Obesity and the Occurrence of Bronchitis in Adolescents

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1 and the Occurrence of Bronchitis in Adolescents Yungling L. Lee 1,2, Yang-Ching Chen 1,3 and Yu-An Chen 1 Objective: Previous studies have shown that an elevated BMI was associated with higher risks of bronchitis among children. The magnitude of how increase in BMI influencing the risk of incident bronchitis remained unexplored. The objective of this study is to assess the association between BMI and the incidence of bronchitis in the Taiwan Children Health Study. Design: A school-based prospective cohort study. Methods: We conducted a population-based prospective cohort study among seventh-grade school children in 14 Taiwanese communities. A total of 3,634 adolescents completed follow-up questionnaire in Associations between BMI and incident bronchitis were analyzed by multiple Poisson regression models, taking overdispersion into account. Results: Among eligible cohort participants without bronchitis at study entry, the proportion of overweight and obesity were 32.1% and 17.9%. Overweight was 40.7% and obesity was 27.7% among those with incident bronchitis. The BMI percentile categories showed significant increasing trends for bronchitis in total eligible children and in girls (P for trend <0.001). Overweight and obesity were both associated with increased risks of incident bronchitis. This association was significant in girls only while stratified by gender. Conclusions: Our data showed that the BMI percentile and weight status were associated with higher risks of incident bronchitis in adolescents, especially in girls. (2013) 21, E149-E153. doi: /oby Introduction Respiratory diseases such as bronchitis, wheeze, or asthma-like symptoms in childhood are growing health problems (1). has also become a global health issue in the past two decades. can lead to several respiratory diseases, such as sleep disordered breathing, impaired pulmonary functions, wheezing, and bronchial hyper-responsiveness (2). Bronchial hyper-reactivity is an obvious characteristic of asthma and can lead to bronchitis in both children and adults (3,4). Although close links between obesity and asthma were discovered in plenty of studies, only few studies showed that an elevated BMI was associated with bronchitis or asthma-like symptoms in children (5,6). Furthermore, in adolescents, links between an increased BMI and development of respiratory symptoms are worth noting (7). Whether or not an increased BMI in adolescence may trigger bronchitis still needs investigation. has been emerging as an important risk factor for respiratory morbidities (8). Though some studies have shown the links between childhood obesity and respiratory symptoms, there is heterogeneity in the published literature regarding gender differences on this relationship. While some studies concluded that BMI was associated with asthma-like symptoms in girls but not in boys (9), another study showed that boys with high BMI had an increased risk of developing asthma (10). Chang et al. even reported no gender difference on the association of obesity with bronchitis in childhood (11). Some studies in adulthood also showed a similar increase on the effect of incident bronchitis due to overweight and obesity in both men and women (12,13). Therefore, we also would like to explore the gender difference in the relationships between BMI and incident bronchitis. In the present study, we examined the relationship between BMI and the occurrence of bronchitis and asthma for adolescents in Taiwan. The aim of our study is to investigate obesity predictors of bronchitis and the magnitude of influence of these predictors. We performed a longitudinal analysis based on our previous Taiwan Children Health Study (TCHS) cohort. 1 Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan 2 Department of Public Health, College of Public Health, National Taiwan University, Taipei, Taiwan 3 Department of Family Medicine, Taipei City Hospital, ZhongXing Branch, Taipei, Taiwan. Correspondence: Yungling L. Lee (leolee@ntu.edu.tw) Disclosure: The authors declared no conflict of interest. See the online ICMJE Conflict of Interest Forms for this article. Additional Supporting Information may be found in the online version of this article. Received: 14 April 2011 Accepted: 29 May 2012 First published online by Nature Publishing Group on behalf of The Society 26 July doi: /oby VOLUME 21 NUMBER 1 JANUARY 2013 E149

2 and the Occurrence of Bronchitis Lee et al. Methods and Procedures Study design The TCHS is a prospective cohort study examining the determinants of adolescents respiratory health (14). A total of 4,134 seventhgrade school children were recruited from public schools from 14 communities in At study entry, the parents or guardians of each participating student provided written informed consent and completed questionnaires that provided information on sociodemographic factors, history of respiratory diseases/symptoms, allergic diseases, family history of allergic diseases, and environmental exposures, including in-utero exposures to maternal smoking and second hand smoke at home. Between October and November 2009, cohort subjects were assessed during school visits by an update questionnaire, which included identical items concerning respiratory outcomes and recent exposure history. The study protocol was approved by the institutional review board of our university hospital and complied with the principles outlined in the Helsinki Declaration (15). Respiratory health outcomes The major outcome of interest in this study was bronchitis. Children without any history of bronchitis at study entry were defined as eligible subjects and were left for further analyses. Participants who were disease-free at baseline and reported a yes answer to the question Has a physician ever diagnosed your child as having bronchitis? on follow-up questionnaire were classified as having incident bronchitis. The incident asthma was defined by the question Has a physician ever diagnosed your child as having asthma? on baseline and follow-up questionnaire. Those with asthma history were considered to be at risk for a new diagnosis of bronchitis and were included in current study. Assessment of childhood obesity Height, weight and lung function were measured during school visits, using standard protocols with shoes and coats removed. BMI was calculated as weight/(height) 2. Children were grouped according to the following sex and age-normalized BMI percentile: (i) BMI percentile <15th, (ii) BMI percentile 15-85th, (iii) BMI percentile th, and (iv) BMI percentile 95th. We defined overweight subjects as having sex and age-normalized BMI 85th percentile and obese ones as having sex and age-normalized BMI 95th percentile. Cut-off points for childhood obesity were established according to new growth charts for Taiwanese children and adolescents, in turn based on World Health Organization standards and health-related physical fitness records in Taiwan (16). Statistical analysis Incidence rates for bronchitis were calculated using the number of new cases divided by the person-years at risk over the 2-year period of follow-up. The association between BMI and disease incidence was examined by fitting Poisson regression models. To account for overdispersion of incidence rates in Poisson models, we performed all analyses by using deviance adjusted variance estimates (17). On the basis of study design and an a priori consideration of potential confounders, we included gender, age, community, and in-utero exposure to maternal smoking in all models. If estimates of BMI changed by >10% when a covariate was added in base models, the covariate would be included in final models (18). Subjects with missing covariate information were included in the model using missing indicators (19). Baseline risks in the analysis of the entire cohort were estimated, and we also calculated risks stratified by different gender. In the final regression models, the association between obesity predictors and bronchitis was adjusted for gender, age, community, in-utero exposure to maternal smoking, current second hand smoke, allergic rhinitis and atopic eczema. We also conducted sensitivity analyses by restricting the cohort to subjects without a history of asthma at study entry. SAS software version 9.1 (SAS Institute, Gary, NC) was used to conduct all analyses. All hypothesis testing was conducted assuming a 0.05 significant level based on a two-sided estimate. Results In 2007, there were 3,870 participants without history of bronchitis at cohort entry. A total of 3,634 adolescents completed the followup questionnaire and lung function tests, with a follow-up rate of 93.9%. The proportion of gender was almost equal and most of the adolescents were 12 to 13 years old at study entry. Approximately 5.5% and 44.9% of the subjects had active smoking and current second hand smoke, respectively. In-utero exposure to maternal smoking was reported for around 3.8% of the participants. In 2009, there were 59 children having bronchitis and 3,575 children without bronchitis. Table 1 presents the distributions of demographic characteristics for the study cohort with and without incident bronchitis. The incidence rate of bronchitis was 8.1/1,000 person-years (girls, 9.8/ 1,000 person-years; boys, 6.3/1,000 person-years). Distribution of BMI percentile for study participants are shown in Table 2. Among eligible cohort participants, the proportion of overweight and obesity were 32.1% and 17.9%. Overweight was 40.7% and obesity was 27.7% among those with incident bronchitis. The proportion of overweight and obesity was 40.5% and 32.4% in girls and 40.9% and 9.1% in boys, respectively. The association between BMI percentile, weight status and incident bronchitis are presented in Table 3. In total eligible children, the BMI percentile categories showed significant increasing trends for bronchitis (P for trend <0.001). Overweight and obesity were both significantly associated with increased risks of bronchitis. In the analysis stratified by gender, a significant increasing trend on the relationship between BMI percentile and bronchitis was also present in girls. Overweight and obesity were also related to bronchitis (relative risk ¼ 1.75, 95% confidence interval and relative risk ¼ 2.90, 95% confidence interval , respectively) in girls, but there was no significant association between obesity and bronchitis in boys. Restricting the analyses to subject without a history of asthma did not substantially alter the above findings (see Supplementary Table S1 online). We also analyzed our data for incident asthma in the TCHS cohort. Similar trends were found between obesity predictors and asthma, but it is difficult to make the conclusion due to small case numbers over the short follow-up period (see Supplementary Table S2 online). Discussion Through our prospective cohort study, we found that overweight or obese adolescents consistently face increased risks of incident E150 VOLUME 21 NUMBER 1 JANUARY

3 TABLE 1 Demographic characteristics of participants with and without incident bronchitis bronchitis. predictors, such as BMI percentile 85-95, BMI percentile 95, overweight and obesity, would significantly increase the risk of incident bronchitis among adolescents between 12 and 15 years of age. We also found female dominant relationships between obesity and incident bronchitis. Our work is a prospective cohort study with a very high follow-up rate. The participants were representative of the native population of Taiwan. Some individual characteristics, such as in-utero exposure to maternal smoking (14), allergy or atopy (20), and residential community, may influence the occurrence of respiratory symptoms in childhood. Current second hand smoke were also found to interfere in the association with respiratory health (21,22). Moreover, atopic character may modify the relationships between obesity and bronchitis, and an association between obesity and non-atopic bronchitis has been suggested in some studies (7,20,23), but not in all (24,25). We adjusted the above covariates in Poisson regression models to minimize the confounding effects. The BMI and overweight/obesity status have been reported as risk factors for respiratory symptoms (6,26). In a large birth cohort study, children with higher BMI at 6-7 years were more likely to have bronchial hyper-responsiveness at 8 years of age compared with children with normal BMI (27). Guerra and colleagues found that BMI 28 would increase the risk of bronchitis in a case-control study (28). Other longitudinal studies also revealed an association between insulin resistance and asthma-like symptoms in adults (29). In present study, bronchitis was considered as an important respiratory phenotype, just like asthma or asthmatic symptoms. We found that overweight and obesity were both significantly associated with higher risks of incident bronchitis in adolescents. During the last decades, the prevalence of obesity has increased worldwide, and this phenomenon has generally affected all age groups (30). Adulthood obesity is usually associated with increased risks of several chronic diseases, such as type 2 diabetes, hypertension, coronary heart disease, and respiratory diseases (31). The relationship between childhood obesity and respiratory phenotypes was also reported in British (2), Chinese (6), and American (5) children between age of 5 and 18. During the process of puberty, teenagers often experience an increase in body weight. Numerous health risks have been associated with overweight in adolescence, including hypertension and respiratory diseases (32). It might be a reason for the adolescence is characterized by rapid hormonal, physical, and behavioral changes, all of which may affect the natural course of respiratory diseases (33). -related relative risks for the most relevant chronic diseases tended to be higher in younger and middle-aged people than in the elderly (34). Whether or not obesity/ overweight at different ages might show different associations with the development of respiratory diseases warrants further investigation. Bronchial hyper-reactivity could lead to the respiratory symptoms in childhood (3,4). A common explanation for the obesity on bronchitis relationship is that obesity causes airflow limitation and a reduction in respiratory system compliance. A combination of excess soft tissue weight compressing the thoracic cage and fatty infiltration of the chest wall leads obese individuals to breath shallower, which may result in dyspnea, chronic cough, or bronchitis (35). These obesity-associated, systemic immunological changes may further influence airway function. By examining the association between VOLUME 21 NUMBER 1 JANUARY 2013 E151

4 and the Occurrence of Bronchitis Lee et al. TABLE 2 Distribution of BMI percentile for participants with and without incident bronchitis exhaled nitric oxide measurement and obesity in adults, McLachlan and colleagues concluded that obesity was associated with airflow obstruction, but was not associated with airway inflammation (36). In the analysis stratified by gender, the effect estimates of overweight/obesity on incident bronchitis were significantly higher in girls, not in boys (Table 3). Our finding was consistent with previous literatures. Tollefsen et al. discovered that girls suffered from higher risks of incident wheeze and asthma than boys during adolescence (37). Chen et al. also found that obesity increased the incidence of asthma in women, but not in men during a 2-year study period (38). A gender shift was noted for the natural course of incident asthma, with a male to female ratio of 1.23 at 0-7 years and 1.48 at years (39). This effect modification by gender suggests that sex hormones could be involved in the causal pathway, and also indicates that obesity would alter the production of hormones associated with puberty in girls and that increased production of female hormones might alter lung development and regulation of airway tone in puberty-aged girls (40). Our study has some limitations. The assessment of respiratory outcomes was based on questionnaire reports and therefore may leads to misclassification of health outcomes and underestimation of the effect estimates. Moreover, the follow-up duration was not long enough, which might be the reason why a significant relationship between obesity and incident asthma was not found. It is possible that the TABLE 3 Incidence rates and relative risks of bronchitis by BMI and weight status, E152 VOLUME 21 NUMBER 1 JANUARY

5 cases of new-onset bronchitis in our study were undiagnosed cases at study entry. However, it seems unlikely because effect estimates did not changed substantially when we restricted the analyses to adolescents without a history of asthma (Supplementary Table S1). In conclusion, adolescents with high BMI percentile, overweight or obesity would face increased risks of the occurrence of bronchitis. prevention campaigns could be useful to avoid adverse respiratory outcomes among school children in the future.o Acknowledgments The authors thank all the field workers who participated in data collection, the school administrators and teachers, and especially the parents and children who participated in this study. This work was supported by the Taiwan National Science Council (Grants # B MY3, # B ) and National Taiwan University. VC 2012 The Society References 1. Eijkemans M, Mommers M, de Vries SI et al. 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