Prenatal polycyclic aromatic hydrocarbon (PAH) exposure and child behavior at age 6-7 years

Frederica P Perera, Deliang Tang, Shuang Wang, Julia Vishnevetsky, Bingzhi Zhang, Diurka Diaz, David Camann, Virginia Rauh, Frederica P Perera, Deliang Tang, Shuang Wang, Julia Vishnevetsky, Bingzhi Zhang, Diurka Diaz, David Camann, Virginia Rauh

Abstract

Background: Airborne polycyclic aromatic hydrocarbons (PAH) are widespread urban air pollutants from fossil fuel burning and other combustion sources. We previously reported that a broad spectrum of combustion-related DNA adducts in cord blood was associated with attention problems at 6-7 years of age in the Columbia Center for Children's Environmental Health (CCCEH) longitudinal cohort study.

Objectives: We evaluated the relationship between behavioral problems and two different measures of prenatal exposure--both specific to PAH--in the same cohort.

Methods: Children of nonsmoking African-American and Dominican women in New York City (NYC) were followed from in utero to 6-7 years. Prenatal PAH exposure was estimated by personal air monitoring of the mothers during pregnancy as well as by the measurement of DNA adducts specific to benzo[a]pyrene (BaP), a representative PAH, in maternal and cord blood. At 6-7 years of age, child behavior was assessed using the Child Behavior Checklist (CBCL) (n = 253). Generalized linear models were used to test the association between prenatal PAH exposure and behavioral outcomes.

Results: In multivariate analyses, high prenatal PAH exposure, whether characterized by personal air monitoring (greater than the median of 2.27 ng/m³) or maternal and cord adducts (detectable or higher), was positively associated with symptoms of Anxious/Depressed and Attention Problems (p ≤ 0.05).

Conclusion: These results provide additional evidence that environmental levels of PAH encountered in NYC air can adversely affect child behavior.

Conflict of interest statement

D. Camann is employed by Southwest Research Institute, a nonprofit, applied research and development organization. The authors declare they have no actual or potential competing financial interests.

References

    1. Abramowitz M, Stegun IA. Dover, NY: Dover Publications; 1968. Handbook of Mathematical Functions.
    1. Achenbach T, Rescorla L. Burlington, VT: University of Vermont, Research Center for Children, Youth & Families; 2001. Manual for the ASEBA School-Age Forms & Profiles.
    1. Alexandrov K, Rojas M, Geneste O, Castegnaro M, Camus AM, Pesruzzelli S, et al. 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. 1992;52(22):6248–6253.
    1. American Psychiatric Association. Washington, DC: American Psychiatric Association; 2000. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. 4th ed.
    1. Anderson LM, Diwan BA, Fear NT, Roman E. Critical windows of exposure for children’s health: cancer in human epidemiological studies and neoplasms in experimental animal models. Environ Health Perspect. 2000;108(suppl 3):573–594.
    1. Archibong AE, Inyang F, Ramesh A, Greenwood M, Nayyar T, Kopsombut P, et al. Alteration of pregnancy related hormones and fetal survival in F-344 rats exposed by inhalation to benzo(a)pyrene. Reprod Toxicol. 2002;16(6):801–808.
    1. Arlt VM, Bieler CA, Mier W, Wiessler M, Schmeiser HH. DNA adduct formation by the ubiquitous environmental contaminant 3-nitrobenzanthrone in rats determined by 32P-postlabeling. Int J Cancer. 2001;93(3):450–454.
    1. Axtell CD, Cox C, Myers GJ, Davidson PW, Choi AL, Cernichiari E, et al. Association between methylmercury exposure from fish consumption and child development at five and a half years of age in the Seychelles Child Development Study: an evaluation of nonlinear relationships. Environ Res. 2000;84(2):71–80.
    1. Bostrom CE, Gerde P, Hanberg A, Jernstrom B, Johansson C, Kyrklund T, et al. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ Health Perspect. 2002;110(suppl 3):451–488.
    1. Bradley RH. The Home Inventory: review and reflections. Adv Child Dev Behav. 1994;25:241–288.
    1. Brown L, Sherbenou RJ, Johnson SK. Austin, TX: PRO-ED, Inc; 1990. Test of Nonverbal Intelligence: A Language-Free Measure of Cognitive Ability. 2nd ed.
    1. Brown LA, Khousbouei H, Goodwin JS, Irvin-Wilson CV, Ramesh A, Sheng L, et al. 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. 2007;28(5):965–978.
    1. Bui QQ, Tran MB, West WL. A comparative study of the reproductive effects of methadone and benzo(a)pyrene in the pregnant and pseudopregnant rat. Toxicology. 1986;42(2–3):195–204.
    1. CDC (Centers for Disease Control and Prevention)/Division of Laboratory Science. Atlanta, GA: CDC; 2003. Whole Blood Lead, Cadmium and Mercury Determined Using Inductively Coupled Plasma Mass Spectrometry. DLS method code 2003-01/OD. CLIA methods.
    1. Choi H, Jedrychowski W, Spengler J, Camann DE, Whyatt RM, Rauh V, et al. International studies of prenatal exposure to polycyclic aromatic hydrocarbons and fetal growth. Environ Health Perspect. 2006;114:1744–1750.
    1. Choi H, Perera FP, Pac A, Wang L, Flak E, Mroz E, et al. Estimating individual-level exposure to airborne polycyclic aromatic hydrocarbons throughout the gestational period based on personal, indoor, and outdoor monitoring. Environ Health Perspect. 2008;116:1509–1518.
    1. Dejmek J, Solansky I, Benes I, Lenícek J, Šrám RJ. The impact of polycyclic aromatic hydrocarbons and fine particles on pregnancy outcome. Environ Health Perspect. 2000;108:1159–1164.
    1. Dohrenwend BS, Krasnoff L, Askenacy A, Dohrenwend B. Exemplification of a method for scaling life events: the PERI life events scale. J Health Soc Behavior. 1978;19:205–229.
    1. Edwards SC, Jedrychowski W, Butscher M, Camann D, Kieltyka A, Mroz E, et al. Prenatal exposure to airborne polycyclic aromatic hydrocarbons and children’s intelligence at 5 years of age in a prospective cohort study in Poland. Environ Health Perspect. 2010;118:1326–1331.
    1. Emslie GJ. Pediatric anxiety—underrecognized and undertreated. N Engl J Med. 2008;359(26):2835–2836.
    1. Fergusson DM, Horwood LJ, Lynskey MT. Maternal smoking before and after pregnancy: effects on behavioral outcomes in middle childhood. Pediatrics. 1993;92(6):815–822.
    1. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368(9553):2167–2178.
    1. Hood DB, Nayyar T, Ramesh A, Greenwood M, Inyang F. Modulation in the developmental expression profile of Sp1 subsequent to transplacental exposure of fetal rats to desorbed benzo[a]pyrene following maternal inhalation. Inhal Toxicol. 2000;12(6):511–535.
    1. Jedrychowski W, Galas A, Pac A, Flak E, Camman D, Rauh V, et al. Prenatal ambient air exposure to polycyclic aromatic hydrocarbons and the occurrence of respiratory symptoms over the first year of life. Eur J Epidemiol. 2005;20(9):775–782.
    1. Manchester DK, Gordon SK, Golas CL, Roberts EA, Okey AB. 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. 1987;47:4861–4868.
    1. McCallister MM, Maguire M, Ramesh A, Aimin Q, Liu S, Khoshbouei H, et al. Prenatal exposure to benzo(a)pyrene impairs later-life cortical neuronal function. Neurotoxicology. 2008;29(5):846–854.
    1. Meyn MS. Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res. 1995;55:5991–6001.
    1. Munnia A, Saletta F, Allione A, Piro S, Confortini M, Matullo G, et al. 32P-Post-labelling method improvements for aromatic compound-related molecular epidemiology studies. Mutagenesis. 2007;22(6):381–385.
    1. National Research Council. Washington, DC: National Academy Press; 1993. Toxicity Testing and Strategies to Determine Needs and Priorities.
    1. Nicol CJ, Harrison ML, Laposa RR, Gimelshtein IL, Wells PG. A teratologic suppressor role for p53 in benzo[a]pyrene-treated transgenic p53-deficient mice. Nat Genet. 1995;10(2):181–187.
    1. Nijland MJ, Ford SP, Nathanielsz PW. Prenatal origins of adult disease. Curr Opin Obstet Gynecol. 2008;20(2):132–138.
    1. Olden K, Poje J. Environmental justice and environmental health. Bull Soc Occup Environ Health. 1995;4:3–4.
    1. Perera F, Herbstman J. Prenatal environmental exposures, epigenetics, and disease. Reprod Toxicol. 2011;31(3):363–373.
    1. Perera FP, Illman SM, Kinney PL, Whyatt RM, Kelvin EA, Shepard P, et al. The challenge of preventing environmentally related disease in young children: community-based research in New York City. Environ Health Perspect. 2002;110:197–204.
    1. Perera FP, Li Z, Whyatt R, Hoepner L, Wang S, Camann D, et al. Prenatal polycyclic aromatic hydrocarbon exposure and child intelligence at age 5. Pediatrics. 2009a;124(2):e195–e202.
    1. Perera FP, Rauh V, Tsai WY, Kinney P, Camann D, Barr D, et al. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect. 2003;111:201–205.
    1. Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, Diaz D, et al. 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. 2006;114:1287–1292.
    1. Perera FP, Tang D, Tu YH, Cruz LA, Borjas M, Bernert T, et al. Biomarkers in maternal and newborn blood indicate heightened fetal susceptibility to procarcinogenic DNA damage. Environ Health Perspect. 2004;112:1133–1136.
    1. Perera FP, Tang D, Whyatt R, Lederman SA, Jedrychowski W. 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. 2005;14(3):709–714.
    1. Perera FP, Tang WY, Herbstman J, Tang D, Levin L, Miller R, et al. 2009bRelation of DNA methylation of 5’-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PLoS ONE 42e4488; doi:10.1371/journal.pone.0004488[Online 16 February 2009]
    1. Perera FP, Wang S, Vishnevetsky J, Zhang B, Cole KJ, Tang D, et al. PAH/aromatic DNA adducts in cord blood and behavior scores in New York City children. Environ Health Perspect. 2011;119:1176–1181.
    1. Petersen NSM, Kolen MJ, Hoover HD. New York:American Council on Education and Macmillan: 1989. Scaling, Norming, and Equating.
    1. Rauh VA, Garfinkel R, Perera FP, Andrews H, Barr DB, Whitehead R, et al. Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first three years of life among inner-city children. Pediatrics. 2006;118(6):e1845–e1859.
    1. Robinson M, Oddy WH, Li J, Kendall GE, de Klerk NH, Silburn SR, et al. Pre- and postnatal influences on preschool mental health: a large-scale cohort study. J Child Psychol Psychiatry. 2008;49(10):1118–1128.
    1. Rodier PM. Environmental causes of central nervous system maldevelopment. Pediatrics. 2004;113(4) suppl:1076–1083.
    1. Rundle A, Hoepner L, Hassoun A, Oberfield S, Freyer G, Holmes D, et al. 2012Association of childhood obesity with maternal exposure to ambient air polycyclic aromatic hydrocarbons during pregnancy. Am J Epidemiol; doi: [Online 13 April 2012]10.1093/aje/kwr455
    1. Saunders CR, Das SK, Ramesh A, Shockley DC, Mukherjee S. Benzo(a)pyrene-induced acute neurotoxicity in the F-344 rat: role of oxidative stress. J Appl Toxicol. 2006;26(5):427–438.
    1. Saunders CR, Ramesh A, Shockley DC. Modulation of neurotoxic behavior in F-344 rats by temporal disposition of benzo(a)pyrene. Toxicol Lett. 2002;129(1–2):33–45.
    1. Saunders CR, Shockley DC, Knuckles ME. Fluoranthene-induced neurobehavioral toxicity in F-344 rats. Int J Toxicol. 2003;22(4):263–276.
    1. Takeda K, Tsukue N, Yoshida S. Endocrine-disrupting activity of chemicals in diesel exhaust and diesel exhaust particles. Environ Sci. 2004;11(1):33–45.
    1. Wasserman GA, Liu X, Pine DS, Graziano JH. Contribution of maternal smoking during pregnancy and lead exposure to early child behavior problems. Neurotoxicol Teratol. 2001;23(1):13–21.
    1. Weitzman M, Gortmaker S, Sobol A. Maternal smoking and behavior problems of children. Pediatrics. 1992;90(3):342–349.
    1. Westfall PH, Young SS. New York:John Wiley & Sons, Inc. 1993. Resampling-Based Multiple Testing: Examples and Methods for p-Value Adjustment.
    1. Wilson VL, Jones PA. Inhibition of DNA methylation by chemical carcinogens in vitro. Cell. 1983;32(1):239–246.
    1. Wood JJ. Effect of anxiety reduction on children’s school performance and social adjustment. Dev Psychol. 2006;42(2):345–349.
    1. Wood KA, Youle RJ. The role of free radicals and p53 in neuron apoptosis in vivo. J Neuroscience. 1995;15:5851–5857.
    1. World Health Organization. In: Environmental Health Criteria 59. Geneva:World Health Organization, 55–128; 1986. Principles for evaluating health risks from chemicals during infancy and early childhood: The need for a special approach.
    1. Wormley DD, Ramesh A, Hood DB. Environmental contaminant-mixture effects on CNS development, plasticity, and behavior. Toxicol Appl Pharmacol. 2004;197(1):49–65.
    1. Wu J, Ramesh A, Nayyar T, Hood DB. Assessment of metabolites and AhR and CYP1A1 mRNA expression subsequent to prenatal exposure to inhaled benzo(a)pyrene. Int J Dev Neurosci. 2003;21(6):333–346.
    1. Yokota S, Mizuo K, Moriya N, Oshio S, Sugawara I, Takeda K. Effect of prenatal exposure to diesel exhaust on dopaminergic system in mice. Neurosci Lett. 2009;449(1):38–41.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel