Abstract
Accumulating evidence witnesses the negative influence of air pollution on human health, but the relationship between air pollution and premature babies has been inconsistent. In this study, the association between weekly average concentration of air pollutants and preterm birth (PTB) was conducted in Xuzhou, a heavy industry city, in China. We constructed a distributed lag non-linear model (DLNM), an ecological study, to access the associations between ambient air pollutants and PTB in this study. Totally, 5408 premature babies were included, and the weekly average levels of PM2.5, PM10, SO2, NO2, O3, and CO were 61.24, 110.21, 22.55, 40.55, 104.45, and 1.04 mg/m3, respectively. We found that PM2.5, PM10, SO2, and NO2 significantly increased the risk of PTB, and the susceptibility windows of these contaminants were the second trimester and third trimester (from 12 to 29 weeks). Every 10 μg/m3 increase of PM2.5, PM10, SO2, and NO2, the greatest relative risk (RR) values and 95% confidence interval (CI) on PTB were 1.0075 [95% CI, 1.0019–1.0131], 1.0053 [95% CI, 1.0014–1.0092], 1.0203 [95% CI, 1.0030–1.0379], and 1.0170 [95% CI, 1.0052–1.0289] in lag 16th, 18th, 19th, and 20th gestational weeks, respectively. No significant influence of O3 and CO were found on preterm birth. Subgroup analysis showed that the risk of premature delivery was higher for younger pregnant women and in warm season. This finding shows that prenatal exposure to ambient air pollutants is associated with preterm birth, and there existed an exposure window period.
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Abbreviations
- PTB:
-
Preterm birth
- DLNM:
-
Distributed lag non-linear model
- AIC:
-
Akaike information criterion
- RR:
-
Relative risk
- CI:
-
Confidential interval
References
Arroyo V, Diaz J, Ortiz C, Carmona R, Saez M, Linares C (2016) Short term effect of air pollution, noise and heat waves on preterm births in Madrid (Spain). Environ Res 145:162–168. https://doi.org/10.1016/j.envres.2015.11.034
Blum JL, Chen LC, Zelikoff JT (2017) Exposure to ambient particulate matter during specific gestational periods produces adverse obstetric consequences in mice. Environ Health Perspect 125:077020. https://doi.org/10.1289/EHP1029
Bove H, Bongaerts E, Slenders E, Bijnens EM, Saenen ND, Gyselaers W, Van Eyken P, Plusquin M, Roeffaers MBJ, Ameloot M, Nawrot TS (2019) Ambient black carbon particles reach the fetal side of human placenta. Nat Commun 10:3866. https://doi.org/10.1038/s41467-019-11654-3
Brauer M, Lencar C, Tamburic L, Koehoorn M, Demers P, Karr C (2008) A cohort study of traffic-related air pollution impacts on birth outcomes. Environ Health Perspect 116:680–686. https://doi.org/10.1289/ehp.10952
Bruckner TA, Modin B, Vagero D (2014) Cold ambient temperature in utero and birth outcomes in Uppsala, Sweden, 1915-1929. Ann Epidemiol 24:116–121. https://doi.org/10.1016/j.annepidem.2013.11.005
Chang HH, Reich BJ, Miranda ML (2012) Time-to-event analysis of fine particle air pollution and preterm birth: results from North Carolina, 2001-2005. Am J Epidemiol 175:91–98. https://doi.org/10.1093/aje/kwr403
Chen R, Zhao Z, Sun Q, Lin Z, Zhao A, Wang C, Xia Y, Xu X, Kan H (2015) Size-fractionated particulate air pollution and circulating biomarkers of inflammation, coagulation, and vasoconstriction in a panel of young adults. Epidemiology 26:328–336. https://doi.org/10.1097/EDE.0000000000000273
Chen G, Guo Y, Abramson MJ, Williams G, Li S (2018) Exposure to low concentrations of air pollutants and adverse birth outcomes in Brisbane, Australia, 2003-2013. Sci Total Environ 622-623:721–726. https://doi.org/10.1016/j.scitotenv.2017.12.050
Cheng P, Peng L, Hao J, Li S, Zhang C, Dou L, Fu W, Yang F, Hao J (2020) Short-term effects of ambient temperature on preterm birth: a time-series analysis in Xuzhou, China. Environ Sci Pollut Res Int 28:12406–12413. https://doi.org/10.1007/s11356-020-11201-4
Clemente DB et al (2016) Prenatal ambient air pollution, placental mitochondrial DNA content, and birth weight in the INMA (Spain) and ENVIRONAGE (Belgium) birth cohorts. Environ Health Perspect 124:659–665. https://doi.org/10.1289/ehp.1408981
da Silva LK, Ota E, Shakya P, Dagvadorj A, Balogun OO, Pena-Rosas JP, De-Regil LM, Mori R (2017) Effects of nutrition interventions during pregnancy on low birth weight: an overview of systematic reviews. BMJ Glob Health 2:e000389. https://doi.org/10.1136/bmjgh-2017-000389
DeFranco E, Moravec W, Xu F, Hall E, Hossain M, Haynes EN, Muglia L, Chen A (2016) Exposure to airborne particulate matter during pregnancy is associated with preterm birth: a population-based cohort study. Environ Health 15:6. https://doi.org/10.1186/s12940-016-0094-3
Estarlich M, Ballester F, Davdand P, Llop S, Esplugues A, Fernandez-Somoano A, Lertxundi A, Guxens M, Basterrechea M, Tardon A, Sunyer J, Iniguez C (2016) Exposure to ambient air pollution during pregnancy and preterm birth: a Spanish multicenter birth cohort study. Environ Res 147:50–58. https://doi.org/10.1016/j.envres.2016.01.037
Gasparrini A, Armstrong B, Kenward MG (2010) Distributed lag non-linear models. Stat Med 29:2224–2234. https://doi.org/10.1002/sim.3940
Gianicolo EAL, Mangia C, Cervino M, Bruni A, Andreassi MG, Latini G (2014) Congenital anomalies among live births in a high environmental risk area-A case-control study in Brindisi (southern Italy). Environ Res 128:9–14. https://doi.org/10.1016/j.envres.2013.11.002
Gianicolo EAL, Eichler M, Muensterer O, Strauch K, Blettner M (2020) Methods for evaluating causality in observational studies. Dtsch Arztebl Int 116:101–107. https://doi.org/10.3238/arztebl.2020.0101
Grevendonk L, Janssen BG, Vanpoucke C, Lefebvre W, Hoxha M, Bollati V, Nawrot TS (2016) Mitochondrial oxidative DNA damage and exposure to particulate air pollution in mother-newborn pairs. Environ Health 15:10. https://doi.org/10.1186/s12940-016-0095-2
Guan T, Xue T, Gao S, Hu M, Liu X, Qiu X, Liu X, Zhu T (2019) Acute and chronic effects of ambient fine particulate matter on preterm births in Beijing, China: A time-series model. Sci Total Environ 650:1671–1677. https://doi.org/10.1016/j.scitotenv.2018.09.279
Ha S, Hu H, Roussos-Ross D, Haidong K, Roth J, Xu X (2014) The effects of air pollution on adverse birth outcomes. Environ Res 134:198–204. https://doi.org/10.1016/j.envres.2014.08.002
Han Y, Jiang P, Dong T, Ding X, Chen T, Villanger GD, Aase H, Huang L, Xia Y (2018) Maternal air pollution exposure and preterm birth in Wuxi, China: effect modification by maternal age. Ecotoxicol Environ Saf 157:457–462. https://doi.org/10.1016/j.ecoenv.2018.04.002
Hannam K, McNamee R, Baker P, Sibley C, Agius R (2014) Air pollution exposure and adverse pregnancy outcomes in a large UK birth cohort: use of a novel spatio-temporal modelling technique. Scand J Work Environ Health 40:518–530. https://doi.org/10.5271/sjweh.3423
Hansen C, Neller A, Williams G, Simpson R (2006) Maternal exposure to low levels of ambient air pollution and preterm birth in Brisbane, Australia. BJOG 113:935–941. https://doi.org/10.1111/j.1471-0528.2006.01010.x
He JR, Liu Y, Xia XY, Ma WJ, Lin HL, Kan HD, Lu JH, Feng Q, Mo WJ, Wang P, Xia HM, Qiu X, Muglia LJ (2016) Ambient temperature and the risk of preterm birth in Guangzhou, China (2001-2011). Environ Health Perspect 124:1100–1106. https://doi.org/10.1289/ehp.1509778
Hyder A, Lee HJ, Ebisu K, Koutrakis P, Belanger K, Bell ML (2014) PM2.5 exposure and birth outcomes: use of satellite- and monitor-based data. Epidemiology 25:58–67. https://doi.org/10.1097/EDE.0000000000000027
Ion R, Bernal AL (2015) Smoking and preterm birth. Reprod Sci 22:918–926. https://doi.org/10.1177/1933719114556486
Ji X, Meng X, Liu C, Chen R, Ge Y, Kan L, Fu Q, Li W, Tse LA, Kan H (2019) Nitrogen dioxide air pollution and preterm birth in Shanghai, China. Environ Res 169:79–85. https://doi.org/10.1016/j.envres.2018.11.007
Jiang LL, Zhang YH, Song GX, Chen GH, Chen BH, Zhao NQ, Kan HD (2007) A time series analysis of outdoor air pollution and preterm birth in Shanghai, China. Biomed Environ Sci 20:426–431
Johnson S, Bobb JF, Ito K, Savitz DA, Elston B, Shmool JL, Dominici F, Ross Z, Clougherty JE, Matte T (2016) Ambient fine particulate matter, nitrogen dioxide, and preterm birth in New York City. Environ Health Perspect 124:1283–1290. https://doi.org/10.1289/ehp.1510266
Kannan S, Misra DP, Dvonch JT, Krishnakumar A (2006) Exposures to airborne particulate matter and adverse perinatal outcomes: a biologically plausible mechanistic framework for exploring potential effect modification by nutrition. Environ Health Perspect 114:1636–1642. https://doi.org/10.1289/ehp.9081
Lavigne E, Yasseen AS 3rd, Stieb DM, Hystad P, van Donkelaar A, Martin RV, Brook JR, Crouse DL, Burnett RT, Chen H, Weichenthal S, Johnson M, Villeneuve PJ, Walker M (2016) Ambient air pollution and adverse birth outcomes: differences by maternal comorbidities. Environ Res 148:457–466. https://doi.org/10.1016/j.envres.2016.04.026
Lee PC, Roberts JM, Catov JM, Talbott EO, Ritz B (2013) First trimester exposure to ambient air pollution, pregnancy complications and adverse birth outcomes in Allegheny County, PA. Matern Child Health J 17:545–555. https://doi.org/10.1007/s10995-012-1028-5
Lee MK, Xu CJ, Carnes MU, Nichols CE, Ward JM, Kwon SO, Kim SY, Kim WJ, London SJ (2019) Genome-wide DNA methylation and long-term ambient air pollution exposure in Korean adults. Clin Epigenetics 11:37. https://doi.org/10.1186/s13148-019-0635-z
Li Z, Yuan X, Fu J, Zhang L, Hong L, Hu L, Liu L (2019) Association of ambient air pollutants and birth weight in Ningbo, 2015-2017. Environ Pollut 249:629–637. https://doi.org/10.1016/j.envpol.2019.03.076
Lin YT, Jung CR, Lee YL, Hwang BF (2015) Associations between ozone and preterm birth in women who develop gestational diabetes. Am J Epidemiol 181:280–287. https://doi.org/10.1093/aje/kwu264
Litmanovitz I, Erez H, Eliakim A, Bauer-Rusek S, Arnon S, Regev RH, Sirota G, Nemet D (2016) The effect of assisted exercise frequency on bone strength in very low birth weight preterm infants: a randomized control trial. Calcif Tissue Int 99:237–242. https://doi.org/10.1007/s00223-016-0145-3
Liu WY, Yu ZB, Qiu HY, Wang JB, Chen XY, Chen K (2018) Association between ambient air pollutants and preterm birth in Ningbo, China: a time-series study. BMC Pediatr 18:305. https://doi.org/10.1186/s12887-018-1282-9
Liu Y, Xu J, Chen D, Sun P, Ma X (2019) The association between air pollution and preterm birth and low birth weight in Guangdong, China. BMC Public Health 19:3. https://doi.org/10.1186/s12889-018-6307-7
Longo LD (1977) The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant. Am J Obstet Gynecol 129:69–103. https://doi.org/10.1016/0002-9378(77)90824-9
Martens DS, Cox B, Janssen BG, Clemente DBP, Gasparrini A, Vanpoucke C, Lefebvre W, Roels HA, Plusquin M, Nawrot TS (2017) Prenatal air pollution and newborns’ predisposition to accelerated biological aging. JAMA Pediatr 171:1160–1167. https://doi.org/10.1001/jamapediatrics.2017.3024
Moller P, Danielsen PH, Karottki DG, Jantzen K, Roursgaard M, Klingberg H, Jensen DM, Christophersen DV, Hemmingsen JG, Cao Y, Loft S (2014) Oxidative stress and inflammation generated DNA damage by exposure to air pollution particles. Mutat Res Rev Mutat Res 762:133–166. https://doi.org/10.1016/j.mrrev.2014.09.001
Nachman RM, Mao G, Zhang X, Hong X, Chen Z, Soria CS, He H, Wang G, Caruso D, Pearson C, Biswal S, Zuckerman B, Wills-Karp M, Wang X (2016) Intrauterine inflammation and maternal exposure to ambient PM2.5 during preconception and specific periods of pregnancy: the Boston Birth Cohort. Environ Health Perspect 124:1608–1615. https://doi.org/10.1289/EHP243
Naz S, Page A, Agho KE (2018) Attributable risk and potential impact of interventions to reduce household air pollution associated with under-five mortality in South Asia. Glob Health Res Policy 3:4. https://doi.org/10.1186/s41256-018-0059-x
Padula AM, Huang H, Baer RJ, August LM, Jankowska MM, Jellife-Pawlowski LL, Sirota M, Woodruff TJ (2018) Environmental pollution and social factors as contributors to preterm birth in Fresno County. Environ Health 17:70. https://doi.org/10.1186/s12940-018-0414-x
Pereira G, Bell ML, Lee HJ, Koutrakis P, Belanger K (2014) Sources of fine particulate matter and risk of preterm birth in Connecticut, 2000-2006: a longitudinal study. Environ Health Perspect 122:1117–1122. https://doi.org/10.1289/ehp.1307741
Peters A, Doring A, Wichmann HE, Koenig W (1997) Increased plasma viscosity during an air pollution episode: a link to mortality? Lancet 349:1582–1587. https://doi.org/10.1016/S0140-6736(97)01211-7
Plusquin M, Guida F, Polidoro S, Vermeulen R, Raaschou-Nielsen O, Campanella G, Hoek G, Kyrtopoulos SA, Georgiadis P, Naccarati A, Sacerdote C, Krogh V, Bas Bueno-de-Mesquita H, Monique Verschuren WM, Sayols-Baixeras S, Panni T, Peters A, Hebels DGAJ, Kleinjans J, Vineis P, Chadeau-Hyam M (2017) DNA methylation and exposure to ambient air pollution in two prospective cohorts. Environ Int 108:127–136. https://doi.org/10.1016/j.envint.2017.08.006
Ritz B, Wilhelm M (2008) Ambient air pollution and adverse birth outcomes: methodologic issues in an emerging field. Basic Clin Pharmacol Toxicol 102:182–190. https://doi.org/10.1111/j.1742-7843.2007.00161.x
Rudra CB, Williams MA, Sheppard L, Koenig JQ, Schiff MA (2011) Ambient carbon monoxide and fine particulate matter in relation to preeclampsia and preterm delivery in western Washington State. Environ Health Perspect 119:886–892. https://doi.org/10.1289/ehp.1002947
Schifano P, Asta F, Dadvand P, Davoli M, Basagana X, Michelozzi P (2016) Heat and air pollution exposure as triggers of delivery: a survival analysis of population-based pregnancy cohorts in Rome and Barcelona. Environ Int 88:153–159. https://doi.org/10.1016/j.envint.2015.12.013
Schraufnagel DE, Balmes JR, Cowl CT, De Matteis S, Jung SH, Mortimer K, Perez-Padilla R, Rice MB, Riojas-Rodriguez H, Sood A, Thurston GD, To T, Vanker A, Wuebbles DJ (2019) Air pollution and noncommunicable diseases: a review by the Forum of International Respiratory Societies’ Environmental Committee, Part 2: Air Pollution and Organ Systems. Chest 155:417–426. https://doi.org/10.1016/j.chest.2018.10.041
Smith RB, Beevers SD, Gulliver J, Dajnak D, Fecht D, Blangiardo M, Douglass M, Hansell AL, Anderson HR, Kelly FJ, Toledano MB (2020) Impacts of air pollution and noise on risk of preterm birth and stillbirth in London. Environ Int 134:105290. https://doi.org/10.1016/j.envint.2019.105290
Sofianopoulou E, Kaptoge S, Gräf S, Hadinnapola C, Treacy CM, Church C, Coghlan G, Gibbs JSR, Haimel M, Howard LS, Johnson M, Kiely DG, Lawrie A, Lordan J, MacKenzie Ross RV, Martin JM, Moledina S, Newnham M, Peacock AJ, Price LC, Rhodes CJ, Suntharalingam J, Swietlik EM, Toshner MR, Wharton J, Wilkins MR, Wort SJ, Pepke-Zaba J, Condliffe R, Corris PA, di Angelantonio E, Provencher S, Morrell NW (2019) Traffic exposures, air pollution and outcomes in pulmonary arterial hypertension: a UK cohort study analysis. Eur Respir J 53:1801429. https://doi.org/10.1183/13993003.01429-2018
Song J, Lu J, Wang E, Lu M, An Z, Liu Y, Zeng X, Li W, Li H, Xu D, Yao S, Wu W (2019a) Short-term effects of ambient temperature on the risk of premature rupture of membranes in Xinxiang, China: a time-series analysis. Sci Total Environ 689:1329–1335. https://doi.org/10.1016/j.scitotenv.2019.06.457
Song J, Lu M, An Z, Liu Y, Zheng L, Li Y, Chao L, Xu D, Yao S, Wu W (2019b) Estimating the acute effects of ambient ozone pollution on the premature rupture of membranes in Xinxiang, China. Chemosphere 227:191–197. https://doi.org/10.1016/j.chemosphere.2019.04.062
Stieb DM, Chen L, Hystad P, Beckerman BS, Jerrett M, Tjepkema M, Crouse DL, Omariba DW, Peters PA, van Donkelaar A, Martin RV, Burnett RT, Liu SL, Smith-Doiron M, Dugandzic RM (2016) A national study of the association between traffic-related air pollution and adverse pregnancy outcomes in Canada, 1999-2008. Environ Res 148:513–526. https://doi.org/10.1016/j.envres.2016.04.025
Suh YJ, Kim H, Seo JH, Park H, Kim YJ, Hong YC, Ha EH (2009) Different effects of PM10 exposure on preterm birth by gestational period estimated from time-dependent survival analyses. Int Arch Occup Environ Health 82:613–621. https://doi.org/10.1007/s00420-008-0380-7
Sun X, Luo X, Zhao C, Chung Ng RW, Lim CE, Zhang B, Liu T (2015) The association between fine particulate matter exposure during pregnancy and preterm birth: a meta-analysis. BMC Pregn Childbirth 15:300. https://doi.org/10.1186/s12884-015-0738-2
Tian L, Qiu H, Pun VC, Lin H, Ge E, Chan JC, Louie PK, Ho KF, Yu IT (2013) Ambient carbon monoxide associated with reduced risk of hospital admissions for respiratory tract infections. Am J Respir Crit Care Med 188:1240–1245. https://doi.org/10.1164/rccm.201304-0676OC
Wang YY, Li Q, Guo Y, Zhou H, Wang X, Wang Q, Shen H, Zhang Y, Yan D, Zhang Y, Zhang H, Li S, Chen G, Zhao J, He Y, Yang Y, Xu J, Wang Y, Peng Z, Wang HJ, Ma X (2018) Association of long-term exposure to airborne particulate matter of 1 mum or less with preterm birth in China. JAMA Pediatr 172:e174872. https://doi.org/10.1001/jamapediatrics.2017.4872
WHO (2018) Preterm Birth. https://www.who.int/news-room/fact-sheets/detail/preterm-birth. Accessed 1st October 2020.
Winckelmans E, Cox B, Martens E, Fierens F, Nemery B, Nawrot TS (2015) Fetal growth and maternal exposure to particulate air pollution--more marked effects at lower exposure and modification by gestational duration. Environ Res 140:611–618. https://doi.org/10.1016/j.envres.2015.05.015
Wu J, Ren C, Delfino RJ, Chung J, Wilhelm M, Ritz B (2009) Association between local traffic-generated air pollution and preeclampsia and preterm delivery in the south coast air basin of California. Environ Health Perspect 117:1773–1779. https://doi.org/10.1289/ehp.0800334
Xiong L, Xu Z, Tan J, Wang H, Liu Z, Wang A, Xie D, Kong F (2019) Acute effects of air pollutants on adverse birth outcomes in Changsha, China: a population data with time-series analysis from 2015 to 2017. Medicine 98:e14127. https://doi.org/10.1097/MD.0000000000014127
Zhang C, Ding R, Xiao C, Xu Y, Cheng H, Zhu F, Lei R, Di D, Zhao Q, Cao J (2017) Association between air pollution and cardiovascular mortality in Hefei, China: a time-series analysis. Environ Pollut 229:790–797. https://doi.org/10.1016/j.envpol.2017.06.022
Zhang Q, Sun S, Sui X, Ding L, Yang M, Li C, Zhang C, Zhang X, Hao J, Xu Y, Lin S, Ding R, Cao J (2020) Associations between weekly air pollution exposure and congenital heart disease. Sci Total Environ 143821:143821. https://doi.org/10.1016/j.scitotenv.2020.143821
Zhang C, Li S, Guo GL, Hao JW, Cheng P, Xiong LL, Chen ST, Cao JY, Guo YW, Hao JH (2021) Acute associations between air pollution on premature rupture of membranes in Hefei. China Environ Geochem Health. https://doi.org/10.1007/s10653-021-00833-1
Zhao N, Qiu J, Zhang Y, He X, Zhou M, Li M, Xu X, Cui H, Lv L, Lin X, Zhang C, Zhang H, Xu R, Zhu D, Lin R, Yao T, Su J, Dang Y, Han X, Zhang H, Bai H, Chen Y, Tang Z, Wang W, Wang Y, Liu X, Ma B, Liu S, Qiu W, Huang H, Liang J, Chen Q, Jiang M, Ma S, Jin L, Holford T, Leaderer B, Bell ML, Liu Q, Zhang Y (2015) Ambient air pollutant PM10 and risk of preterm birth in Lanzhou, China. Environ Int 76:71–77. https://doi.org/10.1016/j.envint.2014.12.009
Zhu J, Lee RW, Twum C, Wei Y (2019) Exposure to ambient PM2.5 during pregnancy and preterm birth in metropolitan areas of the state of Georgia. Environ Sci Pollut Res Int 26:2492–2500. https://doi.org/10.1007/s11356-018-3746-8
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The authors wish to thank all the staff members at Xuzhou Maternity and Child Health Care Hospital In-patient Department and the Xuzhou Center for Disease Prevention and Control for their strong support of this study.
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This work was supported by the National Natural Science Foundation of China (Grant No. 81872635).
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SL, LP, and CZ conceived and designed the research; SL, LP, XCW, GX, PC, JWH, ZHH, MX, and STC collected data; SL and LP wrote the initial paper; SL and CZ revised the paper; JHH had primary responsibility for the final content. All authors read and approved the final manuscript. SL and LP contributed equally to this work.
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Li, S., Peng, L., Wu, X. et al. Long-term impact of ambient air pollution on preterm birth in Xuzhou, China: a time series study. Environ Sci Pollut Res 28, 41039–41050 (2021). https://doi.org/10.1007/s11356-021-13621-2
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DOI: https://doi.org/10.1007/s11356-021-13621-2