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Cited by 282Probiotics and Fermented FoodsGut microbiota and healthCancer Research and Treatments

The Role of Probiotics in Cancer Prevention

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Śliżewska, Katarzyna, Markowiak-Kopeć, Paulina, Śliżewska, Weronika·2020·Cancers
DOI 10.3390/cancers13010020PMC PMC7793079
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Abstract

The gut microbiome can play important role in maintaining homeostasis in the human body. An imbalance in the gut microbiome can lead to pro-inflammatory immune responses and the initiation of disease processes, including cancer. The research results prove some strains of probiotics by modulating intestinal microbiota and immune response can be used for cancer prevention or/and as adjuvant treatment during anticancer chemotherapy. This review presents the latest advances in research into the effectiveness of probiotics in the prevention and treatment support of cancer. The described issues concern to the anticancer activity of probiotic microorganisms and their metabolites. In addition, we described the potential mechanisms of probiotic chemoprevention and the advisability of using probiotics.

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  • Complementary approaches such as prebiotics, probiotics, postbiotics, and fecal microbiota transplantation are under active investigation for their ability to reshape microbial communities.

    “Complementary approaches such as prebiotics, probiotics, postbiotics, and fecal microbiota transplantation are under active investigation for their ability to reshape microbial communities [69,70]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [70]

    The Introduction and section 3.1 describe probiotics as a way to alter gut microbiota composition and report clinical studies investigating that effect (page numbers unavailable). Our copy does not substantiate the same claim for prebiotics, postbiotics, or fecal microbiota transplantation; searches for those terms found no relevant discussion beyond references mentioning prebiotics. (LLM, conf=0.85)

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References 139 · Cited by 282

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  1. [2]Gonzalez A. Stombaugh J. Lozupone C. Turnbaugh P.J. Gordon J.I. Knight R. The mind-body-microbial continuum. Dialogues Clin. Neurosci. 2011 13 55 62 PMC3139398 21485746
  2. [3]Snyder L. Peter J.E. Henkin T.M. Champress W. Molecular Genetics of Bacteria 4th ed. ASM Press Washington, DC, USA 1997 53 66
  3. [4]Joseph N. Vasodavan K. Saipudin N.A. Yusof B.N.M. Kumar S. Nordin S.A. Gut microbiota and short-chain fatty acids (SCFAs) profiles of normal and overweight school children in Selangor after probiotics administration J. Funct. Foods 2009 57 103 111 10.1016/j.jff.2019.03.042 · DOI
  4. [6]Goodman B. Gardner H. The microbiome and cancer J. Pathol. 2018 244 667 676 10.1002/path.5047 29377130 · DOI · Paper page
  5. [8]Hill C. Guarner F. Reid G. Gibson G.R. Merenstein D.J. Pot B. Morelli L. Canani R.B. Flint H.J. Salminen S. 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 11 506 514 10.1038/nrgastro.2014.66 24912386 · DOI
  6. [10]Goldin B.R. Gorbach S.L. Effect of Lactobacillus acidophilus dietary supplements on 1,2-dimethylhydrazine dihydrochloride-induced intestinal cancer in rats J. Natl. Cancer Inst. 1980 64 263 265 10.1093/jnci/64.2.263 6766509 · DOI
  7. [11]Altonsy M.O. Andrews S.C. Tuohy K.M. Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: Mediation by the mitochondrial pathway Int. J. Food Microbiol. 2010 137 190 203 10.1016/j.ijfoodmicro.2009.11.015 20036023 · DOI
  8. [12]Borowicki A. Michelmann A. Stein K. Scharlau D. Scheu K. Fermented wheat aleurone enriched with probiotic strains LGG and Bb12 modulates markers of tumor progression in human colon cells Nutr. Cancer. 2011 63 151 160 10.1080/01635581.2010.516874 21161821 · DOI
  9. [13]Orlando A. Refolo M.G. Messa C. Amati L. Lavermicocca P. Guerra V. Russo F. Antiproliferative and proapoptotic effects of viable or heat-killed Lactobacillus paracasei IMPC2.1 and Lactobacillus rhamnosus GG in HGC-27 gastric and DLD-1 colon cell lines Nutr. Cancer 2012 64 1103 1111 10.1080/01635581.2012.717676 23061912 · DOI
  10. [14]Russo F. Orlando A. Linsalata M. Cavallini A. Messa C. Effects of Lactobacillus rhamnosus GG on the cell growth and polyamine metabolism in HGC-27 human gastric cancer cells Nutr. Cancer. 2007 59 106 114 10.1080/01635580701365084 17927509 · DOI
  11. [15]Sadeghi-Aliabadi H. Mohammadi F. Fazeli H. Mirlohi M. Effects of Lactobacillus plantarum A7 with probiotic potential on colon cancer and normal cells proliferation in comparison with a commercial strain Iran. J. Basic. Med. Sci. 2014 17 815 819 25729553 PMC4340992
  12. [16]Lopez M. Li N. Kataria J. Russell M. Neu J. Live and ultraviolet-inactivated Lactobacillus rhamnosus GG decrease flagellin-induced interleukin-8 production in Caco-2 cells J. Nutr. 2008 138 2264 2268 10.3945/jn.108.093658 18936229 · DOI
  13. [18]Lee J.W. Shin J.G. Kim E.H. Kang H.E. Yim I.B. Kim J.Y. Joo H.G. Woo H.J. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum J. Vet. Sci. 2004 5 41 48 10.4142/jvs.2004.5.1.41 15028884 · DOI · Paper page
  14. [19]Ma E.L. Choi Y.J. Choi J. Pothoulakis C. Rhee S.H. Imet E. The anticancer effect of probiotic Bacillus polyfermenticus on human colon cancer cells is mediated through ErbB2 and ErbB3 inhibition Int. J. Cancer. 2010 127 780 790 19876926 PMC4420487
  15. [20]Saxami G. Karapetsas A. Lamprianidou E. Kotsianidis I. Chlichlia A. Tassou C. Zoumpourliset V. Galanis A. Two potential probiotic lactobacillus strains isolated from olive microbiota exhibit adhesion and anti-proliferative effects in cancer cell lines J. Funct. Foods 2016 24 461 471 10.1016/j.jff.2016.04.036 · DOI · Paper page
  16. [21]Tiptiri-Kourpeti A. Spyridopoulou K. Santarmaki V. Aindelis G. Tompoulidou E. Lampranidou E. Saxami G. Ypsilantis P. Lampri E. Simopoulos C. Lactobacillus casei exerts anti-proliferative effects accompanied by apoptotic cell death and up-regulation of TRAIL in colon carcinoma cells PLoS ONE 2016 11 e0147960 10.1371/journal.pone.0147960 26849051 PMC4744000 · DOI
  17. [22]Han K.J. Lee N.K. Park H. Paik H.D. Anticancer and anti-inflammatory activity of probiotic Lactococcus lactis nk34 J. Microbiol. Biotechnol. 2015 25 1697 1701 10.4014/jmb.1503.03033 26165315 · DOI
  18. [23]Lee N.K. Son S.H. Jeon E.B. Jung G.H. Lee J.Y. Paik H.D. The prophylactic effect of probiotic Bacillus polyfermenticus KU3 against cancer cells J. Funct. Foods 2015 14 513 518 10.1016/j.jff.2015.02.019 · DOI
  19. [24]Chen Z.F. Ai L.Y. Wang J.L. Ren L.L. Yu Y.N. Xu J. Chen H.Y. Yu J. Li M. Qin W.X. Probiotics Clostridium butyricum and Bacillus subtilis ameliorate intestinal tumorigenesis Future. Microbiol. 2015 10 1433 1445 10.2217/fmb.15.66 26346930 · DOI
  20. [25]Ghoneum M. Gimzewski J. Apoptotic effect of a novel kefir product, PFT, on multidrug-resistant myeloid leukemia cells via a hole-piercing mechanism Int. J. Oncol. 2014 44 830 837 10.3892/ijo.2014.2258 24430613 PMC3928472 · DOI
  21. [26]Thirabunyanon M. Hongwittayakorn P. Potential probiotic lactic acid bacteria of human origin induce antiproliferation of colon cancer cells via synergic actions in adhesion to cancer cells and short-chain fatty acid bioproduction Appl. Biochem. Biotechnol. 2013 169 511 525 10.1007/s12010-012-9995-y 23239414 · DOI · Paper page
  22. [27]Cousin F.J. Jouan-Lanhouet S. Dimanche-Boitrel M.T. Corcos L. Jan G. Milk fermented by Propionibacterium freudenreichii induces apoptosis of HGT-1 human gastric cancer cells PLoS ONE 2012 7 31892 10.1371/journal.pone.0031892 22442660 PMC3307715 · DOI
  23. [28]Kim Y. Oh S. Yun H.S. Oh S. Kim S.H. Cell-bound exopolysaccharide from probiotic bacteria induces autophagic cell death of tumour cells Lett. Appl. Microbiol. 2010 51 123 130 10.1111/j.1472-765X.2010.02859.x 20536712 · DOI
  24. [29]Castro M.S. Molina M.A. Di Sciullo P. Azpiroz M.B. Leocata Nieto F. Sterín-Speziale N.B. Mongini C. Manghi M.A. Beneficial activity of Enterococcus faecalis CECT7121 in the anti-lymphoma protective response J. Appl. Microbiol. 2010 109 1234 1243 10.1111/j.1365-2672.2010.04747.x 20477887 · DOI
  25. [30]Thirabunyanon M. Boonprasom P. Niamsup P. Probiotic potential of lactic acid bacteria isolated from fermented dairy milks on antiproliferation of colon cancer cells Biotechnol. Lett. 2009 31 571 576 10.1007/s10529-008-9902-3 19116692 · DOI
  26. [31]Iyer C. Kosters A. Sethi G. Kunnumakkara A.B. Aggarwal B.B. Versalovic J. Probiotic Lactobacillus reuteri promotes TNFinduced apoptosis in human myeloid leukemia-derived cells by modulation of NF-kappaB and MAPK signalling Cell. Microbiol. 2008 10 1442 1452 10.1111/j.1462-5822.2008.01137.x 18331465 · DOI
  27. [32]Kim Y. Lee D. Kim D. Cho J. Yang J. Chung M. Kim K. Ha N. Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212 Arch. Pharm. Res. 2008 31 468 473 10.1007/s12272-001-1180-y 18449504 · DOI
  28. [34]Dubey V. Ghosh A.R. Bishayee K. Khuda-Bukhsh A.R. Appraisal of the anti-cancer potential of probiotic Pediococcus pentosaceus GS4 against colon cancer: In vitro and in vivo approaches J. Funct. Foods 2016 23 66 79 10.1016/j.jff.2016.02.032 · DOI
  29. [35]Talero E. Bolivar S. Ávila-Román J. Alcaide A. Fiorucci S. Motilva V. Inhibition of chronic ulcerative colitis-associated adenocarcinoma development in mice by VSL#3 Inflamm. Bowel. Dis. 2015 21 1027 1037 25793324
  30. [36]Lenoir M. del Carmen S. Cortes-Perez N.G. Lozano-Ojalvo D. Muñoz-Provencio D. Chain F. Langella P. de Moreno de LeBlanc A. LeBlanc J.G. Bermúdez-Humarán L.G. Lactobacillus casei BL23 regulates Tregand Th17 T-cell populations and reduces DMH-associated colorectal cancer J. Gastroenterol. 2016 51 862 873 10.1007/s00535-015-1158-9 26749362 · DOI · Paper page
  31. [37]Gamallat Y. Meyiah A. Kuugbee E.D. Chiwala G. Awadasseid A. Bamba D. Zhang X. Shang X. Luo F. Xin Y. Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model Biomed. Pharmacother. 2016 83 536 541 10.1016/j.biopha.2016.07.001 27447122 · DOI · Paper page
  32. [38]Kuugbee E.D. Shang X. Gamallat Y. Bamba D. Awadasseid A. Suliman M.A. Zang S. Ma Y. Chiwala G. Xin Y. Structural change in microbiota by a probiotic cocktail enhances the gut barier and reduces cancer via TLR2 signaling in a rat model of colon cancer Dig. Dis. Sci. 2016 61 2908 2920 10.1007/s10620-016-4238-7 27384052 · DOI
  33. [39]Zhang M. Fan X. Fang B. Zhu C. Zhu J. Ren F. Effects of Lactobacillus salivarius Ren on cancer prevention and intestinal microbiota in 1, 2-dimethylhydrazine-induced rat model J. Microbiol. 2015 53 398 405 10.1007/s12275-015-5046-z 26025172 · DOI
  34. [40]Walia S. Kamal R. Dhawan D.K. Kanwar S.S. Chemoprevention by probiotics during 1,2-dimethylhydrazine-induced colon carcinogenesis in rats Dig. Dis. Sci. 2018 63 900 909 10.1007/s10620-018-4949-z 29427224 · DOI
  35. [42]Verma A. Shukla G. Synbiotic (Lactobacillus rhamnosus + Lactobacillus acidophilus + inulin) attenuates oxidative stress and colonic damage in 1,2 dimethylhydrazine dihydrochloride-induced colon carcinogenesis in Sprague’ Dawley rats: A long-term study Eur. J. Cancer Prev. 2014 23 550 559 10.1097/CEJ.0000000000000054 25025584 · DOI
  36. [43]Chang J.H. Shim Y.Y. Cha S.K. Reaney M.J.T. Chee K.M. Effect of Lactobacillus acidophilus KFRI342 on the development of chemically induced precancerous growths in the rat colon J. Med. Microbiol. 2012 61 361 368 10.1099/jmm.0.035154-0 22034161 · DOI
  37. [44]Gosai V. Ambalam P. Raman M. Kothari C.R. Kothari R.K. Vyas B.R.M. Sheth N.R. Protective effect of Lactobacillus rhamnosus 231 against N-Methyl-N’-nitro-N-nitrosoguanidine in animal model Gut Microbes 2011 2 319 325 10.4161/gmic.18755 22157237 · DOI
  38. [45]Appleyard C.B. Cruz M.L. Isidro A.A. Arthur J.C. Jobin C. De Simone C. Pretreatment with the probiotic VSL#3 delays transition from inflammation to dysplasia in a rat model of colitis-associated cancer Am. J. Physiol. Liver Physiol. 2011 301 G1004 G1013 PMC3233787 21903764
  39. [46]Bertkova I. Hijova E. Chmelarova A. Mojzisova G. Petrasova D. Strojny L. Bomba A. Zitnan R. The effect of probiotic microorganisms and bioactive compounds on chemically induced carcinogenesis in rats Neoplasma 2010 57 422 428 10.4149/neo_2010_05_422 20568896 · DOI
  40. [47]Kumar A. Singh N.K. Sinha P.R. Inhibition of 1,2-dimethylhydrazine induced colon genotoxicity in rats by the administration of probiotic curd Mol. Biol. Rep. 2010 37 1373 1376 10.1007/s11033-009-9519-1 19330535 · DOI
  41. [48]Park E. Jeon G.I. Park J.S. Paik H.D. A probiotic strain of Bacillus polyfermenticus reduces DMH induced precancerous lesions in F344 male Rat. Biol. Pharm. Bull. 2007 30 569 574 10.1248/bpb.30.569 17329858 · DOI
  42. [49]Rafter J. Bennett M. Caderni G. Clune Y. Hughes R. Karlsson P. Klinder A. O’Riordan M. O’Sullivan G. Pool-Zobel B. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients Am. J. Clin. Nutr. 2007 85 488 496 10.1093/ajcn/85.2.488 17284748 · DOI
  43. [50]Zhong L. Zhang X. Covasa M. Emerging roles of lactic acid bacteria in protection against colorectal cancer World J. Gastroenterol. 2014 20 7878 7886 10.3748/wjg.v20.i24.7878 24976724 PMC4069315 · DOI
  44. [51]Ohigashi S. Hoshino Y. Ohde S. Onodera H. Functional outcome, quality of life, and efficacy of probiotics in postoperative patients with colorectal cancer Surg. Today 2011 41 1200 1206 10.1007/s00595-010-4450-6 21874415 · DOI
  45. [52]Liu Z. Qin H. Yang Z. Xia Y. Liu W. Yang J. Jiang Y. Zhang H. Wang Y. Zheng Q. Randomized clinical trial: The effects of perioperative probiotic treatment on barrier function and post-operative infectious complications in colorectal cancer surgery-A double-blind study Aliment. Pharmacol. Ther. 2011 33 50 63 10.1111/j.1365-2036.2010.04492.x 21083585 · DOI
  46. [53]Österlund P. Ruotsalainen T. Korpela R. Saxelin M. Ollus A. Valta P. Kouri M. Elomaa I. Joensuu H. Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: A randomised study Br. J. Cancer 2007 97 1028 1034 10.1038/sj.bjc.6603990 17895895 PMC2360429 · DOI
  47. [54]El-Nezami H.S. Polychronaki N.N. Ma J. Zhu H. Ling W. Salminen E.K. Juvonen R.O. Salminen S.J. Poussa T. Mykkänen H.M. Probiotic supplementation reduces a biomarker for increased risk of liver cancer in young men from Southern China Am. J. Clin. Nutr. 2006 83 1199 1203 10.1093/ajcn/83.5.1199 16685066 · DOI · Paper page
  48. [55]Rasouli B.S. Ghadimi-Darsajini A. Nekouian R. Iragian G.R. In vitro activity of probiotic Lactobacillus reuteri against gastric cancer progression by downregulation of urokinase plasminogen activator/urokinase plasminogen activator receptor gene expression J. Cancer Res. Ther. 2017 13 246 251 28643742
  49. [56]Ghoneum M. Felo N. Selective induction of apoptosis in human gastric cancer cells by Lactobacillus kefiri (PFT), a novel kefir product Oncol. Rep. 2015 34 1659 1666 10.3892/or.2015.4180 26251956 PMC4564078 · DOI
  50. [57]Chitapanarux I. Chitapanarux T. Traisathit P. Kudumpee S. Tharavichitkul E. Lorvidhaya V. Randomized controlled trial of live Lactobacillus acidophilus plus Bifidobacterium bifidum in prophylaxis of diarrhea during radiotherapy in cervical cancer patients Radiat. Oncol. 2010 5 31 10.1186/1748-717X-5-31 20444243 PMC2874795 · DOI
  51. [58]Toi M. Hirota S. Tomotaki A. Probiotic beverage with soy isoflavone consumption for breast cancer prevention: A case-control study Curr. Nutr. Food Sci. 2013 9 194 200 10.2174/15734013113099990001 23966890 PMC3744907 · DOI
  52. [59]Pala V. Sieri S. Berrino F. Vineis P. Sacerdote C. Palli D. Masala G. Panico S. Mattiello A. Tumino R. Yogurt consumption and risk of colorectal cancer in the Italian European prospective investigation into cancer and nutrition cohort Int. J. Cancer 2011 129 2712 2719 10.1002/ijc.26193 21607947 · DOI
  53. [60]Ohara T. Yoshino K. Kitajima M. Possibility of preventing colorectal carcinogenesis with probiotics Hepatogastroenterol 2010 57 1411 1415 21443095
  54. [61]Hatakka K. Holma R. El-Nezami H. Suomalainen T. Kuisma M. Saxelin M. Poussa T. Mykkänen H. Korpela R. The influence of Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp. shermanii JS on potentially carcinogenic bacterial activity in human colon Int. J. Food Microbiol. 2008 128 406 410 10.1016/j.ijfoodmicro.2008.09.010 18945506 · DOI
  55. [62]Ohashi Y. Nakai S. Tsukamoto T. Habitual intake of lactic acid bacteria and risk reduction of bladder cancer Urol. Int. 2002 68 273 280 10.1159/000058450 12053032 · DOI
  56. [63]Kotzampassi K. Stavrou G. Damoraki G. Georgitsi M. Basdanis G. Tsaousi G. Giamarellos-Bourboulis E.J. A four-probiotics regimen reduces postoperative complications after colorectal surgery: A randomized, double-blind, placebo-controlled study World J. Surg. 2015 39 2776 2783 10.1007/s00268-015-3071-z 25894405 · DOI
  57. [64]Liu Z.H. Huang M.J. Zhang X.W. Wang L. Huang N.Q. Peng H. Lan P. Peng J.S. Yang Z. Xia Y. The effects of perioperative probiotic treatment on serum zonulin concentration and subsequent postoperative infectious complications after colorectal cancer surgery: A double-center and doubleblind randomized clinical trial Am. J. Clin. Nutr. 2013 97 117 126 10.3945/ajcn.112.040949 23235200 · DOI
  58. [65]Zhang J.W. Peng D. Yang B.R. Gao J. Fang W.J. Ying C.M. Preoperative probiotics decrease postoperative infectious complications of colorectal cancer Am. J. M. Sci. 2012 343 199 205 10.1097/MAJ.0b013e31823aace6 22197980 · DOI
  59. [66]Wada M. Nagata S. Saito M. Shimizu T. Yamashiro Y. Matsuki T. Asahara T. Nomoto K. Effects of the enteral administration of Bifidobacterium breve on patients undergoing chemotherapy for pediatric malignancies Support. Care Cancer 2010 18 751 759 10.1007/s00520-009-0711-6 19685085 · DOI
  60. [67]Dos Reis S.A. Da Conceição L.L. Siqueira N.P. Rosa D.D. Da Silva L.L. Peluzio M.C.G. Review of the mechanisms of probiotic actions in the prevention of colorectal cancer Nutr. Res. 2017 37 1 19 10.1016/j.nutres.2016.11.009 28215310 · DOI
  61. [68]Koboziev I. Webb C.R. Furr K.L. Grisham M.B. Role of the enteric microbiota in intestinal homeostasis and inflammation Free. Radic. Biol. Med. 2013 68 122 133 10.1016/j.freeradbiomed.2013.11.008 24275541 PMC3943931 · DOI
  62. [69]Sobhani I. Tap J. Roudot-Thoraval F. Roperch J.P. Letulle S. Langella P. Corthier G. Tran Van Nhieu J. Furet J.P. Microbial dysbiosis in colorectal cancer (CRC) patients PLoS ONE 2011 6 e16393 10.1371/journal.pone.0016393 21297998 PMC3029306 · DOI
  63. [70]Kahouli I. Tomaro-Duchesneau C. Prakash S. Probiotics in colorectal cancer (CRC) with emphasis on mechanisms of action and current perspectives J. Med. Microbiol. 2013 62 1107 1123 10.1099/jmm.0.048975-0 23558140 · DOI
  64. [71]Boleij A. Hechenbleikner E.M. Goodwin A.C. Badani R. Stein E.M. Lazarev M.G. Ellis B. Carroll K.C. Albesiano E. Wick E.C. The bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients Clin. Infect. Dis. 2015 60 208 215 10.1093/cid/ciu787 25305284 PMC4351371 · DOI · Paper page
  65. [72]Ambalam P. Raman M. Purama R.K. Doble M. Probiotics, prebiotics and colorectal cancer prevention Best. Pract. Res. Clin. Gastroenterol. 2016 30 119 131 10.1016/j.bpg.2016.02.009 27048903 · DOI
  66. [73]Molska M. Reguła J. Potential mechanisms of probiotics action in the prevention and treatment of colorectal cancer Nutrients 2019 11 2453 10.3390/nu11102453 31615096 PMC6835638 · DOI
  67. [74]Javanmard A. Ashtari S. Sabet B. Davoodi S.H. Rostami-Nejad M. Akbari M.E. Niaz A. Mortazavian A.M. Probiotics and their role in gastrointestinal cancers prevention and treatment; an overview Gastroenterol. Hepatol. 2018 11 284 295 PMC6204245 30425806
  68. [75]Fooks L. Gibson G. Probiotics as modulators of the gut flora Br. J. Nutr. 2002 88 S39 S49 10.1079/BJN2002628 12215180 · DOI
  69. [76]Ohland C.L. MacNaughton W.K. Probiotic bacteria and intestinal barrier function Am. J. Physiol. Gastrointest. Liver Physiol. 2010 298 807 819 10.1152/ajpgi.00243.2009 20299599 · DOI
  70. [77]Davey M.E. O’Toole G.A. Microbial biofilms: From ecology to molecular genetics Microbiol. Mol. Biol. Rev. 2000 64 847 867 10.1128/MMBR.64.4.847-867.2000 11104821 PMC99016 · DOI
  71. [78]Dieltjens L. Appermans K. Lissens M. Lories B. Kim W. Van der Eycken E.V. Foster K.R. Steenackers H.P. Inhibiting bacterial cooperation is an evolutionarily robust anti-biofilm strategy Nat. Commun. 2020 107 1 11 10.1038/s41467-019-13660-x PMC6952394 31919364 · DOI
  72. [79]Zhu Q. Gao R. Wu W. Qin H. The role of gut microbiota in the pathogenesis of colorectal cancer Tumor Biol. 2013 34 1285 1300 10.1007/s13277-013-0684-4 23397545 · DOI
  73. [80]Goldin B.R. Gorbach S.L. The effect of milk and Lactobacillus feeding on human intestinal bacterial enzyme activity Am. J. Clin. Nutr. 1984 39 756 761 10.1093/ajcn/39.5.756 6424430 · DOI
  74. [81]Tjalsma H. Boleij A. Marchesi J.R. Dutilh B.E. A bacterial driverpassenger model for colorectal cancer: Beyond the usual suspects Nat. Rev. Microbiol. 2012 10 575 582 10.1038/nrmicro2819 22728587 · DOI · Paper page
  75. [83]Boris S. Barbés C. Role played by lactobacilli in controlling the population of vaginal pathogens Microbes. Infect. 2000 2 543 546 10.1016/S1286-4579(00)00313-0 10865199 · DOI
  76. [85]Fung W.Y. Lye H.S. Lim T.J. Kuan C.Y. Liong M.T. Role of probiotic on gut health Probiotics. Biology, genetics and Health Aspects Liong M.T. Springer New York, NY, USA 2001 139 166
  77. [86]Dembele T. Obdrzalek V. Votava M. Inhibition of bacterial pathogens by lactobacilli Zentralbl. Bakteriol. 1998 288 395 401 10.1016/S0934-8840(98)80013-3 9861683 · DOI
  78. [87]Tomás M.S. Otero C.M. Ocaña V. Nader-Macias E.M. Production of antimicrobial substances by lactic acid bacteria I: Determination of hydrogen peroxide Meth. Mol. Biol. 2004 268 337 346 15156044
  79. [88]Klaenhammer T.R. Genetics of bacteriocins produced by lactic acid bacteria FEMS Microbiol. Rev. 1993 12 39 86 10.1016/0168-6445(93)90057-G 8398217 · DOI
  80. [89]Nazir Y. Hussain S.A. Hamid A.A. Song Y. Probiotics and their potential preventive and therapeutic role for cancer, high serum cholesterol, and allergic and HIV diseases BioMed Res. Int. 2018 2018 1 17 10.1155/2018/3428437 PMC6136537 30246019 · DOI
  81. [91]Nielsen D.S. Cho G.S. Hanak A. Huch M. Franz C.M. Arneborg N. The effect of bacteriocin-producing Lactobacillus plantarum strains on the intracellular pH of sessile and planktonic Listeria monocytogenes single cells Int. J. Food Microbiol. 2010 141 S53 S59 10.1016/j.ijfoodmicro.2010.03.040 20447709 · DOI
  82. [92]Drissi F. Buffet S. Raoult D. Merhej V. Common occurrence of antibacterial agents in human intestinal microbiota Front. Microbiol. 2015 6 441 10.3389/fmicb.2015.00441 25999943 PMC4423438 · DOI
  83. [93]Macfarlane S. Macfarlane G.T. Regulation of short-chain fatty acid production Proc. Nutr. Soc. 2003 62 67 72 10.1079/PNS2002207 12740060 · DOI · Paper page
  84. [94]Roediger W.E. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man Gut 1980 21 793 798 10.1136/gut.21.9.793 7429343 PMC1419533 · DOI · Paper page
  85. [96]Topping D.L. Clifton P.M. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides Physiol. Rev. 2001 81 1031 1064 10.1152/physrev.2001.81.3.1031 11427691 · DOI · Paper page
  86. [98]Gantois I. Ducatelle R. Pasmans F. Haesebrouck F. Hautefort I. Thompson A. Hinton J.C. Van Immerseel F. Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression Appl. Environ. Microbiol. 2006 72 946 949 10.1128/AEM.72.1.946-949.2006 16391141 PMC1352287 · DOI
  87. [99]Markowiak-Kopeć P. Śliżewska K. The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome Nutrients 2020 12 1107 10.3390/nu12041107 PMC7230973 32316181 · DOI
  88. [100]Sun M. Wu W. Liu Z. Cong Y. Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases J. Gastroenterol. 2017 52 1 8 10.1007/s00535-016-1242-9 27448578 PMC5215992 · DOI
  89. [101]Kumar M. Nagpal R. Verma V. Kumar A. Kaur N. Hemalatha R. Probiotic metabolites as epigenetic targets in the prevention of colon cancer Nutr. Rev. 2012 71 23 34 10.1111/j.1753-4887.2012.00542.x 23282249 · DOI
  90. [102]Duc N.M. Kim H.R. Chung K.Y. Structural mechanism of G protein activation by G protein-coupled receptor Eur. J. Pharm. 2015 763 214 222 10.1016/j.ejphar.2015.05.016 25981300 · DOI
  91. [103]Soel S.M. Choi O.S. Bang M.H. Yoon Park J.H. Kim W.K. Influence of conjugated linoleic acid isomers on the metastasis of colon cancer cells in vitro and in vivo J. Nutr. Biochem. 2007 18 650 657 10.1016/j.jnutbio.2006.10.011 17368880 · DOI
  92. [104]Bassaganya-Riera J. Viladomiu M. Pedragosa M. Simone C. Hontecillas R. Immunoregulatory mechanisms underlying prevention of colitis-associated colorectal cancer by probiotic bacteria PLoS ONE 2012 7 1 8 10.1371/journal.pone.0034676 PMC3325233 22511958 · DOI
  93. [105]Ewaschuk J.B. Walker J.W. Diaz H. Madsen K.L. Bioproduction of conjugated linoleic acid by probiotic bacteria occurs in vitro and in vivo in mice J. Nutr. 2006 136 1483 1487 10.1093/jn/136.6.1483 16702308 · DOI
  94. [106]Fearon E.R. Molecular genetics of colorectal cancer Annu. Rev. Pathol. Mech. 2011 6 479 507 10.1146/annurev-pathol-011110-130235 21090969 · DOI · Paper page
  95. [107]De Vries E.G. Gietema J.A. de Jong S. Tumor necrosis factor-related apoptosis-inducing ligand pathway and its therapeutic implications Clin. Cancer Res. 2006 12 2390 2393 10.1158/1078-0432.CCR-06-0352 16638843 · DOI
  96. [108]Hwang J.W. Baek Y.M. Yang K.E. Yoo H.S. Cho C.K. Lee Y.W. Lactobacillus casei extract induces apoptosis in gastric cancer by inhibiting NF-κB and mTOR-mediated signalling Integr. Cancer Ther. 2013 12 165 173 10.1177/1534735412442380 22505595 · DOI
  97. [109]Chen H.M. Yu Y.N. Wang J.L. Lin Y.W. Kong X. Yang C.Q. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma Am. J. Clin. Nutr. 2013 97 1044 1052 10.3945/ajcn.112.046607 23553152 · DOI · Paper page
  98. [110]Liu C.T. Chu F.J. Chou C.C. Yu R.C. Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01 Mutat. Res. 2011 721 157 162 10.1016/j.mrgentox.2011.01.005 21262385 · DOI
  99. [111]Nami Y. Abdullah N. Haghshenas B. Radiah D. Rosli R. Khosroushahi A.Y. Probiotic potential and biotherapeutic effects of newly isolated vaginal Lactobacillus acidophilus 36YL strain on cancer cells Anaerobe 2014 28 29 36 10.1016/j.anaerobe.2014.04.012 24818631 · DOI
  100. [112]Shinnoh M. Horinaka M. Yasuda T. Yoshikawa S. Morita M. Clostridium butyricum MIYAIRI 588 shows antitumor effects by enhancing the release of TRAIL from neutrophils through MMP-8 Int. J. Oncol. 2013 42 903 911 10.3892/ijo.2013.1790 23354042 · DOI
  101. [113]Klusek J. Głuszek S. Klusek J. GST gene polymorphisms and the risk of colorectal cancer development Contemp. Oncol. (Pozn.) 2014 18 219 221 10.5114/wo.2014.41388 25258576 PMC4171468 · DOI
  102. [114]Pool-Zobel B. Veeriah S. Bohmer F.D. Modulation of xenobiotic metabolising enzymes by anticarcinogens—Focus on glutathione S-transferases and their role as targets of dietary chemoprevention in colorectal carcinogenesis Mutat. Res. 2005 591 74 92 10.1016/j.mrfmmm.2005.04.020 16083918 · DOI
  103. [115]McIntosh F.M. Maison N. Holtrop G. Young P. Stevens V.J. Ince J. Johnstone A.M. Lobley G.E. Flint H.J. Louis P. Phylogenetic distribution of genes encoding b-glucuronidase activity in human colonic bacteria and the impact of diet on faecal glycosidase activities Environ. Microbiol. 2013 14 1876 1887 10.1111/j.1462-2920.2012.02711.x 22364273 · DOI · Paper page
  104. [116]Hamer H.M. De Preter V. Windey K. Verbeke K. Functional analysis of colonic bacterial metabolism: Relevant to health? Am. J. Physiol. Gastrointest. Liver Physiol. 2012 302 G1 G9 10.1152/ajpgi.00048.2011 22016433 PMC3345969 · DOI
  105. [117]Culpepper B.S.T. Mai V. Evidence for contributions of gut microbiota to colorectal carcinogenesis Curr. Nutr. Rep. 2013 2 10 18 10.1007/s13668-012-0032-0 · DOI
  106. [118]Commane D. Hughes R. Shortt C. Rowland I. The potential mechanisms involved in the anti-carcinogenic action of probiotics Mutat. Res. 2005 591 276 289 10.1016/j.mrfmmm.2005.02.027 16095630 · DOI
  107. [119]Verma A. Shukla G. Probiotics Lactobacillus rhamnosus GG, Lactobacillus acidophilus suppresses DMH-induced procarcinogenic fecal enzymes and preneoplastic aberrant crypt foci in early colon carcinogenesis in sprague dawley rats Nutr. Cancer 2013 65 84 91 10.1080/01635581.2013.741746 23368917 · DOI
  108. [120]Lee D.K. Jang S. Baek E.H. Kim M.J. Lee K.S. Shin H.S. Chung M.J. Kim J.E. Lee K.O. Ha N.J. Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content Lipids Health Dis. 2009 8 1 8 10.1186/1476-511X-8-21 19515264 PMC2707375 · DOI
  109. [121]Bouhnik Y. Flourie B. Andrieux C. Bisetti N. Briet F. Rambaud J. Effects of Bifidobacterium sp fermented milk ingested with or without inulin on colonic bifidobacteria and enzymatic activities in healthy humans Eur. J. Clin. Nutr. 1996 50 269 273 8730616
  110. [122]Ling W. Korpela R. Mykkänen H. Salminen S. Hänninen O. Lactobacillus strain GG supplementation decreases colonic hydrolytic and reductive enzyme activities in healthy female adults J. Nutr. 1994 124 18 23 10.1093/jn/124.1.18 8283290 · DOI
  111. [123]Burns A.J. Rowland I.R. Antigenotoxicity of probiotics and prebiotics on faecal water-induced DNA damage in human colon adenocarcinoma cells Mutat. Res. 2004 551 233 243 10.1016/j.mrfmmm.2004.03.010 15225596 · DOI
  112. [124]Bolognani F. Rumney C.J. Rowland I.R. Influence of carcinogen binding by lactic acid-producing bacteria on tissue distribution and in vivo mutagenicity of dietary carcinogens Food Chem. Toxicol. 1997 35 535 545 10.1016/S0278-6915(97)00029-X 9225011 · DOI
  113. [125]Orrhage K. Sillerstrom E. Gustafsson J.A. Nord C.E. Rafter J. Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria Mutat. Res. 1994 311 239 248 10.1016/0027-5107(94)90182-1 7526189 · DOI
  114. [126]Rowland I.R. Grasso P. Degradation of N-nitrosamines by intestinal bacteria Appl. Envir. Microbiol. 1975 29 7 12 10.1128/AM.29.1.7-12.1975 PMC186900 803287 · DOI
  115. [127]Morotomi M. Mutai M. In vitro binding of potent mutagenic pyrolysates to intestinal bacteria J. Nat. Cancer Instit. 1986 11 195 201 3014197
  116. [128]El-Nezami H. Kankaanp P. Salminen S. Ahokas J. Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B1 Food Chem. Toxicol. 1998 36 321 332 10.1016/S0278-6915(97)00160-9 9651049 · DOI
  117. [131]Borchers A.T. Selmi C. Meyers F.J. Keen C.L. Gershwin M.E. Probiotics and immunity J. Gastroenterol. 2009 44 26 46 10.1007/s00535-008-2296-0 19159071 · DOI
  118. [132]Gόmez-Llorente C. Munoz S. Gil A. Role of toll-like receptors in the development of immunotolerance mediated by probiotics Proc. Nutr. Soc. 2010 69 381 389 10.1017/S0029665110001527 20416121 · DOI
  119. [133]Urbanska A.M. Paul A. Bhahena J. Prakash S. Suppression of tumorigenesis: Modulation of inflammatory cytokines by oral administration of microencapsulated probiotic yogurt formulation Int. J. Inflam. 2010 31 1 10 10.4061/2010/894972 PMC3004002 21188222 · DOI
  120. [134]Ogawa T. Asai Y. Tamai R. Makimura Y. Sakamoto H. Hashikawa S. Yasuda K. Natural killer cell activities of synbiotic Lactobacillus casei ssp. casei in conjunction with dextran Clin. Exp. Immunol. 2006 143 103 109 10.1111/j.1365-2249.2005.02975.x 16367940 PMC1809552 · DOI
  121. [135]Sobhani I. Tap J. Roudot-Thoraval F. Roperch J.P. Letulle S. Langella P. Takeda K. Suzuki T. Shimada S.I. Shida K. Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei shirota Clin. Exp. Immunol. 2006 146 109 115 16968405 PMC1809741
  122. [136]Madsen K.L. Enhancement of epithelial barrier function by probiotics J. Epithel. Biol. Pharmacol. 2012 5 55 59 10.2174/1875044301205010055 · DOI
  123. [137]Ohigashi S. Sudo K. Kobayashi D. Takahashi O. Takahashi T. Asahara T. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer Dig. Dis. Sci. 2013 58 1717 1726 10.1007/s10620-012-2526-4 23306850 · DOI
  124. [138]Crawford N. Brooke B.N. The pH and buffering power of human bile Lancet 1955 268 1096 1097 10.1016/S0140-6736(55)90590-0 14382504 · DOI
  125. [139]Shimizu K. Ogura H. Goto M. Asahara T. Nomoto K. Morotomi M. Yoshiya K. Matsushima A. Sumi Y. Kuwagata Y. Altered gut flora and environment in patients with severe SIRS J. Trauma 2006 60 126 133 10.1097/01.ta.0000197374.99755.fe 16456446 · DOI · Paper page
  126. [140]Kikuchi H. Yajima T. Correlation between water-holding capacity of different types of cellulose in vitro and gastrointestinal retention time in vivo of rats J. Sci. Food Agric. 1992 60 139 146 10.1002/jsfa.2740600202 · DOI
  127. [141]Caballero-Franco C. Keller K. De Simone C. Chadee K. The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells Am. J. Physiol. Gastrointest. Liver Physiol. 2007 292 315 322 16973917

Authors
Śliżewska, K., Markowiak-Kopeć, P., & Śliżewska, W.
Affiliations
  • Lodz University of Technology (PL)
  • Institute of Fermentation Technology and Microbiology, Faculty of Biotechnology and Food Sciences, Lodz University of Technology, Wólczańska 171/173, 90-924 Lodz, Poland
Corresponding author
Śliżewska, Katarzyna
ORCID
Venue
Cancers
Publisher
MDPI AG
Published
2020-12-23
Volume
13
Issue
1
Pages
20
ISSN
2072-6694 (ISSN-L)
DOI
10.3390/cancers13010020
PMC
PMC7793079
OpenAlex
W3115984021
Cited by
282
References
139
Citations by year
2026: 31 · 2025: 70 · 2024: 70 · 2023: 55 · 2022: 40 · 2021: 16
FWCI
2.35
Type
journal article
Language
en
Open access
Licence
Locations
  • Cancers (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
Keywords
probiotics, chemoprevention, gut microbiota, immunomodulation, pro-inflammatory response, anticancer activity, probiotic metabolites, adjuvant chemotherapy, anticancer mechanism

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