Skip to main content
NCBI home page
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 2003 Oct;111(13):1683–1690. doi: 10.1289/ehp.5798

Exposure assessment for endocrine disruptors: some considerations in the design of studies.

Carol Rice 1, Linda S Birnbaum 1, James Cogliano 1, Kathryn Mahaffey 1, Larry Needham 1, Walter J Rogan 1, Frederick S vom Saal 1
PMCID: PMC1241694  PMID: 14527851

Abstract

In studies designed to evaluate exposure-response relationships in children's development from conception through puberty, multiple factors that affect the generation of meaningful exposure metrics must be considered. These factors include multiple routes of exposure; the timing, frequency, and duration of exposure; need for qualitative and quantitative data; sample collection and storage protocols; and the selection and documentation of analytic methods. The methods for exposure data collection and analysis must be sufficiently robust to accommodate the a priori hypotheses to be tested, as well as hypotheses generated from the data. A number of issues that must be considered in study design are summarized here.

Full Text

The Full Text of this article is available as a PDF (137.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akland G. G., Pellizzari E. D., Hu Y., Roberds M., Rohrer C. A., Leckie J. O., Berry M. R. Factors influencing total dietary exposures of young children. J Expo Anal Environ Epidemiol. 2000 Nov-Dec;10(6 Pt 2):710–722. doi: 10.1038/sj.jea.7500129. [DOI] [PubMed] [Google Scholar]
  2. Arnold S. F., Collins B. M., Robinson M. K., Guillette L. J., Jr, McLachlan J. A. Differential interaction of natural and synthetic estrogens with extracellular binding proteins in a yeast estrogen screen. Steroids. 1996 Nov;61(11):642–646. doi: 10.1016/s0039-128x(96)00183-3. [DOI] [PubMed] [Google Scholar]
  3. Bergeron J. M., Crews D., McLachlan J. A. PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination. Environ Health Perspect. 1994 Sep;102(9):780–781. doi: 10.1289/ehp.94102780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernert J. T., Jr, McGuffey J. E., Morrison M. A., Pirkle J. L. Comparison of serum and salivary cotinine measurements by a sensitive high-performance liquid chromatography-tandem mass spectrometry method as an indicator of exposure to tobacco smoke among smokers and nonsmokers. J Anal Toxicol. 2000 Jul-Aug;24(5):333–339. doi: 10.1093/jat/24.5.333. [DOI] [PubMed] [Google Scholar]
  5. Bhattacharya A., Shukla R., Bornschein R. L., Dietrich K. N., Keith R. Lead effects on postural balance of children. Environ Health Perspect. 1990 Nov;89:35–42. doi: 10.1289/ehp.908935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bicknell R. J., Herbison A. E., Sumpter J. P. Oestrogenic activity of an environmentally persistent alkylphenol in the reproductive tract but not the brain of rodents. J Steroid Biochem Mol Biol. 1995 Jul;54(1-2):7–9. doi: 10.1016/0960-0760(95)00118-j. [DOI] [PubMed] [Google Scholar]
  7. Bitman J., Cecil H. C. Estrogenic activity of DDT analogs and polychlorinated biphenyls. J Agric Food Chem. 1970 Nov-Dec;18(6):1108–1112. doi: 10.1021/jf60172a019. [DOI] [PubMed] [Google Scholar]
  8. Brotons J. A., Olea-Serrano M. F., Villalobos M., Pedraza V., Olea N. Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect. 1995 Jun;103(6):608–612. doi: 10.1289/ehp.95103608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Buckley B., Ettinger A., Hore P., Lioy P., Freeman N. Using observational information in planning and implementation of field studies with children as subjects. J Expo Anal Environ Epidemiol. 2000 Nov-Dec;10(6 Pt 2):695–702. doi: 10.1038/sj.jea.7500127. [DOI] [PubMed] [Google Scholar]
  10. Bulger W. H., Muccitelli R. M., Kupfer D. Studies on the in vivo and in vitro estrogenic activities of methoxychlor and its metabolites. Role of hepatic mono-oxygenase in methoxychlor activation. Biochem Pharmacol. 1978;27(20):2417–2423. doi: 10.1016/0006-2952(78)90354-4. [DOI] [PubMed] [Google Scholar]
  11. Colborn T., vom Saal F. S., Soto A. M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993 Oct;101(5):378–384. doi: 10.1289/ehp.93101378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Crews D., Bergeron J. M., McLachlan J. A. The role of estrogen in turtle sex determination and the effect of PCBs. Environ Health Perspect. 1995 Oct;103 (Suppl 7):73–77. doi: 10.1289/ehp.95103s773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cummings A. M., Metcalf J. L. Mechanisms of the stimulation of rat uterine peroxidase activity by methoxychlor. Reprod Toxicol. 1994 Nov-Dec;8(6):477–486. doi: 10.1016/0890-6238(94)90030-2. [DOI] [PubMed] [Google Scholar]
  14. Dietrich K. N., Berger O. G., Succop P. A., Hammond P. B., Bornschein R. L. The developmental consequences of low to moderate prenatal and postnatal lead exposure: intellectual attainment in the Cincinnati Lead Study Cohort following school entry. Neurotoxicol Teratol. 1993 Jan-Feb;15(1):37–44. doi: 10.1016/0892-0362(93)90043-n. [DOI] [PubMed] [Google Scholar]
  15. Dietrich K. N., Krafft K. M., Pearson D. T., Harris L. C., Bornschein R. L., Hammond P. B., Succop P. A. Contribution of social and developmental factors to lead exposure during the first year of life. Pediatrics. 1985 Jun;75(6):1114–1119. [PubMed] [Google Scholar]
  16. Ecobichon D. J., MacKenzie D. O. The uterotropic activity of commercial and isomerically-pure chlorobiphenyls in the rat. Res Commun Chem Pathol Pharmacol. 1974 Sep;9(1):85–95. [PubMed] [Google Scholar]
  17. Fenske R. A. Pesticide exposure assessment of workers and their families. Occup Med. 1997 Apr-Jun;12(2):221–237. [PubMed] [Google Scholar]
  18. Fingerhut M. A., Halperin W. E., Marlow D. A., Piacitelli L. A., Honchar P. A., Sweeney M. H., Greife A. L., Dill P. A., Steenland K., Suruda A. J. Cancer mortality in workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. N Engl J Med. 1991 Jan 24;324(4):212–218. doi: 10.1056/NEJM199101243240402. [DOI] [PubMed] [Google Scholar]
  19. 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 Oct;15(2):143–151. doi: 10.1677/jme.0.0150143. [DOI] [PubMed] [Google Scholar]
  20. Fry D. M. Reproductive effects in birds exposed to pesticides and industrial chemicals. Environ Health Perspect. 1995 Oct;103 (Suppl 7):165–171. doi: 10.1289/ehp.95103s7165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J Mol Biol. 1987 Jul 20;196(2):261–282. doi: 10.1016/0022-2836(87)90689-9. [DOI] [PubMed] [Google Scholar]
  22. Gellert R. J. Kepone, mirex, dieldrin, and aldrin: estrogenic activity and the induction of persistent vaginal estrus and anovulation in rats following neonatal treatment. Environ Res. 1978 Jul;16(1-3):131–138. doi: 10.1016/0013-9351(78)90150-0. [DOI] [PubMed] [Google Scholar]
  23. Gray L. E., Jr, Ostby J., Cooper R. L., Kelce W. R. The estrogenic and antiandrogenic pesticide methoxychlor alters the reproductive tract and behavior without affecting pituitary size or LH and prolactin secretion in male rats. Toxicol Ind Health. 1999 Jan-Mar;15(1-2):37–47. doi: 10.1177/074823379901500105. [DOI] [PubMed] [Google Scholar]
  24. Guillette L. J., Jr, Crain D. A., Rooney A. A., Pickford D. B. Organization versus activation: the role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. Environ Health Perspect. 1995 Oct;103 (Suppl 7):157–164. doi: 10.1289/ehp.95103s7157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hammond B., Katzenellenbogen B. S., Krauthammer N., McConnell J. Estrogenic activity of the insecticide chlordecone (Kepone) and interaction with uterine estrogen receptors. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6641–6645. doi: 10.1073/pnas.76.12.6641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hammond P. B., Dietrich K. N. Lead exposure in early life: health consequences. Rev Environ Contam Toxicol. 1990;115:91–124. doi: 10.1007/978-1-4612-3416-6_3. [DOI] [PubMed] [Google Scholar]
  27. Herbst A. L. Behavior of estrogen-associated female genital tract cancer and its relation to neoplasia following intrauterine exposure to diethylstilbestrol (DES). Gynecol Oncol. 2000 Feb;76(2):147–156. doi: 10.1006/gyno.1999.5471. [DOI] [PubMed] [Google Scholar]
  28. Hubal E. A., Sheldon L. S., Zufall M. J., Burke J. M., Thomas K. W. The challenge of assessing children's residential exposure to pesticides. J Expo Anal Environ Epidemiol. 2000 Nov-Dec;10(6 Pt 2):638–649. doi: 10.1038/sj.jea.7500128. [DOI] [PubMed] [Google Scholar]
  29. Jansen H. T., Cooke P. S., Porcelli J., Liu T. C., Hansen L. G. Estrogenic and antiestrogenic actions of PCBs in the female rat: in vitro and in vivo studies. Reprod Toxicol. 1993 May-Jun;7(3):237–248. doi: 10.1016/0890-6238(93)90230-5. [DOI] [PubMed] [Google Scholar]
  30. Jiang Y., Tsai T. F., Bressler J., Beaudet A. L. Imprinting in Angelman and Prader-Willi syndromes. Curr Opin Genet Dev. 1998 Jun;8(3):334–342. doi: 10.1016/s0959-437x(98)80091-9. [DOI] [PubMed] [Google Scholar]
  31. Jobling S., Reynolds T., White R., Parker M. G., Sumpter J. P. A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ Health Perspect. 1995 Jun;103(6):582–587. doi: 10.1289/ehp.95103582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kashyap R., Iyer L. R., Singh M. M., Kashyap S. K. Evaluation of human exposure to the persistent insecticides DDT and HCH in Ahmedabad, India. J Anal Toxicol. 1993 Jul-Aug;17(4):211–214. doi: 10.1093/jat/17.4.211. [DOI] [PubMed] [Google Scholar]
  33. Kelce W. R., Stone C. R., Laws S. C., Gray L. E., Kemppainen J. A., Wilson E. M. Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist. Nature. 1995 Jun 15;375(6532):581–585. doi: 10.1038/375581a0. [DOI] [PubMed] [Google Scholar]
  34. Korach K. S., Horigome T., Tomooka Y., Yamashita S., Newbold R. R., McLachlan J. A. Immunodetection of estrogen receptor in epithelial and stromal tissues of neonatal mouse uterus. Proc Natl Acad Sci U S A. 1988 May;85(10):3334–3337. doi: 10.1073/pnas.85.10.3334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Krishnan V., Porter W., Santostefano M., Wang X., Safe S. Molecular mechanism of inhibition of estrogen-induced cathepsin D gene expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in MCF-7 cells. Mol Cell Biol. 1995 Dec;15(12):6710–6719. doi: 10.1128/mcb.15.12.6710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. LaKind J. S., Berlin C. M., Naiman D. Q. Infant exposure to chemicals in breast milk in the United States: what we need to learn from a breast milk monitoring program. Environ Health Perspect. 2001 Jan;109(1):75–88. doi: 10.1289/ehp.0110975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Liu H., Wormke M., Safe S. H., Bjeldanes L. F. Indolo[3,2-b]carbazole: a dietary-derived factor that exhibits both antiestrogenic and estrogenic activity. J Natl Cancer Inst. 1994 Dec 7;86(23):1758–1765. doi: 10.1093/jnci/86.23.1758. [DOI] [PubMed] [Google Scholar]
  38. MacLatchy D. L., Van Der Kraak G. J. The phytoestrogen beta-sitosterol alters the reproductive endocrine status of goldfish. Toxicol Appl Pharmacol. 1995 Oct;134(2):305–312. doi: 10.1006/taap.1995.1196. [DOI] [PubMed] [Google Scholar]
  39. Maibach H. I., Feldman R. J., Milby T. H., Serat W. F. Regional variation in percutaneous penetration in man. Pesticides. Arch Environ Health. 1971 Sep;23(3):208–211. doi: 10.1080/00039896.1971.10665987. [DOI] [PubMed] [Google Scholar]
  40. Majdic G., McNeilly A. S., Sharpe R. M., Evans L. R., Groome N. P., Saunders P. T. Testicular expression of inhibin and activin subunits and follistatin in the rat and human fetus and neonate and during postnatal development in the rat. Endocrinology. 1997 May;138(5):2136–2147. doi: 10.1210/endo.138.5.5135. [DOI] [PubMed] [Google Scholar]
  41. Markaverich B. M., Roberts R. R., Alejandro M. A., Johnson G. A., Middleditch B. S., Clark J. H. Bioflavonoid interaction with rat uterine type II binding sites and cell growth inhibition. J Steroid Biochem. 1988;30(1-6):71–78. doi: 10.1016/0022-4731(88)90078-7. [DOI] [PubMed] [Google Scholar]
  42. Markaverich B. M., Webb B., Densmore C. L., Gregory R. R. Effects of coumestrol on estrogen receptor function and uterine growth in ovariectomized rats. Environ Health Perspect. 1995 Jun;103(6):574–581. doi: 10.1289/ehp.95103574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Martin P. M., Horwitz K. B., Ryan D. S., McGuire W. L. Phytoestrogen interaction with estrogen receptors in human breast cancer cells. Endocrinology. 1978 Nov;103(5):1860–1867. doi: 10.1210/endo-103-5-1860. [DOI] [PubMed] [Google Scholar]
  44. Miksicek R. J. Estrogenic flavonoids: structural requirements for biological activity. Proc Soc Exp Biol Med. 1995 Jan;208(1):44–50. doi: 10.3181/00379727-208-43830. [DOI] [PubMed] [Google Scholar]
  45. Mittendorf R. Teratogen update: carcinogenesis and teratogenesis associated with exposure to diethylstilbestrol (DES) in utero. Teratology. 1995 Jun;51(6):435–445. doi: 10.1002/tera.1420510609. [DOI] [PubMed] [Google Scholar]
  46. Mocarelli P., Gerthoux P. M., Ferrari E., Patterson D. G., Jr, Kieszak S. M., Brambilla P., Vincoli N., Signorini S., Tramacere P., Carreri V. Paternal concentrations of dioxin and sex ratio of offspring. Lancet. 2000 May 27;355(9218):1858–1863. doi: 10.1016/S0140-6736(00)02290-X. [DOI] [PubMed] [Google Scholar]
  47. Nagel S. C., vom Saal F. S., Welshons W. V. The effective free fraction of estradiol and xenoestrogens in human serum measured by whole cell uptake assays: physiology of delivery modifies estrogenic activity. Proc Soc Exp Biol Med. 1998 Mar;217(3):300–309. doi: 10.3181/00379727-217-44236. [DOI] [PubMed] [Google Scholar]
  48. Needham L. L., Sexton K. Assessing children's exposure to hazardous environmental chemicals: an overview of selected research challenges and complexities. J Expo Anal Environ Epidemiol. 2000 Nov-Dec;10(6 Pt 2):611–629. doi: 10.1038/sj.jea.7500142. [DOI] [PubMed] [Google Scholar]
  49. Newbold R. R., Hanson R. B., Jefferson W. N., Bullock B. C., Haseman J., McLachlan J. A. Increased tumors but uncompromised fertility in the female descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis. 1998 Sep;19(9):1655–1663. doi: 10.1093/carcin/19.9.1655. [DOI] [PubMed] [Google Scholar]
  50. Olea N., Pulgar R., Pérez P., Olea-Serrano F., Rivas A., Novillo-Fertrell A., Pedraza V., Soto A. M., Sonnenschein C. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect. 1996 Mar;104(3):298–305. doi: 10.1289/ehp.96104298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Paschal D. C., DiPietro E. S., Phillips D. L., Gunter E. W. Age dependence of metals in hair in a selected U.S. population. Environ Res. 1989 Feb;48(1):17–28. doi: 10.1016/s0013-9351(89)80081-7. [DOI] [PubMed] [Google Scholar]
  52. Que Hee S. S., Peace B., Clark C. S., Boyle J. R., Bornschein R. L., Hammond P. B. Evolution of efficient methods to sample lead sources, such as house dust and hand dust, in the homes of children. Environ Res. 1985 Oct;38(1):77–95. doi: 10.1016/0013-9351(85)90074-x. [DOI] [PubMed] [Google Scholar]
  53. Rajapakse Nissanka, Silva Elisabete, Kortenkamp Andreas. Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environ Health Perspect. 2002 Sep;110(9):917–921. doi: 10.1289/ehp.02110917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Ren L., Lewis S. K., Lech J. J. Effects of estrogen and nonylphenol on the post-transcriptional regulation of vitellogenin gene expression. Chem Biol Interact. 1996 Mar 8;100(1):67–76. doi: 10.1016/0009-2797(95)03686-5. [DOI] [PubMed] [Google Scholar]
  55. Rogan W. J., Gladen B. C., Hung K. L., Koong S. L., Shih L. Y., Taylor J. S., Wu Y. C., Yang D., Ragan N. B., Hsu C. C. Congenital poisoning by polychlorinated biphenyls and their contaminants in Taiwan. Science. 1988 Jul 15;241(4863):334–336. doi: 10.1126/science.3133768. [DOI] [PubMed] [Google Scholar]
  56. Rogan W. J. The sources and routes of childhood chemical exposures. J Pediatr. 1980 Nov;97(5):861–865. doi: 10.1016/s0022-3476(80)80289-7. [DOI] [PubMed] [Google Scholar]
  57. Rosenblum E. R., Stauber R. E., Van Thiel D. H., Campbell I. M., Gavaler J. S. Assessment of the estrogenic activity of phytoestrogens isolated from bourbon and beer. Alcohol Clin Exp Res. 1993 Dec;17(6):1207–1209. doi: 10.1111/j.1530-0277.1993.tb05230.x. [DOI] [PubMed] [Google Scholar]
  58. Ruh M. F., Zacharewski T., Connor K., Howell J., Chen I., Safe S. Naringenin: a weakly estrogenic bioflavonoid that exhibits antiestrogenic activity. Biochem Pharmacol. 1995 Oct 26;50(9):1485–1493. doi: 10.1016/0006-2952(95)02061-6. [DOI] [PubMed] [Google Scholar]
  59. Sathyamoorthy N., Wang T. T., Phang J. M. Stimulation of pS2 expression by diet-derived compounds. Cancer Res. 1994 Feb 15;54(4):957–961. [PubMed] [Google Scholar]
  60. Sharpe R. M., Skakkebaek N. E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet. 1993 May 29;341(8857):1392–1395. doi: 10.1016/0140-6736(93)90953-e. [DOI] [PubMed] [Google Scholar]
  61. Shutt D. A., Cox R. I. Steroid and phyto-oestrogen binding to sheep uterine receptors in vitro. J Endocrinol. 1972 Feb;52(2):299–310. doi: 10.1677/joe.0.0520299. [DOI] [PubMed] [Google Scholar]
  62. Skakkebaek N. E., Rajpert-De Meyts E., Main K. M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod. 2001 May;16(5):972–978. doi: 10.1093/humrep/16.5.972. [DOI] [PubMed] [Google Scholar]
  63. Sonnenschein C., Soto A. M., Fernandez M. F., Olea N., Olea-Serrano M. F., Ruiz-Lopez M. D. Development of a marker of estrogenic exposure in human serum. Clin Chem. 1995 Dec;41(12 Pt 2):1888–1895. [PubMed] [Google Scholar]
  64. Soto A. M., Chung K. L., Sonnenschein C. The pesticides endosulfan, toxaphene, and dieldrin have estrogenic effects on human estrogen-sensitive cells. Environ Health Perspect. 1994 Apr;102(4):380–383. doi: 10.1289/ehp.94102380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Soto A. M., Fernandez M. F., Luizzi M. F., Oles Karasko A. S., Sonnenschein C. Developing a marker of exposure to xenoestrogen mixtures in human serum. Environ Health Perspect. 1997 Apr;105 (Suppl 3):647–654. doi: 10.1289/ehp.97105s3647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Soto A. M., Justicia H., Wray J. W., Sonnenschein C. p-Nonyl-phenol: an estrogenic xenobiotic released from "modified" polystyrene. Environ Health Perspect. 1991 May;92:167–173. doi: 10.1289/ehp.9192167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Soto A. M., Sonnenschein C., Chung K. L., Fernandez M. F., Olea N., Serrano F. O. The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ Health Perspect. 1995 Oct;103 (Suppl 7):113–122. doi: 10.1289/ehp.95103s7113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Sumpter J. P., Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect. 1995 Oct;103 (Suppl 7):173–178. doi: 10.1289/ehp.95103s7173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. TULLNER W. W. Uterotrophic action of the insecticide methoxychlor. Science. 1961 Mar 3;133(3453):647–647. doi: 10.1126/science.133.3453.647. [DOI] [PubMed] [Google Scholar]
  70. Titus-Ernstoff L., Hatch E. E., Hoover R. N., Palmer J., Greenberg E. R., Ricker W., Kaufman R., Noller K., Herbst A. L., Colton T. Long-term cancer risk in women given diethylstilbestrol (DES) during pregnancy. Br J Cancer. 2001 Jan 5;84(1):126–133. doi: 10.1054/bjoc.2000.1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Turusov V. S., Trukhanova L. S., Parfenov YuD, Tomatis L. Occurrence of tumours in the descendants of CBA male mice prenatally treated with diethylstilbestrol. Int J Cancer. 1992 Jan 2;50(1):131–135. doi: 10.1002/ijc.2910500126. [DOI] [PubMed] [Google Scholar]
  72. Verdeal K., Brown R. R., Richardson T., Ryan D. S. Affinity of phytoestrogens for estradiol-binding proteins and effect of coumestrol on growth of 7,12-dimethylbenz[a]anthracene-induced rat mammary tumors. J Natl Cancer Inst. 1980 Feb;64(2):285–290. doi: 10.1093/jnci/64.2.285. [DOI] [PubMed] [Google Scholar]
  73. Vine M. F., Stein L., Weigle K., Schroeder J., Degnan D., Tse C. K., Hanchette C., Backer L. Effects on the immune system associated with living near a pesticide dump site. Environ Health Perspect. 2000 Dec;108(12):1113–1124. doi: 10.1289/ehp.001081113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Weisglas-Kuperus N., Patandin S., Berbers G. A., Sas T. C., Mulder P. G., Sauer P. J., Hooijkaas H. Immunologic effects of background exposure to polychlorinated biphenyls and dioxins in Dutch preschool children. Environ Health Perspect. 2000 Dec;108(12):1203–1207. doi: 10.1289/ehp.001081203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Welch R. M., Levin W., Conney A. H. Estrogenic action of DDT and its analogs. Toxicol Appl Pharmacol. 1969 Mar;14(2):358–367. doi: 10.1016/0041-008x(69)90117-3. [DOI] [PubMed] [Google Scholar]
  76. White R., Jobling S., Hoare S. A., Sumpter J. P., Parker M. G. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology. 1994 Jul;135(1):175–182. doi: 10.1210/endo.135.1.8013351. [DOI] [PubMed] [Google Scholar]
  77. Whyatt R. M., Barr D. B. Measurement of organophosphate metabolites in postpartum meconium as a potential biomarker of prenatal exposure: a validation study. Environ Health Perspect. 2001 Apr;109(4):417–420. doi: 10.1289/ehp.01109417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Winter J. S., Hughes I. A., Reyes F. I., Faiman C. Pituitary-gonadal relations in infancy: 2. Patterns of serum gonadal steroid concentrations in man from birth to two years of age. J Clin Endocrinol Metab. 1976 Apr;42(4):679–686. doi: 10.1210/jcem-42-4-679. [DOI] [PubMed] [Google Scholar]
  79. vom Saal F. S., Nagel S. C., Palanza P., Boechler M., Parmigiani S., Welshons W. V. Estrogenic pesticides: binding relative to estradiol in MCF-7 cells and effects of exposure during fetal life on subsequent territorial behaviour in male mice. Toxicol Lett. 1995 May;77(1-3):343–350. doi: 10.1016/0378-4274(95)03316-5. [DOI] [PubMed] [Google Scholar]
  80. vom Saal F. S. Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero. J Anim Sci. 1989 Jul;67(7):1824–1840. doi: 10.2527/jas1989.6771824x. [DOI] [PubMed] [Google Scholar]
  81. vom Saal F. S., Timms B. G., Montano M. M., Palanza P., Thayer K. A., Nagel S. C., Dhar M. D., Ganjam V. K., Parmigiani S., Welshons W. V. Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):2056–2061. doi: 10.1073/pnas.94.5.2056. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Sciences

RESOURCES