Hostname: page-component-745bb68f8f-lrblm Total loading time: 0 Render date: 2025-01-17T15:58:40.232Z Has data issue: false hasContentIssue false
  • English
  • Français

Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data

Published online by Cambridge University Press:  08 March 2007

Beatrice L. Pool-Zobel
Beatrice L. Pool-Zobel*
Affiliation:
Department of Nutritional Toxicology, Institute for Nutritional Sciences, Friedrich-Schiller-University Jena, Dornburger Strasse 25, 07743, Jena, Germany
*
*Corresponding author: Professor Beatrice L. Pool-Zobel, fax +49 3641 949672, email, b8pobe@uni-jena.de
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.

Inulin-type fructans (β(2,1)fructans) extracted from chicory roots (Cichorium intybus) are prebiotic food ingredients, which in the gut lumen are fermented to lactic acid and SCFA. Research in experimental animal models revealed that inulin-type fructans have anticarcinogenic properties. A number of studies report the effects of inulin-type fructans on chemically induced pre-neoplastic lesions (ACF) or tumours in the colon of rats and mice. In twelve studies, there were twenty-nine individual treatment groups of which twenty-four measured aberrant crypt foci (ACF) and five measured tumours. There was a significant reduction of ACF in twenty-one of the twenty-four treatment groups and of tumour incidence in five of the five treatment groups. Higher beneficial effects were achieved by synbiotics (mixtures of probiotics and prebiotics), long-chain inulin-type fructans compared to short-chain derivatives, and feeding high-fat Western style diets. Inulin-type fructans reduced tumour incidence in APCMin mice in two of four studies and reduced growth and metastasising properties of implanted tumour cells in mice (four studies). The effects have been reported to be associated with gut flora-mediated fermentation and production of butyrate. In human cells, inulin-derived fermentation products inhibited cell growth, modulated differentiation and reduced metastasis activities. In conclusion, evidence has been accumulated that shows that inulin-type fructans and corresponding fermentation products reduced the risks for colon cancer. The involved mechanisms included the reduction of exposure to risk factors and suppression of tumour cell survival. Thus, this specific type of dietary fibre exerted both blocking agent and suppressing agent types of chemopreventive activities.

Keywords

Inulin-type fructansColorectal cancerReview
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue S1 , April 2005 , pp. S73 - S90
Copyright
Copyright © The Nutrition Society 2005

References

Alberts, DS, Martinez, ME & Roe, DJ (2000) The Phoenix Colon Cancer Prevention Physicians' Network. Lack of effect of a high-fiber cereal supplement on the recurrence of colorectal adenomas. N Engl J Med 342, 1156–1162.CrossRefGoogle ScholarPubMed
Ames, BN & Gold, LS (1990) Too many rodent carcinogens: mitogenesis increases mutagenesis. Science 249, 970–971.CrossRefGoogle ScholarPubMed
Augeron, C & Laboisse, CL (1984) Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res 44, 3961–3969.Google Scholar
Bartram, HP, Scheppach, W, Schmid, H, Hofmann, A, Dusel, G, Richter, F, Richter, A & Kasper, H (1993) Proliferation of human colonic mucosa as an intermediate biomarker of carcinogenesis: effects of butyrate, desoxycholate, calcium, ammonia, and pH. Cancer Res 53, 3283–3288.Google Scholar
Beyer-Sehlmeyer, G, Glei, M, Hartmann, F, Hughes, R, Persin, C, Böhm, V, Rowland, IR, Schubert, R, Jahreis, G, Pool-Zobel, BL (2003) Butyrate is only one of several growth inhibitors produced during gut flora-mediated fermentation of dietary fibre sources. Br J Nutr 90, 1057–1070.CrossRefGoogle ScholarPubMed
Bingham, SA, Day, NE & Luen, R (2003) Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet 361, 1496–1501.CrossRefGoogle ScholarPubMed
Bird, RP (1987) Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett 37, 147–151.CrossRefGoogle ScholarPubMed
Bolognani, F, Rumney, CJ, Coutts, JT, Pool-Zobel, BL & Rowland, IR (2001) Effect of lactobacilli, bifidobacteria and inulin on the formation of aberrant crypt foci in rats. Eur J Nutr 40, 293–300.CrossRefGoogle ScholarPubMed
Bonithon-Kopp, C, Kronborg, O & Giacosa, A (2000) Calcium and fibre supplementation in prevention of colorectal adenoma recurrence: a randomised intervention trial. Lancet 356, 1300–1306.CrossRefGoogle ScholarPubMed
Bouhnik, Y, Vahedi, K, Achour, L, Attar, A, Salfati, J, Pochart, P, Marteau, P, Flourie, B, Bornet, F & Rambaud, JC (1999) Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. J Nutr 129, 113–116.CrossRefGoogle ScholarPubMed
Caderni, G, Luceri, C, DeFilippo, C, Salvadori, M, Giannini, A, Tessitore, L & Dolara, P (2001) Slow-release pellets of sodium butyrate do not modify azoxymethane (AOM)-induced intestinal carcinogenesis in F344 rats. Carcinogenesis 22, 525–527.CrossRefGoogle Scholar
Campbell, JM, Fahey, GC, Jr, Wolf BW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr 127, 130–136.CrossRefGoogle ScholarPubMed
Compher, CW, Frankel, WL, Tazelaar, J, Lawson, JA, McKinney, S, Segall, S, Kinosian, BP, Williams, NN & Rombeau, JL (1999) Wheat bran decreases aberrant crypt foci, preserves normal proliferation, and increases intraluminal butyrate levels in experimental colon cancer. J Parenter Enteral Nutr 23, 269–277.CrossRefGoogle ScholarPubMed
Corpet, DE & Pierre, F (2003) Point: from animal models to prevention of colon cancer. Systematic review of chemoprevention in Min mice and choice of the model system. Cancer Epidemiol Biomarkers Prev 12, 391–400.Google Scholar
DeFilippo, C, Caderni, G, Bazzicalupo, M, Briani, C, Giannini, A, Fazi, M & Dolara, P (1998) Mutations of the Apc gene in experimental colorectal carcinogenesis induced by azoxymethane in F344 rats. Br J Cancer 77, 2148–2151 Abstr.CrossRefGoogle Scholar
Ebert, MN, Beyer-Sehlmeyer, G, Liegibel, UM, Kautenburger, T, Becker, TW, Pool-Zobel, BL (2001) Butyrate-induces glutathione S-transferase in human colon cells and protects from genetic damage by 4-hydroxynonenal. Nutr Cancer 41, 156–164.CrossRefGoogle Scholar
Ebert, MN, Klinder, A, Schäferhenrich, A, Peters, WHM, Sendt, W, Scheele, J, Pool-Zobel, BL (2003) Expression of glutathione S-transferases (GST) in human colon cells and inducibility of GSTM2 by butyrate. Carcinogenesis 24, 1637–1644.CrossRefGoogle ScholarPubMed
Fazeli, A, Steen, RG, Dickinson, SL, Bautista, D, Dietrich, WF, Bronson, RT, Bresalier, RS, Sander, ES, Costa, J & Weinberg, RA (1997) Effects of p53 mutations on apoptosis in mouse intestinal and human colonic adenomas. Proc Natl Acad Sci USA 94, 10199–10204.CrossRefGoogle ScholarPubMed
Fearon, ER & Vogelstein, B (1990) A genetic model for colorectal tumorigenesis. Cell 61, 759–767.CrossRefGoogle ScholarPubMed
Femia, AP, Luceri, C, Dolara, P, Giannini, A, Biggeri, A, Salvadori, M, Clune, Y, Collins, KJ, Paglierani, M & Caderni, G (2002) Antitumourigenic 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, 1953–1960.CrossRefGoogle Scholar
Ferguson, LR (1999) Natural and man-made mutagens and carcinogens in the diet. Introduction to special issue of mutation research. Mutat Res 443, 1–10.Google Scholar
Ferguson, LR & Harris, PJ (2003) The dietary fibre debate: more food for thought – commentary. Lancet 361, 1487–1488.CrossRefGoogle Scholar
Ferguson, LR, Chavan, RR & Harris, PJ (2001) Changing concepts of dietary fiber: implications for carcinogenesis. Nutr Cancer 39, 155–169.CrossRefGoogle ScholarPubMed
Fodde, R, Smits, R & Clevers, H (2001) APC signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer 1, 55–67.CrossRefGoogle ScholarPubMed
Fuchs, CS, Giovannucci, E, Colditz, GA, Hunter, DJ, Stampfer, MJ, Rosner, B, Speizer, FE & Willett, WC (1999) Dietary fiber and the risk of colo-rectal cancer and adenoma in women. N Engl J Med 340, 169–176.CrossRefGoogle ScholarPubMed
Gallaher, DD & Khil, J (1999) The effect of synbiotics on colon carcinogenesis in rats. J Nutr 129, 1483S–1487S.CrossRefGoogle ScholarPubMed
Gallaher, DD, Stallings, WH, Blessing, LL, Busta, FF & Brady, LJ (1996) Probiotics, cecal microflora, and aberrant crypts in the rat colon. J Nutr 126, 1362–1371.CrossRefGoogle ScholarPubMed
Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125, 1401–1412.CrossRefGoogle ScholarPubMed
Gibson, PR, Rosella, O, Wilson, AJ, Mariadason, JM, Rickard, K, Byron, K & Barkla, DH (1999) Colonic epithelial cell activation and the paradoxical effects of butyrate. Carcinogenesis 20, 539–544.CrossRefGoogle ScholarPubMed
Hague, A, Manning, AM, Hanlon, KA, Huschtscha, LI, Hart, D & Paraskeva, C (1993) Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: implications for the possible role of dietary fibre in the prevention of large-bowel cancer. Int J Cancer 55, 498–505.CrossRefGoogle Scholar
Hague, A, Singh, B & Paraskeva, C (1997) Butyrate acts as a survival factor for colonic epithelial cells: further fuel for the in vivo versus in vitro debate. Gastroenterology 112, 1036–1040.CrossRefGoogle ScholarPubMed
Harris, PJ & Ferguson, LR (1993) Dietary fibre: its composition and role in protection against colorectal cancer. Mutat Res 290, 97–110.CrossRefGoogle ScholarPubMed
Hidaka, H, Eida, T, Takizawa, T, Tokunaga, T & Tashiro, Y (1986) Effects of fructooligosaccharides on intestinal flora and human health. Bifidobacteria Microflora 5, 37–50.CrossRefGoogle Scholar
Hughes, R & Rowland, IR (2001) Stimulation of apoptosis by two prebiotic chicory fructans in the rat colon. Carcinogenesis 22, 43–47.CrossRefGoogle ScholarPubMed
Jacoby, RF, Cole, CE, Lubet, RA & You, M (2001) Effect of the non-specific Cox1/2 inhibitor piroxicam and the ornithine decarboxylase inhibitor difluoromethylornitine (DFMO) on development of intestinal tumours in mice bearing germline alteration the Msh2 or APC genes. Proc Am Assoc Cancer Res 42 263 Abstr., 1422.Google Scholar
Johnson, IT (1995) Butyrate and markers of neoplastic change in the colon. Eur J Cancer Prev 4, 365–371.CrossRefGoogle ScholarPubMed
Johnson, IT, Williamson, G & Musk, SRR (1994) Anticarcinogenic factors in plant foods: a new class of nutrients?. Nutr Res Rev 7, 175–204.CrossRefGoogle Scholar
Klinder, A, Förster, A, Caderni, G, Femia, AP, Pool-Zobel, BL ((2004a)) Fecal water genotoxicity is predictive of tumor-preventive activities by inulin-like oligofructoses, probiotics ( Lactobacillus rhamnosus and Bifidobacterium lactis ) and their synbiotic combination. Nutr Cancer 49, 144–155.CrossRefGoogle ScholarPubMed
Klinder, A, Gietl, E, Hughes, R ((2004b)) Gut fermentation products of inulin-derived prebiotics inhibit markers of tumour progression in human conon tumour cells. Int J Cancer Prev 1, 19–32.Google Scholar
Kobayashi, H, Tan, ME & Fleming, SE (2003) Sodium butyrate inhibits cell growth and stimulates p21 wap/CIPI protein in human colonic adenocarcinoma cells independently of p53 status. Nutr Cancer 46, 202–211.CrossRefGoogle Scholar
Kok, TMCM, van Maanen, JMS (2000) Evaluation of fecal mutagenicity and colorectal cancer risk. Mutat Res 463, 53–101.CrossRefGoogle ScholarPubMed
Koo, M & Rao, AV (1991) Long-term effect of bifidobacteria and Neosugar on precursor lesions of colonic cancer in CF1 mice. Nutr Cancer 16, 249–257.CrossRefGoogle ScholarPubMed
Kruh, J (1982) Effects of sodium butyrate, a new pharmacological agent on cells in culture. Mol Cell Biochem 42, 65–82.Google ScholarPubMed
Levin, B (2003) Potential pitfalls in the use of surrogate endpoints in colorectal adenoma chemoprevention. JNCI Cancer Spectr 95, 697.Google ScholarPubMed
Lipkin, M (in preparation). Effects of Raftilose on tumor occurrence in APC MIN mice. Report, Orafti, Tienen, Belgium.Google Scholar
Lupton, JR (1995) Butyrate and colonic cytokinetics: differences between in vitro and in vivo studies. Eur J Cancer Prev 4, 373–378.CrossRefGoogle ScholarPubMed
Lupton, JR (2004) Microbial degradation products influence colon cancer risk, the butyrate controversy. J Nutr 134, 479–482.CrossRefGoogle ScholarPubMed
McIntosh, GH, Royle, PJ & Pointing, G (2001) Wheat aleurone flour increases cecal β-glucuronidase activity and butyrate concentration and reduce colon adenoma burden in azoxymethane treated rats. J Nutr 131, 127–131.CrossRefGoogle ScholarPubMed
McIntyre, A, Gibson, PR & Young, GP (1993) Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 34, 386–391.CrossRefGoogle ScholarPubMed
McLellan, EA & Bird, RP (1988) Aberrant crypts: potential preneoplastic lesions in the murine colon. Cancer Res 48, 6187–6192.Google ScholarPubMed
Magnuson, B, Carr, I & Bird, RP (1993) Ability of aberrant crypt foci characteristics to predict colonic tumour incidence in rats fed cholic acid. Cancer Res 53, 4499–4504.Google ScholarPubMed
Mariadason, JM, Corner, GA & Augenlicht, LH (2000) Genetic reprogramming in pathways of colonic cell maturation induced by shortchain fatty acids; comparison with trichostatin A, sulindac and curcumin, and implications for chemoprevention of colon cancer. Cancer Res 60, 4561–4572.Google ScholarPubMed
Mariadason, JM, Velchich, A, Wilson, AJ, Augenlicht, LH & Gibson, PR (2001) Resistance to butyrate-induced cell differentiation and apoptosis during spontaneous Caco-2 cell differentiation. Gastroenterology 120, 889–899.CrossRefGoogle ScholarPubMed
Mutanen, M, Pajari, AM & Oikarinen, SI (2000) Beef induces and rye bran prevents the formation of intestinal polyps in Apc Min mice: relation to β-catenin and PKC isozymes. Carcinogenesis 21, 1167–1173.CrossRefGoogle ScholarPubMed
Oberreuther-Moschner, D, Jahreis, G, Rechkemmer, G, Pool-Zobel, BL (2004) Dietary intervention with the probiotics Lactobacillus acidophilus 145 and Bifidobacterium longum 913 modulates the potential of human faecal water to induce damage in HT29clone19A cells. Br J Nutr 91, 925–932.CrossRefGoogle ScholarPubMed
Osswald, K, Becker, TW, Grimm, M, Jahreis, G, Pool-Zobel, BL (2000) Inter- and intra-individual variation of faecal water – genotoxicity in human colon cells. Mutat Res 472, 59–70.CrossRefGoogle ScholarPubMed
Pajari, AM, Rajakangas, J, Päivärinta, E, Kosma, VM, Rafter, J & Mutanen, M (2003) Promotion of intestinal tumour formation by inulin is associated with an accumulation of β-catenin in MIN mice. Int J Cancer 106, 653–660.CrossRefGoogle ScholarPubMed
Pereira, MA, Barnes, LH, Rassman, VL, Kelloff, GV & Steele, VE (1994) Use of azoxymethane-induced foci of aberrant crypts in rat colon to identify potential cancer chemopreventive agents. Carcinogenesis 15, 1049–1054.CrossRefGoogle ScholarPubMed
Perrin, P, Pierre, F, Patry, Y, Champ, M, Berreur, M, Pradal, G, Bornet, P, Meflah, K & Menenteau, J (2001) Only fibres promoting a stable butyrate producing colonic ecosystem decrease the rate of aberrant crypt foci in rats. Gut 48, 53–61.CrossRefGoogle ScholarPubMed
Peters, U, Sinha, R & Chaterjee, N (2003) Dietary fibre and colorectal adenoma in a colorectal cancer early detection programme. Lancet 361, 1401–1405.CrossRefGoogle Scholar
Pierre, F, Perrin, P, Champ, M, Bornet, F, Meflah, K & Menanteau, J (1997) Short chain fructo-oligosaccharides reduce the occurrence of colon tumours and develop gut associated lymphoid tissue in Min mice. Cancer Res 57, 225–228.Google ScholarPubMed
Pietinen, P, Malila, N, Virtanen, M, Hartman, TJ, Tangrea, JA, Albanes, D & Virtamo, J (1999) Diet and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control 10, 387–396.CrossRefGoogle Scholar
Pool-Zobel, BL & Cherbut, C (2003) Discussion forum on ‘diets enriched with cereal brans or inulin modulate protein kinase C activity and isozyme expression in rat colonic mucosa’ – Comments by Pool-Zobel Cherbut. Br J Nutr 89, 283–284.CrossRefGoogle Scholar
Pool-Zobel, BL, Neudecker, C, Domizlaff, I, Ji, S, Schillinger, U, Rumney, CJ, Moretti, M, Villarini, M, Scassellati-Sforzolini, G & Rowland, IR (1996) Lactobacillus - and Bifidobacterium -mediated antigenotoxicity in colon cells of rats: prevention of carcinogen-induced damage in vivo and elucidation of involved mechanisms. Nutr Cancer 26, 365–380.CrossRefGoogle Scholar
Pool-Zobel, BL, Van Loo, J, Rowland, IR & Roberfroid, MB (2002) Experimental evidences on the potential of prebiotic fructans to reduce the risk of colon cancer. Br J Nutr 87, S273–S281.CrossRefGoogle ScholarPubMed
Potter, JD (1999) Colorectal cancer: molecules and populations. J Natl Cancer Inst 91, 916–932.CrossRefGoogle ScholarPubMed
Poulson, M, Mølck, AM & Jacobsen, BL (2002) Different effects of short- and long-chained fructans on large intestinal physiology and carcinogen-induced aberrant crypt foci in rats. Nutr Cancer 42, 194–205.CrossRefGoogle Scholar
Rafter, J, Chin, SM, Andersson, AM, Alder, R, Eng, W & Bruce, R (1987) Cellular toxicity of faecal water depends on diet. Am J Clin Nutr 45, 559–563.CrossRefGoogle ScholarPubMed
Rao, CV, Chou, D, Simi, B, Ku, H & Reddy, BS (1998) Prevention of colonic aberrant crypt foci and modulation of large bowel microbial activity by dietary coffee fiber, inulin and pectin. Carcinogenesis 19, 1815–1819.CrossRefGoogle ScholarPubMed
Reddy, BS, Hamid, R & Rao, CV (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18, 1371–1374.CrossRefGoogle ScholarPubMed
Roberfroid, MB (1998) Prebiotics and synbiotics: concepts and nutritional properties. Br J Nutr 80, S197–S202.CrossRefGoogle ScholarPubMed
Roberfroid, MB, Van Loo, J & Gibson, GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. J Nutr 128, 11–19.CrossRefGoogle ScholarPubMed
Rowland, IR (1991) Nutrition and gut flora metabolism Nutrition, Toxicity and Cancer, 113–136 [Rowland, IR, editors]. Boca Raton, Ann Arbor, Boston, London: CRC Press.Google Scholar
Rowland, IR (1993) Diet, gut microflora and carcinogenesis Food, Nutrition and Chemical Toxicity, 337–341 [Parke, DVWalker, R, editors]. Great Britain: Smith-Gordon.Google Scholar
Rowland, IR, Bearne, CA, Fischer, R, Pool-Zobel, BL (1996) The effect of lactulose on DNA damage induced by 1,2-dimethylhydrazine in the colon of human-flora-associated rats. Nutr Cancer 26, 38–47.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
Schatzkin, A, Lanza, E & Corle, D (2000) The Polyp Prevention Trial Study Group. Lack of effect of a low-fat, high-fiber diet on the recurrence of colorectal adenomas. N Engl J Med 342, 1149–1155.CrossRefGoogle Scholar
Schiffman, MH (1987) Diet and faecal genotoxicity. Cancer Surv 6, 653–672.Google ScholarPubMed
Shoemaker, AR, Luongo, C, Moser, AR, Marton, LJ & Dove, WF (1997) Somatic mutational mechanisms involved in intestinal tumour formation in Min mice. Cancer Res 57, 1999–2006.Google ScholarPubMed
Taper, HS & Roberfroid, M (1999) Influence of inulin and oligofructose on breast cancer and tumour growth. J Nutr 129, 1488S–1491S.CrossRefGoogle Scholar
Taper, HS & Roberfroid, MB (2000) Inhibitory effect of dietary inulin or oligofructose on the development of cancer metastases. Anticancer Res 20, 4291–4294.Google ScholarPubMed
Taper, HS & Roberfroid, MB (2000b) Nontoxic potentiation of cancer chemotherapy by dietary oligofructose or inulin. Nutr Cancer 38, 1–5.CrossRefGoogle ScholarPubMed
Taper, HS & Roberfroid, MB (2002) Inulin/oligofructose and anticancer therapy. Br J Nutr 87, S283–S286.CrossRefGoogle ScholarPubMed
Taper, HS, Lemort, C & Roberfroid, MB (1998) Inhibition effect of dietary inulin and oligofructose on the growth of transplantable mouse tumour. Anticancer Res 18, 4123–4126.Google Scholar
Terpstra, OT, van Blankenstein, M, Dees, J & Eilers, GAM (1987) Abnormal pattern of cell proliferation in the entire colonic mucosa of patients with colon adenoma or cancer. Gastroenterology 92, 704–708.CrossRefGoogle ScholarPubMed
Terry, P, Giovannucci, E, Michels, KB, Bergvist, L, Hansen, H, Holmberb, L & Wolk, A (2001) Fruit, vegetables, dietary fiber, and risk of colorectal cancer. J Natl Cancer Inst 93, 525–533.CrossRefGoogle ScholarPubMed
Thun, MJ, Henley, SJ & Patrono, C (2002) Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 94, 252–266.CrossRefGoogle ScholarPubMed
Van Loo, J (1995) On the presence of inulin and oligofructose as natural ingredients in the Western diet. Crit Rev Food Sci Nutr 35, 525–552.CrossRefGoogle ScholarPubMed
Venturi, M, Hambly, RJ, Glinghammer, B, Rafter, JJ & Rowland, IR (1997) Genotoxic activity in human faecal water and the role of bile acids: a study using the alkaline comet assay. Carcinogenesis 18, 2353–2359.CrossRefGoogle ScholarPubMed
Verghese, M, Rao, DR, Chawan, CB & Shackelford, L (2002) Dietary inulin suppresses azoxymethane-induced preneoplastic aberrant crypt foci in mature Fisher 344 rats. J Nutr 132, 2804–2808.CrossRefGoogle ScholarPubMed
Verghese, M, Rao, DR, Chawan, CB, Williams, LL & Schackelford, LA (2002b) Dietary inulin suppresses azoxymethane-induced aberrant crypt foci and colon tumours at the promotion stage in young Fisher 344 rats. J Nutr 132, 2809–2813.CrossRefGoogle ScholarPubMed
Verghese, M, Walker, LT, Shackelford, L, Chawan, CB, Van Loo, J (2003) Inhibitory effects of non-digestible carbohydrates of different chain lengths on AOM-induced aberrant crypt foci in Fisher 344 rats. In Proceedings of the Second Annual AACR International Conference 'Frontiers in Cancer Prevention Research', Phoenix, AZ, 26–30 October 2003. Poster B186 Abstr.Google Scholar
Wargovich, MJ, Harris, C, Chen, CD, Palmer, C, Steele, VE & Kelloff, GF (1992) Growth kinetics and chemoprevention of aberrant crypts in the rat colon. J Cell Biochem, Suppl. 15G, 51–54.CrossRefGoogle Scholar
Wattenberg, LW (1992) Inhibition of carcinogenesis by minor dietary constituents. Cancer Res 52, Suppl., 2085s–2091s.Google ScholarPubMed
Wollowski, I, Ji, S, Bakalinsky, AT, Neudecker, C, Pool-Zobel, BL (1999) Bacteria used for the production of yogurt inactivate carcinogens and prevent DNA damage in the colon of rats. J Nutr 129, 77–82.CrossRefGoogle ScholarPubMed
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
Yang, K, Fan, K, Shinozaki, H, Newmark, H, Edelmann, W, Kucherlapati, R & Lipkin, M (1999) Sulindac increases carcinoma development in the colons of mice with Apc mutations. Proc Am Assoc Cancer Res 40 523 Abstr. 3488.Google Scholar
Yang, K, Fan, K, Lia, M, Edelmann, W, Augenlicht, LH, Lubet, R, Kopelovich, L, Kucherlapati, R & Lipkin, M (2001) Sulindac increases tumour development in the colon of mice with Mlh1/mutation. Proc Am Assoc Cancer Res 42 264 Abstr. 1423.Google Scholar