Novel combination of prebiotics galacto-oligosaccharides and inulin-inhibited aberrant crypt foci formation and biomarkers of colon cancer in Wistar rats

Nutrients

Volumn 8, Issue 8, 2016, Pages

  Qamar, Tahir Rasool ^a   Syed, Fatima ^a   Nasir, Muhammad ^a   Rehman, Habib ^a   Zahid, Muhammad Nauman ^b   Liu, Rui Hai ^b   Iqbal, Sanaullah ^a  

^a UNIVERSITY OF VETERINARY AND ANIMAL SCIENCES   (Pakistan)

^b Cornell University ^*  (United States)

Author keywords

Biomarkers; Colon cancer; Galacto oligosaccharides; Inulin; Prebiotics

Indexed keywords

AMMONIA; BETA GLUCOSIDASE; BETA GLUCURONIDASE; GALACTOSE OLIGOSACCHARIDE; NITROREDUCTASE; PREBIOTIC AGENT; 1,2 DIMETHYLHYDRAZINE; 4'-GALACTOOLIGOSACCHARIDE; ANTINEOPLASTIC AGENT; BACTERIAL PROTEIN; INULIN; TRISACCHARIDE; TUMOR MARKER; VOLATILE FATTY ACID;

ABERRANT CRYPT FOCUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMOPROPHYLAXIS; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; FOOD INTAKE; HISTOLOGY; MALE; NONHUMAN; PH; RAT; ABERRANT CRYPT FOCI; ANIMAL; CECUM; CHEMISTRY; COLON; COLONIC NEOPLASMS; COMPARATIVE STUDY; DISEASE MODEL; ENZYMOLOGY; FECES; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOLOGY; RANDOMIZATION; STEREOISOMERISM; WISTAR RAT;

1,2-DIMETHYLHYDRAZINE; ABERRANT CRYPT FOCI; AMMONIA; ANIMALS; ANTICARCINOGENIC AGENTS; BACTERIAL PROTEINS; BIOMARKERS, TUMOR; CECUM; COLON; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; FATTY ACIDS, VOLATILE; FECES; HYDROGEN-ION CONCENTRATION; INTESTINAL MUCOSA; INULIN; MALE; PREBIOTICS; RANDOM ALLOCATION; RATS, WISTAR; STEREOISOMERISM; TRISACCHARIDES;

EID: 84982831987     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu8080465     Document Type: Article

References (43)

1. Benson, A.L. Epidemiology, disease progression, and economic burden of colorectal cancer. J. Manag. Care Pharm. 2007, 13, S5-S18. [CrossRef] [PubMed]
2. Watson, A.J.; Collins, P.D. Colon cancer: A civilization disorder. Dig. Dis. 2011, 29, 222-228. [CrossRef] [PubMed]
3. Bastide, N.M.; Pierre, F.H.; Corpet, D.E. Heme iron from meat and risk of colorectal cancer: A meta-analysis and a review of the mechanisms involved. Cancer Prev. Res. 2011, 4, 177-184. [CrossRef] [PubMed]
4. Khan, N.; Afaq, F.; Mukhtar, H. Lifestyle as risk factor for cancer: Evidence from human studies. Cancer Lett. 2010, 293, 133-143. [CrossRef] [PubMed]
5. Van Engeland, M.; Derks, S.; Smits, K.M.; Meijer, G.A.; Herman, J.G. Colorectal cancer epigenetics: Complex simplicity. J. Clin. Oncol. 2011, 29, 1382-1391. [CrossRef] [PubMed]
6. Poulsen, M.; Mortensen, A.; Binderup, M.L.; Langkilde, S.; Markowski, J.; Dragsted, L.O. The effect of apple feeding on markers of colon carcinogenesis. Nutr. Cancer 2011, 63, 402-409. [CrossRef] [PubMed]
7. Tarapore, R.S.; Siddiqui, I.A.; Mukhtar, H. Modulation of wnt/beta-catenin signaling pathway by bioactive food components. Carcinogenesis 2012, 33, 483-491. [CrossRef] [PubMed]
8. Fotiadis, C.I.; Stoidis, C.N.; Spyropoulos, B.G.; Zografos, E.D. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World J. Gastroenterol. 2008, 14, 6453-6457. [CrossRef] [PubMed]
9. Macfarlane, G.T.; Macfarlane, S. Fermentation in the human large intestine: Its physiologic consequences and the potential contribution of prebiotics. J. Clin. Gastroenterol. 2011, 45, S120-S127. [CrossRef] [PubMed]
10. Campbell, J.M.; Fahey, G.C., Jr.; Wolf, B.W. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J. Nutr. 1997, 127, 130-136. [PubMed]
11. Ebert, M.N.; Beyer-Sehlmeyer, G.; Liegibel, U.M.; Kautenburger, T.; Becker, T.W.; Pool-Zobel, B.L. Butyrate induces glutathione s-transferase in human colon cells and protects from genetic damage by 4-hydroxy-2-nonenal. Nutr. Cancer 2001, 41, 156-164. [CrossRef] [PubMed]
12. Torres, D.P.M.; Gonçalves, M.d.P.F.; Teixeira, J.A.; Rodrigues, L.R. Galacto-oligosaccharides: Production, properties, applications, and significance as prebiotics. Compr. Rev. Food Sci. Food Saf. 2010, 9, 438-454. [CrossRef]
13. Laparra, J.M.; Diez-Municio, M.; Herrero, M.; Moreno, F.J. Structural differences of prebiotic oligosaccharides influence their capability to enhance iron absorption in deficient rats. Food Funct. 2014, 5, 2430-2437. [CrossRef] [PubMed]
14. Sivieri, K.; Spinardi-Barbisan, A.L.T.; Barbisan, L.F.; Bedani, R.; Pauly, N.D.; Carlos, I.Z.; Benzatti, F.; Vendramini, R.C.; Rossi, E.A. Probiotic Enterococcus faecium CRL 183 inhibit chemically induced colon cancer in maleWistar rats. Eur. Food Res. Technol. 2008, 228, 231-237. [CrossRef]
15. Gallaher, D.D.; Khil, J. The effect of synbiotics on colon carcinogenesis in rats. J. Nutr. 1999, 129, 1483S-1487S. [PubMed]
16. Femia, A.P.; Luceri, C.; Dolara, P.; Giannini, A.; Biggeri, A.; Salvadori, M.; Clune, Y.; Collins, K.J.; Paglierani, M.; Caderni, G. 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 2002, 23, 1953-1960. [CrossRef] [PubMed]
17. Pool-Zobel, B.; van Loo, J.; Rowland, I.; Roberfroid, M.B. Experimental evidences on the potential of prebiotic fructans to reduce the risk of colon cancer. Br. J. Nutr. 2002, 87 (Suppl. S2), S273-S281. [CrossRef] [PubMed]
18. Reddy, B.S. Prevention of colon cancer by pre- and probiotics: Evidence from laboratory studies. Br. J. Nutr. 1998, 80, S219-S223. [PubMed]
19. Wijnands, M.V.; Appel, M.J.; Hollanders, V.M.; Woutersen, R.A. A comparison of the effects of dietary cellulose and fermentable galacto-oligosaccharide, in a rat model of colorectal carcinogenesis: Fermentable fibre confers greater protection than non-fermentable fibre in both high and low fat backgrounds. Carcinogenesis 1999, 20, 651-656. [CrossRef] [PubMed]
20. Wijnands, M.V.; Schoterman, H.C.; Bruijntjes, J.B.; Hollanders, V.M.; Woutersen, R.A. Effect of dietary galacto-oligosaccharides on azoxymethane-induced aberrant crypt foci and colorectal cancer in fischer 344 rats. Carcinogenesis 2001, 22, 127-132. [CrossRef] [PubMed]
21. Reeves, P.G.; Rossow, K.L.; Lindlauf, J. Development and testing of the ain-93 purified diets for rodents: Results on growth, kidney calcification and bone mineralization in rats and mice. J. Nutr. 1993, 123, 1923-1931. [PubMed]
22. Reagan-Shaw, S.; Nihal, M.; Ahmad, N. Dose translation from animal to human studies revisited. FASEB J. 2008, 22, 659-661. [CrossRef] [PubMed]
23. Dias, M.C.; Spinardi-Barbisan, A.L.; Rodrigues, M.A.; de Camargo, J.L.; Teran, E.; Barbisan, L.F. Lack of chemopreventive effects of ginger on colon carcinogenesis induced by 1,2-dimethylhydrazine in rats. Food Chem. Toxicol. 2006, 44, 877-884. [CrossRef] [PubMed]
24. Dias, M.C.; Vieiralves, N.F.; Gomes, M.I.; Salvadori, D.M.; Rodrigues, M.A.; Barbisan, L.F. Effects of lycopene, synbiotic and their association on early biomarkers of rat colon carcinogenesis. Food Chem. Toxicol. 2010, 48, 772-780. [CrossRef] [PubMed]
25. Iqbal, S.; Nguyen, T.H.; Nguyen, T.T.; Maischberger, T.; Haltrich, D. Beta-galactosidase from Lactobacillus plantarum WCFS1: Biochemical characterization and formation of prebiotic galacto-oligosaccharides. Carbohydr. Res. 2010, 345, 1408-1416. [CrossRef] [PubMed]
26. Lin, H.C.; Visek, W.J. Large intestinal ph and ammonia in rats: Dietary fat and protein interactions. J. Nutr. 1991, 121, 832-843. [PubMed]
27. Bird, R.P. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett. 1995, 93, 55-71. [CrossRef]
28. Goldin, B.R.; Gorbach, S.L. The relationship between diet and rat fecal bacterial enzymes implicated in colon cancer. J. Natl. Cancer Inst. 1976, 57, 371-375. [PubMed]
29. Zhao, G.; Nyman, M.; Åke Jönsson, J. Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography. Biomed. Chromatogr. 2006, 20, 674-682. [CrossRef] [PubMed]
30. Verma, A.; Shukla, G. Administration of prebiotic inulin suppresses 1,2 dimethylhydrazine dihydrochloride induced procarcinogenic biomarkers fecal enzymes and preneoplastic lesions in early colon carcinogenesis in sprague dawley rats. J. Funct. Foods 2013, 5, 991-996. [CrossRef]
31. Aachary, A.A.; Gobinath, D.; Srinivasan, K.; Prapulla, S.G. Protective effect of xylooligosaccharides from corncob on 1,2-dimethylhydrazine induced colon cancer in rats. Bioact. Carbohydr. Diet. Fibre 2015, 5, 146-152. [CrossRef]
32. Pool-Zobel, B.L.; Sauer, J. Overview of experimental data on reduction of colorectal cancer risk by inulin-type fructans. J. Nutr. 2007, 137, 2580S-2584S. [PubMed]
33. Van deWiele, T.; Boon, N.; Possemiers, S.; Jacobs, H.; Verstraete, W. Inulin-type fructans of longer degree of polymerization exert more pronounced in vitro prebiotic effects. J. Appl. Microbiol. 2007, 102, 452-460. [CrossRef] [PubMed]
34. Macfarlane, G.T.; Macfarlane, S. Bacteria, colonic fermentation, and gastrointestinal health. J. AOAC Int. 2012, 95, 50-60. [CrossRef] [PubMed]
35. Daly, K.; Cuff, M.A.; Fung, F.; Shirazi-Beechey, S.P. The importance of colonic butyrate transport to the regulation of genes associated with colonic tissue homoeostasis. Biochem. Soc. Trans. 2005, 33, 733-735. [CrossRef] [PubMed]
36. Vinolo, M.A.; Rodrigues, H.G.; Nachbar, R.T.; Curi, R. Regulation of inflammation by short chain fatty acids. Nutrients 2011, 3, 858-876. [CrossRef] [PubMed]
37. Fung, K.Y.; Cosgrove, L.; Lockett, T.; Head, R.; Topping, D.L. A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate. Br. J. Nutr. 2012, 108, 820-831. [CrossRef] [PubMed]
38. Lupton, J.R.; Marchant, L.J. Independent effects of fiber and protein on colonic luminal ammonia concentration. J. Nutr. 1989, 119, 235-241. [PubMed]
39. De Preter, V.; Vanhoutte, T.; Huys, G.; Swings, J.; de Vuyst, L.; Rutgeerts, P.; Verbeke, K. Effects of Lactobacillus casei shirota, Bifidobacterium breve, and oligofructose-enriched inulin on colonic nitrogen-protein metabolism in healthy humans. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292, G358-G368. [CrossRef] [PubMed]
40. Geboes, K.P.; de Hertogh, G.; de Preter, V.; Luypaerts, A.; Bammens, B.; Evenepoel, P.; Ghoos, Y.; Geboes, K.; Rutgeerts, P.; Verbeke, K. The influence of inulin on the absorption of nitrogen and the production of metabolites of protein fermentation in the colon. Br. J. Nutr. 2006, 96, 1078-1086. [CrossRef] [PubMed]
41. Tappenden, K.A.; Deutsch, A.S. The physiological relevance of the intestinal microbiota—Contributions to human health. J. Am. Coll. Nutr. 2007, 26, 679S-683S. [CrossRef] [PubMed]
42. Klewicka, E.; Zdúnczyk, Z.; Júskiewicz, J. Effect of lactobacillus fermented beetroot juice on composition and activity of cecal microflora of rats. Eur. Food Res. Technol. 2009, 229, 153-157. [CrossRef]
43. Ayesh, R.; Weststrate, J.A.; Drewitt, P.N.; Hepburn, P.A. Safety evaluation of phytosterol esters. Part 5. Faecal short-chain fatty acid and microflora content, faecal bacterial enzyme activity and serum female sex hormones in healthy normolipidaemic volunteers consuming a controlled diet either with or without a phytosterol ester-enriched margarine. Food Chem. Toxicol. 1999, 37, 1127-1138. [PubMed]