Ambient long-term exposure to organophosphorus pesticides and the human gut microbiome: an observational study

Keren Zhang; Kimberly Paul; Jonathan P Jacobs; Myles G Cockburn; Jeff M Bronstein; Irish Del Rosario; Beate Ritz

doi:10.1186/s12940-024-01078-y

Ambient long-term exposure to organophosphorus pesticides and the human gut microbiome: an observational study

Environ Health. 2024 Apr 16;23(1):41. doi: 10.1186/s12940-024-01078-y.

Authors

Keren Zhang¹, Kimberly Paul², Jonathan P Jacobs^{3

4}, Myles G Cockburn⁵, Jeff M Bronstein², Irish Del Rosario¹, Beate Ritz^{6

7}

Affiliations

¹ Department of Epidemiology, UCLA Fielding School of Public Health, Los Angeles, CA, USA.
² Department of Neurology, UCLA David Geffen School of Medicine, Los Angeles, CA, USA.
³ The Vatche and Tamar Manoukian Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.
⁴ Division of Gastroenterology, Hepatology and Parenteral Nutrition, VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA.
⁵ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁶ Department of Epidemiology, UCLA Fielding School of Public Health, Los Angeles, CA, USA. britz@ucla.edu.
⁷ Department of Environmental Health Sciences, UCLA Fielding School of Public Health, Los Angeles, CA, USA. britz@ucla.edu.

Abstract

Background: Organophosphorus pesticides (OP) have been associated with various human health conditions. Animal experiments and in-vitro models suggested that OP may also affect the gut microbiota. We examined associations between ambient chronic exposure to OP and gut microbial changes in humans.

Methods: We recruited 190 participants from a community-based epidemiologic study of Parkinson's disease living in a region known for heavy agricultural pesticide use in California. Of these, 61% of participants had Parkinson's disease and their mean age was 72 years. Microbiome and predicted metagenome data were generated by 16S rRNA gene sequencing of fecal samples. Ambient long-term OP exposures were assessed using pesticide application records combined with residential addresses in a geographic information system. We examined gut microbiome differences due to OP exposures, specifically differences in microbial diversity based on the Shannon index and Bray-Curtis dissimilarities, and differential taxa abundance and predicted Metacyc pathway expression relying on regression models and adjusting for potential confounders.

Results: OP exposure was not associated with alpha or beta diversity of the gut microbiome. However, the predicted metagenome was sparser and less evenly expressed among those highly exposed to OP (p = 0.04). Additionally, we found that the abundance of two bacterial families, 22 genera, and the predicted expression of 34 Metacyc pathways were associated with long-term OP exposure. These pathways included perturbed processes related to cellular respiration, increased biosynthesis and degradation of compounds related to bacterial wall structure, increased biosynthesis of RNA/DNA precursors, and decreased synthesis of Vitamin B1 and B6.

Conclusion: In support of previous animal studies and in-vitro findings, our results suggest that ambient chronic OP pesticide exposure alters gut microbiome composition and its predicted metabolism in humans.

Keywords: Geographic information system; Gut microbiome; Organophosphorus pesticides; Predicted metagenome.

Publication types

Observational Study

MeSH terms

Aged
Bacteria
Gastrointestinal Microbiome*
Humans
Microbiota*
Organophosphorus Compounds
Parkinson Disease*
Pesticides* / adverse effects
RNA, Ribosomal, 16S / genetics

Substances

Organophosphorus Compounds
Pesticides
RNA, Ribosomal, 16S

Abstract

Publication types

MeSH terms

Substances

Grants and funding