The role of heavy metal exposure on the microbiome in the etiology of gastrointestinal disorders: a scoping review

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In recent years, epidemiological studies have increasingly recognized the significance of heavy metals as an important pathogenetic factor in many gastrointestinal diseases, particularly those associated with in gut microbiota functions. The toxicity of heavy metals towards essential intestinal microflora goes beyond causing dysbiotic disorders; it can also exacerbate intestinal infections, alter metabolic processes, and influence the development of antibiotic resistance. Since the negative effects of heavy metals are environmental in nature, there is a need to systematize the etiological role between the effects of heavy metals on the microbiome and possible nosological conditions for a more accurate approach to treatment and further research. Given the environmental origins of the abovementioned effects, there is a need to systematize the impact of heavy metals on the microbiome and their role in disease development to improve approaches to treatment and further research.

We aimed to analyze the latest scientific evidence on the associations between heavy metals exposure and the intestinal microbiome and its role in the development of gastrointestinal disorders. For this scoping review we used PubMed and eLIBRARY.ru databases. We searched for keywords: «gut microbiota», «intestinal infections» (disorders), «antibiotic resistance» «heavy metals» in both Russian and English. Based on the research reviewed in this study, we can infer that heavy metals act as exogenous toxicants contributing to the development of dysbiotic, metabolic and trophic disorders of the gastrointestinal tract. They also influence the progression of infections and the development of antibiotic resistance in bacteria. Further studies should focus on exploring the toxicity of heavy metals in relation to specific populations of intestinal flora and associations with metal and antibiotic resistance. It is important to consider the therapeutic potential of microbiome modulation in the management of gastrointestinal diseases.

作者简介

Olga Delyukina

JCS OLLMED PLUS

Email: pril74@mail.ru
ORCID iD: 0009-0006-1631-986X
SPIN 代码: 8421-4528

MD

俄罗斯联邦, Moscow

Sergey Savko

I.M. Sechenov First Moscow State Medical University

Email: d.t.d.savko@gmail.com
ORCID iD: 0000-0001-9642-5377
SPIN 代码: 8460-5476

Student

俄罗斯联邦, Moscow

Elena Rylina

Peoples’ Friendship University of Russia named after Patrice Lumumba

编辑信件的主要联系方式.
Email: hellch@mail.ru
ORCID iD: 0000-0002-9375-309X
SPIN 代码: 4372-9977

Cand. Sci. (Pharmacy)

俄罗斯联邦, Moscow

Ekaterina Bilous

I.M. Sechenov First Moscow State Medical University

Email: bilousea@gmail.com
ORCID iD: 0009-0002-0504-3352

Student

俄罗斯联邦, Moscow

Tatiana Korobeynikova

I.M. Sechenov First Moscow State Medical University; Peoples’ Friendship University of Russia named after Patrice Lumumba

Email: tatcvetk@ya.ru
ORCID iD: 0000-0002-1373-6354
SPIN 代码: 7764-6486

Cand. Sci. (Engineering), Researcher

俄罗斯联邦, Moscow; Moscow

Anatoly Skalny

I.M. Sechenov First Moscow State Medical University

Email: skalnylab@gmail.com
ORCID iD: 0000-0001-7838-1366
SPIN 代码: 5231-9017

Dr. Sci. (Medicine), Professor

俄罗斯联邦, Moscow

参考

  1. Zhai Q, Li T, Yu L, et al. Effects of subchronic oral toxic metal exposure on the intestinal microbiota of Mice. Science Bulletin. 2017;62(12):831–840. doi: 10.1016/j.scib.2017.01.031
  2. Jin Y, Wu S, Zeng Z, Fu Z. Effects of environmental pollutants on gut microbiota. Environmental Pollution. 2017;222:1–9. doi: 10.1016/j.envpol.2016.11.045
  3. Grabeklis VV, Delyukina OV, Savko SA. Interaction of essential elements and gut microbiota: a literature review // Trace Elements in Medicine. 2023;24(3):12–21. doi: 10.19112/2413-6174-2023-24-3-12-21
  4. Fujishiro H, Hamao S, Tanaka R, et al. Concentration-dependent roles of DMT1 and zip14 in cadmium absorption in Caco-2 cells. The Journal of Toxicological Sciences. 2017;42(5):559–567. doi: 10.2131/jts.42.559
  5. Fujishiro H, Ohashi T, Takuma M, Himeno S. Suppression of ZIP8 expression is a common feature of cadmium-resistant and manganese-resistant RBL-2H3 Cells. Metallomics. 2013;5(5):437–444. doi: 10.1039/c3mt00003f
  6. Breton J, Le Clère K, Daniel C, et al. Chronic ingestion of cadmium and lead alters the bioavailability of essential and heavy metals, gene expression pathways and genotoxicity in mouse intestine. Arch Toxicol. 2013;87(10):1787–1795. doi: 10.1007/s00204-013-1032-6
  7. Sohrabi M, Kheiri Z, Gholami A, et al. The comparison of the plasma levels of the lead element in patients with gastrointestinal cancers and healthy individuals. Asian Pacific Journal of Cancer Prevention. 2019;20(9):2639–2644. doi: 10.31557/apjcp.2019.20.9.2639
  8. Yuan W, Yang N, Li X. Advances in understanding how heavy metal pollution triggers gastric cancer. BioMed Research International. 2016;2016:1–10. doi: 10.1155/2016/7825432
  9. Welling R, Beaumont JJ, Petersen SJ, et al. Chromium VI and stomach cancer: a meta-analysis of the current epidemiological evidence. Occupational and Environmental Medicine. 2015;72(2):151–159. doi: 10.1136/oemed-2014-102178
  10. Giambò F, Italia S, Teodoro M, et al. Influence of toxic metal exposure on the gut microbiota (review). World Academy of Sciences Journal. 2021;3(2). doi: 10.3892/wasj.2021.90
  11. Breton J, Massart S, Vandamme P, et al. Ecotoxicology inside the gut: Impact of heavy metals on the mouse microbiome. BMC Pharmacology and Toxicology. 2013;14:62. doi: 10.1186/2050-6511-14-62
  12. Assefa S, Köhler G. Intestinal microbiome and metal toxicity. Current Opinion in Toxicology. 2020;19:21–27. doi: 10.1016/j.cotox.2019.09.009
  13. Velmurugan G, Ramprasath T, Gilles M, et al. Gut microbiota, endocrine-disrupting chemicals, and the diabetes epidemic. Trends in Endocrinology & Metabolism. 2017;28(8):612–625. doi: 10.1016/j.tem.2017.05.001
  14. Roussos A, Koursarakos P, Patsopoulos D, et al. Increased prevalence of irritable bowel syndrome in patients with bronchial asthma. Respir Med. 2003;97(1):75–79. doi: 10.1053/rmed.2001.1409
  15. Huang Y, Mao K, Chen X, et al. S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense. Science. 2018;359(6371):114–119. doi: 10.1126/science.aam5809
  16. Roncal C, Martínez-Aguilar E, Orbe J, et al. Trimethylamine-N-Oxide (TMAO) predicts cardiovascular mortality in peripheral artery disease. Sci Rep. 2019;9(1):15580. doi: 10.1038/s41598-019-52082-z
  17. Zeisel SH, Warrier M. Trimethylamine N-Oxide, the microbiome, and heart and kidney disease. Annu Rev Nutr. 2017;37:157–181. doi: 10.1146/annurev-nutr-071816-064732
  18. Gadd GM. Heavy metal accumulation by bacteria and other microorganisms. Experientia. 1990;46:834–840. doi: 10.1007/bf01935534
  19. Levinson HS, Mahler I, Blackwelder P, Hood T. Lead resistance and sensitivity in staphylococcus aureus. FEMS Microbiology Letters. 1996;145(3):421–425. doi: 10.1111/j.1574-6968.1996.tb08610.x
  20. Rathnayake IVN, Megharaj M, Krishnamurti GSR, et al. Heavy metal toxicity to bacteria – are the existing growth media accurate enough to determine heavy metal toxicity? Chemosphere. 2013;90(3):1195–1200. doi: 10.1016/j.chemosphere.2012.09.036
  21. Ercal N, Gurer-Orhan H, Aykin-Burns N. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Current Topics in Medicinal Chemistry. 2001;1(6):529–539. doi: 10.2174/1568026013394831
  22. Yazdankhah S, Skjerve E, Wasteson Y. Antimicrobial resistance due to the content of potentially toxic metals in soil and fertilizing products. Microbial Ecology in Health and Disease. 2018;29(1):1548248. doi: 10.1080/16512235.2018.1548248
  23. Tinkov AA, Gritsenko VA, Skalnaya MG, et al. Gut as a target for cadmium toxicity. Environmental Pollution. 2018;235:429–434. doi: 10.1016/j.envpol.2017.12.114
  24. Liu X, Zhang J, Si J, et al. What happens to gut microorganisms and potential repair mechanisms when meet heavy metal(loid)s. Environmental Pollution. 2023;317:120780. doi: 10.1016/j.envpol.2022.120780
  25. Shinkai Y, Kaji T. Cellular defense mechanisms against lead toxicity in the vascular system. Biol Pharm Bull. 2012;35(11):1885–1891. doi: 10.1248/bpb.b212018
  26. Akhpolova VO, Brin VB. Actual concepts of heavy metals’ kinetics and pathogenesis of toxicity. Journal of New Medical Technologies. 2020;27(1):55–61. doi: 10.24411/1609-2163-2020-16578
  27. Chiocchetti GM, Domene A, Kühl AA, et al. In vivo evaluation of the effect of arsenite on the intestinal epithelium and associated microbiota in mice. Archives of Toxicology. 2019;93(8):2127–2139. doi: 10.1007/s00204-019-02510-w
  28. Sterritt RM, Lester JN. Interactions of heavy metals with bacteria. Science of the Total Environment. 1980;14(1):5–17. doi: 10.1016/0048-9697(80)90122-9
  29. Bolan S, Seshadri B, Kunhikrishnan A, et al. Differential toxicity of potentially toxic elements to human gut microbes. Chemosphere. 2022;303(Pt 1):134958. doi: 10.1016/j.chemosphere.2022.134958
  30. Liu Y, Li Y, Liu K, Shen J. Exposing to cadmium stress cause profound toxic effect on microbiota of the mice intestinal tract. PloS One. 2014;9(2):e85323. doi: 10.1371/journal.pone.0085323
  31. Wu B, Cui H, Peng X, et al. Toxicological effects of dietary nickel chloride on intestinal microbiota. Ecotoxicology and Environmental Safety. 2014;109:70–76. doi: 10.1016/j.ecoenv.2014.08.002
  32. Lu K, Abo RP, Schlieper KA, et al. Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environmental Health Perspectives. 2014;122(3):284–291. doi: 10.1289/ehp.1307429
  33. Bisanz JE, Enos MK, Mwanga JR, et al. Randomized open-label pilot study of the influence of probiotics and the gut microbiome on toxic metal levels in Tanzanian pregnant women and school children. MBio. 2014;5(5):e01580–14. doi: 10.1128/mbio.01580-14
  34. Singh R, Gautam N, Mishra A, Gupta R. Heavy metals and living systems: an overview. Indian J Pharmacol. 2011;43(3):246–53. doi: 10.4103/0253-7613.81505
  35. Eggers S, Safdar N, Sethi AK, et al. Urinary lead concentration and composition of the adult gut microbiota in a cross-sectional population-based sample. Environment International. 2019;133(Pt. A.):105122. doi: 10.1016/j.envint.2019.105122
  36. Zhang F, Zheng W, Guo R, Yao W. Effect of dietary copper level on the gut microbiota and its correlation with serum inflammatory cytokines in Sprague-Dawley rats. Journal of Microbiology. 2017;55(9):694–702. doi: 10.1007/s12275-017-6627-9
  37. Wang B, Wu C, Cui L, et al. Dietary aluminium intake disrupts the overall structure of gut microbiota in Wistar rats. Food Science & Nutrition. 2022;10(11):3574–3584. doi: 10.1002/fsn3.2955
  38. Pamer EG. Immune responses to commensal and environmental microbes. Nature Immunology. 2007;8(11):1173–1178. doi: 10.1038/ni1526
  39. Van der Waaij D, Berghuis-de Vries JM, Lekkerkerk-Van der Wees JEC. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. Epidemiology & Infection. 1971;69(3):405–411. doi: 10.1017/s0022172400021653
  40. Lupp C, Robertson ML, Wickham ME, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host & Microbe. 2007;2(2):119–129. doi: 10.1016/j.chom.2007.06.010
  41. Shi HN, Walker A. Bacterial colonization and the development of intestinal defences. Canadian Journal of Gastroenterology. 2004;18(8):493–500. doi: 10.1155/2004/690421
  42. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science. 2004;303(5664):1662–1665. doi: 10.1126/science.1091334
  43. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nature Reviews Immunology. 2013;13(11):790–801. doi: 10.1038/nri3535
  44. Iizasa H, Ishihara S, Richardo T, et al. Dysbiotic infection in the stomach. World Journal of Gastroenterology. 2015;21(40):11450–11457. doi: 10.3748/wjg.v21.i40.11450
  45. Stecher B, Hardt WD. The role of microbiota in infectious disease. Trends in Microbiology. 2008;16(3):107–114. doi: 10.1016/j.tim.2007.12.008
  46. Li Y, Lou J, Hong S, et al. The role of heavy metals in the development of colorectal cancer. BMC Cancer. 2023;23(1):616. doi: 10.1186/s12885-023-11120-w
  47. Golemis EA, Scheet P, Beck TN, et al. Molecular mechanisms of the preventable causes of cancer in the United States. Genes Dev. 2018;32(13–14):868–902. doi: 10.1101/gad.314849.118
  48. Grivennikov SI, Wang K, Mucida D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491(7423):254–258. doi: 10.1038/nature11465
  49. Li S, Liu J, Zheng X, et al. Tumorigenic bacteria in colorectal cancer: mechanisms and treatments. Cancer Biol Med. 2021;19(2):147–162. doi: 10.20892/j.issn.2095-3941.2020.0651
  50. Cuevas-Ramos G, Petit CR, Marcq I, et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 2010;107(25):11537–11542. doi: 10.1073/pnas.1001261107
  51. Xu FF, Imlay JA. Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Appl Environ Microbiol. 2012;78(10):3614–3621. doi: 10.1128/AEM.07368-11
  52. Øyri SF, Műzes G, Sipos F. Dysbiotic gut microbiome: a key element of Crohn’s disease. Comparative Immunology, Microbiology and Infectious Diseases. 2015;43:36–49. doi: 10.1016/j.cimid.2015.10.005
  53. Zechner EL. Inflammatory disease caused by intestinal pathobionts. Current Opinion in Microbiology. 2017;35:64–69. doi: 10.1016/j.mib.2017.01.011
  54. Hou K, Wu ZX, Chen XY, et al. Microbiota in health and diseases. Signal Transduct Target Ther. 2022;7(1):135. doi: 10.1038/s41392-022-00974-4
  55. Loranskaya ID, Khalif IL, Boldyreva MN, Kupaeva VA. Characteristic of microbiome in inflammatory bowel disease. Experimental and Clinical Gastroenterology Journal. 2018;153(5):104–111. EDN: UZLFMJ
  56. Kang S, Denman SE, Morrison M, et al. Dysbiosis of fecal microbiota in Crohn’s disease patients as revealed by a custom phylogenetic microarray. Inflammatory Bowel Diseases. 2010;16(12):2034–2042. doi: 10.1002/ibd.21319
  57. Gîlcă-Blanariu GE, Diaconescu S, Ciocoiu M, Ștefănescu G. New Insights into the role of trace elements in IBD. Biomed Res Int. 2018;2018:1813047. doi: 10.1155/2018/1813047
  58. Yu Q, Zhang S, Li L, et al. Enterohepatic helicobacter species as a potential causative factor in inflammatory bowel disease: a meta-analysis. Medicine (Baltimore). 2015;94(45):e1773. doi: 10.1097/MD.0000000000001773
  59. Schippa S, Conte MP. Dysbiotic events in gut microbiota: impact on human health. Nutrients. 2014;6(12):5786–5805. doi: 10.3390/nu6125786
  60. Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology. 2014;146(6):1513–1524. doi: 10.1053/j.gastro.2014.01.020
  61. Kuzan A. Toxicity of advanced glycation end products (review). Biomed Rep. 2021;14(5):46. doi: 10.3892/br.2021.1422
  62. Aschner M, Skalny AV, Gritsenko VA, et al. Role of gut microbiota in the modulation of the health effects of advanced glycation end-products (review). Int J Mol Med. 2023;51(5):44. doi: 10.3892/ijmm.2023.5247
  63. Parfrey LW, Walters WA, Lauber CL, et al. Communities of microbial eukaryotes in the mammalian gut within the context of environmental eukaryotic diversity. Frontiers in Microbiology. 2014;5:298. doi: 10.3389/fmicb.2014.00298
  64. Pickard JM, Zeng MY, Caruso R, Núñez G. Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease. Immunological Reviews. 2017;279(1):70–89. doi: 10.1111/imr.12567
  65. Liu W, Feng H, Zheng S, et al. Pb toxicity on gut physiology and microbiota. Frontiers in Physiology. 2021;12:574913. doi: 10.3389/fphys.2021.574913
  66. Feng W, Liu J, Huang L, et al. Gut microbiota as a target to limit toxic effects of traditional Chinese medicine: Implications for therapy. Biomedicine & Pharmacotherapy. 2021;133:111047. doi: 10.1016/j.biopha.2020.111047
  67. Li YP, Ben Fekih I, Chi Fru E, et al. Antimicrobial activity of metals and metalloids. Annual Review of Microbiology. 2021;75:175–197. doi: 10.1146/annurev-micro-032921-123231
  68. Bruins MR, Kapil S, Oehme FW. Microbial resistance to metals in the environment. Ecotoxicology and Environmental Safety. 2000;45(3):198–207. doi: 10.1006/eesa.1999.1860
  69. Cánovas D, Cases I, De Lorenzo V. Heavy metal tolerance and metal homeostasis in Pseudomonas putida as revealed by complete genome analysis. Environmental Microbiology. 2003;5(12):1242–1256. doi: 10.1111/j.1462-2920.2003.00463.x
  70. Shamim S. Biosorption of heavy metals. Biosorption. 2018:21–49. doi: 10.5772/intechopen.72099
  71. Pinto E, Sigaud-Kutner TC, Leitao MA, et al. Heavy metal-induced oxidative stress in algae 1. Journal of Phycology. 2003;39(6):1008–1018. doi: 10.1111/j.0022-3646.2003.02-193.x
  72. Schiering N, Kabsch W, Moore MJ, et al. Structure of the detoxification catalyst mercuric ion reductase from Bacillus sp. strain RC607. Nature. 1991;352(6331):168–172. doi: 10.1038/352168a0
  73. Ianeva OD. Mechanisms of bacteria resistance to heavy metals. Mikrobiol Z. 2009;71(6):54–65.
  74. Yenikeyev RR, Tatarinova NY., Zakharchuk LM. Mechanisms of resistance to clinically significant antibiotics of strains of bacteria of the genus Bacillus isolated from samples delivered from the International Space Station. Vestnik Moskovskogo Universiteta. Seriya 16. Biologiya. 2020;75(4):265–272. doi: 10.3103/s0096392520040045
  75. Rensing C, Ghosh M, Rosen BP. Families of soft-metal-ion-transporting ATPases. Journal of Bacteriology. 1999;181(19): 5891–5897. doi: 10.1128/jb.181.19.5891-5897.1999
  76. Silver S, Phung LT. Bacterial heavy metal resistance: new surprises. Annual Review of Microbiology. 1996;50:753–789. doi: 10.1146/annurev.micro.50.1.753
  77. Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiology Reviews. 2003;27(2–3):313–339. doi: 10.1016/s0168-6445(03)00048-2
  78. Davidovich NV, Kukalevskaya NN, Bashilova EN, Bazhukova TA. General principles of antibiotic resistance evolution in bacteria (review of literature). Klinicheskaya Laboratornaya Diagnostika. 2020;65(6):387–393. doi: 10.18821/0869-2084-2020-65-6-387-393
  79. Osipov VA, Tapalsky DV, Skleenova EU, Eidelstein MV. Metallo-beta-lactamases in gram-negative bacterial pathogens: accruing problem in the world and in Belarus. Meditsinskie Novosti. 2013;221(2):84–88. EDN: QABLBP
  80. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. Co-selection of antibiotic and metal resistance. Trends in Microbiology. 2006;14(4):176–182. doi: 10.1016/j.tim.2006.02.006
  81. Pal C, Asiani K, Arya S, et al. Metal resistance and its association with antibiotic resistance. Advances in Microbial Physiology. 2017;70:261–313. doi: 10.1016/bs.ampbs.2017.02.001
  82. Chapman JS. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. International Biodeterioration & Biodegradation. 2003;51(4):271–276. doi: 10.1016/s0964-8305(03)00044-1
  83. Cavaco LM, Hasman H, Stegger M, et al Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrobial Agents and Chemotherapy. 2010;54(9):3605–3608. doi: 10.1128/aac.00058-10
  84. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DJ. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics. 2015;16:964. doi: 10.1186/s12864-015-2153-5
  85. Mata MT, Baquero F, Perez-Diaz JC. A multidrug efflux transporter in Listeria monocytogenes. FEMS Microbiology Letters. 2000;187(2):185–188. doi: 10.1111/j.1574-6968.2000.tb09158.x
  86. Nakajima H, Kobayashi K, Kobayashi M, et al. Overexpression of the robA gene increases organic solvent tolerance and multiple antibiotic and heavy metal ion resistance in Escherichia coli. Applied and Environmental Microbiology. 1995;61(6):2302–2307. doi: 10.1128/aem.61.6.2302-2307.1995
  87. Tuckfield RC, McArthur JV. Spatial analysis of antibiotic resistance along metal contaminated streams. Microbial Ecology. 2008;55(4):595–607. doi: 10.1007/s00248-007-9303-5
  88. Stepanauskas R, Glenn TC, Jagoe CH, et al. Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environmental Microbiology. 2006;8(9):1510–1514. doi: 10.1111/j.1462-2920.2006.01091.x

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