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The association between ambient air pollution control and stroke mortality during the 2010 Asian Games in Guangzhou, China
Atmospheric Environment 217 (2019) 116965
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The association between ambient air pollution control and stroke mortality during the 2010 Asian Games in Guangzhou, China
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Shiyu Zhanga, Jiayun Lvb, Ruilin Mengc, Yin Yanga, Bipin Kumar Acharyaa, Xiangyan Suna, Hualiang Lina, Qiansheng Hud,∗∗, Zengliang Ruana,∗ a
Department of Epidemiology, School of Public Health, Sun Yat-Sen University, Guangzhou, 510080, China Guangzhou Center for Disease Control and Prevention, Guangzhou, 510440, China c Guangdong Provincial Center for Disease Control and Prevention, Guangzhou, 511430, China d Department of Occupational and Environmental Health, School of Public Health, Sun Yat-Sen University, Guangzhou, 510080, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Air pollution Particulate matter Ischemic Hemorrhagic Stroke mortality
Although ambient air pollution has been consistently associated with morbidity and mortality of stroke, there is limited evidence on whether the control of air pollution would associate with a reduced risk of stroke. The citywide air pollution controlling measures during the 2010 Asian Games in Guangzhou provided such an opportunity to answer this question. We collected daily data on the concentrations of air pollutants and mortality from ischemic and hemorrhagic stroke, and compared them for 51 intervention days in 2010 with the corresponding days in 2006–2009 and 2011 (reference period). Poisson-based interrupted time series analysis was employed to estimate the relative risk (RR) and 95% confidence interval (CI). The daily mean concentrations of PM10 (particles with an aerodynamic diameter smaller than 10 μm) was 88.64 μg/m3 during the reference period, and 80.47 μg/m3 during the intervention period. Daily mortality number of total stroke, ischemic and hemorrhagic stroke decreased from 3.67, 2.00 and 1.67 during the reference period, to 3.00, 1.76 and 1.24 during the intervention period; the corresponding RR was 0.79 (95% CI: 0.66–0.94), 0.87 (95% CI: 0.69–1.11) and 0.69 (95% CI: 0.52–0.91), respectively. Our findings show that ambient air pollution controlling measures during the 2010 Asian Games in Guangzhou were associated with a decreased risk of stroke mortality, which suggests a need to reduce air pollution to improve public health.
1. Introduction Stroke is one of the major causes of death and disability in both developing and developed countries (Cabral Norberto et al., 2017; Giroud et al., 2017). The World Health Organization estimated that there were about 25.7 million stroke cases worldwide in 2013, resulting in 6.5 million deaths (Feigin et al., 2017). About 87% of these deaths occurred in low- and middle-income countries (Strong et al., 2007). In China, stroke accounted for about 19% of the total mortality, making it the leading cause of adult disability and the second leading cause of death (Jia et al., 2010; Ning et al., 2017). Thus, it is worthwhile to investigate the determinants of stroke to improve the health level and to prolong the life expectancy for people around the world. In addition to a number of well-recognized hazard factors, such as smoking, hypertension, high cholesterol levels, and diabetes, air
pollution is one of the most frequently mentioned risk factors for stroke (Lin et al., 2017a; Liu et al., 2017a, 2017b). Recent studies in North America, Europe, and Asia have provided evidence of the short-term effect of air pollutants on stroke mortality and hospital admissions (Gutiérrez-Avila et al., 2018; Liu et al., 2017a; Wang et al., 2018; Wilker Elissa et al., 2018). The increasing evidence on the correlation between air pollutants and stroke morbidity and mortality highlighted the necessity of an effective control measure to mitigate the air pollution (Lin et al., 2014). However, questions remain about the effects of air pollution controlling measures on stroke (Bubb et al., 2009). And the opportunity to investigate the health benefits of an air pollution control program is still quite rare. Some examples have been illustrated in previous studies. For example, Friedman et al. examined the effect of air pollution control
∗
Corresponding author. Department of Epidemiology, School of Public Health, Sun Yat-Sen University, No. 74 Zhongshan Road 2, Guangzhou, 510080, China. Corresponding author. Department of Occupational and Environmental Health, School of Public Health, Sun Yat-Sen University, No. 74 Zhongshan Road 2, Guangzhou, 510080, China. E-mail addresses: [email protected] (Q. Hu), [email protected] (Z. Ruan). ∗∗
https://doi.org/10.1016/j.atmosenv.2019.116965 Received 18 January 2019; Received in revised form 26 August 2019; Accepted 5 September 2019 Available online 06 September 2019 1352-2310/ © 2019 Elsevier Ltd. All rights reserved.
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these districts were of high quality (Yu et al., 2012).
measures on asthma hospitalization during the 1996 Summer Olympics in Atlanta, United States (Friedman et al., 2001), when about 30% of the vehicle exhaust and its related pollutants were reduced by transportation control, there was a 40% decrease in acute asthma attacks and Medicaid claims, together with a reduction of 19% pediatric emergency admissions (Friedman et al., 2001). Comprehensive air quality improvement policy was also implemented during the 2008 Summer Olympic Games in Beijing, which was found to have significant beneficial effects on asthma outpatient visits (Li et al., 2011) and heart function in young healthy adults (Wu et al., 2010). Beneficial effect was also proved for the asthma morbidity of children during the 2002 Asian Games, which was celebrated in Busan, Korea (Lee et al., 2007). Although the health benefits of air pollution control measures were observed in above-mentioned studies, no study has specifically examined whether the risk of stroke decreased after such air pollution mitigation programs. The 16th Asian Games was hold in the Chinese city of Guangzhou in 2010. The government of Guangzhou made a great effort to enhance the air quality (Tao et al., 2015). From November 1 to December 21, a series of policies, such as the control of transportation and industrial emission, were implemented for 51 days; under these policies, the heavy trucks were not permitted to drive into the city, and other vehicles could only be driven on alternate days (Tao et al., 2015). Therefore, it provided us a golden opportunity to evaluate the association of air pollution control on stroke mortality. The current study aimed to examine whether there was any reduction in stroke mortality count following the policies of air pollution control during the 2010 Guangzhou Asian Games.
2.2. Data collection Daily stroke deaths were obtained from the Guangzhou Center for Disease Control and Prevention. We collected information on the date and cause of death, age at death, and the deceased's sex. The ischemic and hemorrhagic stroke deaths were coded in the format of International Classification of Diseases revision 10 (ICD 10, I63–I67 and I60–I62, respectively). The daily data on levels of air pollutants between January 1, 2006 and December 21, 2011 were obtained from the Guangdong Environmental Monitoring Center. The Center, which reported daily to China National Environmental Monitoring Centre, is part of a nationwide air monitoring networks. There are three general monitoring sites located in our study area, and data of air pollutants from these monitoring sites were averaged for the present analysis. These stations measure the concentrations of several air pollutants, included particulate matter with an aerodynamic diameter smaller than 10 μm (PM10), sulfur dioxide (SO2), and nitrogen dioxide (NO2). Additionally, meteorological data including relative humidity and daily mean temperature for the same period were obtained from the Meteorological Observation Station of Guangzhou. 2.3. Statistical analysis To evaluate the health benefits of the intervention, two approaches were frequently adopted in previous studies. For one thing, they compared the incidence of a disease during the intervention with that of prior to and after the intervention (Friedman et al., 2001; Li et al., 2010), which was usually confounded by the seasonal trend of incidence rate. For another, they compared the incidence of a disease during the intervention with the same calendar date of other years, which was vulnerable to the long-term trend of the incidence rate. However, additional analyses can be performed for other diseases that should not be impacted by air pollution, or the same disease in other days which was different from the intervention dates. One study suggested another strategy to include a "control” city, which had similarities in geographical and meteorological characteristics with the intervention city but was not affected by such intervention (Sargent et al., 2004). In addition, the reason for the change in stroke mortality count during the Games period could not only be the intervention, but also the inter-annual or long-term mortality variations. However, if the mortality count of the control city remained its consistency during the intervention, we could infer that it was not affected by those variations, and if the same pattern of change also occurs in the control areas, it could not simply be attributed to the intervention.
2. Methods 2.1. Study settings Guangzhou, a city located in the South of China, is the capital city of Guangdong Province. It is in the subtropical zone of humid-monsoon climate with an annual average rainfall of 1500–2000 mm, and its annual average temperature is 22 °C. In 2010, Guangzhou has a population of about 12.7 million permanent residents. In recent years, particulate air pollutants has become a major public health problem in Guangzhou (Jahn et al., 2011). The residents of Yuexiu and Liwan Districts of Guangzhou were chosen as the subjects of our study (Fig. 1). These two districts have a total of 1.9 million permanent residents and cover an area of 92.9 square kilometers. They were selected because of the following reasons. First, daily data of the levels of air pollutants collected from three monitoring sites in these districts were available for analysis. Second, dwellers in these districts were mainly the permanent residents. Moreover, in the light of a previous study, the mortality count data in
Fig. 1. Geographical location of the study areas in China. 2
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In the present study, we compared the daily stroke mortality count, air pollution level and meteorological factors during the intervention days in 2010 with the same calendar dates of 2006–2009 and 2011. The Student's t-test was applied to examine the statistical differences. We used interrupted time-series analysis based on Poisson regression to estimate the associations between air control measures from November 1 to December 21 (51 days) around the 2010 Asian Game period and stroke mortality counts (Bernal et al., 2016). To be specific, the dichotomous study group (intervention or reference) was used as the independent variable, while daily stroke mortality count (continuous number) was used as the dependent variable in this model. We calculated the crude and adjusted relative risk (RR) and its 95% confidence interval (CI) of mortalities from the total stroke, ischemic and hemorrhagic stroke during the intervention, in comparing with the reference period. In the adjusted model, several potential confounders were considered, included daily mean temperature and relative humidity, public holidays, and day of week. The formula for calculation could be specified as follows: The formula for calculation could be specified as follows:
Table 1 Daily stroke mortality count, concentrations of air pollutants and weather characteristics during the 2010 Guangzhou Asian Games (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period). Variables
Mean (SD) Reference period
Stroke mortality count (mean number of deaths Total stroke 3.67 (2.07) Ischemic stroke 2.00 (1.49) Hemorrhagic stroke 1.67 (1.43) Pollutants (μg/m3) PM10 88.64 (43.23) NO2 66.44 (31.79) SO2 34.61 (27.23) Weather Temperature (°C) 18.46 (3.92) Humidity (%) 63.74 (15.15)
% change Intervention period per day) 3.00 (1.43) 1.76 (1.17) 1.24 (0.96)
−18.26 −12.00 −25.75
80.47 (24.12) 64.27 (19.91) 33.15 (16.67)
−9.22 −3.27 −4.22
18.82 (3.47) 62.22 (12.10)
+1.95 −2.38
The minus sign (−) means the number in intervention period were less than the reference period, while the plus sign (+) means the number in intervention period were more than the reference period. Abbreviations: SD = standard deviation; PM10 = particulate matter with an aerodynamic diameter less than or equal to 10 μm; NO2 = nitrogen dioxide; SO2 = sulfur dioxide.
Log(ut ) = α + game + DOW + Holiday + COVs In the formula, μt was the total number of daily stroke mortality counts; game referred to a binary variable that was coded as 0 for reference days and 1 for the intervention days; DOW denoted day of week; Holiday was defined as a binary variable that was coded as 0 for work days and 1 for public holidays; and COVs indicated the other potential confounders as we mentioned above. In order to provide further evidence to support the hypothesis that the reason of change in stroke mortality count was not the inter-annual or long-term mortality variation, we further conducted a series of additional analyses. First, we compared the daily PM10 concentration, stroke mortality count from January to October (the non-intervention months) of 2010 (the year of Guangzhou Asian Games) and the corresponding months during the reference years of 2006–2009 and 2011. Second, the difference in mortality counts of non-respiratory cancers between the 2010 Guangzhou Asian Games period (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period) were also analyzed. Third, we compared the daily stroke mortality count during the 2010 Guangzhou Asian Games (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period) in a control city of Wuhua. This city was selected as the “control” city because of that, it was not impacted by the air pollution control of Guangzhou, and its data on mortality count were of high quality. Additionally, we examined the dose-response associations between three ambient air pollutants (PM10, SO2 and NO2) and stroke mortality counts by using the natural spline smoothing function. All the statistical analyses of this study were performed using the “mgcv” package in R version 3.5.1 (R Foundation for Statistical Computing, Vienna, Austria). We summarized the estimates of results as RR (95% CI) in daily stroke mortality count.
than expected. Fig. 3 displayed the daily concentration of each of the three measured air pollutants (PM10, SO2 and NO2) during the intervention and reference period. It reflects a significant decrease in daily PM10 level, and daily variation of all the three pollutants during the intervention were smaller. The daily mean PM10 level during the intervention was 80.47 μg/m3, about 9.22% lower that reference period. There were moderate decreases of 3.27% and 4.22% in SO2 and NO2 concentrations, and no significant change was observed for meteorological factors (Table 1). Table 2 showed the RR (95% CI) by age group, sex and stroke type. There were significant decreases in the risk of total stroke mortality count during intervention for those aged above 65 years, males and hemorrhagic stroke in Guangzhou. The same pattern of findings was replicated after the adjustment of potential confounders in the multivariate models, and the RR were 0.77 (95% CI: 0.63–0.94) for those above 65 years of age, and 0.75 (95% CI: 0.58–0.97) for males. The largest association was observed for hemorrhagic stroke, with the RR being 0.69 (95% CI: 0.52–0.91). There was no significant change in the risk of total stroke mortality count among the young population, females and ischemic stroke mortality count. In our additional analyses, we compared the differences in daily stroke mortality count from January to October (the non-intervention months) of 2010 (the year of Guangzhou Asian Games) and the corresponding months during the reference years of 2006–2009 and 2011, which did not show significant difference, although the concentration of ambient PM10 was slightly increased by 6.73% (Table s1). Moreover, no significant difference was observed for the daily stroke mortality count in the control city of Wuhua (Figure s1) during the 2010 Guangzhou Asian Games (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period) (Table s2). Furthermore, the number of mortality due to non-respiratory cancers during the 2010 Guangzhou Asian Games (intervention period) was 8.79 (3.34), which was not significantly differ from the corresponding dates during 2006–2009 and 2011 (reference period) of 8.72 (3.12). In addition, the dose-response curves suggested that the concentrations of PM2.5, SO2 and NO2 are positively associated with stroke mortality counts (Figure s2). All these findings from supported our results that the reduction in stroke mortality count could not be attributed to long term or inter-annual variation.
3. Results Table 1 shows the daily stroke mortality count, concentrations of air pollutants and weather characteristics during the period of 2010 Guangzhou Asian Games (intervention period) and the same calendar dates during 2006–2009 and 2011 (reference period). Daily stroke mortality count was decreased from 3.67 during the reference period to 3.00 during the intervention period, with a 18.26% reduction (Table 1, Fig. 2). The daily ischemic stroke mortality count and hemorrhagic stroke mortality count decreased from 2.00 to 1.67 during the reference period to 1.76 and 1.24 during the intervention, corresponding to the overall decreases of 12.00% and 25.75%. Based on the reference averages, this equated to 0.67, 0.24 and 0.43 fewer daily deaths from total stroke, ischemic and hemorrhagic stroke during the intervention 3
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Fig. 2. Time series of daily stroke mortality count during the study periods in Guangzhou.
Fig. 3. Time series of daily concentrations of air pollutants during the study periods in Guangzhou. Abbreviations: PM10 = particulate matter with an aerodynamic diameter smaller than or equal to 10 μm; NO2 = nitrogen dioxide; SO2 = sulfur dioxide.
4. Discussion
organizing multi-sport events, such as the Asian Games, as well as the Olympic Games(Li et al., 2010; Rich et al., 2012). In the past decades, evidence has been accumulated on the association of particulate air pollution and the risk of stroke. Our findings support the previous literatures and also suggested that diminished particulate air pollution was associated with a reduced risk of stroke mortality, particularly the hemorrhagic stroke mortality. Our findings indicated that, by reducing air pollution through the citywide control of
Air pollution control programs have been employed in a number of countries by different approaches such as fuel replacement and emission control (Lee et al., 2007; Lin et al., 2017b). Assessment of the association of air quality regulations has been increasingly regarded necessary for the policy making process of a responsible government. This is of particular importance for the strategy of air control when 4
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ischemic stroke. Moreover, previous findings have displayed that meteorological characteristics could change the pattern of particulate air pollution pattern and might be an important trigger of stroke risk (Piver et al., 1999). For example, wind speed could affect the dispersion of the particles in the air, and moisture levels, especially the relative humidity, were strongly associated with the atmospheric PM concentrations (Rigby and Toumi, 2008). Therefore, we can concluded that the characteristics of meteorological factors could affect human exposure to particulate air pollution (Leitte and Petrescu, 2009). Previous study have found that about 20–50% of PM variability can be explained by the variability of meteorological factors(Sui et al., 2007). Thus, it was significant to include meteorological conditions when analyzing the impacts of air pollution on human health. The underlying reason for the reduction of stroke mortality count in our study remained unclear. Previous studies have found that the inhalation of particulate pollutants could cause and aggravated both systemic inflammation and oxidative stress, in which might lead to autonomic dysfunction, atherosclerosis, as well as direct vascular injury (Dockery and Stone, 2007). Small particles even able to escape from the process of phagocytosis by alveolar macrophages and enter pulmonary interstitial sites, including vascular endothelium. As a result, they may cause inflammation at both epithelial and interstitial tissues, or even enter the circulation, so that it can reach further target sites, including the cardiovascular system, and thus promote the progression of atherosclerosis and precipitate the acute cardiovascular responses (Nemmar et al., 2004). There were several shortcomings in our study. To begin with, our study was ecological in design, so we could not consider the exposure in the individual level. Second, the intervention period was relatively short, and data on other air pollutants were limited (e.g., PM2.5, ozone and carbon monoxide). These factors restricted the statistical power of our study and made it difficult to make a causal inference. Third, some potential confounders which may affect the risk of stroke mortality during the reference and intervention periods were not considered in our study. For example, some people may come to the study areas during the Games and thus significantly increase the population and deaths. So we designed our plan to use the stroke mortality count data of the permanent residents only; and the deceased occurred inside the study area were reported back to their home town (Yu et al., 2012), thus this would not affect our result substantially. There were other conditions might have contributed to the decrease of the stroke mortality count, such as the medical treatment and dietary style. However, no major breakthroughs in medical interventions were concomitantly occurred with the air control program during the Games, so it was unlikely to be a problem.
Table 2 Crude and adjusted RRs of stroke mortality during the 2010 Guangzhou Asian Games (intervention period) compared with the corresponding dates during 2006–2009 and 2011 (reference period).
Age All ages 0-65 > 65 Sex Male Female Stroke type Ischemic Hemorrhagic
Crude RR (95% CI)
P-value
Adjusted RRa (95% CI)
P-value
0.82 (0.69, 0.97) 0.91 (0.61, 1.37) 0.80 (0.66, 0.97)
0.02 0.66 0.02
0.79 (0.66, 0.94) 0.89 (0.58, 1.35) 0.77 (0.63, 0.94)
0.01 0.57 0.01
0.78 (0.61, 0.99) 0.86 (0.67, 1.10)
0.04 0.24
0.75 (0.58, 0.97) 0.83 (0.64, 1.07)
0.03 0.15
0.88 (0.70, 1.10) 0.74 (0.57, 0.97)
0.26 0.03
0.87 (0.69, 1.11) 0.69 (0.52, 0.91)
0.26 0.01
Abbreviations: RR = relative risk; CI = confidence interval. a Time-series Poisson regression model with adjustment of day of week, public holidays, daily mean temperature, and relative humidity.
industrial emission and transportation, a lot of stroke deaths could be avoided. Our finding was in accordance with previous researches, although the key air pollutants and the health outcomes were different (Clancy et al., 2002; Hedley et al., 2002). Of the potential causes related to the decrease of stroke mortality count, air pollution was the most likely one. In the study area, background contamination, vehicle exhaust, power generation plants and industrial emissions were the main sources of ambient air pollutants (Yu et al., 2012). There were more small particulate matters, nitrogen oxides and carbon monoxide emitted from vehicle emissions than nonvehicle sources (Friedman et al., 2001). We observed a large and significant reduction in PM10 level, and to a lesser extent, SO2 and NO2 levels. The relatively smaller decrease in NO2 level was beyond our expectation, and the underlying mechanisms remained unknown. There was a 35% reduction in PM10 concentration after controlling the industrial emission and transportation during the 2008 Beijing Olympics, which was higher than that observed in the present study (Wang et al., 2009), this might because of that the control measures were more tight in Beijing. In our study areas, all the concentrations of pollutants were above the National Air Quality Standard, which suggests to be harmful to the general population. Thus, it was possible that a significant reduction in the risk of stroke mortality occurred after a 9.22% decrease in the level of PM10 in our study. It was also plausible that there were larger percentages of decrease in finer particles, such as PM2.5 and PM1, which were more harmful to human health, and were more likely to be affected by the air pollution control (Li et al., 2012). There was a study estimated that the levels of PM2.5 might have been decreased by about 17.1% during the 2010 Guangzhou Asian Games (Liu et al., 2013). Furthermore, the measures taken to control air pollution might have altered the particles’ chemical composition and toxicity. We found that the decrease in hemorrhagic stroke mortality count took up a large slice of the stroke mortality count reduction, suggesting that the particulate pollutants in ambient air might be more closely related to hemorrhagic stroke than ischemic stroke, this observation was in line with one of our recent study differentiating the adverse effects of air pollutants on hemorrhagic stroke and ischemic stroke in Guangzhou (Lin et al., 2016). The less significant association with ischemic stroke has also been reported in previous studies, for example, one case-crossover study found a closer association between air pollution and hemorrhagic stroke hospital admission than ischemic stroke risk Kaohsiung, Taiwan (Tsai et al., 2003). Moreover, there were two cohort studies (Nafstad et al., 2004; Yorifuji et al., 2010), one case–control study (Oudin et al., 2009) and one ecological study (Maheswaran et al., 2011) which did not find any significant association of ischemic stroke with ambient particulate air pollution. However, inconsistent finding has also been observed in other studies (Lisabeth et al., 2008), which found a stronger impact of air pollutants on
5. Conclusions We found that the daily air pollution levels and stroke mortality count were decreased significantly during the 2010 Guangzhou Asian Games period, but no significant change was observed for meteorological factors. Moreover, the program of air pollution control was associated with a decreased stroke mortality count, especially the hemorrhagic stroke mortality. Our findings support the idea to decrease air pollution through the restriction of transportation and industrial emission to improve public health.
Ethics statement Data were collected as part of government mandated health surveillance and analyzed anonymously, so ethical approval was not needed.
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Declaration of competing interest
Stamatakis, K.A., Qian, Z., Ma, W., 2017b. Mortality benefits of vigorous air quality improvement interventions during the periods of APEC Blue and Parade Blue in Beijing, China. Environ. Pollut. 220, 222–227. Lin, H., Tao, J., Du, Y., Liu, T., Qian, Z., Tian, L., Di, Q., Zeng, W., Xiao, J., Guo, L., Li, X., Xu, Y., Ma, W., 2016. Differentiating the effects of characteristics of PM pollution on mortality from ischemic and hemorrhagic strokes. Int. J. Hyg Environ. Health 219, 204–211. Lin, H., Zhang, Y., Liu, T., Xiao, J., Xu, Y., Xu, X., Qian, Z., Tong, S., Luo, Y., Zeng, W., Ma, W.J., 2014. Mortality reduction following the air pollution control measures during the 2010 Asian Games. Atmos. Environ. 91, 24–31. Lisabeth, L.D., Escobar, J.D., Dvonch, J.T., Sanchez, B.N., Majersik, J.J., Brown, D.L., Smith, M.A., Morgenstern, L.B., 2008. Ambient air pollution and risk for ischemic stroke and transient ischemic attack. Ann. Neurol. 64, 53–59. Liu, H., Tian, Y., Xu, Y., Huang, Z., Huang, C., Hu, Y., Zhang, J., 2017a. Association between ambient air pollution and hospitalization for ischemic and hemorrhagic stroke in China: a multicity case-crossover study. Environ. Pollut. 230, 234–241. Liu, H., Tian, Y., Xu, Y., Zhang, J., 2017b. Ambient particulate matter concentrations and hospitalization for stroke in 26 Chinese cities. Stroke 48, 2052–2059. Liu, H., Wang, X., Zhang, J., He, K., Wu, Y., Xu, J., 2013. Emission controls and changes in air quality in Guangzhou during the Asian Games. Atmos. Environ. 76, 81–93. Maheswaran, R., Pearson, T., Smeeton, N.C., Beevers, S.D., Campbell, M.J., Wolfe, C.D., 2011. Outdoor air pollution and incidence of ischemic and hemorrhagic stroke. Stroke 43, 22–27. Nafstad, P., Håheim, L.L., Wisløff, T., Gram, F., Oftedal, B., Holme, I., Hjermann, I., Leren, P., 2004. Urban air pollution and mortality in a cohort of Norwegian men. Environ. Health Perspect. 112, 610. Nemmar, A., Hoylaerts, M.F., Hoet, P.H.M., Nemery, B., 2004. Possible mechanisms of the cardiovascular effects of inhaled particles: systemic translocation and prothrombotic effects. Toxicol. Lett. 149, 243–253. Ning, X., Sun, J., Jiang, R., Lu, H., Bai, L., Shi, M., Tu, J., Wu, Y., Wang, J., Zhang, J., 2017. Increased stroke burdens among the low-income young and middle aged in rural China. Stroke 48, 77–83. Oudin, A., Stroh, E., Strömberg, U., Jakobsson, K., Björk, J., 2009. Long-term exposure to air pollution and hospital admissions for ischemic stroke. A register-based casecontrol study using modelled NOx as exposure proxy. BMC Public Health 9, 301. Piver, W.T., Ando, M., Ye, F., Portier, C.J., 1999. Temperature and air pollution as risk factors for heat stroke in Tokyo, July and August 1980-1995. Environ. Health Perspect. 107, 911. Rich, D.Q., Kipen, H.M., Huang, W., Wang, G., Wang, Y., Zhu, P., Ohman Strickland, P., Hu, M., Philipp, C., Diehl, S.R., 2012. Association between changes in air pollution levels during the Beijing Olympics and biomarkers of inflammation and thrombosis in healthy young adults. J. Am. Med. Assoc. 307, 2068–2078. Rigby, M., Toumi, R., 2008. London air pollution climatology: indirect evidence for urban boundary layer height and wind speed enhancement. Atmos. Environ. 42, 4932–4947. Sargent, R.P., Shepard, R.M., Glantz, S.A., 2004. Reduced incidence of admissions for myocardial infarction associated with public smoking ban: before and after study. BMJ 328, 977. Strong, K., Mathers, C., Bonita, R., 2007. Preventing stroke: saving lives around the world. Lancet Neurol. 6, 182–187. Sui, K.k.W., Yang, J., Xie, F., Zhao, Y., 2007. Beijing persistent PM10 pollution and its relationship with general meteorological features. Res. Environ. Sci. 20, 77–83. Tao, J., Zhang, L., Zhang, Z., Huang, R., Wu, Y., Zhang, R., Cao, J., Zhang, Y., 2015. Control of PM2.5 in Guangzhou during the 16th asian Games period: implication for hazy weather prevention. Sci. Total Environ. 508, 57–66. Tsai, S.S., Goggins, W.B., Chiu, H.F., Yang, C.Y., 2003. Evidence for an association between air pollution and daily stroke admissions in Kaohsiung, Taiwan. Stroke 34, 2612–2616. Wang, W., Primbs, T., Tao, S., Simonich, S.L.M., 2009. Atmospheric particulate matter pollution during the 2008 Beijing Olympics. Environ. Sci. Technol. 43, 5314–5320. Wang, X., Qian, Z., Wang, X., Hong, H., Yang, Y., Xu, Y., Xu, X., Yao, Z., Zhang, L., Rolling, C.A., Schootman, M., Liu, T., Xiao, J., Li, X., Zeng, W., Ma, W., Lin, H., 2018. Estimating the acute effects of fine and coarse particle pollution on stroke mortality of in six Chinese subtropical cities. Environ. Pollut. 239, 812–817. Wilker Elissa, H., Mostofsky, E., Fossa, A., Koutrakis, P., Warren, A., Charidimou, A., Mittleman Murray, A., Viswanathan, A., 2018. Ambient pollutants and spontaneous intracerebral hemorrhage in greater boston. Stroke 0, 2764–2766. Wu, S., Deng, F., Niu, J., Huang, Q., Liu, Y., Guo, X., 2010. Association of heart rate variability in taxi drivers with marked changes in particulate air pollution in Beijing in 2008. Environ. Health Perspect. 118, 87. Yorifuji, T., Kashima, S., Tsuda, T., Takao, S., Suzuki, E., Doi, H., Sugiyama, M., Ishikawa Takata, K., Ohta, T., 2010. Long-term exposure to traffic-related air pollution and mortality in Shizuoka, Japan. Occup. Environ. Med. 67, 111–117. Yu, I.T.S., Zhang, Y.H., San Tam, W.W., Yan, Q.H., Xu, Y.J., Xun, X.J., Wu, W., Ma, W.J., Tian, L.W., Tse, L.A., Lao, X.Q., 2012. Effect of ambient air pollution on daily mortality rates in Guangzhou, China. Atmos. Environ. 46, 528–535.
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This work was supported by the National Key R&D Program of China (2018YFA0606200) and the Natural Science Foundation of China (81972993). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.atmosenv.2019.116965. References Bernal, J.L., Cummins, S., Gasparrini, A., 2016. Interrupted time series regression for the evaluation of public health interventions: a tutorial. Int. J. Epidemiol. 46, 348–355. Bubb, M.R., Lipfert, F.W., Pope III, C.A., Ezzati, M., Dockery, D.W., 2009. Air pollution and life expectancy. N. Engl. J. Med. 360, 2032–2034. Cabral Norberto, L., Freire Aracélli, T., Conforto Adriana, B., dos Santos, N., Reis Felipe, I., Nagel, V., Guesser Vanessa, V., Safanelli, J., Longo Alexandre, L., 2017. Increase of stroke incidence in young adults in a middle-income country. Stroke 48, 2925–2930. Clancy, L., Goodman, P., Sinclair, H., Dockery, D.W., 2002. Effect of air-pollution control on death rates in Dublin, Ireland: an intervention study. Lancet 360, 1210–1214. Dockery, D.W., Stone, P.H., 2007. Cardiovascular risks from fine particulate air pollution. N. Engl. J. Med. 356, 511–513. Feigin, V.L., Norrving, B., Mensah, G.A., 2017. Global burden of stroke. Circ. Res. 120, 439–448. Friedman, M.S., Powell, K.E., Hutwagner, L., Graham, L.R.M., Teague, W.G., 2001. Impact of changes in transportation and commuting behaviors during the 1996 Summer Olympic Games in Atlanta on air quality and childhood asthma. J. Am. Med. Assoc. 285, 897–905. Giroud, M., Delpont, B., Daubail, B., Blanc, C., Durier, J., Giroud, M., Béjot, Y., 2017. Temporal trends in sex differences with regard to stroke incidence. Stroke 48, 846–849. Gutiérrez-Avila, I., Rojas-Bracho, L., Riojas-Rodríguez, H., Kloog, I., Just Allan, C., Rothenberg Stephen, J., 2018. Cardiovascular and cerebrovascular mortality associated with acute exposure to PM2.5 in Mexico city. Stroke 49, 1734–1736. Hedley, A.J., Wong, C.M., Thach, T.Q., Ma, S., Lam, T.H., Anderson, H.R., 2002. Cardiorespiratory and all-cause mortality after restrictions on sulphur content of fuel in Hong Kong: an intervention study. The Lancet 360, 1646–1652. Jahn, H.J., Schneider, A., Breitner, S., Eißner, R., Wendisch, M., Krämer, A., 2011. Particulate matter pollution in the megacities of the Pearl River Delta, China–A systematic literature review and health risk assessment. Int. J. Hyg Environ. Health 214, 281–295. Jia, Q., Liu, L.P., Wang, Y.J., 2010. Stroke in China. Clin. Exp. Pharmacol. Physiol. 37, 259–264. Lee, J.T., Son, J.Y., Cho, Y.S., 2007. Benefits of mitigated ambient air quality due to transportation control on childhood asthma hospitalization during the 2002 summer asian games in Busan, Korea. J. Air Waste Manag. Assoc. 57, 968–973. Leitte, A.M., Petrescu, C., 2009. Respiratory health, effects of ambient air pollution and its modification by air humidity in Drobeta-Turnu Severin, Romania. Sci. Total Environ. 407, 4004–4011. Li, T.Y., Deng, X.J., Fang, S.J., Wu, D., Li, F., Deng, T., Tan, H.B., Jiang, D.H., 2012. Study on air quality and pollution meteorology conditions of Guangzhou during the 2010 asian games. Environ. Sci. 33, 2932–2938. Li, Y., Wang, W., Kan, H., Xu, X., Chen, B., 2010. Air quality and outpatient visits for asthma in adults during the 2008 Summer Olympic Games in Beijing. Sci. Total Environ. 408, 1226–1227. Li, Y., Wang, W., Wang, J., Zhang, X., Lin, W., Yang, Y., 2011. Impact of air pollution control measures and weather conditions on asthma during the 2008 Summer Olympic Games in Beijing. Int. J. Biometeorol. 55, 547–554. Lin, H., Guo, Y., Di, Q., Zheng, Y., Kowal, P., Xiao, J., Liu, T., Li, X., Zeng, W., Howard, S.W., Nelson, E.J., Qian, Z.M., Ma, W., Wu, F., 2017a. Ambient PM2.5 and stroke: effect modifiers and population attributable risk in six low- and middle-income countries. Stroke 48, 1191–1197. Lin, H., Liu, T., Fang, F., Xiao, J., Zeng, W., Li, X., Guo, L., Tian, L., Schootman, M.,
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The association between ambient air pollution control and stroke mortality during the 2010 Asian Games in Guangzhou, China
T
Shiyu Zhanga, Jiayun Lvb, Ruilin Mengc, Yin Yanga, Bipin Kumar Acharyaa, Xiangyan Suna, Hualiang Lina, Qiansheng Hud,∗∗, Zengliang Ruana,∗ a
Department of Epidemiology, School of Public Health, Sun Yat-Sen University, Guangzhou, 510080, China Guangzhou Center for Disease Control and Prevention, Guangzhou, 510440, China c Guangdong Provincial Center for Disease Control and Prevention, Guangzhou, 511430, China d Department of Occupational and Environmental Health, School of Public Health, Sun Yat-Sen University, Guangzhou, 510080, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Air pollution Particulate matter Ischemic Hemorrhagic Stroke mortality
Although ambient air pollution has been consistently associated with morbidity and mortality of stroke, there is limited evidence on whether the control of air pollution would associate with a reduced risk of stroke. The citywide air pollution controlling measures during the 2010 Asian Games in Guangzhou provided such an opportunity to answer this question. We collected daily data on the concentrations of air pollutants and mortality from ischemic and hemorrhagic stroke, and compared them for 51 intervention days in 2010 with the corresponding days in 2006–2009 and 2011 (reference period). Poisson-based interrupted time series analysis was employed to estimate the relative risk (RR) and 95% confidence interval (CI). The daily mean concentrations of PM10 (particles with an aerodynamic diameter smaller than 10 μm) was 88.64 μg/m3 during the reference period, and 80.47 μg/m3 during the intervention period. Daily mortality number of total stroke, ischemic and hemorrhagic stroke decreased from 3.67, 2.00 and 1.67 during the reference period, to 3.00, 1.76 and 1.24 during the intervention period; the corresponding RR was 0.79 (95% CI: 0.66–0.94), 0.87 (95% CI: 0.69–1.11) and 0.69 (95% CI: 0.52–0.91), respectively. Our findings show that ambient air pollution controlling measures during the 2010 Asian Games in Guangzhou were associated with a decreased risk of stroke mortality, which suggests a need to reduce air pollution to improve public health.
1. Introduction Stroke is one of the major causes of death and disability in both developing and developed countries (Cabral Norberto et al., 2017; Giroud et al., 2017). The World Health Organization estimated that there were about 25.7 million stroke cases worldwide in 2013, resulting in 6.5 million deaths (Feigin et al., 2017). About 87% of these deaths occurred in low- and middle-income countries (Strong et al., 2007). In China, stroke accounted for about 19% of the total mortality, making it the leading cause of adult disability and the second leading cause of death (Jia et al., 2010; Ning et al., 2017). Thus, it is worthwhile to investigate the determinants of stroke to improve the health level and to prolong the life expectancy for people around the world. In addition to a number of well-recognized hazard factors, such as smoking, hypertension, high cholesterol levels, and diabetes, air
pollution is one of the most frequently mentioned risk factors for stroke (Lin et al., 2017a; Liu et al., 2017a, 2017b). Recent studies in North America, Europe, and Asia have provided evidence of the short-term effect of air pollutants on stroke mortality and hospital admissions (Gutiérrez-Avila et al., 2018; Liu et al., 2017a; Wang et al., 2018; Wilker Elissa et al., 2018). The increasing evidence on the correlation between air pollutants and stroke morbidity and mortality highlighted the necessity of an effective control measure to mitigate the air pollution (Lin et al., 2014). However, questions remain about the effects of air pollution controlling measures on stroke (Bubb et al., 2009). And the opportunity to investigate the health benefits of an air pollution control program is still quite rare. Some examples have been illustrated in previous studies. For example, Friedman et al. examined the effect of air pollution control
∗
Corresponding author. Department of Epidemiology, School of Public Health, Sun Yat-Sen University, No. 74 Zhongshan Road 2, Guangzhou, 510080, China. Corresponding author. Department of Occupational and Environmental Health, School of Public Health, Sun Yat-Sen University, No. 74 Zhongshan Road 2, Guangzhou, 510080, China. E-mail addresses: [email protected] (Q. Hu), [email protected] (Z. Ruan). ∗∗
https://doi.org/10.1016/j.atmosenv.2019.116965 Received 18 January 2019; Received in revised form 26 August 2019; Accepted 5 September 2019 Available online 06 September 2019 1352-2310/ © 2019 Elsevier Ltd. All rights reserved.
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these districts were of high quality (Yu et al., 2012).
measures on asthma hospitalization during the 1996 Summer Olympics in Atlanta, United States (Friedman et al., 2001), when about 30% of the vehicle exhaust and its related pollutants were reduced by transportation control, there was a 40% decrease in acute asthma attacks and Medicaid claims, together with a reduction of 19% pediatric emergency admissions (Friedman et al., 2001). Comprehensive air quality improvement policy was also implemented during the 2008 Summer Olympic Games in Beijing, which was found to have significant beneficial effects on asthma outpatient visits (Li et al., 2011) and heart function in young healthy adults (Wu et al., 2010). Beneficial effect was also proved for the asthma morbidity of children during the 2002 Asian Games, which was celebrated in Busan, Korea (Lee et al., 2007). Although the health benefits of air pollution control measures were observed in above-mentioned studies, no study has specifically examined whether the risk of stroke decreased after such air pollution mitigation programs. The 16th Asian Games was hold in the Chinese city of Guangzhou in 2010. The government of Guangzhou made a great effort to enhance the air quality (Tao et al., 2015). From November 1 to December 21, a series of policies, such as the control of transportation and industrial emission, were implemented for 51 days; under these policies, the heavy trucks were not permitted to drive into the city, and other vehicles could only be driven on alternate days (Tao et al., 2015). Therefore, it provided us a golden opportunity to evaluate the association of air pollution control on stroke mortality. The current study aimed to examine whether there was any reduction in stroke mortality count following the policies of air pollution control during the 2010 Guangzhou Asian Games.
2.2. Data collection Daily stroke deaths were obtained from the Guangzhou Center for Disease Control and Prevention. We collected information on the date and cause of death, age at death, and the deceased's sex. The ischemic and hemorrhagic stroke deaths were coded in the format of International Classification of Diseases revision 10 (ICD 10, I63–I67 and I60–I62, respectively). The daily data on levels of air pollutants between January 1, 2006 and December 21, 2011 were obtained from the Guangdong Environmental Monitoring Center. The Center, which reported daily to China National Environmental Monitoring Centre, is part of a nationwide air monitoring networks. There are three general monitoring sites located in our study area, and data of air pollutants from these monitoring sites were averaged for the present analysis. These stations measure the concentrations of several air pollutants, included particulate matter with an aerodynamic diameter smaller than 10 μm (PM10), sulfur dioxide (SO2), and nitrogen dioxide (NO2). Additionally, meteorological data including relative humidity and daily mean temperature for the same period were obtained from the Meteorological Observation Station of Guangzhou. 2.3. Statistical analysis To evaluate the health benefits of the intervention, two approaches were frequently adopted in previous studies. For one thing, they compared the incidence of a disease during the intervention with that of prior to and after the intervention (Friedman et al., 2001; Li et al., 2010), which was usually confounded by the seasonal trend of incidence rate. For another, they compared the incidence of a disease during the intervention with the same calendar date of other years, which was vulnerable to the long-term trend of the incidence rate. However, additional analyses can be performed for other diseases that should not be impacted by air pollution, or the same disease in other days which was different from the intervention dates. One study suggested another strategy to include a "control” city, which had similarities in geographical and meteorological characteristics with the intervention city but was not affected by such intervention (Sargent et al., 2004). In addition, the reason for the change in stroke mortality count during the Games period could not only be the intervention, but also the inter-annual or long-term mortality variations. However, if the mortality count of the control city remained its consistency during the intervention, we could infer that it was not affected by those variations, and if the same pattern of change also occurs in the control areas, it could not simply be attributed to the intervention.
2. Methods 2.1. Study settings Guangzhou, a city located in the South of China, is the capital city of Guangdong Province. It is in the subtropical zone of humid-monsoon climate with an annual average rainfall of 1500–2000 mm, and its annual average temperature is 22 °C. In 2010, Guangzhou has a population of about 12.7 million permanent residents. In recent years, particulate air pollutants has become a major public health problem in Guangzhou (Jahn et al., 2011). The residents of Yuexiu and Liwan Districts of Guangzhou were chosen as the subjects of our study (Fig. 1). These two districts have a total of 1.9 million permanent residents and cover an area of 92.9 square kilometers. They were selected because of the following reasons. First, daily data of the levels of air pollutants collected from three monitoring sites in these districts were available for analysis. Second, dwellers in these districts were mainly the permanent residents. Moreover, in the light of a previous study, the mortality count data in
Fig. 1. Geographical location of the study areas in China. 2
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In the present study, we compared the daily stroke mortality count, air pollution level and meteorological factors during the intervention days in 2010 with the same calendar dates of 2006–2009 and 2011. The Student's t-test was applied to examine the statistical differences. We used interrupted time-series analysis based on Poisson regression to estimate the associations between air control measures from November 1 to December 21 (51 days) around the 2010 Asian Game period and stroke mortality counts (Bernal et al., 2016). To be specific, the dichotomous study group (intervention or reference) was used as the independent variable, while daily stroke mortality count (continuous number) was used as the dependent variable in this model. We calculated the crude and adjusted relative risk (RR) and its 95% confidence interval (CI) of mortalities from the total stroke, ischemic and hemorrhagic stroke during the intervention, in comparing with the reference period. In the adjusted model, several potential confounders were considered, included daily mean temperature and relative humidity, public holidays, and day of week. The formula for calculation could be specified as follows: The formula for calculation could be specified as follows:
Table 1 Daily stroke mortality count, concentrations of air pollutants and weather characteristics during the 2010 Guangzhou Asian Games (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period). Variables
Mean (SD) Reference period
Stroke mortality count (mean number of deaths Total stroke 3.67 (2.07) Ischemic stroke 2.00 (1.49) Hemorrhagic stroke 1.67 (1.43) Pollutants (μg/m3) PM10 88.64 (43.23) NO2 66.44 (31.79) SO2 34.61 (27.23) Weather Temperature (°C) 18.46 (3.92) Humidity (%) 63.74 (15.15)
% change Intervention period per day) 3.00 (1.43) 1.76 (1.17) 1.24 (0.96)
−18.26 −12.00 −25.75
80.47 (24.12) 64.27 (19.91) 33.15 (16.67)
−9.22 −3.27 −4.22
18.82 (3.47) 62.22 (12.10)
+1.95 −2.38
The minus sign (−) means the number in intervention period were less than the reference period, while the plus sign (+) means the number in intervention period were more than the reference period. Abbreviations: SD = standard deviation; PM10 = particulate matter with an aerodynamic diameter less than or equal to 10 μm; NO2 = nitrogen dioxide; SO2 = sulfur dioxide.
Log(ut ) = α + game + DOW + Holiday + COVs In the formula, μt was the total number of daily stroke mortality counts; game referred to a binary variable that was coded as 0 for reference days and 1 for the intervention days; DOW denoted day of week; Holiday was defined as a binary variable that was coded as 0 for work days and 1 for public holidays; and COVs indicated the other potential confounders as we mentioned above. In order to provide further evidence to support the hypothesis that the reason of change in stroke mortality count was not the inter-annual or long-term mortality variation, we further conducted a series of additional analyses. First, we compared the daily PM10 concentration, stroke mortality count from January to October (the non-intervention months) of 2010 (the year of Guangzhou Asian Games) and the corresponding months during the reference years of 2006–2009 and 2011. Second, the difference in mortality counts of non-respiratory cancers between the 2010 Guangzhou Asian Games period (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period) were also analyzed. Third, we compared the daily stroke mortality count during the 2010 Guangzhou Asian Games (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period) in a control city of Wuhua. This city was selected as the “control” city because of that, it was not impacted by the air pollution control of Guangzhou, and its data on mortality count were of high quality. Additionally, we examined the dose-response associations between three ambient air pollutants (PM10, SO2 and NO2) and stroke mortality counts by using the natural spline smoothing function. All the statistical analyses of this study were performed using the “mgcv” package in R version 3.5.1 (R Foundation for Statistical Computing, Vienna, Austria). We summarized the estimates of results as RR (95% CI) in daily stroke mortality count.
than expected. Fig. 3 displayed the daily concentration of each of the three measured air pollutants (PM10, SO2 and NO2) during the intervention and reference period. It reflects a significant decrease in daily PM10 level, and daily variation of all the three pollutants during the intervention were smaller. The daily mean PM10 level during the intervention was 80.47 μg/m3, about 9.22% lower that reference period. There were moderate decreases of 3.27% and 4.22% in SO2 and NO2 concentrations, and no significant change was observed for meteorological factors (Table 1). Table 2 showed the RR (95% CI) by age group, sex and stroke type. There were significant decreases in the risk of total stroke mortality count during intervention for those aged above 65 years, males and hemorrhagic stroke in Guangzhou. The same pattern of findings was replicated after the adjustment of potential confounders in the multivariate models, and the RR were 0.77 (95% CI: 0.63–0.94) for those above 65 years of age, and 0.75 (95% CI: 0.58–0.97) for males. The largest association was observed for hemorrhagic stroke, with the RR being 0.69 (95% CI: 0.52–0.91). There was no significant change in the risk of total stroke mortality count among the young population, females and ischemic stroke mortality count. In our additional analyses, we compared the differences in daily stroke mortality count from January to October (the non-intervention months) of 2010 (the year of Guangzhou Asian Games) and the corresponding months during the reference years of 2006–2009 and 2011, which did not show significant difference, although the concentration of ambient PM10 was slightly increased by 6.73% (Table s1). Moreover, no significant difference was observed for the daily stroke mortality count in the control city of Wuhua (Figure s1) during the 2010 Guangzhou Asian Games (intervention period) and the corresponding dates during 2006–2009 and 2011 (reference period) (Table s2). Furthermore, the number of mortality due to non-respiratory cancers during the 2010 Guangzhou Asian Games (intervention period) was 8.79 (3.34), which was not significantly differ from the corresponding dates during 2006–2009 and 2011 (reference period) of 8.72 (3.12). In addition, the dose-response curves suggested that the concentrations of PM2.5, SO2 and NO2 are positively associated with stroke mortality counts (Figure s2). All these findings from supported our results that the reduction in stroke mortality count could not be attributed to long term or inter-annual variation.
3. Results Table 1 shows the daily stroke mortality count, concentrations of air pollutants and weather characteristics during the period of 2010 Guangzhou Asian Games (intervention period) and the same calendar dates during 2006–2009 and 2011 (reference period). Daily stroke mortality count was decreased from 3.67 during the reference period to 3.00 during the intervention period, with a 18.26% reduction (Table 1, Fig. 2). The daily ischemic stroke mortality count and hemorrhagic stroke mortality count decreased from 2.00 to 1.67 during the reference period to 1.76 and 1.24 during the intervention, corresponding to the overall decreases of 12.00% and 25.75%. Based on the reference averages, this equated to 0.67, 0.24 and 0.43 fewer daily deaths from total stroke, ischemic and hemorrhagic stroke during the intervention 3
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Fig. 2. Time series of daily stroke mortality count during the study periods in Guangzhou.
Fig. 3. Time series of daily concentrations of air pollutants during the study periods in Guangzhou. Abbreviations: PM10 = particulate matter with an aerodynamic diameter smaller than or equal to 10 μm; NO2 = nitrogen dioxide; SO2 = sulfur dioxide.
4. Discussion
organizing multi-sport events, such as the Asian Games, as well as the Olympic Games(Li et al., 2010; Rich et al., 2012). In the past decades, evidence has been accumulated on the association of particulate air pollution and the risk of stroke. Our findings support the previous literatures and also suggested that diminished particulate air pollution was associated with a reduced risk of stroke mortality, particularly the hemorrhagic stroke mortality. Our findings indicated that, by reducing air pollution through the citywide control of
Air pollution control programs have been employed in a number of countries by different approaches such as fuel replacement and emission control (Lee et al., 2007; Lin et al., 2017b). Assessment of the association of air quality regulations has been increasingly regarded necessary for the policy making process of a responsible government. This is of particular importance for the strategy of air control when 4
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ischemic stroke. Moreover, previous findings have displayed that meteorological characteristics could change the pattern of particulate air pollution pattern and might be an important trigger of stroke risk (Piver et al., 1999). For example, wind speed could affect the dispersion of the particles in the air, and moisture levels, especially the relative humidity, were strongly associated with the atmospheric PM concentrations (Rigby and Toumi, 2008). Therefore, we can concluded that the characteristics of meteorological factors could affect human exposure to particulate air pollution (Leitte and Petrescu, 2009). Previous study have found that about 20–50% of PM variability can be explained by the variability of meteorological factors(Sui et al., 2007). Thus, it was significant to include meteorological conditions when analyzing the impacts of air pollution on human health. The underlying reason for the reduction of stroke mortality count in our study remained unclear. Previous studies have found that the inhalation of particulate pollutants could cause and aggravated both systemic inflammation and oxidative stress, in which might lead to autonomic dysfunction, atherosclerosis, as well as direct vascular injury (Dockery and Stone, 2007). Small particles even able to escape from the process of phagocytosis by alveolar macrophages and enter pulmonary interstitial sites, including vascular endothelium. As a result, they may cause inflammation at both epithelial and interstitial tissues, or even enter the circulation, so that it can reach further target sites, including the cardiovascular system, and thus promote the progression of atherosclerosis and precipitate the acute cardiovascular responses (Nemmar et al., 2004). There were several shortcomings in our study. To begin with, our study was ecological in design, so we could not consider the exposure in the individual level. Second, the intervention period was relatively short, and data on other air pollutants were limited (e.g., PM2.5, ozone and carbon monoxide). These factors restricted the statistical power of our study and made it difficult to make a causal inference. Third, some potential confounders which may affect the risk of stroke mortality during the reference and intervention periods were not considered in our study. For example, some people may come to the study areas during the Games and thus significantly increase the population and deaths. So we designed our plan to use the stroke mortality count data of the permanent residents only; and the deceased occurred inside the study area were reported back to their home town (Yu et al., 2012), thus this would not affect our result substantially. There were other conditions might have contributed to the decrease of the stroke mortality count, such as the medical treatment and dietary style. However, no major breakthroughs in medical interventions were concomitantly occurred with the air control program during the Games, so it was unlikely to be a problem.
Table 2 Crude and adjusted RRs of stroke mortality during the 2010 Guangzhou Asian Games (intervention period) compared with the corresponding dates during 2006–2009 and 2011 (reference period).
Age All ages 0-65 > 65 Sex Male Female Stroke type Ischemic Hemorrhagic
Crude RR (95% CI)
P-value
Adjusted RRa (95% CI)
P-value
0.82 (0.69, 0.97) 0.91 (0.61, 1.37) 0.80 (0.66, 0.97)
0.02 0.66 0.02
0.79 (0.66, 0.94) 0.89 (0.58, 1.35) 0.77 (0.63, 0.94)
0.01 0.57 0.01
0.78 (0.61, 0.99) 0.86 (0.67, 1.10)
0.04 0.24
0.75 (0.58, 0.97) 0.83 (0.64, 1.07)
0.03 0.15
0.88 (0.70, 1.10) 0.74 (0.57, 0.97)
0.26 0.03
0.87 (0.69, 1.11) 0.69 (0.52, 0.91)
0.26 0.01
Abbreviations: RR = relative risk; CI = confidence interval. a Time-series Poisson regression model with adjustment of day of week, public holidays, daily mean temperature, and relative humidity.
industrial emission and transportation, a lot of stroke deaths could be avoided. Our finding was in accordance with previous researches, although the key air pollutants and the health outcomes were different (Clancy et al., 2002; Hedley et al., 2002). Of the potential causes related to the decrease of stroke mortality count, air pollution was the most likely one. In the study area, background contamination, vehicle exhaust, power generation plants and industrial emissions were the main sources of ambient air pollutants (Yu et al., 2012). There were more small particulate matters, nitrogen oxides and carbon monoxide emitted from vehicle emissions than nonvehicle sources (Friedman et al., 2001). We observed a large and significant reduction in PM10 level, and to a lesser extent, SO2 and NO2 levels. The relatively smaller decrease in NO2 level was beyond our expectation, and the underlying mechanisms remained unknown. There was a 35% reduction in PM10 concentration after controlling the industrial emission and transportation during the 2008 Beijing Olympics, which was higher than that observed in the present study (Wang et al., 2009), this might because of that the control measures were more tight in Beijing. In our study areas, all the concentrations of pollutants were above the National Air Quality Standard, which suggests to be harmful to the general population. Thus, it was possible that a significant reduction in the risk of stroke mortality occurred after a 9.22% decrease in the level of PM10 in our study. It was also plausible that there were larger percentages of decrease in finer particles, such as PM2.5 and PM1, which were more harmful to human health, and were more likely to be affected by the air pollution control (Li et al., 2012). There was a study estimated that the levels of PM2.5 might have been decreased by about 17.1% during the 2010 Guangzhou Asian Games (Liu et al., 2013). Furthermore, the measures taken to control air pollution might have altered the particles’ chemical composition and toxicity. We found that the decrease in hemorrhagic stroke mortality count took up a large slice of the stroke mortality count reduction, suggesting that the particulate pollutants in ambient air might be more closely related to hemorrhagic stroke than ischemic stroke, this observation was in line with one of our recent study differentiating the adverse effects of air pollutants on hemorrhagic stroke and ischemic stroke in Guangzhou (Lin et al., 2016). The less significant association with ischemic stroke has also been reported in previous studies, for example, one case-crossover study found a closer association between air pollution and hemorrhagic stroke hospital admission than ischemic stroke risk Kaohsiung, Taiwan (Tsai et al., 2003). Moreover, there were two cohort studies (Nafstad et al., 2004; Yorifuji et al., 2010), one case–control study (Oudin et al., 2009) and one ecological study (Maheswaran et al., 2011) which did not find any significant association of ischemic stroke with ambient particulate air pollution. However, inconsistent finding has also been observed in other studies (Lisabeth et al., 2008), which found a stronger impact of air pollutants on
5. Conclusions We found that the daily air pollution levels and stroke mortality count were decreased significantly during the 2010 Guangzhou Asian Games period, but no significant change was observed for meteorological factors. Moreover, the program of air pollution control was associated with a decreased stroke mortality count, especially the hemorrhagic stroke mortality. Our findings support the idea to decrease air pollution through the restriction of transportation and industrial emission to improve public health.
Ethics statement Data were collected as part of government mandated health surveillance and analyzed anonymously, so ethical approval was not needed.
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Declaration of competing interest
Stamatakis, K.A., Qian, Z., Ma, W., 2017b. Mortality benefits of vigorous air quality improvement interventions during the periods of APEC Blue and Parade Blue in Beijing, China. Environ. Pollut. 220, 222–227. Lin, H., Tao, J., Du, Y., Liu, T., Qian, Z., Tian, L., Di, Q., Zeng, W., Xiao, J., Guo, L., Li, X., Xu, Y., Ma, W., 2016. Differentiating the effects of characteristics of PM pollution on mortality from ischemic and hemorrhagic strokes. Int. J. Hyg Environ. Health 219, 204–211. Lin, H., Zhang, Y., Liu, T., Xiao, J., Xu, Y., Xu, X., Qian, Z., Tong, S., Luo, Y., Zeng, W., Ma, W.J., 2014. Mortality reduction following the air pollution control measures during the 2010 Asian Games. Atmos. Environ. 91, 24–31. Lisabeth, L.D., Escobar, J.D., Dvonch, J.T., Sanchez, B.N., Majersik, J.J., Brown, D.L., Smith, M.A., Morgenstern, L.B., 2008. Ambient air pollution and risk for ischemic stroke and transient ischemic attack. Ann. Neurol. 64, 53–59. Liu, H., Tian, Y., Xu, Y., Huang, Z., Huang, C., Hu, Y., Zhang, J., 2017a. Association between ambient air pollution and hospitalization for ischemic and hemorrhagic stroke in China: a multicity case-crossover study. Environ. Pollut. 230, 234–241. Liu, H., Tian, Y., Xu, Y., Zhang, J., 2017b. Ambient particulate matter concentrations and hospitalization for stroke in 26 Chinese cities. Stroke 48, 2052–2059. Liu, H., Wang, X., Zhang, J., He, K., Wu, Y., Xu, J., 2013. Emission controls and changes in air quality in Guangzhou during the Asian Games. Atmos. Environ. 76, 81–93. Maheswaran, R., Pearson, T., Smeeton, N.C., Beevers, S.D., Campbell, M.J., Wolfe, C.D., 2011. Outdoor air pollution and incidence of ischemic and hemorrhagic stroke. Stroke 43, 22–27. Nafstad, P., Håheim, L.L., Wisløff, T., Gram, F., Oftedal, B., Holme, I., Hjermann, I., Leren, P., 2004. Urban air pollution and mortality in a cohort of Norwegian men. Environ. Health Perspect. 112, 610. Nemmar, A., Hoylaerts, M.F., Hoet, P.H.M., Nemery, B., 2004. Possible mechanisms of the cardiovascular effects of inhaled particles: systemic translocation and prothrombotic effects. Toxicol. Lett. 149, 243–253. Ning, X., Sun, J., Jiang, R., Lu, H., Bai, L., Shi, M., Tu, J., Wu, Y., Wang, J., Zhang, J., 2017. Increased stroke burdens among the low-income young and middle aged in rural China. Stroke 48, 77–83. Oudin, A., Stroh, E., Strömberg, U., Jakobsson, K., Björk, J., 2009. Long-term exposure to air pollution and hospital admissions for ischemic stroke. A register-based casecontrol study using modelled NOx as exposure proxy. BMC Public Health 9, 301. Piver, W.T., Ando, M., Ye, F., Portier, C.J., 1999. Temperature and air pollution as risk factors for heat stroke in Tokyo, July and August 1980-1995. Environ. Health Perspect. 107, 911. Rich, D.Q., Kipen, H.M., Huang, W., Wang, G., Wang, Y., Zhu, P., Ohman Strickland, P., Hu, M., Philipp, C., Diehl, S.R., 2012. Association between changes in air pollution levels during the Beijing Olympics and biomarkers of inflammation and thrombosis in healthy young adults. J. Am. Med. Assoc. 307, 2068–2078. Rigby, M., Toumi, R., 2008. London air pollution climatology: indirect evidence for urban boundary layer height and wind speed enhancement. Atmos. Environ. 42, 4932–4947. Sargent, R.P., Shepard, R.M., Glantz, S.A., 2004. Reduced incidence of admissions for myocardial infarction associated with public smoking ban: before and after study. BMJ 328, 977. Strong, K., Mathers, C., Bonita, R., 2007. Preventing stroke: saving lives around the world. Lancet Neurol. 6, 182–187. Sui, K.k.W., Yang, J., Xie, F., Zhao, Y., 2007. Beijing persistent PM10 pollution and its relationship with general meteorological features. Res. Environ. Sci. 20, 77–83. Tao, J., Zhang, L., Zhang, Z., Huang, R., Wu, Y., Zhang, R., Cao, J., Zhang, Y., 2015. Control of PM2.5 in Guangzhou during the 16th asian Games period: implication for hazy weather prevention. Sci. Total Environ. 508, 57–66. Tsai, S.S., Goggins, W.B., Chiu, H.F., Yang, C.Y., 2003. Evidence for an association between air pollution and daily stroke admissions in Kaohsiung, Taiwan. Stroke 34, 2612–2616. Wang, W., Primbs, T., Tao, S., Simonich, S.L.M., 2009. Atmospheric particulate matter pollution during the 2008 Beijing Olympics. Environ. Sci. Technol. 43, 5314–5320. Wang, X., Qian, Z., Wang, X., Hong, H., Yang, Y., Xu, Y., Xu, X., Yao, Z., Zhang, L., Rolling, C.A., Schootman, M., Liu, T., Xiao, J., Li, X., Zeng, W., Ma, W., Lin, H., 2018. Estimating the acute effects of fine and coarse particle pollution on stroke mortality of in six Chinese subtropical cities. Environ. Pollut. 239, 812–817. Wilker Elissa, H., Mostofsky, E., Fossa, A., Koutrakis, P., Warren, A., Charidimou, A., Mittleman Murray, A., Viswanathan, A., 2018. Ambient pollutants and spontaneous intracerebral hemorrhage in greater boston. Stroke 0, 2764–2766. Wu, S., Deng, F., Niu, J., Huang, Q., Liu, Y., Guo, X., 2010. Association of heart rate variability in taxi drivers with marked changes in particulate air pollution in Beijing in 2008. Environ. Health Perspect. 118, 87. Yorifuji, T., Kashima, S., Tsuda, T., Takao, S., Suzuki, E., Doi, H., Sugiyama, M., Ishikawa Takata, K., Ohta, T., 2010. Long-term exposure to traffic-related air pollution and mortality in Shizuoka, Japan. Occup. Environ. Med. 67, 111–117. Yu, I.T.S., Zhang, Y.H., San Tam, W.W., Yan, Q.H., Xu, Y.J., Xun, X.J., Wu, W., Ma, W.J., Tian, L.W., Tse, L.A., Lao, X.Q., 2012. Effect of ambient air pollution on daily mortality rates in Guangzhou, China. Atmos. Environ. 46, 528–535.
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This work was supported by the National Key R&D Program of China (2018YFA0606200) and the Natural Science Foundation of China (81972993). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.atmosenv.2019.116965. References Bernal, J.L., Cummins, S., Gasparrini, A., 2016. Interrupted time series regression for the evaluation of public health interventions: a tutorial. Int. J. Epidemiol. 46, 348–355. Bubb, M.R., Lipfert, F.W., Pope III, C.A., Ezzati, M., Dockery, D.W., 2009. Air pollution and life expectancy. N. Engl. J. Med. 360, 2032–2034. Cabral Norberto, L., Freire Aracélli, T., Conforto Adriana, B., dos Santos, N., Reis Felipe, I., Nagel, V., Guesser Vanessa, V., Safanelli, J., Longo Alexandre, L., 2017. Increase of stroke incidence in young adults in a middle-income country. Stroke 48, 2925–2930. Clancy, L., Goodman, P., Sinclair, H., Dockery, D.W., 2002. Effect of air-pollution control on death rates in Dublin, Ireland: an intervention study. Lancet 360, 1210–1214. Dockery, D.W., Stone, P.H., 2007. Cardiovascular risks from fine particulate air pollution. N. Engl. J. Med. 356, 511–513. Feigin, V.L., Norrving, B., Mensah, G.A., 2017. Global burden of stroke. Circ. Res. 120, 439–448. Friedman, M.S., Powell, K.E., Hutwagner, L., Graham, L.R.M., Teague, W.G., 2001. Impact of changes in transportation and commuting behaviors during the 1996 Summer Olympic Games in Atlanta on air quality and childhood asthma. J. Am. Med. Assoc. 285, 897–905. Giroud, M., Delpont, B., Daubail, B., Blanc, C., Durier, J., Giroud, M., Béjot, Y., 2017. Temporal trends in sex differences with regard to stroke incidence. Stroke 48, 846–849. Gutiérrez-Avila, I., Rojas-Bracho, L., Riojas-Rodríguez, H., Kloog, I., Just Allan, C., Rothenberg Stephen, J., 2018. Cardiovascular and cerebrovascular mortality associated with acute exposure to PM2.5 in Mexico city. Stroke 49, 1734–1736. Hedley, A.J., Wong, C.M., Thach, T.Q., Ma, S., Lam, T.H., Anderson, H.R., 2002. Cardiorespiratory and all-cause mortality after restrictions on sulphur content of fuel in Hong Kong: an intervention study. The Lancet 360, 1646–1652. Jahn, H.J., Schneider, A., Breitner, S., Eißner, R., Wendisch, M., Krämer, A., 2011. Particulate matter pollution in the megacities of the Pearl River Delta, China–A systematic literature review and health risk assessment. Int. J. Hyg Environ. Health 214, 281–295. Jia, Q., Liu, L.P., Wang, Y.J., 2010. Stroke in China. Clin. Exp. Pharmacol. Physiol. 37, 259–264. Lee, J.T., Son, J.Y., Cho, Y.S., 2007. Benefits of mitigated ambient air quality due to transportation control on childhood asthma hospitalization during the 2002 summer asian games in Busan, Korea. J. Air Waste Manag. Assoc. 57, 968–973. Leitte, A.M., Petrescu, C., 2009. Respiratory health, effects of ambient air pollution and its modification by air humidity in Drobeta-Turnu Severin, Romania. Sci. Total Environ. 407, 4004–4011. Li, T.Y., Deng, X.J., Fang, S.J., Wu, D., Li, F., Deng, T., Tan, H.B., Jiang, D.H., 2012. Study on air quality and pollution meteorology conditions of Guangzhou during the 2010 asian games. Environ. Sci. 33, 2932–2938. Li, Y., Wang, W., Kan, H., Xu, X., Chen, B., 2010. Air quality and outpatient visits for asthma in adults during the 2008 Summer Olympic Games in Beijing. Sci. Total Environ. 408, 1226–1227. Li, Y., Wang, W., Wang, J., Zhang, X., Lin, W., Yang, Y., 2011. Impact of air pollution control measures and weather conditions on asthma during the 2008 Summer Olympic Games in Beijing. Int. J. Biometeorol. 55, 547–554. Lin, H., Guo, Y., Di, Q., Zheng, Y., Kowal, P., Xiao, J., Liu, T., Li, X., Zeng, W., Howard, S.W., Nelson, E.J., Qian, Z.M., Ma, W., Wu, F., 2017a. Ambient PM2.5 and stroke: effect modifiers and population attributable risk in six low- and middle-income countries. Stroke 48, 1191–1197. Lin, H., Liu, T., Fang, F., Xiao, J., Zeng, W., Li, X., Guo, L., Tian, L., Schootman, M.,
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