Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T07:11:01.408Z Has data issue: false hasContentIssue false
  • English
  • Français

Enhancement of butyrate production in the rat caecocolonic tract by long-term ingestion of resistant potato starch

Published online by Cambridge University Press:  09 March 2007

Gwenaëlle Le Blay ,
Catherine Michel ,
Hervé M. Blottière  and
Christine Cherbut
Gwenaëlle Le Blay
Affiliation:
Human Nutrition Research Centre, INRA, BP 71627, 44316 Nantes Cedex 03, France
Catherine Michel
Affiliation:
Human Nutrition Research Centre, INRA, BP 71627, 44316 Nantes Cedex 03, France
Hervé M. Blottière
Affiliation:
Human Nutrition Research Centre, INRA, BP 71627, 44316 Nantes Cedex 03, France
Christine Cherbut*
Affiliation:
Human Nutrition Research Centre, INRA, BP 71627, 44316 Nantes Cedex 03, France
*
*Corresponding author: Dr Christine Cherbut, fax +33 2 40 67 50 12, email cherbut@nantes.inra.fr
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.

Some data suggest that the colonic microflora may adapt to produce more butyrate if given time and the proper substrate. To test this hypothesis, we investigated the effect of prolonged feeding of resistant potato starch on butyrate production. Rats were fed on either a low-fibre diet (basal) or the same diet supplemented with 90 g resistant potato starch/kg (PoS) for 0·5, 2 and 6 months. Short-chain fatty acid (SCFA) concentrations were determined in caecal and colonic contents at the end of each ingestion period. Total SCFA concentration increased over time throughout the caecocolonic tract with PoS, but was not modified with the basal diet. While propionate concentration was unchanged, butyrate concentration was highly increased by PoS at each time period in both the caecum and colon. Moreover, the butyrogenic effect of PoS increased over time, and the amount of butyrate was increased 6-fold in the caecum and proximal colon and 3-fold in the distal colon after 6 months compared with 0·5 months. Accordingly, the ratio butyrate: - total SCFA increased over time throughout the caecocolonic tract (12·6 (SE 2·8) v. 28 (SE 1·8) % in the caecum, 10·5 (SE 1·4) v. 26·8 (SE 0·9) % in the proximal colon, and 7·3 (SE 2·4) v. 23·9 (SE 2·7) % in the distal colon at 0·5 v. 6 months respectively), while the proportion of acetate decreased. Neither the proportion nor the concentration of butyrate was modified over time with the basal diet. Butyrate production was thus promoted by long-term ingestion of PoS, from the caecum towards the distal colon, which suggests that a slow adaptive process occurs within the digestive tract in response to a chronic load of indigestible carbohydrates.

Keywords

ButyrateColonic fermentationResistant starch
Type
Research Article
Information
British Journal of Nutrition , Volume 82 , Issue 5 , November 1999 , pp. 419 - 426
Copyright
Copyright © The Nutrition Society 1999

References

Argenzio, RA, Miller, N & von Englehardt, W (1975) Effect of volatile fatty acids on water and ion absorption from the goat colon. American Journal of Physiology 229, 997–1002.CrossRefGoogle ScholarPubMed
Bianchini, F, Caderni, G, Magno, C, Testeloni, G & Dolara, P (1992) Profile of short-chain fatty acids and rectal proliferation in rats fed sucrose or cornstarch diets. Journal of Nutrition 122, 254–261.CrossRefGoogle ScholarPubMed
Brunsgaard, G, Bach Knudsen, KE & Eggum, BO (1995) The influence of the period of adaptation on the digestibility of diets containing different types of indigestible polysaccharides in rats. British Journal of Nutrition 74, 833–848.Google ScholarPubMed
Champ, M, Noah, L, Loizeau, G & Kozlowski, F (1999) Analytical methods for resistant starch. In Complex Carbohydrate in Foods: Definition, Functionality, and Analysis [Cho, S, Prosky, L and Dreher, M, editors]. New York, NY: Marcel Dekker Co.Google Scholar
Cherbut, C (1995) Effects of short chain fatty acids on gastrointestinal motility. In Physiological and Clinical Aspects of Short Chain Fatty Acids, pp. 191–207 [Cummings, JHRombeau, JL and Sakata, T, editors]. Cambridge: Cambridge University Press.Google Scholar
Cherbut, C, Ferrier, L, Rozé, C, Anini, Y, Blottière, H, Lecannu, G & Galmiche, JP (1998) Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat American Journal of Physiology 275, G1415–G1422.Google ScholarPubMed
Cherbuy, C, Darcy-Vrillon, B, Morel, MT, Pegorier, JP & Duée, PH (1995) Effect of germfree state on the capacities of isolated rat colonocytes to metabolize n-butyrate, glucose, and glutamine Gastroenterology 109, 1890–1899.CrossRefGoogle ScholarPubMed
Cotta, MA (1988) Amylolytic activity of selected species of ruminal bacteria Applied Environmental Microbiology 54, 772–776.CrossRefGoogle ScholarPubMed
Darcy-Vrillon, B & Duée, PH (1995) Fibre effect on nutrient metabolism in splanchnic and peripheral tissues. In Dietary Fibre: Mechanisms of Action in Human Physiology and Metabolism, pp. 83–94 [Cherbut, CBarry, JLLairon, D and Durand, M editors]. Paris: John Libbey Eurotext.Google Scholar
El Oufir, L, Flourié, B, Bruley des Varannes, S, Barry, JL, Cloarec, D, Bornet, F & Galmiche, JP (1996) Relations between transit time, fermentation products, and hydrogen-consuming flora in healthy humans Gut 38, 870–877.Google ScholarPubMed
Englyst, HN, Hay, S & Macfarlane, GT (1987) Polysaccharide breakdown by mixed populations of human faecal bacteria FEMS Microbiology and Ecology 95, 163–171.Google Scholar
Faulks, RM, Southon, S & Livesey, G (1989) Utilization of alpha-amylase (EC 3.2.1.1)-resistant maize and pea (Pisum sativum) starch in the rat British Journal of Nutrition 61, 291–300.CrossRefGoogle ScholarPubMed
Hammer, J & Phillips, SF (1993) Fluid loading of the human colon: effects on segmental transit and stool composition Gastro-enterology 105, 988–998.CrossRefGoogle ScholarPubMed
Hyden, S (1955) A turbidimetric method for the determination of higher polyethylene glycols in biological materials Annals of the Royal Agricultural College of Sweden 22, 139–145.Google Scholar
Jouany, JP (1982) Dosage des acides gras volatils (AGV) et des alcools dans les contenus digestifs, les jus d'ensilage, les cultures bactériennes et les contenus des fermenteurs anaérobies (Determination of volatile fatty acids and alcohols in digestive contents, ensilage juices, bacterial cultures and anaerobic fermenter contents) Science des Aliments 2, 131–144.Google Scholar
Key, FB & Mathers, JC (1995) Digestive adaptations of rats given white bread and cooked haricot beans (Phasoleus vulgaris): large bowel fermentation and digestion of complex carbohydrates British Journal of Nutrition 74, 393–406.CrossRefGoogle Scholar
Kleessen, B, Stoof, G, Proll, J, Schmiedl, D, Noack, J & Blaut, M (1997) Feeding resistant starch affects fecal and cecal microflora and short-chain fatty acids in rats Journal of Animal Science 75, 2453–2462.CrossRefGoogle ScholarPubMed
Luick, B & Penner, MH (1991) Nominal response of passage rates to fiber particle size in rats Journal of Nutrition 121, 1940–1947.CrossRefGoogle ScholarPubMed
Macfarlane, GT & Cummings, JH (1991) The colonic flora, fermentation, and large bowel digestive function. In The Large Intestine: Physiology, Pathophysiology and Disease, pp. 51–92 [Phillips, SF, Pemberton, JH and Shorter, RG, editors]. New York, NY: Raven Press.Google Scholar
Macfarlane, GT & Englyst, HN (1986) Starch utilization by the human large intestinal microflora Journal of Applied Bacteriology 60, 195–201.CrossRefGoogle ScholarPubMed
Macfarlane, GT & Gibson, GR (1995) Microbiological aspects of the production of short-chain fatty acids in the large bowel. In Physiological and Clinical Aspects of Short-chain Fatty Acids, pp. 87–105 [Cummings, JHRombeau, JL and Sakata, T editors]. Cambridge: Cambridge University Press.Google Scholar
Macfarlane, GT & Gibson, GR (1997) Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In Gastrointestinal Microbiology: Gastrointestinal Ecosystems and Fermentations, vol. 1, pp. 269–318 [Mackie, RI and White, BA editors]. New York, NY: Chapman & Hall.CrossRefGoogle Scholar
Macfarlane, GT, Hay, S, Macfarlane, S & Gibson, GR (1990) Effect of different carbohydrates on growth, polysaccharidase and glycosidase production by Bacteroides ovatus, in batch and continuous culture Journal of Applied Bacteriology 68, 179–187.CrossRefGoogle ScholarPubMed
Macfarlane, GT & Macfarlane, S (1993) Factors affecting fermentation reactions in the large bowel Proceedings of the Nutrition Society 52, 367–373.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
Martin, LJM, Dumon, HJW & 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, 71–80.3.0.CO;2-H>CrossRefGoogle Scholar
Mathers, JC, Kennard, J & James, OFW (1993) Gastrointestinal responses to oat consumption in young adult and elderly rats: digestion, large bowel fermentation and crypt cell proliferation rates British Journal of Nutrition 70, 567–584.CrossRefGoogle Scholar
Mathers, JC, Smith, H & Carter, S (1997) Dose-response effects of raw potato starch on small-intestinal escape, large-bowel fermentation and gut transit time in the rat British Journal of Nutrition 78, 1015–1029.CrossRefGoogle Scholar
Maurin-Blanchet, H (1997) Le “G.I.R.C.O.R.”, Groupe Interprofessionnel de Réflexion et de Communication sur la Recherche Bulletin de l'Academie Véterinaire de France 70, 295–306.CrossRefGoogle Scholar
Mortensen, FV, Nielsen, H, Aalkjaer, C, Mulvany, MJ & Hessov, I (1994) Short chain fatty acids relax isolated resistant arteries from the human ileum by a mechanism dependent on anion exchange Pharmacology Toxicology 75, 181–185.CrossRefGoogle ScholarPubMed
Phillips, J, Muir, JG, Birkett, A, Lu, ZX, Jones, GP, O'Dea, K & Young, GP (1995) Effect of resistant starch on fecal bulk and fermentation-dependent events in humans American Journal of Clinical Nutrition 62, 121–130.Google Scholar
Reeves, AR, D'Ellia, JN, Frias, J & Salyers, AA (1996) A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch Journal of Bacteriology 178, 823–830.CrossRefGoogle ScholarPubMed
Reid, CA, Hillman, K, Henderson, C & Glass, H (1996) Fermentation of native and processed starches by the porcine caecal anaerobe Clostridium butyricum (NCIMB 7423) Journal of Applied Bacteriology 80, 191–198.CrossRefGoogle Scholar
Roediger, WEW (1995) The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier. In Physiological and Clinical Aspects of Short-chain Fatty Acids, pp. 337–351 [Cummings, JHRombeau, JL and Sakata, T editors]. Cambridge: Cambridge University Press.Google Scholar
Roediger, WEW & Moore, A (1981) The effect of short-chain fatty acids on sodium absorption in the isolated human colon perfused through the vascular bed Digestive Disease and Science 26, 100–106.CrossRefGoogle ScholarPubMed
Ropert, A, Cherbut, C, Roze, C, Le Qullec, A, Holst, JJ, Fu-Cheng, X, Bruley des Varannes, S & Galmiche, JP (1996) Colonic fermentation and proximal gastric tone in humans Gastroenterology 111, 289–296.CrossRefGoogle ScholarPubMed
Sakata, T (1987) Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: a possible explanation for trophic effects of fermentable fibre, gut microbes and luminal trophic factors British Journal of Nutrition 58, 95–103.CrossRefGoogle Scholar
Salvador, V, Cherbut, C, Barry, JL, Bertrand, D, Bonnet, C & Delort-Laval, J (1993) Sugar composition of dietary fibre and short-chain fatty acid production during in vitro fermentation by human bacteria British Journal of Nutrition 70, 189–197.CrossRefGoogle Scholar
Salyers, AA (1985) Breakdown of polysaccharides by human intestinal bacteria Journal of Environmental Pathology, Toxicology and Oncology 5, 211–231.Google ScholarPubMed
Salyers, AA (1995) Fermentation of polysaccharides by human colonic anaerobes. In Dietary Fibre: Mechanisms of Action in Human Physiology and Metabolism, pp. 29–35 [Cherbut, CBarry, JLLairon, D and Durand, M editors]. Paris: John Libbey Eurotext.Google Scholar
Salyers, AA & Leedle, JAZ (1983) Carbohydrate metabolism in the human colon. In The Human Intestinal Flora in Health and Disease, pp. 129–146 [Hendges, D editor]. New York, NY: Academic Press.CrossRefGoogle Scholar
Scheppach, W, Fabian, C, Sachs, M & Kasper, H (1988) The effect of starch malabsorption on fecal short-chain fatty acid excretion in man Scandinavian Journal of Gastroenterology 26, 755–759.Google Scholar
Siavoshian, S, Blottière, HM, Cherbut, C & Galmiche, JP (1997) Butyrate stimulates cyclin D and p21 and inhibits cyclin-dependent kinase 2 expression in HT-29 colonic epithelial cells Biochemical and Biophysical Research Communications 232, 169–172.CrossRefGoogle ScholarPubMed
Silvester, KR, Englyst, HN & Cummings, JH (1995) Ileal recovery of starch from whole diets containing resistant starch measured in vitro and fermentation of ileal effluent American Journal of Clinical Nutrition 62, 403–411.Google Scholar
Tappenden, KA, Thomson, ABR, Wild, GE & McBurney, MI (1997) Short-chain fatty acid-supplemented total parenteral nutrition enhances functional adaptation to intestinal resection in rats Gastroenterology 112, 792–802.CrossRefGoogle ScholarPubMed
Toscani, A, Soprano, DR & Soprano, KJ (1988) Molecular analysis of sodium butyrate-induced growth arrest Oncogenes Research 3, 223–238.Google ScholarPubMed
Tulung, BRémésy, C & Demigné, C (1987) Specific effects of guar gum or gum arabic on adaptation of cecal digestion to high fiber diets in the rat Journal of Nutrition 117, 1556–1561.CrossRefGoogle ScholarPubMed
Van Soest, PJ, Uden, P & Wrick, KF (1983) Critique and evaluation of markers for use in nutrition of humans and farm and laboratory animals Nutrition Reports International 27, 17–28.Google Scholar
Varel, VH, Robinson, IM & Jung, HJG (1987) Influence of dietary fiber on xylanolytic and cellulolytic bacteria of adult pigs Applied Environmental Microbiology 53, 22–26.CrossRefGoogle ScholarPubMed
Weaver, GA, Tangel, CT, Krause, JA, Alpern, HD, Jenkins, PL, Parfitt, MM & Stragand, JJ (1996) Dietary guar gum alters colonic microbiotal fermentation in azoxymethane-treated rats Journal of Nutrition 126, 1979–1991.Google Scholar
Whitehead, RH, Young, GP & Bhathal, PS (1986) Effects of short chain fatty acids on a new human colon carcinoma cell line (LIM1215) Gut 27, 1457–1463.Google ScholarPubMed
Wyatt, GM & Horn, N (1988) Fermentation of resistant food starches by human and rat intestinal bacteria Journal of the Science of Food and Agriculture 44, 281–288.CrossRefGoogle Scholar
Young, GP & Gibson, PR (1995) Butyrate and the human cancer cell. In Physiological and Clinical Aspects of Short Chain Fatty Acids, pp. 319–335 [Cummings, JHRombeau, JL and Sakata, T editors]. Cambridge: Cambridge University Press.Google Scholar