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(Chest. 2003;124:432-437.)
© 2003 American College of Chest Physicians

Leisure-Time Physical Activity Patterns Among US Adults With Asthma*

Earl S. Ford, MD, MPH; Gregory W. Heath, PhD; David M. Mannino, MD, FCCP and Stephen C. Redd, MD

* From the Division of Environmental Hazards and Health Effects (Drs. Ford, Mannino, and Redd), National Center for Environmental Health, and the Division of Nutrition and Physical Activity (Dr. Heath), National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, GA.

Correspondence to: Earl Ford, MD, MPH, Division of Environmental Hazards and Health Effects, National Center for Environmental Health, Centers for Disease Control and Prevention, 1600 Clifton Rd, MS E17, Atlanta, GA 30333; email: esf2{at}cdc.gov


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Little is known about the physical activity patterns among US adults who have asthma.

Methods: Using data for 165,123 respondents of the 2000 Behavioral Risk Factor Surveillance System, we examined leisure-time physical activity.

Results: After adjusting for age, about 30% of participants with current asthma (12,489 participants), 24% with former asthma (4,892 participants), and 27% who never had asthma (147,742 participants) were considered to be inactive (p < 0.001). After adjusting for age, the estimated energy expenditure from leisure-time physical activity was 206 kilocalories (kcal) per week lower among respondents with current asthma than among respondents with former asthma (p < 0.001) and 91 kcal/week lower than respondents who had never had asthma (p < 0.001). About 27% of participants with current asthma, 28% of participants with former asthma, and 28% of participants who had never had asthma were participating in recommended levels of physical activity. Walking was the most frequently reported activity for all three groups (respondents with current asthma, 39%; respondents with former asthma, 39%; and respondents who had never had asthma, 38%. Participants with asthma were less likely to engage in running (p < 0.001), basketball (p = 0.001), golf (p < 0.001), and weightlifting (p = 0.001) but were more likely to use an exercise bicycle (p = 0.035) than were participants without asthma.

Conclusions: Like most US adults, the majority of those with asthma were not meeting the current recommendations for physical activity.

Key Words: asthma • cross-sectional studies • exercise • health surveys


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The health benefits of adequate physical activity are well-recognized.1 Recommendations for physical activity have evolved to the current ones of physical activity of at least a moderate intensity for >= 30 minutes on all or most days of the week.1 2 Despite the benefits of physical activity and the existence of national recommendations, the majority of the US population remains insufficiently active.3

Although current physical activity recommendations apply to people with asthma as well, their condition may cause some to limit participation in physical activity. However, little is known about physical activity patterns of US adults with asthma. Such information is useful to public health professionals and health-care providers in designing programs and providing proper counsel and treatment regimes to promote the health and well-being of people with asthma through the adoption of active lifestyles. This is especially relevant in light of data that show people with asthma are more likely than people without asthma to be obese. To better understand current leisure-time physical activity patterns among US adults with asthma, we examined data from the 2000 Behavioral Risk Factor Surveillance System (BRFSS). Because the BRFSS does not include questions about the relationships between physical activity participation and asthma symptomatology, we were unable to examine this issue.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Since 1983, the Centers for Disease Control and Prevention have supported state-based telephone surveys of risk factors for chronic disease.4 5 6 The BRFSS is a standardized telephone survey carried out by health agencies in the 50 states, the District of Columbia, and three territories (ie, Guam, Puerto Rico, and the Virgin Islands) with assistance from the Centers for Disease Control and Prevention. The primary purpose of the BRFSS is to provide state-specific estimates of the prevalence of behaviors that relate to the leading causes of death in the United States. Each participating state selects an independent probability sample for interview from residents aged >= 18 years in households with telephones. All states in a given year use an identical core questionnaire that is administered over the telephone by trained interviewers.4 5 6

Respondents were classified as currently having asthma (current asthma) if they answered the following two questions affirmatively: "Did a doctor ever tell you that you had asthma?"; and "Do you still have asthma?" Respondents who reported ever being told they had asthma but who no longer had asthma were classified as formerly having asthma (former asthma). Respondents who had never been told that they had asthma were classified as never having had asthma.

Participants were asked "During the past month, did you participate in any physical activities or exercises such as running, calisthenics, golf, gardening, or walking for exercise?" Those who answered affirmatively then were asked to provide information about the type, frequency, and duration of up to two activities. From this information, several indexes of physical activity status were derived. First, respondents who engaged in any physical activity or pair of activities that required rhythmic contraction of large muscle groups at 50% functional capacity for >= 20 min three or more times per week were defined as engaging in regular and vigorous activity. Respondents who engaged in any physical activity or pair of activities for >= 20 min three or more times per week at < 50% of capacity were defined as engaging in regular activity. Respondents who engaged in any physical activity or pair of activities for < 20 min or less than three times per week were defined as engaging in irregular activity. Respondents reporting no physical activity were defined as being physically inactive. In several small studies, the BRFSS physical activity questions were found to have acceptable reliability.7 Although the validity of these questions has not been tested directly, studies of the validity of similar physical activity instruments have suggested that the BRFSS questions should have reasonable validity.7

Second, we calculated the proportions of participants who engaged in vigorous or moderate leisure-time physical activity using different definitions.8 On the basis of published formulas for estimated maximal cardiorespiratory capacity, a respondent was defined as being vigorously active if he or she participated in an activity with a metabolic equivalent (MET) level that >= 60% of the calculated maximal cardiorespiratory capacity at least three times per week for >= 20 min each time. MET values from published tables were assigned to activities.9 One MET is the energy expenditure of approximately 3.5 mL oxygen per kilogram of body weight per minute or 1 kcal/kg body weight per hour. Respondents who engaged in physical activity five times or more per week for at least 30 min on each occasion were designated as participating in moderate-intensity physical activity. Respondents who engaged in leisure-time physical activity that did not meet the criteria for moderate or vigorous physical activity were classified as being insufficiently active. Respondents who did not report engaging in leisure-time physical activity were classified as inactive.

Third, we calculated energy expenditure (in kilocalories per week) for participants. Inactive participants were given a value of 0. For participants who reported participating in one or more physical activities or exercises, the weekly energy expenditure for each activity was calculated as follows: METs x hours per week x weight (in kilograms) and then summed.

We included the following covariates in our analyses: age; sex; race or ethnicity; educational attainment; and body mass index. Body mass index (in kilograms per square meter) was calculated from self-reported weights and heights.

Of the 367,381 people who were contacted, 184,450 participated in the survey. We excluded women who reported being pregnant (2,078 women; 1.1%) and respondents with missing values for asthma (2,536 respondents; 1.4%), age (1,109 respondents; 0.6%), race or ethnicity (1,927 respondents; 1.0%), educational status (471 respondents; 0.3%), physical activity level (2,059 respondents; 1.1%), and body mass index (10,229 respondents; 5.5%). After these exclusions, 165,123 participants (12,489 participants with current asthma, 4,892 participants with former asthma, and 147,742 participants who never had asthma) from the 50 states, the District of Columbia, and Puerto Rico were included in the analyses.

We calculated weighted percentages or means for the different measures of physical activity. We also calculated the mean weekly energy expenditure after capping the calculated energy expenditure of some participants at 8,000 kcal per week (representing about 10 h of vigorous activity per day). Age-adjusted estimates using the direct method were calculated using the US population age structure for 2000. We used a statistical software package (SUDAAN; Research Triangle Institute; Research Triangle Park, NC) to account for the complex sampling design of the survey.10


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
A larger percentage of participants with current asthma were aged 18 to 29 years (p < 0.001), were women (p < 0.001), were African-American (p = 0.001), and had not completed high school (p = 0.009) [Table 1 ]. In addition, participants with asthma were more likely than participants who had never had asthma to be obese (p < 0.001).


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  		Table 1.. Selected Sociodemographic Characteristics by Asthma Status, BRFSS, 2000*

 
About 31% of participants with current asthma were inactive, compared with 28% of participants without asthma (p < 0.001) [Table 2 ]. A smaller percentage of participants with asthma were more vigorously active than were participants without asthma. Similar percentages of participants with and without asthma were irregularly active or regularly active. In addition, the average energy expenditure of participants with current asthma was 91 kcal per week lower than that of participants without asthma (p < 0.001).


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  		Table 2.. Age-Adjusted Percentage of Persons Engaging in Leisure-Time Physical Activity, by Asthma Status, BRFSS, 2000*

 
Asthma status (p = 0.813) was not a significant predictor of achieving recommended levels of physical activity in logistic regression models that included age, sex, race or ethnicity, education, smoking status, and body mass index as covariates. Furthermore, the associations between asthma status and physical activity did not differ significantly by sex (p = 0.901 for the interaction between sex and asthma status). Age appeared to modify the association between asthma status and physical activity, however (p = 0.003 for the interaction between age and asthma status). When we examined the associations between asthma status and physical activity for each of six age strata (ie, 18 to 29 years, 30 to 39 years, 40 to 49 years, 50 to 59 years, 60 to 69 years, and >= 70 years), we found no significant associations for all age strata < 60 years. Among participants who were aged 60 to 69 years, those with former asthma were less likely to engage in physical activity than were those who had never had asthma (odds ratio, 0.63; 95% confidence interval, 0.42 to 0.94). For participants aged >= 70 years, respondents with current asthma were less likely to engage in physical activity than those who never had had asthma (odds ratio, 0.78; 95% confidence interval, 0.63 to 0.97).

In general, the rank order of preferred activities differed little between participants with current asthma, participants with former asthma, and participants who had never had asthma. For all three groups, the most frequently reported physical activity was walking (Table 3 ). Of the most frequently practiced physical activities listed in Table 3 , participants with asthma were less likely than participants without asthma to engage in running (p = <0.001), basketball (p = 0.001), golf (p = <0.001), and weightlifting (p = 0.001) but were more likely to use an exercise bicycle (p = 0.035).


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  		Table 3.. Most Prevalent Physical Activities by Asthma Status, BRFSS, 2000

 

   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Like the rest of the US population, a minority of people with asthma are engaged in the recommended levels of physical activity during leisure time. As a group, people with asthma are slightly more likely than people who have never had asthma to be inactive. Furthermore, they are less likely to participate in more intense or vigorous activities such as running and vigorous sports.

According to current guidelines, Americans should engage in moderate physical activity for at least 30 min on most or all days of the week.2 These goals clearly constitute minimum requirements for physical activity, and exceeding these recommendations is likely to produce additional health benefits. No specific guidelines about physical activity for patients with asthma appear to have been developed. Walking has been advocated as a good way to meet physical activity recommendations because walking is commonly practiced by much of the population, opportunities to walk are ample for most people, and no special equipment is required. Furthermore, studies11 have suggested that walking can convey important health benefits. As for people without asthma, walking is the most commonly reported physical activity among people with asthma.

People with asthma can benefit from adequate physical activity in several ways. First, the well-known benefits from physical activity should accrue to patients with asthma. These include reduced premature mortality and reduced morbidity from a myriad of diseases. Physical activity also contributes to improved social and mental well-being3 and to improved self-image.12 Furthermore, physical activity favorably affects the activities of daily living13 and is associated with better quality of life.14 Second, physical activity may favorably affect their asthma as well.15 16 However, additional research about the possible benefits on asthma symptoms and quality of life has been advocated.17 Evidence suggests that physical activity may reduce the incidence of asthma.18 19 20 Third, the prevalence of obesity among people with asthma is greater than that among those without asthma.21 22 Because obesity has been associated with more severe disease or poorer asthma control, achieving a healthy weight is an important goal among patients with asthma. Physical activity is an important behavior to achieve and maintain a desirable weight.

Relatively, few studies about physical activity patterns among adults with asthma have been conducted. Using data from the 1994 to 1995 Canadian National Population Health Survey,23 researchers found that participants with asthma were about as active as those who did not have asthma. Younger participants with asthma tended to report higher energy expenditures than participants without asthma, whereas older participants with asthma tended to have lower energy expenditures than control participants. Studies of children24 generally also have found that children with asthma are about as active as children who do not have asthma. However, studies have reached different conclusions about whether the cardiorespiratory status of children with asthma differs significantly from that of children without asthma.25 26

The prevalence of exercise-induced asthma may be as high as 13% in the population27 and as high as 90% among people with asthma.28 Undoubtedly, the presence of this condition constitutes a barrier to participation in physical activity for some and may be a reason that people with asthma are less likely to participate in more intense or vigorous activities. Even in the absence of exercise-induced asthma, other people with asthma may perceive their condition as an obstacle to physical activity participation.29 If people with asthma limit their physical activity, they are likely to become deconditioned, thus increasing their reluctance to engage in physical activity.30 Therefore, people with asthma may benefit from better understanding about asthma and physical activity.29 With proper treatment and support, most adults with or without exercise-induced asthma should be able to participate fully in physical activity.13 27 31 32 33 34 Population-based research about the knowledge and attitudes of adults with asthma regarding asthma and physical activity may increase the understanding about the potential barriers to adequate participation in physical activity, and be useful in designing public health and clinical interventions to help adults with asthma become sufficiently active. In one study, children with asthma demonstrated favorable attitudes toward exercise and sports.35 Because the BRFSS does not include questions about the relations between physical activity participation and asthma symptomatology, we were unable to examine this issue.

Because the presence of asthma was based on self-reports, some misclassification of asthma status may have occurred. However, self-reported asthma is commonly used in epidemiologic studies, and the sensitivity and specificity of self-reported asthma is acceptable.36 37 38 Respondents with asthma were not asked about the severity of their condition. Participants could report only a maximum of two activities or exercises. Thus, the physical activity status could have been wrongly assigned and the energy expenditure could have been underestimated for respondents who participated in more than two activities. Furthermore, the BRFSS questionnaire for 2000 did not include questions about other sources of physical activity, such as occupational and household physical activity. In addition, the intensity of participation was not determined for most activities.

In this most detailed and largest examination of leisure-time physical activity patterns among US adults with asthma to date, we have shown that physical activity patterns among adults with asthma are, for the most part, similar to those among adults without asthma. However, a slightly higher percentage of adults with asthma are more inactive than their counterparts. Like most of the US population, the majority of adults with asthma are not meeting the national recommendations for physical activity. Although asthma may make it difficult for some people to participate in the recommended physical activity, the overwhelming majority of people with asthma should be able to participate in physical activity that meets the national recommendations. Health-care providers can help to educate their patients about the importance of being active and to enable their patients to achieve this goal.


   Footnotes
 
Abbreviations: BRFSS = behavioral risk factor surveillance system; kcal = kilocalories; MET = metabolic equivalent

Received for publication September 12, 2002. Accepted for publication January 23, 2003.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. . US Department of Health and Human Services (1996) Physical activity and health: a report of the Surgeon General. US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion. Atlanta, GA:
  2. Pate, RR, Pratt, M, Blair, SN, 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 1995;273,402-407[Abstract]
  3. Pratt, M, Macera, CA, Blanton, C Levels of physical activity and inactivity in children and adults in the United States: current evidence and research issues. Med Sci Sports Exerc 1999;31(suppl),S526-S533[ISI][Medline]
  4. Gentry, EM, Kalsbeek, WD, Hogelin, GC, et al The behavioral risk factor surveys: II. Design, methods, and estimates from combined state data. Am J Prev Med 1985;1,9-14[Medline]
  5. Remington, PL, Smith, MY, Williamson, DF, et al Design, characteristics, and usefulness of state-based behavioral risk factor surveillance: 1981–87. Public Health Rep 1988;103,366-375[ISI][Medline]
  6. Nelson, DE, Holtzman, D, Waller, M, et al Objectives and design of the behavioral risk factor surveillance system. Proceedings of the Section on Survey Methods August 10, 1998 American Statistical Association National Meeting. Dallas TX:
  7. Washburn, RA, Heath, GW, Jackson, AW Reliability and validity issues concerning large-scale surveillance of physical activity. Res Q Exerc Sport 2000;71(suppl),S104-S113[ISI][Medline]
  8. Centers for Disease Control and Prevention. Physical activity trends: United States, 1990–1998. MMWR Morb Mortal Wkly Rep 2001;50,166-169[Medline]
  9. Ainsworth, BE, Haskell, WL, Whitt, MC, et al Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 2000;32(suppl),S498-S504
  10. Shah, BV, Barnwell, BG, Bieler, GS SUDAAN user’s manual, version 7.5. 1997 Research Triangle Institute. Research Triangle Park, NC:
  11. Wannamethee, SG, Shaper, AG Physical activity in the prevention of cardiovascular disease: an epidemiological perspective. Sports Med 2001;31,101-114[CrossRef][ISI][Medline]
  12. Shephard, RJ Training and the respiratory system–therapy for asthma and other obstructive lung diseases? Ann Clin Res 1982;14(suppl),86-96
  13. Clark, CJ, Cochrane, LM Physical activity and asthma. Curr Opin Pulm Med 1999;5,68-75[CrossRef][Medline]
  14. Ford, ES, Moriarty, DG, Zack, MM, et al Self-reported body mass index and health-related quality of life: findings from the Behavioral Risk Factor Surveillance System. Obes Res 2001;9,21-31[ISI][Medline]
  15. Malkia, E, Impivaara, O Intensity of physical activity and respiratory function in subjects with and without bronchial asthma. Scand J Med Sci Sports 1998;8,27-32[ISI][Medline]
  16. van Veldhoven, NH, Vermeer, A, Bogaard, JM, et al Children with asthma and physical exercise: effects of an exercise programme. Clin Rehabil 2001;15,360-370[Abstract/Free Full Text]
  17. Ram, FS, Robinson, SM, Black, PN Effects of physical training in asthma: a systematic review. Br J Sports Med 2000;34,162-167[Abstract/Free Full Text]
  18. Platts-Mills, TA, Carter, MC, Heymann, PW Specific and nonspecific obstructive lung disease in childhood: causes of changes in the prevalence of asthma. Environ Health Perspect 2000;108(suppl),725-731[CrossRef]
  19. Rasmussen, F, Lambrechtsen, J, Siersted, HC, et al Low physical fitness in childhood is associated with the development of asthma in young adulthood: the Odense schoolchild study. Eur Respir J 2000;16,866-870[Abstract]
  20. Huovinen, E, Kaprio, J, Laitinen, LA, et al Social predictors of adult asthma: a co-twin case-control study. Thorax 2001;56,234-236[Abstract/Free Full Text]
  21. Chen, Y, Dales, R, Krewski, D, et al Increased effects of smoking and obesity on asthma among female Canadians: the National Population Health Survey, 1994–1995. Am J Epidemiol 1999;150,255-262[Abstract/Free Full Text]
  22. Young, SY, Gunzenhauser, JD, Malone, KE, et al Body mass index and asthma in the military population of the northwestern United States. Arch Intern Med 2001;161,1605-1611[Abstract/Free Full Text]
  23. Chen, Y, Dales, R, Krewski, D Leisure-time energy expenditure in asthmatics and non-asthmatics. Respir Med 2001;95,13-18[CrossRef][ISI][Medline]
  24. Nystad, W The physical activity level in children with asthma based on a survey among 7–16 year old school children. Scand J Med Sci Sports 1997;7,331-335[ISI][Medline]
  25. Santuz, P, Baraldi, E, Filippone, M, et al Exercise performance in children with asthma: is it different from that of healthy controls? Eur Respir J 1997;10,1254-1260[Abstract]
  26. Wong, TW, Yu, TS, Wang, XR, et al Predicted maximal oxygen uptake in normal Hong Kong Chinese schoolchildren and those with respiratory diseases. Pediatr Pulmonol 2001;31,126-132[CrossRef][ISI][Medline]
  27. Milgrom, H, Taussig, LM Keeping children with exercise-induced asthma active. Pediatrics 1999;104,e38[Abstract/Free Full Text]
  28. McFadden, ER, Jr Exercise-induced airway obstruction. Clin Chest Med 1995;16,671-682[ISI][Medline]
  29. Garfinkel, SK, Kesten, S, Chapman, KR, et al Physiologic and nonphysiologic determinants of aerobic fitness in mild to moderate asthma. Am Rev Respir Dis 1992;145,741-745[ISI][Medline]
  30. Counil, FP, Karila, C, Varray, A, et al Anaerobic fitness in children with asthma: adaptation to maximal intermittent short exercise. Pediatr Pulmonol 2001;31,198-204[CrossRef][ISI][Medline]
  31. Bundgaard, A Exercise and the asthmatic. Sports Med 1985;2,254-266[ISI][Medline]
  32. D’Urzo, A Exercise-induced asthma: what family physicians should do. Can Fam Physician 1995;41,1900-1906[ISI][Medline]
  33. Fowler, C Preventing and managing exercise-induced asthma. Nurse Pract 2001;26,25, 29-33
  34. Sonna, LA, Angel, KC, Sharp, MA, et al The prevalence of exercise-induced bronchospasm among US Army recruits and its effects on physical performance. Chest 2001;119,1676-1684[Abstract/Free Full Text]
  35. Weston, AR, Macfarlane, DJ, Hopkins, WG Physical activity of asthmatic and nonasthmatic children. J Asthma 1989;26,279-286[ISI][Medline]
  36. Harlow, SD, Linet, MS Agreement between questionnaire data and medical records: the evidence for accuracy of recall. Am J Epidemiol 1989;129,233-248[Free Full Text]
  37. Linet, MS, Harlow, SD, McLaughlin, JK, et al A comparison of interview data and medical records for previous medical conditions and surgery. J Clin Epidemiol 1989;42,1207-1213[CrossRef][ISI][Medline]
  38. Toren, K, Brisman, J, Jarvholm, B Asthma and asthma-like symptoms in adults assessed by questionnaires: a literature review. Chest 1993;104,600-608[Abstract/Free Full Text]



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