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The effects of probiotics on colon cancer development

Published online by Cambridge University Press:  14 December 2007

Joseph Rafter*
Affiliation:
Department of Medical Nutrition, Karolinska Institutet, NOVUM, S-141 86 Huddinge, Sweden
*
Corresponding author: Dr Joseph Rafter, fax +46 8 711 66 59, email [email protected]
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Abstract

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While several effects beneficial to health have been attributed to the probiotic lactic acid bacteria, perhaps the most interesting and controversial remains that of anti-cancer activity. The vast majority of studies in this area deal with protective effects against colon cancer. There is no direct experimental evidence for cancer suppression in human subjects as a result of the consumption of probiotic cultures in fermented or unfermented dairy products. However, there is a wealth of indirect evidence, based largely on laboratory studies. Reports in the literature, regarding the anti-cancer effects of lactic acid bacteria, fall into the following categories: in vitro studies, animal studies, epidemiological studies and human dietary intervention studies. Examples of these reports will be given in the present review. The mechanisms by which probiotic bacteria may inhibit colon cancer are still poorly understood. However, several potential mechanisms are being discussed in the literature and these will also be addressed in the present review.

Type
Research Article
Copyright
Copyright © The Author 2004

References

Abdelali, H, Cassand, P, Soussotte, V, Daubeze, M, Bouley, C & Narbonne, JF (1995) Effect of dairy products on initiation of precursor lesions of colon cancer in rats. Nutrition and Cancer 24, 121132.CrossRefGoogle ScholarPubMed
Arimochi, H, Kinouchi, T, Kataoka, K, Kuwahara, T & Ohnishi, Y (1997) Effect of intestinal bacteria on formation of azoxymethane-induced aberrant crypt foci in the rat colon. Biochemical and Biophysical Research Communications 238, 753757.CrossRefGoogle ScholarPubMed
Ayebo, AD, Angelo, IA & Shahani, KM (1980) Effect of ingesting Lactobacillus acidophilus milk upon faecal flora and enzyme activity in humans. Milch Wissenschaft 35, 730733.Google Scholar
Baricault, L, Denariaz, G, Houri, J-J, Bouley, C, Sapin, C & Trugnan, G (1995) Use of HT-29, a cultured human colon cancer cell line, to study the effect of fermented milks on colon cancer cell growth and differentiation. Carcinogenesis 16, 245252.CrossRefGoogle Scholar
Bartram, HP, Scheppach, W, Gerlach, S, Ruckdeschel, G, Kelber, E & Kasper, H (1994) Does yogurt enriched with Bifidobacterium longum affect colonic microbiology and fecal metabolites in healthy subjects? American Journal of Clinical Nutrition 59, 428432.CrossRefGoogle Scholar
Biasco, G, Paganelli, GM, Brandi, G, Brillanti, S, Lami, F, Callegari, C & Gizzi, G (1991) Effect of Lactobacillus acidophilus and Bifidobacterium bifidum on rectal cell kinetics and fecal pH. Italian Journal of Gastroenterology 23, 142.Google ScholarPubMed
Biffi, A, Coradini, D, Larsen, R, Riva, L & Di Fronzo, G (1997) Antiproliferative effect of fermented milk on the growth of a human breast cancer cell line. Nutrition and Cancer 28, 9399.CrossRefGoogle ScholarPubMed
Boutron, MC, Faivre, J, Marteau, P, Couillault, C, Senesse, P & Quipourt, V (1996) Calcium, phosphorous, vitamin D, dairy products and colorectal carcinogenesis: a French case-control study. British Journal of Cancer 74, 145151.CrossRefGoogle ScholarPubMed
Bruce, WR (1987) Recent hypotheses for the origin of colon cancer. Cancer Research 47, 42374242.Google ScholarPubMed
Challa, A, Rao, DR, Chawan, CB & Shackelford, L (1997) Bifidobacterium longum and lactulose suppress azoxymethane-induced colonic aberrant crypt foci in rats. Carcinogenesis 18, 517521.CrossRefGoogle ScholarPubMed
De Simone, C, Vesely, R, Bianchi Salvadori, B & Jirillo, E (1993) The role of probiotics in modulation of the immune system in man and in animals. International Journal of Immunotherapy 9, 2328.Google Scholar
Fang, W-F & Strobel, HW (1978) Activation of carcinogens and mutagens by rat colon mucosa. Cancer Research 38, 29392944.Google ScholarPubMed
Femia, AP, Luceri, C, Dolara, P, Giannini, A, Biggeri, A, Salvadori, M, Clune, Y, Collins, KJ, Paglierani, M, Caderni, G (2002) Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogenesis 23, 19531960.CrossRefGoogle ScholarPubMed
Friend, BA, Farmer, RE & Shahani, KM (1982) Effect of feeding and intraperitoneal implantation of yogurt culture cells on Ehrlich ascites tumour. Milch Wissenschaft 37, 708710.Google Scholar
Gallaher, DD, Stallings, WH, Blessing, LL, Busta, FF & Brady, LJ (1996) Probiotics, cecal microflora, and aberrant crypts in the rat colon. Journal of Nutrition 126, 13621371.CrossRefGoogle ScholarPubMed
Goldin, BR, & Gorbach, SL (1980) Effect of Lactobacillus acidophilus dietary supplements on 1,2-dimethylhydrazine dihydrochloride-induced intestinal cancer in rats. Journal of the National Cancer Institute 64, 263265.CrossRefGoogle ScholarPubMed
Goldin, BR, Gorbach, SL (1984 a) Alterations of the intestinal microflora by diet, oral antibiotics and Lactobacillus: decreased production of free amines from aromatic nitro compounds, azo dyes and glucuronides. Journal of the National Cancer Institute 73, 689695.Google ScholarPubMed
Goldin, BR, Gorbach, SL (1984 b) The effect of milk and lactobacillus feeding on human intestinal bacterial enzyme activity. American Journal of Clinical Nutrition 39, 756761.CrossRefGoogle ScholarPubMed
Goldin, BR, Gualtieri, LJ & Moore, RP (1996) The effect of Lactobacillus GG on the initiation and promotion of DMH-induced intestinal tumours in the rat. Nutrition and Cancer 25, 197204.CrossRefGoogle ScholarPubMed
Goldin, BR, Swenson, L, Dwyer, J, Sexton, M & Gorbach, SL (1980) Effect of diet and Lactobacillus acidophilus supplements on human fecal bacterial enzymes. Journal of the National Cancer Institute 64, 255261.CrossRefGoogle ScholarPubMed
Guarner, F & Schaafsma, GJ (1998) Probiotics. International Journal of Food Microbiology 39, 237238.CrossRefGoogle ScholarPubMed
Hayatsu, H & Hayatsu, T (1993) Suppressing effect of Lactobacillus casei administration on the urinary mutagenicity arising from ingestion of fried ground beef in the human. Cancer Letters 73, 173179.CrossRefGoogle ScholarPubMed
Hirayama, K, Baranczewski, P, Åkerland, J-E, Midtvedt, T, Moller, L & Rafter, J (2000) Effects of human intestinal flora on mutagenicity of and DNA adduct formation from food and environmental mutagens. Carcinogenesis 21, 21052111.CrossRefGoogle ScholarPubMed
Hirayama, K, Itoh, K, Takahashi, E & Mitsuoka, T (1995) Comparison of composition of faecal microbiota and metabolism of faecal bacteria among ‘human-flora-associated’ mice inoculated with faeces from six different human donors. Microbial Ecology in Health and Disease 8, 199211.CrossRefGoogle Scholar
Horie, H, Zeisig, M, Hirayama, K, Midtvedt, T, Moller, L & Rafter, J (2003) Probiotic mixture decreases DNA adduct formation in colonic epithelium induced by the food mutagen 2-amino-9H-pyrido[2,3-b]indole in a human-flora associated mouse model. European Journal of Cancer Prevention 12, 101107.CrossRefGoogle Scholar
Iino, H, Fukaya, K, Hirasawa, Y, Shimizu, K & Seo, G (1993) Stimulation of bacterial growth of some strains of Bifidobacterium by a crude preparation of metabolites from Bacillus mesentericus TO-A. Biomedical Letters 48, 7378.Google Scholar
Intestinal Microecology Group, International Agency for Research on Cancer (1977) Dietary fibre, transit time, faecal bacteria, steroids, and colon cancer in two Scandinavian populations. Lancet ii, 207211.Google Scholar
Kampman, E, Giovannucci, E, van't Veer, P, Rimm, E, Stampfer, MJ, Colditz, GA, Kok, FJ & Willett, WC (1994 a) Calcium, vitamin D, dairy foods, and the occurrence of colorectal adenomas among men and women in two prospective studies. American Journal of Epidemiology 139, 1629.CrossRefGoogle ScholarPubMed
Kampman, E, Goldbohm, RA, van den Brandt, PA & van't Veer, P (1994 b) Fermented dairy products, calcium, and colorectal cancer in the Netherlands cohort study. Cancer Research 54, 31863190.Google ScholarPubMed
Kato, I, Endo, K & Yokokura, T (1994) Effects of oral adminstration of Lactobacillus casei on antitumour responses induced by tumour resection in mice. International Journal of Immunopharmacology 16, 2936.CrossRefGoogle Scholar
Kato, I, Kobayashi, S, Yokokura, T & Mutai, M (1981) Antitumour activity of Lactobacillus casei in mice. Gann 72, 517523.Google Scholar
Kato, I, Yokokura, T & Mutai, M (1983) Macrophage activation by Lactobacillus casei in mice. Microbiology and Immunology 27, 611618.CrossRefGoogle ScholarPubMed
Kulkarni, N & Reddy, BS (1994) Inhibitory effect of Bifidobacterium longum cultures on the azoxymethane-induced aberrant crypt foci formation and faecal bacterial β-glucuronidase. Proceedings of the Society for Experimental Biology and Medicine 207, 278283.CrossRefGoogle ScholarPubMed
Le, MG, Moulton, LH, Hill, C & Kramer, A (1986) Consumption of dairy produce and alcohol in a case-control study of breast cancer. Journal of the National Cancer Institute 77, 633636.CrossRefGoogle Scholar
Lidbeck, A, Geltner-Allinger, U, Orrhage, KM, Ottova, L, Brismar, B, Gustafson, J-A, Rafter, JJ & Nord, CE (1991) Impact of Lactobacillus acidophilus supplements on the faecal microflora and soluble faecal bile acids in colon cancer patients. Microbial Ecology in Health and Disease 4, 8188.CrossRefGoogle Scholar
Lidbeck, A, Overvik, E, Rafter, J, Nord, CD & Gustafson, JA (1992) Effect of Lactobacillus acidophilus supplements on mutagen excretion in feces and urine in humans. Microbial Ecology in Health and Disease 5, 5967.CrossRefGoogle Scholar
Ling, WH, Korpela, R, Mykkanen, H, Salminen, S & Hanninen, O (1994) Lactobacillus strain GG supplementation decreases colonic hydrolytic and reductive enzyme activities in healthy female adults. Journal of Nutrition 124, 1823.CrossRefGoogle ScholarPubMed
Malhotra, SL (1977) Dietary factors in a study of colon cancer from cancer registry, with special reference to the role of saliva, milk, and fermented milk products and vegetable fibre. Medical Hypotheses 3, 122134.CrossRefGoogle Scholar
Matsuzaki, T (1998) Immunomodulation by treatment with Lactobacillus casei strain Shirota. International Journal of Food Microbiology 41, 133140.CrossRefGoogle ScholarPubMed
Modler, GW, McKellar, RC & Yaguchi, M (1990) Bifidobacteria and bifidogenic factors. Canadian Institute of Food Science and Technology Journal 23, 2941.CrossRefGoogle Scholar
Morotomi, M & Mutai, M (1986) In vitro binding of potent mutagenic pyrolysates to intestinal bacteria. Journal of the National Cancer Institute 77, 195201.Google ScholarPubMed
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 (2002) Habitual intake of lactic acid bacteria and risk reduction of bladder cancer. Urologia Internationalis 68, 273280.CrossRefGoogle ScholarPubMed
Onoue, M, Kado, S, Sakaitani, Y, Uchida, K & Morotomi, M (1997) Specific species of intestinal bacteria influence the induction of aberrant crypt foci by 1,2-dimethylhydrazine in rats. Cancer Letters 113, 179186.CrossRefGoogle ScholarPubMed
Orrhage, K, Annas, A, Nord, CE, Brittebo, EB & Rafter, JJ (2002) Effects of lactic acid bacteria on the uptake and distribution of the food mutagen Trp-P-2 in mice. Scandinavian Journal of Gastroenterology 37, 215221.CrossRefGoogle ScholarPubMed
Orrhage, K, Sillerstrom, E, Gustafsson, J-A, Nord, CE & Rafter, JJ (1994) Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria. Mutation Research 311, 239248.CrossRefGoogle ScholarPubMed
Ouwehand, AC, Salminen, S & Isolauri, E (2002) Probiotics: an overview of beneficial effects. Antoine van Leeuwenhoek 82, 279289.CrossRefGoogle ScholarPubMed
Peters, RK, Pike, MC, Garabrant, D & Mack, TM (1992) Diet and colon cancer in Los Angeles County, California. Cancer Causes and Control 3, 457473.CrossRefGoogle ScholarPubMed
Pool-Zobel, BL, Neudecker, C, Domizlaff, I, Ji, S, Schillinger, U, Rumney, C, Moretti, M, Vilarini, I, Scassellati-Sforzolini, R & Rowland, I (1996) Lactobacillus- and bifidobacterium-mediated antigenotoxicity in the colon of rats. Nutrition and Cancer 26, 365380.CrossRefGoogle ScholarPubMed
Reddy, BS (1998) Prevention of colon cancer by pre- and probiotics: evidence from laboratory studies. British Journal of Nutrition 80, S219S223.CrossRefGoogle ScholarPubMed
Reddy, BS & Rivenson, A (1993) Inhibitory effect of Bifidobacterium longum on colon, mammary, and liver carcinogenesis induced by 2-amino-3-methylimidazo(4,5- f )quinoline, a food mutagen. Cancer Research 53, 39143918.Google ScholarPubMed
Reddy, GV, Friend, BA, Shahani, KM & Farmer, RE (1983) Antitumour activity of yogurt components. Journal of Food Protection 46, 811.CrossRefGoogle Scholar
Reddy, GV, Shahani, KM & Benerjee, MR (1973) Inhibitory effect of yogurt on Ehrlich ascites tumor cell proliferation. Journal of the National Cancer Institute 50, 815817.CrossRefGoogle ScholarPubMed
Rowland, IR & Grasso, P (1975) Degradation of N -nitrosamines by intestinal bacteria. Applied Microbiology 29, 712.CrossRefGoogle Scholar
Rowland, IR, Rumney, CJ, Coutts, JT & Lievense, LC (1998) Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis 19, 281285.CrossRefGoogle ScholarPubMed
Salminen, S, Bouley, C, Boutron-Ruault, MC, Cummings, JH, Franck, A, Gibson, GR, Isolauri, E, Moreau, MC, Roberfroid, M & Rowland, I (1998) Functional food science and gastrointestinal physiology and function. British Journal of Nutrition 80, S147S171.CrossRefGoogle ScholarPubMed
Schiffrin, EJ, Rochat, F, Link-Amster, H, Aeschlimann, JM & Donnet-Hughes, A (1995) Immunomodulation of human blood cells following the ingestion of lactic acid bacteria. Journal of Dairy Science 78, 491496.CrossRefGoogle ScholarPubMed
Sekine, K, Kawashima, T, & Hashimoto, Y (1994) Comparison of the TNF-α levels induced by human-derived Bifidobacterium longum and rat-derived Bifidobacterium animalis in mouse peritoneal cells. Bifidobacteria Microflora 13, 7989.CrossRefGoogle Scholar
Sekine, K, Toida, T, Saito, M, Kuboyama, M, Kawashima, T & Hashimoto, Y (1985) A new morphologically characterized cell wall preparation (whole peptidoglycan) from Bifidobacterium infantis with a higher efficacy on the regression of an established tumor in mice. Cancer Research 45, 13001307.Google ScholarPubMed
Seo, G, Akimoto, Y, Hamashima, H, Masuda, K, Shiojima, K, Sakuma, C, Sasatsu, M & Arai, T (2000) A new factor from Bacillus mesentericus which promotes the growth of Bifidobacterium. Microbios 101, 105114.Google ScholarPubMed
Seo, G, Shimizu, K, Sasatsu, M & Kono, M (1989) Inhibition of growth of some enteropathogenic strains in mixed cultures of Streptococcus faecalis and Clostridium butyricum. Microbios Letters 40, 151160.Google Scholar
Shackelford, LA, Rao, DR, Chawan, CB & Pulusani, SR (1983) Effect of feeding fermented milk on the incidence of chemically induced colon tumors in rats. Nutrition and Cancer 5, 159164.CrossRefGoogle ScholarPubMed
Shahani, KM & Ayebo, AD (1980) Role of dietary lactobacilli in gastrointestinal microecology. American Journal of Clinical Nutrition 33, 24482457.CrossRefGoogle ScholarPubMed
Singh, J, Rivenson, A, Tomita, M, Shimamura, S, Ishibashi, N & Reddy, BS (1997) Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18, 833841.CrossRefGoogle ScholarPubMed
Spanhaak, S, Havenaar, R & Schaafsma, G (1998) The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parmeters in humans. European Journal of Clinical Nutrition 52, 899907.CrossRefGoogle Scholar
SYNCAN (2004) Synbiotics and cancer prevention in humans. www.syncan.beGoogle Scholar
van't Veer, P, Dekker, JM, Lamers, JWJ, Kok, FJ, Schouten, EG, Brants, HA, Sturmans, F & Hermus, RJ (1989) Consumption of fermented milk products and breast cancer: a case-control study in The Netherlands. Cancer Research 49, 40204023.Google ScholarPubMed
Venitt, S (1988) Mutagens in human faeces and cancer of the large bowel. In Role of the Gut Flora in Toxicity and Cancer, pp. 399460 [Rowland, IR, editor]. London: Academic Press.CrossRefGoogle Scholar
Weisburger, JH & Wynder, EL (1987) Etiology of colorectal cancer with emphasis on mechanism of action and prevention. In Important Advances in Oncology, pp. 197220 [De Vita, VT, Hellman, S and Rosenberg, SA, editors]. Philadelphia, PA: JB Lippincott.Google Scholar
World Cancer Research Fund/American Institute for Cancer Research (1997) Food, Nutrition and the Prevention of Cancer: a Global Perspective. Washington, DC: American Institute for Cancer Research.Google Scholar
Young, TB & Wolf, DA (1988) Case-control study of proximal and distal colon cancer and diet in Wisconsin. International Journal of Cancer 42, 167175.CrossRefGoogle ScholarPubMed
Zhang, XB & Ohta, Y (1993) Microorganisms in the gastrointestinal tract of the rat prevent absorption of the mutagen-carcinogen 3-amino-1,4-dimethyl-5 H -pyrido(4,3- b)indole. Canadian Journal of Microbiology 39, 841845.CrossRefGoogle Scholar