Bisphenol Compounds on Human Reproduction Health

Hongjie Fan, Kai-Fai Lee

Department of Obstetrics and Gynaecology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, ChinaChina
Department of Obstetrics and Gynaecology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China; Shen Zhen Key Laboratory of Fertility Regulation, The University of Hong Kong-Shenzhen Hospital, Haiyuan 1Hong Kong

DOI: https://doi.org/10.17140/goroj-4-141 · Published 2017-12-08 · Licence: https://creativecommons.org/licenses/by/4.0 · © 2017 The Author(s)

Also available as PDF (figures and tables appear in the PDF).

Keywords: Bisphenol-A; Bisphenol-F; Bisphenol-S; Pregnancy; Reproduction

Introduction

Endocrine disrupting chemicals (EDCs) are various chemicals mimicking hormones present in the body, and they bind and act through hormone receptors to modulate the functions of endocrine systems. In human, the target of EDCs in endocrine system include thyroid, pituitary, adrenal, mammary glands, ovaries, uterus in female, and prostate and testes in male.1 EDCs 2-4 with different hormone-like activities have diverse effect on endocrine systems,2-4 which could be classified into persistent and non-persistent groups depending on their biodegradation and bioaccumulation properties (Table 1).

In various EDCs, bisphenol-A (BPA) is one of the well-studied chemical that might affect human health. Bisphenol compounds are a group of chemicals with two hydroxyphenyl groups, and most of which contains diphenylmethane structure. The naming of each bisphenol chemical is based on the reactant linking two hydroxyphenyls. For example, bisphenol-A has acetone as a bridge linking two phenols. As a result, bisphenol compounds share very simi-

Table 1. Main EDCs and their Effects in Endocrine Systems.

EDCs Major hormonal effect Endocrine effect

Persistent organic pollutants Polychlorobiphenyls (PCBs) Thyroid

dichlorodiphenyltrichloroethane Estrogen (DDT)

Dioxins Anti-androgen

Non-persistent organic pollutants Bisphenol A (BPA) Estrogen

Phthalates Estrogen

Isoflavones Estrogen

lar chemical structure, and the difference is the reactant in the middle (Figure 1).

Among these bisphenols, BPA is the most commonly used chemical nowadays. BPA is heat resistant and has good elasticity. It has been widely used as plastic monomer in the manufacture of polycarbonate plastics and epoxy resins since 1950. Over 6 billion pounds of BPA are produced every year for manufacturing of plastic products, such as plastic bags, paper bags, bottles, microwave box, dental sealants, coated tins, paintings. BPA was firstly found to have the estrogenic effect in 1936.5 Humans are exposed to BPA through dietary intake, dermal contact, and inhalation.6 Since 1999, BPA were detected in human blood, urine, serum and placental tissue.7 In last two decades, serval lines of evidence suggest adverse effect of BPA on human health including obesity, diabetes, abnormal behavior, and female and male reproductive functions.

BPA Levels During Pregnancy

BPA could be detected in the serum of non-pregnant women, and pregnant women at early and late gestational stage, as well as in the fetal cord serum and amniotic fluid (1-2 ng/mL). For amniotic fluid at 15-18 weeks gestation, there was a 5-fold increase in BPA level (8.3 ng/mL).10 After delivery, the placental BPA level was higher (11.2 ng/g tissue) when compared to the maternal serum and umbilical cord blood collected from the same subjects,11 suggesting that BPA could be accumulated at the maternal-fetal interface that might affect fetal development during the whole gestational period.

The association of BPA and pregnancy-associated diseases was reported in several studies. Serum BPA level was

Alter ovarian steroidogenesis, oocyte development, reduce semen quality, learning disability, thyroid cancer, hypertension, diabetes Reduced fertility, spontaneous abortion, type 2 diabetes, breast cancer, reduced bone mineral density Alter steroid hormone metabolism, reduce semen quality, auto-immune disease, diabetes, breast/liver/ lung cancer, cancer mortality

Alter steroidogenesis, reduced female and male fertility, reduced birth weight, asthma, increased children anxiety/depression, type 2 diabetes, breast/prostate cancer, obesity, hypertension Reduced sperm quality and female fertility, endometriosis, preterm birth, pubertal delay, autoimmune disease, children abnormal behaviors Alter steroid hormone metabolism, autoimmune disease, increase bone mineral density, reduce prostate/breast cancer, anti-diabetes effect

much higher in patients with polycystic ovary syndrome (PCOS) than normal female.12 Higher BPA level in follicular fluid (440 pg/ml) was also observed in PCOS patients compared with non- PCOS patients (338 pg/mL).13 Similarly, patients with history of unexplained recurrent spontaneous abortion (RSA) have a 14,15 significantly higher serum BPA level than normal women. In women undergoing in vitro fertilization (IVF), BPA could be detected in most of the cases, and the higher urinary BPA concentrations were found in patients with lower antral follicle 16,17 count (AFC) and number of oocytes retrieved. A positive association was also found between BPA urinary concentrations and implantation failure.18 However, it was also reported that IVF outcomes and endometrial wall thickness were not asso- 7 19 ciated with urinary BPA concentrations,19 but the spontaneous 20 21 preterm birth rate20 and the risk of low birth weight21 were associated with higher urine BPA levels. In patients with uterine 2,8,9 leiomyoma, their urine and plasma BPA levels were not different from the control group,22 and endometriosis was not associated with urinary BPA level in infertile Japanese population.23

Mechanism of BPA in Female Reproduction

As an estrogen-like EDC, the activity of BPA was found to 24be 100 to 10,000-fold lower than that of 17β-estradiol (E2).24- 26 Estrogen receptor α (ERα) and estrogen receptor β (ERβ), and a transmembrane ER called G protein-coupled receptor 30 (GPR30) are the main targets of BPA when it carries out its ef- 27,28 fect. Most of mechanism studies of BPA was performed in in vitro and in vivo animal models. In human, endometrial adenocarcinoma cell line Ishikawa is response to BPA with many genes modulated.29 Human primary endometrial cell prolifera- 30,31 tion was inhibited by BPA, BPA also induced the expression of decidualization makers and several hormone related mol-

ecules in endometrial stromal cells. BPA induces apoptosis, necrosis and the tumor necrosis factor-alpha (TNF-α) expressions in the human primary placental cells and the first trimester 35,36 human chorionic villous explant. Cell migration and invasion of trophoblast cell line HTR-8/SVneo and BeWo was reduced by 37,38 BPA. More detailed mechanism of BPA in animal study was 9,39,40 reviewed elsewhere.

Very few evidence support the detrimental effect of BPA on ovarian function. As mentioned previously, it was found that follicular fluid has a very low BPA level (1-2 ng/ml).10 BPA at supra-physiological level altered the progesterone and estradiol synthesis in luteinized granulosa cells and reduced the expression of steroidogenesis enzymes, such as 3 beta-hydroxysteroid dehydrogenase (3 beta-HSD), CYP11A1 and CYP19A1 in vitro.41 Human oocytes cultured in medium containing BPA (20 ng/mL to 20 μg/mL) exhibited abnormal meiotic maturation, changed spindle morphology and delayed chromosome alignment.42 In sum, the synthesis of hormones and development of oocyte in vitro were significantly affected by BPA.

Other Bisphenols and Female Reproductive Functions

Due to the public concern about the risk of BPA in endocrine related diseases and infertility problems, the usage of BPA has been restricted in some products especially baby bottles in some countries, including Norway, Denmark, Germany, France and USA.43 Several chemicals with similar structures with BPA were used as substitutes, such as bisphenol-F (BPF) and bisphenol-S (BPS), which lack thorough safety investigations.44 Similar to BPA, these bisphenols could bind to the C-terminal ligand-binding domain of estrogen receptor and exhibit similar or weaker 45,46 estrogenic activity as BPA.

BPA, BPF and BPS are detected in our environment including water from rivers, sewage sludge and indoor air. Receipts, paper products, and many canned food and soft drinks were found to have BPS and BPF. In USA, BPF and BPS were detected in most of the human urine samples, albeit less frequent and lower concentrations than BPA in the same sam- 58,59 ple. Low concentration of BPS was detected in some serum samples of pregnant women and the cord blood of the sibling,60 suggesting BPS could also cross the placenta. Importantly, BPA, BPF and BPS could also be detected in breast milk.61

There is no published report regarding the association of BPF or BPS level and diseases related to pregnancy in humans. The potential effect of these bisphenols in reproduction was based on in vitro and in vivo animal studies. In porcine, BPS affected meiotic division of the oocytes and the expression and distribution of ERβ, ERα and aromatase.62 BPS reduced egg production and the gonadosomatic index (gonad weight/ body weight) in zebrafish.63 BPS and BPF increased the uterine 64 65 weight in rats,64 but another study did not find the same effect.65 In fact, the estrogenic and androgenic activities of BPF and BPS were found to have similar order of magnitude and mechanic

32-34 66,67 action as BPA. BPF and BPS also have genotoxicity and mutagenicity as BPA.44 Although, the evidence of BPF and BPS on female reproduction is limited, the activity and mechanism of these two bisphenols is quite similar to BPA, leading to the adverse effect of bisphenols on female reproductive health could not be ignored.

Conclusion

It is widely recognized that BPA is harmful to human health and female reproduction. Whether BPA at current low environmental level poses chronic and transgenerational effect remains unknown.68 Several countries have issued regulations to ban on the usage of BPA in specific products, such as baby bottles. Other bisphenols with similar structure to BPA are used to replace BPA in manufacturing process. Although compiling evidence of these bisphenols on female reproductive functions are lacking, concern about the safety of these bisphenols in public should be raised.

Acknowledgement

Part of the work is supported by Sanming Project of Medicine in Shenzhen (SZSM201612083) and GRF Grant (17120415) to KFL.

Conflicts Of Interest

The authors declare that they have no conflicts of interest.

References

1. GoreACCrewsDDoanLL. Introduction To Endocrine Disrupting Chemicals (EDCs). A Guide for Public Interest Organizations and Policy-Makers. Washington, DC, USA: Endo- 47-49 crine Society; 2014: 7-13. 50-57
2. RochesterJR. Bisphenol A and human health: A review of the literature. Reprod Toxicol. 2013; 42: 132-1055. doi: 10.1016/j. reprotox.2013.08.00810.1016/j.reprotox.2013.08.008 https://doi.org/10.1016/j.reprotox.2013.08.008
3. WuttkeWJarryHSeidlova-WuttkeD. Definition, classification and mechanism of action of endocrine disrupting chemicals. Hormones (Athens). 2010; 9(1): 9-15
4. SchugTTJanesickABlumbergBHeindelJJ. Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol. 2011; 127(3-5): 204-215. doi: 10.1016/j.jsbmb.2011.08.00710.1016/j.jsbmb.2011.08.007 https://doi.org/10.1016/j.jsbmb.2011.08.007
5. DoddsECLawsonW. Synthetic strogenic agents without the phenanthrene nucleus. Nature. 1936; 137(996). doi: 10.1038/137996a010.1038/137996a0 https://doi.org/10.1038/137996a0
6. VandenbergLNHauserRMarcusMOleaNWelshonsWV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007; 24(2): 139-177. doi: 10.1016/j.reprotox.2007.07.01010.1016/j.reprotox.2007.07.010 https://doi.org/10.1016/j.reprotox.2007.07.010
7. SajikiJTakahashiKYonekuboJ. Sensitive method for the determination of bisphenol-A in serum using two systems of high-performance liquid chromatography. J Chromatogr B Biomed Sci Appl. 1999; 736(1-2): 255-261. doi: 10.1016/S0378- 4347(99)00471-510.1016/s0378-4347(99)00471-5 https://doi.org/10.1016/s0378-4347(99)00471-5
8. Vom Saal FS, Nagel SC, Coe BL, Angle BM, Taylor JA. The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Mol Cell Endocrinol. 2012; 354(1-2): 74-84. doi: 10.1016/j.mce.2012.01.001 https://doi.org/10.1016/j.mce.2012.01.001
9. PeretzJVroomanLRickeWA. Bisphenol a and reproductive health: Update of experimental and human evidence, 2007-2013. Environ Health Perspect. 2014; 122(8): 775-786. doi: 10.1289/ehp.130772810.1289/ehp.1307728 https://doi.org/10.1289/ehp.1307728
10. IkezukiYTsutsumiOTakaiYKameiYTaketaniY. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod. 2002; 17(11): 2839-2841
11. SchonfelderGWittfohtWHoppH. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect. 2002; 110(11): A703-A707
12. TakeuchiTTsutsumiOIkezukiYTakaiYTaketaniY. Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr J. 2004; 51(2): 165-169. doi: 10.1507/ endocrj.51.165
13. WangYZhuQDangX. Local effect of bisphenol A on the estradiol synthesis of ovarian granulosa cells from PCOS. Gynecol Endocrinol. 2017; 33(1): 21-25. doi: 10.1080/09513590.2016.118464110.1080/09513590.2016.1184641 https://doi.org/10.1080/09513590.2016.1184641
14. ZhengYMWangYZhaoJ. Association between serum bisphenol-A and recurrent spontaneous abortion: A 1:2 case-control study, China. Zhonghua Liu Xing Bing Xue Za Zhi. 2012; 33(8): 841-845
15. Sugiura-OgasawaraMOzakiYSontaSMakinoTSuzumoriK. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod. 2005; 20(8): 2325-2329. doi: 10.1093/humrep/deh88810.1093/humrep/deh888 https://doi.org/10.1093/humrep/deh888
16. Mok-LinEEhrlichSWilliamsPL. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl. 2010; 33(2): 385-393. doi: 10.1111/j.1365- 2605.2009.01014.x10.1111/j.1365-2605.2009.01014.x https://doi.org/10.1111/j.1365-2605.2009.01014.x
17. SouterISmithKWDimitriadisI. The association of bisphenol-A urinary concentrations with antral follicle counts and other measures of ovarian reserve in women undergoing infertility treatments. Reprod Toxicol. 2013; 42: 224-231. doi: 10.1016/j.reprotox.2013.09.00810.1016/j.reprotox.2013.09.008 https://doi.org/10.1016/j.reprotox.2013.09.008
18. EhrlichSWilliamsPLMissmerSA. Urinary bisphenol A concentrations and implantation failure among women undergoing in vitro fertilization. Environ Health Perspect. 2012; 120(7): 978-983. doi: 10.1289/ehp.110430710.1289/ehp.1104307 https://doi.org/10.1289/ehp.1104307
19. Minguez-AlarconLGaskinsAJChiuYH. Urinary bisphenol A concentrations and association with in vitro fertilization outcomes among women from a fertility clinic. Hum Reprod. 2015; 30(9): 2120-2128. doi: 10.1093/humrep/dev18310.1093/humrep/dev183 https://doi.org/10.1093/humrep/dev183
20. CantonwineDEFergusonKKMukherjeeBMcElrathTFMeekerJD. Urinary bisphenol A levels during pregnancy and risk of preterm birth. Environ Health Perspect. 2015; 123(9): 895-901. doi: 10.1289/ehp.140812610.1289/ehp.1408126 https://doi.org/10.1289/ehp.1408126
21. HuoWXiaWWanY. Maternal urinary bisphenol A levels and infant low birth weight:A nested case-control study of the Health Baby Cohort in China. Environ Int. 2015; 85: 96-103. doi: 10.1016/j.envint.2015.09.00510.1016/j.envint.2015.09.005 https://doi.org/10.1016/j.envint.2015.09.005
22. ShenYXuQRenM. Measurement of phenolic environmental estrogens in women with uterine leiomyoma. PLoS One. 2013; 8(11): e79838. doi: 10.1371/journal.pone.007983810.1371/journal.pone.0079838 https://doi.org/10.1371/journal.pone.0079838
23. ItohHIwasakiMHanaokaT. Urinary bisphenol-A concentration in infertile Japanese women and its association with endometriosis: A cross-sectional study. Environ Health Prev Med. 2007; 12(6): 258-264. doi: 10.1007/BF0289803310.1007/bf02898033 https://doi.org/10.1007/bf02898033
24. KuiperGGLemmenJGCarlssonB. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology. 1998; 139(10): 4252-4263. doi: 10.1210/ endo.139.10.6216
25. HiroiHTsutsumiOMomoedaM. Differential interactions of bisphenol A and 17beta-estradiol with estrogen receptor alpha (ERalpha) and ERbeta. Endocr J. 1999; 46(6): 773-778. doi: 10.1507/endocrj.46.77310.1507/endocrj.46.773 https://doi.org/10.1507/endocrj.46.773
26. FangHTongWPerkinsR. Quantitative comparisons of in vitro assays for estrogenic activities. Environ Health Perspect. 2000; 108(8): 723-729
27. EysterKM. The Estrogen receptors: An overview from different perspectives. Methods Mol Biol. 2016; 1366: 1-10. doi: 10.1007/978-1-4939-3127-9_110.1007/978-1-4939-3127-9_1 https://doi.org/10.1007/978-1-4939-3127-9_1
28. WetherillYBAkingbemiBTKannoJ. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol. 2007; 24(2): 178-198. doi: 10.1016/j.reprotox.2007.05.01010.1016/j.reprotox.2007.05.010 https://doi.org/10.1016/j.reprotox.2007.05.010
29. NaciffJMKhambattaZSReichlingTD. The genomic response of Ishikawa cells to bisphenol A exposure is dose- and time-dependent. Toxicology. 2010; 270(2-3): 137-149. doi: 10.1016/j.tox.2010.02.00810.1016/j.tox.2010.02.008 https://doi.org/10.1016/j.tox.2010.02.008
30. LeeMSHyunSHLeeCK. Impact of xenoestrogens on the growth of human endometrial epithelial cells in a primary culture system. Fertil Steril. 2003; 79(6): 1464-1465. doi: 10.1016/S0015-0282(03)00360-110.1016/s0015-0282(03)00360-1 https://doi.org/10.1016/s0015-0282(03)00360-1
31. BredhultCSahlinLOlovssonM. Gene expression analysis of human endometrial endothelial cells exposed to Bisphenol A. Reprod Toxicol. 2009; 28(1): 18-25. doi: 10.1016/j.reprotox.2009.03.00610.1016/j.reprotox.2009.03.006 https://doi.org/10.1016/j.reprotox.2009.03.006
32. AghajanovaLGiudiceLC. Effect of bisphenol A on human endometrial stromal fibroblasts in vitro. Reprod Biomed Online. 2011. 22(3): 249-256. doi: 10.1016/j.rbmo.2010.12.00710.1016/j.rbmo.2010.12.007 https://doi.org/10.1016/j.rbmo.2010.12.007
33. ForteMMitaLCobellisL. Triclosan and bisphenol a affect decidualization of human endometrial stromal cells. Mol Cell Endocrinol. 2015; 18(15): 30142-30148. doi: 10.1016/j. mce.2015.11.01710.1016/j.mce.2015.11.017 https://doi.org/10.1016/j.mce.2015.11.017
34. MannelliCSzostekAZLukasikK. Bisphenol A modulates receptivity and secretory function of human decidual cells: An in vitro study. Reproduction. 2015; 150(2): 115-125. doi: 10.1530/REP-14-060110.1530/rep-14-0601 https://doi.org/10.1530/rep-14-0601
35. BenachourNArisA. Toxic effects of low doses of Bisphenol-A on human placental cells. Toxicol Appl Pharmacol. 2009; 241(3): 322-328. doi: 10.1016/j.taap.2009.09.00510.1016/j.taap.2009.09.005 https://doi.org/10.1016/j.taap.2009.09.005
36. MorckTJSordaGBechiN. Placental transport and in vitro effects of Bisphenol A. Reprod Toxicol. 2010; 30(1): 131- 137. doi: 10.1016/j.reprotox.2010.02.00710.1016/j.reprotox.2010.02.007 https://doi.org/10.1016/j.reprotox.2010.02.007
37. SpagnolettiAPaulesuLMannelliC. Low concentrations of Bisphenol A and para-Nonylphenol affect extravillous pathway of human trophoblast cells. Mol Cell Endocrinol. 2015; 412: 56-64. doi: 10.1016/j.mce.2015.05.02310.1016/j.mce.2015.05.023 https://doi.org/10.1016/j.mce.2015.05.023
38. WangZYLuJZhangYZ. Effect of Bisphenol A on invasion ability of human trophoblastic cell line BeWo. Int J Clin Exp Pathol. 2015; 8(11): 14355-14364
39. CasertaDDi SegniNMallozziM. Bisphenol A and the female reproductive tract: An overview of recent laboratory evidence and epidemiological studies. Reprod Biol Endocrinol. 2014; 12: 37. doi: 10.1186/1477-7827-12-3710.1186/1477-7827-12-37 https://doi.org/10.1186/1477-7827-12-37
40. Ziv-GalAFlawsJA. Evidence for bisphenol A-induced female infertility: Review (2007-2016). Fertil Steril. 2016; 106(4): 827-856. doi: 10.1016/j.fertnstert.2016.06.02710.1016/j.fertnstert.2016.06.027 https://doi.org/10.1016/j.fertnstert.2016.06.027
41. MansurAAdirMYerushalmiG. Does BPA alter steroid hormone synthesis in human granulosa cells in vitro? Hum Reprod. 2016; 31(7): 1562-1569. doi: 10.1093/humrep/dew08810.1093/humrep/dew088 https://doi.org/10.1093/humrep/dew088
42. MachtingerRCombellesCMMissmerSA. Bisphenol-A and human oocyte maturation in vitro. Hum Reprod. 2013 28(10): 2735-2745. doi: 10.1093/humrep/det31210.1093/humrep/det312 https://doi.org/10.1093/humrep/det312
43. MetzCM. Bisphenol A: Understanding the controversy. Workplace Health Saf. 2016; 64(1): 28-36; quiz 37. doi: 10.1177/216507991562379010.1177/2165079915623790 https://doi.org/10.1177/2165079915623790
44. UsmanAAhmadM. From BPA to its analogues: Is it a safe journey? Chemosphere. 2016; 158: 131-142. doi: 10.1016/j.chemosphere.2016.05.07010.1016/j.chemosphere.2016.05.070 https://doi.org/10.1016/j.chemosphere.2016.05.070
45. ChenDKannanKTanH. Bisphenol analogues other than BPA: Environmental occurrence, human exposure, and toxicity-A review. Environ Sci Technol. 2016; 50(11): 5438-5453. doi: 10.1021/acs.est.5b0538710.1021/acs.est.5b05387 https://doi.org/10.1021/acs.est.5b05387
46. DelfosseVGrimaldiMPonsJL. Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes. Proc Natl Acad Sci U S A. 2012; 109(37): 14930-14935. doi: 10.1073/ pnas.1203574109
47. YamazakiEYamashitaNTaniyasuS. Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotoxicol Environ Saf. 2015; 122: 565-572. doi: 10.1016/j. ecoenv.2015.09.02910.1016/j.ecoenv.2015.09.029 https://doi.org/10.1016/j.ecoenv.2015.09.029
48. RuanTLiangDSongS. Evaluation of the in vitro estrogenicity of emerging bisphenol analogs and their respective estrogenic contributions in municipal sewage sludge in China. Chemosphere. 2015; 124: 150-155. doi: 10.1016/j.chemosphere.2014.12.01710.1016/j.chemosphere.2014.12.017 https://doi.org/10.1016/j.chemosphere.2014.12.017
49. XueJWanYKannanK. Occurrence of bisphenols, bisphenol A diglycidyl ethers (BADGEs), and novolac glycidyl ethers (NOGEs) in indoor air from Albany, New York, USA, and its implications for inhalation exposure. Chemosphere. 2016; 151: 1-8. doi: 10.1016/j.chemosphere.2016.02.03810.1016/j.chemosphere.2016.02.038 https://doi.org/10.1016/j.chemosphere.2016.02.038
50. VinasPCampilloNMartinez-CastilloNHernandez-CordobaM. Comparison of two derivatization-based methods for solid-phase microextraction-gas chromatography-mass spectrometric determination of bisphenol A, bisphenol S and biphenol migrated from food cans. Anal Bioanal Chem. 2010; 397(1): 115-125. doi: 10.1007/s00216-010-3464-710.1007/s00216-010-3464-7 https://doi.org/10.1007/s00216-010-3464-7
51. Gallart-AyalaHMoyanoEGalceranMT. Analysis of bisphenols in soft drinks by on-line solid phase extraction fast liquid chromatography-tandem mass spectrometry. Anal Chim Acta. 2011; 683(2): 227-233. doi: 10.1016/j.aca.2010.10.03410.1016/j.aca.2010.10.034 https://doi.org/10.1016/j.aca.2010.10.034
52. LiaoCKannanK. Concentrations and profiles of bisphenol A and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure. J Agric Food Chem. 2013;. 61(19): 4655-4662. doi: 10.1021/jf400445n10.1021/jf400445n https://doi.org/10.1021/jf400445n
53. Liao C, Kannan K.A survey of bisphenolA and other bisphenol analogues in foodstuffs from nine cities in China. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2014; 31(2): 319-329. doi: 10.1080/19440049.2013.868611 https://doi.org/10.1080/19440049.2013.868611
54. RussoGBarbatoFGrumettoL. Monitoring of bisphenol A and bisphenol S in thermal paper receipts from the Italian market and estimated transdermal human intake: A pilot study. Sci Total Environ. 2017; 599-600: 68-75. doi: 10.1016/j.scitotenv.2017.04.19210.1016/j.scitotenv.2017.04.192 https://doi.org/10.1016/j.scitotenv.2017.04.192
55. LiaoCLiuFKannanK. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol a residues. Environ Sci Technol. 2012; 46(12): 6515-6522. doi: 10.1021/es300876n10.1021/es300876n https://doi.org/10.1021/es300876n
56. GlausiuszJ. Toxicology: The plastics puzzle. Nature. 2014; 508(7496): 306-308
57. JurekA. Leitner E. Analytical determination of bisphenol A (BPA) and bisphenol analogues in paper products by GC-MS/MS. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2017; 34(7):1225-1238. doi: 10.1080/19440049.2017.131907610.1080/19440049.2017.1319076 https://doi.org/10.1080/19440049.2017.1319076
58. ZhouXKramerJPCalafatAMYeX. Automated on-line column-switching high performance liquid chromatography isotope dilution tandem mass spectrometry method for the quantification of bisphenol A, bisphenol F, bisphenol S, and 11 other phenols in urine. J Chromatogr B Analyt Technol Biomed Life Sci. 2014; 944: 152-156. doi: 10.1016/j.jchromb.2013.11.00910.1016/j.jchromb.2013.11.009 https://doi.org/10.1016/j.jchromb.2013.11.009
59. YeXWongLYKramerJ. Urinary concentrations of bisphenol A and three other bisphenols in convenience samples of U.S. Adults during 2000-2014. Environ Sci Technol. 2015; 49(19): 11834-11839. doi: 10.1021/acs.est.5b0213510.1021/acs.est.5b02135 https://doi.org/10.1021/acs.est.5b02135
60. LiuJLiJWuY. Bisphenol A Metabolites and Bisphenol S in Paired Maternal and Cord Serum. Environ Sci Technol. 2017. doi: 10.1021/acs.est.6b0571810.1021/acs.est.6b05718 https://doi.org/10.1021/acs.est.6b05718
61. NiuYWangBZhaoYZhangJShaoB. A highly sensitive and high-throughput method for the analysis of bisphenol analogues and their halogenated derivatives in breast milk. J Agric Food Chem. 2017. doi: 10.1021/acs.jafc.7b0439410.1021/acs.jafc.7b04394 https://doi.org/10.1021/acs.jafc.7b04394
62. ZalmanovaTHoskovaKNevoralJ. Bisphenol S negatively affects the meotic maturation of pig oocytes. Sci Rep. 2017; 7(1): 485. doi: 10.1038/s41598-017-00570-510.1038/s41598-017-00570-5 https://doi.org/10.1038/s41598-017-00570-5
63. JiKHongSKhoYChoiK. Effects of bisphenol S exposure on endocrine functions and reproduction of zebrafish. Environ Sci Technol. 2013; 47(15): 8793-800. doi: 10.1021/es400329t10.1021/es400329t https://doi.org/10.1021/es400329t
64. YamasakiKNodaSImatanakaNYakabeY. Comparative study of the uterotrophic potency of 14 chemicals in a uterotrophic assay and their receptor-binding affinity. Toxicol Lett. 2004; 146(2): 111-120. doi: 10.1016/j.toxlet.2003.07.00310.1016/j.toxlet.2003.07.003 https://doi.org/10.1016/j.toxlet.2003.07.003
65. StrohekerTChagnonMCPinnertMFBergesRCanivenc-LavierMC. Estrogenic effects of food wrap packaging xenoestrogens and flavonoids in female Wistar rats: A comparative study. Reprod Toxicol. 2003; 17(4): 421-432. doi: 10.1016/ S0890-6238(03)00044-3
66. Rochester JR and Bolden AL. Bisphenol S and F: A systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect. 2015; 123(7): 643-650. doi: 10.1289/ehp.1408989 https://doi.org/10.1289/ehp.1408989
67. RosenmaiAKDybdahlMPedersenM. Are structural analogues to bisphenol a safe alternatives? Toxicol Sci. 2014; 139(1): 35-47. doi: 10.1093/toxsci/kfu03010.1093/toxsci/kfu030 https://doi.org/10.1093/toxsci/kfu030
68. HengstlerJGFothHGebelT. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol A. Crit Rev Toxicol. 2011; 41(4): 263-291. doi: 10.3109/10408444.2011.55848710.3109/10408444.2011.558487 https://doi.org/10.3109/10408444.2011.558487