Effects of exposure to polychlorinated biphenyls and organochlorine pesticides on thyroid function during pregnancy

American Journal of Epidemiology

Volumn 168, Issue 3, 2008, Pages 298-310

  Chevrier, Jonathan ^a,b   Eskenazi, Brenda ^a,b   Holland, Nina ^a,b   Bradman, Asa ^a   Barr, Dana B ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL CENTER FOR ENVIRONMENTAL HEALTH   (United States)

Author keywords

DDT; Dichlorodiphenyl dichloroethylene; Hexachlorobenzene; Hydrocarbons, chlorinated; Polychlorinated biphenyls; Pregnancy; Thyroid hormones

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; CHLORPHENOTANE; HEXACHLOROBENZENE; ORGANOCHLORINE PESTICIDE; POLYCHLORINATED BIPHENYL; THYROID HORMONE; THYROTROPIN; THYROXINE;

EMBRYONIC DEVELOPMENT; HEALTH IMPACT; HORMONE; MULTIVARIATE ANALYSIS; NEUROLOGY; ORGANOCHLORINE; PCB; PESTICIDE; POLLUTION EFFECT; POLLUTION EXPOSURE; PREGNANCY; SERUM;

ADULT; ARTICLE; CHILD; CONTROLLED STUDY; COVARIANCE; DATA ANALYSIS; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS DEVELOPMENT; FREE THYROXINE INDEX; HEALTH HAZARD; HUMAN; HUMAN EXPERIMENT; LINEAR REGRESSION ANALYSIS; MALE; MULTIVARIATE ANALYSIS; NERVE CELL DIFFERENTIATION; PREGNANT WOMAN; PRENATAL EXPOSURE; THYROID FUNCTION; THYROID HORMONE BLOOD LEVEL; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; UNITED STATES;

ADOLESCENT; ADULT; BIOLOGICAL MARKERS; CALIFORNIA; COHORT STUDIES; DICHLORODIPHENYL DICHLOROETHYLENE; ENVIRONMENTAL MONITORING; FEMALE; HEXACHLOROBENZENE; HUMANS; HYDROCARBONS, CHLORINATED; INSECTICIDES; MATERNAL EXPOSURE; MEXICAN AMERICANS; PESTICIDES; POLYCHLORINATED BIPHENYLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RETROSPECTIVE STUDIES; THYROID GLAND; THYROTROPIN; THYROXINE;

CALIFORNIA; NORTH AMERICA; SALINAS VALLEY; UNITED STATES;

EID: 47649120165     PISSN: 00029262     EISSN: 14766256     Source Type: Journal    
DOI: 10.1093/aje/kwn136     Document Type: Article

References (73)

1. Needham LL, Ozkaynak H, Whyatt RM, et al. Exposure assessment in the National Children's Study: introduction. Environ Health Perspect 2005;113:1076-82.
2. United Nations Environment Programme. Final act of the Conference of Plenipotentiaries on the Stockholm Convention on Persistent Organic Pollutants. New York, NY: United Nations Environment Programme, 2001.
3. Agency for Toxic Substances and Disease Registry, Centers for Disease Control and Prevention. Toxicological profile for polychlorinated biphenyls (PCBs). Atlanta, GA: Centers for Disease Control and Prevention, 2000:948.
4. Agency for Toxic Substances and Disease Registry, Centers for Disease Control and Prevention. Toxicological profile for hexachlorobenzene. Atlanta, GA: Centers for Disease Control and Prevention, 2002:352.
5. World Health Organization. Indoor residual spraying: use of indoor residual spraying for scaling up global malaria control and elimination. WHO Position Statement. Geneva, Switzerland: World Health Organization, 2006.
6. Grandjean P, Weihe P, Burse VW, et al. Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol Teratol 2001;23:305-17.
7. Jacobson JL, Jacobson SW. Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N Engl J Med 1996;335:783-9.
8. Jacobson JL, Jacobson SW, Humphrey HE. Effects of in utero exposure to polychlorinated biphenyls and related contaminants on cognitive functioning in young children. J Pediatr 1990;116:38-45.
9. Jacobson SW, Fein GG, Jacobson JL, et al. The effect of intrauterine PCB exposure on visual recognition memory. Child Dev 1985;56:853-60.
10. Koopman-Esseboom C, Weisglas-Kuperus N, de Ridder MA, et al. Effects of polychlorinated biphenyl/dioxin exposure and feeding type on infants' mental and psychomotor development. Pediatrics 1996;97:700-6.
11. Rogan WJ, Gladen BC. PCBs, DDE, and child development at 18 and 24 months. Ann Epidemiol 1991;1:407-13.
12. Rogan WJ, Gladen BC, McKinney JD, et al. Neonatal effects of transplacental exposure to PCBs and DDE. J Pediatr 1986;109:335-41.
13. Lilienthal H, Benthe C, Heinzow B, et al. Impairment of schedule-controlled behavior by pre- and postnatal exposure to hexachlorobenzene in rats. Arch Toxicol 1996;70:174-81.
14. Sala M, Ribas-Fitó N, de Muga LE. Hexachlorobenzene and other organochlorine compounds incorporation to the newborns and its effects on neonatal neurological development at 6-8 weeks of life. Organohalogen Compd 1999;44:241-2.
15. Eskenazi B, Marks AR, Bradman A, et al. In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Pediatrics 2006;118:233-41.
16. Ribas-Fitó N, Torrent M, Carrizo D, et al. In utero exposure to background concentrations of DDT and cognitive functioning among preschoolers. Am J Epidemiol 2006;164:955-62.
17. Ribas-Fitó N, Cardo E, Sala M, et al. Breastfeeding, exposure to organochlorine compounds, and neurodevelopment in infants. Pediatrics 2003;111:e580-5. (Electronic article).
18. Porterfield SP. Thyroidal dysfunction and environmental chemicals - potential impact on brain development. Environ Health Perspect 2000;108(suppl 3):433-8.
19. Dunn JT. Iodine supplementation and the prevention of cretinism. Ann N Y Acad Sci 1993;678:158-68.
20. Friedhoff AJ, Miller JC, Armour M, et al. Role of maternal biochemistry in fetal brain development: effect of maternal thyroidectomy on behaviour and biogenic amine metabolism in rat progeny. Int J Neuropsychopharmacol 2000;3:89-97.
21. Auso E, Lavado-Autric R, Cuevas E, et al. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 2004;145:4037-47.
22. Haddow JE, Palomaki GE, Allan WC, et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 1999;341:549-55.
23. Pop VJ, Brouwers EP, Vader HL, et al. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin Endocrinol (Oxf) 2003;59:282-8.
24. Pop VJ, Kuijpens JL, van Baar AL, et al. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin Endocrinol (Oxf) 1999;50:149-55.
25. Smit BJ, Kok JH, Vulsma T, et al. Neurologic development of the newborn and young child in relation to maternal thyroid function. Acta Paediatr 2000;89:291-5.
26. van Raaij JA, Frijters CM, van den Berg KJ. Hexachlorobenzene-induced hypothyroidism. Involvement of different mechanisms by parent compound and metabolite. Biochem Pharmacol 1993;46:1385-91.
27. Sinjari T, Darnerud PO. Hydroxylated polychlorinated biphenyls: placental transfer and effects on thyroxine in the foetal mouse. Xenobiotica 1998;28:21-30.
28. Lilienthal H, Weinand-Harer A, Winterhoff H, et al. Effects of maternal exposure to 3,3′,4,4′-tetrachlorobiphenyl or propylthiouracil in rats trained to discriminate apomorphine from saline. Toxicol Appl Pharmacol 1997;146:162-9.
29. Agency for Toxic Substances and Disease Registry, Centers for Disease Control and Prevention. Toxicological profile for DDT, DDE and DDD. Atlanta, GA: Centers for Disease Control and Prevention, 2002:497.
30. Goldman M. The effect of a single dose of DDT on thyroid function in male rats. Arch Int Pharmacodyn Ther 1981;252:327-34.
31. Takser L, Mergler D, Baldwin M, et al. Thyroid hormones in pregnancy in relation to environmental exposure to organochlorine compounds and mercury. Environ Health Perspect 2005;113:1039-45.
32. Van den Berg M, Birnbaum LS, Denison M, et al. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 2006;93:223-41.
33. Koopman-Esseboom C, Morse DC, Weisglas-Kuperus N, et al. Effects of dioxins and polychlorinated biphenyls on thyroid hormone status of pregnant women and their infants. Pediatr Res 1994;36:468-73.
34. Steuerwald U, Weihe P, Jorgensen PJ, et al. Maternal seafood diet, methylmercury exposure, and neonatal neurologic function. J Pediatr 2000;136:599-605.
35. Visser TJ, Kaptein E, van Toor H, et al. Glucuronidation of thyroid hormone in rat liver: effects of in vivo treatment with microsomal enzyme inducers and in vitro assay conditions. Endocrinology 1993;133:2177-86.
36. van Raaij JA, Kaptein E, Visser TJ, et al. Increased glucuronidation of thyroid hormone in hexachlorobenzene-treated rats. Biochem Pharmacol 1993;45:627-31.
37. Lubet RA, Dragnev KH, Chauhan DP, et al. A pleiotropic response to phenobarbital-type enzyme inducers in the F344/NCr rat. Effects of chemicals of varied structure. Biochem Pharmacol 1992;43:1067-78.
38. Khan MA, Hansen LG. Ortho-substituted polychlorinated biphenyl (PCB) congeners (95 or 101) decrease pituitary response to thyrotropin releasing hormone. Toxicol Lett 2003;144:173-82.
39. Byrne JJ, Carbone JP, Hanson EA. Hypothyroidism and abnormalities in the kinetics of thyroid hormone metabolism in rats treated chronically with polychlorinated biphenyl and polybrominated biphenyl. Endocrinology 1987;121:520-7.
40. Collins WT Jr, Capen CC. Fine structural lesions and hormonal alterations in thyroid glands of perinatal rats exposed in utero and by the milk to polychlorinated biphenyls. Am J Pathol 1980;99:125-42.
41. Chauhan KR, Kodavanti PR, McKinney JD. Assessing the role of ortho-substitution on polychlorinated biphenyl binding to transthyretin, a thyroxine transport protein. Toxicol Appl Pharmacol 2000;162:10-21.
42. Chevrier J, Eskenazi B, Bradman A, et al. Associations between prenatal exposure to polychlorinated biphenyls and neonatal thyroid-stimulating hormone levels in a Mexican-American population, Salinas Valley, California. Environ Health Perspect 2007;115:1490-6.
43. Eskenazi B, Bradman A, Gladstone EA, et al. CHAMACOS, a longitudinal birth cohort study: lessons from the fields. J Child Health 2003;1:3-27.
44. Hogan JW, Roy J, Korkontzelou C. Handling drop-out in longitudinal studies. Stat Med 2004;23:1455-97.
45. Mandel SJ, Spencer CA, Hollowell JG. Are detection and treatment of thyroid insufficiency in pregnancy feasible? Thyroid 2005;15:44-53.
46. Nelson JC, Tomei RT. Direct determination of free thyroxin in undiluted serum by equilibrium dialysis/radioimmunoassay. Clin Chem 1988;34:1737-44.
47. Wang R, Nelson JC, Weiss RM, et al. Accuracy of free thyroxine measurements across natural ranges of thyroxine binding to serum proteins. Thyroid 2000;10:31-9.
48. Glinoer D. The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 1997;18:404-33.
49. Nelson JC, Weiss RM, Wilcox RB. Underestimates of serum free thyroxine (T4) concentrations by free T4 immunoassays. J Clin Endocrinol Metab 1994;79:76-9.
50. Barr JR, Maggio VL, Barr DB, et al. New high-resolution mass spectrometric approach for the measurement of polychlorinated biphenyls and organochlorine pesticides in human serum. J Chromatogr B Analyt Technol Biomed Life Sci 2003;794:137-48.
51. Phillips DL, Pirkle JL, Burse VW, et al. Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding. Arch Environ Contam Toxicol 1989;18:495-500.
52. Bravo R, Caltabiano LM, Weerasekera G, et al. Measurement of dialkyl phosphate metabolites of organophosphorus pesticides in human urine using lyophilization with gas chromatography-tandem mass spectrometry and isotope dilution quantification. J Expo Anal Environ Epidemiol 2004;14:249-59.
53. Wolff MS, Camann D, Gammon M, et al. Proposed PCB congener groupings for epidemiological studies. Environ Health Perspect 1997;105:13-14.
54. Rosner B. Percentage points for a generalized ESD many-outlier procedure. Technometrics 1983;25:165-72.
55. Singh B, Chandran V, Bandhu HK, et al. Impact of lead exposure on pituitary-thyroid axis in humans. Biometals 2000;13:187-92.
56. Satar S, Satar D, Kirim S, et al. Effects of acute organophosphate poisoning on thyroid hormones in rats. Am J Ther 2005;12:238-42.
57. Bondy G, Curran I, Doucet J, et al. Toxicity of trans-nonachlor to Sprague-Dawley rats in a 90-day feeding study. Food Chem Toxicol 2004;42:1015-27.
58. Matsuura I, Saitoh T, Tani E, et al. Evaluation of a two-generation reproduction toxicity study adding endpoints to detect endocrine disrupting activity using lindane. J Toxicol Sci 2005;30(spec no.):135-61.
59. Rathore M, Bhatnagar P, Mathur D, et al. Burden of organochlorine pesticides in blood and its effect on thyroid hormones in women. Sci Total Environ 2002;295:207-15.
60. Maldonado G, Greenland S. Simulation study of confounder-selection strategies. Am J Epidemiol 1993;138:923-36.
61. Lubin JH, Colt JS, Camann D, et al. Epidemiologic evaluation of measurement data in the presence of detection limits. Environ Health Perspect 2004;112:1691-6.
62. Chevrier J, Dewailly E, Ayotte P, et al. Body weight loss increases plasma and adipose tissue concentrations of potentially toxic pollutants in obese individuals. Int J Obes Relat Metab Disord 2000;24:1272-8.
63. Centers for Disease Control and Prevention. Third national report on human exposure to environmental chemicals. Atlanta, GA: Centers for Disease Control and Prevention, 2005:475.
64. Bradman AS, Schwartz JM, Fenster L, et al. Factors predicting organochlorine pesticide levels in pregnant Latina women living in a United States agricultural area. J Expo Sci Environ Epidemiol 2007;17:388-99.
65. Langer P, Kocan A, Tajtakova M, et al. Possible effects of persistent organochlorinated pollutants cocktail on thyroid hormone levels and pituitary-thyroid interrelations. Chemosphere 2007;70:110-18.
66. Longnecker MP, Wolff MS, Gladen BC, et al. Comparison of polychlorinated biphenyl levels across studies of human neurodevelopment. Environ Health Perspect 2003;111:65-70.
67. Juarez de Ku LM, Sharma-Stokkermans M, Meserve LA. Thyroxine normalizes polychlorinated biphenyl (PCB) dose-related depression of choline acetyltransferase (ChAT) activity in hippocampus and basal forebrain of 15-day-old rats. Toxicology 1994;94:19-30.
68. Goldey ES, Crofton KM. Thyroxine replacement attenuates hypothyroxinemia, hearing loss, and motor deficits following developmental exposure to Aroclor 1254 in rats. Toxicol Sci 1998;45:94-105.
69. Goldey ES, Taylor DH. Developmental neurotoxicity following premating maternal exposure to hexachlorobenzene in rats. Neurotoxicol Teratol 1992;14:15-21.
70. Roberts CGP, Ladenson PW. Hypothyroidism. Lancet 2004;363:793-803.
71. Hollowell JG, Staehling NW, Flanders WD, et al. Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab 2002;87:489-99.
72. Fewell Z, Davey Smith G, Sterne JA. The impact of residual and unmeasured confounding in epidemiologic studies: a simulation study. Am J Epidemiol 2007;166:646-55.
73. de Escobar GM, Obregon MJ, del Rey FE. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab 2004;18:225-48.