Prenatal PBDE and PCB Exposures and Reading, Cognition, and Externalizing Behavior in Children

Hongmei Zhang, Kimberly Yolton, Glenys M Webster, Andreas Sjödin, Antonia M Calafat, Kim N Dietrich, Yingying Xu, Changchun Xie, Joseph M Braun, Bruce P Lanphear, Aimin Chen, Hongmei Zhang, Kimberly Yolton, Glenys M Webster, Andreas Sjödin, Antonia M Calafat, Kim N Dietrich, Yingying Xu, Changchun Xie, Joseph M Braun, Bruce P Lanphear, Aimin Chen

Abstract

Background: Prenatal polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) exposures may influence children's neurodevelopment.

Objective: We examined the association of prenatal PBDE and PCB exposures with children's reading skills at ages 5 and 8 years, Full-Scale Intelligence Quotient (FSIQ), and externalizing behavior problems at age 8 years.

Methods: From 239 mother-child pairs recruited (2003-2006) in Cincinnati, Ohio, we measured maternal serum PBDE and PCB concentrations, assessed child's reading skills using the Woodcock-Johnson Tests of Achievement III (WJ-III) at age 5 years and the Wide Range Achievement Test-4 (WRAT-4) at age 8 years, tested FSIQ using the Wechsler Intelligence Scale for Children-IV (WISC-IV), and externalizing behavior problems using the Behavioral Assessment System for Children-2 (BASC-2) at age 8 years. We used multiple linear regression to examine the association of prenatal PBDE and PCB concentrations and reading, FSIQ, and externalizing behavior problems after adjusting for covariates.

Results: An increase of Sum4PBDEs (BDE-47, BDE-99, BDE-100, and BDE-153) by 10 times was not significantly associated with reading scores at age 5 years at the p = 0.05 level but was inversely associated with Reading Composite scores (β: -6.2, 95% CI: -11.7, -0.6) and FSIQ (β: -5.3, 95% CI: -10.6, -0.02) at age 8 years; it was positively associated with the score for externalizing behavior problems (β: 3.5, 95% CI: -0.1, 7.2) at age 8 years. Prenatal Sum4PCBs (PCB-118, -153, -138-158, and -180) was not significantly associated with a child's reading skills, FSIQ, and externalizing behavior problems.

Conclusion: Prenatal PBDE concentration was inversely associated with reading skills and FSIQ and positively associated with externalizing behavior problems at age 8 years. No significant associations were found in prenatal PCB concentration.

Conflict of interest statement

J.M.B. was financially compensated for conducting a re-analysis of a study of child lead exposure for the plaintiffs in a public nuisance case related to childhood lead poisoning. B.P.L. has served as an expert witness and a consultant to the California Attorney General’s Office for the plaintiffs in a public nuisance case related to childhood lead poisoning, but he has not personally received any compensation for these services. B.P.L. has also served as a paid consultant on a U.S. EPA research study related to childhood lead poisoning. None of these activities are directly related to the present study.

The other authors declare they have no actual or potential competing financial interests.

Figures

Figure 1
Figure 1
Concentrations of PBDE and PCB congeners in the pregnant women in the HOME Study and NHANES (2003–2004) (median and interquartile range). Bars represent the interquartile range (IQR) of chemical concentrations in the HOME Study. Medians of chemical concentrations in the NHANES (National Health and Nutrition Examination Survey) pregnant women (2003–2004) were referenced, which did not provide the IQR or the 25th and 75th percentiles (Woodruff et al. 2011). BDE-47, -99, -100, and -153 are the congeners of polybrominated diphenyl ethers (PBDEs); PCB-118, -153, -138-158, and -180 are the congeners of polychlorinated biphenyls (PCBs). Limit of detection (LOD) for NHANES pregnant women (2003–2004) is 4.2, 5.0, 1.4, and 2.2 ng/g lipid for BDE-47, -99, -100, and -153; 0.6 and 1.1 ng/g lipid for PCB-118, and -153, respectively; 0.4 ng/g lipid for PCB-180 and PCD-138-158.
Figure 2
Figure 2
Trend and association of child’s reading scores, FSIQ, and Externalizing Problems scores with prenatal Sum4PBDEs and Sum4PCBs concentrations quartiles. (a) The trend and association of child’s reading scores, FSIQ, and externalizing behavior problems scores with prenatal Sum4PBDEs; (b) The trend and association of child’s reading scores, FSIQ, and externalizing behavior problems scores with prenatal Sum4PCBs. The quartile cutoffs were < 20.70, 20.70–35.64, 35.65–76.00, and ≥ 76.00 ng/g lipid for Sum4PBDEs, and < 21.50, 21.50–31.29, 31.30–42.80, and ≥ 42.80 ng/g for Sum4PCBs, respectively. The score in the 1st quartile is the reference. Note: Adjusted for maternal age, education, race, IQ, household income, parity, married status, smoking (maternal serum cotinine), fish consumption, depression, and child sex, and HOME score. FSIQ, Full-Scale Intelligence Quotient; *< 0.05, #< 0.10.

References

    1. Alm H, Kultima K, Scholz B, Nilsson A, Andrén PE, Fex-Svenningsen A, et al. Exposure to brominated flame retardant PBDE-99 affects cytoskeletal protein expression in the neonatal mouse cerebral cortex. Neurotoxicology. 2008;29:628–637.
    1. Beck AT, Steer RA, Ball R, Ranieri W. Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J Pers Assess. 1996;67:588–597.
    1. Blanco J, Mulero M, López M, Domingo JL, Sánchez DJ. BDE-99 deregulates BDNF, Bcl-2 and the mRNA expression of thyroid receptor isoforms in rat cerebellar granular neurons. Toxicology. 2011;290:305–311.
    1. Bloom MS, Buck Louis GM, Schisterman EF, Liu A, Kostyniak PJ. 2007. Maternal serum polychlorinated biphenyl concentrations across critical windows of human development. Environ Health Perspect 115 1320 1324, doi:10.1289/ehp.10086
    1. Boucher O, Muckle G, Bastien CH. 2009. Prenatal exposure to polychlorinated biphenyls: a neuropsychologic analysis. Environ Health Perspect 117 7 16, doi:10.1289/ehp.11294
    1. Braun JM, Kalkbrenner AE, Just AC, Yolton K, Calafat AM, Sjödin A, et al. 2014. Gestational exposure to endocrine-disrupting chemicals and reciprocal social, repetitive, and stereotypic behaviors in 4- and 5-year-old children: the HOME study. Environ Health Perspect 122 513 520, doi:10.1289/ehp.1307261
    1. Caldwell BM, Bradley RH. Little Rock, AR: University of Arkansas at Little Rock; 1984. Home Observation for Measurement of the Environment.
    1. Chen A, Yolton K, Rauch SA, Webster GM, Hornung R, Sjödin A, et al. 2014. Prenatal polybrominated diphenyl ether exposures and neurodevelopment in U.S. Children through 5 years of age: the HOME study. Environ Health Perspect 122 856 862, doi:10.1289/ehp.1307562
    1. Chen ZJ, Liu HY, Cheng Z, Man YB, Zhang KS, Wei W, et al. Polybrominated diphenyl ethers (PBDEs) in human samples of mother-newborn pairs in South China and their placental transfer characteristics. Environ Int. 2014;73:77–84.
    1. Cho K, Frijters JC, Zhang H, Miller LL, Gruen JR. Prenatal exposure to nicotine and impaired reading performance. J Pediatr. 2013;162:713–718.e2.
    1. Dzwilewski KL, Schantz SL. Prenatal chemical exposures and child language development. J Commun Disord. 2015;57:41–65.
    1. Eskenazi B, Chevrier J, Rauch SA, Kogut K, Harley KG, Johnson C, et al. 2013. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ Health Perspect 121 257 262, doi:10.1289/ehp.1205597
    1. Fan CY, Besas J, Kodavanti PR. Changes in mitogen-activated protein kinase in cerebellar granule neurons by polybrominated diphenyl ethers and polychlorinated biphenyls. Toxicol Appl Pharmacol. 2010;245:1–8.
    1. Faupel-Badger JM, Hsieh CC, Troisi R, Lagiou P, Potischman N. Plasma volume expansion in pregnancy: implications for biomarkers in population studies. Cancer Epidemiol Biomarkers Prev. 2007;16:1720–1723.
    1. Gassmann K, Schreiber T, Dingemans MM, Krause G, Roderigo C, Giersiefer S, et al. BDE-47 and 6-OH-BDE-47 modulate calcium homeostasis in primary fetal human neural progenitor cells via ryanodine receptor-independent mechanisms. Arch Toxicol. 2014;88:1537–1548.
    1. Geraghty SR, Khoury JC, Morrow AL, Lanphear BP. Reporting individual test results of environmental chemicals in breastmilk: potential for premature weaning. Breastfeed Med. 2008;3:207–213.
    1. He P, He W, Wang A, Xia T, Xu B, Zhang M, et al. PBDE-47-induced oxidative stress, DNA damage and apoptosis in primary cultured rat hippocampal neurons. Neurotoxicology. 2008;29:124–129.
    1. He P, Wang AG, Xia T, Gao P, Niu Q, Guo LJ, et al. Mechanisms underlying the developmental neurotoxic effect of PBDE-47 and the enhanced toxicity associated with its combination with PCB153 in rats. Neurotoxicology. 2009;30:1088–1095.
    1. Herbstman JB, Sjödin A, Kurzon M, Lederman SA, Jones RS, Rauh V, et al. 2010. Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect 118 712 719, doi:10.1289/ehp.0901340
    1. Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.
    1. Houston SM, Lebel C, Katzir T, Manis FR, Kan E, Rodriguez GG, et al. Reading skill and structural brain development. Neuroreport. 2014;25:347–352.
    1. Ibhazehiebo K, Iwasaki T, Kimura-Kuroda J, Miyazaki W, Shimokawa N, Koibuchi N. 2011. Disruption of thyroid hormone receptor-mediated transcription and thyroid hormone-induced Purkinje cell dendrite arborization by polybrominated diphenyl ethers. Environ Health Perspect 119 168 175, doi:10.1289/ehp.1002065
    1. Johansson N, Viberg H, Fredriksson A, Eriksson P. Neonatal exposure to deca-brominated diphenyl ether (PBDE 209) causes dose-response changes in spontaneous behaviour and cholinergic susceptibility in adult mice. Neurotoxicology. 2008;29:911–919.
    1. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. Spatio-temporal transcriptome of the human brain. Nature. 2011;478:483–489.
    1. Lesmana R, Shimokawa N, Takatsuru Y, Iwasaki T, Koibuchi N. Lactational exposure to hydroxylated polychlorinated biphenyl (OH-PCB 106) causes hyperactivity in male rat pups by aberrant increase in dopamine and its receptor. Environ Toxicol. 2014;29:876–883.
    1. Mather N, Wendling BJ, Woodcock RW. Itasca, IL: Riverside Publishing; 2001. Essentials of WJ III Tests of Achievement Assessment.
    1. O’Muircheartaigh J, Dean DC, III, Ginestet CE, Walker L, Waskiewicz N, Lehman K, et al. White matter development and early cognition in babies and toddlers. Hum Brain Mapp. 2014;35:4475–4487.
    1. Phillips DL, Pirkle JL, Burse VW, Bernert JT, Jr, Henderson LO, Needham LL. Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding. Arch Environ Contam Toxicol. 1989;18:495–500.
    1. Reynolds CR, Kamphaus RW. Circle Pines, MN: American Guidance Service; 2004. BASC-2: Behavior Assessment System for Children. 2nd ed.
    1. Roze E, Meijer L, Bakker A, Van Braeckel KN, Sauer PJ, Bos AF. 2009. Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect 117 1953 1958, doi:10.1289/ehp.0901015
    1. Sayegh P, Arentoft A, Thaler NS, Dean AC, Thames AD. Quality of education predicts performance on the Wide Range Achievement Test-4th Edition Word Reading subtest. Arch Clin Neuropsychol. 2014;29:731–736.
    1. Schreiber T, Gassmann K, Götz C, Hübenthal U, Moors M, Krause G, et al. 2010. Polybrominated diphenyl ethers induce developmental neurotoxicity in a human in vitro model: evidence for endocrine disruption. Environ Health Perspect 118 572 578, doi:10.1289/ehp.0901435
    1. Sjödin A, Jones RS, Lapeza CR, Focant JF, McGahee EE, III, Patterson DG., Jr Semiautomated high-throughput extraction and cleanup method for the measurement of polybrominated diphenyl ethers, polybrominated biphenyls, and polychlorinated biphenyls in human serum. Anal Chem. 2004;76:1921–1927.
    1. Spann MN, Bansal R, Rosen TS, Peterson BS. Morphological features of the neonatal brain support development of subsequent cognitive, language, and motor abilities. Hum Brain Mapp. 2014;35:4459–4474.
    1. Stewart PW, Lonky E, Reihman J, Pagano J, Gump BB, Darvill T. 2008. The relationship between prenatal PCB exposure and intelligence (IQ) in 9-year-old children. Environ Health Perspect 116 1416 1422, doi:10.1289/ehp.11058
    1. Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev. 2010;20:327–348.
    1. Tagliaferri S, Caglieri A, Goldoni M, Pinelli S, Alinovi R, Poli D, et al. Low concentrations of the brominated flame retardants BDE-47 and BDE-99 induce synergistic oxidative stress-mediated neurotoxicity in human neuroblastoma cells. Toxicol in Vitro. 2010;24:116–122.
    1. Thompson MR, Boekelheide K. Multiple environmental chemical exposures to lead, mercury and polychlorinated biphenyls among childbearing-aged women (NHANES 1999–2004): body burden and risk factors. Environ Res. 2013;121:23–30.
    1. Tibshirani R. Regression shrinkage selection via the LASSO. J R Stat Soc Series B Stat Methodol. 1996;58:267–288.
    1. Totsika V, Sylva K. The home observation for measurement of the environment revisited. Child Adolesc Ment Health. 2004;9:25–35.
    1. Viberg H. Exposure to polybrominated diphenyl ethers 203 and 206 during the neonatal brain growth spurt affects proteins important for normal neurodevelopment in mice. Toxicol Sci. 2009;109:306–311.
    1. Viberg H, Fredriksson A, Eriksson P. Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol Appl Pharmacol. 2003;192:95–106.
    1. Viberg H, Fredriksson A, Eriksson P. Deranged spontaneous behaviour and decrease in cholinergic muscarinic receptors in hippocampus in the adult rat, after neonatal exposure to the brominated flame-retardant, 2,2’,4,4’,5-pentabromodiphenyl ether (PBDE 99). Environ Toxicol Pharmacol. 2005;20:283–288.
    1. Viberg H, Fredriksson A, Eriksson P. Changes in spontaneous behaviour and altered response to nicotine in the adult rat, after neonatal exposure to the brominated flame retardant, decabrominated diphenyl ether (PBDE 209). Neurotoxicology. 2007;28:136–142.
    1. Wechsler D. San Antonio, TX: Psychological Corporation; 2003. Wechsler Intelligence Scale for Children. 4th ed.
    1. Woodruff TJ, Zota AR, Schwartz JM. 2011. Environmental chemicals in pregnant women in the United States: NHANES 2003–2004. Environ Health Perspect 119 878 885, doi:10.1289/ehp.1002727
    1. Xing T, Chen L, Tao Y, Wang M, Chen J, Ruan DY. Effects of decabrominated diphenyl ether (PBDE 209) exposure at different developmental periods on synaptic plasticity in the dentate gyrus of adult rats in vivo. Toxicol Sci. 2009;110:401–410.
    1. Xing TR, Yong W, Chen L, Tang ML, Wang M, Chen JT, et al. Effects of decabrominated diphenyl ether (PBDE 209) on voltage-gated sodium channels in primary cultured rat hippocampal neurons. Environ Toxicol. 2010;25:400–408.
    1. Xue J, Liu SV, Zartarian VG, Geller AM, Schultz BD. Analysis of NHANES measured blood PCBs in the general US population and application of SHEDS model to identify key exposure factors. J Expo Sci Environ Epidemiol. 2014;24:615–621.
    1. Yang D, Lein PJ. Polychlorinated biphenyls increase apoptosis in the developing rat brain. Curr Neurobiol. 2010;1:70–76.
    1. Zhang H, Li X, Nie J, Niu Q. Lactation exposure to BDE-153 damages learning and memory, disrupts spontaneous behavior and induces hippocampus neuron death in adult rats. Brain Res. 2013;1517:44–56.
    1. Zhao Y, Ruan X, Li Y, Yan M, Qin Z. Polybrominated diphenyl ethers (PBDEs) in aborted human fetuses and placental transfer during the first trimester of pregnancy. Environ Sci Technol. 2013;47:5939–5946.

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