Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Air pollution-induced missed abortion risk for pregnancies

Nature Sustainability volume 2, pages 1011–1017 (2019)Cite this article

Subjects

Abstract

Fetus death risk reduction is included in the United Nations Sustainable Development Goals. However, little is known about how missed abortion in the first trimester (MAFT) is related to maternal air pollution exposure. We quantify the link between air pollution exposure and MAFT in Beijing, China, a region with severe MAFT and air quality problems. We analyse the records of 255,668 pregnant women from 2009 to 2017 and contrast them with maternal exposure to air pollutants (particulate matter PM2.5, SO2, O3 and CO). We adjust for confounding factors such as sociodemographic characteristics, spatial autocorrelation and ambient temperature. We find that, for all four pollutants, an increased risk of MAFT is associated with rises in pollutant concentrations and the adjusted odds ratios (ORs) of these associations increase with higher concentrations. For example, the adjusted OR of MAFT risk for a 10.0 μg m−3 increase in SO2 exposure is between 1.29 and 1.41 at concentrations of 7.1–19.5 μg m−3; it drops to 1.17 below this range and rises to 1.52 above it at higher SO2 concentrations. This means that the risk increase is not linear but becomes more severe the higher the pollutant concentration. The findings provide evidence linking fetus disease burden and maternal air pollution exposure.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The ORs and 95% CIs of MAFT associated with maternal exposure to each pollutant in Phase 4.
Fig. 2: The ORs and 95% CIs of the MAFT risks associated with maternal exposure to different average annual air pollutant concentrations.

Similar content being viewed by others

Data availability

The collected data are available from the corresponding authors on reasonable request.

Code availability

The source code is available from the corresponding authors on reasonable request. It is copyrighted by Beijing Normal University and Beijing Obstetrics and Gynecology Hospital and is to be used only for educational and research purposes. Any commercial use is prohibited.

References

  1. Cohen, A. J. et al. Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: an analysis of data from the Global Burden of Diseases Study. Lancet 389, 1907–1918 (2015).

    Google Scholar 

  2. Jing, H. et al. Health impact of China’s air pollution prevention and control action plan: an analysis of national air quality monitoring and mortality data. Lancet Planet. Health 2, e313–e323 (2018).

    Google Scholar 

  3. Shah, P. S. et al. Air pollution and birth outcomes: a systematic review. Environ. Int. 37, 498–516 (2011).

    CAS  Google Scholar 

  4. Malley, C. S. et al. Preterm birth associated with maternal fine particulate matter exposure: a global, regional and national assessment. Environ. Int. 101, 173–182 (2017).

    Google Scholar 

  5. Brook, R. D. et al. Insights into the mechanisms and mediators of the effects of air pollution exposure on blood pressure and vascular function in healthy humans. Hypertension 54, 659–667 (2009).

    CAS  Google Scholar 

  6. Dadvand, P. et al. Ambient air pollution and preeclampsia: a spatiotemporal analysis. Environ. Health Perspect. 121, 1365–1371 (2013).

    Google Scholar 

  7. Ha, S. et al. Ambient air pollution and the risk of pregnancy loss: a prospective cohort study. Fertil. Steril. 109, 148–153 (2017).

    Google Scholar 

  8. Gemzell-Danielsson, K. et al. Misoprostol to treat missed abortion in the first trimester. Int. J. Gynaecol. Obstet. 99, S182–S185 (2007).

    CAS  Google Scholar 

  9. Steer, C. et al. Spontaneous abortion rates after natural and assisted conception. BMJ 299, 1317–1318 (1989).

    CAS  Google Scholar 

  10. Daya, S. in Textbook of Gynecology (ed. Copeland, L. J.) 227–271 (WB Saunder, 2000).

  11. Wood, S. Medical management of missed abortion: a randomized clinical trial. Obstet. Gynecol. 99, 563–566 (2002).

    CAS  Google Scholar 

  12. Farah, S. & Lucy, K. Intrauterine fetal death. Obstet. Gynaecol. Reprod. Med. 19, 1–6 (2009).

    Google Scholar 

  13. Green, R. S. et al. Residential exposure to traffic and spontaneous abortion. Environ. Health Perspect. 117, 1939–1944 (2009).

    CAS  Google Scholar 

  14. Defranco, E. et al. Air pollution and stillbirth risk: exposure to airborne particulate matter during pregnancy is associated with fetal death. PLoS ONE 10, e0120594 (2015).

    Google Scholar 

  15. Hou, H. Y. et al. Does ambient air pollutants increase the risk of fetal loss? A case-control study. Arch. Gynecol. Obstet. 289, 285–291 (2014).

    CAS  Google Scholar 

  16. Liang, X. et al. PM2.5 data reliability, consistency, and air quality assessment in five Chinese cities. J. Geophys. Res. Atmos. 121, 10220–10236 (2016).

    CAS  Google Scholar 

  17. Ji, J. Air pollution and China’s ageing society. Lancet Public Health 3, e457–e458 (2018).

    Google Scholar 

  18. Bowe, B. et al. The 2016 global and national burden of diabetes mellitus attributable to PM2.5, air pollution. Lancet Planet. Health 2, e301–e312 (2018).

    Google Scholar 

  19. Chen, H. Living near major roads and the incidence of dementia, Parkinson’s disease, and multiple sclerosis: a population-based cohort study. Lancet 389, 718–726 (2017).

    Google Scholar 

  20. Smith, R. et al. Impact of London’s road traffic air and noise pollution on birth weight: retrospective population based cohort study. BMJ 359, j5299 (2017).

    Google Scholar 

  21. Wang, Y. et al. Association of long-term exposure to airborne particulate matter of 1 μm or less with preterm birth in China. JAMA Pediatr. 8, e174872 (2018).

    Google Scholar 

  22. Mahalingaiah, S. et al. Perimenarchal air pollution exposure and menstrual disorders. Hum. Reprod. 33, 512–519 (2018).

    CAS  Google Scholar 

  23. Wakefield, J. Bayes factors for genome-wide association studies: comparison with P-values. Genet. Epidemiol. 33, 79–86 (2009).

    Google Scholar 

  24. Lee, M. D. & Wagenmakers, E.-J. Bayesian Cognitive Modeling: A Practical Course (Cambridge Univ. Press, 2013).

  25. Schönbrodt, F. D. & Wagenmakers, E. J. Bayes factor design analysis: planning for compelling evidence. Psychon. Bull. Rev. 25, 128–142 (2018).

    Google Scholar 

  26. Patt, A. G. et al. Estimating least-developed countries’ vulnerability to climate-related extreme events over the next 50 years. Proc. Natl Acad. Sci. USA 107, 1333–1337 (2010).

    CAS  Google Scholar 

  27. Smith, K. R. et al. in Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) 709–794 (Cambridge Univ. Press, 2014).

  28. Weinberg, C. R., Moledor, E. & Baird, D. D. Is there a seasonal pattern in risk of early-pregnancy loss. Epidemiology 5, 484–489 (1994).

    CAS  Google Scholar 

  29. Ciaula, A. & Bilancia, M. Relationships between mild PM10 and ozone urban air levels and spontaneous abortion: clues for primary prevention. Int. J. Environ. Health Res. 25, 640–655 (2015).

    Google Scholar 

  30. Enkhmaa, D. et al. Seasonal ambient air pollution correlates strongly with spontaneous abortion in Mongolia. BMC Pregnancy Childbirth 14, 146 (2014).

    Google Scholar 

  31. Slama, R. et al. Meeting report: atmospheric pollution and human reproduction. Environ. Health Perspect. 116, 791–798 (2008).

    Google Scholar 

  32. Faiz, A. S. et al. Does ambient air pollution trigger stillbirth? Epidemiology 24, 538–544 (2013).

    Google Scholar 

  33. Siddika, N. et al. Prenatal ambient air pollution exposure and the risk of stillbirth: systematic review and meta-analysis of the empirical evidence. Occup. Environ. Med. 73, 573–581 (2016).

    Google Scholar 

  34. Tsamou., M. et al. Air pollution-induced placental epigenetic alterations in early life: a candidate miRNA approach. Epigenetics 13, 135–146 (2016).

    Google Scholar 

  35. Stillerman, K. P. et al. Environmental exposures and adverse pregnancy outcomes: a review of the science. Reprod. Sci. 15, 631–650 (2008).

    Google Scholar 

  36. Perera, F. P. et al. Molecular epidemiologic research on the effects of environmental pollutants on the fetus. Environ. Health Perspect. 107(suppl 3), 451–460 (1999).

    CAS  Google Scholar 

  37. Byrne, J. et al. Morphology of early fetal deaths and their chromosomal characteristics. Teratology 32, 297–315 (1985).

    CAS  Google Scholar 

  38. Šrám, R. J. et al. Ambient air pollution and pregnancy outcomes: a review of the literature. Environ. Health Perspect. 113, 375–382 (2005).

    Google Scholar 

  39. Hardy, K. R. & Thom, S. R. Pathophysiology and treatment of carbon monoxide poisoning. J. Toxicol. Clin. Toxicol. 32, 613–629 (1994).

    CAS  Google Scholar 

  40. Ziaei, S. et al. Effects of carbon monoxide air pollution in pregnancy on neonatal nucleated red blood cells. Paediatr. Perinat. Epidemiol. 19, 27–30 (2005).

    Google Scholar 

  41. Singh, J. & Scott, L. H. Threshold for carbon monoxide induced fetotoxicity. Teratology 30, 253–257 (1984).

    CAS  Google Scholar 

  42. Grace, K. Considering climate in studies of fertility and reproductive health in poor countries. Nat. Clim. Change 7, 479–485 (2017).

    Google Scholar 

  43. Li, X. et al. A new global land-use and land-cover change product at a 1-km resolution for 2010–2100 based on human–environment interactions. Ann. Am. Assoc. Geogr. 107, 1040–1059 (2017).

    Google Scholar 

  44. International Statistical Classification of Diseases and Related Health Problems 10th revision (WHO, 2007).

  45. Altman D. G. Practical Statistics for Medical Research (Chapman and Hall, 1991).

  46. Technical Regulation on Ambient Air Quality Index (on Trial). (Ministry of Environmental Protection of the People’s Republic of China, 2012).

  47. Liu, M. Y. et al. Spatiotemporal variability of NO2 and PM2.5 over Eastern China: observational and model analyses with a novel statistical method. Atmos. Chem. Phys. Discuss. 18, 12933–12952 (2018).

    CAS  Google Scholar 

  48. Zhang, L. et al. Air pollution exposure associates with increased risk of neonatal jaundice. Nat. Commun. 10, 6741 (2019).

  49. Desquilbet, L. & Mariotti, F. Dose–response analyses using restricted cubic spline functions in public health research. Stat. Med. 29, 1037–1057 (2010).

    Google Scholar 

Download references

Acknowledgements

This work was carried out with the support of the National Key Research and Development Program of China (grant no. 2018YFC0213600), the National Natural Science Foundation of China (grant nos. 41775115 and 41371324) and the Beijing Natural Science Foundation (grant no. 7173258).

Author information

Author notes

  1. These authors contributed equally: Liqiang Zhang, Weiwei Liu, Kun Hou.

Authors and Affiliations

  1. State Key Laboratory of Remote Sensing Science, Faculty of Geographical Science, Beijing Normal University, Beijing, China

    Liqiang Zhang, Kun Hou, Ziye Wang, Yuebin Wang, Yanxiao Jiang, Yibo Zheng, Suhong Liu & Panpan Zhu

  2. Beijing Obstetrics and Gynecology Hospital, Capital Medical University, Beijing, China

    Weiwei Liu & Yonglian Lan

  3. Laboratory for Climate and Ocean-Atmosphere Studies, Department of Atmospheric and Oceanic Sciences, School of Physics, Peking University, Beijing, China

    Jintai Lin, Ziwei Wang, Ruijing Ni & Mengyao Liu

  4. State Key Laboratory of Resources and Environment Information System, Institute of Geographical Science and Natural Resources, Chinese Academy of Sciences, Beijing, China

    Chenghu Zhou

  5. School of Surveying and Geo-informatics, Tongji University, Shanghai, China

    Xiaohua Tong

Authors
  1. Liqiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weiwei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kun Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jintai Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chenghu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaohua Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ziye Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuebin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yanxiao Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ziwei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yibo Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yonglian Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Suhong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Ruijing Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Mengyao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Panpan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L.Z. and W.L. jointly designed the study, collected data, performed the analysis and wrote the manuscript. K.H. contributed to the model of the paper. J.L. contributed to the research framework, provided air pollution and meteorological data, contributed to results analysis and edited the paper. C.Z. and X.T. improved the research framework and edited the paper. Z.Y.W., Y.B.W. and Y.L. organized the neonatal and maternal datasets. Z.W.W., R.N. and M.L. generated the air pollution and meteorological datasets. Y.J., Y.Z., S.L. and P.Z. developed the maps and edited figures.

Corresponding authors

Correspondence to Liqiang Zhang, Jintai Lin or Chenghu Zhou.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–12 and Tables 1–8.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, L., Liu, W., Hou, K. et al. Air pollution-induced missed abortion risk for pregnancies. Nat Sustain 2, 1011–1017 (2019). https://doi.org/10.1038/s41893-019-0387-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41893-019-0387-y

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene