Medicine & Science in Sports & Exercise:
Clinical Sciences: Clinical Investigations
Physical Activity and Its Determinants in Severe Chronic Obstructive Pulmonary Disease
GARCIA-AYMERICH, JUDITH1; FÉLEZ, MIQUEL A2; ESCARRABILL, JOAN3; MARRADES, RAMON M.4; MORERA, JOSEP5; ELOSUA, ROBERTO6; ANTÓ, JOSEP M.1,7
1Respiratory and Environmental Health Research Unit, Municipal Institute of Medical Research (IMIM), Barcelona, SPAIN; 2Department of Pneumology, Hospital of Mar, Barcelona, SPAIN; 3Department of Pneumology, University Hospital of Bellvitge, L’Hospitalet de Llobregat, SPAIN; 4Department of Pneumology, Hospital Clinic of Barcelona, SPAIN; 5Department of Pneumology, Germans Trias i Pujol Hospital, Badalona, SPAIN; 6Lipids and Cardiovascular Epidemiology Unit, Municipal Institute of Medical Research (IMIM), Barcelona, SPAIN; and 7Department of Experimental and Health Sciences, Pompeu Fabra University, Barcelona, SPAIN
Address for correspondence: Dr. Judith Garcia-Aymerich, Respiratory and Environmental Health Research Unit, Municipal Institute of Medical Research (IMIM), Doctor Aiguader 80, E-08003-Barcelona, Spain; E-mail: firstname.lastname@example.org.
Submitted for publication January 2004.
Accepted for publication June 2004.
The authors wish to thank Marta Macharé, Milors Maresma, Ana Martín, Ma José Rodríguez, Sandra Alonso, Rosa Reinón, Roser Pedreny, Núria Soler, and Angela Roig for their help in the field work, and Dr. Isabelle Romieu for her comments to a previous version of the results.
This work was supported in part by grants from Agència d’Avaluació de Tecnologia Mèdica (5/34/96) and Generalitat de Catalunya-DURSI 2001/SGR/00406. Judith Garcia-Aymerich was recipient of a grant from Instituto de Salud “Carlos III” (97/4365) from 1997 to 2000.
EFRAM: Estudi dels Factors de Risc d’Agudització de la MPOC (Risk Factors of COPD Exacerbation Study): The EFRAM investigators are: Josep M. Antó (Principal Investigator), Judith Garcia-Aymerich and Jordi Sunyer from the Respiratory and Environmental Health Research Unit, IMIM, Barcelona; Jordi Alonso from the Health Services Research Unit, IMIM, Barcelona; Esther Barreiro and Miquel A. Félez from the Department of Pneumology, Hospital del Mar, Barcelona; Joan Escarrabill, Eva Farrero, and Ma José Redondo from the Department of Pneumology, Hospital Universitari de Bellvitge, L’Hospitalet de Llobregat; Ramon M Marrades, Néstor Soler, and Antoni Torres from the Department of Pneumology, Hospital Clínic i Provincial de Barcelona, Barcelona; Glòria Bonet, José Izquierdo, Eduard Monsó, and Josep Morera from the Department of Pneumology, Hospital Germans Trias i Pujol, Badalona.
Background: Patients with chronic obstructive pulmonary disease (COPD) have a limited exercise capacity. Surprisingly, little is known about their levels of physical activity practice. We assessed the levels and determinants of physical activity practice in severe COPD patients.
Methods: A cross-sectional systematic sample of 346 COPD patients was recruited during 1 yr in four tertiary hospitals of the Barcelona area of Spain. Patients answered a questionnaire, which included physical activity assessment, and performed spirometric tests and blood gases.
Results: Seventy-eight percent of patients walked daily whereas 17% did not practice any physical activity. Median energy expenditure in physical activity was 109 kcal·d−1 (IQR 24–239). The following factors were independently associated with a lower physical activity level in a logistic regression analysis: female sex (OR 2.92, 95% CI 1.11–7.70), older age (1.04, 1.01–1.07 per year), higher socioeconomic status (2.23, 1.24–4.02), diabetes (2.66, 1.40–5.06), lower physical and mental quality of life (0.93, 0.90–0.96 and 0.96, 0.93–0.98, respectively, per unit), and long-term oxygen therapy (2.07, 1.19–3.60). Neither FEV1, previous COPD admissions, body mass index, nor other treatments were related to physical activity practice.
Conclusions: In conclusion, one third of severe COPD patients in our study reported a level of physical activity lower than the equivalent to walking less than 15 min·d−1. Apart from sociodemographic variables, comorbidity, health-related quality of life, and long-term oxygen therapy were the only factors independently associated with a low level of physical activity.
Patients with chronic obstructive pulmonary disease (COPD) are limited in their physical activity due to impairments in ventilatory mechanics, pulmonary gas exchange, cardiac function, and other systemic alterations, such as early lactic acidosis and peripheral muscle dysfunction (8). Consequently, during exercise, COPD patients may feel limited by dyspnea and/or limb symptoms (21). Multidisciplinary respiratory rehabilitation programs have been found effective in reducing dyspnea and improving quality of life, but the individual effects of increasing levels of physical activity practice are not known (23). Our group previously reported a reduction in the risk of admission for a COPD exacerbation in the patients with a higher level of physical activity among a cohort of COPD patients (Risk Factors of COPD Exacerbation Study–EFRAM Study) (14). Despite these antecedents, there is a striking lack of information about the levels and determinants of usual physical activity in COPD patients. This is in contrast with the fact that COPD guidelines recommend to encourage subjects to practice physical activity and that research about determinants of physical activity practice in the general population has been important for health promotion (25). We aimed to assess levels of physical activity practice and its determinants in a cross-sectional sample of 346 COPD patients from the EFRAM study.
A systematic sample was identified, consisting of one of every two patients hospitalized or remaining in the emergency room for at least 18 h for a COPD exacerbation in four tertiary hospitals in the Barcelona area over the recruitment year (from May 1, 1997 to April 30, 1998). Patients were allowed to enter the study as many times as they were hospitalized during the recruitment period, resulting in 346 individuals with 404 admissions. For the present analysis, in patients with more than one admission during the recruitment period, the first one was selected. COPD diagnosis was established by the ward pulmonologist and based on medical history, current symptoms, and available pulmonary function tests, following the European Respiratory Society guidelines. An exacerbation was defined when the patient reported an increase in dyspnea, sputum production or sputum purulence (6). Recruitment methods, including calculation of sample size, and diagnosis criteria have been detailed previously (13,15). The ethics committees of the participating hospitals approved the protocol, and written informed consent was obtained from all patients.
Patients completed a questionnaire and performed spirometric tests and blood gases, when clinically stable, thus providing information on a wide range of variables detailed elsewhere (15). For the present analysis, we used information on sociodemographic and clinical factors, lifestyle, social support, health-related quality of life (HRQL), adherence to medication, and medical care. Most of the questionnaire content was obtained from previously validated instruments, whereas some questions were developed and pilot tested for this study. Socioeconomic status was assigned according to occupation (considering both the current/last specific occupation and the position in that occupation) by using an adapted version of the British Registrar General’s Social Classes (4). HRQL, which measures the impact of an individual’s health on his/her ability to perform and enjoy the activities of daily life, was assessed using the Spanish validation in COPD patients (2) of the 12-item Short-Form Health Survey (SF-12) (35). The SF-12 is a multidimensional generic instrument containing 12 items, and its scores, ranging from 0 (worst health status) to 100 (best health), calculate for two summary measures: physical and mental. This two component summary scores were typified to have a mean of 50 and a standard deviation of 10 in the Spanish general population: all scores above or below 50 are better or worse, respectively, than the Spanish general population (3). Regarding physical activity, patients were asked about the frequency and duration of “walking,” “climbing stairs,” and “any other physical activity,” according to a simplification of the validated Spanish version (11) of the Minnesota Leisure Time Physical Activity Questionnaire, an instrument that measures physical activity in the general population (33). Each specific activity was assigned an intensity code expressed as metabolic equivalent tax (MET) based on the ratio between the metabolic rate during the activity and the basal metabolic rate (BMR) (1). Taking into account the intensity code for each physical activity, the number of times that this activity was performed in a defined period of time (previous month), and the average time spent in each session, the total energy expenditure in physical activity was obtained. For this analysis, we assumed that 1 MET is equal to 1 kcal·min−1 (11), and the unit for the total energy expenditure in physical activity was kilocalories per day. Detailed information about all the remaining variables, sources of questions and methods for spirometry and blood gas measures is available in previous papers (13,15).
Three physical activity groups were defined according to energy expenditure in physical activity (low, moderate, and high), using meaningful cut-offs that produced groups of similar size. The group with “low physical activity” expended 0–53 kcal·d−1, which ranges from “no activity” to “walking 15 min·d−1” or equivalent, whereas the group of “high physical activity” expended >210 kcal·d−1, corresponding to “walking 60 min·d−1 or more” or equivalent. Comparison of patients’ characteristics according to physical activity group was performed with ANOVA (for quantitative variables of normal distribution), Kruskal-Wallis test (for quantitative variables of nonnormal distribution) or χ2 (for qualitative variables). The independent association between patient characteristics and physical activity was obtained through multivariate logistic regression, using the group of low physical activity as the reference category. After a univariate analysis of each variable with physical activity, we selected, for the multivariate analysis, any variable whose univariate analysis had a P value < 0.25, along with all variables of known biological importance (19). Continuous variables were tested both as continuous or as categorical, using statistically and/or clinically meaningful cut-off points. The analysis was performed with Stata, release 7.0 (StataCorp, 2002, College Station, TX).
A total of 346 patients were included. Patient characteristics are shown in Table 1: 92% of them were men, the mean (SD) age was 69 (9) yr, 72% had a low socioeconomic status (IV or V), the mean forced expiratory volume in one second (FEV1) was 35 (16)%, and the mean arterial oxygen pressure (PO2) was 64 (13) mm Hg; the mean number of COPD admissions in the previous year was 1.6, 90% had at least one chronic comorbid condition, and the mean body mass index (BMI) was 26 (5) kg·m−2. Only 5% of subjects were underweight (BMI < 18.5 kg·m−2). Regarding physical activity, 78% of patients walked every day, 51% climbed stairs, and 10% practiced other physical activities, such as swimming, dancing, or gymnastics. A total of 83% of subjects practiced some physical activity. There were no differences in physical activity practice by season. Nineteen subjects had missing values for the time expended in physical activity and therefore were excluded from all subsequent analyses. They were not different of the remaining patients in sociodemographic or clinical factors. Median energy expenditure in physical activity was 109 kcal·d−1 (P25–P75: 24–239) (Table 1). Walking accounted for most (98%) of the total energy expenditure in physical activity. Figure 1 shows that about 20% of patients were totally inactive.
Distribution in the defined groups of physical activity practice showed that 34% of patients reported a level of physical activity lower than the equivalent to walking less than 15 min·d−1. Tables 2 and 3 show characteristics of patients, according to the defined physical activity groups. There was a higher proportion of males, subjects of lower socioeconomic status, and alcohol consumers in the group with high energy expenditure in physical activity. The group with low energy expenditure in physical activity exhibited older age, higher number of COPD admissions in the previous year, higher level of dyspnea, and lower levels in the physical and mental summaries of HRQL. Self-reported diabetes, self-reported cataracts, never having smoked, oral corticosteroids intake, and long-term oxygen therapy (LTOT) use were also more prevalent in the group with low energy expenditure in physical activity. For the remaining factors, including lung function, or drug and nondrug treatments, there were no differences among physical activity groups.
A final multivariate model (Table 4) showed that variables independently associated with low energy expenditure in physical activity were female sex, older age, higher socioeconomic status, self-reported diabetes, lower levels of physical and mental HRQL, and LTOT use. Several combinations of variables for a final multivariate model were tested as sensitivity analyses, and three of them are presented: 1) The inclusion of dyspnea in the final model did not change point estimates or confidence intervals for the other factors, and dyspnea only achieved statistical significance if the mental summary of HRQL was dropped from the model. 2) The inclusion of PO2 in the final model gave similar point estimates, but enlarged confidence intervals for sex and age, probably because of a reduction in the sample size due to a high number (N = 78) of missing values for PO2, and a higher prevalence of women in the group with missing PO2. 3) The exclusion of women from the analysis did not change the results. Analyses were also performed with polytomous logistic regression, yielding the same set of independent variables as in Table 4, with very similar point estimates and wider confidence intervals.
This is the first epidemiological study assessing the levels of physical activity practiced by COPD patients. Seventy-eight percent of patients walked daily whereas 17% did not practice any physical activity. Overall, median energy expenditure in physical activity was 109 kcal·d−1. Several clinical studies have reported levels of physical activities in small convenience samples of COPD patients (7,16,27–29,32). Three of these studies (16,27,29) reported that the level of physical activity in COPD patients was lower than in healthy age-matched controls, although their small sample size and methods of data presentation do not allow for a meaningful comparison with our data. In fact, the comparison of our data with levels of physical activity in other samples is quite difficult due to differences in methods and in populations studied. Physical activity was measured using a validated questionnaire in a representative sample from the general population of the region of Murcia, Spain (34). In that study, median levels of energy expenditure in physical activity for the men aged 61–65 yr were 150 kcal·d−1 higher than the 109 kcal·d−1 of our sample. Among the 236,386 participants in the European Prospective Investigation into Cancer and Nutrition (EPIC study) aged 50–64 yr, over 80% of subjects engaged daily in walking (18), similar to our 78% of patients. In the United States, data from the National Health Interview Survey of 7801 subjects aged 65 yr or older showed that about 69% of men and 75% of women used to walk at least once a week for ≥30 min (36). These data suggest that severe COPD patients have a level of physical activity that is similar to other general populations and probably not far from the general recommendation to “accumulate 30 min or more of moderate-intensity physical activity on most days of the week” (25) (equivalent to an energy expenditure of 120–150 kcal·d−1). Nevertheless, the differences in the physical activity measurement methods, age ranges, and geographic settings (18) as well as the lack in our study of a direct measure of metabolic expenditure due to usual physical activity do not allow for more precise comparisons.
We have also assessed the association between individual characteristics and physical activity. LTOT use was related to a lower level of physical activity. This association could not be explained by hypoxemia, as PO2 was not related to physical activity, although could be probably due to the mobility limitation imposed by domiciliary LTOT. Use of liquid oxygen could avoid this limitation, but we did not collect data on types of oxygen, and it is likely that only few patients (less than 5%) were using liquid oxygen at the time of the study, according to previous reports in our area (17).
We found a cross-sectional association between both physical and mental summaries of HRQL and physical activity, as has already been reported by studies in older adults. Prospective studies have demonstrated a longitudinal association between physical activity and better health status (30), but no information is yet available regarding the inverse association, that is, a longitudinal association between HRQL and physical activity. Dyspnea was associated with lower physical activity practice, according to previous clinical studies (27,32). Our finding confirms that dyspnea not only limits exercise capacity (21) in experimental conditions (a measure of the performance or physical fitness) but also limits physical activity under real conditions (the behavior). The fact that dyspnea only achieved statistical significance in the final multivariate model if mental HRQL was excluded may reflect factors more related to behavior than to physiology, as suggested by a previous experimental study that claimed that more importance needs to be given to symptom tolerance and motivation when interpreting findings involving dyspnea (21).
Women and older subjects exhibited lower levels of energy expenditure in physical activity, according to a large number of previous studies in the general population (25), and also in our geographic area (9). The independent association between high socioeconomic status and lower physical activity level that we have found is in contradiction with most previous reports (25), even in Barcelona (9). We cannot exclude that high SES patients were less likely to be included in our sample, being selection bias a possible explanation for the present results. Self-reported diabetes was also found to be associated with a lower level of physical activity, according to previous reports (5). Studies in diabetic patients (Types 1 and 2) have demonstrated that this association may be explained by several alterations of the disease, including hypoglycemia, peripheral and autonomic neuropathy, peripheral artery disease, nephropathy, and retinopathy (5).
Surprisingly, FEV1 was not related to physical activity in our patients, in contrast with two clinical studies including convenience samples of COPD subjects that found a correlation between daily movements, measured by pedometer (27) and accelerometer (32), and FEV1. In addition, the EPIC study reported a cross-sectional positive association between physical activity and FEV1 values and a slower decline of FEV1 among the physically more active participants, in a large cohort from the general population from which respiratory patients had been excluded (20). Unfortunately, we did not obtain data on other parameters of lung function (e.g., dynamic hyperinflation) that probably have a more prominent role than FEV1 in exercise limitation (24).
We did not find an association between BMI and physical activity in our COPD patients, despite the fact that many studies in the general population have demonstrated an increased risk of inactivity among obese persons (25) and an increased risk of overweight in subjects with lower physical activity level (22). We found a normal range of BMI values, in accordance with a previous study that reported a lower prevalence of low weight syndrome in COPD subjects from the Mediterranean area compared with northern countries (10). Probably, differences in the BMI of COPD patients in different geographical areas, as well as differences in the role of nutritional status between COPD and healthy subjects, could explain the lack of association between BMI and physical activity in our study.
The main limitation of the current study is that its cross-sectional design makes it impossible to demonstrate cause-effect relationships. An additional problem arises in our data because the outcome (physical activity level) could have influenced some of the exposures, both through a direct effect on exposure or through an effect on reported or measured exposure. To help with causality assessment, we considered dose-response or checkmark patterns (12) (results not shown; data available from the authors). Unfortunately, we found inconsistent patterns for all continuous exposure variables (previous COPD admissions, dyspnea, FEV1, PO2, BMI, and physical and mental summaries of HRQL), which did not allow inferring about direction of the association and which, otherwise, may be the result of several methodological limitations (an inappropriate comparison group, nonlinearity of associations, or nonnormality of distributions (12)).
The validity of the questionnaire in quantifying physical activity could be argued. It has been reported that it underestimates daily physical activity compared with direct techniques (31). Despite that, our results regarding the proportion of subjects practicing physical activities (e.g., walking), or its comparison with other populations, would be still valid. In addition, a possible underestimation of physical activity quantification would be equal for all individuals, which does not influence the relation between physical activity group and the several factors tested.
As has been previously argued (13–15), patients included in our study were mostly males, 69 yr old on average, had a mean FEV1 predicted of 36% and had experienced a mean of 1.6 admissions in the year before recruitment. These characteristics represent the usual pattern of COPD admissions in Barcelona tertiary hospitals and probably elsewhere, with the exception of male predominance, which is in agreement with COPD gender distribution in Spain (26). However, one should be cautious in generalizing the results, as patients in earlier or advanced stages of the disease may exhibit different patterns of physical activity practice.
In conclusion, one third of COPD patients in our study reported a level of physical activity lower than the equivalent to walking less than 15 min·d−1. Apart from sociodemographic variables, comorbidity, health-related quality of life, and LTOT were the only factors independently associated with low level of physical activity. These results can be useful in the design of rehabilitation programs and should stimulate further interest in investigating and improving the physical activity practice in people with COPD.
1. Ainsworth, B. E., W. L. Haskell, A. S. Leon, et al. Compendium of physical activities: classification of energy costs of human physical activities. Med. Sci. Sports Exerc
. 25:71–80, 1993.
2. Alonso, J., L. Prieto, M. Ferrer, et al. Testing the measurement properties of the Spanish version of the SF-36 Health Survey among male patients with chronic obstructive pulmonary disease. Quality of Life in COPD Study Group. J. Clin. Epidemiol
. 51:1087–1094, 1998.
3. Alonso J., E. Regidor, G. Barrio, L. Prieto, C. Rodriguez, and L. de la Fuente. [Population reference values of the Spanish version of the Health Questionnaire SF-36] Valores poblacionales de referencia de la versión española del Cuestionario de Salud SF-36. Med. Clin. (Barc.)
4. Alvarez-Darde T., C., J. Alonso, A. Domingo, and E. Regidor. 1995. [Social Class assessment in Health Sciences]. Barcelona: SG Editores, p. 117.
5. American Diabetes Association. Diabetes mellitus and exercise. Diabetes Care
6. Anthonisen, N. R., J. Manfreda, C. P. W. Warren, E. S. Hershfield, G. K. M. Harding, and N. A. Nelson. Antibiotic therapy in exacerbations of chronic obstructive pulmonary disease. Ann. Intern. Med
. 106:196–204, 1987.
7. Baarends, E. M., A. M. Schols, K. R. Westerterp, and E. F. Wouters. Total daily energy expenditure relative to resting energy expenditure in clinically stable patients with COPD. Thorax
8. Belman, M. J. Exercise in patients with chronic obstructive pulmonary disease. Thorax
9. Borrell, C., F. Dominguez-Berjon, M. I. Pasarin, I. Rohlfs, J. Ferrando, and E. Fernández. Social inequalities in health related behaviours in Barcelona. J. Epidemiol. Community Health
10. Coronell, C., M. Orozco-Levi, A. Ramírez-Sarmiento, J. Martínez-Llorens, J. Broquetas, and J. Gea. [Low-weight syndrome associated with COPD in our setting]. Síndrome de bajo peso asociado a la EPOC en nuestro medio. Arch. Bronconeumol
. 38:580–584, 2002.
11. Elosua, R., J. Marrugat, L. Molina S. Pons, E. Pujol, and MARATHOM investigators. Validation of the Minnesota Leisure Time Physical Activity Questionnaire in Spanish men: the MARATHOM investigators. Am. J. Epidemiol
. 139:1197–209, 1994.
12. Flanders, W. D., L. Lin, J. L. Pirkle, and S. Caudill. Assessing the direction of causality in cross-sectional studies. Am. J. Epidemiol
. 135:926–935, 1992.
13. Garcia-Aymerich, J., E. Barreiro, E. Farrero, et al. Patients hospitalized for COPD have a high prevalence of modifiable risk factors for exacerbation (EFRAM study). Eur. Respir J
. 16:1037–1042, 2000.
14. Garcia-Aymerich, J., E. Farrero, M. A. Félez, et al. Risk factors of re-hospitalisation for a COPD exacerbation: a prospective study. Thorax
15. Garcia-Aymerich, J., E. Monsó, R. M. Marrades, et al. Risk factors for hospitalisation for a chronic obstructive pulmonary disease exacerbation: EFRAM study. Am. J. Respir. Crit. Care Med
. 164:1002–1007, 2001.
16. Gosker, H. R., N. H. Lencer, F. M. Franssen, G. J. Van der Vusse, E. F. Wouters, and A. M. Schols. Striking similarities in systemic factors contributing to decreased exercise capacity in patients with severe chronic heart failure or COPD. Chest
17. Granados, A., J. Escarrabill, J. M. Borràs, V. Sánchez, and A. J. Jovell. [Appropriate use and effectiveness of chronic domiciliary oxygen therapy in Catalonia] Utilización apropiada y efectividad: la oxigenoterapia crónica domiciliaria en Cataluña. Med. Clin. (Barc.)
18. Haftenberger, M., A. J. Schuit, M. J. Tormo, et al. Physical activity of subjects aged 50–64 years involved in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr
. 5:1163–1176, 2002.
19. Hosmer, D. W. and S. Lemeshow. Applied Logistic Regression
. New York: John Wiley & Sons, 1995, pp. 82–91.
20. Jakes, R. W., N. E. Day, B. Patel, et al. Physical inactivity is associated with lower forced expiratory volume in 1 second: European Prospective Investigation into Cancer-Norfolk Prospective Population Study. Am. J. Epidemiol
. 156:139–147, 2002.
21. Killian, K. J., P. Leblanc, D. H. Martin, E. Summers, N. L. Jones, and J.M. Campbell. Exercise capacity and ventilatory, circulatory and symptom limitation in patients with chronic airflow limitation. Am. Rev. Respir. Dis
. 146:935–940, 1992.
22. Kopelman, P. G. Obesity as a medical problem. Nature
23. Lacasse, Y., G. H. Guyatt, and R. S. Goldstein. The components of a respiratory rehabilitation program: a systematic overview. Chest
24. Marin, J. M., S. J. Carrizo, M. Gascon, A. Sánchez, B. A. Gallego, and B. R. Celli. Inspiratory capacity, dynamic hyperinflation, breathlessness, and exercise performance during the 6-minute-walk test in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med
. 163:1395–1399, 2001.
25. Pate, R. R., M. Pratt, S. N. Blair, et al. Physical activity and public health: a recommendation from the Centers for Disease Control and Prevention and the American College of Sports Medicine. JAMA
26. Pena, V. S., M. Miravitlles, R. Gabriel, et al. Geographic variations in prevalence and underdiagnosis of COPD: results of the IBERPOC multicentre epidemiological study. Chest
27. Schönhofer, B., P. Ardes, M. Geibel, D. Köhler, and P. W. Jones. Evaluation of a movement detector to measure daily activity in patients with chronic lung disease. Eur. Respir J
. 10:2814–2819, 1997.
28. Serres, I., V. Gautier, A. Varray, and C. Préfaut. Impaired skeletal muscle endurance related to physical inactivity and altered lung function in COPD. Chest
29. Slinde, F., L. Ellegard, A. M. Gronberg, S. Larsson, and L. Rossander-Hulthén. Total energy expenditure in underweight patients with severe chronic obstructive pulmonary disease living at home. Clin. Nutr
. 22:159–165, 2003.
30. Spirduso, W. W., and D. L. Cronin. Exercise dose-response effects on quality of life and independent living in older adults. Med. Sci. Sports Exerc
. 33:S598–S608, 2001.
31. Starling, R. D., D. E. Matthews, P. A. Ades, and E. T. Poehlman. Assessment of physical activity in older individuals: a doubly labeled water study. J. Appl. Physiol
. 86:2090–2096, 1999.
32. Steele, B. G., L. Holt, B. Belza, S. Ferris, S. Lakshminaryan, and D. M. Buchner. Quantitating physical activity in COPD using a triaxial accelerometer. Chest
33. Taylor, H. L., D. R. Jacobs Jr., B. Schucker, J. Knudsen, A. S. Leon, and G. Debacker. A questionnaire for the assessment of leisure time physical activities. J. Chronic Dis
. 31:741–755, 1978.
34. Tormo Díaz, M. J., C. Navarro Sánchez, M. D. Chirlaque López, and D. Pérez Flores. [Cardiovascular risk factors in the region of Murcia, Spain] Factores de riesgo cardiovascular en la Región de Murcia, España. Rev. Esp. Salud Pública
35. Ware, J. E., M. Kosinski, and S. D. Keller. A 12-item short-form health survey: construction of scales and preliminary tests of reliability and validity. Med. Care
36. Yusuf, H. R., J.B. Croft, W.H. Giles, et al. Leisure-time physical activity among older adults: United States, 1990. Arch Intern Med
. 156:1321–1326, 1996.
COPD; EXERCISE; EPIDEMIOLOGY; MULTIVARIATE ANALYSIS; CROSS-SECTIONAL STUDIES; QUESTIONNAIRE
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