Maternal hair—An appropriate matrix for detecting maternal exposure to pesticides during pregnancy

https://doi.org/10.1016/j.envres.2006.02.006Get rights and content

Abstract

The detection of exposure of pregnant women to toxicants in the environment is important because these compounds can be harmful to the health of the woman and her fetus. The aim of this study was to analyze for pesticides/herbicides in paired maternal hair and blood samples to determine the most appropriate matrix for detecting maternal exposure to these compounds. A total of 449 pregnant women were prospectively recruited at midgestation from an agricultural site in the Philippines where a preliminary survey indicated significant use at home and on the farm of the following compounds: propoxur, cyfluthrin, chlorpyrifos, cypermethrin, pretilachlor, bioallethrin, malathion, diazinon, and transfluthrin. Paired maternal hair and blood samples were obtained from each subject upon recruitment into the study (midgestation) and at birth and were analyzed for the above compounds, as well as lindane and DDT [1,1,1-trichloro-2-2-bis(p-chlorophenyl) ethane], and some of their known metabolites by gas chromatography/mass spectrometry. The highest exposure rate was seen for propoxur and bioallethrin and maternal hair analysis provided the highest detection rate for these two compounds, compared to blood, at both time periods: (1) At midgestation, 10.5% positive for propoxur in hair compared to 0.7% in blood (P<0.001) and for bioallethrin, 11.9% positive in hair compared to 0% in blood (P0.001), and (2) at birth, 11.8% positive for propoxur in hair compared to 4% in blood (P0.001) and for bioallethrin, 7.8% in hair compared to 0% in blood (P0.001). A small number of maternal hair samples were also positive for malathion, chlorpyrifos, pretilachlor, and DDT. Only a few of the pesticide metabolites were detected, principally 3-phenoxybenzoic acid, malathion monocarboxylic acid, and DDE [1,1,dichloro-2-2-bis(p-chlorophenyl)ethylene], and they were mostly found in maternal blood. There was a significant association between the use of the home spray pesticide, Baygon, and propoxur in maternal hair at birth (P=0.001) and between the use of a slow-burning mosquito coil and the presence of bioallethrin in maternal hair at midgestation and at birth (P=0.001, P0.041, respectively). There is significant exposure of the pregnant woman to pesticides, particularly to pesticides that are used at home. Our study demonstrates the advantages of analyzing maternal hair as a readily available biologic matrix for studying maternal exposure to toxicants in the environment, compared to blood. For propoxur, there was a 3- to 15-fold higher detection rate of the pesticide in maternal hair as compared to blood. As for the other pesticides, bioallethrin, malathion, chlorpyrifos, and DDT were exclusively found in maternal hair compared to blood. On the other hand, pesticide metabolites were infrequently found in maternal hair or maternal blood. Pesticides in blood most likely represent acute exposure, whereas pesticides in hair represent past and/or concurrent exposure. The high sensitivity, wide window of exposure, availability, and ease of hair collection are distinct advantages in using hair to detect exposure to pesticides among pregnant women. However, pesticides in maternal hair may also be secondary to passive exposure and therefore not truly representative of the internal pesticide dose. Finally, the analysis of maternal hair for pesticides as an index of maternal exposure to pesticides in the environment allows the institution of measures to prevent further exposure during pregnancy.

Introduction

Due to widespread use of pesticides, vast quantities are released and dispersed into the environment and are found in the air, water, soil, food sources, and other biological materials (U.S. EPA, 1998). The exposure of the pregnant woman to toxicants in the environment, specifically pesticides, is harmful both to her and her fetus. The transfer of pesticides across the placenta, from the mother to the fetus, is likely governed by a number of factors that affect most xenobiotics, including the concentration gradient of the pesticide between the maternal and fetal blood, the surface area of the placenta, the thickness of the membrane barrier, and the diffusion constant, which is determined by the physicochemical characteristics of the pesticides, such as molecular weight, pKa (the pH at which the pesticide is 50% ionized), lipid solubility, and state of ionization (Ostrea et al., 2004). In animal and human studies, the organochlorines, being highly lipophilic, cross the placenta more readily than the other pesticides, such as parathion, chlorpyrifos, or carbamate, and with a positive correlation existing between maternal and cord blood levels (Abdel-Rahman et al., 2002; Sala et al., 2001; Abu-Qare et al., 2000; Covaci et al., 2002a, Covaci et al., 2002b; Waliszewski et al., 2001).

Some pesticides are neurotoxicants, and aberrations in neuronal proliferation, migration, differentiation, synaptogenesis, myelination, and apoptosis in the fetus have been described in animals and humans exposed to these compounds (Barone et al., 2000; Eriksson, 1997). Depending on the degree of maternal exposure to the toxicants, potential adverse effects in the infant may occur and these effects may be dose dependent. Gross neurologic damage has been reported in infants born to mothers who had accidentally ingested food heavily contaminated with polychlorbiphenyl (Chen et al., 1992; Rogan et al., 1988). Chromosomal abnormalities, DNA damage, and predisposition to leukemia have been observed in infants born to mothers who were antenatally exposed to pesticides (Au et al., 1999; Buckley et al., 1989; Daniels et al., 1997; Ford et al., 1998; Infante-Rivard et al., 1991, Infante-Rivard et al., 1999; Shu et al., 1988; Ma et al., 2002). Most maternal exposures to toxicants in the environment are subtle and subclinical; however, serious concerns about their adverse effects on the fetus and the child have been raised, including developmental, learning, and behavioral difficulties, such as mental retardation, learning disability, attention deficit hyperactivity disorder, and autism (Boyle et al., 1994; California HHS, 1999; Schettler et al., 2000). Substantial evidence from animal and human data has demonstrated that a variety of chemicals commonly encountered in industry and the home can contribute to these disorders, even at low levels of exposure (Crump et al., 1998; Schantz and Bowman, 1989; Holene et al., 1998; Jacobson and Jacobson, 1990; Rosenstein and Chernoff, 1978). In one study, the carbamate, propoxur was observed to impair reflex development in the offspring of rats prenatally exposed to low levels of the pesticide (Rosenstein and Chernoff, 1978). In humans, abnormal reflexes in newborn infants, as assessed by the Brazelton Neonatal Behavioral Assessment Scale, were associated with maternal exposure to environmental organophosphates during pregnancy (Young et al., 2005).

It is therefore essential that reliable measures of exposure, particularly subclinical exposure, of pregnant women to toxicants in the environment be available to identify the women at risk and to initiate preventive measures to minimize further exposure. The aim of this study was to detect and compare pesticide exposure among pregnant women through the analysis of maternal hair and blood at midgestation and at birth.

Section snippets

Study group

Pregnant women were prospectively recruited at midgestation from the Outpatient Clinic of the Provincial Hospital in Malolos, an agricultural town in the province of Bulacan, Philippines. Informed consent was obtained from the subjects and maternal blood and hair were obtained upon recruitment (Sample A) and at delivery (Sample B). Maternal hair samples about the size of a pencil eraser in diameter were obtained from the base of the scalp. The hair samples were wrapped in aluminum foil and

Evaluation of analytical performance of maternal blood and hair analyses

Several classes of parent pesticides and their selected metabolites were effectively separated on the DB5-MS column using the oven programs we developed. Similar effective separation of parent compounds and metabolites were shown for blood (Corrion et al., 2005), and validation data for blood are presented in that paper. Limits of detection for blood in the current study ranged from 3.10–98.00 ng mL−1. The parent pesticides and their respective classes and metabolites are listed in Table 1, Table

Clinical study

A total of 449 pregnant women were studied with paired maternal hair (MH) and blood (MB) obtained at midgestation (A) and at delivery (B). The sociodemographic and environmental characteristics of the study population are shown in Table 3. The subjects had a mean age of 25.4 yr and a median gravidity of 2 and parity of 1. About 74% were married, 96.5% had attained at least a high school education, and 76.3% were homemakers. The average numbers of people and families per household were 5.4 and

Hair analysis for pesticides

The detection of pesticide exposure among pregnant women is important because of the potential toxicity of these compounds and of the need to initiate measures that can prevent further exposure. A survey of the literature has shown that maternal blood, plasma, and serum (James et al., 2002; Jarrell et al., 1998; Klopov et al., 1998; Sandanger et al., 2004) and occasionally maternal urine (Berkowitz et al., 2004; Young et al., 2005) and amniotic fluid (Bradman et al., 2003; Foster et al., 2000)

Conclusion

In conclusion, there is significant exposure of pregnant woman to pesticides, particularly to those used at home. The study results demonstrate the usefulness of maternal hair as a readily available, minimally invasive, and sensitive biological matrix for studying potential maternal exposure to toxicants in the environment. Pesticides in blood most likely represent acute exposure, whereas pesticides in hair represent past and/or concurrent exposure. The wide window of exposure, availability,

Acknowledgments

We acknowledge the invaluable help and participation in this research of Essie Ann M. Ramos, Abner M. Hornedo, Patrocinio C. Mateo, Philip Cruz, Lilibeth R. Avendano, Rubilyn S. Obando, Maribel V. Santiago, Roberta S. Briones, Rozza D.C. Villavicencio, and Cecilia C. Santiago.

This study is supported by grants from National Institutes of Child Health and Human Development, United States National Institutes of Health (1RO1HD039428), the United States Environmental Protection Agency (RFA

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      According to the literature the hair needs to be washed (Covaci et al., 2008; Zhang et al., 2007; Tsatsakis et al., 2008). Covaci et al. (2008, 2002) incubate the samples overnight; it is possible to pulverize the hair in a mill (Ostrea et al., 2006; Zhang et al., 2007; Tsatsakis et al., 2008) or submit a denaturation with HNO3 (Kucharska et al., 2014). Due to the meconium nature, it pre-treatment will consist basically in a homogenization by stirring in vortex (Hong et al., 2002; Bielawski et al., 2005).

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    Assurance for the conduct of human investigation: This study was conducted in accordance with national and institutional guidelines for the protection of human subjects. The study was approved by the Human Investigation Committee (HIC) of Wayne State University, Detroit, Michigan and the Human Investigational Review Board of the Bulacan Provincial Hospital, Bulacan, Philippines.

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