Article Text

Chronic effects of ambient air pollution on lung function among Chinese children
  1. Yang Gao1,
  2. Emily Y Y Chan1,
  3. Li Ping Li2,
  4. Qi Qiang He3,
  5. Tze Wai Wong1
  1. 1School of Public Health and Primary Care, the Chinese University of Hong Kong, Hong Kong, China
  2. 2Injury Prevention Research Center, Medical College of Shantou University, Shantou, China
  3. 3School of Public Health, Wuhan University, Wuhan, China
  1. Correspondence to Professor Tze Wai Wong, School of Public Health and Primary Care, the Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China; twwong{at}cuhk.edu.hk

Abstract

Objectives To examine the association between long-term exposure to air pollution and lung function among Chinese schoolchildren in Southern China (Hong Kong).

Methods We conducted a cross-sectional study among 3168 schoolchildren (aged 8–10 years) in 3 districts in Hong Kong. Annual means of ambient PM10 (particulate matter <10 µm), SO2, NO2 and O3 from 1996 to 2003 were used to estimate the individual exposure of the subjects. Children's lung function was measured for forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), forced expiratory flow between 25% and 75% of FVC (FEF25–75) and forced expiratory flow at 75% of FVC (FEF75). Analysis of covariance was performed separately by gender to estimate the impact of air pollution on lung function, with adjustment for socioeconomic characteristics, respiratory morbidities, height and weight, physical activity level, indoor air contaminants and short-term exposure to the air pollutants.

Results After controlling for potential confounding factors, FEV1, FEF25–75 and FEF75 for boys in a high-pollution district (HPD) were significantly lower than those in a low-pollution district (LPD) by 3.0%, 7.6% and 8.4%, respectively. No significant differences were found for girls. Results from the comparison between a moderate-pollution district (MPD) and the HPD were similar. There were no differences between children in the LPD and MPD, except that a higher FEF75 was found in boys in the MPD. PM10 is the primary pollutant responsible for the lung function deficit. Asthmatic children were more vulnerable to exposure to air pollution.

Conclusions Long-term exposure to higher ambient air pollution levels was associated with lower lung function in Chinese schoolchildren, especially among boys. Adverse effects were observed on large and small airways, with a stronger effect on the latter.

  • air pollution
  • lung function
  • chronic effect

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What is already known on this topic

  • Exposure to ambient air pollution can cause diverse adverse health effects.

  • Chronic effects on children's lung function and lung growth are still not very clear.

  • Studies in China are scarce, though it is the country with the largest population and third largest land area in the world.

What this study adds

  • Our findings add to the evidence of chronic adverse effects on large and small airways in Chinese boys, but not in girls.

  • The observed effects are independent of short-term exposure.

  • Our findings suggest that there is a need of stricter air pollution control measures in China to protect lung of the children.

Background

Lung function is known as an objective measure of respiratory health and an early predictor of cardiorespiratory morbidity and mortality. The acute effects of ambient air pollution on lung function have been well documented in animal models and human chamber studies, as well as epidemiological studies such as panel studies and pollution episodes.1–3 However, the chronic effects at current ambient concentrations are still not clear.1 Children are a particularly vulnerable population because they spend more time outdoors, are more physically active and have higher ventilation rates than adults. Furthermore, children's lungs are growing and their immune systems are still immature.4

An increasing number of studies have focused on the long-term effects of ambient air pollution on children's lung function. However, the outcomes are equivocal.5–11 Baseline findings from the Children's Health Study in the USA showed several air pollutants (including PM10 (particulate matter <10 µm), PM2.5, acid vapour, NO2 and O3) were associated with lung function, with girls and those who spent more time outdoors being more vulnerable than their counterparts.5 After an 8-year follow-up, the study revealed the strongest associations were between forced expiratory volume in 1 s (FEV1) and a correlated set of pollutants, specifically, acid vapour, PM2.5 and elemental carbon, and similar effects were seen in boys and girls.6–8 However, no association with O3 was found in the study period. A 3.5-year Austrian cohort study on O3 concluded that medium-term effects (exposure for several months) on lung growth in school children were evident, while long-term effects were not associated with lung function partially due to reversibility.11 Most studies have been conducted in Western countries, and evidence in China is scarce, though it is the country with the largest population and the third largest land area in the world.12–14 Owing to differences in the ethnicity and lifestyle of children in China and Western countries, it might not be appropriate to directly apply results from overseas studies for Chinese children. In this cross-sectional study, we examined the relationship between long-term exposure to ambient air pollution and lung function among Chinese children. We studied subjects exposed to three levels of air pollution in order to test whether there would be a monotonic exposure–response relationship between air pollution and lung function. We also explored gender differences in the children's response to air pollution and adverse effects among asthmatic children.

Methods

Selection of districts and participants

The study was conducted from March to June 2004. Three districts, designated as low, moderate and high pollution, were selected based on historical data on annual mean concentrations of PM10, as it is the major pollutant in Hong Kong and existing evidence suggests that particulate matter may be the most relevant air pollutant with regard to the cause of lung function deficit from long-term exposure in children.6–8 ,14 Three to four primary schools in each district that were located within 1 km of the local air monitoring station were invited to participate into the study. The selected schools were all public schools and similar in school size, number of students, source of students, area of playgrounds and sports facilities in order to minimise differences across schools. All eligible students in grades 3 and 4 were investigated and written consents were obtained from their parents in advance. Approval was obtained from the Ethics Committees at the Chinese University of Hong Kong. The following are the selection criteria for our subjects: (1) children who had been living in their school district for more than 12 consecutive months before the study; (2) children of Chinese ethnicity; (3) children aged 8–10 years.

Data collection

Ambient air pollutants were studied for PM10, NO2, SO2 and O3, which were continuously measured in Hong Kong.14 The annual mean average in 1996–2003 and in the year prior to the study (May 2003 to April 2004) were used to estimate the lifetime and current exposure levels of the participants, respectively. Two measures of short-term exposure were also collected: one was the hourly mean average in the period 7:00 to 14:00 on the 13 test days; and the other was the 24 h means for PM10, NO2, SO2 and 8 h maximal mean for O3 on 1 day before the test. The daily mean temperature (°C) and daily mean relative humidity (%) on the test days were also retrieved as potential confounding factors.

Two self-administered questionnaires were developed based on the Children's Questionnaire of the American Thoracic Society (ATS-DLD-78-C) to collect the children's personal and household information.15 Parents reported on socioeconomic status, the child's current and past history of respiratory conditions, parental history of asthma and housing indoor environmental factors, as well as the children's birth weight, birthplace and history of breast feeding. Students reported on their gender, smoking habits, time spent outdoors, amount and type of physical activities, participation in sports teams in their schools and playing with furry toys in the past 12 months. Height (cm) and weight (kg) were measured following standard anthropometric methods. Body mass index (BMI; kg/m2) was calculated.

Forced expiratory spirograms and maximal expiratory flow-volume curves were simultaneously measured on four Vitalograph Compact Dry Spirometers according to the recommendations and cautions of the American Thoracic Society.16 Each student was measured five times with correct standing posture and at least three acceptable tests were obtained.16 Forced vital capacity (FVC), FEV1, forced expiratory flow between 25% and 75% of FVC (FEF25–75), and forced expiratory flow at 75% of FVC (FEF75) were derived from the best curve of each student. The volumes were directly read from charts at body temperature and pressure, saturated with water vapour conditions, on the presumption that the temperature was 23±2°C. Predicted FVC, FEV1 and FEF25–75 (%) were calculated from the children's height (cm) separately by gender according to reference values for Chinese children.17 R2 values of the equations ranged from 0.45 to 0.90. R2 values for boys were higher than for girls, with FVC being the highest and FEF25–75 being the lowest.

Data analysis

Data analysis was performed using SPSS for Windows V.16.0 (SPSS Inc., Chicago, Illinois, USA). One-way analysis of variance (ANOVA) and analysis of covariance (ANCOVA) were performed to compare children's lung function among the three districts with different air pollution levels before and after adjustment for potential confounders. Least significant difference was applied for pairwise comparisons. Adjusted mean and mean difference and SE values were derived. Background variables, including gender (for asthmatic children only), age, father's job and birthplace were adjusted for regardless of their significance. Other confounders were selected in a stepwise manner by a multiple linear regression model using p<0.10 and p<0.15 as entry and removal criteria, with adjustment for the background variables. Linearity was tested with scatterplots for each pair of dependant and independent variables. Suitable variable transformation was performed where there was a need. Multicollinearity among independent variables, as well as normality, linearity, homoscedasticity and independence of residuals were tested for assumptions of the linear regression models when building up the models. Tolerance was checked for multicollinearity and residuals plots were plotted for checking the other assumptions. Appropriate non-linear transformation was made where necessary. The two measures of short-term air pollutant concentrations (on and 1 day before the test) were separately selected for each outcome.

Results

Figure 1 depicts the long-term trends of pollutants in the three districts. Annual mean averages in 1996–2003 and annual means in the past year are also presented. Short-term pollutant concentrations varied from 20–94 µg/m3 for PM10, 25–97 µg/m3 for NO2, 8–82 µg/m3 for SO2 and 6–109 µg/m3 for O3. Ranges of air temperature and relative humidity were 19.7–5.1°C and 72% to 87%, respectively.

Figure 1

Annual mean concentrations of air pollutants from 1996–2004. Annual means in 2002 in the MPD were not calculated due to insufficient data. O3 measurements in the LPD only started in 1998. Annual mean averages in 1996–2003 and annual means in the past year (May 2003 to April 2004) are given in boxes. HPD, high-pollution district; LPD, low-pollution district; MPD, moderate-pollution district.

Of 3186 eligible students in 11 primary schools, 82.9% (n=2641) took part in the study. Around 90% of the participants (n=2391) completed the questionnaire survey and lung function tests. There were 331 participants with data excluded due to failure to meet our selection criteria. Finally, 2060 children were included in the data analysis (1064 boys and 996 girls). Table 1 compares the distribution of their personal and household characteristics and table 2 compares children's age, anthropometry and lung function. Boys had significant higher values for all lung function indices than girls except for FEF75. The between-group differences by district achieved significance for FEV1, FEF25–75 and FEF75 among boys, with the highest means being found in the moderate-pollution district (MPD). The measured lung function was lower than predicted values except for FVC in boys, with measured FEF25–75 being only 64.4% to 75.8% of predicted FEF25–75 in both genders. The between-group differences achieved statistical significance for predicted FEF25–75 in boys, as well as for predicted FVC and predicted FEV1 in girls.

Table 1

Characteristics of the subjects

Table 2

Distribution of age, anthropometry and lung function of the participants by gender

Table 3 presents the adjusted means and mean differences in lung function after controlling for confounders. Lung function results among boys in the high-pollution district (HPD) were significantly lower than those in the low-pollution district (LPD) and MPD by 0.048 litres (3.0%) and 0.057 litres (3.5%) for FEV1, 0.133 litres/s (7.6%) and 0.195 litres/s (10.8%) for FEF25–75, and 0.068 litres/s (8.4%) and 0.140 litres/s (15.9%) for FEF75. Differences between the LPD and MPD were insignificant except that a higher FEF75 was observed among boys in the MPD (by 0.072 litres/s or 8.9%). Girls appeared to be less influenced by air pollution exposure compared to boys and no significant differences were found among the districts. Given PM10 is the major pollutant locally, we further estimated lung function changes per unit increase of the annual means for PM10 in the three districts. The PM10 annual means of the LPD, MPD and HPD were 48.9, 55.0 and 57.6 µg/m3, respectively (figure 1). The FEV1, FEF25–75 and FEF75 of boys significantly decreased by 0.008 litres, 0.027 litres/s and 0.022 litres/s, respectively, along with a 1 µg/m3 increase of annual mean for PM10 (table 4). No significant relationship was observed for boy's FVC or for all lung function indicators of girls. The results were in line with those in table 3.

Table 3

Adjusted means (M) and mean differences (MD) for lung function by gender

Table 4

Lung function changes per unit increase of annual means for PM10 (particulate matter <10 µm; 1 µg/m3) in the study districts

In the year prior to the study, PM10 levels in the MPD were similar to that in the LPD. We therefore combined data from the LPD and MPD and compared them to that in the HPD to estimate the PM10 effects on lung function. The results were similar to our original three-district analyses. Significant deficits in FEV1, FEF25–75 and FEF75 among boys remained, but the differences were smaller (decreased by 3.2%, 9.1% and 12.3%, respectively). We also compared the results of combined data from the MPD and HPD with that in the LPD to test the NO2 effects, as the annual mean concentrations in the MPD and HPD were similar in the past year. However, no significant relationship was observed.

We compared each lung function index with adjustment for all the same covariates. The results did not change greatly from the original findings except for a marginally lower FEF25–75 among girls in the HPD compared to those in the LPD (see online supplementary data table S6). In addition, we compared predicted FVC, FEV1 and FEF25–75 by district. The results were also similar (see online supplementary data table S7). Overall, the results across different analyses were similar, suggesting that our findings are robust.

Table 5 examines the relationship between air pollution exposure and lung function among asthmatic children. Asthma prevalence in the LPD, MPD and HPD was 2.6%, 2.1% and 3.3%, respectively, and there was no significant difference across districts without or with adjustment for other confounders (data not shown). Clear exposure–response relationships were observed between air pollution levels and all lung function indices among asthmatic children. Adverse effects were higher for flow measures than volume measures and were larger when comparing the HPD to the LPD than to the MPD, with a deficit ranging from 12.2% to 58.2%. The associations observed among non-asthmatic children were similar to those among all students in terms of direction and magnitude (data not shown).

Table 5

Adjusted means/mean differences (M/MD) for lung function among asthmatic children

Discussion

This study revealed that primary-school-age boys in the HPD had significantly reduced lung function, as measured by FEV1, FEF25–75 and FEF75, when compared to those in the LPD and MPD, while the adverse effects among girls were not significant. Lung function deficits were larger for the flow measures than the volume measures and among currently asthmatic children.

Our findings support the hypothesis of adverse effects of air pollution on lung function among Chinese schoolchildren, and agree with earlier studies in Southern China.12 ,13 Yu et al12 in a cross-sectional study in Hong Kong indicated that FEV1 and FEF25–75 were significantly lower among boys in a more polluted district compared to those in a less polluted district. Decrements in FEV1 and FEF25–75 were 3.0% and 7.1%, respectively, which are of similar magnitude with our findings between the HPD and LPD. In that study, similar adverse effects were also observed among girls. A study in Guangzhou followed primary schoolchildren up for 6 months and revealed significant growth deficits in FEV1, FEF25–75 and FEF75 for boys in more polluted areas but not for girls, which is consistent with our findings and suggests that boys are more likely to be adversely affected by exposure to ambient air pollution.13 In brief, studies from Southern China including this one are generally agreement with most published overseas studies in support of our research hypothesis on outdoor air pollution and children's lung function.5–7 18–24 However, some studies failed to observe the negative associations.9 ,25

Lung function tests have been widely used in clinical practice and epidemiological studies. During the test, lung volumes below about two-thirds of maximal expiration are mainly limited by the physical factors of lower airways and lung parenchyma. The expiratory flows are typically limited by the progression of airway obstruction. Flow limitation in large airways would reduce expiratory flow rates at all lung volumes, while flow limitation in small airways would reduce flow rates at low lung volumes.26 FVC indicates the maximum volume of air exhaled from the lungs in a forced breath, FEV1 mainly reflects the mechanical properties of large airway, while FEF25–75 and FEF75 are measures more indicative of peripheral small airway functions.27 It has been suggested that small airways might receive the highest tissue doses of air pollution and undergo preclinical structural changes before the larger airways are affected.1 Our finding of larger deficits in FEF25–75 and FEF75 lends support to this hypothesis along with previous studies.12 ,13 ,21 ,22 ,24 In addition, the reduction in FEV1 also suggests the adverse effect of air pollution exposure on the development of large airways.

As in most observational studies on air pollution and health, it is difficult to distinguish the effects of individual pollutants on lung function as we only had three exposure clusters. All four pollutants probably contributed to the adverse effects observed among boys in the HPD. Our analyses after combining the districts with similar PM10 and NO2 levels respectively revealed significant deficits in FEV1, FEF25–75 and FEF75 among boys living in the high-PM10 district (the HPD) compared to those in the low-PM10 districts (combination of the MPD and LPD), but no relationship with NO2. In addition, there was a monotonic exposure–response relationship between PM10 and lung function among the asthmatic children, who are more vulnerable than general children (table 5). The results collectively support our hypothesis that PM10 is the most relevant pollutant impacting on lung function. However, we failed to observe a monotonic relationship between PM10 concentration level and lung function. The MPD and not LPD showed the highest lung function figures for boys, though the differences between the two districts did not reach statistical significance (table 3). It is possible that the higher O3 concentrations in the LPD may also have adverse effects on lung function, especially on the small airways as reflected by table 3, and therefore attenuate the favourable effects of low PM10 exposure level. In addition, PM10 annual means in the MPD were even higher than the HPD in the initial 2 years of the study, but decreased against the time and at last became similarly low with the LPD. Our observation suggests that the relatively higher exposure to PM10 in the early years may have had not much impact on the children's current lung function or the impact, if it existed, may have been caught up with later on when the exposure level was lowered, as observed in previous studies.1

We observed gender differences in the adverse effects of air pollution on lung function, with boys being more vulnerable to exposure. In this study, boys were exposed to outdoor air pollution for a longer time than girls. The average mean time spent outdoors in boys was 0.9 h/week higher than in girls (13.7 h/week vs 12.8 h/week, p=0.011). A higher proportion of boys were physically active (39.2% vs 34.8%, p=0.047), which could result in the exposure to higher doses of air pollutants by boys than girls. It is reasonable to assume that spending more time outdoors and being more physically active collectively contributed to our observation of a strong link between air pollution and lung function in boys. Consistent with our findings, He et al13 reported a similar pattern. An 8-year cohort study in the USA also observed a larger freeway effect in boys than in girls.23 In contrast, some studies found girls more vulnerable.5 There are also other studies showing no gender difference.8 Thus, the effects of gender as a modifier on the association between air pollution and lung function are still not clear.

In this study, several potential confounding factors related to lung function or exposure level were studied. We did not find significant influences from socioeconomic status on lung function. Low birth weight and having been breast fed could not explain our outcomes, except breast feeding appeared to have a favourable effect on lung function among asthmatic children. Wheezing, asthma and lifetime bronchitis were negatively associated with some lung function indices, while being physically active appears to benefit lung function in girls only. Several household environmental factors were also examined. Burning incense and passive smoking at home had adverse effects in girls but not in boys, suggesting that girls were more exposed to indoor air pollution. Short-term exposure to ambient air pollution could also play a role in adverse effects on lung function. We found that the 24 h mean concentration of SO2 on the day prior to the test was significantly associated with most lung function indices for both sexes.

The following are limitations of our study. First, we could not establish the temporal order of cause and effect because of the cross-sectional study design. Moreover, ambient air pollutant concentrations were used as a proxy of individual exposure, which could result in exposure misclassification. Although lung function tests have been widely used in epidemiological studies, the results are highly dependent on the subjective efforts of the subjects. Several attempts were made during the test to minimise potential measurement bias. All tests were performed in the morning at school to avoid circadian variation. Each spirometer was operated by the same trained investigator throughout the whole study and calibration was undertaken before and after each test day. In addition, all students were briefed in detail and had observed demonstrations of how to perform the test before being tested. They were also asked to keep the standard body and head position and received verbal encouragement during the test. The lack of post-bronchodilator lung function is a limitation as it would provide more information regarding whether the pollution related effect on lung function was reversible or not.28 ,29 In future studies, we would include this important measure so that we can assess the possible reversibility of lung function impairment.

In conclusion, we found that long-term exposure to higher ambient air pollution levels was associated with lower lung function in Chinese schoolchildren, especially among boys. Adverse effects were observed on large and small airways, with a stronger effect on the latter. This inverse relationship was independent of short-term exposure to air pollution. Our study provides evidence to support stricter air pollution control measures in Hong Kong and China to protect the lungs of children. A cohort study with a long follow-up period would provide better insight on the effects of air pollution on the rate of lung growth in children, and on the gender-different responses to exposure.

Acknowledgments

We are very grateful to the students, their parents, the teachers in the participating schools and all of the field investigators. Special thanks to Professor Wing Kin Gary Wong, Department of Paediatrics, The Chinese University of Hong Kong, for providing us valuable comments in revisions.

References

Supplementary materials

  • Supplementary Data

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Footnotes

  • Contributors YG designed the study, conducted the survey, performed the data analysis and wrote up the manuscript. EYYC participated in writing up the manuscript and revised it. LPL and QQH revised the manuscript. TWW led and supervised the study and revised the manuscript.

  • Funding None.

  • Competing interests None.

  • Provenance and peer review Not commissioned; externally peer reviewed.