Maternal hair—An appropriate matrix for detecting maternal exposure to pesticides 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
References (49)
- et al.
A multi-analytes method for the quantification of contemporary pesticides in human serum and plasma using high-resolution mass spectrometry
J. Chromatogr. B
(2002) - et al.
Detection of prenatal exposure to several classes of environmental toxicants and their metabolites by gas chromatography/mass spectrometry in maternal and umbilical cord blood
J. Chromatogr. B
(2005) - et al.
Distribution of PCBs and organochlorine pesticides in umbilical cord and maternal serum
Sci. Total Environ.
(2002) - et al.
Hair analysis: another approach for the assessment of human exposure to selected persistent organochlorine pollutants
Chemosphere
(2002) - et al.
Behavioural hyperactivity in rats following postnatal exposure to sub-toxic doses of polychlorinated biphenyl congeners 153 and 126
Behav. Brain Res.
(1998) - et al.
Effects of in utero exposure to PCBs and related contaminants on cognitive functioning in young children
J. Pediatr.
(1990) - et al.
Evaluation of reproductive outcome in women inadvertently exposed to hexachlorobenzene in southeastern Turkey in the 1950s
Reprod. Toxicol.
(1998) - et al.
Prevalence of fetal exposure to environmental toxins as determined by meconium analysis
Neurotoxicology
(2002) - et al.
Drugs that affect the fetus and newborn infant via the placenta or breast milk
Pediatr. Clin. North Am.
(2004) - et al.
Levels of hexachlorobenzene and other organochlorine compounds in cord blood: exposure across placenta
Chemosphere
(2001)
Learning in monkeys exposed perinatally to 2.3.7.8-tetrachlorodibenzo p-dioxin (TODD)
Neurotoxicol. Teratol.
Association between in utero organophospbhate pesticide exposure and abnormal reflexes in neonates
Neurotoxicology
Pharmacokinetic profile and placental transfer of a single intravenous injection of [(14)C]chlorpyrifos in pregnant rats
Arch. Toxicol.
Placental transfer and pharmacokinetics of a single dermal dose of [14C] methyl parathion in rats
Toxicol. Sci.
The relationship between levels of PCBs and pesticides in human hair and blood: preliminary results
Environ. Health Perspect.
Cytogenetic effects from exposure to mixed pesticides and the influence from genetic susceptibility
Environ. Health Perspect.
Vulnerable processes of nervous system development: a review of markers and methods
Neurotoxicology
In utero pesticide exposure, maternal paraoxonase activity and head circumference
Environ. Health Perspect.
Prevalence and health impact of developmental disabilities in US children
Pediatrics
Measurement of pesticides and other toxicants in amniotic fluid as a potential biomarker of prenatal exposure: a validation study
Environ. Health Perspect.
Occupational exposures of parents of children with acute nonlymphocytic leukemia: a report from the Childrens Cancer Study Group
Cancer Res.
Cognitive development of Yu-Cheng (oil disease) children prenatally exposed to heat-degraded PCBs
J. Am. Med. Assoc.
Influence of prenatal mercury exposure upon scholastic and psychological test performance: benchmark analysis of a New Zealand cohort
Risk Anal.
Cited by (48)
Applying hair exposome for linking environmental exposure to reproductive health: A comprehensive review and research perspective
2024, Hygiene and Environmental Health AdvancesBiomonitoring of organic pollutants in pet dog plasma samples in North-Western Spain
2023, Science of the Total EnvironmentMethods for environmental monitoring of pesticide exposure
2020, Exposure and Risk Assessment of Pesticide Use in Agriculture: Approaches, Tools and AdvancesScreening of organic pollutants in pet hair samples and the significance of environmental factors
2018, Science of the Total EnvironmentOptimization of selective pressurized liquid extraction of organic pollutants in placenta to evaluate prenatal exposure
2017, Journal of Chromatography APerspective on pre- and post-natal agro-food exposure to persistent organic pollutants and their effects on quality of life
2017, Environment InternationalCitation Excerpt :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).
- ☆
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.