Association between bisphenol A levels during pregnancy and spontaneous abortion: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

ZOU Xuanmin ^1,2 , CHEN Chen ^1,2 , GUAN Tianyue ^1,2 ,  HAO Jiahu ^1,2

1. School of Public Health, Anhui Medical University, Hefei 230032, P. R. China;
2. MOE Key Laboratory of Population Health Across Life Cycle, NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Provincial Key Laboratory of Population Health and Aristogenics, Hefei 230032, P. R. China;

Corresponding author：

HAO Jiahu, Email: jia7218@126.com

Keywords：

Bisphenol A; Spontaneous abortion; Meta-analysis; Case-control study; Cohort study

DOI：

10.7507/1672-2531.202205002

Video：

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Objective To systematically review the association between exposure to bisphenol A during pregnancy and spontaneous abortion. Methods The PubMed, Web of Science, EMbase, CNKI, WanFang Data and VIP databases were electronically searched to identify cohort studies and case-control studies related to bisphenol A exposure and spontaneous abortion from inception to April 1^st, 2022. Two reviewers independently screened the literature, extracted data, and assessed the risk of bias of the included studies. Meta-analysis was then performed using Stata 16.0 software. Results A total of 7 case-control studies and 1 cohort study were included, with a total of 1 179 subjects. The results of meta-analysis showed that there was a statistically significant difference in bisphenol A concentrations between the spontaneous abortion group and the control group regardless of whether the sample source was serum or urine (SMD_serum=1.05, 95%CI 0.34 to 1.77, P=0.004; SMD_urine=0.20, 95%CI 0.02 to 0.38, P=0.027). Conclusion The current evidence shows that exposure to bisphenol A during pregnancy may lead to unexplained recurrent spontaneous abortion. Due to the limited quantity and quality of the included studies, more high-quality studies are needed to verify the above conclusion.

Citation： ZOU Xuanmin, CHEN Chen, GUAN Tianyue, HAO Jiahu. Association between bisphenol A levels during pregnancy and spontaneous abortion: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2022, 22(10): 1149-1154. doi: 10.7507/1672-2531.202205002 Copy

1.	赵艳辉, 庞泓, 高铭, 等. 早期自然流产的遗传学因素分析. 中国优生与遗传杂志, 2019, 27(1): 55-57,65.
2.	ESHRE Guideline Group on RPL, Bender AR, Christiansen OB, et al. ESHRE guideline: recurrent pregnancy loss. Hum Reprod Open, 2018, 2018(2): hoy004.
3.	Rai R, Regan L. Recurrent miscarriage. Lancet, 2006, 368(9535): 601-611.
4.	Zhang C, Deng X, Zhang X, et al. Association between serum TNF-α levels and recurrent spontaneous miscarriage: a meta-analysis. Am J Reprod Immunol, 2016, 75(2): 86-93.
5.	Zhu D, Zou H, Liu J, et al. Inhibition of HMGB1 ameliorates the maternal-fetal interface destruction in unexplained recurrent spontaneous abortion by suppressing pyroptosis activation. Front Immunol, 2021, 12: 782792.
6.	Pei CZ, Kim YJ, Baek KH. Pathogenetic factors involved in recurrent pregnancy loss from multiple aspects. Obstet Gynecol Sci, 2019, 62(4): 212-223.
7.	Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev, 2009, 30(4): 293-342.
8.	吴海瑛, 陈临琪, 王凤云, 等. 双酚A与女童性早熟的关系. 临床儿科杂志, 2015, (2): 155-159.
9.	Vandenberg LN, Hauser R, Marcus M, et al. Human exposure to bisphenol A (BPA). Reprod Toxicol, 2007, 24(2): 139-177.
10.	Schönfelder G, Wittfoht W, Hopp H, et al. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect, 2002, 110(11): A703-707.
11.	Sugiura-Ogasawara M, Ozaki Y, Sonta S, et al. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod, 2005, 20(8): 2325-2329.
12.	刘银梅. 双酚A与不明原因复发性流产的1: 2病例-对照研究. 苏州: 苏州大学, 2011.
13.	郑艳敏, 王燕, 赵静, 等. 血清双酚A含量与复发性流产的1: 2病例对照研究. 中华流行病学杂志, 2012, 33(8): 841-845.
14.	郑艳敏. 尿液/血清中双酚A水平与不明原因复发性流产风险关系的比较研究. 苏州: 苏州大学, 2013.
15.	Lathi RB, Liebert CA, Brookfield KF, et al. Conjugated bisphenol A in maternal serum in relation to miscarriage risk. Fertil Steril, 2014, 102(1): 123-128.
16.	李娜. 双酚A对稽留流产影响及其相关机制研究. 长春: 吉林大学, 2014.
17.	Shen Y, Zheng Y, Jiang J, et al. Higher urinary bisphenol A concentration is associated with unexplained recurrent miscarriage risk: evidence from a case-control study in eastern China. PLoS One, 2015, 10(5): e0127886.
18.	谢倩. 环境雌激素双酚A对女性生殖功能的影响. 泰安: 泰山医学院, 2016.
19.	Peng F, Ji W, Zhu F, et al. A study on phthalate metabolites, bisphenol A and nonylphenol in the urine of Chinese women with unexplained recurrent spontaneous abortion. Environ Res, 2016, 150: 622-628.
20.	王明远, 陈诚, 潘峰, 等. 双酚A与不明原因复发性流产发生关系的病例对照研究. 第三军医大学学报, 2017, 39(6): 579-583.
21.	Ao J, Huo X, Zhang J, et al. Environmental exposure to bisphenol analogues and unexplained recurrent miscarriage: a case-control study. Environ Res, 2022, 204(Pt C): 112293.
22.	自然流产诊治中国专家共识编写组. 自然流产诊治中国专家共识(2020年版). 中国实用妇科与产科杂志, 2020, 36(11): 1082-1090.
23.	Hahn RG, Yanase F, Zdolsek JH, et al. Serum creatinine levels and Nephrocheck® values with and without correction for urine dilution-a multicenter observational study. Front Med (Lausanne), 2022, 9: 847129.
24.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
25.	Luo D, Wan X, Liu J, et al. Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Stat Methods Med Res, 2018, 27(6): 1785-1805.
26.	Wan X, Wang W, Liu J, et al. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol, 2014, 14: 135.
27.	刘东苹. 流产后关爱门诊护理对女性重复流产的控制及避孕依从性的影响观察. 实用妇科内分泌电子杂志, 2019, 6(18): 161,166.
28.	Whitley CE, Rose SB, Sim D, et al. Association between women's use of long-acting reversible contraception and declining abortion rates in New Zealand. J Womens Health (Larchmt), 2020, 29(1): 21-28.
29.	Kosarac I, Kubwabo C, Lalonde K, et al. A novel method for the quantitative determination of free and conjugated bisphenol A in human maternal and umbilical cord blood serum using a two-step solid phase extraction and gas chromatography/tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci, 2012, 898: 90-94.
30.	Li Q, Davila J, Kannan A, et al. Chronic exposure to bisphenol A affects uterine function during early pregnancy in mice. Endocrinology, 2016, 157(5): 1764-1774.
31.	Tran DN, Jung EM, Ahn C, et al. Effects of bisphenol A and 4-tert-octylphenol on embryo implantation failure in mouse. Int J Environ Res Public Health, 2018, 15(8): 1614.
32.	Du Y, Chen L, Lin J, et al. Chromosomal karyotype in chorionic villi of recurrent spontaneous abortion patients. Biosci Trends, 2018, 12(1): 32-39.
33.	Ogasawara M, Aoki K, Okada S, et al. Embryonic karyotype of abortuses in relation to the number of previous miscarriages. Fertil Steril, 2000, 73(2): 300-304.
34.	Brieño-Enríquez MA, Reig-Viader R, Cabero L, et al. Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro. Mol Hum Reprod, 2012, 18(4): 171-183.

1. 赵艳辉, 庞泓, 高铭, 等. 早期自然流产的遗传学因素分析. 中国优生与遗传杂志, 2019, 27(1): 55-57,65.
2. ESHRE Guideline Group on RPL, Bender AR, Christiansen OB, et al. ESHRE guideline: recurrent pregnancy loss. Hum Reprod Open, 2018, 2018(2): hoy004.
3. Rai R, Regan L. Recurrent miscarriage. Lancet, 2006, 368(9535): 601-611.
4. Zhang C, Deng X, Zhang X, et al. Association between serum TNF-α levels and recurrent spontaneous miscarriage: a meta-analysis. Am J Reprod Immunol, 2016, 75(2): 86-93.
5. Zhu D, Zou H, Liu J, et al. Inhibition of HMGB1 ameliorates the maternal-fetal interface destruction in unexplained recurrent spontaneous abortion by suppressing pyroptosis activation. Front Immunol, 2021, 12: 782792.
6. Pei CZ, Kim YJ, Baek KH. Pathogenetic factors involved in recurrent pregnancy loss from multiple aspects. Obstet Gynecol Sci, 2019, 62(4): 212-223.
7. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev, 2009, 30(4): 293-342.
8. 吴海瑛, 陈临琪, 王凤云, 等. 双酚A与女童性早熟的关系. 临床儿科杂志, 2015, (2): 155-159.
9. Vandenberg LN, Hauser R, Marcus M, et al. Human exposure to bisphenol A (BPA). Reprod Toxicol, 2007, 24(2): 139-177.
10. Schönfelder G, Wittfoht W, Hopp H, et al. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect, 2002, 110(11): A703-707.
11. Sugiura-Ogasawara M, Ozaki Y, Sonta S, et al. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod, 2005, 20(8): 2325-2329.
12. 刘银梅. 双酚A与不明原因复发性流产的1: 2病例-对照研究. 苏州: 苏州大学, 2011.
13. 郑艳敏, 王燕, 赵静, 等. 血清双酚A含量与复发性流产的1: 2病例对照研究. 中华流行病学杂志, 2012, 33(8): 841-845.
14. 郑艳敏. 尿液/血清中双酚A水平与不明原因复发性流产风险关系的比较研究. 苏州: 苏州大学, 2013.
15. Lathi RB, Liebert CA, Brookfield KF, et al. Conjugated bisphenol A in maternal serum in relation to miscarriage risk. Fertil Steril, 2014, 102(1): 123-128.
16. 李娜. 双酚A对稽留流产影响及其相关机制研究. 长春: 吉林大学, 2014.
17. Shen Y, Zheng Y, Jiang J, et al. Higher urinary bisphenol A concentration is associated with unexplained recurrent miscarriage risk: evidence from a case-control study in eastern China. PLoS One, 2015, 10(5): e0127886.
18. 谢倩. 环境雌激素双酚A对女性生殖功能的影响. 泰安: 泰山医学院, 2016.
19. Peng F, Ji W, Zhu F, et al. A study on phthalate metabolites, bisphenol A and nonylphenol in the urine of Chinese women with unexplained recurrent spontaneous abortion. Environ Res, 2016, 150: 622-628.
20. 王明远, 陈诚, 潘峰, 等. 双酚A与不明原因复发性流产发生关系的病例对照研究. 第三军医大学学报, 2017, 39(6): 579-583.
21. Ao J, Huo X, Zhang J, et al. Environmental exposure to bisphenol analogues and unexplained recurrent miscarriage: a case-control study. Environ Res, 2022, 204(Pt C): 112293.
22. 自然流产诊治中国专家共识编写组. 自然流产诊治中国专家共识(2020年版). 中国实用妇科与产科杂志, 2020, 36(11): 1082-1090.
23. Hahn RG, Yanase F, Zdolsek JH, et al. Serum creatinine levels and Nephrocheck® values with and without correction for urine dilution-a multicenter observational study. Front Med (Lausanne), 2022, 9: 847129.
24. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
25. Luo D, Wan X, Liu J, et al. Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Stat Methods Med Res, 2018, 27(6): 1785-1805.
26. Wan X, Wang W, Liu J, et al. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol, 2014, 14: 135.
27. 刘东苹. 流产后关爱门诊护理对女性重复流产的控制及避孕依从性的影响观察. 实用妇科内分泌电子杂志, 2019, 6(18): 161,166.
28. Whitley CE, Rose SB, Sim D, et al. Association between women's use of long-acting reversible contraception and declining abortion rates in New Zealand. J Womens Health (Larchmt), 2020, 29(1): 21-28.
29. Kosarac I, Kubwabo C, Lalonde K, et al. A novel method for the quantitative determination of free and conjugated bisphenol A in human maternal and umbilical cord blood serum using a two-step solid phase extraction and gas chromatography/tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci, 2012, 898: 90-94.
30. Li Q, Davila J, Kannan A, et al. Chronic exposure to bisphenol A affects uterine function during early pregnancy in mice. Endocrinology, 2016, 157(5): 1764-1774.
31. Tran DN, Jung EM, Ahn C, et al. Effects of bisphenol A and 4-tert-octylphenol on embryo implantation failure in mouse. Int J Environ Res Public Health, 2018, 15(8): 1614.
32. Du Y, Chen L, Lin J, et al. Chromosomal karyotype in chorionic villi of recurrent spontaneous abortion patients. Biosci Trends, 2018, 12(1): 32-39.
33. Ogasawara M, Aoki K, Okada S, et al. Embryonic karyotype of abortuses in relation to the number of previous miscarriages. Fertil Steril, 2000, 73(2): 300-304.
34. Brieño-Enríquez MA, Reig-Viader R, Cabero L, et al. Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro. Mol Hum Reprod, 2012, 18(4): 171-183.

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