Boys with high body masses have an increased risk of developing asthma: findings from the National Longitudinal Survey of Youth (NLSY)

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Abstract

Objective:

To determine the relation between body mass index and the development of asthma in children.

Design:

Prospective study of 4393 asthma-free children followed for up to 14 years.

Setting:

Children of participants in the National Longitudinal Survey of Youth.

Methods:

Analysis was limited to children who were followed from birth and were asthma-free during the first 24 months of life. The outcome was the development of asthma during follow-up (incident asthma). Body mass index (BMI) was our main predictor of interest. Survival analyses, using time to development of asthma as the main endpoint, were stratified by sex and controlled for race/ethnicity, poverty status, and prenatal maternal smoking.

Results:

Asthma developed in 218 (5.0 %) children during the follow-up period. The relation between BMI and incident asthma varied by sex. A BMI 85th percentile at age 2–3 years was a risk factor for subsequent asthma development in boys (hazard ratio (HR) 1.6 95% confidence interval (CI) 1.1, 2.4) but not girls (HR 0.8, 95% CI 0.5, 1.4). Similarly, boys with BMIs always 85th percentile were at increased risk for subsequent asthma development (HR 2.4, 95% CI 1.4, 4.4) but not girls (HR 1.5, 95% CI 0.7, 2.9).

Conclusion:

Boys with high body masses may be at an increased risk for developing asthma.

Introduction

Asthma is an important cause of morbidity and mortality in the United States and asthma prevalence has increased since the 1980s.1, 2 A combination of environmental and lifestyle factors may be related to the rise in asthma cases.3

The incidence of obesity in children and adults has risen concurrently with asthma in the last 20 years.4, 5 Obese patients are observed to have changes in lung function.6, 7, 8, 9 In addition, adipose tissue is biologically active, associated with elevated markers of systemic inflammation that might contribute to asthma.10 Cross-sectional studies in children and adults have confirmed a strong association between obesity and asthma in both males and females.11, 12, 13, 14, 15, 16 However, most longitudinal studies linking obesity and the development of asthma or asthma-like symptoms have been in adults.17, 18, 19, 20 One longitudinal study in children, by Castro-Rodriguez et al., analyzing results of the Tucson Children's Respiratory Study, is limited by smaller numbers and the non-national data sample.18 Another study found an effect in boys, but not in girls.21

This study examines the relationship between obesity and asthma in children using prospective, nationally representative data from the National Longitudinal Survey of Youth (NLSY).

Materials and methods

Study population

The study population consists of children born to women enrolled in the NLSY. The NLSY is a national sample of young adults who were interviewed yearly or biyearly from 1979 to 2000, as well as a supplemental sample of Hispanics, African Americans, and whites of lower socioeconomic status. Children of these participants were included in the survey starting in 1986, with data collected prospectively in ‘rounds’ every 2 years. Details of NLSY assessment methodology, attrition, and other matters are described in detail elsewhere.4, 22, 23 Informed consent was obtained from all adult participants.

In order to examine risk factors for the development of asthma, the analysis was restricted to children who first entered the cohort prior to age 2 years and were asthma-free prior to age 2 years and at the time of their first body mass index (BMI) measurement (measured at age 2 or 3 years). In addition, the analysis was limited to subjects who participated in at least two rounds of the survey.

Participants

Of the 11 300 children who were surveyed at some point in NLSY the following were excluded: 5574 whose initial participation occurred after age 24 months, 586 who only participated in one survey, 58 who had asthma prior to age 24 months, 94 who had asthma at their first survey with a classifiable BMI, and 595 who did not have a classifiable BMI at the baseline evaluation. The final analytic cohort contained 4393 subjects.

Demographics, and variable definitions

The following variables were included in the analysis: sex, race/ethnicity (black, Hispanic, or white), poverty status, prenatal maternal smoking history, birth weight, and BMI. Children were classified as having a mention of poverty if this was noted in any survey they participated in. Weights and heights were measured either by an in-home interviewer using a portable scale and tape measure or reported by the parent.4 In this analysis, 69% of the height and 61% of the weights were measured. The BMI was calculated by dividing the weight in kilograms by the height in m2. Observations from subjects in whom the BMI was 10 or 70 kg/m2 were excluded as likely measurement errors, reporting errors, or signs of extreme medical condition.4 The most recent Centers for Disease Control and Prevention (CDC) National Center for Health Statistics (NCHS) growth curves were used to determine the BMI percentile.24 Children were classified based on their BMI percentile at the baseline evaluation into three mutually exclusive categories (<25th, 25th–84th, and 85th percentile).25 Children were also classified using the same three categories at the subsequent evaluations they participated in. Asthma-free children were categorized based on their BMI classifications over multiple visits into four categories: always <25th percentile, always 85th percentile, at least one time 85th percentile, and others (consisting of children not in one of the other three categories).

Children who were previously ‘asthma-free’ were classified as developing asthma (incident asthma) if their parent reported they either had asthma that limited their activity or required the use of medication or frequent attention from a doctor.

Statistical analysis

For analyses, both SAS and SUDAAN26, 27 were used. Person-years at risk were determined by using the time from the baseline evaluation to either the final evaluation or the evaluation during which asthma was reported. Cox proportional hazard regression models were developed using the SAS procedure PHREG to account for differential follow-up in study participants. The time of follow-up was the underlying time metric. Plots of the log–log survival curves for each covariate were used to demonstrate that the proportional hazards assumptions were met. The effect of BMI was analyzed in two different ways: as a time varying covariate and as an independent variable at each of the first four evaluations. Models were developed to determine whether the BMI predicted the development of asthma, after adjusting for race, sex, prenatal maternal smoking history, birth weight, and poverty status. HR and 95% CI are reported. In addition, we repeated the analyses in subgroups stratified by sex, due the previous reported evidence of different effects of BMI on asthma incidence in males compared to females.18, 19, 21

Results

Of the 4393 children in our analytic cohort, all of whom were initially surveyed prior to age 24 months and asthma free at that time, 218 (5.0 %) developed asthma during the follow-up period of 26 657 person-years1. In the 5574 children excluded because they were not followed since birth, 364 (6.5 %) had asthma noted at least once (either at baseline or follow-up). Other demographic characteristics of the population are shown in Table 1.

Table 1 Demographic characteristics of subjects, number developing asthma, person-years of follow-up, and incidence rate of asthma

The demographic characteristics of our analytic cohort for each round of the survey are shown in Table 2. From 1986 through 2000, the proportion of subjects with at least one mention of poverty decreased from 46.2 to 37.0%, the proportion of children with prenatal maternal smoking reported decreased from 36.3 to 24.9%, and the mean BMI percentile increased from 51 in 1988 to 65 in 2000 (P<0.05 for test of trend for each comparison).

Table 2 Demographic characteristics of subjects included in study by study year

The overall incidence of asthma in our cohort was 8.2 cases per 1000 person-years at risk (Table 1). The median age for new cases of asthma was 7.6 years (25th percentile 4.3 years, 75th percentile 9.8 years). These data also suggested a higher rate of incident asthma among children whose BMI was 85th percentile compared to those <25th percentile (10.4 vs 6.4 cases per 1000 person-years) and among boys compared to girls (9.5 vs 6.8 cases per 1000 person-years, Table 1).

The overall incidence of asthma among boys decreased from 9.5 cases per 1000 person-years at age 2–3 years to 7.5 cases per 1000 person years at age 8–9 years, while this rate increased among girls, from 6.8 to 7.5 cases per 1000 person-years (Tables 3 and 4). The overall survival curves depicting the development of asthma by baseline BMI category showed that a higher proportion of children 85th percentile developed asthma, compared to children in the other groups (Figure 1). The relation between BMI and incident asthma varied by sex. For example, a higher proportion of boys than girls whose BMI was 85th percentile at baseline developed asthma (13.7 vs 6.7 cases per 1000 person years, Tables 3 and 4).

Table 3 Number of boys developing asthma, person-years of follow-up, and incidence rate of asthma, stratified by baseline body mass index (BMI) categories and aggregated BMI categories over the first two, first three and first four surveys
Table 4 Number of girls developing asthma, person-years of follow-up, and incidence rate of asthma, stratified by baseline body mass index (BMI) categories and aggregated BMI categories over the first two, first three and first four surveys From the National Longitudinal Survey of Youth, 1986–2000.
Figure 1
figure1

Incident cases of asthma among children asthma-free at the baseline evaluation (age 2–3 years), stratified by the baseline body mass index (BMI) category. From the National Longitudinal Survey of Youth, 1986–2000.

Variables in the multivariate proportional hazard models that predicted incident asthma included male sex (HR 1.4, 95% CI 1.04, 1.8), prenatal maternal smoking (HR 1.5, 95% CI 1.1, 2.1), a BMI 85th percentile at age 4–5 years (HR 1.8, 95% CI 1.2, 2.6) or BMI as a time varying covariate always 85th percentile (HR 2.0, 95% CI 1.3, 3.1, Table 5). In the stratified analyses, there was evidence that the relation between BMI and asthma development varied by sex. A BMI 85th percentile at age 2–3 was a risk factor for asthma development in boys (HR 1.6, 95% CI 1.1, 2.4) but not girls (HR 0.8, 95% CI 0.5, 1.4). Similarly, when looking at BMI as a time varying covariate, boys with BMIs always 85th percentile were at increased risk for subsequent asthma development (HR 2.4, 95% CI 1.4, 4.4) but not girls (HR 1.5, 95% CI 0.7, 2.9) (Table 5). In a similar analysis restricted to children with only measured heights and weights at each visit (2036 of 4393), results were similar (data not shown).

Table 5 Results of multivariate proportional hazards models predicting the development of asthma in the overall group and stratified by sex

Discussion

In this longitudinal study of 4393 children followed for up to 14 years, the overall incidence of asthma was 8.2 cases per 1000 person-years at risk. The relationship between BMI and asthma development varied by sex: boys, but not girls, whose BMI was 85th percentile at age 2–3 years were more likely to develop asthma and this increased risk (when looking at BMI as a time varying covariate) persisted for boys, but not girls (Table 5).

The primary finding was that some children with high BMIs were more likely to develop asthma during follow-up. Previous studies of the relation between incident asthma and body mass in children have been limited in sample size,18 duration of follow-up,21 and age at which the cohort started follow-up.18, 21 In one study of school-age children, 6-year-old girls who became obese by age 11 or 13 were more likely to report asthma like symptoms,18 whereas in another study, 7-year-old boys who were overweight or obese were more likely to report asthma over the next 4 years.21 The present study differs from these previous ones in that all participants were studied from birth and were followed for up to 14 years. Thus, the different outcomes observed in prior studies may be a function of the age at which the children were studied and duration of follow-up.

The relation between obesity and asthma has been the subject of multiple studies in recent years. Proposed mechanisms for this observation include genetic factors,13, 17, 28 obesity-related inflammation,10, 29 pulmonary dysfunction,7, 17, 30, 31, 32 sedentary lifestyle,13, 17, 33, 34 dietary differences,17, 33, 35, 36 sex hormone levels,13, 18 increased respiratory symptoms and medication use,37 and gastric reflux.13, 31 The present findings neither support nor refute any of these proposed mechanisms.

This analysis attempted to determine whether a BMI <25th percentile was a risk factor for asthma development during follow-up. The data suggested this might be a risk factor in 4–7 year old children,5 but was not statistically significant. Some studies have suggested a curvilinear relation between bronchial responsiveness or asthma incidence and BMI.9, 19 Asthma is a chronic illness and some chronic illnesses are associated with lower BMIs.38, 39 In addition, asthma has several different phenotypic presentations, so it is possible that different phenotypes of asthma may be affected by BMI in different ways.40

In this study, the overall incidence of asthma among included children was 8.2 per 1000 person-years at risk. This rate is comparable to that seen in several studies of children,41, 42, 43 but less than the rate of 22.6 per 1000 person-years at risk reported by Gilliland et al.21 This study was designed to look at the effect of BMI on incident asthma, and standards for classifying BMI in children do not exist prior to age 24 months. Thus, the study had to exclude children who had asthma prior to age 24 months and those whose first BMI was obtained at the same time they were reported to have asthma. A result of this is that the overall incidence of asthma in all of the children followed from birth in this cohort would have been higher than 8.2 per 1000.

This study is subject to several limitations. Asthma was proxy-reported and not verified by either the use of medical records, physician contact, or other means. The definition of asthma used in this study was not the traditional one (has your child ever been diagnosed by a physician with asthma?)2 but limited to those children whose parents reported that they had a condition that limited their ability to attend school, play, work, or participate in games or sports OR required frequent attention from a doctor or regular use of medicine. Thus, this analysis may not have included children with very mild asthma who did not meet those criteria. Also, there is no way to separate out true asthma from obesity-related dyspnea. Another possibility is that children with high BMIs may be more likely to have activity limitations or require more frequent use of medication, thus resulting in their being counted as asthma cases more than similar children with normal BMIs. Finally, we only saw a significant effect of elevated BMI on asthma among boys, who had a higher incidence of asthma than girls in this study. If, however, this study could be extended into young adulthood, when the incidence of asthma among women increases above that seen in men, the relation between elevated BMI and asthma could also be seen among women.

In conclusion, this analysis suggests a complex relation between BMI and incident asthma among children that may vary by sex. This finding needs further study with more traditional assessments of asthma outcomes. Overall, this study found that boys with high BMIs were at increased risk for developing asthma, although there appear to be vulnerable ages for both boys and girls during which being overweight increases the risk for the development of asthma.

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Correspondence to D M Mannino.

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Mannino, D., Mott, J., Ferdinands, J. et al. Boys with high body masses have an increased risk of developing asthma: findings from the National Longitudinal Survey of Youth (NLSY). Int J Obes 30, 6–13 (2006) doi:10.1038/sj.ijo.0803145

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Keywords

  • asthma
  • body mass index
  • children

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