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Using systematic reviews for hazard and risk assessment of endocrine disrupting chemicals

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Abstract

The possibility that endocrine disrupting chemicals (EDCs) in our environment contribute to hormonally related effects and diseases observed in human and wildlife populations has caused concern among decision makers and researchers alike. EDCs challenge principles traditionally applied in chemical risk assessment and the identification and assessment of these compounds has been a much debated topic during the last decade. State of the science reports and risk assessments of potential EDCs have been criticized for not using systematic and transparent approaches in the evaluation of evidence. In the fields of medicine and health care, systematic review methodologies have been developed and used to enable objectivity and transparency in the evaluation of scientific evidence for decision making. Lately, such approaches have also been promoted for use in the environmental health sciences and risk assessment of chemicals. Systematic review approaches could provide a tool for improving the evaluation of evidence for decision making regarding EDCs, e.g. by enabling systematic and transparent use of academic research data in this process. In this review we discuss the advantages and challenges of applying systematic review methodology in the identification and assessment of EDCs.

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References

  1. US CDC. National report on human exposure to environmental chemicals. 2015. http://www.cdc.gov/exposurereport/faq.html. Accessed 21 November 2015.

  2. FDA US. Endocrine disruptor knowledge base. 2010. http://www.fda.gov/ScienceResearch/BioinformaticsTools/EndocrineDisruptorKnowledgebase/default.htm. Accessed August 20, 2012.

  3. TEDX. TEDX list of potential endocrine disruptors. 2015. http://endocrinedisruption.org/endocrine-disruption/tedx-list-of-potential-endocrine-disruptors/overview. Accessed 21 November 2015.

  4. Kavlock RJ, Daston GP, DeRosa C, Fenner-Crisp P, Gray LE, Kaattari S, et al. 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(Supp 4):715–40.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Myers JP, Zoeller RT, FS v S. A clash of old and new scientific concepts in toxicity, with important implications for public health. Environ Health Perspect. 2009;117(11):1652–5.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Molander L, Ruden C. Narrow-and-sharp or broad-and-blunt–regulations of hazardous chemicals in consumer products in the European Union. Regul Toxicol Pharmacol. 2012;62(3):523–31.

    Article  PubMed  Google Scholar 

  7. Bergman A, Heindel JJ, Kasten T, Kidd KA, Jobling S, Neira M, et al. The impact of endocrine disruption: a consensus statement on the state of the science. Environ Health Perspect. 2013;121(4):A104–6.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Vandenberg LN, Luthi D, Quinerly D. Plastic bodies in a plastic world: multi-disciplinary approaches to study endocrine disrupting chemicals. J Clean Prod. 2015. doi:10.1016/j.jclepro.2015.01.071.

    Google Scholar 

  9. Bergman Å, Heindel J, Jobling S, Kidd K, Zoeller R, eds. The State-of-the-Science of Endocrine Disrupting Chemicals – 2012. WHO (World Health Organization)/UNEP (United Nations Environment Programme). available from: http://www.who.int/iris/bitstream/10665/78101/1/9789241505031_eng.pdf: 2013.

  10. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A, Prins GS, et al. EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals. Endocr Rev. 2015;36(6):E1–150.

    Article  CAS  PubMed  Google Scholar 

  11. Diamanti-Kandarakis E, Bourguignon JP, Guidice LC, Hauser R, Prins GS, Soto AM, et al. Endocrine-disrupting chemical: an endocrine society scientific statement. Endocr Rev. 2009;30:293–342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A, Prins GS, et al. Executive summary to EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals. Endocr Rev. 2015;36(6):593–602.

    Article  CAS  PubMed  Google Scholar 

  13. Kortenkamp A, Martin O, Faust M, Evans R, McKinlay R, Orton F, et al. State of the Art Assessment of Endocrine Disruptors, Final Report. Brussels: European Commission; 2011. p. 442.

    Google Scholar 

  14. Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM, et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from the endocrine society. Endocrinology. 2012;153(9):4097–110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jr. Jacobs DR, Lee DH, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33(3):378–455.

  16. US EPA. State of the science evaluation: nonmonotonic dose responses as they apply to estrogen, androgen, and thyroid pathways and EPA testing and assessment procedures. 2013.

  17. Rhomberg LR, Goodman JE, Foster WG, Borgert CJ, Van Der Kraak G. A critique of the European commission document, "state of the art assessment of endocrine disrupters". Crit Rev Toxicol. 2012;42(6):465–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kortenkamp A, Martin O, Evans R, Orton F, McKinlay R, Rosivatz E, et al. Response to a critique of the European commission document, "state of the art assessment of endocrine disrupters" by rhomberg and colleagues–letter to the editor. Crit Rev Toxicol. 2012;42(9):787–9 author reply 90-1.

    Article  PubMed  Google Scholar 

  19. Dietrich DR, Aulock SV, Marquardt H, Blaauboer B, Dekant W, Kehrer J, et al. Scientifically unfounded precaution drives European commission's recommendations on EDC regulation, while defying common sense, well-established science and risk assessment principles. Chem Biol Interact. 2013;205(1):A1–5.

    Article  CAS  PubMed  Google Scholar 

  20. Gore AC, Balthazart J, Bikle D, Carpenter DO, Crews D, Czernichow P, et al. Policy decisions on endocrine disruptors should be based on science across disciplines: a response to Dietrich et al. Endocrinology. 2013;154(11):3957–60.

    Article  CAS  PubMed  Google Scholar 

  21. Bergman A, Andersson AM, Becher G, van den Berg M, Blumberg B, Bjerregaard P, et al. Science and policy on endocrine disrupters must not be mixed: a reply to a "common sense" intervention by toxicology journal editors. Environ Heal. 2013;12:69.

    Article  Google Scholar 

  22. Zoeller RT, Bergman A, Becher G, Bjerregaard P, Bornman R, Brandt I, et al. A path forward in the debate over health impacts of endocrine disrupting chemicals. Environ Heal. 2014;13(1):118.

    Article  CAS  Google Scholar 

  23. Lamb JC, Boffetta P, Foster WG, Goodman JE, Hentz KL, Rhomberg LR, et al. Critical comments on the WHO-UNEP state of the science of endocrine disrupting chemicals - 2012. Regul Toxicol Pharmacol. 2014;69(1):22–40.

    Article  PubMed  Google Scholar 

  24. Bergman A, Becher G, Blumberg B, Bjerregaard P, Bornman R, Brandt I, et al. Manufacturing doubt about endocrine disrupter science - a rebuttal of industry-sponsored critical comments on the UNEP/WHO report "state of the science of endocrine disrupting chemicals 2012". Regul Toxicol Pharmacol. 2015;73(3):1007–17.

    Article  PubMed  Google Scholar 

  25. Lamb JC, Boffetta P, Foster WG, Goodman JE, Hentz KL, Rhomberg LR, et al. Comments on the opinions published by bergman et al. (2015) on critical comments on the WHO-UNEP state of the science of endocrine disrupting chemicals (lamb et al. 2014). Regul Toxicol Pharmacol. 2015;73(3):754–7.

    Article  PubMed  Google Scholar 

  26. Michaels D Doubt is their product. Sci Am. 2005;292(6):96–101.

    Article  PubMed  Google Scholar 

  27. Michaels D Manufactured uncertainty: protecting public health in the age of contested science and product defense. Ann N Y Acad Sci. 2006;1076:149–62. doi:10.1196/annals.1371.058.

    Article  CAS  PubMed  Google Scholar 

  28. Rhomberg LR, Goodman JE. Low-dose effects and nonmonotonic dose-responses of endocrine disrupting chemicals: has the case been made? Regul Toxicol Pharmacol. 2012;64(1):130–3.

    Article  CAS  PubMed  Google Scholar 

  29. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). Memorandum on the use of the scientific literature for human health risk assessment purposes - weighing of evidence and expression of uncertainty. available from: http://ec.europa.eu/health/scientific_committees/emerging/docs/scenihr_s_001.pdf2012.

  30. Weed DL. Weight of evidence: a review of concepts and methods. Risk Anal. 2005;25(6):1545–57.

    Article  PubMed  Google Scholar 

  31. (ECHA) ECA. Evaluation under REACH, Progress Report 2012. available from: www.echa.europa.eu. 2013.

  32. EFSA. Guidance of EFSA Application of systematic review methodology to food and feed safety assessments to support decision making. EFSA J. 2010;8:90.

  33. OECD. Manual for the assessment of chemicals. Chapter 3: Data evaluation. Available from: http://www.oecd.org2005.

  34. US EPA. Determining the adequacy of existing data. Available from: http://www.epa.gov/quality 1999.

  35. Silbergeld E, Scherer RW. Evidence-based toxicology: strait is the gate, but the road is worth taking. ALTEX. 2013;30(1):67–73.

    Article  PubMed  Google Scholar 

  36. Tyl RW. In honor of the teratology society's 50th anniversary: the role of teratology society members in the development and evolution of in vivo developmental toxicity test guidelines. Birth Defects Res (Part C). 2010;90:99–102.

    Article  CAS  Google Scholar 

  37. Tyl RW. Basic exploratory research versus guideline-compliant studies used for hazard evaluation and risk assessment: bisphenol a as a case study. Environ Health Perspect. 2009;117(111):1644–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. European Chemicals Agency (ECHA). Guidance on information requirements and chemical safety assessment. Part B: Hazard assessment. Available from: http://echa.europa.eu/documents/10162/13643/information_requirements_part_b_en.pdf. 2011.

  39. Schug TT, Abagyan R, Blumberg B, Collins TJ, Crews D, DeFur PL, et al. Designing endocrine disruption out of the next generation of chemicals. Green Chem. 2013;15:181–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Myers JP, FS v S, BT A, Arizono K, Belcher S, Colborn T, et al. Why public health agencies cannot depend upon 'good laboratory practices' as a criterion for selecting data: the case of bisphenol-a. Environ Health Perspect. 2009;117(3):309–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR, Lee DH, et al. Regulatory decisions on endocrine disrupting chemicals should be based on the principles of endocrinology. Reprod Toxicol. 2013;38C:1–15.

    Article  CAS  Google Scholar 

  42. FS v S, BT A, SM B, LS B, DA C, Eriksen M, et al. Chapel hill bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol. 2007;24(2):131–8.

    Article  CAS  Google Scholar 

  43. FS v S, JP M. Good laboratory practices are not synonymous with good scientific practices, accurate reporting, or valid data. Environ Health Perspect. 2010;118(2):A60.

    Google Scholar 

  44. Gore AC. Editorial: an international riposte to naysayers of endocrine-disrupting chemicals. Endocrinology. 2013;154(11):3955–6.

    Article  CAS  PubMed  Google Scholar 

  45. Gore AC, Heindel JJ, Zoeller RT. Endocrine disruption for endocrinologists (and others). Endocrinology. 2006;147(Suppl 6):S1–3.

    Article  CAS  PubMed  Google Scholar 

  46. Kanno J, Onyon L, Haseman J, Fenner-Crisp P, Ashby J, Owens W. The OECD program to validate the rat uterotrophic bioassay to screen compounds for in vivo estrogenic responses: phase 1. Environ Health Perspect. 2001;109:785–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kanno J, Onyon L, Peddada S, Ashby J, Jacob E, Owens W. The OECD Program to validate the rat uterotrophic bioassay. Phase 2: coded single-dose studies. Environ Health Perspect. 2003;111(12):1550–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kanno J, Onyon L, Peddada S, Ashby J, Jacob E, Owens W. The OECD Program to validate the rat uterotrophic bioassay. Phase 2: dose-response studies. Environ Health Perspect. 2003;111(12):1530–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Birnbaum LS, Bucher JR, Collman GW, Zeldin DC, Johnson AF, Schug TT, et al. Consortium-based science: the NIEHS's multipronged, collaborative approach to assessing the health effects of bisphenol a. Environ Health Perspect. 2012;120(12):1640–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Birnbaum LS. State of the science of endocrine disruptors. Environ Health Perspect. 2013;121(4):A107.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Catanese MC, Suvorov A, Vandenberg LN. Beyond a means of exposure: a new view of the mother in toxicology research. Toxicol Res. 2015;4:592–612.

    Article  CAS  Google Scholar 

  52. Slovic P, Malmfors T, Mertz CK, Neil N, Purchase IFH. Evaluating chemical risks: results of a survey of the British toxicology society. Hum Exp Toxicol. 1997;16(6):289–304.

    Article  CAS  PubMed  Google Scholar 

  53. Krimsky S The weight of scientific evidence in policy and law. Am J Public Health. 2005;95(Suppl 1):S129–36.

    Article  PubMed  Google Scholar 

  54. Linkov I, Loney D, Cormier S, Satterstrom FK, Bridges T. Weight-of-evidence evaluation in environmental assessment: review of qualitative and quantitative approaches. Sci Total Environ. 2009;407:5199–205.

    Article  CAS  PubMed  Google Scholar 

  55. Doull J, Rozman KK, Lowe MC. Hazard evaluation in risk assessment: whatever happened to sound scientific judgment and weight of evidence? Drug Metab Rev. 1996;28(1–2):285–99.

    Article  CAS  PubMed  Google Scholar 

  56. Woodruff TJ, Zeise L, Axelrad DA, Guyton KZ, Janssen S, Miller M, et al. Meeting report: moving upstream-evaluating adverse upstream end points for improved risk assessment and decision-making. Environ Health Perspect. 2008;116(11):1568–75.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Alcock RE, Macgillivray BH, Busby JS. Understanding the mismatch between the demands of risk assessment and practice of scientists–the case of deca-BDE. Environ Int. 2011;37(1):216–25.

    Article  CAS  PubMed  Google Scholar 

  58. EFSA. Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food (AFC) related to 2,2-BIS(4-HYDROXYPHENYL)PROPANE. The EFSA Journal. 2006;428:1–75.

    Google Scholar 

  59. Hengstler JG, Foth H, Gebel T, Kramer PJ, Lilienblum W, Schweinfurth H, et al. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol a. Crit Rev Toxicol. 2011;41(4):263–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. NTP. NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. In: NIH Publication No 08–5994. available from: https://ntp.niehs.nih.gov/ntp/ohat/bisphenol/bisphenol.pdf. 2008.

  61. Lewis RW. Risk assessment of 'endocrine substances': guidance on identifying endocrine disruptors. Toxicol Lett. 2013;223(3):287–90.

    Article  CAS  PubMed  Google Scholar 

  62. Chen CW. Assessment of endocrine disruptors: approaches, issues, and uncertainties. Folia Histochem Cytobiol. 2001;39(Suppl 2):20–3.

    PubMed  Google Scholar 

  63. EFSA. Use of the benchmark dose approach in risk assessment. EFSA J. 2009;1150:1–72.

    Google Scholar 

  64. US EPA. Benchmark dose technical guidance. available from: http://www2.epa.gov/risk/benchmark-dose-technical-guidance 2012.

  65. Hass U, Christiansen S, Axelstad M, Sorensen KD, Boberg J. Input for the REACH-review in 2013 on endocrine disrupters. available from: http://www.mst.dk/NR/rdonlyres/54DB4583-B01D-45D6-AA99-28ED75A5C0E4/154979/ReachreviewrapportFINAL21March.pdf 2013.

  66. Slob W Thresholds in toxicology and risk assessment. Int J Toxicol. 1999;18:259–68.

    Article  CAS  Google Scholar 

  67. Rajapakse N, Silva E, Kortenkamp A. Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone activity. Environ Health Perspect. 2002;110:917–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, FS v S. Large effects from small exposures: I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ Health Perspect. 2003;111:994–1006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ryan BC, Vandenbergh JG. Intrauterine position effects. Neurosci Biobehav Rev. 2002;26:665–78.

    Article  PubMed  Google Scholar 

  70. Heindel JJ, Balbus J, Birnbaum L, Brune-Drisse MN, Grandjean P, Gray K, et al. Developmental origins of health and disease: integrating environmental influences. Endocrinology. 2015;156(10):3416–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Silbergeld EK, Flaws JA, Brown KM. Organizational and activational effects of estrogenic endocrine disrupting chemicals. Cad Saude Publica. 2002;18(2):495–504.

    Article  PubMed  Google Scholar 

  72. Wallen K The organizational hypothesis: reflections on the 50th anniversary of the publication of phoenix, Goy, gerall, and young (1959). Horm Behav. 2009;55(5):561–5.

    Article  PubMed  Google Scholar 

  73. Purchase IF, Auton TR. Thresholds in chemical carcinogenesis. Regul Toxicol Pharmacol. 1995;22(3):199–205.

    Article  CAS  PubMed  Google Scholar 

  74. Neumann HG. Risk assessment of chemical carcinogens and thresholds. Crit Rev Toxicol. 2009;39(6):449–61.

    Article  CAS  PubMed  Google Scholar 

  75. Calafat AM, Ye X, Silva MJ, Kuklenyik Z, Needham LL. Human exposure assessment to environmental chemicals using biomonitoring. Int J Androl. 2006;29(1):166–71 discussion 81-5.

    Article  CAS  PubMed  Google Scholar 

  76. Needham LL, Calafat AM, Barr DB. Assessing developmental toxicant exposures via biomonitoring. Basic Clin Pharmacol Toxicol. 2008;102:100–8.

    Article  CAS  PubMed  Google Scholar 

  77. Woodruff TJ, Zota AR, Schwartz JM. Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ Health Perspect. 2011;119(6):878–85.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Munn S, Heindel J. Assessing the risk of exposures to endocrine disrupting chemicals. Chemosphere. 2013;93(6):845–6.

    Article  CAS  PubMed  Google Scholar 

  79. Beausoleil C, Ormsby JN, Gies A, Hass U, Heindel JJ, Holmer ML, et al. Low dose effects and non-monotonic dose responses for endocrine active chemicals: science to practice workshop: workshop summary. Chemosphere. 2013;93(6):847–56.

    Article  CAS  PubMed  Google Scholar 

  80. Melnick R, Lucier G, Wolfe M, Hall R, Stancel G, Prins G, et al. Summary of the national toxicology program's report of the endocrine disruptors low-dose peer review. Environ Health Perspect. 2002;110(4):427–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Swan SH, Sathyanarayana S, Barrett ES, Janssen S, Liu F, Nguyen RH, et al. First trimester phthalate exposure and anogenital distance in newborns. Hum Reprod. 2015;30(4):963–72.

    Article  CAS  PubMed  Google Scholar 

  82. Barrett ES, Parlett LE, Wang C, Drobnis EZ, Redmon JB, Swan SH. Environmental exposure to di-2-ethylhexyl phthalate is associated with low interest in sexual activity in premenopausal women. Horm Behav. 2014;66(5):787–92.

    Article  CAS  PubMed  Google Scholar 

  83. Lam T, Williams PL, Lee MM, Korrick SA, Birnbaum LS, Burns JS, et al. Prepubertal serum concentrations of organochlorine pesticides and age at sexual maturity in Russian boys. Environ Health Perspect. 2015;123(11):1216–21.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Braun JM, Chen A, Romano ME, Calafat AM, Webster GM, Yolton K, et al. Prenatal perfluoroalkyl substance exposure and child adiposity at 8 years of age: the HOME study. Obesity (Silver Spring). 2016;24(1):231–7.

    Article  CAS  Google Scholar 

  85. Webster GM, Rauch SA, Ste Marie N, Mattman A, Lanphear BP, SA V. Cross-Sectional Associations of Serum Perfluoroalkyl Acids and Thyroid Hormones in U.S. Adults: Variation According to TPOAb and Iodine Status (NHANES 2007-2008). Environ Health Perspect. 2015. doi:10.1289/ehp.1409589.

    Google Scholar 

  86. Engel SM, Bradman A, Wolff MS, Rauh VA, Harley KG, Yang JH, et al. Prenatal organophosphorus pesticide exposure and child neurodevelopment at 24 months: an analysis of four birth cohorts. Environ Health Perspect. 2015. doi:10.1289/ehp.1409474.

    Google Scholar 

  87. Werner EF, Braun JM, Yolton K, Khoury JC, Lanphear BP. The association between maternal urinary phthalate concentrations and blood pressure in pregnancy: the HOME study. Environ Heal. 2015;14:75.

    Article  Google Scholar 

  88. Vandenberg LN, Ehrlich S, Belcher SM, Ben-Jonathan N, Dolinoy DC, Hugo ER, et al. Low dose effects of bisphenol a: an integrated review of in vitro, laboratory animal and epidemiology studies. Endocrine Disruptors. 2013;1(1):e25078.

    Article  Google Scholar 

  89. Birnbaum LS. Environmental chemicals: evaluating low-dose effects. Environ Health Perspect. 2012;120(4):A143–4.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Acevedo N, Davis B, Schaeberle CM, Sonnenschein C, Soto AM. Perinatally administered bisphenol a as a potential mammary gland carcinogen in rats. Environ Health Perspect. 2013;121(9):1040–6.

    PubMed  PubMed Central  Google Scholar 

  91. Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, et al. Perinatal exposure to environmentally relevant levels of bisphenol a decreases fertility and fecundity in CD-1 mice. Environ Health Perspect. 2011;119(4):547–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. McLachlan JA, Newbold RR, Shah HC, Hogan MD, Dixon RL. Reduced fertility in female mice exposed transplacentally to diethylstilbestrol (DES). Fertil Steril. 1982;38:364–71.

    CAS  PubMed  Google Scholar 

  93. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, et al. Bisphenol A exposure causes meiotic aneuploidy in the female mouse. Curr Biol. 2003;13(7):546–53.

    Article  CAS  PubMed  Google Scholar 

  94. Prins GS, Ye SH, Birch L, Ho SM, Kannan K. Serum bisphenol a pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod Toxicol. 2011;31(1):1–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Jenkins S, Rowell C, Wang J, Lamartiniere CA. Prenatal TCDD exposure predisposes for mammary cancer in rats. Reprod Toxicol. 2007;23(3):391–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Lamartiniere CA, Jenkins S, Betancourt AM, Wang J, Russo J. Exposure to the endocrine disruptor bisphenol a alters susceptibility for mammary cancer. Horm Mol Biol Clin Investig. 2011;5(2):45–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. White SS, Stanko JP, Kato K, Calafat AM, Hines EP, Fenton SE. Gestational and chronic low-dose PFOA exposures and mammary gland growth and differentiation in three generations of CD-1 mice. Environ Health Perspect. 2011;119(8):1070–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, Rubin BS, et al. Perinatal exposure to the xenoestrogen bisphenol-a induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod Toxicol. 2008;26:210–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Sharpe RM, Rivas A, Walker M, McKinnell C, Fisher JS. Effect of neonatal treatment of rats with potent or weak (environmental) oestrogens, or with a GnRH antagonist, on leydig cell development and function through puberty into adulthood. Int J Androl. 2003;26(1):26–36.

    Article  CAS  PubMed  Google Scholar 

  100. Do RP, Stahlhut RW, Ponzi D, Vom Saal FS, Taylor JA. Non-monotonic dose effects of in utero exposure to di(2-ethylhexyl) phthalate (DEHP) on testicular and serum testosterone and anogenital distance in male mouse fetuses. Reprod Toxicol. 2012;34(4):614–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 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;146:607–12.

    Article  CAS  PubMed  Google Scholar 

  102. Richter CA, Taylor JA, Ruhlen RL, Welshons WV, FS v S. Estradiol and bisphenol a stimulate androgen receptor and estrogen receptor gene expression in fetal mouse prostate mesenchyme cells. Environ Health Perspect. 2007;115(6):902–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Gore AC, Walker DM, Zama AM, Armenti AE, Uzumcu M. Early life exposure to endocrine-disrupting chemicals causes lifelong molecular reprogramming of the hypothalamus and premature reproductive aging. Mol Endocrinol. 2011;25(12):2157–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Patisaul HB, Sullivan AW, Radford ME, Walker DM, Adewale HB, Winnik B, et al. Anxiogenic effects of developmental bisphenol a exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy. PLoS One. 2012;7(9):e43890.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol a. Endocrinology. 2006;147(8):3681–91.

    Article  CAS  PubMed  Google Scholar 

  106. Palanza P, Morellini F, Parmigiani S, FS v S. Ethological methods to study the effects of maternal exposure to estrogenic endocrine disrupters: a study with methoxychlor. Neurotoxicol Teratol. 2002;24(1):55–69.

    Article  CAS  PubMed  Google Scholar 

  107. Palanza P, Parmigiani S, Liu H, FS v S. Prenatal exposure to low doses of the estrogenic chemicals diethylstilbestrol and o,p'-DDT alters aggressive behavior of male and female house mice. Pharmacol Biochem Behav. 1999;64(4):665–72.

    Article  CAS  PubMed  Google Scholar 

  108. Palanza P, Parmigiani S, FS v S. Effects of prenatal exposure to low doses of diethylstilbestrol, o,p'DDT, and methoxychlor on postnatal growth and neurobehavioral development in male and female mice. Horm Behav. 2001;40:252–65.

    Article  CAS  PubMed  Google Scholar 

  109. Steinberg RM, Juenger TE, Gore AC. The effects of prenatal PCBs on adult female paced mating reproductive behaviors in rats. Horm Behav. 2007;51(3):364–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. NRC. Toxicity-pathway-based risk assessment: preparing for paradigm change. available from: http://www.nap.edu/download.php?record_id=12913# 2010.

  111. Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, et al. Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem. 2010;29(3):730–41.

    Article  CAS  PubMed  Google Scholar 

  112. Gee D Late lessons from early warnings: toward realism and precaution with endocrine-disrupting substances. Environ Health Perspect. 2006;114(Suppl 1):152–60.

    PubMed  PubMed Central  Google Scholar 

  113. Vandenberg LN, Bowler AG. Non-monotonic dose responses in EDSP tier 1 guideline assays. Endocrine Disruptors. 2014;2(1):e964530.

    Article  Google Scholar 

  114. Zoeller RT, Vandenberg LN. Assessing dose-response relationships for endocrine disrupting chemicals (EDCs): a focus on non-monotonicity. Environ Heal. 2015;14(1):42.

    Article  CAS  Google Scholar 

  115. Vandenberg LN. Low-dose effects of hormones and endocrine disruptors. Vitam Horm. 2014;94:129–65.

    Article  PubMed  CAS  Google Scholar 

  116. Vandenberg LN. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol a as a case study. Dose-Response. 2013;12(2):259–76.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. EFSA. EFSA's 17th Scientific Colloquium on low dose response in toxicology and risk assessment. available from: http://www.efsa.europa.eu/en/supporting/doc/353e.pdf 2012.

  118. FS v S, BT A, SM B, DA C, Crews D, LC G, et al. Flawed experimental design reveals the need for guidelines requiring appropriate positive controls in endocrine disruption research. Toxicol Sci. 2010;115(2):612–3.

    Article  CAS  Google Scholar 

  119. Phoenix CH, Goy RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology. 1959;65:369–82.

    Article  CAS  PubMed  Google Scholar 

  120. Heindel JJ, Vandenberg LN. Developmental origins of health and disease: a paradigm for understanding disease etiology and prevention. Curr Opin Pediatr. 2015;27(2):248–53.

    Article  CAS  PubMed  Google Scholar 

  121. Heindel JJ. Role of exposure to environmental chemicals in the developmental basis of reproductive disease and dysfunction. Semin Reprod Med. 2006;24(3):168–77.

    Article  CAS  PubMed  Google Scholar 

  122. Matthews SJ, McCoy C. Thalidomide: a review of approved and investigational uses. Clin Ther. 2003;25(2):342–95.

    Article  CAS  PubMed  Google Scholar 

  123. Vargesson N Thalidomide-induced limb defects: resolving a 50-year-old puzzle. BioEssays. 2009;31(12):1327–36.

    Article  CAS  PubMed  Google Scholar 

  124. Ruegg J, Penttinen-Damdimopoulou P, Makela S, Pongratz I, Gustafsson JA. Receptors mediating toxicity and their involvement in endocrine disruption. EXS. 2009;99:289–323.

    CAS  PubMed  Google Scholar 

  125. Ellis-Hutchings RG, Rasoulpour RJ, Terry C, Carney EW, Billington R. Human relevance framework evaluation of a novel rat developmental toxicity mode of action induced by sulfoxaflor. Crit Rev Toxicol. 2014;44(Suppl 2):45–62.

    Article  CAS  PubMed  Google Scholar 

  126. Tian J, Feng Y, Fu H, Xie HQ, Jiang JX, Zhao B. The aryl hydrocarbon receptor: a key bridging molecule of external and internal chemical signals. Environ Sci Technol. 2015;49(16):9518–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924–6.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Higgins J, Green S. Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0 (updated March 2011). http://handbook.cochrane.org/(accessed 3 February 2013). 2011.

  129. Eden J, Levit L, Berg A, Morton S. Finding out what works in health care. Institute of Medicine of the National Academies: Standards for Systematic Reviews; 2011.

    Google Scholar 

  130. Agerstrand M, Beronius A. Weight of Evidence evaluation and Systematic Review in EU chemical risk assessment: Foundation is laid but guidance is needed. Environment International. 2015.

  131. US EPA. Framework for human health risk assessment to inform decision making, 2014.

  132. Birnbaum LS, Thayer KA, Bucher JR, Wolfe MS. Implementing systematic review at the national toxicology program: status and next steps. Environ Health Perspect. 2013;121(4):A108–9.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Rooney AA, Boyles AL, Wolfe MS, Bucher JR, Thayer KA. Systematic review and evidence integration for literature-based environmental health science assessments. Environ Health Perspect. 2014;122(7):711–8.

    PubMed  PubMed Central  Google Scholar 

  134. Woodruff TJ, Sutton P. An evidence-based medicine methodology to bridge the gap between clinical and environmental health sciences. Health Aff. 2011;30(5):931–7.

    Article  Google Scholar 

  135. Beronius A, Molander L, Ruden C, Hanberg A. Facilitating the use of non-standard in vivo studies in health risk assessment of chemicals: a proposal to improve evaluation criteria and reporting. J Appl Toxicol. 2014;34(6):607–17.

    Article  CAS  PubMed  Google Scholar 

  136. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Landis SC, Amara SG, Asadullah K, Austin CP, Blumenstein R, Bradley EW, et al. A call for transparent reporting to optimize the predictive value of preclinical research. Nature. 2012;490(7419):187–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Agerstrand M, Breitholtz M, Ruden C. Comparison of four different methods for reliability evaluation of ecotoxicity data: a case study of non-standard test data used in environmental risk assessment of pharmaceutical substances. Environ Sci Eur. 2011;23:17.

    Article  Google Scholar 

  139. Klimisch HJ, Andreae M, Tillmann U. A systematic approach for evaluating the quality of experimental toxicological and ecotoxicological data. Regul Toxicol Pharmacol. 1997;25(1):1–5.

    Article  CAS  PubMed  Google Scholar 

  140. Hunt PA, Vandevoort CA, Woodruff T, Gerona R. Invalid controls undermine conclusions of FDA studies. Toxicol Sci. 2014;141(1):1–2.

    Article  PubMed  Google Scholar 

  141. Schneider K, Schwarz M, Burkholder I, Kopp-Schneider A, Edler L, Kinsner-Ovaskainen A, et al. "ToxRTool", a new tool to assess the reliability of toxicological data. Toxicol Lett. 2009;189(2):138–44.

    Article  CAS  PubMed  Google Scholar 

  142. Molander L, Agerstrand M, Beronius A, Hanberg A, Ruden C. Science in risk assessment and policy (SciRAP) – an online resource for evaluating and reporting in vivo (Eco) toxicity studies. Hum Ecol Risk Assess. 2015;21:753–62.

    Article  CAS  Google Scholar 

  143. Hayes TB. Atrazine has been used safely for 50 years? In: JE E, CA B, CA M, editors. Wildlife Ecotoxicology: Forensic Approaches. editors ed. New York, NY: Spring Science + Business Media, LLC; 2011. p. 301–24.

    Chapter  Google Scholar 

  144. Ruhlen RL, Taylor JA, Mao J, Kirkpatrick J, Welshons WV, FS v S. Choice of animal feed can alter fetal steroid levels and mask developmental effects of endocrine disrupting chemicals. J Develop Origins Health Disease. 2011:1–13.

  145. FS v S, Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect. 2005;113:926–33.

    Article  CAS  Google Scholar 

  146. FS v S, CA R, RR R, SC N, BG T, WV W. The importance of appropriate controls, animal feed, and animal models in interpreting results from low-dose studies of bisphenol. A Birth Defects Res (Part A). 2005;73:140–5.

    Article  CAS  Google Scholar 

  147. FS v S, WV W. Large effects from small exposures. II. The importance of positive controls in low-dose research on bisphenol. A Environmental Research. 2006;100:50–76.

    Article  CAS  Google Scholar 

  148. Mesnage R, Defarge N, Rocque LM. Spiroux de vendomois J, seralini GE. Laboratory rodent diets contain toxic levels of environmental contaminants: implications for regulatory tests. PLoS One. 2015;10(7):e0128429.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Vandenberg LN, Welshons WV, Vom Saal FS, Toutain PL, Myers JP. Should oral gavage be abandoned in toxicity testing of endocrine disruptors? Environ Heal. 2014;13(1):46.

    Article  CAS  Google Scholar 

  150. Vandenberg LN, Catanese MC. Casting a wide net for endocrine disruptors. Chem Biol. 2014;21(6):705–6.

    Article  CAS  PubMed  Google Scholar 

  151. FS v S, SC N, BG T, WV W. Implications for human health of the extensive bisphenol a literature showing adverse effects at low doses: a response to attempts to mislead the public. Toxicology. 2005;212(2–3):244–52 author reply 53-4.

    Google Scholar 

  152. Damstra T, Barlow S, Bergman A. In: Kavlock RJ, van der Kraak G, editors. Global assessment of the state-of-the-science of endocrine disruptors. Geneva, Switzerland: World Health Organization; 2002.

    Google Scholar 

  153. WHO. State of the science of endocrine disrupting chemicals - 2012. An assessment of the state of the science of endocrine disruptors prepared by a group of experts for the United Nations Environment Programme (UNEP) and WHO. 2013.

  154. Dechanet C, Anahory T, Mathieu Daude JC, Quantin X, Reyftmann L, Hamamah S, et al. Effects of cigarette smoking on reproduction. Hum Reprod Update. 2011;17(1):76–95.

    Article  CAS  PubMed  Google Scholar 

  155. Oppeneer SJ, Robien K. Bisphenol A exposure and associations with obesity among adults: a critical review. Public Health Nutr. 2014;1-17.

  156. Kuo CC, Moon K, Thayer KA, Navas-Acien A. Environmental chemicals and type 2 diabetes: an updated systematic review of the epidemiologic evidence. Current Diabetes rEports. 2013;13(6):831–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Goodman M, Mandel JS, DeSesso JM, Scialli AR. Atrazine and pregnancy outcomes: a systematic review of epidemiologic evidence. Birth Defects Res B Dev Reprod Toxicol. 2014;101(3):215–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Salay E, Garabrant D. Polychlorinated biphenyls and thyroid hormones in adults: a systematic review appraisal of epidemiological studies. Chemosphere. 2009;74(11):1413–9.

    Article  CAS  PubMed  Google Scholar 

  159. Johnson PI, Sutton P, Atchley DS, Koustas E, Lam J, Sen S, et al. The navigation guide-evidence-based medicine meets environmental health: systematic review of human evidence for PFOA effects on fetal growth. Environ Health Perspect. 2014;122(10):1028–39.

    PubMed  PubMed Central  Google Scholar 

  160. Koustas E, Lam J, Sutton P, Johnson PI, Atchley DS, Sen S, et al. The navigation guide-evidence-based medicine meets environmental health: systematic review of nonhuman evidence for PFOA effects on fetal growth. Environ Health Perspect. 2014;122(10):1015–27.

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Trasande L, Zoeller RT, Hass U, Kortenkamp A, Grandjean P, Myers JP, et al. Estimating burden and disease costs of exposure to endocrine-disrupting chemicals in the European Union. J Clin Endocrinol Metab. 2015;100(4):1245–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Mackay B Canada's new toxic hit list called "inadequate". CMAJ. 2007;176(4):431–2.

    Article  PubMed  PubMed Central  Google Scholar 

  163. Environmental Health Perspectives. Instructions to Authors. 2015. http://ehp.niehs.nih.gov/instructions-to-authors/#what. Accessed 22 November 2015.

  164. PLOS ONE. Best practices in research reporting. 2015. http://journals.plos.org/plosone/s/best-practices-in-research-reporting. Accessed 22 November 2015.

  165. Pae CU. Why systematic review rather than narrative review? Psychiatry Investigation. 2015;12(3):417–9.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

LNV was supported by start-up funds from the University of Massachusetts and Award Number K22ES025811 from the National Institute of Environmental Health Sciences of the National Institutes of Health. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The authors thank many colleagues for helpful discussions about systematic reviews and EDCs.

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Correspondence to Laura N. Vandenberg.

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LNV has been reimbursed for travel expenses by numerous organizations including SweTox, Israel Environment Fund, the Mexican Endocrine Society, Advancing Green Chemistry, ShiftCon, US EPA, CropLife America, the World Federation of Scientists, BeautyCounter, and many universities, to speak about endocrine disrupting chemicals.

AB has no conflicts of interest to declare.

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Beronius, A., Vandenberg, L.N. Using systematic reviews for hazard and risk assessment of endocrine disrupting chemicals. Rev Endocr Metab Disord 16, 273–287 (2015). https://doi.org/10.1007/s11154-016-9334-7

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