Developmental treatment with bisphenol a or ethinyl estradiol causes few alterations on early preweaning measures

Toxicological Sciences

Volumn 124, Issue 1, 2011, Pages 149-160

  Ferguson, Sherry A ^a   Law, Charles D ^a   Abshire, Jordan S ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Anogenital distance; Behavior; Bisphenol A; Developmental; Rat; Righting reflex

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CORTICOSTERONE; ESTRADIOL; ETHINYLESTRADIOL; GHRELIN; LEPTIN; LIOTHYRONINE; LUTEINIZING HORMONE; TESTOSTERONE; THYROXINE;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; BRAIN WEIGHT; BREEDING; CONTROLLED STUDY; EAR; ENVIRONMENTAL EXPOSURE; EYE DEVELOPMENT; FEMALE; LACTATION; LATENT PERIOD; MALE; NONHUMAN; PERINATAL PERIOD; PROGENY; RAT; RISK ASSESSMENT; SPRAGUE DAWLEY RAT; WEANING;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHINYL ESTRADIOL; FEMALE; GENITALIA; GESTATIONAL AGE; HORMONES; MALE; ORGAN SIZE; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROPORTIONAL HAZARDS MODELS; RATS; RATS, SPRAGUE-DAWLEY; REFLEX, RIGHTING; WEANING;

EID: 84155196848     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr201     Document Type: Article

References (83)

1. Akingbemi, B. T., Sottas, C.M., Koulova, A. I., Klinefelter, G. R., andHardy, M.P. (2004). Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associatedwith reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 145, 592-603.
2. Alonso-Magdalena, P., Vieira, E., Soriano, S., Menes, L., Burks, D., Quesada, I., and Nadal, A. (2010). Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ. Health Perspect. 118, 1243-1250.
3. Arabo, A., Lefebvre, M., Fermanel, M., and Caston, J. (2005). Administration of 17alpha-ethinylestradiol during pregnancy elicits modifications of maternal behavior and emotional alteration of the offspring in the rat. Brain Res. Dev. Brain Res. 156, 93-103.
4. Ashby, J., and Lefevre, P. A. (1997). The weanling male rat as an assay for endocrine disruption: preliminary observations. Regul. Toxicol. Pharmacol. 26, 330-337.
5. Bai, Y., Chang, F., Zhou, R., Jin, P. P., Matsumoto, H., Sokabe, M., and Chen, L. (2011). Increase of anteroventral periventricular kisspeptin neurons and generation of E2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology 152, 1562-1571.
6. Balcombe, J. P., Barnard, N. D., and Sandusky, C. (2004). Laboratory routines cause animal stress. Contemp. Top. Lab. Anim. Sci. 43, 42-51.
7. Ball, E. R., Caniglia, M. K., Wilcox, J. L., Overton, K. A., Burr, M. J., Wolfe, B. D., Sanders, B.J., Wisniewski, A.B., and Wrenn, C.C. (2010). Effects of genistein in the maternal diet on reproductive development and spatial learning in male rats. Horm. Behav. 57, 313-322.
8. Bar, A., Til, H. P., and Timonen, M. (1995). Subchronic oral toxicity study with regular and enzymatically depolymerized sodium carboxymethylcellulose in rats. Food Chem. Toxicol. 33, 909-917.
9. Becker, L. A., Kunkel, A. J., Brown, M. R., Ball, E. E., and Williams, M. T. (2005). Effects of dietary phytoestrogen exposure during perinatal period. Neurotoxicol. Teratol. 27, 825-834.
10. Beronius, A., Ruden, C., Hakansson, H., and Hanberg, A. (2010). Risk to all or none? A comparative analysis of controversies in the health risk assessment of bisphenol A. Reprod. Toxicol 29, 132-146.
11. Boctor, S. Y., Wang, C., and Ferguson, S. A. (2008). Neonatal PCP is more potent than ketamine at modifying preweaning behaviors of Sprague-Dawley rats. Toxicol. Sci. 106, 172-179.
12. Bushnik, T., Haines, D., Levallois, P., Levesque, J., Van Oostdam, J., and Viau, C. (2010). Lead and bisphenol A concentrations in the Canadian population. Health Rep. 21, 7-18.
13. Buynitsky, T., and Mostofsky, D. I. (2009). Restraint stress in biobehavioral research: recent developments. Neurosci. Biobehav. Rev. 33, 1089-1098.
14. Cagen, S. Z., Waechter, J. M., Jr, Dimond, S. S., Breslin, W. J., Butala, J. H., Jekat, F. W., Joiner, R.L., Shiotsuka, R.N., Veenstra, G.E., and Harris, L.R. (1999). Normal reproductive organ development in Wistar rats exposed to bisphenol A in the drinking water. Regul. Toxicol. Pharmacol. 30(2 Pt 1), 130-139.
15. Calafat, A. M., Ye, X., Wong, L. Y., Reidy, J. A., and Needham, L. L. (2008). Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ. Health Perspect. 116, 39-44.
16. Cardoso, N., Pandolfi, M., Ponzo, O., Carbone, S., Szwarcfarb, B., Scacchi, P., and Reynoso, R. (2010). Evidence to suggest glutamic acid involvement in Bisphenol A effect at the hypothalamic level in prepubertal male rats. Neuro. Endocrinol. Lett. 31, 512-516.
17. Christiansen, S., Scholze, M., Dalgaard, M., Vinggaard, A. M., Axelstad, M., Kortenkamp, A., and Hass, U. (2009). Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ. Health Perspect. 117, 1839-1846.
18. Cooke, B., Hegstrom, C. D., Villeneuve, L. S., and Breedlove, S. M. (1998). Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol. 19, 323-362.
19. de Castro, V. L., de Mello, M. A., Diniz, C., Morita, L., Zucchi, T., and Poli, P. (2007). Neurodevelopmental effects of perinatal fenarimol exposure on rats. Reprod. Toxicol. 23, 98-105.
20. Delclos, K. B., Weis, C. C., Bucci, T. J., Olson, G., Mellick, P., Sadovova, N., Latendresse, J.R., Thorn, B., and Newbold, R.R. (2009). 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. 27, 117-132.
21. Díeguez, C., da Boit, K., Novelle, M. G., Martínez de Morentin, P. B., Nogueiras, R., and López, M. (2010). New insights in ghrelin orexigenic effect. Front. Horm. Res. 38, 196-205.
22. Diel, P., Schmidt, S., Vollmer, G., Janning, P., Upmeier, A., Michna, H., Bolt, H.M., and Degen, G.H. (2004). Comparative responses of three rat strains (DA/Han, Sprague-Dawley and Wistar) to treatment with environmental estrogens. Arch. Toxicol. 78, 183-193.
23. Doerge, D. R., Twaddle, N. C., Vanlandingham, M., and Fisher, J. W. (2010a). Pharmacokinetics of bisphenol A in neonatal and adult Sprague-Dawley rats. Toxicol. Appl. Pharmacol. 247, 158-165.
24. Doerge, D. R., Vanlandingham, M., Twaddle, N. C., and Delclos, K. B. (2010b). Lactational transfer of bisphenol A in Sprague-Dawley rats. Toxicol. Lett. 199, 372-376.
25. Dohler, K. D., and Wuttke, W. (1976). Circadian fluctuations of serum hormone levels in prepubertal male and female rats. Acta Endocrinol. (Copenh.) 83, 269-279.
26. Ema, M., Fujii, S., Furukawa, M., Kiguchi, M., Ikka, T., and Harazono, A. (2001). Rat two-generation reproductive toxicity study of bisphenol A. Reprod. Toxicol. 15, 505-523.
27. Ferguson, S. A., Delclos, K. B., Newbold, R. R., and Flynn, K. M. (2003a). Dietary ethinyl estradiol exposure during development causes increased voluntary sodium intake and mild maternal and offspring toxicity in rats. Neurotoxicol. Teratol. 25, 491-501.
28. Ferguson, S. A., Garey, J., Smith, M. E., Twaddle, N. C., Doerge, D. R., and Paule, M. G. (2010). Preweaning behaviors, developmental landmarks, and acrylamide and glycidamide levels after pre- and postnatal acrylamide treatment in rats. Neurotoxicol. Teratol. 32, 373-382.
29. Ferguson, S. A., Gray, E. P., and Cada, A. M. (2003b). Early behavioral development in the spontaneously hypertensive rat: a comparison with the Wistar-Kyoto and Sprague-Dawley strains. Behav. Neurosci. 117, 263-270.
30. Ferguson, S. A., Paule, M. G., and Holson, R. R. (2001). Neonatal dexamethasone on day 7 in rats causes behavioral alterations reflective of hippocampal, but not cerebellar, deficits. Neurotoxicol. Teratol. 23, 57-69.
31. Ferguson, S. A., Racey, F. D., Paule, M. G., and Holson, R. R. (1993). Behavioral effects of methylazoxymethanol-induced micrencephaly. Behav. Neurosci. 107, 1067-1076.
32. Food and Agriculture Organization of the United Nations, World Health Organization, 2010 Food and Agriculture Organization of the United Nations, World Health Organization. (2010). Joint FAO/WHO Expert Meeting to Review Toxicological and Health Aspects of Bisphenol A Ottawa, Canada. p Available at: http://www.who.int/foodsafety/chem/chemicals/BPA_Summary2010.pdf. Accessed June 22, 2011.
33. Fritz, H., and Becker, H. (1981). The suitability of carboxymethylcellulose as a vehicle in reproductive studies. Arzneimittelforschung 31, 813-815.
34. Gallavan, R. H., Jr, Holson, J. F., Stump, D. G., Knapp, J. F., and Reynolds, V. L. (1999). Interpreting the toxicologic significance of alterations in anogenital distance: potential for confounding effects of progeny body weights. Reprod. Toxicol. 13, 383-390.
35. Goodman, J. E., McConnell, E. E., Sipes, I. G., Witorsch, R. J., Slayton, T. M., Yu, C. J., Lewis, A.S., and Rhomberg, L.R. (2006). An updated weight of the evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit. Rev. Toxicol. 36, 387-457.
36. Grotjan, H. E., and Johnson, D. C. (1976). Temporal variations in reproductive hormones in the immature male rat. Proc. Soc. Exp. Biol. Med. 152, 381-384.
37. Grün, F. (2010). Obesogens. Curr. Opin. Endocrinol. Diabetes Obes. 17, 453-459.
38. Hassouna, R., Zizzari, P., and Tolle, V. (2010). The ghrelin/obestatin balance in the physiological and pathological control of growth hormone secretion, body composition and food intake. J. Neuroendocrinol. 22, 793-804.
39. Howdeshell, K. L., Furr, J., Lambright, C. R., Wilson, V. S., Ryan, B. C., and Gray, L. E., Jr. (2008). Gestational and lactational exposure to ethinyl estradiol, but not bisphenol A, decreases androgen-dependent reproductive organ weights and epididymal sperm abundance in the male long evans hooded rat. Toxicol. Sci. 102, 371-382.
40. Howdeshell, K. L., Peterman, P. H., Judy, B. M., Taylor, J. A., Orazio, C. E., Ruhlen, R. L., Vom Saal, F.S., and Welshons, W.V. (2003). Bisphenol A is released from used polycarbonate animal cages into water at room temperature. Environ. Health Perspect. 111, 1180-1187.
41. Hunt, P. A., Susiarjo, M., Rubio, C., and Hassold, T. J. (2009). The bisphenol A experience: a primer for the analysis of environmental effects on mammalian reproduction. Biol. Reprod. 81, 807-813.
42. Jahn-Eimermacher, A., Lasarzik, I., and Raber, J. (2011). Statistical analysis of latency outcomes in behavioral experiments. Behav. Brain Res. 221, 271-275.
43. Kalbfleisch, J. D., and Prentice, R. L. (2002). The Statistical Analysis of Failure Time Data. 2nd ed.. Wiley-Interscience, Hoboken, NJ.
44. Kalra, P. S., and Kalra, S. P. (1977). Circadian periodicities of serum androgens, progesterone, gonadotropins and luteinizing hormone-releasing hormone in male rats: the effects of hypothalamic deafferentation, castration and adrenalectomy. Endocrinology 101, 1821-1827.
45. Kang, J. H., Kondo, F., and Katayama, Y. (2006). Human exposure to bisphenol A. Toxicology 226, 79-89.
46. Kim, J. C., Shin, H. C., Cha, S. W., Koh, W. S., Chung, M. K., and Han, S. S. (2001). Evaluation of developmental toxicity in rats exposed to the environmental estrogen bisphenol A during pregnancy. Life Sci. 69, 2611-2625.
47. Kwon, S., Stedman, D. B., Elswick, B. A., Cattley, R. C., and Welsch, F. (2000). Pubertal development and reproductive functions of Crl:CD BR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol. Sci. 55, 399-406.
48. Lakind, J. S., and Naiman, D. Q. (2008). Bisphenol A (BPA) daily intakes in the United States: estimates from the 2003-2004 NHANES urinary BPA data. J. Expo. Sci. Environ. Epidemiol. 18, 608-615.
49. Latendresse, J. R., Bucci, T. J., Olson, G., Mellick, P., Weis, C. C., Thorn, B., Newbold, R.R., and Delclos, K.B. (2009). 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. 28, 342-353.
50. Li, A. A., Baum, M. J., McIntosh, L. J., Day, M., Liu, F., and Gray, L. E., Jr. (2008). Building a scientific framework for studying hormonal effects on behavior and on the development of the sexually dimorphic nervous system. Neurotoxicology 29, 504-519.
51. Littell, R. C., Milliken, G. A., Stroup, W. W., and Wolfinger, R. (1996). SAS System for Mixed Models. SAS Publishing, Cary, NC.
52. Maccari, S., and Morley-Fletcher, S. (2007). Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32(Suppl. 1), S10-S15.
53. Matta, S. G., and Elberger, A. J. (2007). Combined exposure to nicotine and ethanol throughout full gestation results in enhanced acquisition of nicotine self-administration in young adult rat offspring. Psychopharmacology (Berl.) 193, 199-213.
54. Mock, E. J., Norton, H. W., and Frankel, A. I. (1978). Daily rhythmicity of serum testosterone concentration in the male laboratory rat. Endocrinology 103, 1111-1121.
55. Monje, L., Varayoud, J., Luque, E. H., and Ramos, J. G. (2007). Neonatal exposure to bisphenol A modifies the abundance of estrogen receptor alpha transcripts with alternative 5'-untranslated regions in the female rat preoptic area. J. Endocrinol. 194, 201-212.
56. Morris, J. A., Jordan, C. L., and Breedlove, S. M. (2004). Sexual differentiation of the vertebrate nervous system. Nat. Neurosci. 7, 1034-1039.
57. Myers, M. G., Jr, Leibel, R. L., Seeley, R. J., and Schwartz, M. W. (2010). Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol. Metab. 21, 643-651.
58. Nakamura, D., Yanagiba, Y., Duan, Z., Ito, Y., Okamura, A., Asaeda, N., Tagawa, Y., Li, C., Taya, K., Zhang, S.Y., et al. (2010). Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol. Toxicol. Lett. 194, 16-25.
59. National Research Council, 1996 National Research Council. (1996). Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington, DC.
60. National Toxicology Program. (2010). Multigenerational Reproductive Toxicology Study of Ethinyl Estradiol (CAS No. 57-63-6) in Sprague-Dawley Rats[SE16]. Research Triangle Park, NC. Available at: http://ntp.niehs.nih.-gov/ntp/htdocs/LT_rpts/TR547.pdf. Accessed June 22, 2011.
61. Newbold, R. R. (2010). Impact of environmental endocrine disrupting chemicals on the development of obesity. Hormones (Athens) 9, 206-217.
62. Newbold, R. R., Padilla-Banks, E., and Jefferson, W. N. (2009). Environmental estrogens and obesity. Mol. Cell Endocrinol. 304, 84-89.
63. Palanza, P., Gioiosa, L., vom Saal, F. S., and Parmigiani, S. (2008). Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ. Res. 108, 150-157.
64. Palanza, P. L., Howdeshell, K. L., Parmigiani, S., and vom Saal, F. S. (2002). Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ. Health Perspect. 110(Suppl. 3), 415-422.
65. Richter, C. A., Birnbaum, L. S., Farabollini, F., Newbold, R. R., Rubin, B. S., Talsness, C. E., Vandenbergh, G., Walser-Kuntz, D.R., and vom Saal, F.S. (2007). In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24, 199-224.
66. Ryan, B. C. (2005). Developmental exposure to environmental estrogens alters adult behavior in female rodents. Dissertation, North Carolina State University, Raleigh, NC.
67. Ryan, B. C., Hotchkiss, A. K., Crofton, K. M., and Gray, L. E., Jr. (2010). In utero and lactational exposure to bisphenol A, in contrast to ethinyl estradiol, does not alter sexually dimorphic behavior, puberty, fertility, and anatomy of female LE rats. Toxicol. Sci. 114, 133-148.
68. Sahambi, S. K., Pelland, A., Cooke, G. M., Schrader, T., Tardif, R., Charbonneau, M., Krishnan, K., Haddad, S., Cyr, D.G., and Devine, P.J. (2010). Oral p-tert-octylphenol exposures induce minimal toxic or estrogenic effects in adult female Sprague-Dawley rats. J. Toxicol. Environ. Health A 73, 607-622.
69. Sawaki, M., Noda, S., Muroi, T., Mitoma, H., Takakura, S., Sakamoto, S., and Yamasaki, K. (2003). In utero through lactational exposure to ethinyl estradiol induces cleft phallus and delayed ovarian dysfunction in the offspring. Toxicol. Sci. 75, 402-411.
70. Scientific Panel on Food Additives F, Processing Aids and Materials in Contact with Food. (2006). Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food on a request from the commission related to bisphenol A. EFSA J 7, 1-75.
71. Somm, E., Schwitzgebel, V. M., Toulotte, A., Cederroth, C. R., Combescure, C., Nef, S., Aubert, M.L., and Hüppi, P.S. (2009). Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ. Health Perspect. 117, 1549-1555.
72. Stoker, T. E., Gibson, E. K., and Zorrilla, L. M. (2010). Triclosan exposure modulates estrogen-dependent responses in the female Wistar rat. Toxicol. Sci. 117, 45-53.
73. Stump, D. G., Beck, M. J., Radovsky, A., Garman, R. H., Freshwater, L. L., Sheets, L. P., Marty, M.S., Waechter, J.M., Jr., Dimond, S.S., Van Miller, J.P., et al. (2010). Developmental neurotoxicity study of dietary bisphenol A in Sprague-Dawley rats. Toxicol. Sci. 115, 167-182.
74. Suzuki, K., Simpson, K. A., Minnion, J. S., Shillito, J. C., and Bloom, S. R. (2010). The role of gut hormones and the hypothalamus in appetite regulation. Endocr. J. 57, 359-372.
75. Takagi, H., Shibutani, M., Masutomi, N., Uneyama, C., Takahashi, N., Mitsumori, K., and Hirose, M. (2004). Lack of maternal dietary exposure effects of bisphenol A and nonylphenol during the critical period for brain sexual differentiation on the reproductive/endocrine systems in later life. Arch. Toxicol. 78, 97-105.
76. Taxvig, C., Vinggaard, A. M., Hass, U., Axelstad, M., Metzdorff, S., and Nellemann, C. (2008). Endocrine-disrupting properties in vivo of widely used azole fungicides. Int. J. Androl. 31, 170-177.
77. Tinwell, H., Haseman, J., Lefevre, P. A., Wallis, N., and Ashby, J. (2002). Normal sexual development of two strains of rat exposed in utero to low doses of bisphenol A. Toxicol. Sci. 68, 339-348.
78. Tominaga, T., Negishi, T., Hirooka, H., Miyachi, A., Inoue, A., Hayasaka, I., and Yoshikawa, Y. (2006). Toxicokinetics of bisphenol A in rats, monkeys and chimpanzees by the LC-MS/MS method. Toxicology 226, 208-217.
79. Tyl, R. W., Myers, C.B., Marr, M.C., Thomas, B.F., Keimowitz, A.R., Brine, D.R., Veselica, M.M., Fail, P.A., Chang, T.Y., Seely, J.C., et al. (2002). Three-generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley rats. Toxicol. Sci. 68, 121-146.
80. von Goetz, N., Wormuth, M., Scheringer, M., and Hungerbü hler, K. (2010). Bisphenol a: how the most relevant exposure sources contribute to total consumer exposure. Risk Anal. 30, 473-487.
81. Weinstock, M. (2001). Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog. Neurobiol. 65, 427-451.
82. Wolstenholme, J. T., Rissman, E. F., and Connelly, J. J. (2011). The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm. Behav. 59, 296-305.
83. Xiao, Q., Li, Y., Ouyang, H., Xu, P., and Wu, D. (2006). High-performance liquid chromatographic analysis of bisphenol A and 4-nonylphenol in serum, liver and testis tissues after oral administration to rats and its application to toxicokinetic study. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 830, 322-329.