226
Views
4
CrossRef citations to date
0
Altmetric
Original Articles

Windows of sensitivity to toxic chemicals in the development of reproductive effects: an analysis of ATSDR’s toxicological profile database

, , &
Pages 553-578 | Received 04 Apr 2018, Accepted 29 Jun 2018, Published online: 19 Jul 2018

References

  • Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. 1989. Molecular biology of the cell. In: Control of gene expression. 2nd ed. New York: Garland Publishing, Inc.; p. 690–693.
  • Al-Hamood MH, Elbetieha A, Bataineh H. 1998. Sexual maturation and fertility of male and female mice exposed prenatally and postnatally to trivalent and hexavalent chromium compounds. Reprod Fertil Dev. 10:179–183.
  • Ambrose AM, Christenson HC, Robbins DJ, Rather LJ. 1953. Toxicological and pharmacological studies on chlordane. Archives of Industrial Hygiene and Occupational Medicine. 7:197–210.
  • Ambrose AM, Larson PS, Borzelleca JF, Hennigar GR Jr. 1970. Toxicologic studies on diethyl-1-(2,4-dichlorophenyl)-2-chlorovinyl phosphate. Toxicol Appl Pharmacol. 17:323–336.
  • Aoyama H, Hojo H, Takahashi KL, Shimizu N, Araki M, Harigae M, Tanaka N, Shirasaka N, Kuwahara M, Nakashima N, et al. 2005. A two-generation reproductive toxicity study of 2,4dichlorophenol in rats. J Toxicol Sci 30 Spec. 59–78.
  • Argus. 1997. Oral (gavage) two-generation (one litter per generation) reproduction study of pentachlorophenol in rats. Horsham (PA): Argus Research Laboratories, Inc.
  • Arias E, MacDorman MF, Strobino DM, Guyer B. 2003. Annual summary of vital statistics–2002. Pediatrics. 112(6 Pt 1):1215–1230.
  • Arnault E, Doussau M, Pesty A, Gouget B, Van der Meeren A, Fouchet P, Lefevre B. 2008. Natural uranium disturbs mouse folliculogenesis in vivo and oocyte meiosis in vitro. Toxicology. 247(2–3):80–87.
  • Arrebola JP, Molina-Molina JM, Fernández MF, Saenz JM, Amaya E, Indiveri P, Hill EM, Scholze M, Orton F, Kortenkamp A, et al. 2015. A novel biomarker for anti-androgenic activity in placenta reveals risks of urogenital malformations. Reproduction. 149(6):605–613.
  • ASRM (American Society for Reproductive Medicine) 2017. Quick facts about infertility.[accessed 2017 October 13]. www.asrm.org
  • [ATSDR] Agency for Toxic Substances and Disease Registry. 2018. Framework for Assessing Health Impacts of Multiple Chemicals and Other Stressors (Update). [Accessed 2018 June 01]. https://www.atsdr.cdc.gov/interactionprofiles/ip-ga/ipga.pdf
  • Banu SK, Samuel JB, Arosh JA, Burghardt RC, Aruldhas MM. 2008. Lactational exposure to hexavalent chromium delays puberty by impairing ovarian development, steroidogenesis and pituitary hormone synthesis in developing Wistar rats. Toxicol Appl Pharmacol. 232(2):180–189.
  • Basharova GR. 1996. Reproduction in families of workers exposed to 2,4,5-T intoxication. Organohalogen compounds. 30:315–318.
  • Bell DR, Clode S, Fan MQ, Fernandes A, Foster PM, Jiang T, Loizou G, MacNicoll A, Miller BG, Rose M, et al. 2007a. Toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the developing male Wistar(Han) rat. I: No decrease in epididymal sperm count after a single acute dose. Toxicol Sci. 99(1):214–223.
  • Bell DR, Clode S, Fan MQ, Fernandes A, Foster PM, Jiang T, Loizou G, MacNicoll A, Miller BG, Rose M, et al. 2007b. Toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the developing male Wistar(Han) rat. II: Chronic dosing causes developmental delay. Toxicol Sci. 99(1):224–233.
  • Bellinger DC. 2005. Teratogen update: lead and pregnancy. Birth Defects Res A Clin Mol Teratol. 73(6):409–420.
  • Bellingham M, Fowler PA, Amezaga MR, Rhind SM, Cotinot C, Mandon-Pepin B, Sharpe RM, Evans NP. 2009. Exposure to a complex cocktail of environmental endocrine-disrupting compounds disturbs the kisspeptin/GPR54 system in ovine hypothalamus and pituitary gland. Environ Health Perspect. 117(10):1556–1562.
  • Bellingham M, Fowler PA, MacDonald ES, Mandon-Pepin B, Cotinot C, Rhind S, Sharpe RM, Evans NP. 2016. Timing of maternal exposure and foetal sex determine the effects of low-level chemical mixture exposure on the foetal neuroendocrine system in sheep. J Neuroendocrinol. 28(12):1–11.
  • Bjerke DL, Peterson RE. 1994. Reproductive toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in male rats: different effects of in utero versus lactational exposure. Toxicol Appl Pharmacol. 127:241–249.
  • Bjerke DL, Sommer RJ, Moore RW, Peterson RE. 1994. Effects of in utero and lactational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on responsiveness of the male rat reproductive system to testosterone stimulation in adulthood. Toxicol Appl Pharmacol. 127:250–257.
  • Bloom MS, Fitzgerald EF, Kim K, Neamtiu I, Gurzau ES. 2010. Spontaneous pregnancy loss in humans and exposure to arsenic in drinking water. Int J Hyg Environ Health. 213(6):401–413.
  • Bolon B, Bucci TJ, Warbritton AR, Chen JJ, Mattison DR, Heindel JJ. 1997. Differential follicle counts as a screen for chemically induced ovarian toxicity in mice: results from continuous breeding bioassays. Fundam Appl Toxicol. 39(1):1–10.
  • Brown NM, Manzolillo PA, Zhang J-X, Wang J, Lamartiniere CA. 1998. Prenatal TCDD and predisposition to mammary cancer in the rat. Carcinogenesis. 19:1623–1629.
  • Bruner-Tran KL, Osteen KG. 2011. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol. 31(3):344–350.
  • Buck Louis GM, Rios LI, McLain A, Cooney MA, Kostyniak PJ, Sundaram R. 2011. Persistent organochlorine pollutants and menstrual cycle characteristics. Chemosphere. 85(11):1742–1748.
  • Buser MC, Pohl HR. 2015. Windows of sensitivity to toxic chemicals in the development of cleft palates. J Toxicol Environ Health, Part B: Critical Reviews. 18(5):242–257.
  • Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. 1992. Evidence for decreasing quality of semen during past 50 years. BMJ. 305(6854):609–613.
  • Carlson BM. 2014. Human embryology and developmental biology. Saunders WB, Ed. 5th. Philadelphia: Saunders-Elsevier. Print.
  • Caserta D, Graziano A, Lo Monte G, Bordi G, Moscarini M. 2013. Heavy metals and placental fetal-maternal barrier: a mini-review on the major concerns. Eur Rev Med Pharmacol Sci. 17(16):2198–2206.
  • Chandra A, Copen CE, Stephen EH. 2013. Infertility and impaired fecundity in the United States, 1982–2010: data from The National Survey of Family Growth. National Health Statistics Reports. (67):1-18. Hyattsville, MD: National Center for Health Statistics.
  • Chapin RE, Harris MW, Davis BJ, Ward SM, Wilson RE, Mauney MA, Lockhart AC, Smialowicz RJ, Moser VC, Burka LT, et al. 1997. The effects of perinatal/juvenile methoxychlor exposure on adult rat nervous, immune, and reproductive system function. Fundam Appl Toxicol. 40:138–157.
  • Chernoff N, Linder RE, Scott TM, Rogers EH, Carver BD, Kavlock RJ. 1979. Fetotoxicity and cataractogenicity of mirex in rats and mice with notes on kepone. Environ Res. 18:257–269.
  • Chernoff N, Rogers EH. 1976. Fetal toxicity of kepone in rats and mice. Toxicol Appl Pharmacol. 38:189–194.
  • Cho SI, Damokosh AI, Ryan LM, Chen D, Hu YA, Smith TJ, Christiani DC, Xu X. 2001. Effects of exposure to organic solvents on menstrual cycle length. J Occup Environ Med. 43(6):567–575.
  • Cohn BA, Cirillo PM, Wolff MS, Schwingl PJ, Cohen RD, Sholtz RI, Ferrara A, Christianson RE, van den Berg BJ, Siiteri PK. 2003. DDT and DDE exposure in mothers and time to pregnancy in daughters. Lancet. 361(9376):2205–2206.
  • Colomina MT, Roig JL, Torrente M, Vicens P, Domingo JL. 2005. Concurrent exposure to aluminum and stress during pregnancy in rats: effects on postnatal development and behavior of the offspring. Neurotoxicol Teratol. 27(4):565–574.
  • Cooke GM, Tryphonas H, Pulido O, Caldwell D, Bondy GS, Forsyth D. 2004. Oral (gavage), in utero and postnatal exposure of Sprague-Dawley rats to low doses of tributyltin chloride. Part 1: toxicology, histopathology and clinical chemistry. Food Chem Toxicol. 42(2):211–220.
  • Cox K, Kyriakou A, Amjad B, O'Toole S, Flett ME, Welsh M, Ahmed SF, Cascio S. 2016. Shorter anogenital and anoscrotal distances correlate with the severity of hypospadias: a prospective study. J Pediatr Urol. S1477-5131(16):30232–30237.
  • Cragin LA, Kesner JS, Bachand AM, Barr DB, Meadows JW, Krieg EF, Reif JS. 2011. Menstrual cycle characteristics and reproductive hormone levels in women exposed to atrazine in drinking water. Environ Res. 111(8):1293–1301.
  • Dalsenter PR, Dallegrave E, Mello JR, Langeloh A, Oliveria RT, Fagi AS. 1999. Reproductive effects of endosulfan on male offspring of rats exposed during pregnancy and lactation. Hum Exp Toxicol. 18(9):583–589.
  • Dalsenter PR, Faqi AS, Webb J, Merker HJ, Chahoud I. 1997. Reproductive toxicity and toxicokinetics of lindane in the male offspring of rats exposed during lactation. Hum Exp Toxiol. 16:146–153.
  • Davis DL, Gottlieb MB, Stampnitzky JR. 1998. Reduced ratio of male to female births in several industrial countries: a sentinel health indicator? JAMA. 279(13):1018–1023.
  • De Rosa C, Richter P, Pohl H, Jones D. 1998. Environmental exposures that affect the endocrine system: public health implications. J Toxicol Environ Health, Part B: Critical Reviews. 1(1):3–26.
  • Dearth RK, Hiney JK, Srivastava V, Burdkick SB, Bratton GR, Dees WL. 2002. Effects of lead (Pb) exposure during gestation and lactation on female pubertal development in the rat. Reprod Toxicol. 16:343–352.
  • Diamanti-Kandarakis E, Bourguignon JP, Giudice LC. 2009. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr Rev. 30(4):293–342.
  • Diel P, Schmidt S, Vollmer G, Janning P, Wpmeier A, Michna H, Bolt HM, Degen GH. 2004. Comparative responses of three rat strains (DA/Han, Sprague-Dawley and Wistar) to treatment with environmental estrogens. Arch Toxicol.. 78(4):183–193.
  • Dienhart MK, Sommer RJ, Peterson RE, Hirschfield AN, Silbergeld EK. 2000. Gestational exposure to 2,3,7,8tetrachlorodibenzo-p-dioxin induces developmental defects in the rat vagina. Toxicol Sci. 56(1):141–149.
  • Dimich-Ward H, Hertzman C, Teschke K, Hershler R, Marion SA, Ostry A, Kelly S. 1996. Reproductive effects of paternal exposure to chlorophenate wood preservatives in the sawmill industry. Scand J Work Environ Health. 22:267–273.
  • Dodd DE, Fowler EH, Snellings WM, Pritts IM, Tyl RW, Lyon JP, O'Neal FO, Kimmerle G. 1987. Reproduction and fertility evaluations in CD rats following nitrobenzene inhalation. Fundam Appl Toxicol. 8:493–505.
  • EHRT. 1987. Screening of priority chemicals for reproductive hazards: benzethonium chloride (CAS No. 121-54-O); 3-ethoxy-1-propanol (CAS No. 111-35-3); acetone (CAS No. 67-64-l). Environmental Health Research and Testing, Inc. Cincinnati, OH. NTIS PB89–139083.
  • 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(5):e18973.
  • Eisenberg ML, Lipshultz LI. 2015. Anogenital distance as a measure of human male fertility. J Assist Reprod Genet. 32(3):479–484.
  • Eisenberg ML, Shy M, Walters RC, Lipshultz LI. 2012. The relationship between anogenital distance and azoospermia in adult men. Int J Androl. 35(5):726–730.
  • Ellis-Hutchings RG, Cherr GN, Hanna LA, Keen CL. 2006. Polybrominated diphenyl ether (PBDE)induced alterations in vitamin A and thyroid hormone concentrations in the rat during lactation and early postnatal development. Toxicol Appl Pharmacol. 215(2):135–145.
  • Ema M, Miyawaki E, Kawashima K. 2000a. Critical period for adverse effects on development of reproductive system in male offspring of rats given di-n-butyl phthalate during late pregnancy. Toxicol Lett. 111:271–278.
  • Ema M, Miyawaki E, Kawashima K. 2000b. Effects of dibutyl phthalate on reproductive function in pregnant and pseudopregnant rats. Reprod Toxicol. 14:13–19.
  • Eskenazi B, Warner M, Mocarelli P, Samuels S, Needham LL, Patterson DG Jr., Lippman S, Vercellini P, Gerthoux PM, Brambilla P, et al. 2002. Serum dioxin concentrations and menstrual cycle characteristics. Am J Epidemiol. 156(4):383–392.
  • Fenton SE, Hamm JT, Birnbaum LS, Youngblood GL. 2002. Persistent abnormalities in the rat mammary gland following gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci. 67(1):63–74.
  • Fernandez MF, Olmos B, Granada A, Lopez-Espinosa MJ, Molina-Molina JM, Fernandez JM, Cruz M, Olea-Serrano F, Olea N. 2007. Human exposure to endocrine-disrupting chemicals and prenatal risk factors for cryptorchidism and hypospadias: a nested case-control study. Environ Health Perspect. 115(Suppl 1):8–14.
  • Franczak A, Nynca A, Valdez KE, Mizinga KM, Petroff BK. 2006. Effects of acute and chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin on the transition to reproductive senescence in female Sprague-Dawley rats. Biol Reprod. 74(1):125–130.
  • Gellert R, Heinrichs W. 1975. Effects of DDT homologs administered to female rats during the perinatal period. Biol Neonate. 26:283–290.
  • Gellert RJ, Wilson C. 1979. Reproductive function in rats exposed prenatally to pesticides and polychlorinated biphenyls (PCB). Environ Res. 18:437–443.
  • Gill MW, Swanson MS, Murphy SR,Bailey GP. 2000. Two-generation reproduction and developmental neurotoxicity study with sodium chlorite in the rat. J Appl Toxicol. 20:291–303.
  • Grant DL, Phillips WE, Hatina GV. 1977. Effect of hexachlorobenzene on reproduction in the rat. Arch Environ Contam Toxicol. 5:207–216.
  • Grant LD, Kimmel CA, West GL, Martinez-Vargas CM, Howard JL. 1980. Chronic low-level lead toxicity in the rat: II. Effects on postnatal physical and behavioral development. Toxicol Appl Pharmacol. 56:42–58.
  • Gray LE, Wolf C, Mann P, Ostby JS. 1997. In utero exposure to low doses of 2,3,7,8-tetrachlorodibenzop-dioxin alters reproductive development of female Long Evans Hooded rat offspring. Toxicol Appl Pharmacol. 146:237–244.
  • Gray LE, Ostby J, Furr J, Price M, Veeramachaneni DN, Parks L. 2000. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci. 58:350–365.
  • Gray LE Jr., Ostby JS. 1995. In utero 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters reproductive morphology and function in female rate offspring. Tox Appl Pharm. 133:285–294.
  • Gray LE Jr, Ostby J, Ferrell J, Rehnberg G, Linder R, Cooper R, Goldman J, Slott V, Laskey J. 1989. A dose-response analysis of methoxychlor-induced alterations of reproductive development and function in the rat. Fundam Appl Toxicol. 12:92–108.
  • Gray LE, 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. Toxicol Ind Health. 15(1–2):94–118.
  • Gulati DK, Hope E, Mounce RC. 1988. Chloroform: reproduction and fertility assessment in CD-l mice when administered by gavage. Report by Environmental Health Research and Testing, Inc., Lexington, KY to National Toxicology Program, National Institute of Environmental Health Sciences, Research Triangle Park, NC.
  • Gupta C. 2000. Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals (44516). Proc Soc Exp Biol Med. 244(2):61–68.
  • Hamm TE Jr., Raynor TH, Phelps MC, Auman CD, Adams WT, Proctor JE, Wolkowski-Tyl R. 1985. Reproduction in Fischer-344 rats exposed to methyl chloride by inhalation for two generations. Fund Appl Toxicol. 5:568–577.
  • Harris SJ, Cecil HC, Bitman J. 1974. Effect of several dietary levels of technical methoxychlor on reproduction in rats. J Agric Food Chem. 22:969–973.
  • Haskell Laboratories. 1966. Three-generation study on rats with 2,2-bis(p-methoxyphenyl)-1,1,1trichloroethane (methoxychlor). Haskell Laboratory Report No. 102–166.
  • He P, Wang A, Niu Q, Guo L, Xia T, Chen X. 2011. Toxic effect of PBDE-47 on thyroid development, learning, and memory, and the interaction between PBDE-47 and PCB153 that enhances toxicity in rats. Toxicol Ind Health. 27(3):279–288.
  • Heimler I, Trewin AL, Chaffin CL, Rawlins RG, Hutz RJ. 1998. Modulation of ovarian follicle maturation and effects on apoptotic cell death in Holtzman rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in utero and lactationally. Reprod Toxicol. 12:69–73.
  • Hertz-Picciotto I. 2000. The evidence that lead increases the risk for spontaneous abortion. Am J Ind Med. 38(3):300–309.
  • Hixson EJ, Hathaway. 1986. Effect of disulfoton (DI-SYSTON) on reproduction in rats. Study No. 82-67 l-02. Report No. 90965. Mobay Corporation, Corporate Toxicology Department, Stilwell (Kansas).
  • Hsu PC, Pan MH, Li LA, Chen CJ, Tsai SS, Guo YL. 2007. Exposure in utero to 2,2ʹ,3,3ʹ,4,6ʹ- hexachlorobiphenyl (PCB 132) impairs sperm function and alters testicular apoptosis-related gene expression in rat offspring. Toxicol Appl Pharmacol. 221(1):68–75.
  • Hurst CH, Abbott B, Schmid JE, Birnbaum LS. 2002. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) disrupts early morphogenetic events that form the lower reproductive tract in female rat fetuses. Toxicol Sci. 65(1):87–98.
  • Iavicoli I, Carelli G, Stanek EJ 3rd, Castellino N, Calabrese EJ. 2004. Effects of low doses of dietary lead on puberty onset in female mice. Reprod Toxicol. 19(1):35–41.
  • Ikeda M, Mitsui T, Setani K, Tamura M, Kakeyama M, Sone H, Tohyama C, Tomita T. 2005a. In utero and lactational exposure to 2,3,7,8tetrachlorodibenzo-p-dioxin in rats disrupts brain sexual differentiation. Toxicol Appl Pharmacol. 205(1):98–105.
  • Ikeda M, Tamura M, Yamashita J, Suzuki C, Tomita T. 2005b. Repeated in utero and lactational 2,3,7,8tetrachlorodibenzo-p-dioxin exposure affects male gonads in offspring, leading to sex ratio changes in F2 progeny. Toxicol Appl Pharmacol. 206(3):351–355.
  • Inano H, Suzuki K, Ishii-Ohba H, Imada Y, Kumagai R, Kurihara S, Salto A. 1989. Steroid hormone production on testis, ovary, and adrenal gland of immature rats irradiated in utero with 60Co. Radiat Res. 117:293–303.
  • Ingber SZ, Pohl HR. 2016. Windows of sensitivity to toxic chemicals in the motor effects development. Regul Toxicol Pharmacol. 74:93–104.
  • Ishihara K, Ohsako S, Tasaka K, Harayama H, Miyake M, Warita K, Tanida T, Misuhashi T, Nanmori T, Tabuchi Y, et al. 2010. When does the sex ratio of offspring of the paternal 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) exposure decrease: in the spermatozoa stage or at fertilization? Reprod Toxicol. 29(1):68–73.
  • Ishihara K, Warita K, Tanida T, Sugawara T, Kitagawa H, Hoshi N. 2007. Does paternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) affect the sex ratio of offspring?. J Vet Med Sci. 69(4):347352.
  • Jablonska O, Shi Z, Valdez KE, Ting AY, Patroff BK. 2010. Temporal and anatomical sensitivities to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin leading to premature acyclicity with age in rats. Int J Androl. 33(2):405–412.
  • Jin MH, Hong CH, Lee HY, Kang HJ, Han SW 2010. Toxic effects of lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on development of male reproductive system: involvement of antioxidants, oxidants, and p53 protein. Environ Toxicol. 25(1):1–8.
  • Jørgensen N, Joensen UN, Jensen TK, Jensen MB, Almstrup K, Olesen IA, Juul A, Andersson AM, Carlsen E, Petersen JH, et al. 2012. Human semen quality in the new millennium: a prospective cross-sectional population-based study of 4867 men. BMJ Open. 2(4).
  • Kabir ER, Rahman MS, Rahman I. 2015. A review on endocrine disruptors and their possible impacts on human health. Environ Toxicol Pharmacol. 40(1):241–258.
  • Kakeyama M, Sone H, Tohyama C. 2008. Perinatal exposure of female rats to 2,3,7,8tetrachlorodibenzo-p-dioxin induces central precocious puberty in the offspring. J Endocrinol. 197(2):351–358.
  • Keil DE, Warren DA, Jenny MJ, EuDaly JG, Smythe J, Peden-Adams MM. 2003. Immunological function in mice exposed to JP-8 jet fuel in utero. Toxicol Sci. 76(2):347–356.
  • Kelce W, Stone C, Laws S, Gray LE, Kemppainen JA, Wilson EM. 1995. Persistent DDT metabolite p,p’-DDE is a potent androgen receptor antagonist. Nature. 375:581–585.
  • Keplinger M, Deichmann W, Sala F 1970. Effects of combinations of pesticides on reproduction in mice. In: Deichmann W, ed. Pesticide symposia. 6th-7th International-American Conference of Toxicology and Occupational Medicine, University of Miami Medical School, Miami, FL, 125–138.
  • Kodavanti PR, Coburn CG, Moser VC, MacPhail RC, Fenton SE, Stoker TE, Rayner JL, Kannan K, Birnbaum LS. 2010. Developmental exposure to a commercial PBDE mixture, DE-71: neurobehavioral, hormonal, and reproductive effects. Toxicol Sci. 116(1):297–312.
  • Kristensen SL, Ramlau-Hansen CH, Ernst E, Olsen SF, Bonde JP, Vested A, Halldorsson TI, Rantakokko P, Kiviranta H, Toft G. 2016. Prenatal exposure to persistent organochlorine pollutants and female reproductive function in young adulthood. Environ Int. 92-93:366–372.
  • Kuriyama SN, Chahoud I. 2004. In utero exposure to low-dose 2,3ʹ,4,4ʹ,- 5pentachlorobiphenyl (PCB 118) impairs male fertility and alters neurobehavior in rat offspring. Toxicology. 202(3):185–197.
  • Kuriyama SN, Talsness CE, Grote K, Chahoud I. 2005. Developmental exposure to low dose PBDE 99: effects on male fertility and neurobehavior in rat offspring. Environ Health Perspect. 113(2):149–154.
  • Lagarde F, Beausoleil C, Belcher SM, Belzunces LP, Emond C, Guerbet M, Rousselle C. 2015. Non-monotonic dose-response relationships and endocrine disruptors: a qualitative method of assessment. Environ Health. 14: 13.
  • Lea RG, Amezaga MR, Loup B, Mandon-Pepin B, Stefansdottir A, Filis P, Kyle C, Zhang Z, Allen C, Pudrie L, Jouneau L, et al. 2016. The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals. Sci Rep. 6:22279.
  • Lemasters GK, Perreault SD, Hales BF, Hatch M, Hirschfield AN, Hughes CL, Kimmel GL, Lamb JC, Pryor JL, Rubin C, et al. 2000. Workshop to identify critical windows of exposure for children’s health: reproductive health in children and adolescents work group summary. Environ Health Perspect. 108(Suppl 3):505–509.
  • Lewis BC, Hudgins S, Lewis A, Schorr K, Sommer R, Peterson RE, Flaws JA, Furth PA. 2001. In utero and lactational treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin impairs mammary gland differentiation but does not block the response to exogenous estrogen in the postpubertal female rat. Toxicol Sci. 62(1):46–53.
  • Lin CC, Huang CN, Hwang YH, Wang JD, Weng SP, Shie RH, Chen PC. 2013b. Shortened menstrual cycles in LCD manufacturing workers. Occup Med (Lond). 63(1):45–52.
  • Lin CC, Huang CN, Wang JD, Hwang YH, Shie RH, Chang YY, Weng SP, Chen PC. 2013a. Exposure to multiple low-level chemicals in relation to reproductive hormones in premenopausal women involved in liquid crystal display manufacture. Int J Environ Res Public Health. 10(4):1406–1417.
  • Loeffler IK, Peterson RE. 1999. Interactive effects of TCDD and p,p’-DDE on male reproductive tract development in in utero and lactationally exposed rats. Toxicol Appl Pharmacol. 154:28–39.
  • Lyngsø J, Ramlau-Hansen CH, Høyer BB, Stovring H, Bonde JP, Jonsson BA, Lindh CH, Pedersen HS, Ludwicki JK, Zviezdai V, et al. 2014. Menstrual cycle characteristics in fertile women from Greenland, Poland and Ukraine exposed to perfluorinated chemicals: a cross-sectional study. Hum Reprod. 29(2):359–367.
  • Mably TA, Moore RW, Peterson RE. 1992. In utero and lactational exposure of male rats to 2,3,7,8-tetrachlordibenzo-p-dioxin. 1. Effects on androgenic status. Toxicol Appl Pharmacol. 114(1):97–107.
  • Mackenzie KM, Angevine DM. 1981. Infertility in mice exposed in utero to benzo[a]pyrene. Biol Reprod. 24:183–191.
  • McDiarmid MA, Gardiner PM, Jack BW. 2008. The clinical content of preconception care: environmental exposures. Am J Obstet Gynecol. 199(6 Suppl 2):S357–61.
  • Meerts IA, Hoving S, Van Den Berg JHJ, Weijers BM, Swarts HJM, van der Beek EM, Bergman AL, Koeman J, Brouwer AA. 2004. Effects of in utero exposure to 4-hydroxy2,3,3ʹ,4ʹ,5-pentachlorobiphenyl (4-OH-CB107) on developmental landmarks steroid hormone levels, and female estrus cyclicity in rats. Toxicol Sci. 82(1):259–267.
  • Mendiola J, Melgarejo M, Moñino-García M, Cutillas-Tolin A, Noquera-Velasco JA, Torres-Cantero AM. 2015. Is anogenital distance associated with semen quality in male partners of subfertile couples?. Andrology. 3(4):672–676.
  • Mocarelli P, Gerthoux PM, Ferrari E, Patterson DG Jr., Kieszak SM, Brambilla P, Vincoli N, Signorini S, Tramacere P, Carreri V, et al. 2000. Paternal concentrations of dioxin and sex ratio of offspring. Lancet. 355(9218):1858–1863.
  • Moore RW, Rudy TA, Lin T-M, Ko K, Peterson RE. 2001. Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer. Environ Health Perspect. 109:229–237.
  • Morgan AM, El-Tawil OS. 2003. Effects of ammonium metavanadate on fertility and reproductive performance of adult male and female rats. Pharmacol Res. 47(1):75–85.
  • Morrissey RE, Lamb JC, Morris RW, Chapin RE, Gulati DK, Heindel JJ. 1989. Results and evaluations of 48 continuous breeding reproduction studies conducted in mice. Fundam Appl Toxicol. 13(4):747–777.
  • Mu D, Gao F, Fan Z, Shen H, Peng H, Hu J 2015. Correction to levels of phthalate metabolites in urine of pregnant women and risk of clinical pregnancy loss. Environ Sci Technol. 49(21):13081.
  • Murray FJ, Smith FA, Nitschke KD, Hurniston CG. Kociba RJ, Schwetz BA. 1979. Three-generation reproduction study of rats given 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the diet. Toxicol Appl Pharmacol. 50:241–251.
  • Mylchreest E, Cattley RC, Foster PMD. 1998a. Di(n-butyl) phthalate disrupts prenatal androgen-regulated male reproductive development in a manner different from flutamide. Toxicologist. 42(1–S):176.
  • Mylchreest E, Cattley RC, Foster PMD. 1998b. Male reproductive tract malformations in rats following gestational and lactational exposure to di(n-butyl) phthalate: an antiandrogenic mechanism? Toxicol Sci. 43:47–60.
  • Mylchreest E, Sar M, Cattley RC, Foster PM. 1999. Disruption of androgen-related male reproductive development by di(n-butyl) phthalate during late gestation in rats is different from flutamide. Toxicol Appl Pharm. 156:81–95.
  • Mylchreest E, Wallace DG, Cattley RC, Foster PM. 2000. Dose-dependent alterations in androgen-regulated male reproductive development in rats exposed to di(n-butyl) phthalate during late gestation. Toxicol Sci. 55:143–151.
  • Nobunaga T, Satoh H, Suzuki T. 1979. Effects of sodium selenite on methylmercury embryotoxicity and teratogenicity in mice. Toxicol Appl Pharmacol. 47:79–88.
  • NTP. 1986. Ethylene glycol: reproduction and fertility assessment in CD-1 mice when administered in drinking water. Research Triangle Park (NC): National Toxicology Program.; p. PB86177383.
  • NTP. 1990. Reproductive Toxicity of 1,2,3-Trichloropropane administered by Gavage in CD-1 Swiss Mice. National Toxicology Program, Department of Health and Human Services, National Institute of Health, Research Triangle Park, NC.
  • NTP. 1991. Final report on the reproductive toxicity of tris(2-chloroethyl)phosphate reproduction and fertility assessment in Swiss CD-1 mice when administered via gavage.
  • NTP. 1995. Toxicity studies of dibutyl phthalate (CAS no. 84-74-2) administered in feed to F344/N and B6C3F1 mice. National Toxicology Program Toxicity Report Series, 30. Research Triangle Park, NC: National Toxicology Program/National Institutes of Health.
  • Ogata R, Omura M, Shimasaki Y, Kubo K, Oshima Y, Aou S, Inoue N. 2001. Two-generation reproductive toxicity study of tributyltin chloride in female rats. J Toxicol Environ Health A. 63(2):127–144.
  • Ohsako S, Miyabara Y, Nishimura N, Kurosawa S, Sakaue M, Ishimura R, Sato M, Takeda K, Aoki Y, Sone H, et al. 2001. Maternal exposure to a low dose of 2,3,7,8tetrachlorodibenzo-p-dioxin (TCDD) suppressed the development of reproductive organs of male rats: dose-dependent increase of mRNA levels of 5alpha-reductase type 2 in contrast to decrease of androgen receptor in the pubertal ventral prostate. Toxicol Sci. 60(1):132–143.
  • Ohsako S, Miyabara Y, Sakaue M, Ishimura R, Kakeyama M, Izumi H, Yonemoto J, Tohyama C. 2002. Developmental stage-specific effects of perinatal 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on reproductive organs of male rat offspring. Toxicol Sci. 66(2):283–292.
  • Osborne G, Rudel R, Schwarzman M. 2015. Evaluating chemical effects on mammary gland development: A critical need in disease prevention. Reprod Toxicol. 54:148–155.
  • Peng F, Ji W, Zhu F, Peng D, Yang M, Liu R, Pu Y, Yin L. 2016. A study on phthalate metabolites, bisphenol A and nonylphenol in the urine of Chinese women with unexplained recurrent spontaneous abortion. Environ Res. 150:622–628.
  • Phillips KP, Tanphaichitr N. 2008. Human exposure to endocrine disrupters and semen quality. Toxicol Environ Health B Crit Rev. 11(3–4):188–220.
  • Pohl HR, Abadin HG. 2008. Chemical mixtures: evaluation of risk for child-specific exposures in a multi-stressor environment. Toxicol Appl Pharmacol. 233:116–125.
  • Price SK. 2006. Prevalence and correlates of pregnancy loss history in a national sample of children and families. Matern Child Health J. 10:489–500.
  • Rice DC. 1999. Effect of exposure to 3,3ʹ,4,4ʹ,5-pentachlorobiphenyl (PCB 126) throughout gestation and lactation on development and spatial delayed alternation performance in rats. Neurotoxicol Teratol. 21(1):59–69.
  • Rider CV, Furr JR, Wilson VS, Gray LE Jr. 2010. Cumulative effects of in utero administration of mixtures of reproductive toxicants that disrupt common target tissues via diverse mechanisms of toxicity. Int J Androl. 33(2):443–462.
  • Rolland M, Le Moal J, Wagner V, Royere D, De Mouzon J. 2013. Decline in semen concentration and morphology in a sample of 26,609 men close to general population between 1989 and 2005 in France. Hum Reprod. 28(2):462–470.
  • Ronis MJ, Badger TM, Shema SJ, Roberson PK, Shaikh F. 1996. Reproductive toxicity and growth effects in rats exposed to lead at different periods during development. Toxicol Appl Pharmacol. 136:361–371.
  • Ronis MJJ, Badger TM, Shema SJ, Roberson PK, Shaikh F. 1998a. Effects on pubertal growth and reproduction in rats exposed to lead perinatally or continuously throughout development. J Toxicol Environ Health. 53(4):327–341.
  • Ronis MJJ, Badger TM, Shema SJ, Roberson PK, Templer L, RInger D, Thomas PE. 1998c. Endocrine mechanisms underlying the growth effects of developmental lead exposure in the rat. J Toxicol Environ Health. 54:101–120.
  • Ronis MJJ, Gandy J, Badger T. 1998b. Endocrine mechanisms underlying reproductive toxicity in the developing rat chronically exposed to dietary lead. J Toxicol Environ Health. 54:77–99.
  • Rudel RA, Fenton SE, Ackerman JM, Euling SY, Makris SL. 2011. Environmental exposures and mammary gland development: state of the science, public health implications, and research recommendations. Environ Health Perspect. 119(8):1053–1061.
  • Sager D, Girard D, Nelson D. 1991. Early postnatal exposure to PCBs: sperm function in rats. Environ Toxicol Chem. 10:737–746.
  • Sager DB. 1983. Effect of postnatal exposure to polychlorinated biphenyls on adult male reproductive function. Environ Res. 31:76–94.
  • Sager DB, Girard DM. 1994. Long-term effects on reproductive parameters in female rats after translactational exposure to PCBs. Environ Res. 66(1):52–76.
  • Sager DB, Shih-Schroeder W, Girard D. 1987. Effect of early postnatal exposure to polychlorinated biphenyls (PCBs) on fertility in male rats. Bull Environ Contam Toxicol. 38:946–953.
  • Saidi JA, Chang DT, Goluboff ET, Bagiella E, Olsen G, Fisch H. 1999. Declining sperm counts in the United States? A critical review. J Urol. 16(2):460–462.
  • Saillenfait AM, Payan JP, Fabry JP, Beydon D, Langonne I, Gallissot F, Sabate JP. 1998. Assessment of developmental toxicity, metabolism, and placental transfer of di-n-butyl phthalate administered to pregnant rats. Toxicol Sci. 45:212–224.
  • Salisbury TB, Marcinkiewicz JL. 2002. In utero and lactational exposure to 2,3,7,8tetrachlorodibenzo-p-dioxin and 2,3,4,7,8-pentachlorodibenzofuran reduces growth and disrupts reproductive parameters in female rats. Biol Reprod. 66(6):1621–1626.
  • Samuel JB, Stanley JA, Roopha DP, Vengatesh G, Anbalagan J, Banu SK, Aruldhas MM. 2011. Lactational hexavalent chromium exposure-induced oxidative stress in rat uterus is associated with delayed puberty and impaired gonadotropin levels. Hum Exp Toxicol. 30(2):91–101.
  • Sasser LB, Miller RA, Kalkwarf DR, Cushing JA, Dacre JC. 1996. Subchronic toxicity evaluation of sulfur mustard in rats. J Appl Toxicol. 16(1):5–13.
  • Schroeder HA, Mitchener M. 1971. Toxic effects of trace elements on reproduction of mice and rats. Arch Environ Health. 23:102–106.
  • Schroeder RE. 1994. A two-generation reproduction study in rats with methanearsonic acid (MAA). Luxembourg Industries (Pamol) Ltd. Submitted to the U.S. Environmental Protection Agency. MRID43178301.
  • Schwetz BA, Keeler PA, Gehring PJ. 1974. The effect of purified and commercial grade pentachlorophenol on rat embryonal and fetal development. Toxicol Appl Pharmacol. 28:151–161.
  • Semczuk M, Semczuk-Sikora A. 2001. New data on toxic metal intoxication (Cd, Pb, and Hg in particular) and Mg status during pregnancy. Med Sci Monit. 7(2):332–340.
  • Senichenkova IN 1991. Embryotoxic effect of pollutants in the industrial environment: formalehdye and gasoline. Institute of Obstetrics and Gynecology, Academy of Medical Sciences of the USSR, Leningrad.
  • Senichenkova IN, Chebotar NA. 1996. Effects of gasoline and formaldehyde on prenatal development of rats with induced iron microelementosis. Ontogenez. 27:90–94.
  • Shi Z, Valdez KE, Ting AY, Franczak A, Gum SL, Petroff BK. 2007. Ovarian endocrine disruption underlies premature reproductive senescence following environmentally relevant chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biol Reprod. 76(2):198–202.
  • Simanainen U, Haavisto T, Tuomisto JT, Paranko J, Toppari J, Tuomisto J, Peterson RE, Viluksela M. 2004. Pattern of male reproductive system effects after in utero and lactational 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) exposure in three differentially TCDD-sensitive rat lines. Toxicol Sci. 80(1):101–108.
  • Sinha N, Adhikari N, Saxena DK. 2001. Effect of endosulfan during fetal gonadal differentiation on spermatogenesis in rats. Environ Toxicol Pharmacol. 10(1–2):29–32.
  • Skakkebaek NE, Rajpert-De Meytes E, Buck Louis GM, Toppari J, Andersson AM, Eisenberg ML, Jensen TK, Jorgensen N, Swan SH, Sapra KJ, et al. 2016. Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiological Reviews. 96(1):55–97.
  • Skakkebaek NE, Rajpert-De M, Main KM. 2001. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects: opinion. Human Reproduction. 16(5):972–978.
  • Spyker JM, Avery DL. 1977. Neurobehavioral effects of prenatal exposure to the organophosphate diazinon in mice. J Toxicol Environ Health. 3(5–6):989–1002.
  • Srivastava S, Seth PK, Srivastava SP. 1992. Biochemical and morphological studies in testes of rat offspring of mothers exposed to styrene during lactation. Pharmacol Toxicol. 70:314–316.
  • Stoker TE, Laws SC, Crofton KM, Hedge JM, Ferrell JM, Cooper RL. 2004. Assessment of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture, in the EDSP male and female pubertal protocols. Toxicol Sci. 78(1):144155.
  • Suzuki K, Takahashi M, Ishii-Ohba H, Ikeda K, Inano H. 1990. Steroidogenesis in the testes and the adrenals of adult male rats after gamma-irradiation in utero at late pregnancy. J Steroid Biochem. 35(2):301–305.
  • Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, Mao CS, Redmon JB, Ternand CL, Sullivan S. 2005. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect. 113(8):1056–1061.
  • Swan SH, Sathyanarayana S, Barrett ES, Janssen S, Liu F, Nguyen RH, Redmon JB; TIDES Study Team. 2015. First trimester phthalate exposure and anogenital distance in newborns. Hum Reprod. 30(4):963–972.
  • Talsness CE, Kuriyama SN, Sterner-Kock A, Schnitker P, Grande SW, Shakibaei M, Andrade A, Grote K, Chahoud I. 2008. In utero and lactational exposures to low doses of polybrominated diphenyl ether-47 alter the reproductive system and thyroid gland of female rat offspring. Environ Health Perspect. 116(3):308–314.
  • Talsness CE, Shakibaei M, Kuriyama SN, Grande SW, Sterner-Kock A, Schnitker P, de Souza C, Grote K, Chahoud I. 2005. Ultrastructural changes observed in rat ovaries following in utero and lactational exposure to low doses of a polybrominated flame retardant. Toxicol Lett. 157(3):189–202.
  • Thiel R, Chahoud I. 1997. Postnatal development and behaviour of Wistar rats after prenatal toluene exposure. Arch Toxicol. 71(4):258–265.
  • Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ Jr, Jegou B, Jensen TK, Jouannet P, Keiding N, et al. 1996. Male reproductive health and environmental xenoestrogens. Environmental Health Perspectives. 104(Suppl 4):741–803.
  • Traina ME, Rescia M, Urbani E, Mantovani A, Macri C, Ricciardi C, Stazi AV, Fazzi P, Cordelli E, Eleuteri P, et al. 2003. Long-lasting effects of lindane on mouse spermatogenesis induced by in utero exposure. Reprod Toxicol. 17(1):25–35.
  • Tseng LH, Hsu PC, Lee CW, Tsai SS, Pan MH, Li MH. 2013. Developmental exposure to decabrominated diphenyl ether (BDE-209): effects on sperm oxidative stress and chromatin DNA damage in mouse offspring. Environ Toxicol. 28(7):380–389.
  • Uzumcu M, Zachow R. 2007. Developmental exposure to environmental endocrine disruptors: consequences within the ovary and on female reproductive function. Reproductive Toxicology. 23:337–352.
  • Vahter M. 2008. Health effects of early life exposure to arsenic. Basic Clin Pharmacol Toxicol. 102(2):204–211.
  • Vahter M. 2009. Effects of arsenic on maternal and fetal health. Annu Rev Nutr. 29:381–399.
  • Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr., Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, et al. 2012. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 33(3):378–455.
  • Virtanen H, Rajpertdemeyts E, Main K, Skakkebaek NE, Toppari J. 2005. Testicular dysgenesis syndrome and the development and occurrence of male reproductive disorders. Toxicology and Applied Pharmacology. 207(2):501–505.
  • Weir RJ, Fisher RS. 1972. Toxicologic studies on borax and boric acid. Toxicol Appl Pharmacol. 23:351–364.
  • Wennborg H, Bodin L, Vainio H, Axelsson G. 2001. Solvent use and time to pregnancy among female personnel in biomedical laboratories in Sweden. Occup Environ Med. 58(4):225–231.
  • White SS, Calafat AM, Kuklenyik Z, Villanueva L, Zehr RD, Helfant L, Strynar MJ, Lindstrom AB, Thibodeaux JR, Wood C, et al. 2007. Gestational PFOA exposure of mice is associated with altered mammary gland development in dams and female offspring. Toxicol Sci. 96(1):133–144.
  • York RG, Barnett J, Brown WR, Garman RH, Mattie DR, Dodd D. 2004. A rat neurodevelopmental evaluation of offspring, including evaluation of adult and neonatal thyroid, from mothers treated with ammonium perchlorate in drinking water. Int J Toxicol. 23:191–214.
  • You L, Casanova M, Archibeque-Engle S, Sar M, Fan LQ, Heck HA. 1998. Impaired male sexual development in perinatal Sprague-Dawley and Long-Evans hooded rats exposed in utero and lactationally to p,p’-DDE. Toxicol Sci. 45:162–173.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.