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1 310 Adverse Effects of Air Pollution on Respiratory Health Yu et al Adverse Effects of Low-Level Air Pollution on the Respiratory Health of Schoolchildren in Hong Kong Tak-sun Ignatius Yu, MPH Tze Wai Wong, MSc Xiao Rong Wang, PhD Hong Song, MB Siu Lan Wong, MPhil Jin Ling Tang, PhD To evaluate the respiratory effects of long-term exposure to air pollution, schoolchildren (ages 8 to 12 years) from two districts in Hong Kong with contrasting air quality were studied. Parents of 1660 children completed questionnaires on respiratory symptoms, and 1294 children had their ventilatory function tested with a spirometer. After adjustment for relevant covariates, children living in the more polluted district had increased odds ratios for frequent cough (1.74), frequent sputum (1.87), chronic sputum (1.84), and doctor-diagnosed asthma (1.98). Children of both sexes in the more polluted district had significantly poorer lung function, and the differences among girls were more marked. The study provides additional evidence for the adverse effects of long-term exposure to relatively low-level air pollution. (J Occup Environ Med. 2001;43: ) From the Department of Community & Family Medicine (Dr Yu, Dr TW Wong, Dr Wang, Dr Song, Dr SL Wong, Dr Tang) and the Centre for Environmental Studies (Dr Yu, Dr TW Wong, Dr Song), The Chinese University of Hong Kong. Address correspondence to: Dr Tak-sun Ignatius Yu, Associate Professor, Department of Community & Family Medicine, The Chinese University of Hong Kong, 4/F, Lek Yuen Health Centre, Shatin, New Territories, Hong Kong; iyu@cuhk.edu.hk. Copyright by American College of Occupational and Environmental Medicine Hong Kong is a small territory with a large population and an intermixture of industry, commerce, and residential areas linked with an overloaded vehicular transport network system. There has been considerable public concern in recent years about the health effects of air pollution. In 1988, two-thirds of the complaints received by the Hong Kong Environmental Protection Department were related to poor air quality, and the maximum daily air pollution concentrations exceeded air quality objectives on 38 occasions. 1 Since then, a series of interventions to reduce air pollution have been taken (eg, implementation of a smoky vehicle control program in 1988, and legislation to restrict the sulfur content of industrial fuel oil in 1990). The latter intervention resulted in reductions in sulfur dioxide (SO 2 ) levels by 80% in the most heavily polluted districts and a gradual decrease in total and respirable suspended particulates (RSP). 2,3 A study linking air pollution and children s respiratory health in Hong Kong showed an apparently larger decrease for respiratory symptoms in a polluted district compared with a less polluted district between 1989 and 1990 to 1991 following the intervention. 4 Little is known whether repeated exposures to currently lower levels of air pollution in Hong Kong would produce adverse health effects. Moreover, few Hong Kong studies have reported longterm effects of air pollution on pulmonary function in children. 5

2 JOEM Volume 43, Number 4, April Methods Study Population The study was performed in children who attended primary schools in two districts of Hong Kong. One district (Kwun Tong) was relatively highly polluted because of the presence of industries and a high concentration of automobiles (labeled as the high-pollution district, or HPD); the other district (Shatin) was a new town with mainly residential buildings and some commercial activities (labeled as the low-pollution district, or LPD). Third- to sixth-grade students of four schools from each district, chosen for their proximity to the environmental monitoring stations fixed by the Environmental Protection Department, were invited to participate in the survey. Nearly all primary-school children in Hong Kong live in the vicinity of their schools. Only children between 8 and 12 years old were included. Concentrations of Air Pollutants The Environmental Protection Department routinely performed 24- hour monitoring for a number of specific air pollutants in different districts of Hong Kong. SO 2 was measured using continuous ultraviolet-fluorescence analysers (TECO43); nitrogen dioxide (NO 2 ) by dual-channel chemiluminescent analyzers (Monitor 8840); and RSP by high-volume samplers (Sierra Andersen, Andersen Instruments, Inc, Smyma, GA) on 3-day cycles. Figure 1 shows the monthly average levels of SO 2,NO 2, and RSP in the two districts during the period April 1994 to March The mean annual concentrations over that period were 22.8 g/m 3, 58.5 g/m 3, and 57.6 g/m 3 in HPD, and 11.8 g/m 3, 42.9 g/m 3 and 44.9 g/m 3 in LPD for SO 2,NO 2 and RSP, respectively. The Air Quality Objectives of Hong Kong for annual concentrations were 80 g/m 3 for SO 2, and NO 2, and 55 g/m 3 for RSP. 3 Fig 1. Monthly mean concentrations of air pollutants during the period of April 1994 to March 1995 in the two districts of Hong Kong. Questionnaires Self-administered questionnaires modified from the American Thoracic Society (DLD-78-C) 6 were prepared for both parents and children. The questions for the parents concerned information regarding their children s current and past history of respiratory symptoms, respiratory illness diagnosed by physicians, indoor environmental factors at home, smoking history of family members, and their socioeconomic status. The questionnaires answered by the children were similar but included additional questions about their own smoking habits. The agreement for reported respiratory symptoms was generally poor between the children and their parents. 7 Responses from the parents on children s respiratory symptoms and illness and household and family conditions were used for subsequent analysis. The information on smoking habits of the children was obtained from the questionnaires completed by the children. A respiratory illness was defined as a doctor-diagnosed disease. A respiratory symptom occurring in the previous 12 months was considered to be present when a positive answer was given for the following items: Frequent cough: Does the child usually have a cough apart from colds? Chronic cough: Does the child cough on most days (4 or more days per week) for as much as 3 months of the year? Frequent sputum: Does the child usually bring up phlegm apart from colds? Chronic sputum: Does the child bring up phlegm on most days (4 or more days per week) for as much as 3 months of the year? Wheezing: Does the child ever sound wheezy or whistling apart from colds? Wheezing with shortness of breath: Has the child ever had an attack of wheezing that has caused him/her to be short of breath? Pulmonary Function Testing For students having consent from their parents, a trained technician administered the ventilatory function test using a dry spirometer (Vitalograph Ltd, Buckingham, England). Parameters obtained included forced vital capacity (FVC), forced expiratory volume in one second (FEV 1 ), the ratio of FEV 1 /FVC, and forced expiratory flow rate between 25% and 75% of FVC (FEF ). All tests were performed in the morning and with the child in a standing position and wearing nose clips. The best test (with the highest FVC and FEV 1 ) from at least three expiratory maneuvers was chosen. The values were corrected to the conditions of body temperature and pressure saturated with water vapor. Each child s height and weight were measured before beginning the expiratory maneuvers. Data Analysis Statistical analysis was performed by using the Statistical Package for the Social Sciences, version 7.0. The prevalence of respiratory symptoms,

3 312 Adverse Effects of Air Pollution on Respiratory Health Yu et al TABLE 1 Participation of Schoolchildren From the Two Districts in Hong Kong a LPD HPD Total n % n % n % No. of participating schools No. of eligible children ,711 No. of questionnaires by parents , No. of questionnaires by children , No. performing spirometric tests , a LPD, low-pollution district (Shatin); HPD, high-pollution district (Kwun Tong). illnesses, and relevant risk factors in the two districts was compared using the chi-squared test. Logistic regression analysis was applied to obtain adjusted estimates of odds ratios (ORs) of risk factors for respiratory symptoms and illnesses. The set of independent variables under consideration included: district (indicating pollution), sex, age, passive smoking, active smoking, father s occupation, cooking at home, burning incense at home, burning mosquito coils at home, having pets at home, and the recent purchase of new furniture. The district, age, and sex were included in all of the models. The other variables related to the health outcomes were selected using a forward stepwise approach. In the analysis of ventilatory function, multiple linear regression models were applied to select the related factors, using the stepwise procedure. Analysis of covariance was then used to estimate the difference in ventilatory parameters between the two districts, adjusting for age, height, body mass index (BMI) and other covariates that were found to be significant in the multiple linear regression models. Results Table 1 summarizes the number of subjects and response rates for the different components of the study in the two districts. The response rate from parents was high (97%) in both districts. Lung function testing was performed in 1294 children (76% of all eligible children). All children had been living in the same district for at least 1 year, and 85% of them for more than 3 years. The general data of 1660 children whose parents completed the questionnaires are summarized in Table 2. The children in the LPD were significantly younger than those in the HPD, and more boys in the LPD than in the HPD were born in Hong Kong. There was no difference in the prevalence of active smoking between the two districts. The factors potentially related to indoor air pollution at home were not significantly different between the two districts, with the exceptions that more boys in the HPD lived in a home with smokers and more boys in the LPD had pets in their homes. For respiratory symptoms and respiratory illnesses, both boys and girls in the HPD tended to have higher crude prevalences than those in the LPD, except for bronchitis in boys (Table 2). The differences between the two districts in the prevalence of frequent and chronic sputum for boys, and in frequent sputum, doctor-diagnosed asthma, and sinusitis for girls, were statistically significant. Estimates of adjusted ORs and their 95% confidence intervals computed from multiple logistic regression are presented in Table 3. The district differences for frequent cough (OR, 1.74), frequent sputum (OR, 1.87), chronic sputum (OR, 1.84), and asthma (OR, 1.98) reached statistical significance after adjusting for age, sex, and other relevant covariates. In addition, boys had significantly higher risk than girls for frequent sputum, wheezing with shortness of breath, and asthma. Passive smoking was associated only with sinusitis, and active smoking was not identified as an independent risk factor. The summary results of ventilatory function are showed in Table 4. In both sexes, the adjusted means were higher in the LPD. The differences in the parameters between the two districts were statistically significant, except for FVC in boys. The district differences in lung volume were generally greater in girls (50 ml for FVC, and 83 ml for FEV 1 ) than in boys (29 ml for FVC and 54 ml for FEV 1 ). No effect of either active or passive smoking on any parameter of ventilatory function was observed. The recent purchase of new furniture at home was associated with a decrease in FEV 1 /FVC and FEF in boys. Girls whose fathers held blue-collar jobs, and girls born in the mainland of China, had higher FVC and FEV 1 levels. Discussion Schoolchildren from a more polluted district in Hong Kong were found to have poorer respiratory health, when compared with those from a less polluted district, in terms of having more respiratory symptoms and illnesses and lower ventilatory capacities. The increased risks for frequent cough, frequent and chronic sputum, and asthma remained significant after adjusting for confounders. These observations could not be attributed to acute exposure to high levels of pollutants or to air pollution

4 JOEM Volume 43, Number 4, April TABLE 2 Prevalence (%) of Background Characteristics, Symptoms, and Diseases by District and Sex a Boys Girls LPD (n 392) HPD (n 402) LPD (n 420) HPD (n 446) Characteristics Age 10 years *** *** Place of birth (born in Hong Kong) *** Active smoking Passive smoking in the home ** Parents with white-collar job Cooking in the home Burning incense in the home Burning mosquito coils in the home Pets in the home * Recent purchase of new furniture Respiratory symptoms Frequent cough without cold Chronic cough for 3 months Frequent sputum without cold * ** Chronic sputum for 3 months ** Wheezing Wheezing with shortness of breath Respiratory diseases Bronchitis Asthma * Sinusitis * Allergic rhinitis a LPD, low-pollution district; HPD, high-pollution district. * P 0.05; ** P 0.01; *** P 0.001, using chi-squared tests. episodes. According to the monitoring records of the Environmental Protection Department, no incident of unusually high air pollution was recorded in either district during or in the year before the survey. The respiratory health of schoolchildren might also be affected by indoor air pollution. An exhaustive list of factors that might be related to poor indoor air quality was studied, and some individual factors (burning mosquito coils, having pets, recent purchase of new furniture) were found to affect certain health outcomes. Passive smoking had an effect only on sinusitis in this study. Although passive smoking has been reported to have adverse effects on respiratory health and pulmonary function, such effects were more related to smoking by mothers The lack of health effects attributable to passive smoking in this study might be explained by the low exposure of our children to smoking mothers, because the prevalence of smoking among female individuals in Hong Kong was quite low. Socioeconomic status could also affect respiratory health. Girls with fathers holding blue-collar jobs had better FVC and FEV 1 levels. It was also noted that some health outcomes were affected by the place of birth. Children born in the mainland of China generally had less bronchitis and allergic rhinitis than those born locally in Hong Kong, and the girls had higher FVC and FEF levels. Such findings were in accordance with other recent studies indicating that children born in Hong Kong had higher risks of asthma and respiratory symptoms than those born in the mainland of China. 12,13 This difference was assumed to be associated with different early life experiences of these two groups. In the present study, more children in the HPD were born in the mainland of China than in the less polluted district (14% vs 6%). Therefore, the difference in place of birth was not an explanation for the district difference in the health outcomes of this study. Although the response rate for the parent s questionnaire was very high, about a quarter of the children did not participate in the spirometry testing because of the lack of consent from parents, and this might introduce selection bias. We believe that the choice of not participating in the tests was more likely due to personal health reasons rather than the perception of poor air quality. Furthermore, a comparison between the participants and non-participants found no apparent differences in demographic background and reported respiratory symptoms and illnesses. Thus, it was unlikely that the findings were biased by self-selection. The associations between chronic exposures to low or moderate levels of air pollution and adverse respiratory health effects in this study were most likely true. Several studies have identified health effects, including increased mortality, 14 increased re-

5 314 Adverse Effects of Air Pollution on Respiratory Health Yu et al TABLE 3 Adjusted ORs and 95% CIs of Risk Factors for Respiratory Ailments a Respiratory Ailments and factors Included in Models OR 95% CI Frequent cough Age 10 yr Male HPD 1.74 * Chronic cough Age 10 yr Male HPD Burning mosquito 3.44 * coils in home Frequent sputum Age 10 yr 1.87 * Male 1.46 * HPD 1.87 * Have pets at home 2.03 * Chronic sputum Age 10 yr Male HPD 1.84 * Burning mosquito 3.64 * coils in home Wheezing Age 10 yr Male HPD Wheezing with shortness of breath Age 10 yr Male 1.78 * HPD Bronchitis Age 10 yr 1.20 * Male HPD Born in Hong Kong 3.10 * Asthma Age 10 yr Male 1.94 * HPD 1.98 * Sinusitis Age 10 yr 1.45 * Male HPD Passive smoking 2.17 * Allergic rhinitis Age 10 yr Male HPD Born in Hong Kong 2.29 * a OR, odds ratio; CI, confidence interval; HPD, high-pollution district. * P value 0.05 in logistic regression models. spiratory symptoms, 15,16 and decreased pulmonary function 9,17 at concentration levels of air pollutants around or below current air quality guidelines recommended by the World Health Organization. 18 In the present study, although there were contrasting levels of air pollution between the two districts, the levels of the primary pollutants SO 2,NO 2, and RSP in both districts were below or near the Ambient Air Quality Objectives currently applied in Hong Kong. At such relatively low levels of air pollution, we could still observe significant differences in respiratory outcomes, especially in ventilatory function. The findings were similar to those of a Canadian study in which levels of air pollutants in the two comparison regions were even lower than those of the present study. 19 Significant regional differences in FVC and FEV 1 were observed, despite the lack of differences in respiratory symptoms and illnesses. This implies that the changes of ventilatory function are sensitive indicators for determining effects of low-level air pollution. Nevertheless, it is difficult to attribute the health effects to a specific air pollutant, because these pollutants constitute independent risks but may act synergistically. 20,21 Besides the NO 2,SO 2, and RSP recorded in the present study, other pollutants (eg, ozone) might be partly responsible for the adverse health effects, as documented by other studies. 19,22 In accord with the findings of a previous Hong Kong study focusing on bronchial responsiveness associated with air pollution in children, 5 a remarkable effect of long-term exposure to air pollution on pulmonary function was detected in this study. This effect was reflected by small but statistically significant decrements of both ventilatory volume and flow in the children living in the more polluted district. It has been demonstrated that the adverse effects of acute air pollution on pulmonary function in children might be reversible if levels of air pollutants were reduced. 23,24 The significance and prognostic relevance of the observed decrements in ventilatory function found in this study, which might be a consequence of cumulative losses, remains unclear. Some researchers have suggested that small declines in ventilatory function in childhood might affect the rate of lung growth and contribute to the development of airway obstructive diseases in adulthood. 25,26 Thus, there might be serious public health consequences if small decreases in ventilatory function were associated causally with chronic exposure to air pollution, especially if the size of the exposed population is large. 19 It was of interest that boys and girls seemed to be somewhat different in their response to air pollution. Boys in general had more respiratory symptoms and illnesses than girls. On the other hand, girls had a greater decline in ventilatory volumes when exposed to pollution. Although many investigators did not report analysis stratified by sex, a few found inconsistent differences between boys and girls with respect to the effects of air pollution. Two studies reported that respiratory symptoms and illness associated with air pollution were more prevalent in boys than in girls. 27,28 Conversely, van Vliet P et al 29 found that relationships between truck traffic intensity and chronic respiratory symptoms were more pronounced in girls than in boys. Similar to our results, Spinaci and colleagues found that boys had higher lung volume levels and lower airflow rates than girls. 11 To date, there is still no satisfactory explanation to the gender difference, but this phenomena is worth noting in future studies. In conclusion, this study demonstrated differences in respiratory symptoms/illnesses and ventilatory function between children living in two districts having contrasting levels of air pollution. The differences in health outcomes were likely attributable to differences in ambient air quality. The study provides further evidence for the effects of chronic exposure to low-level air pollution on the respiratory health and pulmo-

6 JOEM Volume 43, Number 4, April TABLE 4 Comparison of Lung Function Parameters Between the Two Districts by Sex a Sex and District Observed Mean Adjusted Mean b HPD LPD (95% CI) Adjusted Covariates Boys FVC (L) LPD Age HPD ( 0.075,0.018) BMI ** R c FEV 1 (L) LPD Age HPD ( 0.097, 0.011) * BMI ** R FEV 1 /FVC (%) LPD Age HPD ( 2.77, 0.33) * BMI ** ( ) d Height Furniture ** ( ) e R FEF (L/sec) LPD Age * HPD ( 0.253, 0.059) ** BMI Furniture * ( ) R Girls FVC (L) LPD Age ** HPD ( 0.092, 0.009) * BMI ** POB * Occupation *f R FEV 1 (L) LPD Age ** HPD ( 0.122, 0.045) ** BMI ** Occupation ** R FEV 1 /FVC (%) LPD Age HPD ( 3.03, 0.93) ** BMI ** ( ) Height R FEF (L/sec) LPD Age ** HPD ( 0.249, 0.064) ** BMI POB ** R a HPD, high-pollution district; LPD, low-pollution district; CI, confidence interval; FVC, forced vital capacity; BMI, body mass index; FEV 1, forced expiratory volume in one second; FEF 25 75, forced expiratory flow rate between 25% and 75% of FVC; POB, place of birth in China. b Adjusted means were calculated using analysis of covariance adjusting for listed covariates. c R 2 given for multiple linear regression model with listed covariates. d ( ) indicates a negative relationship. e Furniture indicates recent purchase of new furniture. f Occupation indicates blue-collar job held by father. * P 0.05; ** P nary function of primary schoolchildren. The findings imply that the present Air Quality Objectives are insufficient to protect the health of the community and should be revised. Acknowledgments This study was supported in part by a grant from the Environment and Conservation Fund

7 316 Adverse Effects of Air Pollution on Respiratory Health Yu et al of the Hong Kong Government. We are grateful to the children, their parents, and their teachers who participated in this study; to all field investigators; and to our colleagues in the Environmental Protection Department, Hong Kong Government, for their professional advice. References 1. Environmental Protection Department. Environment Hong Kong A Review of Hong Kong: Government Printer; Environmental Protection Department. Environment Hong Kong A Review of Hong Kong: Government Printer; Environmental Protection Department. Environment Hong Kong A Review of Hong Kong: Government Printer; Peters J, Hedley AJ, Wong CM, Lam TH, Liu J, Spiegelhalter DJ. Effects of an ambient air pollution intervention and environmental tobacco smoke on children s respiratory health in Hong Kong. Int J Epidemiol. 1996;25: Tam AY, Wong CM, Lam TH, Ong SG, Peters J, Hedley AJ. Bronchial responsiveness in children exposed to atmospheric pollution in Hong Kong. Chest. 1994;106: Ferris BG. Epidemiology Standardization Project. Am Rev Respir Dis. 1978;118: Wong TW, Yu TS, Liu JLY, Wong SL. Agreement on responses to respiratory illnesses questionnaire. Arch Dis Child. 1998;78: Ware JH, Dockery DW, Spiro A III, Speizer FE, Ferris BG Jr. Passive smoking, gas cooking, and respiratory health of children living in six cities. Am Rev Respir Dis. 1984;129: Guandolo VL, Feroli EJ, Mella GW, Weiss IP. Involuntary smoking and incidence of respiratory illness during the first year of life. Pediatrics. 1985;75: Schmitzberger R, Rhomberg K, Buchele H, et al. Effects of air pollution on the respiratory tract of children. Pediatr Pulmonol. 1993; 15: Spinaci S, Arossa W, Bugiani M, Natale P, Bucca C, Candussio G. The effects of air pollution on the respiratory health of children: a cross-sectional study. Pediatr Pulmonol. 1985; 1: Leung R, Ho P. Asthma, allergy and atopy in three south-east Asia populations. Thorax. 1994;49: Lau YL, Karlberg J. Prevalence and risk factors of children asthma, rhinitis and eczema in Hong Kong. J Paediatr Child Health. 1998;34: Katsouyanni K, Katsouyanni A, Messari I, et al. Air pollution and cause specific mortality in Athens. J Epidemiol Community Health. 1990;44: Pope CA, Dockery DW. Acute health effects of PM 10 on symptomatic and asymptomatic children. Am Rev Respir Dis. 1992;145: Roemer W, Hoek G, Brunekreef B. Acute effects of moderately elevated wintertime air pollution on respiratory health. Am Rev Respir Dis. 1993;147: Hoke G, Brunekreef B. Effects of lowlevel winter air pollution concentrations on respiratory health of Dutch children. Environ Res. 1994;64: World Health Organization. Air Quality Guidelines for Europe.Copenhagen: WHO Regional Publications; Stern BR, Raizenne ME, Burnett RT, Jones L, Kearney J, Franklin CA. Air pollution and childhood respiratory health: exposure to sulfate and ozone in 10 Canadian rural communities. Environ Res. 1994;66: Ware JH, Ferris BG, Dockery DW, Spengler JD, Stram DO, Speizer FE. Effects of ambient sulphur oxides and suspended particles on respiratory health of preadolescent children. Am Rev Respir Dis. 1986;133: Jaakkola JJK, Paunio M, Virtanen M, Heinonen OP. Low-level air pollution and upper respiratory infections in children. Am J Public Health. 1991;81: Schwartz J. Lung function and chronic exposure to air pollution: a crosssectional analysis of NHANES II. Environ Res. 1989;50: Dassen W, Hoek BG, Hofschreuder P, et al. Decline in children s pulmonary function during an air pollution episode. J Air Pollut Control Assoc. 1986;36: Arossa W, Spinci S, Bugiani M, Narale P, Bucca C, de Candussio G. Changes in lung function of children after an air pollution decrease. Arch Environ Health. 1987;42: Burrows B, Taussig LM. As the twig is bent, the tree inclines (perhaps). Am Rev Respir Dis. 1980;122: Samet JM, Tager IB, Sprizer FE. The relationship between respiratory illness in childhood and chronic airflow obstruction in adulthood. Am Rev Respir Dis. 1983;127: Cuijpers CEJ, Swaen GMH, Wesseling G, Sturmans F, Wouters EFM. Adverse effects of the indoor environment on respiratory health in primary school children. Environ Res. 1995;86: Pershagen G, Rylander E, Norberg S, Eriksson M, Nordavall SL. Air pollution involving nitrogen dioxide exposure and wheezing bronchitis in children. Int J Epidemiol. 1995;24: van Vliet P, Knape M, de Hartog J, Janssen N, Harssema H, Brunekreef B. Motor vehicle exhaust and chronic respiratory symptoms in children living near freeways. Environ Res. 1997;74: