A plea for risk assessment of endocrine disrupting chemicals

Toxicology

Volumn 314, Issue 1, 2013, Pages 51-59

  Testai, Emanuela ^a   Galli, Corrado L ^b   Dekant, Wolfgang ^c   Marinovich, Marina ^b   Piersma, Aldert H ^d   Sharpe, Richard M ^e  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Endocrine active substances (EASs); Endocrine disrupters (EDs); Exposure; Monotonic dose response; Regulatory decisions; Risk assessment

Indexed keywords

ENDOCRINE DISRUPTOR; ESTROGEN; ESTROGEN RECEPTOR; INDUSTRIAL CHEMICAL; ISOFLAVONE DERIVATIVE; PHTHALIC ACID; TESTOSTERONE;

ADVERSE OUTCOME; ARTICLE; BIOTRANSFORMATION; BRAIN DEVELOPMENT; CONCEPTUAL FRAMEWORK; ENDOCRINE FUNCTION; ENDOCRINE SYSTEM; ENVIRONMENTAL EXPOSURE; ESTROGEN BLOOD LEVEL; FOOD INTAKE; HAZARD ASSESSMENT; HOMEOSTASIS; HORMONAL REGULATION; HORMONE ACTION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MALE GENITAL SYSTEM DISEASE; NONHUMAN; PREGNANCY; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; REFERENCE VALUE; REPRODUCTIVE TOXICITY; RISK ASSESSMENT; SPECIES DIFFERENCE; TOXICOKINETICS; ANIMAL; DOSE RESPONSE; TOXICITY; TOXICITY TESTING;

ANIMALIA;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; HUMANS; RISK ASSESSMENT; TOXICITY TESTS;

EID: 84884960409     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.07.018     Document Type: Article

References (69)

1. Ashby J. Endocrine disruption occurring at doses lower than those predicted by classical chemical toxicity evaluations: The case bisphenol A. Pure Appl. Chem. 2003, 75:2167-2179.
2. BfR Joint DE - UK position paper. Regulatory definition of an endocrine disrupter in relation to potential threat to human health 2011, Bundesinstitut Risikobewertun, Available at:. http://wwwbfrbundde/cm/349/regulatory_definition_of_an_endocrine_disrupter_in_relation_to_potential_threat_to_human_healthpdf.
3. Blaauboer B.J. Biokinetic modelling and in vitro-in vivo extrapolations. J. Toxicol. Environ. Health B 2010, 13:242-252.
4. Blaauboer B.J., Boekelheide K., Clewell H.J., Daneshian M., Dingemans M.M.L., Goldberg A.M., Heneweer M., Jaworska J., Kramer N.I., Leist M., Seibert H., Testai E., Vandebriel R., Yager J., Zurlo J. Biomarkers in in vitro systems: their use in in vitro-in vivo extrapolations for risk assessment ALTEX-Altern. Anim. Exp. 2012, 29:411-425.
5. Boobis A.R., Doe J.E., Heinrich-Hirsch B., Meek M.E., Munn S., Ruchirawat M., Schlatter J., Seed J., Vickers C. IPCS framework for analyzing the relevance of a noncancer mode of action for humans. Crit. Rev. Toxicol. 2008, 38:87-96.
6. Boobis A.R., Daston G.P., Preston R.J., Olin S.S. Application of key events analysis to chemical carcinogens and noncarcinogens. Crit. Rev. Food Sci. Nutr. 2009, 49:690-707.
7. Carmichael N., Bausen M., Boobis A.R., Cohen S.M., Embry M., Fruijtier-Polloth C., Greim H., Lewis R., Bette Meek M.E., Mellor H., Vickers C., Doe J. Using mode of action information to improve regulatory decision-making: an ECETOC/ILSI RF/HESI workshop overview. Crit. Rev. Toxicol. 2011, 41:175-186.
8. Coecke S., Pelkonen O., Leite S.B., Bernauer U., Bessems J.G.M., Bois F.Y., Gundert-Remy U., Loizou G., Testai E., Zaldívar J.-M. Toxicokinetics as a key to the integrated toxicity risk assessment based primarily on non-animal approaches. Toxicol. in Vitro 2013, 27:1570-1577.
9. Colburn T., Clement C. Advances in Modern Environmental Toxicology 1992, vol. 21. Princeton Scientific Publishing, Princeton, NJ.
10. Courant F., Antignac J.P., Laille J., Monteau F., Andre F., Le Bizec B. Exposure assessment of prepubertal children to steroid endocrine disruptors. 2. Determination of steroid hormones in milk, egg, and meat samples. J. Agric. Food Chem. 2008, 56:3176-3184.
11. Courant F., Antignac J.P., Maume D., Monteau F., Andre F., Le Bizec B. Determination of naturally occurring oestrogens and androgens in retail samples of milk and eggs. Food Addit. Contam. 2007, 24:1358-1366.
12. Delclos K.B., Bucci T.J., Lomax L.G., Latendresse J.R., Warbritton A., Weis C.C., Newbold R.R. Effects of dietary genistein exposure during development on male and female CD (Sprague-Dawley) rats. Reprod. Toxicol. 2001, 15:647-663.
13. Delclos K.B., Weis C.C., Bucci T.J., Olson G., Mellick P., Sadovova N., Latendresse J.R., Thorn B., Newbold R.R. Overlapping but distinct effects of genistein and ethinyl estradiol (EE(2)) in female Sprague-Dawley rats in multigenerational reproductive and chronic toxicity studies. Reprod. Toxicol. 2009, 27:117-132.
14. EC-Weybridge European workshop on the impact of endocrine disrupters on human health and wildlife. Report of Proceedings 1996.
15. EDSTAC Endocrine Disruptor Screening and Testing Advisory Committee Final Report 1998 1998, Available at: http://wwwepagov/endo/pubs/edspoverview/finalrpthtm.
16. EFSA Scientific opinion on bisphenol A: evaluation of a study investigating its neurodevelopmental toxicity, review of recent scientific literature on its toxicity and advice on the Danish risk assessment of bisphenol A of the EFSA Panel on Food contact materials, enzymes, flavourings and processing aids (CEF). EFSA Journal 2010, 8((9) 1929):1-116.
17. EFSA Scientific report of the endocrine active substances task force. EFSA J. 2010, 8((11) 1932):59.
18. EFSA Scientific Opinion on Exploring options for providing advice about possible human health risks based on the concept of Threshold of Toxicological Concern (TTC). EFSA J. 2012, 10(7):2750.
19. EFSA EFSA Scientific Colloquium XVII: low-dose-response in toxicology and risk assessment 2012, 64 pp. Available from: http://www.efsa.europa.eu/en/supporting/doc/353e.pdf.
20. EFSA Scientific Opinion on the hazard assessment of endocrine disruptors: Scientific criteria for identification of endocrine disruptors and appropriateness of existing test methods for assessing effects mediated by these substances on human health and the environment. EFSA J. 2013.
21. Ekuase E.J., Liu Y., Lehmler H.J., Robertson L.W., Duffel M.W. Structure-activity relationships for hydroxylated polychlorinated biphenyls as inhibitors of the sulfation of dehydroepi-androsterone catalyzed by human hydroxysteroid sulfotransferase SULT2A1. Chem. Res. Toxicol. 2011, 24:1720-1728.
22. European Commission, 2000. Report of the EC Scientific Steering Committee's Working Group on Harmonization of Risk Assessement Procedures in the Scientific Committes advising the European Commisssion in the area of human and environmental health.
23. EU FP7 Project PredictIV. Profiling the toxicity of new drugs: a non animal-based approach integrating toxico-dynamics and biokinetics. Web site:. http://www.predict-iv.toxi.uni-wuerzburg.de/.
24. Flouriot G., Pakdel F., Ducouret B., Valotaire Y. Influence of xenobiotics on rainbow trout liver estrogen receptor and vitellogenin gene expression. J. Mol. Endocrinol. 1995, 15:143-151.
25. Goodman and Gilmans The Pharmacological Basis of Therapeutics 2013, The McGraw-Hill Companies, Inc., New York. 12th ed. L.L. Brunton, B.A. Chabner, B.C. Knollmann (Eds.).
26. Goodman J.E., McConnell E.E., Sipes I.G., Witorsch R.J., Slayton T.M., Yu C.J., Lewis A.S., Rhomberg L.R. An updated weight of the evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit. Rev. Toxicol. 2006, 36:387-457.
27. Heger N.E., Hall S.J., Sandrof M.A., McDonnell E.V., Hensley J.B., McDowell E.N., Martin K.A., Gaido K.W., Johnson K.J., Boekelheide K. Human fetal testis xenografts are resistant to phthalate-induced endocrine disruption. Environ. Health Perspect. 2012, 120:1137-1143.
28. Hermsen S.A., Pronk T.E., van den Brandhof E.J., van der Ven L.T., Piersma A.H. Concentration-response analysis of differential gene expression in the zebrafish embryotoxicity test following flusilazole exposure. Toxicol Sci. 2012, 127:303-312.
29. Jobling S., Sumpter J.P. Detergent components in sewage effluent are weakly estrogenic to fish: an in vitro study using rainbow trout (Oncorhynchus myxiss) hepatocytes. Aquat. Toxicol. 1993, 27:361-372.
30. Johnson K.J., Heger N.E., Boekelheide K. Of mice and men (and rats): phthalate-induced fetal testis endocrine disruption is species-dependent. Toxicol. Sci. 2012, 129:235-248.
31. Karbe E., Williams G.M., Lewis R.W., Kimber I., Foster P.M. Distinguishing between adverse and non-adverse effects. Session summary. Exp. Toxicol. Pathol. 2002, 54:51-55.
32. Kavlock R.J., Daston G.P., DeRosa C., Fenner-Crisp P., Gray L.E., Kaattari S., Lucier G., Luster M., Mac M.J., Maczka C., Miller R., Moore J., Rolland R., Scott G., Sheehan D.M., Sinks T., Tilson H.A. Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environ. Health Perspect. 1996, 104(Suppl. 4):715-740.
33. Kortenkamp A., Martin O., Faust M., Evans R., McKinlay R., Orton F., Rosivatz E. State of the art assessment of endocrine disrupters. Final Report 2011, Available at: http://eceuropaeu/environment/endocrine/documents/4_SOTA EDC. Final Report V3 6 Feb 12pdf.
34. Latendresse J.R., Bucci T.J., Olson G., Mellick P., Weis C.C., Thorn B., Newbold R.R., Delclos K.B. Genistein and ethinyl estradiol dietary exposure in multigenerational and chronic studies induce similar proliferative lesions in mammary gland of male Sprague-Dawley rats. Reprod. Toxicol. 2009, 28:342-353.
35. Liu Y., Smart J.T., Song Y., Lehmler H.J., Robertson L.W., Duffel M.W. Structure-activity relationships for hydroxylated polychlorinated biphenyls as substrates and inhibitors of rat sulfotransferases and modification of these relationships by changes in thiol status. Drug Metab. Dispos. 2009, 37:1065-1072.
36. Marx-Stoelting P., Pfeil R., Solecki R., Ulbrich B., Grote K., Ritz V., Banasiak U., Heinrich-Hirsch B., Moeller T., Chahoud I., Hirsch-Ernst K.I. Assessment strategies and decision criteria for pesticides with endocrine disrupting properties relevant to humans. Reprod. Toxicol. 2011, 31:574-584.
37. Matthews S.G. Antenatal glucocorticoids and programming of the developing CNS. Pediatr. Res. 2000, 47:291-300.
38. Mitchell R.T., Childs A.J., Anderson R.A., van den Driesche S., Saunders P.T., McKinnell C., Wallace W.H., Kelnar C.J., Sharpe R.M. Do phthalates affect steroidogenesis by the human fetal testis? Exposure of human fetal testis xenografts to di-n-butyl phthalate. J. Clin. Endocrinol. Metab. 2012, 97:E341-E348.
39. Mitchell R.T., Sharpe R.M., Anderson R.A., McKinnell C., Macpherson S., Smith L.B., Wallace W.H., Kelnar C.J., van den Driesche S. Diethylstilboestrol exposure does not reduce testosterone production in human fetal testis xenografts. Plos ONE 2013, 8(4):e61726. 10.1371/journal.pone.0061726.
40. NRC Toxicity Testing in the 21st Century: A Vision and a Strategy 2007.
41. NRDC Endocrine disruptors. National Resources Defence Council 1998, Available at:. http://wwwnrdcorg/health/effects/qendocasp.
42. OECD Conceptual framework for the testing and assessment of endocrine disrupting chemicals 2002, Organisation for Economic Co-operation and Development, Available at:. http://wwwoecdorg/document/58/0,3343,en_2649_34377_2348794_1_1_1_1,00html.
43. OECD Draft Guidance Document 116 on the Design and Conduct of Chronic Toxicity and Carcinogenicity Studies, Supporting TG 451, 452 and 453 2010, Organisation for Economic Co-operation and Development, Available at: http://wwwoecdorg/chemicalsafety/testingofchemicals/46766792pdf.
44. OECD Guidance Document on the Assessment of Chemicals for Endocrine Disruption, Version 9 2010, Organisation for Economic Co-operation and Development, Available at: http://wwwoecdorg/chemicalsafety/testingofchemicals/46436593pdf.
45. OECD, Draft Guidance Document 151 in support of OECD Test Guideline 443 on an Extended One Generation Reproductive Toxicity Study, 2012, Organization for Economic Co-operation and Development.
46. Piersma A.H., Hernandez L.G., van Benthem J., Muller J.J., van Leeuwen F.X., Vermeire T.G., van Raaij M.T. Reproductive toxicants have a threshold of adversity. Crit. Rev. Toxicol. 2011, 41:545-554.
47. Phillips K.P., Foster W.G., Leiss W., Sahni V., Karyakina N., Turner M.C., Kacew S., Krewski D. Assessing and Managing Risks Arising from Exposure to Endocrine-Active Chemicals. J. Toxicol. Environ. Health B 2008, 11:351-372.
48. Piersma A.H., Bosgra S., van Duursen M.B., Hermsen S.A., Jonker L.R., Kroese E.D., van der Linden S.C., Man H., Roelofs M.J., Schulpen S.H., Schwarz M., Uibel F., van Vugt-Lussenburg B.M., Westerhout J., Wolterbeek A.P., van der Burg B. Evaluation of an alternative in vitro test battery for detecting reproductive toxicants. Reprod. Toxicol. 2013, 16(38C):53-64. [Epub ahead of print]. 10.1016/j.reprotox.2013.03.002.
49. Rhomberg L.R., Goodman J.E. Low-dose effects and nonmonotonic dose-responses of endocrine disrupting chemicals: has the case been made?. Regul. Toxicol. Pharmacol. 2012, 64:130-133.
50. Safe S.H. Environmental and dietary estrogens and human health: is there a problem?. Environ. Health Perspect. 1995, 103:346-351.
51. Safe S. Endocrine disruptors and falling sperm counts: lessons learned or not!. Asian J. Androl. 2013, 15:191-194.
52. SCHER/SCENIHR/SCCS (Scientific Committee on Health and Environmental Risks/Scientific Committee on Emerging and Newly Identified Health Risks/Scientific Committee on Consumer Safety) Toxicity and Assessment of Chemical Mixtures 2011, 50 pp. Available from: http://ec.europa.eu/health/scientific_committees/environmental_risks/docs/scher_o_155.pdf.
53. Sharpe R.M. The 'oestrogen hypothesis'- where do we standnow?. Int J Androl 2003, 26:2-15.
54. Sharpe R.M., Irvine D.S. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health?. BMJ 2004, 328:447-451.
55. Sharpe R.M. Environmental/lifestyle effects on spermatogenesis. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2010, 365(1546):1697-1712.
56. Sharpe R.M. Is it time to end concerns over the estrogenic effects of bisphenol A?. Toxicol. Sci. 2010, 114:1-4.
57. Slob W., Moerbeek M., Rauniomaa E., Piersma A.H. A statistical evaluation of toxicity study designs for the estimation of the benchmark dose in continuous endpoints. Toxicol. Sci. 2005, 84:167-185.
58. U.S. EPA-SAP (U.S. Environmental Protection Agency-FIFRA Scientific Advisory Panel), 2011. Integrated Approaches to Testing and Assessment Strategies: Use of New Computational and Molecular Tools. FIFRA SAP. Final FIFRA SAP IATA Meeting Report May 2011. EPAHQ-OPP-2011-0284-0054, 81 pp.
59. van Dartel D.A., Pennings J.L., de la Fonteyne L.J., Brauers K.J., Claessen S., van Delft J.H., Kleinjans J.C., Piersma A.H. Concentration-dependent gene expression responses to flusilazole in embryonic stem cell differentiation cultures. Toxicol. Appl. Pharmacol. 2011, 251:110-118.
60. Vandenberg L.N., Colborn T., Hayes T.B., Heindel J.J., Jacobs D.R., Lee D.H., Shioda T., Soto A.M., vom Saal F.S., Welshons W.V., Zoeller R.T., Myers J.P. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 2012, 33:378-455.
61. Vandenberg L.N., Maffini M.V., Sonnenschein C., Rubin B.S., Soto A.M. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev. 2009, 30:75-95.
62. vom Saal F.S., Akingbemi B.T., Belcher S.M., Crain D.A., Crews D., Guidice L.C., Hunt P.A., Leranth C., Myers J.P., Nadal A., Olea N., Padmanabhan V., Rosenfeld C.S., Schneyer A., Schoenfelder G., Sonnenschein C., Soto A.M., Stahlhut R.W., Swan S.H., Vandenberg L.N., Wang H.S., Watson C.S., Welshons W.V., Zoeller R.T. Flawed experimental design reveals the need for guidelines requiring appropriate positive controls in endocrine disruption research. Toxicol. Sci. 2010, 115:612-613. (author reply 614-620).
63. Welshons W.V., Thayer K.A., Judy B.M., Taylor J.A., Curran E.M., vom Saal F.S. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ. Health Perspect. 2003, 111(8):994-1004.
64. WHO/IPCS Global Assessment of the State-of-the-Science of Endocrine Disruptors 2002, 180. WHO/PCS/EDC/02.2, World Health Organisation, Geneva.
65. WHO/IPCS Exposure Assessment and Risk Assessment Terminology 2004, Available at: http://wwwwhoint/ipcs/methods/harmonization/areas/terminology/en/indexhtml.
66. WHO/UNEP (World Health Organization/United Nations Environment Programme) State of the Science of Endocrine Disrupting Chemicals 2012, Åke Bergman, Jerrold J. Heindel, Susan Jobling, Karen A. Kidd, R. Thomas Zoeller (Eds.).
67. Witorsch R.J. Endocrine disruptors: can biological effects and environmental risks be predicted?. Regul. Toxicol. Pharmacol. 2002, 36:118-130.
68. Yang X., Doerge D.R., Fisher J.W. Prediction and evaluation of route dependent dosimetry of BPA in rats at different life stages using a physiologically based pharmacokinetic model. Toxicol. Appl. Pharmacol. 2013, 270:45-59.
69. Zoeller R.T., Brown T.R., Doan L.L., Gore A.C., Skakkebaek N.E., Soto A.M., Woodruff T.J., Vom Saal F.S. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology 2012, 153:4097-4110.