The role of bisphenol A and its analogues as endocrine disruptors influencing the thyroid gland: a short review

Justyna Milczarek-Banach; Piotr Miśkiewicz

doi:10.20883/medical.e441

Authors

Justyna Milczarek-Banach Department of Internal Medicine and Endocrinology, Medical University of Warsaw https://orcid.org/0000-0001-6548-6118
Piotr Miśkiewicz Department of Internal Medicine and Endocrinology, Medical University of Warsaw https://orcid.org/0000-0003-4015-6491

DOI:

https://doi.org/10.20883/medical.e441

Keywords:

bisphenol A, thyroid, hypothyroidism, endocrine disrupting chemical, plastic, autoimmunity

Abstract

Bisphenols (BPs) are common plastic additives widely used in industry, hence, human exposure to BPs is inevitable. The best known BP is bisphenol A (BPA), the production of which and its analogues has been increasing worldwide. This chemical is classified as an endocrine-disrupting chemical, inferring with hormonal homeostasis. Indeed, BPA is associated with the development of oestrogen-dependent neoplasms, infertility, metabolic disorders and neurobehavioral disturbances. However, there is a lack of evidence regarding the impact of BPA and its analogues on the thyroid, with most studies mainly performed on animals or in vitro. This review aims to summarise the knowledge regarding the relationship between BPA and its analogues on the thyroid gland.

Downloads

Download data is not yet available.

References

Braun JM, Hauser R. Bisphenol A and childrenʼs health. Current Opinion in Pediatrics. 2011 Apr;23(2):233-239. https://doi.org/10.1097/mop.0b013e3283445675

Carwile JL, Luu HT, Bassett LS, Driscoll DA, Yuan C, Chang JY, Ye X, Calafat AM, Michels KB. Polycarbonate Bottle Use and Urinary Bisphenol A Concentrations. Environmental Health Perspectives. 2009 Sep;117(9):1368-1372. https://doi.org/10.1289/ehp.0900604

Fenichel P, Chevalier N, Brucker-Davis F. Bisphenol A: An endocrine and metabolic disruptor. Annales d'Endocrinologie. 2013 Jul;74(3):211-220. https://doi.org/10.1016/j.ando.2013.04.002

Geens T, Goeyens L, Kannan K, Neels H, Covaci A. Levels of bisphenol-A in thermal paper receipts from Belgium and estimation of human exposure. Science of The Total Environment. 2012 Oct;435-436:30-33. https://doi.org/10.1016/j.scitotenv.2012.07.001

Hehn RS. NHANES Data Support Link between Handling of Thermal Paper Receipts and Increased Urinary Bisphenol A Excretion. Environmental Science & Technology. 2015 Dec 17;50(1):397-404. https://doi.org/10.1021/acs.est.5b04059

Rubin BS. Bisphenol A: An endocrine disruptor with widespread exposure and multiple effects. The Journal of Steroid Biochemistry and Molecular Biology. 2011 Oct;127(1-2):27-34. https://doi.org/10.1016/j.jsbmb.2011.05.002

Geens T, Aerts D, Berthot C, Bourguignon J, Goeyens L, Lecomte P, Maghuin-Rogister G, Pironnet A, Pussemier L, Scippo M, Van Loco J, Covaci A. A review of dietary and non-dietary exposure to bisphenol-A. Food and Chemical Toxicology. 2012 Oct;50(10):3725-3740. https://doi.org/10.1016/j.fct.2012.07.059

Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Urinary, Circulating, and Tissue Biomonitoring Studies Indicate Widespread Exposure to Bisphenol A. Environmental Health Perspectives. 2010 Aug;118(8):1055-1070. https://doi.org/10.1289/ehp.0901716

La Merrill MA, Vandenberg LN, Smith MT, Goodson W, Browne P, Patisaul HB, Guyton KZ, Kortenkamp A, Cogliano VJ, Woodruff TJ, Rieswijk L, Sone H, Korach KS, Gore AC, Zeise L, Zoeller RT. Consensus on the key characteristics of endocrine-disrupting chemicals as a basis for hazard identification. Nature Reviews Endocrinology. 2019 Nov 12;16(1):45-57. https://doi.org/10.1038/s41574-019-0273-8

Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM, Woodruff TJ, Vom Saal FS. Endocrine-Disrupting Chemicals and Public Health Protection: A Statement of Principles from The Endocrine Society. Endocrinology. 2012 Sep 1;153(9):4097-4110. https://doi.org/10.1210/en.2012-1422

Rutkowska A, Rachoń D, Milewicz A, Ruchała M, Bolanowski M, Jędrzejuk D, Bednarczuk T, Górska M, Hubalewska-Dydejczyk A, Kos-Kudła B, Lewiński A, Zgliczyński W. Polish Society of Endocrinology Position statement on endocrine disrupting chemicals (EDCs). Endokrynologia Polska. 2015;66(3):276-85. https://doi.org/10.5603/EP.2015.0035

Konduracka E, Krzemieniecki K, Gajos G. Relationship between everyday use cosmetics and female breast cancer. Polish Archives of Internal Medicine. 2014 Apr 2;124(5):264-269. https://doi.org/10.20452/pamw.2257

López-Carrillo L, Hernández-Ramírez RU, Calafat AM, Torres-Sánchez L, Galván-Portillo M, Needham LL, Ruiz-Ramos R, Cebrián ME. Exposure to Phthalates and Breast Cancer Risk in Northern Mexico. Environmental Health Perspectives. 2010 Apr;118(4):539-544. https://doi.org/10.1289/ehp.0901091

Rutkowska AZ, Szybiak A, Serkies K, Rachoń D. Endocrine disrupting chemicals as the potential risk factor for estrogen-dependent cancers. Polish Archives of Internal Medicine. 2016 Aug 9;. https://doi.org/10.20452/pamw.3481

Mantzouki C, Bliatka D, Iliadou PK, Margeli A, Papassotiriou I, Mastorakos G, Kousta E, Goulis DG. Serum Bisphenol A concentrations in men with idiopathic infertility. Food and Chemical Toxicology. 2019 Mar;125:562-565. https://doi.org/10.1016/j.fct.2019.02.016

Konieczna A, Rachoń D, Owczarek K, Kubica P, Kowalewska A, Kudłak B, Wasik A, Namieśnik J. Serum bisphenol A concentrations correlate with serum testosterone levels in women with polycystic ovary syndrome. Reproductive Toxicology. 2018 Dec;82:32-37. https://doi.org/10.1016/j.reprotox.2018.09.006

Wassenaar PNH, Trasande L, Legler J. Systematic Review and Meta-Analysis of Early-Life Exposure to Bisphenol A and Obesity-Related Outcomes in Rodents. Environmental Health Perspectives. 2017 Oct 3;125(10):106001. https://doi.org/10.1289/ehp1233

Perera F, Nolte EL, Wang Y, Margolis AE, Calafat AM, Wang S, Garcia W, Hoepner LA, Peterson BS, Rauh V, Herbstman J. Bisphenol A exposure and symptoms of anxiety and depression among inner city children at 10–12 years of age. Environmental Research. 2016 Nov;151:195-202. https://doi.org/10.1016/j.envres.2016.07.028

Kitamura S. Comparative Study of the Endocrine-Disrupting Activity of Bisphenol A and 19 Related Compounds. Toxicological Sciences. 2005 Jan 19;84(2):249-259. https://doi.org/10.1093/toxsci/kfi074

Chevrier J, Gunier RB, Bradman A, Holland NT, Calafat AM, Eskenazi B, Harley KG. Maternal Urinary Bisphenol A during Pregnancy and Maternal and Neonatal Thyroid Function in the CHAMACOS Study. Environmental Health Perspectives. 2013 Jan;121(1):138-144. https://doi.org/10.1289/ehp.1205092

Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, Kanamoto N, Hataya Y, Shimatsu A, Kuzuya H, Nakao K. Thyroid Hormone Action Is Disrupted by Bisphenol A as an Antagonist. The Journal of Clinical Endocrinology & Metabolism. 2002 Nov 1;87(11):5185-5190. https://doi.org/10.1210/jc.2002-020209

Lee S, Kim C, Youn H, Choi K. Thyroid hormone disrupting potentials of bisphenol A and its analogues - in vitro comparison study employing rat pituitary (GH3) and thyroid follicular (FRTL-5) cells. Toxicology in Vitro. 2017 Apr;40:297-304. https://doi.org/10.1016/j.tiv.2017.02.004

Lee J, Kim S, Choi K, Ji K. Effects of bisphenol analogs on thyroid endocrine system and possible interaction with 17β-estradiol using GH3 cells. Toxicology in Vitro. 2018 Dec;53:107-113. https://doi.org/10.1016/j.tiv.2018.08.005

Higashihara N, Shiraishi K, Miyata K, Oshima Y, Minobe Y, Yamasaki K. Subacute oral toxicity study of bisphenol F based on the draft protocol for the “Enhanced OECD Test Guideline no. 407”. Archives of Toxicology. 2007 Jul 13;81(12):825-832. https://doi.org/10.1007/s00204-007-0223-4

Zoeller RT, Bansal R, Parris C. Bisphenol-A, an Environmental Contaminant that Acts as a Thyroid Hormone Receptor Antagonist in Vitro, Increases Serum Thyroxine, and Alters RC3/Neurogranin Expression in the Developing Rat Brain. Endocrinology. 2005 Feb 1;146(2):607-612. https://doi.org/10.1210/en.2004-1018

Lee S, Kim C, Shin H, Kho Y, Choi K. Comparison of thyroid hormone disruption potentials by bisphenols A, S, F, and Z in embryo-larval zebrafish. Chemosphere. 2019 Apr;221:115-123. https://doi.org/10.1016/j.chemosphere.2019.01.019

Völkel W, Colnot T, Csanády GA, Filser JG, Dekant W. Metabolism and Kinetics of Bisphenol A in Humans at Low Doses Following Oral Administration. Chemical Research in Toxicology. 2002 Oct;15(10):1281-1287. https://doi.org/10.1021/tx025548t

Andrianou XD, Gängler S, Piciu A, Charisiadis P, Zira C, Aristidou K, Piciu D, Hauser R, Makris KC. Human Exposures to Bisphenol A, Bisphenol F and Chlorinated Bisphenol A Derivatives and Thyroid Function. Carvalho DPD. PLOS ONE. 2016 Oct 26;11(10):e0155237. https://doi.org/10.1371/journal.pone.0155237

Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL. Urinary Concentrations of Bisphenol A and 4-Nonylphenol in a Human Reference Population. Environmental Health Perspectives. 2005 Apr;113(4):391-395. https://doi.org/10.1289/ehp.7534

Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reproductive Toxicology. 2007 Aug;24(2):139-177. https://doi.org/10.1016/j.reprotox.2007.07.010

Schmutzler C, Bacinski A, Gotthardt I, Huhne K, Ambrugger P, Klammer H, Schlecht C, Hoang-Vu C, Grüters A, Wuttke W, Jarry H, Köhrle J. The Ultraviolet Filter Benzophenone 2 Interferes with the Thyroid Hormone Axis in Rats and Is a Potent in Vitro Inhibitor of Human Recombinant Thyroid Peroxidase. Endocrinology. 2007 Jun 1;148(6):2835-2844. https://doi.org/10.1210/en.2006-1280

Kudo Y. In Vitro and in Vivo Analysis of the Thyroid Disrupting Activities of Phenolic and Phenol Compounds in Xenopus laevis. Toxicological Sciences. 2005 Jan 5;84(1):29-37. https://doi.org/10.1093/toxsci/kfi049

Xu X, Liu Y, Sadamatsu M, Tsutsumi S, Akaike M, Ushijima H, Kato N. Perinatal bisphenol A affects the behavior and SRC-1 expression of male pups but does not influence on the thyroid hormone receptors and its responsive gene. Neuroscience Research. 2007 Jun;58(2):149-155. https://doi.org/10.1016/j.neures.2007.02.011

Nieminen P, Lindström-Seppä P, Juntunen M, Asikainen J, Mustonen A, Karonen S, Mussalo-Rauhamaa H, Kukkonen J. In vivo effects of bisphenol A on the polecat (mustela putorius). Journal of Toxicology and Environmental Health. Part A. 2002;65:933-45.

Aung MT, Johns LE, Ferguson KK, Mukherjee B, McElrath TF, Meeker JD. Thyroid hormone parameters during pregnancy in relation to urinary bisphenol A concentrations: A repeated measures study. Environment International. 2017 Jul;104:33-40. https://doi.org/10.1016/j.envint.2017.04.001

Romano ME, Webster GM, Vuong AM, Thomas Zoeller R, Chen A, Hoofnagle AN, Calafat AM, Karagas MR, Yolton K, Lanphear BP, Braun JM. Gestational urinary bisphenol A and maternal and newborn thyroid hormone concentrations: The HOME Study. Environmental Research. 2015 Apr;138:453-460. https://doi.org/10.1016/j.envres.2015.03.003

Meeker JD, Ferguson KK. Relationship between Urinary Phthalate and Bisphenol A Concentrations and Serum Thyroid Measures in U.S. Adults and Adolescents from the National Health and Nutrition Examination Survey (NHANES) 2007–2008. Environmental Health Perspectives. 2011 Oct;119(10):1396-1402. https://doi.org/10.1289/ehp.1103582

Geens T, Dirtu AC, Dirinck E, Malarvannan G, Van Gaal L, Jorens PG, Covaci A. Daily intake of bisphenol A and triclosan and their association with anthropometric data, thyroid hormones and weight loss in overweight and obese individuals. Environment International. 2015 Mar;76:98-105. https://doi.org/10.1016/j.envint.2014.12.003

Minatoya M, Sasaki S, Araki A, Miyashita C, Itoh S, Yamamoto J, Matsumura T, Mitsui T, Moriya K, Cho K, Morioka K, Minakami H, Shinohara N, Kishi R. Cord Blood Bisphenol A Levels and Reproductive and Thyroid Hormone Levels of Neonates. Epidemiology. 2017 Oct;28:S3-S9. https://doi.org/10.1097/ede.0000000000000716

Derwahl M, Nicula D. Estrogen and its role in thyroid cancer. Endocrine Related Cancer. 2014 Jul 22;21(5):T273-T283. https://doi.org/10.1530/erc-14-0053

Klinge. Estradiol-induced proliferation of papillary and follicular thyroid cancer cells is mediated by estrogen receptors α and β. International Journal of Oncology. 2010 Mar 24;36(5). https://doi.org/10.3892/ijo_00000588

Liu J, Chen G, Meng X, Liu Z, Dong S. Serum levels of sex hormones and expression of their receptors in thyroid tissue in female patients with various types of thyroid neoplasms. Pathology - Research and Practice. 2014 Dec;210(12):830-835. https://doi.org/10.1016/j.prp.2014.09.002

Zhou Z, Zhang J, Jiang F, Xie Y, Zhang X, Jiang L. Higher urinary bisphenol A concentration and excessive iodine intake are associated with nodular goiter and papillary thyroid carcinoma. Bioscience Reports. 2017 Jul 27;37(4). https://doi.org/10.1042/bsr20170678

Marotta V, Russo G, Gambardella C, Grasso M, La Sala D, Chiofalo MG, D'Anna R, Puzziello A, Docimo G, Masone S, Barbato F, Colao A, Faggiano A, Grumetto L. Human exposure to bisphenol AF and diethylhexylphthalate increases susceptibility to develop differentiated thyroid cancer in patients with thyroid nodules. Chemosphere. 2019 Mar;218:885-894. https://doi.org/10.1016/j.chemosphere.2018.11.084

Li L, Ying Y, Zhang C, Wang W, Li Y, Feng Y, Liang J, Song H, Wang Y. Bisphenol A exposure and risk of thyroid nodules in Chinese women: A case-control study. Environment International. 2019 May;126:321-328. https://doi.org/10.1016/j.envint.2019.02.026

Wang N, Zhou Y, Fu C, Wang H, Huang P, Wang B, Su M, Jiang F, Fang H, Zhao Q, Chen Y, Jiang Q. Influence of Bisphenol A on Thyroid Volume and Structure Independent of Iodine in School Children. Gao C. PLOS ONE. 2015 Oct 23;10(10):e0141248. https://doi.org/10.1371/journal.pone.0141248

Chailurkit L, Aekplakorn W, Ongphiphadhanakul B. The Association of Serum Bisphenol A with Thyroid Autoimmunity. International Journal of Environmental Research and Public Health. 2016 Nov 17;13(11):1153. https://doi.org/10.3390/ijerph13111153

Özaydın T, Öznurlu Y, Sur E, Çelik İ, Uluışık D. The effects of bisphenol A on some plasma cytokine levels and distribution of CD8+ and CD4+ T lymphocytes in spleen, ileal Peyer’s patch and bronchus associated lymphoid tissue in rats. Acta Histochemica. 2018 Nov;120(8):728-733. https://doi.org/10.1016/j.acthis.2018.08.002

Aljadeff G, Longhi E, Shoenfeld Y. Bisphenol A: A notorious player in the mosaic of autoimmunity. Autoimmunity. 2018 Nov 17;51(8):370-377. https://doi.org/10.1080/08916934.2018.1551374

Kharrazian D. The Potential Roles of Bisphenol A (BPA) Pathogenesis in Autoimmunity. Autoimmune Diseases. 2014;2014:1-12. https://doi.org/10.1155/2014/743616

Jensen CD, Andersen KE. Two cases of occupational allergic contact dermatitis from a cycloaliphatic epoxy resin in a neat oil: Case Report. Environmental Health. 2003 Mar 26;2(1). https://doi.org/10.1186/1476-069x-2-3

Hannu T, Frilander H, Kauppi P, Kuuliala O, Alanko K. IgE-Mediated Occupational Asthma from Epoxy Resin. International Archives of Allergy and Immunology. 2009;148(1):41-44. https://doi.org/10.1159/000151504