Next Article in Journal
Membrane Hormone Receptors and Their Signaling Pathways as Targets for Endocrine Disruptors
Previous Article in Journal
Publisher’s Note: We Changed Page Numbers to Article Numbers for Articles Published in Journal of Xenobiotics Volumes 1–9
Previous Article in Special Issue
Photodegradation of Flucetosulfuron, a Sulfonylurea-Based Herbicide in the Aqueous Media Is Influenced by Ultraviolet Irradiation
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Perspective

Impact of Cumulative Environmental and Dietary Xenobiotics on Human Microbiota: Risk Assessment for One Health

by
Pilar Ortiz
1,2,
Alfonso Torres-Sánchez
1,2,
Ana López-Moreno
1,2,3,
Klara Cerk
1,2,†,
Ángel Ruiz-Moreno
1,2,
Mercedes Monteoliva-Sánchez
1,2,
Antonis Ampatzoglou
1,2,†,
Margarita Aguilera
1,2,3,*,‡ and
Agnieszka Gruszecka-Kosowska
1,2,4,*,‡
1
Department of Microbiology, Faculty of Pharmacy, University of Granada, Campus of Cartuja, 18071 Granada, Spain
2
Institute of Nutrition and Food Technology “José Mataix” (UGR-INYTA), Centre of Biomedical Research, University of Granada, 18016 Granada, Spain
3
IBS (Instituto de Investigación Biosanitaria ibs.), 18012 Granada, Spain
4
Department of Environmental Protection, Faculty of Geology, Geophysics and Environmental Protection, AGH University of Science and Technology, Al. Mickiewicza 30, 30-059 Krakow, Poland
*
Authors to whom correspondence should be addressed.
EU-FORA Fellowship Programme hosted at UGR-INYTA.
These authors contributed equally to this work.
J. Xenobiot. 2022, 12(1), 56-63; https://doi.org/10.3390/jox12010006
Submission received: 20 December 2021 / Revised: 3 March 2022 / Accepted: 10 March 2022 / Published: 17 March 2022

Abstract

:
Chemical risk assessment in the context of the risk analysis framework was initially designed to evaluate the impact of hazardous substances or xenobiotics on human health. As the need of multiple stressors assessment was revealed to be more reliable regarding the occurrence and severity of the adverse effects in the exposed organisms, the cumulative risk assessment started to be the recommended approach. As toxicant mixtures and their “cocktail effects” are considered to be main hazards, the most important exposure for these xenobiotics would be of dietary and environmental origin. In fact, even a more holistic prism should currently be considered. In this sense, the definition of One Health refers to simultaneous actions for improving human, animal, and environmental health through transdisciplinary cooperation. Global policies necessitate going beyond the classical risk assessment for guaranteeing human health through actions and implementation of the One Health approach. In this context, a new perspective is proposed for the integration of microbiome biomarkers and next generation probiotics potentially impacting and modulating not only human health, but plant, animal health, and the environment.

1. Introduction

Ongoing pollution due to anthropogenic activities poses a significant threat to the environment and health of its inhabitants. Until recently, human health was the primary focus of risk assessment in the context of the risk analysis framework. However, international policies [1] are starting to reflect research results revealing that humans are not a separate but an integral cog in the complex machine of the Earth’s ecosystem. Since the interdependencies between human, animal and plant health and the environment were realised, health started to be regarded through the prism of an integrated approach that is being called One Health. The definition of One Health refers to the holistic approach for simultaneously improving human, animal, and environmental health through transdisciplinary cooperation [2]. In this context, the human gut microbiome can be also considered as an important element of the next generation risk assessment in support of this One Health approach (Figure 1).
Anthropogenic activities, such as industrial processes, urbanization, waste disposal, agriculture, breeding, etc., introduce directly to the ecosystem various compounds, with the important common feature of being foreign to the biological system, and, as such, may cause unprecedented adverse effects in the ecosystem. These foreign to the body or the biological system substances are referred as xenobiotics [3]. Currently, the most investigated groups of xenobiotics, i.e., pesticides, preservatives, plasticizers, personal care products, dyes, and pigments, have been found in the following products: plant control constituents, drugs, pesticides, cosmetics, flavourings, fragrances, food additives, industrial chemicals, and environmental pollutants [4]. On the other hand, these contaminants may also enter the ecosystem indirectly due to instability of the environment caused by environmental degradation (such as deforestation) and climate change. Moreover, these xenobiotics do not always remain in the same chemical form but can be transformed during chemical, physical, and biological processes [5].
Xenobiotic dietary exposure is a global health concern nowadays. As dietary intake is the most important exposure pathway related to the xenobiotic intake, the quality and quantity of food consumed is of particular interest among the research community.
Xenobiotics may alter the microbiota composition, leading to a state of dysbiosis, which is linked to multiple diseases and adverse health outcomes, including increased toxicity of some xenobiotics. Toxicomicrobiomics studied the mutual influences and alterations between the ever-changing microbiome cloud and xenobiotics of various origins, with emphasis on their fate and toxicity [6,7]. These bidirectional interactions could be diverse: (1) Individual gut microbiome (human/animals) might be negatively affected by several contaminants or xenobiotics with pathophysiologic impact through triggering microbial composition disequilibrium; (2) Gut microbiota could protect against the carcinogenic and genotoxic substances by degrading or biotransforming them to less toxic compounds or facilitating their excretion; (3) Gut microbiota may also detoxify xenobiotics, for example, into genotoxins, or may reverse the detoxification implied by host metabolism; (4) Gut microbiota is capable of transforming xenobiotics towards lower toxic and mutagenic substances, thus it may be able to lessen the chances of dysbiosis effects.
However, dietary contaminants and hazardous substances present in environmental compartments may also significantly affect human health. Remarkably, regarding xenobiotic metabolism, participation of human gut microbiota might mediate long term physiological impact, affecting the balance between eubiosis and dysbiosis. However, to understand the key mechanisms a multidisciplinary approach is needed. Xenobiotics that alter the gut microbial composition and metabolism is categorized into a subgroup termed “microbiota disrupting chemicals” (MDCs) [8]. These MDCs might have the ability to promote changes in the microbiota that have been associated with intestinal, hormonal, and chronic or long-term systemic diseases in the host.
A collection of MDCs and their effects on the microbiota has widely explained by several authors: bisphenol [9,10]; phthalates, such as diethylhexylphthalate [11,12]; heavy metals. Many heavy metals have shown disrupting properties, and human exposure occurs through diet and water, inhalation of polluted air, smoking, and dermal absorption [13,14,15]. Triclosan and parabens: Triclosan is a well-known preservative [16]. Parabens are widely used as preservatives in cosmetics, personal care products, drugs, and foods [17]. Polybrominated diphenyl ethers (PBDEs) are environmentally persistent chemicals widely used as flame retardants [18] that have been shown to alter microbiota [19]. Pesticides have been shown to have important implications for environmental, animal, and human health [20]. Glyphosate and chlorpyrifos exposure occur mainly through diet and drinking water [21]. They have been reported to interfere with gut microbial communities and enteroendocrine cells [22,23]. Diazinon, an organophosphate pesticide with estrogenic activity [24], has shown to alter the structure of the gut microbiome community, functional metagenome, and associated metabolic profiles in a sex-related manner in murine models [25]. Organochlorine pesticides with endocrine disrupting capacity have also been associated with alterations in gut microbiota [26,27]. Antibiotics are also MDCs of concern, especially because of their contribution to antimicrobial resistance, a critical One Health issue [28]. Directly and indirectly (e.g., via reducing short-chain fatty acid production), they can have profound short and long-term negative effects on the gut microbiome, including altering its composition and opening a niche for pathogens [29]. Additionally, due to ingestion exposure to antibiotic-resistant microorganisms and given its high microbial density, the gut microbiome is emerging as a reservoir for antibiotic resistance genes and their horizontal transfer to commensals and, importantly, pathogens [30,31].
The cumulative exposure to xenobiotics and overall outcome could hugely impact health research. Therefore, interaction among distinct scientific disciplines as microbiology, nutrition, toxicology, environmental protection, and both personalised medicine and nutrition are needed. Moreover, multiple technologies, communities and professional domains should converge in order to obtain relevant outcomes. Research in risk assessment, including microbiota, metabolome, and omics technologies, favours new progress to evaluate the factors and substances that affect human health. Studies employing holistic analysis of human microbiota as metabolic node for health impact is the first step of this perspective goal.
The main objective of this work is to pay attention to the upmost scientific information about the interaction between the human microbiota and exposure to xenobiotics in the diet and environment.

2. Key Challenges of Gut Microbial Metabolism Research

Regarding the implementation of current EU policies, emissions of hazardous substances should be limited and controlled [32]. However, even so, xenobiotics already present in the environment cause a major problem, as demonstrated by the fact that even extensive human biomonitoring studies do not approach, adequately, the real body burden scenario [33]. Xenobiotics can be found everywhere in daily life, from food, cosmetics, and homecare products to prescription and over-the-counter drugs, gasoline, alcoholic beverages, and paper receipts. Thus, preventing long-term exposure to these harmful substances and mitigating their impacts become health and environmental priorities.
Interestingly, despite food being the source of energy and nutrients for the human body to grow, develop, and perform everyday activities, it may also contain xenobiotic substances. The rising of the global population results in higher food demand and consequently necessitates incremental increases in food resources [34]. Developed countries have incorporated much more processed foods and artificial products into the diet of their populations to keep up with the rapid pace of modern lifestyles. Cumulative exposure to contaminants and the physiological impact and mechanisms are poorly investigated [35]. Importantly, long-term exposure contributes to host gut microbiome dysbiosis [36], which previously had only been associated with changes in diet or antibiotic use [37,38]. Moreover, dysbiosis associated with xenobiotic exposure varies from person to person, depends on life stage and, overall, appears to be a strongly personalised effect [39].
As xenobiotic mixtures are increasingly ubiquitous in the environment nowadays [40], the question of how much the environment is polluted does not suffice anymore. The key question raised recently by the research community as well as by key environmental and health authorities, organisations, and agencies, such as EFSA, WHO, EEA, USEPA, etc., is what adverse health effects are caused by everyday contact with xenobiotics. In this context, the risk assessment consists of four crucial parts. The first step is hazard identification, followed by exposure assessment, hazard characterisation, and, finally, risk characterization (Figure 1). Regarding xenobiotics, the following challenges can be observed. Firstly, exact concentrations of defined xenobiotics are needed for reliable risk assessment. It means that specific xenobiotics entering the body via ingestion of food and via other exposure routes (e.g., inhalation or skin contact) facilitated by environmental pollution must be identified and their concentrations in foods/environment be elucidated. Secondly, xenobiotics may not remain in the same chemical form, but they may be transformed in other chemicals less or more toxic comparing with the parent compound. Moreover, the total concentration of xenobiotics does not always raise concerns, as only the bio-accessible proportions are responsible for adverse health effects. Additionally, the bio-accessibility of each xenobiotic is regulated by complex ADME processes (absorption, distribution, metabolism, excretion) taking place in living organisms.
Xenobiotic ADME processes involve genes, enzymes, and pathways not only of human origin, but also from the human microbiota, which has started to be investigated thoroughly in latest years. The current knowledge has shown that innovative microbiota biocomponents and functional analyses could contribute to increase the metabolites, analytes and enzymatic repertoire beyond the microbial taxonomic principal components analyses that were widely used in studies of the microbiome and toxicant exposures [41]. Recent research advancements have focused on molecular data for involving microbiome biomarkers in the prevention of diseases and dysfunctions triggered by xenobiotic exposures [42,43]. Integrative omics data and technologies [44,45] became essential tools for determining the holistic impact of microbiome on health-diseases balance (Figure 1). These findings strengthen the rationale for using a homologous model for toxicology. To study effects of exposures on the human microbiome in vitro systems may be preferable [46]. Moreover, the microbiome seems be particularly sensitive to xenobiotic influence during key life stages [47].
Personalized nutrition treatments based on next generation probiotics able to detoxify xenobiotics is envisaged as closing the circle of promoting the One Health approach [48]. Moreover, beneficial microbes isolated from the human gut microbiota could be further proposed for being used as plant probiotics, animal probiotics, and, even for bioremediation, having a potential positive modulation capacity in the context of One Health. The results of specific microbiota metabolizing particular xenobiotics and especially those used in bioremediation should be accompanied in parallel by environmental biosafety assessments [49].
Accordingly, as there is a strong drive-in international policy for next generation (non-animal) testing methods the human gut microbiota may become a plausible substitute to anticipate assessments and avoiding animal testing, when possible [50]. Specific consortia of human gut microbiota might be used in research studies to define the related ADME processes in cellular, organ-on-a-chip or organoids models [51] for analysing the fate of xenobiotics and inducting the effects in health and environment, such as for BPA biodegradation [52]. This contrasts with toxicological studies on animals, which are commonly used for environmental risk assessments performed up to now. Thus, the human gut microbiota approach seems to more relevant as results from traditional toxicology tests are performed on animals and in terms of acute exposure (short time, high doses) and, thus, must be extrapolated from animals to humans, as well as from high to low doses and long-term exposure that is specific for environmental exposure. Additionally, research determining the individual exposure levels of the human population depending on the composition of the intestinal microbiota may be performed as differences among individuals in the population are observed. The interindividual variations can be related to dietary habits, level of pollution, and ethnical and geographical differences [53].
According to Humboldt-Dachroeden et al. [54], One Health approach has the potential to become a comprehensive research field, however up to now environmental perspective of this approach is stunted in comparison for instance with epidemiological, microbiological, or public health perspectives. Environmental issues have gained even greater interest in terms of climate change and related adverse effects. Climate change disturbs the ecological and environmental integrity of living systems by causing lifecycle changes that at the end adversely affect among others food security and food safety, as well as related responses at local, regional, and global level [55]. In accordance with food security and food safety, European Union has launched the Farm to Fork Strategy, being the central part of the European Green Deal, for making food systems fair, healthy, and environmentally friendly, in one word—sustainable [56]. Food production is inseparably related with soil, thus in accordance with Green Deal Targets, European Commission has launched Mission Soils for achieving soil relevant targets in the perspective of 2030. Among Mission Soils’ targets related with the related with the One Health are following: reducing overall use and risk of chemical pesticides by 50%, reduce fertilizer us by at least 20%, reduce nutrient loses by at least 50%, reduce microplastic release into the environment by 30%, reduce the greenhouse gas emissions by at least 55% compared to 1990 levels, and 25% of organic farming land use [57]. Thus, considering above clauses, the perspective and priority in the scientific research should be better focused on xenobiotics that influence the greatest the food safety and security such as plant protection products, i.e., pesticides, food contact materials, i.e., plasticizers such as BPA and analogues, phthalates, and heavy metals circulating in the food chain.

3. Conclusions

Global policies necessitate going beyond the traditional methodologies towards cumulative risk assessment implementations for guarantying the human health through integrative actions and implementation of the One Health approach. What is more, the One Health approach has already been incorporated in the education of future consumers, assessors, managers, and scientists, and it is a key driving force in organising access to transdisciplinary science through international partnerships, joint research projects, and global conferences and social channel communications. In this sense, there is already a body of knowledge and scientific evidence to support the key role of microbiome biomarkers and its derived bioresources for contributing to modulate and intervene for improving global health. In the context of environmental health, soil is the first link-chain in the food production cycle, and afterward has a great impact on human and animal health. Thus, there is the necessity to link the environmental and microbiological research related with xenobiotics in the food chain.

Author Contributions

Conceptualization, M.A. and A.G.-K.; validation, All Authors; formal analysis, A.G.-K.; investigation, P.O., A.T.-S., A.L.-M. and Á.R.-M.; resources, M.A.; data curation, A.A. and K.C.; writing—original draft preparation, A.G.-K.; writing—review and editing, A.G.-K., M.A. and A.A.; visualization, All authors; supervision, M.M.-S.; project administration, M.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. The APC was funded by authors’ voucher.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

EU-FORA Programme (Cycle 2020/2021 and 2021/2022). This work was carried out within the frame of FEDER-Microbiota Infrastructure: IE_2019-198. OBEMIRISK EFSA-Partnering Grant GP/EFSA/ENCO/2018/03-GA04. Framework/Authors belong to and BIO190 Group and Plan Propio (University of Granada).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bronzwaer, S.; Geervliet, M.; Hugas, M.; Url, B. EFSA’s Expertise Supports One Health Policy Needs. EFSA J. 2021, 19, e190501. [Google Scholar] [CrossRef] [PubMed]
  2. Buschhardt, T.; Günther, T.; Skjerdal, T.; Torpdahl, M.; Gethmann, J.; Filippitzi, M.-E.; Maassen, C.; Jore, S.; Ellis-Iversen, J.; Filter, M. A One Health Glossary to Support Communication and Information Exchange between the Human Health, Animal Health and Food Safety Sectors. One Health 2021, 13, 100263. [Google Scholar] [CrossRef] [PubMed]
  3. Ramaka, S.; Srinivas, R.; Vasudeva, M.S.; Raghuram Rao, A. Xenobiotics in Health and Disease: The Two Sides of a Coin: A Clinician’s Perspective. Open Acc. J. Toxicol. 2020, 4, 555641. [Google Scholar] [CrossRef]
  4. Štefanac, T.; Grgas, D.; Landeka Dragičević, T. Xenobiotics—Division and Methods of Detection: A Review. J. Xenobiot. 2021, 11, 130–141. [Google Scholar] [CrossRef] [PubMed]
  5. Koppel, N.; Maini Rekdal, V.; Balskus, E.P. Chemical Transformation of Xenobiotics by the Human Gut Microbiota. Science 2017, 356, eaag2770. [Google Scholar] [CrossRef] [PubMed]
  6. Abdelsalam, N.A.; Ramadan, A.T.; ElRakaiby, M.T.; Aziz, R.K. Toxicomicrobiomics: The Human Microbiome vs. Pharmaceutical, Dietary, and Environmental Xenobiotics. Front. Pharmacol. 2020, 11, 390. [Google Scholar] [CrossRef]
  7. Aziz, R.K. Toxicomicrobiomics: Narrowing the Gap between Environmental and Medicinal Toxicogenomics. OMICS A J. Integr. Biol. 2018, 22, 788–789. [Google Scholar] [CrossRef]
  8. 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. [Google Scholar] [CrossRef]
  9. Larsson, K.; Lindh, C.H.; Jönsson, B.A.; Giovanoulis, G.; Bibi, M.; Bottai, M.; Bergström, A.; Berglund, M. Phthalates, Non-Phthalate Plasticizers and Bisphenols in Swedish Preschool Dust in Relation to Children’s Exposure. Environ. Int. 2017, 102, 114–124. [Google Scholar] [CrossRef]
  10. Lei, M.; Menon, R.; Manteiga, S.; Alden, N.; Hunt, C.; Alaniz, R.C.; Lee, K.; Jayaraman, A. Environmental Chemical Diethylhexyl Phthalate Alters Intestinal Microbiota Community Structure and Metabolite Profile in Mice. mSystems 2019, 4, e00724-19. [Google Scholar] [CrossRef] [Green Version]
  11. Adamovsky, O.; Buerger, A.N.; Vespalcova, H.; Sohag, S.R.; Hanlon, A.T.; Ginn, P.E.; Craft, S.L.; Smatana, S.; Budinska, E.; Persico, M.; et al. Evaluation of Microbiome-Host Relationships in the Zebrafish Gastrointestinal System Reveals Adaptive Immunity Is a Target of Bis(2-Ethylhexyl) Phthalate (DEHP) Exposure. Environ. Sci. Technol. 2020, 54, 5719–5728. [Google Scholar] [CrossRef] [PubMed]
  12. Wang, G.; Chen, Q.; Tian, P.; Wang, L.; Li, X.; Lee, Y.-K.; Zhao, J.; Zhang, H.; Chen, W. Gut Microbiota Dysbiosis Might Be Responsible to Different Toxicity Caused by Di-(2-Ethylhexyl) Phthalate Exposure in Murine Rodents. Environ. Pollut. 2020, 261, 114164. [Google Scholar] [CrossRef] [PubMed]
  13. Sabra, S.; Malmqvist, E.; Saborit, A.; Gratacós, E.; Gomez Roig, M.D. Heavy Metals Exposure Levels and Their Correlation with Different Clinical Forms of Fetal Growth Restriction. PLoS ONE 2017, 12, e0185645. [Google Scholar] [CrossRef] [PubMed]
  14. Zhou, C.; Xu, P.; Huang, C.; Liu, G.; Chen, S.; Hu, G.; Li, G.; Liu, P.; Guo, X. Effects of Subchronic Exposure of Mercuric Chloride on Intestinal Histology and Microbiota in the Cecum of Chicken. Ecotoxicol. Environ. Saf. 2020, 188, 109920. [Google Scholar] [CrossRef] [PubMed]
  15. Zhao, Y.; Zhou, C.; Wu, C.; Guo, X.; Hu, G.; Wu, Q.; Xu, Z.; Li, G.; Cao, H.; Li, L.; et al. Subchronic Oral Mercury Caused Intestinal Injury and Changed Gut Microbiota in Mice. Sci. Total Environ. 2020, 721, 137639. [Google Scholar] [CrossRef] [PubMed]
  16. Chen, J.; Hartmann, E.M.; Kline, J.; Van Den Wymelenberg, K.; Halden, R.U. Assessment of Human Exposure to Triclocarban, Triclosan and Five Parabens in U.S. Indoor Dust Using Dispersive Solid Phase Extraction Followed by Liquid Chromatography Tandem Mass Spectrometry. J. Hazard Mater. 2018, 360, 623–630. [Google Scholar] [CrossRef] [PubMed]
  17. Quirós-Alcalá, L.; Buckley, J.P.; Boyle, M. Parabens and Measures of Adiposity among Adults and Children from the U.S. General Population: NHANES 2007–2014. Int. J. Hyg. Environ. Health 2018, 221, 652–660. [Google Scholar] [CrossRef] [PubMed]
  18. Poston, R.G.; Saha, R.N. Epigenetic Effects of Polybrominated Diphenyl Ethers on Human Health. Int. J. Environ. Res. Public Health 2019, 16, 2703. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Chen, L.; Hu, C.; Lai, N.L.-S.; Zhang, W.; Hua, J.; Lam, P.K.S.; Lam, C.W.J.; Zhou, B. Acute Exposure to PBDEs at an Environmentally Realistic Concentration Causes Abrupt Changes in the Gut Microbiota and Host Health of Zebrafish. Environ. Pollut. 2018, 240, 17–26. [Google Scholar] [CrossRef]
  20. 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, 425–434. [Google Scholar] [CrossRef]
  21. Gillezeau, C.; Alpert, N.; Joshi, P.; Taioli, E. Urinary Dialkylphosphate Metabolite Levels in US Adults—National Health and Nutrition Examination Survey 1999–2008. Int. J. Environ. Res. Public Health 2019, 16, 4605. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Li, J.-W.; Fang, B.; Pang, G.-F.; Zhang, M.; Ren, F.-Z. 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. [Google Scholar] [CrossRef] [PubMed]
  23. Mendler, A.; Geier, F.; Haange, S.-B.; Pierzchalski, A.; Krause, J.L.; Nijenhuis, I.; Froment, J.; Jehmlich, N.; Berger, U.; Ackermann, G.; et al. Mucosal-Associated Invariant T-Cell (MAIT) Activation Is Altered by Chlorpyrifos- and Glyphosate-Treated Commensal Gut Bacteria. J. Immunotoxicol. 2020, 17, 10–20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Manabe, M.; Kanda, S.; Fukunaga, K.; Tsubura, A.; Nishiyama, T. Evaluation of the Estrogenic Activities of Some Pesticides and Their Combinations Using MtT/Se Cell Proliferation Assay. Int. J. Hyg. Environ. Health 2006, 209, 413–421. [Google Scholar] [CrossRef] [PubMed]
  25. 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, 198–206. [Google Scholar] [CrossRef] [Green Version]
  26. Liang, Y.; Zhan, J.; Liu, D.; Luo, M.; Han, J.; Liu, X.; Liu, C.; Cheng, Z.; Zhou, Z.; Wang, P. Organophosphorus Pesticide Chlorpyrifos Intake Promotes Obesity and Insulin Resistance through Impacting Gut and Gut Microbiota. Microbiome 2019, 7, 19. [Google Scholar] [CrossRef] [Green Version]
  27. Zhang, Y.; Li, Z.; Kholodkevich, S.; Sharov, A.; Chen, C.; Feng, Y.; Ren, N.; Sun, K. Effects of Cadmium on Intestinal Histology and Microbiota in Freshwater Crayfish (Procambarus clarkii). Chemosphere 2020, 242, 125105. [Google Scholar] [CrossRef]
  28. O’Neill, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. Government of the United Kingdom. Available online: https://apo.org.au/node/63983 (accessed on 2 March 2022).
  29. Lindell, A.E.; Zimmermann-Kogadeeva, M.; Patil, K.R. Multimodal Interactions of Drugs, Natural Compounds and Pollutants with the Gut Microbiota. Nat. Rev. Microbiol. 2022, 6, 235. [Google Scholar] [CrossRef]
  30. Penders, J.; Stobberingh, E.; Savelkoul, P.; Wolffs, P. The Human Microbiome as a Reservoir of Antimicrobial Resistance. Front. Microbiol. 2013, 4, 87. [Google Scholar] [CrossRef] [Green Version]
  31. Anthony, W.E.; Burnham, C.A.D.; Dantas, G.; Kwon, J.H. The Gut Microbiome as a Reservoir for Antimicrobial Resistance. J. Infect. Dis. 2021, 223, S209–S213. [Google Scholar] [CrossRef]
  32. Directive 2010/75/EU of the European Parliament and of the Council of 24 November 2010 on Industrial Emissions (Integrated Pollution Prevention and Control). OJ L 334, 17.12.2010, pp. 17–119. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32010L0075 (accessed on 14 December 2021).
  33. Apel, P.; Rousselle, C.; Lange, R.; Sissoko, F.; Kolossa-Gehring, M.; Ougier, E. Human Biomonitoring Initiative (HBM4EU)—Strategy to Derive Human Biomonitoring Guidance Values (HBM-GVs) for Health Risk Assessment. Int. J. Hyg. Environ. Health 2020, 230, 113622. [Google Scholar] [CrossRef] [PubMed]
  34. Eshel, G.; Shepon, A.; Makov, T.; Milo, R. Land, Irrigation Water, Greenhouse Gas, and Reactive Nitrogen Burdens of Meat, Eggs, and Dairy Production in the United States. Proc. Natl. Acad. Sci. USA 2014, 111, 11996–12001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Hu, J.; Raikhel, V.; Gopalakrishnan, K.; Fernandez-Hernandez, H.; Lambertini, L.; Manservisi, F.; Falcioni, L.; Bua, L.; Belpoggi, F.; Teitelbaum, S.L.; et al. Effect of Postnatal Low-Dose Exposure to Environmental Chemicals on the Gut Microbiome in a Rodent Model. Microbiome 2016, 4, 26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Sharma, S.; Tripathi, P. Gut Microbiome and Type 2 Diabetes: Where We Are and Where to Go? J. Nutr. Biochem. 2019, 63, 101–108. [Google Scholar] [CrossRef] [PubMed]
  37. Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An Obesity-Associated Gut Microbiome with Increased Capacity for Energy Harvest. Nature 2006, 444, 1027–1031. [Google Scholar] [CrossRef]
  38. Singh, R.K.; Chang, H.-W.; Yan, D.; Lee, K.M.; Ucmak, D.; Wong, K.; Abrouk, M.; Farahnik, B.; Nakamura, M.; Zhu, T.H.; et al. Influence of Diet on the Gut Microbiome and Implications for Human Health. J. Transl. Med. 2017, 15, 73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Katsi, V.; Didagelos, M.; Skevofilax, S.; Armenis, I.; Kartalis, A.; Vlachopoulos, C.; Karvounis, H.; Tousoulis, D. GUT Microbiome-GUT Dysbiosis-Arterial Hypertension: New Horizons. Curr. Hypertens. Rev. 2019, 15, 40–46. [Google Scholar] [CrossRef]
  40. Liess, M.; Henz, S.; Shahid, N. Modeling the Synergistic Effects of Toxicant Mixtures. Environ. Sci. Eur. 2020, 32, 119. [Google Scholar] [CrossRef]
  41. 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, 287–293. [Google Scholar] [CrossRef]
  42. Silbergeld, E.K. The Microbiome: Modulator of Pharmacological and Toxicological Exposures and Responses. Toxicol. Pathol. 2017, 45, 190–194. [Google Scholar] [CrossRef]
  43. Malaisé, Y.; Ménard, S.; Cartier, C.; Lencina, C.; Sommer, C.; Gaultier, E.; Houdeau, E.; Guzylack-Piriou, L. Consequences of Bisphenol a Perinatal Exposure on Immune Responses and Gut Barrier Function in Mice. Arch. Toxicol. 2017, 7, 14472. [Google Scholar] [CrossRef] [PubMed]
  44. Graw, S.; Chappell, K.; Washam, C.L.; Gies, A.; Bird, J.; Robeson, M.S.; Byrum, S.D. Multi-Omics Data Integration Considerations and Study Design for Biological Systems and Disease. Mol. Omics 2021, 17, 170–185. [Google Scholar] [CrossRef] [PubMed]
  45. Knight, R.; Vrbanac, A.; Taylor, B.C.; Aksenov, A.; Callewaert, C.; Debelius, J.; Gonzalez, A.; Kosciolek, T.; McCall, L.-I.; McDonald, D.; et al. Best Practices for Analysing Microbiomes. Nat. Rev. Microbiol. 2018, 16, 410–422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Marzorati, M.; Van de Wiele, T. An Advanced In Vitro Technology Platform to Study the Mechanism of Action of Prebiotics and Probiotics in the Gastrointestinal Tract. J. Clin. Gastroenterol. 2016, 50, S124. [Google Scholar] [CrossRef]
  47. Dietert, R.R. The Microbiome in Early Life: Self-Completion and Microbiota Protection as Health Priorities. Birth Defects Res. B Dev. Reprod. Toxicol. 2014, 101, 333–340. [Google Scholar] [CrossRef] [PubMed]
  48. López-Moreno, A.; Acuña, I.; Torres-Sánchez, A.; Ruiz-Moreno, Á.; Cerk, K.; Rivas, A.; Suárez, A.; Monteoliva-Sánchez, M.; Aguilera, M. Next Generation Probiotics for Neutralizing Obesogenic Effects: Taxa Culturing Searching Strategies. Nutrients 2021, 13, 1617. [Google Scholar] [CrossRef] [PubMed]
  49. Ben, G.H.; Bouri, M.; Mougou Hamdane, A.; Schuster, C.; Leclerque, A.; Rhouma, A. Bacillus Velezensis Strain MBY2, a Potential Agent for the Management of Crown Gall Disease. PLoS ONE 2021, 16, e0252823. [Google Scholar] [CrossRef]
  50. Sonnenburg, J.L.; Bäckhed, F. Diet–microbiota interactions as moderators of human metabolism. Nature 2016, 535, 56–64. [Google Scholar] [CrossRef]
  51. De Gregorio, V.; Telesco, M.; Corrado, B.; Rosiello, V.; Urciuolo, F.; Netti, P.A.; Imparato, G. Intestine-Liver Axis On-Chip Reveals the Intestinal Protective Role on Hepatic Damage by Emulating Ethanol First-Pass Metabolism. Front. Bioeng. Biotechnol. 2020, 8, 163. [Google Scholar] [CrossRef]
  52. López-Moreno, A.; Aguilera, M. Probiotics Dietary Supplementation for Modulating Endocrine and Fertility Microbiota Dysbiosis. Nutrients 2020, 12, 757. [Google Scholar] [CrossRef] [Green Version]
  53. Fallani, M.; Young, D.; Scott, J.; Norin, E.; Amarri, S.; Adam, R.; Aguilera, M.; Khanna, S.; Gil, A.; Edwards, C.A.; et al. Intestinal Microbiota of 6-Week-Old Infants across Europe: Geographic Influence beyond Delivery Mode, Breast-Feeding, and Antibiotics. J. Pediatr. Gastroenterol. Nutr. 2010, 51, 77–84. [Google Scholar] [CrossRef] [PubMed]
  54. Humboldt-Dachroeden, S.; Rubin, O.; Sylvester Frid-Nielsen, S. The State of One Health Research across Disciplines and Sectors—A Bibliometric Analysis. One Health 2020, 10, 100146. [Google Scholar] [CrossRef] [PubMed]
  55. Essack, S.Y. Environment: The Neglected Component of the One Health Triad. Lancet Planet Health 2018, 2, 238–239. [Google Scholar] [CrossRef]
  56. Farm to Fork Strategy. European Commission. Available online: https://ec.europa.eu/food/horizontal-topics/farm-fork-strategy_es (accessed on 2 March 2022).
  57. Caring for Soil Is Caring for Life. Available online: https://ec.europa.eu/info/publications/caring-soil-caring-life_en (accessed on 2 March 2022).
Figure 1. Risk assessment of xenobiotics in an accordance with the One Health approach.
Figure 1. Risk assessment of xenobiotics in an accordance with the One Health approach.
Jox 12 00006 g001
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Ortiz, P.; Torres-Sánchez, A.; López-Moreno, A.; Cerk, K.; Ruiz-Moreno, Á.; Monteoliva-Sánchez, M.; Ampatzoglou, A.; Aguilera, M.; Gruszecka-Kosowska, A. Impact of Cumulative Environmental and Dietary Xenobiotics on Human Microbiota: Risk Assessment for One Health. J. Xenobiot. 2022, 12, 56-63. https://doi.org/10.3390/jox12010006

AMA Style

Ortiz P, Torres-Sánchez A, López-Moreno A, Cerk K, Ruiz-Moreno Á, Monteoliva-Sánchez M, Ampatzoglou A, Aguilera M, Gruszecka-Kosowska A. Impact of Cumulative Environmental and Dietary Xenobiotics on Human Microbiota: Risk Assessment for One Health. Journal of Xenobiotics. 2022; 12(1):56-63. https://doi.org/10.3390/jox12010006

Chicago/Turabian Style

Ortiz, Pilar, Alfonso Torres-Sánchez, Ana López-Moreno, Klara Cerk, Ángel Ruiz-Moreno, Mercedes Monteoliva-Sánchez, Antonis Ampatzoglou, Margarita Aguilera, and Agnieszka Gruszecka-Kosowska. 2022. "Impact of Cumulative Environmental and Dietary Xenobiotics on Human Microbiota: Risk Assessment for One Health" Journal of Xenobiotics 12, no. 1: 56-63. https://doi.org/10.3390/jox12010006

APA Style

Ortiz, P., Torres-Sánchez, A., López-Moreno, A., Cerk, K., Ruiz-Moreno, Á., Monteoliva-Sánchez, M., Ampatzoglou, A., Aguilera, M., & Gruszecka-Kosowska, A. (2022). Impact of Cumulative Environmental and Dietary Xenobiotics on Human Microbiota: Risk Assessment for One Health. Journal of Xenobiotics, 12(1), 56-63. https://doi.org/10.3390/jox12010006

Article Metrics

Back to TopTop