The Effect of Bifidobacteria and Various Oligosaccharides Consumption on the Risk of Colon Cancer in Rats

  • Khil, Jin-Mo (Department of Culinary Science, Honam University)
  • Published : 2005.11.01

Abstract

This study examined the effect of viable bifidobacteria and non-digestible carbohydrates on the cecal pH, colonic neoplastic lesion (aberrant crypt) and proliferating cell nuclear antigen (PCNA) labeling index in carcinogen-treated mts. Animals received s.c. injection of dimethylhydrazine (DMH) (15 mg/kg body weight) twice 3 days apart. Three days after the second carcinogen administration, the treatments were begun. 1he treatments were basal diet (AIN-76) with skim milk (Basal/skim), or the following diets with daily gavage of $10^8$ bifidobacteria: basal (Basal/bifido), $2\%$ fructo-oligosaccharide (FOS/bifido), $2\%$ soybean oligosaccharide (SBO/bifido), $2\%$ wheat bran oligosaccharide (WBO/bifido) and $8.4\%$ wheat bran (WB/bifido). After 4 weeks of treatment, cecal pH was measured using a pH probe. The number of aberrant crypt (AC), aberrant crypt foci (ACF) and crypt multiplicity were enumerated and colonic PCNA labeling index was determined using immunohistochemistry. Cecal pH was significantly reduced in SBO/bifido and FOS/bifido groups compared to control group. However, there were no significant differences in either number of AC or rates of cell proliferation as shown by PCNA labeling index among the groups, although mts fed FOS/bifido reduced the numbers of ACF compared to Basal/skim group. The SBO/bifido group did not reduce the number of ACF or PCNA labeling index. Also, other oligosaccharides did not reduce the risk of colon cancer compared to control group. The concomitant reduction of cecal pH and number of ACF suggest that the combination of bifidobacteria and FOS may reduce the risk of colon cancer.

Keywords

References

  1. Gorbach SL. The intestinal microflora and its colon cancer connection. Infection 10(6):379-384, 1982 https://doi.org/10.1007/BF01642307
  2. Lidbeck A, Nord CE, Gustafsson J-A, Rafter J. Lactobacilli, anticarcinogenic activities and human intestinal microflora. Eur J Cancer Prev 1:341-353, 1992 https://doi.org/10.1097/00008469-199208000-00002
  3. Cummings JH, Macfarlane GT. Colonic microflora: nutrition and health. Nutrition 13:476-478, 1997 https://doi.org/10.1016/S0899-9007(97)00114-7
  4. Fuller R. Probiotics in man and animals. J Appl Bacteriol 66:365-378, 1989 https://doi.org/10.1111/j.1365-2672.1989.tb05105.x
  5. Sanders ME. Summary of conclusions from a concensus panel of experts on health attributes of lactic cultures: significance to fluid milk products containing cultures. J Dairy Sci 76:1819-1828, 1993 https://doi.org/10.3168/jds.S0022-0302(93)77514-1
  6. Reddy BS, Rivenson A. Inhibitory effect of Bifidobacterium longum on colon, mammary, and liver carcinogenesis induced by 2-amino-3-methylimidazol[4,5-f]quinoline, a food mutagen. Cancer Res 53:3914-3918, 1993
  7. Singh J, Rivenson A, Tomita M, Shimamura S, Ishibashi N, Reddy BS. Bifidobacterium longum, a lactic acid-producing intestinal microflora inhibit colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis 18:1371-1377, 1997 https://doi.org/10.1093/carcin/18.7.1371
  8. Roller M, Pietro Femia A, Caderni G, Rechkemmer G, Watzi B. Intestinal immunity of rats with colon cancer is modulated by oligo-fructose-enriched inulin combined with lactobacillus rhamnosus and bifidobacterium lactis. Br J Nutr 92(6):931-938, 2004 https://doi.org/10.1079/BJN20041289
  9. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401-1412, 1995
  10. Saarela M, Lahteenmaki L, Crittenden R, Salminen S, Mattila-Sandholm T. Gut bacteria and health foods-the European perspective. Int J Food Microbiol 15:99-117, 2002 https://doi.org/10.1016/0168-1605(92)90139-T
  11. Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108:975-982, 1995 https://doi.org/10.1016/0016-5085(95)90192-2
  12. Dzouzi BZ, Andrieux C. Comprred effects of three oligooaccharides on metabolism of intestinal microflora in rats inoculated with a human fecal flora. Br J Nutr 78:313-324, 1997 https://doi.org/10.1079/BJN19970149
  13. Boulnik Y, Raskine L, Simoneau G, Vicant E, Neut C, Flourie B, Brouns F, Barnet FR. The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. Am J Clin Nutr 80:1658-1664, 2004 https://doi.org/10.1093/ajcn/80.6.1658
  14. Tzortzis G, Goulas AK, Gee JM, Gibson GR. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J Nutr 135:1726-1731, 2005
  15. Koo M, Lao AV. Long term effect of bifidobacteria and neosugar on precursor lesions of colonic cancer in mice. Nutr Cancer 16:249-257, 1991 https://doi.org/10.1080/01635589109514163
  16. Bird RP. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett 93:55-71, 1995 https://doi.org/10.1016/0304-3835(95)03788-X
  17. Bird RP, Good CK. The significance of aberrant crypt foci in understanding the pathogenesis of colon cancer. Toxieol Lett 112-113:395-402, 2000 https://doi.org/10.1016/S0378-4274(99)00261-1
  18. Risio M. Cell proliferation in colorectal tumor progression: an immunohistochemical approach to intermediate biomarkers. J Cellular Biochem Suppl 16G:79-87, 1992
  19. Kelloff GJ, Malone WF, Boone CW, Steele VE, Doody LA. Intermediate biomarkers of precancer and their application in chemoprevention. J Cellular Bioehem Suppl 16G:15-21, 1992
  20. Yamashita N, Minamoto T, Onda M, Esumi H. Increased cell proliferation of azoxymethane-induced aberrant crypt foci of rat colon. Jpn J Cancer Res 85:692-698, 1994 https://doi.org/10.1111/j.1349-7006.1994.tb02416.x
  21. Bird RP. Observations and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett 37:147-151, 1987 https://doi.org/10.1016/0304-3835(87)90157-1
  22. Kulkarni N, Reddy BS. Inhibitory effect of bifidobacterium longum cultures on the azoxymethane-induced aberrant crypt foci formation and fecal bacterial ${\beta}$-glucuronidase. Proc Soc Exp Biol Med 207:278-283, 1994
  23. Reddy BS, Hamid R, Rao CV. Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18:1371-1374, 1997 https://doi.org/10.1093/carcin/18.7.1371
  24. Hsu CK, Liao JW, Chung YC, Hsieh CP, Chan YC. Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J Nutr 134:1523-1528, 2004
  25. Rowland IR, Rumney CJ, Coutts JT, Lievense LC. Effect of Bifidobacterium longum and inulin in gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis 19:281-285, 1998 https://doi.org/10.1093/carcin/19.2.281
  26. Gallaher DD, Stallings WH, Blessing LL, Busta FF, Brady LJ. Probiotics, cecal microflora, and aberrant crypts in the rat colon. J Nutr 126:1362-1371, 1996
  27. Hill MJ, Draser BS, Williams REO, Meade TW, Cox G, Simpson JEP, Morson BC. Fecal bile acids and clostridia in patients with cancer of the large bowl. Lancet 1:535-538, 1975
  28. Bustos-Fernandez L, dePaolo I, Hamamura S, Gonzalez E, Celener D, Caldarini M. Does secretin influence rat colonic absorption and secretion? Am J Gastroenterol 70:265-269, 1978
  29. Paganelli GM, Biasco G, Santucci R, Brandi G, Lalli AA, Miglioli M, Barbara L. Rectal cell proliferation and colorectal cancer risk level in patients with non-familial adenomatous polyps of the large bowel. Cancer 68:2451-2454, 1991 https://doi.org/10.1002/1097-0142(19911201)68:11<2451::AID-CNCR2820681121>3.0.CO;2-4
  30. Chang W-C L, Chapkin RS, Lupton JR. Fish oil blocks azoxymethane-induced rat colon tumorigenesis by increasing cell differentiation and apoptosis rather than decreasing cell proliferation. J Nutr 128:491-497, 1998
  31. American institute of Nutrition. Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. J Nutr 107:1340-1348, 1977 https://doi.org/10.1093/jn/107.7.1340