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First trimester maternal exposures to endocrine disrupting chemicals and metals and fetal size in the Michigan Mother–Infant Pairs study

Published online by Cambridge University Press:  30 January 2019

Jaclyn M. Goodrich Open the ORCID record for Jaclyn M. Goodrich [Opens in a new window] ,
Mary E. Ingle ,
Steven E. Domino ,
Marjorie C. Treadwell ,
Dana C. Dolinoy ,
Charles Burant ,
John D. Meeker  and
Vasantha Padmanabhan
Jaclyn M. Goodrich*
Affiliation:
Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA
Mary E. Ingle
Affiliation:
Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA
Steven E. Domino
Affiliation:
Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, MI, USA
Marjorie C. Treadwell
Affiliation:
Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, MI, USA
Dana C. Dolinoy
Affiliation:
Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA
Charles Burant
Affiliation:
Department of Internal Medicine, University of Michigan, Ann Arbor, MI, USA
John D. Meeker
Affiliation:
Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA
Vasantha Padmanabhan*
Affiliation:
Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, MI, USA Department of Pediatrics, University of Michigan, Ann Arbor, MI, USA
*
Address for correspondence: J. M. Goodrich, University of Michigan School of Public Health, Environmental Health Sciences, 1415 Washington Heights, Ann Arbor, MI 48109, USA. E-mail: gaydojac@umich.edu V. Padamanabhan, University of Michigan, Pediatrics, 1137 Catherine St., Ann Arbor, MI, 48109, USA. Email: vasantha@umich.edu
Address for correspondence: J. M. Goodrich, University of Michigan School of Public Health, Environmental Health Sciences, 1415 Washington Heights, Ann Arbor, MI 48109, USA. E-mail: gaydojac@umich.edu V. Padamanabhan, University of Michigan, Pediatrics, 1137 Catherine St., Ann Arbor, MI, 48109, USA. Email: vasantha@umich.edu
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Abstract

Exposures to endocrine disrupting chemicals and metals are near ubiquitous worldwide, and their potential impact on children is a major public health concern. This pilot study was designed to characterize exposures to phthalates, phenols and metals among pregnant women in the first trimester, and to examine associations with fetal biometrics and birth weight. A total of 41 chemicals and elements were analyzed in urine from 56 mothers with full-term newborns from the Michigan Mother–Infant Pairs study. Bivariate analyses identified predictors of exposure biomarkers. Associations between birth weight, Fenton z-scores and second trimester fetal biometrics with toxicants were examined via multivariable linear regression. An average of 30 toxicants were detected in maternal urine. Fast food consumption was associated with several phthalate metabolites, phenols and metals, and canned food consumption with bisphenol F (P <0.05). Mono (3-carboxypropyl) phthalate was significantly associated with higher birth weight and Fenton z-score while the opposite was observed for bisphenol S. Estimated femur length from ultrasonography was significantly inversely associated with arsenic, barium and lead. While limited by sample size, this study is one of the first to evaluate birth outcomes with respect to emerging endocrine disrupting chemicals and to examine associations between toxicants and fetal biometrics. Exposure assessment was provided by the National Institute of Environmental Health Sciences’ Children’s Health Exposure Analysis Resource (NIEHS CHEAR), a resource available to children’s studies with the goal of combining data across cohorts in an effort to characterize the impact of toxicants on child health from birth and beyond.

Keywords

birth outcomesmetalsphenolsphthalatesprenatal exposures
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 10 , Issue 4 , August 2019 , pp. 447 - 458
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

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Footnotes

a

These authors contributed equally to this work.

b

These authors also contributed equally to this work.

References

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.CrossRefGoogle ScholarPubMed
2. Rosofsky, A, Janulewicz, P, Thayer, KA, et al. Exposure to multiple chemicals in a cohort of reproductive-aged Danish women. Environ Res. 2017; 154, 73–85.CrossRefGoogle Scholar
3. Lee, WC, Fisher, M, Davis, K, Arbuckle, TE, Sinha, SK. Identification of chemical mixtures to which Canadian pregnant women are exposed: The MIREC Study. Environ Int. 2017; 99, 321–330.CrossRefGoogle ScholarPubMed
4. Katsikantami, I, Sifakis, S, Tzatzarakis, MN, et al. A global assessment of phthalates burden and related links to health effects. Environ Int. 2016; 97, 212–236.CrossRefGoogle ScholarPubMed
5. Arbuckle, TE, Liang, CL, Morisset, AS, et al. Maternal and fetal exposure to cadmium, lead, manganese and mercury: The MIREC study. Chemosphere. 2016; 163, 270–282.CrossRefGoogle ScholarPubMed
6. Ettinger, AS, Arbuckle, TE, Fisher, M, et al. Arsenic levels among pregnant women and newborns in Canada: results from the Maternal-Infant Research on Environmental Chemicals (MIREC) cohort. Environ Res. 2017; 153, 8–16.CrossRefGoogle ScholarPubMed
7. Arbuckle, TE, Marro, L, Davis, K, et al. Exposure to free and conjugated forms of bisphenol A and triclosan among pregnant women in the MIREC cohort. Environ Health Perspect. 2015; 123, 277–284.CrossRefGoogle ScholarPubMed
8. Chen, A, Dietrich, KN, Huo, X, Ho, S-m. Developmental neurotoxicants in e-waste: an emerging health concern. Environ Health Perspect. 2011; 119, 431–438.CrossRefGoogle ScholarPubMed
9. Montes-Grajales, D, Fennix-Agudelo, M, Miranda-Castro, W. Occurrence of personal care products as emerging chemicals of concern in water resources: a review. Sci Total Environ. 2017; 595, 601–614.CrossRefGoogle ScholarPubMed
10. Ferguson, KK, Peterson, KE, Lee, JM, et al. Prenatal and peripubertal phthalates and bisphenol A in relation to sex hormones and puberty in boys. Reprod Toxicol. 2014; 47, 70–76.CrossRefGoogle ScholarPubMed
11. Rajesh, P, Balasubramanian, K. Phthalate exposure in utero causes epigenetic changes and impairs insulin signalling. J Endocrinol. 2014; 223, 47–66.CrossRefGoogle ScholarPubMed
12. Tellez-Rojo, MM, Cantoral, A, Cantonwine, DE, et al. Prenatal urinary phthalate metabolites levels and neurodevelopment in children at two and three years of age. Sci Total Environ. 2013; 461-462, 386–390.CrossRefGoogle ScholarPubMed
13. Yang, TC, Peterson, KE, Meeker, JD, et al. Bisphenol A and phthalates in utero and in childhood: association with child BMI z-score and adiposity. Environ Res. 2017; 156, 326–333.CrossRefGoogle ScholarPubMed
14. Onishchenko, N, Tamm, C, Vahter, M, et al. Developmental exposure to methylmercury alters learning and induces depression-like behavior in male mice. Toxicol Sci. 2007; 97, 428–37, Epub 2007 Jan 4.CrossRefGoogle ScholarPubMed
15. Faulk, C, Barks, A, Sanchez, BN, et al. Perinatal lead (Pb) exposure results in sex-specific effects on food intake, fat, weight, and insulin response across the murine life-course. PLoS One. 2014; 9, e104273.CrossRefGoogle ScholarPubMed
16. Weinhouse, C, Anderson, OS, Bergin, IL, et al. Dose-dependent incidence of hepatic tumors in adult mice following perinatal exposure to bisphenol A. Environ Health Perspect. 2014; 122, 485–491.CrossRefGoogle ScholarPubMed
17. Harley, KG, Aguilar Schall, R, Chevrier, J, et al. Prenatal and postnatal bisphenol A exposure and body mass index in childhood in the CHAMACOS cohort. Environ Health Perspect. 2013; 121, 514–520.CrossRefGoogle ScholarPubMed
18. Barker, DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261, 412–417.CrossRefGoogle ScholarPubMed
19. Oken, E, Gillman, MW. Fetal origins of obesity. Obes Res. 2003; 11, 496–506.CrossRefGoogle ScholarPubMed
20. Johnsson, IW, Haglund, B, Ahlsson, F, Gustafsson, J. A high birth weight is associated with increased risk of type 2 diabetes and obesity. Pediatr Obes. 2015; 10, 77–83.CrossRefGoogle ScholarPubMed
21. Govarts, E, Remy, S, Bruckers, L, et al. Combined effects of prenatal exposures to environmental chemicals on birth weight. Int J Environ Res Public Health. 2016; 13, E495.CrossRefGoogle ScholarPubMed
22. Gonzalez-Cossio, T, Peterson, KE, Sanin, LH, et al. Decrease in birth weight in relation to maternal bone-lead burden. Pediatrics. 1997; 100, 856–62.CrossRefGoogle ScholarPubMed
23. Laine, JE, Bailey, KA, Rubio-Andrade, M, et al. Maternal arsenic exposure, arsenic methylation efficiency, and birth outcomes in the Biomarkers of Exposure to ARsenic (BEAR) pregnancy cohort in Mexico. Environ Health Perspect. 2015; 123, 186–192.CrossRefGoogle ScholarPubMed
24. Geer, LA, Pycke, BF, Waxenbaum, J, et al. Association of birth outcomes with fetal exposure to parabens, triclosan and triclocarban in an immigrant population in Brooklyn, New York. J Hazard Mater. 2017; 323(Pt A), 177–183.CrossRefGoogle Scholar
25. Ferguson, KK, Meeker, JD, Cantonwine, DE, et al. Urinary phthalate metabolite and bisphenol A associations with ultrasound and delivery indices of fetal growth. Environ Int. 2016; 94, 531–537.CrossRefGoogle ScholarPubMed
26. Marchlewicz, EH, Dolinoy, DC, Tang, L, et al. Lipid metabolism is associated with developmental epigenetic programming. Sci Rep. 2016; 6, 34857.CrossRefGoogle ScholarPubMed
27. Veiga-Lopez, A, Kannan, K, Liao, C, et al. Gender-specific effects on gestational length and birth weight by early pregnancy BPA exposure. J Clin Endrocrinol Metab. 2015; 100, E1394–E1403.CrossRefGoogle ScholarPubMed
28. Watkins, DJ, Milewski, S, Domino, SE, Meeker, JD, Padmanabhan, V. Maternal phthalate exposure during early pregnancy and at delivery in relation to gestational age and size at birth: a preliminary analysis. Reprod Toxicol. 2016; 65, 59–66.CrossRefGoogle ScholarPubMed
29. Fenton, TR, Kim, JH. A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr. 2013; 13, 59.CrossRefGoogle ScholarPubMed
30. Verburg, BO, Steegers, EA, De Ridder, M, et al. New charts for ultrasound dating of pregnancy and assessment of fetal growth: longitudinal data from a population-based cohort study. Ultrasound Obstet Gynecol: The Official Journal of the International Society of Ultrasound in Obstetrics and Gynecology. 2008; 31, 388–396.CrossRefGoogle ScholarPubMed
31. Perng, W, Watkins, DJ, Cantoral, A, et al. Exposure to phthalates is associated with lipid profile in peripubertal Mexican youth. Environ Res. 2017; 154, 311–317.CrossRefGoogle ScholarPubMed
32. Pearson, MA, Lu, C, Schmotzer, BJ, Waller, LA, Riederer, AM. Evaluation of physiological measures for correcting variation in urinary output: implications for assessing environmental chemical exposure in children. J Expos Sci Environ Epidemiol. 2008; 19, 336–342.CrossRefGoogle ScholarPubMed
33. Zota, AR, Calafat, AM, Woodruff, TJ. Temporal trends in phthalate exposures: findings from the National Health and Nutrition Examination Survey, 2001-2010. Environ Health Perspect. 2014; 122, 235–241.CrossRefGoogle ScholarPubMed
34. Chen, D, Kannan, K, Tan, H, et al. Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity – a review. Environ Sci Technol. 2016; 50, 5438–5453.CrossRefGoogle ScholarPubMed
35. Lewin, A, Arbuckle, TE, Fisher, M, et al. Univariate predictors of maternal concentrations of environmental chemicals: The MIREC study. Int J Hyg Environ Health. 2017; 220, 77–85.CrossRefGoogle ScholarPubMed
36. Pycke, BF, Geer, LA, Dalloul, M, Abulafia, O, Halden, RU. Maternal and fetal exposure to parabens in a multiethnic urban U.S. population. Environ Int. 2015; 84, 193–200.CrossRefGoogle Scholar
37. Hanna-Attisha, M, LaChance, J, Sadler, RC, Champney Schnepp, A. Elevated blood lead levels in children associated with the flint drinking water crisis: a spatial analysis of risk and public health response. Am J Public Health. 2016; 106, 283–290.CrossRefGoogle ScholarPubMed
38. Hopenhayn, C, Huang, B, Christian, J, et al. Profile of urinary arsenic metabolites during pregnancy. Environ Health Perspect. 2003; 111, 1888–1891.CrossRefGoogle ScholarPubMed
39. Zota, AR, Phillips, CA, Mitro, SD. Recent fast food consumption and bisphenol A and phthalates exposures among the U.S. population in NHANES, 2003-2010. Environ Health Perspect. 2016; 124, 1521–1528.CrossRefGoogle ScholarPubMed
40. Prevention CfDCa. Fourth Report on Human Exposure to Environmental Chemicals, Updated Tables (January 2017). Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, 2017.Google Scholar
41. Johns, LE, Ferguson, KK, Soldin, OP, et al. Urinary phthalate metabolites in relation to maternal serum thyroid and sex hormone levels during pregnancy: a longitudinal analysis. Reprod Biol Endocrinol. 2015; 13, 4.CrossRefGoogle ScholarPubMed
42. Bellavia, A, Hauser, R, Seely, EW, et al. Urinary phthalate metabolite concentrations and maternal weight during early pregnancy. Int J Hyg Environ Health. 2017; 220, 1347–1355.CrossRefGoogle ScholarPubMed
43. Vrijkotte, TGM, Hrudey, EJ, Twickler, MB. Early maternal thyroid function during gestation is associated with fetal growth, particularly in male newborns. J Clin Endocrinol Metab. 2017; 102, 1059–1066.Google ScholarPubMed
44. Kim, SY, Sharma, AJ, Sappenfield, W, Wilson, HG, Salihu, HM. Association of maternal body mass index, excessive weight gain, and gestational diabetes mellitus with large-for-gestational-age births. Obstet Gynecol. 2014; 123, 737–744.CrossRefGoogle ScholarPubMed
45. Sathyanarayana, S, Barrett, E, Nguyen, R, et al. First trimester phthalate exposure and infant birth weight in the infant development and environment study. Int J Environ Res Public Health. 2016; 13, E945.CrossRefGoogle ScholarPubMed
46. Liu, J, Li, J, Wu, Y, et al. Bisphenol A metabolites and bisphenol S in paired maternal and cord serum. Environ Sci Technol. 2017; 51, 2456–2463.CrossRefGoogle ScholarPubMed
47. Catanese, MC, Vandenberg, LN. Bisphenol S (BPS) alters maternal behavior and brain in mice exposed during pregnancy/lactation and their daughters. Endocrinology. 2017; 158, 516–530.Google ScholarPubMed
48. Ivry Del Moral, L, Le Corre, L, Poirier, H, et al. Obesogen effects after perinatal exposure of 4,4’-sulfonyldiphenol (bisphenol S) in C57BL/6 mice. Toxicology. 2016; 357-358, 11–20.CrossRefGoogle Scholar
49. Castro, B, Sanchez, P, Torres, JM, et al. Bisphenol S affect differently 5-alpha-reductase expression and dopamine-serotonin systems in the prefrontal cortex of juvenile female rats. Environ Res. 2015; 142, 281–287.CrossRefGoogle ScholarPubMed
50. Cantonwine, DE, Ferguson, KK, Mukherjee, B, et al. Utilizing longitudinal measures of fetal growth to create a standard method to assess the impacts of maternal disease and environmental exposure. PLoS One. 2016; 11, e0146532.CrossRefGoogle ScholarPubMed
51. Lopes, KRM, Souza, ASR, Figueiroa, JN, Alves, JGB. Correlation between pre-pregnancy body mass index and maternal visceral adiposity with fetal biometry during the second trimester. Int J Gynaecol Obstet: The Official Organ of the International Federation of Gynaecology and Obstetrics. 2017; 138, 133–137.CrossRefGoogle ScholarPubMed
52. Wu, CT, Lu, TY, Chan, DC, et al. Effects of arsenic on osteoblast differentiation in vitro and on bone mineral density and microstructure in rats. Environ Health Perspect. 2014; 122, 559–565.CrossRefGoogle Scholar
53. 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.CrossRefGoogle ScholarPubMed
54. Wang, H, Li, J, Hao, JH, et al. High serum lead concentration in the first trimester is associated with an elevated risk of small-for-gestational-age infants. Toxicol Appl Pharmacol. 2017; 332, 75–80.CrossRefGoogle ScholarPubMed
55. Beier, EE, Maher, JR, Sheu, T-J, et al. Heavy metal lead exposure, osteoporotic-like phenotype in an animal model, and depression of Wnt signaling. Environ Health Perspect. 2013; 121, 97–104.CrossRefGoogle Scholar
56. P. Mattson, M, Calabrese, E. Hormesis: What it is and Why it Matters, 2009; pp. 1–13.CrossRefGoogle Scholar
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