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An overview of yeast probiotics as cancer biotherapeutics: possible clinical application in colorectal cancer

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Abstract

The previous reports have established a strong link between diet, lifestyle, and gut microbiota population with the onset of the colorectal cancer (CRC). Administration of probiotics has become a particular interest in prevention and treatment of CRC. As potential dietary complements, probiotics might be able to lower the risk of CRC and manage the safety of traditional cancer therapies such as surgery, radiation therapy, and chemotherapy. This review investigates the promising effects of probiotics as biotherapeutics, with due attention to possible clinical application of yeast probiotics in prevention and treatment of CRC. In addition, various underlying anti-cancer mechanisms are covered here based on scientific evidence and findings from numerous experimental studies. Application of probiotics as biotherapeutics in CRC, however, needs to be approved by human clinical trials. It is of prime concern, to find potential probiotic strains, effective doses for administrations and regimes, and molecular mechanisms involved in prevention and treatment.

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References

  1. Cronin KA, Lake AJ, Scott S, Sherman RL, Noone AM, Howlader N, et al. Annual report to the nation on the status of cancer, part I: national cancer statistics. Cancer. 2018;124(13):2785–2800.

    PubMed  Google Scholar 

  2. Bassaganya-Riera J, Hontecillas R. Dietary conjugated linoleic acid and n-3 polyunsaturated fatty acids in inflammatory bowel disease. Curr Opin Clin Nutr Metab Care. 2010;13(5):569–73. https://doi.org/10.1097/MCO.0b013e32833b648e.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. https://doi.org/10.3322/caac.21262.

    Article  PubMed  Google Scholar 

  4. Silva FC, Valentin MD, Ferreira Fde O, Carraro DM, Rossi BM. Mismatch repair genes in Lynch syndrome: a review. Sao Paulo Med J. 2009;127(1):46–51.

    PubMed  Google Scholar 

  5. Sheridan C. Amgen punts on deCODE’s genetics know-how. Nat Biotechnol. 2013;31(2):87–8. https://doi.org/10.1038/nbt0213-87.

    Article  CAS  Google Scholar 

  6. Ghaemmaghami S, Hedayati M, Mohaddes SM, Mohammadi MG, Rahmati M, Zarghami N. Visfatin proliferative effect on HCT-116 colorectal cancer cell line. Adv Environ Biol. 2014;8(9):55–60.

    Google Scholar 

  7. Bagheri R, Sanaat Z, Zarghami N. Synergistic effect of free and nano-encapsulated chrysin-curcumin on inhibition of hTERT gene expression in SW480 colorectal cancer cell line. Drug Res. 2018;68(06):335–43.

    CAS  Google Scholar 

  8. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506.

    PubMed  Google Scholar 

  9. Smith IM, Baker A, Arneborg N, Jespersen L. Non‐S accharomyces yeasts protect against epithelial cell barrier disruption induced by Salmonella enterica subsp. enterica serovar Typhimurium. Lett Appl Microbiol. 2015;61(5):491–7.

    CAS  PubMed  Google Scholar 

  10. Ricci A, Allende A, Bolton D, Chemaly M, Davies R, Girones R, et al. Update of the list of QPS‐recommended biological agents intentionally added to food or feed as notified to EFSA 5: suitability of taxonomic units notified to EFSA until september 2016. EFSA J. 2017;15(3):1–178.

    Google Scholar 

  11. Saber A, Alipour B, Faghfoori Z, Yari KA. Cellular and molecular effects of yeast probiotics on cancer. Crit Rev Microbiol. 2017;43(1):96–115.

    PubMed  Google Scholar 

  12. Moslehi-Jenabian S, Lindegaard L, Jespersen L. Beneficial effects of probiotic and food borne yeasts on human health. Nutrients. 2010;2(4):449–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Pontier-Bres R, Munro P, Boyer L, Anty R, Imbert V, Terciolo C, et al. Saccharomyces boulardii modifies Salmonella typhimurium traffic and host immune responses along the intestinal tract. PLoS ONE. 2014;9(8):e103069.

    PubMed  PubMed Central  Google Scholar 

  14. Bisson J-F, Hidalgo S, Rozan P, Messaoudi M. Preventive effects of different probiotic formulations on travelers’ diarrhea model in wistar rats. Dig Dis Sci. 2010;55(4):911–9.

    PubMed  Google Scholar 

  15. Smith IM, Christensen JE, Arneborg N, Jespersen L. Yeast modulation of human dendritic cell cytokine secretion: an in vitro study. PLoS ONE. 2014;9(5):e96595.

    PubMed  PubMed Central  Google Scholar 

  16. Bin Z, Ya-Zheng X, Zhao-Hui D, Bo C, Li-Rong J, Vandenplas Y. The efficacy of Saccharomyces boulardii CNCM I-745 in addition to standard Helicobacter pylori eradication treatment in children. Pediatr Gastroenterol Hepatol Nutr. 2015;18(1):17–22.

    PubMed  PubMed Central  Google Scholar 

  17. Qamar A, Aboudola S, Warny M, Michetti P, Pothoulakis C, LaMont JT, et al. Saccharomyces boulardii stimulates intestinal immunoglobulin a immune response to clostridium difficiletoxin a in mice. Infect Immun. 2001;69(4):2762–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. McFarland LV. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol. 2010;16(18):2202.

    PubMed  PubMed Central  Google Scholar 

  19. Kogani G, Pajtinka M, Babincova M, Miadokova E, Rauko P, Slamenova D, et al. Yeast cell wall polysaccharides as antioxidants and antimutagens: Can they fight cancer? Minireview. Neoplasma. 2008;55(5):387.

    Google Scholar 

  20. Gedek B. Adherence of Escherichia coli serogroup O 157 and the Salmonella typhimurium mutant DT 104 to the surface of Saccharomyces boulardii. Mycoses. 1999;42(4):261–4.

    CAS  PubMed  Google Scholar 

  21. Martins FS, Vieira AT, Elian SD, Arantes RM, Tiago FC, Sousa LP, et al. Inhibition of tissue inflammation and bacterial translocation as one of the protective mechanisms of Saccharomyces boulardii against Salmonella infection in mice. Microbes Infect. 2013;15(4):270–9.

    CAS  PubMed  Google Scholar 

  22. Chen X, Kokkotou EG, Mustafa N, Bhaskar KR, Sougioultzis S, O’Brien M, et al. Saccharomyces boulardii inhibits ERK1/2 mitogen-activated protein kinase activation both in vitro and in vivo, and protects against Clostridium difficile toxin A-induced enteritis. J Biol Chem. 2006;281(34):24449–54.

    CAS  PubMed  Google Scholar 

  23. Holzapfel WH, Schillinger U. Introduction to pre-and probiotics. Food Res Int. 2002;35(2–3):109–16.

    Google Scholar 

  24. Bromberg-White JL, Andersen NJ, Duesbery NS. MEK genomics in development and disease. Brief Funct Genom. 2012;11(4):300–10.

    CAS  Google Scholar 

  25. Swidsinski A, Loening–Baucke V, Verstraelen H, Osowska S, Doerffel Y. Biostructure of fecal microbiota in healthy subjects and patients with chronic idiopathic diarrhea. Gastroenterology. 2008;135(2):568–79.

    PubMed  Google Scholar 

  26. Yu A-Q, Li L. The potential role of probiotics in cancer prevention and treatment. Nutr Cancer. 2016;68(4):535–44.

    PubMed  Google Scholar 

  27. Chiu Y-H, Hsieh Y-J, Liao K-W, Peng K-C. Preferential promotion of apoptosis of monocytes by Lactobacillus casei rhamnosus soluble factors. Clin Nutr. 2010;29(1):131–40.

    CAS  PubMed  Google Scholar 

  28. Chong ESL. A potential role of probiotics in colorectal cancer prevention: review of possible mechanisms of action. World J Microbiol Biotechnol. 2014;30(2):351–74.

    CAS  PubMed  Google Scholar 

  29. Zhong L, Zhang X, Covasa M. Emerging roles of lactic acid bacteria in protection against colorectal cancer. World J Gastroenterol. 2014;20(24):7878.

    PubMed  PubMed Central  Google Scholar 

  30. Gagnière J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, et al. Gut microbiota imbalance and colorectal cancer. World J Gastroenterol. 2016;22(2):501.

    PubMed  PubMed Central  Google Scholar 

  31. Koi M, Okita Y, Carethers JM. Fusobacterium nucleatum infection in colorectal cancer: linking inflammation, DNA mismatch repair and genetic and epigenetic alterations. J Anus Rectum Colon. 2018;2(2):37–46.

    PubMed  PubMed Central  Google Scholar 

  32. Li S, Konstantinov SR, Smits R, Peppelenbosch MP. Bacterial biofilms in colorectal cancer initiation and progression. Trends Mol Med. 2017;23(1):18–30.

    PubMed  Google Scholar 

  33. Zackular JP, Baxter NT, Chen GY, Schloss PD. Manipulation of the gut microbiota reveals role in colon tumorigenesis. mSphere. 2016;1(1):e00001–e00015.

    PubMed  Google Scholar 

  34. Jurjus A, Eid A, Al Kattar S, Zeenny MN, Gerges-Geagea A, Haydar H, et al. Inflammatory bowel disease, colorectal cancer and type 2 diabetes mellitus: the links. BBA Clin. 2016;5:16–24.

    PubMed  Google Scholar 

  35. Nosho K, Sukawa Y, Adachi Y, Ito M, Mitsuhashi K, Kurihara H, et al. Association of Fusobacterium nucleatum with immunity and molecular alterations in colorectal cancer. World J Gastroenterol. 2016;22(2):557.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Mumy KL, Chen X, Kelly CP, McCormick BA. Saccharomyces boulardii interferes with Shigella pathogenesis by postinvasion signaling events. Am J Physiol-Gastrointest Liver Physiol. 2008;294(3):G599–G609.

    CAS  PubMed  Google Scholar 

  37. Chen X, Fruehauf J, Goldsmith JD, Xu H, Katchar KK, Koon HW, et al. Saccharomyces boulardii inhibits EGF receptor signaling and intestinal tumor growth in Apcmin mice. Gastroenterology. 2009;137(3):914–23.

    CAS  PubMed  Google Scholar 

  38. Chen X, Yang G, Song J-H, Xu H, Li D, Goldsmith J, et al. Probiotic yeast inhibits VEGFR signaling and angiogenesis in intestinal inflammation. PLoS ONE. 2013;8(5):e64227.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Mirone G, Shukla A, Marfe G. Signaling mechanisms of resistance to EGFR-and anti-angiogenic inhibitors cancer. Crit Rev Oncol Hematol. 2016;97:85–95.

    PubMed  Google Scholar 

  40. Ghoneum M, Gollapudi S. Synergistic role of arabinoxylan rice bran (MGN-3/Biobran) in S. cerevisiae-induced apoptosis of monolayer breast cancer MCF-7 cells. Anticancer Res. 2005;25(6B):4187–96.

    CAS  PubMed  Google Scholar 

  41. Ghoneum M, El-Din NKB, Noaman E, Tolentino L. Saccharomyces cerevisiae, the baker’s yeast, suppresses the growth of Ehrlich carcinoma-bearing mice. Cancer Immunol Immunother. 2008;57(4):581–92.

    PubMed  Google Scholar 

  42. Collier C, Carroll J, Ballou M, Starkey J, Sparks J. Oral administration of Saccharomyces cerevisiae boulardii reduces mortality associated with immune and cortisol responses to Escherichia coli endotoxin in pigs. J Anim Sci. 2011;89(1):52–8.

    CAS  PubMed  Google Scholar 

  43. Dalmasso G, Loubat A, Dahan S, Calle G, Rampal P, Czerucka D. Saccharomyces boulardii prevents TNF-α-induced apoptosis in EHEC-infected T84 cells. Res Microbiol. 2006;157(5):456–65.

    CAS  PubMed  Google Scholar 

  44. Dahan S, Dalmasso G, Imbert V, Peyron JF, Rampal P, Czerucka D. Saccharomyces boulardii interferes with enterohemorrhagic Escherichia coli-induced signaling pathways in T84 cells. Infect Immun. 2003;71(2):766–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Pothoulakis C. Review article: anti-inflammatory mechanisms of action of Saccharomyces boulardii. Aliment Pharmacol Ther. 2009;30(8):826–33. https://doi.org/10.1111/j.1365-2036.2009.04102.x.

    Article  CAS  PubMed  Google Scholar 

  46. Buts JP, De Keyser N. Transduction pathways regulating the trophic effects of Saccharomyces boulardii in rat intestinal mucosa. Scand J Gastroenterol. 2010;45(2):175–85. https://doi.org/10.3109/00365520903453141.

    Article  CAS  PubMed  Google Scholar 

  47. Shamekhi S, Abdolalizadeh J, Ostadrahimi A, Mohammadi SA, Barzegari A, Lotfi H, et al. Apoptotic effect of Saccharomyces cerevisiae on human colon cancer SW480 cells by regulation of Akt/NF-kB signaling pathway. Probiotics Antimicrob Proteins. 2019. https://doi.org/10.1007/s12602-019-09528-7.

    Article  Google Scholar 

  48. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357(9255):539–45.

    CAS  PubMed  Google Scholar 

  49. Kao A-P, Wang K-H, Long C-Y, Chai C-Y, Tsai C-F, Hsieh T-H, et al. Interleukin-1β induces cyclooxygenase-2 expression and promotes the invasive ability of human mesenchymal stem cells derived from ovarian endometrioma. Fertil Steril. 2011;96(3):678–84.

    CAS  PubMed  Google Scholar 

  50. Sougioultzis S, Simeonidis S, Bhaskar KR, Chen X, Anton PM, Keates S, et al. Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-κB-mediated IL-8 gene expression. Biochem Biophys Res Commun. 2006;343(1):69–766.

    CAS  PubMed  Google Scholar 

  51. Van der Aa Kühle A, Skovgaard K, Jespersen L. In vitro screening of probiotic properties of Saccharomyces cerevisiae var. boulardii and food-borne Saccharomyces cerevisiae strains. Int J Food Microbiol. 2005;101(1):29–39.

    PubMed  Google Scholar 

  52. Kamada N, Seo S-U, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321.

    CAS  PubMed  Google Scholar 

  53. Yeretssian G. Effector functions of NLRs in the intestine: innate sensing, cell death, and disease. Immunol Res. 2012;54(1–3):25–36.

    CAS  PubMed  Google Scholar 

  54. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012;489(7415):231.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Martins FS, Elian SD, Vieira AT, Tiago FC, Martins AK, Silva FC, et al. Oral treatment with Saccharomyces cerevisiae strain UFMG 905 modulates immune responses and interferes with signal pathways involved in the activation of inflammation in a murine model of typhoid fever. Int J Med Microbiol. 2011;301(4):359–64.

    PubMed  Google Scholar 

  56. Martins AK, Martins FS, Gomes DA, Elian SD, Vieira AT, Teixeira MM, et al. Evaluation of in vitro antagonism and of in vivo immune modulation and protection against pathogenic experimental challenge of two probiotic strains of Bifidobacterium animalis var. lactis. Arch Microbiol. 2010;192(12):995–1003.

    CAS  PubMed  Google Scholar 

  57. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Greten FR, Eckmann L, Greten TF, Park JM, Li Z-W, Egan LJ, et al. IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004;118(3):285–96.

    CAS  PubMed  Google Scholar 

  59. Weston S, Parish C. Modification of lymphocyte migration by mannans and phosphomannans. Different carbohydrate structures control entry of lymphocytes into spleen and lymph nodes. J Immunol. 1991;146(12):4180–6.

    CAS  PubMed  Google Scholar 

  60. Su CG, Wen X, Bailey ST, Jiang W, Rangwala SM, Keilbaugh SA, et al. A novel therapy for colitis utilizing PPAR-γ ligands to inhibit the epithelial inflammatory response. J Clin Investig. 1999;104(4):383–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Foligné B, Dewulf J, Vandekerckove P, Pignède G, Pot B. Probiotic yeasts: anti-inflammatory potential of various non-pathogenic strains in experimental colitis in mice. World J Gastroenterol. 2010;16(17):2134.

    PubMed  PubMed Central  Google Scholar 

  62. Jawhara S, Poulain D. Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically-induced colitis. Med Mycol. 2007;45(8):691–700.

    CAS  PubMed  Google Scholar 

  63. Tiago F, Porto B, Ribeiro N, Moreira L, Arantes R, Vieira A, et al. Effect of Saccharomyces cerevisiae strain UFMG A-905 in experimental model of inflammatory bowel disease. Benef Microbes. 2015;6(6):807–15.

    CAS  PubMed  Google Scholar 

  64. Lee SK, Kim HJ, Chi SG, Jang JY, Nam KD, Kim NH, et al. Saccharomyces boulardii activates expression of peroxisome proliferator-activated receptor-gamma in HT-29 cells. Korean J Gastroenterol Taehan Sohwagi Hakhoe Chi. 2005;45(5):328–34.

    PubMed  Google Scholar 

  65. Hjortmo SB, Hellström AM, Andlid TA. Production of folates by yeasts in Tanzanian fermented togwa. FEMS Yeast Res. 2008;8(5):781–7.

    CAS  PubMed  Google Scholar 

  66. Patring JD, Hjortmo SB, Jastrebova JA, Svensson UK, Andlid TA, Jägerstad IM. Characterization and quantification of folates produced by yeast strains isolated from kefir granules. Eur Food Res Technol. 2006;223(5):633–7.

    CAS  Google Scholar 

  67. Patring JD, Jastrebova JA, Hjortmo SB, Andlid TA, Jägerstad IM. Development of a simplified method for the determination of folates in baker's yeast by HPLC with ultraviolet and fluorescence detection. J Agric Food Chem. 2005;53(7):2406–11.

    CAS  PubMed  Google Scholar 

  68. Choi S-W, Mason JB. Folate and carcinogenesis: an integrated scheme1–3. J Nutr. 2000;130(2):129–32.

    CAS  PubMed  Google Scholar 

  69. Thakur S, Thakur SD, Wani NA, Kaur J. Reduced expression of folate transporters in kidney of a rat model of folate oversupplementation. Genes Nutr. 2014;9(1):369.

    PubMed  Google Scholar 

  70. Bishehsari F, Mahdavinia M, Vacca M, Malekzadeh R, Mariani-Costantini R. Epidemiological transition of colorectal cancer in developing countries: environmental factors, molecular pathways, and opportunities for prevention. World J Gastroenterol. 2014;20(20):6055.

    PubMed  PubMed Central  Google Scholar 

  71. Takata Y, Shrubsole MJ, Li H, Cai Q, Gao J, Wagner C, et al. Plasma folate concentrations and colorectal cancer risk: a case-control study nested within the Shanghai Men's Health Study. Int J Cancer. 2014;135(9):2191–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Liu Z, Choi SW, Crott JW, Smith DE, Mason JB. Multiple B-vitamin inadequacy amplifies alterations induced by folate depletion in p53 expression and its downstream effector MDM2. Int J Cancer. 2008;123(3):519–25.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Vetvicka V, Volny T, Saraswat-Ohri S, Vashishta A, Vancikova Z, Vetvickova J. Glucan and resveratrol complex–possible synergistic effects on immune system. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2007;151(1):41–6.

    CAS  Google Scholar 

  74. Jabber AJ. The effect of beta glucan extract of Saccharomyces cerevieses on cancer cell growth in vitro. Iraqi J Cancer Med Genet. 2018;5(1):53–8.

    Google Scholar 

  75. Javmen A, Grigiškis S, Gliebutė R. β-glucan extraction from Saccharomyces cerevisiae yeast using Actinomyces rutgersensis 88 yeast lyzing enzymatic complex. Biologija. 2012;58(2):51–9.

    CAS  Google Scholar 

  76. Song HS, Moon K-Y. In vitro antioxidant activity profiles of β-glucans isolated from yeast Saccharomyces cerevisiae and mutant Saccharomyces cerevisiae IS2. Food Sci Biotechnol. 2006;15(3):437–40.

    CAS  Google Scholar 

  77. Novak M, Vetvicka V. Glucans as biological response modifiers. Endocr Metab Immune Disord-Drug Targets. 2009;9(1):67–75.

    CAS  PubMed  Google Scholar 

  78. Carpenter K, Breslin W, Davidson T, Adams A, McFarlin B. Baker’s yeast β-glucan supplementation increases monocytes and cytokines post-exercise: implications for infection risk? Br J Nutr. 2013;109(3):478–86.

    CAS  PubMed  Google Scholar 

  79. Zhang M, Kim JA, Huang AY-C. Optimizing tumor microenvironment for cancer immunotherapy: β-glucan-based nanoparticles. Front Immunol. 2018;9:341.

    PubMed  PubMed Central  Google Scholar 

  80. Volman JJ, Ramakers JD, Plat J. Dietary modulation of immune function by β-glucans. Physiol Behav. 2008;94(2):276–84.

    CAS  PubMed  Google Scholar 

  81. Zhao W, Liu Y, Latta M, Ma W, Wu Z, Chen P. Probiotics database: a potential source of fermented foods. Int J Food Prop. 2019;22(1):198–217.

    Google Scholar 

  82. Tao L, Wang B, Zhong Y, Pow SH, Zeng X, Qin C, et al. Database and bioinformatics studies of probiotics. J Agric Food Chem. 2017;65(35):7599–606.

    CAS  PubMed  Google Scholar 

  83. Fortin O, Aguilar-Uscanga B, Vu KD, Salmieri S, Lacroix M. Cancer chemopreventive, antiproliferative, and superoxide anion scavenging properties of Kluyveromyces marxianus and Saccharomyces cerevisiae var. boulardii cell wall components. Nutr Cancer. 2018;70(1):83–96.

    CAS  PubMed  Google Scholar 

  84. Yoon TJ, Kim TJ, Lee H, Shin KS, Yun YP, Moon WK, et al. Anti-tumor metastatic activity of beta-glucan purified from mutated Saccharomyces cerevisiae. Int Immunopharmacol. 2008;8(1):36–42. https://doi.org/10.1016/j.intimp.2007.10.005.

    Article  CAS  PubMed  Google Scholar 

  85. Kim MJ, Hong SY, Kim SK, Cheong C, Park HJ, Chun HK, et al. β-Glucan enhanced apoptosis in human colon cancer cells SNU-C4. Nutr Res Pract. 2009;3(3):180–4. https://doi.org/10.4162/nrp.2009.3.3.180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Magnani M, Castro-Gomez RH, Nobrega Aoki M, Pereira Gregório E, Libos F, Ehara Watanabe MA. Effects of carboxymethyl-glucan from Saccharomyces cerevisiae on the peripheral blood cells of patients with advanced prostate cancer. Exp Ther Med. 2010;1(5):859–62.

    CAS  Google Scholar 

  87. Liu F, Wang Z, Liu J, Li W. Radioprotective effect of orally administered beta-d-glucan derived from Saccharomyces cerevisiae. Int J Biol Macromol. 2018;115:572–9.

    CAS  PubMed  Google Scholar 

  88. Kotzampassi K, Stavrou G, Damoraki G, Georgitsi M, Basdanis G, Tsaousi G, et al. A four-probiotics regimen reduces postoperative complications after colorectal surgery: a randomized, double-blind, placebo-controlled study. World J Surg. 2015;39(11):2776–833.

    PubMed  Google Scholar 

  89. Consoli MLD, da Silva RS, Nicoli JR, Bruña-Romero O, da Silva RG, de Vasconcelos GS, et al. Randomized clinical trial: impact of oral administration of Saccharomyces boulardii on gene expression of intestinal cytokines in patients undergoing colon resection. J Parenter Enter Nutr. 2016;40(8):1114–21.

    CAS  Google Scholar 

  90. Williams NT. Probiotics. Am J Health Syst Pharm. 2010;67(6):449–58.

    CAS  PubMed  Google Scholar 

  91. Kothari D, Patel S, Kim S-K. Probiotic supplements might not be universally-effective and safe: a review. Biomed Pharmacother. 2019;111:537–47.

    CAS  PubMed  Google Scholar 

  92. Saber A, Alipour B, Faghfoori Z, Khosroushahi AY. Secretion metabolites of dairy Kluyveromyces marxianus AS41 isolated as probiotic, induces apoptosis in different human cancer cell lines and exhibit anti-pathogenic effects. J Funct Foods. 2017;34:408–21.

    CAS  Google Scholar 

  93. Saber A, Alipour B, Faghfoori Z, Khosroushahi AY. Secretion metabolites of probiotic yeast, Pichia kudriavzevii AS-12, induces apoptosis pathways in human colorectal cancer cell lines. Nutr Res. 2017;41:36–46.

    CAS  PubMed  Google Scholar 

  94. Rajan T, Benluvankar V, Vincent S. Saccharomyces cerevisiae-induced apoptosis of monolayer cervical cancer cells. Asian J Pharm Clin Res. 2017;10(8):63–6.

    CAS  Google Scholar 

  95. Fortin O, Aguilar-Uscanga BR, Vu KD, Salmieri S, Lacroix M. Effect of Saccharomyces boulardii cell wall extracts on colon cancer prevention in male F344 rats treated with 1, 2-dimethylhydrazine. Nutr Cancer. 2018;70(4):632–42.

    CAS  PubMed  Google Scholar 

  96. Mo L, Chen Y, Li W, Guo S, Wang X, An H, et al. Anti-tumor effects of (1→3)-β-d-glucan from Saccharomyces cerevisiae in S180 tumor-bearing mice. Int J Biol Macromol. 2017;95:385–92.

    CAS  PubMed  Google Scholar 

  97. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14(2):195–206.

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut. 2014;63(12):1932–42.

    CAS  PubMed  Google Scholar 

  99. Kuboniwa M, Hasegawa Y, Mao S, Shizukuishi S, Amano A, Lamont RJ, et al. P. gingivalis accelerates gingival epithelial cell progression through the cell cycle. Microbes Infect. 2008;10(2):122–8.

    CAS  PubMed  Google Scholar 

  100. Kara I, Yildirim F, Ozgen O, Erganis S, Aydogdu M, Dizbay M, et al. Saccharomyces cerevisiae fungemia after probiotic treatment in an intensive care unit patient. Journal Mycol Med. 2018;28(1):218–21. https://doi.org/10.1016/j.mycmed.2017.09.003.

    Article  CAS  Google Scholar 

  101. Eren Z, Gurol Y, Sonmezoglu M, Eren HS, Celik G, Kantarci G. Saccharomyces cerevisiae fungemia in an elderly patient following probiotic treatment. Mikrobiyol Bul. 2014;48(2):351–5. https://doi.org/10.5578/mb.6970.

    Article  PubMed  Google Scholar 

  102. Cesaro S, Chinello P, Rossi L, Zanesco L. Saccharomyces cerevisiae fungemia in a neutropenic patient treated with Saccharomyces boulardii. Support Care Cancer. 2000;8(6):504–5. https://doi.org/10.1007/s005200000123.

    Article  CAS  PubMed  Google Scholar 

  103. Lestin F, Pertschy A, Rimek D. Fungemia after oral treatment with Saccharomyces boulardii in a patient with multiple comorbidities. Dtsch Med Wochenschr (1946). 2003;128(48):2531–3. https://doi.org/10.1055/s-2003-44948.

    Article  CAS  Google Scholar 

  104. Landaburu MF, Lopez Daneri GA, Relloso S, Zarlenga LJ, Vinante MA, Mujica MT. Fungemia following Saccharomyces cerevisiae var. boulardii probiotic treatment in an elderly patient. Rev Argent Microbiol. 2019. https://doi.org/10.1016/j.ram.2019.04.002.

    Article  PubMed  Google Scholar 

  105. Henry S, D'Hondt L, Andre M, Holemans X, Canon JL. Saccharomyces cerevisiae fungemia in a head and neck cancer patient: a case report and review of the literature. Acta Clin Belg. 2004;59(4):220–2. https://doi.org/10.1179/acb.2004.032.

    Article  CAS  PubMed  Google Scholar 

  106. Hennequin C, Kauffmann-Lacroix C, Jobert A, Viard J, Ricour C, Jacquemin J, et al. Possible role of catheters in Saccharomyces boulardii fungemia. Eur J Clin Microbiol Infect Dis. 2000;19(1):16–20.

    CAS  PubMed  Google Scholar 

  107. Riquelme AJ, Calvo MA, Guzmán AM, Depix MS, García P, Pérez C, et al. Saccharomyces cerevisiae fungemia after Saccharomyces boulardii treatment in immunocompromised patients. J Clin Gastroenterol. 2003;36(1):41–3.

    PubMed  Google Scholar 

  108. Ohishi A, Takahashi S, Ito Y, Ohishi Y, Tsukamoto K, Nanba Y, et al. Bifidobacterium septicemia associated with postoperative probiotic therapy in a neonate with omphalocele. J Pediatr. 2010;156(4):679–81.

    PubMed  Google Scholar 

  109. Molinaro M, Aiazzi M, La AT, Cini E, Banfi R. Lactobacillus rhamnosus sepsis in a preterm infant associated with probiotic integrator use: a case report. Recent Prog Med. 2016;107(9):485–6.

    Google Scholar 

  110. Naqvi S, Nagendra V, Hofmeyr A. Probiotic related Lactobacillus rhamnosus endocarditis in a patient with liver cirrhosis. IDCases. 2018;13:e00439.

    CAS  PubMed  Google Scholar 

  111. Sherid M, Samo S, Sulaiman S, Husein H, Sifuentes H, Sridhar S. Liver abscess and bacteremia caused by lactobacillus: role of probiotics? Case report and review of the literature. BMC Gastroenterol. 2016;16(1):138.

    PubMed  PubMed Central  Google Scholar 

  112. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet (London, England). 2008;371(9613):651–9. https://doi.org/10.1016/s0140-6736(08)60207-x.

    Article  Google Scholar 

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Acknowledgements

This is a report of database from Ph.D. thesis of S. Shamekhi registered in Nutrition Research Center, Tabriz University of Medical Sciences, Tabriz, Iran (Grant no: 5/71/1228, Thesis no: 95/4-1/2).

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Shamekhi, S., Lotfi, H., Abdolalizadeh, J. et al. An overview of yeast probiotics as cancer biotherapeutics: possible clinical application in colorectal cancer. Clin Transl Oncol 22, 1227–1239 (2020). https://doi.org/10.1007/s12094-019-02270-0

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