Cancer Chemopreventive Effects of Lactic Acid Bacteria

  • Kim, Jong-Eun (Department of Agricultural Biotechnology, Seoul National University) ;
  • Kim, Ji-Yeon (Nutrition and Functional Food Headquarters, Korea Food and Drug Administration) ;
  • Lee, Ki-Won (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Lee, Hyong-Joo (Department of Agricultural Biotechnology, Seoul National University)
  • Published : 2007.08.30

Abstract

Lactic acid bacteria (LAB) provide several potential health and nutritional benefits, including improving the nutritional value of food, controlling serum cholesterol levels, and controlling some types of cancer. Numerous in vitro, in vivo, human, and epidemiological studies have provided evidence of the chemopreventive effects of LAB on colon, bladder, liver, breast, and gastric cancers. These effects act via diverse mechanisms, including alteration of the gastrointestinal micro flora, enhancement of the host's immune response, and antioxidative and antiproliferative activities. This review discusses the recent progresses on the chemopreventive effects of LAB on specific cancer types and the underlying molecular mechanisms.

Keywords

References

  1. Agha-Mohammadi, S. and M. T. Lotze. 2000. Immunomodulation of cancer: Potential use of selectively replicating agents. J. Clin. Invest. 105: 1173-1176 https://doi.org/10.1172/JCI10026
  2. Aso, Y. and H. Akazan. 1992. Prophylactic effect of a Lactobacillus casei preparation on the recurrence of superficial bladder cancer. Urol. Int. 49: 125-129 https://doi.org/10.1159/000282409
  3. Bae, E. A., D. H. Kim, and M. J. Han. 2000. Anti- Helicobacter pylori activity of Bifidobacterium spp. J Microbiol. Biotechnol. 10: 532-534
  4. Bae, J. M., K. W. Jung, and Y. J. Won. 2002. Estimation of cancer deaths in Korea for the upcoming years. J. Korean Med. Sci. 17: 611-615 https://doi.org/10.3346/jkms.2002.17.5.611
  5. Baricault, L., G. Denariaz, J. J. Houri, C. Bouley, C. Sapin, and G. Trugnan. 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 https://doi.org/10.1093/carcin/16.2.245
  6. Biffi, A., D. Coradini, R. Larsen, L. Riva, and G. Di Fronzo. 1997. Antiproliferative effect of fermented milk on the growth of a human breast cancer cell line. Nutr. Cancer 28: 93-99 https://doi.org/10.1080/01635589709514558
  7. Burns, A. J. and I. R. Rowland. 2004. Antigenotoxicity of probiotics and prebiotics on faecal water-induced DNA damage in human colon adenocarcinoma cells. Mutat. Res. 551: 233-243 https://doi.org/10.1016/j.mrfmmm.2004.03.010
  8. Cerutti, P. A. 1985. Prooxidant states and tumor promotion. Science 227: 375-381 https://doi.org/10.1126/science.2981433
  9. Chang, H. C., Y. D. Choi, and H. J. Lee. 1996. Molecular cloning of a $\beta$-D-galactosidase gene from Lactococcus lactis subsp. lactis 7962. J Microbiol. Biotechnol. 6: 386-390
  10. Chang, J. H., J. H. Shin, I. S. Chung, and H. J. Lee. 1999. Improved menthol production using suspension cultures of Mentha piperita with pectinase elicitation. J. Microbiol. Biotechnol. 9: 358-360
  11. Choi, S. S., Y. Kim, K. S. Han, S. You, S. Oh, and S. H. Kim. 2006. Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett. Appl. Microbiol. 42: 452-458 https://doi.org/10.1111/j.1472-765X.2006.01913.x
  12. Clausen, M. R. and P. B. Mortensen. 1997. Lactulose, disaccharides and colonic flora. Clinical consequences. Drugs 53: 930-942 https://doi.org/10.2165/00003495-199753060-00003
  13. de Moreno de LeBlanc, A., C. Matar, N. LeBlanc, and G. Perdigon. 2005. Effects of milk fermented by Lactobacillus helveticus R389 on a murine breast cancer model. Breast Cancer Res. 7: R477-R486 https://doi.org/10.1186/bcr1032
  14. El-Nezami, H. S., N. N. Polychronaki, J. Ma, H. Zhu, W. Ling, E. K. Salminen, R. O. Juvonen, S. J. Salminen, T. Poussa, and H. M. Mykkanen. 2006. Probiotic supplementation reduces a biomarker for increased risk of liver cancer in young men from Southern China. Am. J. Clin. Nutr. 83: 1199-1203 https://doi.org/10.1093/ajcn/83.5.1199
  15. Felley, C. and P. Michetti. 2003. Probiotics and Helicobacter pylori. Best Pract. Res. Clin. Gastroenterol. 17: 785-791 https://doi.org/10.1016/S1521-6918(03)00070-2
  16. Fujino, T. 2001. The tumor-preventing effect of a mixture of several lactic acid bacteria on 1,2-dimethylhydrazine-induced colon carcinogenesis in mice. Oncol. Rep. 8: 1073-1078
  17. Gibson, G. R. and R. Fuller. 2000. Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. J. Nutr. 130: 391S-395S
  18. Gilliland, S. E. 1990. Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol. Rev. 7: 175-188 https://doi.org/10.1111/j.1574-6941.1990.tb01683.x
  19. Goldin, B. and S. L. Gorbach. 1977. Alterations in fecal microflora enzymes related to diet, age, Lactobacillus supplements, and dimethylhydrazine. Cancer 40: 2421- 2426 https://doi.org/10.1002/1097-0142(197711)40:5+<2421::AID-CNCR2820400905>3.0.CO;2-I
  20. Goldin, B. R. and S. L. Gorbach. 1980. Effect of Lactobacillus acidophilus dietary supplements on 1,2-dimethylhydrazine dihydrochloride-induced intestinal cancer in rats. J. Natl. Cancer Inst. 64: 263-265 https://doi.org/10.1093/jnci/64.2.263
  21. Goldin, B. R. and S. L. Gorbach. 1984. The effect of milk and Lactobacillus feeding on human intestinal bacterial enzyme activity. Am. J. Clin. Nutr. 39: 756-761 https://doi.org/10.1093/ajcn/39.5.756
  22. Gotteland, M. and S. Cruchet. 2003. Suppressive effect of frequent ingestion of Lactobacillus johnsonii La1 on Helicobacter pylori colonization in asymptomatic volunteers. J. Antimicrob. Chemother. 51: 1317-1319 https://doi.org/10.1093/jac/dkg227
  23. Guarner, F. and J.-R. Malagelada. 2003. Gut flora in health and disease. Lancet 361: 512-519 https://doi.org/10.1016/S0140-6736(03)12489-0
  24. Halliwell, B. 2007. Oxidative stress and cancer: Have we moved forward? Biochem. J. 401: 1-11 https://doi.org/10.1042/BJ20061131
  25. Han, S. Y., C. S. Huh, Y. T. Ahn, K. S. Lim, Y. J. Baek, and D. H. Kim. 2005. Hepatoprotective effect of lactic acid bacteria, inhibitors of beta-glucuronidase production against intestinal microflora. Arch. Pharm. Res. 28: 325-329 https://doi.org/10.1007/BF02977800
  26. Hanahan, D. and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100: 57-70 https://doi.org/10.1016/S0092-8674(00)81683-9
  27. Hur, H. J., K. W. Lee, H. Y. Kim, D. K. Chung, and H. J. Lee. 2006. In vitro immunopotentiating activities of cellular fractions of lactic acid bacteria isolated from kimchi and Bifidobacteria. J. Microbiol. Biotechnol. 16: 661-666
  28. Hur, H. J., K. W. Lee, and H. J. Lee. 2004. Production of nitric oxide, tumor necrosis factor-alpha and interleukin-6 by RAW264.7 macrophage cells treated with lactic acid bacteria isolated from kimchi. Biofactors 21: 123-125 https://doi.org/10.1002/biof.552210124
  29. Ishikawa, H., I. Akedo, T. Otani, T. Suzuki, T. Nakamura, I. Takeyama, S. Ishiguro, E. Miyaoka, T. Sobue, and T. Kakizoe. 2005. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int. J. Cancer 116: 762-767 https://doi.org/10.1002/ijc.21115
  30. Jemal, A., R. Siegel, E. Ward, T. Murray, J. Xu, and M. J. Thun. 2007. Cancer statistics, 2007. CA Cancer J. Clin. 57: 43-66 https://doi.org/10.3322/canjclin.57.1.43
  31. Kabir, A. M., Y. Aiba, A. Takagi, S. Kamiya, T. Miwa, and Y. Koga. 1997. Prevention of Helicobacter pylori infection by lactobacilli in a gnotobiotic murine model. Gut 41: 49-55 https://doi.org/10.1136/gut.41.1.49
  32. Kaizu, H., M. Sasaki, H. Nakajima, and Y. Suzuki. 1993. Effect of antioxidative lactic acid bacteria on rats fed a diet deficient in vitamin E. J. Dairy Sci. 76: 2493-2499 https://doi.org/10.3168/jds.S0022-0302(93)77584-0
  33. Kato, I., T. Yokokura, and M. Mutai. 1988. Correlation between increase in Ia-bearing macrophages and induction of T cell-dependent antitumor activity by Lactobacillus casei in mice. Cancer Immunol. Immunother. 26: 215-221
  34. Kato, I., T. Yokokura, and M. Mutai. 1983. Macrophage activation by Lactobacillus casei in mice. Microbiol. Immunol. 27: 611-618 https://doi.org/10.1111/j.1348-0421.1983.tb00622.x
  35. Kim, D. W., Y. J. Bang, D. S. Heo, and N. K. Kim. 2002. Colorectal cancer in Korea: Characteristics and trends. Tumori 88: 262-265 https://doi.org/10.1177/030089160208800402
  36. Kim, J. E., D. W. Jeong, and H. J. Lee. 2007. Expression, purification, and characterization of arginine deiminase from Lactococcus lactis ssp. lactis ATCC 7962 in Escherichia coli BL21. Protein Expr. Purif. 53: 9-15 https://doi.org/10.1016/j.pep.2006.12.002
  37. Kim, J. Y., S. Lee, D. W. Jeong, S. Hachimura, S. Kaminogawa, and H. J. Lee. 2005. Effects of intraperitoneal administration of Lactococcus lactis ssp. lactis cellular fraction on immune response. Food Sci. Biotechnol. 14: 405-409
  38. Kim, J. Y., S. Lee, D. W. Jeong, S. Hachimura, S. Kaminogawa, and H. J. Lee. 2006. In vivo immunopotentiating effects of cellular components from Lactococcus lactis ssp. lactis. J Microbiol. Biotechnol. 16: 786-790
  39. Kim, J. Y., H. J. Woo, Y. S. Kim, K. H. Kim, and H. J. Lee. 2003. Cell cycle dysregulation induced by cytoplasm of Lactococcus lactis ssp. lactis in SNUC2A, a colon cancer cell line. Nutr. Cancer 46: 197-201 https://doi.org/10.1207/S15327914NC4602_13
  40. Kim, J. Y., H. J. Woo, Y. S. Kim, and H. J. Lee. 2002. Screening for antiproliferative effects of cellular components from lactic acid bacteria against human cancer cell lines. Biotechnol. Lett. 24: 1431-1436 https://doi.org/10.1023/A:1019875204323
  41. Kim, S. Y., K. W. Lee, J. Y. Kim, and H. J. Lee. 2004. Cytoplasmic fraction of Lactococcus lactis ssp. lactis induces apoptosis in SNU-1 stomach adenocarcinoma cells. Biofactors 22: 119-122 https://doi.org/10.1002/biof.5520220123
  42. Kim, T. S., J. W. Hur, M. A. Yu, C. I. Cheigh, K. N. Kim, J. K. Hwang, and Y. R. Pyun. 2003. Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J. Food Prot. 66: 3-12 https://doi.org/10.4315/0362-028X-66.1.3
  43. Kim, Y., J. Y. Choi, K. M. Lee, S. K. Park, S. H. Ahn, D. Y. Noh, Y. C. Hong, D. Kang, and K. Y. Yoo. 2007. Dosedependent protective effect of breast-feeding against breast cancer among ever-lactated women in Korea. Eur. J. Cancer Prev. 16: 124-129 https://doi.org/10.1097/01.cej.0000228400.07364.52
  44. Kubota, Y. 1990. Fecal intestinal flora in patients with colon adenoma and colon cancer. Nippon Shokakibyo Gakkai Zasshi 87: 771-779
  45. Kulkarni, N. and B. S. Reddy. 1994. Inhibitory effect of Bifidobacterium longum cultures on the azoxymethaneinduced aberrant crypt foci formation and fecal bacterial beta-glucuronidase. Proc. Soc. Exp. Biol. Med. 207: 278-283
  46. Lankaputhra, W. E. and N. P. Shah. 1998. Antimutagenic properties of probiotic bacteria and of organic acids. Mutat. Res. 397: 169-182 https://doi.org/10.1016/S0027-5107(97)00208-X
  47. Lee, H. M. and Y. Lee. 2006. Isolation of Lactobacillus plantarum from kimchi and its inhibitory activity on the adherence and growth of Helicobacter pylori. J Microbiol. Biotechnol. 16: 1513-1517
  48. Lee, J. E., G. J. Woo, and H. J. Lee. 1996. Tetramethylpyrazine production by immobilized culture of Lactococcus lactis subsp. lactis biovar. diacetilactis FC1. J Microbiol. Biotechnol. 6: 137-141
  49. Lee, J. M., J. Y. Choi, J. H. Lee, H. C. Chang, D. K. Chung, J. H. Kim, and H. J. Lee. 1999. Cloning and expression of the UDP-galactose-4-epimerase gene (galE) constituting the gal/lac operon of Lactococcus lactis ssp. lactis ATCC7962. J Microbiol. Biotechnol. 9: 393-397
  50. Lee, J. W., J. G. Shin, E. H. Kim, H. E. Kang, I. B. Yim, J. Y. Kim, H. G. Joo, and H. J. Woo. 2004. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J. Vet. Sci. 5: 41-48
  51. Lee, K. H., J. Y. Park, S. J. Jeong, G. H. Kwon, H. J. Lee, H. C. Chang, D. K. Chung, J. H. Lee, and J. H. Kim. 2007. Characterization of paraplantaricin C7, a novel bacteriocin produced by Lactobacillus paraplantarum C7 isolated from kimchi. J. Microbiol. Biotechnol. 17: 287-296
  52. Lee, K. W. and H. J. Lee. 2006. The roles of polyphenols in cancer chemoprevention. Biofactors 26: 105-121 https://doi.org/10.1002/biof.5520260202
  53. Lee, K. W., H. J. Lee, H. Y. Cho, and Y. J. Kim. 2005. Role of the conjugated linoleic acid in the prevention of cancer. Crit. Rev. Food Sci. Nutr. 45: 135-144 https://doi.org/10.1080/10408690490911800
  54. Lim, B. K., R. Mahendran, Y. K. Lee, and B. H. Bay. 2002. Chemopreventive effect of Lactobacillus rhamnosus on growth of a subcutaneously implanted bladder cancer cell line in the mouse. Jpn. J. Cancer Res. 93: 36-41 https://doi.org/10.1111/j.1349-7006.2002.tb01198.x
  55. Lin, D. C. 2003. Probiotics as functional foods. Nutr. Clin. Pract. 18: 497-506 https://doi.org/10.1177/0115426503018006497
  56. Lin, M. Y. and F. J. Chang. 2000. Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig. Dis. Sci. 45: 1617-1622 https://doi.org/10.1023/A:1005577330695
  57. Lin, M. Y. and C. L. Yen. 1999. Antioxidative ability of lactic acid bacteria. J. Agric. Food Chem. 47: 1460-1466 https://doi.org/10.1021/jf981149l
  58. Lin, M. Y. and C. L. Yen. 1999. Inhibition of lipid peroxidation by Lactobacillus acidophilus and Bifidobacterium longum. J. Agric. Food Chem. 47: 3661-3664 https://doi.org/10.1021/jf981235l
  59. Lorca, G. L., T. Wadstrom, G. F. Valdez, and A. Ljungh. 2001. Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr. Microbiol. 42: 39-44 https://doi.org/10.1007/s002840010175
  60. Matsuzaki, T. 1998. Immunomodulation by treatment with Lactobacillus casei strain Shirota. Int. J. Food Microbiol. 41: 133-140 https://doi.org/10.1016/S0168-1605(98)00046-4
  61. Nanji, A. A., U. Khettry, and S. M. Sadrzadeh. 1994. Lactobacillus feeding reduces endotoxemia and severity of experimental alcoholic liver (disease). Proc. Soc. Exp. Biol. Med. 205: 243-247
  62. Oberfield, R. A., G. Steele Jr., J. L. Gollan, and D. Sherman. 1989. Liver cancer. CA Cancer J. Clin. 39: 206-218 https://doi.org/10.3322/canjclin.39.4.206
  63. Ohashi, Y., S. Nakai, T. Tsukamoto, N. Masumori, H. Akaza, N. Miyanaga, T. Kitamura, K. Kawabe, T. Kotake, M. Kuroda, S. Naito, H. Koga, Y. Saito, K. Nomata, M. Kitagawa, and Y. Aso. 2002. Habitual intake of lactic acid bacteria and risk reduction of bladder cancer. Urol. Int. 68: 273-280 https://doi.org/10.1159/000058450
  64. Orrhage, K., E. Sillerstrom, J. A. Gustafsson, C. E. Nord, and J. Rafter. 1994. Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria. Mutat. Res. 311: 239-248 https://doi.org/10.1016/0027-5107(94)90182-1
  65. Park, A., A. Rae-Jun, K. H. Lee, S. J. Kim, J. Y. Park, S. J. Nam, H. D. Yun, H. J. Lee, H. C. Chang, D. K. Chung, J. H. Lee, Y. H. Park, and J. H. Kim. 2002. Isolation of Lactococcus lactis strain with $\beta$-galactosidase activity from kimchi and cloning of lacZ gene from the isolated strain. J Microbiol. Biotechnol. 12: 157-161
  66. Park, I. S., Y. C. Lee, H. J. Park, T. I. Kim, S. I. Lee, H. Kim, K. S. Chung, and Y. C. Lee-Kim. 2001. Helicobacter pylori infection in Korea. Yonsei Med. J. 42: 457-470 https://doi.org/10.3349/ymj.2001.42.4.457
  67. Park, S. Y., G. E. Ji, Y. T. Ko, H. K. Jung, Z. Ustunol, and J. J. Pestka. 1999. Potentiation of hydrogen peroxide, nitric oxide, and cytokine production in RAW 264.7 macrophage cells exposed to human and commercial isolates of Bifidobacterium. Int. J. Food Microbiol. 46: 231-241 https://doi.org/10.1016/S0168-1605(98)00197-4
  68. Peek, R. M. Jr. and M. J. Blaser. 2002. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2: 28-37 https://doi.org/10.1038/nrc703
  69. Perdigon, G., M. E. de Macias, S. Alvarez, G. Oliver, and A. A. de Ruiz Holgado. 1986. Effect of perorally administered lactobacilli on macrophage activation in mice. Infect. Immun. 53: 404-410
  70. Perdigon, G., M. E. Nader de Macias, S. Alvarez, G. Oliver, and A. A. Pesce de Ruiz Holgado. 1987. Enhancement of immune response in mice fed with Streptococcus thermophilus and Lactobacillus acidophilus. J. Dairy Sci. 70: 919-926 https://doi.org/10.3168/jds.S0022-0302(87)80095-4
  71. Pool-Zobel, B. L., B. Bertram, M. Knoll, R. Lambertz, C. Neudecker, U. Schillinger, P. Schmezer, and W. H. Holzapfel. 1993. Antigenotoxic properties of lactic acid bacteria in vivo in the gastrointestinal tract of rats. Nutr. Cancer 20: 271-281 https://doi.org/10.1080/01635589309514295
  72. Rafter, J., M. Bennett, G. Caderni, Y. Clune, R. Hughes, P. C. Karlsson, A. Klinder, M. O'Riordan, G. C. O'Sullivan, B. Pool-Zobel, G. Rechkemmer, M. Roller, I. Rowland, M. Salvadori, H. Thijs, J. Van Loo, B. Watzl, and J. K. Collins. 2007. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. Am. J. Clin. Nutr. 85: 488-496 https://doi.org/10.1093/ajcn/85.2.488
  73. Reddy, B. S. and A. Rivenson. 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 Res. 53: 3914-3918
  74. Rokka, S., A. Pihlanto, H. Korhonen, and V. Joutsjoki. 2006. In vitro growth inhibition of Helicobacter pylori by lactobacilli belonging to the Lactobacillus plantarum group. Lett. Appl. Microbiol. 43: 508-513 https://doi.org/10.1111/j.1472-765X.2006.01998.x
  75. Rowland, I. R., C. J. Rumney, J. T. Coutts, and L. C. Lievense. 1998. Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis 19: 281-285 https://doi.org/10.1093/carcin/19.2.281
  76. Saito, H., H. Tomioka, and K. Nagashima. 1987. Protective and therapeutic efficacy of Lactobacillus casei against experimental murine infections due to Mycobacterium fortuitum complex. J. Gen. Microbiol. 133: 2843-2851
  77. Sekine, K., T. Kawashima, and Y. Hashimoto. 1994. Comparison of the TNF-$\alpha$ levels induced by human-derived Bifidobacterium longum and rat-derived Bifidobacterium animalis in mouse peritoneal cells. Bifidobacteria Microflora 13: 79-89 https://doi.org/10.12938/bifidus1982.13.2_79
  78. Sellers, W. R. and D. E. Fisher. 1999. Apoptosis and cancer drug targeting. J. Clin. Invest. 104: 1655-1661 https://doi.org/10.1172/JCI9053
  79. Sengupta, N., E. Siddiqui, and F. H. Mumtaz. 2004. Cancers of the bladder. J. R. Soc. Health 124: 228-229 https://doi.org/10.1177/146642400412400520
  80. Seow, S. W., J. N. B. Rahmat, A. A. K. Mohamed, R. Mahendran, Y. K. Lee, and B. H. Bay. 2002. Lactobacillus species is more cytotoxic to human bladder cancer cells than Mycobacterium bovis (Bacillus Calmette-Guerin). J. Urol. 168: 2236-2239 https://doi.org/10.1016/S0022-5347(05)64362-5
  81. Sgouras, D., P. Maragkoudakis, K. Petraki, B. Martinez- Gonzalez, E. Eriotou, S. Michopoulos, G. Kalantzopoulos, E. Tsakalidou, and A. Mentis. 2004. In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota. Appl. Environ. Microbiol. 70: 518-526 https://doi.org/10.1128/AEM.70.1.518-526.2004
  82. Singh, J., A. Rivenson, M. Tomita, S. Shimamura, N. Ishibashi, and B. S. Reddy. 1997. Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18: 833-841 https://doi.org/10.1093/carcin/18.4.833
  83. Sporn, M. B. and N. Suh. 2000. Chemoprevention of cancer. Carcinogenesis 21: 525-530 https://doi.org/10.1093/carcin/21.3.525
  84. Stiles, M. E. and W. H. Holzapfel. 1997. Lactic acid bacteria of foods and their current taxonomy. Int. J. Food Microbiol. 36: 1-29 https://doi.org/10.1016/S0168-1605(96)01233-0
  85. Surh, Y. J. 2003. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 3: 768-780 https://doi.org/10.1038/nrc1189
  86. Teitelbaum, J. E. and W. A. Walker. 2002. Nutritional impact of pre- and probiotics as protective gastrointestinal organisms. Annu. Rev. Nutr. 22: 107-138 https://doi.org/10.1146/annurev.nutr.22.110901.145412
  87. Tolley, D. A., M. K. B. Parmar, K. M. Grigor, and G. Lallemand. 1996. The effect of intravesical mitomycin C on recurrence of newly diagnosed superficial bladder cancer: A further report with 7 years of followup. J. Urol. 155: 1233- 1238 https://doi.org/10.1016/S0022-5347(01)66226-8
  88. van't Veer, P., J. M. Dekker, J. W. Lamers, F. J. Kok, E. G. Schouten, H. A. Brants, F. Sturmans, and R. J. Hermus. 1989. Consumption of fermented milk products and breast cancer: A case-control study in The Netherlands. Cancer Res. 49: 4020-4023
  89. Vanderhoof, J. A. and R. J. Young. 1998. Use of probiotics in childhood gastrointestinal disorders. J. Pediatr. Gastroenterol. Nutr. 27: 323-332 https://doi.org/10.1097/00005176-199809000-00011
  90. Yasui, H., K. Shida, T. Matsuzaki, and T. Yokokura. 1999. Immunomodulatory function of lactic acid bacteria. Antonie Van Leeuwenhoek 76: 383-389 https://doi.org/10.1023/A:1002041616085
  91. Yasutake, N., T. Matsuzaki, K. Kimura, S. Hashimoto, T. Yokokura, and Y. Yoshikai. 1999. The role of tumor necrosis factor (TNF)-alpha in the antitumor effect of intrapleural injection of Lactobacillus casei strain Shirota in mice. Med. Microbiol. Immunol. 188: 9-14 https://doi.org/10.1007/s004300050099
  92. Zhang, X. B. and Y. Ohta. 1991. Binding of mutagens by fractions of the cell wall skeleton of lactic acid bacteria on mutagens. J. Dairy Sci. 74: 1477-1481 https://doi.org/10.3168/jds.S0022-0302(91)78306-9