Abstract
The potential association between maternal exposure to PM10 ranging from 3 months prior to conception to the end of the early trimester and the risk of anorectal atresia/stenosis in offspring has not been established. Thus, we determined the association between maternal exposure to PM10 and risk of anorectal atresia/stenosis in offspring in this study. We recruited 713 patients including 480 male and 233 female with anorectal atresia/stenosis and 7950 randomly selected healthy offspring from the Maternal and Child Health Certificate Registry of Liaoning Province and delivered between 1 January 2010 and 31 December 2015. Monthly PM10 concentrations were retrieved from the Environment Protection Bureau of each city in Liaoning Province. We established a multivariable logistic regression model to calculate the adjusted odds ratios (ORs) and 95% confidence intervals (CIs). Maternal exposure to PM10 was associated with an increased risk for anorectal atresia/stenosis in offspring during the 3 months prior to conception (per 10 μg/m3 increment: OR = 1.15, 95% CI = 1.03–1.20; per SD [27 μg/m3] increment: OR = 1.33, 95% CI = 1.09–1.63) and the first trimester (per 10 μg/m3 increment: OR = 1.08, 95% CI = 1.00–1.17; per SD [28 μg/m3] increment: OR = 1.26, 95% CI = 1.01–1.57). Evaluation of the association with a shorter exposure window (1 month) revealed a positive association between anorectal atresia/stenosis and PM10 from the 3rd month prior to pregnancy to each month of the 1st trimester. Maternal exposure to PM10 3 months prior to conception and during the 1st trimester was associated with an increased risk of anorectal atresia/stenosis in the offspring. Future perspective cohort studies are needed to confirm our findings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- PM:
-
Particulate matter
- SD:
-
Standard deviation
- OR:
-
Odds ratio
- CI:
-
Confidence intervals
- TPM:
-
Total particulate matter
- ROS:
-
Reactive oxygen species
- EM:
-
Embryonic movement
References
Austin PC (2011) An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivariate Behav Res. 46:399–424. https://doi.org/10.1080/00273171.2011.568786
Bell ML, Belanger K (2012) Review of research on residential mobility during pregnancy: consequences for assessment of prenatal environmental exposures. J Expo Sci Environ Epidemiol. 22:429–438. https://doi.org/10.1038/jes.2012.42
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
Chow JC, Watson JG, Mauderly JL, Costa DL, Wyzga RE, Vedal S, Hidy GM, Altshuler SL, Marrack D, Heuss JM, Wolff GT, Pope CR, Dockery DW (2006) Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc. 56:709–742. https://doi.org/10.1080/10473289.2006.10464545
Coker E, Ghosh J, Jerrett M, Gomez-Rubio V, Beckerman B, Cockburn M, Liverani S, Su J, Li A, Kile ML, Ritz B, Molitor J (2015) Modeling spatial effects of PM(2.5) on term low birth weight in Los Angeles County. Environ Res. 142:354–364. https://doi.org/10.1016/j.envres.2015.06.044
Correa A, Botto L, Liu Y, Mulinare J, Erickson JD (2003) Do multivitamin supplements attenuate the risk for diabetes-associated birth defects? Pediatrics. 111:1146–1151
Ejaz S, Ashraf M, Nawaz M, Lim CW, Kim B (2009)Anti-angiogenic and teratological activities associated with exposure to total particulate matter from commercial cigarettes. Food Chem Toxicol. 47:368–376. https://doi.org/10.1016/j.fct.2008.11.029
Girguis MS, Strickland MJ, Hu X, Liu Y, Bartell SM, Vieira VM (2016) Maternal exposure to traffic-related air pollution and birth defects in Massachusetts. Environ Res. 146:1–9. https://doi.org/10.1016/j.envres.2015.12.010
Guan WJ, Zheng XY, Chung KF, Zhong NS (2016) Impact of air pollution on the burden of chronic respiratory diseases in China: time for urgent action. Lancet. 388:1939–1951. https://doi.org/10.1016/S0140-6736(16)31597-5
Hu CY, Huang K, Fang Y, Yang XJ, Ding K, Jiang W, Hua XG, Huang DY, Jiang ZX, Zhang XJ (2020) Maternal air pollution exposure and congenital heart defects in offspring: a systematic review and meta-analysis. Chemosphere. 253:126668. https://doi.org/10.1016/j.chemosphere.2020.126668
Huang J, Okuka M, McLean M, Keefe DL, Liu L (2009) Effects of cigarette smoke on fertilization and embryo development in vivo. Fertil Steril. 92:1456–1465. https://doi.org/10.1016/j.fertnstert.2008.07.1781
Huang YH, Wu QJ, Chen YL, Jiang CZ, Gong TT, Li J, Li LL, Zhou C (2018) Trends in the prevalence of congenital hydrocephalus in 14 cities in Liaoning province, China from 2006 to 2015 in a population-based birth defect registry from the Liaoning Women and Children’s Health Hospital. Oncotarget 9:14472–14480. https://doi.org/10.18632/oncotarget.24239
International Clearinghouse for Birth Defects Surveillance and Research (ICBDSR). Annual Report 2006 with data for 2004. Roma: The International Centre on Birth Defects, 2006
Jezek P, Hlavata L (2005) Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int J Biochem Cell Biol. 37:2478–2503. https://doi.org/10.1016/j.biocel.2005.05.013
Jin L, Qiu J, Zhang Y, Qiu W, He X, Wang Y, Sun Q, Li M, Zhao N, Cui H, Liu S, Tang Z, Chen Y, Yue L, Da Z, Xu X, Huang H, Liu Q, Bell ML, Zhang Y (2015) Ambient air pollution and congenital heart defects in Lanzhou. China. Environ Res Lett. 10. https://doi.org/10.1088/1748-9326/10/7/074005
Liu FH, Dai HX, Gong TT, Zhang JY, Li J, Chen ZJ, Li LL, Chen YL, Liu S, Jiang CZ, Huang YH, Zhao YH, Wu QJ (2020) Maternal preconception and first trimester exposure to PM10 and the risk of oral clefts in offspring: a population-based, case-control study. Occup Environ Med. 77:721–727. https://doi.org/10.1136/oemed-2020-106434
Mainolfi MB, Salihu HM, Wilson RE, Mbah AK (2013)Low-level exposure to air pollution and risk of adverse birth outcomes in Hillsborough County. Florida. J Occup Environ Med. 55:490–494. https://doi.org/10.1097/JOM.0b013e31828df013
Maisonet M, Correa A, Misra D, Jaakkola JJ (2004) A review of the literature on the effects of ambient air pollution on fetal growth. Environ Res. 95:106–115. https://doi.org/10.1016/j.envres.2004.01.001
Massarsky A, Jayasundara N, Bailey JM, Oliveri AN, Levin ED, Prasad GL, Di Giulio RT (2015) Teratogenic, bioenergetic, and behavioral effects of exposure to total particulate matter on early development of zebrafish (Danio rerio) are not mimicked by nicotine. Neurotoxicol Teratol. 51:77–88. https://doi.org/10.1016/j.ntt.2015.09.006
Morris JK, Springett AL, Greenlees R, Loane M, Addor MC, Arriola L, Barisic I, Bergman JEH, Csaky-Szunyogh M, Dias C, Draper ES, Garne E, Gatt M, Khoshnood B, Klungsoyr K, Lynch C, McDonnell R, Nelen V, Neville AJ et al (2018) Trends in congenital anomalies in Europe from 1980 to 2012. PLoS One. 13:e0194986. https://doi.org/10.1371/journal.pone.0194986
Ritz B, Wilhelm M, Hoggatt KJ, Ghosh JK (2007) Ambient air pollution and preterm birth in the environment and pregnancy outcomes study at the University of California. Los Angeles. Am J Epidemiol. 166:1045–1052. https://doi.org/10.1093/aje/kwm181
Salavati N, Strak M, Burgerhof J, de Walle H, Erwich J, Bakker MK (2018) The association of air pollution with congenital anomalies: an exploratory study in the northern Netherlands. Int J Hyg Environ Health. 221:1061–1067. https://doi.org/10.1016/j.ijheh.2018.07.008
Schembari A, Nieuwenhuijsen MJ, Salvador J, de Nazelle A, Cirach M, Dadvand P, Beelen R, Hoek G, Basagana X, Vrijheid M (2014)Traffic-related air pollution and congenital anomalies in Barcelona. Environ Health Perspect. 122:317–323. https://doi.org/10.1289/ehp.1306802
Song C, Wu L, Xie Y, He J, Chen X, Wang T, Lin Y, Jin T, Wang A, Liu Y, Dai Q, Liu B, Wang YN, Mao H (2017) Air pollution in China: status and spatiotemporal variations. Environ Pollut. 227:334–347. https://doi.org/10.1016/j.envpol.2017.04.075
Stoll C, Alembik Y, Roth MP, Dott B (1997) Risk factors in congenital anal atresias. Ann Genet. 40:197–204. https://doi.org/10.7499/j.issn.1008-8830.2016.06.014
Teng C, Wang Z, Yan B (2016) Fine particle-induced birth defects: impacts of size, payload, and beyond. Birth Defects Res C Embryo Today. 108:196–206. https://doi.org/10.1002/bdrc.21136
Theron A, Numanoglu A (2017) Birth prevalence of anorectal malformations for the Western Cape Province, South Africa, 2005 to 2012. Eur J Pediatr Surg. 27:449–454. https://doi.org/10.1055/s-0036-1597945
Vinceti M, Malagoli C, Malavolti M, Cherubini A, Maffeis G, Rodolfi R, Heck JE, Astolfi G, Calzolari E, Nicolini F (2016) Does maternal exposure to benzene and PM10 during pregnancy increase the risk of congenital anomalies? A population-based case-control study. Sci Total Environ. 541:444–450. https://doi.org/10.1016/j.scitotenv.2015.09.051
Waller DK, Shaw GM, Rasmussen SA, Hobbs CA, Canfield MA, Siega-Riz AM, Gallaway MS, Correa A (2007) Prepregnancy obesity as a risk factor for structural birth defects. Arch Pediatr Adolesc Med. 161:745–750. https://doi.org/10.1001/archpedi.161.8.745
Wang C, Li L, Cheng W (2015) Anorectal malformation: the etiological factors. Pediatr Surg Int. 31:795–804. https://doi.org/10.1007/s00383-015-3685-0
Wang L, Xiang X, Mi B, Song H, Dong M, Zhang S, Bi Y, Zhao Y, Li Q, Zhang Q, Zhang L, Yan H, Wang D, Dang S (2019) Association between early prenatal exposure to ambient air pollution and birth defects: evidence from newborns in Xi’an. China. J Public Health (Oxf). 41:494–501. https://doi.org/10.1093/pubmed/fdy137
Xu L, Li X, Dai L, Yuan X, Liang J, Zhou G, Li Q, He C, Miao L, Wang Y, Zhu J (2011) Assessing the trend of gastroschisis prevalence in China from 1996 to 2007 using two analytical methods. Birth Defects Res A Clin Mol Teratol. 91:177–184. https://doi.org/10.1002/bdra.20753
Yu X, Du Z, Sun X, Shi C, Zhang H, Hu T (2015) Aberrant Cosmc genes result in Tn antigen expression in human colorectal carcinoma cell line HT-29. Int J Clin Exp Pathol. 8:2590–2602
Zhang JY, Gong TT, Huang YH, Li J, Liu S, Chen YL, Li LL, Jiang CZ, Chen ZJ, Wu QJ (2020a) Association between maternal exposure to PM10 and polydactyly and syndactyly: a population-based case-control study in Liaoning province. China. Environ Res. 187:109643. https://doi.org/10.1016/j.envres.2020.109643
Zhang JY, Wu QJ, Huang YH, Li J, Liu S, Chen YL, Li LL, Jiang CZ, Chen ZJ (2020b) Association between maternal exposure to ambient PM10 and neural tube defects: a case-control study in Liaoning Province. China. Int J Hyg Environ Health. 225:113453. https://doi.org/10.1016/j.ijheh.2020.113453
Zhang, T. N., Gong, T. T., Chen, Y. L., Wu, Q. J., Zhang, Y., Jiang, C. Z., Li, J., Li, L. L., Zhou, C., Huang, Y. H., 2017. Time trends in the prevalence and epidemiological characteristics of neural tube defects in Liaoning Province, China, 2006-2015: a population-based study. Oncotarget. 8, 17092-17104. 10.18632/oncotarget.15060
Zhu Y, Zhang C, Liu D, Grantz KL, Wallace M, Mendola P (2015) Maternal ambient air pollution exposure preconception and during early gestation and offspring congenital orofacial defects. Environ Res. 140:714–720. https://doi.org/10.1016/j.envres.2015.06.002
Funding
This study was supported by the Liaoning Providence Science and Technology Project (2015225025 for Yan-Hong Huang) and the Shenyang Science and Technology Project (F15-139-9-09 for Yan-Hong Huang).
Author information
Authors and Affiliations
Contributions
Tie-Ning Zhang: writing—original draft preparation. Qi-Jun Wu: writing—reviewing and editing. Yan-Hong Huang: conceptualization and methodology. Jing Li: data curation. Zong-Jiao Chen: validation. Li-Li Li: software. Yan-Ling Chen: investigation. Shu Liu: visualization. Cheng-Zhi Jiang: software. Yu-Hong Zhao: supervision.
Corresponding authors
Ethics declarations
Ethics approval
This study has been approved by the Institutional Review Board of Liaoning Women and Children’s Health Hospital.
Consent to participate
Informed written consent was taken voluntarily from each eligible participant.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 1402 kb)
Rights and permissions
About this article
Cite this article
Zhang, TN., Wu, QJ., Huang, YH. et al. Association between maternal exposure to PM10 and risk of anorectal atresia/stenosis in offspring: a population-based case-control study in Liaoning Province, China. Environ Sci Pollut Res 29, 21328–21338 (2022). https://doi.org/10.1007/s11356-021-16573-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16573-9