Gestational exposure to endocrine disrupting chemicals in relation to infant birth weight: a Bayesian analysis of the HOME Study

Meghan M Woods, Bruce P Lanphear, Joseph M Braun, Lawrence C McCandless, Meghan M Woods, Bruce P Lanphear, Joseph M Braun, Lawrence C McCandless

Abstract

Background: Pregnant women are exposed to a mixture of endocrine disrupting chemicals (EDCs). Gestational EDC exposures may be associated with changes in fetal growth that elevates the risk for poor health later in life, but few studies have examined the health effects of simultaneous exposure to multiple chemicals. This study aimed to examine the association of gestational exposure to five chemical classes of potential EDCs: phthalates and bisphenol A, perfluoroalkyl substances (PFAS), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and organochlorine pesticides (OCPs) with infant birth weight.

Methods: Using data from the Health Outcomes and Measures of Environment (HOME) Study, we examined 272 pregnant women enrolled between 2003-2006. EDC concentrations were quantified in blood and urine samples collected at 16 and 26 weeks gestation. We used Bayesian Hierarchical Linear Models (BHLM) to examine the associations between newborn birth weight and 53 EDCs, 2 organochlorine pesticides (OPPs) and 2 heavy metals.

Results: For a 10-fold increase in chemical concentration, the mean differences in birth weights (95% credible intervals (CI)) were 1 g (-20, 23) for phthalates, -11 g (-52, 34) for PFAS, 0.2 g (-9, 10) for PCBs, -4 g (-30, 22) for PBDEs, and 7 g (-25, 40) for OCPs.

Conclusion: Gestational exposure to phthalates, PFAS, PCBs, PBDEs, OCPs or OPPs had null or small associations with birth weight. Gestational OPP, Pb, and PFAS exposures were most strongly associated with lower birth weight.

Keywords: Birth weight; Endocrine disruptors; Environmental exposure; Maternal exposure; Pregnancy.

Conflict of interest statement

Ethics approval and consent to participate

The Institutional Review Boards (IRBs) of Cincinnati Children’s Hospital Medical Center (CCHMC) and participating delivery hospitals approved the HOME Study. After research assistants explained study protocols, all women provided written informed consent for themselves and their children.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Posterior 95% CIs of BHLM regression coefficients, HOME Study, 2003-2006, n=272, Cincinnati, OH
Fig. 2
Fig. 2
Posterior 50% CIs of BHLM regression coefficients, HOME Study, 2003-2006, n=272, Cincinnati, OH

References

    1. Serrano SE, Karr CJ, Seixas NS, Nguyen RHN, Barrett ES, Janssen S, Redmon B, Swan SH, Sathyanarayana S. Dietary phthalate exposure in pregnant women and the impact of consumer practices. Int J Environ Res Public Health. 2014;11(6):6193–6215. doi: 10.3390/ijerph110606193.
    1. Lundqvist C, Zuurbier M, Leijs M, Johansson C, Ceccatelli S, Saunders M, Schoeters G, Tusscher GT, Koppe JG. The effects of PCBs and dioxins on child health. Acta Paediatr Suppl. 2006;95(Supplement 453):55–64. doi: 10.1080/08035320600886257.
    1. Ryu MH, Jha A, Ojo OO, Mahood TH, Basu S, Detillieux KA, Nikoobakht N, Wong CS, Loewen M, Becker AB, Halayko AJ. Chronic exposure to perfluorinated compounds: impact on airway hyper-responsiveness and inflammation. Am J Physiol Lung Cell Mol Physiol. 2014;307:L765–L774. doi: 10.1152/ajplung.00100.2014.
    1. Braun JM, Sathyanarayana S, Hauser R. Phthalate exposure and children's health. Curr Opin Pediatr. 2013;25:247–254. doi: 10.1097/MOP.0b013e32835e1eb6.
    1. de Cock M, de Boer MR, Lamoree J, Legler J, van de Bor M. First year growth in relation to prenatal exposure to endocrine disruptors - a Dutch prospective cohort study. Int J Environ Res Public Health. 2014;11:7001-7021.
    1. Woodruff TJ, Zota AR, Schwartz JM. Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ Health Perspect. 2011;119:878–885. doi: 10.1289/ehp.1002727.
    1. Arbuckle TE, Davis K, Marro L, Fisher M, Legrand M, LeBlanc A, Gaudrea E, Foster WG, Choeurng V, Fraser WD, the MIREC Study Group Phthalate and bisphenol A exposure among pregnant women in Canada - results from the MIREC study. Environ Int. 2014;68:55–65. doi: 10.1016/j.envint.2014.02.010.
    1. Lien Y-J, Ku H-Y, Su P-H, Chen S-J, Chen H-Y, Liao P-C, Chen W-J, Wang S-L. Prenatal exposure to phthalate esters and behavioral syndromes in children at 8 years of age: Taiwan maternal and infant cohort study. Environ Health Perspect. 2015;123:95–100. doi: 10.1289/ehp.123-A95.
    1. Sathyanarayana S, Braun JM, Yolton K, Liddy S, Lanphear BP. Case report: high prenatal bisphenol A exposure and infant neonatal neurobehavior. Environ Health Perspect. 2011;119:1170–1175. doi: 10.1289/ehp.1003064.
    1. Braun JM, Kalkbrenner AE, Just AC, Yolton K, Calafat AM, Sjodin A, Hauser R, Webster GM, Chen A, Lanphear BP. 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. 2014;112:513–520.
    1. Agency for Toxic Substances and Disease Registry (ATSDR). Public Health Statement perfluoroalkyls. 2015. . Accessed 12 Oct 2016.
    1. Agency for Toxic Substances and Disease Registry (ATSDR). Public Health Statement Polychlorinated biphenyls (PCBs). 2000. . Accessed 12 October 2016.
    1. Harley KG, Chevrier J, Schall RA, Sjodin A, Bradman A, Eskenazi B. Association of prenatal exposure to polybrominated diphenyl ethers and infant birth weight. Am J Epidemiol. 2011;174:885–892. doi: 10.1093/aje/kwr212.
    1. Rauch SA, Braun JM, Boyd Barr D, Calafat AM, Khoury J, Montesano MA, Yolton K, Lanphear BP. Associations of prenatal exposure to organophosphate pesticide metabolites with gestational age and birth weight. Environ Health Perspect. 2012;120:1055–1060. doi: 10.1289/ehp.1104615.
    1. Birks L, Casas M, Garcia AM, Alexander J, Barros H, Bergstrom A, Bonde JP, Burdorf A, Costet N, Danileviciute A, Eggesbo M, Fernandez MF, Gonzalez-Galarzo MC, Grazuleviciene R, Hanke W, Jaddoe V, Kogevinas M, Kull I, Lertxundi A, Melaki V, Nybo Anderson A-M, Olea N, Polanska K, Rusconi F, Santa-Marina L, Santos AC, Vrijkotte T, Zugna D, Nieuwenhuijsen M, Corder S, Vrijheid M. Occupational exposure to endocrine-disrupting chemicals and birth weight and length of gestation: A European meta-analysis. Environ Health Perspect. 2016;124:1785–1793. doi: 10.1289/EHP208.
    1. Eriksson JG, Forsen T, Tuomilehto J, Osmond C, Barker DJP. Early growth and coronary heart disease later in life: longitudinal study. BMJ. 2001;332:949–953. doi: 10.1136/bmj.322.7292.949.
    1. Class QA, Rickert ME, Lichtenstein P, D'Onofrio Birth weight, physical morbidity and mortality: a population-based sibling-comparison study. Am J Epidemiol. 2014;179:550–558. doi: 10.1093/aje/kwt304.
    1. Lenters V, Portengen L, Rignell-Hydbom A, Jonsson BAG, Lindh CH, Piersma AH, Toft F, Bonde JP, Heederik D, Rylander L, Vermeulen R. Prenatal phthalate, perfluoroalkyl acid, and organochlorine exposures and term birth weight in three birth cohorts: multi-pollutant models based on elastic net regression. Environ Health Perspect. 2016;124:365–372.
    1. Johnson PI, Sutton P, Atchley DS, Koustas E, Lam J, Sen S, Robinson DA, Axelrad DA, Woodruff TJ. The navigation guide - evidence based medicine meets environmental health: systematic review of human evidence for PFOA effects on fetal growth. Environ Health Perspect. 2014;122:1028–1039.
    1. Maisonet M, Terrell ML, McGeehin MA, Christensen KY, Holmes A, Calafat AM, Marcus M. Maternal concentrations of polyfluoroakyl compounds during pregnancy and fetal and postnatal growth in British girls. Environ Health Perspect. 2012;120(10):1432–1437. doi: 10.1289/ehp.1003096.
    1. Govarts E, Nieuwenhuijsen M, Schoeters G, Ballester F, Bloemen K, de Boer M, Chevrier C, Eggesbe M, Guxens M, Kramer U, Legler J, Martinez D, Palkovicova L, Patelarou E, Ranft U, Rautio A, Petersen MS, Slama R, Stigum H, Toft G, Trnovec T, Vandentorren S, Weihe P, Kuperus NW, Wilhelm M, Wittsiepe J, Bonde JP, OBELIX/ENRIECO Birth weight and prenatal exposure to polychlorinated biphenyls (PCBs) and dichlorodiphenyldichloroethylene (DDE): A meta-analysis within 12 European birth cohorts. Environ Health Perspect. 2012;120:162–170. doi: 10.1289/ehp.1103767.
    1. Philippat C, Mortamais M, Chevrier C, Petit C, Calafat AM, Ye X, Silva MJ, Brambilla C, Pin I, Charles M-A, Cordier S, Slama R. Exposure to phthalates and phenols during pregnancy and offspring size at birth. Environ Health Perspect. 2012;120:464–470. doi: 10.1289/ehp.1103634.
    1. Wolff MS, Engel SM, Berkowitz GS, Ye X, Silva MJ, Zhu C, Wetmur J, Calafat AM. Prenatal phenol and phthalate exposures and birth outcomes. Environ Health Perspect. 2008;116:1092–1097. doi: 10.1289/ehp.11007.
    1. Zhang Y, Lin L, Cao Y, Chen B, Zheng L, Ge R-S. Phthalate levels and low birth weight: A nested case-control study of Chinese newborns. J Pediatr. 2009;155:500–504. doi: 10.1016/j.jpeds.2009.04.007.
    1. Fenster L, Eskenazi B, Anderson M, Bradman A, Harley K, Hernandez H, Hubbard A, Barr DB. Association of in utero organochlorine pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect. 2005;114:597–602. doi: 10.1289/ehp.8423.
    1. Serme-Gbedo YK, Abdelouahab N, Pasquier J-C, Cohen AA, Takser L. Maternal levels of endocrine disruptors, polybrominated diphenyl ethers, in early pregnancy are not associated with lower birth weight in the Canadian birth cohort GESTE. Environ Health. 2016;15:49–59. doi: 10.1186/s12940-016-0134-z.
    1. Lignell S, Aune M, Darnerud PO, Hanberg A, Larsson SC, Glynn A. Prenatal exposure to polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) may influence birth weight among infants in a Swedish cohort with background exposure: a cross-sectional study. Environ Health. 2013;12:44–53. doi: 10.1186/1476-069X-12-44.
    1. MacLehose RF, Dunson DB, Herring AH, Hoppin AJ. Bayesian Methods for highly correlated exposure data. Epidemiol. 2007;18(2):199–207. doi: 10.1097/01.ede.0000256320.30737.c0.
    1. Sun Z, Tao Y, Li S, Ferguson KK, Meeker JD, Park SK, Batterman SA, Mukgerjee B. Statistical strategies for constructing health risk models with multiple pollutants and their interactions: possible choices and comparisons. Environ Health. 2013;12:85–104. doi: 10.1186/1476-069X-12-85.
    1. Agier L, Portengen L, Chadeau-Hyam M, Basagana X, Giorgis-Allemand L, Siroux V, Robinson O, Vlaanderen J, Gonzalez JR, Nieuwenhuijsen MJ, Vineis P, Vrijheid M, Slama R, Vermeulen RA. systematic comparison of linear regression-based statistical methods to assess exposome-health associations. Environ Health Perspect. 2016;124:1848–1856. doi: 10.1289/EHP172.
    1. Gennings C, Carrico C, Factor-Litvak P, Krigbaum N, Cirilllo PM, Cohn BAA. cohort study evaluation of maternal PCB exposure related to time to pregnancy in daughters. Environ Health. 2013;12:66–77. doi: 10.1186/1476-069X-12-66.
    1. Billonet C, Sherrill D, Annesi-Maesano I. Estimating the health effects of exposure to a multi-pollutant mixture. Ann Epidemiol. 2012;22:126–141. doi: 10.1016/j.annepidem.2011.11.004.
    1. Gelman A, Hill J, Yajima M. Why we (usually) don’t have to worry about multiple comparisons. J Res Educ Effect. 2012;5(2):189–211. doi: 10.1080/19345747.2011.618213.
    1. Braun JM, Kalloo G, Chen A, Dietrich KN, Liddy-Hicks S, Morgan S, Xu Y, Yolton K, Lanphear BP. Cohort profile: The Health Outcomes and Measures of the Environment (HOME) study. Int J Epidemiol. Advance Access published March 22, 2016; doi:10.1093/ije/dyw006
    1. Whitcomb BW, Schisterman EF. Assays with lower detection limits: implications for epidemiological investigations. Pediatr Perinat Epidemiol. 2008;22:597–602. doi: 10.1111/j.1365-3016.2008.00969.x.
    1. Cole SR, Chu H, Nie L, Schisterman EF. Estimating the odds ration when exposure has a limit of detection. Int J Epidemiol. 2009;38:1674–1680. doi: 10.1093/ije/dyp269.
    1. Braun JM, Smith KW, Williams PL, Calafat AM, Berry K, Ehrlich S, Hauser R. Variability of urinary phthalate metabolite and bisphenol a concentrations before and during pregnancy. Environ Health Perspect. 2012;120:739–745. doi: 10.1289/ehp.1104139.
    1. Gollenberg AL, Hediger ML, Lee PA, Himes JH, Buck Louis GM. Association between lead and cadmium and reproductive hormones in peripubertal U.S. girls. Environ Health Perspect. 2010;118:1782–1787.
    1. Xie X, Ding G, Cui C, Chen L, Gao Y, Zhou Y, Shi R, Tian Y. The effects of low-level prenatal lead exposure on birth outcomes. Environ Pollut. 2013;175:30–34. doi: 10.1016/j.envpol.2012.12.013.
    1. Core Team R. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2015.
    1. Stan Development Team. Stan: A C++ library for probability and sampling, version 2.6.0. 2014. .
    1. Friedman J, Hastie T, Tibshirani R. Regularization paths for generalized linear models via coordinate descent. J Stat Softw. 2010;33(1):1–22. doi: 10.18637/jss.v033.i01.
    1. Wei T, Simko V. corrplot: visualization of a correlation matrix. R package version 0.77. 2016.
    1. Monteagudo C, Mariscal-Arcas M. Heras-Gonzalez, Ibanez-Peinado D, Rivas A, Olea-Serrano F. Effects of maternal diet and environmental exposure to organochlorine pesticides on newborn weight in Southern Spain. Chemosphere. 2016;156:135–142. doi: 10.1016/j.chemosphere.2016.04.103.
    1. Taylor CM, Golding J, Emond AM. Adverse effects of maternal lead levels on birth outcomes in the ALSPAC study: a prospective birth cohort study. BJOG. 2015;122:322–328. doi: 10.1111/1471-0528.12756.
    1. Zhu M, Fitzgerald ER, Gelberg KH, Lin Shao, Druschel CM. Maternal low-level lead exposure and fetal growth. Environ Health Perspect. 2010;118:1471–5.
    1. Li L, Laurent O, Spatial WJ. variability of the effect of air pollution on term birth weight: evaluating influential factors using Bayesian hierarchical models. Environ Health. 2016;15:14–27. doi: 10.1186/s12940-016-0112-5.
    1. Chen Y-H, Ferguson KK, Meeker JD, McElrath TF, Mukherjee B. Statistical methods for modeling repeated measures of maternal environmental exposure biomarkers during pregnancy in association with preterm birth. Environ Health. 2015;14:9–21. doi: 10.1186/1476-069X-14-9.
    1. Kark M, Tynelius P, Rasumssen F. Associations between birth weight and weight change during infancy and later childhood with systolic blood pressure at age 15 years: the COMPASS study. Paediatr Perinat Epidemiol. 2009;23:245–253. doi: 10.1111/j.1365-3016.2008.01007.x.
    1. Zhang J, Kim S, Grewal J, Albert PS. Predicting large fetuses at birth: do multiple ultrasound examinations and longitudinal statistical modeling improve prediction? Paediatr Perinat Epidemiol. 2012;26:199–207. doi: 10.1111/j.1365-3016.2012.01261.x.
    1. Efron B, Morris C. Data analysis using Stein's estimator and its generalizations. J Am Statistic Assoc. 1975;70:311–319. doi: 10.1080/01621459.1975.10479864.

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