Chronic effects of ambient air pollution on respiratory morbidities among Chinese children: a cross-sectional study in Hong Kong

Air pollution is a major environmental health risk in both developing and developed countries [1, 2]. It has been estimated that globally each year about 1.3 million premature deaths are attributed to ambient air pollution. In general, people living in less polluted cities have better respiratory and cardiovascular health and the related disease burden can be reduced by improving the ambient air quality [1]. Children are vulnerable to ambient air pollution as they spend more time outdoors, are more physically active, and have higher ventilation rates than adults. Though acute health effects on children’s respiratory morbidities from short-term exposure to air pollution have been well documented, the chronic effects from long-term exposure are still subject to debate. Two Harvard studies revealed chronic adverse effects on children’s cough and bronchitis from exposure to particulate matters (PMs) and sulphur dioxide (SO₂) [3, 4], whilst a Southern California 24-city study reported insignificant associations between PMs and SO₂ and childhood respiratory morbidities [5]. In addition, this study observed a significant association between nitrogen dioxide (NO₂) and wheezing in boys [5]. Several studies in Europe and Asia have suggested that traffic-related pollution is significantly associated with children’s asthma, allergic rhinitis, and related symptoms [6‐9]. Whilst findings from the International Study of Asthma and Allergies in Childhood (ISAAC) indicated that particulate matters than 10 μm in aerodynamic diameter (PM₁₀) was not significantly associated with asthma and rhinoconjunctivities [10].

Hong Kong is located on the coast of Southern China and has a subtropical climate. The ambient air pollution level has improved since 1990, as the result of the implementation of a series of government regulations to restrict fuel’s sulphur content. However, in recent years, progress improvement has slowed down and the air quality has deteriorated, due to the fact that the local air quality is being influenced by the regional air pollution problem of the entire Southern China [11]. Previous studies in the 1990’s have revealed significant adverse effects of ambient air pollution on respiratory morbidities among Hong Kong school children, including cough, phlegm, and asthma [12]. Decreased bronchial hyperactivity among asthmatic children was also observed after a marked reduction in ambient PM₁₀ and SO₂ concentrations [13]. In addition, a four-city study in China showed significant associations between PMs and persistent cough, persistent phlegm, and bronchitis [14]. However, no significant adverse effect was found for SO₂ and nitrogen oxides (NO_x) [14]. These Chinese studies were conducted at least a decade ago and air pollution levels at that time were relatively high. Furthermore, none of these studies considered the potential health effects of ozone (O₃), which is currently a routinely monitored air pollutant in urban China. This study primarily aims to investigate the associations between exposure to ambient air pollution and respiratory morbidities among Chinese primary school children in Hong Kong. In addition, the risks from indoor household factors for respiratory health were also examined.

A total of 3,186 children in 11 primary schools were approached and 2,641 (82.9%) participated in the study. More than 95% of the participants (n = 2,534) completed questionnaires and finally 2,203 students (1141 boys and 1062 girls) met our selection criteria and were included in data analyses. Of the 331 students who were excluded from data analysis, 93 were living in other districts (cross-district students), 149 had lived in their school’s district for less than 12 consecutive months, and 89 were below 8 or above 10 years old.

The averages of historical annual means for PM₁₀, NO₂, SO₂ and O₃ in the past decade were 48.9 μg/m³, 48.4 μg/m³, 13.4 μg/m³, 38.6 μg/m³ in LPD, 55.0 μg/m³, 71.0 μg/m³, 16.3 μg/m³, 22.9 μg/m³ in MPD, and 57.6 μg/m³, 57.6 μg/m³, 18.6 μg/m³, 25.8 μg/m³ in HPD, respectively. O₃ concentrations steadily increased over time, whilst no obvious increasing or decreasing trends were observed for the other three pollutants. PM₁₀, NO₂ and SO₂ were positively correlated with each other, with significant correlations between PM₁₀ and SO₂, and between PM₁₀ and NO₂ (r = 0.70 and 0.51 respectively, P < 0.05). O₃ was negatively correlated with the other three pollutants, and significantly correlated with PM₁₀ and NO₂ (r = −0.59 and −0.61 respectively, P < 0.05). The negative correlations for O₃ with PM₁₀ and NO₂ are due to motor vehicles, which is the major source of air pollution in Hong Kong. O₃ is readily scavenged by reactions with nitric oxide emitted from motor vehicles. In the past 12 months, the annual means for PM₁₀, NO₂, SO₂ and O₃ were 55.1 μg/m³, 51.4 μg/m³, 15.4 μg/m³, 42.5 μg/m³ in LPD, 56.3 μg/m³, 64.7 μg/m³, 15.2 μg/m³, 35.2 μg/m³ in MPD, and 63.8 μg/m³, 64.1 μg/m³, 22.2 μg/m³, 31.7 μg/m³ in HPD, respectively. Compared with the historical data, the concentrations of PM₁₀ and SO₂ in LPD, and that of NO₂ in HPD had increased in the past 12 months towards the levels monitored in MPD.

Table 1 demonstrates the comparison of the participants’ characteristics across districts after stratification by gender. Significant differences were observed in: father’s job, birth place, breastfeeding history, parental allergy, physical activity, member of team sports, playing with furry toys, household mould, pets, burning incense at home, passive smoking, and house ventilation in summer and winter, for single or both genders.

Table 2 demonstrates the prevalence of respiratory morbidities by gender and district. Few students (<6.0%) experienced wheezing symptoms, chronic cough and phlegm without colds, in the past 12 months, whilst cough at night, phlegm with colds, and sneeze with itchy-watery eyes were common (20%-32.3%). Few students were diagnosed with asthma, whilst more than 30% of them had allergic rhinitis. In addition, differences across districts reached significance in the following morbidities: cough at night in girls, sneeze with itchy-watery eyes and life-time allergic rhinitis in boys, and phlegm without colds, current and life-time allergic rhinitis in both genders.

Tables 3 and 4 present the risks of ambient air pollution for respiratory morbidities after stratification by gender and adjustment for other risk factors. Compared to those in LPD, girls in HPD were at significantly higher risk for cough at night and phlegm without colds (OR_adj. = 1.81, 95%CI = 1.17-2.78; and OR_adj. = 3.84, 95%CI = 1.78-8.47, P < 0.05), and girls in MPD were at significantly higher risk for cough at night only (OR_adj. = 1.65, 95%CI = 1.08-2.52, P < 0.05). Contrary to our hypothesis, both boys and girls in MPD were significantly less likely to have current and life-time allergic rhinitis compared to their counterparts in LPD (adjusted ORs ranged from 0.71 to 0.56, P < 0.05). In addition, boys in HPD were found to be at marginally significant higher risk for wheezing symptoms, phlegm without colds, and current and life-time asthma compared to those in LPD (adjusted ORs ranged from 1.71 to 2.82, P < 0.10). Marginal significance for elevated risk for cough at night was also found among boys in MPD (OR_adj. = 1.43, 95%CI = 0.98-2.08, P < 0.10).

In the multivariable analysis (Tables 3 and 4), age, father’s job and birth place were adjusted for in all models no matter their significance. Blue-collar job of father was significantly and negatively associated with phlegm without colds and life-time allergic rhinitis for girls (adjusted ORs ranged from 0.56 to 0.71, P < 0.05). Boys born in Hong Kong were significantly less likely to have cough at night (OR_adj. = 0.63, 95%CI = 0.40-0.98, P < 0.05), but significantly more likely to suffer from sneeze with itchy-watery eyes, and allergic rhinitis (adjusted ORs ranged from 1.80 to 2.27, P < 0.05). Parental asthma and parental allergy were risk factors for most respiratory conditions (adjusted ORs ranged from 1.89 to 5.32, P < 0.05). In terms of the other confounders, physical activity, being a member of a sports team, raising pets, and more-ventilated in summer were significantly and negatively associated with some respiratory conditions; whilst children with low birth weight, spending more time outdoors, playing with furry toys, having mould at home, new furniture, burning incense, passive smoking and more-ventilated in winter were significantly more vulnerable to some morbidities (Tables 3 and 4). It is worth noting that more-ventilated in summer seemed to be a protective factor for allergic rhinitis, and sneeze with itchy-watery eyes, whilst more-ventilated in winter had adverse effects on allergic rhinitis. In addition, being physically active was a significantly high risk factor for life-time asthma in girls.

We hypothesised that exposure to current air pollution (in the past 12 months) would have more influence on respiratory symptoms and diseases (in the past 12 months), when compared to historical exposure. Thus, the average monthly means for the air pollutants over the past 12 months allowed us to estimate the associations between some individual pollutants and current symptoms and diseases through regrouping the districts as follows: 1) LPD and MPD were combined together and then compared with HPD, as PM₁₀ in LPD and MPD were both at a low level (55.1 μg/m³ and 56.3 μg/m³ respectively); 2) MPD and HPD were combined and then compared with LPD to reflect the same high level of NO₂ in MPD and HPD (64.7 μg/m³ and 63.8 μg/m³ respectively). Significant or marginally significant adjusted ORs and their 95% CIs after regrouping are presented in Table 5. Boys in HPD were at significantly higher risk for wheezing symptoms and phlegm without colds compared to those in the combined LPD and MPD (adjusted ORs ranged from 2.03-2.76, P < 0.05), suggesting that it was PM₁₀, but not NO₂, which was mainly responsible for these adverse effects. However, both PM₁₀ and NO₂ contributed to the adverse effects on cough and phlegm in girls, as shown in Table 5 (adjusted ORs ranged from 1.71-2.87, P < 0.05). Contrary to our hypothesis, NO₂ was significantly and negatively associated with current allergic rhinitis in girls.

We conducted a cross-sectional study among 2,203 Hong Kong primary school students aged 8–10 years and uncovered certain adverse effects of ambient air pollution on respiratory symptoms and diseases. Girls living in HPD were at significantly higher risk for cough at night and phlegm without colds. Marginal significance for elevated risks was found for wheezing symptoms, phlegm without colds, and asthma in HPD boys, as well as chronic cough in HPD girls. Both genders in MPD were significantly less likely to have allergic rhinitis. Individual pollutant analysis further revealed that PM₁₀ was the major pollutant responsible for the adverse effects on wheezing and phlegm in boys, whilst both PM₁₀ and NO₂ were contributing to cough and phlegm in girls.

Our findings confirmed similar adverse effects of air pollution in several one-city cross-sectional studies in China [12, 20‐25]. Higher prevalence rates of wheezing, cough, phlegm and asthma were consistently found among children living in high pollution areas, though outcome indicators across the studies were not exactly the same. In a previous study in Hong Kong, Yu et al. revealed that children living in a high pollution district were at high risk for frequent cough, frequent phlegm and asthma, but not for wheezing, bronchitis and allergic rhinitis [12]. Marginal significance was found for high risks for chronic cough and wheezing with shortness of breath [12]. In Yu’s study, the risk of ambient air pollution was estimated without further breakdown by gender and therefore the potential gender difference in response to exposure was unclear. In addition, the air pollutants assessed in the previous study consisted of only PM₁₀, SO₂, and NO₂. The differences in the annual mean concentrations of the three pollutants between high and low pollution districts in Yu’s study were larger than those between HPD and LPD in the current study.

In this study, further individual pollutant analyses suggests that PM₁₀ was mainly responsible for the elevated risk for some respiratory morbidities in children (including wheezing for boys, cough for girls, and phlegm for both genders), whilst NO₂ could negatively affect cough and phlegm for girls only. PM₁₀ is a mixture of solid, liquid or solid and liquid particles, and a large body of chemicals within PM₁₀ (e.g. sulphates, polycyclic aromatic hydrocarbons, metals) can solely, or in combination, cause biological harm, which gives scientific support for its stronger associations with respiratory morbidities than the other pollutants observed in this study. Similar to our results, two previous cross-sectional studies in China, examining the health effects of individual pollutants, found that PMs were more responsible for the adverse effects than other pollutants [14, 26]. A four-city study in China reported a significantly adverse effect of PM₁₀ on phlegm, whilst the effects of NO_x and SO₂ were weak and insignificant [14]. A six-city study in Northern China (Liaoning Province) found that total suspended particles (TSP), NO_x and SO₂ were significantly and positively associated with cough, phlegm, and asthma in single pollutant models, whilst the adverse effects of SO₂ on all morbidities and that of NO_x on asthma decreased and were no longer significant in three-pollutant models, suggesting TSP was a stronger pollutant than the two other gaseous pollutants [26]. A meta-analysis involving four cross-sectional studies in China, examining the relationship between long-term exposure to ambient air pollution and child respiratory symptoms and diseases, indicated that an increase of per μg/m³ annual mean for PM₁₀ could increase the likelihood of respiratory morbidity by 0.44% (S.E. 0.02) [27]. It is noteworthy that, in our study, the results of the individual pollutant analysis (Table 5) should be considered cautiously, as we were unable to remove the potential effects of other pollutants from that of the individual pollutant. For instance, the combination of the two low PM₁₀ districts (LPD + MPD) also had lower levels of SO₂ compared to HPD, which limited our ability to distinguish the health effects of PM₁₀ from SO₂. Similarly, the combination of the two high NO₂ districts (MPD + HPD) was also low in O_3, if taking O₃ into consideration.

Contrary to our hypothesis, we found significantly negative associations between air pollution and allergic rhinitis. Compared to LPD, children of both genders in MPD were less likely to suffer from allergic rhinitis. After regrouping the districts, results from the further individual pollutant analysis, showed that children in the high NO₂ but low O₃ districts (MPD + HPD) were less likely to suffer from allergic rhinitis than those in the low NO₂ but high O₃ district (LPD) in girls only (Table 5). It is biologically impossible that exposure to high NO₂ could be of benefit to health. Thus, the high O₃ in LPD might have contributed to the negative associations. In our study, O₃ was negatively correlated with the three other pollutants due to the fact that background O₃ in more polluted areas can be removed through reacting with NO [11]. In line with our study, a cross-sectional study in 331,686 middle-school students in Taiwan reported that allergic rhinitis was positively associated with long-term exposure to O₃ [10]. However, other studies failed to find any chronic adverse effects of O₃ on respiratory morbidities (including allergic rhinitis) in school children [5, 28]. Unlike acute effects, the chronic effect of O₃ has not yet been well documented. One possibility is that the strong associations between PMs and respiratory morbidities in many studies may make it difficult to assess the individual role of ozone per se [2].

The gender-different responses to air pollution and greater NO₂ effects on girls observed in our study were consistent with some previous studies [29‐31], while other studies reported no gender differences [9], or greater effects of NO₂ on boys [5]. Children with fathers in blue-collar jobs in this study were less likely to suffer from phlegm without colds and allergic rhinitis, which confirmed the findings from another study in Hong Kong [12]. Children born in Hong Kong were at higher risk for allergic rhinitis, reflecting the fact that the prevalence of allergic rhinitis was higher in Hong Kong Children than those in other places of China [12, 18]. Low birth weight was a risk factor for wheezing with shortness of breath and chronic cough, which is consistent with results from a study in China [26]. Children spending more time outdoors are expected to be exposed to more air pollution, however we only found an adverse relationship with cough at night in girls. In terms of housing environmental factors, we found that mould, passive smoking, burning incense, and adding new furniture were positively associated with some respiratory morbidities, in line with the findings from many other studies around the world. A more ventilated home in winter was a risk factor, whilst a more ventilated home in summer was a protective factor for respiratory morbidities. One possibility is that ambient air pollution in winter was heavy; thus, more ventilation might increase the exposure level to ambient air pollution, and therefore increase the likelihood of respiratory morbidities. However, outdoor air quality in summer was relatively clear, and therefore good ventilation could improve the indoor air quality and reduce the risks for respiratory symptoms and diseases. Some factors in our study were observed to have opposite associations with respiratory conditions, contrary to our hypothesis, such as being a team sport member for current asthma in boys, and pet keeping for life-time asthma in girls. It is possible that asthmatic children might not join in any team sports, and families with asthmatic children might avoid keeping pets, because parents of asthmatic children in Hong Kong are well aware of these two risk factors.

This study is subject to several limitations. It is a cross-sectional study, and therefore we are unable to establish the temporal order of cause and effect. Exposure misclassification may inevitably exist and bias our findings most likely towards the null, like other studies using ambient air monitoring data as a proxy of personal exposure levels [32]. As individual exposures among children living in the same district can vary largely due to influences from diverse micro-environmental and personal factors, such as different air pollution levels at home and different physical activity levels. Though we controlled for several potential household and behavioural factors, the bias could not be entirely corrected. Recall bias may be unavoidable with self-reported retrospective data. For example, parents were more likely to recall severe respiratory conditions than mild ones, and recent episodes than older ones. Such bias may have introduced misclassification of diseases and resulted in underestimations of the adverse health effects [32]. In this study, we only recruited Chinese students, although overall less than 1% of students in Hong Kong mainstream primary schools are non-Chinese. However, our results are unable to reflect the situation of non-Chinese children in Hong Kong. The length of residual time of the participants may affect the associations between air pollution and respiratory morbidities, especially for life-time diseases. However, we did not collect such data, and therefore could not control for its influence. If students in HPD had ever lived in a less polluted district than HPD, and/or students in LPD had ever lived in a more polluted district than LPD, the health risks of air pollution in this study might have been underestimated, and vice versa. Unlike those in western countries, most families having children in Hong Kong would not prefer to move in order to create a stable environment for their children’s growth. As shown in this study, only 5.6% of the participants (149/2641) had ever moved from one district to another over the past 12 months. Thus, the confounding effect of the length of time living in an area might not be a major threat to this study. In the future, there is a need for cohort studies to confirm the associations between air pollution and children’s respiratory morbidities observed in this study. In addition, the relatively small differences in air pollution level across the three study districts limits our ability to test significant effects of air pollution on children’s respiratory morbidities. Further studies should enlarge the range of air pollutant concentrations via multi-city studies. There were only three districts in this study; we were therefore unable to distinguish health effects of individual pollutant (e.g. PM₁₀) from those of other pollutants.

In conclusion, we have confirmed certain adverse effects on child respiratory health from exposure to ambient air pollution in a Chinese urban setting. The adverse effects observed for PM₁₀ appear to be stronger than other pollutants. Girls were more vulnerable to NO₂ than boys. Our findings may be transferable to other developing countries characterized by similar air pollution patterns to China. Along with the publicity of air quality monitoring data and the introduction of PM_2.5 as a routine monitoring air pollutant in some big Chinese cities in 2012, the relatively high level of ambient air pollution and its health impact have been recently received unprecedented attentions from the Chinese public. There is an urgent call for the government to take effective actions to reduce air pollution level. Our findings provide some evidence for professionals and policy-makers to improve air quality, in particular PM₁₀ and NO₂, to protect the health of children.