This review aims to give an overview of available published evidence concerning the association between physical activity and asthma in children, adolescents and adults.
We included all original articles in which both physical activity and asthma were assessed in case-control, cross-sectional or longitudinal (cohort) studies. Excluded were studies concerning physical fitness, studies in athletes, therapeutic or rehabilitation intervention studies such as physical training or exercise in asthma patients. Methodological quality of the included articles was assessed according to the Newcastle-Ottawa Scale (NOS).
A literature search was performed until June 2011 and resulted in 6,951 publications derived from PubMed and 1,978 publications from EMBASE. In total, 39 studies met the inclusion criteria: 5 longitudinal studies (total number of subjects n = 85,117) with physical activity at baseline as exposure, and asthma incidence as outcome. Thirty-four cross-sectional studies (n = 661,222) were included. Pooling of the longitudinal studies showed that subjects with higher physical activity levels had lower incidence of asthma (odds ratio 0.88 (95% CI: 0.77–1.01)). When restricting pooling to the 4 prospective studies with moderate to good study quality (defined as NOS≥5) the pooled odds ratio only changed slightly (0.87 (95% CI: 0.77–0.99)). In the cross-sectional studies, due to large clinical variability and heterogeneity, further statistical analysis was not possible.
The available evidence indicates that physical activity is a possible protective factor against asthma development. The heterogeneity suggests that possible relevant effects remain hidden in critical age periods, sex differences, or extremes of levels of physical activity (e.g. sedentary). Future longitudinal studies should address these issues.
Citation: Eijkemans M, Mommers M, Draaisma JMT, Thijs C, Prins MH (2012) Physical Activity and Asthma: A Systematic Review and Meta-Analysis. PLoS ONE 7(12): e50775. doi:10.1371/journal.pone.0050775
Editor: Adrian V. Hernandez, Universidad Peruana de Ciencias Aplicadas (UPC), Peru
Received: July 17, 2012; Accepted: October 24, 2012; Published: December 20, 2012
Copyright: © 2012 Eijkemans et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors have no support or funding to report.
Competing interests: The authors have declared that no competing interests exist.
The prevalence of asthma has increased significantly during the past decades . Concurrently, the prevalence of overweight has increased, while physical activity levels have decreased substantially , . In 2005, less than half (49.1%) of US adults met the CDC/ACSM (Centers for Disease Control and Prevention/American College of Sports Medicine) physical activity recommendation (at least 30 minutes of moderately intense activity on five days per week or vigorously intense activity for a minimum of 20 minutes on three days each week) . Physical inactivity is an important risk factor, because it is potentially modifiable and therefore an opportunity for prevention. Several studies have shown that training improves cardiopulmonary fitness, asthma symptoms and quality of life in asthmatic subjects . This evidence suggests that training and high levels of physical activity play a role in the course and severity of asthma. Besides this, an etiological relation between physical activity levels and development of incident asthma might also be possible. Different hypotheses have been suggested to explain the possible protective character of physical activity against asthma development such as reducing airway inflammation, a central feature of asthma . Another explanation is that physical activity could positively influence the patency of bronchioles: poor mucociliary clearance from decreased epithelial stimulation secondary to decreased activity can cause excess mucus and airway edema. Decreased deep inspiration and sigh rate during physical inactivity could lead to smooth muscle latching and subsequent increased risk of asthmatic symptoms .
We performed a systematic literature review to evaluate the potential causal relation between physical (in)activity and asthma development, and a pooled analysis to estimate the effect size.
We conducted an electronic search in PubMed (US National Library of Medicine) and EMBASE to obtain all publications on studies that reported on physical activity and asthma published until June 2011. The PubMed search used the Medical Subject Headings (MeSH) terms “motor activity” or text word terms “activity”, “physical activity”, “physical exercise” or “sedentary”, as well as the MeSH term “asthma” or text word terms “asthma”, “asthmatic”, “wheeze” or “wheezing”. The EMBASE search used the MeSH terms “motor activity” or “physical activity” or text word terms “physical activity”, “physical exercise”, “sedentary”, as well as the MeSH terms “asthma” or “wheezing” or the text word terms “asthma”, “asthmatic”, “wheeze” or “wheezing”. These terms were searched using limits that included all articles published in the English language. There were no age restrictions.
We conformed to the MOOSE (Meta-analysis Of Observational Studies in Epidemiology) guidelines for reporting  and PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) statement .
Our primary research question concerned the role of habitual physical activity in the development of incident asthma. Therefore, we searched for longitudinal studies in which the exposure (physical activity) precedes the outcome (onset of asthma). In addition, we included studies that looked into asthma prevalence in different physical activity levels. For this goal, we searched cross-sectional studies that investigated physical activity levels in subjects with asthma compared to controls. For maximal sensitivity, a broad inclusion strategy was used. Inclusion criteria were: original articles in which physical activity as well as asthma was studied, and a control group consisting of healthy subjects or general population. Excluded were studies that did not concern habitual physical activity such as studies in athletes, physical fitness, therapeutic or rehabilitation intervention studies such as physical training in asthma patients. Two investigators (ME, MM) independently assessed whether articles met the inclusion criteria. In case of disagreement, consensus was reached through discussion.
Quality assessment and data extraction
Methodological quality of included articles was assessed according to the Newcastle-Ottawa Scale (NOS). This instrument was developed to assess the quality of nonrandomized studies. Its content validity and inter-rater reliability has been established . The NOS gives predefined criteria, some of which have to be further specified for the specific topic. We specified these criteria in a consensus meeting with all authors (criteria are presented in figure S1 and S2) before assessing the studies. In short, longitudinal studies were assessed for quality of selection (representativeness, selection of controls, ascertainment of exposure, no asthma at start of study); comparability (confounding); and outcome (assessment of outcome, length and adequacy of follow-up). Gender, weight, and smoking were identified as important confounders. Studies could be awarded a maximum score of 9 points. Studies with scores of 5 points or more were considered to be of moderate to good study quality. However, all studies were used for analysis, irrespective of NOS score. Quality assessment was done by all five authors using the NOS. Each single article was assessed by at least three authors independently. In case of disagreement the other two authors were consulted. Quality assessment was completed before data extraction was started. Data were extracted from the full text article. Quantitative results were extracted from text and tables, choosing preferably those adjusted for important confounders (gender, weight, and smoking). Data-extraction in the longitudinal studies was performed independently by two authors (ME, CT). If essential data were lacking in the original studies, their authors were contacted.
Analyses were performed using the statistical software Review Manager version 5 . Heterogeneity among studies was assessed using the chi-square test (significant at p<0.05) and the Higgins I2 test . A random effects model with the Mantel–Haenszel method was used for pooling the results of different studies. Pooled odds ratios (OR) with 95% confidence intervals (CI) were calculated for the longitudinal studies and a subgroup of the cross-sectional studies, namely those studies that used a motion sensor for measuring physical activity levels. We decided to refrain from statistical pooling of the other cross-sectional studies because of substantial clinical and methodological heterogeneity.
The search resulted in 6,951 publications derived from PubMed, and 1,978 studies from EMBASE. Based on titles and abstracts, 8,790 articles were excluded at first screening because they did not meet the eligibility criteria, such as experimental studies with intermediate outcomes (such as inflammatory markers) but no asthma as clinical outcome, case reports and studies with case series without control group, and studies of exercise induced asthma in athletes. Full-text copies of the remaining 139 potentially relevant studies were obtained. Ninety-five studies were excluded because they did not meet the inclusion criteria. Four were excluded because they were duplicate publications of the same studies. One study was not available in full-text. The remaining 39 studies were included for this systematic review. Five studies were longitudinal studies and 34 were cross-sectional in design (figure 1).
Figure 1. flow diagram of study inclusion.doi:10.1371/journal.pone.0050775.g001
All 39 studies were assessed using the adjusted NOS scale (see figure S1 and S2 for the adjusted NOS scales), of which the majority (79%) scored 5 points or more, indicating a moderate to good study quality (table S1 and S2). When grouped by study quality, we could not detect a clear pattern in study results or study characteristics (tables 1 and 2). The authors of 4 articles , , ,  were contacted to obtain essential data that were lacking in the original studies, of which 3 replied , , .
Table 1. Overview of longitudinal studies on physical activity at baseline and incident asthma.doi:10.1371/journal.pone.0050775.t001
Table 2. Overview of cross-sectional studies on physical activity and asthma prevalence.doi:10.1371/journal.pone.0050775.t002
Study characteristics and odds ratios of the longitudinal studies , , , ,  are summarized in table 1. All 5 studies looked into physical activity levels of subjects at baseline and incident asthma during follow up. Follow up duration ranged between 5 and 10 years. Physical activity was assessed by questionnaires. Different reference categories, subgroups and confounders were used (table 1). Asthma diagnosis was defined as doctor's diagnosis, either through self report or linkage to an insurance registry.
Statistical analysis and pooling
Data of the 5 longitudinal studies were pooled using a random effects model (figure 2). Data on studies with more than two groups of different physical activity levels were converted into two groups, namely low physical activity and high physical activity, of which low physical activity was used as reference category. In case of an uneven number of groups, the reference category consisted of the lowest physical activity levels including the middle group.
Figure 2. pooling of longitudinal data: physical activity at baseline and risk of asthma incidence.
M-H; Mantel-Haenszel method, Random effects, CI; confidence interval. Not adjusted for potential confounders. Low physical activity used as reference category. Note that odds ratios are different of those in table 1 because reference categories were reversed and/or the number of categories was converted into two categories per study. For example Beckett et al. and Lucke et al. use high physical activity as reference category; in our meta-analysis we standardized low physical activity as reference category. In studies were more than two categories of physical activity were used (such as Beckett et al. who used 5 levels of physical activity), these were converted into two categories (in case of Becket et al. we converted the highest two levels into high physical activity, and the lowest three levels into low physical activity).doi:10.1371/journal.pone.0050775.g002
Pooled odds ratio was 0.88 (95% CI: 0.77–1.01). Chi-square test for heterogeneity was borderline significant (p = 0.07). Higgins I2 index was 45%, indicating moderate inconsistency. These results are not adjusted for potential confounders as the majority of studies did not provide adjusted results. When we restricted analysis to the studies with moderate to good study quality, identified by NOS scores of 5 or higher, 4 studies remained , , , . Sensitivity analysis showed a consistent result: the pooled odds ratio did not change much (0.87 (95% CI: 0.77–0.99)) but did reach statistical significance.
Study characteristics and results of the 34 cross-sectional studies , , , , , , , , , , , , , , , , , , , , , [ 39], , , , , , , , , , , , ,  are summarized in table 2. The vast majority (25 studies) examined children of different age spans, 8 studies included only adults, and one study included both children (12 years and older) and adults (table 2).
Physical activity was assessed by motion sensors in 7 studies , , , , , , , all examining children (n = 2916). In these studies, asthma was defined as self reported doctor's diagnosis or asthma symptoms. Two studies ,  combined self reported asthma diagnosis with spirometry. Not enough data were available for pooling in one study (i.e. standard deviations were missing despite contacting the authors).  Data of the other 6 studies using motion sensors were pooled: standard mean difference −0.19 (95% CI −0.69; +0.32) (figure 3). Testing for heterogeneity showed a highly significant result (p<0.00001) and high inconsistency (I2 = 94%).
Figure 3. pooling of cross-sectional data using motion sensors: physical activity measured by motion sensors and asthma prevalence.
Random effects, CI; confidence interval. Not adjusted for potential confounders. Low physical activity used as reference category.doi:10.1371/journal.pone.0050775.g003
The other 27 studies used only questionnaires to assess physical activity levels. Methods were diverse (table 2): the majority focused on activity by counting frequency and duration of activity per time unit (month, week, day). , , , , , , , , , , , , , , ,  Others looked into the proportion of subjects that was physically active , , , , , ,  or met the physical activity recommendation. , , , ,  A relatively small number of studies focused on energy expenditure per day  or metabolic equivalent of task (MET). , , ,  Besides physical activity, inactivity (television watching, sedentary time) was also investigated by 9 studies. , , , , , , , ,  Asthma was defined as self reported doctor's diagnosis or asthma symptoms. Only three studies combined questionnaire based asthma diagnosis with spirometry. , , 
We decided to refrain from statistical pooling due to heterogeneity of study designs, populations, and measurement methods for both physical activity and asthma outcome.
In total, 13 studies (564,394 subjects in total) reported a statistically significant association between high physical activity levels and lower asthma prevalence. , , , , , , , , , , , ,  In contrast, 3 studies (total of 1,773 subjects) found a statistically significant association between high physical activity levels and higher asthma prevalence. , ,  Eighteen studies (95,055 subjects) obtained no significant results. , , , , , , , , , , , , , , , , , 
This systematic review gives an overview of the published evidence concerning the association between physical activity and asthma. Our primary research question was aimed at the etiological association between different physical activity levels and subsequent asthma incidence. In an extensive search, we only found 5 longitudinal studies that met the inclusion criteria and could be of use in answering this question. Although the number of longitudinal studies was small, the total accrued number of subjects was considerable (n = 85,117). Pooling showed that subjects with higher physical activity levels might have lower risk of developing asthma.
Thirty-four studies were cross-sectional in design. Due to large clinical variability and heterogeneity we had to refrain from further statistical analysis, except for a small group of studies using a motion sensor to measure physical activity. Despite this limitation, however, we can draw some conclusions: a substantial number of included cross-sectional studies, with the largest total study population, did find an association between high physical activity levels and low asthma prevalence. This seems consistent with physical activity being protective against asthma. However, we can not rule out publication bias. Moreover, cross-sectional studies are not suited to give insight into the causal relation between physical activity and subsequent asthma incidence. Besides the hypothesis that subjects with higher physical activity levels have a lower risk of developing asthma (protective), reverse causality is also possible. There are several hypotheses why asthma patients (with asthma as exposure) could have lower physical activity levels (outcome), such as fear for symptoms of shortness of breath, wrongful education, or by asthma that is not well regulated.
In contrast to the studies that were cross-sectional in design, this reverse causality does not play a role in interpreting the results of the 5 longitudinal studies. In all 5 studies physical activity levels were measured before asthma was diagnosed. However, the results could be influenced by protopathic bias (e.g. physical activity restricted by respiratory complaints that precede an asthma diagnosis) or earlier diagnosis of asthma through exercise-induced symptoms. The first would lead to overestimation of the true association between low physical activity levels and subsequent asthma development; whereas the second would lead to an underestimation. Unfortunately, none of the longitudinal studies addressed these biases.
It is important to realize that there are several limitations to this review. First of all, due to the fact that this research is based on published material, publication bias is an important factor. Furthermore, studies showed substantial heterogeneity in different areas such as population (number, age, gender, race, duration of follow-up), exposure variables (physical activity measured by questionnaires, whether or not validated, or measured by motion sensors) and outcome variables (asthma diagnosis as self reported doctor's diagnosis, asthma symptoms or spirometry). Analysis showed borderline statistical heterogeneity. The small number of longitudinal studies prevented us from performing meta-regression or subgroup analysis. Confounding is an important issue, because other risk factors (such as smoking and obesity) could be associated with both low habitual physical activity as well as asthma development. First and second-hand cigarette smoke exposure is already established as an independent risk factor for developing asthma.  It is suggested that obesity is a risk factor for asthma development.  In our meta-analysis of longitudinal studies, pooling of results adjusted for confounders was not sensible because only three studies presented such results. However, adjusted odds ratios were never lower than unadjusted odds ratios (see table S3), so that a pooled effect for the adjusted results would be higher than the odds ratio of 0.88 (95% CI: 0.77–1.01) found for the unadjusted result.
Another limitation might be the fact that the validity of the NOS score recently has been questioned by Stang who believes that the NOS provides a quality score that has unknown validity at best.  We noted that some methodological pitfalls were not well represented in the NOS scale: reverse causation and protopathic bias or confounding by indication (e.g. advice to remain physically active for children with respiratory complaints).
In conclusion, the results of available published evidence indicate that high physical activity levels are a possible protective factor against asthma development. The heterogeneity suggests that possible relevant effects remain hidden in critical age periods, sex differences, or extremes of levels of physical activity (e.g. sedentary). Future longitudinal studies should address these issues.
NOS scale physical activity and asthma longitudinal studies. NOS: Newcastle-Ottawa Scale. Adjusted NOS scale for physical activity and asthma in longitudinal studies.
NOS scale physical activity and asthma cross-sectional studies. NOS: Newcastle-Ottawa Scale. Adjusted NOS scale for physical activity and asthma in cross-sectional studies.
PRISMA 2009 Checklist. PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) checklist adjusted for this study.
NOS scores of longitudinal studies. NOS: Newcastle-Ottawa Scale. Result of quality assessment of longitudinal studies on physical activity and asthma using NOS scores. We refer to figure S1 for the adjusted NOS for longitudinal studies, which was used as a scoring list.
NOS scores of cross-sectional studies. NOS: Newcastle-Ottawa Scale. Result of quality assessment of cross-sectional studies on physical activity and asthma using NOS scores. We refer to figure S2 for the adjusted NOS for cross-sectional studies, which was used as a scoring list.
Data extraction of longitudinal studies. CI; confidence interval, PA; physical activity, aHR; adjusted hazard ratio, OR; odds ratio; aOR; adjusted odds ratio, BMI; body mass index. Data extraction of longitudinal studies concerning baseline physical activity and asthma incidence. * p<0.05, #a used as reference category for pooling in this review, #1 adjusted for age, race, sex, center, and maximal education, #2 adjusted for BMI, smoking status, menopausal status, education level, working status, co-morbidities, #3 adjusted for age, atopy, and respiratory symptoms.
Analyzed the data: ME. Wrote the paper: ME MM CT JD MP. Quality assessment: ME MM CT JD MP. Literature search: ME MM. Inclusion: ME MM. Data-extraction of longitudinal studies: ME CT. Data-extraction of cross-sectional studies: ME. Analysis: ME.
- 1. Burr ML, Wat D, Evans C, Dunstan FD, Doull IJ (2006) Asthma prevalence in 1973, 1988 and 2003. Thorax 61: 296–299. doi: 10.1136/thx.2005.045682
- 2. Flegal KM, Carroll MD, Ogden CL, Curtin LR (2010) Prevalence and trends in obesity among US adults, 1999–2008. JAMA 303: 235–241. doi: 10.1001/jama.2009.2014
- 3. Livingstone MB, Robson PJ, Wallace JM, McKinley MC (2003) How active are we? Levels of routine physical activity in children and adults. Proc Nutr Soc 62: 681–701. doi: 10.1079/pns2003291
- 4. Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, et al. (2007) Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 39: 1423–1434. doi: 10.1249/mss.0b013e3180616b27
- 5. Ram FS, Robinson SM, Black PN, Picot J (2005) Physical training for asthma. Cochrane Database Syst Rev CD001116. doi: 10.1002/14651858.cd001116.pub2
- 6. Ford ES (2002) Does exercise reduce inflammation? Physical activity and C-reactive protein among U.S. adults. Epidemiology 13: 561–568. doi: 10.1097/00001648-200209000-00012
- 7. Lucas SR, Platts-Mills TA (2005) Physical activity and exercise in asthma: relevance to etiology and treatment. J Allergy Clin Immunol 115: 928–934. doi: 10.1016/j.jaci.2005.01.033
- 8. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, et al. (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283: 2008–2012. doi: 10.1001/jama.283.15.2008
- 9. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339: b2535. doi: 10.1136/bmj.b2535
- 10. Wells GA SB, O'Connell D, Peterson J, Welch V, Losos M, et al.. The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. Available: http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed 2 November 2012.
- 11. Higgins JPT GSe Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2 [updated September 2009]. The Cochrane Collaboration, 2009. Available: http://www.cochrane-handbook.org. Accessed 2 November 2012.
- 12. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327: 557–560. doi: 10.1136/bmj.327.7414.557
- 13. Firrincieli V, Keller A, Ehrensberger R, Platts-Mills J, Shufflebarger C, et al. (2005) Decreased physical activity among Head Start children with a history of wheezing: use of an accelerometer to measure activity. Pediatr Pulmonol 40: 57–63. doi: 10.1002/ppul.20214
- 14. Lucke J, Waters B, Hockey R, Spallek M, Gibson R, et al. (2007) Trends in women's risk factors and chronic conditions: findings from the Australian Longitudinal Study on Women's Health. Womens Health (Lond Engl) 3: 423–432. doi: 10.2217/17455057.3.4.423
- 15. Vogelberg C, Hirsch T, Radon K, Dressel H, Windstetter D, et al. (2007) Leisure time activity and new onset of wheezing during adolescence. Eur Respir J 30: 672–676. doi: 10.1183/09031936.00152906
- 16. Walders-Abramson N, Wamboldt FS, Curran-Everett D, Zhang L (2009) Encouraging physical activity in pediatric asthma: a case-control study of the wonders of walking (WOW) program. Pediatr Pulmonol 44: 909–916. doi: 10.1002/ppul.21077
- 17. Beckett WS, Jacobs DR Jr, Yu X, Iribarren C, Williams OD (2001) Asthma is associated with weight gain in females but not males, independent of physical activity. Am J Respir Crit Care Med 164: 2045–2050. doi: 10.1164/ajrccm.164.11.2004235
- 18. Benet M, Varraso R, Kauffmann F, Romieu I, Anto JM, et al. (2011) The effects of regular physical activity on adult-onset asthma incidence in women. Respir Med 105: 1104–1107. doi: 10.1016/j.rmed.2011.03.016
- 19. Huovinen E, Kaprio J, Koskenvuo M (2003) Factors associated to lifestyle and risk of adult onset asthma. Respir Med 97: 273–280. doi: 10.1053/rmed.2003.1419
- 20. Thomsen SF, Ulrik CS, Kyvik KO, Larsen K, Skadhauge LR, et al. (2006) Risk factors for asthma in young adults: a co-twin control study. Allergy 61: 229–233. doi: 10.1111/j.1398-9995.2006.01004.x
- 21. Bener A, Abdulrazzaq YM, Al-Mutawwa J, Debuse P (1996) Genetic and environmental factors associated with asthma. Hum Biol 68: 405–414.
- 22. Berntsen S, Carlsen KC, Anderssen SA, Mowinckel P, Hageberg R, et al. (2009) Norwegian adolescents with asthma are physical active and fit. Allergy 64: 421–426. doi: 10.1111/j.1398-9995.2008.01845.x
- 23. Chen Y, Dales R, Krewski D (2001) Leisure-time energy expenditure in asthmatics and non-asthmatics. Respir Med 95: 13–18. doi: 10.1053/rmed.2000.0961
- 24. Cheng BL, Huang Y, Shu C, Lou XL, Fu Z, et al. (2010) A cross-sectional survey of participation of asthmatic children in physical activity. World J Pediatr 6: 238–243. doi: 10.1007/s12519-010-0222-z
- 25. Chiang LC, Huang JL, Fu LS (2006) Physical activity and physical self-concept: comparison between children with and without asthma. J Adv Nurs 54: 653–662. doi: 10.1111/j.1365-2648.2006.03873.x
- 26. Corbo GM, Forastiere F, De Sario M, Brunetti L, Bonci E, et al. (2008) Wheeze and asthma in children: associations with body mass index, sports, television viewing, and diet. Epidemiology 19: 747–755. doi: 10.1097/ede.0b013e3181776213
- 27. Dogra S, Meisner BA, Baker J (2008) Psychosocial predictors of physical activity in older aged asthmatics. Age Ageing 37: 449–454. doi: 10.1093/ageing/afn114
- 28. Eijkemans M, Mommers M, de Vries SI, van Buuren S, Stafleu A, et al. (2008) Asthmatic symptoms, physical activity, and overweight in young children: a cohort study. Pediatrics 121: e666–672. doi: 10.1542/peds.2007-1236
- 29. Ford ES, Heath GW, Mannino DM, Redd SC (2003) Leisure-time physical activity patterns among US adults with asthma. Chest 124: 432–437. doi: 10.1378/chest.124.2.432
- 30. Gannotti M, Veneri D, Roberts D (2007) Weight status and physical activity in third graders with chronic health conditions. Pediatr Phys Ther 19: 301–308. doi: 10.1097/pep.0b013e318157da3d
- 31. Glazebrook C, McPherson AC, Macdonald IA, Swift JA, Ramsay C, et al. (2006) Asthma as a barrier to children's physical activity: implications for body mass index and mental health. Pediatrics 118: 2443–2449. doi: 10.1542/peds.2006-1846
- 32. Jones SE, Merkle SL, Fulton JE, Wheeler LS, Mannino DM (2006) Relationship between asthma, overweight, and physical activity among U.S. high school students. J Community Health 31: 469–478. doi: 10.1007/s10900-006-9026-4
- 33. Kilpelainen M, Terho EO, Helenius H, Koskenvuo M (2006) Body mass index and physical activity in relation to asthma and atopic diseases in young adults. Respir Med 100: 1518–1525. doi: 10.1016/j.rmed.2006.01.011
- 34. Kitsantas A, Zimmerman BJ (2000) Self-efficacy, activity participation, and physical fitness of asthmatic and nonasthmatic adolescent girls. J Asthma 37: 163–174. doi: 10.3109/02770900009055439
- 35. Lang DM, Butz AM, Duggan AK, Serwint JR (2004) Physical activity in urban school-aged children with asthma. Pediatrics 113: e341–346. doi: 10.1542/peds.113.4.e341
- 36. Malkia E, Impivaara O (1998) Intensity of physical activity and respiratory function in subjects with and without bronchial asthma. Scand J Med Sci Sports 8: 27–32. doi: 10.1111/j.1600-0838.1998.tb00225.x
- 37. Nystad W (1997) The physical activity level in children with asthma based on a survey among 7–16 year old school children. Scand J Med Sci Sports 7: 331–335. doi: 10.1111/j.1600-0838.1997.tb00162.x
- 38. Ownby DR, Peterson EL, Nelson D, Joseph CC, Williams LK, et al. (2007) The relationship of physical activity and percentage of body fat to the risk of asthma in 8- to 10-year-old children. J Asthma 44: 885–889. doi: 10.1080/02770900701752698
- 39. Priftis KN, Panagiotakos DB, Antonogeorgos G, Papadopoulos M, Charisi M, et al. (2007) Factors associated with asthma symptoms in schoolchildren from Greece: the Physical Activity, Nutrition and Allergies in Children Examined in Athens (PANACEA) study. J Asthma 44: 521–527. doi: 10.1080/02770900701496023
- 40. Ritz T, Rosenfield D, Steptoe A (2010) Physical activity, lung function, and shortness of breath in the daily life of individuals with asthma. Chest 138: 913–918. doi: 10.1378/chest.08-3073
- 41. Romieu I, Mannino DM, Redd SC, McGeehin MA (2004) Dietary intake, physical activity, body mass index, and childhood asthma in the Third National Health And Nutrition Survey (NHANES III). Pediatr Pulmonol 38: 31–42. doi: 10.1002/ppul.20042
- 42. Rundle A, Goldstein IF, Mellins RB, Ashby-Thompson M, Hoepner L, et al. (2009) Physical activity and asthma symptoms among New York City Head Start Children. J Asthma 46: 803–809. doi: 10.1080/02770900903114564
- 43. Strine TW, Balluz LS, Ford ES (2007) The associations between smoking, physical inactivity, obesity, and asthma severity in the general US population. J Asthma 44: 651–658. doi: 10.1080/02770900701554896
- 44. Teramoto M, Moonie S (2011) Physical Activity Participation among Adult Nevadans with Self-Reported Asthma. J Asthma 517–522. doi: 10.3109/02770903.2011.567426
- 45. Trzcieniecka-Green A, Bargiel-Matusiewicz K, Wilczynska-Kwiatek A (2009) Quality of life and activity of children suffering from bronchial asthma. Eur J Med Res 14 Suppl 4: 147–150.
- 46. Tsai HJ, Tsai AC, Nriagu J, Ghosh D, Gong M, et al. (2007) Associations of BMI, TV-watching time, and physical activity on respiratory symptoms and asthma in 5th grade schoolchildren in Taipei, Taiwan. J Asthma 44: 397–401. doi: 10.1080/02770900701364304
- 47. Tsai HJ, Tsai AC (2009) The association of BMI and sedentary time with respiratory symptoms and asthma in 5th grade schoolchildren in Kaohsiung, Taiwan. J Asthma 46: 9–15. doi: 10.1080/02770900802444229
- 48. Vahlkvist S, Pedersen S (2009) Fitness, daily activity and body composition in children with newly diagnosed, untreated asthma. Allergy 64: 1649–1655. doi: 10.1111/j.1398-9995.2009.02081.x
- 49. van Gent R, van der Ent CK, van Essen-Zandvliet LE, Rovers MM, Kimpen JL, et al. (2007) No differences in physical activity in (un)diagnosed asthma and healthy controls. Pediatr Pulmonol 42: 1018–1023. doi: 10.1002/ppul.20672
- 50. Vlaski E, Stavric K, Seckova L, Kimovska M, Isjanovska R (2008) Influence of physical activity and television-watching time on asthma and allergic rhinitis among young adolescents: preventive or aggravating? Allergol Immunopathol (Madr) 36: 247–253. doi: 10.1016/s0301-0546(08)75218-2
- 51. Vogt R, Bersamin A, Ellemberg C, Winkleby MA (2008) Evaluation of risk factors and a community intervention to increase control and treatment of asthma in a low-income semi-rural California community. J Asthma 45: 568–574. doi: 10.1080/02770900802005269
- 52. Weston AR, Macfarlane DJ, Hopkins WG (1989) Physical activity of asthmatic and nonasthmatic children. J Asthma 26: 279–286. doi: 10.3109/02770908909073264
- 53. DiFranza JR, Aligne CA, Weitzman M (2004) Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 113: 1007–1015.
- 54. Flaherman V, Rutherford GW (2006) A meta-analysis of the effect of high weight on asthma. Arch Dis Child 91: 334–339. doi: 10.1136/adc.2005.080390
- 55. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25: 603–605. doi: 10.1007/s10654-010-9491-z