Elsevier

Environmental Research

Volume 156, July 2017, Pages 597-604
Environmental Research

Effect of exposure to p,p´-DDE during the first half of pregnancy in the maternal thyroid profile of female residents in a Mexican floriculture area

https://doi.org/10.1016/j.envres.2017.04.013Get rights and content

Highlights

  • p,p´-DDE exposure increased maternal TT3 serum levels during first half of pregnancy.

  • This suggests that p,p´-DDE could act as a thyroid disruptor during pregnancy.

  • Basic and epidemiological research is needed to confirm or refute these findings.

Abstract

Background

Dichlorodiphenyldichloroethene (p,p´-DDE), the main metabolite of dichlorodiphenyltrichloroethane (DDT), has been associated with changes in human thyroid hormone levels. Maternal thyroid hormones are essential for adequate fetal neurodevelopment during the first half of pregnancy.

Objective

To evaluate the association between maternal p,p´-DDE concentration and the maternal thyroid profile during the first half of pregnancy.

Materials and Methods

We analyzed the information of 430 pregnant women from a Mexican floriculture area, with a gestational age ≤16 weeks. By questionnaire, we obtained sociodemographic, reproductive, and life-style, information. Serum concentrations of thyroid stimulating hormone (TSH), and total and free T3 and T4 were determined by means of Enzyme-Linked ImmunoSorbent Assay (ELISA). p,p´-DDE was analyzed by Gas Chromatography. The association between p,p´-DDE and thyroid profile was assessed through linear and logistic regression models.

Results

Thirty eight percent of women had p,p´-DDE levels below the Limit of Detection and 12.3% below the Limit of Quantification. Within the quantifiable range, median was 53.03 ng/g. TSH >2.5 mIU/L was present in 9.3% of women; 47.7% had isolated hypothyroxinemia; 3.5% had subclinical hypothyroidism, and 5.8% had overt hypothyroidism. We observed a significant positive association between quantifiable p,p´-DDE and total T3 serum levels in comparison with those with concentrations below the Limit of Detection (β=0.19; 95% CI=0.06, 0.34). There were no significant associations with other hormones of the thyroid profile or with clinical diagnosis.

Conclusions

Our findings suggest that p,p´-DDE exposure, even at low concentrations, could disrupt thyroid homeostasis during pregnancy.

Introduction

Thyroid hormones (TH) play a basic role in human brain maturation; therefore, reduction in TH availability during critical periods of embryonic and fetal development has been associated with psychomotor delay during infancy. The fetal thyroid gland begins to concentrate iodine after week 11 of gestation and at the maturation of the fetal hypothalamus-hypophysis-thyroid axis efficiently secretes iodized hormones at approximately week 18 (Taylor and Lebovic, 2007, Cooper et al., 2007). Thus, during the first half of pregnancy, the fetus depends on the adequate maternal thyroid function for proper development of the nervous system.

Prenatal exposure to DDT and p,p´-DDE, its main metabolite, has been associated with impaired neurodevelopment in humans (Eskenazi et al., 2009, Torres-Sánchez et al., 2013). Because organochlorine (OC) compounds are considered endocrine disruptors, they may mimic or interfere the action of thyroid hormones (Kezios et al., 2013), so thyroid disruption has been one of the biological mechanisms proposed to explain their neurotoxic effect (Porterfield, 2000; Corlbon, 2004). Some studies conducted in animal models have shown that DDT and p,p´-DDE reduce the expression of deiodinase 2 (D2), compete for the transporter proteins of thyroid hormones (TransThyRetin [TTR] and Thyroid Binding Globuline [TBG]), induce hepatic enzymes of the CYP450 complex and glucuronyltransferase, and act on the thyroid hormone receptors located within the hypothalamus-hypophysis-thyroid axis, altering thyroid homeostasis (Liu et al., 2011, Liu et al., 2014).

In humans, the association between p,p´-DDE and the thyroid function has been studied to a lesser extent. Studies carried out in pregnant women are scarce, and show inconsistent results. Some authors report a negative association between p,p´-DDE levels and total Triiodothyronine (total T3) (Takser et al., 2005); others find a negative association with free Thyroxine (free T4) and a positive one with Thyroid Stimulating Hormone (TSH) (Lopez-Espinosa et al., 2009), whereas three other studies find no association (Chevrier et al., 2008; Alvarez-Pedrerol et al., 2009; Kim et al., 2013).

In Mexico, DDT was widely used in agriculture and in malaria control campaigns and other vector-borne diseases. Its use for the control of agricultural pests was restricted in 1991, and in 1999, for the control of malaria (Yáñez et al., 2002). However, due to its high persistence in the environment, recent studies have revealed the presence of p,p´-DDE in serum samples (Trejo-Acevedo et al., 2012), adipose tissue (Galván-Portillo et al., 2002; Waliszewski et al., 2004), umbilical cord blood (Barraza-Vázquez et al., 2008), and maternal milk (López Guzmán et al., 2006).

Estado de México, Mexico, is a geographical area where floriculture represents one of the main economic activities and DDT was used to control pests that affected the flower crops. In a previous study in male floriculture workers, conducted by our research group in this area, we found a positive association between p,p´-DDE serum levels and total T3 and total T4, and a non-significant TSH reduction (Blanco-Muñoz et al., 2016). To date, we do not have knowledge about studies in Mexico that have evaluated this topic in pregnant women. Given the relevance of the thyroid function during pregnancy, the objective of this study was to evaluate the association between serum p,p´-DDE concentrations and maternal thyroid profile in pregnant women residing in a floriculture area of Estado de México.

Section snippets

Study design and population

Between June 2013 and December 2015, a pregnancy cohort study was assembled in a floriculture area of Estado de Mexico, Mexico. The main objective was to evaluate the effect of p,p′-DDE and organophosphate pesticides exposure during pregnancy on the occurrence of adverse reproductive outcomes, with a particular interest in maternal thyroid profile.

Pregnant women were identified at local health centers during their first prenatal visit or at the corresponding laboratory when pregnancy

Characteristics of the Study Population

Average gestational age at study entry was 10±2.86 weeks (range: 4–16 weeks). Most women were young (24.0±5.75 years), married or living in common law marriage (88%), and with average schooling of 9 years ±2.58. At least one previous pregnancy was reported by 59% of women, and 37% had a history of adverse reproductive outcomes, mainly abortion (19%). Around 34% of women reported previous tobacco smoking, but only two smoked during the current pregnancy. Consumption of alcoholic beverages during

Discussion

Our results showed that p,p´-DDE, even at relatively low concentrations, was positively associated with serum maternal total T3 levels during the first half of the pregnancy, without significant associations with TSH or other thyroid profile hormones.

To our knowledge, this is the first study in Mexico that had evaluated the association between p,p´-DDE exposure and the thyroid profile in pregnant women. We observed low p,p´-DDE concentrations in our study population; this could be because the

Funding sources

This study was supported by the National Council of Science and Technology of Mexico (CONACyT); grant no. 180956.

Study approval

The research that produced this article followed the guidelines of the Declaration of Helsinki of the World Medical Association. Institutional review board approval was obtained from the Ethics Committee of Instituto Nacional de Salud Pública of México. The participation of subjects did not occur until after informed consent was obtained.

Acknowledgments

We are grateful to the women who participated in the study and to the Statal Health Services of Estado de México and Rosa Ma. Garcia for support in chemical analyses.

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