Elsevier

Environmental Research

Volume 177, October 2019, 108632
Environmental Research

Pesticide exposure and cognitive function: Results from the Hellenic Longitudinal Investigation of Aging and Diet (HELIAD)

https://doi.org/10.1016/j.envres.2019.108632Get rights and content

Highlights

  • The role of chronic pesticide exposure on cognitive function remains contradictory.

  • Data from HELIAD study was used in order to the role of self-reported pesticide exposure on cognitive function be assessed.

  • Associations between z-scores of cognitive performance and self-reported pesticide exposure were examined.

  • Non-demented individuals, who had been living in areas near sprayed fields, had poorer neuropsychological performance.

  • Self-reported exposure to pesticides was negatively associated with cognitive performance.

Abstract

Background

Results from studies to date, regarding the role of chronic pesticide exposure on cognitive function remain contradictory.

Objective

To investigate the relationship between self-reported pesticide exposure and cognitive function.

Methods

Data from a population-based cohort study of older adults (HEllenic Longitudinal Investigation of Aging and Diet) in Greece was used. Pesticide exposure classification was based on 1) living in areas that were being sprayed; 2) application of spray insecticides/pesticides in their gardens; and 3) occupational application of sprays. Associations between z-scores of cognitive performance and self-reported pesticide exposure were examined with linear regression analyses. Adjusted models were applied, for all analyses.

Results

Non-demented individuals who reported that they had been living in areas near sprayed fields, had poorer neuropsychological performance, compared to those who had never lived in such areas. Sub-analyses revealed poorer performance in language, executive and visual-spatial functioning, and attention. These associations remained after a sensitivity analysis excluding subjects with mild cognitive impairment.

Conclusion

Self-reported exposure to pesticides was negatively associated with cognitive performance.

Introduction

Alzheimer's Disease (AD) is a neurodegenerative disorder with an irreversible and progressive course (Wang et al., 2017), constituting the main cause of dementia (Scheltens et al., 2016). Approximately 40 million people have dementia worldwide, a number which is thought to be doubling every two decades (Prince et al., 2013). Among European citizens over the age of 65 years, the prevalence of AD is estimated to be around 5% (Niu et al., 2017).

The pathophysiology of dementia remains largely unknown (Elahi and Miller, 2017). However, there is evidence to suggest that genetic factors could explain a high proportion of dementia cases (Cuyvers and Sleegers, 2016; Loy et al., 2014). Moreover, environmental factors, including smoking (Zhong et al., 2015), obesity (Singh-Manoux et al., 2018), pesticide exposure (Killin et al., 2016), alongside the effect of epigenetic mechanisms (Maloney and Lahiri, 2016), as a potential connecting link between genetic and environmental factors, may also constitute modifiable causes of the development and course of dementia.

Several studies have examined the contribution of chronic pesticide exposure to the risk of dementia and AD. More specifically, increased risk of AD due to occupational exposure to pesticides was originally reported in the Canadian Study of Health and Aging (1994). Afterwards, it was shown that in occupationally exposed people, cognitive impairment appears to persist even after retirement from work (Baldi et al., 2003), and that the risk of AD and dementia may be increased in later life (Hayden et al., 2010). Accordingly, environmental pesticide exposure, in areas with a high level of pesticide use, was associated with AD and a few other neurodegenerative and psychiatric disorders as well (Parron et al., 2011). More recently, a study in Chile (Corral et al., 2017) has shown that even indirect exposure to pesticides, referring to people who never used pesticides but who lived in areas environmentally exposed to chronic use of pesticides, affects cognitive functioning. In a recent systematic review, pesticide exposure was even characterized as a moderate putative risk factor of dementia (Killin et al., 2016), and an additional positive association between pesticide exposure and AD was suggested in a recent meta-analysis (Yan et al., 2016), confirming that pesticide exposure might indeed be a risk factor for AD.

Pesticide exposure has also been associated with mild cognitive impairment (MCI) (Bosma et al., 2000), as well as vascular dementia (VD) and PD-dementia, but not frontotemporal lobar degeneration (FTLD) (Zaganas et al., 2013). In addition, different aspects of cognitive performance (selective attention, symbol-digit, Mini-Mental State Examination score, reaction time tests) seem to be adversely influenced by pesticide exposure (Baldi et al., 2011; Rohlman et al., 2007; Zaganas et al., 2013).

Nevertheless, other studies have revealed a weak or no evident association between AD and pesticide exposure (French et al., 1985; Gauthier et al., 2001; Gun et al., 1997; Povey et al., 2014; Tyas et al., 2001). Interestingly, pesticide exposure was negatively associated with non-vascular dementia among men, in a prospective Dutch cohort study (Koeman et al., 2015).

Overall, findings from studies regarding the role of pesticides in cognitive performance and dementia remain contradictory. One of the methodological limitations in the current literature includes the focus on specific neuropsychological tests, or specific phenotypes, without covering a broad range of cognitive performance as expressed with measurements of major cognitive domains. Furthermore, there is limited data and awareness regarding the actual exposure of the Greek population to pesticides (Dardiotis et al., 2014; Tsolaki et al., 1999). Our group recently explored the frequency, types and attitudes towards the use of pesticides (Moza et al., 2019). In the present article, we present the results from an analysis regarding self-reported pesticide exposure in a Greek cohort, based on an ongoing epidemiological study the Hellenic Longitudinal Investigation of Aging and Diet (HELIAD) (Anastasiou et al., 2017; Dardiotis et al., 2014; Kosmidis et al., 2018; Ntanasi et al., 2018a, 2018b; Tsapanou et al., 2017a, 2017b).

Section snippets

Study population

Details regarding the study design have been extensively described previously (Anastasiou et al., 2017; Dardiotis et al., 2014; Kosmidis et al., 2018; Ntanasi et al., 2018a; Tsapanou et al., 2017a, 2017b). In brief, the participants’ recruitment began in 2011, for baseline assessment, and a three-year follow-up, is currently being conducted.

Participants were selected based on random sampling among a municipal roster of individuals over the age of 64 years. No weighting or further stratification

Main results

From eligible participants (excluding those who had incomplete data, who had relocated, could not actively be recruited, died or were not contacted yet from the initial sample), 56.4% agreed to participate in HELIAD. To date, a total of 1462 Thessaly inhabitants have completed the detailed risk factor questionnaires. A cohort of 1397 non-demented (1218 cognitively healthy individuals and 179 individuals with MCI) individuals was included in the present analyses.

Comparisons of participant

Discussion

In the present study, we evaluated a relatively large number of individuals and examined the relationship between the level of self-reported pesticide exposure and cognitive function. We found that non-demented individuals who reported that they had been living in areas near sprayed fields, had lower cognitive performance, compared to those who had never lived in such areas. Specifically, they had poorer performance in executive functioning, visuospatial perception, language and attention

Declaration of interest

Efthimios Dardiotis, Vasileios Siokas, Sotiria Moza, Mary H. Kosmidis, Christina Vogiatzi, Athina-Maria Aloizou, Nikoletta Geronikola, Eva Ntanasi, Ioannis Zalonis, Mary Yannakoulia, and Georgios M. Hadjigeorgiou declare that they have no conflict of interest. Nikolaos Scarmeas reports personal fees from Merck Consumer Health and personal fees from NIH unrelated to this manuscript.

Funding

This study was supported by the following grants:IIRG-09- 133014 from the Alzheimer's Association; 189 10276/8/9/2011 from the ESPA-EU program Excellence Grant (ARISTEIA), which is co-funded by the European Social Fund and Greek National resources, and ΔΥ2β/οικ.51657/14.4.2009 from the Ministry for Health and Social Solidarity (Greece).

References (63)

  • B. Maloney et al.

    Epigenetics of dementia: understanding the disease as a transformation rather than a state

    Lancet Neurol.

    (2016)
  • H. Niu

    Prevalence and incidence of Alzheimer's disease in Europe: a meta-analysis

    Neurologia

    (2017)
  • T. Parron

    Association between environmental exposure to pesticides and neurodegenerative diseases

    Toxicol. Appl. Pharmacol.

    (2011)
  • A.C. Povey

    Pesticide exposure and screen-positive neuropsychiatric disease in British sheep farmers

    Environ. Res.

    (2014)
  • D.S. Rohlman

    Neurobehavioral performance of adult and adolescent agricultural workers

    Neurotoxicology (Little Rock)

    (2007)
  • P. Scheltens

    Alzheimer's disease

    Lancet

    (2016)
  • A. Singh-Manoux

    Obesity trajectories and risk of dementia: 28 years of follow-up in the Whitehall II Study

    Alzheimers Dement

    (2018)
  • A. Tsapanou

    Sleep quality and duration in relation to memory in the elderly: initial results from the Hellenic longitudinal investigation of aging and diet

    Neurobiol. Learn. Mem.

    (2017)
  • A. Tsapanou

    Dataset on the associations between sleep quality/duration and cognitive performance in cognitively healthy older adults

    Data Brief

    (2017)
  • A.M. Tsatsakis

    Pesticide levels in head hair samples of Cretan population as an indicator of present and past exposure

    Forensic Sci. Int.

    (2008)
  • I. Zaganas

    Linking pesticide exposure and dementia: what is the evidence?

    Toxicology

    (2013)
  • AmericanPsychiatricAssociation

    Diagnostic and Statistical Manual of Mental Disorders

    (2000)
  • C.A. Anastasiou

    Mediterranean diet and cognitive health: initial results from the Hellenic longitudinal investigation of ageing and Diet

    PLoS One

    (2017)
  • I. Baldi

    Neurodegenerative diseases and exposure to pesticides in the elderly

    Am. J. Epidemiol.

    (2003)
  • I. Baldi

    Neurobehavioral effects of long-term exposure to pesticides: results from the 4-year follow-up of the PHYTONER study

    Occup. Environ. Med.

    (2011)
  • A.L. Benton

    Contributions to Neuropsychological Assessment: a Clinical Manual

    (1994)
  • A. Bougea

    Higher probability of prodromal Parkinson disease is related to lower cognitive performance

    Neurology

    (2019)
  • V.P. Bozikas

    Do age and education contribute to performance on the clock drawing test? Normative data for the Greek population

    J. Clin. Exp. Neuropsychol.

    (2008)
  • S. Cloutier

    Patterns of cognitive decline prior to dementia in persons with mild cognitive impairment

    J. Alzheimer's Dis.

    (2015)
  • E. Dardiotis

    The Hellenic Longitudinal Investigation of Aging and Diet (HELIAD): rationale, study design, and cohort description

    Neuroepidemiology

    (2014)
  • F.M. Elahi et al.

    A clinicopathological approach to the diagnosis of dementia

    Nat. Rev. Neurol.

    (2017)
  • Cited by (22)

    • Combined exposure to multiple metals and cognitive function in older adults

      2021, Ecotoxicology and Environmental Safety
      Citation Excerpt :

      It has been widely reported that age, education, sleep disturbances, less physical activity, and genetic disposition were among the determinants of cognitive function for older adults (Davies et al., 2016; Yaffe et al., 2014). Recently, there is increasing evidence suggesting that environmental exposures may have a detrimental effect on the cognitive function for older adults (Chen et al., 2021; Dardiotis et al., 2019; Petkus et al., 2021; Salinas-Rodríguez et al., 2018). Among the environmental chemicals exposed to humans, multiple metals play significant roles in the neuropathological changes for older adults.

    • Neurobehavioral anomalies in zebrafish after sequential exposures to DDT and chlorpyrifos in adulthood: Do multiple exposures interact?

      2021, Neurotoxicology and Teratology
      Citation Excerpt :

      Future studies may be able to use these fish to investigate what cell- and molecular-level changes may lead to changes in mood and behavior, and to verify that the apparent similarities in behavioral outcomes result from convergent mechanisms of persistent toxicity. By contrast, cognitive problems, particularly memory issues in older adults (Dardiotis et al., 2019; Kim et al., 2019), were not well modeled by the current battery. Rather than impairing place discrimination in the NPR task, insecticide exposures tended to enhance reactivity to the novel stimulus, specifically towards aversion for the CPF-exposed fish and generally for DDT-exposed fish.

    • Pesticides, cognitive functions and dementia: A review

      2020, Toxicology Letters
      Citation Excerpt :

      Crucially, the high-pesticide exposure group was found to perform worse than the pyridostigmine bromide exposure group on several cognitive tasks, with the worst level of performance being reported for the visual memory recall test (Sullivan et al., 2018). Finally, data from a population-based cohort study of older adults (HEllenic Longitudinal Investigation of Aging and Diet-HELIAD) in Greece, suggested that non-demented individuals who reported that they had been living in areas near sprayed fields, presented an overall poorer neuropsychological performance, particularly evident in language, executive and visual-spatial functioning, and attention (Dardiotis et al., 2019c). Table 1 presents an overview of the selected and included studies that have so far investigated the relationship between pesticide exposure and various cognitive functions in humans.

    View all citing articles on Scopus
    View full text