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Phthalate and bisphenol A exposure during in utero windows of susceptibility in relation to reproductive hormones and pubertal development in girls.
Environ Res. 2017 11; 159:143-151.ER

Abstract

BACKGROUND

Over the past several decades, the age of pubertal onset in girls has shifted downward worldwide. As early pubertal onset is associated with increased risky behavior and psychological issues during adolescence and cardiometabolic disease and cancer in adulthood, this is an important public health concern. Exposure to endocrine disrupting chemicals during critical windows of in utero development may play a role in this trend. Our objective was to investigate trimester-specific phthalate and BPA exposure in relation to pubertal development among girls in the Early Life Exposure in Mexico to Environmental Toxicants (ELEMENT) birth cohort.

METHODS

We measured maternal urinary phthalate metabolites and BPA in samples collected during the first, second, and third trimesters of pregnancy. To assess reproductive development among their female children, we measured serum testosterone, estradiol, dehydroepiandrosterone sulfate (DHEA-S), inhibin B, and sex hormone-binding globulin (SHBG), and assessed sexual maturation, including Tanner staging for breast and pubic hair development and menarche status, at age 8-13 years (n = 120). We used linear and logistic regression to examine measures of trimester-specific in utero exposure as predictors of peripubertal hormone levels and pubertal onset, respectively. In secondary analyses, we evaluated estimated exposure at the midpoint of the first trimester and rates of change in exposure across pregnancy in relation to outcomes.

RESULTS

Several phthalate metabolites measured throughout in utero development were associated with higher serum testosterone concentrations, while a number of metabolites measured in the third trimester were associated with higher DHEA-S. For example, an interquartile range (IQR) increase in mean monoethyl phthalate (MEP) levels across pregnancy was associated with 44% higher peripubertal testosterone (95% CI: 13-83%), while an IQR increase in di-2-ethylhexyl phthalate metabolites (ΣDEHP) specifically in the third trimester was associated with 25% higher DHEA-S (95%CI: 4.7-47%). In IQR increase in mean mono-2-ethylhexyl phthalate (MEHP) levels across pregnancy was associated with lower odds of having a Tanner Stage >1 for breast development (OR = 0.32, 95%CI: 0.11-0.95), while MEHP in the third trimester was associated with higher odds of having a Tanner Stage >1 for pubic hair development (OR = 3.76, 95%CI: 1.1-12.8). Results from secondary analyses were consistent with findings from our main analysis.

CONCLUSION

These findings suggest that female reproductive development may be more vulnerable to the effects of phthalate or BPA exposure during specific critical periods of in utero development. This highlights the need for comprehensive characterizations of in utero exposure and consideration of windows of susceptibility in developmental epidemiological studies. Future research should consider repeated measures of in utero phthalate and BPA exposure within each trimester and across pregnancy.

Authors+Show Affiliations

Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA. Electronic address: debjwat@umich.edu.Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA.Center for Nutrition and Health Research, Instituto Nacional de Salud Pública, Cuernavaca, MOR, Mexico.Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA; Pediatric Endocrinology, Child Health Evaluation and Research Unit (CHEAR), University of Michigan, Ann Arbor, MI, USA.Center for Nutrition and Health Research, Instituto Nacional de Salud Pública, Cuernavaca, MOR, Mexico.American British Cowdray (ABC) Hospital, Mexico City, Mexico.Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA; Center for Human Growth and Development, University of Michigan, Ann Arbor, MI, USA.Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA.

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

28800472

Citation

Watkins, Deborah J., et al. "Phthalate and Bisphenol a Exposure During in Utero Windows of Susceptibility in Relation to Reproductive Hormones and Pubertal Development in Girls." Environmental Research, vol. 159, 2017, pp. 143-151.
Watkins DJ, Sánchez BN, Téllez-Rojo MM, et al. Phthalate and bisphenol A exposure during in utero windows of susceptibility in relation to reproductive hormones and pubertal development in girls. Environ Res. 2017;159:143-151.
Watkins, D. J., Sánchez, B. N., Téllez-Rojo, M. M., Lee, J. M., Mercado-García, A., Blank-Goldenberg, C., Peterson, K. E., & Meeker, J. D. (2017). Phthalate and bisphenol A exposure during in utero windows of susceptibility in relation to reproductive hormones and pubertal development in girls. Environmental Research, 159, 143-151. https://doi.org/10.1016/j.envres.2017.07.051
Watkins DJ, et al. Phthalate and Bisphenol a Exposure During in Utero Windows of Susceptibility in Relation to Reproductive Hormones and Pubertal Development in Girls. Environ Res. 2017;159:143-151. PubMed PMID: 28800472.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Phthalate and bisphenol A exposure during in utero windows of susceptibility in relation to reproductive hormones and pubertal development in girls. AU - Watkins,Deborah J, AU - Sánchez,Brisa N, AU - Téllez-Rojo,Martha Maria, AU - Lee,Joyce M, AU - Mercado-García,Adriana, AU - Blank-Goldenberg,Clara, AU - Peterson,Karen E, AU - Meeker,John D, Y1 - 2017/08/08/ PY - 2017/05/15/received PY - 2017/06/28/revised PY - 2017/07/30/accepted PY - 2017/8/12/pubmed PY - 2017/10/17/medline PY - 2017/8/12/entrez KW - Adrenarche KW - Bisphenol A KW - In utero KW - Phthalates KW - Pregnancy KW - Puberty KW - Windows of susceptibility SP - 143 EP - 151 JF - Environmental research JO - Environ. Res. VL - 159 N2 - BACKGROUND: Over the past several decades, the age of pubertal onset in girls has shifted downward worldwide. As early pubertal onset is associated with increased risky behavior and psychological issues during adolescence and cardiometabolic disease and cancer in adulthood, this is an important public health concern. Exposure to endocrine disrupting chemicals during critical windows of in utero development may play a role in this trend. Our objective was to investigate trimester-specific phthalate and BPA exposure in relation to pubertal development among girls in the Early Life Exposure in Mexico to Environmental Toxicants (ELEMENT) birth cohort. METHODS: We measured maternal urinary phthalate metabolites and BPA in samples collected during the first, second, and third trimesters of pregnancy. To assess reproductive development among their female children, we measured serum testosterone, estradiol, dehydroepiandrosterone sulfate (DHEA-S), inhibin B, and sex hormone-binding globulin (SHBG), and assessed sexual maturation, including Tanner staging for breast and pubic hair development and menarche status, at age 8-13 years (n = 120). We used linear and logistic regression to examine measures of trimester-specific in utero exposure as predictors of peripubertal hormone levels and pubertal onset, respectively. In secondary analyses, we evaluated estimated exposure at the midpoint of the first trimester and rates of change in exposure across pregnancy in relation to outcomes. RESULTS: Several phthalate metabolites measured throughout in utero development were associated with higher serum testosterone concentrations, while a number of metabolites measured in the third trimester were associated with higher DHEA-S. For example, an interquartile range (IQR) increase in mean monoethyl phthalate (MEP) levels across pregnancy was associated with 44% higher peripubertal testosterone (95% CI: 13-83%), while an IQR increase in di-2-ethylhexyl phthalate metabolites (ΣDEHP) specifically in the third trimester was associated with 25% higher DHEA-S (95%CI: 4.7-47%). In IQR increase in mean mono-2-ethylhexyl phthalate (MEHP) levels across pregnancy was associated with lower odds of having a Tanner Stage >1 for breast development (OR = 0.32, 95%CI: 0.11-0.95), while MEHP in the third trimester was associated with higher odds of having a Tanner Stage >1 for pubic hair development (OR = 3.76, 95%CI: 1.1-12.8). Results from secondary analyses were consistent with findings from our main analysis. CONCLUSION: These findings suggest that female reproductive development may be more vulnerable to the effects of phthalate or BPA exposure during specific critical periods of in utero development. This highlights the need for comprehensive characterizations of in utero exposure and consideration of windows of susceptibility in developmental epidemiological studies. Future research should consider repeated measures of in utero phthalate and BPA exposure within each trimester and across pregnancy. SN - 1096-0953 UR - https://www.unboundmedicine.com/medline/citation/28800472/Phthalate_and_bisphenol_A_exposure_during_in_utero_windows_of_susceptibility_in_relation_to_reproductive_hormones_and_pubertal_development_in_girls_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0013-9351(17)30910-6 DB - PRIME DP - Unbound Medicine ER -