Neurobehavioral function and low-level metal exposure in adolescents

International Journal of Hygiene and Environmental Health

Volumn 218, Issue 1, 2015, Pages 139-146

  Kicinski, Michal ^a   Vrijens, Jan ^b   Vermier, Griet ^c   Hond, Elly Den ^d   Schoeters, Greet ^d,e   Nelen, Vera ^f   Bruckers, Liesbeth ^a   Sioen, Isabelle ^g   Baeyens, Willy ^b   Van Larebeke, Nicolas ^b,g   Viaene, Mineke K ^h   Nawrot, Tim S ^a,i  

^a HASSELT UNIVERSITY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c Integrated Psychiatric Centre OPZ   (Belgium)

^d FLEMISH INSTITUTE FOR TECHNOLOGICAL RESEARCH VITO   (Belgium)

^e UNIVERSITY OF ANTWERP   (Belgium)

^f Provincial Institute for Hygiene   (Belgium)

^g GHENT UNIVERSITY   (Belgium)

^h Department of Neurology   (Belgium)

ⁱ UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Adolescents; Cognition; Copper; Lead; Metals; Neurotoxicity

Indexed keywords

COPPER; LEAD; POLLUTANT;

ADOLESCENT; ATTENTION; COGNITION; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; FEMALE; HUMAN; MALE; POLLUTANT; SHORT TERM MEMORY; TOXICITY;

ADOLESCENT; ATTENTION; COGNITION; COPPER; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; FEMALE; HUMANS; LEAD; MALE; MEMORY, SHORT-TERM;

EID: 84927692009     PISSN: 14384639     EISSN: 1618131X     Source Type: Journal    
DOI: 10.1016/j.ijheh.2014.09.002     Document Type: Article

References (89)

1. Amin-zaki L., Majeed M.A., Clarkson T.W., Greenwood M.R. Methylmercury poisoning in Iraqi children: clinical observations over two years. Br. Med. J. 1978, 1:613-616.
2. ATSDR Toxicological Profile for Lead 2007, U.S. Department of Health and Human Services.
3. Bahrami Samani E., Ganjali M., Eftekhari S. A latent variable model for mixed continuous and ordinal responses with nonignorable missing responses: assessing the local influence via covariance structure. Sankhya, Ser. B 2010, 72:38-57.
4. Baker E.L., Letz R.E., Fidler A.T., Shalat S., Plantamura D., Lyndon M. A computer-based neurobehavioral evaluation system for occupational and environmental epidemiology: methodology and validation studies. Neurobehav. Toxicol. Teratol. 1985, 7:369-377.
5. Boucher O., Burden M.J., Muckle G., Saint-Amour D., Ayotte P., Dewailly E., Nelson C.A., Jacobson S.W., Jacobson J.L. 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.
6. Bull R., Espy K.A., Wiebe S.A. Short-term memory, working memory, and executive functioning in preschoolers: longitudinal predictors of mathematical achievement at age 7 years. Dev. Neuropsychol. 2008, 33:205-228.
7. Canfield R.L., Henderson C.R., Cory-Slechta D.A., Cox C., Jusko T.A., Lanphear B.P. Intellectual impairment in children with blood lead concentrations below 10 microgram per deciliter. N. Engl. J. Med. 2003, 348:1517-1526.
8. Catalano P.J., Ryan L.M. Bivariate latent variable models for clustered discrete and continuous outcomes. J. Am. Stat. Assoc. 1992, 87:651-658.
9. CDC Preventing Lead Poisoning in Young Children 2005, Centers for Disease Control and Prevention.
10. CDC Fourth National Report on Human Exposure to Environmental Chemicals. Updated tables 2014, Centers for Disease Control and Prevention.
11. Chambers A., Krewski D., Birkett N., Plunkett L., Hertzberg R., Danzeisen R., Aggett P.J., Starr T.B., Baker S., Dourson M., Jones P., Keen C.L., Meek B., Schoeny R., Slob W. An exposure-response curve for copper excess and deficiency. J. Toxicol. Environ. Health B: Crit. Rev. 2010, 13:546-578.
12. Criswell S., Sterling C., Swisher L., Evanoff B., Racette B.A. Sensitivity and specificity of the finger tapping task for the detection of psychogenic movement disorders. Parkinsonism Relat. Disord. 2010, 16:197-201.
13. Davidson P.W., Myers G.J., Cox C., Wilding G.E., Shamlaye C.F., Huang L.S., Cernichiari E., Sloane-Reeves J., Palumbo D., Clarkson T.W. Methylmercury and neurodevelopment: longitudinal analysis of the Seychelles child development cohort. Neurotoxicol. Teratol. 2006, 28:529-535.
14. Debes F., Budtz-Jorgensen E., Weihe P., White R.F., Grandjean P. Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicol. Teratol. 2006, 28:363-375.
15. Dehn M. Working Memory and Academic Learning: Assessment and Intervention 2008, John Wiley & Sons, Inc., Hoboken, NJ.
16. Desai V., Kaler S.G. Role of copper in human neurological disorders. Am. J. Clin. Nutr. 2008, 88:855-858.
17. Emsley C.L., Gao S., Li Y., Liang C., Ji R., Hall K.S., Cao J., Ma F., Wu Y., Ying P., Zhang Y., Sun S., Unverzagt F.W., Slemenda C.W., Hendrie H.C. Trace element levels in drinking water and cognitive function among elderly Chinese. Am. J. Epidemiol. 2000, 151:913-920.
18. EPA Toxicological Review of Thallium Compounds 2009, U.S. Environmental Protection Agency.
19. Epstein J.N., Erkanli A., Conners C.K., Klaric J., Costello J.E., Angold A. Relations between continuous performance test performance measures and ADHD behaviors. J. Abnorm. Child Psychol. 2003, 31:543-554.
20. Fischer P.W.F., L'Abbé M.R., Giroux A. Effects of age, smoking, drinking, exercise and estrogen use on indices of copper status in healthy adults. Nutr. Res. 1990, 10:1081-1090.
21. Franzen M. Reliability and Validity in Neuropsychological Assessment 2000, Springer. second ed.
22. Freire C., Ramos R., Lopez-Espinosa M.J., Diez S., Vioque J., Ballester F., Fernandez M.F. Hair mercury levels, fish consumption, and cognitive development in preschool children from Granada, Spain. Environ. Res. 2010, 110:96-104.
23. Gao S., Jin Y., Unverzagt F.W., Ma F., Hall K.S., Murrell J.R., Cheng Y., Shen J., Ying B., Ji R., Matesan J., Liang C., Hendrie H.C. Trace element levels and cognitive function in rural elderly Chinese. J. Gerontol., A: Biol. Sci. Med. Sci. 2008, 63:635-641.
24. Gao Y., De Galan S., De Brauwere A., Baeyens W., Leermakers M. Mercury speciation in hair by headspace injection-gas chromatography-atomic fluorescence spectrometry (methylmercury) and combustion-atomic absorption spectrometry (total Hg). Talanta 2010, 82:1919-1923.
25. Gao Y., Yan C.H., Tian Y., Wang Y., Xie H.F., Zhou X., Yu X.D., Yu X.G., Tong S., Zhou Q.X., Shen X.M. Prenatal exposure to mercury and neurobehavioral development of neonates in Zhoushan City, China. Environ. Res. 2007, 105:390-399.
26. Gilbert S.G., Weiss B. A rationale for lowering the blood lead action level from 10 to 2μg/dL. Neurotoxicology 2006, 27:693-701.
27. Grandjean P., Weihe P., White R.F., Debes F., Araki S., Yokoyama K., Murata K., Sorensen N., Dahl R., Jorgensen P.J. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 1997, 19:417-428.
28. Greene W., Henscher D. Bivariate and multivariate ordered choice models. Modeling Ordered Choices 2010, 222-229. Cambridge University Press, Cambridge. W. Greene, D. Henscher (Eds.).
29. Hamadani J.D., Tofail F., Nermell B., Gardner R., Shiraji S., Bottai M., Arifeen S.E., Huda S.N., Vahter M. Critical windows of exposure for arsenic-associated impairment of cognitive function in pre-school girls and boys: a population-based cohort study. Int. J. Epidemiol. 2011, 40:1593-1604.
30. Hanna C.P., Tyson J.F., McIntosh S. Determination of inorganic arsenic and its organic metabolites in urine by flow-injection hydride generation atomic absorption spectrometry. Clin. Chem. 1993, 39:1662-1667.
31. Harada M., Nakanishi J., Yasoda E., Pinheiro M.C., Oikawa T., de Assis Guimaraes G., da Silva Cardoso B., Kizaki T., Ohno H. Mercury pollution in the Tapajos River basin, Amazon: mercury level of head hair and health effects. Environ. Int. 2001, 27:285-290.
32. He M.D., Xu S.C., Zhang X., Wang Y., Xiong J.C., Zhang X., Lu Y.H., Zhang L., Yu Z.P., Zhou Z. Disturbance of aerobic metabolism accompanies neurobehavioral changes induced by nickel in mice. Neurotoxicology 2013, 38:9-16.
33. Heitland P., Koster H.D. Fast simple and reliable routine determination of 23 elements in urine by ICP-MS. J. Anal. At. Spectrom. 2004, 19:1552-1558.
34. Izenman A. Multivariate regression. Modern Multivariate Statistical Techmiques. Regression, Classification, and Manifold Learning 2008, 159-194. Springer, New York. A. Izenman (Ed.).
35. Jedrychowski W., Perera F., Jankowski J., Rauh V., Flak E., Caldwell K.L., Jones R.L., Pac A., Lisowska-Miszczyk I. Fish consumption in pregnancy, cord blood mercury level and cognitive and psychomotor development of infants followed over the first three years of life: Krakow epidemiologic study. Environ. Int. 2007, 33:1057-1062.
36. Jiang C., Zeng Z.B. Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 1995, 140:1111-1127.
37. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283:65-87.
38. Jusko T.A., Henderson C.R., Lanphear B.P., Cory-Slechta D.A., Parsons P.J., Canfield R.L. Blood lead concentrations <10μg/dL and child intelligence at 6 years of age. Environ. Health Perspect. 2007, 116:243-248.
39. Karada M. Congenital Minamata disease: intrauterine methylmercury poisoning. Teratology 1978, 18:285-288.
40. Kicinski M., Viaene M.K., Den Hond E., Schoeters G., Covaci A., Dirtu A.C., Nelen V., Bruckers L., Croes K., Sioen I., Baeyens W., Van Larebeke N., Nawrot T.S. Neurobehavioral function and low-level exposure to brominated flame retardants in adolescents: a cross-sectional study. Environ. Health 2012, 11:86.
41. Kitazawa M., Cheng D., LaFerla F.M. Chronic copper exposure exacerbates both amyloid and tau pathology and selectively dysregulates CDK5 in a mouse model of AD. J. Neurochem. 2009, 108:1550-1560.
42. Knott S.A., Haley C.S. Multitrait least squares for quantitative trait loci detection. Genetics 2000, 156:899-911.
43. Kuo H.C., Huang C.C., Tsai Y.T., Chu C.C., Hsieh S.T., Chu N.S. Acute painful neuropathy in thallium poisoning. Neurology 2005, 65:302-304.
44. Kuoppamaki M., Rothwell J.C., Brown R.G., Quinn N., Bhatia K.P., Jahanshahi M. Parkinsonism following bilateral lesions of the globus pallidus: performance on a variety of motor tasks shows similarities with Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 2005, 76:482-490.
45. Lam P.K., Kritz-Silverstein D., Barrett Connor E., Milne D., Nielsen F., Gamst A., Morton D., Wingard D. Plasma trace elements and cognitive function in older men and women: the Rancho Bernardo study. J. Nutr. Health Aging 2008, 12:22-27.
46. Landrigan P.J., Baloh R.W., Barthel W.F., Whitworth R.H., Staehling N.W., Rosenblum B.F. Neuropsychological dysfunction in children with chronic low-level lead absorption. Lancet 1975, 305:708-712.
47. Lanphear B.P., Dietrich K., Auinger P., Cox C. Cognitive deficits associated with blood lead concentrations <10μg/dL in US children and adolescents. Public Health Rep. 2000, 115:521-529.
48. Lanphear B.P., Hornung R., Khoury J., Yolton K., Baghurst P., Bellinger D.C., Canfield R.L., Bornschein R., Greene T., Rothenberg S.J., Needleman H.L., Schnaas L., Wasserman G., Graziano J., Roberts R. Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ. Health Perspect. 2005, 113:894-899.
49. Letz R. NES3 User's Manual 2000, Neurobehavioral Systems Inc., Atlanta, GA.
50. Levy F., Hobbes G. Discrimination of attention deficit hyperactivity disorder by the continuous performance test. J. Paediatr. Child Health 1997, 33:384-387.
51. Lidsky T.I., Schneider J.S. Lead neurotoxicity in children: basic mechanisms and clinical correlates. Brain 2003, 126:5-19.
52. Linder M.C., Hazegh-Azam M. Copper biochemistry and molecular biology. Am. J. Clin. Nutr. 1996, 63:797s-811s.
53. Lu J., Wu D., Zheng Y., Sun D., Hu B., Shan Q., Zhang Z., Fan S. Trace amounts of copper exacerbate beta amyloid-induced neurotoxicity in the cholesterol-fed mice through TNF-mediated inflammatory pathway. Brain Behav. Immun. 2009, 23:193-203.
54. Madsen E., Gitlin J.D. Copper and iron disorders of the brain. Annu. Rev. Neurosci. Annu. Rev. 2007, 317-337.
55. Mao X., Ye J., Zhou S., Pi R., Dou J., Zang L., Chen X., Chao X., Li W., Liu M., Liu P. The effects of chronic copper exposure on the amyloid protein metabolism associated genes' expression in chronic cerebral hypoperfused rats. Neurosci. Lett. 2012, 518:14-18.
56. Marsh D., Myers G., Clarkson T., Amin-Zaki L., Tikriti S., Majeed M. Fetal methylmercury poisoning: clinical and toxicological data on 29 cases. Ann. Neurol. 1980, 7:348-353.
57. McDowell M.A., Dillon C.F., Osterloh J., Bolger P.M., Pellizzari E., Fernando R., Montes de Oca R., Schober S.E., Sinks T., Jones R.L., Mahaffey K.R. Hair mercury levels in U.S. children and women of childbearing age: reference range data from NHANES 1999-2000. Environ. Health Perspect. 2004, 112:1165-1171.
58. Michos C., Kalfakakou V., Karkabounas S., Kiortsis D., Evangelou A. Changes in copper and zinc plasma concentrations during the normal menstrual cycle in women. Gynecol. Endocrinol. 2010, 26:250-255.
59. Morris M. Dietary copper and high saturated and trans fat intakes associated with cognitive decline. Arch. Neurol. 2006, 63:1085-1088.
60. Murray R., Bender D., Botham K., Kennelly P., Rodwell V., Weil P. Harpers Illustrated Biochemistry 2012, The McGraw-Hill Companies, Inc., New York. 29th ed.
61. Needleman H.L., Schell A., Bellinger D., Leviton A., Allred E.N. The long-term effects of exposure to low doses of lead in childhood. An 11-year follow-up report. N. Engl. J. Med. 1990, 322:83-88.
62. Nordberg M., Winblad B., Basun H. Cadmium concentration in blood in an elderly urban population. Biometals 2000, 13:311-317.
63. Phillips S.M., Sherwin B.B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 1992, 17:497-506.
64. Pocock S.J., Smith M., Baghurst P. Environmental lead and children's intelligence: a systematic review of the epidemiological evidence. BMJ 1994, 309:1189-1197.
65. Pollak Y., Weiss P.L., Rizzo A.A., Weizer M., Shriki L., Shalev R.S., Gross-Tsur V. The utility of a continuous performance test embedded in virtual reality in measuring ADHD-related deficits. J. Dev. Behav. Pediatr. 2009, 30:2-6.
66. Riccio C.A., Reynolds C.R., Lowe P., Moore J.J. The continuous performance test: a window on the neural substrates for attention?. Arch. Clin. Neuropsychol. 2002, 17:235-272.
67. Riederer A.M., Belova A., George B.J., Anastas P.T. Urinary cadmium in the 1999-2008 U.S. National Health and Nutrition Examination Survey (NHANES). Environ. Sci. Technol. 2013, 47:1137-1147.
68. Roels H.A., Bowler R.M., Kim Y., Claus Henn B., Mergler D., Hoet P., Gocheva V.V., Bellinger D.C., Wright R.O., Harris M.G., Chang Y., Bouchard M.F., Riojas-Rodriguez H., Menezes-Filho J.A., Tellez-Rojo M.M. Manganese exposure and cognitive deficits: a growing concern for manganese neurotoxicity. Neurotoxicology 2012, 33:872-880.
69. Rosado J.L., Ronquillo D., Kordas K., Rojas O., Alatorre J., Lopez P., Garcia-Vargas G., Caamano M., Cebriaín M.E., Stoltzfus R.J. Arsenic exposure and cognitive performance in Mexican school children. Environ. Health Perspect. 2007, 115:1371-1375.
70. Rosenberg L., Park S. Verbal and spatial functions across the menstrual cycle in healthy young women. Psychoneuroendocrinology 2002, 27:835-841.
71. Rubin D., Schenker N. Multiple imputation for interval estimation from simple random samples with ignorable nonresponse. J. Am. Stat. Assoc. 1986, 81:366-374.
72. Salustri C., Barbati G., Ghidoni R., Quintiliani L., Ciappina S., Binetti G., Squitti R. Is cognitive function linked to serum free copper levels? A cohort study in a normal population. Clin. Neurophysiol. 2010, 121:502-507.
73. Santamaria A.B., Sulsky S.I. Risk assessment of an essential element: manganese. J. Toxicol. Environ. Health, A 2010, 73:128-155.
74. Schafer J.L., Graham J.W. Missing data: our view of the state of the art. Psychol. Methods 2002, 7:147-177.
75. Schroijen C., Baeyens W., Schoeters G., Den Hond E., Koppen G., Bruckers L., Nelen V., Van De Mieroop E., Bilau M., Covaci A., Keune H., Loots I., Kleinjans J., Dhooge W., Van Larebeke N. Internal exposure to pollutants measured in blood and urine of Flemish adolescents in function of area of residence. Chemosphere 2008, 71:1317-1325.
76. Sparks D.L., Schreurs B.G. Trace amounts of copper in water induce beta-amyloid plaques and learning deficits in a rabbit model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11065-11069.
77. Squitti R., Lupoi D., Pasqualetti P., Dal Forno G., Vernieri F., Chiovenda P., Rossi L., Cortesi M., Cassetta E., Rossini P.M. Elevation of serum copper levels in Alzheimers disease. Neurology 2002, 59:1153-1161.
78. Starks S.E., Gerr F., Kamel F., Lynch C.F., Jones M.P., Alavanja M.C., Sandler D.P., Hoppin J.A. Neurobehavioral function and organophosphate insecticide use among pesticide applicators in the Agricultural Health Study. Neurotoxicol. Teratol. 2012, 34:168-176.
79. Strauss E., Sherman E., Spreen O. Tests of motor function. A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary 2006, 1042-1079. Oxford University Press, New York, NY. third ed. E. Strauss, E. Sherman, O. Spreen (Eds.).
80. Sunderman F.W., Dingle B., Hopfer S.M., Swift T. Acute nickel toxicity in electroplating workers who accidently ingested a solution of nickel sulfate and nickel chloride. Am. J. Ind. Med. 1988, 14:257-266.
81. Swanson L., Kim K. Working memory, short-term memory, and naming speed as predictors of children's mathematical performance. Intelligence 2007, 35:151-168.
82. Van Kempen E., Fischer P., Janssen N., Houthuijs D., Van Kamp I., Stansfeld S., Cassee F. Neurobehavioral effects of exposure to traffic-related air pollution and transportation noise in primary schoolchildren. Environ. Res. 2012, 115:18-25.
83. Vermeir G., Viaene M., Staessen J., Hond E.D., Roels H.A. Neurobehavioural investigations in adolescents exposed to environmental pollutants. Environ. Toxicol. Pharmacol. 2005, 19:707-713.
84. Viaene M.K., Masschelein R., Leenders J., De Groof M., Swerts L.J., Roels H.A. Neurobehavioural effects of occupational exposure to cadmium: a cross sectional epidemiological study. Occup. Environ. Med. 2000, 57:19-27.
85. Wang S., Zhang J., Zeng X., Zeng Y., Wang S., Chen S. Association of traffic-related air pollution with children's neurobehavioral functions in Quanzhou, China. Environ. Health Perspect. 2009, 117:1612-1618.
86. Wasserman G.A., Liu X., Parvez F., Ahsan H., Factor-Litvak P., Kline J., Van Geen A., Slavkovich V., LoIacono N.J., Levy D., Cheng Z., Graziano J.H. Water arsenic exposure and intellectual function in 6-year-old children in Araihazar, Bangladesh. Environ. Health Perspect. 2006, 115.
87. White M.A., Sabbioni E. Trace element reference values in tissues from inhabitants of the European Union X. A study of 13 elements in blood and urine of a United Kingdom population. Sci. Total Environ. 1998, 216:253-270.
88. Wright R.O., Baccarelli A. Metals and neurotoxicology. J. Nutr. 2007, 137:2809-2813.
89. Yoon F.B., Fitzmaurice G.M., Lipsitz S.R., Horton N.J., Laird N.M., Normand S.L. Alternative methods for testing treatment effects on the basis of multiple outcomes: simulation and case study. Stat. Med. 2011, 30:1917-1932.