COPD assessment test (CAT): simple tool for evaluating quality of life of chemical warfare patients with chronic obstructive pulmonary disease

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1 The Clinical Respiratory Journal ORIGINAL ARTICLE COPD assessment test (CAT): simple tool for evaluating quality of life of chemical warfare patients with chronic obstructive pulmonary disease Shahrzad M. Lari 1, Hassan Ghobadi, 2 Davood Attaran, 1 Afsoun Mahmoodpour, 2 Omid Shadkam 1 and Maryam Rostami 1 1 Mashhad University of Medical Sciences, COPD Research Center, School of Medicine, Mashhad, Iran 2 Ardabil University of Medical Sciences, Department of Internal Medicine, Ardabil, Iran Abstract Background: Chronic obstructive pulmonary disease (COPD) is one of the serious late pulmonary complications caused by sulphur mustard exposure. Health status evaluations of chemical warfare patients with COPD are important to the management of these patients. The aim of this study was to determine the efficacy of the COPD assessment test (CAT) in evaluating the health-related quality of life (HRQOL) of chemical warfare patients with COPD. Methods: Eighty-two consecutive patients with stable COPD were enrolled in this study. All subjects were visited by one physician, and the HRQOL was evaluated by the CAT and St. George Respiratory Questionnaires (SGRQs). In addition, a standard spirometry test, 6-min walk distance test and pulse oxymetry were conducted. The severity of the COPD was determined using Global Initiative for Chronic Obstructive Lung Disease (GOLD) staging and the body mass index, obstruction, dyspnoea and exercise (BODE) index. Results: The mean age of the patients was ± 7.08 years. The mean CAT score was ± Thirty-five (43%) patients were in CAT stage 3. There were statistically significant correlations between the CAT and the SGRQ (r = 0.70, P = 0.001) and the BODE index (r = 0.70, P = 0.001). A statistically significant inverse correlation was found between the CAT score and the forced expiratory volume in 1 s (r = 0.30, P = 0.03). Conclusions: Our results demonstrated that the CAT is a simple and valid tool for assessment of HRQOL in chemical warfare patients with COPD and can be used in clinical practice. Please cite this paper as: Lari SM, Ghobadi H, Attaran D, Mahmoodpour A, Shadkam O and Rostami M. COPD assessment test (CAT): simple tool for evaluating quality of life of chemical warfare patients with chronic obstructive pulmonary disease. Clin Respir J 2014; 8: Key words COPD quality of life spirometry sulphur mustard Correspondence Dr. Hassan Ghobadi, Ardabil University of Medical Sciences, Department of Internal Medicine, Imam Khomeini Hospital, Postal Code: , Ardabil, Iran. Tel: +98 (451) Fax: +98 (451) h.ghobadi@arums.ac.ir; larish@mums.ac.ir Received: 09 November 2012 Revision requested: 16 July 2013 Accepted: 25 July 2013 DOI: /crj Authorship and contributorship The study was designed by S.M.L, H.G, and D.A, O.S, A.M, and M.R have collected the data. Data analysis was performed by SML. Drafting the manuscript was performed by SML and HG. Ethics The study was approved by the ethics committee of the Mashhad University of Medical Sciences. All patients gave informed consent. The manuscript has been read and approved by all co-authors. Conflict of interest None of the authors have a conflict of interest to declare in relation to this work. Introduction During the Iran Iraq conflict ( ), more than Iranians were exposed to sulphur mustard (SM). SM, as a toxic alkylating gas, can cause serious early and late complications (1, 2). Currently, approximately patients are suffering from the late complications of SM exposure (3, 4). SM is absorbed 116 The Clinical Respiratory Journal (2014) ISSN

2 Lari et al. COPD assessment test in chemical warfare patients by lungs, skin, anterior segment of eyes and gasterointestinal tract (1). Depending to the mode of SM exposure and the dose of it, the early complications of SM toxicity appear after variable period of time (1). The most common early complications of SM toxicity in lungs are injury and irritation of respiratory tract resulting in laryngeal injury, tracheobronchitis, mucosal necrosis of respiratory tract and infection (1). The lungs, skin and nervous system are the major organs that are affected by SM exposure in the late phase. Among these organs, pulmonary complications are the most common problem (1, 5). A variety of different conditions can be seen in survivors (2, 6), including asthma, bronchiectasis, pulmonary fibrosis, chronic bronchiolitis and chronic obstructive pulmonary disease (COPD). The exact pathogenesis of the late pulmonary complications has not defined yet (5). The previous studies have shown that maybe systemic inflammation and oxidative stress have role in late phase (2, 4). Functional lung impairments in chemical warfare patients can adversely affect the physical, social and psychological health; these factors are known as the health-related quality of life (7, 8). The mainstay of COPD treatment focuses on alleviating symptoms, preventing exacerbation and hospitalisation, and improving the health-related quality of life and exercise capacity (9, 10). It is recommended that in addition to considering pulmonary function test results, the patient s health status, which is a combination of symptoms, the level of daily activity and the total impact of COPD on the patient s life, be evaluated and used for treatment guidance (11 13). Different questionnaires are available to assess the health-related quality of life, including the Clinical COPD Questionnaire (14), the Chronic Respiratory Questionnaire (15) and the St. Georges Respiratory Questionnaire (SGRQ) (16). These questionnaires are valid but complex (11). Recently, a short and simple health status questionnaire designed by Jones and colleagues, the COPD assessment test (CAT), was shown to correlate well with the SGRQ (11, 12). CAT is valid and has valuable measurement properties (11). The CAT score is associated with important clinical parameters and can be used in routine clinical practice to evaluate the health status during stable and exacerbated disease conditions (17, 18). Scores are also sensitive to improvements in patient health following COPD exacerbations (19). Additionally, the CAT questionnaire is a valuable tool for measuring outcomes of COPD patients (20). This study was designed to evaluate the performance of the CAT questionnaire in chemical warfare patients diagnosed with COPD and the questionnaire s ability to identify the severity of disease. Materials and methods Subjects A total of 82 chemical warfare patients with all levels of COPD in stable condition were entered into this crosssectional study from March 2010 to April All patients had validated documents demonstrating SM exposure and suffered from important late complications. According to the American Thoracic Society (ATS) definition (21), patients with a forced expiratory volume in 1 s (FEV 1 )/forced vital capacity (FVC) <0.7 after a 400 μg dose of the bronchodilator inhaled albuterol were included in the study. Current or ex-smokers were excluded for any of the following conditions: an FEV 1 increase of more than 12% and 200 ml after bronchodilator administration; a hospitalisation or exacerbation in the past 2 months; difficulty in walking; or a diagnosis of asthma, bronchiectasis or tuberculosis. Assessment of health-related quality of life Each patient was visited by one pulmonologist. The SGRQs, which included the symptoms, activity and impact, were completed for all patients (22). The scores of the SGRQs were calculated using an Excel-based scoring calculator (22). The calculated totals from the SGRQs were divided into four stages (9): Stage 1: 0 29 Stage 2: Stage 3: Stage 4: 60 The quality of life was also evaluated using the CAT questionnaire consisting of eight questions regarding cough, phlegm, chest tightness, breathlessness during activities, activity limitations at home, confidence in leaving home, sleep and energy (9). The scoring range of each item is between 0 and 5, with a maximum score of 40 (9). According to the total CAT scores, the patients were included in the following stages (11): Stage 1: <10 Stage 2: Stage 3: >20 Stage 4: >30 It must be noted that the validated and reliable Farsi version of the SGRQ (23) and the CAT (24) were used in this study. The Clinical Respiratory Journal (2014) ISSN

3 COPD assessment test in chemical warfare patients Lari et al. Lung function studies Standard spirometry tests (multifunctional spirometer HI-801; Chest MI, Inc., Tokyo, Japan) were performed in all patients. The FEV 1, FVC and FEV 1 /FVC were measured and expressed as a percentage of the predicted values. The best of three consecutive spirometry recordings was used. The severity of the airway obstruction was determined according to the Global Initiative for Chronic Obstructive Lung Disease (GOLD) guidelines (25), including: Stage 1( mild) FEV FVC < 70%, FEV 80% 1 1 Stage 2( moderate) FEV1 FVC < 70%, 50% FEV < 80% 1 Stage 3( severe) FEV FVC < 70%, 30% FEV < 50% 1 1 Stage 4( very severe) FEV FVC < 70%, FEV < 30% 1 1 All patients performed the 6-min walk distance (6MWD) test in a 30-metre flat indoor corridor according to ATS guidelines (25). The percent of oxygen saturation (SpO 2 ) (PC60C, Devon Medical, King of Prussia, PA, USA) was recorded using a pulse oximeter both before and after the 6MWD. The severity of dyspnoea was graded between 0 and 4 based on the patient s response following the Modified Medical Research Council scale (MMRC) (26). Weight (fully dressed) and height (without shoes) were recorded for each subject. Body mass index (BMI) was calculated as the weight (kg) divided by the height (m) squared. The BMI, obstruction, dyspnoea and exercise capacity (BODE) index was calculated for all patients using the BMI, the FEV 1, the MMRC scale and the 6MWD yielding total values in the range between 0 and 10 (26). The BODE index was categorised into four subgroups including: Subgroup1: 0 2 indexes Subgroup 2: 3 4 indexes Subgroup 3: 5 6 indexes Subgroup 4: 7 10 indexes Furthermore, according to GOLD 2011 guideline (27), we divided patients in four groups based on GOLD stage, CAT score, MMRC score and frequency of exacerbations in last year. It must be noted that all patients were received inhaled long-acting beta-2 agonists (LABAs), inhaled corticosteroids (ICS), anti-muscarinic agents and long-term oxygen therapy according to their GOLD stages based on GOLD guideline (25). This study was approved by the ethics committee of the Mashhad University of Medical Sciences (code number: ). All patients provided informed consent. Statistical analysis The data were analysed using the Statistical Package for Social Sciences (SPSS, version 11.5, Chicago, IL, USA). The variables are presented as percentages and means ± standard deviations (SDs). Descriptive statistics were used to summarise the demographic characteristics of the patients. The normality of continuous variables was checked using the one sample Kolmogorov Smirnov test. For continuous and categorical variables, independent Student s t tests and chi-square tests were used to evaluate the statistical significance of any differences and relationships between parameters, respectively. Pearson and Spearman correlation coefficients were calculated. Also for comparison of variables among groups, analysis of variance test was used. A logistic regression analysis was used to assess the relationship between age and CAT score. P values less than 0.05 were considered significant. Results All patients were male. The mean age of the patients was ± 7.08 (SD) years. The majority of the patients (37/82) were in GOLD stage 1. The mean CAT score was ± 8.28 (SD). Thirty-five (43%) patients were in CAT stage 3. The demographic characteristics of the patients are shown in Table 1. According to the GOLD 2011 guideline, the majority of patients (93%) were in groups B or D [A 6(7%), B 63(77%) and D 13(16%)]. Forty-five (55%) patients were on inhaled LABA, 30 (36%) on ICS, 50 (60%) on inhaled antimuscarinic agent. Additionally, nocturnal oxygen therapy was prescribed for five (6%) patients. There was a moderate statistically significant inverse correlation between mean FEV 1 and duration of disease (r = 0.5, P = 0.04). Also, there was a weak relationship between mean CAT score and duration of disease (r = 0.3, P = 0.03). The distribution of mean CAT scores for the different stages of GOLD are shown in Table 2. There was a statistically significant difference in the mean CAT scores of patients in GOLD stage 3 compared with the patients in stage <3 as shown in Fig. 1 (P = 0.02). There was a statistically significant correlation between the total SQRQ score and the CAT score (r = 0.70, 118 The Clinical Respiratory Journal (2014) ISSN

4 Lari et al. COPD assessment test in chemical warfare patients Table 1. The demographic and paraclinical data of 82 mustard lung patients Data Value Age (years) ± 7.08 BMI (kg/m 2 ) ± 4.62 Duration of disease (years) ± 5.17 FEV 1 (% pred.) ± MWT (m) 295 ± 164 CAT score ± 8.2 Total SGRQ score ± SpO 2 (%) ± 3.53 GOLD stage 1: 37 (45%) 2: 32 (39%) 3: 8 (10%) 4: 5 (6%) CAT stage 1: 4 (5%) 2: 14 (17%) 3: 35 (43%) 4: 29 (35%) SGRQ stage 1: 9 (11%) 2: 12 (14.5%) 3: 18 (22%) 4: 43 (52.5%) BODE subgroups 1: 38 (46%) 2: 18 (22%) 3: 18 (22%) 4: 8 (10%) The data are presented as mean ± standard deviation. BMI, body mass index; CAT, COPD assessment test; COPD, chronic obstructive pulomary disease; FEV 1, forced expiratory volume in 1 s; GOLD, Global Initiative for Chronic Obstructive Lung Disease; 6MWT, 6-min walk test; SGRQ, St. George respiratory questionnaire. P = 0.001), as shown in Fig. 2. There was also a statistically significant inverse correlation between the FEV 1 and the CAT score (r = 0.3, P = 0.03), as shown in Fig. 3. Additionally, there was a statistically significant correlation between the CAT score and the BODE index (r = 0.70, P = 0.001). The mean CAT scores in four subgroups of BODE index are shown in Fig. 4. There was statistically significant difference in mean CAT scores among subgroups (P < 0.001). Table 2. The mean CAT score for different stages of GOLD GOLD Value Stage 1 (4 patients) ± 8.87 Stage 2 (14 patients) ± 7.90 Stage 3 (35 patients) ± 2.77 Stage 4 (29 patients) 29 ± 9.43 The data are presented as mean ± standard deviation. CAT, COPD assessment test; COPD, chronic obstructive pulomary disease; GOLD, Global Initiative for Chronic Obstructive Lung Disease There was no statistically significant correlation between the mean CAT score and the age of the patients (r = 0.1, P = 0.3). Also, we performed a logistic regression analysis that showed that the CAT score is independent to age of the patients (β=0.19, P = 0.08). Discussion GOLD1,2 The results of our study demonstrated the validity of the CAT questionnaire for the assessment of the health-related quality of life in chemical warfare patients with COPD. We found a strong correlation between the CAT and the SGRQ. In addition, a moderate-to-strong correlation was found between the CAT score and the severity of COPD using both the GOLD stages and BODE index. Our results are compatible with the study conducted by Jones and colleagues regarding the role of CAT in determining the health-related quality of life and the severity of lung disease (9). As mentioned earlier, SM is a highly toxic gas that can cause serious long-term pulmonary issues and disability in chemical warfare patients. COPD caused by SM exposure is one of the main pulmonary complications (28). The important feature of late pulmonary complication of SM lung injury is the progressive nature of disorder after a single SM exposure (29). As we found in our study, FEV 1 and CAT scores had significant correlations with duration of disease that strengthens the progressive and severe nature of SM lung injury. Additionally, there are some aspects that differentiate the COPD because of SM from COPD because of other causes especially smoking. For example, smoking cessation can improve the acceleration decline of lung function in COPD patients (29, GOLD3,4 Figure 1. The comparison of the mean chronic obstructive pulmonary disease assessment test (CAT) scores between patients with mild-to-moderate [Global Initiative for Chronic Obstructive Lung Disease (GOLD) 1,2] and severe-to-very-severe (GOLD 3,4) stages (P = 0.02). Significant. The Clinical Respiratory Journal (2014) ISSN

5 COPD assessment test in chemical warfare patients Lari et al. Figure 2. The correlation of the mean chronic obstructive pulmonary disease assessment test (CAT) and total St. Georges Respiratory Questionnaire (SGRQ) scores (r = 0.7, P = 0.001). 30), but in COPD because of SM, despite the discontinuation of exposure, the deterioration of lung function is encountered in patients (29). Furthermore responses to the therapeutic options are not as well as COPD because of smoking (29). Considering the large population of chemical warfare patients and the important impact of pulmonary disease on their daily activities, it is recommended that a quality-of-life assessment be conducted for these patients (31). There are many standard questionnaires, such as SQRQ and CAT (12, 16), for the health status evaluation of COPD patients. Previous studies (2, 8) of chemical warfare patients have demonstrated that the SGRQ is a useful method for the assessment of Figure 3. The correlation of the mean chronic obstructive pulmonary disease assessment test (CAT) score and the forced expiratory volume in 1 s (FEV 1) (r = 0.3, P = 0.03). 120 The Clinical Respiratory Journal (2014) ISSN

6 Lari et al. COPD assessment test in chemical warfare patients Subgroup 1 Subgroup 2 Subgroup 3 Subgroup 4 Figure 4. The frequency of mean chronic obstructive pulmonary disease assessment test (CAT) scores in different subgroups of body mass index, obstruction, dyspnoea and exercise index (P < 0.001). Significant. health-related quality of life. Our results demonstrate that the CAT questionnaire is also a valuable tool for determining the health status of chemical warfare patients. Jones and colleagues (9) showed a strong correlation between the CAT score and the SQRQ total score. In our study, a strong correlation between the CAT score and the SGRQ was found, which supports the aforementioned study. For evaluating the severity of airflow obstruction, the GOLD staging was determined for all patients. There were statistically significant differences in the mean CAT scores between the mild-to-moderate and severe-to-very-severe stages. Jones and colleagues showed a significant difference in the CAT score between the GOLD stages II III and III IV (9). In addition, we also found a significant inverse correlation between the mean CAT score and the mean FEV 1 values that was compatible to the finding of Fadaii and colleagues who showed significant inverse correlation between total CAT score and FEV 1 in chemical warfare patients with COPD (32). This inverse correlation indicates that with the progression of airflow obstruction, the impairments in health status will become more apparent. After dividing the patients in groups according to GOLD 2011 guideline, the majority of patients were in group B. It means that these patients are more symptomatic compared with their lung function tests. Although it must be noted that because the distribution of our patients were not even among groups, finding of a unique feature regarding to GOLD 2011 classification in chemical warfare patients compared with COPD patients because of smoking is not possible by our study. Currently, it is well accepted that spirometry alone is not sufficient for determining the health status in COPD (33, 34). Other important clinical parameters, including BMI, exercise tolerance and the level of dyspnoea, should be considered in addition to the FEV 1. These additional parameters are known as the BODE index (26). The health-related quality of life may be adversely impacted by the progression of COPD, as assessed by the BODE index (35). In this study, there was strong correlation between the CAT score and the BODE index. This finding strengthens the efficacy of the CAT for use with chemical warfare patients. Additionally, we found a statistically significant difference in mean CAT score among BODE subgroups means that higher CAT scores were existed in higher BODE subgroups. In our study, the CAT score was not influenced by the age of the patients. This finding was compatible with the results of the Jones and colleagues study (9). This finding suggests that the quality of life in chemical warfare patients is not dependent on the age of the patients, and the severity of pulmonary disease is the sole determining factor. The limitations of our study should be noted. Only patients with stable COPD were included in this study. The CAT questionnaire should be evaluated for chemical warfare patient with exacerbated COPD for comparison. Additionally, because we performed a cross-sectional study and each sequential patient according to inclusion criteria were entered into the study, the majority of the patients were in mild-tomoderate stages of COPD. Further research should include more severe and very severe cases of COPD in chemical warfare patients for better exploration of significant role of CAT questionnaire; it is highly recommended to expand the number of patients in severe and very severe stages. It must be noted that our finding does not imply that CAT is only valuable in mild-to-moderate stages of COPD. Finally, for better comparison, our findings, considering the COPD patients caused by smoke as control group, would be supportive. Conclusion Health-related quality of life is strongly influenced by the severity of the pulmonary disease in chemical warfare patients with COPD, and evaluation of it is highly recommended in routine clinical evaluations. The CAT questionnaire is a simple and valid instrument for the assessment of health-related quality of life in chemical warfare patients with COPD. The CAT has a significant correlation with the SGRQ for these patients and is linked to the severity of the disease according to the GOLD staging and the BODE index. The Clinical Respiratory Journal (2014) ISSN

7 COPD assessment test in chemical warfare patients Lari et al. Acknowledgements This study was financially supported by the research council of Mashhad University of Medical Sciences (MUMS) and Ardabil University of Medical Sciences. The authors wish to thank M. Aalami and H. Sadraei for their valuable assistance in data collection. References 1. Balali-Mood M, Hefazi M. Comparison of early and late toxic effects of sulfur mustard in Iranian veterans. Basic Clin Pharmacol Toxicol. 2006;99(4): Attaran D, Lari SM, Towhidi M, Marallu HG, Ayatollahi H, Khajehdaluee M, Ghanei M, Basiri R. Interleukin-6 and airflow limitation in chemical warfare patients with chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2010;5: Ghanei M, Amiri S, Akbari H, Kosari F, Khalili AR, Alaeddini F, Aslani J, Giardina C, Haines DD. Correlation of sulfur mustard exposure and tobacco use with expression (immunoreactivity) of p53 protein in bronchial epithelium of Iranian mustard lung patients. Mil Med. 2007;172(1): Attaran D, Lari SM, Khajehdaluee M, Ayatollahi H, Towhidi M, Marallu HG, Mazloomi M, Mood MB. Highly sensitive C-reactive protein levels in Iranian patients with pulmonary complication of sulfur mustard poisoning and its correlation with severity of airway diseases. Hum Exp Toxicol. 2009;28(12): Lari SM, Attaran D, Towhidi M. COPD due sulfur mustard (Mustard lung). In: Ong KC, editor. Chronic Obstructive Pulmonary Disease Current Concepts and Practice. Croatia, InTech, 2012: Khateri S, Ghanei M, Keshavarz S, Soroush M, Haines D. Incidence of lung, eye, and skin lesions as late complications in 34,000 Iranians with wartime exposure to mustard agent. J Occup Environ Med. 2003;45(11): Mahler DA. How should health-related quality of life be assessed in patients with COPD? Chest. 2000;117 (Suppl. 2): 54S 8S. 8. Attaran D, Khajedaloui M, Jafarzadeh R, Mazloomi M. Health related quality of life in patients with chemical warfare induced COPD. Arch Iran Med. 2006;9(4): Jones PW, Brusselle G, Dal Negro RW, et al. Properties of the COPD assessment test in a cross-sectional European study. Eur Respir J. 2011;38(1): Celli BR, MacNee W. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J. 2004;23(6): Jones PW, Harding G, Berry P, Wiklund I, Chen WH, Leidy K. Development and first validation of the COPD assessment test. Eur Respir J. 2009;34(3): Jones PW, Tabberer M, Chen WH. Creating scenarios of the impact of COPD and their relationship to COPD assessment test (CAT ) scores. BMC Pulm Med. 2011;11: Gold PM. The 2007 GOLD Guidelines: a comprehensive care framework. Respiratory Care. 2009;54(8): van der Molen T, Willemse BW, Schokker S, ten Hacken NH, Postma DS, Juniper EF. Developement, validity and responsiveness of the clinical COPD questionnaire. Health Qual Life Outcomes. 2003;1: Guyatt GH, Berman LB, Townsend M, Pugsley SO, Chambers W. A measure of quality of life for clinical trials in chronic lung disease. Thorax. 1987;42(10): Jones PW, Quirk FH, Baveystock CM. The St Georges respiratory questionnaire. Respir Med. 1991;85(Suppl. B): Kelly JL, Bamsey O, Smith C, Lord VM, Shrikrishna D, Jones PW, Polkey MI, Hopkinson NS. Health status assessment in routine clinical practice: the chronic obstructive pulmonary disease assessment test score in outpatients. Respiration. 2012;84(3): Mackay AJ, Donaldson GC, Patel AR, Jones PW, Hurst JR, Wedzicha JA. Utility of the COPD Assessment Test (CAT) to Evaluate Severity of COPD Exacerbations. Am J Respir Crit Care Med. 2012;185(1): Jones PW, Harding G, Wiklund I, Berry P, Tabberer M, Yu R, Leidy NK. Tests of the responsiveness of the chronic obstructive pulmonary disease (COPD assessment test TM (CAT) following acute exacerbation and pulmonary rehabilitation). Chest. 2012;142(1): Dodd JW, Hogg L, Nolan J, Jefford H, Grant A, Lord VM, et al. The COPD assessment test (CAT): response to pulmonary rehabilitation. A multicenter, prospective study. Thorax. 2011;66(5): American Thoracic Society. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1995;52: S77 S Jones PW, Spencer S, Adie S. The St George Respiratory Questionnaire Manual. London, Respiratory Medicine, Halvani A, Pourfarokh P, Nasiriani K. Quality of life and related factors in patients with chronic obstructive pulmonary disease. Tanaffos. 2006;5: Available at: _Farsi.htm CAT-Iran/Farsi, Version of Sep 10-Mapi Research Institute, GlaxoSmithKline). 25. American Thoracic Society. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166: Celli BR, Cote CG, Marin JM, Casanova C, Montes de Oca M, Mendez RA, Pinto Plata V, Cabral HJ. The body mass index, airflow obstruction, dyspnea and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(10): The Clinical Respiratory Journal (2014) ISSN

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