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Abstract

Endocrine disrupting chemicals are common in our environment and act on hormone systems and signaling pathways to alter physiological homeostasis. Gestational exposure can disrupt developmental programs, permanently altering tissues with impacts lasting into adulthood. The brain is a critical target for developmental endocrine disruption, resulting in altered neuroendocrine control of hormonal signaling, altered neurotransmitter control of nervous system function, and fundamental changes in behaviors such as learning, memory, and social interactions. Human cohort studies reveal correlations between maternal/fetal exposure to endocrine disruptors and incidence of neurodevelopmental disorders. Here, we summarize the major literature findings of endocrine disruption of neurodevelopment and concomitant changes in behavior by four major endocrine disruptor classes:bisphenol A, polychlorinated biphenyls, organophosphates, and polybrominated diphenyl ethers. We specifically review studies of gestational and/or lactational exposure to understand the effects of early life exposure to these compounds and summarize animal studies that help explain human correlative data.

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2020-02-10
2024-04-18
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Literature Cited

  1. 1. 
    US Environ. Prot. Agency 1997. Special report on environmental endocrine disruption: an effects assessment and analysis Rep., EPA/630/R-96/012, US Environ. Prot. Agency Washington, DC: https://archive.epa.gov/raf/web/pdf/endocrine.pdf
  2. 2. 
    Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A et al. 2015. EDC-2: The Endocrine Society's second Scientific Statement on endocrine-disrupting chemicals. Endocr. Rev. 36:E1–150
    [Google Scholar]
  3. 3. 
    Falconer IR, Chapman HF, Moore MR, Ranmuthugala G 2006. Endocrine-disrupting compounds: a review of their challenge to sustainable and safe water supply and water reuse. Environ. Toxicol. 21:181–91
    [Google Scholar]
  4. 4. 
    Rubin BS. 2011. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J. Steroid Biochem. Mol. Biol. 127:27–34
    [Google Scholar]
  5. 5. 
    Rudel RA, Perovich LJ. 2009. Endocrine disrupting chemicals in indoor and outdoor air. Atmos. Environ. 43:170–81
    [Google Scholar]
  6. 6. 
    Gore AC. 2010. Neuroendocrine targets of endocrine disruptors. Hormones 9:16–27
    [Google Scholar]
  7. 7. 
    Patisaul HB, Polston EK. 2008. Influence of endocrine active compounds on the developing rodent brain. Brain Res. Rev. 57:352–62
    [Google Scholar]
  8. 8. 
    Clotfelter ED, Bell AM, Levering KR 2004. The role of animal behaviour in the study of endocrine-disrupting chemicals. Anim. Behav. 68:665–76
    [Google Scholar]
  9. 9. 
    Balakrishnan B, Thorstensen E, Ponnampalam A, Mitchell MD 2011. Passage of 4-nonylphenol across the human placenta. Placenta 32:788–92
    [Google Scholar]
  10. 10. 
    Wan Y, Choi K, Kim S, Ji K, Chang H et al. 2010. Hydroxylated polybrominated diphenyl ethers and bisphenol A in pregnant women and their matching fetuses: placental transfer and potential risks. Environ. Sci. Technol. 44:5233–39
    [Google Scholar]
  11. 11. 
    Chen M, Fan Z, Zhao F, Gao F, Mu D et al. 2016. Occurrence and maternal transfer of chlorinated bisphenol A and nonylphenol in pregnant women and their matching embryos. Environ. Sci. Technol. 50:970–77
    [Google Scholar]
  12. 12. 
    Gould JC, Leonard LS, Maness SC, Wagner BL, Conner K et al. 1998. Bisphenol A interacts with the estrogen receptor α in a distinct manner from estradiol. Mol. Cell. Endocrinol. 142:203–14
    [Google Scholar]
  13. 13. 
    Tohmé M, Prudhomme SM, Boulahtouf A, Samarut E, Brunet F et al. 2014. Estrogen-related receptor γ is an in vivo receptor of bisphenol A. FASEB J 28:3124–33
    [Google Scholar]
  14. 14. 
    Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH et al. 1998. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139:4252–63
    [Google Scholar]
  15. 15. 
    Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M et al. 2002. Thyroid hormone action is disrupted by bisphenol A as an antagonist. J. Clin. Endocrinol. Metab. 87:5185–90
    [Google Scholar]
  16. 16. 
    Lee HJ. 2003. Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol. Sci. 75:40–46
    [Google Scholar]
  17. 17. 
    Alonso-Magdalena P, Laribi O, Ropero AB, Fuentes E, Ripoll C et al. 2005. Low doses of bisphenol A and diethylstilbestrol impair Ca2+ signals in pancreatic α-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ. Health Perspect. 113:969–77
    [Google Scholar]
  18. 18. 
    Prasanth GK, Divya LM, Sadasivan C 2010. Bisphenol-A can bind to human glucocorticoid receptor as an agonist: an in silico study. J. Appl. Toxicol. 30:769–74
    [Google Scholar]
  19. 19. 
    Vandenberg LN. 2013. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol A as a case study. Dose-Response 12:259–76
    [Google Scholar]
  20. 20. 
    Yang C-W, Chou W-C, Chen K-H, Cheng A-L, Mao I-F et al. 2014. Visualized gene network reveals the novel target transcripts Sox2 and Pax6 of neuronal development in trans-placental exposure to bisphenol A. PLOS ONE 9:e100576
    [Google Scholar]
  21. 21. 
    Ellis P, Fagan BM, Magness ST, Hutton S, Taranova O et al. 2004. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26:148–65
    [Google Scholar]
  22. 22. 
    Haubst N, Berger J, Radjendirane V, Graw J, Favor J et al. 2004. Molecular dissection of Pax6 function: the specific roles of the paired domain and homeodomain in brain development. Development 131:6131–40
    [Google Scholar]
  23. 23. 
    Kinch CD, Ibhazehiebo K, Jeong J-H, Habibi HR, Kurrasch DM 2015. Low-dose exposure to bisphenol A and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish. PNAS 112:1475–80
    [Google Scholar]
  24. 24. 
    Kim K, Son TG, Park HR, Kim SJ, Kim HS et al. 2009. Potencies of bisphenol A on the neuronal differentiation and hippocampal neurogenesis. J. Toxicol. Environ. Health A 72:1343–51
    [Google Scholar]
  25. 25. 
    Xu X-h, Zhang J, Wang Y-M, Ye Y-P, Luo Q-Q 2010. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-d-aspartate receptors of hippocampus in male offspring mice. Horm. Behav. 58:326–33
    [Google Scholar]
  26. 26. 
    Cao J, Rebuli ME, Rogers J, Todd KL, Leyrer SM et al. 2013. Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala. Toxicol. Sci. 133:157–73
    [Google Scholar]
  27. 27. 
    Kimura E, Matsuyoshi C, Miyazaki W, Benner S, Hosokawa M et al. 2015. Prenatal exposure to bisphenol A impacts neuronal morphology in the hippocampal CA1 region in developing and aged mice. Arch. Toxicol. 90:691–700
    [Google Scholar]
  28. 28. 
    Elsworth JD, Jentsch JD, VandeVoort CA, Roth RH, Redmond DE, Leranth C 2013. Prenatal exposure to bisphenol A impacts midbrain dopamine neurons and hippocampal spine synapses in non-human primates. Neurotoxicology 35:113–20
    [Google Scholar]
  29. 29. 
    Liu Z-H, Ding J-J, Yang Q-Q, Song H-Z, Chen X-T et al. 2016. Early developmental bisphenol-A exposure sex-independently impairs spatial memory by remodeling hippocampal dendritic architecture and synaptic transmission in rats. Sci. Rep. 6:32492
    [Google Scholar]
  30. 30. 
    Shikimi H, Sakamoto H, Mezaki Y, Ukena K, Tsutsui K 2004. Dendritic growth in response to environmental estrogens in the developing Purkinje cell in rats. Neurosci. Lett. 364:114–18
    [Google Scholar]
  31. 31. 
    Bowman RE, Luine V, Khandaker H, Villafane JJ, Frankfurt M 2014. Adolescent bisphenol-A exposure decreases dendritic spine density: role of sex and age. Synapse 68:498–507
    [Google Scholar]
  32. 32. 
    Eilam-Stock T, Serrano P, Frankfurt M, Luine V 2012. Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats. Behav. Neurosci. 126:175–85
    [Google Scholar]
  33. 33. 
    Lam SH, Hlaing MM, Zhang X, Yan C, Duan Z et al. 2011. Toxicogenomic and phenotypic analyses of bisphenol-A early-life exposure toxicity in zebrafish. PLOS ONE 6:e28273
    [Google Scholar]
  34. 34. 
    Ramos B, Gaudillière B, Bonni A, Gill G 2007. Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. PNAS 104:9882–87
    [Google Scholar]
  35. 35. 
    Zhou X, Qyang Y, Kelsoe JR, Masliah E, Geyer MA 2007. Impaired postnatal development of hippocampal dentate gyrus in Sp4 null mutant mice. Genes Brain Behav 6:269–76
    [Google Scholar]
  36. 36. 
    Tando S, Itoh K, Yaoi T, Ikeda J, Fujiwara Y, Fushiki S 2007. Effects of pre- and neonatal exposure to bisphenol A on murine brain development. Brain Dev 29:352–56
    [Google Scholar]
  37. 37. 
    Tando S, Itoh K, Yaoi T, Ogi H, Goto S et al. 2014. Bisphenol A exposure disrupts the development of the locus coeruleus-noradrenergic system in mice. Neuropathology 34:527–34
    [Google Scholar]
  38. 38. 
    Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM 2006. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 147:3681–91
    [Google Scholar]
  39. 39. 
    Facciolo RM, Alo R, Madeo M, Canonaco M, Dessi-Fulgheri F 2002. Early cerebral activities of the environmental estrogen bisphenol A appear to act via the somatostatin receptor subtype sst2. Environ. Health Perspect. 110:Suppl. 3397–402
    [Google Scholar]
  40. 40. 
    Nishizawa H, Manabe N, Morita M, Sugimoto M, Imanishi S, Miyamoto H 2003. Effects of in utero exposure to bisphenol A on expression of RARα and RXRα mRNAs in murine embryos. J. Reprod. Dev. 49:539–45
    [Google Scholar]
  41. 41. 
    Patisaul HB, Todd KL, Mickens JA, Adewale HB 2009. Impact of neonatal exposure to the ERα agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology 30:350–57
    [Google Scholar]
  42. 42. 
    Braun JM, Yolton K, Dietrich KN, Hornung R, Ye X et al. 2009. Prenatal bisphenol A exposure and early childhood behavior. Environ. Health Perspect. 117:1945–52
    [Google Scholar]
  43. 43. 
    Evans SF, Kobrosly RW, Barrett ES, Thurston SW, Calafat AM et al. 2014. Prenatal bisphenol A exposure and maternally reported behavior in boys and girls. Neurotoxicology 45:91–99
    [Google Scholar]
  44. 44. 
    Perera F, Vishnevetsky J, Herbstman JB, Calafat AM, Xiong W et al. 2012. Prenatal bisphenol A exposure and child behavior in an inner-city cohort. Environ. Health Perspect. 120:1190–94
    [Google Scholar]
  45. 45. 
    Braun JM, Kalkbrenner AE, Calafat AM, Yolton K, Ye X et al. 2011. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 128:873–82
    [Google Scholar]
  46. 46. 
    Casas M, Forns J, Martínez D, Avella-García C, Valvi D et al. 2015. Exposure to bisphenol A during pregnancy and child neuropsychological development in the INMA-Sabadell cohort. Environ. Res. 142:671–79
    [Google Scholar]
  47. 47. 
    Anderson OS, Peterson KE, Sanchez BN, Zhang Z, Mancuso P, Dolinoy DC 2013. Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J 27:1784–92
    [Google Scholar]
  48. 48. 
    Zhou R, Bai Y, Yang R, Zhu Y, Chi X et al. 2011. Abnormal synaptic plasticity in basolateral amygdala may account for hyperactivity and attention-deficit in male rat exposed perinatally to low-dose bisphenol-A. Neuropharmacology 60:789–98
    [Google Scholar]
  49. 49. 
    Nakamura K, Itoh K, Dai H, Han L, Wang X et al. 2012. Prenatal and lactational exposure to low-doses of bisphenol A alters adult mice behavior. Brain Dev 34:57–63
    [Google Scholar]
  50. 50. 
    Fujimoto T, Kubo K, Aou S 2006. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res 1068:49–55
    [Google Scholar]
  51. 51. 
    Ohtani N, Iwano H, Suda K, Tsuji E, Tanemura K et al. 2017. Adverse effects of maternal exposure to bisphenol F on the anxiety- and depression-like behavior of offspring. J. Vet. Med. Sci. 79:432–39
    [Google Scholar]
  52. 52. 
    Xu X, Hong X, Xie L, Li T, Yang Y et al. 2012. Gestational and lactational exposure to bisphenol-A affects anxiety- and depression-like behaviors in mice. Horm. Behav. 62:480–90
    [Google Scholar]
  53. 53. 
    Porrini S, Belloni V, Seta DD, Farabollini F, Giannelli G, Dessì-Fulgheri F 2005. Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats. Brain Res. Bull. 65:261–66
    [Google Scholar]
  54. 54. 
    Farabollini F, Porrini S, Della Seta D 2002. Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ. Health Perspect. 110:Suppl. 3409–14
    [Google Scholar]
  55. 55. 
    Wolstenholme JT, Taylor JA, Shetty SRJ, Edwards M, Connelly JJ, Rissman EF 2011. Gestational exposure to low dose bisphenol A alters social behavior in juvenile mice. PLOS ONE 6:e25448
    [Google Scholar]
  56. 56. 
    Hass U, Christiansen S, Boberg J, Rasmussen MG, Mandrup K, Axelstad M 2016. Low-dose effect of developmental bisphenol A exposure on sperm count and behaviour in rats. Andrology 4:594–607
    [Google Scholar]
  57. 57. 
    Xu X, Liu Y, Sadamatsu M, Tsutsumi S, Akaike M et al. 2007. Perinatal bisphenol A affects the behavior and SRC-1 expression of male pups but does not influence on the thyroid hormone receptors and its responsive gene. Neurosci. Res. 58:149–55
    [Google Scholar]
  58. 58. 
    Craig ZR, Wang W, Flaws JA 2011. Endocrine-disrupting chemicals in ovarian function: effects on steroidogenesis, metabolism and nuclear receptor signaling. Reproduction 142:633–46
    [Google Scholar]
  59. 59. 
    Jansen HT, Cooke PS, Porcelli J, Liu TC, Hansen LG 1993. Estrogenic and antiestrogenic actions of PCBs in the female rat: in vitro and in vivo studies. Reprod. Toxicol. 7:237–48
    [Google Scholar]
  60. 60. 
    Bonefeld-Jorgensen EC, Andersen HR, Rasmussen TH, Vinggaard AM 2001. Effect of highly bioaccumulated polychlorinated biphenyl congeners on estrogen and androgen receptor activity. Toxicology 158:141–53
    [Google Scholar]
  61. 61. 
    Mandal PK. 2005. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. B 175:221–30
    [Google Scholar]
  62. 62. 
    Safe S, Wang F, Porter W, Duan R, McDougal A 1998. Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol. Lett. 102–103:343–47
    [Google Scholar]
  63. 63. 
    Ritter R, Scheringer M, MacLeod M, Moeckel C, Jones KC, Hungerbuhler K 2011. Intrinsic human elimination half-lives of polychlorinated biphenyls derived from the temporal evolution of cross-sectional biomonitoring data from the United Kingdom. Environ. Health Perspect. 119:225–31
    [Google Scholar]
  64. 64. 
    Milbrath MO, Wenger Y, Chang CW, Emond C, Garabrant D et al. 2009. Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ. Health Perspect. 117:417–25
    [Google Scholar]
  65. 65. 
    Lancz K, Murinova L, Patayova H, Drobna B, Wimmerova S et al. 2015. Ratio of cord to maternal serum PCB concentrations in relation to their congener-specific physicochemical properties. Int. J. Hyg. Environ. Health 218:91–98
    [Google Scholar]
  66. 66. 
    Vizcaino E, Grimalt JO, Fernandez-Somoano A, Tardon A 2014. Transport of persistent organic pollutants across the human placenta. Environ. Int. 65:107–15
    [Google Scholar]
  67. 67. 
    Morse DC, Groen D, Veerman M, van Amerongen CJ, Koeter HB et al. 1993. Interference of polychlorinated biphenyls in hepatic and brain thyroid hormone metabolism in fetal and neonatal rats. Toxicol. Appl. Pharmacol. 122:27–33
    [Google Scholar]
  68. 68. 
    Ness DK, Schantz SL, Moshtaghian J, Hansen LG 1993. Effects of perinatal exposure to specific PCB congeners on thyroid hormone concentrations and thyroid histology in the rat. Toxicol. Lett. 68:311–23
    [Google Scholar]
  69. 69. 
    Schantz SL, Seo B-W, Moshtaghian J, Amin S 1997. Developmental exposure to polychlorinated biphenyls or dioxin: do changes in thyroid function mediate effects on spatial learning?. Am. Zool. 37:399–408
    [Google Scholar]
  70. 70. 
    Gauger KJ, Kato Y, Haraguchi K, Lehmler HJ, Robertson LW et al. 2004. Polychlorinated biphenyls (PCBs) exert thyroid hormone-like effects in the fetal rat brain but do not bind to thyroid hormone receptors. Environ. Health Perspect. 112:516–23
    [Google Scholar]
  71. 71. 
    Dickerson SM, Cunningham SL, Patisaul HB, Woller MJ, Gore AC 2011. Endocrine disruption of brain sexual differentiation by developmental PCB exposure. Endocrinology 152:581–94
    [Google Scholar]
  72. 72. 
    Walker DM, Goetz BM, Gore AC 2014. Dynamic postnatal developmental and sex-specific neuroendocrine effects of prenatal polychlorinated biphenyls in rats. Mol. Endocrinol. 28:99–115
    [Google Scholar]
  73. 73. 
    Ernfors P, Lee KF, Jaenisch R 1994. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147–50
    [Google Scholar]
  74. 74. 
    Jones KR, Farinas I, Backus C, Reichardt LF 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989–99
    [Google Scholar]
  75. 75. 
    Bavithra S, Sugantha Priya E, Selvakumar K, Krishnamoorthy G, Arunakaran J 2015. Effect of melatonin on glutamate: BDNF signaling in the cerebral cortex of polychlorinated biphenyls (PCBs)-exposed adult male rats. Neurochem. Res. 40:1858–69
    [Google Scholar]
  76. 76. 
    Giordano T, Pan JB, Casuto D, Watanabe S, Arneric SP 1992. Thyroid hormone regulation of NGF, NT-3 and BDNF RNA in the adult rat brain. Brain Res. Mol. Brain Res. 16:239–45
    [Google Scholar]
  77. 77. 
    Hany J, Lilienthal H, Sarasin A, Roth-Harer A, Fastabend A et al. 1999. Developmental exposure of rats to a reconstituted PCB mixture or Aroclor 1254: effects on organ weights, aromatase activity, sex hormone levels, and sweet preference behavior. Toxicol. Appl. Pharmacol. 158:231–43
    [Google Scholar]
  78. 78. 
    Colciago A, Casati L, Mornati O, Vergoni AV, Santagostino A et al. 2009. Chronic treatment with polychlorinated biphenyls (PCB) during pregnancy and lactation in the rat: Part 2: Effects on reproductive parameters, on sex behavior, on memory retention and on hypothalamic expression of aromatase and 5alpha-reductases in the offspring. Toxicol. Appl. Pharmacol. 239:46–54
    [Google Scholar]
  79. 79. 
    Clements RJ, Lawrence RC, Blank JL 2009. Effects of intrauterine 2,3,7,8-tetrachlorodibenzo-p-dioxin on the development and function of the gonadotrophin releasing hormone neuronal system in the male rat. Reprod. Toxicol. 28:38–45
    [Google Scholar]
  80. 80. 
    Takeda T, Matsumoto Y, Koga T, Mutoh J, Nishimura Y et al. 2009. Maternal exposure to dioxin disrupts gonadotropin production in fetal rats and imprints defects in sexual behavior. J. Pharmacol. Exp. Ther. 329:1091–99
    [Google Scholar]
  81. 81. 
    Seegal RF, Brosch KO, Okoniewski RJ 2005. Coplanar PCB congeners increase uterine weight and frontal cortical dopamine in the developing rat: implications for developmental neurotoxicity. Toxicol. Sci. 86:125–31
    [Google Scholar]
  82. 82. 
    Morse DC, Seegal RF, Borsch KO, Brouwer A 1996. Long-term alterations in regional brain serotonin metabolism following maternal polychlorinated biphenyl exposure in the rat. Neurotoxicology 17:631–38
    [Google Scholar]
  83. 83. 
    Hood DB, Woods L, Brown L, Johnson S, Ebner FF 2006. Gestational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure effects on sensory cortex function. Neurotoxicology 27:1032–42
    [Google Scholar]
  84. 84. 
    Tomasini MC, Beggiato S, Ferraro L, Tanganelli S, Marani L et al. 2012. Prenatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin produces alterations in cortical neuron development and a long-term dysfunction of glutamate transmission in rat cerebral cortex. Neurochem. Int. 61:759–66
    [Google Scholar]
  85. 85. 
    Morse DC, Plug A, Wesseling W, van den Berg KJ, Brouwer A 1996. Persistent alterations in regional brain glial fibrillary acidic protein and synaptophysin levels following pre- and postnatal polychlorinated biphenyl exposure. Toxicol. Appl. Pharmacol. 139:252–61
    [Google Scholar]
  86. 86. 
    Roegge CS, Morris JR, Villareal S, Wang VC, Powers BE et al. 2006. Purkinje cell and cerebellar effects following developmental exposure to PCBs and/or MeHg. Neurotoxicol. Teratol. 28:74–85
    [Google Scholar]
  87. 87. 
    Nishijo M, Kuriwaki J, Hori E, Tawara K, Nakagawa H, Nishijo H 2007. Effects of maternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on fetal brain growth and motor and behavioral development in offspring rats. Toxicol. Lett. 173:41–47
    [Google Scholar]
  88. 88. 
    Vreugdenhil HJ, Mulder PG, Emmen HH, Weisglas-Kuperus N 2004. Effects of perinatal exposure to PCBs on neuropsychological functions in the Rotterdam cohort at 9 years of age. Neuropsychology 18:185–93
    [Google Scholar]
  89. 89. 
    Gladen BC, Rogan WJ, Hardy P, Thullen J, Tingelstad J, Tully M 1988. Development after exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene transplacentally and through human milk. J. Pediatr. 113:991–95
    [Google Scholar]
  90. 90. 
    Jacobson SW, Fein GG, Jacobson JL, Schwartz PM, Dowler JK 1985. The effect of intrauterine PCB exposure on visual recognition memory. Child Dev 56:853–60
    [Google Scholar]
  91. 91. 
    Jacobson JL, Jacobson SW, Humphrey HE 1990. Effects of in utero exposure to polychlorinated biphenyls and related contaminants on cognitive functioning in young children. J. Pediatr. 116:38–45
    [Google Scholar]
  92. 92. 
    Nishijo M, Tawara K, Nakagawa H, Honda R, Kido T et al. 2008. 2,3,7,8-Tetrachlorodibenzo-p-dioxin in maternal breast milk and newborn head circumference. J. Expo. Sci. Environ. Epidemiol. 18:246–51
    [Google Scholar]
  93. 93. 
    Tai PT, Nishijo M, Anh NT, Maruzeni S, Nakagawa H et al. 2013. Dioxin exposure in breast milk and infant neurodevelopment in Vietnam. Occup. Environ. Med. 70:656–62
    [Google Scholar]
  94. 94. 
    Nishijo M, Pham TT, Nguyen AT, Tran NN, Nakagawa H et al. 2014. 2,3,7,8-Tetrachlorodibenzo-p-dioxin in breast milk increases autistic traits of 3-year-old children in Vietnam. Mol. Psychiatry 19:1220–26
    [Google Scholar]
  95. 95. 
    Tran NN, Pham TT, Ozawa K, Nishijo M, Nguyen AT et al. 2016. Impacts of perinatal dioxin exposure on motor coordination and higher cognitive development in Vietnamese preschool children: a five-year follow-up. PLOS ONE 11:e0147655
    [Google Scholar]
  96. 96. 
    Schantz SL, Moshtaghian J, Ness DK 1995. Spatial learning deficits in adult rats exposed to ortho-substituted PCB congeners during gestation and lactation. Fundam. Appl. Toxicol. 26:117–26
    [Google Scholar]
  97. 97. 
    Seo BW, Sparks AJ, Medora K, Amin S, Schantz SL 1999. Learning and memory in rats gestationally and lactationally exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Neurotoxicol. Teratol. 21:231–39
    [Google Scholar]
  98. 98. 
    Weinand-Harer A, Lilienthal H, Bucholski KA, Winneke G 1997. Behavioral effects of maternal exposure to an ortho-chlorinated or a coplanar PCB congener in rats. Environ. Toxicol. Pharmacol. 3:97–103
    [Google Scholar]
  99. 99. 
    Schantz SL, Seo BW, Moshtaghian J, Peterson RE, Moore RW 1996. Effects of gestational and lactational exposure to TCDD or coplanar PCBs on spatial learning. Neurotoxicol. Teratol. 18:305–13
    [Google Scholar]
  100. 100. 
    Piedrafita B, Erceg S, Cauli O, Monfort P, Felipo V 2008. Developmental exposure to polychlorinated biphenyls PCB153 or PCB126 impairs learning ability in young but not in adult rats. Eur. J. Neurosci. 27:177–82
    [Google Scholar]
  101. 101. 
    Widholm JJ, Clarkson GB, Strupp BJ, Crofton KM, Seegal RF, Schantz SL 2001. Spatial reversal learning in Aroclor 1254-exposed rats: sex-specific deficits in associative ability and inhibitory control. Toxicol. Appl. Pharmacol. 174:188–98
    [Google Scholar]
  102. 102. 
    Curran CP, Nebert DW, Genter MB, Patel KV, Schaefer TL et al. 2011. In utero and lactational exposure to PCBs in mice: adult offspring show altered learning and memory depending on Cyp1a2 and Ahr genotypes. Environ. Health Perspect. 119:1286–93
    [Google Scholar]
  103. 103. 
    Schantz SL, Levin ED, Bowman RE, Heironimus MP, Laughlin NK 1989. Effects of perinatal PCB exposure on discrimination-reversal learning in monkeys. Neurotoxicol. Teratol. 11:243–50
    [Google Scholar]
  104. 104. 
    Kuriyama SN, Chahoud I. 2004. In utero exposure to low-dose. 2: ,3′,4,4′,5-pentachlorobiphenyl (PCB 118) impairs male fertility and alters neurobehavior in rat offspring. Toxicology 202:185–97
    [Google Scholar]
  105. 105. 
    Nguon K, Baxter MG, Sajdel-Sulkowska EM 2005. Perinatal exposure to polychlorinated biphenyls differentially affects cerebellar development and motor functions in male and female rat neonates. Cerebellum 4:112–22
    [Google Scholar]
  106. 106. 
    Rice DC. 1999. Effect of exposure to 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) throughout gestation and lactation on development and spatial delayed alternation performance in rats. Neurotoxicol. Teratol. 21:59–69
    [Google Scholar]
  107. 107. 
    Pantaleoni GC, Fanini D, Sponta AM, Palumbo G, Giorgi R, Adams PM 1988. Effects of maternal exposure to polychlorobiphenyls (PCBs) on F1 generation behavior in the rat. Fundam. Appl. Toxicol. 11:440–49
    [Google Scholar]
  108. 108. 
    Agrawal AK, Tilson HA, Bondy SC 1981. 3,4,3′,4′-Tetrachlorobiphenyl given to mice prenatally produces long-term decreases in striatal dopamine and receptor binding sites in the caudate nucleus. Toxicol. Lett. 7:417–24
    [Google Scholar]
  109. 109. 
    Tilson HA, Davis GJ, McLachlan JA, Lucier GW 1979. The effects of polychlorinated biphenyls given prenatally on the neurobehavioral development of mice. Environ. Res. 18:466–74
    [Google Scholar]
  110. 110. 
    Nguyen AT, Nishijo M, Hori E, Nguyen NM, Pham TT et al. 2013. Influence of maternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on socioemotional behaviors in offspring rats. Environ. Health Insights 7: https://doi.org/10.4137/ehi.s10346
    [Crossref] [Google Scholar]
  111. 111. 
    Bushnell PJ, Moser VC, MacPhail RC, Oshiro WM, Derr-Yellin EC et al. 2002. Neurobehavioral assessments of rats perinatally exposed to a commercial mixture of polychlorinated biphenyls. Toxicol. Sci. 68:109–20
    [Google Scholar]
  112. 112. 
    Schantz SL, Seo BW, Wong PW, Pessah IN 1997. Long-term effects of developmental exposure to 2,2′,3,5′,6-pentachlorobiphenyl (PCB 95) on locomotor activity, spatial learning and memory and brain ryanodine binding. Neurotoxicology 18:457–67
    [Google Scholar]
  113. 113. 
    Roegge CS, Wang VC, Powers BE, Klintsova AY, Villareal S et al. 2004. Motor impairment in rats exposed to PCBs and methylmercury during early development. Toxicol. Sci. 77:315–24
    [Google Scholar]
  114. 114. 
    Bjerke DL, Brown TJ, MacLusky NJ, Hochberg RB, Peterson RE 1994. Partial demasculinization and feminization of sex behavior in male rats by in utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin is not associated with alterations in estrogen receptor binding or volumes of sexually differentiated brain nuclei. Toxicol. Appl. Pharmacol. 127:258–67
    [Google Scholar]
  115. 115. 
    Negishi T, Shimomura H, Koyama T, Kawasaki K, Ishii Y et al. 2006. Gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin affects social behaviors between developing rhesus monkeys (Macaca mulatta). Toxicol. Lett. 160:233–44
    [Google Scholar]
  116. 116. 
    Sullivan PJ, Clark JJJ, Agardy FJ, Rosenfeld PF 2007. Synthetic chemicals in a balanced diet. Toxic Legacy: Synthetic Toxins in the Food, Water and Air of American Cities SJ Sullivan, JJJ Clark, FJ Hardy, PF Rosenfeld 37–87 Burlington, MA: Academic
    [Google Scholar]
  117. 117. 
    Bonner MR, Coble J, Blair A, Beane Freeman LE, Hoppin JA et al. 2007. Malathion exposure and the incidence of cancer in the agricultural health study. Am. J. Epidemiol. 166:1023–34
    [Google Scholar]
  118. 118. 
    Roberts JR, Reigart JR. 2013. Organophosphate insecticides. Recognition and Management of Pesticide Poisonings JR Roberts, JR Reigart 43–55 Washington, DC: US Environ. Prot. Agency https://www.epa.gov/sites/production/files/documents/rmpp_6thed_ch5_organophosphates.pdf
    [Google Scholar]
  119. 119. 
    Aldridge WN, Miles JW, Mount DL, Verschoyle RD 1979. The toxicological properties of impurities in malathion. Arch. Toxicol. 42:95–106
    [Google Scholar]
  120. 120. 
    Kralj MB, Černigoj U, Franko M, Trebše P 2007. Comparison of photocatalysis and photolysis of malathion, isomalathion, malaoxon, and commercial malathion—products and toxicity studies. Water Res 41:4504–14
    [Google Scholar]
  121. 121. 
    World Health Organ 2010. The WHO recommended classification of pesticides by hazard and guidelines to classification 2009 Rep., Int. Prog. Chem. Safety, World Health Organ Geneva: https://www.who.int/foodsafety/publications/classification-pesticides/en/
  122. 122. 
    Brouwer A, Ahlborg UG, van Leeuwen FX, Feeley MM 1998. Report of the WHO working group on the assessment of health risks for human infants from exposure to PCDDs, PCDFs and PCBs. Chemosphere 37:1627–43
    [Google Scholar]
  123. 123. 
    Jajoo M, Saxena S, Pandey M 2010. Transplacentally acquired organophosphorus poisoning in a newborn: case report. Ann. Trop. Paediatr. 30:137–39
    [Google Scholar]
  124. 124. 
    Eskenazi B, Bradman A, Castorina R 1999. Exposures of children to organophosphate pesticides and their potential adverse health effects. Environ. Health Perspect. 107:Suppl. 3409–19
    [Google Scholar]
  125. 125. 
    Chanda SM, Pope CN. 1996. Neurochemical and neurobehavioral effects of repeated gestational exposure to chlorpyrifos in maternal and developing rats. Pharmacol. Biochem. Behav. 53:771–76
    [Google Scholar]
  126. 126. 
    Lassiter TL, Barone S Jr, Moser VC, Padilla S 1999. Gestational exposure to chlorpyrifos: dose response profiles for cholinesterase and carboxylesterase activity. Toxicol. Sci 52:92–100
    [Google Scholar]
  127. 127. 
    Richardson JR, Chambers JE. 2004. Neurochemical effects of repeated gestational exposure to chlorpyrifos in developing rats. Toxicol. Sci. 77:83–90
    [Google Scholar]
  128. 128. 
    da Silva AP, Meotti FC, Santos AR, Farina M 2006. Lactational exposure to malathion inhibits brain acetylcholinesterase in mice. Neurotoxicology 27:1101–5
    [Google Scholar]
  129. 129. 
    Selmi S, El-Fazaa S, Gharbi N 2012. Oxidative stress and cholinesterase inhibition in plasma, erythrocyte and brain of rats’ pups following lactational exposure to malathion. Environ. Toxicol. Pharmacol. 34:753–60
    [Google Scholar]
  130. 130. 
    Chanda SM, Harp P, Liu J, Pope CN 1995. Comparative developmental and maternal neurotoxicity following acute gestational exposure to chlorpyrifos in rats. J. Toxicol. Environ. Health 44:189–202
    [Google Scholar]
  131. 131. 
    Qiao D, Seidler FJ, Abreu-Villaça Y, Tate CA, Cousins MM, Slotkin TA 2004. Chlorpyrifos exposure during neurulation: cholinergic synaptic dysfunction and cellular alterations in brain regions at adolescence and adulthood. Dev. Brain Res. 148:43–52
    [Google Scholar]
  132. 132. 
    Qiao D, Seidler FJ, Tate CA, Cousins MM, Slotkin TA 2003. Fetal chlorpyrifos exposure: adverse effects on brain cell development and cholinergic biomarkers emerge postnatally and continue into adolescence and adulthood. Environ. Health Perspect. 111:536–44
    [Google Scholar]
  133. 133. 
    Mullins RJ, Xu S, Pereira EF, Pescrille JD, Todd SW et al. 2015. Prenatal exposure of guinea pigs to the organophosphorus pesticide chlorpyrifos disrupts the structural and functional integrity of the brain. Neurotoxicology 48:9–20
    [Google Scholar]
  134. 134. 
    Garcia SJ, Seidler FJ, Slotkin TA 2003. Developmental neurotoxicity elicited by prenatal or postnatal chlorpyrifos exposure: effects on neurospecific proteins indicate changing vulnerabilities. Environ. Health Perspect. 111:297–303
    [Google Scholar]
  135. 135. 
    Garcia SJ, Seidler FJ, Qiao D, Slotkin TA 2002. Chlorpyrifos targets developing glia: effects on glial fibrillary acidic protein. Brain Res. Dev. Brain Res. 133:151–61
    [Google Scholar]
  136. 136. 
    Garcia SJ, Seidler FJ, Slotkin TA 2005. Developmental neurotoxicity of chlorpyrifos: targeting glial cells. Environ. Toxicol. Pharmacol. 19:455–61
    [Google Scholar]
  137. 137. 
    Salama M, Lotfy A, Fathy K, Makar M, El-Emam M et al. 2015. Developmental neurotoxic effects of malathion on 3D neurosphere system. Appl. Transl. Genom. 7:13–18
    [Google Scholar]
  138. 138. 
    Roy TS, Seidler FJ, Slotkin TA 2004. Morphologic effects of subtoxic neonatal chlorpyrifos exposure in developing rat brain: regionally selective alterations in neurons and glia. Brain Res. Dev. Brain Res. 148:197–206
    [Google Scholar]
  139. 139. 
    Aldridge JE, Seidler FJ, Meyer A, Thillai I, Slotkin TA 2003. Serotonergic systems targeted by developmental exposure to chlorpyrifos: effects during different critical periods. Environ. Health Perspect. 111:1736–43
    [Google Scholar]
  140. 140. 
    Aldridge JE, Meyer A, Seidler FJ, Slotkin TA 2005. Alterations in central nervous system serotonergic and dopaminergic synaptic activity in adulthood after prenatal or neonatal chlorpyrifos exposure. Environ. Health Perspect. 113:1027–31
    [Google Scholar]
  141. 141. 
    Chen XP, Wang X, Dong JY 2011. Different reaction patterns of dopamine content to prenatal exposure to chlorpyrifos in different periods. J. Appl. Toxicol. 31:355–59
    [Google Scholar]
  142. 142. 
    Zhang J, Dai H, Deng Y, Tian J, Zhang C et al. 2015. Neonatal chlorpyrifos exposure induces loss of dopaminergic neurons in young adult rats. Toxicology 336:17–25
    [Google Scholar]
  143. 143. 
    Slotkin TA, Seidler FJ. 2007. Prenatal chlorpyrifos exposure elicits presynaptic serotonergic and dopaminergic hyperactivity at adolescence: critical periods for regional and sex-selective effects. Reprod. Toxicol. 23:421–27
    [Google Scholar]
  144. 144. 
    Meyer A, Seidler FJ, Aldridge JE, Tate CA, Cousins MM, Slotkin TA 2004. Critical periods for chlorpyrifos-induced developmental neurotoxicity: alterations in adenylyl cyclase signaling in adult rat brain regions after gestational or neonatal exposure. Environ. Health Perspect. 112:295–301
    [Google Scholar]
  145. 145. 
    Venerosi A, Tait S, Stecca L, Chiarotti F, De Felice A et al. 2015. Effects of maternal chlorpyrifos diet on social investigation and brain neuroendocrine markers in the offspring—a mouse study. Environ. Health 14:32
    [Google Scholar]
  146. 146. 
    Haviland JA, Butz DE, Porter WP 2010. Long-term sex selective hormonal and behavior alterations in mice exposed to low doses of chlorpyrifos in utero. Reprod. Toxicol. 29:74–79
    [Google Scholar]
  147. 147. 
    De Felice A, Greco A, Calamandrei G, Minghetti L 2016. Prenatal exposure to the organophosphate insecticide chlorpyrifos enhances brain oxidative stress and prostaglandin E2 synthesis in a mouse model of idiopathic autism. J. Neuroinflamm. 13:149
    [Google Scholar]
  148. 148. 
    Ouardi FZ, Anarghou H, Malqui H, Ouasmi N, Chigr M et al. 2019. Gestational and lactational exposure to malathion affects antioxidant status and neurobehavior in mice pups and offspring. J. Mol. Neurosci. 69:17–27
    [Google Scholar]
  149. 149. 
    Eaton DL, Daroff RB, Autrup H, Bridges J, Buffler P et al. 2008. Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit. Rev. Toxicol. 38:Suppl. 21–125
    [Google Scholar]
  150. 150. 
    Silver MK, Shao J, Ji C, Zhu B, Xu L et al. 2018. Prenatal organophosphate insecticide exposure and infant sensory function. Int. J. Hyg. Environ. Health 221:469–78
    [Google Scholar]
  151. 151. 
    Silver MK, Shao J, Zhu B, Chen M, Xia Y et al. 2017. Prenatal naled and chlorpyrifos exposure is associated with deficits in infant motor function in a cohort of Chinese infants. Environ. Int. 106:248–56
    [Google Scholar]
  152. 152. 
    Wang Y, Zhang Y, Ji L, Hu Y, Zhang J et al. 2017. Prenatal and postnatal exposure to organophosphate pesticides and childhood neurodevelopment in Shandong, China. Environ. Int. 108:119–26
    [Google Scholar]
  153. 153. 
    Young JG, Eskenazi B, Gladstone EA, Bradman A, Pedersen L et al. 2005. Association between in utero organophosphate pesticide exposure and abnormal reflexes in neonates. Neurotoxicology 26:199–209
    [Google Scholar]
  154. 154. 
    Eskenazi B, Marks AR, Bradman A, Harley K, Barr DB et al. 2007. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ. Health Perspect. 115:792–98
    [Google Scholar]
  155. 155. 
    Bouchard MF, Chevrier J, Harley KG, Kogut K, Vedar M et al. 2011. Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ. Health Perspect. 119:1189–95
    [Google Scholar]
  156. 156. 
    Rauh VA, Garfinkel R, Perera FP, Andrews HF, Hoepner L et al. 2006. Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first 3 years of life among inner-city children. Pediatrics 118:e1845–59
    [Google Scholar]
  157. 157. 
    Rauh V, Arunajadai S, Horton M, Perera F, Hoepner L et al. 2011. Seven-year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ. Health Perspect. 119:1196–201
    [Google Scholar]
  158. 158. 
    Yolton K, Xu Y, Sucharew H, Succop P, Altaye M et al. 2013. Impact of low-level gestational exposure to organophosphate pesticides on neurobehavior in early infancy: a prospective study. Environ. Health 12:79
    [Google Scholar]
  159. 159. 
    Levin ED, Addy N, Baruah A, Elias A, Christopher NC et al. 2002. Prenatal chlorpyrifos exposure in rats causes persistent behavioral alterations. Neurotoxicol. Teratol. 24:733–41
    [Google Scholar]
  160. 160. 
    Icenogle LM, Christopher NC, Blackwelder WP, Caldwell DP, Qiao D et al. 2004. Behavioral alterations in adolescent and adult rats caused by a brief subtoxic exposure to chlorpyrifos during neurulation. Neurotoxicol. Teratol. 26:95–101
    [Google Scholar]
  161. 161. 
    Mamczarz J, Pescrille JD, Gavrushenko L, Burke RD, Fawcett WP et al. 2016. Spatial learning impairment in prepubertal guinea pigs prenatally exposed to the organophosphorus pesticide chlorpyrifos: toxicological implications. Neurotoxicology 56:17–28
    [Google Scholar]
  162. 162. 
    Venerosi A, Ricceri L, Scattoni ML, Calamandrei G 2009. Prenatal chlorpyrifos exposure alters motor behavior and ultrasonic vocalization in CD-1 mouse pups. Environ. Health 8:12
    [Google Scholar]
  163. 163. 
    De Felice A, Venerosi A, Ricceri L, Sabbioni M, Scattoni ML et al. 2014. Sex-dimorphic effects of gestational exposure to the organophosphate insecticide chlorpyrifos on social investigation in mice. Neurotoxicol. Teratol. 46:32–39
    [Google Scholar]
  164. 164. 
    N'Go PK, Azzaoui F-Z, Ahami AOT, Soro PR, Najimi M, Chigr F 2013. Developmental effects of Malathion exposure on locomotor activity and anxiety-like behavior in Wistar rat. Health 5:603–11
    [Google Scholar]
  165. 165. 
    Ricceri L, Venerosi A, Capone F, Cometa MF, Lorenzini P et al. 2006. Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice. Toxicol. Sci. 93:105–13
    [Google Scholar]
  166. 166. 
    Venerosi A, Ricceri L, Rungi A, Sanghez V, Calamandrei G 2010. Gestational exposure to the organophosphate chlorpyrifos alters social-emotional behaviour and impairs responsiveness to the serotonin transporter inhibitor fluvoxamine in mice. Psychopharmacology 208:99–107
    [Google Scholar]
  167. 167. 
    Braquenier JB, Quertemont E, Tirelli E, Plumier JC 2010. Anxiety in adult female mice following perinatal exposure to chlorpyrifos. Neurotoxicol. Teratol. 32:234–39
    [Google Scholar]
  168. 168. 
    Silva JG, Boareto AC, Schreiber AK, Redivo DD, Gambeta E et al. 2017. Chlorpyrifos induces anxiety-like behavior in offspring rats exposed during pregnancy. Neurosci. Lett. 641:94–100
    [Google Scholar]
  169. 169. 
    Carr RL, Armstrong NH, Buchanan AT, Eells JB, Mohammed AN et al. 2017. Decreased anxiety in juvenile rats following exposure to low levels of chlorpyrifos during development. Neurotoxicology 59:183–90
    [Google Scholar]
  170. 170. 
    Costa LG, Giordano G, Tagliaferri S, Caglieri A, Mutti A 2008. Polybrominated diphenyl ether (PBDE) flame retardants: environmental contamination, human body burden and potential adverse health effects. Acta Biomed 79:172–83
    [Google Scholar]
  171. 171. 
    Darnerud PO, Eriksen GS, Johannesson T, Larsen PB, Viluksela M 2001. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ. Health Perspect. 109:Suppl. 149–68
    [Google Scholar]
  172. 172. 
    Hooper K, McDonald TA. 2000. The PBDEs: an emerging environmental challenge and another reason for breast-milk monitoring programs. Environ. Health Perspect. 108:387–92
    [Google Scholar]
  173. 173. 
    Phillips AL, Chen A, Rock KD, Horman B, Patisaul HB, Stapleton HM 2016. Transplacental and lactational transfer of Firemaster® 550 components in dosed Wistar rats. Toxicol. Sci. 153:246–57
    [Google Scholar]
  174. 174. 
    Meerts IA, Letcher RJ, Hoving S, Marsh G, Bergman A et al. 2001. In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PDBEs, and polybrominated bisphenol A compounds. Environ. Health Perspect. 109:399–407
    [Google Scholar]
  175. 175. 
    Ren XM, Guo LH, Gao Y, Zhang BT, Wan B 2013. Hydroxylated polybrominated diphenyl ethers exhibit different activities on thyroid hormone receptors depending on their degree of bromination. Toxicol. Appl. Pharmacol. 268:256–63
    [Google Scholar]
  176. 176. 
    Stoker TE, Cooper RL, Lambright CS, Wilson VS, Furr J, Gray LE 2005. In vivo and in vitro anti-androgenic effects of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture. Toxicol. Appl. Pharmacol. 207:78–88
    [Google Scholar]
  177. 177. 
    Yang W, Mu Y, Giesy JP, Zhang A, Yu H 2009. Anti-androgen activity of polybrominated diphenyl ethers determined by comparative molecular similarity indices and molecular docking. Chemosphere 75:1159–64
    [Google Scholar]
  178. 178. 
    Costa LG, Giordano G. 2011. Is decabromodiphenyl ether (BDE-209) a developmental neurotoxicant. Neurotoxicology 32:9–24
    [Google Scholar]
  179. 179. 
    Szabo DT, Richardson VM, Ross DG, Diliberto JJ, Kodavanti PR, Birnbaum LS 2009. Effects of perinatal PBDE exposure on hepatic phase I, phase II, phase III, and deiodinase 1 gene expression involved in thyroid hormone metabolism in male rat pups. Toxicol. Sci. 107:27–39
    [Google Scholar]
  180. 180. 
    Rice DC, Reeve EA, Herlihy A, Zoeller RT, Thompson WD, Markowski VP 2007. Developmental delays and locomotor activity in the C57BL6/J mouse following neonatal exposure to the fully-brominated PBDE, decabromodiphenyl ether. Neurotoxicol. Teratol. 29:511–20
    [Google Scholar]
  181. 181. 
    Kodavanti PR, Coburn CG, Moser VC, MacPhail RC, Fenton SE et al. 2010. Developmental exposure to a commercial PBDE mixture, DE-71: neurobehavioral, hormonal, and reproductive effects. Toxicol. Sci. 116:297–312
    [Google Scholar]
  182. 182. 
    Fujimoto H, Woo GH, Inoue K, Takahashi M, Hirose M et al. 2011. Impaired oligodendroglial development by decabromodiphenyl ether in rat offspring after maternal exposure from mid-gestation through lactation. Reprod. Toxicol. 31:86–94
    [Google Scholar]
  183. 183. 
    Lin SM, Chen FA, Huang YF, Hsing LL, Chen LL et al. 2011. Negative associations between PBDE levels and thyroid hormones in cord blood. Int. J. Hyg. Environ. Health 214:115–20
    [Google Scholar]
  184. 184. 
    Vuong AM, Braun JM, Webster GM, Zoeller RT, Hoofnagle AN et al. 2018. Polybrominated diphenyl ether (PBDE) exposures and thyroid hormones in children at age 3 years. Environ. Int. 117:339–47
    [Google Scholar]
  185. 185. 
    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 27:279–88
    [Google Scholar]
  186. 186. 
    Kim TH, Lee YJ, Lee E, Kim MS, Kwack SJ et al. 2009. Effects of gestational exposure to decabromodiphenyl ether on reproductive parameters, thyroid hormone levels, and neuronal development in Sprague-Dawley rats offspring. J. Toxicol. Environ. Health A 72:1296–303
    [Google Scholar]
  187. 187. 
    Chevrier J, Harley KG, Bradman A, Sjodin A, Eskenazi B 2011. Prenatal exposure to polybrominated diphenyl ether flame retardants and neonatal thyroid-stimulating hormone levels in the CHAMACOS study. Am. J. Epidemiol. 174:1166–74
    [Google Scholar]
  188. 188. 
    Bernal J. 2005. Thyroid hormones and brain development. Vitam. Horm. 71:95–122
    [Google Scholar]
  189. 189. 
    Alm H, Kultima K, Scholz B, Nilsson A, Andren PE et al. 2008. Exposure to brominated flame retardant PBDE-99 affects cytoskeletal protein expression in the neonatal mouse cerebral cortex. Neurotoxicology 29:628–37
    [Google Scholar]
  190. 190. 
    Viberg H, Eriksson P. 2011. Differences in neonatal neurotoxicity of brominated flame retardants, PBDE 99 and TBBPA, in mice. Toxicology 289:59–65
    [Google Scholar]
  191. 191. 
    Viberg H. 2003. Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol. Appl. Pharmacol. 192:95–106
    [Google Scholar]
  192. 192. 
    Hallgren S, Fredriksson A, Viberg H 2015. More signs of neurotoxicity of surfactants and flame retardants—neonatal PFOS and PBDE 99 cause transcriptional alterations in cholinergic genes in the mouse CNS. Environ. Toxicol. Pharmacol. 40:409–16
    [Google Scholar]
  193. 193. 
    Sun W, Du L, Tang W, Kuang L, Du P et al. 2017. PBDE-209 exposure damages learning and memory ability in rats potentially through increased autophagy and apoptosis in the hippocampus neuron. Environ. Toxicol. Pharmacol. 50:151–58
    [Google Scholar]
  194. 194. 
    Cheng J, Gu J, Ma J, Chen X, Zhang M, Wang W 2009. Neurobehavioural effects, redox responses and tissue distribution in rat offspring developmental exposure to BDE-99. Chemosphere 75:963–68
    [Google Scholar]
  195. 195. 
    Johansson N, Viberg H, Fredriksson A, Eriksson P 2008. Neonatal exposure to deca-brominated diphenyl ether (PBDE 209) causes dose-response changes in spontaneous behaviour and cholinergic susceptibility in adult mice. Neurotoxicology 29:911–19
    [Google Scholar]
  196. 196. 
    Haave M, Folven KI, Carroll T, Glover C, Heegaard E et al. 2011. Cerebral gene expression and neurobehavioural development after perinatal exposure to an environmentally relevant polybrominated diphenylether (BDE47). Cell Biol. Toxicol. 27:343–61
    [Google Scholar]
  197. 197. 
    Faass O, Ceccatelli R, Schlumpf M, Lichtensteiger W 2013. Developmental effects of perinatal exposure to PBDE and PCB on gene expression in sexually dimorphic rat brain regions and female sexual behavior. Gen. Comp. Endocrinol. 188:232–41
    [Google Scholar]
  198. 198. 
    Lilienthal H, Hack A, Roth-Harer A, Grande SW, Talsness CE 2006. Effects of developmental exposure to 2,2,4,4,5-pentabromodiphenyl ether (PBDE-99) on sex steroids, sexual development, and sexually dimorphic behavior in rats. Environ. Health Perspect. 114:194–201
    [Google Scholar]
  199. 199. 
    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. 113:149–54
    [Google Scholar]
  200. 200. 
    Llansola M, Erceg S, Monfort P, Montoliu C, Felipo V 2007. Prenatal exposure to polybrominated diphenylether 99 enhances the function of the glutamate-nitric oxide-cGMP pathway in brain in vivo and in cultured neurons. Eur. J. Neurosci. 25:373–79
    [Google Scholar]
  201. 201. 
    Xing T, Chen L, Tao Y, Wang M, Chen J, Ruan DY 2009. Effects of decabrominated diphenyl ether (PBDE 209) exposure at different developmental periods on synaptic plasticity in the dentate gyrus of adult rats in vivo. Toxicol. Sci. 110:401–10
    [Google Scholar]
  202. 202. 
    Donauer S, Chen A, Xu Y, Calafat AM, Sjodin A, Yolton K 2015. Prenatal exposure to polybrominated diphenyl ethers and polyfluoroalkyl chemicals and infant neurobehavior. J. Pediatr. 166:736–42
    [Google Scholar]
  203. 203. 
    Vuong AM, Yolton K, Webster GM, Sjodin A, Calafat AM et al. 2016. Prenatal polybrominated diphenyl ether and perfluoroalkyl substance exposures and executive function in school-age children. Environ. Res. 147:556–64
    [Google Scholar]
  204. 204. 
    Zhang H, Yolton K, Webster GM, Sjodin A, Calafat AM et al. 2017. Prenatal PBDE and PCB exposures and reading, cognition, and externalizing behavior in children. Environ. Health Perspect. 125:746–52
    [Google Scholar]
  205. 205. 
    Vuong AM, Yolton K, Poston KL, Xie C, Webster GM et al. 2017. Prenatal and postnatal polybrominated diphenyl ether (PBDE) exposure and measures of inattention and impulsivity in children. Neurotoxicol. Teratol. 64:20–28
    [Google Scholar]
  206. 206. 
    Vuong AM, Braun JM, Yolton K, Xie C, Webster GM et al. 2017. Prenatal and postnatal polybrominated diphenyl ether exposure and visual spatial abilities in children. Environ. Res. 153:83–92
    [Google Scholar]
  207. 207. 
    Ding G, Yu J, Cui C, Chen L, Gao Y et al. 2015. Association between prenatal exposure to polybrominated diphenyl ethers and young children's neurodevelopment in China. Environ. Res. 142:104–11
    [Google Scholar]
  208. 208. 
    Gascon M, Fort M, Martinez D, Carsin AE, Forns J et al. 2012. Polybrominated diphenyl ethers (PBDEs) in breast milk and neuropsychological development in infants. Environ. Health Perspect. 120:1760–65
    [Google Scholar]
  209. 209. 
    Eskenazi B, Chevrier J, Rauch SA, Kogut K, Harley KG et al. 2013. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ. Health Perspect. 121:257–62
    [Google Scholar]
  210. 210. 
    Sagiv SK, Kogut K, Gaspar FW, Gunier RB, Harley KG et al. 2015. Prenatal and childhood polybrominated diphenyl ether (PBDE) exposure and attention and executive function at 9–12 years of age. Neurotoxicol. Teratol. 52:151–61
    [Google Scholar]
  211. 211. 
    Herbstman JB, Sjodin A, Kurzon M, Lederman SA, Jones RS et al. 2010. Prenatal exposure to PBDEs and neurodevelopment. Environ. Health Perspect. 118:712–19
    [Google Scholar]
  212. 212. 
    Cowell WJ, Lederman SA, Sjodin A, Jones R, Wang S et al. 2015. Prenatal exposure to polybrominated diphenyl ethers and child attention problems at 3–7 years. Neurotoxicol. Teratol. 52:143–50
    [Google Scholar]
  213. 213. 
    Cowell WJ, Margolis A, Rauh VA, Sjodin A, Jones R et al. 2018. Associations between prenatal and childhood PBDE exposure and early adolescent visual, verbal and working memory. Environ. Int. 118:9–16
    [Google Scholar]
  214. 214. 
    Branchi I, Alleva E, Costa LG 2002. Effects of perinatal exposure to a polybrominated diphenyl ether (PBDE 99) on mouse neurobehavioural development. Neurotoxicology 23:375–84
    [Google Scholar]
  215. 215. 
    Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A et al. 2006. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–76
    [Google Scholar]
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