Human Oral Buccal Microbiomes Are Associated with Farmworker Status and Azinphos-Methyl Agricultural Pesticide Exposure

Abstract

In a longitudinal agricultural community cohort sampling of 65 adult farmworkers and 52 adult nonfarmworkers, we investigated agricultural pesticide exposure-associated changes in the oral buccal microbiota. We found a seasonally persistent association between the detected blood concentration of the insecticide azinphos-methyl and the taxonomic composition of the buccal swab oral microbiome. Blood and buccal samples were collected concurrently from individual subjects in two seasons, spring/summer 2005 and winter 2006. Mass spectrometry quantified blood concentrations of the organophosphate insecticide azinphosmethyl. Buccal oral microbiome samples were 16S rRNA gene DNA sequenced, assigned to the bacterial taxonomy, and analyzed after "centered-log-ratio" transformation to handle the compositional nature of the proportional abundances of bacteria per sample. Nonparametric analysis of the transformed microbiome data for individuals with and without azinphos-methyl blood detection showed significant perturbations in seven common bacterial taxa (Ͼ0.5% of sample mean read depth), including significant reductions in members of the common oral bacterial genus Streptococcus. Diversity in centered-log-ratio composition between individuals' microbiomes was also investigated using principal-component analysis (PCA) to reveal two primary PCA clusters of microbiome types. The spring/summer "exposed" microbiome cluster with significantly less bacterial diversity was enriched for farmworkers and contained 27 of the 30 individuals who also had azinphos-methyl agricultural pesticide exposure detected in the blood. IMPORTANCEIn this study, we show in human subjects that organophosphate pesticide exposure is associated with large-scale significant alterations of the oral buccal microbiota composition, with extinctions of whole taxa suggested in some individuals. The persistence of this association from the spring/summer to the winter also suggests that long-lasting effects on the commensal microbiota have occurred. The important health-related outcomes of these agricultural community individuals' pesticide-associated microbiome perturbations are not understood at this time. Future investigations should index medical and dental records for common and chronic diseases that may be interactively caused by this association between pesticide exposure and microbiome alteration.KEYWORDS farmworkers, azinphos-methyl, oral, microbiome, bacteria, buccal mucosa, 16S rRNA, sequencing

Characterizing the Neurodevelopmental Pesticide Exposome in a Children’s Agricultural Cohort

“…In particular, we focused on a timepoint prior to the AZM phase-out (2005) and near the end of the phase-out (2011) to assess how substitutions away from AZM affected the overall neurodevelopmental pesticide exposome. This approach of using pesticide levels in household dust as an indicator of child pesticide exposure is supported by dust correlations of urinary biomarkers and dust pesticide levels in previous work published on this cohort [28][29][30]. Furthermore, there is strong evidence that changes in the use of agricultural pesticides is reflected in the household dust of farmworker households [31].…”

Endocrine Disruptors in Food: Impact on Gut Microbiota and Metabolic Diseases

“…The results showed that workers exposed to azinfos-methyl had a decrease in common genera found in the human oral microbiome (Streptococcus, Micrococcineae, Gemella, Haemophilus, Halomonas, Actinomycineae, and Granulicatella). Although more studies are needed to confirm the results of Stanaway et al (2017) [84], the data obtained indicate that the oral microbiome could be used as a simple biomarker for assessing pesticide exposure in epidemiological studies.…”

“…Finally, an epidemiological study in humans carried out by Stanaway et al (2017) [84] found that exposure to agricultural pesticides can cause dysbiosis of the human oral microbiota. A cohort of 65 agricultural workers and 52 non-agricultural workers was studied.…”

Synthetic Pesticides Used in Agricultural Production Promote Genetic Instability and Metabolic Variability in Candida spp.

“…Pesticides comprise a wide range of chemicals of different classes used to ensure higher crop yields, but on the other hand, many adverse effects have been detected in animals and humans after acute or chronic exposure to pesticides, including cancer [ 1 , 2 ], lower fertility [ 3 , 4 ], metabolic changes [ 5 , 6 ] and changes in gastrointestinal microbiomes [ 7 , 8 ]. Symbiotic microorganisms play crucial roles in many important processes, such as vitamin synthesis [ 9 ], energy metabolism [ 10 ], neurodevelopment [ 11 ] and immune system modulation [ 12 ].…”