In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study

Brenda Eskenazi, Jonathan Chevrier, Stephen A Rauch, Katherine Kogut, Kim G Harley, Caroline Johnson, Celina Trujillo, Andreas Sjödin, Asa Bradman, Brenda Eskenazi, Jonathan Chevrier, Stephen A Rauch, Katherine Kogut, Kim G Harley, Caroline Johnson, Celina Trujillo, Andreas Sjödin, Asa Bradman

Abstract

Background: California children's exposures to polybrominated diphenyl ether flame retardants (PBDEs) are among the highest worldwide. PBDEs are known endocrine disruptors and neurotoxicants in animals.

Objective: Here we investigate the relation of in utero and child PBDE exposure to neurobehavioral development among participants in CHAMACOS (Center for the Health Assessment of Mothers and Children of Salinas), a California birth cohort.

Methods: We measured PBDEs in maternal prenatal and child serum samples and examined the association of PBDE concentrations with children's attention, motor functioning, and cognition at 5 (n = 310) and 7 years of age (n = 323).

Results: Maternal prenatal PBDE concentrations were associated with impaired attention as measured by a continuous performance task at 5 years and maternal report at 5 and 7 years of age, with poorer fine motor coordination-particularly in the nondominant-at both age points, and with decrements in Verbal and Full-Scale IQ at 7 years. PBDE concentrations in children 7 years of age were significantly or marginally associated with concurrent teacher reports of attention problems and decrements in Processing Speed, Perceptual Reasoning, Verbal Comprehension, and Full-Scale IQ. These associations were not altered by adjustment for birth weight, gestational age, or maternal thyroid hormone levels.

Conclusions: Both prenatal and childhood PBDE exposures were associated with poorer attention, fine motor coordination, and cognition in the CHAMACOS cohort of school-age children. This study, the largest to date, contributes to growing evidence suggesting that PBDEs have adverse impacts on child neurobehavioral development.

Conflict of interest statement

The contents of this publication are solely the authors’ responsibility and do not necessarily represent the official views of the UC MEXUS, NIEHS, National Institutes of Health, the U.S. EPA, or the Centers for Disease Control and Prevention.

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

Figures

Figure 1
Figure 1
The point estimate and 95% CI for each quartile (Q) of maternal ∑PBDE concentration for outcomes that showed overall associations and evidence of nonlinearity (at p < 0.1). The quartile ranges for maternal PBDEs were ≤ 14.4, 14.5–24.78, 24.8–41.97, and ≥ 42 ng/g lipid. Tests for trend come from models using PBDE quartile (1–4) as a continuous variable.

References

    1. Achenbach T, Rescorla L. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families; 2000. Manual for the ASEBA Preschool Forms & Profiles.
    1. Adams W, Sheslow D. Wilmington, DE: Wide Range, Inc; 1995. Wide Range Assessment of Visual Motor Abilities (WRAVMA)
    1. American Psychiatric Association. Washington, DC: American Psychiatric Association; 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th ed.
    1. Barr JR, Maggio VL, Barr DB, Turner WE, Sjödin A, Sandau CD, et al. New high-resolution mass spectrometric approach for the measurement of polychlorinated biphenyls and organochlorine pesticides in human serum. J Chromatogr B Analyt Technol Biomed Life Sci. 2003;794(1):137–148.
    1. Birnbaum LS, Staskal DF. Brominated flame retardants: cause for concern? Environ Health Perspect. 2004;112:9–17.
    1. Bouchard MF, Chevrier J, Harley KG, Kogut K, Vedar M, Calderon N, et al. Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ Health Perspect. 2011;119:1189–1195.
    1. Bradman A, Castorina R, Sjödin A, Fenster L, Jones RS, Harley KG, et al. Factors associated with serum polybrominated diphenyl ether (PBDE) levels among school-age children in the CHAMACOS cohort. Environ Sci Technol. 2012;46(13):7373–7381.
    1. Bradman A, Eskenazi B, Barr D, Bravo R, Castorina R, Chevrier J, et al. Organophosphate urinary metabolite levels during pregnancy and after delivery in women living in an agricultural community. Environ Health Perspect. 2005;113:1802–1807.
    1. Bravo R, Driskell WJ, Whitehead RD, Jr, Needham LL, Barr DB. Quantitation of dialkyl phosphate metabolites of organophosphate pesticides in human urine using GC-MS-MS with isotopic internal standards. J Anal Toxicol. 2002;26(5):245–252.
    1. Caldwell B, Bradley R 1984. Home Observation for Measurement of The Environment. Little Rock, AR:University of Arkansas.
    1. California Department of Consumer Affairs. Technical Bulletin 117: Requirements, Test Procedure and Apparatus for Testing the Flame Retardance of Resilient Filling Materials Used in Upholstered Furniture. 2000. Available: [accessed 23 June 2010]
    1. Castorina R, Bradman A, Sjödin A, Fenster L, Jones RS, Harley KG, et al. Determinants of serum polybrominated diphenyl ether (PBDE) levels among pregnant women in the CHAMACOS cohort. Environ Sci Technol. 2011;45(15):6553–6560.
    1. Chao HR, Wang SL, Lee WJ, Wang YF, Papke O. Levels of polybrominated diphenyl ethers (PBDEs) in breast milk from central Taiwan and their relation to infant birth outcome and maternal menstruation effects. Environ Int. 2007;33(2):239–245.
    1. Chevrier J, Harley KG, Bradman A, Gharbi M, Sjödin A, Eskenazi B. Polybrominated diphenyl ether (PBDE) flame retardants and thyroid hormone during pregnancy. Environ Health Perspect. 2010;118:1444–1449.
    1. Conners CK 2001. Conner’s Rating Scales–Revised (CSR-R) Technical Manual (includes auxilliary scales: CADS-P and CADS-T). North Tonawanda, NY:Multi-Health Systems Inc.
    1. Conners CK, Staff M 2001. Conners’ Kiddie Continuous Performance Test (K-CPT): Computer Program for Windows Technical Guide and Software Manual. Toronto, ON, Canada:Multi-Health Systems Inc.
    1. Darnerud PO, Aune M, Larsson L, Hallgren S. Plasma PBDE and thyroxine levels in rats exposed to Bromkal or BDE-47. Chemosphere. 2007;67(9):S386–S392.
    1. Dunn L, Dunn L 1981. Peabody Picture Vocabulary Test, Revised. Circle Pines, MN:American Guidance Service.
    1. Eskenazi B, Fenster L, Castorina R, Marks AR, Sjödin A, Rosas LG, et al. A comparison of PBDE serum concentrations in Mexican and Mexican-American children living in California. Environ Health Perspect. 2011;119:1442–1448.
    1. Eskenazi B, Harley K, Bradman A, Weltzien E, Jewell NP, Barr DB, et al. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect. 2004;112:1116–1124.
    1. Eskenazi B, Marks AR, Bradman A, Fenster L, Johnson C, Barr DB, et al. In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Pediatrics. 2006;118(1):233–241.
    1. Eskenazi B, Marks AR, Bradman A, Harley K, Barr DB, Johnson C, et al. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ Health Perspect. 2007;115:792–798.
    1. Gascon M, Fort M, Martinez D, Carsin AE, Forns J, Grimalt JO, et al. Polybrominated diphenyl ethers (PBDEs) in breast milk and neuropsychological development in infants. Environ Health Perspect. 2012;120:1760–1765.
    1. Gascon M, Vrijheid M, Martinez D, Forns J, Grimalt JO, Torrent M, et al. Effects of pre and postnatal exposure to low levels of polybromodiphenyl ethers on neurodevelopment and thyroid hormone levels at 4 years of age. Environ Int. 2011;37(3):605–611.
    1. Geyer HJ, Schramm K-W, Darnerud PO, Aune M, Feicht A, Fried KW. Terminal elimination half-lives of the brominated flame retardants TBBPA, HBCD, and lower brominated PBDEs in humans. Organohalogen Compounds. 2004;66:3867–3872.
    1. Grandjean P, Weihe P, Burse VW, Needham LL, Storr-Hansen E, Heinzow B, et al. Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol Teratol. 2001;23(4):305–317.
    1. Harley KG, Chevrier J, Schall RA, Sjödin A, Bradman A, Eskenazi B. Association of prenatal exposure to polybrominated diphenyl ethers and infant birth weight. Am J Epidemiol. 2011;174(8):885–892.
    1. Herbstman JB, Sjödin A, Apelberg BJ, Witter FR, Halden RU, Patterson DG, et al. Birth delivery mode modifies the associations between prenatal polychlorinated biphenyl (PCB) and polybrominated diphenyl ether (PBDE) and neonatal thyroid hormone levels. Environ Health Perspect. 2008;116:1376–1382.
    1. Herbstman JB, Sjödin A, Kurzon M, Lederman SA, Jones RS, Rauh V, et al. Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect. 2010;118:712–719.
    1. Hoffman K, Adgent M, Goldman BD, Sjödin A, Daniels JL. Lactational exposure to polybrominated diphenyl ethers and its relation to social and emotional development among toddlers. Environ Health Perspect. 2012;120:1438–1442.
    1. Jacobson JL, Jacobson SW. Prenatal exposure to polychlorinated biphenyls and attention at school age. J Pediatr. 2003;143(6):780–788.
    1. Koopman-Esseboom C, Weisglas-Kuperus N, de Ridder MA, Van der Paauw CG, Tuinstra LG, Sauer PJ. Effects of polychlorinated biphenyl/dioxin exposure and feeding type on infants’ mental and psychomotor development. Pediatrics. 1996;97(5):700–706.
    1. Lubin JH, Colt JS, Camann D, Davis S, Cerhan JR, Severson RK, et al. Epidemiologic evaluation of measurement data in the presence of detection limits. Environ Health Perspect. 2004;112:1691–1696.
    1. Marks AR, Harley K, Bradman A, Kogut K, Barr DB, Johnson C, et al. Organophosphate pesticide exposure and attention in young Mexican-American children: the CHAMACOS study. Environ Health Perspect. 2010;118:1768–1774.
    1. McCarthy D. 1972. McCarthy Scales of Children’s Abilities. New York:Psychological Corporation.
    1. Nelson JC, Tomei RT. Direct determination of free thyroxin in undiluted serum by equilibrium dialysis/radioimmunoassay. Clin Chem. 1988;34(9):1737–1744.
    1. Noyes PD, Hinton DE, Stapleton HM. Accumulation and debromination of decabromodiphenyl ether (BDE-209) in juvenile fathead minnows (Pimephales promelas) induces thyroid disruption and liver alterations. Toxicol Sci. 2011;122(2):265–274.
    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(4):495–500.
    1. Radloff L. The CES-D Scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1(3):385–401.
    1. Reynolds CR, Kamphaus RW. 2004. BASC-2: Behaviour Assessment System for Children, Second Edition Manual. Circle Pines, MN:AGS Publishing.
    1. Richardson VM, Staskal DF, Ross DG, Diliberto JJ, DeVito MJ, Birnbaum LS. Possible mechanisms of thyroid hormone disruption in mice by BDE 47, a major polybrominated diphenyl ether congener. Toxicol Appl Pharmacol. 2008;226(3):244–250.
    1. Rogan W, Gladen B. PCBs, DDE, and child development at 18 and 24 months. Ann Epidemiol. 1991;1(5):407–413.
    1. Rohlman DS, Gimenes LS, Eckerman DA, Kang SK, Farahat FM, Anger WK. Development of the Behavioral Assessment and Research System (BARS) to detect and characterize neurotoxicity in humans. Neurotoxicology. 2003;24(4–5):523–531.
    1. Rose M, Bennett DH, Bergman A, Fangstrom B, Pessah IN, Hertz-Picciotto I. PBDEs in 2–5 year-old children from California and associations with diet and indoor environment. Environ Sci Technol. 2010;44(7):2648–2653.
    1. Roze E, Meijer L, Bakker A, Van Braeckel KN, Sauer PJ, Bos AF. Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect. 2009;117:1953–1958.
    1. Sagiv SK, Thurston SW, Bellinger DC, Altshul LM, Korrick SA. Neuropsychological measures of attention and impulse control among 8-year-old children exposed prenatally to organochlorines. Environ Health Perspect. 2012;120:904–909.
    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(7):1921–1927.
    1. Sjödin A, Papke O, McGahee E, Focant JF, Jones RS, Pless-Mulloli T, et al. Concentration of polybrominated diphenyl ethers (PBDEs) in household dust from various countries. Chemosphere. 2008;73(1) suppl:S131–S136.
    1. Stapleton HM, Kelly SM, Allen JG, McClean MD, Webster TF. Measurement of polybrominated diphenyl ethers on hand wipes: estimating exposure from hand-to-mouth contact. Environ Sci Technol. 2008;42(9):3329–3334.
    1. Viberg H, Fredriksson A, Eriksson P. Neonatal exposure to the brominated flame retardant 2,2’,4,4’,5-pentabromodiphenyl ether causes altered susceptibility in the cholinergic transmitter system in the adult mouse. Toxicol Sci. 2002a;67(1):104–107.
    1. Viberg H, Fredriksson A, Eriksson P. Reston, VA: Society of Toxicology, 132; 2002b. Neonatal exposure to a brominated flame retardant, 2,2’,4,4’,5,5’-hexabromodiphenyl ether (PBDE 153) affects behaviour and cholinergic nicotinic receptors in brain of adult mice [Abstract 643]. In: The Toxicologist: Proceedings of the 41st Annual Meeting of the Society of Toxicology, 17–21 March 2002, Nashville, TN.
    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(2):95–106.
    1. Wechsler D. 2003. Wechsler Intelligence Scale for Children–Fourth Edition (WISC-IV) Administration and Scoring Manual. San Antonio, TX:Harcourt Assessment Incorporated.
    1. Zhou T, Taylor MM, DeVito MJ, Crofton KM. Developmental exposure to brominated diphenyl ethers results in thyroid hormone disruption. Toxicol Sci. 2002;66(1):105–116.
    1. Zota AR, Rudel RA, Morello-Frosch RA, Brody JG. Elevated house dust and serum concentrations of PBDEs in California: unintended consequences of furniture flammability standards? Environ Sci Technol. 2008;42(21):8158–8164.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel