Login Register Cart 0
Generic placeholder image

Letters in Functional Foods

Editor-in-Chief

ISSN (Print): 2666-9390
ISSN (Online): 2666-9404

Back
Journal Home About Journal Editorial Board Current Issue Volumes/Issues
Subscribe
Review Article

Effects of Pesticides Carried by Foods on Human Gut Microbiota

Author(s): Lucía Varela Rodríguez, Aroa Lopez-Santamarina*, Alicia del Carmen Mondragón, Patricia Regal, Alexandre Lamas, Jose Antonio Rodriguez, José Manuel Miranda and Carlos Manuel Franco

Volume 1, 2024

Published on: 21 September, 2023

Article ID: e160523216967 Pages: 12

DOI: 10.2174/2666939001666230516140536

Price: $65

Abstract

The human gut microbiota is part of a delicate ecosystem that also involves the individual in which it is hosted and the environment. Humans and their gut microbiota depend on each other to maintain good health, but many external factors can contribute to the disruption of this balance and lead to diseases. Pesticides are a good example of environmental pollutants to which humans are exposed on a daily basis, mainly through diet. As a result, the composition and functionality of the gut microbiota can be compromised, as the gastrointestinal tract is the first physical and biological barrier with which they interact. Finally, through multiple and complex mechanisms, all this has repercussions on the health status of the host, and the adverse effects of this gut microbiota–pesticide interaction can manifest themselves in various ways, such as alteration of the diversity and abundance of the different bacteria, both beneficial and pathogenic, that colonize the gastrointestinal tract, metabolic and endocrine disorders, inflammation, dysregulation of the immune system and neurological disorders, among many others. Therefore, this work aims to summarize the latest scientific evidence on the effects of pesticides on the gut microbiota and the possible implications for human health as well as animal models and in vitro cultures on which the different tests are carried out.

[1]
Wold Health Organization. 2022. Available From: https://www.who.int/es/news-room/fact-sheets/detail/pesticide-residues-in-food
[2]
Yuan X, Pan Z, Jin C, Ni Y, Fu Z, Jin Y. Gut microbiota: An underestimated and unintended recipient for pesticide-induced toxicity. Chemosphere 2019; 227: 425-34.
[http://dx.doi.org/10.1016/j.chemosphere.2019.04.088] [PMID: 31003127]
[3]
ComisiónEuropeaFood Safety. Clorpirifos y Clorpirifos-metilo Available From: https://ec.europa.eu/food/plants/pesticides/approval-active-substances/renewal-approval/chlorpyrifos-chlorpyrifos-methyl_en [Accessed on: Mar 30th, 2022].
[4]
EFSA. Plaguicides. 2022. Available From: https://www.efsa.europa.eu/es/topics/topic/pesticides [Accessed on:April 3, 2022].
[5]
EFSA. Pesticides: Maximum residue limits. 2022. Available From: https://www.efsa.europa.eu/es/topics/topic/pesticides#l%C3%ADmites-m%C3%A1ximos-de-residuos [Accessed on: May 7, 2022].
[6]
EPA, United States Enviromental Protection Agency Basic information on pesticide ingredients. 2022. Available From: https://www.epa.gov/ingredients-used-pesticide-products/basic-information-about-pesticide-ingredients [Accessed on: May 7,2022].
[7]
CodexAlimentarius.Maximum Residue Limits for Pesticides: Glossary of Terms. 2022. Available From: https://www.fao.org/fao-who-codexalimentarius/codex-texts/dbs/pestres/glossary/es/#:~:text=El%20t%C3%A9rmino%20incluye%20las%20sustancias,proteger%20el%20producto%20 contra%20el [Accessed on: Mar 5, 2022].
[8]
Giambò F, Teodoro M, Costa C, Fenga C. Toxicology and microbiota: How do pesticides influence gut microbiota? A review. Int J Environ Res Public Health 2021; 18(11): 5510.
[http://dx.doi.org/10.3390/ijerph18115510] [PMID: 34063879]
[9]
Andreo-Martínez P, García-Martínez N, Sánchez-Samper EP. The intestinal microbiota and its relationship with mental illness through the microbiota-gut-brain axis. Journal of Disability, Clinic and Neurosciences 2017; 4(2): 52-8.
[http://dx.doi.org/10.14198/DCN.2017.4.2.05]
[10]
Roca-Saavedra P, Mendez-Vilabrille V, Miranda JM, et al. Food additives, contaminants and other minor components: Effects on human gut microbiota—a review. J Physiol Biochem 2018; 74(1): 69-83.
[http://dx.doi.org/10.1007/s13105-017-0564-2] [PMID: 28488210]
[11]
Sarron E, Pérot M, Barbezier N, Delayre-Orthez C, Gay-Quéheillard J, Anton PM. Early exposure to food contaminants reshapes matura-tion of the human brain-gut-microbiota axis. World J Gastroenterol 2020; 26(23): 3145-69.
[http://dx.doi.org/10.3748/wjg.v26.i23.3145] [PMID: 32684732]
[12]
Ghaisas S, Maher J, Kanthasamy A. Gut microbiome in health and disease: Linking the microbiome–gut–brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacol Ther 2016; 158: 52-62.
[http://dx.doi.org/10.1016/j.pharmthera.2015.11.012] [PMID: 26627987]
[13]
Jin Y, Wu S, Zeng Z, Fu Z. Effects of environmental pollutants on gut microbiota. Environ Pollut 2017; 222: 1-9.
[http://dx.doi.org/10.1016/j.envpol.2016.11.045] [PMID: 28086130]
[14]
Tu P, Chi L, Bodnar W, et al. Gut microbiome toxicity: Connecting the environment and gut microbiome-associated diseases. Toxics 2020; 8(1): 19.
[http://dx.doi.org/10.3390/toxics8010019] [PMID: 32178396]
[15]
Hampl R, Stárka L. Endocrine disruptors and gut microbiome interactions. Physiol Res 2020; 69 (Suppl. 2): S211-23.
[http://dx.doi.org/10.33549/physiolres.934513] [PMID: 33094620]
[16]
Rives C, Fougerat A, Ellero-Simatos S, et al. Oxidative stress in NAFLD: Role of nutrients and food contaminants. Biomolecules 2020; 10(12): 1702.
[http://dx.doi.org/10.3390/biom10121702] [PMID: 33371482]
[17]
Aguilera M, Gálvez-Ontiveros Y, Rivas A. Endobolome, a new concept for determining the influence of microbiota disrupting chemicals (MDC) in relation to specific endocrine pathogenesis. Front Microbiol 2020; 11: 578007.
[http://dx.doi.org/10.3389/fmicb.2020.578007] [PMID: 33329442]
[18]
Zhou M, Zhao J. A review on the health effects of pesticides based on host gut microbiome and metabolomics. Front Mol Biosci 2021; 8: 632955.
[http://dx.doi.org/10.3389/fmolb.2021.632955] [PMID: 33628766]
[19]
Barnett JA, Gibson DL. Separating the empirical wheat from the pseudoscientific chaff: A critical review of the literature surrounding glyphosate, dysbiosis and wheat-sensitivity. Front Microbiol 2020; 11: 556729.
[http://dx.doi.org/10.3389/fmicb.2020.556729] [PMID: 33101230]
[20]
Flandroy L, Poutahidis T, Berg G, et al. The impact of human activities and lifestyles on the interlinked microbiota and health of humans and of ecosystems. Sci Total Environ 2018; 627: 1018-38.
[http://dx.doi.org/10.1016/j.scitotenv.2018.01.288] [PMID: 29426121]
[21]
Abdelsalam NA, Ramadan AT, ElRakaiby MT, Aziz RK. Toxicomicrobiomics: The human microbiome vs. pharmaceutical, dietary, and environmental xenobiotics. Front Pharmacol 2020; 11: 390.
[http://dx.doi.org/10.3389/fphar.2020.00390] [PMID: 32372951]
[22]
Balaguer-Trias J, Deepika D, Schuhmacher M, Kumar V. Impact of contaminants on microbiota: Linking the gut–brain axis with neurotoxicity. Int J Environ Res Public Health 2022; 19(3): 1368.
[http://dx.doi.org/10.3390/ijerph19031368] [PMID: 35162390]
[23]
Rueda-Ruzafa L, Cruz F, Roman P, Cardona D. Gut microbiota and neurological effects of glyphosate. Neurotoxicology 2019; 75: 1-8.
[http://dx.doi.org/10.1016/j.neuro.2019.08.006] [PMID: 31442459]
[24]
Di Ciaula A, Baj J, Garruti G, et al. Liver steatosis, gut-liver axis, microbiome and environmental factors. A never-ending bidirectional cross-talk. J Clin Med 2020; 9(8): 2648.
[http://dx.doi.org/10.3390/jcm9082648] [PMID: 32823983]
[25]
Wang H, Yang F, Zhang S, Xin R, Sun Y. Genetic and environmental factors in Alzheimer’s and Parkinson’s diseases and promising therapeutic intervention via fecal microbiota transplantation. NPJ Parkinsons Dis 2021; 7(1): 70.
[http://dx.doi.org/10.1038/s41531-021-00213-7] [PMID: 34381040]
[26]
Koontz JM, Dancy BCR, Horton CL, Stallings JD, DiVito VT, Lewis JA. The role of the human microbiome in chemical toxicity. Int J Toxicol 2019; 38(4): 251-64.
[http://dx.doi.org/10.1177/1091581819849833] [PMID: 31220972]
[27]
Atashgahi S, Shetty SA, Smidt H, de Vos WM. Flux. Impact, and fate of halogenated xenobiotic compounds in the gut. Front Physiol 2018; 9: 888.
[http://dx.doi.org/10.3389/fphys.2018.00888] [PMID: 30042695]
[28]
Chiu K, Warner G, Nowak RA, Flaws JA, Mei W. The impact of environmental chemicals on the gut microbiome. Toxicol Sci 2020; 176(2): 253-84.
[http://dx.doi.org/10.1093/toxsci/kfaa065] [PMID: 32392306]
[29]
Gillois K, Lévêque M, Théodorou V, Robert H, Mercier-Bonin M. Mucus: An underestimated gut target for environmental pollutants and food additives. Microorganisms 2018; 6(2): 53.
[http://dx.doi.org/10.3390/microorganisms6020053] [PMID: 29914144]
[30]
Średnicka P, Juszczuk-Kubiak E, Wójcicki M, Akimowicz M, Roszko MŁ. Probiotics as a biological detoxification tool of food chemical contamination: A review. Food Chem Toxicol 2021; 153: 112306.
[http://dx.doi.org/10.1016/j.fct.2021.112306] [PMID: 34058235]
[31]
Giambò F, Costa C, Teodoro M, Fenga C. Role-playing between environmental pollutants and human Gut microbiota: A complex bidirectional interaction. Front Med (Lausanne) 2022; 9: 810397.
[http://dx.doi.org/10.3389/fmed.2022.810397] [PMID: 35252248]
[32]
Dempsey JL, Little M, Cui JY. Gut microbiome: An intermediary to neurotoxicity. Neurotoxicology 2019; 75: 41-69.
[http://dx.doi.org/10.1016/j.neuro.2019.08.005] [PMID: 31454513]
[33]
Huang R. Gut microbiota: A key regulator in the effects of environmental hazards on modulates insulin resistance. Front Cell Infect Microbiol 2022; 11: 800432.
[http://dx.doi.org/10.3389/fcimb.2021.800432] [PMID: 35111696]
[34]
Ramakrishnan B, Maddela NR, Venkateswarlu K, Megharaj M. Linkages between plant rhizosphere and animal gut environments: Interaction effects of pesticides with their microbiomes. Environ Adv 2021; 5: 100091.
[http://dx.doi.org/10.1016/j.envadv.2021.100091]
[35]
Velmurugan G, Ramprasath T, Gilles M, Swaminathan K, Ramasamy S. Gut microbiota, endocrine-disrupting chemicals, and the diabetes epidemic. Trends Endocrinol Metab 2017; 28(8): 612-25.
[http://dx.doi.org/10.1016/j.tem.2017.05.001] [PMID: 28571659]
[36]
Feng P, Ye Z, Kakade A, Virk A, Li X, Liu P. A review on gut remediation of selected environmental contaminants: Possible roles of probiotics and gut microbiota. Nutrients 2018; 11(1): 22.
[http://dx.doi.org/10.3390/nu11010022] [PMID: 30577661]
[37]
Ren XM, Kuo Y, Blumberg B. Agrochemicals and obesity. Mol Cell Endocrinol 2020; 515: 110926.
[http://dx.doi.org/10.1016/j.mce.2020.110926] [PMID: 32619583]
[38]
Tang Q, Tang J, Ren X, Li C. Glyphosate exposure induces inflammatory responses in the small intestine and alters gut microbial composition in rats. Environ Pollut 2020; 261: 114129.
[http://dx.doi.org/10.1016/j.envpol.2020.114129] [PMID: 32045792]
[39]
Luo T, Wang C, Pan Z, Jin C, Fu Z, Jin Y. Maternal polystyrene microplastic exposure during gestation and lactation altered metabolic homeostasis in the dams and their F1 and F2 offspring. Environ Sci Technol 2019; 53(18): 10978-92.
[http://dx.doi.org/10.1021/acs.est.9b03191] [PMID: 31448906]
[40]
Kalofiri P, Balias G, Tekos F. The EU endocrine disruptors’ regulation and the glyphosate controversy. Toxicol Rep 2021; 8: 1193-9.
[http://dx.doi.org/10.1016/j.toxrep.2021.05.013] [PMID: 34150528]
[41]
Nielsen LN, Roager HM, Casas ME, et al. Glyphosate has limited short-term effects on commensal bacterial community composition in the gut environment due to sufficient aromatic amino acid levels. Environ Pollut 2018; 233: 364-76.
[http://dx.doi.org/10.1016/j.envpol.2017.10.016] [PMID: 29096310]
[42]
Shehata AA, Schrödl W, Aldin AA, Hafez HM, Krüger M. The effect of glyphosate on potential pathogens and beneficial members of poultry microbiota in vitro. Curr Microbiol 2013; 66(4): 350-8.
[http://dx.doi.org/10.1007/s00284-012-0277-2] [PMID: 23224412]
[43]
Ackermann W, Coenen M, Schrödl W, Shehata AA, Krüger M. The influence of glyphosate on the microbiota and production of botulinum neurotoxin during ruminal fermentation. Curr Microbiol 2015; 70(3): 374-82.
[http://dx.doi.org/10.1007/s00284-014-0732-3] [PMID: 25407376]
[44]
Dechartres J, Pawluski JL, Gueguen MM, et al. Glyphosate and glyphosate‐based herbicide exposure during the peripartum period affects maternal brain plasticity, maternal behaviour and microbiome. J Neuroendocrinol 2019; 31(9): e12731.
[http://dx.doi.org/10.1111/jne.12731] [PMID: 31066122]
[45]
Caioni G, Cimini A, Benedetti E. Food contamination: An unexplored possible link between dietary habits and Parkinson’s disease. Nutrients 2022; 14(7): 1467.
[http://dx.doi.org/10.3390/nu14071467] [PMID: 35406080]
[46]
Kittle RP, McDermid KJ, Muehlstein L, Balazs GH. Effects of glyphosate herbicide on the gastrointestinal microflora of Hawaiian green turtles (Chelonia mydas) Linnaeus. Mar Pollut Bull 2018; 127: 170-4.
[http://dx.doi.org/10.1016/j.marpolbul.2017.11.030] [PMID: 29475651]
[47]
Aitbali Y, Ba-M’hamed S, Elhidar N, Nafis A, Soraa N, Bennis M. Glyphosate based- herbicide exposure affects gut microbiota, anxiety and depression-like behaviors in mice. Neurotoxicol Teratol 2018; 67: 44-9.
[http://dx.doi.org/10.1016/j.ntt.2018.04.002] [PMID: 29635013]
[48]
Lozano VL, Defarge N, Rocque LM, et al. Sex-dependent impact of Roundup on the rat gut microbiome. Toxicol Rep 2018; 5: 96-107.
[http://dx.doi.org/10.1016/j.toxrep.2017.12.005] [PMID: 29854581]
[49]
Mao Q, Manservisi F, Panzacchi S, et al. The Ramazzini Institute 13-week pilot study on glyphosate and Roundup administered at human-equivalent dose to Sprague Dawley rats: effects on the microbiome. Environ Health 2018; 17(1): 50.
[http://dx.doi.org/10.1186/s12940-018-0394-x] [PMID: 29843725]
[50]
Kan H, Zhao F, Zhang XX, Ren H, Gao S. Correlations of gut microbial community shift with hepatic damage and growth inhibition of carassius auratus induced by pentachlorophenol exposure. Environ Sci Technol 2015; 49(19): 11894-902.
[http://dx.doi.org/10.1021/acs.est.5b02990] [PMID: 26378342]
[51]
Réquilé M, Gonzàlez Alvarez DO, Delanaud S, et al. Use of a combination of in vitro models to investigate the impact of chlorpyrifos and inulin on the intestinal microbiota and the permeability of the intestinal mucosa. Environ Sci Pollut Res Int 2018; 25(23): 22529-40.
[http://dx.doi.org/10.1007/s11356-018-2332-4] [PMID: 29808406]
[52]
Reygner J, Joly Condette C, Bruneau A, et al. Changes in composition and function of human intestinal microbiota exposed to chlorpyrifos in oil as assessed by the SHIME(®) model. Int J Environ Res Public Health 2016; 13(11): 1088.
[http://dx.doi.org/10.3390/ijerph13111088] [PMID: 27827942]
[53]
Joly Condette C, Bach V, Mayeur C, Gay-Quéheillard J, Khorsi-Cauet H. Chlorpyrifos exposure during perinatal period affects intestinal microbiota associated with delay of maturation of digestive tract in rats. J Pediatr Gastroenterol Nutr 2015; 61(1): 30-40.
[http://dx.doi.org/10.1097/MPG.0000000000000734] [PMID: 25643018]
[54]
Liang Y, Zhan J, Liu D, et al. Organophosphorus pesticide chlorpyrifos intake promotes obesity and insulin resistance through impacting gut and gut microbiota. Microbiome 2019; 7(1): 19.
[http://dx.doi.org/10.1186/s40168-019-0635-4] [PMID: 30744700]
[55]
Li JW, Fang B, Pang GF, Zhang M, Ren FZ. Age- and diet-specific effects of chronic exposure to chlorpyrifos on hormones, inflammation and gut microbiota in rats. Pestic Biochem Physiol 2019; 159: 68-79.
[http://dx.doi.org/10.1016/j.pestbp.2019.05.018] [PMID: 31400786]
[56]
Zhao Y, Zhang Y, Wang G, Han R, Xie X. Effects of chlorpyrifos on the gut microbiome and urine metabolome in mouse (Mus musculus). Chemosphere 2016; 153: 287-93.
[http://dx.doi.org/10.1016/j.chemosphere.2016.03.055] [PMID: 27018521]
[57]
Fang B, Li JW, Zhang M, Ren FZ, Pang GF. Chronic chlorpyrifos exposure elicits diet-specific effects on metabolism and the gut microbiome in rats. Food Chem Toxicol 2018; 111: 144-52.
[http://dx.doi.org/10.1016/j.fct.2017.11.001] [PMID: 29109040]
[58]
Gao B, Bian X, Mahbub R, Lu K. Sex-specific effects of organophosphate diazinon on the gut microbiome and its metabolic functions. Environ Health Perspect 2017; 125(2): 198-206.
[http://dx.doi.org/10.1289/EHP202] [PMID: 27203275]
[59]
Zhan J, Liang Y, Liu D, et al. Pectin reduces environmental pollutant-induced obesity in mice through regulating gut microbiota: A case study of p,p′-DDE. Environ Int 2019; 130: 104861.
[http://dx.doi.org/10.1016/j.envint.2019.05.055] [PMID: 31195221]
[60]
Liang Y, Liu D, Zhan J, et al. New insight into the mechanism of POP-induced obesity: Evidence from DDE-altered microbiota. Chemosphere 2020; 244: 125123.
[http://dx.doi.org/10.1016/j.chemosphere.2019.125123] [PMID: 32050320]
[61]
Jin Y, Zeng Z, Wu Y, Zhang S, Fu Z. Oral exposure of mice to carbendazim induces hepatic lipid metabolism disorder and gut microbiota dysbiosis. Toxicol Sci 2015; 147(1): 116-26.
[http://dx.doi.org/10.1093/toxsci/kfv115] [PMID: 26071454]
[62]
Jin C, Zeng Z, Wang C, et al. Insights into a possible mechanism underlying the connection of carbendazim-induced lipid metabolism disorder and gut microbiota dysbiosis in mice. Toxicol Sci 2018; 166(2): 382-93.
[http://dx.doi.org/10.1093/toxsci/kfy205] [PMID: 30496565]
[63]
Jin C, Zeng Z, Fu Z, Jin Y. Oral imazalil exposure induces gut microbiota dysbiosis and colonic inflammation in mice. Chemosphere 2016; 160: 349-58.
[http://dx.doi.org/10.1016/j.chemosphere.2016.06.105] [PMID: 27393971]
[64]
Yan S, Tian S, Meng Z, et al. Synergistic effect of ZnO NPs and imidacloprid on liver injury in male ICR mice: Increase the bioavailability of IMI by targeting the gut microbiota. Environ Pollut 2022; 294: 118676.
[http://dx.doi.org/10.1016/j.envpol.2021.118676] [PMID: 34906595]
[65]
Wu S, Jin C, Wang Y, Fu Z, Jin Y. Exposure to the fungicide propamocarb causes gut microbiota dysbiosis and metabolic disorder in mice. Environ Pollut 2018; 237: 775-83.
[http://dx.doi.org/10.1016/j.envpol.2017.10.129] [PMID: 29137890]
[66]
Zhang R, Pan Z, Wang X, et al. Short-term propamocarb exposure induces hepatic metabolism disorder associated with gut microbiota dysbiosis in adult male zebrafish. Acta Biochim Biophys Sin (Shanghai) 2018; 51(1): 88-96.
[http://dx.doi.org/10.1093/abbs/gmy153] [PMID: 30544157]
[67]
Mumolo MG, Rettura F, Melissari S, et al. Is gluten the only culprit for nonceliac gluten/wheat sensitivity? Nutrients 2020; 12(12): 3785.
[http://dx.doi.org/10.3390/nu12123785] [PMID: 33321805]
[68]
Evariste L, Barret M, Mottier A, Mouchet F, Gauthier L, Pinelli E. Gut microbiota of aquatic organisms: A key endpoint for ecotoxicological studies. Environ Pollut 2019; 248: 989-99.
[http://dx.doi.org/10.1016/j.envpol.2019.02.101] [PMID: 31091643]
[69]
Silva MH. Chlorpyrifos and Δ9 Tetrahydrocannabinol exposure and effects on parameters associated with the endocannabinoid system and risk factors for obesity. Current Research in Toxicology 2021; 2: 296-308.
[http://dx.doi.org/10.1016/j.crtox.2021.08.002] [PMID: 34467221]
[70]
Mohajer N, Du CY, Checkcinco C, Blumberg B. Obesogens: How they are identified and molecular mechanisms underlying their action. Front Endocrinol (Lausanne) 2021; 12: 780888.
[http://dx.doi.org/10.3389/fendo.2021.780888] [PMID: 34899613]
[71]
Chen H, Ritz B. The search for environmental causes of Parkinson’s disease: Moving forward. J Parkinsons Dis 2018; 8(s1): S9-S17.
[http://dx.doi.org/10.3233/JPD-181493] [PMID: 30584168]
[72]
Muturi EJ, Dunlap C, Smartt CT, Shin D. Resistance to permethrin alters the gut microbiota of Aedes aegypti. Sci Rep 2021; 11(1): 14406.
[http://dx.doi.org/10.1038/s41598-021-93725-4] [PMID: 34257327]
[73]
Syromyatnikov MY, Isuwa MM, Savinkova OV, Derevshchikova MI, Popov VN. The effect of pesticides on the microbiome of animals. Agriculture 2020; 10(3): 79.
[http://dx.doi.org/10.3390/agriculture10030079]
[74]
Argou-Cardozo I, Zeidán-Chuliá F. Clostridium bacteria and autism spectrum conditions: A systematic review and hypothetical contribution of environmental glyphosate levels. Med Sci 2018; 6(2): 29.
[http://dx.doi.org/10.3390/medsci6020029] [PMID: 29617356]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy