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Evaluation of the Role of Probiotics As a New Strategy to Eliminate Microbial Toxins: a Review

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Abstract

Probiotics are living microorganisms that have favorable effects on human and animal health. The most usual types of microorganisms recruited as probiotics are lactic acid bacteria (LAB) and bifidobacteria. To date, numerous utilizations of probiotics have been reported. In this paper, it is suggested that probiotic bacteria can be recruited to remove and degrade different types of toxins such as mycotoxins and algal toxins that damage host tissues and the immune system causing local and systemic infections. These microorganisms can remove toxins by disrupting, changing the permeability of the plasma membrane, producing metabolites, inhibiting the protein translation, hindering the binding to GTP binding proteins to GM1 receptors, or by preventing the interaction between toxins and adhesions. Here, we intend to review the mechanisms that probiotic bacteria use to eliminate and degrade microbial toxins.

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References

  1. Fao/Who (2001) Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. World Health Organization and Food and Agriculture Organization of the United Nations, London, Ontario, Canada. http://www.fao.org/documents/pub_dett.asp?lang=en&pub_id=61756.Accessed 25 Sep 2020

  2. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  3. Zendeboodi F, Khorshidian N, Mortazavian AM, Da Cruz AG (2020) Probiotic: conceptualization from a new approach. Curr Opin Food Sci 32:103–123. https://doi.org/10.1016/j.cofs.2020.03.009

    Article  Google Scholar 

  4. Amara A, Shibl A (2015) Role of probiotics in health improvement, infection control and disease treatment and management. Saudi Pharm J 23(2):107–114. https://doi.org/10.1016/j.jsps.2013.07.001

    Article  CAS  PubMed  Google Scholar 

  5. Kerry RG, Patra JK, Gouda S, Park Y, Shin H-S, Das G (2018) Benefaction of probiotics for human health: a review. J Food Drug Anal 26(3):927–939. https://doi.org/10.1016/j.jfda.2018.01.002

    Article  CAS  Google Scholar 

  6. Kim S-K, Guevarra RB, Kim Y-T, Kwon J, Kim H, Cho JH, Kim HB, Lee J-H (2019) Role of probiotics in human gut microbiome-associated diseases. J Microbiol Biotechnol 29:1335–1340. https://doi.org/10.4014/jmb.1906.06064

    Article  PubMed  Google Scholar 

  7. Hori T, Matsuda K, Oishi K (2020) Probiotics: a dietary factor to modulate the gut microbiome, host immune system, and gut-brain interaction. Microorganisms 8(9):1401–1424. https://doi.org/10.3390/microorganisms8091401

    Article  CAS  PubMed Central  Google Scholar 

  8. Yeşilyurt N, Yılmaz B, Agagunduz D, Capasso R (2021) Involvement of probiotics and postbiotics in the immune system modulation. Biologics 1(2):89–110. https://doi.org/10.3390/biologics1020006

    Article  Google Scholar 

  9. Eslami M, Bahar A, Keikha M, Karbalaei M, Kobyliak N, Yousefi B (2020) Probiotics function and modulation of the immune system in allergic diseases. Allergol Immunopathol (Madr) 48(6):771–778. https://doi.org/10.1016/j.aller.2020.04.005

    Article  CAS  Google Scholar 

  10. Sharma S, Agarwal N, Verma P (2012) Probiotics: the emissaries of health from microbial world. J Appl Pharm Sci 2(1):138–143

    Google Scholar 

  11. Palai S, Derecho CMP, Kesh SS, Egbuna C, Onyeike PC (2020) Prebiotics, probiotics, synbiotics and its importance in the management of diseases. In: Egbun C, Dable Tupas G. (eds) Functional foods and nutraceuticals. Springer, Cham. https://doi.org/10.1007/978-3-030-42319-3_10

  12. Gonzalez-Herrera SM, Bermudez-Quinones G, Ochoa-Martínez LA, Rutiaga-Quinones OM, Gallegos-Infante JA (2021) Synbiotics: a technological approach in food applications. J Food Sci Technol 58(3):811–824. https://doi.org/10.1007/s13197-020-04532-0

    Article  PubMed  Google Scholar 

  13. Johnson A, Deshmukh P, Kaushik S, Sharma V (2019) Microbial bio-production of proteins and valuable metabolites. In: Singh DP, Gupta VK, Prabha R (eds) Microbial Interventions in Agriculture and Environment: Volume 1 : Research Trends, Priorities and Prospects. Springer Singapore, Singapore, 381–418. https://doi.org/10.1007/978-981-13-8391-5_15

  14. Li Z, Li X, Jian M, Geleta GS, Wang Z (2020) Two-dimensional layered nanomaterial-based electrochemical biosensors for detecting microbial toxins. Toxins 12(1):20. https://doi.org/10.3390/toxins12010020

    Article  CAS  Google Scholar 

  15. Tilley SJ, Saibil HR (2006) The mechanism of pore formation by bacterial toxins. Curr Opin Struct Biol 16(2):230–236. https://doi.org/10.1016/j.sbi.2006.03.008

    Article  CAS  PubMed  Google Scholar 

  16. Schmitt CK, Meysick KC, O'Brien AD (1999) Bacterial toxins: friends or foes? Emerg Infect Dis 5(2):224–234. https://doi.org/10.3201/eid0502.990206

  17. Murray PR, Rosenthal KS, Pfaller MA (2020) Medical microbiology. 9thed. Section 4. Elsevier Health Sciences

  18. Pfliegler WP, Pusztahelyi T, Pócsi I (2015) Mycotoxins–prevention and decontamination by yeasts. Microb Physiol 55(7):805–818. https://doi.org/10.1002/jobm.201400833

    Article  CAS  Google Scholar 

  19. Matsuda Y, Wakai T, Kubota M, Osawa M, Sanpei A, Fujimaki S (2013) Mycotoxins are conventional and novel risk biomarkers for hepatocellular carcinoma. World J Gastroenterol 19(17):2587–2590. https://doi.org/10.3748/wjg.v19.i17.2587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Doi K, Uetsuka K (2014) Mechanisms of mycotoxin-induced dermal toxicity and tumorigenesis through oxidative stress-related pathways. J Toxicol Pathol 27(1):1–10 https://doi.org/10.1293/tox.2013-0062

  21. Biernasiak J, Piotrowska M, Libudzisz Z (2006) Detoxification of mycotoxins by probiotic preparation for broiler chickens. Mycotoxin Res 22(4):230–235. https://doi.org/10.1007/BF02946747

    Article  CAS  PubMed  Google Scholar 

  22. Sezer Ç, Guven A, Bilge Oral N, Vatansever L (2013) Detoxification of aflatoxin B1 by bacteriocins and bacteriocinogenic lactic acid bacteria. Turkish J Vet Anim Sci 37(5):594–601. https://doi.org/10.3906/vet-1301-31

    Article  CAS  Google Scholar 

  23. Talebi E, Khademi M, Rastad A (2011) An over review on effect of aflatoxin in animal husbandry. Asian J Exp Biol Sci 2(3):754–757

    CAS  Google Scholar 

  24. Motawe H, Salam AA, El Meleigy K (2014) Reducing the toxicity of aflatoxin in broiler chickens diet by using probiotic and yeast. Int J Poult Sci 13(7):397–407. https://doi.org/10.3923/ijps.2014.397.407

    Article  Google Scholar 

  25. Qureshi H, Hamid SS, Ali SS, Anwar J, Iqbal M, Khan NA (2014) Is aflatoxin B1 a biomarker for pathogenic potential of Aspergillus flavus? J Cell Sci Ther 5(6):188. https://doi.org/10.4172/2157-7013.1000188

    Article  CAS  Google Scholar 

  26. Bin-Umer MA, Mclaughlin JE, Butterly MS, Mccormick S, Tumer NE (2014) Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes. Proc Natl Acad SciUSA 111(32):11798–11803. https://doi.org/10.1073/pnas.1403145111

    Article  CAS  Google Scholar 

  27. Aliabadi MA, Alikhani FE, Mohammadi M, Darsanaki RK (2013) Biological control of aflatoxins. Eur J Exp Biol 3(2):162–166

    Google Scholar 

  28. Peng WX, Marchal JL, Van der Poel AF (2018) Strategies to prevent and reduce mycotoxins for compound feed manufacturing. Anim Feed Sci Technol 237:129–153. https://doi.org/10.1016/j.anifeedsci.2018.01.017

    Article  CAS  Google Scholar 

  29. Indresh H, Umakantha B (2013) Effects of ochratoxin and T-2 toxin combination on performance, biochemical and immune status of commercial broilers. Vet World 6(11):945–949. https://doi.org/10.14202/vetworld.2013.945-949

  30. Kotowicz NK, Frąc M, Lipiec J (2014) The importance of Fusarium fungi in wheat cultivation–pathogenicity and mycotoxins production: A review. J Anim Plant Sci 21(2):3326–3343. https://doi.org/10.1021/acs.orglett.5b01299

    Article  CAS  Google Scholar 

  31. Khosravi AR, Shokri H, Zaboli F (2013) Grain-borne mycoflora and fumonisin B1 from fresh-harvested and stored rice in northern Iran. Jundishapur J Microbiol 6(5):6414. https://doi.org/10.5812/jjm.6414

    Article  Google Scholar 

  32. Palumbo JD, O’Keeffe TL, Gorski L (2013) Multiplex PCR analysis of fumonisin biosynthetic genes in fumonisin-nonproducing Aspergillus niger and A. awamori strains. Mycologia 105(2):277–284. https://doi.org/10.3852/11-418

  33. CfD C (1997) Prevention (1997) Results of the public health response to pfiesteria workshop-Atlanta, Georgia, September 29–30. MMWR Morb Mortal Wkly Rep 46(40):951–952. https://doi.org/10.1289/ehp.01109s5639

    Article  Google Scholar 

  34. Lehane L (2000) Paralytic shellfish poisoning: a review. National Office of Animal and Plant Health, Agriculture, Fisheries and Forestry, Canberra, Australia. pp 1–5

  35. Corbel S, Mougin C, Bouaïcha N (2014) Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96:1–15. https://doi.org/10.1016/j.chemosphere.2013.07.056

    Article  CAS  PubMed  Google Scholar 

  36. Cheung MY, Liang S, Lee J (2013) Toxin-producing cyanobacteria in freshwater: a review of the problems, impact on drinking water safety, and efforts for protecting public health. J Microbiol 51(1):1–10. https://doi.org/10.1007/s12275-013-2549-3

    Article  CAS  PubMed  Google Scholar 

  37. Manage PM, Edwards C, Lawton LA (2010) Bacterial degradation of microcystin. In: Hamamura N, Suzuki S, Mendo S, Barroso CM, Iwata H, Tanabe S (Eds) Biological responses to contaminants. Interdisc. Stud Environ Chem 3:97–110.

  38. Lemes GA, Kist LW, Bogo MR, Yunes JS (2015) Biodegradation of [D-Leu1] microcystin-LR by a bacterium isolated from the sediments of the Patos Lagoon estuary, Brazil. J Venom Anim Toxins Incl Trop Dis 21:4. https://doi.org/10.1186/s40409-015-0001-3

    Article  PubMed  PubMed Central  Google Scholar 

  39. Nybom S (2013) Biodegradation of Cyanobacterial toxins. environmental biotechnology-new approaches and prospective applications, Marian Petre, IntechOpen, https://doi.org/10.5772/55511. Available from: https://www.intechopen.com/chapters/42611

  40. Papatheodorou P, Barth H, Minton N, Aktories K (2018) Cellular uptake and mode-of-action of Clostridium difficile Toxins. Adv Exp Med Biol 1050:77–96. https://doi.org/10.1007/978-3-319-72799-86

    Article  PubMed  Google Scholar 

  41. Paladine HL, Desai UA (2018) Vaginitis: diagnosis and treatment. Am Fam Physician 97(5):321–329

    PubMed  Google Scholar 

  42. Larsen JM (2017) The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology 151:363–374. https://doi.org/10.1111/imm.12760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Smith SB, Ravel J (2017) The vaginal microbiota, host defence and reproductive physiology. J Physiol 595(2):451–463. https://doi.org/10.1113/JP271694

    Article  CAS  PubMed  Google Scholar 

  44. Atassi F, Brassart D, Grob P, Graf F, Servin AL (2006) Lactobacillus strains isolated from the vaginal microbiota of healthy women inhibit Prevotella bivia and Gardnerella vaginalis in coculture and cell culture. Immunol Med Microbiol 48(3):424–432. https://doi.org/10.1111/j.1574-695X.2006.00162.x

    Article  CAS  Google Scholar 

  45. Coudeyras S, Jugie G, Vermerie M, Forestier C (2008) Adhesion of human probiotic Lactobacillus rhamnosus to cervical and vaginal cells and interaction with vaginosis-associated pathogens. Infect Dis Obstet Gynecol 2008:549640. https://doi.org/10.1155/2008/549640

    Article  CAS  PubMed  Google Scholar 

  46. Anukam KC, Osazuwa E, Osemene GI, Ehigiagbe F, Bruce AW, Reid G (2006) Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. MicrobesInfect 8:2772–2776.https://doi.org/10.1016/j.micinf.2006.08.008

  47. Tan KS, Song KP, Ong G (2002) Cytolethal distending toxin of Actinobacillus actinomycetemcomitans: occurrence and association with periodontal disease. J Periodont Res 37(4):268–272. https://doi.org/10.1034/j.1600-0765.2002.01618.x

    Article  CAS  Google Scholar 

  48. Jaffar N, Ishikawa Y, Mizuno K, Okinaga T, Maeda T (2016) Mature biofilm degradation by potential probiotics: Aggregatibacter actinomycetemcomitans versus Lactobacillus spp. PLoS ONE 11(7):e0159466. https://doi.org/10.1371/journal.pone.0159466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Paletta ACC, Castro VS, Conte-Junior CA (2020) Shiga toxin-producing and enteroaggregative Escherichia coli in animal, foods, and humans: pathogenicity mechanisms, detection methods and epidemiology. Curr Microbiol 77(4):612–620. https://doi.org/10.1007/s00284-019-01842-1

    Article  CAS  PubMed  Google Scholar 

  50. Ogawa M, Shimizu K, Nomoto K, Tanaka R, Hamabata T, Yamasaki S, Takeda T, Takeda Y (2001) Inhibition of in vitro growth of Shiga toxin-producing Escherichia coli O157:H7 by probiotic Lactobacillus strains due to production of lactic acid. Int J Food Microbiol 68:135–140. https://doi.org/10.1016/S0168-1605(01)00465-2

    Article  CAS  PubMed  Google Scholar 

  51. Roussel C, Sivignon A, de Vallée A, Garrait G, Denis S, Tsilia V, Ballet N, Vandekerckove P, Van de Wiele T, Barnich N, Blanquet-Diot S (2018) Anti-infectious properties of the probiotic Saccharomyces cerevisiae CNCM I-3856 on enterotoxigenic E. coli (ETEC) strain H10407. Appl Microbiol Biotechnol 102(14):6175–6189. https://doi.org/10.1007/s00253-018-9053-y

  52. Fitzpatrick LR (2013) Probiotics for the treatment of Clostridium difficile associated disease. World J Gastrointest Pathophysiol 4(3):47–52. https://doi.org/10.4291/wjgp.v4.i3.47

    Article  PubMed  PubMed Central  Google Scholar 

  53. Amalaradjou MAR, Bhunia AK (2013) Bioengineered probiotics, a strategic approach to control enteric infections. Bioengineered 4(6):379–387. https://doi.org/10.4161/bioe.23574

    Article  PubMed  PubMed Central  Google Scholar 

  54. Culligan EP, Hill C, Sleator RD (2009) Probiotics and gastrointestinal disease: successes, problems and future prospects. Gut Pathog 1(1):19. https://doi.org/10.1186/1757-4749-1-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Sleator RD, Hill C (2008) Engineered pharmabiotics with improved therapeutic potential. Hum Vaccin 4(4):271–274. https://doi.org/10.4161/hv.4.4.6315

    Article  CAS  PubMed  Google Scholar 

  56. Sakarya S, Gunay N (2014) Saccharomyces boulardii expresses neuraminidase activity selective for α2,3-linked sialic acid that decreases Helicobacter pyloriadhesion to host cells. APMIS 122(10):941–950. https://doi.org/10.1111/apm.12237

    Article  CAS  PubMed  Google Scholar 

  57. Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H (2002) Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Microbiol Immunol 32(2):105–110. https://doi.org/10.1111/j.1574-695X.2002.tb00541.x

    Article  CAS  Google Scholar 

  58. Koo OK, Amalaradjou MAR, Bhunia AK (2012) Recombinant probiotic expressing Listeria adhesion protein attenuates Listeria monocytogenes virulence in vitro. PLoS ONE 7(1):e29277. https://doi.org/10.1371/journal.pone.0029277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mathipa MG, Thantsha MS, Bhunia AK (2019) Lactobacillus casei expressing internalins A and B reduces Listeria monocytogenes interaction with Caco-2 cells in vitro. Microb Biotechnol 12(4):715–729. https://doi.org/10.1111/1751-7915.13407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Watts RE, Tan CK, Ulett GC, Carey AJ, Totsika M, Idris A, Paton AW, Morona R, Paton JC, Schembri MA (2012) Escherichia coli 83972 expressing a p fimbriae oligosaccharide receptor mimic impairs adhesion of uropathogenic E. coli. J Infect Dis 206(8):1242–1249. https://doi.org/10.1093/infdis/jis493

  61. Hostetter SJ, Helgerson AF, Paton JC, Paton AW, Cornick NA (2014) Therapeutic use of a receptor mimic probiotic reduces intestinal Shiga toxin levels in a piglet model of hemolytic uremic syndrome. BMC Res Notes 7(1):331. https://doi.org/10.1186/1756-0500-7-331

    Article  PubMed  PubMed Central  Google Scholar 

  62. Paton AW, Morona R, Paton JC (2000) A new biological agent for treatment of Shiga toxigenic Escherichia coli infections and dysentery in humans. Nat Med 6(3):265–270. https://doi.org/10.1038/73111

    Article  CAS  PubMed  Google Scholar 

  63. Paton AW, Jennings MP, Morona R, Wang H, Focareta A, Roddam LF, Paton JC (2005) Recombinant probiotics for treatment and prevention of enterotoxigenic Escherichia coli diarrhea. Gastroenterology 128(5):1219–1228. https://doi.org/10.1053/j.gastro.2005.01.050

    Article  CAS  PubMed  Google Scholar 

  64. Sola-Oladokun B, Culligan EP, Sleator RD (2017) Engineered probiotics: applications and biological containment. Annu Rev Food Sci Technol 8:353–370. https://doi.org/10.1146/annurev-food-030216-030256

    Article  PubMed  Google Scholar 

  65. Mazhar SF, Afzal M, Almatroudi A, Munir S, Ashfaq UA, Rasool M, Raza H, Munir HMW, Rajoka MSR, Khurshid M (2020) The prospects for the therapeutic implications of genetically engineered probiotics. J Food Qual 2020:9676452. https://doi.org/10.1155/2020/9676452

    Article  CAS  Google Scholar 

  66. Pothoulakis C (2009) Review article: anti-inflammatory mechanisms of action of Saccharomyces boulardii. J Food Qual 30(8):826–833. https://doi.org/10.1111/j.1365-2036.2009.04102.x

    Article  CAS  Google Scholar 

  67. Castagliuolo I, Lamont JT, Nikulasson ST, Pothoulakis C (1996) Saccharomyces boulardii protease inhibits Clostridium difficile toxin A effects in the rat ileum. Infect Immun 64(12):5225–5232. https://doi.org/10.1128/iai.64.12.5225-5232.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Rea MC, Clayton E, O’Connor PM, Shanahan F, Kiely B, Ross RP, Hill C (2007) Antimicrobial activity of lacticin 3,147 against clinical Clostridium difficile strains. J Med Microbiol 56(7):940–946. https://doi.org/10.1099/jmm.0.47085-0

    Article  CAS  PubMed  Google Scholar 

  69. Draper LA, Cotter PD, Hill C, Ross RP (2013) The two peptide lantibiotic lacticin 3147 acts synergistically with polymyxin to inhibit Gram negative bacteria. BMC Microbiol 13(1):212. https://doi.org/10.1186/1471-2180-13-212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Asahara T, Shimizu K, Nomoto K, Hamabata T, Ozawa A, Takeda Y (2004) Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157:H7. Infect Immun 72(4):2240–2247. https://doi.org/10.1128/IAI.72.4.2240-2247.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kawarizadeh A, Tabatabaei M, Hosseinzadeh S, Farzaneh M, Pourmontaseri M (2019) The effects of probiotic Bacillus coagulans on the cytotoxicity and expression of alpha toxin gene of Clostridium perfringens type A. Anaerobe 59:61–67. https://doi.org/10.1016/j.anaerobe.2019.05.008

    Article  CAS  PubMed  Google Scholar 

  72. Nybom SMK, Dziga D, Heikkilä JE, Kull TPJ, Salminen SJ, Meriluoto JAO (2012) Characterization of microcystin-LR removal process in the presence of probiotic bacteria. Toxicon 59(1):171–181. https://doi.org/10.1016/j.toxicon.2011.11.008

    Article  CAS  PubMed  Google Scholar 

  73. Heikkilä JE, Nybom SMK, Salminen SJ, Meriluoto JAO (2012) Removal of cholera toxin from aqueous solution by probiotic bacteria. Pharmaceuticals 5(6):665–673. https://doi.org/10.3390/ph5060665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Mousavi Khaneghah A, Hashemi Moosavi M, Oliveira CAF, Vanin F, Sant’Ana AS (2020) Electron beam irradiation to reduce the mycotoxin and microbial contaminations of cereal-based products: an overview. Food Chem Toxicol 143:111557. https://doi.org/10.1016/j.fct.2020.111557

    Article  CAS  PubMed  Google Scholar 

  75. Jerushalmi S, Maymon M, Dombrovsky A, Freeman S (2020) Effects of cold plasma, gamma and e-beam irradiations on reduction of fungal colony forming unit levels in medical cannabis inflorescences. J Cannabis Res 2(1):12. https://doi.org/10.1186/s42238-020-00020-6

    Article  PubMed  PubMed Central  Google Scholar 

  76. Mendes-Oliveira G, Jensen JL, Keener KM, Campanella OH (2019) Modeling the inactivation of Bacillus subtilis spores during cold plasma sterilization. Innov Food Sci Emerg Technol 52:334–342. https://doi.org/10.1016/j.ifset.2018.12.011

    Article  CAS  Google Scholar 

  77. Afsah-Hejri L, Hajeb P, Ehsani RJ (2020) Application of ozone for degradation of mycotoxins in food: a review. Compr Rev Food Sci Food Saf 19(4):1777–1808. https://doi.org/10.1111/1541-4337.12594

    Article  CAS  PubMed  Google Scholar 

  78. Nunes VMR, Moosavi M, Mousavi Khaneghah A, Oliveira CAF (2021) Innovative modifications in food processing to reduce the levels of mycotoxins. Curr Opin Food Sci 38:155–161. https://doi.org/10.1016/j.cofs.2020.11.010

    Article  Google Scholar 

  79. Montaseri H, Arjmandtalab S, Dehghanzadeh G, Karami S, Razmjoo M, Sayadi M, Oryan A (2014) Effect of production and storage of probiotic yogurt on aflatoxin M1 residue. J Food Qual Hazards Control 1(1):7–14

    CAS  Google Scholar 

  80. Khalel AS, Khaled JM, Kandeal SA (2012) Enzymatic activity and some molecular properties of Trichosporon mycotoxinivorans yeast and their effects on liver function in mice. Afr J Microbiol Res 6(10):2567–2573. https://doi.org/10.5897/AJMR.9000286

    Article  CAS  Google Scholar 

  81. Hamidi A, Mirnejad R, Yahaghi E, Behnod V, Mirhosseini A, Amani S, Sattari S, Darian EK (2013) The aflatoxin B1 isolating potential of two lactic acid bacteria. Asian Pac J Trop Biomed 3(9):732–736. https://doi.org/10.1016/S2221-1691(13)60147-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Blagojev N, Skrinjar M, Veskovic-Moracanic S, Soso V (2012) Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotechnol Lett 17(3):7219–7226

    CAS  Google Scholar 

  83. Panwar R, Kumar N, Kashyap V, Ram C, Kapila R (2019) Aflatoxin M1 detoxification ability of probiotic lactobacilli of Indian origin in in vitro digestion model. Probiotics Antimicrob Proteins 11(2):460–469. https://doi.org/10.1007/s12602-018-9414-y

  84. Adunphatcharaphon S, Petchkongkaew A, Visessanguan W (2021) In vitro mechanism assessment of zearalenone removal by plant-derived Lactobacillus plantarum BCC 47723. Toxins 13(4):286. https://doi.org/10.3390/toxins13040286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Nesic K, Habschied K, Mastanjevic K (2021) Possibilities for the biological control of mycotoxins in food and feed. Toxins 13(3):198. https://doi.org/10.3390/toxins13030198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Franco T, Garcia S, Hirooka E, Ono Y, Dos Santos J (2011) Lactic acid bacteria in the inhibition of Fusarium graminearum and deoxynivalenol detoxification. J Appl Microbiol 111(3):739–748. https://doi.org/10.1111/j.1365-2672.2011.05074.x

    Article  CAS  PubMed  Google Scholar 

  87. Bianchini A, Bullerman LB (2009) Biological control of molds and mycotoxins in foods. ACS symposium series, Oxford University Press 1031:1–16. https://doi.org/10.1021/bk-2009-1031.ch001

    Article  CAS  Google Scholar 

  88. Lavermicocca P, Valerio F, Evidente A, Lazzaroni S, Corsetti A, Gobbetti M (2000) Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl Environ Microbiol 66(9):4084–4090. https://doi.org/10.1128/AEM.66.9.4084-4090.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Arqués JL, Rodríguez E, Langa S, Landete JM, Medina M (2015) Antimicrobial activity of lactic acid bacteria in dairy products and gut: effect on pathogens. Biomed Res Int 2015:584183. https://doi.org/10.1155/2015/584183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Talarico TL, Dobrogosz WJ (1989) Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri. Antimicrob Agents Chemother 33(5):674–679. https://doi.org/10.1128/AAC.33.5.674

  91. Jorgensen MR, Kragelund C, Po J, Keller MK, Twetman S (2017) Probiotic Lactobacillus reuteri has antifungal effects on oral Candida species in vitro. J Oral Microbiol 9(1):1274582. https://doi.org/10.1080/20002297.2016.1274582

    Article  PubMed  PubMed Central  Google Scholar 

  92. Gourama H, Bullerman LB (1995) Aspergillus flavus and Aspergillus parasiticus: aflatoxigenic fungi of concern in foods and feeds: a review. J Food Prot 58(12):1395–1404. https://doi.org/10.4315/0362-028X-58.12.1395

    Article  CAS  PubMed  Google Scholar 

  93. El-Melegy KM, Abdel-Salam A, Abdel-Shafea Y, Abdel-Rhman A, Abdel-Shafi S (2017) Inhibition of aflatoxin B1 production by bacteria. J Anim Poult Prod 8(5):91–95. https://doi.org/10.21608/JAPPMU.2017.45783

  94. Ghonaimy G, Yonis A, Abol-Ela M (2007) Inhibition of Aspergillus flavus and A. parasiticus fungal growth. J Egyp Soc Toxicol 37:53–60

    Google Scholar 

  95. Boudergue C, Burel C, Dragacci S, Favort MC, Fremy JM, Massimi C, PrigentT P, Debongnie P, Pussemier L, Boudra H (2009) Review of mycotoxin-detoxifying agents used as feed additives: mode of action, efficacy and feed/food safety. EFSA Supporting Publications 6(9):22. https://doi.org/10.2903/sp.efsa.2009.EN-22

    Article  Google Scholar 

  96. Devreese M, De Backer P, Croubels S (2013) Different methods to counteract mycotoxin production and its impact on animal health. Vlaams Diergeneeskd Tijdschr. 82(4):181–190. https://doi.org/10.21825/vdt.v82i4.16695

  97. Haskard CA, El-Nezami HS, Kankaanpaa PE, Salminen S, Ahokas JT (2001) Surface binding of aflatoxin B1 by lactic acid bacteria. Appl Environ Microbiol 67(7):3086–3091. https://doi.org/10.1128/AEM.67.7.3086-3091.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Shah N, Wu X (1999) Aflatoxin B1 binding abilities of probiotic bacteria. Biosci Microbiota 18(1):43–48. https://doi.org/10.12938/bifidus1996.18.43

  99. Kasmani FB, Torshizi K, Allameh A, Shariatmadari F (2012) Aflatoxin detoxification potential of lactic acid bacteria isolated from Iranian poultry. Iran J Vet Res 13(2):152–155

    Google Scholar 

  100. Oluwafemi F, Kumar M, Bandyopadhyay R, Ogunbanwo T, Ayanwande KB (2010) Bio-detoxification of aflatoxin B1 in artificially contaminated maize grains using lactic acid bacteria. Toxin Rev 29:115–122. https://doi.org/10.3109/15569543.2010.512556

    Article  CAS  Google Scholar 

  101. Sohrabi Balsini M, Edalatian Dovom MR, Kadkhodaee R, Habibi Najafi MB, Yavarmanesh M (2021) Effect of digestion and thermal processing on the stability of microbial cell-aflatoxin B1 complex. LWT 142:110994. https://doi.org/10.1016/j.lwt.2021.110994

    Article  CAS  Google Scholar 

  102. Shafiq SA (2015) Using of Iraqi probiotic to detoxify patulin in albino mice. IJIAS 11(2):282

    Google Scholar 

  103. Adami Ghamsari F, Tajabadi Ebrahimi M, Bagheri Varzaneh M, Iranbakhsh A, Akhavan Sepahi A (2021) In vitro reduction of mycotoxin deoxynivalenol by organic adsorbent. J Food Process Preserv 45(3):e15212. https://doi.org/10.1111/jfpp.15212

    Article  CAS  Google Scholar 

  104. Niderkorn V, Boudra H, Morgavi D (2006) Binding of Fusarium mycotoxins by fermentative bacteria in vitro. J Appl Microbiol 101(4):849–856. https://doi.org/10.1111/j.1365-2672.2006.02958.x

    Article  CAS  PubMed  Google Scholar 

  105. Fuchs S, Sontag G, Stidl R, Ehrlich V, Kundi M, Knasmüller S (2008) Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food Chem Toxicol 46(4):1398–1407. https://doi.org/10.1016/j.fct.2007.10.008

    Article  CAS  PubMed  Google Scholar 

  106. Slizewska K, Smulikowska S (2011) Detoxification of aflatoxin B. J Anim Feed Sci 20:300–309. https://doi.org/10.22358/jafs/66187/2011

  107. Elsanhoty RM, Salam SA, Ramadan MF, Badr FH (2014) Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control 43:129–134. https://doi.org/10.1016/j.foodcont.2014.03.002

    Article  CAS  Google Scholar 

  108. Saladino F, Posarelli E, Luz C, Luciano FB, Rodriguez-Estrada MT, Manes J, Meca G (2018) Influence of probiotic microorganisms on aflatoxins B1 and B2 bioaccessibility evaluated with a simulated gastrointestinal digestion. J Food Compost Anal 68:128–132. https://doi.org/10.1016/j.jfca.2017.01.010

    Article  CAS  Google Scholar 

  109. Tajik H, Sayadi M (2020) Effects of probiotic bacteria of Lactobacillus acidophilus and Lactobacillus casei on aflatoxin B1 detoxification within a simulated gastrointestinal tract model. Toxin Rev 0(0):1-8 https://doi.org/10.1080/15569543.2020.1843180

  110. Markowiak P, Slizewska K, Nowak A, Chlebicz A, Zbikowski A, Pawłowski K, Szeleszczuk P (2019) Probiotic microorganisms detoxify ochratoxin A in both a chicken liver cell line and chickens. J Sci Food Agric 99(9):4309–4318. https://doi.org/10.1002/jsfa.9664

    Article  CAS  PubMed  Google Scholar 

  111. Abrunhosa L, Ines A, Rodrigues AI, Guimaraes A, Pereira VL, Parpot P, Mendes-Faia A, Venancio A (2014) Biodegradation of ochratoxin A by Pediococcus parvulus isolated from Douro wines. Int J Food Microbiol 188:45–52. https://doi.org/10.1016/j.ijfoodmicro.2014.07.019

    Article  CAS  PubMed  Google Scholar 

  112. Guo HW, Chang J, Wang P, Yin QQ, Liu CQ, Xu XX, Dang XW, Hu XF, Wang QL (2021) Effects of compound probiotics and aflatoxin-degradation enzyme on alleviating aflatoxin-induced cytotoxicity in chicken embryo primary intestinal epithelium, liver and kidney cells. AMB Express 11(1):35–47. https://doi.org/10.1186/s13568-021-01196-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Liu C, Chang J, Wang P, Yin Q, Huang W, Dang X, Lu F, Gao T (2019) Zearalenone biodegradation by the combination of probiotics with cell-free extracts of Aspergillus oryzae and its mycotoxin-alleviating effect on pig production performance. Toxins 11(10):552. https://doi.org/10.3390/toxins11100552

    Article  CAS  PubMed Central  Google Scholar 

  114. Nybom SM, Salminen SJ, Meriluoto JA (2007) Removal of microcystin-LR by strains of metabolically active probiotic bacteria. FEMS Microbiol Lett 270(1):27–33. https://doi.org/10.1111/j.1574-6968.2007.00644.x

    Article  CAS  PubMed  Google Scholar 

  115. Nybom S, Dziga D, Heikkila J, Kull T, Salminen S, Meriluoto J (2012) Characterization of microcystin-LR removal process in the presence of probiotic bacteria. Toxicon 59(1):171–181. https://doi.org/10.1016/j.toxicon.2011.11.008

    Article  CAS  PubMed  Google Scholar 

  116. Khani S, Hosseini M, H, Taheri M, R Nourani M, A Imani Fooladi A, (2012) Probiotics as an alternative strategy for prevention and treatment of human diseases: a review. Inflamm Allergy Drug Targets 11(2):79–89. https://doi.org/10.2174/187152812800392832

    Article  CAS  PubMed  Google Scholar 

  117. Fooladi AAI, Hosseini HM, Nourani MR, Khani S, Alavian SM (2013) Probiotic as a novel treatment strategy against liver disease. Hepat Mon 13(2):e7521. https://doi.org/10.5812/hepatmon.7521

    Article  Google Scholar 

  118. Aziz I, Mumtaz S, Bholah H, Chowdhury FU, Sanders DS, Ford AC (2015) High prevalence of idiopathic bile acid diarrhea among patients with diarrhea-predominant irritable bowel syndrome based on Rome III criteria. Clin Gastroenterol Hepatol 13:1650–1655. https://doi.org/10.1016/j.cgh.2015.03.002

    Article  PubMed  Google Scholar 

  119. Heyman M, Menard S (2002) Probiotic microorganisms: how they affect intestinal pathophysiology. Cell Mol Life Sci 59(7):1151–1165. https://doi.org/10.1007/s00018-002

  120. Sekhar MS, Unnikrishnan M, Vijayanarayana K, Rodrigues GS, Mukhopadhyay C (2014) Topical application/formulation of probiotics: will it be a novel treatment approach for diabetic foot ulcer? Med Hypotheses 82(1):86–88. https://doi.org/10.1016/j.mehy.2013.11.013

    Article  CAS  Google Scholar 

  121. Castellazzi AM, Valsecchi C, Caimmi S, Licari A, Marseglia A, Leoni MC, Caimmi D, Miraglia del Giudice M, Leonardi S, La Rosa M (2013) Probiotics and food allergy. Ital J Pediatr 39(47):e57

  122. Puri S, Grover S, Puri N, Dewan A, Gupta A (2011) Use of probiotics for oral health. Oral Health Comm Dent 5:149–152. https://doi.org/10.1186/1824-7288-39-47

    Article  CAS  Google Scholar 

  123. Monachese M, Cunningham-Rundles S, Diaz M, Guerrant R, Hummelen R, Kemperman R, Kerac M, Kort R, Merenstein DJ, Panigrahi P (2011) Probiotics and prebiotics to combat enteric infections and HIV in the developing world: a consensus report. Gut Microbes 2(3):198–207. https://doi.org/10.4161/gmic.2.3.16106

    Article  PubMed  Google Scholar 

  124. Fabbri A, Travaglione S, Fiorentini C (2010) Escherichia coli cytotoxic necrotizing factor 1 (CNF1): toxin biology, in vivo applications and therapeutic potential. Toxins 2(2):283–296. https://doi.org/10.3390/toxins2020283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Fukui-Miyazaki A, Kamitani S, Miyake M, Horiguchi Y (2010) Association of Bordetella dermonecrotic toxin with the extracellular matrix. BMC Microbiol 10(1):247. https://doi.org/10.1186/1471-2180-10-247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Duan Q, Xia P, Nandre R, Zhang W, Zhu G (2019) Review of newly identified functions associated with the heat-labile toxin of enterotoxigenic Escherichia coli. Front Cell Infect Microbiol 9:292. https://doi.org/10.3389/fcimb.2019.00292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Abdolamir Ghadaksaz, Somayeh Mousavi Nodoushan, Hamid Sedighian, and Elham Behzadi contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Abdolamir Ghadaksaz

  2. Applied Microbiology Research Center, Systems Biology and Poisonings Institute, Baqiyatallah University of Medical Sciences, Vanak Sq. Molasadra St, Tehran, Iran

    Somayeh Mousavi Nodoushan, Hamid Sedighian & Abbas Ali Imani Fooladi

  3. Department of Microbiology, College of Basic Sciences, Shahr-E-Qods Branch, Islamic Azad University, Tehran, Iran

    Elham Behzadi

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Ghadaksaz, A., Nodoushan, S.M., Sedighian, H. et al. Evaluation of the Role of Probiotics As a New Strategy to Eliminate Microbial Toxins: a Review. Probiotics & Antimicro. Prot. 14, 224–237 (2022). https://doi.org/10.1007/s12602-021-09893-2

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