Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T09:20:23.082Z Has data issue: false hasContentIssue false

Potato and high-amylose maize starches are not equivalent producers of butyrate for the colonic mucosa

Published online by Cambridge University Press:  09 March 2007

Lucile J. M. Martin
Affiliation:
Ecole Nationale Vétérinaire, Laboratoire de Nutrition et Alimentation, CP 3013, 44087 Nantes Cedex 03, France Institut National de la Recherche Agronomique, Laboratoire Fonctions Digestives et Nutrition Humaine BP 71627, 44316 Nantes Cedex 03, France CRNH groupe métabolisme, Hôtel Dieu, Place A. Ricordeau, 44093 Nantes Cedex 01, France
Henri J. W. Dumon
Affiliation:
Ecole Nationale Vétérinaire, Laboratoire de Nutrition et Alimentation, CP 3013, 44087 Nantes Cedex 03, France CRNH groupe métabolisme, Hôtel Dieu, Place A. Ricordeau, 44093 Nantes Cedex 01, France
Gérard Lecannu
Affiliation:
Institut National de la Recherche Agronomique, Laboratoire Fonctions Digestives et Nutrition Humaine BP 71627, 44316 Nantes Cedex 03, France CRNH groupe métabolisme, Hôtel Dieu, Place A. Ricordeau, 44093 Nantes Cedex 01, France
Martine M. J. Champ*
Affiliation:
Institut National de la Recherche Agronomique, Laboratoire Fonctions Digestives et Nutrition Humaine BP 71627, 44316 Nantes Cedex 03, France CRNH groupe métabolisme, Hôtel Dieu, Place A. Ricordeau, 44093 Nantes Cedex 01, France
*
*Correspondong author:Dr Martine Champ, fax +33 2 4067 5012, email [email protected]
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.

Portal appearance of short-chain fatty acids (SCFA) produced from fermentation of three different resistant starch (RS) sources (raw potato starch, high-amylose maize starch and retrograded high-amylose maize starch) was investigated in pigs. The catheterization technique coupled with determination of portal blood flow was used to estimate SCFA uptake by the colonic mucosa. Our hypothesis was that these three RS were not equivalent butyrate providers for the colonic mucosa and that butyrate uptake would therefore be different after in vivo fermentation of each starch. The starches induced different patterns of appearance of SCFA in the portal blood; raw potato starch was the only RS source to show a significant appearance of butyrate in the portal blood. Thus, uptake of butyrate by the colonic mucosa apparently differed between starches. This finding suggests that butyrate uptake does not only depend on the flow of butyrate appearing in the lumen. Indeed, for unexplained reasons, utilization of butyrate by the colonic mucosa appeared to be less efficient when the butyrate was produced from fermentation of potato starch than when it was produced from fermentation of the other RS sources.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Annison, G and Topping, DL (1994) Nutritional role of resistant starch: chemical structurevs physiological function. Annual Review of Nutrition 14, 297320.CrossRefGoogle ScholarPubMed
Argenzio, RA (1982) Volatile fatty acid production and absorption from the large intestine of the pig. In Physiologie Digestive chez le Porc (Digestive Physiology of the Pig. Les Colloques de l'INRA no. 12, pp. 207215 [Laplace, JP, Corring, T and Rerat, A, editors]. Paris: INRA.Google Scholar
Argenzio, RA and Southworth, M (1975) Sites of organic acid production and absorption in the gastrointestinal tract of the pig. American Journal of Physiology 228, 454460.CrossRefGoogle ScholarPubMed
Asp, NG (1992) Resistant starch. European Journal of Clinical Nutrition 46 (Suppl. 2), 148.Google ScholarPubMed
Bach Knudsen, KE and EGudmand-Høyer (1991) Methodological aspects of in vivo methods for measuring starch digestibility: animal models In Methodological Aspects of Methods for the Measurement of Starch Digestibility. Report of a European Flair Concerted Action Workshop pp. 4057 [Gudmand-H?yer, E,editor]. Copenhagen: Gentofle University Hospital.Google Scholar
Bingham, SA (1990) Mechanisms and experimental and epidemiological evidence relating dietary fibre (non-starch polysaccharides) and starch to protection against large bowel cancer. Proceedings of the Nutrition Society 49, 153171.CrossRefGoogle ScholarPubMed
Brighenti, F, (1997) Simple method for quantitative analysis of short chain fatty acids in serum by gas–liquid chromatography In Plant Polysaccharides in Human Nutrition: Structure, Function, Digestive Fate and Metabolic Effects pp. 114119. [Guillon, F, Andersson, H, Asp, NG, Bach Knudsen, KE, Champ, M, Robertson, J and Van Loo, J, editors]. Nantes, France:INRA.Google Scholar
Brighenti, F, Casiraghi, MC and Baggio, C (1998) Resistant starch in the Italian diet. British Journal of Nutrition 80, 333341.Google ScholarPubMed
Caderni, G, Luceri, C, Lancioni, L and Dolara, P (1996) Dietary sucrose, glucose, fructose, and starches affect colonic functions in rats. Nutrition and Cancer 25, 179186.CrossRefGoogle ScholarPubMed
Calvert, RJ, Otsuka, M and Satchithanandam, S (1989) Consumption of raw potato starch alters intestinal function and colonic cell proliferation in the rat. Journal of Nutrition 119, 16101616.CrossRefGoogle ScholarPubMed
Conway, PL, GRGibson and GTMacfarlane (1995) Microbial ecology of the human large intestine.In Human Colonic Bacteria: Role in Nutrition, Physiology and Pathology, pp. 124 [Gibson, GR and Macfarlane, GT, editors]. Boca Raton, FL: CRC Press.Google Scholar
Cummings, JH and Englyst, HN (1987) Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 45, 12431255.CrossRefGoogle ScholarPubMed
Darcy-Vrillon, B, Cherbuy, C, Morel, MT, Durand, M and Duée, PH (1996) Short-chain fatty acid and glucose metabolism in isolated pig colonocytes: modulation by NH4+. Molecular and Cellular Biochemistry 156, 145151.CrossRefGoogle ScholarPubMed
Demigné, C and Reacute, ;meacute, ; syC, (1982) Influence of unrefined potato starch on cecal fermentations and volatile fatty acid absorption in rats. Journal of Nutrition 112, 22272234.CrossRefGoogle ScholarPubMed
Demigné, C,(1994) Short chain fatty acid and hepatic metabolism Short Chain Fatty Acids. Falk Symposium no. pp. 272282[Binder, HJ, Cummings, J and Soergel, KH,editors]. Dordrecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Ellis, PR, Roberts, FG, Low, AG and Morgan, LM (1995) The effect of high-molecular-weight guar gum on net apparent insulin and gastric inhibitory polypeptide production in the growing pig: relationship to rheological changes in jejunal digesta. British Journal of Nutrition 74, 539556.CrossRefGoogle ScholarPubMed
Giusi-Périer, A, Fiszlewicz, M and Rérat, A (1989) Influence of diet composition on intestinal volatile fatty acid and nutrient absorption in unanesthetized pigs. Journal of Animal Science 67, 386402.CrossRefGoogle ScholarPubMed
Hague, A, Singh, B and Paraskeva, C (1997) Butyrate acts as survival factor for colonic epithelial cells: further fuel for the in vivo versus in vitro debate. Gastroenterology 112, 10361040.CrossRefGoogle ScholarPubMed
Hylla, S, Gostner, A, Dusel, G, Bartram, H-P, Christl, SU, Kasper, H and Scheppach, W (1998) Effects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. American Journal of Clinical Nutrition 67, 136142.CrossRefGoogle Scholar
Kristiansen, E, Meyer, O and Thorup, I (1996) Refined carbohydrate enhancement of aberrant crypt foci (ACF) in rat colon induced by food-borne carcinogen 2-amino-3-methyl-imidazo[4,5-f]quinoline (IQ). Cancer Letters 105, 147151.CrossRefGoogle ScholarPubMed
Mallett, AK, Bearne, CA, Young, PJ, Rowland, IR and Berry, C (1988) Influence of starches of low digestibility on the rat caecal microflora. British Journal of Nutrition 60, 597604.CrossRefGoogle ScholarPubMed
Martin, LMJ, Dumon, HJW and Champ, MMJ (1998) Production of short chain fatty acids from resistant starch in a pig model. Journal of the Science of Food and Agriculture 77, 7180.3.0.CO;2-H>CrossRefGoogle Scholar
Mathers, JC and Dawson, LD (1991) Large bowel fermentation in rats eating processed potatoes. British Journal of Nutrition 66, 313329.CrossRefGoogle ScholarPubMed
Noah, L, Krempf, M, Lecannu, G, Maugère, P and Champ, M (2000) Bioavailability of starch and postprandial changes in splanchnic glucose metabolism in pigs. American Journal of Physiology 278, E181E188.Google ScholarPubMed
Perrin, P; 1996 Modulation of cancer cells phenotype in rats by butyrate: application to immunotherapy and prevention for colon cancerPhD Thesis, University of Nantes, France.Google Scholar
Perrin, P, Pierre, F, Patry, Y, Champ, M, Berreur, M, Pradal, G, Bornet, F, Méflah, K and Ménanteau, J (2000) Only fibers promoting a stable butyrate-producing colonic ecosystem decrease the rate of aberrant crypt foci in rats. Gut.(In the Press)Google Scholar
Rérat, AA (1996) Influence of the nature of carbohydrate intake on the absorption chronology of reducing sugars and volatile fatty acids in pigs. Reproduction Nutrition Développement 36, 319.CrossRefGoogle Scholar
Reacute;rat, AA, Fislewicz, M, Giusi, A and Vaugelade, P (1987) Influence of meal frequency on postprandial variations in the production and absorption of volatile fatty acids in the digestive tract of conscious pigs. Journal of Animal Science 64, 448456.Google Scholar
Rérat, AA, Giusi-Périer, A and Vaissade, P (1993) Absorption balances and kinetics of nutrients and bacterial metabolites in conscious pigs after intake of maltose or maltitol-rich diets. Journal of Animal Science 71, 24732488.CrossRefGoogle ScholarPubMed
Reacute;rat, AA, Vaugelade, P, & Villiers, PA (1980) A new method for measuring the absorption of nutrients in the pig: Critical examination. In Current Concepts of Digestion and Absorption in Pigs, pp. 177214 [AG, Low and Partridge, IG, editors]. Ayr, UK: NIRD-HRI.Google Scholar
Roediger, WEW,(1995) The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier Physiological and Clinical Aspects of Short Chain Fatty Acids pp. 337351[Cummings, JH, Rombeau, JL and Sakata, T, editors].Cambridge:Cambridge University Press.Google Scholar
Sakamoto, J, Nakaji, S, Sugawara, K, Iwane, S and Munakata, A (1996) Comparison of resistant starch with cellulose diet on 1,2-dimethylhydrazine-induced colonic carcinogenesis in rats. Gastroenterology 110, 116120.CrossRefGoogle Scholar
Southgate, DA (1998) How much and what classes of carbohydrate reach the colon. European Journal of Cancer Prevalence 7, S81S82.CrossRefGoogle ScholarPubMed
Stephen, AM (1991) Starch and dietary fiber: their physiological and epidemiological interrelationships. Canadian Journal of Physiology and Pharmacology 69, 116120.CrossRefGoogle ScholarPubMed
Thorup, I, Meyer, O and Kristiansen, E (1995) Effect of potato starch, cornstarch, and sucrose on aberrant crypt foci in rats exposed to azoxymethane. Anticancer Research 15, 21012106.Google ScholarPubMed
Topping, DL, Illman, RJ, Taylor, MN and McIntosh GH (1985) Effects of wheat bran and porridge oats on hepatic portal venous volatile fatty acids in the pig. Annals of Nutrition and Metabolism 29, 325331.CrossRefGoogle ScholarPubMed
Van der Meulen, J, Bakker, GCM, Bakker, JGM, de Visser, H, Jongbloed, AW and Everts, H (1997) Effect of resistant starch on net portal-drained viscera flux of glucose, volatile fatty acids, urea, and ammonia in growing pigs. Journal of Animal Science 75, 26972704.CrossRefGoogle ScholarPubMed
Yen, JT, Nienaber, JA, Hill, DA and Pond, WG (1991) Potential contribution of absorbed volatile fatty acids to whole-animal energy requirement in conscious swine. Journal of Animal Science 69, 20012012.CrossRefGoogle ScholarPubMed
Young, GP, McIntyre, A, Albert, V, Folino, M, Muir, JG and Gibson, PR (1996) Wheat bran suppresses potato starch–potentially colorectal tumorigenesis at the aberrant crypt stage in a rat model. Gastroenterology 110, 508514.CrossRefGoogle ScholarPubMed