The Impact of Pesticide Residues on the Gut Microbiome and Human Health: A Food Safety Perspective
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The main aspects analysed are (1) effects of individual or combined pesticides on the composition, diversity and function of gut microbiome using in vivo or in vitro models; (2) health implications resulting from the pesticide-microbiome interactions and underlying mechanisms; (3) establishment of causality; and (4) influence of the gut microbiome on the metabolism and bioavailability of pesticides. The research was also scoped to identify current gaps, limitations and needs for the eventual consideration of microbiome-related data in chemical risk assessment.
With this work, ESF contributes to the FAO global programme on the impact of food systems on NCDs and obesity, by understanding the potential health implications of gut microbiome-pesticide interactions. The outcomes will provide information which can be used to improve nutritional strategies and food safety policies.
Food and Agriculture Organization of the United Nations
An intergovernmental organization, the Food and Agriculture Organization of the United Nations (FAO) has 194 Member Nations, two associate members and one member organization, the European Union. Its employees come from various cultural backgrounds and are experts in the multiple fields of activity FAO engages in. FAO’s staff capacity allows it to support improved governance inter alia, generate, develop and adapt existing tools and guidelines and provide targeted governance support as a resource to country and regional level FAO offices. Headquartered in Rome, Italy, FAO is present in over 130 countries.Founded in 1945, the Food and Agriculture Organization (FAO) leads international efforts to defeat hunger. Serving both developed and developing countries, FAO provides a neutral forum where all nations meet as equals to negotiate agreements and debate policy. The Organization publishes authoritative publications on agriculture, fisheries, forestry and nutrition.
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The Impact of Pesticide Residues on the Gut Microbiome and Human Health - Food and Agriculture Organization of the United Nations
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FAO. 2023. The impact of pesticide residues on the gut microbiome and human health – A food safety perspective. Food Safety and Quality Series, No. 19. Rome. https://doi.org/10.4060/cc5306en
The designations employed and the presentation of material in this information product do not imply the expression of any opinion whatsoever on the part of the Food and Agriculture Organization of the United Nations (FAO) concerning the legal or development status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of specific companies or products of manufacturers, whether or not these have been patented, does not imply that these have been endorsed or recommended by FAO in preference to others of a similar nature that are not mentioned.
ISSN 2415-1173 [Print]
ISSN 2664-5246 [Online]
ISBN 978-92-5-138312-4
© FAO, 2023
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Cover photographs [from left to right]:
© FAO/Michael Tewelde; © FAO/Alessandra Benedetti; © Bibbidistudio/Shutterstock.com
Design and layout: studio Pietro Bartoleschi
CONTENTS
Acknowledgements
Acronyms and abbreviations
Executive summary
CHAPTER 1
INTRODUCTION
CHAPTER 2
METHODOLOGY
Scientific literature research: search criteria and strategy
Screening of articles and selection criteria
Pesticide dose normalization related to the acceptable daily intake
CHAPTER 3
FINDINGS
Individual pesticides
2,4-dichlorophenoxyacetic acid (2,4-D)
Aldicarb
Carbendazim
Chlorpyrifos
Deltamethrin
Diazinon
Endosulfan
Epoxiconazole
Glyphosate
Imazalil
Malathion
Monocrotophos
Penconazole
Permethrin
Propamocarb
By-products
Pesticide mixture and multi-residue exposure
CHAPTER 4
DISCUSSION
Doses and exposure
Models
Study of the microbiome and microbiome host relationship - methods
Sampling
Analytical considerations
Pesticide mixture, pesticide formulations and co-exposure with other xenobiotics
CHAPTER 5
CHALLENGES
Relevance of alterations to the microbiome and host caused by pesticide exposure
Causality
Gut microbiome in pesticide risk assessment
CHAPTER 6
CONCLUSIONS
Recommendations
BIBLIOGRAPHY
ANNEX I
METHODOLOGY NOTES
ANNEX II
FINDINGS
ANNEX III
PESTICIDE CLASSIFICATION
FIGURES
1. Gastrointestinal environment and microbiota niches
2. Examples of taxonomical composition of the gut microbiota
3. Risk analysis process for the evaluation/re-evaluation of a pesticide
4. Graphic representation of the article selection process for literature review
5. Experimental pesticide doses used in the different studies relative to their corresponding ADI
TABLE
1. Manuscript coding
AI.1 Initial search query terms and results from PubMed, Web of Science and Scopus
AI.2 Search query terms and results for pesticide main use from PubMed, Web of Science and Scopus
AI.3 Search query terms and results for specific pesticides from PubMed and Web of Science
AI.4 Search query terms and results for pesticide mixtures from PubMed and Web of Science
AI.5 Search query terms and results for pesticide chemical types from PubMed and Web of Science
AII.1 Summary of experimental studies reporting the impact of 2,4-D on the gut microbiome and its effects on the host’s health
AII.2 Summary of experimental studies reporting the impact of aldicarb on the gut microbiome and its effects on the host’s health
AII.3 Summary of experimental studies reporting the impact of carbendazim on the gut microbiome and its effects on the host’s health
AII.4 Summary of experimental studies reporting the impact of chlorpyrifos on the gut microbiome and its effects on the host’s health
AII.5 Summary of experimental studies reporting the impact of deltamethrin on the gut microbiome and its effects on the host’s health
AII.6 Summary of experimental studies reporting the impact of diazinon on the gut microbiome and its effects on the host’s health
AII.7 Summary of experimental studies reporting the impact of endosulfan on the gut microbiome and its effects on the host’s health
AII.8 Summary of experimental studies reporting the impact of epoxiconazole on the gut microbiome and its effects on the host’s health
AII.9 Summary of experimental studies reporting the impact of glyphosate on the gut microbiome and its effects on the host’s health
AII.10 Summary of experimental studies reporting the impact of imazalil on the gut microbiome and its effects on the host’s health
AII.11 Summary of experimental studies reporting the impact of malathion on the gut microbiome and its effects on the host’s health
AII.12 Summary of experimental studies reporting the impact of monocrotophos on the gut microbiome and its effects on the host’s health
AII.13 Summary of experimental studies reporting the impact of penconazole on the gut microbiome and its effects on the host’s health
AII.14 Summary of experimental studies reporting the impact of permethrin on the gut microbiome and its effects on the host’s health
AII.15 Summary of experimental studies reporting the impact of propamocarb on the gut microbiome and its effects on the host’s health
AII.16 Summary of experimental studies reporting the impact of diethyl phosphate (non-specifc organophosphorus pestidide) on the gut microbiome and its effects on the host’s health
AII.17 Summary of experimental studies reporting the impact of pesticide metabolites or byproducts, p,p'-dichlorodiphenyldichloroethylene (p,p'-DDE) β-hexachlorocyclohexane (β-HCH) on the gut microbiome and its effects on the host’s health92
AII.18 Summary of experimental studies reporting the impact of pesticide mixtures on the gut microbiome and its effects on the host’s health 93
ACKNOWLEDGEMENTS
The research and drafting of the publication were carried out by Carmen Diaz-Amigo (Food Systems and Food Safety Division [ESF], FAO) and Sarah Najera Espinosa (ESF) under the technical leadership and guidance of Catherine Bessy, Senior Food Safety Officer (ESF).
The support and guidance of Markus Lipp, Senior Food Safety Officer (ESF), and the technical inputs and insights provided by Vittorio Fattori, Food Safety Officer (ESF), during the entire process of the publication’s development are gratefully recognized.
FAO is grateful to the expert Mark Feeley (Consultant, Canada) for his insightful comments and recommendations to improve the draft.
Finally, special thanks go out to Karel Callens Senior Advisor to Chief Economist, Governance and Policy Support Unit (DDCG, FAO) and Fanette Fontaine, Science Policy Advisor (DDCG), for their pioneer initiative at FAO bringing attention to and starting a dialogue on the impact of microbiomes in food systems.
ACRONYMS AND ABBREVIATIONS
EXECUTIVE SUMMARY
© IAEA/Louise