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. 2017 Dec 15;8(4):341–345.

Effects of bisphenol-S low concentrations on oxidative stress status and in vitro fertilization potential in mature female mice

Alireza Nourian 1, Ali Soleimanzadeh 1,*, Ali Shalizar Jalali 2, Gholamreza Najafi 2
PMCID: PMC5756255  PMID: 29326794

Abstract

Bisphenol-S (BPS) is a new bisphenol-A substitute widely used in many plastic products. Bisphenol-A as a main member of bisphenol family has been known as an endocrine system disrupter chemical compound. Like other members of bisphenol family, there is public health concern about the toxic effects of BPS on reproductive system, thus, we examined BPS effects on in vitro fertilization (IVF) potential and oxidative stress status in a murine model. Adult female mice (n = 70) were randomly divided into control and BPS-treated groups. Bisphenol-S was administered at doses of 0, 1, 5, 10, 50 and 100 µg kg-1 body weight per day intraperitoneally for 21 consecutive days. Twenty-Four hr after the last treatment, five mice in each group were super-ovulated and the oocytes were harvested for IVF. All ovaries were collected and used for biochemical factors analyses. Bisphenol-S exposure at doses more than 10 µg kg-1 induced developmental arrest of pre-implantation embryos. Further, lipid peroxidation measurement in ovaries indicated that all doses of BPS cause oxidative stress in female mice. In conclusion, BPS administration even in low doses can result in female reproductive toxicities and oxidative stress in mice.

Key Words: Bisphenol-S, In vitro fertilization, Mouse, Oxidative stress

Introduction

Endocrine disrupter chemicals (EDCs) are exogenous chemicals which interrupt the physiological function of estrogen due to their high affinity to estrogen receptors.1 Because of the harmful potential of EDCs on human health, they have been widely investigated in the last two decades.2 Bisphenol-A (BPA) is one of the main EDCs being used in many modern life materials such as plastic containers, adhesives, paints, dental sealants, infants feeding bottles and paper products.3 The worldwide production of BPA was nearly over three million tons in 2003.4 The BPA can be absorbed through ingestion, inhalation and skin and can be detected in blood, urine, amniotic fluid and fetal plasma samples in nMol concentration which is harmful for fetal development and differentiation.5

Previously, detrimental effects of BPA on female reproductive system have been shown.6-11 The BPA has been detected in serum and follicular fluid of women with polycystic ovary syndrome.12,13 Moreover, in utero exposure of BPA affects early ovarian development in pregnant mice and inhibits germ cell nest breakdown in ovary.14

Because of public health concern, many countries use BPA-substitutes in their new products, however, toxic effects of these materials have been addressed recently in animal model studies.15

Bisphenol-S (BPS), a BPA-substitute, is widely used in many new products such as baby bottles and food containers, especially BPA-free labeled ones and its production increases annually.15,16 The BPS was named as a safe substitute because of better stability at high temperature and sunlight and lesser estrogenic activity.17-21

Estrogenic effects as well as oxidative properties of bisphenol family were examined previously. It has been reported that they can induce oxidative stress in many tissues including testis, brain, liver and kidney.22,23 It was found that BPS has less oxidative effects on blood cells compared to BPA, bisphenol-F (BPF) and bisphenol-AF, but BPS and BPA have much destructive effects on proteins.16,24 In vitro study on human peripheral blood mononuclear cells revealed that BPS doesn’t induce significant DNA damage.25

Accordingly, administration of BPA induced dose dependent testicular toxicity in mice and rats.26 Further, it has been reported that BPA reduces sperm quality via disruption of extracellular-signal-regulated kinase pathway.27 Recently, evaluation of BPS and BPF effects on human and mouse fetal testis cultures showed that BPS can suppress testosterone production.28 Histological and biochemical evidence in rat model study demonstrated that BPS causes testicular toxicities.29

Based on this concept, current study was designed to elucidate the dose dependent effects of BPS exposure on in vitro fertilization (IVF) outcome and oxidative stress status by using mice as an animal model.

Materials and Methods

Chemicals. The BPS (99%, 4, 4′-Sulfonyldiphenol), (CAS No. 80-09-1) and ethanol (ACS grade; CAS No. 64-17-5) were purchased from Sigma-Aldrich Company (St. Louis, USA).

Animals. Seventy sexually adult, same cycling stage, female mice (age 70-80 days) were obtained from Animal Resources Center of the Faculty of Veterinary Medicine, Urmia University. In the first stage of study, estrus cycle stage was determined by vaginal smears for all mice.30 Mice were housed in groups of ten animals per case (standard cage) with 12-12 hr dark-light cycle. Animals were fed by soy free food and had free access to water. The experiments were performed on animals in accordance with the guidelines of the ethical committee for research on laboratory animals of Urmia University (3/PD/47, 2016).

Experimental protocol. Mice were adapted to environment for seven days. Different doses (0, 1.00, 5.00, 10.00, 50.00 and 100.00 µg kg-1 body weight per day; IP) of BPS were used for 21 consecutive days in this study based on previous studies and one group was served as a control group.31 Twenty-four hr after the last treatment, five mice in each group were euthanized by combination of ketamine (45 mg kg-1; IP) and xylazine (35 mg kg-1; IP).31 Then, ovaries were collected immediately and used for biochemical analyses.

Oocytes collection and IVF assays. Five mature female mice were chosen randomly in each group and super-ovulated as previously described.32 Five to 10 IU of pregnant mare’s serum gonadotropin (PMSG; Intervet International BV, Boxmeer, The Netherlands) and 7.50 IU human chorionic gonadotropin (hCG; Intervet International BV) were injected intraperitoneally 48 hr and 12 hr before experiment into all mice, respectively. Human tubal fluid (HTF; Sigma) medium was equilibrated with 5% CO2 at 37 °C in incubator (SINA Company, Tehran, Iran) for 24 hr before experiment. Mouse sperm was prepared by harvesting one mouse caudal epididymis and incubated for 1 hr in HTF medium before the experiment for capacitation. In the day of experiment, all cumulus-oocyte complexes were collected and incubated for 1 hr. Metaphase II arrested mouse oocytes were inseminated with capacitated sperms as described above and 4 hr later, all fertilized zygotes were transferred to HTF cleavage medium. All zygotes were evaluated 24 hr, 48 hr and five days after insemination. Intact, fragmented and/or lysed embryos which did not develop, were recorded as arrested embryos. In the current study, the rate of cell lyses was recorded as follows: Type I: fully lysed, necrotic and/or fragmented embryos, Type II: embryos with partially lysed/fragmented blastomeres and Type III: embryos with some lysed/fragmented blastomeres and/or cytoplasmic vesicles.33

Lipid peroxidation. Malondialdehyde (MDA) is commonly used as an indicator of lipid peroxidation in oxidative stress status examination. A volume of 300 µL of 10.00% trichloro-acetic acid (Sigma) was added to150 µL of ovarian tissue samples and centrifuged at 1000 rpm for 10 min at 4 ˚C, then, incubated in 300 µL of 67.00% thio-barbituric acid (TBA; Sigma) at 100 ˚C for 25 min. Five min after cooling of the solution, pink color was appeared because of MDA-TBA reaction and evaluated using a spectrometer (model Novaspec II; Biochrom Ltd., Cambridge, UK) at a wave length of 535 nm.34

Statistical analysis. The data were analyzed by SPSS (version 20; SPSS Inc., Chicago, USA) and one-way ANOVA. A p value less than 0.05 was considered statistically significant.

Results

In vitro fertilization. As shown in Table 1, BPS exposure at 10.00, 50.00 and 100.00 µg kg-1 caused significant reduction in fertilization rate. The 2-cell embryo percentage was changed even in low doses of BPS, however, doses more than 10.00 µg kg-1 induced meaningful reduction. In addition, blastocyst rate reduction was statistically significant following 10.00, 50.00 and 100.00 µg kg-1 BPS administration. Moreover, 5.00 µg kg-1 of BPS induced reduction in blastocyst rate which wasn’t statistically meaningful. According to Table 2, all concentrations of BPS inhibited embryo development and increased embryo arrest, however, statistical analyses revealed that BPS treatment only at doses of 50.00 and 100.00 µg kg-1 resulted in significant increase of total and type I embryo arrests.

Lipid peroxidation. The antioxidant status in ovarian tissues based on MDA measurement in control, control sham, BPS 1, BPS 5, BPS 10, BPS 50 and BPS 100, groups were 3.87 ± 0.94, 3.80 ± 0.83, 4.52 ± 1.13, 4.97 ± 1.07, 6.26 ± 0.71, 8.73 ± 1.39 and 9.11 ± 1.23, respectively. The BPS administration led to MDA elevation in mice ovaries in a dose dependent manner.

Table 1.

Dose dependent effect of bisphenol-S on in vitro fertilization outcome in experimental groups. Data are presented as mean ± SE.

Groups Oocyte number Fertilization rate (%) 2-cell embryos (%) Blastocysts (%)
Control 88 80.68 ± 1.18(71.00)a 85.91 ± 0.83(61.00) a 59.15 ± 1.40(42.00) a
Control sham 86 83.72 ± 0.79(72.00) a 86.11 ± 1.45(62.00) a 59.72 ± 1.12(43.00) a
BPS 1 82 80.48 ± 1.21(66.00) a 83.33 ± 1.35(55.00)ac 57.57 ± 1.45(38.00) a
BPS 5 75 77.33 ± 1.30(58.00) a 77.58 ± 0.69(45.00) ac 56.89 ± 0.84(33.00)ab
BPS 10 61 60.65 ± 0.92(37.00)b 67.56 ± 0.81(25.00) ac 51.35 ± 0.79(19.00) b
BPS 50 57 50.87 ± 1.16(29.00) b 65.51 ± 1.47(19.00) ac 31.03 ± 1.31(9.00)c
BPS 100 37 56.75 ± 0.63(21.00) b 61.90 ± 1.15(13.00) ac 33.33 ± 0.94(7.00)c
Open in a new tab
abc

Means within a column with different superscript letters denote significant differences (p < 0.05).

Table 2.

Dose dependent effect of bisphenol-S on embryo arrest in experimental groups. Data are presented as mean ± SE.

Groups Arrested embryos (%) Type 1 (%) Type 2 (%) Type 3 (%)
Control 40.84 ± 0.48(29.00) a 7.40 ± 0.83(5.00)a 9.85 ± 1.19(7.00) a 23.94 ± 0.72(17.00) a
Control sham 40.27 ± 1.16(29.00.00) a 2.77 ± 0.51(2.00) a 12.50 ± 0.65(9.00)ac 25.00 ± 1.18(18.00) a
BPS 1 42.42 ± 0.76(28.00) a 9.09 ± 0.89(6.00) ac 15.15 ± 0.92(10.00) ac 18.18 ± 1.32(12.00) a
BPS 5 43.10 ± 0.39(25.00)ac 10.34 ± 0.47(6.00)ad 13.79 ± 1.26(8.00) ac 18.96 ± 0.49(11.00) a
BPS 10 48.64 ± 1.24(18.00)ab 21.62 ± 0.71(8.00)bcd 13.51 ± 1.40(5.00) ac 13.51 ± 0.81(5.00) a
BPS 50 68.96 ± 1.49(20.00)bd 34.48 ± 0.63(10.00)b 24.13 ± 0.79(7.0)bc 10.34 ± 1.64(3.00) a
BPS 100 66.66 ± 0.55(14.00)bcd 28.57 ± 1.24(6.00)bcd 28.57 ± 0.97(6.00) ac 9.52 ± 1.04(2.00) a
Open in a new tab
abcd

Means within a column with different superscript letters denote significant differences (p < 0.05).

Discussion

The BPS, a substitute of BPA, has been introduced to the manufacture as a safer alternative to BPA in multiple products.35 Moreover, BPS exhibits less estrogenic activities in comparison to BPA.36 Similarly, BPS has been shown to have apoptotic and oxidative properties as well as toxic effects in male reproductive system and it induces DNA damages.16,29,37-39 This study was conducted to determine the effects of BPS on female mice fertility and oxidative stress status in ovarian tissue.

Recently, EDCs effects on fertility have caused great concern.40,41 In our study, fertilization rates, 2-cell embryo numbers and blastocyst percentages reduced significantly in 10.00, 50.00 and 100.00 µg kg-1 groups compared to control group. Comparison between higher (10.00, 20.00 and 50.00 µg kg-1) and lower (0.00, 1.00 and 5.00 µg kg-1) doses of BPS, revealed that BPS doesn’t have significant effects on IVF outcomes in low doses. However, there were slight reductions in 2-cell and blastocyst rates in lower dosages of BPS which were not statistically meaningful. Previous studies have reported that BPS causes male and female gonadal weight along with egg production and hatchability reductions.15 Furthermore, it has been suggested that BPA concentration in blood and follicular fluid can be associated with embryo quality, implantation rate and IVF outcomes.42 It has been shown that low (1.00 µg L-1) and high (100.00 µg L-1) concentrations of BPS have negative impacts on egg production, fertilization and hatching rates which confirm our findings.43

In this study, higher doses of BPS induced remarkable oxidant/antioxidant imbalance in ovarian tissue compared to lower doses, however, all BPS-treated groups showed MDA elevation in ovarian tissues compared to the control group. These findings are in agreement with the previous report in which it was indicated that BPS disturbs oxidant/antioxidant balance in testicular tissue.29 Furthermore, in vitro studies have demonstrated that BPS plays important roles in oxidative stress induction.25,41,44,45

In conclusion, this study highlighted hidden aspects of BPS exposure particularly in female reproductive system and early embryo development. Further studies are required to uncover precise mechanisms of BPS-induced embryo toxicities.

Acknowledgments

The authors would like to sincerely thank the Faculty of Veterinary Medicine and Urmia University Research Council for the approval and support of this research.

References

  • 1.Schöpel M, Herrmann C, Scherkenbeck J, et al. The bisphenol A analogue bisphenol S binds to K‐Ras4B–implications for ‘BPA‐free’plastics. FEBS Letters. 2016;590(3):369–375. doi: 10.1002/1873-3468.12056. [DOI] [PubMed] [Google Scholar]
  • 2.Sifakis S, Androutsopoulos VP, Tsatsakis AM, et al. Human exposure to endocrine disrupting chemicals: Effects on the male and female reproductive system. Environ Toxicol Pharmacol. 2017;51:56–70. doi: 10.1016/j.etap.2017.02.024. [DOI] [PubMed] [Google Scholar]
  • 3.Qiu W, Zhao Y, Yang M, et al. Actions of bisphenol A and bisphenol S on the reproductive neuroendocrine system during early development in zebrafish. Endocrinology. 2015;157(2):636–647. doi: 10.1210/en.2015-1785. [DOI] [PubMed] [Google Scholar]
  • 4.Richter CA, Birnbaum LS, Farabollini F, et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007;24(2):199–224. doi: 10.1016/j.reprotox.2007.06.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Gerona RR, Woodruff TJ, Dickenson CA, et al. Bisphenol-A (BPA), BPA glucuronide, and BPA sulfate in midgestation umbilical cord serum in a northern and central California population. Environ Sci Technol. 2013;47(21):12477–12485. doi: 10.1021/es402764d. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Tarantino G, Valentino R, Somma CD, et al. Bisphenol A in polycystic ovary syndrome and its association with liver–spleen axis. Clin Endocrinol. 2013;78(3):447–453. doi: 10.1111/j.1365-2265.2012.04500.x. [DOI] [PubMed] [Google Scholar]
  • 7.Papalou O, Diamanti-Kandarakis E. The role of stress in PCOS. Expert Rev Endocrinol Metab. 2017;12(1):87–95. doi: 10.1080/17446651.2017.1266250. [DOI] [PubMed] [Google Scholar]
  • 8.Zhou C, Wang W, Peretz J, et al. Bisphenol A exposure inhibits germ cell nest breakdown by reducing apoptosis in cultured neonatal mouse ovaries. Reprod Toxicol. 2015;57:87–99. doi: 10.1016/j.reprotox.2015.05.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Ganesan S, Keating AF. Bisphenol A-induced ovotoxicity involves DNA damage induction to which the ovary mounts a protective response indicated by increased expression of proteins involved in DNA repair and xenobiotic biotransformation. Toxicol Sci. 2016;152(1):169–180. doi: 10.1093/toxsci/kfw076. [DOI] [PubMed] [Google Scholar]
  • 10.Santamaría C, Durando M, de Toro MM, et al. Ovarian dysfunctions in adult female rat offspring born to mothers perinatally exposed to low doses of bisphenol. J Steroid Biochem Mol Biol. 2016;158:220–230. doi: 10.1016/j.jsbmb.2015.11.016. [DOI] [PubMed] [Google Scholar]
  • 11.Zhang R, Liu R, Zong W. Bisphenol S interacts with catalase and induces oxidative stress in mouse liver and renal cells. J Agric Food Chem. 2016;64(34):6630–6640. doi: 10.1021/acs.jafc.6b02656. [DOI] [PubMed] [Google Scholar]
  • 12.Kandaraki E, Chatzigeorgiou A, Livadas S, et al. Endocrine disruptors and polycystic ovary syndrome (PCOS): Elevated serum levels of bisphenol A in women with PCOS. J Clin Endocrinol Metab. 2010;96(3):E480–E484. doi: 10.1210/jc.2010-1658. [DOI] [PubMed] [Google Scholar]
  • 13.Boutzios G, Mina A, Papoutsis I, et al. Follicular fluid bisphenol A levels are higher and correlate negatively with the number of oocytes in women with tubal factor infertility compared to women with polycystic ovary syndrome. Endocrine Abstracts . 2016;41:EP661. doi:10. 1530/endoabs.41.EP661. [Google Scholar]
  • 14.Wang W, Hafner KS, Flaws JA. In utero bisphenol A exposure disrupts germ cell nest breakdown and reduces fertility with age in the mouse. Toxicol Appl Pharmacol. 2014;276(2):157–164. doi: 10.1016/j.taap.2014.02.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Rochester JR, 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. doi: 10.1289/ehp.1408989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Michalowicz J, Mokra K, Bąk A. Bisphenol A and its analogs induce morphological and biochemical alterations in human peripheral blood mononuclear cells (in vitro study) Toxicol In Vitro. 2015;29(7):1464–1472. doi: 10.1016/j.tiv.2015.05.012. [DOI] [PubMed] [Google Scholar]
  • 17.Lotti N, Colonna M, Fiorini M, et al. Poly (ethylene terephthalate), modified with bisphenol S units, with increased glass transition temperature. J Appl Polym Sci. 2013;128(1):416–423. [Google Scholar]
  • 18.Molina-Molina JM, Amaya E, Grimaldi M, et al. In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-A congeners and derivatives via nuclear receptors. Toxicol Appl Pharmacol. 2013;272(1):127–136. doi: 10.1016/j.taap.2013.05.015. [DOI] [PubMed] [Google Scholar]
  • 19.Chen MY, Ike M, Fujita M. Acute toxicity, mutagenicity, and estrogenicity of bisphenol‐A and other bisphenols. Environ Toxicol. 2002;17(1):80–86. doi: 10.1002/tox.10035. [DOI] [PubMed] [Google Scholar]
  • 20.Rwei SP, Kao SC, Liou GS, et al. Curing and pyrolysis of epoxy resins containing 2-(6-oxido-6H-dibenz (c, e)(1, 2) oxaphosphorin-6-yl)-1, 4-naphthalenediol or bisphenol S. Colloid Polym Sci. 2003;281(5):407–415. [Google Scholar]
  • 21.Michałowicz J. Bisphenol A–sources, toxicity and biotransformation. Environ Toxicol Pharmacol. 2014;37(2):738–758. doi: 10.1016/j.etap.2014.02.003. [DOI] [PubMed] [Google Scholar]
  • 22.Kabuto H, Amakawa M, Shishibori T. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes under-development of the brain and testis in mice. Life Sci. 2004;74(24):2931–2940. doi: 10.1016/j.lfs.2003.07.060. [DOI] [PubMed] [Google Scholar]
  • 23.Aydoğan M, Korkmaz A, Barlas N, et al. The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicol. 2008;249(1):35–39. doi: 10.1016/j.tox.2008.04.002. [DOI] [PubMed] [Google Scholar]
  • 24.Mokra K, Kocia M, Michałowicz J. Bisphenol A and its analogs exhibit different apoptotic potential in peripheral blood mononuclear cells (in vitro study) Food Chem Toxicol. 2015;84:79–88. doi: 10.1016/j.fct.2015.08.007. [DOI] [PubMed] [Google Scholar]
  • 25.Mokra K, Kuźmińska-Surowaniec A, Woźniak K, et al. Evaluation of DNA-damaging potential of bisphenol A and its selected analogs in human peripheral blood mononuclear cells (in vitro study) Food Chem Toxicol. 2017;100:62–69. doi: 10.1016/j.fct.2016.12.003. [DOI] [PubMed] [Google Scholar]
  • 26.Takahashi O, Oishi S. Testicular toxicity of dietarily or parenterally administered bisphenol A in rats and mice. Food Chem Toxicol. 2003;41(7):1035–1044. doi: 10.1016/s0278-6915(03)00031-0. [DOI] [PubMed] [Google Scholar]
  • 27.Li J, Mao R, Zhou Q, et al. Exposure to bisphenol A (BPA) in Wistar rats reduces sperm quality with disruption of ERK signal pathway. Toxicol Mech Methods. 2016;26(3):180–188. doi: 10.3109/15376516.2016.1139024. [DOI] [PubMed] [Google Scholar]
  • 28.Eladak S, Grisin T, Moison D, et al. A new chapter in the bisphenol A story: Bisphenol S and bisphenol F are not safe alternatives to this compound. Fertil Steril. 2015;103(1):11–21. doi: 10.1016/j.fertnstert.2014.11.005. [DOI] [PubMed] [Google Scholar]
  • 29.Ullah H, Jahan S, Ain QU, et al. Effect of bisphenol S exposure on male reproductive system of rats: A histological and biochemical study. Chemosphere. 2016;152:383–391. doi: 10.1016/j.chemosphere.2016.02.125. [DOI] [PubMed] [Google Scholar]
  • 30.Byers SL, Wiles MV, Dunn SL, et al. Mouse estrous cycle identification tool and images. PloS One. 2012;7(4):e35538. doi: 10.1371/journal.pone.0035538. doi: 10.1371/journal.pone.0035538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Jalali AS, Najafi G, Hosseinchi M, et al. Royal jelly alleviates sperm toxicity and improves in vitro fertilization outcome in stanozolol-treated mice. Iran J Reprod Med. 2015;13(1):15–22. [PMC free article] [PubMed] [Google Scholar]
  • 32.Babaei M, Najafi G, Jalali AS, et al. Effects of unilateral iatrogenic vas deferens trauma on fertility: An experimental in vitro fertilization mice model study. Bull Emerg Trauma. 2015;3(4):122–127. [PMC free article] [PubMed] [Google Scholar]
  • 33.Armand Z, Najafi G, Farokhi F, et al. Attenuation of cyclosporine-induced sperm impairment and embryotoxicity by crataegus monogyna fruit aqueous extract. Cell J. 2013;15(3):198–205. [PMC free article] [PubMed] [Google Scholar]
  • 34.Hosseinzadeh H, Sadeghnia HR. Safranal, a constituent of Crocus sativus (saffron), attenuated cerebral ischemia induced oxidative damage in rat hippo-campus. J Pharm Pharm Sci. 2005;8(3):394–399. [PubMed] [Google Scholar]
  • 35.Chen Y, Shu L, Qiu Z, et al. Exposure to the BPA-substitute bisphenol S causes unique alterations of germline function. PLoS Genet. 2016;12(7):e1006223. doi: 10.1371/journal.pgen.1006223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Papapostolou M. In vitro approach to test estrogen-like activity of six bisphenol A analogues. MSc Thesis. Wageningen University: Wageningen, The Netherlands; 2016. [Google Scholar]
  • 37.Liang S, Yin L, Yu K, et al. High-content analysis provides mechanistic insights into the testicular toxicity of bisphenol A and selected analogues in mouse spermatogonial cells. Toxicol Sci. 2017;155(1):43–60. doi: 10.1093/toxsci/kfw178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Ullah H, Ambreen A, Ahsan N, et al. Bisphenol S induces oxidative stress and DNA damage in rat spermatozoa in vitro and disrupts daily sperm production in vivo. Toxicol Environ Chem. 2017;99(5-6):1–13. [Google Scholar]
  • 39.Maćczak A, Cyrkler M, Bukowska B, et al. Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study) Toxicol In Vitro. 2017;41:143–149. doi: 10.1016/j.tiv.2017.02.018. [DOI] [PubMed] [Google Scholar]
  • 40.Mínguez-Alarcón L, Gaskins AJ, Chiu YH, et al. 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/dev183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Mínguez-Alarcón L, Hauser R, Gaskins AJ. Effects of bisphenol A on male and couple reproductive health: A review. Fertil Steril. 2016;106(4):864–870. doi: 10.1016/j.fertnstert.2016.07.1118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Machtinger R, Orvieto R. Bisphenol A, oocyte maturation, implantation, and IVF outcome: Review of animal and human data. Reprod Biomed Online. 2014;29(4):404–410. doi: 10.1016/j.rbmo.2014.06.013. [DOI] [PubMed] [Google Scholar]
  • 43.Naderi M, Wong MY, Gholami F. Developmental exposure of zebrafish (Danio rerio) to bisphenol-S impairs subsequent reproduction potential and hormonal balance in adults. Aquat Toxicol. 2014;148:195–203. doi: 10.1016/j.aquatox.2014.01.009. [DOI] [PubMed] [Google Scholar]
  • 44.Huc L, Lemarié A, Guéraud F, et al. Low concentrations of bisphenol A induce lipid accumulation mediated by the production of reactive oxygen species in the mitochondria of HepG2 cells. Toxicol In Vitro. 2012;26(5):709–717. doi: 10.1016/j.tiv.2012.03.017. [DOI] [PubMed] [Google Scholar]
  • 45.Yazdani M, Andresen AM, Gjøen T. Short-term effect of bisphenol-A on oxidative stress responses in Atlantic salmon kidney cell line: A transcriptional study. Toxicol Mech Meth. 2016;26(4):295–300. doi: 10.1080/15376516.2016.1177864. [DOI] [PubMed] [Google Scholar]

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