Risk of learning and behavioral disorders following prenatal and early postnatal exposure to tetrachloroethylene (PCE)-contaminated drinking water
Introduction
Tetrachloroethylene (PCE, Perc or perchloroethylene) is a manufactured chemical used mainly for fabric dry cleaning and metal degreasing. PCE is one of the most commonly detected solvents in groundwater [30] and at United States Environmental Protection Agency (USEPA) Superfund sites [35]. As of 1997, 771 National Priority List (NPL) sites around the United States had evidence of PCE contamination [35]. In addition, PCE had been found in 38% of the 9232 surface water sampling sites in the United States [35].
PCE and its main metabolite dichloroacetylene (DCA) are recognized human and animal neurotoxicants [44], [45], [23], [42], [16]. These fat soluble substances have a high affinity for the lipophilic tissues of the central nervous system [2]. PCE also readily crosses both the placental and blood brain barriers [23].
Most of the relevant epidemiological literature has examined neurological sequelae among adults with occupational exposures to mixtures of organic solvents. Impairments in cognition and vision have been observed, as have mood changes [50], [21], [37], [17], [33], [31], [32], [9], [39], [22], [10], [11], [12], [46], [34], [19], [49]. The cognitive sequelae observed following mixed organic solvent exposures included diminished performance on measures of memory, attention/executive function, and motor skills. The results from the few studies examining adult occupational exposures to only PCE are mixed. Some studies found diminished performance on measures of attention/executive function among the PCE exposed subjects compared to unexposed controls [44], [19], while other studies did not find adverse effects [12], [19]. All studies that examined visuospatial abilities found a diminished performance in the PCE exposed group compared to unexposed controls [44], [12].
The maturation of the nervous system is more complex than any other organ, thus making it exquisitely vulnerable to chemical insults. Depending on timing, type, and dose, an exposure occurring during the developmental period can result in long-term alterations in brain structure and function. The vulnerable window for neurotoxic agents is long, extending from the prenatal period through adolescence and early adulthood. The functional domains of the nervous system (language, visuospatial, learning and memory and motor abilities) develop at different times with different windows of vulnerability and different sensitivities to environmental agents [[29], [1], [38], [18], [14], [24]–[25], [8], [7]].
To date, three studies have examined effects of maternal occupational mixed solvent exposure during the prenatal period on neurodevelopment. The study by Eskenazi et al. [15] showed no significant difference in general mental abilities, using the McCarthy Scales of Children's Abilities, between exposed and unexposed children at ages 3–4 years. Domain specific functions (i.e. memory or language specific tests) were not examined.
In contrast, Till et al. [43] found that prenatal maternal exposure to organic solvent mixtures was associated with worse performance on measures of expressive and receptive language, and reduced graphomotor skills (using NEPSY tests) among children at ages 3–7 years. Study parents also rated exposed children as having more behavioral problems on the child behavior checklist than unexposed children.
Laslo-Baker et al. [27] examined children exposed to organic solvent mixtures during the prenatal period and neurobehavioral performance at ages 3–7 years. Exposed children scored lower on neurobehavioral tests of general intelligence, language and motor abilities. General intelligence was assessed with the Wechsler Preschool and Primary Scale of Intelligence (WPPSI) and Wechsler Intelligence Scale for Children III (WISC III). Language was assessed using the Preschool Language Scale 3 (PSL 3) and Clinical Evaluation of Language Fundamentals 3 (CELF 3). Motor abilities were assessed with the grooved pegboard test.
Unlike the occupational studies described above, the present study examined PCE exposure from an unusual environmental scenario. In early 1980 it was discovered that PCE had been leaching into the drinking water supplies of many New England towns during the previous 15 years. Investigations revealed that the public water distribution systems in many of these towns had installed vinyl-lined asbestos-cement (VL/AC) pipes and that PCE had leached into the water from the liner. Approximately 660 miles of these pipes were installed in Massachusetts from 1968 through early 1980; a large proportion was installed in eight Cape Cod towns [26] (Fig. 1). The pipe manufacturing practice involved spraying a mixture of vinyl toluene resin and PCE onto the interior of the pipe. It was believed that the PCE would volatilize and disappear before the pipes were installed. However, PCE measurements taken in 1980 from Cape Cod public drinking water supplies ranged from 1.5 µg/L to 7750 µg/L [13]. State officials decided that the most appropriate remedy was to flush and bleed the VL/AC pipes in order to reduce the PCE concentrations to levels determined to be safe at the time. The 1980 action level was set to 40 µg/L to address this problem; the current United States Environmental Protection Agency (USEPA) maximum contaminant level (MCL) is 5 µg/L [45].
This scenario presented a unique and valuable setting for examining the health effects of PCE exposure because many people were exposed to a large range of levels, and other water contaminants were rare. Furthermore, the VL/AC pipes were irregularly distributed according to the replacement and expansion needs of the towns. As part of a population-based study that examined the connection between exposure to PCE-contaminated drinking water and adverse reproductive and developmental outcomes, the current study investigated the impact of prenatal and early postnatal PCE exposure on learning, attention and behavior.
Section snippets
Study population selection
All children born between 1969 and 1983 whose mothers lived in one of eight Cape Cod towns with VL/AC water distribution pipes at the time of birth were eligible for the study. These towns were Barnstable, Brewster, Bourne, Chatham, Falmouth, Mashpee, Provincetown, and Sandwich (Fig. 1). Eligible children were identified by reviewing Massachusetts birth certificates. The residence listed on the birth certificate was cross-matched with a database of all street locations with VL/AC pipes to
Results
A total of 2086 subjects were available for the final analysis. According to the initial exposure designation, there were 1063 exposed and 1023 unexposed children. Following the in-depth exposure assessment, there were 1349 exposed and 737 unexposed children (Table 1). A total of 444 subjects switched exposure groups: 365 unexposed children switched to the exposed group and 79 exposed children switched to unexposed group. The primary reason for switching from the unexposed to exposed group was
Discussion
The results of this study suggest that prenatal and early postnatal exposure to PCE are not associated with later disorders of attention, learning and behavior using questionnaire-based outcome measures and at the exposure levels experienced by this study population. While modest associations were seen for some outcomes (i.e., received a diagnosis of ADD or HD, special class placement for academic or behavioral problems, and lower educational attainment, being placed on an IEP), the
Conflict of interest
All authors (Patricia Janulewicz, Roberta White, Michael Winter, Janice Weinberg, Lisa Gallagher, Veronica Vieira, Thomas Webster, and Ann Aschengrau) attest to having no conflict of interest.
Acknowledgements
This research was supported by a grant from the National Institute of Environmental Health Sciences, Superfund Basic Research Program (5 P42 ES007381). The study sponsors have had no role in study design, data collection, analysis, interpretation of results, manuscript writing or the decision to submit this paper for publication. This paper's contents are solely the responsibility of the authors and do not necessarily represent the official views of NIEHS, NIH. This study was approved by the
References (50)
- et al.
Neurobehavioral and neurophysiological outcome of chronic low-level tetrachloroethene exposure measured in neighborhoods of dry cleaning shops
Environ. Res.
(1995) - et al.
Mood and behavioral symptoms in individuals with chronic solvent exposure
Psychiatry Res.
(2000) - et al.
Environmental health of children
J. Pediatr. Health Care
(2003) Pesticides and children
Toxicol. Appl. Pharmacol.
(2004)- et al.
Neurobehavioral effects of exposure to trichloroethylene through a municipal water supply
Environ. Res.
(2003) - et al.
Neurobehavioral effects of exposure to trichloroethylene through a municipal water supply
Environ. Res.
(2003) - et al.
Prenatal exposure to organic solvents and child neurobehavioral performance
Neurotoxicol. Teratol.
(2001) - et al.
Neurobehavioral effects of occupational exposure to low-level organic solvents among Taiwanese workers in paint factories
Environ. Res.
(1997) - et al.
Long-term neuropsychological impact of brief occupational exposure to organic solvents
Arch Clin Neuropsychol
(2005) - et al.
Workshop to identify critical windows of exposure for children's health: neurobehavioral work group summary
Environ. Health Perspect.
(2000)
Estimating exposure to volatile organic compounds from municipal water-supply systems: use of a better computational model
Environ. Health Arch.
Essentials of Epidemiology in Public Health
Perchloroethylene-contaminated drinking water and the risk of breast cancer: additional results from Cape Cod, Massachusetts, USA
Environ. Health Perspect.
Environmental health hazards: how children are different from adults
Future Child.
How are children different from adults?
Environ. Health Perspect.
The psychological effects of exposure to mixed organic solvents on car painters
Disabil. Rehabil.
Neuropsychological dysfunction, mood disturbance, and emotional status of munitions workers
Appl. Neuropsychol.
Neuropsychological function in retired workers with previous long-term occupational exposure to solvents
Occup. Environ. Med.
In utero exposure to organic solvents and human neurodevelopment
Dev. Med. Child Neurol.
Occupational and Environmental Neurotoxicology
Cognitive effects of chronic exposure to lead and solvents
Am. J. Ind. Med.
Neurobehavioral and health-related deficits in solvent-exposed painters
Am. J. Ind. Med.
Generalized Additive Models
Cited by (22)
Dielectric barrier discharge plasma as excellent method for Perchloroethylene removal from aqueous environments: Degradation kinetic and parameters modeling
2017, Journal of Molecular LiquidsCitation Excerpt :Potential environmental exposure paths to Perchloroethylene generally occurred via air, rainwater, surface water and drinking-water [1]. Winte M.R et al. have reported PCE concentrations up to 7.750 ppm in water [5]. Former study evidences have shown that Perchloroethylene (PCE) is toxic and carcinogen for humans [6–9].
Childhood and adolescent fish consumption and adult neuropsychological performance: An analysis from the Cape Cod Health Study
2017, Neurotoxicology and TeratologyStructural Magnetic Resonance Imaging in an adult cohort following prenatal and early postnatal exposure to tetrachloroethylene (PCE)-contaminated drinking water
2013, Neurotoxicology and TeratologyCitation Excerpt :The database also contained information on the installation year and diameter of the pipes. This tentative designation was based on visual inspection of the maps of water pipes in the immediate vicinity of the birth residence (Janulewicz et al., 2008). The study was approved by the Institutional Review Boards (IRBs) of the Massachusetts Department of Public Health and Boston University Medical Center, and by the 24A/B/11B Review Committee at the Massachusetts Department of Public Health.
Adult neuropsychological performance following prenatal and early postnatal exposure to tetrachloroethylene (PCE)-contaminated drinking water
2012, Neurotoxicology and TeratologyCitation Excerpt :More extensive exposure assessments were conducted following the return of self-administered questionnaires which included residential histories as well as information on the drinking water source. For a more detailed explanation see Janulewicz et al. (2008). The study was approved by the Institutional Review Boards (IRB) of the Massachusetts Department of Public Health and Boston University Medical Center and the 24A/B/11B Review Committee at the Massachusetts Department of Public Health.
Contribution of compressional waves to the identification and quantification of a water contaminant
2010, Sensors and Actuators, B: ChemicalCitation Excerpt :Volatile organic compounds (VOC's) are a group of commonly used chemicals that evaporate or volatilize, when exposed to air. They are considered to be potentially carcinogenic and mutagenic [11–13] and include compounds such as dichloromethane, 1,2-dichloroethane, benzene, chloroform, toluene, trichloroethylene and tetrachloroethylene, among others. The release of such compounds in surface water has lead to large environmental catastrophes.
Drug use disorder following early life exposure to tetrachloroethylene (PCE)-contaminated drinking water: A retrospective cohort study
2020, Environmental Health: A Global Access Science Source