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Research advances in identification procedures of endocrine disrupting chemicals

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Abstract

Endocrine disrupting chemicals (EDCs) are increasingly concerned substance endangering human health and environment. However, there is no unified standard for identifying chemicals as EDCs, which is also controversial internationally. In this review, the procedures for EDC identification in different organizations/countries were described. Importantly, three aspects to be considered in identifying chemical substances as EDCs were summarized, which were mechanistic data, animal experiments, and epidemiological information. The relationships between them were also discussed. To elaborate more clearly on these three aspects of evidence, scientific data on some chemicals including bisphenol A, 1,2-dibromo-4-(1,2 dibromoethyl) cyclohexane and perchlorate were collected and evaluated. Altogether, the above three chemicals were assessed for interfering with hormones and elaborated their health hazards from macroscopic to microscopic. This review is helpful for standardizing the identification procedure of EDCs.

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References

  • Abass K et al (2016) New approaches in human health risk assessment. Int J Circumpolar Health 75:33845

    Google Scholar 

  • Abdel-Maksoud FM et al (2019) Prenatal exposures to bisphenol A and di (2-ethylhexyl) phthalate disrupted seminiferous tubular development in growing male rats. Reprod Toxicol 88:85–90

    CAS  Google Scholar 

  • Adami HO et al (2011) Toxicology and epidemiology: improving the science with a framework for combining toxicological and epidemiological evidence to establish causal inference. Toxicol Sci 122:223–234

    CAS  Google Scholar 

  • Ahmed RA et al (2014) Effect of prenatal exposure to bisphenol a on the vagina of albino rats: immunohistochemical and ultrastructural study. Folia Morphol (warsz) 73:399–408

    CAS  Google Scholar 

  • Ahsan N et al (2018) Comparative effects of Bisphenol S and Bisphenol A on the development of female reproductive system in rats; a neonatal exposure study. Chemosphere 197:336–343

    CAS  Google Scholar 

  • Åke Bergman JJH, Jobling S, Kidd KA Thomas Zoeller R (2012) State of the science of endocrine disrupting chemicals 2012. United Nations Environment Programme and World Health Organization

  • Akingbemi BT et al (2004) Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 145:592–603

    CAS  Google Scholar 

  • An BS et al (2013) Effects of estrogen and estrogenic compounds, 4-tert-octylphenol, and bisphenol A on the uterine contraction and contraction-associated proteins in rats. Mol Cell Endocrinol 375:27–34

    CAS  Google Scholar 

  • Andersen HR et al (1999) Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals. Environ Health Perspect 107(Suppl 1):89–108

    CAS  Google Scholar 

  • Andersson NAM, Barmaz AD, Grignard S, Kienzler E, Lepper A, Lostia P, Munn AM, Parra Morte S, Pellizzato JM, Tarazona F, Terron J, Van der Linden AS (2018) Guidance for the identification of endocrine disruptors in the context of Regulations (EU) No 528/2012 and (EC) No 1107/2009. Efsa J 16:e05311

    Google Scholar 

  • Gentles A et al (2005) Evaluation of adult quail and egg production following exposure to perchlorate-treated water. Environ Toxicol Chem 24:1930–1934

    CAS  Google Scholar 

  • Ankley GT et al (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29:730–741

    CAS  Google Scholar 

  • Ankley G, Francis E, Gray E, Kavlock R, McMaster S, Reese D, Sayles G, Sergeant A, Vallero D (1998) Research plan for endocrine disruptors. Office of Research and Development US Environmental Protection Agency Research Plan for Endocrine Disruptors

  • ANSES (2021) ANSES's work and involvement in the area of endocrine disruptors. https://www.anses.fr/en/content/ansess-work-and-involvement-area-endocrine-disruptors#regulatory. Accessed 27 May 2021

  • Asnake S et al (2014) 1,2-Dibromo-4-(1,2 dibromoethyl) cyclohexane (TBECH)-mediated steroid hormone receptor activation and gene regulation in chicken LMH cells. Environ Toxicol Chem 33:891–899

    CAS  Google Scholar 

  • Autrup H et al (2015) Principles of pharmacology and toxicology also govern effects of chemicals on the endocrine system. Toxicol Sci 146:11–15

    CAS  Google Scholar 

  • Azzouz A, Ballesteros E (2012) Combined microwave-assisted extraction and continuous solid-phase extraction prior to gas chromatography-mass spectrometry determination of pharmaceuticals, personal care products and hormones in soils, sediments and sludge. Sci Total Environ 419:208–215

    CAS  Google Scholar 

  • Behnia F et al (2016) High bisphenol A (BPA) concentration in the maternal, but not fetal, compartment increases the risk of spontaneous preterm delivery. J Matern Fetal Neonatal Med 29:3583–3589

    CAS  Google Scholar 

  • Bereketoglu C et al (2021) The brominated flame retardants TBECH and DPTE alter prostate growth, histology and gene expression patterns in the mouse. Reprod Toxicol 102:43–55

    CAS  Google Scholar 

  • Berg C et al (2001) Effects of bisphenol A and tetrabromobisphenol A on sex organ development in quail and chicken embryos. Environ Toxicol Chem 20:2836–2840

    CAS  Google Scholar 

  • Bergman Å et al (2013) Science and policy on endocrine disrupters must not be mixed: a reply to a “common sense” intervention by toxicology journal editors. Environ Health 12:69

    Google Scholar 

  • Bernanke J, Köhler HR (2009) The impact of environmental chemicals on wildlife vertebrates. Rev Environ Contam Toxicol 198:1–47

    CAS  Google Scholar 

  • Bhan A et al (2014) Bisphenol-A and diethylstilbestrol exposure induces the expression of breast cancer associated long noncoding RNA HOTAIR in vitro and in vivo. J Steroid Biochem Mol Biol 141:160–170

    CAS  Google Scholar 

  • Boberg J et al (2020) Using assessment criteria for pesticides to evaluate the endocrine disrupting potential of non-pesticide chemicals: case butylparaben. Environ Int 144:105996

    CAS  Google Scholar 

  • Bosquiazzo VL et al (2010) Effects of neonatal exposure to bisphenol A on steroid regulation of vascular endothelial growth factor expression and endothelial cell proliferation in the adult rat uterus. Biol Reprod 82:86–95

    CAS  Google Scholar 

  • Bouskine A et al (2009) Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor. Environ Health Perspect 117:1053–1058

    CAS  Google Scholar 

  • Bradford CM et al (2005) Perchlorate affects thyroid function in eastern mosquitofish (Gambusia holbrooki) at environmentally relevant concentrations. Environ Sci Technol 39:5190–5195

    CAS  Google Scholar 

  • Brown FR et al (2014) Levels of non-polybrominated diphenyl ether brominated flame retardants in residential house dust samples and fire station dust samples in California. Environ Res 135:9–14

    CAS  Google Scholar 

  • Browne P et al (2017) Application of adverse outcome pathways to U.S. EPA’s endocrine disruptor screening program. Environ Health Perspect. 125:096001

    Google Scholar 

  • Browne P et al (2020) OECD approaches and considerations for regulatory evaluation of endocrine disruptors. Mol Cell Endocrinol 504:110675

    CAS  Google Scholar 

  • Cantonwine D et al (2010) Bisphenol a exposure in Mexico City and risk of prematurity: a pilot nested case control study. Environ Health 9:62

    Google Scholar 

  • Casas M, Gascon M (2020) Prenatal exposure to endocrine-disrupting chemicals and asthma and allergic diseases. J Investig Allergol Clin Immunol 30:215–228

    CAS  Google Scholar 

  • Chen H et al (2019) A review of toxicity induced by persistent organic pollutants (POPs) and endocrine-disrupting chemicals (EDCs) in the nematode Caenorhabditis elegans. J Environ Manage 237:519–525

    CAS  Google Scholar 

  • Chen L et al (2016) A review of reproductive toxicity of microcystins. J Hazard Mater 301:381–399

    CAS  Google Scholar 

  • Chen L et al (2021) Effects of acute exposure to microcystins on hypothalamic-pituitary-adrenal (HPA), -gonad (HPG) and -thyroid (HPT) axes of female rats. Sci Total Environ 778:145196

    CAS  Google Scholar 

  • Chen Q et al (2018) Activation of steroid hormone receptors: shed light on the in silico evaluation of endocrine disrupting chemicals. Sci Total Environ 631–632:27–39

    Google Scholar 

  • China, The Ministry of Agriculture of the People's Republic of China (2015) Evaluation method of pesticide endocrine disrupting effects (NY/T 2873-2015)

  • Clayton EM et al (2011) The impact of bisphenol A and triclosan on immune parameters in the U.S. population, NHANES 2003–2006. Environ Health Perspect 119:390–396

    CAS  Google Scholar 

  • Crane HM et al (2005) Effects of ammonium perchlorate on thyroid function in developing fathead minnows. Pimephales Promelas Environ Health Perspect 113:396–401

    CAS  Google Scholar 

  • Crump D et al (2014) 1,2-Dibromo-4-(1,2-dibromoethyl)-cyclohexane and tris(methylphenyl) phosphate cause significant effects on development, mRNA expression, and circulating bile acid concentrations in chicken embryos. Toxicol Appl Pharmacol 277:279–287

    CAS  Google Scholar 

  • Curran IH et al (2017) Toxicologic effects of 28-day dietary exposure to the flame retardant 1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane (TBECH) in F344 rats. Toxicology 377:1–13

    CAS  Google Scholar 

  • Currier HA et al (2013) An assessment of in ovo toxicity of the flame retardant 1,2-dibromo-4-(1,2-dibromoethyl) cyclohexane (TBECH) in the zebra finch. Bull Environ Contam Toxicol 91:455–459

    CAS  Google Scholar 

  • Dang Z et al (2012) Evaluation of the Daphnia magna reproduction test for detecting endocrine disruptors. Chemosphere 88:514–523

    CAS  Google Scholar 

  • Diamanti-Kandarakis E et al (2009) Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr Rev 30:293–342

    CAS  Google Scholar 

  • Dietrich DR et al (2013) Scientifically unfounded precaution drives European Commission’s recommendations on EDC regulation, while defying common sense, well-established science and risk assessment principles. Toxicol in Vitro 27:2110–2114

    Google Scholar 

  • Dohán O et al (2007) The Na+/I symporter (NIS) mediates electroneutral active transport of the environmental pollutant perchlorate. Proc Natl Acad Sci U S A 104:20250–20255

    Google Scholar 

  • EC (1998) What are endocrine disruptors? European Commission, https://ec.europa.eu/environment/chemicals/endocrine/definitions/endodis_en.htm. Accessed 21 Jul 2022

  • ECHA (2011) Candidate List of substances of very high concern for Authorisation. https://echa.europa.eu/regulations/reach/understanding-reach. Accessed 9 Jan 2021

  • ECHA/EFSA (2018) Guidance for the identification of endocrine disruptors in the context of regulations (EU) No 528/2012 and (EC) No 1107/2009, 16(6):5311

  • EPA (2014) Framework for human health risk assessment to inform decision making. https://www.epa.gov/risk/framework-human-health-risk-assessment-inform-decision-making. Accessed 21 Jul 2022

  • Fabian E et al (2019) In vitro-to-in vivo extrapolation (IVIVE) by PBTK modeling for animal-free risk assessment approaches of potential endocrine-disrupting compounds. Arch Toxicol 93:401–416

    CAS  Google Scholar 

  • Ferguson KK et al (2014) Prenatal and peripubertal phthalates and bisphenol A in relation to sex hormones and puberty in boys. Reprod Toxicol 47:70–76

    CAS  Google Scholar 

  • Forner-Piquer I et al (2020) Effects of BPA on zebrafish gonads: focus on the endocannabinoid system. Environ Pollut 264:114710

    CAS  Google Scholar 

  • Foster PMD (2005) Mode of action: Impaired fetal leydig cell function - effects on male reproductive development produced by certain phthalate esters. Crit Rev Toxicol 35:713–719

    CAS  Google Scholar 

  • Gallo MV et al (2016) Endocrine disrupting chemicals and ovulation: is there a relationship? Environ Res 151:410–418

    CAS  Google Scholar 

  • Gámez JM et al (2015) Exposure to a low dose of bisphenol A impairs pituitary-ovarian axis in prepubertal rats: effects on early folliculogenesis. Environ Toxicol Pharmacol 39:9–15

    Google Scholar 

  • Gardell AM et al (2017) Exogenous iodide ameliorates perchlorate-induced thyroid phenotypes in threespine stickleback. Gen Comp Endocrinol 243:60–69

    CAS  Google Scholar 

  • Gauthier LT et al (2009) Temporal trends and spatial distribution of non-polybrominated diphenyl ether flame retardants in the eggs of colonial populations of Great Lakes herring gulls. Environ Sci Technol 43:312–317

    CAS  Google Scholar 

  • Gemmill B et al (2011) Toxicokinetics of tetrabromoethylcyclohexane (TBECH) in juvenile brown trout (Salmo trutta) and effects on plasma sex hormones. Aquat Toxicol 101:309–317

    CAS  Google Scholar 

  • Gentes ML et al (2012) Novel flame retardants in urban-feeding ring-billed gulls from the St. Lawrence River. Canada Environ Sci Technol 46:9735–9744

    CAS  Google Scholar 

  • Gilbert ME, Sui L (2008) Developmental exposure to perchlorate alters synaptic transmission in hippocampus of the adult rat. Environ Health Perspect 116:752–760

    CAS  Google Scholar 

  • Giommi C, Habibi HR, Candelma M, Carnevali O, Maradonna F (2021) Probiotic administration mitigates bisphenol A reproductive toxicity in zebrafish. Int J Mol Sci 22(17). https://doi.org/10.3390/ijms22179314

  • Golden R et al (2005) A review of the endocrine activity of parabens and implications for potential risks to human health. Crit Rev Toxicol 35:435–458

    CAS  Google Scholar 

  • Guillette LJ Jr, Gunderson MP (2001) Alterations in development of reproductive and endocrine systems of wildlife populations exposed to endocrine-disrupting contaminants. Reproduction 122:857–864

    CAS  Google Scholar 

  • Hatef A et al (2012) Adverse effects of bisphenol A on reproductive physiology in male goldfish at environmentally relevant concentrations. Ecotoxicol Environ Saf 76:56–62

    CAS  Google Scholar 

  • Hauser R et al (2015) Male reproductive disorders, diseases, and costs of exposure to endocrine-disrupting chemicals in the European Union. J Clin Endocrinol Metab 100:1267–1277

    CAS  Google Scholar 

  • Health, Japan Ministry of Health (2015) The Endocrine Disruptor Page. Japan Ministry of Health, http://www.nihs.go.jp/edc/english/actions/index.htm. Accessed 1 Apr 2022

  • Ho V et al (2022) Endocrine disruptors: challenges and future directions in epidemiologic research. Environ Res 204:111969

    CAS  Google Scholar 

  • Hu JMY et al (2021) Prenatal exposure to endocrine disrupting chemical mixtures and infant birth weight: a Bayesian analysis using kernel machine regression. Environ Res 195:110749

    CAS  Google Scholar 

  • IPCS (2002) Global Assessment of the State-of-the-Science of Endocrine Disruptors. . In: B. S. WHO/PCS/EDC/02.2. Eds. Damstra T, Bergman A, Kavlock R, and Van Der Kraak G. Geneva, Switzerland: World Health Organization. , (Ed.). IPCS (International Programme on Chemical Safety). http://www.who.int/ipcs/publications/new_issues/endocrine_disruptors/en/. Accessed 25 Mar 2022

  • Isanhart JP et al (2005) Effects of perchlorate exposure on resting metabolism, peak metabolism, and thyroid function in the prairie vole (Microtus ochrogaster). Environ Toxicol Chem 24:678–684

    CAS  Google Scholar 

  • Jaladanki CK et al (2021) Virtual screening of potentially endocrine-disrupting chemicals against nuclear receptors and its application to identify PPARγ-bound fatty acids. Arch Toxicol 95:355–374

    CAS  Google Scholar 

  • Jeong J, Kim H, Choi J (2019) In silico molecular docking and in vivo validation with Caenorhabditis elegans to discover molecular initiating events in adverse Outcome pathway framework: Case study on endocrine-disrupting chemicals with estrogen and androgen receptors. Int J Mol Sci 20(5). https://doi.org/10.3390/ijms20051209

  • Julien E et al (2009) The key events dose-response framework: a cross-disciplinary mode-of-action based approach to examining dose-response and thresholds. Crit Rev Food Sci Nutr 49:682–689

    CAS  Google Scholar 

  • Kahn LG et al (2020) Endocrine-disrupting chemicals: implications for human health. Lancet Diabetes Endocrinol 8:703–718

    CAS  Google Scholar 

  • Kang Y et al (2014) Daphnia magna may serve as a powerful tool in screening endocrine disruption chemicals (EDCs). Environ Sci Technol 48:881–882

    CAS  Google Scholar 

  • Kassotis CD et al (2020) Endocrine-disrupting chemicals: economic, regulatory, and policy implications. Lancet Diabetes Endocrinol 8:719–730

    CAS  Google Scholar 

  • Khalaf H et al (2009) Diastereomers of the brominated flame retardant 1,2-dibromo-4-(1,2 dibromoethyl)cyclohexane induce androgen receptor activation in the hepg2 hepatocellular carcinoma cell line and the lncap prostate cancer cell line. Environ Health Perspect 117:1853–1859

    CAS  Google Scholar 

  • Kharlyngdoh JB et al (2016) TBECH, 1,2-dibromo-4-(1,2 dibromoethyl) cyclohexane, alters androgen receptor regulation in response to mutations associated with prostate cancer. Toxicol Appl Pharmacol 307:91–101

    CAS  Google Scholar 

  • Kharlyngdoh JB et al (2018) Androgen receptor modulation following combination exposure to brominated flame-retardants. Sci Rep 8:4843

    Google Scholar 

  • Klebe G (2006) Virtual ligand screening: strategies, perspectives and limitations. Drug Discov Today 11:580–594

    CAS  Google Scholar 

  • Klimisch HJ et al (1997) A systematic approach for evaluating the quality of experimental toxicological and ecotoxicological data. Regul Toxicol Pharmacol 25:1–5

    CAS  Google Scholar 

  • Korach KS (1993) Editorial: surprising places of estrogenic activity. Endocrinology 132:2277–2278

    CAS  Google Scholar 

  • Kuang Y et al (2014) Interference of the endocrine disrupting chemicals on androgen receptor function. Journal of Chongqing Normal University. Nat Sci Edition 31:16–22

    CAS  Google Scholar 

  • La Merrill MA et al (2020) Consensus on the key characteristics of endocrine-disrupting chemicals as a basis for hazard identification. Nat Rev Endocrinol 16:45–57

    Google Scholar 

  • Lahnsteiner F et al (2005) Effect of bisphenol A on maturation and quality of semen and eggs in the brown trout. Salmo Trutta F Fario Aquat Toxicol 75:213–224

    CAS  Google Scholar 

  • Larsson A et al (2006) Identification of the brominated flame retardant 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane as an androgen agonist. J Med Chem 49:7366–7372

    CAS  Google Scholar 

  • Lee DH, Jacobs DR Jr (2015) Methodological issues in human studies of endocrine disrupting chemicals. Rev Endocr Metab Disord 16:289–297

    CAS  Google Scholar 

  • Lee HA et al (2013) Effect of urinary bisphenolA on androgenic hormones and insulin resistance in preadolescent girls: a pilot study from the Ewha Birth & Growth Cohort. Int J Environ Res Public Health 10:5737–5749

    CAS  Google Scholar 

  • Legler J et al (2015) Obesity, diabetes, and associated costs of exposure to endocrine-disrupting chemicals in the European Union. J Clin Endocrinol Metab 100:1278–1288

    CAS  Google Scholar 

  • Li Y et al (2012a) Differential estrogenic actions of endocrine-disrupting chemicals Bisphenol A, Bisphenol AF, and zearalenone through estrogen receptor α and β in Vitro. Environ Health Perspect 120:1029–1035

    CAS  Google Scholar 

  • Lisco G, De Tullio A, Giagulli VA, De Pergola G, Triggiani V (2020) Interference on iodine uptake and human thyroid function by perchlorate-contaminated water and food. Nutrients 12(6). https://doi.org/10.3390/nu12061669

  • Liu PY et al (2017) Tetrabromoethylcyclohexane affects gonadal differentiation and development in the frog Pelophylax nigromaculatus. Aquat Toxicol 192:40–47

    CAS  Google Scholar 

  • Liu R et al (2022) Effects of bisphenol A on reproductive toxicity and gut microbiota dysbiosis in male rats. Ecotoxicol Environ Saf 239:113623

    CAS  Google Scholar 

  • Liu X et al (2021a) Chronic exposure of BPA impairs male germ cell proliferation and induces lower sperm quality in male mice. Chemosphere 262:127880

    CAS  Google Scholar 

  • Liu Y et al (2021b) Brominated flame retardants (BFRs) in marine food webs from Bohai Sea. China Sci Total Environ 772:145036

    CAS  Google Scholar 

  • Liu Y et al (2021c) Bioaccumulation and reproductive toxicity of bisphenol A in male-pregnant seahorse (Hippocampus erectus) at environmentally relevant concentrations. Sci Total Environ 753:141805

    CAS  Google Scholar 

  • Luccio-Camelo DC, Prins GS (2011) Disruption of androgen receptor signaling in males by environmental chemicals. J Steroid Biochem Mol Biol 127:74–82

    CAS  Google Scholar 

  • Ma Y et al (2019) The adverse health effects of bisphenol A and related toxicity mechanisms. Environ Res 176:108575

    CAS  Google Scholar 

  • Mahalingam S et al (2017) The effects of in utero bisphenol A exposure on ovarian follicle numbers and steroidogenesis in the F1 and F2 generations of mice. Reprod Toxicol 74:150–157

    CAS  Google Scholar 

  • Markey CM et al (2001) In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 65:1215–1223

    CAS  Google Scholar 

  • Marteinson SC et al (2020) A review of 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane in the environment and assessment of its persistence, bioaccumulation and toxicity. Environ Res 195:110497

    Google Scholar 

  • Marteinson SC, Fernie KJ (2019) Is the current-use flame retardant, DBE-DBCH, a potential obesogen? Effects on body mass, fat content and associated behaviors in American kestrels. Ecotoxicol Environ Saf 169:770–777

    CAS  Google Scholar 

  • Marteinson SC et al (2015) Exposure to the androgenic brominated flame retardant 1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane alters reproductive and aggressive behaviors in birds. Environ Toxicol Chem 34:2395–2402

    CAS  Google Scholar 

  • Marteinson SC et al (2012) The flame retardant β-1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane: fate, fertility, and reproductive success in American kestrels (Falco sparverius). Environ Sci Technol 46:8440–8447

    CAS  Google Scholar 

  • Marteinson SC et al (2017) Disruption of thyroxine and sex hormones by 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (DBE-DBCH) in American kestrels (Falco sparverius) and associations with reproductive and behavioral changes. Environ Res 154:389–397

    CAS  Google Scholar 

  • McNabb FM et al (2004a) Does thyroid function in developing birds adapt to sustained ammonium perchlorate exposure? Toxicol Sci 82:106–113

    CAS  Google Scholar 

  • McNabb FM et al (2004b) Ammonium perchlorate effects on thyroid function and growth in bobwhite quail chicks. Environ Toxicol Chem 23:997–1003

    CAS  Google Scholar 

  • Meng Z et al (2019) Effects of perinatal exposure to BPA, BPF and BPAF on liver function in male mouse offspring involving in oxidative damage and metabolic disorder. Environ Pollut 247:935–943

    CAS  Google Scholar 

  • Miao Y et al (2023) Within-day variability, predictors, and risk assessments of exposure to parabens among Chinese adult men. Environ Res 218:115026

    CAS  Google Scholar 

  • Mínguez-Alarcón L et al (2015) Urinary bisphenol A concentrations and association with in vitro fertilization outcomes among women from a fertility clinic. Hum Reprod 30:2120–2128

    Google Scholar 

  • Molina A et al (2018) Hypothalamic-pituitary-ovarian axis perturbation in the basis of bisphenol A (BPA) reproductive toxicity in female zebrafish (Danio rerio). Ecotoxicol Environ Saf 156:116–124

    CAS  Google Scholar 

  • Molina AM et al (2021) Proteomic profile of the effects of low-dose bisphenol A on zebrafish ovaries. Food Chem Toxicol 156:112435

    CAS  Google Scholar 

  • Moral R et al (2008) Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J Endocrinol 196:101–112

    CAS  Google Scholar 

  • Mukhi S, Patiño R (2007) Effects of prolonged exposure to perchlorate on thyroid and reproductive function in zebrafish. Toxicol Sci 96:246–254

    CAS  Google Scholar 

  • Muñoz JP et al (2021) Glyphosate and the key characteristics of an endocrine disruptor: a review. Chemosphere 270:128619

    Google Scholar 

  • Mustieles V et al (2018) Bisphenol A and reproductive hormones and cortisol in peripubertal boys: The INMA-Granada cohort. Sci Total Environ 618:1046–1053

    CAS  Google Scholar 

  • Newbold RR et al (2007) Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol 24:253–258

    CAS  Google Scholar 

  • Nguyen KH et al (2017) Biotransformation of the flame retardant 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (TBECH) in Vitro by Human Liver Microsomes. Environ Sci Technol 51:10511–10518

    CAS  Google Scholar 

  • Niklas Andersson MA, Auteri D, Barmaz S, Grignard E, Kienzler A, Lepper P, Lostia AM, Munn S, Morte JMP, Pellizzato F, Tarazona J, Terron A, Van der Linden S (2018) Guidance for the identification of endocrine disruptors in the context of Regulations (EU) No 528/2012 and (EC) No 1107/2009. European Food Safety Authority. https://doi.org/10.2903/j.efsa.2018.5311

  • Nowak K et al (2018) Parabens and their effects on the endocrine system. Mol Cell Endocrinol 474:238–251

    CAS  Google Scholar 

  • OECD (2018a) Revised guidance document 150 on standardised test guidelines for evaluating chemicals for endocrine disruption. OECD Series on Testing and Assessment. OECD Publishing. https://doi.org/10.1787/9789264304741-en. Paris

  • OECD (2018b) Revised guidance document 150 on standardised test guidelines for evaluating chemicals for endocrine disruption. OECD Series on Testing and Assessment. https://doi.org/10.1787/9789264304741-en

  • OEHHA (2011) Green chemistry hazard traits, section 69403.4 endocrine toxicity, California Code of Regulations, Division 4.5, Title 22, Chapter 54. https://oehha.ca.gov/media/downloads/risk-assessment/gcisor121710.pdf. Accessed 1 Apr 2022

  • Palioura E, Diamanti-Kandarakis E (2015) Polycystic ovary syndrome (PCOS) and endocrine disrupting chemicals (EDCs). Rev Endocr Metab Disord 16:365–371

    CAS  Google Scholar 

  • Park BJ et al (2011) Thyroid axis disruption in juvenile brown trout (Salmo trutta) exposed to the flame retardant β-tetrabromoethylcyclohexane (β-TBECH) via the diet. Environ Sci Technol 45:7923–7927

    CAS  Google Scholar 

  • Patiño R et al (2003) Effects of ammonium perchlorate on the reproductive performance and thyroid follicle histology of zebrafish. Environ Toxicol Chem 22:1115–1121

    Google Scholar 

  • Patisaul HB et al (2018) Animal models of endocrine disruption. Best Pract Res Clin Endocrinol Metab 32:283–297

    CAS  Google Scholar 

  • Porta M (2016) A Dictionary of Epidemiology, 6th edn. Oxford University Press, Oxford, UK

    Google Scholar 

  • Porter E et al (2014) Use of an avian hepatocyte assay and the avian Toxchip Polymerse chain reaction array for testing prioritization of 16 organic flame retardants. Environ Toxicol Chem 33:573–582

    CAS  Google Scholar 

  • Pradhan A et al (2013) The brominated flame retardant TBECH activates the zebrafish (Danio rerio) androgen receptor, alters gene transcription and causes developmental disturbances. Aquat Toxicol 142–143:63–72

    Google Scholar 

  • Raghavan R et al (2018) Pharmacologic and environmental endocrine disruptors in the pathogenesis of hypospadias: a review. Curr Environ Health Rep 5:499–511

    CAS  Google Scholar 

  • Ramírez V et al (2022) Role of endocrine disrupting chemicals in children’s neurodevelopment. Environ Res 203:111890

    Google Scholar 

  • Rebuli ME et al (2014) Investigation of the effects of subchronic low dose oral exposure to bisphenol A (BPA) and ethinyl estradiol (EE) on estrogen receptor expression in the juvenile and adult female rat hypothalamus. Toxicol Sci 140:190–203

    CAS  Google Scholar 

  • Ruan Y et al (2018a) Temporal changes and stereoisomeric compositions of 1,2,5,6,9,10-hexabromocyclododecane and 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane in marine mammals from the South China Sea. Environ Sci Technol 52:2517–2526

    CAS  Google Scholar 

  • Ruan Y et al (2019) Stereoisomer-specific occurrence, distribution, and fate of chiral brominated flame retardants in different wastewater treatment systems in Hong Kong. J Hazard Mater 374:211–218

    CAS  Google Scholar 

  • Ruan Y et al (2018b) Stereoisomer-specific trophodynamics of the chiral brominated flame retardants HBCD and TBECH in a marine food web, with implications for human exposure. Environ Sci Technol 52:8183–8193

    CAS  Google Scholar 

  • Rudén C (2006) What influences a health risk assessment? Toxicol Lett 167:201–204

    Google Scholar 

  • Russell WMS, Burch RL, Hume CW (1959) The principles of humane experimental technique. Methuen, London, Vol. 238, Chapter: 5 replacement

  • Rybacka A et al (2015) Identifying potential endocrine disruptors among industrial chemicals and their metabolites–development and evaluation of in silico tools. Chemosphere 139:372–378

    CAS  Google Scholar 

  • Safety, International Programme on Chemical Safety (2002) Global assessment of the state of the science of endocrine disruptors, an assessment prepared by an expert group on behalf of the World Health Organization, the International Labour Organization, and the United Nations Environment Programme. WHO/PCS/EDC/02.2

  • Sahlström LM et al (2014) Brominated flame retardants in matched serum samples from Swedish first-time mothers and their toddlers. Environ Sci Technol 48:7584–7592

    Google Scholar 

  • Salgueiro-González N et al (2015) Analysis and occurrence of endocrine-disrupting chemicals in airborne particles. TrAC - Trends Anal Chem 66:45–52

    Google Scholar 

  • Sarink D et al (2021) BPA, parabens, and phthalates in relation to endometrial cancer risk: a case-control study nested in the multiethnic cohort. Environ Health Perspect 129:57702

    CAS  Google Scholar 

  • SCHEER-Scientific Committee on Health, Environmental and Emerging Risks (SCHEER) (2018) Memorandum on weight of evidence and uncertainties

  • Schmidt F et al (2012) Effects of the anti-thyroidal compound potassium-perchlorate on the thyroid system of the zebrafish. Aquat Toxicol 109:47–58

    CAS  Google Scholar 

  • Schneider M et al (2019) In silico predictions of endocrine disruptors properties. Endocrinology 160:2709–2716

    CAS  Google Scholar 

  • Seed J et al (2005) Overview: using mode of action and life stage information to evaluate the human relevance of animal toxicity data. Crit Rev Toxicol 35:664–672

    Google Scholar 

  • Segner H (2009) Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption. Comp Biochem Physiol C Toxicol Pharmacol 149:187–195

    Google Scholar 

  • Serrano-Nascimento C et al (2018) Evaluation of hypothalamus-pituitary-thyroid axis function by chronic perchlorate exposure in male rats. Environ Toxicol 33:209–219

    CAS  Google Scholar 

  • Seyoum A et al (2021) Sublethal effects of DBE-DBCH diastereomers on physiology, behavior, and gene expression of Daphnia magna. Environ Pollut 284:117091

    CAS  Google Scholar 

  • Shanle EK, Xu W (2011) Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action. Chem Res Toxicol 24:6–19

    CAS  Google Scholar 

  • Shen Y et al (2015) Higher urinary bisphenol A concentration is associated with unexplained recurrent miscarriage risk: evidence from a case-control study in eastern China. PLoS ONE 10:e0127886

    Google Scholar 

  • Sifakis S et al (2017) Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environ Toxicol Pharmacol 51:56–70

    CAS  Google Scholar 

  • Siglin JC et al (2000) A 90-day drinking water toxicity study in rats of the environmental contaminant ammonium perchlorate. Toxicol Sci 57:61–74

    CAS  Google Scholar 

  • Sonich-Mullin C et al (2001) IPCS conceptual framework for evaluating a mode of action for chemical carcinogenesis. Regul Toxicol Pharmacol 34:146–152

    CAS  Google Scholar 

  • Spinder N et al (2021) Maternal occupational exposure to endocrine-disrupting chemicals and urogenital anomalies in the offspring. Hum Reprod 37:142–151

    CAS  Google Scholar 

  • Steinmaus C et al (2016) Thyroid hormones and moderate exposure to perchlorate during pregnancy in women in Southern California. Environ Health Perspect 124:861–867

    CAS  Google Scholar 

  • Stojak BL et al (2019) Acute β-tetrabromoethylcyclohexane (β-TBECH) treatment inhibits the electrical activity of rat Purkinje neurons. Chemosphere 231:301–307

    CAS  Google Scholar 

  • Sun J, Fang R, Wang H, Xu DX, Yang J, Huang X, Cozzolino D, Fang M, Huang Y (2022) A review of environmental metabolism disrupting chemicals and effect biomarkers associating disease risks: Where exposomics meets metabolomics. Environ Int 158. https://doi.org/10.1016/j.envint.2021.106941

  • Tay JH et al (2019) Serum concentrations of legacy and emerging halogenated flame retardants in a Norwegian cohort: relationship to external exposure. Environ Res 178:108731

    CAS  Google Scholar 

  • Terry MB et al (2019) Environmental exposures during windows of susceptibility for breast cancer: a framework for prevention research. Breast Cancer Res 21:96

    Google Scholar 

  • Testai E et al (2013) A plea for risk assessment of endocrine disrupting chemicals. Toxicology 314:51–59

    CAS  Google Scholar 

  • Thomas P, Dong J (2006) Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J Steroid Biochem Mol Biol 102:175–179

    CAS  Google Scholar 

  • Thuett KA et al (2002) Effects of in utero and lactational ammonium perchlorate exposure on thyroid gland histology and thyroid and sex hormones in developing deer mice (peromyscus maniculatus) through postnatal day 21. J Toxicol Environ Health A 65:2119–2130

    CAS  Google Scholar 

  • U.S.EPA (1998) Endocrine Disruptor Screening Program (EDSP) 1998 Federal Register Notices. https://www.epa.gov/endocrine-disruption/endocrine-disruptor-screening-program-edsp-1998-federal-register-notices. Accessed 25 Jul 2022

  • Usmani KA et al (2006) Inhibition of the human liver microsomal and human cytochrome P450 1A2 and 3A4 metabolism of estradiol by deployment-related and other chemicals. Drug Metab Dispos 34:1606–1614

    CAS  Google Scholar 

  • Usmani KA et al (2003) Inhibition and activation of the human liver microsomal and human cytochrome P450 3A4 metabolism of testosterone by deployment-related chemicals. Drug Metab Dispos 31:384–391

    CAS  Google Scholar 

  • van den Hove MF et al (1999) Hormone synthesis and storage in the thyroid of human preterm and term newborns: effect of thyroxine treatment. Biochimie 81:563–570

    Google Scholar 

  • Vandenberg LN et al (2016) A proposed framework for the systematic review and integrated assessment (SYRINA) of endocrine disrupting chemicals. Environ Health 15:74

    Google Scholar 

  • Vandenberg LN et al (2008) Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol 26:210–219

    CAS  Google Scholar 

  • Vandenberg LN et al (2020) Agrochemicals with estrogenic endocrine disrupting properties: lessons learned? Mol Cell Endocrinol 518:110860

    CAS  Google Scholar 

  • Viguié C et al (2018) Evidence-based adverse outcome pathway approach for the identification of BPA as en endocrine disruptor in relation to its effect on the estrous cycle. Mol Cell Endocrinol 475:10–28

    Google Scholar 

  • Wang Q, Kelly BC (2017) Occurrence and distribution of halogenated flame retardants in an urban watershed: comparison to polychlorinated biphenyls and organochlorine pesticides. Environ Pollut 231:252–261

    CAS  Google Scholar 

  • Wang Q et al (2016) Reprogramming of the epigenome by MLL1 links early-life environmental exposures to prostate cancer risk. Mol Endocrinol 30:856–871

    CAS  Google Scholar 

  • Wang X et al (2020) Tetrabromoethylcyclohexane (TBECH) exhibits immunotoxicity in murine macrophages. Environ Toxicol 35:159–166

    CAS  Google Scholar 

  • Watson CS et al (2007) Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids 72:124–134

    CAS  Google Scholar 

  • Wee SY, Aris AZ (2017) Endocrine disrupting compounds in drinking water supply system and human health risk implication. Environ Int 106:207–233

    CAS  Google Scholar 

  • Williams-Ashman HG (1965) Androgenic control of nucleic acid and protein synthesis in male accessory genital organs. J Cell Physiol. 66. Suppl 1:111–124

    Google Scholar 

  • Wisniewski P et al (2015) Adult exposure to bisphenol A (BPA) in Wistar rats reduces sperm quality with disruption of the hypothalamic-pituitary-testicular axis. Toxicology 329:1–9

    CAS  Google Scholar 

  • Wong LI et al (2016) The effects of the organic flame-retardant 1,2-dibromo-4-(1,2-dibromoethyl) cyclohexane (TBECH) on androgen signaling in human prostate cancer cell lines. J Biochem Mol Toxicol 30:239–242

    CAS  Google Scholar 

  • Wu D et al (2020) Impairment of learning and memory induced by perinatal exposure to BPA is associated with ERα-mediated alterations of synaptic plasticity and PKC/ERK/CREB signaling pathway in offspring rats. Brain Res Bull 161:43–54

    CAS  Google Scholar 

  • Xu D et al (2021) Association between semen microcystin levels and reproductive quality: a cross-sectional study in Jiangsu and Anhui Provinces, China. Environ Health Perspect 129:127702

    CAS  Google Scholar 

  • Xu G et al (2022) Male reproductive toxicity induced by microcystin-leucine-arginine (MC-LR). Toxicon 210:78–88

    CAS  Google Scholar 

  • Xu X et al (2017) Body burden of heavy metals among HIV high risk population in USA. Environ Pollut 220:1121–1126

    CAS  Google Scholar 

  • Yaoi T et al (2008) Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem Biophys Res Commun 376:563–567

    CAS  Google Scholar 

  • Yigit F, Daglioglu S (2010) Histological changes in the uterus of the hens after embryonic exposure to bisphenol A and diethylstilbestrol. Protoplasma 247:57–63

    CAS  Google Scholar 

  • York RG et al (2005) Refining the effects observed in a developmental neurobehavioral study of ammonium perchlorate administered orally in drinking water to rats. I. Thyroid and reproductive effects. Int J Toxicol 24:403–418

    CAS  Google Scholar 

  • Zamora AN et al (2021) Exposure to phenols, phthalates, and parabens and development of metabolic syndrome among Mexican women in midlife. Front Public Health 9:620769

    Google Scholar 

  • Zgheib E et al (2021) Identification of non-validated endocrine disrupting chemical characterization methods by screening of the literature using artificial intelligence and by database exploration. Environ Int 154:106574

    CAS  Google Scholar 

  • Zhang S et al (2022) A new identity of microcystins: environmental endocrine disruptors? An evidence-based review. Sci Total Environ 851:158262

    CAS  Google Scholar 

  • Zoeller RT (2006) Collision of basic and applied approaches to risk assessment of thyroid toxicants. Ann N Y Acad Sci 1076:168–190

    CAS  Google Scholar 

  • Zoeller RT et al (2014) A path forward in the debate over health impacts of endocrine disrupting chemicals. Environ Health 13:118

    Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (Grant Nos. 82273594, 82073512, and 81773384).

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Huizhen Zhang: conceptualization, writing—review and editing, supervision, and funding acquisition. Xing Guo: conceptualization, methodology, software, writing—original draft preparation, and visualization. Bing Liu: conceptualization, methodology, software, writing—original draft preparation, and visualization. Haohao Liu: software and writing—review and editing. Xingde Du: methodology, writing—review and editing, and visualization. Xinghai Chen: writing—review. Wenjun Wang: writing—review. Shumeng Yuan: software. Bingyu Zhang: software. Yongshui Wang: software. Hongxiang Guo: conceptualization and writing—review and editing.

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Correspondence to Huizhen Zhang.

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Guo, X., Liu, B., Liu, H. et al. Research advances in identification procedures of endocrine disrupting chemicals. Environ Sci Pollut Res 30, 83113–83137 (2023). https://doi.org/10.1007/s11356-023-27755-y

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