Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Review

Bisphenol a and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies

Authors: Donatella Caserta, Noemi Di Segni, Maddalena Mallozzi, Valentina Giovanale, Alberto Mantovani, Roberto Marci, Massimo Moscarini

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

Login to get access

Abstract

Bisphenol A (BPA) is a high production volume monomer used for making a wide variety of polycarbonate plastics and resins. A large body of evidence links BPA to endocrine disruption in laboratory animals, and a growing number of epidemiological studies support a link with health disorders in humans. The aim of this review is to summarize the recent experimental studies describing the effects and mechanisms of BPA on the female genital tract and to compare them to the current knowledge regarding the impact of BPA impact on female reproductive health. In particular, BPA has been correlated with alterations in hypothalamic-pituitary hormonal production, reduced oocyte quality due to perinatal and adulthood exposure, defective uterine receptivity and the pathogenesis of polycystic ovary syndrome. Researchers have reported conflicting results regarding the effect of BPA on premature puberty and endometriosis development. Experimental studies suggest that BPA’s mechanism of action is related to life stage and that its effect on the female reproductive system may involve agonism with estrogen nuclear receptors as well as other mechanisms (steroid biosynthesis inhibition). Notwithstanding uncertainties and knowledge gaps, the available evidence should be seen as a sufficient grounds to take precautionary actions against excess exposure to BPA.
Literature
1.
go back to reference Gregoraszczuk EL, Ptak A: Endocrine-Disrupting Chemicals: Some Actions of POPs on Female Reproduction. Int J Endocrinol. 2013, 2013: 828532-PubMedCentralPubMed Gregoraszczuk EL, Ptak A: Endocrine-Disrupting Chemicals: Some Actions of POPs on Female Reproduction. Int J Endocrinol. 2013, 2013: 828532-PubMedCentralPubMed
2.
go back to reference Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, Vom Saal FS: In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007, 24: 199-224. 10.1016/j.reprotox.2007.06.004.PubMedCentralCrossRefPubMed Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, Vom Saal FS: In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007, 24: 199-224. 10.1016/j.reprotox.2007.06.004.PubMedCentralCrossRefPubMed
3.
go back to reference Rubin BS: Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011, 127: 27-34. 10.1016/j.jsbmb.2011.05.002.CrossRefPubMed Rubin BS: Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011, 127: 27-34. 10.1016/j.jsbmb.2011.05.002.CrossRefPubMed
4.
go back to reference Caserta D, Mantovani A, Marci R, Fazi A, Ciardo F, La Rocca C, Maranghi F, Moscarini M: Environment and women's reproductive health. Human Reprod Update. 2011, 17: 418-33. 10.1093/humupd/dmq061.CrossRef Caserta D, Mantovani A, Marci R, Fazi A, Ciardo F, La Rocca C, Maranghi F, Moscarini M: Environment and women's reproductive health. Human Reprod Update. 2011, 17: 418-33. 10.1093/humupd/dmq061.CrossRef
5.
go back to reference Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, Sonnenschein C, Watson CS, Zoeller RT, Belcher SM: In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol. 2007, 24 (2): 178-98. 10.1016/j.reprotox.2007.05.010.CrossRefPubMed Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, Sonnenschein C, Watson CS, Zoeller RT, Belcher SM: In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol. 2007, 24 (2): 178-98. 10.1016/j.reprotox.2007.05.010.CrossRefPubMed
6.
go back to reference Alonso-Magdalena P, Laribi O, Ropero AB, Fuentes E, Ripoll C, Soria B, Nadal A: Low doses of bisphenol A and diethylstilbestrol impair Ca2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ Health Perspect. 2005, 113: 969-77. 10.1289/ehp.8002.PubMedCentralCrossRefPubMed Alonso-Magdalena P, Laribi O, Ropero AB, Fuentes E, Ripoll C, Soria B, Nadal A: Low doses of bisphenol A and diethylstilbestrol impair Ca2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ Health Perspect. 2005, 113: 969-77. 10.1289/ehp.8002.PubMedCentralCrossRefPubMed
7.
go back to reference Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, Gadbois JL, Tharp AP, Whitt GS, Sonnenschein C, Soto AM: Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect. 2011, 119 (4): 547-52.PubMedCentralCrossRefPubMed Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, Gadbois JL, Tharp AP, Whitt GS, Sonnenschein C, Soto AM: Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect. 2011, 119 (4): 547-52.PubMedCentralCrossRefPubMed
8.
go back to reference Maffini MV, Rubin BS, Sonnenschein C, Soto AM: Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol Cell Endocrinol. 2006, 254–255: 179-86.CrossRefPubMed Maffini MV, Rubin BS, Sonnenschein C, Soto AM: Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol Cell Endocrinol. 2006, 254–255: 179-86.CrossRefPubMed
9.
go back to reference Nah WH, Park MJ, Gye MC: Effects of early prepubertal exposure to bisphenol A on the onset of puberty, ovarian weights, and estrous cycle in female mice. Clin Exp Reprod Med. 2011, 38: 75-81. 10.5653/cerm.2011.38.2.75.PubMedCentralCrossRefPubMed Nah WH, Park MJ, Gye MC: Effects of early prepubertal exposure to bisphenol A on the onset of puberty, ovarian weights, and estrous cycle in female mice. Clin Exp Reprod Med. 2011, 38: 75-81. 10.5653/cerm.2011.38.2.75.PubMedCentralCrossRefPubMed
10.
go back to reference Ehrlich S, Williams PL, Missmer SA, Flaws JA, Ye X, Calafat AM, Petrozza JC, Wright D, Hauser R: Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF. Hum Reprod. 2012, 27: 3583-92. 10.1093/humrep/des328.PubMedCentralCrossRefPubMed Ehrlich S, Williams PL, Missmer SA, Flaws JA, Ye X, Calafat AM, Petrozza JC, Wright D, Hauser R: Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF. Hum Reprod. 2012, 27: 3583-92. 10.1093/humrep/des328.PubMedCentralCrossRefPubMed
11.
go back to reference Caserta D, Ciardo F, Bordi G, Guerranti C, Fanello E, Perra G, Borghini F, La Rocca C, Tait S, Bergamasco B, Stecca L, Marci R, Lo Monte G, Soave I, Focardi S, Mantovani A, Moscarini M: Correlation of endocrine disrupting chemicals serum levels and white blood cells gene expression of nuclear receptors in a population of infertile women. Int J Endocrinol. 2013, 2013: 510703-PubMedCentralCrossRefPubMed Caserta D, Ciardo F, Bordi G, Guerranti C, Fanello E, Perra G, Borghini F, La Rocca C, Tait S, Bergamasco B, Stecca L, Marci R, Lo Monte G, Soave I, Focardi S, Mantovani A, Moscarini M: Correlation of endocrine disrupting chemicals serum levels and white blood cells gene expression of nuclear receptors in a population of infertile women. Int J Endocrinol. 2013, 2013: 510703-PubMedCentralCrossRefPubMed
12.
go back to reference Rochester JR: Bisphenol A and human health: A review of the literature. Reprod Toxicol. 2013, 42: 132-55.CrossRefPubMed Rochester JR: Bisphenol A and human health: A review of the literature. Reprod Toxicol. 2013, 42: 132-55.CrossRefPubMed
13.
go back to reference Cantonwine DE, Hauser R, Meeker JD: Bisphenol A and Human Reproductive Health. Expert Rev Obstet Gynecol. 2013, 8 (4): 329-335. 10.1586/17474108.2013.811939.CrossRef Cantonwine DE, Hauser R, Meeker JD: Bisphenol A and Human Reproductive Health. Expert Rev Obstet Gynecol. 2013, 8 (4): 329-335. 10.1586/17474108.2013.811939.CrossRef
14.
go back to reference Balabanič D, Rupnik M, Klemenčič AK: Negative impact of endocrine-disrupting compounds on human reproductive health. Reprod Fertil Dev. 2011, 23: 403-16.PubMed Balabanič D, Rupnik M, Klemenčič AK: Negative impact of endocrine-disrupting compounds on human reproductive health. Reprod Fertil Dev. 2011, 23: 403-16.PubMed
15.
go back to reference Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, Vom Saal FS: Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond B Biol Sci. 2009, 27: 2079-96.CrossRef Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, Vom Saal FS: Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond B Biol Sci. 2009, 27: 2079-96.CrossRef
16.
go back to reference Monje L, Varayoud J, Munoz-de-toro M, Luque EH, Ramos JG: Exposure of neonatal female rats to bisphenol A disrupt hypothalamic LHRH pre-mRNA processing and estrogen receptor alpha expression in nuclei controlling estrous cyclicity. Reprod Toxicol. 2010, 30: 625-34. 10.1016/j.reprotox.2010.08.004.CrossRefPubMed Monje L, Varayoud J, Munoz-de-toro M, Luque EH, Ramos JG: Exposure of neonatal female rats to bisphenol A disrupt hypothalamic LHRH pre-mRNA processing and estrogen receptor alpha expression in nuclei controlling estrous cyclicity. Reprod Toxicol. 2010, 30: 625-34. 10.1016/j.reprotox.2010.08.004.CrossRefPubMed
17.
go back to reference Patisaul HB, Fortino AE, Polston EK: Neonatal ginestein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol. 2006, 28: 111-118. 10.1016/j.ntt.2005.11.004.CrossRefPubMed Patisaul HB, Fortino AE, Polston EK: Neonatal ginestein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol. 2006, 28: 111-118. 10.1016/j.ntt.2005.11.004.CrossRefPubMed
18.
go back to reference Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM: Evidence of altered brain sexual differentiation in mice exposed perinatally to low environmentally relevant levels of bisphenol A. Endocrinology. 2006, 147: 3681-3691. 10.1210/en.2006-0189.CrossRefPubMed Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM: Evidence of altered brain sexual differentiation in mice exposed perinatally to low environmentally relevant levels of bisphenol A. Endocrinology. 2006, 147: 3681-3691. 10.1210/en.2006-0189.CrossRefPubMed
19.
go back to reference Wolstenholme JT, Rissman EF, Connelly JJ: The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm Behav. 2011, 59: 296-305. 10.1016/j.yhbeh.2010.10.001.PubMedCentralCrossRefPubMed Wolstenholme JT, Rissman EF, Connelly JJ: The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm Behav. 2011, 59: 296-305. 10.1016/j.yhbeh.2010.10.001.PubMedCentralCrossRefPubMed
20.
go back to reference Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller RL, Perera FP, Champagne FA: Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci U S A. 2013, 110 (24): 9956-61. 10.1073/pnas.1214056110.PubMedCentralCrossRefPubMed Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller RL, Perera FP, Champagne FA: Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci U S A. 2013, 110 (24): 9956-61. 10.1073/pnas.1214056110.PubMedCentralCrossRefPubMed
21.
go back to reference Fernandez M, Bianchi M, Lux-Lantos V, Libertun C: Neonatal exposure to bisphenol A alters reproductive parameters and gonadotropin releasing hormone signalling in female rats. Environ Health perspect. 2009, 117: 757-762. 10.1289/ehp.0800267.PubMedCentralCrossRefPubMed Fernandez M, Bianchi M, Lux-Lantos V, Libertun C: Neonatal exposure to bisphenol A alters reproductive parameters and gonadotropin releasing hormone signalling in female rats. Environ Health perspect. 2009, 117: 757-762. 10.1289/ehp.0800267.PubMedCentralCrossRefPubMed
22.
go back to reference Maranghi F, Mantovani A: Targeted toxicological testing to investigate the role of endocrine disrupters in puberty disorders. Reproductive Toxicology. 2012, 33: 290-6. 10.1016/j.reprotox.2012.01.009.CrossRefPubMed Maranghi F, Mantovani A: Targeted toxicological testing to investigate the role of endocrine disrupters in puberty disorders. Reproductive Toxicology. 2012, 33: 290-6. 10.1016/j.reprotox.2012.01.009.CrossRefPubMed
23.
go back to reference Navarro VM, Sánchez-Garrido MA, Castellano JM, Roa J, García-Galiano D, Pineda R, Aguilar E, Pinilla L, Tena-Sempere M: Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology. 2009, 150: 2359-67. 10.1210/en.2008-0580.CrossRefPubMed Navarro VM, Sánchez-Garrido MA, Castellano JM, Roa J, García-Galiano D, Pineda R, Aguilar E, Pinilla L, Tena-Sempere M: Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology. 2009, 150: 2359-67. 10.1210/en.2008-0580.CrossRefPubMed
24.
go back to reference Bai Y, Chang F, Zhou R, Jin PP, Matsumoto H, Sokabe M, Chen L: Increase of anteroventral periventricular kisspeptin neurons and generation of E2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology. 2011, 152: 1562-71. 10.1210/en.2010-1042.CrossRefPubMed Bai Y, Chang F, Zhou R, Jin PP, Matsumoto H, Sokabe M, Chen L: Increase of anteroventral periventricular kisspeptin neurons and generation of E2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology. 2011, 152: 1562-71. 10.1210/en.2010-1042.CrossRefPubMed
25.
go back to reference Xi W, Lee CK, Yeung WS, Giesy JP, Wong MH, Zhang X, Hecker M, Wong CK: Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus-pituitary-gonadal axis of CD-1 mice. Reprod Toxicol. 2011, 31: 409-17. 10.1016/j.reprotox.2010.12.002.CrossRefPubMed Xi W, Lee CK, Yeung WS, Giesy JP, Wong MH, Zhang X, Hecker M, Wong CK: Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus-pituitary-gonadal axis of CD-1 mice. Reprod Toxicol. 2011, 31: 409-17. 10.1016/j.reprotox.2010.12.002.CrossRefPubMed
26.
go back to reference Wolff MS, Britton JA, Boguski L, Hochman S, Maloney N, Serra N, Liu Z, Berkowitz G, Larson S, Forman J: Environmental exposures and puberty in inner-city girls. Environ Res. 2008, 107: 393-400. 10.1016/j.envres.2008.03.006.PubMedCentralCrossRefPubMed Wolff MS, Britton JA, Boguski L, Hochman S, Maloney N, Serra N, Liu Z, Berkowitz G, Larson S, Forman J: Environmental exposures and puberty in inner-city girls. Environ Res. 2008, 107: 393-400. 10.1016/j.envres.2008.03.006.PubMedCentralCrossRefPubMed
27.
go back to reference Qiao L, Zheng L, Cai D: Study on the levels of bisphenol A, octylphenol, 4-nonylphenol in serum of precocious girls. Wei Sheng Yan Jiu. 2010, 39: 9-12.PubMed Qiao L, Zheng L, Cai D: Study on the levels of bisphenol A, octylphenol, 4-nonylphenol in serum of precocious girls. Wei Sheng Yan Jiu. 2010, 39: 9-12.PubMed
28.
go back to reference Doerge DR, Twaddle NC, Vanlandingham M, Fisher JW: Pharmacokinetics of bisphenol in neonatal and adult CD-1 mice: inter-species comparisons with Sprague–Dawley rats and rhesus monkeys. Toxicol Lett. 2011, 207: 298-305. 10.1016/j.toxlet.2011.09.020.CrossRefPubMed Doerge DR, Twaddle NC, Vanlandingham M, Fisher JW: Pharmacokinetics of bisphenol in neonatal and adult CD-1 mice: inter-species comparisons with Sprague–Dawley rats and rhesus monkeys. Toxicol Lett. 2011, 207: 298-305. 10.1016/j.toxlet.2011.09.020.CrossRefPubMed
29.
go back to reference Zhang HQ, Zhang XF, Zhang LJ, Chao HH, Pan B, Feng YM, Li L, Sun XF, Shen W: Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes. Mol Biol Rep. 2012, 39: 5651-7. 10.1007/s11033-011-1372-3.CrossRefPubMed Zhang HQ, Zhang XF, Zhang LJ, Chao HH, Pan B, Feng YM, Li L, Sun XF, Shen W: Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes. Mol Biol Rep. 2012, 39: 5651-7. 10.1007/s11033-011-1372-3.CrossRefPubMed
30.
go back to reference Hunt PA, Lawson C, Gieske M, Murdoch B, Smith H, Marre A, Hassold T, VandeVoort CA: Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc Natl Acad Sci USA. 2012, 109: 17525-30. 10.1073/pnas.1207854109.PubMedCentralCrossRefPubMed Hunt PA, Lawson C, Gieske M, Murdoch B, Smith H, Marre A, Hassold T, VandeVoort CA: Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc Natl Acad Sci USA. 2012, 109: 17525-30. 10.1073/pnas.1207854109.PubMedCentralCrossRefPubMed
31.
go back to reference Susiarjo M, Hassold TJ, Freeman E, Hunt PA: Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLos Genet. 2007, 12: 3- Susiarjo M, Hassold TJ, Freeman E, Hunt PA: Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLos Genet. 2007, 12: 3-
32.
go back to reference Rivera OE, Varayoud J, Rodríguez HA, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A or diethylstilbestrol alters the ovarian follicular dynamics in the lamb. Reprod Toxicol. 2011, 32: 304-12. 10.1016/j.reprotox.2011.06.118.CrossRefPubMed Rivera OE, Varayoud J, Rodríguez HA, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A or diethylstilbestrol alters the ovarian follicular dynamics in the lamb. Reprod Toxicol. 2011, 32: 304-12. 10.1016/j.reprotox.2011.06.118.CrossRefPubMed
33.
go back to reference Karavan JR, Pepling ME: Effects of estrogenic compounds on neonatal oocyte development. Reprod Toxicol. 2012, 34: 51-6. 10.1016/j.reprotox.2012.02.005.CrossRefPubMed Karavan JR, Pepling ME: Effects of estrogenic compounds on neonatal oocyte development. Reprod Toxicol. 2012, 34: 51-6. 10.1016/j.reprotox.2012.02.005.CrossRefPubMed
34.
go back to reference Lawson C, Gieske M, Murdoch B, Ye P, Li Y, Hassold T, Hunt PA: Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod. 2011, 84: 79-86. 10.1095/biolreprod.110.084814.PubMedCentralCrossRefPubMed Lawson C, Gieske M, Murdoch B, Ye P, Li Y, Hassold T, Hunt PA: Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod. 2011, 84: 79-86. 10.1095/biolreprod.110.084814.PubMedCentralCrossRefPubMed
35.
go back to reference Rodríguez HA, Santambrosio N, Santamaría CG, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol. 2010, 30 (4): 550-7. 10.1016/j.reprotox.2010.07.008.CrossRefPubMed Rodríguez HA, Santambrosio N, Santamaría CG, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol. 2010, 30 (4): 550-7. 10.1016/j.reprotox.2010.07.008.CrossRefPubMed
36.
go back to reference Chao HH, Zhang XF, Chen B, Pan B, Zhang LJ, Li L, Sun XF, Shi QH, Shen W: Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem Cell Biol. 2012, 137: 249-59. 10.1007/s00418-011-0894-z.CrossRefPubMed Chao HH, Zhang XF, Chen B, Pan B, Zhang LJ, Li L, Sun XF, Shi QH, Shen W: Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem Cell Biol. 2012, 137: 249-59. 10.1007/s00418-011-0894-z.CrossRefPubMed
37.
go back to reference Lee SG, Kim JY, Chung JY, Kim YJ, Park JE, Oh S, Yoon YD, Yoo KS, Yoo YH, Kim JM: Bisphenol A exposure during adulthood causes augmentation of follicular atresia and luteal regression by decreasing 17β-estradiol synthesis via downregulation of aromatase in rat ovary. Environ Health Perspect. 2013, 121: 663-9. 10.1289/ehp.1205823.PubMedCentralCrossRefPubMed Lee SG, Kim JY, Chung JY, Kim YJ, Park JE, Oh S, Yoon YD, Yoo KS, Yoo YH, Kim JM: Bisphenol A exposure during adulthood causes augmentation of follicular atresia and luteal regression by decreasing 17β-estradiol synthesis via downregulation of aromatase in rat ovary. Environ Health Perspect. 2013, 121: 663-9. 10.1289/ehp.1205823.PubMedCentralCrossRefPubMed
38.
go back to reference Peretz J, Gupta RK, Singh J, Hernandez-Ochoa I, Flaws JA: Bisphenol A impairs follicle growth, inhibits steroidogenesis, and downregulates rate-limiting enzymes in the estradiol biosynthesis pathway. Toxicol Sci. 2011, 119: 209-17. 10.1093/toxsci/kfq319.PubMedCentralCrossRefPubMed Peretz J, Gupta RK, Singh J, Hernandez-Ochoa I, Flaws JA: Bisphenol A impairs follicle growth, inhibits steroidogenesis, and downregulates rate-limiting enzymes in the estradiol biosynthesis pathway. Toxicol Sci. 2011, 119: 209-17. 10.1093/toxsci/kfq319.PubMedCentralCrossRefPubMed
39.
go back to reference Grasselli F, Baratta L, Baioni L, Bussolati S, Ramoni R, Grolli S, Basini G: Bisphenol A disrupts granulosa cell function. Domest Anim Endocrinol. 2010, 39: 34-9. 10.1016/j.domaniend.2010.01.004.CrossRefPubMed Grasselli F, Baratta L, Baioni L, Bussolati S, Ramoni R, Grolli S, Basini G: Bisphenol A disrupts granulosa cell function. Domest Anim Endocrinol. 2010, 39: 34-9. 10.1016/j.domaniend.2010.01.004.CrossRefPubMed
40.
go back to reference Romani F, Tropea A, Scarinci E, Dello Russo C, Lisi L, Catino S, Lanzone A, Apa R: Endocrine disruptors and human corpus luteum: in vitro effects of phenols on luteal cells function. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2013, 31: 170-80. 10.1080/10590501.2013.782180.CrossRefPubMed Romani F, Tropea A, Scarinci E, Dello Russo C, Lisi L, Catino S, Lanzone A, Apa R: Endocrine disruptors and human corpus luteum: in vitro effects of phenols on luteal cells function. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2013, 31: 170-80. 10.1080/10590501.2013.782180.CrossRefPubMed
41.
go back to reference Dominguez MA, Petre MA, Neal MS, Foster WG: Bisphenol A concentration-dependently increases human granulosa-lutein cell matrix metalloproteinase-9 (MMP-9) enzyme output. Reprod Toxicol. 2008, 25: 420-5. 10.1016/j.reprotox.2008.05.059.CrossRefPubMed Dominguez MA, Petre MA, Neal MS, Foster WG: Bisphenol A concentration-dependently increases human granulosa-lutein cell matrix metalloproteinase-9 (MMP-9) enzyme output. Reprod Toxicol. 2008, 25: 420-5. 10.1016/j.reprotox.2008.05.059.CrossRefPubMed
42.
go back to reference Brieño-Enríquez MA, Reig-Viader R, Cabero L, Toran N, Martínez F, Roig I, Garcia Caldés M: Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro. Mol Human Reprod. 2012, 18: 171-83. 10.1093/molehr/gar074.CrossRef Brieño-Enríquez MA, Reig-Viader R, Cabero L, Toran N, Martínez F, Roig I, Garcia Caldés M: Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro. Mol Human Reprod. 2012, 18: 171-83. 10.1093/molehr/gar074.CrossRef
43.
go back to reference Machtinger R, Combelles CM, Missmer SA, Correia KF, Williams P, Hauser R, Racowsky C: Bisphenol-A and human oocyte maturation in vitro. Human Reprod. 2013, 28: 2735-45. 10.1093/humrep/det312.CrossRef Machtinger R, Combelles CM, Missmer SA, Correia KF, Williams P, Hauser R, Racowsky C: Bisphenol-A and human oocyte maturation in vitro. Human Reprod. 2013, 28: 2735-45. 10.1093/humrep/det312.CrossRef
44.
go back to reference Bloom MS, Kim D, Vom Saal FS, Taylor JA, Cheng G, Lamb JD, Fujimoto VY: Bisphenol A exposure reduces the estradiol response to gonadotropin stimulation during in vitro fertilization. Fertil Steril. 2011, 96 (3): 672-677. 10.1016/j.fertnstert.2011.06.063.PubMedCentralCrossRefPubMed Bloom MS, Kim D, Vom Saal FS, Taylor JA, Cheng G, Lamb JD, Fujimoto VY: Bisphenol A exposure reduces the estradiol response to gonadotropin stimulation during in vitro fertilization. Fertil Steril. 2011, 96 (3): 672-677. 10.1016/j.fertnstert.2011.06.063.PubMedCentralCrossRefPubMed
45.
go back to reference Caserta D, Bordi G, Ciardo F, Marci R, La Rocca C, Tait S, Bergamasco B, Stecca L, Mantovani A, Guerranti C, Fanello EL, Perra G, Borghini F, Focardi SE, Moscarini M: The influence of endocrine disruptors in a selected population of infertile women. Gynecol Endocrinol. 2013, 29: 444-7. 10.3109/09513590.2012.758702.CrossRefPubMed Caserta D, Bordi G, Ciardo F, Marci R, La Rocca C, Tait S, Bergamasco B, Stecca L, Mantovani A, Guerranti C, Fanello EL, Perra G, Borghini F, Focardi SE, Moscarini M: The influence of endocrine disruptors in a selected population of infertile women. Gynecol Endocrinol. 2013, 29: 444-7. 10.3109/09513590.2012.758702.CrossRefPubMed
46.
go back to reference Sugiura-Ogasawara M, Ozaki Y, Sonta S, Makino T, Suzumori K: Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod. 2005, 20 (8): 2325-9. 10.1093/humrep/deh888.CrossRefPubMed Sugiura-Ogasawara M, Ozaki Y, Sonta S, Makino T, Suzumori K: Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod. 2005, 20 (8): 2325-9. 10.1093/humrep/deh888.CrossRefPubMed
47.
go back to reference Zheng YM, Wang Y, Zhao J, Dai YH, Luo XM, Shen ZJ, Chen X, Yuan W, Shen YP: Association between serum bisphenol-A and recurrent spontaneous abortion: a 1:2 case–control study, China [abstract]. Zhonghua Liu Xing Bing Xue Za Zhi. 2012, 33 (8): 841-5.PubMed Zheng YM, Wang Y, Zhao J, Dai YH, Luo XM, Shen ZJ, Chen X, Yuan W, Shen YP: Association between serum bisphenol-A and recurrent spontaneous abortion: a 1:2 case–control study, China [abstract]. Zhonghua Liu Xing Bing Xue Za Zhi. 2012, 33 (8): 841-5.PubMed
48.
go back to reference Mendoza-Rodríguez CA, García-Guzmán M, Baranda-Avila N, Morimoto S, Perrot-Applanat M, Cerbón M: Administration of bisphenol A to dams during perinatal period modifies molecular and morphological reproductive parameters of the offspring. Reprod Toxicol. 2011, 31: 177-83. 10.1016/j.reprotox.2010.10.013.CrossRefPubMed Mendoza-Rodríguez CA, García-Guzmán M, Baranda-Avila N, Morimoto S, Perrot-Applanat M, Cerbón M: Administration of bisphenol A to dams during perinatal period modifies molecular and morphological reproductive parameters of the offspring. Reprod Toxicol. 2011, 31: 177-83. 10.1016/j.reprotox.2010.10.013.CrossRefPubMed
49.
go back to reference Aghajanova L, Giudice LC: Effect of bisphenol A on human endometrial stromal fibroblasts in vitro. Reprod Biomed Online. 2011, 22: 249-56. 10.1016/j.rbmo.2010.12.007.CrossRefPubMed Aghajanova L, Giudice LC: Effect of bisphenol A on human endometrial stromal fibroblasts in vitro. Reprod Biomed Online. 2011, 22: 249-56. 10.1016/j.rbmo.2010.12.007.CrossRefPubMed
50.
go back to reference Bredhult C, Sahlin L, Olovsson M: Gene expression analysis of human endometrial endothelial cells exposed to Bisphenol A. Reprod Toxicol. 2009, 28: 18-25. 10.1016/j.reprotox.2009.03.006.CrossRefPubMed Bredhult C, Sahlin L, Olovsson M: Gene expression analysis of human endometrial endothelial cells exposed to Bisphenol A. Reprod Toxicol. 2009, 28: 18-25. 10.1016/j.reprotox.2009.03.006.CrossRefPubMed
51.
go back to reference Newbold RR, Jefferson WN, Padilla-Banks E: Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect. 2009, 117: 879-85. 10.1289/ehp.0800045.PubMedCentralCrossRefPubMed Newbold RR, Jefferson WN, Padilla-Banks E: Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect. 2009, 117: 879-85. 10.1289/ehp.0800045.PubMedCentralCrossRefPubMed
52.
go back to reference Hiroi H, Tsutsumi O, Takeuchi T, Momoeda M, Ikezuki Y, Okamura A, Yokota H, Taketani Y: Differences in serum bisphenol a concentrations in premenopausal normal women and women with endometrial hyperplasia. Endocr J. 2004, 51: 595-600. 10.1507/endocrj.51.595.CrossRefPubMed Hiroi H, Tsutsumi O, Takeuchi T, Momoeda M, Ikezuki Y, Okamura A, Yokota H, Taketani Y: Differences in serum bisphenol a concentrations in premenopausal normal women and women with endometrial hyperplasia. Endocr J. 2004, 51: 595-600. 10.1507/endocrj.51.595.CrossRefPubMed
53.
go back to reference Varayoud J, Ramos JG, Bosquiazzo VL, Lower M, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology. 2011, 152: 1101-11. 10.1210/en.2009-1037.CrossRefPubMed Varayoud J, Ramos JG, Bosquiazzo VL, Lower M, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology. 2011, 152: 1101-11. 10.1210/en.2009-1037.CrossRefPubMed
54.
go back to reference Bromer JG, Zhou Y, Taylor MB, Doherty L, Taylor HS: Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 2010, 24: 2273-80. 10.1096/fj.09-140533.PubMedCentralCrossRefPubMed Bromer JG, Zhou Y, Taylor MB, Doherty L, Taylor HS: Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 2010, 24: 2273-80. 10.1096/fj.09-140533.PubMedCentralCrossRefPubMed
55.
go back to reference Xiao S, Diao H, Smith MA, Song X, Ye X: Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod Toxicol. 2011, 32: 434-41.PubMedCentralPubMed Xiao S, Diao H, Smith MA, Song X, Ye X: Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod Toxicol. 2011, 32: 434-41.PubMedCentralPubMed
56.
go back to reference Ehrlich S, Williams PL, Missmer SA, Flaws JA, Berry KF, Calafat AM, Ye X, Petrozza JC, Wright D, Hauser R: Urinary bisphenol A concentrations and implantation failure among women undergoing in vitro fertilization. Environ Health Perspect. 2012, 120: 978-83. 10.1289/ehp.1104307.PubMedCentralCrossRefPubMed Ehrlich S, Williams PL, Missmer SA, Flaws JA, Berry KF, Calafat AM, Ye X, Petrozza JC, Wright D, Hauser R: Urinary bisphenol A concentrations and implantation failure among women undergoing in vitro fertilization. Environ Health Perspect. 2012, 120: 978-83. 10.1289/ehp.1104307.PubMedCentralCrossRefPubMed
57.
go back to reference Tarantino G, Valentino R, Di Somma C, D'Esposito V, Passaretti F, Pizza G, Brancato V, Orio F, Formisano P, Colao A, Savastano S: Bisphenol A in polycystic ovary syndrome and its association with liver-spleen axis. Clin Endocrinol. 2013, 78: 447-53. 10.1111/j.1365-2265.2012.04500.x.CrossRef Tarantino G, Valentino R, Di Somma C, D'Esposito V, Passaretti F, Pizza G, Brancato V, Orio F, Formisano P, Colao A, Savastano S: Bisphenol A in polycystic ovary syndrome and its association with liver-spleen axis. Clin Endocrinol. 2013, 78: 447-53. 10.1111/j.1365-2265.2012.04500.x.CrossRef
58.
go back to reference Kandaraki E, Chatzigeorgiou A, Livadas S, Palioura E, Economou F, Koutsilieris M, Palimeri S, Panidis D, Diamanti-Kandarakis E: Endocrine disruptors and polycystic ovary syndrome (PCOS): elevated serum levels of bisphenol A in women with PCOS. J Clin Endocrinol Metab. 2011, 96: 480-4. 10.1210/jc.2010-1658.CrossRef Kandaraki E, Chatzigeorgiou A, Livadas S, Palioura E, Economou F, Koutsilieris M, Palimeri S, Panidis D, Diamanti-Kandarakis E: Endocrine disruptors and polycystic ovary syndrome (PCOS): elevated serum levels of bisphenol A in women with PCOS. J Clin Endocrinol Metab. 2011, 96: 480-4. 10.1210/jc.2010-1658.CrossRef
59.
go back to reference Fernández M, Bourguignon N, Lux-Lantos V, Libertun C: Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ Health Perspect. 2010, 118: 1217-22. 10.1289/ehp.0901257.PubMedCentralCrossRefPubMed Fernández M, Bourguignon N, Lux-Lantos V, Libertun C: Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ Health Perspect. 2010, 118: 1217-22. 10.1289/ehp.0901257.PubMedCentralCrossRefPubMed
60.
go back to reference Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Michels KB, Hunter DJ: In utero exposure and the incidence of endometriosis. Fertil Steril. 2004, 82: 1501-1508. 10.1016/j.fertnstert.2004.04.065.CrossRefPubMed Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Michels KB, Hunter DJ: In utero exposure and the incidence of endometriosis. Fertil Steril. 2004, 82: 1501-1508. 10.1016/j.fertnstert.2004.04.065.CrossRefPubMed
61.
go back to reference Signorile PG, Spugnini EP, Mita L, Mellone P, D’Avino A, Bianco M, Diano N, Caputo L, Rea F, Viceconte R, Portaccio M, Viggiano E, Citro G, Pierantoni R, Sica V, Vincenzi B, Mita DG, Baldi F, Baldi A: Pre-natal exposure of mice to bisphenol A elicits an endometriosis-likephenotype in female offspring. Gen Comp Endocrinol. 2010, 168: 318-25. 10.1016/j.ygcen.2010.03.030.CrossRefPubMed Signorile PG, Spugnini EP, Mita L, Mellone P, D’Avino A, Bianco M, Diano N, Caputo L, Rea F, Viceconte R, Portaccio M, Viggiano E, Citro G, Pierantoni R, Sica V, Vincenzi B, Mita DG, Baldi F, Baldi A: Pre-natal exposure of mice to bisphenol A elicits an endometriosis-likephenotype in female offspring. Gen Comp Endocrinol. 2010, 168: 318-25. 10.1016/j.ygcen.2010.03.030.CrossRefPubMed
62.
go back to reference Cobellis L, Colacurci N, Trabucco E, Carpentiero C, Grumetto L: Measurement of bisphenol A and bisphenol B levels in human blood sera from healthy and endometriotic women. Biomed Chromatogr. 2009, 23: 1186-90. 10.1002/bmc.1241.CrossRefPubMed Cobellis L, Colacurci N, Trabucco E, Carpentiero C, Grumetto L: Measurement of bisphenol A and bisphenol B levels in human blood sera from healthy and endometriotic women. Biomed Chromatogr. 2009, 23: 1186-90. 10.1002/bmc.1241.CrossRefPubMed
63.
go back to reference Buck Louis GM, Peterson CM, Chen Z, Croughan M, Sundaram R, Stanford J, Varner MW, Kennedy A, Giudice L, Fujimoto VY, Sun L, Wang L, Guo Y, Kannan K: Bisphenol A and phthalates and endometriosis: the Endometriosis: Natural History, Diagnosis and Outcomes Study. Fertil Ster. 2013, 100: 162-9. 10.1016/j.fertnstert.2013.03.026.CrossRef Buck Louis GM, Peterson CM, Chen Z, Croughan M, Sundaram R, Stanford J, Varner MW, Kennedy A, Giudice L, Fujimoto VY, Sun L, Wang L, Guo Y, Kannan K: Bisphenol A and phthalates and endometriosis: the Endometriosis: Natural History, Diagnosis and Outcomes Study. Fertil Ster. 2013, 100: 162-9. 10.1016/j.fertnstert.2013.03.026.CrossRef
64.
go back to reference Itoh H, Iwasaki M, Hanaoka T, Sasaki H, Tanaka T, Tsugane S: Urinary bisphenol-A concentration in infertile Japanese women and its association with endometriosis: A cross-sectional study. Environ Health Prev Med. 2007, 12: 258-64. 10.1007/BF02898033.PubMedCentralCrossRefPubMed Itoh H, Iwasaki M, Hanaoka T, Sasaki H, Tanaka T, Tsugane S: Urinary bisphenol-A concentration in infertile Japanese women and its association with endometriosis: A cross-sectional study. Environ Health Prev Med. 2007, 12: 258-64. 10.1007/BF02898033.PubMedCentralCrossRefPubMed
Metadata
Title
Bisphenol a and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies
Authors
Donatella Caserta
Noemi Di Segni
Maddalena Mallozzi
Valentina Giovanale
Alberto Mantovani
Roberto Marci
Massimo Moscarini
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-37

Other articles of this Issue 1/2014

Reproductive Biology and Endocrinology 1/2014 Go to the issue