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Restoration of the integrity of rat caeco-colonic mucosa by resistant starch, but not by fructo-oligosaccharides, in dextran sulfate sodium-induced experimental colitis

Published online by Cambridge University Press:  07 June 2007

Noëlle M. Moreau ,
Lucile J. Martin ,
Claire S. Toquet ,
Christian L. Laboisse ,
Patrick G. Nguyen ,
Brigitte S. Siliart ,
Henri J. Dumon  and
Martine M. J. Champ
Noëlle M. Moreau
Affiliation:
Unité de Nutrition et d'Endocrinologie, Ecole Nationale Vétérinaire, Nantes, France Centre de Recherche en Nutrition Humaine, Nantes, France
Lucile J. Martin*
Affiliation:
Unité de Nutrition et d'Endocrinologie, Ecole Nationale Vétérinaire, Nantes, France Centre de Recherche en Nutrition Humaine, Nantes, France
Claire S. Toquet
Affiliation:
Centre de Recherche en Nutrition Humaine, Nantes, France INSERM U539, Faculté de Médecine, Nantes, France Service d'Anatomie Pathologique, CHU, Nantes, France
Christian L. Laboisse
Affiliation:
Centre de Recherche en Nutrition Humaine, Nantes, France INSERM U539, Faculté de Médecine, Nantes, France Service d'Anatomie Pathologique, CHU, Nantes, France
Patrick G. Nguyen
Affiliation:
Unité de Nutrition et d'Endocrinologie, Ecole Nationale Vétérinaire, Nantes, France Centre de Recherche en Nutrition Humaine, Nantes, France
Brigitte S. Siliart
Affiliation:
Unité de Nutrition et d'Endocrinologie, Ecole Nationale Vétérinaire, Nantes, France Centre de Recherche en Nutrition Humaine, Nantes, France
Henri J. Dumon
Affiliation:
Unité de Nutrition et d'Endocrinologie, Ecole Nationale Vétérinaire, Nantes, France Centre de Recherche en Nutrition Humaine, Nantes, France
Martine M. J. Champ
Affiliation:
Unité des Fonctions Digestives et Nutrition Humaine, Institut National de la Recherche Agronomique, Nantes, France Centre de Recherche en Nutrition Humaine, Nantes, France
*
*Corresponding author: Dr Lucile Martin, fax +33 2 40 68 77 46, email lucile.martin@vet-nantes.fr
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Abstract

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Butyrate is recognised as efficient in healing colonic inflammation, but cannot be used as a long-term treatment. Dietary fibre that produces a high-butyrate level when fermented represents a promising alternative. We hypothesised that different types of dietary fibre do not have the same efficiency of healing and that this could be correlated to their fermentation characteristics. We compared short-chain fructo-oligosaccharides (FOS) and type 3 resistant starch (RS) in a previously described dextran sulfate sodium (DSS)-induced colitis model. Seventy-two Sprague–Dawley rats received water (control rats) or DSS (50g DSS/l for 7d then 30g DSS/l for 7 (day 7) or 14 (day 14) d). The rats were fed a basal diet (BD), or a FOS or RS diet creating six groups: BD-control, BD-DSS, FOS-control, FOS-DSS, RS-control and RS-DSS. Caeco-colonic inflammatory injuries were assessed macroscopically and histologically. Short-chain fatty acids (SCFA) were quantified in caeco-colon, portal vein and abdominal aorta. At days 7 and 14, caecal and distal macroscopic and histological observations were improved in RS-DSS compared with BD-DSS and also with FOS-DSS rats. Caeco-colonic SCFA were reduced in FOS-DSS and RS-DSS groups compared with healthy controls. The amount of butyrate was higher in the caecum of the RS-DSS rats than in the BD-DSS and FOS-DSS rats, whereas distal butyrate was higher in FOS-DSS rats. Partially explained by higher luminal levels of SCFA, especially butyrate, the healing effect of RS confirms the involvement of some types of dietary fibre in inflammatory bowel disease. Moreover, the ineffectiveness of FOS underlines the importance of the type of dietary substrate.

Keywords

Fructo-oligosaccharideResistant starchDextran sulfate sodiumShort-chain fatty acidsButyrate
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 1 , July 2003 , pp. 75 - 85
Copyright
Copyright © The Nutrition Society 2003

References

Ahmad, MS, Krishnan, S, Ramakrishna, BS, Mathan, M, Pulimood, AB & Murthy, SN (2000) Butyrate and glucose metabolism by colonocytes in experimental colitis in mice. Gut 46, 493–499.CrossRefGoogle ScholarPubMed
Andoh, A, Bamba, T & Sasaki, M (1999) Physiological and anti-inflammatory roles of dietary fiber and butyrate in intestinal functions. J Parenter Enteral Nutr 23, S70–S73.CrossRefGoogle ScholarPubMed
Appleyard, CB & Wallace, JL (1995) Reactivation of hapten-induced colitis and its prevention by anti-inflammatory drugs. Am J Physiol 269, G119–G125.Google ScholarPubMed
Araki, Y, Andoh, A, Koyama, S, Fujiyama, Y, Kanauchi, O & Bamba, T (2000 a) Effects of germinated barley foodstuff on microflora and short-chain fatty acid production in dextran sulfate sodium-induced colitis in rats. Biosci Biotechnol Biochem 64, 1794–1800.CrossRefGoogle ScholarPubMed
Araki, Y, Fujiyama, Y, Andoh, A, Koyama, S, Kanauchi, O & Bamba, T (2000 b) The dietary combination of germinated barley foodstuff plus Clostridium butyricum suppresses the dextran sulfate sodium-induced experimental colitis in rats. Scand J Gastroenterol 35, 1060–1067.Google ScholarPubMed
Basson, MD & Sgambati, SA (1998) Effects of short-chain fatty acids on human rectosigmoid mucosal colonocyte brush-border enzymes. Metabolism 47, 133–134.CrossRefGoogle ScholarPubMed
Breuer, RI, Buto, SK & Christ, ML (1991) Rectal irrigation with short-chain fatty acids for distal ulcerative colitis. Preliminary report. Dig Dis Sci 36, 185–187.CrossRefGoogle ScholarPubMed
Brighenti, F (1997) Simple method for quantitative analysis in short chain fatty acids in serum by gas liquid chromatography. In Plant Polysaccharides in Human Nutrition: Structure, Function, Digestive Fate and Metabolic Effects. pp 114–119. [Guillon, F, Abraham, G, Amado, R. et al. , editors]. Nantes: J. Agro-Industrial Research.Google Scholar
Brown, I, Warhurst, M, Arcot, J, Playne, M, Illman, RJ & Topping, DL (1997) Fecal numbers of bifidobacteria are higher in pigs fed Bifidobacterium longum with a high amylose cornstarch than with a low amylose cornstarch. J Nutr 127, 1822–1827.CrossRefGoogle ScholarPubMed
Bustos-Fernandez, L, de Paolo, IL & Hamamura, S (1978) Does secretin influence rat colonic absorption and secretion?. Am J Gastroenterol 70, 265–269.Google ScholarPubMed
Butzner, JD, Parmar, R, Bell, CJ & Dalal, V (1996) Butyrate enema therapy stimulates mucosal repair in experimental colitis in the rat. Gut 38, 568–573.CrossRefGoogle ScholarPubMed
Chapman, MA (2001) The role of the colonic flora in maintaining a healthy large bowel mucosa. Ann R Coll Surg Engl 83, 75–80.Google ScholarPubMed
Chapman, MA, Grahn, MF, Boyle, MA, Hutton, M, Rogers, J & Williams, NS (1994) Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative colitis. Gut 35, 73–76.CrossRefGoogle ScholarPubMed
Cherbut, C, Michel, C & Lecannu, G (2003) The prebiotic characteristics of fructooligosaccharides are necessary for reduction of TNBS-induced colitis in rats. J Nutr 133, 21–27.CrossRefGoogle ScholarPubMed
Clausen, MR & Mortensen, PB (1994) Kinetic studies on the metabolism of short-chain fatty acids and glucose by isolated rat colonocytes. Gastroenterology 106, 423–432.CrossRefGoogle Scholar
Cresci, A, Orpianesi, C, Silvi, S, Mastrandrea, V & Dolara, P (1999) The effect of sucrose or starch-based diet on short-chain fatty acids and faecal microflora in rats. J Appl Microbiol 86, 245–250.CrossRefGoogle ScholarPubMed
Demigné, C & Rémésy, C (1982) Influence of unrefined potato starch on cecal fermentations and volatile fatty acid absorption in rats. J Nutr 112, 2227–2234.CrossRefGoogle ScholarPubMed
Den Hond, E, Hiele, M, Evenepoel, P, Peeters, M, Ghoos, Y & Rutgeerts, P (1998) In vivo butyrate metabolism and colonic permeability in extensive ulcerative colitis. Gastroenterology 115, 584–590.CrossRefGoogle ScholarPubMed
Djouzi, Z & Andrieux, C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. Br J Nutr 78, 313–324.CrossRefGoogle ScholarPubMed
Fernandez-Banares, F, Hinojosa, J & Sanchez-Lombrana, JL et al. (1999) Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative colitis. Spanish Group for the Study of Crohn's Disease and Ulcerative Colitis (GETECCU). Am J Gastroenterol 94, 427–433.CrossRefGoogle Scholar
Finnie, I, Dwarakanath, A, Taylor, B & Rhodes, J (1995) Colonic mucin synthesis is increased by sodium butyrate. Gut 36, 93–99.CrossRefGoogle ScholarPubMed
Firmansyah, A, Penn, D & Lebenthal, E (1989) Isolated colonocyte metabolism of glucose, glutamine, n-butyrate, and beta-hydroxybutyrate in malnutrition. Gastroenterology 97, 622–629.CrossRefGoogle ScholarPubMed
Fleming, SE, Fitch, MD, DeVries, S, Liu, ML & Kight, C (1991) Nutrient utilization by cells isolated from rat jejunum, cecum and colon. J Nutr 121, 869–878.CrossRefGoogle ScholarPubMed
Frankel, W, Lew, J & Su, B (1994) Butyrate increases colonocyte protein synthesis in ulcerative colitis. J Surg Res 57, 210–214.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
Jacobasch, G, Schmiedl, D, Kruschewski, M & Schmehl, K (1999) Dietary resistant starch and chronic inflammatory bowel diseases. Int J Colorectal Dis 14, 201–211.CrossRefGoogle ScholarPubMed
Kanauchi, O, Iwanaga, T & Andoh, A (2001) Dietary fiber fraction of germinated barley foodstuff attenuated mucosal damage and diarrhea, and accelerated the repair of the colonic mucosa in an experimental colitis. J Gastroenterol Hepatol 16, 160–168.CrossRefGoogle Scholar
Kanauchi, O, Iwanaga, T & Mitsuyama, K (1999) Butyrate from bacterial fermentation of germinated barley foodstuff preserves intestinal barrier function in experimental colitis in the rat model. J Gastroenterol Hepatol 14, 880–888.CrossRefGoogle ScholarPubMed
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. J Anim Sci 75, 2453–2462.CrossRefGoogle ScholarPubMed
Le Blay, G, Michel, C, Blottiere, HM & Cherbut, C (1999) Enhancement of butyrate production in the rat caecocolonic tract by long-term ingestion of resistant potato starch. Br J Nutr 82, 419–426.CrossRefGoogle ScholarPubMed
Le Blay, G, Michel, C, Blottiere, HM & Cherbut, C (1999) Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. J Nutr 129, 2231–2235.CrossRefGoogle Scholar
Liu, Q, Shimoyama, T, Suzuki, K, Umeda, T, Nakaji, S & Sugawara, K (2001) Effect of sodium butyrate on reactive oxygen species generation by human neutrophils. Scand J Gastroenterol 36, 744–750.CrossRefGoogle ScholarPubMed
Marx, SP, Winkler, S & Hartmeier, W (2000) Metabolization of beta-(2,6)-linked fructose-oligosaccharides by different bifidobacteria. FEMS Microbiol Lett 182, 163–169.Google ScholarPubMed
Moreau, N, Toquet, C & Laboisse, C (2002) Predominance of caecal injury in a new dextran sulfate sodium treatment in rats: histopathological and fermentative characteristics. Eur J Gastroenterol Hepatol 14, 535–542.CrossRefGoogle Scholar
Nancey, S, Bienvenu, J, Coffin, B, Andre, F, Descos, L & Flourie, B (2002) Butyrate strongly inhibits in vitro stimulated release of cytokines in blood. Dig Dis Sci 47, 921–928.CrossRefGoogle ScholarPubMed
Pierre, F, Perrin, P, Champ, M, Bornet, F, Meflah, K & Menanteau, J (1997) Short-chain fructo-oligosaccharides reduce the occurrence of colon tumors and develop gut-associated lymphoid tissue in Min mice. Cancer Res 57, 225–228.Google ScholarPubMed
Perrin, P, Pierre, F & Patry, Y (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
Pitcher, MC & Cummings, JH (1996) Hydrogen sulphide: a bacterial toxin in ulcerative colitis?. Gut 39, 1–4.CrossRefGoogle ScholarPubMed
Pitcher, MCL, Beatty, ER & Gibson, GR (1995) Incidence and activities of sulphate-reducing bacteria in patients with ulcerative colitis. Gut 36, A63Google Scholar
Roediger, WE (1980) Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21, 793–798.CrossRefGoogle ScholarPubMed
Roediger, WE (1980) The colonic epithelium in ulcerative colitis: an energy-deficiency disease?. Lancet 2, 712–715.CrossRefGoogle ScholarPubMed
Roediger, WE (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424–429.CrossRefGoogle ScholarPubMed
Roediger, WE (1993) The imprint of disease on short-chain fatty acid metabolism by colonocytes. In Short-chain Fatty Acids, Proceedings of the 73rd Falk Symposium, 1989, pp 195–205. [Binder, HJ, Cummings, J and Soergel, K, editors]. DorDrecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Roediger, WE (1995) The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired conocyte barrier. In Physiological and Clinical Aspects of Short-chain fatty acids. pp 337–351. [Cummings, J, Rombeau, J and Sakata, T, editors]. Cambridge, MA: Cambridge University Press.Google Scholar
Roediger, WE, Babidge, W & Millard, S (1996) Methionine derivatives diminish sulphide damage to colonocytes – implications for ulcerative colitis. Gut 39, 77–81.CrossRefGoogle ScholarPubMed
Roediger, WE, Duncan, A, Kapaniris, O & Millard, S (1993) Reducing sulfur compounds of the colon impair colonocyte nutrition: implications for ulcerative colitis. Gastroenterology 104, 802–809.CrossRefGoogle ScholarPubMed
Roediger, WE, Duncan, A, Kapaniris, O & Millard, S (1993) Sulphide impairment of substrate oxidation in rat colonocytes: a biochemical basis for ulcerative colitis?. Clin Sci (Lond) 85, 623–627.CrossRefGoogle ScholarPubMed
Roediger, WE, Moore, J & Babidge, W (1997) Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Dig Dis Sci 42, 1571–1579.CrossRefGoogle ScholarPubMed
Roediger, WE & Nance, S (1990) Selective reduction of fatty acid oxidation in colonocytes: correlation with ulcerative colitis. Lipids 25, 646–652.CrossRefGoogle ScholarPubMed
Sakamoto, J, Nakaji, S, Sugawara, K, Iwane, S & Munakata, A (1996) Comparison of resistant starch with cellulose diet on 1,2-dimethylhydrazine-induced colonic carcinogenesis in rats. Gastroenterology 110, 116–120.CrossRefGoogle Scholar
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. Br J Nutr 58, 95–103.CrossRefGoogle ScholarPubMed
Scheppach, W, Muller, JG & Boxberger, F (1997) Histological changes in the colonic mucosa following irrigation with short-chain fatty acids. Eur J Gastroenterol Hepatol 9, 163–168.CrossRefGoogle ScholarPubMed
Scheppach, W, Sommer, H & Kirchner, T (1992) Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103, 51–56.CrossRefGoogle ScholarPubMed
Segain, JP, Raingeard de la Bletiere, D & Bourreille, A (2000) Butyrate inhibits inflammatory responses through NFkB inhibition: implications for Crohn's disease. Gut 47, 397–403.CrossRefGoogle Scholar
Stein, J, Schroder, O, Milovic, V & Caspary, WF (1995) Mercaptopropionate inhibits butyrate uptake in isolated apical membrane vesicles of the rat distal colon. Gastroenterology 108, 673–679.CrossRefGoogle ScholarPubMed
Steinhart, AH, Brzezinski, A & Baker, JP (1994) Treatment of refractory ulcerative proctosigmoiditis with butyrate enemas. Am J Gastroenterol 89, 179–183.Google ScholarPubMed
Tappenden, KA & McBurney, MI (1998) Systemic short-chain fatty acids rapidly alter gastrointestinal structure function, and expression of early response genes. Dig Dis Sci 43, 1526–1536.CrossRefGoogle ScholarPubMed
Widdel, F (1988) Microbiology and ecology of sulfate- and sulfur-reducing bacteria. In Biology of Anaerobic Microorganisms. pp 469–585. [Zehnder, AJB, editor]. New York: John Wiley and Sons.Google Scholar