Prenatal Polybrominated Diphenyl Ether Exposure and Body Mass Index in Children Up To 8 Years of Age

Ann M Vuong, Joseph M Braun, Andreas Sjödin, Glenys M Webster, Kimberly Yolton, Bruce P Lanphear, Aimin Chen, Ann M Vuong, Joseph M Braun, Andreas Sjödin, Glenys M Webster, Kimberly Yolton, Bruce P Lanphear, Aimin Chen

Abstract

Background: Prenatal exposure to endocrine disruptors has been associated with increased risk of childhood obesity. However, epidemiologic studies on polybrominated diphenyl ethers (PBDEs) are limited despite animal studies indicating PBDEs' potential role as an obesogen.

Objectives: We investigated whether maternal concentrations of BDEs 28, 47, 99, 100, 153, and ΣPBDEs during pregnancy were associated with anthropometric measures in children aged 1-8 years.

Methods: We examined 318 mother-child pairs in the Health Outcomes and Measures of the Environment (HOME) Study, a birth cohort enrolled from 2003 through 2006 (Cincinnati, OH). Serum PBDEs were measured at 16 ± 3 weeks gestation. We measured child height (1-8 years), weight (1-8 years), body mass index (BMI) (2-8 years), waist circumference (4-8 years), and body fat (8 years). To account for repeated measures, we used linear mixed models and generalized estimating equations to estimate associations between maternal PBDEs and child anthropometric measures.

Results: We found no statistically significant associations between prenatal PBDEs and height or weight z-score. A 10-fold increase in maternal serum BDE-153 was associated with lower BMI z-score (β = -0.36; 95% CI: -0.60, -0.13) at 2-8 years, smaller waist circumference (β = -1.81 cm; 95% CI: -3.13, -0.50) at 4-8 years, and lower percent body fat (β = -2.37%; 95% CI: -4.21, -0.53) at 8 years. A decrease in waist circumference at 4-8 years was observed with a 10-fold increase in BDE-100 (β = -1.50 cm; 95% CI: -2.93, -0.08) and ΣPBDEs (β = -1.57 cm; 95% CI: -3.11, -0.02).

Conclusions: Reverse causality may have resulted in prenatal PBDEs, particularly BDE-153, and decreased BMI, waist circumference, and body fat. Citation: Vuong AM, Braun JM, Sjödin A, Webster GM, Yolton K, Lanphear BP, Chen A. 2016. Prenatal polybrominated diphenyl ether exposure and body mass index in children up to 8 years of age. Environ Health Perspect 124:1891-1897; http://dx.doi.org/10.1289/EHP139.

Conflict of interest statement

The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the NIEHS or the Centers for Disease Control and Prevention (CDC). B.P.L. served as an expert witness in California for the plaintiffs in a public nuisance case of childhood lead poisoning, a Proposition 65 case on behalf of the California Attorney General’s Office, a case involving lead-contaminated water in a new housing development in Maryland, and a Canadian tribunal on trade dispute about using lead-free galvanized wire in stucco lathing, but he received no personal compensation for these services. He is currently representing the government of Peru as an expert witness in a suit involving Doe Run vs. Peru, but he is receiving no personal compensation. The other authors declare they have no actual or potential competing financial interests.

Figures

Figure 1
Figure 1
Estimated differences and 95% CIs from multiple linear mixed models for associations between polybrominated diphenyl ether (ng/g lipid) tertiles and BMI z-score, waist circumference, or body fat percentage in children. All models were adjusted for maternal age, race, education, income, maternal smoking status, maternal depression, prepregnancy BMI, and maternal fruit and vegetable intake during pregnancy. Waist circumference and body fat percentage models were additionally adjusted for child sex and age (months). Children included in the models were 2–8 years for BMI z-score, 4–8 years for waist circumference, and 8 years for body fat percentage. PBDE tertile ranges in ng/g lipid: BDE-28 (0.2–0.7, 0.8–1.3, 1.4–31.4), BDE-47 (1.5–13.1, 13.2–27.9, 28.0–1,290), BDE-99 (0.6–2.9, 3.0–6.0, 6.1–465), BDE-100 (0.4–2.4, 2.5–5.6, 5.7–172), BDE-153 (0.5–3.0, 3.1–6.8, 6.9–152), and ∑PBDEs (4.5–24.9, 25.0–52.9, 53.0–2,047).

References

    1. Abdelouahab N, Langlois MF, Lavoie L, Corbin F, Pasquier JC, Takser L. Maternal and cord-blood thyroid hormone levels and exposure to polybrominated diphenyl ethers and polychlorinated biphenyls during early pregnancy. Am J Epidemiol. 2013;178:701–713.
    1. Ahmed RG. Early weaning PCB 95 exposure alters the neonatal endocrine system: thyroid adipokine dysfunction. J Endocrinol. 2013;219:205–215.
    1. Auwerx J. PPARgamma, the ultimate thrifty gene. Diabetologia. 1999;42:1033–1049.
    1. Bastos Sales L, Kamstra JH, Cenijn PH, van Rijt LS, Hamers T, Legler J. Effects of endocrine disrupting chemicals on in vitro global DNA methylation and adipocyte differentiation. Toxicol In Vitro. 2013;27:1634–1643.
    1. Beck AT, Steer RA, Brown GK. 1996. BDI-II, Beck Depression Inventory: Manual. 2nd ed. San Antonio, TX:Psychological Corporation.
    1. Bondy GS, Lefebvre DE, Aziz S, Cherry W, Coady L, Maclellan E, et al. Toxicologic and immunologic effects of perinatal exposure to the brominated diphenyl ether (BDE) mixture DE-71 in the Sprague-Dawley rat. Environ Toxicol. 2013;28:215–228.
    1. Braun JM, Lanphear BP, Calafat AM, Deria S, Khoury J, Howe CJ, et al. 2014. Early-life bisphenol A exposure and child body mass index: a prospective cohort study. Environ Health Perspect 122 1239 1245, doi:10.1289/ehp.1408258
    1. Chevrier J. Invited commentary: maternal plasma polybrominated diphenyl ethers and thyroid hormones—challenges and opportunities. Am J Epidemiol. 2013;178:714–719.
    1. Chevrier J, Dewailly É, Ayotte P, Mauriège P, Després JP, Tremblay A. Body weight loss increases plasma and adipose tissue concentrations of potentially toxic pollutants in obese individuals. Int J Obes Relat Metab Disord. 2000;24:1272–1278.
    1. Daniels SR. Complications of obesity in children and adolescents. Int J Obes (Lond) 2009;33(suppl 1):S60–S65.
    1. Daubié S, Bisson JF, Lalonde R, Schroeder H, Rychen G. Neurobehavioral and physiological effects of low doses of polybrominated diphenyl ether (PBDE)-99 in male adult rats. Toxicol Lett. 2011;204:57–63.
    1. Dufault C, Poles G, Driscoll LL. Brief postnatal PBDE exposure alters learning and the cholinergic modulation of attention in rats. Toxicol Sci. 2005;88:172–180.
    1. Erkin-Cakmak A, Harley KG, Chevrier J, Bradman A, Kogut K, Huen K, et al. 2015. In Utero and childhood polybrominated diphenyl ether exposures and body mass at age 7 years: the CHAMACOS study. Environ Health Perspect 123 636 642, doi:10.1289/ehp.1408417
    1. Fernie KJ, Laird Shutt J, Ritchie IJ, Letcher RJ, Drouillard K, Bird DM. Changes in the growth, but not the survival, of American kestrels (Falco sparverius) exposed to environmentally relevant polybrominated diphenyl ethers. J Toxicol Environ Health A. 2006;69:1541–1554.
    1. Gee JR, Moser VC. Acute postnatal exposure to brominated diphenylether 47 delays neuromotor ontogeny and alters motor activity in mice. Neurotoxicol Teratol. 2008;30:79–87.
    1. Glynn AW, Granath F, Aune M, Atuma S, Darnerud PO, Bjerselius R, et al. 2003. Organochlorines in Swedish women: determinants of serum concentrations. Environ Health Perspect 111 349 355, doi:10.1289/ehp.5456
    1. Greenland S. Avoiding power loss associated with categorization and ordinal scores in dose-response and trend analysis. Epidemiology. 1995;6:450–454.
    1. Hoppe AA, Carey GB. Polybrominated diphenyl ethers as endocrine disruptors of adipocyte metabolism. Obesity (Silver Spring) 2007;15:2942–2950.
    1. Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.
    1. Imbeault P, Chevrier J, Dewailly E, Ayotte P, Després JP, Tremblay A, et al. Increase in plasma pollutant levels in response to weight loss in humans is related to in vitro subcutaneous adipocyte basal lipolysis. Int J Obes Relat Metab Disord. 2001;25:1585–1591.
    1. Jones R, Edenfield E, Anderson S, Zhang Y, Sjodin A. Semi-automated extraction and cleanup method for measuring persistent organic pollutants in human serum. Organohalogen Compounds. 2012;74:97–98.
    1. Kamstra JH, Hruba E, Blumberg B, Janesick A, Mandrup S, Hamers T, et al. Transcriptional and epigenetic mechanisms underlying enhanced in vitro adipocyte differentiation by the brominated flame retardant BDE-47. Environ Sci Technol. 2014;48:4110–4119.
    1. Kim TH, Lee YJ, Lee E, Kim MS, Kwack SJ, Kim KB, et al. Effects of gestational exposure to decabromodiphenyl ether on reproductive parameters, thyroid hormone levels, and neuronal development in Sprague-Dawley rats offspring. J Toxicol Environ Health A. 2009;72:1296–1303.
    1. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, et al. CDC growth charts: United States. Adv Data. 2000;314:1–27.
    1. Kuriyama SN, Wanner A, Fidalgo-Neto AA, Talsness CE, Koerner W, Chahoud I. Developmental exposure to low-dose PBDE-99: tissue distribution and thyroid hormone levels. Toxicology. 2007;242:80–90.
    1. Leijs MM. Amsterdam: University of Amsterdam; 2010. Toxic Effects of Dioxins, PCBs and PBDEs in Adolescents [PhD Dissertation].
    1. Lim JS, Lee DH, Jacobs DR., Jr Association of brominated flame retardants with diabetes and metabolic syndrome in the U.S. population, 2003–2004. Diabetes Care. 2008;31:1802–1807.
    1. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the global burden of disease study 2013. Lancet. 2014;384:766–781.
    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. Pucci E, Chiovato L, Pinchera A. Thyroid and lipid metabolism. Int J Obes Relat Metab Disord. 2000;24(suppl 2):S109–S112.
    1. Ross MG, Desai M, Khorram O, McKnight RA, Lane RH, Torday J. Gestational programming of offspring obesity: a potential contributor to Alzheimer’s disease. Curr Alzheimer Res. 2007;4:213–217.
    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. Skinner AC, Skelton JA. Prevalence and trends in obesity and severe obesity among children in the United States, 1999–2012. JAMA Pediatr. 2014;168:561–566.
    1. Stapleton HM, Eagle S, Anthopolos R, Wolkin A, Miranda ML. 2011. Associations between polybrominated diphenyl ether (PBDE) flame retardants, phenolic metabolites, and thyroid hormones during pregnancy. Environ Health Perspect 119 1454 1459, doi:10.1289/ehp.1003235
    1. Staskal DF, Hakk H, Bauer D, Diliberto JJ, Birnbaum LS. Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicol Sci. 2006;94:28–37.
    1. Suvorov A, Battista MC, Takser L. Perinatal exposure to low-dose 2,2’,4,4’-tetrabromodiphenyl ether affects growth in rat offspring: what is the role of IGF-1? Toxicology. 2009;260:126–131.
    1. Suvorov A, Takser L. 2010. Global gene expression analysis in the livers of rat offspring perinatally exposed to low doses of 2,2’,4,4’-tetrabromodiphenyl ether. Environ Health Perspect 118 97 102, doi:10.1289/ehp.0901031
    1. Ta TA, Koenig CM, Golub MS, Pessah IN, Qi L, Aronov PA, et al. Bioaccumulation and behavioral effects of 2,2’,4,4’-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice. Neurotoxicol Teratol. 2011;33:393–404.
    1. Talsness CE, Kuriyama SN, Sterner-Kock A, Schnitker P, Grande SW, Shakibaei M, et al. 2008. In utero and lactational exposures to low doses of polybrominated diphenyl ether-47 alter the reproductive system and thyroid gland of female rat offspring. Environ Health Perspect 116 308 314, doi:10.1289/ehp.10536
    1. Tung EW, Boudreau A, Wade MG, Atlas E. 2014. Induction of adipocyte differentiation by polybrominated diphenyl ethers (PBDEs) in 3T3-L1 cells. PLoS One 9 e94583, doi:10.1371/journal.pone.0094583
    1. Turyk ME, Anderson HA, Steenport D, Buelow C, Imm P, Knobeloch L. Longitudinal biomonitoring for polybrominated diphenyl ethers (PBDEs) in residents of the Great Lakes basin. Chemosphere. 2010;81:517–522.
    1. Valvi D, Casas M, Mendez MA, Ballesteros-Gómez A, Luque N, Rubio S, et al. Prenatal bisphenol A urine concentrations and early rapid growth and overweight risk in the offspring. Epidemiology. 2013;24:791–799.
    1. Verhulst SL, Nelen V, Hond ED, Koppen G, Beunckens C, Vael C, et al. 2009. Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life. Environ Health Perspect 117 122 126, doi:10.1289/ehp.0800003
    1. Vuong AM, Webster GM, Romano ME, Braun JM, Zoeller RT, Hoofnagle AN, et al. 2015. Maternal polybrominated diphenyl ether (PBDE) exposure and thyroid hormones in maternal and cord sera: the HOME Study, Cincinnati, USA. Environ Health Perspect 123 1079 1085, doi:10.1289/ehp.1408996
    1. Walford RL, Mock D, MacCallum T, Laseter JL. Physiologic changes in humans subjected to severe, selective calorie restriction for two years in Biosphere 2: health, aging, and toxicological perspectives. Toxicol Sci. 1999;52(2) suppl:61–65.
    1. Warner M, Wesselink A, Harley KG, Bradman A, Kogut K, Eskenazi B. Prenatal exposure to dichlorodiphenyltrichloroethane and obesity at 9 years of age in the CHAMACOS study cohort. Am J Epidemiol. 2014;179:1312–1322.
    1. Webster BH Jr, Bishaw A. Washington, DC: U.S. Census Bureau; 2007. Income, Earnings, and Poverty Data from the 2006 American Community Survey. ACS-08. Available: [accessed 2 June 2015]
    1. Windham GC, Pinney SM, Sjodin A, Lum R, Jones RS, Needham LL, et al. Body burdens of brominated flame retardants and other persistent organo-halogenated compounds and their descriptors in US girls. Environ Res. 2010;110:251–257.
    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. Zhou T, Taylor MM, DeVito MJ, Crofton KM. Developmental exposure to brominated diphenyl ethers results in thyroid hormone disruption. Toxicol Sci. 2002;66:105–116.

Source: PubMed

3
Abonnieren