Zhang Junfeng, Zhu Tong, Kipen Howard, Wang Guangfa, Huang Wei, Rich David, Zhu Ping, Wang Yuedan, Lu Shou-En, Ohman-Strickland Pamela, Diehl Scott, Hu Min, Tong Jian, Gong Jicheng, Thomas Duncan
University of Medicine and Dentistry of New Jersey-School of Public Health, Piscataway, NJ, USA.
Res Rep Health Eff Inst. 2013 Feb(174):5-174.
Associations between air pollution and cardiorespiratory mortality and morbidity have been well established, but data to support biologic mechanisms underlying these associations are limited. We designed this study to examine several prominently hypothesized mechanisms by assessing Beijing residents' biologic responses, at the biomarker level, to drastic changes in air quality brought about by unprecedented air pollution control measures implemented during the 2008 Beijing Olympics. To test the hypothesis that changes in air pollution levels are associated with changes in biomarker levels reflecting inflammation, hemostasis, oxidative stress, and autonomic tone, we recruited and retained 125 nonsmoking adults (19 to 33 years old) free of cardiorespiratory and other chronic diseases. Using the combination of a quasi-experimental design and a panel-study approach, we measured biomarkers of autonomic dysfunction (heart rate [HR*] and heart rate variability [HRV]), of systemic inflammation and oxidative stress (plasma C-reactive protein [CRP], fibrinogen, blood cell counts and differentials, and urinary 8-hydroxy-2'-deoxyguanosine [8-OHdG]), of pulmonary inflammation and oxidative stress (fractional exhaled nitric oxide [FeNO], exhaled breath condensate [EBC] pH, EBC nitrate, EBC nitrite, EBC nitrite+nitrate [sum of the concentrations of nitrite and nitrate], and EBC 8-isoprostane), of hemostasis (platelet activation [plasma sCD62P and sCD40L], platelet aggregation, and von Willebrand factor [vWF]), and of blood pressure (systolic blood pressure [SBP] and diastolic blood pressure [DBP]). These biomarkers were measured on each subject twice before, twice during, and twice after the Beijing Olympics. For each subject, repeated measurements were separated by at least one week to avoid potential residual effects from a prior measurement. We measured a large suite of air pollutants (PM2.5 [particulate matter < or = 2.5 microm in aerodynamic diameter] and constituents, sulfur dioxide [SO2], carbon monoxide [CO], nitrogen dioxide [NO2], and ozone [O3]) throughout the study at a central Beijing site near the residences and workplaces of the subjects on a daily basis. Total particle number (TPN) was also measured at a separate site. We used a time-series analysis to assess changes in pollutant concentration by period (pre-, during-, and post-Olympics periods). We used mixed-effects models to assess changes in biomarker levels by period and to estimate changes associated with increases in pollutant concentrations, controlling for ambient temperature, relative humidity (RH), sex, and the day of the week of the biomarker measurements. We conducted sensitivity analyses to assess the impact of potential temporal confounding and exposure misclassification. We observed reductions in mean concentrations for all measured pollutants except O3 from the pre-Olympics period to the during-Olympics period. On average, elemental carbon (EC) changed by -36%, TPN by -22%, SO2 by -60%, CO by -48%, and NO2 by -43% (P < 0.05 for all these pollutants). Reductions were observed in mean concentrations of PM2.5 (by -27%), sulfate (SO4(2-)) (by -13%), and organic carbon (OC) (by -23%); however, these values were not statistically significant. Both 24-hour averages and 1-hour maximums of O3 increased (by 20% and 17%, respectively) from the pre-Olympics to the during-Olympics period. In the post-Olympics period after the pollution control measures were relaxed, mean concentrations of most pollutants (with the exception of SO4(2-) and O3) increased to levels similar to or higher than pre-Olympics levels. Concomitantly and consistent with the hypothesis, we observed, from the pre-Olympics to the during-Olympics period, statistically significant (P < or = 0.05) or marginally significant (0.05 < P < 0.1) decreases in HR (-1 bpm or -1.7% [95% CI, -3.4 to -0.1]), SBP (-1.6 mmHg or -1.8% [95% CI, -3.9 to 0.4]), 8-OHdG (-58.3% [95% CI, -72.5 to -36.7]), FeNO (-60.3% [95% CI, -66.0 to -53.6]), EBC nitrite (-30.0% [95% CI, -39.3 to -19.3]), EBC nitrate (-21.5% [95% CI, -35.5 to -4.5]), EBC nitrite+nitrate (-17.6% [95% CI, -28.4 to -5.1]), EBC hydrogen ions (-46% [calculated from EBC pH], or +3.5% in EBC pH [95% CI, 2.2 to 4.9]), sCD62P (-34% [95% CI, -38.4 to -29.2]), sCD40L (-5.7% [95% CI, -10.5 to -0.7]), and vWF (-13.1% [95% CI, -18.6 to -7.5]). Moreover, the percentages of above-detection values out of all observations were significantly lower for plasma CRP and EBC 8-isoprostane in the during-Olympics period compared with the pre-Olympics period. In the post-Olympics period, the levels of the following biomarkers reversed (increased, either with or without statistical significance) from those in the during-Olympics period: SBP (10.7% [95% CI, 2.8 to 18.6]), fibrinogen (4.3% [95% CI, -1.7 to 10.2), neutrophil count (4.7% [95% CI, -7.7 to 17.0]), 8-OHdG (315% [95% CI, 62.0 to 962]), FeNO (130% [95% CI, 62.5 to 225]), EBC nitrite (159% [95% CI, 71.8 to 292]), EBC nitrate (161% [95% CI, 48.0 to 362]), EBC nitrite+nitrate (124% [95% CI, 50.9 to 233]), EBC hydrogen ions (146% [calculated from EBC pH] or -4.8% in EBC pH [95% CI, -9.4 to -0.21), sCD62P (33.7% [95% CI, 17.7 to 51.8]), and sCD40L (9.1% [95% CI, -3.7 to 23.5]). Furthermore, these biomarkers also showed statistically significant associations with multiple pollutants across different lags after adjusting for meteorologic parameters. The associations were in the directions hypothesized and were consistent with the findings from the comparisons between periods, providing further evidence that the period effects were due to changes in air quality, independent of season and meteorologic conditions or other potential confounders. Contrary to our hypothesis, however, we observed increases in platelet aggregation, red blood cells (RBCs) and white blood cells (WBCs) associated with the during-Olympics period, as well as significant negative associations of these biomarkers with pollutant concentrations. We did not observe significant changes in any of the HRV indices and DBP by period. However, we observed associations between a few HRV indices and pollutant concentrations. Changes in air pollution levels during the Beijing Olympics were associated with acute changes in biomarkers of pulmonary and systemic inflammation, oxidative stress, and hemostasis and in measures of cardiovascular physiology (HR and SBP) in healthy, young adults. These changes support the prominently hypothesized mechanistic pathways underlying the cardiorespiratory effects of air pollution.
空气污染与心肺疾病死亡率和发病率之间的关联已得到充分证实,但支持这些关联背后生物学机制的数据有限。我们设计了这项研究,通过评估北京居民在生物标志物水平上对2008年北京奥运会期间实施的前所未有的空气污染控制措施所带来的空气质量急剧变化的生物学反应,来检验几种主要的假设机制。为了检验空气污染水平的变化与反映炎症、止血、氧化应激和自主神经张力的生物标志物水平变化相关的假设,我们招募并保留了125名无心血管和其他慢性疾病的非吸烟成年人(19至33岁)。采用准实验设计和面板研究方法相结合的方式,我们测量了自主神经功能障碍(心率[HR*]和心率变异性[HRV])、全身炎症和氧化应激(血浆C反应蛋白[CRP]、纤维蛋白原、血细胞计数及分类、尿8-羟基-2'-脱氧鸟苷[8-OHdG])、肺部炎症和氧化应激(呼出一氧化氮分数[FeNO]、呼出气冷凝物[EBC]pH值、EBC硝酸盐、EBC亚硝酸盐、EBC亚硝酸盐+硝酸盐[亚硝酸盐和硝酸盐浓度之和]、EBC 8-异前列腺素)、止血(血小板活化[血浆sCD62P和sCD40L]、血小板聚集、血管性血友病因子[vWF])以及血压(收缩压[SBP]和舒张压[DBP])的生物标志物。这些生物标志物在每位受试者北京奥运会前测量两次、奥运会期间测量两次、奥运会后测量两次。对于每位受试者,重复测量至少间隔一周,以避免先前测量的潜在残留影响。在整个研究过程中,我们在北京城区靠近受试者住所和工作场所的一个中心站点每天测量一大组空气污染物(PM2.5[空气动力学直径≤2.5微米的颗粒物]及其成分、二氧化硫[SO2]、一氧化碳[CO]、二氧化氮[NO2]和臭氧[O3])。还在另一个站点测量了总颗粒数(TPN)。我们采用时间序列分析来评估不同时期(奥运会前、奥运会期间、奥运会后)污染物浓度的变化。我们使用混合效应模型来评估不同时期生物标志物水平的变化,并估计与污染物浓度增加相关的变化,同时控制环境温度、相对湿度(RH)、性别以及生物标志物测量的星期几。我们进行了敏感性分析,以评估潜在的时间混杂和暴露错误分类的影响。我们观察到,从奥运会前到奥运会期间,除O3外,所有测量污染物的平均浓度均有所降低。平均而言,元素碳(EC)变化了-36%,TPN变化了-22%,SO2变化了-60%,CO变化了-48%,NO2变化了-43%(所有这些污染物的P<0.05)。PM2.5(-27%)、硫酸盐(SO4(2-))(-13%)和有机碳(OC)(-23%)的平均浓度也有所降低;然而,这些值无统计学意义。从奥运会前到奥运会期间,O3的24小时平均值和1小时最大值均有所增加(分别增加了20%和17%)。在污染控制措施放松后的奥运会后时期,大多数污染物(SO4(2-)和O3除外)的平均浓度增加到与奥运会前水平相似或更高的水平。与此同时,与假设一致,我们观察到,从奥运会前到奥运会期间,HR(-1次/分钟或-1.7%[95%CI,-3.4至-0.1])、SBP(-1.6毫米汞柱或-1.8%[95%CI,-3.9至0.4])、8-OHdG(-58.3%[95%CI,-72.5至-36.7])、FeNO(-60.3%[95%CI,-66.0至-53.6])、EBC亚硝酸盐(-30.0%[95%CI,-39.3至-19.3])、EBC硝酸盐(-21.5%[95%CI,-35.5至-4.5])、EBC亚硝酸盐+硝酸盐(-17.6%[95%CI,-28.4至-5.1])、EBC氢离子(-46%[根据EBC pH计算]或EBC pH增加3.5%[95%CI,2.2至4.9])、sCD62P(-34%[95%CI,-38.4至-29.2])、sCD40L(-5.7%[95%CI,-10.5至-0.7])和vWF(-13.1%[95%CI,-18.6至-7.5])出现了具有统计学意义(P≤0.05)或边缘显著意义(0.05<P<0.1)的下降。此外,与奥运会前时期相比,奥运会期间血浆CRP和EBC 8-异前列腺素所有观察值中高于检测值的百分比显著降低。在奥运会后时期,以下生物标志物的水平与奥运会期间相比发生了逆转(升高,有或无统计学意义):SBP(10.7%[95%CI,2.8至18.6])、纤维蛋白原(4.3%[95%CI,-1.7至10.2])、中性粒细胞计数(4.7%[95%CI,-7.7至17.0])、8-OHdG(315%[95%CI,62.0至962])、FeNO(130%[95%CI,62.5至225])、EBC亚硝酸盐(159%[95%CI,71.8至292])、EBC硝酸盐(161%[95%CI,48.0至362])、EBC亚硝酸盐+硝酸盐(124%[95%CI,50.9至233])、EBC氢离子(-(根据EBC pH计算)或EBC pH降低4.8%[95%CI,-9.4至-0.21])、sCD62P(33.7%[95%CI,17.7至51.8])和sCD40L(9.1%[95%CI,-3.7至23.5])。此外,在调整气象参数后,这些生物标志物在不同滞后时间也与多种污染物呈现出统计学显著关联。这些关联方向与假设一致,且与不同时期比较的结果相符,进一步证明了时期效应是由空气质量变化导致的,独立于季节、气象条件或其他潜在混杂因素。然而,与我们的假设相反,我们观察到奥运会期间血小板聚集、红细胞(RBC)和白细胞(WBC)增加,并且这些生物标志物与污染物浓度存在显著负相关。我们未观察到不同时期HRV指数和DBP有显著变化。然而,我们观察到一些HRV指数与污染物浓度之间存在关联。北京奥运会期间空气污染水平的变化与健康年轻成年人肺部和全身炎症、氧化应激、止血的生物标志物以及心血管生理指标(HR和SBP)的急性变化相关。这些变化支持了空气污染对心肺影响背后主要假设的机制途径。