Upstream adverse effects in risk assessment: A model of polychlorinated biphenyls, thyroid hormone disruption and neurological outcomes in humans

Environmental Research

Volumn 117, Issue , 2012, Pages 90-99

  Wise, Amber ^a   Parham, Fred ^b   Axelrad, Daniel A ^c   Guyton, Kathryn Z ^c   Portier, Christopher ^b   Zeise, Lauren ^d   Zoeller, R Thomas ^e   Woodruff, Tracey J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^d CALIFORNIA ENVIRONMENTAL PROTECTION AGENCY   (United States)

^e UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Environmental chemical exposure; Neurodevelopmental outcomes; Polychlorinated biphenyls; Quantitative risk assessment; Thyroid hormone

Indexed keywords

LIOTHYRONINE; POLYCHLORINATED BIPHENYL DERIVATIVE; THYROID HORMONE; THYROTROPIN; THYROXINE;

CHEMICAL POLLUTANT; COGNITION; DECISION MAKING; EPIDEMIOLOGY; HORMONE; META-ANALYSIS; NEUROLOGY; PCB; POLLUTION EXPOSURE; QUANTITATIVE ANALYSIS; RISK ASSESSMENT;

ARTICLE; BODY BURDEN; COGNITION; HEALTH SURVEY; HUMAN; INTELLIGENCE QUOTIENT; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; RISK ASSESSMENT;

BODY BURDEN; CHILD; CHILD DEVELOPMENT; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS; HUMANS; INFANT; INTELLIGENCE; INTELLIGENCE TESTS; MALE; MODELS, BIOLOGICAL; POLYCHLORINATED BIPHENYLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REGRESSION ANALYSIS; RISK ASSESSMENT; THYROID HORMONES;

EID: 84864940396     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2012.05.013     Document Type: Article

References (87)

1. Abdelouahab N., et al. Gender differences in the effects of organochlorines, mercury, and lead on thyroid hormone levels in lakeside communities of Quebec (Canada). Environ. Res. 2008, 107:380-392.
2. Alvarez-Pedrerol M., et al. Organochlorine compounds, iodine intake, and thyroid hormone levels during pregnancy. Environ. Sci. Technol. 2009, 43:7909-7915.
3. Andersen S., et al. Narrow individual variations in serum T(4) and T(3) in normal subjects: a clue to the understanding of subclinical thyroid disease. J. Clin. Endocrinol. Metab. 2002, 87:1068-1072.
4. Auso E., et al. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 2004, 145:4037-4047.
5. Axelrad D.A., et al. Dose-response relationship of prenatal mercury exposure and IQ: an integrative analysis of epidemiologic data. Environ. Health Perspect. 2007, 115:609-615.
6. Bernal J. Thyroid hormone receptors in brain development and function. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3:249-259.
7. Bloom M.S., et al. Exploring associations between serum levels of select organochlorines and thyroxine in a sample of New York state sportsmen: the New York State Angler Cohort Study. Environ. Res. 2003, 93:52-66.
8. Brucker-Davis F. Effects of environmental synthetic chemicals on thyroid function. Thyroid 1998, 8:827-856.
9. Burman K. Commentary: discordant measurements of serum triiodothyronine (T4), thyroxine (T3) and thyroid-stimulating hormone (TSH). Clin. Chem. 2008, 54:1246.
10. Caldwell K.L., et al. Urinary iodine concentration: United States National Health and Nutrition Examination Survey 2001-2002. Thyroid 2005, 15:692-699.
11. Chevrier J., 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, 115:1490-1496.
12. Chevrier J., et al. Effects of exposure to polychlorinated biphenyls and organochlorine pesticides on thyroid function during pregnancy. Am. J. Epidemiol. 2008, 168:298-310.
13. Covaci A., et al. Distribution of PCBs and organochlorine pesticides in umbilical cord and maternal serum. Sci. Total Environ. 2002, 298:45-53.
14. Crofton K.M. Thyroid disrupting chemicals: mechanisms and mixtures. Int. J. Androl. 2008, 31:209-223.
15. Dallaire R., et al. Thyroid function and plasma concentrations of polyhalogenated compounds in Inuit adults. Environ. Health Perspect. 2009, 117:1380-1386.
16. Dallaire R., et al. Thyroid hormone levels of pregnant Inuit women and their infants exposed to environmental contaminants. Environ. Health Perspect. 2009, 117:1014-1020.
17. Dersimonian R., Laird N. Metaanlysis in clinical-trials. Controlled Clin. Trials 1986, 7:177-188.
18. DeVito M., et al. Screening methods for thyroid hormone disruptors. Environ. Health Perspect. 1999, 107:407-415.
19. Gilbert M.E., Sui L. Dose-dependent reductions in spatial learning and synaptic function in the dentate gyrus of adult rats following developmental thyroid hormone insufficiency. Brain Res. 2006, 1069:10-22.
20. Glinoer D., Rovet J. Gestational hypothyroxinemia and the beneficial effects of early dietary iodine fortification. Thyroid 2009, 19:431-434.
21. Goodman M., et al. Using systematic reviews and meta-analyses to support regulatory decision-making for neurotoxicants: lessons learned from a case study of PCBs. Environ. Health Perspect. 2010, 118:727-734.
22. Gray K.A., et al. In utero exposure to background levels of polychlorinated biphenyls and cognitive functioning among school-age children. Am. J. Epidemiol. 2005, 162:17-26.
23. Grellier J., et al. Exposure to disinfection by-products, fetal growth, and prematurity a systematic review and meta-analysis. Epidemiology 2010, 21:300-313.
24. Haddow J.E. Subclinical hypothyroidism and pregnancy outcomes. Obstet. Gynecol. 2005, 106:198. (Author reply 198-9).
25. Haddow J.E., et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N. Engl. J. Med. 1999, 341:549-555.
26. Heyerdahl S., Oerbeck B. Congenital hypothyroidism: developmental outcome in relation to levothyroxine treatment variables. Thyroid 2003, 13:1029-1038.
27. Hood A., et al. Induction of T(4) UDP-GT activity, serum thyroid stimulating hormone, and thyroid follicular cell proliferation in mice treated with microsomal enzyme inducers. Toxicol. Appl. Pharmacol. 2003, 188:6-13.
28. Howdeshell K.L. A model of the development of the brain as a construct of the thyroid system. Environ. Health Perspect. 2002, 110:337-348.
29. Jacobson J.L., Jacobson S.W. Sources and implications of interstudy and interindividual variability in the developmental neurotoxicity of PCBs. Neurotoxicol. Teratol. 1996, 18:257-264.
30. Jacobson J.L., Jacobson S.W. Prenatal exposure to polychlorinated biphenyls and attention at school age. J. Pediatr. 2003, 143:780-788.
31. Jacobson J.L., et al. Effects of in utero exposure to polychlorinated biphenyls and related contaminants on cognitive functioning in young children. J. Pediatr. 1990, 116:38-45.
32. Juni P., et al. The hazards of scoring the quality of clinical trials for meta-analysis. J. Am. Med. Assoc. 1999, 282:1054-1060.
33. Klein R.Z., Mitchell M.L. Maternal hypothyroidism and child development. Horm. Res. 1999, 52:55-59.
34. Klein R.Z., et al. Relation of severity of maternal hypothyroidism to cognitive development of offspring. J. Med. Screen. 2001, 8:18-20.
35. Koopman-Esseboom C., et al. Effects of dioxins and polychlorinated biphenyls on thyroid hormone status of pregnant women and their infants. Pediatr. Res. 1994, 36:468-473.
36. Kooistra L., et al. Neonatal effects of maternal hypothyroxinemia during early pregnancy. Pediatrics 2006, 117:161-167.
37. LaFranchi S.H., Austin J. How should we be treating children with congenital hypothyroidism?. J. Pediatr. Endocrinol. Metab. 2007, 20:559-578.
38. Langer P. Persistent organochlorinated pollutants (PCB, DDE, HCB, dioxins, furans) and the thyroid-review 2008. Endocr. Regul. 2008, 42:79-104.
39. Liu J., et al. Alteration of thyroid homeostasis by UDP-glucuronosyltransferase inducers in rats: a dose-response study. J. Pharmcol. Exp. Ther. 1995, 273:977-985.
40. Longnecker M.P., et al. Polychlorinated biphenyl (PCB) exposure in relation to thyroid hormone levels in neonates. Epidemiology 2000, 11:249-254.
41. Longnecker M.P., et al. Comparison of polychlorinated biphenyl levels across studies of human neurodevelopment. Environ. Health Perspect. 2003, 111:65-70.
42. Lopez-Espinosa M.-J., et al. Association between thyroid hormone levels and 4,4'-DDE concentrations in pregnant women (Valencia, Spain). Environ. Res. 2009, 109:479-485.
43. Maervoet J., et al. Association of thyroid hormone concentrations with levels of organochlorine compounds in cord blood of neonates. Environ. Health Perspect. 2007, 115:1780-1786.
44. Matthews J., et al. Co-planar 3,3',4,4' 5-pentachlorinated biphenyl and non-co-planar 2,2',4,6,6'-pentachlorinated biphenyl differentially induce recruitment of oestrogen receptor alpha to aryl hydrocarbon receptor target genes. Biochem. J. 2007, 406:343-353.
45. Meeker J.D., et al. Serum PCBs, p,p'-DDE and HCB predict thyroid hormone levels in men. Environ. Res. 2007, 104:296-304.
46. Miller M.D., et al. Thyroid-disrupting chemicals: interpreting upstream biomarkers of adverse outcomes. Environ. Health Perspect. 2009, 117:1033-1041.
47. Morreale de Escobar G. The role of thyroid hormone in fetal neurodevelopment. J. Pediatr. Endocrinol. Metab. 2001, 13:1453-1462.
48. Morreale de Escobar G., et al. Role of thyroid hormone during early brain development. Eur. J. Endocrinol. 2004, 151:U25-U37.
49. Morreale de Escobar G., et al. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia?. J. Clin. Endocrinol. Metab. 2000, 85:3975-3987.
50. Nagayama J., et al. Postnatal exposure to chlorinated dioxins and related chemicals on thyroid hormone status in Japanese breast-fed infants. Chemosphere 1998, 37:1789-1793.
51. National Research Council, 2007. Toxicity Testing in the 21st Century: A Vision and a Strategy. National Academies of Science, Washington D.C., p. 196.
52. National Research Council, 2009. Science and Decisions: Advancing Risk Assessment. National Academy of Science, (Ed.), Washington D.C.
53. Oerbeck B., et al. Congenital hypothyroidism: influence of disease severity and l-thyroxine treatment on intellectual, motor, and school-associated outcomes in young adults. Pediatrics 2003, 112:923-930.
54. Otake T., et al. Thyroid hormone status of newborns in relation to in utero exposure to PCBs and hydroxylated PCB metabolites. Env. Res. 2007, 105:240-246.
55. Parham, F.M., et al., 2012. Upstream Adverse Effects in Risk Assessment: Modeling Polychlorinated Biphenyls and Thyroid Hormone Disruption Outcomes in Animals and Humans Env. Res. 116, 74-84, http://dx.doi.org/10.1016/j.envres.2012.04.003.
56. Patandin S., et al. Effects of environmental exposure to polychlorinated biphenyls and dioxins on cognitive abilities in Dutch children at 42 months of age. J. Pediatr. 1999, 134:33-41.
57. Persky V., et al. The effects of PCB exposure and fish consumption on endogenous hormones. Env. Health. Perspect. 2001, 109:1275-1283.
58. Pessah I.N., et al. Enantiomeric specificity of (-)-2,2',3,3',6,6'-hexachlorobiphenyl toward ryanodine receptor types 1 and 2. Chem. Res. Toxicol. 2009, 22:201-207.
59. Pop V.J., et al. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin. Endocrinol. (Oxf.) 2003, 59:282-288.
60. Pop V.J., et al. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin. Endocrinol. (Oxf.) 1999, 50:149-155.
61. Sala M., et al. Association between serum concentrations of hexachlorobenzene and polychlorobiphenyls with thyroid hormone and liver enzymes in a sample of the general population. Occup. Environ. Med. 2001, 58:172-177.
62. Salay E., Garabrant D. Polychlorinated biphenyls and thyroid hormones in adults: a systematic review appraisal of epidemiological studies. Chemosphere 2009, 74:1413-1419.
63. Schantz S.L., et al. Effects of PCB exposure on neuropsychological function in children. Environ. Health Perspect. 2003, 111:357-376.
64. Selva K.A., et al. Neurodevelopmental outcomes in congenital hypothyroidism: comparison of initial T4 dose and time to reach target T4 and TSH. J. Pediatr. 2005, 147:775-780.
65. Simic N., et al. Impact of neonatal thyroid hormone insufficiency and medical morbidity on infant neurodevelopment and attention following preterm birth. Thyroid 2009, 19:395-401.
66. Smallridge R.C., et al. Thyroid function inside and outside of pregnancy: what do we know and what don't we know?. Thyroid 2005, 15:54-59.
67. Stewart P.W., et al. The relationship between prenatal PCB exposure and intelligence (IQ) in 9-year-old children. Environ. Health Perspect. 2008, 116:1416-1422.
68. Stewart P.W., et al. Cognitive development in preschool children prenatally exposed to PCBs and MeHg. Neurotoxicol. Teratol. 2003, 25:11-22.
69. Sugatani J., et al. The phenobarbital response enhancer modelu in the human bilirubin UDP-glucuronosyltransferase UGT1A1 gene and regulation by the nuclear receptor CAR. Hepatology 2001, 33:1232-1238.
70. Takser L., et al. Thyroid hormones in pregnancy in relation to environmental exposure to organochlorine compounds and mercury. Env. Health Perspect. 2005, 113:1039-1045.
71. Turyk M.E., et al. Relationships of thyroid hormones with polychlorinated biphenyls, dioxins, furans, and DDE in adults. Environ. Health Perspect. 2007, 115:1197-1203.
72. US Environmental Protection Agency, 2005. Regulatory Impact Analysis of the Clean Air Mercury Rule. Office of Air Quality Planning and Standards, Research Triangle Park, NC.
73. US Environmental Protection Agency, 2008a. Lead; Renovation, Repair and Painting Program; Lead Hazard information Pamphlet; Notice of Availability; Final Rule, vol. 73, Federal Register, p. 79.
74. US Environmental Protection Agency. 2008b, National Ambient Air Quality Standards for Lead; Final Rule, vol. 73, Federal Register, pp. 66964-67062.
75. US Environmental Protection Agency. 2008c, Regulatory Impact Analysis of the Proposed Revisions to the National Ambient Air Quality Standards. Office of Air Quality Planning and Standards, Health and Environmental Impact Division, Research Triangle Park, p. 177.
76. US Environmental Protection Agency. 2010, Integrated Risk Information System: Glossary, vol. 2010, Washington, DC.
77. van der Sluijs Veer L., et al. Quality of life, developmental milestones, and self-esteem of young adults with congenital hypothyroidism diagnosed by neonatal screening. J. Clin. Endocrinol. Metab. 2008, 93:2654-2661.
78. Vermiglio F., et al. Attention deficit and hyperactivity disorders in the offspring of mothers exposed to mild-moderate iodine deficiency: a possible novel iodine deficiency disorder in developed countries. J. Clin. Endocrinol. Metab. 2004, 89:6054-6060.
79. Visser T.J., 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, 133:2177-2186.
80. Vreugdenhil H.J.I., et al. Effects of prenatal PCB and dioxin background exposure on cognitive and motor abilities in Dutch children at school age. J. Pediatr. 2002, 140:48-56.
81. Wang S.L., et al. Body burdens of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls and their relations to estrogen metabolism in pregnant women. Environ. Health Perspect. 2006, 114:740-745.
82. Woodruff T.J., et al. Meeting report: moving upstream-evaluating adverse upstream end points for improved risk assessment and decision-making. Environ. Health Perspect. 2008, 116:1568-1575.
83. Yang D., et al. Developmental exposure to polychlorinated biphenyls interferes with experience-dependent dendritic plasticity and ryanodine receptor expression in weanling rats. Environ. Health Perspect. 2009, 117:426-435.
84. Yang J.M., et al. Development of TEFs for PCB congeners by using an alternative biomarker-thyroid hormone levels. Regul. Toxicol. Pharmacol. 2010, 56:225-236.
85. Zoeller R.T. Environmental chemicals as thyroid hormone analogues: new studies indicate that thyroid hormone receptors are targets of industrial chemicals?. Mol. Cell. Endocrinol. 2005, 242:10-15.
86. Zoeller R.T. Environmental chemicals impacting the thyroid: targets and consequences. Thyroid 2007, 17:811-817.
87. Zoeller R.T., Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 2004, 16:809-818.