strategies for lung function tests. Eur Respir J 2005; 26:948–968.  Back to cited text no. 12
    
13.
Engelen MP, Wouters EF, Deutz NE, Menheere PP, Schols AM. Factors contributing to alterations in skeletal muscle and plasma amino acid profiles in patients with chronic obstructive pulmonary disease. Am J Clin Nutr 2000; 72:1480–1487.  Back to cited text no. 13
    
14.
Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructivepulmonary disease. Am J Clin Nutr 2005; 82:53–59.  Back to cited text no. 14
    
15.
Jones SE, Maddocks M, Kon SS, Canavan JL, Nolan CM, Clark AL et al. Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax 2015; 70:213–218.  Back to cited text no. 15
    
16.
Van Helvoort HA, Heijdra YF, Thijs HM, Vina J, Wanten GJ, Dekhuijzen PN. Exercise-induced systemic effects in muscle-wasted patients with COPD. Med Sci Sports Exerc 2006; 38:1543–1552.  Back to cited text no. 16
    
17.
Tunsupon P, Mador MJ. The influence of body composition on pulmonary rehabilitation outcomes in chronic obstructive pulmonary disease patients. Lung 2017; 195:729–738.  Back to cited text no. 17
    
18.
Maltais F, Decramer M, Casaburi R, Barreiro E, Burelle Y, Debigare R et al. An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2014; 189:15–62.  Back to cited text no. 18
    
19.
Criner G, Cordova C, Furukawa S, Kuzma M, Travaline JM, Leyenson V et al. Prospective randomized trial comparing bilateral lung volume reduction surgery to pulmonary rehabilitation in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999; 160:2018–2027.  Back to cited text no. 19
    
20.
Troosters T, Gosselink R, Decramer M. Short- and long-term effects of outpatient rehabilitation in patients with chronic obstructive pulmonary disease: a randomized trial. Am J Med 2000; 109:207–212.  Back to cited text no. 20
    
21.
Griffiths TL, Burr ML, Campbell IA, Lewis-Jenkins V, Mullins J, Shiels K et al. Results at 1 year of outpatient multidisciplinary pulmonary rehabilitation: a randomized controlled trial. The Lancet 2000; 355:362–368.  Back to cited text no. 21
    
22.
Ali MS, Talwar D, Jain SK. The effect of a short-term pulmonary rehabilitation on exercise capacity and quality of life in patients hospitalized with acute exacerbation of chronic obstructive pulmonary disease. Indian J Chest Dis Allied Sci 2014; 56:13–19.  Back to cited text no. 22
    
23.
Ries AL, Kaplan RM, Limberg TM, Prewitt LM. Effects of pulmonary rehabilitation on physiologic and psychosocial outcomes in patients with chronic obstructive pulmonary disease. Ann Intern Med 1995; 122:823–832.  Back to cited text no. 23
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and me...
Results
Discussion
Conclusion
References
Article Tables

 Article Access Statistics
    Viewed351    
    Printed27    
    Emailed0    
    PDF Downloaded47    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]