Early-life exposure to polycyclic aromatic hydrocarbons and ADHD behavior problems

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Perera, Frederica P ^a,b   Chang, Hsin Wen ^a,b   Tang, Deliang ^a,b   Roen, Emily L ^a,b   Herbstman, Julie ^a,b   Margolis, Amy ^b,c   Huang, Tzu Jung ^a,b   Miller, Rachel L ^a,b,c   Wang, Shuang ^a,b   Rauh, Virginia ^b  

^a Department of Environmental Health Sciences Mailman School of Public Health Columbia University ^*  (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c Department of Biostatistics Mailman School of Public Health Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; POLYCYCLIC AROMATIC HYDROCARBON;

AFRICAN AMERICAN; AIR POLLUTION; ARTICLE; ATTENTION DEFICIT DISORDER; BLOOD SAMPLING; CHILD; CHILD BEHAVIOR CHECKLIST; COHORT ANALYSIS; CONNERS PARENT RATING SCALE REVISED; DEMOGRAPHY; DIETARY INTAKE; DISEASE ASSOCIATION; DNA ADDUCT; DOMINICAN (DOMINICA); DSM-IV; FEMALE; FOLLOW UP; HUMAN; MAJOR CLINICAL STUDY; MALE; MATERNAL BLOOD; NEWBORN; OUTCOME ASSESSMENT; PASSIVE SMOKING; PERINATAL DRUG EXPOSURE; PREGNANCY; PRENATAL EXPOSURE; PRESCHOOL CHILD; PROSPECTIVE STUDY; RATING SCALE; SCHOOL CHILD; SMOKING; SOCIAL STATUS; STRUCTURED QUESTIONNAIRE; UMBILICAL CORD BLOOD; UNITED STATES; URBAN AREA; URINALYSIS; ADOLESCENT; ADULT; ADVERSE EFFECTS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; ENVIRONMENTAL EXPOSURE; ETHNOLOGY; HISPANIC; INFANT; YOUNG ADULT;

ADOLESCENT; ADULT; AFRICAN AMERICANS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CHILD; CHILD, PRESCHOOL; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; ENVIRONMENTAL EXPOSURE; FEMALE; HISPANIC AMERICANS; HUMANS; INFANT; INFANT, NEWBORN; MALE; MATERNAL EXPOSURE; NEW YORK CITY; POLYCYCLIC HYDROCARBONS, AROMATIC; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; YOUNG ADULT;

EID: 84910623332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111670     Document Type: Article

References (87)

1. Bostrom CE, Gerde P, Hanberg A., Jernstrom B, Johansson C, et al. (2002) Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ Health Perspect 110: 451-488.
2. Perera FP, Illman SM, Kinney P.L., Whyatt RM, Kelvin EA, et al. (2002) The challenge of preventing environmentally related disease in young children: community-based research in New York City. Environ Health Perspect 110: 197-204.
3. Woodruff TJ, Parker JD, Kyle A.D., Schoendorf KC (2003) Disparities in exposure to air pollution during pregnancy. Environmental Health Perspectives 111: 942-946.
4. Jerrett M (2009) Global Geographies of Injustice in Traffic-Related Air Pollution Exposure. Epidemiology 20: 231-233 210.1097/EDE.1090b1013e318197 76a31819771.
5. Morello-Frosch R, Zuk M, Jerrett M., Shamasunder B, Kyle AD (2011) Understanding The Cumulative Impacts Of Inequalities In Environmental Health: Implications For Policy. Health Affairs 30: 879-887.
6. Perera FP, Tang D, Wang S., Vishnevetsky J, Zhang B, et al. (2012) Prenatal Polycyclic Aromatic Hydrocarbon (PAH) Exposure and Child Behavior at age 6-7. Environ Health Perspect.
7. Mooney LA, Santella RM, Covey L, Jeffrey A.M., Bigbee W., et al. (1995) Decline of DNA damage and other biomarkers in peripheral blood following smoking cessation. Cancer Epidemiol Biomarkers Prev 4: 627-634.
8. Godschalk RWL, Van Schooten FJ, Bartsch H (2003) A critical evaluation of DNA adducts as biological markers for human exposure to polycyclic aromatic compounds. Journal of Biochemistry and Molecular Biology 36: 1-11.
9. Veglia F, Loft S, Matullo G., Peluso M, Munnia A, et al. (2008) DNA adducts and cancer risk in prospective studies: a pooled analysis and a meta-analysis. Carcinogenesis 29: 932-936.
10. Anderson LM, Diwan BA, Fear N.T., Roman E (2000) Critical windows of exposure for children's health: cancer in human epidemiological studies and neoplasms in experimental animal models. Environ Health Perspect 108: 573-594.
11. National Research Council (1993) Toxicity Testing and Strategies to Determine Needs and Priorities. Washington, D.C.: National Academy Press.
12. Perera FP, Tang D, Jedrychowski W., Hemminki K, Santella RM, et al. (2004) Biomarkers in maternal and newborn blood indicate heightened fetal susceptibility to procarcinogenic DNA damage. Environ Health Perspect 112: 1133-1136.
13. Grandjean P, Landrigan PJ (2006) Developmental neurotoxicity of industrial chemicals. Lancet 368: 2167-2178.
14. Stein J, Schettler T, Wallinga D., Valenti M (2002) In harm's way: toxic threats to child development. J Dev Behav Pediatr 23: S13-22.
15. Shonkoff JP, Garner AS, Committee on Psychosocial Aspects of Child And Family Health, Committee on Early Childhood, Adoption, and Dependent Care, Section on Developmental and Behavioral Pediatrics (2012) The Lifelong Effects of Early Childhood Adversity and Toxic Stress. Pediatrics 129: E232-E246.
16. Brown LA, Khousbouei H, Goodwin J.S., Irvin-Wilson CV, Ramesh A, et al. (2007) Down-regulation of early ionotrophic glutamate receptor subunit developmental expression as a mechanism for observed plasticity deficits following gestational exposure to benzo(a)pyrene. Neurotoxicology 28: 965-978.
17. Wormley DD, Ramesh A, Hood DB (2004) Environmental contaminant-mixture effects on CNS development, plasticity, and behavior. Toxicol Appl Pharmacol 197: 49-65.
18. Grova N, Valley A, Turner J.D., Morel A., Muller CP, et al. (2007) Modulation of behavior and NMDA-R1 gene mRNA expression in adult female mice after sub-acute administration of benzo(a)pyrene. Neurotoxicology 28: 630-636.
19. Schellenberger MT, Grova N, Farinelle S., Willième S, Schroeder H., et al. (2013) Modulation of benzo[a]pyrene induced neurotoxicity in female mice actively immunized with a B[a]P-diphtheria toxoid conjugate. Toxicology and Applied Pharmacology 271: 175-183.
20. Perera FP, Rauh V, Whyatt R.M., Tsai WY, Tang D, et al. (2006) Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect 114: 1287-1292.
21. Perera FP, Li Z, Whyatt R., Hoepner L, Wang S, et al. (2009) Prenatal polycyclic aromatic hydrocarbon exposure and child intelligence at age 5. Pediatrics 124: e195-e202.
22. Bostic JQ, Prince JB (2008) Child and adolescent psychiatric disorders. In: Stern TA, Rosenbaum JF, Fava M, Biederman J, Rauch SL, editors. Massachusetts General Hospital Comprehensive Clinical Psychiatry. 1st ed. Philadelphia, PA: Elsevier Mosby.
23. Wilens TE, Biederman J, Brown S., Tanguay S, Monuteaux MC, et al. (2002) Psychiatric Comorbidity and Functioning in Clinically Referred Preschool Children and School-Age Youths With ADHD. Journal of the American Academy of Child & Adolescent Psychiatry 41: 262-268.
24. Spencer TJ, Biederman J, Mick E (2007) Attention-deficit/hyperactivity disorder: diagnosis, lifespan, comorbidities, and neurobiology. J Pediatr Psychol 32: 631-642.
25. Biederman J, Faraone SV, Keenan K, Benjamin J., Krifcher B, et al. (1992) Further Evidence for Family-Genetic Risk-Factors in Attention-Deficit Hyperactivity Disorder - Patterns of Comorbidity in Probands and Relatives in Psychiatrically and Pediatrically Referred Samples. Archives of General Psychiatry 49: 728-738.
26. Spencer T, Biederman J, Wilens T (1999) Attention-deficit/hyperactivity disorder and comorbidity. Pediatr Clin North Am 46: 915-927, vii.
27. Charach A, Yeung E, Climans T., Lillie E (2011) Childhood Attention-Deficit/Hyperactivity Disorder and Future Substance Use Disorders: Comparative Meta-Analyses. Journal of the American Academy of Child and Adolescent Psychiatry 50: 9-21.
28. Lee SS, Humphreys KL, Flory K, Liu R., Glass K (2011) Prospective association of childhood attention-deficit/hyperactivity disorder (ADHD) and substance use and abuse/dependence: a meta-analytic review. Clin Psychol Rev 31: 328-341.
29. Groenman AP, Oosterlaan J, Rommelse N., Franke B, Roeyers H, et al. (2013) Substance use disorders in adolescents with attention deficit hyperactivity disorder: a 4-year follow-up study. Addiction 108: 1503-1511.
30. Shaw M, Hodgkins P, Caci H., Young S, Kahle J, et al. (2012) A systematic review and analysis of long-term outcomes in attention deficit hyperactivity disorder: effects of treatment and non-treatment. BMC Med 10: 99.
31. Banerjee TD, Middleton F, Faraone SV (2007) Environmental risk factors for attention-deficit hyperactivity disorder. Acta Paediatr 96: 1269-1274.
32. Froehlich TE, Anixt JS, Loe I.M., Chirdkiatgumchai V., Kuan L, et al. (2011) Update on environmental risk factors for attention-deficit/hyperactivity disorder. Curr Psychiatry Rep 13: 333-344.
33. Siddique S, Banerjee M, Ray M.R., Lahiri T (2011) Attention-deficit hyperactivity disorder in children chronically exposed to high level of vehicular pollution. Eur J Pediatr 170: 923-929.
34. Newman NC, Ryan P, Lemasters G., Levin L, Bernstein D, et al. (2013) Traffic-related air pollution exposure in the first year of life and behavioral scores at 7 years of age. Environ Health Perspect 121: 731-736.
35. Chiu YHM, Bellinger DC, Coull B.A., Anderson S., Barber R, et al. (2013) Associations between Traffic-Related Black Carbon Exposure and Attention in a Prospective Birth Cohort of Urban Children. Environ Health Perspect 121: 859-864.
36. Perera FP, Rauh V, Tsai W.Y., Kinney P., Camann D, et al. (2003) Effects of transplacental exposure to environmental pollutants on birth outcomes in a multi-ethnic population. Environ Health Perspect 111: 201-205.
37. Schuurmans C, Kurrasch DM (2013) Neurodevelopmental consequences of maternal distress: what do we really know? Clinical Genetics 83: 108-117.
38. Bergman K, Sarkar P, O'Connor TG, Modi N, Glover V (2007) Maternal Stress During Pregnancy Predicts Cognitive Ability and Fearfulness in Infancy. Journal of the American Academy of Child & Adolescent Psychiatry 46: 1454-1463.
39. Barry TD, Dunlap ST, Cotten S.J., Lochman JE, Wells KC (2005) The Influence of Maternal Stress and Distress on Disruptive Behavior Problems in Boys. Journal of the American Academy of Child & Adolescent Psychiatry 44: 265-273.
40. Dohrenwend BS, Krasnoff L, Askenacy A., Dohrenwend B (1978) Exemplification of a method for scaling life events: the PERI life events scale. J Health Soc Behavior 19: 205-229.
41. Brown L, Sherbenou RJ, Johnson SK (1990) Test of non-verbal intelligence: a language-free measure of cognitive ability. 2nd edition. Austin, Tx: PRO-ED, Inc.
42. Caldwell BM, Bradley RH (1979) Home observation for measurement of the environment. Little Rock, AK: University of Arkansas Press.
43. Conners C, Erhardt D, Sparrow E (1999) Conners' Adult ADHD rating scales: Technical manual. New York: Multi-Health Systems.
44. Todd RD, Rasmussen ER, Neuman R.J., Reich W., Hudziak JJ, et al. (2001) Familiality and heritability of subtypes of attention deficit hyperactivity disorder in a population sample of adolescent female twins. Am J Psychiatry 158: 1891-1898.
45. Achenbach T, Rescorla L (2001) Child Behavior Checklist for age 6-18. Burlington VT: ASEBA, 6-1-01 Edition.
46. Alexandrov K, Rojas M, Geneste O., Castegnaro M, Camus AM, et al. (1992) An improved fluorometric assay for dosimetry of benzo(a)pyrene diol-epoxide-DNA adducts in smokers' lung: comparisons with total bulky adducts and aryl hydrocarbon hydroxylase activity. Cancer Res 52: 6248-6253.
47. Li Z, Romanoff LC, Trinidad D.A., Hussain N., Jones RS, et al. (2006) Measurement of urinary monohydroxy polycyclic aromatic hydrocarbons using automated liquid-liquid extraction and gas chromatography/isotope dilution high-resolution mass spectrometry. Anal Chem 78: 5744-5751.
48. Li Z, Sandau CD, Romanoff L.C., Caudill SP, Sjodin A, et al. (2008) Concentration and profile of 22 urinary polycyclic aromatic hydrocarbon metabolites in the US population. Environ Res 107: 320-331.
49. Miller RL, Garfinkel R, Lendor C., Hoepner L, Li Z, et al. (2010) Polycyclic aromatic hydrocarbon metabolite levels and pediatric allergy and asthma in an inner-city cohort. Pediatr Allergy Immunol 21: 260-267.
50. Jongeneelen FJ, van Leeuwen FE, Oosterink S, Anzion RB, van der Loop F, et al. (1990) Ambient and biological monitoring of cokeoven workers: determinants of the internal dose of polycyclic aromatic hydrocarbons. Br J Ind Med 47: 454-461.
51. Hauser R, Meeker JD, Park S, Silva M.J., Calafat AM (2004) Temporal variability of urinary phthalate metabolite levels in men of reproductive age. Environ Health Perspect 112: 1734-1740.
52. Perera F, Vishnevetsky J, Herbstman J.B., Calafat AM, Xiong W, et al. (2012) Prenatal bisphenol a exposure and child behavior in an inner-city cohort. Environ Health Perspect 120: 1190-1194.
53. Achenbach T, Rescorla L (2001) Manual for the ASEBA School-Age Forms & Profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth & Families.
54. Conners CK (1997) Conners' Rating Scales-Revised (CRS-R): User's Manual Toronto, ON: Multi-Health Systems Inc.
55. Conners CK, Parker JDA, Sitarenios G, Epstein JN (1998) The Revised Conners' Parent rating Scale (CPRS-R): Factor structure, reliability, and criterion validity. Journal of Abnormal Child Psychology 26: 2567-2268.
56. Rodriguez-Barranco M, Lacasana M, Aguilar-Garduno C, Alguacil J., Gil F, et al. (2013) Association of arsenic, cadmium and manganese exposure with neurodevelopment and behavioural disorders in children: a systematic review and meta-analysis. Sci Total Environ 454-455: 562-577.
57. Cornelius MD, De Genna NM, Leech SL, Willford JA, Goldschmidt L, et al. (2011) Effects of prenatal cigarette smoke exposure on neurobehavioral outcomes in 10-year-old children of adolescent mothers. Neurotoxicol Teratol 33: 137-144.
58. Bouchard M, Laforest F, Vandelac L., Bellinger D, Mergler D (2007) Hair manganese and hyperactive behaviors: pilot study of school-age children exposed through tap water. Environ Health Perspect 115: 122-127.
59. Wasserman GA, Staghezza-Jaramillo B, Shrout P., Popovac D, Graziano J (1998) The effect of lead exposure on behavior problems in preschool children. Am J Public Health 88: 481-486.
60. American Psychiatric Association, American Psychiatric Association, Task Force on DSM-IV (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR. Washington, DC: American Psychiatric Association. xxxvii, 943p. p.
61. de Graaf R, Kessler RC, Fayyad J, ten Have M, Alonso J, et al. (2008) The prevalence and effects of adult attention-deficit/hyperactivity disorder (ADHD) on the performance of workers: results from the WHO World Mental Health Survey Initiative. Occup Environ Med 65: 835-842.
62. Kupper T, Haavik J, Drexler H., Ramos-Quiroga JA, Wermelskirchen D, et al. (2012) The negative impact of attention-deficit/hyperactivity disorder on occupational health in adults and adolescents. Int Arch Occup Environ Health 85: 837-847.
63. Wu SY, Gau SS (2013) Correlates for academic performance and school functioning among youths with and without persistent attention-deficit/hyperactivity disorder. Res Dev Disabil 34: 505-515.
64. Jacobson LA, Ryan M, Denckla M.B., Mostofsky SH, Mahone EM (2013) Performance Lapses in Children with Attention-Deficit/Hyperactivity Disorder Contribute to Poor Reading Fluency. Arch Clin Neuropsychol.
65. Ek U, Westerlund J, Holmberg K., Fernell E (2011) Academic performance of adolescents with ADHD and other behavioural and learning problems- a population-based longitudinal study. Acta Paediatr 100: 402-406.
66. Strine TW, Lesesne CA, Okoro C.A., McGuire LC, Chapman DP, et al. (2006) Emotional and behavioral difficulties and impairments in everyday functioning among children with a history of attention-deficit/hyperactivity disorder. Prev Chronic Dis 3: A52.
67. CDC (2013) ADHD, Data and Statistics, National Center on Birth Defects and Developmental Disabilities.
68. Pelham WE, Foster EM, Robb JA (2007) The economic impact of attention-deficit/hyperactivity disorder in children and adolescents. J Pediatr Psychol 32: 711-727.
69. Perera FP, Tang D, Whyatt R., Lederman SA, Jedrychowski W (2005) DNA damage from polycyclic aromatic hydrocarbons measured by benzo[a]pyrene-DNA adducts in mothers and newborns from Northern Manhattan, the World Trade Center Area, Poland, and China. Cancer Epidemiol Biomarkers Prev 14: 709-714.
70. Castano-Vinyals G, D'Errico A, Malats N, Kogevinas M (2004) Biomarkers of exposure to polycyclic aromatic hydrocarbons from environmental air pollution. Occup Environ Med 61: e12.
71. Strickland P, Kang D, Sithisarankul P (1996) Polycyclic aromatic hydrocarbon metabolites in urine as biomarkers of exposure and effect. Environ Health Perspect 104 Suppl 5: 927-932.
72. Zhao ZH, Quan WY, Tian DH (1990) Urinary 1-Hydroxypyrene as an Indicator of Human Exposure to Ambient Polycyclic Aromatic-Hydrocarbons in a Coal-Burning Environment. Science of the Total Environment 92: 145-154.
73. Archibong AE, Inyang F, Ramesh A., Greenwood M, Nayyar T, et al. (2002) Alteration of pregnancy related hormones and fetal survival in F-344 rats exposed by inhalation to benzo(a)pyrene. Reprod Toxicol 16: 801-808.
74. Bui QQ, Tran MB, West WL (1986) A comparative study of the reproductive effects of methadone and benzo(a)pyrene in the pregnant and pseudopregnant rat. Toxicology 42: 195-204.
75. Takeda K, Tsukue N, Yoshida S (2004) Endocrine-disrupting activity of chemicals in diesel exhaust and diesel exhaust particles. Environ Sci 11: 33-45.
76. Dejmek J, Solansky I, Benes I., Lenicek J, Sram RJ (2000) The impact of polycyclic aromatic hydrocarbons and fine particles on pregnancy outcome. Environ Health Perspect 108: 1159-1164.
77. Manchester DK, Gordon SK, Golas C.L., Roberts EA, Okey AB (1987) Ah receptor in human placenta: stabilization by molybdate and characterization of binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin, 3-methylcholanthrene, and benzo(a)pyrene. Cancer Res 47: 4861-4868.
78. Meyn MS (1995) Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res 55: 5991-6001.
79. Nicol CJ, Harrison ML, Laposa R.R., Gimelshtein IL, Wells PG (1995) A teratologic suppressor role for p53 in benzo[a]pyrene-treated transgenic p53-deficient mice. Nat Genet 10: 181-187.
80. Wood KA, Youle RJ (1995) The role of free radicals and p53 in neuron apoptosis in vivo. J Neuroscience 15: 5851-5857.
81. Saunders CR, Das SK, Ramesh A, Shockley D.C., Mukherjee S (2006) Benzo(a)pyrene-induced acute neurotoxicity in the F-344 rat: role of oxidative stress. J Appl Toxicol 26: 427-438.
82. Wilson VL, Jones PA (1983) Inhibition of DNA methylation by chemical carcinogens in vitro. Cell 32: 239-246.
83. Stiles J, Jernigan TL (2010) The basics of brain development. Neuropsychol Rev 20: 327-348.
84. Garzon DL, Huang H, Todd RD (2008) Do Attention Deficit/Hyperactivity Disorder and Oppositional Defiant Disorder Influence Preschool Unintentional Injury Risk? Archives of Psychiatric Nursing 22: 288-296.
85. Wood JJ (2006) Effect of anxiety reduction on children's school performance and social adjustment. Dev Psychol 42: 345-349.
86. Knapp M, King D, Healey A., Thomass C (2011) Economic Outcomes in Adulthood and their Associations with Antisocial Conduct, Attention Deficit and Anxiety Problems in Childhood. Journal of Mental Health Policy and Economics 14: 137-147.
87. Kotsopoulos N, Connolly MP, Sobanski E, Postma MJ (2013) The fiscal consequences of ADHD in Germany: a quantitative analysis based on differences in educational attainment and lifetime earnings. J Ment Health Policy Econ 16: 27-33.