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ORIGINAL ARTICLE

Pathway from Central Obesity to Childhood Asthma Physical Fitness and Sedentary Time Are Leading Factors Yang-Ching Chen1,2, Yu-Kang Tu1, Kuo-Chin Huang3, Pau-Chung Chen4, Da-Chen Chu2,5, and Yungling Leo Lee1,6 1 Institute of Epidemiology and Preventive Medicine and 4Institute of Occupational Medicine and Industrial Hygiene, College of Public Health, National Taiwan University, Taipei, Taiwan; 2Taipei City Hospital, ZhongXing Branch, Taipei, Taiwan; 3Department of Family Medicine, National Taiwan University Hospital, Taipei, Taiwan; 5Institute of Public Health and Community Medicine Research Center, National Yang-Ming University, Taipei, Taiwan; and 6Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan

Abstract Rationale: Available prospective studies of obesity and asthma have used only body mass index (BMI) as an indicator for adiposity; studies using detailed obesity measures are lacking, and the role of physical fitness level and sedentary time remains unexplored in the link between obesity and asthma.

interrelation among obesity, sedentary time, physical fitness level, and asthma; a structural equation model was used to explore the pathogenesis among these factors. Asthma incidence was analyzed during a 2-year follow-up among centrally obese and nonobese groups in baseline children without asthma.

Objectives: To compare various anthropometric measures of obesity in relation to childhood asthma, and to further characterize the interrelations among central obesity, physical fitness level, sedentary time, and asthma.

Measurements and Main Results: Central obesity most accurately predicts asthma. Low physical fitness levels and high screen time increase the risk of central obesity, which leads to asthma development. Obesity-related reduction in pulmonary function is a possible mechanism in the pathway from central obesity to asthma.

Methods: The nationwide Taiwan Children Health Study followed

Conclusions: Central obesity measures should be incorporated in

2,758 schoolchildren from fourth to sixth grade, annually collecting data regarding physical fitness, sedentary time, obesity measures (comprising body weight and height, abdominal and hip circumference, skin fold thickness, and body composition), asthma, and pulmonary function tests. The generalized estimating equation was used for 3 years of repeated measurements to analyze the

Obesity and asthma severely deteriorate child health. Epidemiologic studies have consistently demonstrated that obesity is closely linked to asthma, and that obesity typically antedates asthma occurrence. A recent metaanalysis that included six relevant child studies showed that overweight children exhibited increased risk

childhood asthma risk predictions. Children are encouraged to increase their physical fitness levels and reduce their sedentary time to prevent central obesity–related asthma. Keywords: central obesity; physical fitness; sedentary time; pulmonary function; asthma

of incident asthma (1). A positive doseresponse relationship between body mass index (BMI) and asthma risk was also observed. Available prospective studies of obesity and asthma have primarily used BMI as an indicator of adiposity. Alternative obesity measures that account for fat distribution

include skinfold thickness, waist and hip circumference, and body composition. Two studies explored the relationship between skinfold thickness and asthma, but yielded inconsistent results (2, 3). One study observed no significant relationship between body fat percentage (measured using bioelectrical impedance) and asthma

( Received in original form January 19, 2014; accepted in final form March 25, 2014 ) Supported by grants #98-2314-B-002-138-MY3 and #101-2314-B-532-002-MY3 from Taiwan National Science Council. Author Contributions: Y.-C.C. contributed the cohort data collection, statistical analysis, interpretation of data, and writing. Y.-K.T. assisted in the critical part of the statistical analysis and data interpretation. K.-C.H., P.-C.C., and D.-C.C. contributed to critically revising this manuscript for intellectual content. Y.L.L. reviewed the study design and supervised the study. Correspondence and requests for reprints should be addressed to Yungling Leo Lee, M.D., Ph.D., #17 Xuzhou Road, Zhongzheng District, Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei 100, Taiwan. E-mail: [email protected] This article has an online supplement, which is accessible from this issue’s table of contents at www.atsjournals.org Am J Respir Crit Care Med Vol 189, Iss 10, pp 1194–1203, May 15, 2014 Copyright © 2014 by the American Thoracic Society Originally Published in Press as DOI: 10.1164/rccm.201401-0097OC on March 26, 2014 Internet address: www.atsjournals.org

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American Journal of Respiratory and Critical Care Medicine Volume 189 Number 10 | May 15 2014

ORIGINAL ARTICLE

At a Glance Commentary Scientific Knowledge on the Subject:

Prospective studies have suggested that obesity antedates development of asthma. The role of physical fitness and sedentary time remain unexplored in the link between obesity and asthma. What This Study Adds to the Field: Among various obesity

measures, central obesity most accurately predicts asthma; physical fitness and sedentary time are leading factors in the pathway from central obesity to asthma and decreased pulmonary function is a possible mechanism in this link. Children are encouraged to increase their physical fitness levels and reduce sedentary time to prevent central obesity–induced asthma. (4). In a pediatric study, Vahlkvist and coworkers (5) noted that children with asthma were less fit and had a higher body fat percentage compared with children without asthma. A cross-sectional study by Musaad and coworkers (6) demonstrated that abdominal obesity was more strongly related to childhood allergic asthma than was BMI. Moreover, another recent crosssectional study by Forno and coworkers (7) reported that BMI, percent body fat, and waist circumference (WC) were all associated with increased risk of asthma. Besides, fat-free mass was noted to be inversely correlated to adult asthma (8). The results of the above studies were not consistent. Children studies using detailed obesity measures, such as total body fat or fat-free mass, are lacking and may provide additional insight into the obesity-asthma link. Sedentary time, which is defined as the time spent in sitting behaviors, is associated with deleterious health consequences, such as all-cause mortality (9), obesity (10), and adverse metabolic profiles (11). Screen time, defined as time engaging with screen media, has been correlated with low cardiorespiratory fitness levels in previous longitudinal studies (12, 13). Although studies have confirmed the associations between physical fitness level, sedentary time, and obesity, studies exploring how

physical fitness level and sedentary time affect asthma development are scant (14, 15). The role of physical fitness level and sedentary time in the link between obesity and asthma remains largely unexplored. Only one study concerning the obesityasthma link adjusted physical activity as a confounder; however, the study concluded that the obesity-asthma relationship was independent of physical activity (16). Because physical fitness and sedentary time are correlated with obesity and asthma (14, 15, 17), we hypothesize that they are intermediate or precipitating factors in the pathogenesis from obesity to asthma. The Taiwan Children Health Study (TCHS) followed 2,758 schoolchildren from the fourth to sixth grades, annually collecting data on physical fitness, sedentary time, obesity measures, and respiratory outcomes. Therefore, the TCHS data provide a unique opportunity to test our hypothesis: exploring the relationship between central obesity and childhood asthma; and investigating the interrelations among central obesity, physical fitness level, sedentary time, and asthma. Moreover, according to previous literature, one possible biologic mechanism from central obesity to asthma could be mediated by poor pulmonary function (18, 19). Therefore, we also aim to examine the role of pulmonary function between central obesity and childhood asthma.

Methods Measurements and Data Collection

The TCHS is a nationwide prospective multidisciplinary study of a school-based cohort, comprising two parts. The first cohort of seventh- to eighth-grade children was enrolled in 2007, and the second cohort of fourth-grade schoolchildren was enrolled in 2010 (20). The analysis herein involved data from the second cohort because it contained several obesity measures. A questionnaire was distributed to parents to address child respiratory health and associated confounders, and a questionnaire was given to children to assess the time spent on sedentary behaviors (only collected in 2010 and 2012). Between 2010 and 2012, we performed the annual follow-ups approximately from April to June regarding the parent and child questionnaires, obesity

Chen, Tu, Huang, et al.: Obesity, Physical Fitness, and Childhood Asthma

measures, physical fitness levels, and pulmonary function tests. Our study followed the guiding principles of the Declaration of Helsinki (21) and the protocol was approved by the Institutional Review Board at National Taiwan University Hospital. Outcome Definition

We used parent-reported questionnaire to define the lifetime occurrence of physiciandiagnosed asthma. The question was “Has a doctor ever diagnosed your child as having asthma”? Additionally, active asthma cases were distinguished from normal children by asking two questions: “Has a doctor ever diagnosed your child as having asthma”? and “Did your child ever experience difficulty breathing, or did you observe any wheezing or whistling from his or her chest in the past 12 months”? If the answers were “Yes” to both questions, we classified the child as an active asthma case. Moreover, during the follow-up surveys, the questionnaire responses of the parents were used to categorize the incident asthma statuses of the child participants. Obesity Measures

Body weight was determined using a body composition machine that comprised an electronic scale (IOI 353; Jawon Medical, Korea; accuracy, 0.1 kg); the participants were weighed wearing light clothing and no shoes. Body height was measured to the nearest 0.1 cm by using the wall-mounted stadiometer (MAGATA, BW-120, Taiwan) at each school. BMI was calculated as weight divided by (height)2 (kg/m2) and was converted into age- and sex-specific BMI percentiles (22).WC was measured to the nearest 1 mm by using a flexible tape at the natural waist (midpoint between the lower ribcage and the iliac crest) and hip circumference was measured at the level of the maximal posterior extension of the buttocks. Three central obesity measures were taken: (1) WC, (2) waist-to-hip ratio (WHR), and (3) waist-to-height ratio (WHtR). Participants who exhibited sexand age-specific central obesity measures greater than or equal to 85th percentile were classified as exhibiting central obesity. Skinfold thickness was measured in duplicate to the nearest 0.5 mm by using Lange calipers (Beta Technology, Santa Cruz, CA). Two skinfold sites over the bilateral triceps and gastrocnemius were measured based on standard procedures. 1195

ORIGINAL ARTICLE The same investigator took all measurements. The skinfold sums were calculated by adding the average skinfold of the bilateral triceps and gastrocnemius. The body fat percentage was calculated based on the skinfolds according to equations from previous literature (23). Resistance and reactance were measured using a tetrapolar multifrequency bioelectrical impedance analysis (BIA) machine (IOI 353; Jawon Medical), which yielded detailed body composition data, such as body fat percentage, total body fat, fat-free mass, total body water, and total body muscle. Children were asked to avoid fluid or food intake and vigorous exercise 2 hours before BIA measurements. Physical Fitness and Sedentary Time

Physical fitness tests were annually performed using a standardized protocol at each school during the follow-up surveys (24). Among these tests, an 800-m sprint was used to determine the cardiorespiratory endurance of each child. Starting from a resting position, the 800-m sprint was measured using electronic time measurement (seconds) at a precision of 1 per 100 seconds. The physical fitness index (z score) was calculated based on the speed of the 800-m sprint, using sex- and agespecific means and standard deviations. We defined a high physical fitness level as a positive z score in the 800-m sprint. We used the Chinese version of the International Physical Activity Questionnaire (25) to determine child sedentary time. Sedentary time was defined as the hours per day that children spent sitting without doing physical activities. Screen time was the sum of hours per day spent watching television, using a computer, or playing videogames. Sedentary and screen times during school days and holidays were separately determined and the average daily sedentary and screen times were calculated using weighted means. The cut-off point used to establish an excessive sedentary time was an age- and sex-specific median split. Screen time was classified as high if children reported more than 2 hours per day (13). Pulmonary Function Tests

The pulmonary function tests were performed according to our previous standardized protocol (26). Five pulmonary function indices were analyzed: (1) FVC, (2) FEV1, (3) FEV1/FVC, (4) maximal mid1196

expiratory flow, and (5) peak expiratory flow. We obtained sex-specific percentages for the predicted pulmonary function indices; details of this method were listed in a previous study (26). Statistical Analysis

The normality of the continuous variables was tested using a Kolmogorov-Smirnov test. The continuous variables were expressed as mean 6 standard deviation and categorical variables were expressed as frequencies and percentages. We first categorized distinct obesity measures by using age- and sex-specific percentiles (,25, >25% to ,85%, and >85%) and the study population as reference. To evaluate the repeated measurements throughout the 3-year follow-up period, we used generalized estimating equations (GEE) (27) to examine the interrelations among central obesity, physical fitness level, sedentary time, and respiratory outcomes (active and physician-diagnosed asthma). The primary advantage of GEE is that it accounts for within-child association. The correlation structure assumed for repeated measurements is a working independence correlation. We considered various confounders, namely, age, sex, parental educational level, family income, family history of atopy, whether the mother

breastfed, and whether the child was exposed to in utero maternal smoke. Subjects with missing covariate information were included in the model using missing indicators. All analyses were conducted using SAS software version 9.2 (SAS Institute, Cary, NC). The statistical significance was set at 5%, based on two-sided estimation. A structural equation model (SEM) was applied to the data from the 3-year followup, using Mplus software (Mplus version 5; Muthen and Muthen, Los Angeles, CA). The skewed-distributed continuous variables were log-transformed. We assumed that physical fitness level and sedentary time determined central obesity, which subsequently caused asthma. Furthermore, we hypothesized that the biologic pathway from central obesity to asthma could be mediated by poor pulmonary function. We used a linear combination of the respiratory outcomes and pulmonary function indices (FEV1/ FVC) from survey 1 to 3. An estimated coefficient/SE value estimate of 1.96 or larger was considered statistically significant (equivalent to the 0.05 level). The final model was reached when the comparative fit index was greater than 0.90, the Tucker-Lewis index was greater than 0.90, and the root mean square error of approximation approached 0.05.

Table 1: Characteristics of All Participants of Fourth, Fifth, and Sixth Grade in Taiwan Children Health Study

Parameter Age Male sex BMI, kg/m2 Body fat percentage from skinfold, % Sum of skinfolds, mm WC, cm WHR WHtR Body fat percentage from BIA, % Total body fat, kg Fat-free mass, kg Total body water, kg Total body muscle, kg Physical fitness index Sedentary time, h/d Screen time, h/d Pulmonary function FEV1/FVC, % Active asthma Physician-diagnosed asthma

Survey 1 (n = 2,758)

Survey 2 (n = 2,150)

Survey 3 (n = 1,933)

9.7 1,409 18.6 23.2 29.9 62.1 0.82 0.45 17.3 6.8 29.8 21.5 27.7 0.00 6.88 1.94 90.8 127 243

10.6 (0.5) 1,075 (50.0) 19.3 (3.8) 28.1 (8.5) 37.3 (12.3) 65.5 (10.0) 0.82 (0.06) 0.45 (0.06) 17.7 (7.7) 7.9 (5.3) 33.5 (5.9) 24.2 (4.3) 31.1 (5.4) 20.04 (0.99) — — 90.8 (6.7) 101 (4.7) 198 (9.2)

11.7 965 20.4 25.7 33.7 64.9 0.78 0.44 19.6 9.6 36.4 26.6 33.7 0.16 4.67 2.94 92.2 68 188

(0.5) (51.1) (3.8) (8.1) (11.7) (9.9) (0.06) (0.06) (7.5) (4.5) (5.7) (4.1) (5.2) (1.00) (5.02) (1.99) (6.7) (4.6) (8.8)

(0.5) (49.9) (4.1) (7.6) (11.1) (10.4) (0.24) (0.06) (7.8) (5.9) (6.3) (4.2) (5.8) (1.07) (2.40) (2.49) (6.7) (3.5) (9.7)

Definition of abbreviations: BIA = bioelectrical impedance analysis; BMI = body mass index; WC = waist circumference; WHR = waist-to-hip ratio; WHtR = waist-to-height ratio. All data are presented as means (SD) or numbers (%).

American Journal of Respiratory and Critical Care Medicine Volume 189 Number 10 | May 15 2014

ORIGINAL ARTICLE Table 2: Associations between Obesity Measures and Asthma Using Generalized Estimating Equation Model

Obesity Measures

OR1 (95% CI)

BMI percentiles ,25% 1 >25% to ,85% 1.67 (1.12–2.51) >85% 2.16 (1.31–3.57) P for trend 0.002 Body fat percentage from skinfold ,25% 1 >25% to ,85% 1.23 (0.86–1.76) >85% 1.76 (1.12–2.77) P for trend 0.02 Sum of skinfolds ,25% 1 >25% to ,85% 1.19 (0.84–1.70) >85% 1.74 (1.11–2.73) P for trend 0.02 WC ,25% 1 >25% to ,85% 2.12 (1.39–3.24) >85% 2.61 (1.53–4.43) P for trend ,0.001 WHR ,25% 1 >25% to ,85% 1.65 (1.18–2.30) >85% 2.23 (1.44–3.46) P for trend ,0.001 WHtR ,25% 1 >25% to ,85% 1.50 (1.03–2.18) >85% 2.09 (1.29–3.39) P for trend 0.002 Body fat percentage from BIA ,25% 1 >25% to ,85% 1.02 (0.72–1.45) >85% 1.30 (0.80–2.09) P for trend 0.34 Total body fat ,25% 1 >25% to ,85% 1.28 (0.87–1.87) >85% 1.60 (0.97–2.63) P for trend 0.06 Fat-free mass ,25% 1 >25% to ,85% 1.38 (0.91–2.10) >85% 1.62 (0.97–2.70) P for trend 0.06 Total body water ,25% 1 >25% to ,85% 1.38 (0.91–2.10) >85% 1.59 (0.95–2.67) P for trend 0.07 Total body muscle ,25% 1 >25% to ,85% 1.39 (0.91–2.11) >85% 1.58 (0.94–2.66) P for trend 0.07

Active Asthma OR2 (95% CI)

OR3 (95% CI)

Physician-diagnosed Asthma OR1 (95% CI) OR2 (95% CI) OR3 (95% CI)

1 1.51 (0.89–2.55) 2.48 (1.35–4.55) 0.003

1 1.45 (0.93–2.27) 2.33 (1.39–3.92) 0.002

1 1.15 (0.88–1.50) 1.42 (1.01–1.99) 0.05

1 1.14 (0.87–1.49) 1.35 (0.96–1.91) 0.10

1 1.20 (0.90–1.59) 1.59 (1.12–2.27) 0.01

1 1.35 (0.84–2.16) 2.25 (1.26–4.04) 0.001

1 1.17 (0.78–1.73) 1.99 (1.20–3.99) 0.02

1 1.02 (0.80–1.31) 1.12 (0.80–1.58) 0.54

1 1.01 (0.78–1.30) 1.19 (0.84–1.69) 0.42

1 1.05 (0.81–1.37) 1.34 (0.94–1.92) 0.16

1 1.30 (0.81–2.08) 2.23 (1.26–3.98) 0.01

1 1.12 (0.76–1.68) 1.98 (1.20–3.25) 0.02

1 1.04 (0.81–1.33) 1.15 (0.82–1.62) 0.44

1 1.03 (0.80–1.33) 1.21 (0.85–1.71) 0.35

1 1.07 (0.82–1.40) 1.38 (0.97–1.98) 0.11

1 2.03 (1.18–3.48) 3.18 (1.69–5.99) ,0.001

1 1.84 (1.16–2.92) 2.70 (1.57–4.66) ,0.001

1 1.13 (0.88–1.46) 1.29 (0.92–1.81) 0.14

1 1.13 (0.87–1.46) 1.27 (0.90–1.78) 0.17

1 1.20 (0.91–1.59) 1.39 (0.97–1.99) 0.07

1 1.70 (1.06–2.71) 3.06 (1.75–5.34) ,0.001

1 1.51 (1.01–2.25) 2.42 (1.49–3.93) ,0.001

1 1.05 (0.83–1.82) 1.36 (0.99–1.87) 0.09

1 1.08 (0.86–1.37) 1.38 (0.99–1.90) 0.08

1 1.09 (0.84–1.41) 1.53 (1.09–2.17) 0.03

1 1.44 (0.89–2.32) 2.76 (1.54–4.93) 0.001

1 1.20 (0.80–1.80) 2.30 (1.40–3.77) 0.003

1 1.07 (0.84–1.34) 1.44 (1.04–2.00) 0.05

1 1.06 (0.84–1.35) 1.45 (1.04–2.05) 0.05

1 1.02 (0.78–1.33) 1.56 (1.11–2.20) 0.03

1 0.95 (0.59–1.54) 1.38 (0.75–2.55) 0.38

1 1.00 (0.65–1.54) 1.55 (0.91–2.65) 0.15

1 1.06 (0.82–1.32) 1.23 (0.87–1.75) 0.27

1 1.08 (0.84–1.40) 1.26 (0.88–1.81) 0.23

1 1.03 (0.77–1.38) 1.22 (0.83–1.80) 0.35

1 1.22 (0.72–2.07) 1.90 (1.00–3.60) 0.06

1 1.27 (0.80–2.03) 1.77 (1.01–3.09) 0.05

1 1.22 (0.93–1.59) 1.24 (0.86–1.78) 0.21

1 1.23 (0.94–1.62) 1.21 (0.83–1.75) 0.24

1 1.22 (0.90–1.65) 1.19 (0.80–1.78) 0.32

1 1.41 (0.80–2.49) 1.85 (0.95–3.60) 0.07

1 1.42 (0.87–2.33) 1.79 (1.00–3.21) 0.04

1 0.98 (0.75–1.29) 0.86 (0.59–1.25) 0.46

1 0.98 (0.74–1.30) 0.82 (0.56–1.18) 0.33

1 1.10 (0.81–1.48) 0.94 (0.63–1.39) 0.87

1 1.41 (0.80–2.48) 1.83 (0.94–3.56) 0.07

1 1.41 (0.87–2.31) 1.76 (0.99–3.16) 0.05

1 0.98 (0.75–1.29) 0.85 (0.59–1.23) 0.42

1 0.98 (0.74–1.30) 0.81 (0.55–1.17) 0.30

1 1.09 (0.81–1.47) 0.92 (0.62–1.38) 0.82

1 1.40 (0.79–2.46) 1.86 (0.95–3.62) 0.06

1 1.41 (0.86–2.31) 1.81 (1.01–3.21) 0.04

1 0.98 (0.75–1.28) 0.83 (0.57–1.20) 0.36

1 0.97 (0.74–1.28) 0.78 (0.54–1.14) 0.24

1 1.10 (0.81–1.47) 0.92 (0.62–1.37) 0.82

Definition of abbreviations: BIA = bioelectrical impedance analysis; BMI = body mass index; CI = confidence interval; OR = odds ratios; WC = waist circumference; WHR = waist-to-hip ratio; WHtR = waist-to-height ratio. OR1: adjusted for age, sex, parental education, family income, family history of atopy, breastfeeding, and in utero smoking. OR2: adjusted for age, sex, parental education, family income, family history of atopy, breastfeeding, in utero smoking, and physical fitness. OR3: adjusted for age, sex, parental education, family income, family history of atopy, breastfeeding, in utero smoking, and sedentary time.

Chen, Tu, Huang, et al.: Obesity, Physical Fitness, and Childhood Asthma

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ORIGINAL ARTICLE Table 3: Associations between Physical Fitness, Sedentary Time, and Asthma Using Generalized Estimating Equation Model Physical Fitness/Sedentary Time Physical fitness High Low P value Sedentary time Low High P value Screen time Low High P value

OR1 (95% CI)

Active Asthma OR2 (95% CI)

OR3 (95% CI)

Physician-diagnosed Asthma OR1 (95% CI) OR2 (95% CI) OR3 (95% CI)

1 1 1 1 1 1.16 (0.89–1.50) 1.15 (0.87–1.51) 1.03 (0.77–1.36) 0.95 (0.79–1.14) 0.93 (0.77–1.52) 0.28 0.33 0.86 0.56 0.44

1 0.90 (0.79–1.09) 0.29

1 1 1 1 1 1.26 (0.91–1.76) 1.32 (0.95–1.85) 1.27 (0.91–1.78) 0.96 (0.78–1.19) 0.93 (0.75–1.15) 0.16 0.10 0.16 0.73 0.50

1 0.91 (0.74–1.26) 0.39

1 1 1 1 1 1.06 (0.78–1.43) 1.09 (0.79–1.50) 1.04 (0.76–1.42) 0.93 (0.76–1.15) 0.86 (0.69– 1.07) 0.72 0.61 0.81 0.52 0.73

1 0.85 (0.68–1.05) 0.14

Definition of abbreviations: CI = confidence interval; OR = odds ratios. OR1: adjusted for age, sex, parental education, family income, family history of atopy, breastfeeding, and in utero smoking. OR2: adjusted for age, sex, parental education, family income, family history of atopy, breastfeeding, in utero smoking, and waist-to-hip ratio. OR3: adjusted for age, sex, parental education, family income, family history of atopy, breastfeeding, in utero smoking, and waist circumference.

To address reverse causation, we restricted our analysis to 2,515 fourth graders without asthma and observed the incidence of asthma during a 2-year follow-up among centrally obese and nonobese groups in survey 1. Moreover, we chose fourth graders without central obesity and compared the incidence of central obesity during a 2-year follow-up among disparate physical fitness level and sedentary time groups in survey 1. The PROC LIFEREG procedure of SAS was used to calculate the hazard risk ratio.

Results Characteristics of Study Participants

The study population comprised a total of 2,758 fourth-grade schoolchildren in 2010. The average annual follow-up rate was 83.9% after three surveys. The BMI, total body fat, fat-free mass, total body muscle, and body fat percentage from BIA gradually increased throughout adolescence (Table 1). The prevalence of overweight children rose from 30.8% in survey 1, to 32.1% in survey 2, and finally to 34.4% in survey 3. The average sedentary time in survey 1 was 6.88 hours per day; it declined to 4.67 hours per day in survey 3. In survey 1, 8.8% of children had physician-diagnosed asthma and 4.6% exhibited active asthma in the previous 12 months. Tables 2–4 included GEE model results using repeated measurement of the 3-year data. Table 5 demonstrated SEM results in the total study population (n = 2,758). In Table 6, we demonstrated the survival analysis using 1198

children without asthma (n = 2,515), and in Table 7, non–centrally obese participants (WC group, n = 1,980; WHR group, n = 1,979; WHtR group, n = 1,994) in survey 1. Central Obesity Predicts Asthma the Most among Various Obesity Measures

In Table 2, although BMI percentiles reflect significant dose responsiveness in relation to active asthma, three central obesity indicators (WC, WHR, and WHtR) consistently revealed more significant doseresponsive relationships. Comparing two

asthma outcomes, central obesity indicators significantly related to active asthma rather than physician-diagnosed asthma. This likely resulted because active asthma reflected a recent asthma status (within 12 mo), which should be more closely correlated to recent obesity measures compared with a lifetime diagnosis of asthma. OR1 was produced by GEE models adjusting for age, sex, parental education, family income, family history of atopy, breastfeeding, and in utero smoking. To examine the role of physical fitness and sedentary time in the relationships among

Table 4: Associations between Physical Fitness, Sedentary Time, and Central Obesity Using Generalized Estimating Equation Model Physical Fitness/Sedentary Time Physical fitness High Low P value Sedentary time Low High P value Screen time Low High P value

WC (>85%) OR (95% CI)

Central Obesity WHR (>85%) OR (95% CI)

WHtR (>85%) OR (95% CI)

1 1.14 (1.12–1.16) ,0.001

1 1.11 (1.09–1.14) ,0.001

1 1.13 (1.11–1.16) ,0.001

1 1.02 (1.00–1.05) 0.06

1 1.01 (0.98–1.03) 0.59

1 1.01 (0.99–1.04) 0.22

1 1.06 (1.03–1.08) ,0.001

1 1.03 (1.00–1.05) 0.04

1 1.05 (1.02–1.07) ,0.001

Definition of abbreviations: CI = confidence interval; OR = odds ratios; WC = waist circumference; WHR = waist-to-hip ratio; WHtR = waist-to-height ratio. Models were adjusted by age, sex, parental education, family income, family history of atopy, breastfeeding, and in utero smoking.

American Journal of Respiratory and Critical Care Medicine Volume 189 Number 10 | May 15 2014

ORIGINAL ARTICLE Table 5: Standardized Path Coefficients for Pathways from Physical Fitness, Sedentary Time to Central Obesity, and Asthma in Structural Equation Model Model for Active Asthma Pathway Positive link from central obesity to asthma Negative link from physical fitness to central obesity Positive link from sedentary time to central obesity Negative link from physical fitness to sedentary time Link from physical fitness to asthma Link from sedentary time to asthma Negative link from central obesity to pulmonary function Negative link from pulmonary function to asthma Link from sedentary time to pulmonary function Indirect Effect From physical fitness to asthma From sedentary time to asthma From central obesity to asthma Model fitness Chi-square test of model fit (P value) CFI TLI RMSEA

Model for Physiciandiagnosed Asthma

0.10*

0.08*



20.42†

0.12†

0.12†

20.20†

20.21†

0.01

0.05

0.02

20.02

20.25†

20.26†

20.09†

20.12†

0.06

0.05

20.05‡ 0.01* 0.02‡

20.03* 0.01 0.03†

,0.001 0.98 0.97 0.02

,0.001 0.98 0.97 0.02

20.42

Definition of abbreviations: CFI = comparative fit index; RMSEA = root mean square of approximation; TLI = Tucker-Lewis index. *P , 0.05. † P , 0.001. ‡ P , 0.01.

central obesity and asthma, we additionally adjusted physical fitness to produce OR2 and sedentary time to yield OR3. Comparing OR1 with OR2 showed that estimated effect of active asthma changed by more than 10% when physical fitness was introduced to the base model (the risk of active asthma in WC >85% vs. ,25%, OR1 = 2.61; OR2 = 3.18); this suggests that physical fitness is a crucial confounder, instead of intermediate factor, in the relationship between central obesity and asthma. A SEM was used to confirm the association between central obesity and asthma (Table 5, Figure 1). The standardized path coefficients for the pathways from central obesity to asthma were significantly positive (0.1 in the model for active asthma; 0.08 in the model for physician-diagnosed asthma). Furthermore, to prove the temporal association, we calculated the incidence of asthma among

distinct central obesity groups for a 2-year follow-up period in children without asthma of survey 1 (Table 6; see Figure E1 in the online supplement). The incidence of active asthma in the greater than or equal to 85% group was consistently higher than that of the less than 25% group, based on all central obesity indicators (the incidences of active asthma: WC >85% group vs. ,25% group was 2.54 vs. 1.91 cases per 100 person-years; WHR >85% group vs. ,25% group was 3.19 vs. 1.84 cases per 100 person-years; WHtR >85% group vs. ,25% group was 2.69 vs. 1.92 cases per 100 person-years). The findings were nearly identical regarding the outcome of physician-diagnosed asthma. Low Physical Fitness Levels and High Screen Time Increase the Risk of Central Obesity

The physical fitness index was negatively associated with all obesity measures,

Chen, Tu, Huang, et al.: Obesity, Physical Fitness, and Childhood Asthma

whereas sedentary and screen times were positively associated with obesity measures throughout the 3 years of repeated measurements (Table 4). Regarding the effect on central obesity, each unit increase in the physical fitness index related to a 0.05-cm reduction in WC. An additional hour of screen time per day correlated to a 0.35-cm increase in WC. The SEM (Table 5, Figure 1) results showed a negative link between physical fitness and central obesity and positive link between sedentary time and central obesity (standardized path coefficients, 20.42 and 0.12, respectively). We determined that physical fitness and sedentary time were negatively correlated (standardized path coefficients, 20.20). Table 7 and Figure E2 show that the incidence of central obesity was consistently higher in the low physical fitness group than in the high physical fitness group for all central obesity indicators. The incidence of central obesity, as demonstrated using WC, was 5.11 and 2.62 cases per 100 person-years in the low- and high-level physical fitness groups, respectively; high sedentary and screen times also yielded high incidences of central obesity. Physical Fitness Levels and Sedentary Time Indirectly Influence Asthma Risk through Central Obesity

Table 3 shows the associations among physical fitness, sedentary time, and asthma based on the GEE model. Regardless of the confounders adjusted in the model, no significant relationships were observed. The SEM results (Table 5, Figure 1) show that the links between physical fitness level or sedentary time and asthma were nonsignificant. However, the physical fitness levels and sedentary time indirectly and significantly affected asthma. Although physical fitness levels and sedentary time did not directly influence asthma risk, they were mediated through central obesity. Obesity-related Reductions in Pulmonary Function Are a Possible Mechanism Linking Central Obesity to Asthma

Among the five pulmonary function indices, FEV1/FVC displayed the most significant associations with the obesity measures (see Table E1). Therefore, we chose FEV1/FVC as the representative index of pulmonary function in the SEM; the SEM results show that a high degree of central obesity causes correspondingly poor pulmonary 1199

ORIGINAL ARTICLE Table 6: Incidence and Hazard Ratios of Asthma during 2-Year Follow-up among Fourth Graders with No Asthma Central Obesity Measures in Survey 1 WC ,85% >85% WHR ,85% >85% WHtR ,85% >85%

Active Asthma Incidence HR* (95% CI)

Physician-diagnosed Asthma Incidence HR* (95% CI)

1.91 2.54

1 1.21 (0.56–2.60)

3.20 3.70

1 1.22 (0.60–2.50)

1.84 3.19

1 1.20 (0.56–2.56)

3.28 3.35

1 1.53 (0.64–3.66)

1.92 2.69

1 1.56 (0.76–3.19)

3.31 3.10

1 1.17 (0.57–2.39)

Definition of abbreviations: CI = confidence interval; HR = hazard ratios; WC = waist circumference; WHR = waist-to-hip ratio; WHtR = waist-to-height ratio. Unit of incidence: cases per 100 person-years. *Models are adjusted by age, sex, parental education, family income, family history of atopy, breastfeeding, and in utero smoking.

function, increasing the risk of asthma (Table 5, Figure 1).

Discussion By comparing various obesity measures among children, we revealed that central obesity is the critical obesity measure for predicting asthma. Exploring the pathogenesis from central obesity to asthma showed that low physical fitness levels and high sedentary time are precipitating factors, rather than intermediate factors, in the pathway from central obesity to asthma. Decreased pulmonary function is a possible mechanism in the link between central obesity and asthma. The finding that central obesity relates to asthma and incident asthma supports the

reports of the few previous cross-sectional studies (6, 28, 29). However, these studies reported that the correlations were observed only in restricted asthma phenotypes, such as nonatopic asthma (29), children with asthma that exhibited allergic rhinitis (6), or only in women (28). These discrepancies likely resulted from the differing races of the study participants and the misclassification of asthma phenotypes. Only one longitudinal adult study in Sweden attained findings similar to those in the current study (30). Adolescence is the critical period for developing central obesity (31); however, this study was the first children study to compare the associations among various obesity measures and asthma, using 3-year repeated measurements. The possible mechanisms of central obesity–related

asthma include the mechanical compression of abdominal obesity on the thoracic cage and the influence of proinflammatory mediators (produced by visceral fat) on airway remodeling. Consistent with previous crosssectional studies (32, 33), the SEM results yielded a significant inverse correlation between physical fitness levels and sedentary time. A recent longitudinal study demonstrated that excessive screen time during childhood predicts low cardiorespiratory fitness levels in adolescence (13). Additionally, previous studies regarding the relationship between physical fitness level and sedentary time and central obesity have been scarce and primarily cross-sectional (17, 34, 35). One adult study concluded that sedentary behavior is not associated with abdominal obesity (36). According to a review of the literature, this is the first study to show that low physical fitness levels and high sedentary time predict the development of central obesity, based on a 2-year follow-up study. Adolescence is a critical time for changes in body composition, sedentary lifestyle, and physical fitness levels. To prevent central obesity–related cardiometabolic and respiratory diseases in the teenage years and later life, improvements in physical fitness levels and decreases in sedentary behaviors must be advocated. Because physical fitness levels and sedentary time were proposed as possible pathways linking obesity and asthma, we used SEM to examine their roles. This is the first study to show that low physical fitness levels and high sedentary time indirectly

Table 7: Incidence and Hazard Ratios of Central Obesity during Two-year Follow-up among Fourth Graders without Central Obesity Physical Fitness/Sedentary Time in Survey 1 Physical fitness High Low Sedentary time Low High Screen time Low High

WC (>85%) Incidence HR* (95% CI)

WHR (>85%) Incidence HR* (95% CI)

WHtR (>85%) Incidence HR* (95% CI)

2.62 5.11

1 1.87 (1.23–2.83)

5.24 9.25

1 1.58 (1.14–2.18)

2.01 4.74

1 1.66 (1.18–2.34)

3.93 3.66

1 1.12 (0.82–1.54)

6.80 7.37

1 0.94 (0.73–1.23)

2.97 3.77

1 1.24 (0.93–1.67)

3.30 5.37

1 1.26 (0.92–1.72)

6.50 8.39

1 1.01 (0.76–1.33)

2.70 5.05

1 1.15 (0.87–1.53)

Definition of abbreviations: CI = confidence interval; HR = hazard ratios; WC = waist circumference; WHR = waist-to-hip ratio; WHtR = waist-to-height ratio. Unit of incidence: cases per 100 person-years. *Models are adjusted by age, sex, parental education, family income, family history of atopy, breastfeeding, and in utero smoking.

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ORIGINAL ARTICLE

Figure 1. Structural equation model with pathways from physical fitness, sedentary time to central obesity, and asthma. Latent variables are depicted as ovals and rectangles represent indicator and other measured variables. Significant relationships are shown by boldface lines. Insignificant relationships are shown by dashed lines. The directions of the arrows distinguish between predictors and outcomes. Pf 1–3 = physical fitness index in survey 1–3; Sedt 1, 3 = average daily sedentary time in survey 1 and survey 3; Screen 1, 3 = average daily screen time in survey 1 and survey 3; WHR 1–3 = waist-to-hip ratio in survey 1–3.

affect the development of asthma and are mediated by central obesity. The GEE and SEM analyses yielded no direct association between physical fitness levels or sedentary time and asthma. The SEM data (not shown) could not prove whether intermediate factors of physical fitness levels or sedentary time affected the pathway from central obesity to asthma. Furthermore, we investigated the direction of the pathophysiology by calculating the incidence from low physical fitness levels and high sedentary time to central obesity, and from central obesity to asthma. The reverse causality that children with asthma are inactive, leading to further risk of overweight, was not supported by a previous pediatric cohort study (37). In clinical practice, many physicians emphasize the effect of physical fitness training to lessen symptoms and improve quality of life in children with asthma. This might explain why we did not observe lower levels of physical fitness in children with asthma. Previous studies exploring the relationship among physical fitness levels, sedentary time, and asthma have used diverse methodologies and yielded inconsistent results. Two 10-year follow-up studies revealed that low physical fitness levels in childhood were associated with developing asthma in young adulthood. Rasmussen and coworkers (15) determined that physical fitness levels (measured by bicycle

ergometer) were weakly correlated with incident asthma during adolescence. Ortega and coworkers (14) subsequently discovered that the protective effect of high cardiorespiratory fitness levels on incident asthma was particularly significant among obese individuals. This study supported our finding that the association between physical fitness levels and asthma is mediated by adiposity. However, these studies evaluated physical fitness levels only at the beginning of the study rather than repeatedly recording these levels throughout the study period. In addition, Sherriff and coworkers (38) demonstrated that excessive television viewing duration in children who exhibited no symptoms of wheezing at 3.5 years of age was associated with incident asthma in later childhood; however, no direct association was indicated between sedentary behaviors and bronchial hyperresponsiveness, which should be similar to asthma. The exact mechanism warrants exploration in subsequent studies. We discovered that central obesity–related decline in pulmonary function (measured using FEV 1 /FVC) is a pathway that links to asthma. Similar findings have been reported in the literature in adult and child studies (39, 40). Abdominal obesity measures are more accurate predictors of pulmonary function than are body weight or BMI

Chen, Tu, Huang, et al.: Obesity, Physical Fitness, and Childhood Asthma

(41, 42). A longitudinal study that used a 7-year follow-up period indicated that changes in WC were associated with changes in FEV 1 (43). Abdominal obesity may mechanically restrict the diaphragm and limit lung expansion, triggering asthma attacks. The major strengths of our study lie in the prospective design and the large population-based child study that involved various obesity and physical fitness measures and questionnaires, which were annually repeated for 3 years. Furthermore, we used multiple exposure and outcome measures to address possible misclassifications. The results were similar regardless of the exposures and outcomes used. We discovered novel interrelations among central obesity, physical fitness levels, sedentary time, and asthma that were independent of various confounders and robust in the three distinct statistical analyses. The study was limited by the questionnaire-derived sedentary time that the children self-reported; however, the relationships among sedentary time, physical fitness levels, and obesity were consistent with those reported in the literature. We used the same validated questionnaire, the International Physical Activity Questionnaire, in 2010 and 2012 surveys. The participants were likely sufficiently mature to validly report their sedentary time and parent-reported asthma was used to assess the outcomes. The SEM and incident rate calculations yielded similar findings for active and physiciandiagnosed asthma. Furthermore, selfreported asthma questionnaires are widely used in epidemiologic studies and have been proven a valid measure of asthma. Another limitation of the study is that we used an 800-m sprint performed at a school as an indicator of physical fitness level rather than using accelerometers or bicycle ergometers; however, an 800-m sprint performed using standardized protocol is similar to the vigorous exercise attained using bicycle or accelerometers to represent cardiorespiratory fitness. Repeated 3-year measurements also improved the validity and accuracy of the study. Besides, BIA measurements vary among different ethnic groups and are influenced by consumption of food and vigorous exercise. Our BIA machine used predictive equations adjusted for Asian population and we tried to perform the measurement under 1201

ORIGINAL ARTICLE standardized protocols. BIA is still considered a reliable and practical tool to estimate percent body fat in children (44). Given the burdens of childhood obesity and asthma, these findings may have critical implications for physicians and in future disease-prevention policies.

Children are encouraged to increase their physical fitness levels and reduce their sedentary time to prevent central obesity–induced asthma. Reducing central obesity enhances pulmonary function, preventing the occurrence of asthma. n

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Pathway from central obesity to childhood asthma. Physical fitness and sedentary time are leading factors.

Available prospective studies of obesity and asthma have used only body mass index (BMI) as an indicator for adiposity; studies using detailed obesity...
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