Abstract
The developmental origins of health and disease (DOHaD) paradigm, which was first presented as the Barker hypothesis, has been widely accepted in a variety of medical disciplines, ranging from public health to internal medicine, nutritional sciences, gynecology, pediatrics, and environmental health. Prenatal exposure to industrial chemicals at low doses has been shown to have a critical window during gestation and induce abnormalities later in life following a definite latent period. Such exposure scenarios can now be considered as a critical component that may act as initiating or modifying factors for health and disease status later in life and support the DOHaD paradigm. Exogenous chemicals include methylmercury, pesticides (organophosphates and neonicotinoids), tobacco, polychlorinated biphenyls and dioxins, and diethylstilbestrol, and their late-onset health outcomes include cancers and neurocognitive behavioral abnormalities. In order to understand the DOHaD paradigm, attention needs to be drawn to chemical exposure during the early life stages. Subtle alterations in developmental neurotoxicity that can only be detected by cutting-edge technology using a hypothesis-driven approach are discussed in the present study.
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Abbreviations
- ADI:
-
Allowable daily intake
- AhR:
-
Aryl hydrocarbon receptor
- AVPV:
-
Anteroventral periventricular nucleus
- BPA:
-
Bisphenol A
- CPF:
-
Chlorpyrifos
- DES:
-
Diethylstilbestrol
- DL:
-
Dioxin-like
- DOHaD:
-
Developmental origins of health and disease
- EDCs:
-
Endocrine-disrupting chemicals
- FOAD:
-
Fetal origins of adult disease
- JECFA:
-
Joint FAO/WHO Expert Committee on Food Additives
- MPOA:
-
Medial preoptic area
- nAChR:
-
Nicotinic acetylcholine receptor
- PCB:
-
Polychlorinated biphenyl
- PCDD:
-
Polychlorinated dibenzo-p-dioxin
- PCDF:
-
Polychlorinated dibenzofuran
- TCDD:
-
2,3,7,8-tetrachlorodibenzo-p-dioxin
References
Inadera H. Developmental origins of obesity and type 2 diabetes: molecular aspects and role of chemicals. Environ Health Prev Med. 2013;18(3):185–97. https://doi.org/10.1007/s12199-013-0328-8.
Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359(1):61–73. https://doi.org/10.1056/NEJMra0708473.
Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4(2B):611–24.
Gillman MW, Barker D, Bier D, Cagampang F, Challis J, Fall C, et al. Meeting report on the 3rd International Congress on Developmental Origins of Health and Disease (DOHaD). Pediatr Res. 2007;61(5 Pt 1):625–9. https://doi.org/10.1203/pdr.0b013e3180459fcd.
Colborn T. Pesticides—how research has succeeded and failed to translate science into policy: endocrinological effects on wildlife. Environ Health Perspect. 1995;103(Suppl 6):81–5.
Colborn T, Dumanoski D, Myers JP. Our stolen future: are we threatening our fertility, intelligence, and survival?—a scientific detective story. New York: The Spieler Agency; 1996.
International Programme on Chemical Safety. Global assessment of the state-of-the-science of endocrine disruptors. Geneva: World Health Organisation; 2002.
Barker DJ, Eriksson JG, Forsen T, Osmond C. Infant growth and income 50 years later. Arch Dis Child. 2005;90(3):272–3. https://doi.org/10.1136/adc.2003.033464.
Grun F, Blumberg B. Perturbed nuclear receptor signaling by environmental obesogens as emerging factors in the obesity crisis. Rev Endocr Metab Disord. 2007;8(2):161–71. https://doi.org/10.1007/s11154-007-9049-x.
Bezek S, Ujhazy E, Mach M, Navarova J, Dubovicky M. Developmental origin of chronic diseases: toxicological implication. Interdiscip Toxicol. 2008;1(1):29–31. https://doi.org/10.2478/v10102-010-0029-8.
Grandjean P, Bellinger D, Bergman A, Cordier S, Davey-Smith G, Eskenazi B, et al. The faroes statement: human health effects of developmental exposure to chemicals in our environment. Basic Clin Pharmacol Toxicol. 2008;102(2):73–5. https://doi.org/10.1111/j.1742-7843.2007.00114.x.
Rosenfeld CS. Effects of maternal diet and exposure to bisphenol A on sexually dimorphic responses in conceptuses and offspring. Reprod Domest Anim. 2012;47(Suppl 4):23–30. https://doi.org/10.1111/j.1439-0531.2012.02051.x.
Heindel JJ, Skalla LA, Joubert BR, Dilworth CH, Gray KA. Review of developmental origins of health and disease publications in environmental epidemiology. Reprod Toxicol. 2017;68:34–48. https://doi.org/10.1016/j.reprotox.2016.11.011.
Harada M. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol. 1995;25(1):1–24. https://doi.org/10.3109/10408449509089885.
Newbold RR. Prenatal exposure to diethylstilbestrol and long-term impact on the breast and reproductive tract in humans and mice. J Dev Orig Health Dis. 2012;3(2):73–82. https://doi.org/10.1017/S2040174411000754.
National Cancer Institute. Diethylstilbestrol (DES) and Cancer. https://www.cancer.gov/about-cancer/causes-prevention/risk/hormones/des-fact-sheet.
Larson PS, Ungarelli RA, de Las Morenas A, Cupples LA, Rowlings K, Palmer JR, et al. In utero exposure to diethylstilbestrol (DES) does not increase genomic instability in normal or neoplastic breast epithelium. Cancer. 2006;107(9):2122–6. https://doi.org/10.1002/cncr.22223.
Mizutani T. DES Yakugai. Tokyo: Hon-no-izumi Co.; 2004.
McLachlan JA, Newbold RR, Bullock B. Reproductive tract lesions in male mice exposed prenatally to diethylstilbestrol. Science. 1975;190(4218):991–2.
Nomura T, Kanzaki T. Induction of urogenital anomalies and some tumors in the progeny of mice receiving diethylstilbestrol during pregnancy. Cancer Res. 1977;37(4):1099–104.
Weisburger JH. Nakahara memorial lecture. Application of the mechanisms of nutritional carcinogenesis to the prevention of cancer. Princess Takamatsu Symp. 1985;16:11–26.
Abel EL, Angel JM, Kiguchi K, DiGiovanni J. Multi-stage chemical carcinogenesis in mouse skin: fundamentals and applications. Nat Protoc. 2009;4(9):1350–62. https://doi.org/10.1038/nprot.2009.120.
Newbold RR, McLachlan JA. Vaginal adenosis and adenocarcinoma in mice exposed prenatally or neonatally to diethylstilbestrol. Cancer Res. 1982;42(5):2003–11.
Tohyama C. Developmental neurotoxicity guidelines: problems and perspectives. J Toxicol Sci. 2016;41(Special):SP69–79. https://doi.org/10.2131/jts.41.SP69.
Grandjean P, Landrigan PJ. Neurobehavioural effects of developmental toxicity. Lancet Neurol. 2014;13(3):330–8. https://doi.org/10.1016/S1474-4422(13)70278-3.
WHO. Evaluation of certain food additives and contaminants. Sixty-first report of the Joint FAO/WHO Expert Committee on Food Additives. Geneva: WHO; 2004.
WHO. Arsenic fact sheet. 2016. http://www.who.int/mediacentre/factsheets/fs372/en/.
Smith AH, Marshall G, Liaw J, Yuan Y, Ferreccio C, Steinmaus C. Mortality in young adults following in utero and childhood exposure to arsenic in drinking water. Environ Health Perspect. 2012;120(11):1527–31. https://doi.org/10.1289/ehp.1104867.
Steinmaus CM, Ferreccio C, Romo JA, Yuan Y, Cortes S, Marshall G, et al. Drinking water arsenic in northern Chile: high cancer risks 40 years after exposure cessation. Cancer Epidemiol Biomark Prev. 2013;22(4):623–30. https://doi.org/10.1158/1055-9965.EPI-12-1190.
Cohen G, Jeffery H, Lagercrantz H, Katz-Salamon M. Long-term reprogramming of cardiovascular function in infants of active smokers. Hypertension. 2010;55(3):722–8. https://doi.org/10.1161/HYPERTENSIONAHA.109.142695.
Ekblad M, Korkeila J, Lehtonen L. Smoking during pregnancy affects foetal brain development. Acta Paediatr. 2015;104(1):12–8. https://doi.org/10.1111/apa.12791.
Xiao D, Huang X, Yang S, Zhang L. Direct effects of nicotine on contractility of the uterine artery in pregnancy. J Pharmacol Exp Ther. 2007;322(1):180–5. https://doi.org/10.1124/jpet.107.119354.
Chen R, Clifford A, Lang L, Anstey KJ. Is exposure to secondhand smoke associated with cognitive parameters of children and adolescents?—a systematic literature review. Ann Epidemiol. 2013;23(10):652–61. https://doi.org/10.1016/j.annepidem.2013.07.001.
Herrmann M, King K, Weitzman M. Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment. Curr Opin Pediatr. 2008;20(2):184–90. https://doi.org/10.1097/MOP.0b013e3282f56165.
Council on Environmental Health. Pesticide exposure in children. Pediatrics. 2012;130(6):e1757–63. https://doi.org/10.1542/peds.2012-2757.
Bouchard MF, Bellinger DC, Wright RO, Weisskopf MG. Attention-deficit/hyperactivity disorder and urinary metabolites of organophosphate pesticides. Pediatrics. 2010;125(6):e1270–7. https://doi.org/10.1542/peds.2009-3058.
Bouchard MF, Chevrier J, Harley KG, Kogut K, Vedar M, Calderon N, et al. Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ Health Perspect. 2011;119(8):1189–95. https://doi.org/10.1289/ehp.1003185.
Rauh V, Arunajadai S, Horton M, Perera F, Hoepner L, Barr DB, et al. Seven-year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ Health Perspect. 2011;119(8):1196–201. https://doi.org/10.1289/ehp.1003160.
Rauh VA, Perera FP, Horton MK, Whyatt RM, Bansal R, Hao X, et al. Brain anomalies in children exposed prenatally to a common organophosphate pesticide. Proc Natl Acad Sci U S A. 2012;109(20):7871–6. https://doi.org/10.1073/pnas.1203396109.
Sanchez-Santed F, Colomina MT, Herrero Hernandez E. Organophosphate pesticide exposure and neurodegeneration. Cortex. 2016;74:417–26. https://doi.org/10.1016/j.cortex.2015.10.003.
Stallones L, Beseler CL. Assessing the connection between organophosphate pesticide poisoning and mental health: a comparison of neuropsychological symptoms from clinical observations, animal models and epidemiological studies. Cortex. 2016;74:405–16. https://doi.org/10.1016/j.cortex.2015.10.002.
Lu C, Toepel K, Irish R, Fenske RA, Barr DB, Bravo R. Organic diets significantly lower children’s dietary exposure to organophosphorus pesticides. Environ Health Perspect. 2006;114(2):260–3.
Sadaria AM, Supowit SD, Halden RU. Halden mass balance assessment for six neonicotinoid insecticides during conventional wastewater and wetland treatment: nationwide reconnaissance in United States wastewater. Environ Sci Technol. 2016;50:6199–206. https://doi.org/10.1021/acs.est.6b01032.
Ueyama J, Harada KH, Koizumi A, Sugiura Y, Kondo T, Saito I, et al. Temporal levels of urinary neonicotinoid and dialkylphosphate concentrations in Japanese women between 1994 and 2011. Environ Sci Technol. 2015;49(24):14522–8. https://doi.org/10.1021/acs.est.5b03062.
Osaka A, Ueyama J, Kondo T, Nomura H, Sugiura Y, Saito I, et al. Exposure characterization of three major insecticide lines in urine of young children in Japan-neonicotinoids, organophosphates, and pyrethroids. Environ Res. 2016;147:89–96. https://doi.org/10.1016/j.envres.2016.01.028.
Sano K, Isobe T, Yang J, Win-Shwe TT, Yoshikane M, Nakayama SF, et al. In utero and lactational exposure to acetamiprid induces abnormalities in socio-sexual and anxiety-related behaviors of male mice. Front Neurosci. 2016;10:228. https://doi.org/10.3389/fnins.2016.00228.
Kimura-Kuroda J, Komuta Y, Kuroda Y, Hayashi M, Kawano H. Nicotine-like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PLoS One. 2012;7(2):e32432. https://doi.org/10.1371/journal.pone.0032432.
Schecter A, Gasiewicz TA, editors. Dioxin and health. 2nd ed. Hoboken: Wiley; 2005. https://doi.org/10.1002/0471722014.
Yoshioka W, Peterson RE, Tohyama C. Molecular targets that link dioxin exposure to toxicity phenotypes. J Steroid Biochem Mol Biol. 2011;127(1–2):96–101. https://doi.org/10.1016/j.jsbmb.2010.12.005.
Myers JP, vom Saal FS, Akingbemi BT, Arizono K, Belcher S, Colborn T, et al. Why public health agencies cannot depend on good laboratory practices as a criterion for selecting data: the case of bisphenol A. Environ Health Perspect. 2009;117(3):309–15. https://doi.org/10.1289/ehp.0800173.
Konkle AT, McCarthy MM. Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology. 2011;152(1):223–35. https://doi.org/10.1210/en.2010-0607.
EFSA Panel on Food Contact Materials, Enzymes, Flavourings and Processing Aids. Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs: executive summary. 2015. https://efsa.onlinelibrary.wiley.com/doi/abs/10.2903/j.efsa.2015.3978. Accessed 20 Sept 2018.
Leranth C, Hajszan T, Szigeti-Buck K, Bober J, MacLusky NJ. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci U S A. 2008;105(37):14187–91. https://doi.org/10.1073/pnas.0806139105.
MacLusky NJ, Hajszan T, Leranth C. The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ Health Perspect. 2005;113(6):675–9.
Kimura E, Matsuyoshi C, Miyazaki W, Benner S, Hosokawa M, Yokoyama K, et al. Prenatal exposure to bisphenol A impacts neuronal morphology in the hippocampal CA1 region in developing and aged mice. Arch Toxicol. 2016;90(3):691–700. https://doi.org/10.1007/s00204-015-1485-x.
Poimenova A, Markaki E, Rahiotis C, Kitraki E. Corticosterone-regulated actions in the rat brain are affected by perinatal exposure to low dose of bisphenol A. Neuroscience. 2010;167(3):741–9. https://doi.org/10.1016/j.neuroscience.2010.02.051.
Tian YH, Baek JH, Lee SY, Jang CG. Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice. Synapse. 2010;64(6):432–9. https://doi.org/10.1002/syn.20746.
Xu X, Hong X, Xie L, Li T, Yang Y, Zhang Q, et al. Gestational and lactational exposure to bisphenol-A affects anxiety- and depression-like behaviors in mice. Horm Behav. 2012;62(4):480–90.
Luo G, Wang S, Li Z, Wei R, Zhang L, Liu H, et al. Maternal bisphenol a diet induces anxiety-like behavior in female juvenile with neuroimmune activation. Toxicol Sci. 2014;140(2):364–73. https://doi.org/10.1093/toxsci/kfu085.
Wolstenholme JT, Goldsby JA, Rissman EF. Transgenerational effects of prenatal bisphenol A on social recognition. Horm Behav. 2013;64(5):833–9. https://doi.org/10.1016/j.yhbeh.2013.09.007.
Walker DM, Gore AC. Epigenetic impacts of endocrine disruptors in the brain. Front Neuroendocrinol. 2017;44:1–26. https://doi.org/10.1016/j.yfrne.2016.09.002.
Endo T, Kakeyama M, Uemura Y, Haijima A, Okuno H, Bito H, et al. Executive function deficits and social-behavioral abnormality in mice exposed to a low dose of dioxin in utero and via lactation. PLoS One. 2012;7(12):e50741. https://doi.org/10.1371/journal.pone.0050741.
Haijima A, Endo T, Zhang Y, Miyazaki W, Kakeyama M, Tohyama C. In utero and lactational exposure to low doses of chlorinated and brominated dioxins induces deficits in the fear memory of male mice. Neurotoxicology. 2010;31(4):385–90. https://doi.org/10.1016/j.neuro.2010.04.004.
Hojo R, Stern S, Zareba G, Markowski VP, Cox C, Kost JT, et al. Sexually dimorphic behavioral responses to prenatal dioxin exposure. Environ Health Perspect. 2002;110(3):247–54.
Ishihara K, Warita K, Tanida T, Sugawara T, Kitagawa H, Hoshi N. Does paternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) affect the sex ratio of offspring? J Vet Med Sci. 2007;69(4):347–52.
Kakeyama M, Endo T, Zhang Y, Miyazaki W, Tohyama C. Disruption of paired-associate learning in rat offspring perinatally exposed to dioxins. Arch Toxicol. 2014;88(3):789–98. https://doi.org/10.1007/s00204-013-1161-y.
Markowski VP, Zareba G, Stern S, Cox C, Weiss B. Altered operant responding for motor reinforcement and the determination of benchmark doses following perinatal exposure to low-level 2,3,7,8-tetrachlorodibenzo-p-dioxin. Environ Health Perspect. 2001;109(6):621–7.
Mitsui T, Sugiyama N, Maeda S, Tohyama C, Arita J. Perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin suppresses contextual fear conditioning-accompanied activation of cyclic AMP response element-binding protein in the hippocampal CA1 region of male rats. Neurosci Lett. 2006;398(3):206–10. https://doi.org/10.1016/j.neulet.2005.12.087.
Schantz SL, Seo BW, Moshtaghian J, Peterson RE, Moore RW. Effects of gestational and lactational exposure to TCDD or coplanar PCBs on spatial learning. Neurotoxicol Teratol. 1996;18(3):305–13.
Kimura E, Kubo K, Matsuyoshi C, Benner S, Hosokawa M, Endo T, et al. Developmental origin of abnormal dendritic growth in the mouse brain induced by in utero disruption of aryl hydrocarbon receptor signaling. Neurotoxicol Teratol. 2015;52(Pt A):42–50. https://doi.org/10.1016/j.ntt.2015.10.005.
Hood DB, Woods L, Brown L, Johnson S, Ebner FF. Gestational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure effects on sensory cortex function. Neurotoxicology. 2006;27(6):1032–42. https://doi.org/10.1016/j.neuro.2006.05.022.
Kakeyama M, Sone H, Miyabara Y, Tohyama C. Perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin alters activity-dependent expression of BDNF mRNA in the neocortex and male rat sexual behavior in adulthood. Neurotoxicology. 2003;24(2):207–17. https://doi.org/10.1016/S0161-813X(02)00214-0.
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Tohyama, C. (2019). Maternal Exposure to Environmental Chemicals and Health Outcomes Later in Life. In: Sata, F., Fukuoka, H., Hanson, M. (eds) Pre-emptive Medicine: Public Health Aspects of Developmental Origins of Health and Disease. Current Topics in Environmental Health and Preventive Medicine. Springer, Singapore. https://doi.org/10.1007/978-981-13-2194-8_1
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