Elsevier

NeuroToxicology

Volume 30, Issue 2, March 2009, Pages 231-239
NeuroToxicology

Neurobehavioral effects of ambient air pollution on cognitive performance in US adults

https://doi.org/10.1016/j.neuro.2008.12.011Get rights and content

Abstract

Background

In vivo animal experiments demonstrate neurotoxicity of exposures to particulate matter (PM) and ozone, but only one small epidemiological study had linked ambient air pollution with central nervous system (CNS) functions in children.

Objectives

To examine the neurobehavioral effects associated with long-term exposure to ambient PM and ozone in adults.

Methods

We conducted a secondary analysis of the Neurobehavioral Evaluation System-2 (NES2) data (including a simple reaction time test [SRTT] measuring motor response speed to a visual stimulus; a symbol-digit substitution test [SDST] for coding ability; and a serial-digit learning test [SDLT] for attention and short-term memory) from 1764 adult participants (aged 37.5 ± 10.9 years) of the Third National Health and Nutrition Examination Survey in 1988–1991. Based on ambient PM10 (PM with aerodynamic diameter <10 μm) and ozone data from the EPA Aerometric Information Retrieval System database, estimated annual exposure prior to the examination were aggregated at the centroid of each census-block group of geocoded residences, using distance-weighted averages from all monitors in the residing and adjoining counties. Generalized linear models were constructed to examine the associations, adjusting for potential confounders.

Results

In age- and sex-adjusted models, PM10 predicted reduced CNS functions, but the association disappeared after adjustment for sociodemographic factors. There were consistent associations between ozone and reduced performance in NES2. In models adjusting for demographics, socioeconomic status, lifestyle, household and neighborhood characteristics, and cardiovascular risk factors, ozone predicted high scores in SDST and SDLT, but not in SRTT. Each 10-ppb increase in annual ozone was associated with increased SDST and SDLT scores by 0.16 (95%CI: 0.01, 0.23) and 0.56 (95%CI: 0.07, 1.05), equivalent to 3.5 and 5.3 years of aging-related decline in cognitive performance.

Conclusions

Our study provides the first epidemiological data supporting the adverse neurobehavioral effects of ambient air pollutants in adults.

Introduction

Ambient air pollution, especially the particulate matters (PM), has increasingly been appreciated as a threat to cardiopulmonary health (Kaiser, 2005, Nel, 2005). Following several reports in the early 1990s showing excessive mortality associated with unexpectedly low PM concentrations (Pope and Dockery, 2006), hundreds of epidemiologic studies have reported fairly consistent associations between elevated PM concentrations over short periods of 1 or several days and increased cardiovascular mortality and morbidity (e.g., hospitalizations, emergency visits). Recent meta-analyses also confirmed a consistent and positive association between short-term ambient ozone and cardiovascular mortality (Bell et al., 2005, Ito et al., 2005, Levy et al., 2005). Short-term elevations of PM and ozone can increase ischemic stroke mortality (Henrotin et al., 2007, Hong et al., 2002) and morbidity (Chan et al., 2006, Wellenius et al., 2005). In addition, large cohort studies have demonstrated that long-term exposures to ambient air pollutants are associated with increased cardiovascular mortality (Dockery et al., 1993, Pope et al., 2002) and PM exposure increases the risks for coronary heart diseases and stroke. (Miller et al., 2007) Paralleling this epidemiologic literature are intriguing findings from clinical experiments (Brook et al., 2002, Rundell et al., 2007) and in vivo animal models (Sun et al., 2005, Suwa et al., 2002), all pointing to the possibility that ambient air pollutants can perturb endothelial function, damage microvasculature, and eventually cause progression of atherosclerosis. Given the strong associations of cognitive aging with these clinical conditions and neuropathological processes (Knopman et al., 2001), it is plausible that long-term exposures to ambient air pollutants may affect neurocognitive function in humans. Various in vivo experiments with exposures to ozone, PM, or particles–ozone mixtures have found the neurotoxic effects in different animal models (Dorado-Martinez et al., 2001, Elder et al., 2006, Rivas-Arancibia et al., 1998, Sirivelu et al., 2006, Sorace et al., 2001), supporting the adverse neurocognitive effect of exposure to ambient air pollution. In the recent cross-sectional analysis of extant neurocognitive function data collected among 202 children enrolled in a birth cohort, high levels of black carbon (a marker for traffic particles) were associated with decreased cognitive function across assessments of verbal and nonverbal intelligence and memory constructs (Suglia et al., 2008). However, epidemiological data linking the cognitive function in adults with exposure to ambient air pollution are still lacking. The following study was carried out to address this significant data gap.

Section snippets

Study design

Our secondary analyses used the extant data on central nervous system (CNS) function from the Third National Health and Nutrition Examination Survey (NHANES III) conducted by the National Center for Health Statistics (NCHS) of the Centers for Disease Control and Prevention between 1988 and 1994. Details about this survey and related methods have been published (NCHS, 1995). In brief, the NHANES III followed a multi-stage stratified random sampling of the U.S. population, with oversampling of

Characteristics of study population

Table 1 shows the population characteristics of the source population of adult participants in NHANES-III, 1988–1991. Compared to participants with estimable air pollutant data (N = 3944), subjects with missing exposure data were slightly younger (p < 0.0001) and more likely to be non-Hispanic whites (p < 0.0001), had lower family income (p < 0.001), and more likely came from rural areas (p < 0.001) or communities with lower poverty-income ratio (p < 0.0001). These comparisons denoted that the missing data

Discussion

Our analyses demonstrated that, reduced performance in neurobehavioral tests in US adults (aged 20–59 years) was associated with estimated increasing levels of estimated annual exposure to ambient ozone prior to the examination in 1988–1991. Such a putatively ozone-associated CNS effect could not be completely attributable to the between-individual differences in demographics, socioeconomic factors, lifestyles, household characteristics, urban/rural locations, and conventional CVD risk factors.

Conclusions

Our study provided the first epidemiological data supporting the adverse effects of ambient air pollutants on CNS in adults. Longitudinal studies are needed to fully investigate whether long-term exposure to air pollution causes neurobehavioral changes and subsequent development of neurocognitive impairments, including cognitive decline (global and within specific domains) and dementia.

Conflict of interest

The authors declare that there are no conflicts of interest.

Acknowledgements

This work was supported in part by the National Institute of Environmental Health Sciences grant ES00002 and Environmental Protection Agency (EPA) grants EPA R827353 and R832416. The authors thank two anonymous reviewers for helpful comments.

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