Interpreting epidemiologic studies of developmental neurotoxicity: Conceptual and analytic issues

Neurotoxicology and Teratology

Volumn 31, Issue 5, 2009, Pages 267-274

  Bellinger, David C ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Causal models; Confounding; Developmental neurotoxicology; Effect modification; Epidemiology

Indexed keywords

NEUROTOXIN;

ACCURACY; ALZHEIMER DISEASE; ANALYTIC METHOD; ANALYTICAL ERROR; ATTENTION DEFICIT DISORDER; CHILD DEVELOPMENT; COMORBIDITY; CONCEPT ANALYSIS; CONDUCT DISORDER; CRIMINAL BEHAVIOR; DISEASE COURSE; DISEASE PREDISPOSITION; DNA DAMAGE; ENVIRONMENTAL EXPOSURE; EPIDEMIOLOGICAL DATA; EPIGENETICS; FOOD CONTAMINATION; GENETIC POLYMORPHISM; HUMAN; INTELLIGENCE QUOTIENT; METHODOLOGY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NEUROTOXICITY; PARENTAL ATTITUDE; POPULATION RESEARCH; PREDICTION; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; RISK ASSESSMENT; RISK FACTOR; SOCIAL ASPECT; SOCIAL STATUS; STANDARDIZATION; STATISTICAL MODEL; STATISTICAL SIGNIFICANCE; TOXICOKINETICS; VALIDITY;

BRAIN; CHILD; CHILD, PRESCHOOL; DOSE-RESPONSE RELATIONSHIP, DRUG; EPIDEMIOLOGIC STUDIES; HUMANS; NEUROTOXICITY SYNDROMES; REPRODUCIBILITY OF RESULTS; RISK ASSESSMENT; TOXICOLOGY;

EID: 69549108113     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2009.06.006     Document Type: Review

References (82)

1. Altman D.G., Schulz K.F., Moher D., Egger M., Davidoff F., Elbourne D., Gotzsche P.C., Lang T., and for the CONSORT Group. The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Ann. Intern. Med. 17 (2001) 663-694
2. Amler R.W., Barone S., Belger A., Berlin C.M., Cox C., Frank H., Goodman M., Harry J., Hooper S.R., Ladda R., LaKind J.S., Lipkin P.H., Lipsitt L.P., Lorber M.N., Myers G., Mason A.M., Needham L.L., Sonawane B., Wachs T.D., and Yager J.W. Hershey Medical Center Technical Workshop Report: optimizing the design and interpretation of epidemiologic studies for assessing neurodevelopmental effects from in utero chemical exposure. Neurotoxicology 27 (2006) 861-874
3. Bellinger D.C. Effect modification in epidemiologic studies of low-level neurotoxicant exposures and health outcomes. Neurotoxicol. Teratol. 22 (2000) 133-140
4. Bellinger D.C. What is an adverse effect? A possible resolution of clinical and epidemiological perspectives on neurobehavioral toxicity. Environ. Res. 95 (2004) 394-405
5. Bellinger D.C. Interpretation of small effect sizes in occupational and environmental neurotoxicology: individual versus population risk. Neurotoxicology 28 (2007) 245-251
6. Bergdahl I.A. Response to: "What is the meaning of non-linear dose-response relationships between blood lead concentrations and IQ?". Neurotoxicology 27 (2006) 1125
7. Blair A., Stewart P., Lubin J.H., and Forastiere F. Methodological issues regarding confounding and exposure misclassification in epidemiological studies of occupational exposures. Am. J. Ind. Med. 50 (2007) 199-207
8. Bower T.S., and Beck B.D. What is the meaning of non-linear dose-response relationships between blood-lead concentrations and IQ?. Neurotoxicology 27 (2006) 520-524
9. Braun J.M., Kahn R.S., Froehlich T., Auinger P., and Lanphear B.P. Exposures to environmental toxicants and attention deficit hyperactivity disorder in U.S. children. Environ. Health Perspect. 114 (2006) 1904-1909
10. Braun J.M., Froehlich T.E., Daniels J.L., Dietrich K.N., Hornung R., Auinger P., and Lanphear B.P. Association of environmental toxicants and conduct disorder in U.S. children: NHANES 2001-2004. Environ. Health Perspect. 116 (2008) 956-962
11. Budtz-Jorgensen E., Keiding N., and Grandjean P. Effects of exposure imprecision on estimation of the benchmark dose. Risk Anal. 24 (2004) 1689-1696
12. Budtz-Jørgensen E., Grandjean P., and Weihe P. Separation of risks and benefits of seafood intake. Environ. Health Perspect. 115 (2007) 323-327
13. Budtz-Jørgensen E., Keiding N., Grandjean P., and Weihe P. Confounder selection in environmental epidemiology: assessment of health effects of prenatal mercury exposure. Ann. Epidemiol. 17 (2007) 27-35
14. Cernichiari E., Brewer R., Myers G.J., Marsh D.O., Lapham L.W., Cox C., Shamlaye C.F., Berlin M., Davidson P.W., and Clarkson T.W. Monitoring methylmercury during pregnancy: maternal hair predicts fetal brain exposure. Neurotoxicology 16 (1995) 705-710
15. Chan A.W., Hrobjartsson A., Haahr M.T., Gotzsche P.C., and Altman D.G. Empirical evidence for selective reporting of outcomes in randomized trials. JAMA 291 (2004) 2457-2465
16. Choi A.L., Cordier S., Weihe P., and Grandjean P. Negative confounding in the evaluation of toxicity: the case of methylmercury in fish and seafood. Crit. Rev. Toxicol. 38 (2008) 877-893
17. Cory-Slechta D.A. Studying toxicants as single chemicals: does this strategy adequately identify neurotoxic risk?. Neurotoxicology 26 (2005) 491-510
18. Cory-Slechta D.A., Virgolini M.B., Rossi-George A., Thiruchelvam M., Lisek R., and Weston D. Lifetime consequences of combined maternal lead and stress. Basic Clin. Pharmacol. Toxicol. 102 (2008) 218-227
19. Damman O., and Leviton A. Perinatal brain damage causation. Dev. Neurosci. 29 (2007) 280-288
20. Davidson P.W., Strain J.J., Myers G.J., Thurston S.W., Bonham M.P., Shamlaye C.F., et al. Neurodevelopmental effects of maternal nutritional status and exposure to methylmercury from eating fish during pregnancy. Neurotoxicology 29 (2008) 767-775
21. Dohrenwend B.P., Levav I., Shrout P.E., Schwartz S., Naveh G., Link B.G., Skodol A.E., and Stueve A. Socioeconomic status and psychiatric disorders: the causation-selection issue. Science 255 (1992) 946-952
22. Echeverria D., Woods J.S., Heyer N.J., Rohlman D.S., Farin F.M., Bittner A.C., Li T., and Garabedian C. Chronic low-level mercury exposure, BDNF polymorphism, and associations with cognitive and motor function. Neurotoxicol. Teratol. 27 (2005) 781-796
23. Echeverria D., Woods J.S., Heyer N.J., Rohlman D., Farin F.M., Li T., and Garabedian C.E. The association between a genetic polymorphism of coproporphyrinogen oxidase, dental mercury exposure and neurobehavioral response in humans. Neurotoxicol. Teratol. 28 (2006) 39-48
24. Fewell Z., Davey Smith G., and Sterne J.A. The impact of residual and unmeasured confounding in epidemiologic studies: a simulation study. Am. J. Epidemiol. 166 (2007) 646-655
25. Fewtrell L.J., Pruss-Ustun A., Landrigan P., and Ayuso-Mateos J.L. Estimating the global burden of disease of mild mental retardation and cardiovascular diseases from environmental lead exposure. Environ. Res. 94 (2004) 120-133
26. Froehlich T.E., Lanphear B.P., Dietrich K.N., Cory-Slechta D.A., Wang N., and Kahn R.S. Interactive effects of a DRD4 polymorphism, lead, and sex on executive functions in children. Biol. Psychiatry 62 (2007) 243-249
27. Grandjean P., Weihe P., Burse V.W., Needham L.L., Storr-Hansen E., Heinzow B., Debes F., Murata K., Simonsen H., Ellefsen P., Budtz-Jørgensen E., Keiding N., and White R.F. Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol. Teratol. 23 (2001) 305-317
28. Grandjean P., and Budtz-Jørgensen E. Total imprecision of exposure biomarkers: implications for calculating exposure limits. Am. J. Ind. Med. 50 (2007) 712-719
29. Greenland S., and Brumback B. An overview of relations among causal modeling methods. Int. J. Epidemiol. 31 (2002) 1030-1037
30. Guilarte T.R., Toscano C.D., McGlothan J.L., and Weaver S.A. Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann. Neurol. 53 (2003) 50-56
31. Gump B.B., Reihman J., Stewart P., Lonky E., Darvill T., and Matthews K.A. Blood lead (Pb) levels: a potential environmental mechanism explaining the relation between socioeconomic status and cardiovascular reactivity in children. Health Psychol. 26 (2007) 296-304
32. Heyer N.J., Echeverria D., Farin F.M., and Woods J.S. The association between serotonin transporter gene promoter polymorphism (5-HTTLPR), self-reported symptoms, and dental mercury exposure. J. Toxicol. Environ. Health A. 71 (2008) 1318-1326
33. Hornung R., Lanphrea B., and Dietrich K. Response to: "What is the meaning of non-linear dose-response relationships between blood lead concentrations and IQ?". Neurotoxicology 27 (2006) 635
34. Hu H., Téllez-Rojo M.M., Bellinger D., Smith D., Ettinger A.S., Lamadrid-Figueroa H., Schwartz J., Schnaas L., Mercado-García A., and Hernández-Avila M. Fetal lead exposure at each stage of pregnancy as a predictor of infant mental development. Environ. Health Perspect. 114 (2006) 1730-1735
35. Huang L.S., Cox C., Wilding G.E., Myers G.J., Davidson P.W., Shamlaye C.F., Cernichiari E., Sloane-Reeves J., and Clarkson T.W. Using measurement error models to assess effects of prenatal and postnatal methylmercury exposure in the Seychelles Child Development Study. Environ. Res. 93 (2003) 115-122
36. Ioannidis J.P. Why most published research findings are wrong. PLoS Med. 2 (2005) e124
37. Ioannidis J.P. Why most discovered true associations are inflated. Epidemiology 19 (2008) 640-648
38. Jurek A.M., Greenland S., Maldonado G., and Church T.R. Proper interpretation of non-differential misclassification effects: expectations vs. observations. Int. J. Epidemiol. 34 (2005) 680-687
39. Jusko T.A., Lockhart D.W., Sampson P.D., Henderson C.R., and Canfield R.L. Response to: "What is the meaning of non-linear dose-response relationships between blood lead concentrations and IQ?". Neurotoxicology 27 (2006) 1123-1125
40. Kaur P., Heggland I., Aschner M., and Syversen T. Docosahexaenoic acid may act as a neuroprotector for methylmercury-induced neurotoxicity in primary neural cell cultures. Neurotoxicology 29 (2008) 978-987
41. Kent D.M., and Hayward R.A. Limitations of applying summary results of clinical trials to individual patients. JAMA 298 (2007) 1209-1212
42. Kile M.L., Houseman E.A., Breton C.V., Quamruzzaman Q., Rahman M., Mahiuddin G., and Christiani D.C. Association between total ingested arsenic and toenail arsenic concentrations. J. Environ. Sci. Health A. Tox Hazard Subst. Environ. Eng. 42 (2007) 1827-1834
43. Kordas K., Canfield R.L., López P., Rosado J.L., Vargas G.G., Cebrián M.E., Rico J.A., Ronquillo D., and Stoltzfus R.J. Deficits in cognitive function and achievement in Mexican first-graders with low blood lead concentrations. Environ. Res. 100 (2006) 371-386
44. Lanphear B.P., Hornung R., Khoury J., Yolton K., Baghurst P., Bellinger D.C., Canfield R.L., Dietrich K.N., Bornschein R., Greene T., Rothenberg S.J., Needleman H.L., Schnaas L., Wasserman G., Graziano J., and Roberts R. Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ. Health Perspect. 113 (2005) 894-899
45. J. Little, J.P. Higgins, J.P. Ioannidis, D. Moher, F. Gagnon, E. von Elm, M.J. Khoury, B. Cohen, G. Davey-Smith, J. Grimshaw, P. Scheet, M. Gwinn, R.E. Williamson, G.Y. Zou, K. Hutchings, C.Y. Johnson, V. Tait, M. Wiens, J. Golding, C. van Duijn, J. McLaughlin, A. Paterson, G. Wells, I. Fortier, M. Freedman, M. Zecevic, R. King, C. Infante-Rivard, A. Stewart, N. Birkett, STrengthening the REporting of Genetic Associarion Studies (STREGA)-an extension of the STROBE statement. American Journal of Epidemiology 170 (2009) 269-279.
46. McGowan P.O., Meaney M.J., and Szyf M. Diet and the epigenetic (re)programming of phenotypic differences in behavior. Brain. Res. 1237 (2008) 12-24
47. Moher D., Cook D.J., Eastwood S., Olkin I., Rennie D., and Stroup D.F. Improving the quality of reports of meta-analyses of randomized controlled trials: the QUOROM statement. Br. J. Surg. 87 (2000) 1448-1454
48. Muir T., and Zegarac M. Societal costs of exposure to toxic substances: economic and health costs of four case studies that are candidates for environmental causation. Environ. Health Perspect. 109 Suppl 6 (2001) 885-903
49. Needleman H.L., McFarland C., Ness R.B., Fienberg S.E., and Tobin M.J. Bone lead levels in adjudicated delinquents. A case control study. Neurotoxicol. Teratol. 24 (2002) 711-717
50. Oken E., Radesky J.S., Wright R.O., Bellinger D.C., Amarasiriwardena C.J., Kleinman K.P., Hu H., and Gillman M.W. Maternal fish intake during pregnancy, blood mercury levels, and child cognition at age 3 years in a US cohort. Am. J. Epidemiol. 167 (2008) 1171-1181
51. Oken E., Wright R.O., Kleinman K.P., Bellinger D., Amarasiriwardena C.J., Hu H., Rich-Edwards J.W., and Gillman M.W. Maternal fish consumption, hair mercury, and infant cognition in a U.S. cohort. Environ. Health Perspect. 113 (2005) 1376-1380
52. Pardini D.A. Novel insights into longstanding theories of bidirectional parent-child influences: introduction to the special section. J. Abn. Child Psychol. 36 (2008) 627-631
53. Pearce N. Analytical implications of epidemiological concepts of interaction. Int. J. Epidemiol. 17 (1989) 976-980
54. Pocock S.J., Collier T.J., Dandreo K.J., de Stavola B.I., Goldman M.B., Kalish L.A., Kasten L.E., and McCormack V.A. Issues in the reporting of epidemiological studies: a survey of recent practice. BMJ 329 (2004) 883-888
55. Rajan P., Kelsey K.T., Schwartz J.D., Bellinger D.C., Weuve J., Spiro A., Sparrow D., Smith T.J., Nie H., Weisskopf M.G., Hu H., and Wright R.O. Interaction of the delta-aminolevulinic acid dehydratase polymorphism and lead burden on cognitive function: the VA normative aging study. J. Occup. Environ. Med. 50 (2008) 1053-1061
56. Rice D.C. Assessing the effects of environmental toxicant exposure in developmental epidemiological studies: issues for risk assessment. Neurotoxicology 26 (2005) 483-489
57. Rice D.C., Schoeny R., and Mahaffey K. Methods and rationale for derivation of a reference dose for methylmercury by the U.S. EPA. Risk Anal. 23 (2003) 107-115
58. Rose G. Sick individuals and sick populations. Int. J. Epidemiol. 14 (1985) 32-38
59. Rose G. Ancel Keys lecture. Circulation 84 (1991) 1405-1409
60. Rose G., and Day S. The population mean predicts the number of deviant individuals. BMJ 301 (1990) 1031-1034
61. Rothman K., and Greenland S. Causation and causal inference in epidemiology. Am. J. Public. Health 95 Suppl 1 (2005) S144-150
62. Sale A., Cenni M.C., Ciucci F., Putignano E., Chieri S., and Maffei L. Maternal enrichment during pregnancy accelerates retinal development of the fetus. PLoS One 11 (2007) e1160
63. Schnaas L., Rothenberg S.J., Flores M.F., Martinez S., Hernandez C., Osorio E., Velasco S.R., and Perroni E. Reduced intellectual development in children with prenatal lead exposure. Environ. Health Perspect. 114 (2006) 791-797
64. Schneider J.S., and Decamp E. Postnatal lead poisoning impairs behavioral recovery following brain damage. Neurotoxicology 28 (2007) 1153-1157
65. Stangle D.E., Strawderman M.S., Kuypers D.S.M., and Strupp B.J. Reductions in blood lead overestimate reductions in brain lead following repeated succimer regimens in a rodent model of childhood lead exposure. Environ. Health Perspect. 112 (2004) 302-308
66. Stewart P., Fitzgerald S., Reihman J., Gump B., Lonky E., Darvill T., Pagano J., and Hauser P. Prenatal PCB exposure, the corpus callosum, and response inhibition. Environ. Health Perspect. 111 (2003) 1670-1677
67. Stewart P.W., Reihman J., Lonky E.I., Darvill T.J., and Pagano J. Cognitive development in preschool children prenatally exposed to PCBs and MeHg. Neurotoxicol. Teratol. 25 (2003) 11-22
68. Stewart P. The critical concept of control in human neurobehavioral toxicology studies: We can, and must, do better. In: Bellinger D.C. (Ed). Human Developmental Neurotoxicology (2006), Taylor & Francis Group, New York 361-378
69. Stone S.P., Cooper B.S., Kibbler C.C., Cookson B.D., Roberts J.A., Medley G.F., Duckworth G., Lai R., Ebrahim S., Brown E.M., Wiffen P.J., and Davey P.G. The ORION statement: guidelines for transparent reporting of outbreak reports and intervention studies of nosocomial infections. Lancet. Infect. Dis. 7 (2007) 282-288
70. Strain J.J., Davidson P.W., Bonham M.P., Duffy E.M., Stokes-Riner A., Thurston S.W., Wallace J.M., Robson P.J., Shamlaye C.F., Georger L.A., Sloane-Reeves J., Cernichiari E., Canfield R.L., Cox C., Huang L.S., Janciuras J., Myers G.J., and Clarkson T.W. Associations of maternal long-chain polyunsaturated fatty acids, methyl mercury, and infant development in the Seychelles Child Development Nutrition Study. Neurotoxicology 29 (2008) 776-782
71. Tiffany-Castiglioni E., Hong S., Qian Y., Tang Y., and Donnelly K.C. In vitro models for assessing neurotoxicity of mixtures. Neurotoxicology 27 (2006) 835-839
72. Vineis P., and Kriebel D. Causal models in epidemiology: past inheritance and genetic future. Environ. Health 5 (2006) 21
73. von Elm E., and Egger M. The scandal of poor epidemiological research. BMJ 329 (2004) 868-869
74. von Elm E., Altman D.G., Egger M., Pocock S.J., Gotzsche P.C., Vandenbroucke J.P., and for the STROBE Initative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J. Clin. Epidemiol. 61 (2008) 344-349
75. Wallace C.S., Reitzenstein J., and Withers G.S. Diminished experience-dependent neuroanatomical plasticity: evidence for an improved biomarker of subtle neurotoxic damage to the developing rat brain. Environ. Health Perspect. 111 (2003) 1294-1298
76. Wang F.T., Hu H., Schwartz J., Weuve J., Spiro A.S., Sparrow D., Nie H., Silverman E.K., Weiss S.T., and Wright R.O. Modifying effects of the HFE polymorphisms on the association between lead burden and cognitive decline. Environ. Health Perspect. 115 (2007) 1210-1215
77. Weiss B., and Bellinger D.C. Social ecology of children's vulnerability to environmental pollutants. Environ. Health Perspect. 114 (2006) 1479-1485
78. Weisskopf M.G., Hu H., Sparrow D., Lenkinski R.E., and Wright R.O. Proton magnetic resonance spectroscopic evidence of glial effects of cumulative lead exposure in the adult human hippocampus. Environ. Health Perspect. 115 (2007) 519-523
79. Wright J.P., Dietrich K.N., Ris M.D., Hornung R.W., Wessel S.D., Lanphear B.P., Ho M.M., and Rae M.N. Association of prenatal and childhood blood lead concentrations with criminal arrests in early adulthood. PLoS Med. 5 (2008) e101
80. Wright R.O., Amarasiriwardena C., Woolf A.D., Jim R., and Bellinger D.C. Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology 27 (2006) 210-216
81. Wu J., Bashia M.R., and Zawia N.H. The environment, epigenetics and amyloidogenesis. J. Mol. Neurosci. 34 (2008) 1-7
82. Yuan W., Holland S.K., Cecil K.M., Dietrich K.N., Wessel S.D., Altaye M., Hornung R.W., Ris M.D., Egelhoff J.C., and Lanphear B.P. The impact of early childhood lead exposure on brain organization: a functional magnetic resonance imaging study of language function. Pediatrics 118 (2006) 971-977