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Arabinoxylan-oligosaccharides (AXOS) reduce preneoplastic lesions in the colon of rats treated with 1,2-dimethylhydrazine (DMH)

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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.

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References

  1. 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

    Google Scholar 

  2. Anonymous (2000) Approved methods of the American Association of Cereal Chemists, 10th edn. AACC, St. Paul, MN, USA

    Google Scholar 

  3. AOAC (1995) Official methods of analysis, 16th edition. Method 990.03. Association of Official Analytical Chemists, WA, USA

    Google Scholar 

  4. Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  Google Scholar 

  5. 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

    Article  CAS  Google Scholar 

  6. 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

    CAS  Google Scholar 

  7. 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

    CAS  Google Scholar 

  8. 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

    CAS  Google Scholar 

  9. 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

    CAS  Google Scholar 

  10. 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

    CAS  Google Scholar 

  11. 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 

  12. 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

    Article  CAS  Google Scholar 

  13. 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

    CAS  Google Scholar 

  14. 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

    Article  CAS  Google Scholar 

  15. 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

    Article  CAS  Google Scholar 

  16. European Community: European Community Regulations on the Care and Use of Laboratory Animals (1986) (Law 86/609/EC)

  17. 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

    Article  CAS  Google Scholar 

  18. 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

    Article  CAS  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412

    CAS  Google Scholar 

  22. 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

    Google Scholar 

  23. 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

    Article  CAS  Google Scholar 

  24. 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

    CAS  Google Scholar 

  25. Izydorczyk MS, Biliaderis CG (1995) Cereal arabinoxylans: in structure and physicochemical properties. Carbohydr Polym 28:33–48

    Article  CAS  Google Scholar 

  26. 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

    Article  CAS  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    CAS  Google Scholar 

  30. 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

    Article  CAS  Google Scholar 

  31. 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

    Article  CAS  Google Scholar 

  32. 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

    Article  CAS  Google Scholar 

  33. Pretlow TP, Pretlow TG (2005) Mutant KRAS in aberrant crypt foci (ACF): initiation of colorectal cancer? Biochim Biophys Acta 1756:83–96

    CAS  Google Scholar 

  34. Reddy BS, Hamid R, Rao CV (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18:1371–1374

    Article  CAS  Google Scholar 

  35. 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

    Article  CAS  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Van Loo J (2004) Prebiotics promote good health. The basis, the potential, and the emerging evidence. J Clin Gastroenterol 38:S70–S75

    Article  Google Scholar 

  39. 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

    CAS  Google Scholar 

  40. 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

    Article  CAS  Google Scholar 

  41. Yamada H, Itoh K, Morishita Y, Taniguchi H (1993) Structure and properties of oligosaccharides from wheat bran. Cereal Food World 38:490–492

    CAS  Google Scholar 

  42. 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

    CAS  Google Scholar 

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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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Correspondence to Giovanna Caderni.

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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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