Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-25T01:34:31.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Lactic acid bacteria and cancer: mechanistic perspective

Published online by Cambridge University Press:  09 March 2007

J. Rafter
J. Rafter*
Affiliation:
Department of Medical Nutrition, Karolinska Institute, NOVUM, S-141 86 Huddinge, Sweden
*
*Corresponding author: Dr J. Rafter, fax +46 8 7116659, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Colorectal cancer is one of the most important causes of cancer morbidity and mortality in Western countries. While a myriad of healthful effects have been attributed to the probiotic lactic acid bacteria (LAB), perhaps the most controversial remains that of anticancer activity. It should be pointed out that there is no direct experimental evidence for cancer suppression in man as a result of consumption of lactic cultures in fermented or unfermented dairy products. However, there is a wealth of indirect evidence, based largely on laboratory studies, in the literature. The precise mechanisms by which LAB may inhibit colon cancer are presently unknown. However, such mechanisms might include: alteration of the metabolic activities of intestinal microflora; alteration of physico-chemical conditions in the colon; binding and degrading potential carcinogens; quantitative and/or qualitative alterations in the intestinal microflora incriminated in producing putative carcinogen(s) and promoters (e.g. bile acid-metabolising bacteria); production of antitumourigenic or antimutagenic compounds; enhancing the host's immune response; and effects on physiology of the host. These potential mechanisms are addressed in the present paper.

Keywords

Lactic acid bacteriaIntestinal microfloraChemopreventionColon cancer
Type
Research Article
Information
British Journal of Nutrition , Volume 88 , Issue S1 , September 2002 , pp. S89 - S94
Copyright
Copyright © The Nutrition Society 2002

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, 121–132.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, 753–757.CrossRefGoogle ScholarPubMed
Ayebo, AD, Angelo, IA & Shahani, KM (1980) Effect of ingesting Lactobacillus acidophilus milk upon fecal flora and enzyme activity in humans. Milchwissenschaft 35, 730–733.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, 245–252.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, 428–432.CrossRefGoogle Scholar
Biasco, G, Paganelli, G, Brandi, G, Brillianti, S & Lami, F (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, 93–99.CrossRefGoogle ScholarPubMed
Bruce, WR (1987) Recent hypotheses for the origin of colon cancer. Cancer Research 47, 4237–4242.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, 517–521.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, 23–28.Google Scholar
Fang, W-F & Strobel, HW (1978) Activation of carcinogens and mutagens by rat colon mucosa. Cancer Research 38, 2939–2944.Google ScholarPubMed
Friend, BA, Farmer, RE & Shahani, KM (1982) Effect of feeding and intraperitoneal implantation of yogurt culture cells on Ehrlich ascites tumour. Milchwissenschaft 37, 708–710.Google Scholar
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, 263–265.CrossRefGoogle Scholar
Goldin, BR & Gorbach, SL (1984a) 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, 689–695.Google ScholarPubMed
Goldin, BR & Gorbach, SL (1984b) The effect of milk and lactobacillus feeding on human intestinal bacterial enzyme activity. American Journal of Clinical Nutrition 39, 756–761.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, 255–261.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, 173–179.CrossRefGoogle ScholarPubMed
Hirayama, K & Rafter, J (2000) The role of probiotic bacteria in cancer prevention. Microbes and Infection 2, 681–686.CrossRefGoogle ScholarPubMed
Intestinal Microecology Group, International Agency for Research on Cancer (1977) Dietary fibre, transit time, fecal bacteria, steroids and colon cancer in two Scandinavian populations. Lancet 2, 207–211.Google Scholar
Kampman, E, Giovannucci, E, van't Veer, P, Rimm, E, Stampfer, MJ, Colditz, GA, Kok, FJ & Willett, WC (1994a) Calcium, vitamin D, dairy foods and the occurrence of colorectal adenomas among men and women in two prospective studies. American Journal of Epidemiology 139, 16–29.CrossRefGoogle ScholarPubMed
Kampman, E, Goldbohm, RA, van den Brandt, PA & van't Veer, P (1994b) Fermented dairy products, calcium and colorectal cancer in the Netherlands cohort study. Cancer Research 54, 3186–3190.Google ScholarPubMed
Kato, I, Endo, K & Yokokura, T (1994) Effects of oral administration of Lactobacillus casei on antitumour responses induced by tumour resection in mice. International Journal of Immunopharmacology 16, 29–36.CrossRefGoogle Scholar
Kato, I, Kobayashi, S, Yokokura, T & Mutai, M (1981) Antitumour activity of Lactobacillus casei in mice. Gann 72, 517–523.Google Scholar
Kato, I, Yokokura, T & Mutai, M (1983) Macrophage activation by Lactobacillus casei in mice. Microbiology and Immunology 27, 611–618.CrossRefGoogle ScholarPubMed
Kohwi, T, Imai, K, Tamura, A & Hashimoto, Y (1978) Antitumour effect of Bifidobacterium infantis in mice. Gann 69, 613–618.Google Scholar
Kulkarni, N & Reddy, BS (1994) Inhibitory effect of Bifidobacterium longum cultures on the azoxymethane-induced aberrant crypt foci formation and fecal bacterial β-glucuronidase. Proceedings of the Society for Experimental Biology and Medicine 207, 278–283.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, 633–636.CrossRefGoogle Scholar
Lee, S-M & Lee, W-K (2000) Inhibitory effects of lactic acid bacteria (LAB) on the azoxymethane-induced colonic preneoplastic lesions. Journal of Microbiology 38, 169–175.Google Scholar
Lidbeck, A, Geltner-Allinger, U, Orrhage, KM, Ottava, L, Brismar, B, Gustafsson, 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 & Disease 4, 81–88.CrossRefGoogle Scholar
Lidbeck, A, Overvik, E, Rafter, J, Nord, CE & Gustafsson, J-A (1992) Effect of Lactobacillus acidophilus supplements on mutagen excretion in feces and urine in humans. Microbial Ecology in Health & Disease 5, 59–67.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, 18–23.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, 122–134.CrossRefGoogle Scholar
Matsuzaki, T (1998) Immunomodulation by treatment with Lactobacillus casei strain Shirota. International Journal of Food Microbiology 41, 133–140.CrossRefGoogle ScholarPubMed
Modler, GW, McKellar, RC & Yaguchi, M (1990) Bifidobacteria and bifidogenic factors. Canadian Institute of Food Science and Technology Journal 23, 29–41.CrossRefGoogle Scholar
Morotomi, M & Mutai, M (1986) In vitro binding of potent mutagenic pyrolysates to intestinal bacteria. Journal of the National Cancer Institute 77, 195–201.Google ScholarPubMed
Orrhage, K, Sillerstrom, E, Gustafsson, J-A, Nord, CE & Rafter, J (1994) Binding of mutagenic heterocyclic amines by intestinal and LAB. Mutation Research 311, 239–248.CrossRefGoogle Scholar
Peters, RK, Pike, MC, Garabrant, D & Mack, TM (1992) Diet and colon cancer in Los Angeles County, California. Cancer Causes Control 3, 457–473.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, 365–380.CrossRefGoogle ScholarPubMed
Reddy, BS (1998) Prevention of colon cancer by pre-and probiotics: evidence from laboratory studies. British Journal of Nutrition 80, S219–S223.CrossRefGoogle ScholarPubMed
Reddy, GV, Friend, BA, Shahani, KM & Farmer, RE (1983) Antitumour activity of yogurt components. Journal of Food Protection 46, 8–11.CrossRefGoogle Scholar
Reddy, GV, Shahani, KM & Banerjee, MR (1973) Inhibitory effect of yogurt on Ehrlich ascites tumour cell proliferation. Journal of the National Cancer Institute 50, 815–817.CrossRefGoogle Scholar
Rowland, IR & Grasso, P (1975) Degradation of N-nitrosamines by intestinal bacteria. Applied Microbiology 29, 7–12.CrossRefGoogle ScholarPubMed
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, 281–285.CrossRefGoogle ScholarPubMed
Salminen, S, Bouley, C, Boutron-Ruault, M-C, Cummings, JH, Franck, A, Gibson, GR, Isolauri, E, Moreau, M-C, Roberfroid, M & Rowland, I (1998) Functional food science and gastrointestinal physiology and function. British Journal of Nutrition 80, Suppl. 1, S147–S171.CrossRefGoogle ScholarPubMed
Sant, M, Capocaccia, E, Verdecchia, A, Gatta, G, Micheli, A, Mariotto, A, Hakulinen, T & Berrino, F (1995) Comparisions of colon-cancer survival among European countries: The Eurocare Study. International Journal of Cancer 63, 43–48.CrossRefGoogle Scholar
Schiffrin, EJ, Rochat, F, Link-Amster, H, Aeschlimann, JM & Donnet-Hughes, A (1995) Immunomodulation of human blood cells following the ingestion of LAB. Journal of Dairy Science 78, 491–496.CrossRefGoogle Scholar
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, 79–89.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 tumour in mice. Cancer Research 45, 1300–1307.Google ScholarPubMed
Shahani, KM & Ayebo, AD (1980) Role of dietary lactobacilli in gastrointestinal microecology. American Journal of Clinical Nutrition 33, 2448–2457.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, 899–907.CrossRefGoogle Scholar
SYNCAN (2001) \\http:www.snycan.beGoogle Scholar
van't Veer, P, Dekker, JM, Lamers, JWJ, Kok, FJ, Schouten, EG, Brants, HAM, Sturmans, F & Hermus, RJJ (1989) Consumption of fermented milk products and breast cancer: a case–control study in the Netherlands. Cancer Research 49, 4020–4023.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. 399–460 [Rowland, I, 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. 197–220. [De Vita, VT, Hellman, S and Rosenberg, SA, editors]. Philadelphia: JB Lippincott.Google Scholar
Yamazaki, K, Tsunoda, A, Sibusawa, M, Tsunoda, Y, Kusano, M, Fukuchi, K, Yamanaka, M, Kushima, M, Nomoto, K & Morotomi, M (2000) The effects of an oral administration of Lactobacillus casei Shirota on azoxymethane-induced colonic aberrant crypt foci and colon cancer in rats. Oncology Reports 7, 977–982.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, 167–175.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-5H-pyrido[4,3-b]indole. Canadian Journal of Microbiology 39, 841–845.CrossRefGoogle ScholarPubMed