Impact of Bisphenol S as an Endocrine Disruptor in a Freshwater Fish, Oreochromis mossambicus

Authors

  • Department of Zoology, University College, Thiruvananthapuram - 695034, Kerala
  • Department of Zoology, University College, Thiruvananthapuram - 695034, Kerala
  • Department of Zoology, University College, Thiruvananthapuram - 695034, Kerala
  • Department of Zoology, University College, Thiruvananthapuram - 695034, Kerala
  • Department of Zoology, University College, Thiruvananthapuram - 695034, Kerala

DOI:

https://doi.org/10.18311/jer/2019/27184

Keywords:

Bisphenol S, DNA Fragmentation, Endocrine Disruption, Thyroxine, Triiodothyronine

Abstract

Endocrine Disrupting Chemicals (EDCs) have the potential to alter the hormonal pathways concerned with regulation of the normal homeostatic mechanisms. The adverse effects of EDCs can be observed in areas where pollution is high, particularly in aquatic ecosystems, where persistent environmental chemicals accumulate. In the present study, we investigated the endocrine disrupting effects of Bisphenol S (BPS), if any, in the levels of thyroxine, triiodothyronine, cortisol and sex steroidal [17βestradiol (E2) and testosterone(T)] hormones in juvenile as well as adult Oreochromis mossambicus. Drastic changes in serum thyroxine and triiodothyronine levels showed that BPS treatment resulted in disruption of thyroid gland function. Alteration to significant levels in serum cortisol indicated acute stress and impairment of hypothalamic-pituitaryinterrenal axis. Significant changes (p<0.05) occurred in the steroidal hormone levels which are biomarkers of endocrine disruption as they affect hypothalamic-pituitary-gonadal axis in fish. Bisphenol S also revealed estrogenic potency by inducing significant alteration in the E2/T ratio. DNA fragmentation, if any, induced by BPS was also analyzed in juvenile fish. There was no significant DNA fragmentation observed in gel electrophoresis, but a significant elevation was seen in percent fragmented DNA in the diphenylamine method. Therefore, it could be concluded that BPS at different sublethal concentrations have a profound impact on endocrine physiology of fish.

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References

Kinnberg K, Toft G. Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulata). Ecotoxicol Environ Saf. 2003; 54:1624. doi.org/10.1016/s0147-6513 (02)00010-6. https://doi.org/10.1016/S0147-6513(02)00010-6.

Marino M, Pellegrini M, La Rosa P, Acconcia F. Susceptibility of estrogen receptor rapid responses to xenoestrogens: Physiological outcomes. Steroids. 2012; 77:910-917. https:// doi.org/10.1016/j.steroids.2012.02.019. PMid:22410438

Ropero AB, Alonso-Magdalena P, Ripoll C, Fuentes E, Nadal A. Rapid endocrine disruption: environmental estrogen actions triggered outside the nucleus. J Steroid Biochem Mol Biol. 2006; 102:163-169. https://doi.org/10.1016/j.jsbmb.2006.09.019. PMid:17084624.

Tabb MM, Blumberg B. New modes of action for endocrinedisrupting chemicals. Mol Endocrinol. 2006; 20:475-482. https://doi.org/10.1210/me.2004-0513. PMid:16037129.

Scholz S, Mayer I. Molecular biomarkers of endocrine disruption in small model fish. Mol Cell Endocrinol. 2008; 293: 57-70. https://doi.org/10.1016/j.mce.2008.06.008. PMid:18619515.

Mendil D, Demirci Z, Tuzen M, Soylak M. Seasonal investigation of trace element contents in commercially valuable fish species from the black sea, Turkey. Food Chem Toxicol. 2010; 48: 865-870. https://doi.org/10.1016/j.fct.2009.12.023. PMid:20036302.

Erler C, Novak J. Bisphenol A exposure: Human risk and health policy. J Pediatr Nurs. 2010; 25:400-407. https://doi.org/10.1016/j.pedn.2009.05.006. PMid:20816563.

Asimakopoulos AG, Thomaidis NS, Koupparis MA. Recent trends in biomonitoring of bisphenol A, 4-t-octylphenol, and 4-nonylphenol. Toxicol Lett. 2012; 210:141-154. https://doi.org/10.1016/j.toxlet.2011.07.032. PMid:21888958.

European Commission (EC). Bisphenol A: EU ban on baby bottles to enter into force tomorrow. European Union, Brussels. 2011.

US Food and Drug Administration. Update on bisphenol A for use in food contact applications. Silver Spring (MD): US Food and Drug Administration. 2010.

Health Canada. Government of Canada acts to protect newborns and infants from bisphenol A in polycarbonate plastic baby bottles. 2009.

Liao C, Liu F, Kannan K. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol A residues. Environ Sci Technol. 2012; 46:6515-6522. https://doi.org/10.1021/es300876n. PMid:22591511.

Lotti N, Colonna M, Fiorini M, Finelli L, Berti C. Poly(butylene terephthalate) modified with ethoxylated bisphenol S with increased glass transition temperature and improved thermal stability. Polymer. 2011; 52:904-911. https://doi.org/10.1016/j.polymer.2011.01.018.

Naderi M, Wong MYL, 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. https://doi.org/10.1016/j.aquatox.2014.01.009. PMid:24508763.

Ji K, Hong S, Kho Y, Choi K. Effects of bisphenol S exposure on endocrine functions and reproduction of zebra fish. Environ Sci Technol. 2013; 47:8793-8800. https://doi.org/10.1021/es400329t. PMid:23806087.

Nelson JC, Wilcox RB. Analytical performance of free and total thyroxine assays. Clin Chem.1996; 42:146-154. https://doi.org/10.1093/clinchem/42.1.146.

Bablok W. A general regression procedure for method transformation. Application of linear regression procedures for method comparison studies in clinical chemistry, Part III. J Clin Chem Clin Biochem. 1988; 26:783-790. https:// doi.org/10.1515/cclm.1988.26.11.783. PMid:3235954.

Iqbal MJ, Dalton M, Sawers RS. Binding of testosterone and estradiol to sex hormone binding globulin, human serum albumin and other plasma proteins: Evidence for non-specific binding of estradiol to sex hormone binding globulin. Clin Sci. 1983; 64:307-314. https://doi.org/10.1042/cs0640307. PMid:6681600.

Wheeler MJ. The determination of bio-available testosterone. Ann Clin Biochem. 1995; 32:345-357. https:// doi.org/10.1177/000456329503200401. PMid:7486793.

Iwasa M, Maeno Y, Inoue H, Koyama H, Matoba R. Induction of apoptotic cell death in rat thymus and spleen after a bolus injection of methamphetamine. Int J Legal Med. 1996; 109:23-28. https://doi.org/10.1007/ BF01369597. PMid:8876318.

Wolozin B, Iwasaki K, Vito P, Ganjei JK, Lacana E, Sunderland T. Participation of presenilin 2 in apoptosis: enhanced basal activity conferred by an Alzheimer mutation. Science. 1996; 274:1710-1713. https://doi.org/10.1126/science.274.5293.1710. PMid:8939861.

Duncan DB. Multiple Range and Multiple F Tests. Biometrics. 1995; 11:1-42. https://doi.org/10.2307/3001478.

Hecker M, Tyler CR, Hoffmann M Maddix S, Karbe I. Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe river, Germany. Environ Sci Technol. 2002; 36:2311-2321. https://doi.org/10.1021/ es010186h. PMid:12075783.

Soffker M, Tyler CR. Endocrine disrupting chemicals and sexual behaviors in fish - a critical review on effects and possible consequences. Crit Rev Toxicol. 2012; 42:653668. https://doi.org/10.3109/10408444.2012.692114. PMid:22697575.

Wendelaar Bonga SE. The stress response in fish. Physiol Rev. 1997; 77:591-625. https://doi.org/10.1152/ physrev.1997.77.3.591. PMid:9234959.

Mommsen TP, Vijayan MM, Moon TW. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish. 1999; 9: 211-268. https://doi.org/10.1023/A:1008924418720.

Norris DO. Vertebrate Endocrinology, 3rd ed. Academic Press, Inc., San Diego. 1997.

Barton BA. Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol. 2002; 42:517-525. https://doi.org/10.1093/icb/42.3.517. PMid:21708747.

Bury NR, Eddy FB, Codd GA. Stress responses of brown trout, Salmo Trutta L., to the cyanobacterium, Microcystis aeruginosa. Environ Toxicol Water Qual.1996; 11:187-193. https://doi.org/10.1002/(SICI)10982256(1996)11:3<187::AID-TOX3>3.0.CO;2-5.

Ernst B, Hoeger SJ, O'Brien E, Dietrich DR. Physiological stress and pathology in European whitefish (Coregonus lavaretus) induced by subchronic exposure to environmentally relevant densities of Planktothrix rubescens. Aquat Toxicol. 2007; 82:15-26. https://doi.org/10.1016/j.aquatox.2007.01.007. PMid:17320197.

Donaldson EM, Dye HM. Corticosteroid concentrations in sockeye salmon (Oncorhynchus nerka) exposed to low concentrations of copper. J Fish Res Bd Can. 1975; 33:533539. https://doi.org/10.1139/f75-065.

Hill CW, Fromm PO. Response of interrenal gland of rainbow trout (Salmo gairdneri) to stress. Gen Comp Endocrinol. 1968; 11:69-77. https://doi.org/10.1016/00166480(68)90108-1.

James VA, Wigham T. The effects of cadmium on prolactin cell activity and plasma cortisol levels in the rainbow trout (Salmo gairdneri). Aquat Toxicol. 1986; 8:273-280. https:// doi.org/10.1016/0166-445X(86)90079-2.

Richard AC, Daniel C, Anderson P, Hontela A. Effect of subchronic exposure to cadmium chloride on endocrine and metabolic functions in rainbow trout (Onchorhynchus mykiss). Arch Environ Contam Toxicol. 1998; 34:377-381. https://doi.org/10.1007/s002449900333. PMid:9543508.

Pandya P, Upadhyay A, Thakkar B, Parikh P. Evaluating the toxicological effects of agrochemicals on glucocorticoid receptor and serum cortisol level in Mozambique tilapia. Cogent Biol. 2018; 4:1. https://doi.org/10.1080/23312025.2 018.1480338.

Ezemonye LIN, Ikpesu TO. Evaluation of sublethal effects of endosulfan on cortisol secretion, glutathione s-transferase and acetycholinesterase activities in Clarias gariepinus. Food Chem Toxicol. 2010; 49:1898-1903. https://doi.org/10.1016/j.fct.2010.10.025. PMid:21056611.

Thangavel P, Sumathiral K, Maheswari S, Rita S, Ramaswamy M. Hormone profile of an edible, freshwater teleost, Sarotherodon mossambicus (Peters) under endosulfan toxicity. Pest Biochem Physiol. 2010; 97:229-234. https:// doi.org/10.1016/j.pestbp.2010.03.001.

Akhtar SM, Pal AK, Sahu NP, Alexander C, Gupta SK, Choudhar AK, Rajan MG. Stress mitigating and immunomodulatory effect of dietary pyridoxine in Labeo rohita (Hamilton) fingerlings. Aquac Res. 2010; 41:9911002. https://doi.org/10.1111/j.1365-2109.2009.02383.x.

Martí­nez-Porchas M, Martí­nez-Córdova LR, RamosEnriquez R. Cortisol and glucose: reliable indicators of fish stress. Pan-American J Aquat Sci. 2009; 4:158-178.

Campinho MA. Teleost metamorphosis: The role of thyroid hormone. Front Endocrinol. 2019; 10:383. https:// doi.org/10.3389/fendo.2019.00383. PMid:31258515 PMCid:PMC6587363.

Blanton ML, Specker JL. The Hypothalamic-PituitaryThyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol. 2007; 37:97-115. https:// doi.org/10.1080/10408440601123529. PMid:17364706.

Van der Geyten S, Mol KA, PluymersW, Kühn ER, Darras VM. Changes in plasma T3 during fasting/refeeding in tilapia (Oreochromis niloticus) are mainly regulated through changes in hepatic type II iodothyronine deiodinase. Fish Physiol Biochem.1998; 19:135-143. https://doi.org/10.1023/A:1007790527748.

Ruby SM, Idler DR, So YP. Plasma vitellogenin, 17βestradiol, T3 and T4 levels in sexually maturing rainbow trout, Oncorhynchus mykiss following sublethal HCN exposure. Aquat Toxicol. 1993; 26:91-101. https:// doi.org/10.1016/0166-445X(93)90007-N.

Abdolali M, Negin S, Parvin K. Effects of the environmental endocrine disrupting compound benzo[a] pyrene on thyroidal status of Abu mullet (Liza abu) during shortterm exposure. Toxicol Rep. 2018; 5:377-382. https:// doi.org/10.1016/j.toxrep.2018.02.018. PMid:29854607 PMCid:PMC5977374.

Cao C, Wang Q, Jiao F, Zhu G. Impact of co-exposure with butachlor and triadimefon on thyroid endocrine system in larval zebrafish. Experiment Toxicol Pathol. 2016; 68(8):463-469. https://doi.org/10.1016/j.etp.2016.07.004. PMid:27480594.

Yu L, Chen M, Liu Y, Gui W, Zhu G. Thyroid endocrine disruption in zebrafish larvae following exposure to hexaconazole and tebuconazole. Aquat Toxicol. 2013; 138139:35-42. https://doi.org/10.1016/j.aquatox.2013.04.001. PMid:23685399.

Teles M, Santos MA, Pacheco M. Physiological and genetic responses of European eel (Anguilla anguilla) to short-term chromium or copper exposure- influence of pre exposure to a PAH-like compound. Environ Toxicol. 2005; 20:92-99. https://doi.org/10.1002/tox.20082. PMid:15712285.

Li D, Xie P, Zhang XZ. Changes in plasma thyroid hormones and cortisol levels in crucian carp (Carassius auratus) exposed to the extracted microcystins. Chemosphere. 2008; 74: 13-18. https://doi.org/10.1016/j. chemosphere.2008.09.065. PMid:18990424.

Morgado I, Campinho MA, Costa R, Jacinto R, Power DM. Disruption of the thyroid system by diethylstilbestrol and ioxynil in the sea bream (Sparus aurata). Aquat Toxicol. 2009; 92:271-280. https://doi.org/10.1016/j.aquatox.2009.02.015. PMid:19375178.

Guo Y, Zhou B. Thyroid endocrine system disruption by pentachlorophenol: an in vitro and in vivo assay. Aquat Toxicol. 2013; 142-143:138-145. https://doi.org/10.1016/j.aquatox.2013.08.005. PMid:24001430.

McCormick SD, O'Dea MF, Moeckel AM, Lerner DT, Björnsson BT. Endocrine disruption of parr-smolt transformation and seawater tolerance of Atlantic salmon by 4-nonylphenol and 17βestradiol. Gen Comp Endocrinol. 2005; 142:280-288. https://doi.org/10.1016/j.ygcen.2005.01.015. PMid:15935154.

Zhang DH, Zhou EX, Yang ZL. Waterborne exposure to BPS causes thyroid endocrine disruption in zebrafish larvae. PLOS ONE. 2017; 12(5):e0176927. https://doi.org/10.1371/journal.pone.0176927. PMid:28467477 PMCid:PMC5415059.

Power DM, Llewellyn L, Faustino M, Nowell MA, Björnsson BT, Einarsdottir IE, Canario AV, Sweeney GE. Thyroid hormones in growth and development of fish. Comp Biochem Physiol C Toxicol Pharmacol. 2001; 130(4):447459. https://doi.org/10.1016/S1532-0456(01)00271-X.

Stephens SM, Brown JA, Frankling SC. Stress responses of larval turbot, Scophthalmus maximus L, exposed to sublethal concentrations of petroleum hydrocarbons. Fish Physiol Biochem. 1997; 17:433-439. https://doi.org/10.1023/A:1007799928020.

Waring CP, Moore A. The effect of atrazine on Atlantic salmon (Salmo salar) smolts in freshwater and after seawater transfer. Aquat Toxicol. 2004; 66:93-104. https:// doi.org/10.1016/j.aquatox.2003.09.001. PMid:14687982.

Heuer H, Visser Th. J. Pathophysiological importance of thyroid hormone transporters. Endocrinology. 2009; 150:1078-1083. https://doi.org/10.1210/en.2008-1518. PMid:19179441.

Hess RA. Estrogen in the adult male reproductive tract: A review. Reprod Biol Endocrinol. 2003; 1:52. https:// doi.org/10.1186/1477-7827-1-52. PMid:12904263 PMCid:PMC179885.

Chaves-Pozo E, Arjona FJ, Garcí­a-López A, Garcí­a-Alcázar A, Meseguer J, Garcí­a-Ayala A. Sex steroids and metabolic parameter levels in a seasonal breeding fish (Sparus aurata L). Gen Comp Endocrinol. 2008; 156:531-536. https://doi.org/10.1016/j.ygcen.2008.03.004. PMid:18407272.

Valero Y, Miriam Sánchez-Hernández M, Alicia Garcí­aAlcázar A, Alfonsa Garcí­a-Ayala A, Alberto Cuesta A, Elena Chaves-Pozo E. Characterization of the annual regulation of reproductive and immune parameters on the testis of European sea bass. Cell Tissue Res. 2015; 362:215-229. https://doi.org/10.1007/s00441-015-2172-1. PMid:25896883.

Aruna Devi C. Role of Bisphenol A as an endocrine disruptor in a freshwater fish, Anabas testudineus, PhD Thesis. University of Kerala, Thiruvananthapuram, India. 2013.

Naderi M, Zargham D, Asadi A, Bashti T, Kamayi K. Short-term responses of selected endocrine parameters in juvenile rainbow trout (Oncorhynchus mykiss) exposed to 4-nonylphenol. Toxicol Ind Health. 2015; 31:12181228. https://doi.org/10.1177/0748233713491806. PMid:23771873.

Spanò L, Tyler CR, Aerle RV, Devos P, Mandiki SNM, Silvestre F, Thomé JP, Kestemont P. Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat Toxicol. 2004; 66(4):369-379. https://doi.org/10.1016/j.aquatox.2003.10.009. PMid:15168945.

Mills LJ, Chichester C. Review of evidence: Are endocrinedisrupting chemicals in the aquatic environment impacting fish populations? Sci Total Environ. 2005; 343:1-34. https://doi.org/10.1016/j.scitotenv.2004.12.070. PMid:15862833.

Nakamura D, Yanagiba Y, Duan Z, Ito Y, Okamura A, Asaeda N. Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol. Toxicol Lett. 2010; 194:16-25. https://doi.org/10.1016/j.toxlet.2010.02.002. PMid:20144698.

Yang Q, Yang X, Liu J, Ren W, Chen Y, Shen S. Effects of BPF on steroid hormone homeostasis and gene expression in the hypothalamic-pituitary-gonadal axis of zebrafish. Environ Sci Pollut Res Int. 2017; 24:21311-21322. https:// doi.org/10.1007/s11356-017-9773-z. PMid:28741210.

Webb P, Nguyen P, Kushner PJ. Differential SERM effects on corepressor binding dictate ERα activity in vivo. J Biol Chem. 2003; 278:6912-6920. https://doi.org/10.1074/jbc.M208501200. PMid:12482846.

Hinck JE, Blazer VS, Denslow ND, Meyers MS, Gross TS, Tillitt DE. Biomarkers of contaminant exposure in Northern Pike (Esox lucius) from the Yukon River Basin, Alaska. Arch Environ Contam Toxicol. 2007; 52:549-562. https:// doi.org/10.1007/s00244-006-0134-z. PMid:17396212.

Dutta HM, Nath A, Adhikari S, Roy PK, Singh NK, Datta Munshi JS. Sublethal malathion induced changes in the ovary of an air-breathing catfish, Heteropneustes fossilis. A histological study. Hydrobiologia. 1994; 294:215-218.

https://doi.org/10.1007/BF00021294.

Dogan D, Can C. Endocrine disruption and altered biochemical indices in male Oncorhynchus mykiss in response to dimethoate. Pest Biochem Physiol. 2011; 99:157-161. https://doi.org/10.1016/j.pestbp.2010.11.012.

Folmar LC, Denslow ND, Rao V, Chow M, Crain DA, Enblom J, Marcino J, Guillete LJ. Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ Health Perspect. 1996; 104:1096-1101. https://doi.org/10.1289/ehp.961041096.

PMid:8930552 PMCid:PMC1469501.

Borg B. Androgens in teleost fishes. Comp Biochem Physiol. 1994; 109C:219-245. https://doi.org/10.1016/0742-8413(94)00063-G.

Bergh A. Paracrine regulation of Leydig cells by the seminiferous tubules. Int J Androl. 1983; 6:57-65. https://doi.org/10.1111/j.1365-2605.1983.tb00323.x. PMid:6840880.

Park CB, Aoki JY, Lee JS, Nagae M, Lee YD, Sakakura Y, Hagiwara A, Soyano K. The effects of 17β estradiol on various reproductive parameters in the hermaphrodite fish Kryptolebias marmoratus. Aquat Toxicol. 2010; 96(4):273-279. https://doi.org/10.1016/j.aquatox.2009.11.006. PMid:20006390.

Labadie P, Budzinski H. Alteration of steroid hormone profile in juvenile turbot (Psetta maxima) as a consequence of short-term exposure to 17α-ethynylestradiol. Chemosphere. 2006; 64:1274-1286. https://doi.org/10.1016/j.chemosphere.2005.12.065. PMid:16490234.

Sayed AEDH, Mahmoud UM, Mekkawy IA. Reproductive biomarkers to identify endocrine disruption in Clarias gariepinus exposed to 4-nonylphenol. Ecotoxicol Environ Saf. 2012; 78:310-319. https://doi.org/10.1016/j.ecoenv.2011.11.041. PMid:22177982.

Hunter GA, Donaldson EM. Hormonal sex control and its application to fish culture. In W.S. Hoar, D.J. Randall and E.M. Donaldson (eds). Fish Physiol. Vol. IX B, New York: Academic Press. 1983; 1:223-303. https://doi.org/10.1016/ S1546-5098(08)60305-2.

Baldigo BP, Sloan RJ, Smith SB, Denslow ND, Blazer VS, Gross TS. Polychlorinated biphenyls, mercury, and potential endocrine disruption in fish from the Hudson River, New York, USA. Aquat Sci. 2006; 68:206-228. https:// doi.org/10.1007/s00027-006-0831-8.

Folmar LC, Denslow ND, Kroll K, Orlando EF, Enblom J, Marcino J, Metcalfe C, Guillete LJ. Altered serum sex steroids and vitellogenin induction in walleye (Stizostedion citreum) collected near a metropolitan sewage treatment plant. Arch Environ Contam Toxicol. 2001; 40:392-398. https://doi.org/10.1007/s002440010188. PMid:11443371.

Connell D, Lam P, Richardson B, Wu R. Introduction to ecotoxicology. Oxford, UK: Blackwell Science; 1999.

Steinert SA. DNA damage as a bivalve biomarker. Biomarkers. 1999; 4:492-496. https://doi.org/10.1080/135475099230651. PMid:23902394.

Black MC, Ferell JR, Horning RC, Martin LK. DNA strand breakage in freshwater mussels (Anodonta grandis) exposed to lead in laboratory and field. Environ Toxicol Chem.1996; 15:802-808. https://doi.org/10.1002/etc.5620150528.

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2021-03-31

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Anjali, V. R., Remya, V. S., Reshmi, S., Shehna Mahim, S., & Aruna Devi, C. (2021). Impact of Bisphenol S as an Endocrine Disruptor in a Freshwater Fish, <i>Oreochromis mossambicus</i>. Journal of Endocrinology and Reproduction, 23(2), 49–63. https://doi.org/10.18311/jer/2019/27184

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