Environmental Tobacco Smoke Exposure and Chinese Schoolchildren s Respiratory Health. A Prospective Cohort Study

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1 Environmental Tobacco Smoke Exposure and Chinese Schoolchildren s Respiratory Health A Prospective Cohort Study Qi-Qiang He, PhD, Tze-Wai Wong, MSc, Lin Du, MMed, Zhuo-Qin Jiang, MMed, Tak-sun Ignatius Yu, MPH, Hong Qiu, MMed, Yang Gao, PhD, Andromeda H.S. Wong, MSc, Wei-Jia Liu, MMed, Jia-Gang Wu, MMed This activity is available for CME credit. See page A3 for information. Background: Although China is the most coveted cigarette market worldwide, few studies have examined the longitudinal effects of environmental tobacco smoke (ETS) on health. Purpose: To examine the relationship between exposure to ETS and respiratory health in Chinese schoolchildren. Methods: The study subjects included 1718 children, who were never-smokers, aged years and asthma-free at baseline. The children performed spirometric tests in 2006 and 18 months later. Parents reported the children s respiratory symptoms and illnesses, ETS exposure, and other related information by self-administered survey at both assessment points. The data were analyzed in Results: Signifıcant exposure response relationships were found between ETS exposure and coughing at night (p for trend 0.001); sneezing (p for trend 0.031); and sneezing with itchy, watery eyes (p for trend 0.006) in the fırst survey, and coughing at night (p for trend 0.019); phlegm without a cold (p for trend 0.001); and sneezing (p for trend 0.036) in the second survey. Compared with those who reported no ETS exposure in either survey, children who had a high ETS exposure ( 5 cigarettes/day) in either survey had lower growth rates in forced expiratory flow between 25% and 75% of forced vital capacity (FEF ; 0.104, p 0.020) and forced expiratory flow at 25% of forced vital capacity (FEF 25 ; 0.077, p 0.027). A monotonic exposure response effect was observed between ETS exposure and the defıcits in the growth rate of FEF 25 and FEF Conclusions: Exposure to ETS increased the risks of respiratory symptoms in Chinese school-aged children and was associated with impaired lung function growth. A dose response relationship was observed for the latter effect. (Am J Prev Med 2011;41(5): ) 2011 American Journal of Preventive Medicine Introduction From the School of Public Health, Wuhan University (He), Wuhan, Hubei, China; School of Public Health and Primary Care, The Chinese University of Hong Kong (He, TW Wong, Yu, Gao, Qiu, AHS Wong), Hong Kong Special Administrative Region, China; School of Public Health, Sun Yat-sen University (Jiang), Guangzhou, Guangdong, China; and the Guangzhou Center for Disease Control and Prevention (Du, Liu, Wu), Guangzhou, Guangdong, China Address correspondence to: Tze-Wai Wong, MSc, 4/F, School of Public Health and Primary Care, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong twwong@cuhk.edu.hk /$17.00 doi: /j.amepre The health effects of environmental tobacco smoke (ETS) have been studied extensively. 1 3 Tobacco smoke contains more than 4000 chemical compounds. Of these, several that are potent respiratory irritants (e.g., ammonia, dimethylnitrosamine, formaldehyde, acrolein) are generated at very high s. These chemicals go directly into the air from a burning cigarette, polluting the environment and affecting the health of nonsmokers as well. 4 Children have been identifıed as being particularly vulnerable to ETS exposure. 5 Although ETS exposure has been shown to be associated with deleterious effects in children, fındings on the causal relationship between ETS and respiratory health have been conflicting. 3,6 In analyzing the data from 1661 never-smokers who were followed up for 11 years, Gerbase reported that ETS exposure was associated with chronic bronchitis. 7 However, in a cohort of New Zealand children observed from ages 9 to 15 years, no detrimental effects of ETS exposure were detected for spirometric parameters in either gender. 8 Methodologic 2011 American Journal of Preventive Medicine Published by Elsevier Inc. Am J Prev Med 2011;41(5):

2 488 He et al / Am J Prev Med 2011;41(5): differences and variations in outcome defınitions might have been responsible for the inconsistent fındings. Most studies to date on the effects of ETS are based on Caucasians and are cross-sectional in design. Few studies have been conducted in China, which has a high proportion of smokers ( 67% male and 4% female) among those aged 15 years. 9 Environmental tobacco smoke has become a major public health problem in China. Data from two national surveys revealed that the prevalence of ETS exposure was 53.5% in and 51.9% in Of 540 million Chinese people who are exposed to ETS, 150 million are children aged 15 years. 10 A previous study 11 has also found racial differences in urinary cotinine, a toxic metabolite of nicotine and an objective measure of exposure to smoking. Therefore, a study of ETS exposure among Chinese children and their respiratory health is needed. This relationship was explored in a prospective cohort study in Chinese school-aged children in Guangzhou, China. The hypothesis in the current study was that exposure to ETS is associated with adverse effects on children s respiratory health. Methods Study Population and Design This was a prospective study on air pollution and schoolchildren s respiratory health in Guangzhou, China. Details of the study design and methods have been described previously. 12 Briefly, three districts representing various air-pollution s were selected on the basis of annual average air-pollutant concentrations. Students in Grades 3 and 4 were recruited from one to four primary schools located within 1 km from the local air-monitoring station in each district. They were assessed at baseline (September November 2006) and at follow-up after 18 months (March May 2008). Parents of the children provided informed consent before the study, which was approved by the Medical Research Ethics Committee of Sun Yat-sen University. Of 2179 participants assessed at baseline, 1827 (83.84%) were assessed at follow-up. Of these children, 109 were excluded for the following reasons: 57 had no ETS exposure information; 37 had physician-diagnosed asthma reported by their parents at baseline; and 15 additional children indicated that they had ever smoked (eight at baseline and seven at follow-up). Data from a total of 1718 (78.84%) children were analyzed in Exposures A self-administered standardized survey 13 completed by the parents was used to collect information about the children s respiratory symptoms and illnesses and personal and household environmental data (including ETS exposure) at baseline and follow-up. The surveys used at follow-up were the same as those used at the baseline study, except for the omission of data about basic information (e.g., SES). The children were also asked to complete a short questionnaire relating to the frequency and extent of their physical activities and their active smoking histories. Domestic ETS exposure was defıned as a positive response to the question Does anyone regularly smoke inside the children s bedroom? An additional question was On average, about how many cigarettes are smoked inside this house each day? Responses were separated into fıve categories: 0, 1 5, 6 10, 11 20, 20. To facilitate data analysis, the latter three categories were collapsed into one group: ETS exposure to 5 cigarettes/day. The exposure was assumed to be stable at both baseline and follow-up. Outcomes The presence of a respiratory symptom/illness was defıned as an affırmative answer to the following corresponding survey question: Wheezing: Has your child s chest ever sounded wheezy or whistling including at times when he/she had a cold during the past 12 months? Coughing at night: Has your child had a dry cough at night, apart from a cough associated with a cold or flu, or a chest infection during the past 12 months (excluding throat clearing)? Phlegm without a cold: Does your child usually seem congested in the chest or bring up phlegm when he/she did not have a cold during the past 12 months? Sneezing: Has your child had a problem with sneezing or a running or blocked nose when he/she did not have cold or flu during the past 12 months? Sneezing with itchy, watery eyes: Has this nasal problem been accompanied by itchy, watery eyes? Allergic rhinitis: Has your child been diagnosed with allergic rhinitis by a physician during the past 12 months? Bronchitis: Has your child been diagnosed with bronchitis by a physician during the past 12 months? In each survey, a spirometry test was performed in all subjects by the same group of technicians according to standardized methods, 14 using a Minato AS-505 portable electric spirometer. All forced expiratory maneuvers were performed in a standing position with a nose clip. A 2-L syringe was used to calibrate the spirometer before and after each fıeldwork session. The children were asked to perform a minimum of three reproducible forced expiratory measures (within 5% of the maximum forced vital capacity [FVC]). The output from the curve with the largest FVC and forced expiratory volume in 1 second (FEV 1 ) was chosen for further analysis. Before the spirometry, the subject s height (standing erect without shoes) and weight (in lightweight clothes) were measured. BMI was calculated using standard formula. Statistical Analysis The changes in height, weight, BMI, and the spirometric indices FVC; FEV 1 ; and forced expiratory flows at 25% (FEF 25 ), 75% (FEF 75 ), and between 25% and 75% (FEF ) of forced vital capacity between the baseline and the follow-up measurements were calculated for each child. The growth rates of spirometric indices were then annualized and presented as difference per year (dpy). In the analysis of associations between ETS exposure and lung function growth, children were classifıed into three groups: no ETS exposure at baseline and followup; low ETS exposure (1 5 cigarettes/day ETS exposure reported in either survey); and high s of ETS exposure ( 5 cigarettes/day ETS exposure reported in either survey). One-way ANOVA and a 2 test were used to compare the differences in continuous and categoric variables among the groups, respectively. The effects of ETS exposure on respiratory symptoms/illnesses were determined by multivariate logistic regression, after adjustment for potential confounding factors. Dif-

3 Table 1. Baseline characteristics of study children Characteristics ferences of lung function were compared by ANCOVA among the groups. Multivariate linear regression was performed to investigate the association between the growth rates of lung function and ETS exposure, with no ETS exposure used as the referent group. Tests for trend were conducted by including ETS exposure group as a continuous variable. All statistical analyses were performed using the SPSS, version Results No ETS exposure, n (%) (n 1521) ETS exposure (cigarettes/day) M (SE) 1 5 (n 127) 5 (n 70) In the baseline study, a total of 2407 (94.8%) participants performed the spirometry tests, and 2179 (90.5%) accomplished acceptable and reproducible tests (on three attempts). This report included 1718 children (858 boys and 860 girls) with an age range of 8 13 years (mean age years, SD 0.86 years) at baseline. Compared to 461 children whose parents did not participate in the follow-up survey (lost to follow-up or excluded from the study), the participant children had similar personal characteristics, including age, anthropometric characteristics, and spirometric indices. There were more boys and a higher prevalence of paternal allergy and asthma among the nonparticipants (data not shown). Table 1 shows the baseline characteristics of study children according to ETS exposure history. Children with different ETS exposure status had broadly similar characteristics, except that subjects who had ETS exposure with 1 5 cigarettes/ day were slightly but signifıcantly younger than those who had no exposure to ETS. The effects of ETS exposure on the prevalence of respiratory symptoms/ illnesses are presented in Table 2. Compared to the children who had no ETS exposure, children exposed to ETS had increased risks of coughing at night and sneezing both baseline and follow-up; sneezing with itchy, watery eyes at baseline; and phlegm without a cold at follow-up, respectively. Exposure response relationships were also observed between ETS exposure and coughing at night (p for trend 0.001); sneezing (p for trend 0.031); and sneezing with itchy, watery eyes (p for trend 0.006) in the baseline study and coughing at night (p for trend 0.019); phlegm without a cold (p for trend 0.001); and sneezing (p for trend 0.036) in the follow-up study. Table 3 shows the differences in lung function among children with varying ETS exposure. Children with ETS exposure of 5 cigarettes/day at baseline had lower FEF 75 and children with ETS exposure of 1 5 cigarettes/day at follow-up had lower FEF than those who had no ETS exposure. Table 4 shows the association between ETS exposure and lung function growth. Children whose parents reported a high ETS exposure ( 5 cigarettes/day) in either survey had lower growth rates in FEF ( 0.104, p 0.020) and FEF 25 ( 0.077, p 0.027) when compared with those who had no ETS exposure. There was also a monotonic exposure response relationship between ETS exposure and the defıcits in the growth rate of FEF 25 and FEF Discussion p-value Boys 745 (86.8) 72 (8.4) 41 (4.8) Allergy 130 (90.3) 10 (6.9) 4 (2.8) Maternal education 6 years 105 (88.2) 11 (9.2) 3 (2.5) Parental allergy 164 (85.9) 16 (8.4) 11 (5.8) Parental asthma 24 (85.7) 3 (10.7) 1 (3.6) Household characteristics He et al / Am J Prev Med 2011;41(5): New furniture 190 (90.5) 13 (6.2) 7 (3.3) Decor 183 (88.0) 13 (6.3) 12 (5.8) Carpet 110 (88.7) 8 (6.5) 6 (4.8) Physically active a 553 (88.8) 44 (7.3) 26 (3.9) Anthropometric characteristics Age (years) 10.1 (0.9) 9.9 (0.8) 10.0 (0.8) Height (cm) (7.1) (6.9) (8.2) Weight (kg) 32.9 (7.6) 32.1 (7.7) 32.9 (9.3) BMI 17.0 (2.9) 16.9 (2.9) 17.0 (3.3) a Defined as participation 3 times/week in sports and/or vigorous free-play lasting 30 minutes per session ETS, environmental tobacco smoke Exposure to ETS was associated with increased risks for coughing at night; phlegm without a cold; sneezing; and sneezing with itchy, watery eyes in schoolchildren. ETS exposure also had deleterious effects on lung function November 2011

4 490 He et al / Am J Prev Med 2011;41(5): Table 2. Effects of ETS exposure on the prevalence of respiratory symptoms/diseases First survey Second survey No ETS exposure ETS exposure (cigarettes/day) No ETS exposure ETS exposure (cigarettes/day) (n 1521) 1 5 (n 127) 5 (n 70) (n 1572) 1 5 (n 94) 5 (n 52) OR OR (95% CI) OR (95% CI) p for trend OR OR (95% CI) OR (95% CI) p for trend Wheezing 1.00 NA 1.26 (0.37, 4.31) NA 1.93 (0.23, 16.32) Coughing at night * (1.01, 2.96) 2.75** (1.46, 5.18) (0.69, 2.44) 2.42* (1.16, 5.05) Phlegm without a cold (0.33, 2.84) 2.22 (0.81, 6.09) (0.86, 4.18) 5.24*** (2.27, 12.10) Sneezing * (1.01, 2.39) 1.67 (0.93, 3.03) (0.70, 2.64) 1.85* (1.15, 2.98) Sneezing with itchy, watery eyes * (1.01, 4.93) 2.75* (1.13, 6.68) (0.36, 2.63) 2.03 (0.61, 6.74) Allergic rhinitis (0.45, 2.74) 0.34 (0.08, 1.54) (0.64, 2.36) 0.79 (0.30, 2.08) Bronchitis (0.60, 2.67) 0.34 (0.08, 1.47) (0.36, 4.07) 2.39 (0.68, 8.46) Note: ORs were adjusted for district, gender, age, BMI, allergy, parental allergy and asthma, physical activity, maternal education, and household characteristics (furniture, decor, carpet). *p 0.05, **p 0.01, ***p 0.001; compared with no ETS exposure ETS, environmental tobacco smoke; NA, not assessed (no case in group) (mean FEF 75 in liters/second: vs ; mean FEF in liters/second: vs ), and the growth rates (mean difference in FEF in liters/second: 0.20 vs 0.27 vs 0.30; mean difference in FEF 25 in liters/second: 0.09 vs 0.14 vs 0.17 from a high to no ETS exposure) of lung function. A monotonic exposure response relationship was observed in FEF 25 and FEF These fındings suggest a causal relationship between ETS and children s respiratory health. To date, few cohort studies have addressed the effects of ETS on respiratory symptoms/diseases. In the current study, several symptoms showed a dose response relationship with ETS exposure at baseline and follow-up, although only coughing at night and sneezing were consistent in having signifıcant p-values for trends. A possible explanation is that the presence of uncontrolled confounding factors biased the OR toward the null. The associations of ETS exposure with coughing at night; sneezing; sneezing with itchy, watery eyes; and phlegm without a cold are in accordance with fındings from two cross-sectional studies. 15,16 No relationship was observed between ETS and allergic rhinitis. This fınding lends support to Strachan and Cook s 17 conclusion (in a Table 3. Effects of ETS exposure on children s lung function, mean (SE) First survey Second survey No ETS exposure (n 1521) ETS exposure (cigarettes/day) No ETS exposure ETS exposure (cigarettes/day) 1 5 (n 127) 5 (n 70) (n 1572) 1 5 (n 94) 5 (n 52) FVC (L) 1.84 (0.01) 1.87 (0.02) 1.86 (0.03) 2.29 (0.01) 2.30 (0.03) 2.27 (0.04) FEV 1 (L) 1.67 (0.01) 1.71 (0.02) 1.65 (0.03) 2.07 (0.01) 2.03 (0.03) 2.03 (0.04) FEF (L/s) 2.09 (0.01) 2.12 (0.05) 1.97 (0.07) 2.57 (0.02) 2.41 (0.07)* 2.45 (0.09) FEF 75 (L/s) 2.78 (0.02) 2.75 (0.08) 2.52 (0.12)* 3.53 (0.03) 3.39 (0.11) 3.36 (0.14) FEF 25 (L/s) 1.34 (0.01) 1.37 (0.04) 1.32 (0.05) 1.61 (0.01) 1.50 (0.06) 1.54 (0.07) Note: Mean (SE) values are adjusted for district, gender, age, height, BMI, and physical activity. *p 0.05, compared with no ETS exposure ETS, environmental tobacco smoke; FEF, forced expiratory flow; FEF 25, FEF at 25%; FEF 75, FEF at 75%; FEF 25 75, FEF between 25% and 75%; FEV 1, forced expiratory volume in 1 second; FVC, forced vital capacity

5 Table 4. Multivariate linear regression analysis correlating lung function growth a during follow-up with ETS exposure status FVC dpy (L) Mean SE p-value No ETS exposure 0.28 Low ETS exposure exposure p for trend FEV 1 dpy (L) No ETS exposure 0.25 Low ETS exposure exposure p for trend FEF dpy (L/s) No ETS exposure 0.30 Low ETS exposure exposure p for trend FEF 75 dpy (L/s) No ETS exposure 0.48 Low ETS exposure exposure p for trend FEF 25 dpy (L/s) No ETS exposure 0.17 Low ETS exposure exposure p for trend Note: No ETS exposure no ETS exposure in both surveys (n 1431); low exposure 1 5 cigarettes/day ETS exposure in either survey (n 204); high exposure 5 cigarettes/day ETS exposure in either survey (n 83). a Adjusted for district, gender, age in 2008, height in 2006, change in height between 2006 and 2008, BMI in 2006, change in BMI between 2006 and 2008, lung function indices in 2006, and physical activity. ETS, environmental tobacco smoke; dpy, difference per year; FEF, forced expiratory flow; FEF 25, FEF at 25%; FEF 75, FEF at 75%; FEF 25 75, FEF between 25% and 75%; FEV 1, forced expiratory volume in 1 second; FVC, forced vital capacity He et al / Am J Prev Med 2011;41(5): systematic review of 36 publications) that ETS was unlikely to increase the risk of sensitization in children. Two previous prospective studies 18,19 have demonstrated relationships between ETS exposure and wheezing in infants. Moreover, some epidemiologic studies 20,21 indicated increased risks associated with ETS exposure in the development of childhood asthma. However, there were too few children with asthma in the current study. Underreporting, possibly due to underdiagnosis, is a possible explanation for the lack of an association. Nevertheless, compared with those who had no ETS exposure, a higher risk (OR 1) for wheezing was observed in the current study in children exposed to ETS of more than 5 cigarettes per day at baseline and follow-up. Among longitudinal studies on children s lung function, fındings have been inconsistent regarding the effects of ETS exposure. Dodge 22 found no differences in pulmonary function or yearly lung growth rates among subjects grouped by exposure to ETS during 4 years of study. In contrast, Wang et al. 23 observed reduced FEV 1, FEV 1 / FVC, and FEF in children followed up annually between ages 6 and 18 years. Tager and colleagues 24 found that maternal cigarette smoking lowered the expected average annual increase in FEV 1 in a cohort of children observed prospectively for 7 years. The current results are in line with these fındings, suggesting that ETS exposure has a substantial effect on children s lung function, as seen in other cohort 25,26 and cross-sectional studies. 1,2,20 Corbo et al. 27 found that persistent exposure to ETS was associated mainly with defıcits in the small airways, and that the FEV 1 measurement was not sensitive enough to detect the adverse effects of ETS. In the current study, defıcits were observed in FEF but not FEV 1 and FVC. In clinical practice, the FVC measurement is used mostly for the evaluation of large-airway functions; FEV 1 reflects airway obstruction in both large and small airways, whereas FEF 25, FEF 75, and FEF reflect peripheral small-airway functions. The effects on FEF might be more functional (a temporary narrowing) than structural (permanent reduction in size of the airways), which might explain why FVC, which represents overall lung capacity, was not affected. Lung function defıcits may persist into adulthood, with adverse health consequences such as chronic obstructive pulmonary diseases and cardiovascular diseases. Hence, the current results indicate a need for control of ETS exposure in Chinese children. 28 Both pre- and post-natal exposures to ETS might affect children s respiratory function. 29 A strong correlation between fetal and postnatal ETS exposure makes discrimination among various health effects much more diffıcult. It was not possible to assess maternal smoking (prevalence about 1%). 30 The effects of in utero exposure remain controversial. 8,20,25,31,32 November 2011

6 492 He et al / Am J Prev Med 2011;41(5): Limitations of the current study include seasonal variation in respiratory illnesses, as well as misclassifıcation and recall bias. ETS exposure was not confırmed by urinary cotinine s. Urinary cotinine is a highly sensitive and specifıc test for passive smoking but can indicate only recent exposure to ETS. 2 To date, there is no reliable biological marker for the assessment of ETS exposure. The questions that were used to identify domestic ETS exposure lacked precision. Regularly smoking was not defıned, nor were parents asked to report their own smoking status. Finally, exposure to ETS was assumed to be stable, but might have changed over time. In 1995, the Guangzhou government enacted anti-smoking legislation that prohibited smoking in public places, including schools and public transportation vehicles but not homes. 33 Strengths of the current study include the longitudinal design, the large sample size, and a high follow-up rate. The participants personal characteristics were broadly similar to those of the participants lost to follow-up. Moreover, the spirometric tests in both the baseline and follow-up studies were carried out using a standard protocol by the same group of technicians, who were unaware of the ETS exposure status of the subjects. Thus, the likelihood of selection and measurement biases is minimal. Conclusion The current study provides additional evidence that ETS exposure affects the respiratory health of Chinese schoolchildren. Given the high prevalence of smoking among the Chinese population and the large number of schoolchildren exposed to ETS, the fındings indicate a need for strong public health measures to protect children from exposure to ETS. As the home is the most common source of ETS exposure for children, this problem cannot be solved by the current law banning smoking in public places and schools. 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