Endocrine disruptors and female fertility: a review of pesticide and plasticizer effects

Abstract

An ongoing interest in environmental exposures and female fertility has led to an increasing number of studies focusing on endocrine-disrupting chemicals (EDCs). Both natural and synthetic compounds have the ability to impact reproductive health by altering the structure and/or function of genes and proteins that facilitate normal ovarian and endometrial functions. This mini-review aims to summarize the effects of some of the most common EDCs on female fertility, including the effects of pesticides and plasticizer alternatives (phthalates, bisphenol A), based on available data in human studies. A literature search was performed using the key words “pesticides, fertility, reproduction, plasticizers, bisphenol A, phthalate, miscarriage, and in vitro fertilization.” The data supporting EDCs’ role in female infertility remain limited, but existing evidence suggests that exposure may have an adverse impact. Accumulating evidence in animal studies provides important insights into the mechanisms underlying EDC effects. As dose-response dynamics are better elucidated, understanding the effects of EDCs on female fertility will help in the development of guidelines for both industry and individuals. An ongoing interest in environmental exposures and female fertility has led to an increasing number of studies focusing on endocrine-disrupting chemicals (EDCs). Both natural and synthetic compounds have the ability to impact reproductive health by altering the structure and/or function of genes and proteins that facilitate normal ovarian and endometrial functions. This mini-review aims to summarize the effects of some of the most common EDCs on female fertility, including the effects of pesticides and plasticizer alternatives (phthalates, bisphenol A), based on available data in human studies. A literature search was performed using the key words “pesticides, fertility, reproduction, plasticizers, bisphenol A, phthalate, miscarriage, and in vitro fertilization.” The data supporting EDCs’ role in female infertility remain limited, but existing evidence suggests that exposure may have an adverse impact. Accumulating evidence in animal studies provides important insights into the mechanisms underlying EDC effects. As dose-response dynamics are better elucidated, understanding the effects of EDCs on female fertility will help in the development of guidelines for both industry and individuals. Discuss: You can discuss this article with its authors and other readers at https://www.fertstertdialog.com/posts/xfre-d-21-00206 Endocrine-disrupting chemicals (EDCs) comprise a diverse group of chemical compounds that have recently become a topic of interest because of their potentially harmful effects on human health. Some EDCs are naturally occurring compounds; however, most EDCs are synthetic and were released into the environment without any prior knowledge of their effects on human and animal health. These natural and synthetic compounds have the ability to alter the actions of endogenous hormones and as a result, EDCs may disrupt the functions of the endocrine system. Although the term “endocrine disruptor” was first proposed 30 years ago, the United States Environmental Protection Agency has now identified 1,482 man-made chemicals that are considered EDCs (1Green M.P. Harvey A.J. Finger B.J. Tarulli G.A. Endocrine disrupting chemicals: impacts on human fertility and fecundity during the peri-conception period.Environ Res. 2021; 194: 110694Crossref PubMed Scopus (33) Google Scholar). More recently, the American College of Obstetricians and Gynecologists has partnered with the American Society for Reproductive Medicine to publish committee opinion regarding EDCs and reproductive health (2Segal T.R. Giudice L.C. Before the beginning: environmental exposures and reproductive and obstetrical outcomes.Fertil Steril. 2019; 112: 613-621Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). Despite their identification, understanding their mechanism of action and potential negative health implications remain incomplete. This review will focus on the effects of 2 common classes of EDCs on female fertility. An exhaustive review of EDCs and female reproduction and fertility is beyond the scope of this mini-review; our aim is to summarize the effects of 2 of the most common EDCs—pesticides and plasticizer alternatives (phthalates, bisphenol A [BPA])—on the basis of available data in human studies (Table 1) (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google Scholar, 4Chevrier C. Warembourg C. Gaudreau E. Monfort C. Le Blanc A. Guldner L. et al.Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to-pregnancy.Epidemiology. 2013; 24: 251-260Crossref PubMed Scopus (60) Google Scholar, 5Petro E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google Scholar, 6Venners S.A. Korrick S. Xu X. Chen C. Guang W. Huang A. et al.Preconception serum DDT and pregnancy loss: a prospective study using a biomarker of pregnancy.Am J Epidemiol. 2005; 162: 709-716Crossref PubMed Scopus (76) Google Scholar, 7Jirsová S. Masata J. Jech L. Zvárová J. Effect of polychlorinated biphenyls (PCBs) and 1,1,1-trichloro-2,2,-bis (4-chlorophenyl)-ethane (DDT) in follicular fluid on the results of in vitro fertilization-embryo transfer (IVF-ET) programs.Fertil Steril. 2010; 93: 1831-1836Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar, 8Williams A.L. Watson R.E. DeSesso J.M. Developmental and reproductive outcomes in humans and animals after glyphosate exposure: a critical analysis.J Toxicol Environ Health B Crit Rev. 2012; 15: 39-96Crossref PubMed Scopus (99) Google Scholar, 9Mok-Lin E. Ehrlich S. Williams P.L. Petrozza J. Wright D.L. Calafat A.M. et al.Urinary bisphenol A concentrations and ovarian response among women undergoing IVF.Int J Androl. 2010; 33: 385-393Crossref PubMed Scopus (90) Google Scholar, 10Ehrlich S. Williams P.L. Missmer S.A. Flaws J.A. Ye X. Calafat A.M. et al.Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF.Hum Reprod. 2012; 27: 3583-3592Crossref PubMed Scopus (180) Google Scholar, 11Deng T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google Scholar, 12Lathi R.B. Liebert C.A. Brookfield K.F. Taylor J.A. vom Saal F.S. Fujimoto V.Y. et al.Conjugated bisphenol A in maternal serum in relation to miscarriage risk.Fertil Steril. 2014; 102: 123-128Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 13Shen Y. Zheng Y. Jiang J. Liu Y. Luo X. Shen Z. 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; 10e0127886Google Scholar, Y. S. T. to bisphenol A is associated with recurrent Reprod. 2005; PubMed Scopus Google Scholar, A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google Scholar, M.P. exposure to and and to the on Environmental Steril. 2015; Full Text Full Text PDF PubMed Scopus (79) Google Scholar, L. Gaskins A.J. Y.H. Williams P.L. S. et al.Urinary bisphenol A concentrations and with in vitro outcomes among women from a fertility Reprod. 2015; PubMed Scopus Google Scholar, Gaskins A.J. Souter I. S. et al.Urinary phthalate concentrations and reproductive outcomes among women undergoing in vitro results from the Health PubMed Scopus Google Scholar, A.M. J. et exposure to and to a first pregnancy Reprod. Google Scholar, K.F. effects on oocyte Reprod. 2021; PubMed Scopus Google of pesticides and on female on female on female and pregnancy and (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google and number of C. Warembourg C. Gaudreau E. Monfort C. Le Blanc A. Guldner L. et al.Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to-pregnancy.Epidemiology. 2013; 24: 251-260Crossref PubMed Scopus (60) Google Scholar, 5Petro E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google Scholar). of miscarriage (1Green M.P. Harvey A.J. Finger B.J. Tarulli G.A. Endocrine disrupting chemicals: impacts on human fertility and fecundity during the peri-conception period.Environ Res. 2021; 194: 110694Crossref PubMed Scopus (33) Google on pregnancy E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google and number of C. Warembourg C. Gaudreau E. Monfort C. Le Blanc A. Guldner L. et al.Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to-pregnancy.Epidemiology. 2013; 24: 251-260Crossref PubMed Scopus (60) Google Scholar, 5Petro E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google on pregnancy E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google and number of C. Warembourg C. Gaudreau E. Monfort C. Le Blanc A. Guldner L. et al.Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to-pregnancy.Epidemiology. 2013; 24: 251-260Crossref PubMed Scopus (60) Google Scholar, 5Petro E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google on pregnancy E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google of miscarriage (1Green M.P. Harvey A.J. Finger B.J. Tarulli G.A. Endocrine disrupting chemicals: impacts on human fertility and fecundity during the peri-conception period.Environ Res. 2021; 194: 110694Crossref PubMed Scopus (33) Google Scholar, 6Venners S.A. Korrick S. Xu X. Chen C. Guang W. Huang A. et al.Preconception serum DDT and pregnancy loss: a prospective study using a biomarker of pregnancy.Am J Epidemiol. 2005; 162: 709-716Crossref PubMed Scopus (76) Google with number of pregnancy S. Masata J. Jech L. Zvárová J. Effect of polychlorinated biphenyls (PCBs) and 1,1,1-trichloro-2,2,-bis (4-chlorophenyl)-ethane (DDT) in follicular fluid on the results of in vitro fertilization-embryo transfer (IVF-ET) programs.Fertil Steril. 2010; 93: 1831-1836Abstract Full Text Full Text PDF PubMed Scopus (47) Google with miscarriage to pregnancy A.L. Watson R.E. DeSesso J.M. Developmental and reproductive outcomes in humans and animals after glyphosate exposure: a critical analysis.J Toxicol Environ Health B Crit Rev. 2012; 15: 39-96Crossref PubMed Scopus (99) Google and oocyte E. Ehrlich S. Williams P.L. Petrozza J. Wright D.L. Calafat A.M. et al.Urinary bisphenol A concentrations and ovarian response among women undergoing IVF.Int J Androl. 2010; 33: 385-393Crossref PubMed Scopus (90) Google Scholar, 10Ehrlich S. Williams P.L. Missmer S.A. Flaws J.A. Ye X. Calafat A.M. et al.Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF.Hum Reprod. 2012; 27: 3583-3592Crossref PubMed Scopus (180) Google and normal T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google Scholar). of miscarriage R.B. Liebert C.A. Brookfield K.F. Taylor J.A. vom Saal F.S. Fujimoto V.Y. et al.Conjugated bisphenol A in maternal serum in relation to miscarriage risk.Fertil Steril. 2014; 102: 123-128Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 13Shen Y. Zheng Y. Jiang J. Liu Y. Luo X. Shen Z. 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; 10e0127886Google Scholar, Y. S. T. to bisphenol A is associated with recurrent Reprod. 2005; PubMed Scopus Google with fecundity A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google Scholar, M.P. exposure to and and to the on Environmental Steril. 2015; Full Text Full Text PDF PubMed Scopus (79) Google Scholar). with of L. Gaskins A.J. Y.H. Williams P.L. S. et al.Urinary bisphenol A concentrations and with in vitro outcomes among women from a fertility Reprod. 2015; PubMed Scopus Google in as and oocyte pregnancy and Gaskins A.J. Souter I. S. et al.Urinary phthalate concentrations and reproductive outcomes among women undergoing in vitro results from the Health PubMed Scopus Google on to pregnancy A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google of normal T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google Scholar). fecundity A.M. J. et exposure to and to a first pregnancy Reprod. Google between on T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google Scholar). on to pregnancy A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google of normal K.F. effects on oocyte Reprod. 2021; PubMed Scopus Google between on T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google Scholar). on to pregnancy A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google to pregnancy A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google EDC endocrine-disrupting DDT in a EDC endocrine-disrupting DDT This review was using a PubMed search for human studies between and using the pesticides, fertility, reproduction, plasticizers, bisphenol A, phthalate, miscarriage, and in vitro that were for studies that at reproductive outcomes in including to pregnancy and assisted reproductive including oocyte pregnancy and of the mechanisms underlying the effects of EDCs in with outcomes of ovarian that reproductive data were from this studies focusing on the effects of EDC exposure on as and considered to the scope of this are in and are in are in the United States (2Segal T.R. Giudice L.C. Before the beginning: environmental exposures and reproductive and obstetrical outcomes.Fertil Steril. 2019; 112: 613-621Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). of can and the of exposure can and (2Segal T.R. Giudice L.C. Before the beginning: environmental exposures and reproductive and obstetrical outcomes.Fertil Steril. 2019; 112: 613-621Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). fertility because of exposure to pesticides has in studies. to pesticides was associated with in in a C. Warembourg C. Gaudreau E. Monfort C. Le Blanc A. Guldner L. et al.Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to-pregnancy.Epidemiology. 2013; 24: 251-260Crossref PubMed Scopus (60) Google Scholar). of and associated with a to for maternal and was for the exposure of and C. Warembourg C. Gaudreau E. Monfort C. Le Blanc A. Guldner L. et al.Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to-pregnancy.Epidemiology. 2013; 24: 251-260Crossref PubMed Scopus (60) Google Scholar). of this study the of as a for maternal exposure pregnancy and on for to the study was to women were the to pesticides has to impact oocyte and development are on between the oocyte and its the follicular may to women undergoing follicular fluid and were associated with and the of to the number of E.M. Leroy J.L. Covaci A. Fransen E. De Neubourg D. Dirtu A.C. et al.Endocrine-disrupting chemicals in human follicular fluid impair in vitro oocyte developmental competence.Hum Reprod. 2012; 27: 1025-1033Crossref PubMed Scopus (79) Google Scholar). associations were between follicular pesticide and pregnancy the of other the follicular in the and of a Although for as a exposures were and of the was have to A of the and Reproductive Health prospective study an between pesticide residue intake from the consumption of fruits and vegetables and pregnancy outcomes in women undergoing (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google Scholar). a of women undergoing intake of residue fruits and vegetables was associated with of pregnancy and of (3Chiu Y.H. Williams P.L. Gillman M.W. Gaskins A.J. Mínguez-Alarcón L. Souter I. et al.Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology.J Am Med Assoc Intern Med. 2018; 178: 17-26Google Scholar). Although for infertility pesticide on the intake is an important the a study of women between exposure to the (DDT) and adverse outcomes S. Masata J. Jech L. Zvárová J. Effect of polychlorinated biphenyls (PCBs) and 1,1,1-trichloro-2,2,-bis (4-chlorophenyl)-ethane (DDT) in follicular fluid on the results of in vitro fertilization-embryo transfer (IVF-ET) programs.Fertil Steril. 2010; 93: 1831-1836Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar). of DDT in the follicular fluid were associated with a in the number of pregnancy S. Masata J. Jech L. Zvárová J. Effect of polychlorinated biphenyls (PCBs) and 1,1,1-trichloro-2,2,-bis (4-chlorophenyl)-ethane (DDT) in follicular fluid on the results of in vitro fertilization-embryo transfer (IVF-ET) programs.Fertil Steril. 2010; 93: 1831-1836Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar). a review of studies exposure to a common effects of glyphosate on reproductive health A.L. Watson R.E. DeSesso J.M. Developmental and reproductive outcomes in humans and animals after glyphosate exposure: a critical analysis.J Toxicol Environ Health B Crit Rev. 2012; 15: 39-96Crossref PubMed Scopus (99) Google Scholar). some studies both and female and to pregnancy and A.L. Watson R.E. DeSesso J.M. Developmental and reproductive outcomes in humans and animals after glyphosate exposure: a critical analysis.J Toxicol Environ Health B Crit Rev. 2012; 15: 39-96Crossref PubMed Scopus (99) Google Scholar). may to study environmental infertility of exposure and/or the study of pesticide studies an between pesticides and early pregnancy but are by between and of serum pesticide by et A prospective the serum DDT in between and after for and other a of early pregnancy in the serum DDT group with the S.A. Korrick S. Xu X. Chen C. Guang W. Huang A. et al.Preconception serum DDT and pregnancy loss: a prospective study using a biomarker of pregnancy.Am J Epidemiol. 2005; 162: 709-716Crossref PubMed Scopus (76) Google Scholar). The of this study its prospective of women to and of human to including early pregnancy occurring Although human studies on the studies that exposure to pesticides ovarian exposure of to a pesticide in in of and ovarian I. T. Flaws J.A. by altering and in in PubMed Scopus Google Scholar). exposure to during early development in of in and important in the of and of ovarian and A.M. effects of endocrine-disrupting chemicals on female an ovarian 2010; PubMed Scopus Google Scholar). vitro studies to of and K.F. effects on oocyte Reprod. 2021; PubMed Scopus Google Scholar). A review of the mechanisms by pesticides female reproductive function is by and A.M. effects of endocrine-disrupting chemicals on female an ovarian 2010; PubMed Scopus Google Scholar). are to a to and to The and are in and as and (2Segal T.R. Giudice L.C. Before the beginning: environmental exposures and reproductive and obstetrical outcomes.Fertil Steril. 2019; 112: 613-621Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). can and to the for pesticide exposure A, oocyte and review of animal and human 2014; Full Text Full Text PDF PubMed Scopus Google Scholar). studies to the of plasticizer exposures on natural have A of women of the from an between urinary phthalate and a to with a of A.M. J. et exposure to and to a first pregnancy Reprod. Google Scholar). et A.M. J. bisphenol A, and the of and the Steril. 2014; Full Text Full Text PDF PubMed Scopus Google between female urinary phthalate concentrations and to the study a and were in a of et M.P. exposure to and and to the on Environmental Steril. 2015; Full Text Full Text PDF PubMed Scopus (79) Google between urinary phthalate and to this study on of to the and the urinary was in the first women may have exposures to chemicals were M.P. exposure to and and to the on Environmental Steril. 2015; Full Text Full Text PDF PubMed Scopus (79) Google Scholar). An between and infertility has in studies focusing on effects on oocyte in women undergoing et E. Ehrlich S. Williams P.L. Petrozza J. Wright D.L. Calafat A.M. et al.Urinary bisphenol A concentrations and ovarian response among women undergoing IVF.Int J Androl. 2010; 33: 385-393Crossref PubMed Scopus (90) Google a negative between urinary and oocyte in women undergoing with an in the number of in of urinary in women undergoing Ehrlich et S. Williams P.L. Missmer S.A. Flaws J.A. Ye X. Calafat A.M. et al.Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF.Hum Reprod. 2012; 27: 3583-3592Crossref PubMed Scopus (180) Google a dose-response between urinary concentrations and oocyte and et Gaskins A.J. Souter I. S. et al.Urinary phthalate concentrations and reproductive outcomes among women undergoing in vitro results from the Health PubMed Scopus Google phthalate metabolites in women undergoing for and infertility the urinary phthalate concentrations were associated with oocyte pregnancy and after Gaskins A.J. Souter I. S. et al.Urinary phthalate concentrations and reproductive outcomes among women undergoing in vitro results from the Health PubMed Scopus Google Scholar). the et T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google urinary phthalate metabolites in women undergoing at a Although urinary were with the of normal was between any of the urinary phthalate concentrations and of a on pregnancy early miscarriage T. Du Y. Wang Y. Teng X. Hua X. Yuan X. et al.The associations of urinary phthalate metabolites with the intermediate and pregnancy outcomes of women receiving IVF/ICSI treatments: a prospective single-center study.Ecotoxicol Environ Saf. 2020; 188: 109884Crossref PubMed Scopus (18) Google Scholar). prospective study of women undergoing between the urinary in to 2 oocyte and of pregnancy L. Gaskins A.J. Y.H. Williams P.L. S. et al.Urinary bisphenol A concentrations and with in vitro outcomes among women from a fertility Reprod. 2015; PubMed Scopus Google Scholar). Although for as and a is the of compounds in serum at the of the may the of exposure in relation to during the results can to naturally is to miscarriage et R.B. Liebert C.A. Brookfield K.F. Taylor J.A. vom Saal F.S. Fujimoto V.Y. et al.Conjugated bisphenol A in maternal serum in relation to miscarriage risk.Fertil Steril. 2014; 102: 123-128Abstract Full Text Full Text PDF PubMed Scopus (62) Google a prospective study of women undergoing The serum concentrations during the were in women in R.B. Liebert C.A. Brookfield K.F. Taylor J.A. vom Saal F.S. Fujimoto V.Y. et al.Conjugated bisphenol A in maternal serum in relation to miscarriage risk.Fertil Steril. 2014; 102: 123-128Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar). A has for both and R.B. Liebert C.A. Brookfield K.F. Taylor J.A. vom Saal F.S. Fujimoto V.Y. et al.Conjugated bisphenol A in maternal serum in relation to miscarriage risk.Fertil Steril. 2014; 102: 123-128Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar). to this study was the of serum during early pregnancy after a case-control study including with recurrent miscarriage, urinary were with an of recurrent miscarriage Y. Zheng Y. Jiang J. Liu Y. Luo X. Shen Z. 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; 10e0127886Google Scholar). Although women with of recurrent miscarriage were was The study on of pregnancy and were after the of A study by et Y. S. T. to bisphenol A is associated with recurrent Reprod. 2005; PubMed Scopus Google serum in women with a of pregnancy and pregnancy outcomes The serum were in women with recurrent pregnancy with and but serum miscarriage Y. S. T. to bisphenol A is associated with recurrent Reprod. 2005; PubMed Scopus Google Scholar). the of exposure to miscarriage was of the studies have into the potential effects of exposures on and miscarriage in have the mechanisms by impact female fertility and an in oocyte associated with and in group a in oocyte in with (2Segal T.R. Giudice L.C. Before the beginning: environmental exposures and reproductive and obstetrical outcomes.Fertil Steril. 2019; 112: 613-621Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar, A.M. effects of endocrine-disrupting chemicals on female an ovarian 2010; PubMed Scopus Google Scholar). studies for adverse effects of exposure on and have by and and and Flaws exposures and function in A. Flaws J.A. for bisphenol female a review Steril. Full Text Full Text PDF PubMed Scopus Google Scholar). in vitro studies have adverse effects of on exposure of to in in and of and oocyte A, oocyte and review of animal and human 2014; Full Text Full Text PDF PubMed Scopus Google Scholar). exposure in of the and A, oocyte and review of animal and human 2014; Full Text Full Text PDF PubMed Scopus Google Scholar). the mechanisms female fertility in studies of and of in of and and in in the study by et I. A. and mechanisms of action on reproductive and reproductive a literature J Environ 2020; Scopus Google studies important into the mechanisms underlying fertility after exposure to The data supporting the role of pesticides and in female infertility and miscarriage to as interest in the of the human literature is based on studies and results are in because of and of exposures metabolites and of the data an negative of EDCs on female fertility, in in the by et (1Green M.P. Harvey A.J. Finger B.J. Tarulli G.A. Endocrine disrupting chemicals: impacts on human fertility and fecundity during the peri-conception period.Environ Res. 2021; 194: 110694Crossref PubMed Scopus (33) Google Scholar). the scope of this but of is the of EDC

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