Emerging roles of lactic acid bacteria in protection against colorectal cancer

World Journal of Gastroenterology

Volumn 20, Issue 24, 2014, Pages 7878-7886

  Zhong, Li ^a,b   Zhang, Xufei ^a,b   Covasa, Mihai ^a,c,d  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b HEBEI UNIVERSITY   (China)

^c UMR1319 MICALIS   (France)

^d STEFAN CEL MARE UNIVERSITY OF SUCEAVA   (Romania)

Author keywords

Carcinogenesis; Gastrointestinal; Gut bacteria; Microbiota; Probiotics

Indexed keywords

CASPASE 10; CASPASE 8; CASPASE 9; CYTOCHROME C; FAS ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; PROBIOTIC AGENT; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL XL; TUMOR NECROSIS FACTOR; ANTIOXIDANT; LACTIC ACID;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; BACTERIAL STRAIN; CANCER DIAGNOSIS; CANCER GROWTH; CARCINOGENESIS; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; DNA DAMAGE; EPIGENETICS; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; LACTIC ACID BACTERIUM; LACTOBACILLUS ACIDOPHILUS; NONHUMAN; REVIEW; RISK FACTOR; ANIMAL; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PATHOLOGY;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; COLORECTAL NEOPLASMS; DNA DAMAGE; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; LACTIC ACID; LACTOBACILLUS; OXIDATIVE STRESS; PROBIOTICS;

EID: 84903151248     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i24.7878     Document Type: Review

References (80)

1. Tenesa A, Dunlop MG. New insights into the aetiology of colorectal cancer from genome-wide association studies. Nat Rev Genet 2009; 10: 353-358 [PMID: 19434079 DOI: 10.1038/nrg2574]
2. Garagnani P, Pirazzini C, Franceschi C. Colorectal cancer microenvironment: among nutrition, gut microbiota, inflammation and epigenetics. Curr Pharm Des 2013; 19: 765-778 [PMID: 23016865]
3. Daniluk U. Probiotics, the new approach for cancer prevention and/or potentialization of anti-cancer treatment? J Clin Exp Oncol 2012; 1: 1000e105
4. Rowland IR. The role of the gastrointestinal microbiota in colorectal cancer. Curr Pharm Des 2009; 15: 1524-1527 [PMID: 19442169]
5. Zhu Q, Gao R, Wu W, Qin H. The role of gut microbiota in the pathogenesis of colorectal cancer. Tumour Biol 2013; 34: 1285-1300 [PMID: 23397545 DOI: 10.1007/s13277-013-0684-4]
6. Food and Agriculture Organization/World Health Organization. Report of Joint FAO/WHO (Food and agriculture organization/World health organization) Working group on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada: Guidelines for the evaluation of probiotics in food, 2002: 1-11
7. Fotiadis CI, Stoidis CN, Spyropoulos BG, Zografos ED. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World J Gastroenterol 2008; 14: 6453-6457 [PMID: 19030195]
8. Masood MI, Qadir MI, Shirazi JH, Khan IU. Beneficial effects of lactic acid bacteria on human beings. Crit Rev Microbiol 2011; 37: 91-98 [PMID: 21162695 DOI: 10.3109/1040841x.2010.536522]
9. Hove H, Nørgaard H, Mortensen PB. Lactic acid bacteria and the human gastrointestinal tract. Eur J Clin Nutr 1999; 53: 339-350 [PMID: 10369488]
10. Chouraqui JP, Van Egroo LD, Fichot MC. Acidified milk formula supplemented with bifidobacterium lactis: impact on infant diarrhea in residential care settings. J Pediatr Gastroenterol Nutr 2004; 38: 288-292 [PMID: 15076628]
11. Gaón D, García H, Winter L, Rodríguez N, Quintás R, González SN, Oliver G. Effect of Lactobacillus strains and Saccharomyces boulardii on persistent diarrhea in children. Medicina (B Aires) 2003; 63: 293-298 [PMID: 14518142]
12. Pohjavuori E, Viljanen M, Korpela R, Kuitunen M, Tiittanen M, Vaarala O, Savilahti E. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow's milk allergy. J Allergy Clin Immunol 2004; 114: 131-136 [PMID: 15241356 DOI: 10.1016/j.jaci.2004.03.036]
13. Bourlioux P, Koletzko B, Guarner F, Braesco V. The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium "The Intelligent Intestine," held in Paris, June 14, 2002. Am J Clin Nutr 2003; 78: 675-683 [PMID: 14522724]
14. Azcárate-Peril MA, Sikes M, Bruno-Bárcena JM. The intestinal microbiota, gastrointestinal environment and colorectal cancer: a putative role for probiotics in prevention of colorectal cancer? Am J Physiol Gastrointest Liver Physiol 2011; 301: G401-G424 [PMID: 21700901 DOI: 10.1152/ajpgi.00110.2011]
15. del Carmen S, de LeBlanc AM, Miyoshi A, Rocha CS, Azevedo V, LeBlanc JG. Potential application of probiotics in the prevention and treatment of inflammatory bowel diseases. Ulcers 2011; 2011: 1-13
16. Rafter JJ. The role of lactic acid bacteria in colon cancer prevention. Scand J Gastroenterol 1995; 30: 497-502 [PMID: 7569753]
17. Bengmark S, Gil A. Bioecological and nutritional control of disease: prebiotics, probiotics and synbiotics. Nutr Hosp 2006; 21 Suppl 2: 72-84, 73-86 [PMID: 16771075]
18. Hirayama K, Rafter J. The role of lactic acid bacteria in colon cancer prevention: mechanistic considerations. Antonie Van Leeuwenhoek 1999; 76: 391-394 [PMID: 10532395]
19. de Vries EG, Gietema JA, de Jong S. Tumor necrosis factorrelated apoptosis-inducing ligand pathway and its therapeutic implications. Clin Cancer Res 2006; 12: 2390-2393 [PMID: 16638843 DOI: 10.1158/1078-0432.ccr-06-0352]
20. Bucur O, Ray S, Bucur MC, Almasan A. APO2 ligand/tumor necrosis factor-related apoptosis-inducing ligand in prostate cancer therapy. Front Biosci 2006; 11: 1549-1568 [PMID: 16368536]
21. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007; 35: 495-516 [PMID: 17562483 DOI: 10.108 0/01926230701320337]
22. Fesik SW. Promoting apoptosis as a strategy for cancer drug discovery. Nat Rev Cancer 2005; 5: 876-885 [PMID: 16239906 DOI: 10.1038/nrc1736]
23. Chen CC, Lin WC, Kong MS, Shi HN, Walker WA, Lin CY, Huang CT, Lin YC, Jung SM, Lin TY. Oral inoculation of probiotics Lactobacillus acidophilus NCFM suppresses tumour growth both in segmental orthotopic colon cancer and extra-intestinal tissue. Br J Nutr 2012; 107: 1623-1634 [PMID: 21992995 DOI: 10.1017/s0007114511004934]
24. Iyer C, Kosters A, Sethi G, Kunnumakkara AB, Aggarwal BB, Versalovic J. Probiotic Lactobacillus reuteri promotes TNF-induced apoptosis in human myeloid leukemia-derived cells by modulation of NF-kappaB and MAPK signalling. Cell Microbiol 2008; 10: 1442-1452 [PMID: 18331465 DOI: 10.1111/j.1462-5822.2008.01137.x]
25. Kim Y, Oh S, Yun HS, Oh S, Kim SH. Cell-bound exopolysaccharide from probiotic bacteria induces autophagic cell death of tumour cells. Lett Appl Microbiol 2010; 51: 123-130 [PMID: 20536712 DOI: 10.1111/j.1472-765X.2010.02859.x]
26. Baldwin C, Millette M, Oth D, Ruiz MT, Luquet FM, Lacroix M. Probiotic Lactobacillus acidophilus and L. casei mix sensitize colorectal tumoral cells to 5-fluorouracil-induced apoptosis. Nutr Cancer 2010; 62: 371-378 [PMID: 20358475 DOI: 10.1080/01635580903407197]
27. Amaretti A, di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A. Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 2013; 97: 809-817 [PMID: 22790540 DOI: 10.1007/ s00253-012-4241-7]
28. Amanatidou A, Bennik MH, Gorris LG, Smid EJ. Superoxide dismutase plays an important role in the survival of Lactobacillus sake upon exposure to elevated oxygen. Arch Microbiol 2001; 176: 79-88 [PMID: 11479706]
29. Bruno-Bárcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM. Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl Environ Microbiol 2004; 70: 4702-4710 [PMID: 15294805 DOI: 10.1128/ aem.70.8.4702-4710.2004]
30. Kullisaar T, Songisepp E, Mikelsaar M, Zilmer K, Vihalemm T, Zilmer M. Antioxidative probiotic fermented goats' milk decreases oxidative stress-mediated atherogenicity in human subjects. Br J Nutr 2003; 90: 449-456 [PMID: 12908907]
31. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A. Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 2002; 72: 215-224 [PMID: 11845820]
32. Lee J, Hwang KT, Heo MS, Lee JH, Park KY. Resistance of Lactobacillus plantarum KCTC 3099 from Kimchi to oxidative stress. J Med Food 2005; 8: 299-304 [PMID: 16176138 DOI: 10.1089/jmf.2005.8.299]
33. Lin MY, Chang FJ. Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 2000; 45: 1617-1622 [PMID: 11007114]
34. Choi SS, Kim Y, Han KS, You S, Oh S, Kim SH. Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett Appl Microbiol 2006; 42: 452-458 [PMID: 16620202 DOI: 10.1111/j.1472-765X.2006.01913.x]
35. Koller VJ, Marian B, Stidl R, Nersesyan A, Winter H, Simić T, Sontag G, Knasmüller S. Impact of lactic acid bacteria on oxidative DNA damage in human derived colon cells. Food Chem Toxicol 2008; 46: 1221-1229 [PMID: 17942208 DOI: 10.1016/j.fct.2007.09.005]
36. Annuk H, Shchepetova J, Kullisaar T, Songisepp E, Zilmer M, Mikelsaar M. Characterization of intestinal lactobacilli as putative probiotic candidates. J Appl Microbiol 2003; 94: 403-412 [PMID: 12588549]
37. Kumar M, Kumar A, Nagpal R, Mohania D, Behare P, Verma V, Kumar P, Poddar D, Aggarwal PK, Henry CJ, Jain S, Yadav H. Cancer-preventing attributes of probiotics: an update. Int J Food Sci Nutr 2010; 61: 473-496 [PMID: 20187714 DOI: 10.3109/09637480903455971]
38. Uccello M, Malaguarnera G, Basile F, D'Agata V, Malaguarnera M, Bertino G, Vacante M, Drago F, Biondi A. Potential role of probiotics on colorectal cancer prevention. BMC Surg 2012; 12 Suppl 1: S35 [PMID: 23173670 DOI: 10.1186/1471-24 82-12-s1-s35]
39. Jounai K, Ikado K, Sugimura T, Ano Y, Braun J, Fujiwara D. Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells. PLoS One 2012; 7: e32588 [PMID: 22505996 DOI: 10.1371/journal.pone.0032588]
40. Gabrilovich D, Pisarev V. Tumor escape from immune response: mechanisms and targets of activity. Curr Drug Targets 2003; 4: 525-536 [PMID: 14535653]
41. Loredana Baffoni FG, Gioia DD, Biavati B. Role of int stinal microbiota in colon cancer prevention. Ann Microbiol 2012; 62: 15-30
42. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006; 6: 24-37 [PMID: 16397525 DOI: 10.1038/nrc1782]
43. Pessi T, Sütas Y, Hurme M, Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy 2000; 30: 1804-1808 [PMID: 11122221]
44. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGFbeta-bearing regulatory cells. J Immunol 2005; 174: 3237-3246 [PMID: 15749854]
45. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 2001; 121: 580-591 [PMID: 11522742]
46. Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, Bavari S, Klaenhammer TR. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci USA 2005; 102: 2880-2885 [PMID: 15710900 DOI: 10.1073/pnas.0500098102]
47. Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, Molle D, Lortal S, Altermann E, Klaenhammer TR, van Kooyk Y. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci USA 2008; 105: 19474-19479 [PMID: 19047644 DOI: 10.1073/pnas.0810305105]
48. Mohamadzadeh M, Duong T, Sandwick SJ, Hoover T, Klaenhammer TR. Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. Proc Natl Acad Sci USA 2009; 106: 4331-4336 [PMID: 19246373 DOI: 10.1073/ pnas.0900029106]
49. Goh YJ, Azcárate-Peril MA, O'Flaherty S, Durmaz E, Valence F, Jardin J, Lortal S, Klaenhammer TR. Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactoba- cillus acidophilus NCFM. Appl Environ Microbiol 2009; 75: 3093-3105 [PMID: 19304841 DOI: 10.1128/aem.02502-08]
50. Goh YJ, Klaenhammer TR. Genomic features of Lactobacillus species. Front Biosci (Landmark Ed) 2009; 14: 1362-1386 [PMID: 19273135]
51. Mayer ML, Phillips CM, Townsend RA, Halperin SA, Lee SF. Differential activation of dendritic cells by Toll-like receptor agonists isolated from the Gram-positive vaccine vector Streptococcus gordonii. Scand J Immunol 2009; 69: 351-356 [PMID: 19284500 DOI: 10.1111/j.1365-3083.2009.02232.x]
52. Mayer ML, Phillips CM, Stadnyk AW, Halperin SA, Lee SF. Synergistic BM-DC activation and immune induction by the oral vaccine vector Streptococcus gordonii and exogenous tumor necrosis factor. Mol Immunol 2009; 46: 1883-1891 [PMID: 19278729 DOI: 10.1016/j.molimm.2009.02.008]
53. Mohamadzadeh M, Pfeiler EA, Brown JB, Zadeh M, Gramarossa M, Managlia E, Bere P, Sarraj B, Khan MW, Pakanati KC, Ansari MJ, O'Flaherty S, Barrett T, Klaenhammer TR. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 2011; 108 Suppl 1: 4623-4630 [PMID: 21282652 DOI: 10.1073/pnas.1005066107]
54. Khazaie K, Zadeh M, Khan MW, Bere P, Gounari F, Dennis K, Blatner NR, Owen JL, Klaenhammer TR, Mohamadzadeh M. Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 2012; 109: 10462-10467 [PMID: 22689992 DOI: 10.1073/ pnas.1207230109]
55. Galdeano CM, de Moreno de LeBlanc A, Vinderola G, Bonet ME, Perdigón G. Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clin Vaccine Immunol 2007; 14: 485-492 [PMID: 17360855 DOI: 10.1128/cvi.00406-06]
56. Lee JW, Shin JG, Kim EH, Kang HE, Yim IB, Kim JY, Joo HG, Woo HJ. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J Vet Sci 2004; 5: 41-48 [PMID: 15028884]
57. Takagi A, Matsuzaki T, Sato M, Nomoto K, Morotomi M, Yokokura T. Enhancement of natural killer cytotoxicity delayed murine carcinogenesis by a probiotic microorganism. Carcinogenesis 2001; 22: 599-605 [PMID: 11285195]
58. Matsuzaki T, Yokokura T, Mutai M. Antitumor effect of intrapleural administration of Lactobacillus casei in mice. Cancer Immunol Immunother 1988; 26: 209-214 [PMID: 3133110]
59. Matsuzaki T. Immunomodulation by treatment with Lactobacillus casei strain Shirota. Int J Food Microbiol 1998; 41: 133-140 [PMID: 9704862]
60. Takagi A, Ikemura H, Matsuzaki T, Sato M, Nomoto K, Morotomi M, Yokokura T. Relationship between the in vitro response of dendritic cells to Lactobacillus and prevention of tumorigenesis in the mouse. J Gastroenterol 2008; 43: 661-669 [PMID: 18807127 DOI: 10.1007/s00535-008-2212-7]
61. Lee do K, Jang S, Kim MJ, Kim JH, Chung MJ, Kim KJ, Ha NJ. Anti-proliferative effects of Bifidobacterium adolescentis SPM0212 extract on human colon cancer cell lines. BMC Cancer 2008; 8: 310 [PMID: 18950540 DOI: 10.1186/1471-2407-8-310]
62. Coppedè F. Epigenetic biomarkers of colorectal cancer: Focus on DNA methylation. Cancer Lett 2014; 342: 238-247 [PMID: 22202641 DOI: 10.1016/j.canlet.2011.12.030]
63. Migliore L, Migheli F, Spisni R, Coppedè F. Genetics, cytogenetics, and epigenetics of colorectal cancer. J Biomed Biotechnol 2011; 2011: 792362 [PMID: 21490705 DOI: 10.1155/2011/792362]
64. Berni Canani R, Di Costanzo M, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics 2012; 4: 4 [PMID: 22414433 DOI: 10.1186/1868-7083-4-4]
65. Acharya MR, Sparreboom A, Venitz J, Figg WD. Rational development of histone deacetylase inhibitors as anticancer agents: a review. Mol Pharmacol 2005; 68: 917-932 [PMID: 15955865 DOI: 10.1124/mol.105.014167]
66. Marks PA, Richon VM, Miller T, Kelly WK. Histone deacetylase inhibitors. Adv Cancer Res 2004; 91: 137-168 [PMID: 15327890 DOI: 10.1016/s0065-230x(04)91004-4]
67. Waldecker M, Kautenburger T, Daumann H, Busch C, Schrenk D. Inhibition of histone-deacetylase activity by shortchain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 2008; 19: 587-593 [PMID: 18061431 DOI: 10.1016/j.jnutbio.2007.08.002]
68. Waldecker M, Kautenburger T, Daumann H, Veeriah S, Will F, Dietrich H, Pool-Zobel BL, Schrenk D. Histone-deacetylase inhibition and butyrate formation: Fecal slurry incubations with apple pectin and apple juice extracts. Nutrition 2008; 24: 366-374 [PMID: 18262392 DOI: 10.1016/j.nut.2007.12.013]
69. Dashwood RH, Ho E. Dietary histone deacetylase inhibitors: from cells to mice to man. Semin Cancer Biol 2007; 17: 363-369 [PMID: 17555985 DOI: 10.1016/j.semcancer.2007.04.001]
70. Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, Tjønneland A, Overvad K, Martinez C, Dorronsoro M, Gonzalez CA, Key TJ, Trichopoulou A, Naska A, Vineis P, Tumino R, Krogh V, Bueno-de-Mesquita HB, Peeters PH, Berglund G, Hallmans G, Lund E, Skeie G, Kaaks R, Riboli E. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet 2003; 361: 1496-1501 [PMID: 12737858]
71. Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, Miene C, Munjal U, Stein K, Glei M. Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 2009; 682: 39-53 [PMID: 19383551 DOI: 10.1016/j.mrrev.2009.04.001]
72. Lightfoot YL, Mohamadzadeh M. Tailoring gut immune responses with lipoteichoic acid-deficient Lactobacillus acidophilus. Front Immunol 2013; 4: 25 [PMID: 23390423 DOI: 10.3389/fimmu.2013.00025]
73. Lightfoot YL, Yang T, Sahay B, Mohamadzadeh M. Targeting aberrant colon cancer-specific DNA methylation with lipoteichoic acid-deficient Lactobacillus acidophilus. Gut Microbes 2013; 4: 84-88 [PMID: 23137966 DOI: 10.4161/ gmic.22822]
74. 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 [PMID: 23239414 DOI: 10.1007/s12010-012-9995-y]
75. Escamilla J, Lane MA, Maitin V. Cell-free supernatants from probiotic Lactobacillus casei and Lactobacillus rhamnosus GG decrease colon cancer cell invasion in vitro. Nutr Cancer 2012; 64: 871-878 [PMID: 22830611 DOI: 10.1080/01635581.20 12.700758]
76. SYNCAN. Synbiotics and cancer prevention in humans. Available from: URL: http://www.syncan.be/
77. Liu Z, Qin H, Yang Z, Xia Y, Liu W, Yang J, Jiang Y, Zhang H, Yang Z, Wang Y, Zheng Q. Randomised 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 [PMID: 21083585 DOI: 10.1111/ j.1365-2036.2010.04492.x]
78. 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 [PMID: 21874415 DOI: 10.1007/s00595-010-4450-6]
79. Ohashi Y, Nakai S, Tsukamoto T, Masumori N, Akaza H, Miyanaga N, Kitamura T, Kawabe K, Kotake T, Kuroda M, Naito S, Koga H, Saito Y, Nomata K, Kitagawa M, Aso Y. Habitual intake of lactic acid bacteria and risk reduction of bladder cancer. Urol Int 2002; 68: 273-280 [PMID: 12053032]
80. Brim H, Kumar K, Nazarian J, Hathout Y, Jafarian A, Lee E, Green W, Smoot D, Park J, Nouraie M, Ashktorab H. SLC5A8 gene, a transporter of butyrate: a gut flora metabolite, is frequently methylated in African American colon adenomas. PLoS One 2011; 6: e20216 [PMID: 21687703 DOI: 10.1371/journal.pone.0020216]