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(Chest. 2005;128:3048-3054.)
© 2005 American College of Chest Physicians

Sex Specificity of Asthma Associated With Objectively Measured Body Mass Index and Waist Circumference*

The Humboldt Study

Yue Chen, PhD; Donna Rennie, PhD; Yvon Cormier, MD and James Dosman, MD

* From the Department of Epidemiology and Community Medicine (Dr. Chen), Faculty of Medicine, University of Ottawa, Ottawa, ON; Institute of Agricultural, Rural and Environmental Health (Drs. Rennie and Dosman), University of Saskatchewan, Saskatoon, SK; and Centre de Pneumologie (Dr. Cormier), Hôpital and Université Laval, Sainte-Foy, PQ, Canada.

Correspondence to: Yue Chen, PhD, Department of Epidemiology and Community Medicine, Faculty of Medicine, University of Ottawa, 451 Smyth Rd, Ottawa, ON, Canada K1H 8M5; e-mail: ychen{at}uottawa.ca


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To investigate the possibility of sex specificity for the association of obesity and asthma using objective measures of body mass index (BMI) and waist circumference (WC).

Design: Cross-sectional study of adults (n = 2,057) living in Humboldt, SK, Canada in 2003.

Setting: A rural community.

Measurements: Ever-asthma was defined as lifetime physician-diagnosed asthma, and recent asthma was defined as asthma diagnosed by a physician during the past 12 months. BMI and WC were objectively measured.

Results: Among the participants, 5.6% of men and 10.0% of women reported having ever-asthma, and 2.7% and 6.0% had recent asthma, respectively. Higher levels of both BMI and WC were significantly associated with asthma in women but not in men. The adjusted odds ratios for women with a BMI of at least 30.0 kg/m2 relative to women with a BMI of < 25.0 kg/m2 were 2.06 (95% confidence interval [CI], 1.42 to 4.05) for ever-asthma and 3.47 (95% CI, 1.64 to 7.32) for recent asthma.

Conclusions: Our study demonstrated that the increased risk of asthma associated with obesity was only significant in women but not in men even when BMI was objectively measured, and this association was robust to the anthropometric measures.

Key Words: asthma • body mass index • obesity • sex • waist girth


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The results from epidemiologic studies for asthma associated with obesity are relatively consistent in adults as compared with those in children; however, the role of sex needs to be further clarified. Studies of women from four different countries1234 and of men and women combined56 have indicated that obesity is significantly related to increased prevalence and incidence of asthma. Several other cross-sectional and longitudinal studies have further examined sex specificity and found that the obesity and asthma association is either only significant in women but not in men,78910 or is stronger in women than in men.11

Whether this sex specificity is real is still questionable. Santillan and Camargo12 found a similar result that only obese women but not men had an increased risk of asthma when self-reported body mass index (BMI) was used. However, when obesity was defined using objectively measured BMI, an elevated risk of asthma was observed in both obese women and men12; the authors suspected that obesity measurement bias is likely a reason for the observed sex-related difference in the association between obesity and asthma.

BMI is a better indicator of fat mass in adults than in children but may not be equally good for men and women, which can be another reason for the observed sex-related association between obesity and asthma. Other anthropometric measures such as waist circumference (WC) and waist-to-hip ratio (WHR) are frequently used as indicators of overweight or obesity in epidemiologic studies of cardiovascular disease and diabetes but have rarely been used in asthma studies. One study13 has demonstrated that asthma symptoms were significantly associated with higher levels of BMI and WC in women and not in men. In this same study,13 WHR was not a predictor for asthma in either men or women; this study provided new evidence for the obesity and asthma association in women using a different anthropometric measure. However, the sample size of the study was relatively small; therefore, the evidence for sex modification was not very strong. In the present study, we objectively measured weight, height, and WC in adults who were living in the town of Humboldt, Saskatchewan, and examined the sex differences in the association between obesity defined by BMI and WC and physician-diagnosed asthma.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
This cross-sectional study was conducted in the town of Humboldt, Saskatchewan, in 2003. The target population of the study was all the town residents ≥ 6 years old and was conducted among children (6 to 17 years old) and adults (18 to 79 years old), separately. This analysis was based on data from 2,057 adult residents 18 to 79 years old, who represented 71% of the target population. Almost all of the study population were white.

Humboldt is a service center, and agriculture is the main industry in the town. Canvassers contacted all households within the town and surrounding areas and asked all eligible adult subjects in each home to participate in the study and to complete a written consent of participation. A questionnaire left by the canvassers was completed in the home by each subject and returned during a prearranged clinic visit. The questionnaire requested information on sociodemographic factors, allergy, smoking, alcohol consumption, exercise, and the home environment.

An appointment was made for each adult participant to visit a clinic, where height, weight, and were measured. Weight was measured to the nearest 0.1 kg using a calibrated hospital spring scale with subjects dressed in normal indoor clothing without shoes. Height and WC were measured in centimeters. Height was measured against a wall using a fixed tape measure with participants standing shoeless on a hard surface. WC was measured between the lowest rib and the iliac crest, horizontally through the narrowest part of the torso.14 BMI was calculated as weight/height. Subjects were grouped into three categories based on BMI (< 25.0, 25.0 to 29.9, and ≥ 30 kg/m2) and two categories based on WC (< 100 cm and ≥ 100 cm).

Respondents who answered the following question affirmatively were considered as having recent asthma: "During the past 12 months, has a doctor ever said you had asthma?" Ever-asthma was defined as asthma that had ever been diagnosed by a physician during the patient’s lifetime.

Current smokers were participants who reported smoking every day or almost every day and had smoked at least 20 packs during their lifetime. Ex-smokers were those who were regular smokers but at the time of the survey had quit for at least 6 months. Participants in the low-education category did not proceed beyond secondary school; the high-education category included subjects admitted to college or university, as well as those with a postsecondary school certificate or diploma. Subjects were classified into low-income (< $50,000/yr) and high-income (≥ $50,000/yr) groups based on total household income. A positive history of respiratory allergy was defined by an affirmative response to the question: "Have you ever had an allergic reaction to things that are inhaled (eg, pollen, dust, animal fur or smoke)?" Other variables included in the analysis were age (years), household size (fewer than three people or three or more people), number of bedrooms (fewer than four, and four or more), pets at home (yes, no), regular drinking (yes, no), and household dampness (yes, no). The presence of home dampness was assessed by a positive response to the question: "Does your house have any damage caused by dampness (wet spots on walls, floors)?" A regular drinker was defined as a person who drank alcoholic beverages at least once per week on average.

The relationships between BMI, WC, and asthma were examined for men and women separately. We calculated the prevalence of asthma and corresponding 95% confidence intervals (CIs) according to various risk factors. Logistic regression models were used to evaluate associations between obesity variables and the prevalence of asthma, taking other important variables into consideration. Model parameters were estimated by the method of maximum likelihood and were tested for significance using the Wald statistic.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The prevalences of both ever-asthma and recent asthma were higher in women (10.0% and 6.0%) than in men (5.7% and 2.7%, respectively). Obesity was prevalent in this rural town, with 38.2% of men and 33.7% of women having a BMI ≥ 30 kg/m2. The mean of BMI was 29.2 kg/m2 for men and 28.4 kg/m2 for women. Seventy-four men (8.3%) and 120 women (10.3%) refused to have their WC measured, and their average BMIs were similar when compared to the overall averages (Table 1 ), suggesting that overweight or obesity is not likely an important reason for the missing data.


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  		Table 1.. Comparison of BMI by WC in Men and Women, the Humboldt Study, 2003

 
Table 2 shows that the prevalence of asthma was increased with increasing BMI and WC in women but not in men. For both ever-asthma and recent asthma, the prevalence was approximately twofold higher in women with a BMI of 30 kg/m2 compared with those with a BMI < 25 kg/m2, or in women with a WC of 100 cm vs those with a WC of < 100 cm.


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  		Table 2.. Prevalence of Asthma Associated With BMI and WC, the Humboldt Study, 2003

 
Table 3 shows the prevalence of ever-asthma stratified by other potential risk factors including age, home environment variables, allergy history, education, income, smoking, and alcohol use. Respiratory allergy was strongly associated with asthma in both men and women. Home dampness was a determinant for asthma only in women. In women more so than men, the prevalence of asthma tended to be lower for regular alcohol drinkers than nondrinkers.


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  		Table 3.. Prevalence of Ever-Asthma According to Various Risk Factors, the Humboldt Study, 2003

 
A multiple logistic regression model was used to assess the independent effect of BMI and WC on the prevalence of asthma after controlling for potential confounders in women and men. For ever asthma, the adjusted odds ratios (ORs) for women with a BMI of at least 30 kg/m2 and a BMI of 25.0 to 29.9 kg/m2 compared with a BMI of < 25 kg/m2 were 2.06 (95% CI, 1.42 to 4.05) and 1.62 (95% CI, 0.93 to 2.83), respectively (Table 4 ). The corresponding ORs for recent asthma tended to be higher. The risk of asthma in women with a WC ≥ 100 cm was approximately twofold higher than those with a WC < 100 cm (Table 4). Higher levels of BMI and WC were not associated with increased risks of ever-asthma and recent asthma in men (Table 5 ).


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  		Table 4.. Unadjusted and Adjusted ORs and 95% CIs for Asthma in Relation to BMI and WC in Women, the Humboldt Study, 2003*

 

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  		Table 5.. Unadjusted and Adjusted ORs and 95% CIs for Asthma in Relation to Body Mass Index and Waist Circumference in Men, the Humboldt Study, 2003*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In this study, we used objectively measured BMI to define overweight (BMI 25.0 to 29.9 kg/m2) and obesity (BMI ≥ 30.0 kg/m2) and found that both overweight and obesity were associated with an increased risk of recent asthma and that obesity was significantly associated with an increased risk of ever-asthma in women. These results are consistent with two previous Canadian studies.78 Based on data from a representative Canadian population, Chen et al78 found that obesity defined by self-reported BMI was positively related to both prevalence and incidence of asthma in women but not in men. Although race may play a role in sex modification of the obesity and asthma association,15 the present study is not the case because almost all participants are white.

Reporting biases of body weight and height have been well documented. Women tend to underreport their body weight, and men tend to overreport their height, with an ultimate result of underreporting in BMI. However, it is not known if these reporting biases are differential in terms of self-reported asthma and sex and if the reporting biases cause a biased estimate of obesity and asthma association. So far, most studies of the obesity and asthma association in adults are based on data of self-reported BMI. An important question is whether or not a systematic bias exists that would result in a false sex specificity in the obesity and asthma association. In a recent study of 961 Mexican adults, Santillan and Camargo12 found that obesity defined by objectively measured BMI was a risk factor for asthma diagnosis in both men (OR, 2.5; 95% CI, 1.1 to 5.9) and women (OR, 2.3; 95% CI, 1.5 to 3.8). However, when self-reported BMI was used, the ORs declined to 1.3 (95% CI, 0.6 to 2.9) in men and 1.7 (95% CI, 1.1 to 2.7) in women,12 suggesting that self-reported BMI underestimates the obesity and asthma association particularly in men and causes a false sex difference. Contrary to these results, our study did not observe any positive association between objectively measured BMI and the prevalence of asthma (either recent asthma or ever-asthma) in men, and the OR estimates for asthma associated with obesity in women were significant and were comparable to previous estimates among the general Canadian population.78 Reasons for the discrepancy in sex specificity between our study and the study by Santillan and Camargo12 are not known. The sample size of our study is larger, resulting in more precise estimates. Overweight and obesity are more common in our study population as compared with the general Canadian population, and the prevalence of asthma is much higher in women than in men. Different populations may also have different self-reporting biases associated with both the exposure (obesity) and outcome (asthma).

Obesity is defined as an increase in body weight resulting from excessive body fat. BMI is an indirect measurement of body fat and is frequently used in large-scale epidemiologic studies. BMI is sex and age dependent, with females subjects having higher fat mass values than male subjects.16 Equivalent BMI values may represent different levels of adiposity in different sex and age groups. BMI is a less ideal measure of overweight and obesity in children, which may partly explain the contradictory results for studies from children populations.17 However, we do not know if it is related to the observed sex specificity in adults; therefore, other measures of obesity will provide important information. In a study of 135 Hispanic men and 398 women, Del-Rio-Navarro et al13 measured WC and WHR and found that asthma symptoms were associated with higher levels of both WC and BMI but not with WHR in women. In men, none of these anthropometric measures were related to asthma symptoms. In our study, we found that women with a WC > 100 cm had a significantly increased risk of self-reported physician-diagnosed asthma, which was independent of covariates measured in the study. Consistently, WC was not associated with asthma in men. Compared with WHR, WC is a more convenient measure and a better indicator of visceral adipose tissue because it is less likely to be influenced by sex or degree of obesity18 and is a better correlate of the visceral adipose tissue.19 It has been suggested that WC instead of WHR should be used as an index of abdominal visceral adipose tissue deposition, and WC values above approximately 100 cm are most likely to be associated with potentially "atherogenic" metabolic disturbances.20

Our study has further demonstrated that the impact of overweight and obesity on asthma is sex related in adults. Longitudinal studies have indicated that obesity is likely a cause of asthma in women. The reasons for this are not known although various possibilities have been discussed.782122 Asthma is more common in women than in men, which is reflected in various frequency measures including prevalence,23 incidence,24 and hospitalization.2526 Based on a total of 9,486,173 hospital records in Canada for a 3-year period, Chen et al25 found that the cumulative incidence of asthma hospitalization was substantially higher for young boys than girls, and it was reversed for adults.25 A recent study27 also found that exogenous hormone replacement therapy in postmenopausal women was associated with an increased risk of asthma. The sex hormone theory is worth further investigation.

Airways hyperresponsiveness is an important feature of asthma. If obesity causes asthma, we expect a similar association between obesity and airway hyperresponsiveness in women. However, studies282930313233 have so far provided only conflicting results and have shown no clear sex-related pattern of such an association. Obesity was found to be associated with asthma-like symptoms but not with atopy.34

The mechanical theory suggests a possibility that fat mass-loading the chest causes dyspnea and asthma-like symptoms such as wheeze and shortness of breath, which may result in overdiagnosis and therefore overreporting of asthma. An analysis35 of 16,171 American men and women combined found that the highest BMI quintile had the greatest risk of self-reported asthma, bronchodilator use, and dyspnea with exertion but had the lowest risk for significant airflow obstruction, suggesting an overreporting of asthma in obese subjects. A study36 of 16,191 adult Europeans, however, demonstrated that after adjusting for nocturnal gastroesophageal reflux, habitual snoring, and other confounders, obesity remained significantly related to the onset of asthma, wheeze, and nighttime symptoms. Although there are a number of other speculations of mechanisms for the linkage between obesity and asthma,7821223738394041 we believe that more attention should be paid to the sex specificity in future studies.

Compared with men, women are also more susceptible to asthma and other obstructive airway diseases in response to other risk factors such as smoking.74243 A smaller airway size relative to lung size in women44 may increase the susceptibility to obstructive airway diseases in response to environmental exposure. It needs to be further explored if individuals with small relative airway calibers have increased susceptibility to the obesity effect.

Reporting bias of asthma is always a concern in large-scale epidemiologic studies,3941 and is likely to be different between men and women. In a nested case-control study of airway obstructive diseases, Guerra et al9 studied physician-confirmed incident cases of asthma in persons at least 20 years of age and found that a measured BMI of ≥ 28 kg/m2 was significantly associated with a increased risk of receiving a diagnosis of asthma (OR, 2.10; 95% CI, 1.31 to 3.36). Compared to 16% of control subjects, 30% of the patients with asthma were overweight or obese regardless of whether BMI was assessed before the diagnosis or the onset of asthma.9 The association between elevated BMI and asthma was only significant among women.9 In our study, the prevalence of asthma is comparable to the estimates from the Canadian Community Health Survey45 at a national level. It would be ideal to use a more comprehensive definition of asthma, which includes important characteristics such as wheeze, reversible airflow obstruction, physician diagnosis, measured reactivity, and eosinophilic airway inflammation; however, such a definition is not practical in large-scale epidemiologic study.46 For a practical approach, it is important to ensure that the operational definition used is stated clearly and does not introduce a systematic bias when asthmatic status among groups is compared.46 There is evidence that using less strict definition of asthma, such as ours, is likely to provided a less strong association between obesity and asthma.1 It suggests that reporting bias is likely to be nondifferential even if there is one.

In this study, approximately 8% of male participants refused to have their WC measured, and these men had an increased risk of asthma compared with those having their WC measured. There are no clear explanations for such an increase since we do not know why people refused to have their WC measured. The mean BMI value for these individuals with missing WC data was similar to the average for all participants; therefore, there should be some reasons other than being overweight or obese.

In summary, our study demonstrated that obesity defined by objectively measured BMI was associated with an increased risk of asthma only in women but not in men, suggesting that self-reporting bias does not explain the sex specificity of the obesity effect. The WC measure provided further evidence for the obesity and asthma relationship in women. The mechanisms for this relationship need to be further explored.


   Footnotes
 
Abbreviations: BMI = body mass index; CI = confidence interval; OR = odds ratio; WC = waist circumference; WHR = waist-to-hip ratio

This study was supported be a grant from the Canadian Institutes of Health Research, 200203MOP-100752-POP-CCAA-11829.

Dr. Chen currently holds a Canadian Institutes of Health Research Investigator Award.

Received for publication March 18, 2005. Accepted for publication April 29, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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