Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins

Robin Mesnage; Ruth C.E. Bowyer; Souleiman El Balkhi; Franck Saint-Marcoux; Arnaud Gardere; Quinten Raymond Ducarmon; Anoecim Robecca Geelen; Romy Daniëlle Zwittink; Dimitris Tsoukalas; Evangelia Sarandi; Efstathia I. Paramera; Timothy Spector; Claire J. Steves; Michael N. Antoniou

doi:10.1186/s12940-022-00860-0

Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins

Robin Mesnage, Ruth C.E. Bowyer, Souleiman El Balkhi, Franck Saint-Marcoux, Arnaud Gardere, Quinten Raymond Ducarmon, Anoecim Robecca Geelen, Romy Daniëlle Zwittink, Dimitris Tsoukalas, Evangelia Sarandi, Efstathia I. Paramera, Timothy Spector, Claire J. Steves, Michael N. Antoniou^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

Abstract

Background: Dietary habits have a profound influence on the metabolic activity of gut microorganisms and their influence on health. Concerns have been raised as to whether the consumption of foodstuffs contaminated with pesticides can contribute to the development of chronic disease by affecting the gut microbiome. We performed the first pesticide biomonitoring survey of the British population, and subsequently used the results to perform the first pesticide association study on gut microbiome composition and function from the TwinsUK registry. Methods: Dietary exposure of 186 common insecticide, herbicide, or fungicide residues and the faecal microbiome in 65 twin pairs in the UK was investigated. We evaluated if dietary habits, geographic location, or the rural/urban environment, are associated with the excretion of pesticide residues. The composition and metabolic activity of faecal microbiota was evaluated using shotgun metagenomics and metabolomics respectively. We performed a targeted urine metabolomics analysis in order to evaluate whether pesticide urinary excretion was also associated with physiological changes. Results: Pyrethroid and/or organophosphorus insecticide residues were found in all urine samples, while the herbicide glyphosate was found in 53% of individuals. Food frequency questionnaires showed that residues from organophosphates were higher with increased consumption of fruit and vegetables. A total of 34 associations between pesticide residue concentrations and faecal metabolite concentrations were detected. Glyphosate excretion was positively associated with an overall increased bacterial species richness, as well as to fatty acid metabolites and phosphate levels. The insecticide metabolite Br2CA, reflecting deltamethrin exposure, was positively associated with the phytoestrogens enterodiol and enterolactone, and negatively associated with some N-methyl amino acids. Urine metabolomics performed on a subset of samples did not reveal associations with the excretion of pesticide residues. Conclusions: The consumption of conventionally grown fruit and vegetables leads to higher ingestion of pesticides with unknown long-term health consequences. Our results highlight the need for future dietary intervention studies to understand effects of pesticide exposure on the gut microbiome and possible health consequences.

Original language	English
Article number	46
Journal	Environmental Health: A Global Access Science Source
Volume	21
Issue number	1
DOIs	https://doi.org/10.1186/s12940-022-00860-0
Publication status	Published - Dec 2022

Keywords

Biomonitoring
Dietary habits
Food intake
Gut microbiota
Pesticides

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1186/s12940-022-00860-0

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Mesnage, R., Bowyer, R. C. E., El Balkhi, S., Saint-Marcoux, F., Gardere, A., Ducarmon, Q. R., Geelen, A. R., Zwittink, R. D., Tsoukalas, D., Sarandi, E., Paramera, E. I., Spector, T., Steves, C. J., & Antoniou, M. N. (2022). Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins. Environmental Health: A Global Access Science Source, 21(1), [46]. https://doi.org/10.1186/s12940-022-00860-0

@article{67d5dcf4147e46b1903dea103bede955,

title = "Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins",

abstract = "Background: Dietary habits have a profound influence on the metabolic activity of gut microorganisms and their influence on health. Concerns have been raised as to whether the consumption of foodstuffs contaminated with pesticides can contribute to the development of chronic disease by affecting the gut microbiome. We performed the first pesticide biomonitoring survey of the British population, and subsequently used the results to perform the first pesticide association study on gut microbiome composition and function from the TwinsUK registry. Methods: Dietary exposure of 186 common insecticide, herbicide, or fungicide residues and the faecal microbiome in 65 twin pairs in the UK was investigated. We evaluated if dietary habits, geographic location, or the rural/urban environment, are associated with the excretion of pesticide residues. The composition and metabolic activity of faecal microbiota was evaluated using shotgun metagenomics and metabolomics respectively. We performed a targeted urine metabolomics analysis in order to evaluate whether pesticide urinary excretion was also associated with physiological changes. Results: Pyrethroid and/or organophosphorus insecticide residues were found in all urine samples, while the herbicide glyphosate was found in 53% of individuals. Food frequency questionnaires showed that residues from organophosphates were higher with increased consumption of fruit and vegetables. A total of 34 associations between pesticide residue concentrations and faecal metabolite concentrations were detected. Glyphosate excretion was positively associated with an overall increased bacterial species richness, as well as to fatty acid metabolites and phosphate levels. The insecticide metabolite Br2CA, reflecting deltamethrin exposure, was positively associated with the phytoestrogens enterodiol and enterolactone, and negatively associated with some N-methyl amino acids. Urine metabolomics performed on a subset of samples did not reveal associations with the excretion of pesticide residues. Conclusions: The consumption of conventionally grown fruit and vegetables leads to higher ingestion of pesticides with unknown long-term health consequences. Our results highlight the need for future dietary intervention studies to understand effects of pesticide exposure on the gut microbiome and possible health consequences.",

keywords = "Biomonitoring, Dietary habits, Food intake, Gut microbiota, Pesticides",

author = "Robin Mesnage and Bowyer, {Ruth C.E.} and {El Balkhi}, Souleiman and Franck Saint-Marcoux and Arnaud Gardere and Ducarmon, {Quinten Raymond} and Geelen, {Anoecim Robecca} and Zwittink, {Romy Dani{\"e}lle} and Dimitris Tsoukalas and Evangelia Sarandi and Paramera, {Efstathia I.} and Timothy Spector and Steves, {Claire J.} and Antoniou, {Michael N.}",

note = "Funding Information: This work was funded by the Sustainable Food Alliance (USA) whose support is gratefully acknowledged. The code used for this analysis is available from the corresponding author on request. Computational analyses were performed using MetaPhlAn v.3.0.14 (https://github.com/biobakery/MetaPhlAn). Functional potential profiling was carried out with HUMAnN v.2.0 (https://github.com/biobakery/humann). Funding Information: This work was funded by the Sustainable Food Alliance (USA) whose support is gratefully acknowledged. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s12940-022-00860-0",

language = "English",

volume = "21",

journal = "Environmental Health",

issn = "1476-069X",

publisher = "BioMed Central",

number = "1",

}

Mesnage, R , Bowyer, RCE, El Balkhi, S, Saint-Marcoux, F, Gardere, A, Ducarmon, QR, Geelen, AR, Zwittink, RD, Tsoukalas, D, Sarandi, E, Paramera, EI, Spector, T, Steves, CJ & Antoniou, MN 2022, 'Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins', Environmental Health: A Global Access Science Source, vol. 21, no. 1, 46. https://doi.org/10.1186/s12940-022-00860-0

TY - JOUR

T1 - Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins

AU - Mesnage, Robin

AU - Bowyer, Ruth C.E.

AU - El Balkhi, Souleiman

AU - Saint-Marcoux, Franck

AU - Gardere, Arnaud

AU - Ducarmon, Quinten Raymond

AU - Geelen, Anoecim Robecca

AU - Zwittink, Romy Daniëlle

AU - Tsoukalas, Dimitris

AU - Sarandi, Evangelia

AU - Paramera, Efstathia I.

AU - Spector, Timothy

AU - Steves, Claire J.

AU - Antoniou, Michael N.

N1 - Funding Information: This work was funded by the Sustainable Food Alliance (USA) whose support is gratefully acknowledged. The code used for this analysis is available from the corresponding author on request. Computational analyses were performed using MetaPhlAn v.3.0.14 (https://github.com/biobakery/MetaPhlAn). Functional potential profiling was carried out with HUMAnN v.2.0 (https://github.com/biobakery/humann). Funding Information: This work was funded by the Sustainable Food Alliance (USA) whose support is gratefully acknowledged. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Background: Dietary habits have a profound influence on the metabolic activity of gut microorganisms and their influence on health. Concerns have been raised as to whether the consumption of foodstuffs contaminated with pesticides can contribute to the development of chronic disease by affecting the gut microbiome. We performed the first pesticide biomonitoring survey of the British population, and subsequently used the results to perform the first pesticide association study on gut microbiome composition and function from the TwinsUK registry. Methods: Dietary exposure of 186 common insecticide, herbicide, or fungicide residues and the faecal microbiome in 65 twin pairs in the UK was investigated. We evaluated if dietary habits, geographic location, or the rural/urban environment, are associated with the excretion of pesticide residues. The composition and metabolic activity of faecal microbiota was evaluated using shotgun metagenomics and metabolomics respectively. We performed a targeted urine metabolomics analysis in order to evaluate whether pesticide urinary excretion was also associated with physiological changes. Results: Pyrethroid and/or organophosphorus insecticide residues were found in all urine samples, while the herbicide glyphosate was found in 53% of individuals. Food frequency questionnaires showed that residues from organophosphates were higher with increased consumption of fruit and vegetables. A total of 34 associations between pesticide residue concentrations and faecal metabolite concentrations were detected. Glyphosate excretion was positively associated with an overall increased bacterial species richness, as well as to fatty acid metabolites and phosphate levels. The insecticide metabolite Br2CA, reflecting deltamethrin exposure, was positively associated with the phytoestrogens enterodiol and enterolactone, and negatively associated with some N-methyl amino acids. Urine metabolomics performed on a subset of samples did not reveal associations with the excretion of pesticide residues. Conclusions: The consumption of conventionally grown fruit and vegetables leads to higher ingestion of pesticides with unknown long-term health consequences. Our results highlight the need for future dietary intervention studies to understand effects of pesticide exposure on the gut microbiome and possible health consequences.

AB - Background: Dietary habits have a profound influence on the metabolic activity of gut microorganisms and their influence on health. Concerns have been raised as to whether the consumption of foodstuffs contaminated with pesticides can contribute to the development of chronic disease by affecting the gut microbiome. We performed the first pesticide biomonitoring survey of the British population, and subsequently used the results to perform the first pesticide association study on gut microbiome composition and function from the TwinsUK registry. Methods: Dietary exposure of 186 common insecticide, herbicide, or fungicide residues and the faecal microbiome in 65 twin pairs in the UK was investigated. We evaluated if dietary habits, geographic location, or the rural/urban environment, are associated with the excretion of pesticide residues. The composition and metabolic activity of faecal microbiota was evaluated using shotgun metagenomics and metabolomics respectively. We performed a targeted urine metabolomics analysis in order to evaluate whether pesticide urinary excretion was also associated with physiological changes. Results: Pyrethroid and/or organophosphorus insecticide residues were found in all urine samples, while the herbicide glyphosate was found in 53% of individuals. Food frequency questionnaires showed that residues from organophosphates were higher with increased consumption of fruit and vegetables. A total of 34 associations between pesticide residue concentrations and faecal metabolite concentrations were detected. Glyphosate excretion was positively associated with an overall increased bacterial species richness, as well as to fatty acid metabolites and phosphate levels. The insecticide metabolite Br2CA, reflecting deltamethrin exposure, was positively associated with the phytoestrogens enterodiol and enterolactone, and negatively associated with some N-methyl amino acids. Urine metabolomics performed on a subset of samples did not reveal associations with the excretion of pesticide residues. Conclusions: The consumption of conventionally grown fruit and vegetables leads to higher ingestion of pesticides with unknown long-term health consequences. Our results highlight the need for future dietary intervention studies to understand effects of pesticide exposure on the gut microbiome and possible health consequences.

KW - Biomonitoring

KW - Dietary habits

KW - Food intake

KW - Gut microbiota

KW - Pesticides

UR - http://www.scopus.com/inward/record.url?scp=85129445971&partnerID=8YFLogxK

U2 - 10.1186/s12940-022-00860-0

DO - 10.1186/s12940-022-00860-0

M3 - Article

C2 - 35501856

AN - SCOPUS:85129445971

SN - 1476-069X

VL - 21

JO - Environmental Health

JF - Environmental Health

IS - 1

M1 - 46

ER -

Impacts of dietary exposure to pesticides on faecal microbiome metabolism in adult twins

Abstract

Keywords

UN SDGs

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