Prenatal and 5-year p,p'-DDE exposures are associated with altered sensory processing in school-aged children in Nunavik: A visual evoked potential study

NeuroToxicology

Volumn 44, Issue , 2014, Pages 8-16

  Cartier, Chloé ^a,b   Muckle, Gina ^c,d   Jacobson, Sandra W ^e   Jacobson, Joseph L ^e   Dewailly, Éric ^c,d   Ayotte, Pierre ^c,d   Chevrier, Cécile ^b   Saint Amour, Dave ^a,f  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITÉ LAVAL   (Canada)

^d LAVAL UNIVERSITY   (Canada)

^e WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Neurotoxicity; P,p' DDE; P,p' DDT; Sensory processing; Visual evoked potentials

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; CHLORPHENOTANE; OMEGA 3 FATTY ACID;

ARTICLE; BLOOD ANALYSIS; CANADA; CHILD; ENVIRONMENTAL EXPOSURE; EVOKED VISUAL RESPONSE; FEMALE; HUMAN; LONGITUDINAL STUDY; MALE; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; SEA FOOD; UMBILICAL CORD BLOOD; VISION; ADOLESCENT; BLOOD SAMPLING; BRAIN FUNCTION; CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIETARY INTAKE; DISEASE ASSOCIATION; EYE DEVELOPMENT; FUNCTIONAL ASSESSMENT; OUTCOME ASSESSMENT; PRENATAL EXPOSURE; SCHOOL CHILD; SENSORY DYSFUNCTION; UMBILICAL CORD; VISUAL SYSTEM FUNCTION; BLOOD; BRAIN; DRUG EFFECTS; FOLLOW UP; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PREGNANCY;

ADOLESCENT; BRAIN; CHILD; DDT; DICHLORODIPHENYL DICHLOROETHYLENE; EVOKED POTENTIALS, VISUAL; FEMALE; FOLLOW-UP STUDIES; HUMANS; LONGITUDINAL STUDIES; MALE; PHOTIC STIMULATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; QUEBEC;

EID: 84901188393     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.04.009     Document Type: Article

References (85)

1. Abb M., Breuer J.V., Zeitz C., Lorenz W. Analysis of pesticides and PCBs in waste wood and house dust. Chemosphere 2010, 81:488-493.
2. Adetona O., Horton K., Sjodin A., Jones R., Hall D.B., Aguillar-Villalobos M., et al. Concentrations of select persistent organic pollutants across pregnancy trimesters in maternal and in cord serum in Trujillo, Peru. Chemosphere 2013, 91:1426-1433.
3. Ayotte P., Muckle G., Jacobson J.L., Jacobson S.W., Dewailly E. Assessment of pre- and postnatal exposure to polychlorinated biphenyls: lessons from the Inuit Cohort Study. Environ Health Perspect 2003, 111:1253-1258. Inuit Cohort Study.
4. Barrie L.A., Gregor D., Hargrave B., Lake R., Muir D., Shearer R., et al. Arctic contaminants: sources, occurrence and pathways. Sci Total Environ 1992, 122:1-74.
5. Beyer C. Estrogen and the developing mammalian brain. Anat Embryol 1999, 199:379-390.
6. Boucher O., Bastien C.H., Muckle G., Saint-Amour D., Jacobson S.W., Jacobson J.L. Behavioural correlates of the P3b event-related potential in school-age children. Int J Psychophysiol 2010, 76:148-157.
7. Boucher O., Bastien C.H., Saint-Amour D., Dewailly E., Ayotte P., Jacobson J.L., et al. Prenatal exposure to methylmercury and PCBs affects distinct stages of information processing: an event-related potential study with Inuit children. Neurotoxicology 2010, 18:18.
8. Boucher O., Burden M.J., Muckle G., Saint-Amour D., Ayotte P., Dewailly E., et al. Response inhibition and error monitoring during a visual go/no-go task in inuit children exposed to lead, polychlorinated biphenyls, and methylmercury. Environ Health Perspect 2012, 120:608-615.
9. Boucher O., Muckle G., Saint-Amour D., Dewailly E., Ayotte P., Jacobson S.W., et al. The relation of lead neurotoxicity to the event-related potential P3b component in Inuit children from Arctic Quebec. Neurotoxicology 2009, 30:1070-1077.
10. Bradley A., Freeman R.D. Contrast sensitivity in children. Vision Res 1982, 22:953-959.
11. Cartier C., Saint-Amour D. Prenatal omega-3 fatty acids intake and visual function. Nutrition, diet, the eye and vision 2014, 253-261. Elsevier. V. Preedy (Ed.).
12. CDC Fourth national report on human exposure to environmental chemicals 2009, Department of Health and Human Services, Center for Disease Control and Prevention, Atlanta, GA, US.
13. Cohn B.A., Wolff M.S., Cirillo P.M., Sholtz R.I. DDT and breast cancer in young women: new data on the significance of age at exposure. Environ Health Perspect 2007, 115:1406-1414.
14. Colborn T. Neurodevelopment and endocrine disruption. Environ Health Perspect 2004, 112:944-949.
15. Danzo B.J. Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ Health Perspect 1997, 105:294-301.
16. Davies T.G., Field L.M., Usherwood P.N., Williamson M.S. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 2007, 59:151-162.
17. de Courten C., Garey L.J. Morphological development of the primary visual pathway in the child. J Fr Ophtalmol 1983, 6:187-202.
18. De Jager C., Farias P., Barraza-Villarreal A., Avila M.H., Ayotte P., Dewailly E., et al. Reduced seminal parameters associated with environmental DDT exposure and p,p'-DDE concentrations in men in Chiapas, Mexico: a cross-sectional study. J Androl 2006, 27:16-27.
19. Dewailly E., Ayotte P., Bruneau S., Gingras S., Belles-Isles M., Roy R. Susceptibility to infections and immune status in Inuit infants exposed to organochlorines. Environ Health Perspect 2000, 108:205-211.
20. Dewailly E., Ayotte P., Bruneau S., Laliberte C., Muir D.C., Norstrom R.J. Inuit exposure to organochlorines through the aquatic food chain in Arctic Quebec. Environ Health Perspect 1993, 101:618-620.
21. Di Russo F., Martinez A., Sereno M.I., Pitzalis S., Hillyard S.A. Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp 2002, 15:95-111.
22. Di Russo F., Pitzalis S., Spitoni G., Aprile T., Patria F., Spinelli D., et al. Identification of the neural sources of the pattern-reversal VEP. NeuroImage 2005, 24:874-886.
23. Diaz G., Ortiz R., Schettino B., Vega S., Gutierrez R. Organochlorine pesticides residues in bottled drinking water from Mexico City. Bull Environ Contam Toxicol 2009, 82:701-704.
24. Ellemberg D., Lewis T.L., Liu C.H., Maurer D. Development of spatial and temporal vision during childhood. Vision Res 1999, 39:2325-2333.
25. Eskenazi B., Marks A.R., Bradman A., Fenster L., Johnson C., Barr D.B., et al. In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Pediatrics 2006, 118:233-241.
26. Ethier A.A., Muckle G., Bastien C., Dewailly E., Ayotte P., Arfken C., et al. Effects of environmental contaminant exposure on visual brain development: a prospective electrophysiological study in school-aged children. Neurotoxicology 2012, 33:1075-1085.
27. Facemire C.F., Gross T.S., Guillette L.J. Reproductive impairment in the Florida panther: nature or nurture?. Environ Health Perspect 1995, 103(Suppl 4):79-86.
28. Fry D.M., Toone C.K. DDT-induced feminization of gull embryos. Science 1981, 213:922-924.
29. Grandjean P., Landrigan P.J. Developmental neurotoxicity of industrial chemicals. Lancet 2006, 368:2167-2178.
30. Gray L.E., Ostby J., Furr J., Wolf C.J., Lambright C., Parks L., et al. Effects of environmental antiandrogens on reproductive development in experimental animals. Hum Reprod Update 2001, 7:248-264.
31. Guillette L.J., Gross T.S., Masson G.R., Matter J.M., Percival H.F., Woodward A.R. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect 1994, 102:680-688.
32. HealthCanada Report on human biomonitoring of Environmental Chemicals in Canada 2010, Health Canada, Ottawa, Ontario, Available: http://www.hc-sc.gc.ca/ewh-semt/pubs/contaminants/chms-ecms/index-eng.php [accessed 5 May 2014].
33. Hermanowicz A., Nawarska Z., Borys D., Maslankiewicz A. The neutrophil function and infectious diseases in workers occupationally exposed to organochloride insecticides. Int Arch Occup Environ Health 1982, 50:329-340.
34. Hollingshead AB. Four factor index of social status. Yale University, Department of Sociology, 1975. Unpublished manuscript.
35. Howdeshell K.L. A model of the development of the brain as a construct of the thyroid system. Environ Health Perspect 2002, 110(Suppl 3):337-348.
36. Huttenlocher P.R., de Courten C., Garey L.J., Van der Loos H. Synaptogenesis in human visual cortex-evidence for synapse elimination during normal development. Neurosci Lett 1982, 33:247-252.
37. Jacobson J.L., Jacobson S.W. Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N Engl J Med 1996, 335:783-789.
38. Jacobson J.L., Jacobson S.W., Muckle G., Kaplan-Estrin M., Ayotte P., Dewailly E. Beneficial effects of a polyunsaturated fatty acid on infant development: evidence from the inuit of Arctic Quebec. J Pediatr 2008, 152:356-364.
39. Jacques C., Levy E., Muckle G., Jacobson S.W., Bastien C., Dewailly E., et al. Long-term effects of prenatal omega-3 fatty acid intake on visual function in school-age children. J Pediatr 2011, 158(83-90):e1.
40. Kaushik C.P., Sharma H.R., Kaushik A. Organochlorine pesticide residues in drinking water in the rural areas of Haryana, India. Environ Monit Assess 2012, 184:103-112.
41. Kelce W.R., Stone C.R., Laws S.C., Gray L.E., Kemppainen J.A., Wilson E.M. Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist. Nature 1995, 375:581-585.
42. Korrick S.A., Sagiv S.K. Polychlorinated biphenyls, organochlorine pesticides and neurodevelopment. Curr Opin Pediatr 2008, 20:198-204.
43. Luck S.J. An introduction to the event-related potential technique 2005, The Massachussets Institute of Technology Press, Cambridge, MA.
44. Maldonado G., Greenland S. Simulation study of confounder-selection strategies. Am J Epidemiol 1993, 138:923-936.
45. Matsumura F., Narahashi T. ATPase inhibition and electrophysiological change caused by DDT and related neuroactive agents in lobster nerve. Biochem Pharmacol 1971, 20:825-837.
46. Matsumura F., Patil K.C. Adenosine triphosphatase. Sensitive to DDT in synapses of rat brain. Science 1969, 166:121-122.
47. McGlynn K.A., Quraishi S.M., Graubard B.I., Weber J.P., Rubertone M.V., Erickson R.L. Persistent organochlorine pesticides and risk of testicular germ cell tumors. J Natl Cancer Inst 2008, 100:663-671.
48. Moccia R.D., Fox G.A., Britton A. A quantitative assessment of thyroid histopathology of herring gulls (Larus argentatus) from the Great Lakes and a hypothesis on the causal role of environmental contaminants. J Wildl Dis 1986, 22:60-70.
49. Molloy C., Doyle L.W., Makrides M., Anderson P.J. Docosahexaenoic acid and visual functioning in preterm infants: a review. Neuropsychol Rev 2012, 22:425-437.
50. Montgomery M.P., Kamel F., Saldana T.M., Alavanja M.C., Sandler D.P. Incident diabetes and pesticide exposure among licensed pesticide applicators: Agricultural Health Study, 1993-2003. Am J Epidemiol 2008, 167:1235-1246.
51. Morse N.L. Benefits of docosahexaenoic acid, folic acid, vitamin D and iodine on foetal and infant brain development and function following maternal supplementation during pregnancy and lactation. Nutrients 2012, 4:799-840.
52. Muckle G., Ayotte P., Dewailly E.E., Jacobson S.W., Jacobson J.L. Prenatal exposure of the northern Quebec Inuit infants to environmental contaminants. Environ Health Perspect 2001, 109:1291-1299.
53. Muckle G., Dewailly E., Ayotte P. Prenatal exposure of Canadian children to polychlorinated biphenyls and mercury. Can J Public Health 1998, 89(Suppl 1):2-7. S20-S25.
54. Multigner L., Ndong J.R., Giusti A., Romana M., Delacroix-Maillard H., Cordier S., et al. Chlordecone exposure and risk of prostate cancer. J Clin Oncol 2010, 28:3457-3462.
55. Murata K., Weihe P., Renzoni A., Debes F., Vasconcelos R., Zino F., et al. Delayed evoked potentials in children exposed to methylmercury from seafood. Neurotoxicol Teratol 1999, 21:343-348.
56. Narahashi T., Haas H.G. DDT: interaction with nerve membrane conductance changes. Science 1967, 157:1438-1440.
57. Odom J.V., Bach M., Barber C., Brigell M., Marmor M.F., Tormene A.P., et al. Visual evoked potentials standard (2004). Doc Ophthalmol 2004, 108:115-123.
58. Otto D.A. The assessment of neurotoxicity in children. Electrophysiological methods. Monogr Am Assoc Ment Defic 1987, 8:139-158.
59. Patayova H., Wimmerova S., Lancz K., Palkovicova L., Drobna B., Fabisikova A., et al. Anthropometric, socioeconomic, and maternal health determinants of placental transfer of organochlorine compounds. Environ Sci Pollut Res Int 2013, 20:8557-8566.
60. Patel C.J., Bhattacharya J., Butte A.J. An Environment-Wide Association Study (EWAS) on type 2 diabetes mellitus. PLoS One 2010, 5:e10746.
61. Plusquellec P., Muckle G., Dewailly E., Ayotte P., Begin G., Desrosiers C., et al. The relation of environmental contaminants exposure to behavioral indicators in Inuit preschoolers in Arctic Quebec. Neurotoxicology 2010, 31:17-25.
62. Porterfield S.P., Hendrich C.E. The role of thyroid hormones in prenatal and neonatal neurological development-current perspectives. Endocr Rev 1993, 14:94-106.
63. Puertas R., Lopez-Espinosa M.J., Cruz F., Ramos R., Freire C., Perez-Garcia M., et al. Prenatal exposure to mirex impairs neurodevelopment at age of 4 years. Neurotoxicology 2010, 31:154-160.
64. Qu W., Suri R.P., Bi X., Sheng G., Fu J. Exposure of young mothers and newborns to organochlorine pesticides (OCPs) in Guangzhou, China. Sci Total Environ 2010, 408:3133-3138.
65. Rhainds M., Levallois P., Dewailly E., Ayotte P. Lead, mercury, and organochlorine compound levels in cord blood in Quebec, Canada. Arch Environ Health 1999, 54:40-47.
66. Ribas-Fito N., Cardo E., Sala M., Eulalia de Muga M., Mazon C., Verdu A., et al. Breastfeeding, exposure to organochlorine compounds, and neurodevelopment in infants. Pediatrics 2003, 111:e580-e585.
67. Ribas-Fito N., Torrent M., Carrizo D., Julvez J., Grimalt J.O., Sunyer J. Exposure to hexachlorobenzene during pregnancy and children's social behavior at 4 years of age. Environ Health Perspect 2007, 115:447-450.
68. Ribas-Fito N., Torrent M., Carrizo D., Munoz-Ortiz L., Julvez J., Grimalt J.O., et al. In utero exposure to background concentrations of DDT and cognitive functioning among preschoolers. Am J Epidemiol 2006, 164:955-962.
69. Rice D., Barone S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 2000, 108(Suppl 3):511-533.
70. Rice D.C. Issues in developmental neurotoxicology: interpretation and implications of the data. Can J Public Health 1998, 89(Suppl 1):S31-S36. S4-S40.
71. Riva E., Grandi F., Massetto N., Radaelli G., Giovannini M., Zetterstrom R., et al. Polychlorinated biphenyls in colostral milk and visual function at 12 months of life. Acta Paediatr 2004, 93:1103-1107.
72. Rogan W.J., Gladen B.C., McKinney J.D., Carreras N., Hardy P., Thullen J., et al. Neonatal effects of transplacental exposure to PCBs and DDE. J Pediatr 1986, 109:335-341.
73. Romieu I., Hernandez-Avila M., Lazcano-Ponce E., Weber J.P., Dewailly E. Breast cancer, lactation history, and serum organochlorines. Am J Epidemiol 2000, 152:363-370.
74. Sagiv S.K., Thurston S.W., Bellinger D.C., Tolbert P.E., Altshul L.M., Korrick S.A. Prenatal organochlorine exposure and behaviors associated with attention deficit hyperactivity disorder in school-aged children. Am J Epidemiol 2010, 171:593-601.
75. Saint-Amour D., Roy M.S., Bastien C., Ayotte P., Dewailly E., Despres C., et al. Alterations of visual evoked potentials in preschool Inuit children exposed to methylmercury and polychlorinated biphenyls from a marine diet. Neurotoxicology 2006, 27:567-578.
76. Saint-Amour D., Saron C.D., Schroeder C.E., Foxe J.J. Can whole brain nerve conduction velocity be derived from surface-recorded visual evoked potentials? A re-examination of Reed, Vernon, and Johnson (2004). Neuropsychologia 2005, 43:1838-1844.
77. Sala M., Ribas-Fito N., Cardo E., de Muga M.E., Marco E., Mazon C., et al. Levels of hexachlorobenzene and other organochlorine compounds in cord blood: exposure across placenta. Chemosphere 2001, 43:895-901.
78. Shen H., Main K.M., Andersson A.M., Damgaard I.N., Virtanen H.E., Skakkebaek N.E., et al. Concentrations of persistent organochlorine compounds in human milk and placenta are higher in Denmark than in Finland. Hum Reprod 2008, 23:201-210.
79. Sjodin A., Wong L.Y., Jones R.S., Park A., Zhang Y., Hodge C., et al. Serum concentrations of polybrominated diphenyl ethers (PBDEs) and polybrominated biphenyl (PBB) in the United States population: 2003-2004. Environ Sci Technol 2008, 42:1377-1384.
80. Tan J., Loganath A., Chong Y.S., Obbard J.P. Exposure to persistent organic pollutants in utero and related maternal characteristics on birth outcomes: a multivariate data analysis approach. Chemosphere 2009, 74:428-433.
81. Thompson C.C., Potter G.B. Thyroid hormone action in neural development. Cereb Cortex 2000, 10:939-945.
82. Torres-Sanchez L., Rothenberg S.J., Schnaas L., Cebrian M.E., Osorio E., Del Carmen Hernandez M., et al. In utero p,p'-DDE exposure and infant neurodevelopment: a perinatal cohort in Mexico. Environ Health Perspect 2007, 115:435-439.
83. Valvi D., Mendez M.A., Martinez D., Grimalt J.O., Torrent M., Sunyer J., et al. Prenatal concentrations of polychlorinated biphenyls, DDE, and DDT and overweight in children: a prospective birth cohort study. Environ Health Perspect 2012, 120:451-457.
84. Wang R.Y., Jain R.B., Wolkin A.F., Rubin C.H., Needham L.L. Serum concentrations of selected persistent organic pollutants in a sample of pregnant females and changes in their concentrations during gestation. Environ Health Perspect 2009, 117:1244-1249.
85. Weiss B. Endocrine disruptors as a threat to neurological function. J Neurol Sci 2011, 305:11-21.