Abstract
Background
Prebiotics are non-digestible compounds that beneficially affect the host by stimulating the growth and/or activity of one or a limited number of resident colonic bacteria in the gut. Reported beneficial effects of prebiotics include reduced gut infections, better absorption of minerals, and notably, antitumorigenic effects. Arabinoxylan (AX)-oligosaccharides (AXOS) have been suggested to exert prebiotic effects in the gut, but their effect on colon carcinogenesis has not been studied so far.
Aim of the study
To test the effect of AXOS in a rat colon carcinogenesis model.
Methods
We determined the occurrence of two types of preneoplastic lesions [aberrant crypt foci (ACF) and mucin depleted foci (MDF)] in the colon of rats treated with the colon carcinogen 1,2-dimethylhydrazine (DMH) and fed either a control diet or a diet containing AXOS (4.8% w/w) (15 rats in each group).
Results
Thirteen weeks after DMH treatment, MDF counts were significantly lower in the entire colon of AXOS fed rats (MDF/colon were 7.5 ± 0.6 and 5.5 ± 0.6, in Control and AXOS groups, respectively, means ± SE, P < 0.05). Although the number of ACF in the entire colon was not significantly different between Control and AXOS fed rats, AXOS fed rats had significantly fewer ACF in the distal part of the colon than Control group rats (ACF/distal colon were 135.5 ± 15 and 84.4 ± 11, in Control and AXOS groups, respectively, means ± SE, P < 0.05).
Conclusions
The present study shows that dietary intake of AXOS by rats reduces the occurrence of two types of preneoplastic lesions, thus suggesting a chemopreventive effect on colon carcinogenesis that should be confirmed in a long-term carcinogenesis experiment.
References
Andersson R, Aman P (2001) Cereal arabinoxylan: occurrence, structure and properties. In: McCleary BV, Prosky L (eds) Advanced dietary fibre technology. Blackwell Science Ltd, Oxford, pp 301–314
Anonymous (2000) Approved methods of the American Association of Cereal Chemists, 10th edn. AACC, St. Paul, MN, USA
AOAC (1995) Official methods of analysis, 16th edition. Method 990.03. Association of Official Analytical Chemists, WA, USA
Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489
Boyle FG, Wrenn JM, Marsh BB, Anderson WI, Angelosanto FA, McCartney AL, Lien EL (2008) Safety evaluation of oligofructose: 13 week rat study and in vitro mutagenicity. Food Chem Toxicol 46:3132–3139
Buddington KK, Donahoo JB, Buddington RK (2002) Dietary oligofructose and inulin protect mice from enteric and systemic pathogens and tumor inducers. J Nutr 132:472–477
Caderni G, Femia AP, Giannini A, Favuzza A, Luceri C, Salvadori M, Dolara P (2003) Identification of mucin-depleted foci in the unsectioned colon of azoxymethane-treated rats: correlation with carcinogenesis. Cancer Res 63:2388–2392
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
Cleemput G, Roels SP, van Oort MG, Grobet PJ, Delcour JA (1993) Heterogeneity in the structure of water soluble arabinoxylans in European wheat flours of variable breadmaking quality. Cereal Chem 70:324–329
Cloetens L, De Preter V, Swennen K, Broekaert WF, Courtin CM, Delcour JA, Rutgeerts P, Verbeke K (2008) Dose-response effect of arabinoxylo-oligosaccharides on gastrointestinal motility and on colonic bacterial metabolism in healthy volunteers. J Am Coll Nutr 27:512–518
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
Courtin CM, Swennen K, Broekaert WF, Swennen Q, Buyse J, Decuypere E, Michiels CW, De Ketelaere B, Delcour JA (2008) Effects of dietary inclusion of xylooligosaccharides, arabinoxylooligosaccharides and soluble arabinoxylan on the microbial composition of caecal contents of chickens. J Sci Food Agric 88:2517–2522
Courtin CM, Broekaert WF, Aerts G, Van Craeyveld V, Delcour JA (2009) Occurrence of arabinoxylo-oligosaccharides and arabinogalactan peptides in beer. J Am Soc Brew Chem 67:112–117
Courtin CM, Swennen K, Broekaert WF, Lescroart O, Onagbesan O, Buyse J, Decuypere E, Van de Wiele T, Marzoratti M, Verstraete W, Huyghebaert G, Delcour JA (2008) Dietary inclusion of wheat bran arabinoxylooligosaccharides has beneficial nutritional effects on chickens. Cereal Chem 85:607–613
Eeckhaut V, Van Immerseel F, Dewulf J, Pasmans F, Haesebrouck F, Ducatelle R, Courtin CM, Delcour JA, Broekaert WF (2008) Arabinoxylooligosaccharides from wheat bran inhibit Salmonella colonization in broiler chickens. Poult Sci 87:2329–2334
European Community: European Community Regulations on the Care and Use of Laboratory Animals (1986) (Law 86/609/EC)
Femia AP, Luceri C, Dolara P, Giannini A, Biggeri A, Salvadori M, Clune Y, Collins KJ, Paglierani M, Caderni G (2002) 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 23:1953–1960
Femia AP, Caderni G, Bottini C, Salvadori M, Dolara P, Tessitore L (2007) Mucin-depleted foci are modulated by dietary treatments and show deregulation of proliferative activity in carcinogen-treated rodents. Int J Cancer 120:2301–2305
Femia AP, Dolara P, Caderni G (2004) Mucin-depleted foci (MDF) in the colon of rats treated with azoxymethane (AOM) are useful biomarkers for colon carcinogenesis. Carcinogenesis 25:277–281
Femia AP, Giannini A, Fazi M, Tarquini E, Salvadori M, Roncucci L, Tonelli F, Dolara P, Caderni G (2008) Identification of mucin depleted foci in the human colon. Cancer Prev Res 1:562–567
Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412
Grootaert C, Van den Abbeele P, Marzorati M, Broekaert WF, Courtin CM, Delcour JA, Verstraete W, Van de Wiele T (2009) Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol Ecol 69:231–242
Hartmann G, Piber M, Koehler P (2005) Isolation and chemical characterisation of water-extractable arabinoxylans from wheat and rye during breadmaking. Eur Food Res Technol 221:487–492
Hsu CK, Liao JW, Chung YC, Hsieh CP, Chan YC (2004) Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesions development in rats. J Nutr 134:1523–1528
Izydorczyk MS, Biliaderis CG (1995) Cereal arabinoxylans: in structure and physicochemical properties. Carbohydr Polym 28:33–48
Katapodis P, Vardakou M, Kalogeris E, Kekos D, Macris BJ, Christakopoulos P (2003) Enzymic production of a feruloylated oligosaccharide with antioxidant activity from wheat flour arabinoxylan. Eur J Nutr 42:55–60
Kimura Y, Kono S, Toyomura K, Nagano J, Mizoue T, Moore MA, Mibu R, Tanaka M, Kakeji Y, Maehara Y, Okamura T, Ikejiri K, Futami K, Yasunami Y, Maekawa T, Takenaka K, Ichimiya H, Imaizumi N (2007) Meat, fish and fat intake in relation to subsite-specific risk of colorectal cancer: The Fukuoka Colorectal Cancer Study. Cancer Sci 98:590–597
Koushik A, Hunter DJ, Spiegelman D, Beeson WL, van den Brandt PA, Buring JE, Calle EE, Cho E, Fraser GE, Freudenheim JL, Fuchs CS, Giovannucci EL, Goldbohm RA, Harnack L, Jacobs DR Jr, Kato I, Krogh V, Larsson SC, Leitzmann MF, Marshall JR, McCullough ML, Miller AB, Pietinen P, Rohan TE, Schatzkin A, Sieri S, Virtanen MJ, Wolk A, Zeleniuch-Jacquotte A, Zhang SM, Smith-Warner SA (2007) Fruits, vegetables, and colon cancer risk in a pooled analysis of 14 cohort studies. J Natl Cancer Inst 99(19):1471–1483
Macfarlane GT, Steed H, Macfarlane S (2008) Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J Appl Microbiol 104:305–344
Ohta T, Semboku N, Kuchii A, Egashira Y, Sanada H (1997) Antioxidant activity of corn bran cell-wall fragments in the LDL oxidation system. J Agric Food Chem 45:1644–1648
Pierre F, Santarelli R, Taché S, Guéraud F, Corpet DE (2008) Beef meat promotion of dimethylhydrazine-induced colorectal carcinogenesis biomarkers is suppressed by dietary calcium. Br J Nutr 99:1000–1006
Plate AY, Gallaher DD (2006) Effects of indole-3-carbinol and phenethyl isothiocyanate on colon carcinogenesis induced by azoxymethane in rats. Carcinogenesis 27:287–292
Pretlow TP, Pretlow TG (2005) Mutant KRAS in aberrant crypt foci (ACF): initiation of colorectal cancer? Biochim Biophys Acta 1756:83–96
Reddy BS, Hamid R, Rao CV (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18:1371–1374
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
Swennen K, Courtin CM, Lindemans GCJE, Delcour JA (2006) Large scale production and characterisation of wheat bran arabinoxylooligosaccharides. J Sci Food Agric 86:1722–1731
Van Craeyveld V, Swennen K, Dornez E, Van de Wiele T, Marzorati M, Verstraete W, Delaedt Y, Onagbesan O, Decuypere E, Buyse J, De Ketelaere B, Broekaert WF, Delcour JA, Courtin CM (2008) Structurally different wheat-derived arabinoxylooligosaccharides have different prebiotic and fermentation properties in rats. J Nutr 138:2348–2355
Van Loo J (2004) Prebiotics promote good health. The basis, the potential, and the emerging evidence. J Clin Gastroenterol 38:S70–S75
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
Wijnands MV, Schoterman HC, Bruijntjes JB, Hollanders VM, Woutersen RA (2001) Effect of dietary galacto-oligosaccharides on azoxymethane-induced aberrant crypt foci and colorectal cancer in Fischer 344 rats. Carcinogenesis 22:127–132
Yamada H, Itoh K, Morishita Y, Taniguchi H (1993) Structure and properties of oligosaccharides from wheat bran. Cereal Food World 38:490–492
Younes H, Garleb K, Behr S, Rémésy C, Demigné C (1995) Fermentable fibers or oligosaccharides reduce urinary nitrogen excretion by increasing urea disposal in the rat cecum. J Nutr 125:1010–1016
Acknowledgments
Supported by Fondo Ateneo ex-60% of the University of Florence.
Conflict of interests statement
WFB, CMC, IEJAF, and JAD hold stock (options) of Fugeia NV. WFB and JAD are directors of Fugeia NV.
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Femia, A.P., Salvadori, M., Broekaert, W.F. et al. Arabinoxylan-oligosaccharides (AXOS) reduce preneoplastic lesions in the colon of rats treated with 1,2-dimethylhydrazine (DMH). Eur J Nutr 49, 127–132 (2010). https://doi.org/10.1007/s00394-009-0050-x
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DOI: https://doi.org/10.1007/s00394-009-0050-x