Low-dose effects of Bisphenol a on early sexual development in male and female rats

Reproduction

Volumn 147, Issue 4, 2014, Pages 477-487

  Christiansen, Sofie ^a   Axelstad, Marta ^a   Boberg, Julie ^a   Vinggaard, Anne Marie ^a   Pedersen, Gitte Alsing ^a   Hass, Ulla ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOGENITAL DISTANCE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG SURVEILLANCE PROGRAM; FEEDING; FEMALE; GESTATIONAL AGE; LACTATION; MALE; NEWBORN; NIPPLE MALFORMATION; NONHUMAN; PREGNANCY; PRENATAL DEVELOPMENT; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; RAT; SEXUAL DEVELOPMENT; YOUNG ADULT; ANIMAL; BRAIN; DRUG EFFECTS; EMBRYOLOGY; PATHOPHYSIOLOGY; PRENATAL EXPOSURE; REPRODUCTION; SEX DETERMINATION PROCESS; SEXUAL MATURATION; TOXICITY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BENZHYDRYL COMPOUNDS; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; MALE; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; REPRODUCTION; SEX DETERMINATION PROCESSES; SEXUAL MATURATION;

EID: 84896374277     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0377     Document Type: Article

References (79)

1. ANSES 2011 French Agency for Food, Environmental and Occupational Health & Safety Collective expert report. Health effects of Bisphenol A.
2. Ashby J, Tinwell H & Haseman J 1999 Lack of effects for low dose levels of bisphenol A and diethylstilbestrol on the prostate gland of CF1 mice exposed in utero. Regulatory Toxicology and Pharmacology 30 156-166. (doi:10.1006/rtph.1999.1317) (Pubitemid 29517469)
3. Ayyanan A, Laribi O, Schuepbach-Mallepell S, Schrick C, Gutierrez M, Tanos T, Lefebvre G, Rougemont J, Yalcin-Ozuysal O & Brisken C 2011 Perinatal exposure to bisphenol A increases adult mammary gland progesterone response and cell number. Molecular Endocrinology 25 1915-1923. (doi:10.1210/me.2011-1129)
4. Bonefeld-Jorgensen EC, Long M, Hofmeister MV & Vinggaard AM 2007 Endocrine-disrupting potential ofbisphenolA, bisphenolA dimethacrylate, 4-n-nonylphenol, and 4-n-octylphenolin vitro: new data and a brief review. Environmental Health Perspectives 115 69-76. (doi:10.1289/ehp. 9368)
5. Bongiovanni AM & Kellenbenz G 1962 The adrenogenital syndrome with deficiency of 3b-hydroxysteroid dehydrogenase. Journal of Clinical Investigation 41 2086-2092. (doi:10.1172/JCI104666)
6. Bowman CJ, Barlow NJ, Turner KJ, Wallace DG & Foster PM 2003 Effects of in utero exposure to finasteride on androgen-dependent reproductive development in the male rat. Toxicological Sciences 74 393-406. (doi:10.1093/toxsci/kfg128) (Pubitemid 36958308)
7. Casanova M, You L, Gaido KW, Archibeque-Engle S, Janszen DB & Heck HA 1999 Developmental effects of dietary phytoestrogens in Sprague-Dawley rats and interactions of genistein and daidzein with rat estrogen receptors a and b in vitro. Toxicological Sciences 51 236-244. (doi:10.1093/toxsci/51.2.236) (Pubitemid 29496230)
8. Chapin RE, Adams J, Boekelheide K, Gray LE, Hayward SW, Lees PSJ, McIntyre BS, Portier KM, Schnorr TM, Selevan SG et al. 2008 NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Research. Part B, Developmental and Reproductive Toxicology 83 157-395. (doi:10.1002/bdrb.20147) (Pubitemid 352002664)
9. Chitra KC, Latchoumycandane C & Mathur PP 2003 Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology 185 119-127. (doi:10.1016/S0300-483X (02) 00597-8) (Pubitemid 36050735)
10. Christiansen S, Scholze M, Axelstad M, Boberg J, Kortenkamp A & Hass U 2008 Combined exposure to anti-androgens causes markedly increased frequencies of hypospadias in the rat. International Journal of Andrology 31 241-248. (doi:10.1111/j.1365-2605.2008.00866.x)
11. Christiansen S, Scholze M, Dalgaard M, Vinggaard AM, Axelstad M, Kortenkamp A & Hass U 2009 Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environmental Health Perspectives 117 1839-1846. (doi:10.1289/ehp. 0900689)
12. Christiansen S, Boberg J, Axelstad M, Dalgaard M, Vinggaard AM, Metzdorff S & Hass U 2010 Low-dose perinatal exposure to di (2-ethylhexyl) phthalate induces anti-androgenic effects in male rats. Reproductive Toxicology 30 313-321. (doi:10.1016/j.reprotox.2010. 04.005)
13. Christiansen S, Kortenkamp A, Axelstad M, Boberg J, Scholze M, Jacobsen PR, Faust M, Lichtensteiger W, Schlumpf M, Burdorf A et al. 2012 Mixtures of endocrine disrupting contaminants modeled on human high end exposures: an exploratory study in rats. International Journal of Andrology 35 303-316. (doi:10.1111/j.1365-2605.2011.01242.x)
14. Clark RL, Antonello JM, Grossman SJ, Wise LD, Anderson C, Bagdon WJ, Prahalada S, MacDonald JS & Robertson RT 1990 External genitalia abnormalities in male rats exposed in utero to finasteride, a 5a-reductase inhibitor. Teratology 42 91-100. (doi:10.1002/tera.1420420111) (Pubitemid 20227615)
15. Delclos KB, Weis CC, Bucci TJ, Olson G, Mellick P, Sadovova N, Latendresse JR, Thorn B & Newbold RR 2009 Overlapping but distinct effects of genistein and ethinyl estradiol (EE2) in female Sprague-Dawley rats in multigenerational reproductive and chronic toxicity studies. Reproductive Toxicology 27 117-132. (doi:10.1016/j.reprotox.2008.12.005)
16. Della Seta D, Minder I, Dessi-Fulgheri F & Farabollini F 2005 Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Research Bulletin 65 255-260. (doi:10.1016/j.brainresbull. 2004.11.017) (Pubitemid 40461971)
17. EFSA 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 2, 2-bis (4-hydroxyphenyl) propane (Bisphenol A). EFSA Journal 428 1-75.
18. EFSA 2008 Toxicokinetics of Bisphenol A - Scientific Opinion of the Panel on Food additives, Flavourings, Processing aids and Materials in Contact with Food, question number EFSA-Q-2008-382. EFSA Journal.
19. EFSA 2010 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, question number EFSA-Q-2009-00864, EFSA-Q-2010-01023, EFSA-Q-2010-00709, adopted on 23 September 2010. EFSA Journal 8 1829.
20. EFSA 2013 DRAFT Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs. 1-314. EFSA.
21. Eisenberg ML, Hsieh MH, Walters RC, Krasnow R & Lipshultz LI 2011 The relationship between anogenital distance, fatherhood, and fertility in adult men. PLoS ONE 6 e18973. (doi:10.1371/journal.pone.0018973)
22. Eisenberg ML, Jensen TK, Walters RC, Skakkebaek NE & Lipshultz LI 2012a The relationship between anogenital distance and reproductive hormone levels in adult men. Journal of Urology 187 594-598. (doi:10.1016/j. juro.2011.10.041)
23. Eisenberg ML, Shy M, Chanc Walters R & Lipshultz LI 2012b The relationship between anogenital distance and azoospermia in adult men. International Journal of Andrology 35 726-730. (doi:10.1111/j.1365-2605.2012. 01275.x)
24. Elswick BA, Welsch F & Janszen DB 2000 Effect of different sampling designs on outcome of endocrine disruptor studies. Reproductive Toxicology 14 359-367. (doi:10.1016/S0890-6238 (00) 00092-7) (Pubitemid 30610119)
25. Farris EJ 1949 Breeding of the rat. In The Rat in Laboratory Investigation, Farris EJ, Griffith JQ (eds). pp 1-18. New York: Hafner Publishing Company.
26. Gioiosa L, Fissore E, Ghirardelli G, Parmigiani S & Palanza P 2007 Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Hormones and Behavior 52 307-316. (doi:10.1016/j.yhbeh.2007. 05.006) (Pubitemid 47267910)
27. Golub MS, Wu KL, Kaufman FL, Li LH, Moran-Messen F, Zeise L, Alexeeff GV & Donald JM 2010 Bisphenol A: developmental toxicity from early prenatal exposure. Birth Defects Research. Part B, Developmental and Reproductive Toxicology 89 441-466. (doi:10.1002/bdrb.20275)
28. Gonçalves CR, Cunha RW, Barros DM & Martinez PE 2010 Effects of prenatal and postnatal exposure to a low dose of bisphenol A on behavior and memory in rats. Environmental Toxicology and Pharmacology 30 195-201. (doi:10.1016/j.etap. 2010.06.003)
29. Gray LE Jr, Wolf C, Lambright C, Mann P, Price M, Cooper RL & Ostby J 1999 Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p, p'-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat. Toxicology and Industrial Health 15 94-118. (doi:10.1191/074823399678846664) (Pubitemid 30484120)
30. Gupta C 2000 Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals. Proceedings of the Society for Experimental Biology and Medicine 224 61-68. (doi:10.1046/j.1525-1373.2000. 22402.x) (Pubitemid 30314397)
31. Hass U, Scholze M, Christiansen S, Dalgaard M, Vinggaard AM, Axelstad M, Metzdorff SB & Kortenkamp A 2007 Combined exposure to anti-androgens exacerbates disruption of sexual differentiation in the rat. Environmental Health Perspectives 115 (Suppl 1) 122-128. (doi:10.1289/ehp. 9360)
32. Honma S, Suzuki A, Buchanan DL, Katsu Y, Watanabe H & Iguchi T 2002 Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reproductive Toxicology 16 117-122. (doi:10.1016/S0890-6238 (02) 00006-0) (Pubitemid 34457183)
33. Hotchkiss AK, Parks-Saldutti LG, Ostby JS, Lambright C, Furr J, Vandenbergh JG & Gray LE Jr 2004 A mixture of the "antiandrogens" linuron and butyl benzyl phthalate alters sexual differentiation of the male rat in a cumulative fashion. Biology of Reproduction 71 1852-1861. (doi:10.1095/biolreprod.104.031674) (Pubitemid 39586929)
34. Howdeshell KL, Furr J, Lambright CR, Wilson VS, Ryan BC & Gray LE 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. Toxicological Sciences 102 371-382. (doi:10.1093/toxsci/kfm306) (Pubitemid 351404908)
35. Hsieh MH, Breyer BN, Eisenberg ML & Baskin LS 2008 Associations among hypospadias, cryptorchidism, anogenital distance, and endocrine disruption. Current Urology Reports 9 132-142. (doi:10.1007/s11934-008-0025-0) (Pubitemid 351480794)
36. Jacobsen PR, Axelstad M, Boberg J, Isling LK, Christiansen S, Mandrup KR, Berthelsen LO, Vinggaard AM & Hass U 2012 Persistent developmental toxicity in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reproductive Toxicology 34 237-250. (doi:10.1016/j.reprotox.2012.05. 099)
37. Kanno J, Onyon L, Haseman J, Fenner-Crisp P, Ashby J & Owens W 2001 The OECD program to validate the rat uterotrophic bioassay to screen compounds for in vivo estrogenic responses: phase 1. Environmental Health Perspectives 109 785-794. (doi:10.1289/ehp. 01109785) (Pubitemid 32910300)
38. Kobayashi K, Kubota H, Ohtani K, Hojo R & Miyagawa M 2012 Lack of effects for dietary exposure of bisphenol A during in utero and lactational periods on reproductive development in rat offspring. Journal of Toxicological Sciences 37 565-573. (doi:10.2131/jts.37.565)
39. Levy JR, Faber KA, Ayyash L & Hughes CL Jr 1995 The effect of prenatal exposure to the phytoestrogen genistein on sexual differentiation in rats. Proceedings of the Society for Experimental Biology and Medicine 2008 60-66.
40. Liao C & Kannan K 2011 Widespread occurrence of bisphenol A in paper and paper products: implications for human exposure. Environmental Science & Technology 45 9372-9379. (doi:10.1021/es202507f)
41. Mandrup KR, Jacobsen PR, Isling LK, Axelstad M, Dreisig K, Hadrup N, Vinggaard AM, Hass U & Boberg J 2013 Effects of perinatal ethinyl estradiol exposure in male and female Wistar rats. Reproductive Toxicology 42 C 180-191. (doi:10.1016/j.reprotox.2013.09.001)
42. Mendiola J, Stahlhut RW, Jørgensen N, Liu F & Swan SH 2011 Shorter anogenital distance predicts poorer semen quality in young men in Rochester, New York. Environmental Health Perspectives 119 958-963. (doi:10.1289/ehp. 1103421)
43. Metzdorff SB, Dalgaard M, Christiansen S, Axelstad M, Hass U, Kiersgaard MK, Scholze M, Kortenkamp A & Vinggaard AM 2007 Dysgenesis and histological changes of genitals and perturbations of gene expression in male rats after in utero exposure to antiandrogen mixtures. Toxicological Sciences 98 87-98. (doi:10.1093/toxsci/kfm079) (Pubitemid 47073823)
44. Miao M, Yuan W, He Y, Zhou Z, Wang J, Gao E, Li G & Li DK 2011 In utero exposure to bisphenol-A and anogenital distance of male offspring. Birth Defects Research. Part A, Clinical and Molecular Teratology 91 867-872. (doi:10.1002/bdra.22845)
45. Munoz-de-Toro M, Markey CM, Wadia PR, Luque EH, Rubin BS, Sonnenschein C & Soto AM 2005 Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 146 4138-4147. (doi:10.1210/en. 2005-0340) (Pubitemid 41175786)
46. Nagel SC, Vom SF, Thayer KA, Dhar MG, BoechlerM& Welshons WV1997 Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol [see comments]. Environmental Health Perspectives 105 70-76. (doi:10.1289/ehp. 9710570)
47. OECD 2012 Test No. 443: Extended One-Generation Reproductive Toxicity Study, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing. (doi:10.1787/9789264185371-en)
48. OECD 2013 Guidance Document 151. In support of OECD Test Guideline 443 on an extended one generation reproductive toxicity study. OECD.
49. Ostby JS & Gray LE 2004 Transgenerational (in utero/lactational) exposure to investigate the effects of endocrine disrupting compounds (EDCs) in rats. Current Protocols in Toxicology. Chapter 16: Unit 16. 8. (doi:10.1002/0471140856.tx1608s19)
50. Ostby J, Kelce WR, Lambright C, Wolf CJ, Mann P & Gray LE Jr 1999 The fungicide procymidone alters sexual differentiation in the male rat by acting as an androgen-receptor antagonist in vivo and in vitro. Toxicology and Industrial Health 15 80-93. (Pubitemid 30484119)
51. Paris F, Balaguer P, Térouanne B, Servant N, Lacoste C, Cravedi JP, Nicolas JC & Sultan C 2002 Phenylphenols, biphenols, bisphenol-A and 4-tert-octylphenol exhibit a and b estrogen activities and antiandrogen activity in reporter cell lines. Molecular and Cellular Endocrinology 193 43-49. (doi:10.1016/S0303-7207 (02) 00094-1) (Pubitemid 34823606)
52. Parks LG, Ostby JS, Lambright CR, Abbott BD, Klinefelter GR, Barlow NJ & Gray LE Jr 2000 The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicological Sciences 58 339-349. (doi:10.1093/toxsci/58.2.339) (Pubitemid 32042432)
53. Prins GS & Korach KS 2008 The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids 73 233-244. (doi:10.1016/j.steroids.2007.10.013)
54. Prins GS, Ye SH, Birch L, Ho SM & Kannan K 2011 Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reproductive Toxicology 31 1-9. (doi:10.1016/j.reprotox.2010.09.009)
55. Reif DM, Martin MT, Tan SW, Houck KA, Judson RS, Richard AM, Knudsen TB, Dix DJ & Kavlock RJ 2010 Endocrine profiling and prioritization of environmental chemicals using ToxCast data. Environmental Health Perspectives 118 1714-1720. (doi:10.1289/ehp. 1002180)
56. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR & vom Saal FS 2007 In vivo effects of bisphenol A in laboratory rodent studies. Reproductive Toxicology 24 199-224. (doi:10.1016/j.reprotox.2007.06.004) (Pubitemid 47385096)
57. Rubin BS, Murray MK, Damassa DA, King JC & Soto AM 2001 Perinatal exposure to low doses of bisphenol A affects bodyweight, patterns of estrous cyclicity, and plasma LH levels. Environmental Health Perspectives 109 657-680.
58. Ryan BC & Vandenbergh JG 2006 Developmental exposure to environmental estrogens alters anxiety and spatial memory in female mice. Hormones and Behavior 50 85-93. (doi:10.1016/j.yhbeh.2006.01.007) (Pubitemid 43776845)
59. Ryan BC, Hotchkiss AK, Crofton KM & Gray LE 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. Toxicological Sciences 114 133-148. (doi:10.1093/toxsci/kfp266)
60. vom Saal FS, Nagel SC, Coe BL, Angle BM & Taylor JA 2012 The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Molecular and Cellular Endocrinology 354 74-84. (doi:10.1016/j.mce.2012.01.001)
61. Sakaue M, Ohsako S, Ishimura R, Kurosawa S, Kurohmaru M, Hayashi Y, Aoki Y, Yonemoto J & Tohyama C 2001 Bisphenol-A affects spermatogenesis in the adult rat even at a low dose. Journal of Occupational Health 43 185-190. (doi:10.1539/joh.43.185) (Pubitemid 32785817)
62. Salian S, Doshi T & Vanage G 2009 Perinatal exposure of rats to bisphenol A affects the fertility of male offspring. Life Sciences 85 742-752. (doi:10.1016/j.lfs.2009.10.004)
63. Salian S, Doshi T & Vanage G 2011 Perinatal exposure of rats to bisphenol A affects fertility of male offspring an overview. Reproductive Toxicology 31 359-362. (doi:10.1016/j.reprotox.2010.10.008)
64. Sánchez P, Castro B, Torres JM, Olmo A, Moral R & Ortega E 2013 Bisphenol A modifies the regulation exerted by testosterone on 5a-reductase isozymes in ventral prostate of adult rats. BioMed Research International 2013 1-7. (doi:10.1155/2013/629235)
65. Shelby MD 2008 NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. NTP CERHR. NTP CERHR MON, vii-ix, 1-64 passim.
66. Swan SH 2008 Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environmental Research 108 177-184. (doi:10.1016/j.envres.2008.08.007)
67. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, Mao CS, Redmon JB, Ternand CL, Sullivan S et al. 2005 Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environmental Health Perspectives 113 1056-1061. (doi:10.1289/ehp. 8100) (Pubitemid 41149638)
68. Talsness C, Fialkowski O, Gericke C, Merker HJ & Chahoud I 2000 The effects of low and high doses of bisphenol A on the reproductive system of female and male rat offspring. Congenital Anomalies 40 S94-S107.
69. Timms BG, Howdeshell KL, Barton L, Bradley S, Richter CA & vom Saal FS 2005 Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. PNAS 102 7014-7019. (doi:10.1073/pnas.0502544102) (Pubitemid 40675432)
70. Tyl RW, Myers CB, Marr MC, Thomas BF, Keimowitz AR, Brine DR, Veselica MM, Fail PA, Chang TY, Seely JC et al. 2002 Three-generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley rats. Toxicological Sciences 68 121-146. (doi:10.1093/toxsci/68.1.121) (Pubitemid 34785236)
71. Tyl RW, Myers CB, Marr MC, Sloan CS, Castillo NP, Veselica MM, Seely JC, Dimond SS, Van Miller JP, Shiotsuka RN et al. 2008 Two-generation reproductive toxicity study of dietary bisphenol A in CD-1 (Swiss) mice. Toxicological Sciences 104 362-384. (doi:10.1093/toxsci/kfn084) (Pubitemid 352038259)
72. US FDA 2008 Draft assessment of bisphenol A for use in food contact applications. Available on-line at: www.fda.gov, 1-105.
73. US FDA 2010 Update on Bisphenol A for Use in Food Contact Applications U. S. Food and Drug Administration. US FDA. Available on-line at: www.fda.gov, 1-7. http://www.fda.gov/downloads/NewsEvents/Public HealthFocus/UCM197778.pdf.
74. Vinggaard AM, Korner W, Lund KH, Bolz U & Petersen JH 2000 Identification and quantification of estrogenic compounds in recycled and virgin paper for household use as determined by an in vitro yeast estrogen screen and chemical analysis. Chemical Research in Toxicology 13 1214-1222. (doi:10.1021/tx000146b) (Pubitemid 32104000)
75. Vom SF, Cooke PS, Buchanan DL, Palanza P, Thayer KA, Nagel SC, Parmigiani S & Welshons WV 1998 A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicology and Industrial Health 14 239-260. (doi:10.1177/0748233 79801400115) (Pubitemid 28044978)
76. Welsh M, Saunders P, Fisken M, Scott HM, Hutchison GR, Smith L & Sharpe RM 2008 Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. Journal of Clinical Investigation 118 1479-1490. (doi:10.1172/JCI34241) (Pubitemid 351500441)
77. Welsh M, MacLeod DJ, Walker M, Smith LB & Sharpe RM 2010 Critical androgen-sensitive periods of rat penis and clitoris development. International Journal of Andrology 33 e144-e152. (doi:10.1111/j.1365-2605.2009.00978.x)
78. WHO 2011 Toxicological and Health Aspects of Bisphenol A. Report of joint FAO/WHO expert meeting (p. 1-60). Ottawa Canada, November, 2010. World Health Organisation, 2011. ISBN 978 92 14 156427 4. Available online at: who.int. Ref Type: Report.
79. Zhang X, Chang H, Wiseman S, He Y, Higley E, Jones P, Wong CKC, Al-Khedhairy A, Giesy JP & Hecker M 2011 Bisphenol A disrupts steroidogenesis in human H295R cells. Toxicological Sciences 121 320-327. (doi:10.1093/toxsci/kfr061)