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Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats

Published online by Cambridge University Press:  09 March 2007

Brigitta Kleessen*
Affiliation:
German Institute of Human Nutrition (DIFE) Potsdam-Rehbrücke, D-14558 Bergholz-Rehbrücke, Germany
Ludger Hartmann
Affiliation:
German Institute of Human Nutrition (DIFE) Potsdam-Rehbrücke, D-14558 Bergholz-Rehbrücke, Germany
Michael Blaut
Affiliation:
German Institute of Human Nutrition (DIFE) Potsdam-Rehbrücke, D-14558 Bergholz-Rehbrücke, Germany
*
*Corresponding Author: Dr Brigitta Kleessen, fax +49 33200 88 444, email [email protected]
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Abstract

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The effects of fructans in the diet on the mucosal morphometry (height of villi, depth of the crypts, number of goblet cells), the thickness of the epithelial mucus layer and the histochemical composition of intestinal mucosubstances in the distal jejunum and the distal colon were investigated by comparing germ-free (GF) rats, rats harbouring Bacteroides vulgatus and Bifidobacterium longum (diassociated (DA) rats), and rats with a human faecal flora (HFA). The rats were fed either a commercial standard diet (ST) or ST + (50 g oligofructose (OF)–long-chain inulin (lcIN))/kg. Changes in total bacteria, bifidobacteria and BacteroidesPrevotella in response to feeding these diets were investigated by fluorescent in situ hybridization with 16S rRNA-targeted probes both in intestinal contents (lumen bacteria) and tissue sections (mucosa-associated bacteria). The OF–lcIN-containing diet resulted in higher villi and deeper crypts in bacteria-associated, but not in GF rats. In DA and HFA rats, the colonic epithelial mucus layer was thicker and the numbers of the goblet cells were greater than in GF rats. These effects were enhanced by the OF–lcIN-containing diet. In both dietary groups, bacterial colonization of GF rats caused an increase in neutral mucins in the distal jejunum and colon. Bacteria-associated rats had more acidic mucins in the colon than GF rats, and the OF–lcIN-containing diet stimulated sulfomucins as the predominant type of acidic mucins, while sialomucins dominated in the ST-fed groups. The number of mucosa-associated bifidobacteria detected in the colon of DA and HFA rats was greater with OF–lcIN than ST (4·9 and 5·4 v. 3·5 and 4·0 log10/mm2 mucosal surface respectively), whereas the number of luminal bifidobacteria was only affected by fructans in DA rats. Bacteroides did not differ between the groups. The stabilisation of the gut mucosal barrier, either by changes in the mucosal architecture itself, in released mucins or by stimulation of mucosal bifidobacteria with fructans, could become an important topic in the treatment and prophylaxis of gastrointestinal disorders and health maintenance.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Amann, RI, Ludwig, W & Schleifer, K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbial Reviews 59 143169.Google Scholar
Bernet, MF, Brassart, D, Neeser, J-R & Servin, AL (1993) Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen–cell interactions. Applied and Environmental Microbiology 59 41214128.CrossRefGoogle ScholarPubMed
Brockhausen, I, Schutzbach, J & Kuhns, W (1998) Glycoproteins and their relationship to human disease. Acta Anatomica (Basel) 161 3678.Google Scholar
Campbell, JM, Fahey, GC & Bryan, WW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. Journal of Nutrition 127 130136.Google Scholar
Corfield, AP, Myerscough, N, Gough, M, Brockhausen, I, Schauer, R & Paraskeva, C (1995) Glycosylation pattern of mucins in colonic disease. Biochemical Society Transactions 23 840845.Google Scholar
Deplancke, B & Gaskins, HR (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. American Journal of Clinical Nutrition 73, Suppl., 1131S1141S.Google Scholar
Djouzi, Z & Andrieux, C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. British Journal of Nutrition 78 313324.Google Scholar
Filipe, MI (1979) Mucins in the human gastrointestinal epithelium: a review. Investigative Cell Pathology 2 195216.Google ScholarPubMed
Fontaine, N, Meslin, JC, Lory, S & Andrieux, C (1996) Intestinal mucin distribution in the germ-free rat and in the heteroxenic rat harbouring a human bacterial flora: effect of inulin in the diet. British Journal of Nutrition 75 881892.Google Scholar
Forstner, JF (1978) Intestinal mucins in health and disease. Digestion 17 234263.Google Scholar
Gibson, GR, Beatty, EB, Wang, X & Cummings, JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108 975982.CrossRefGoogle ScholarPubMed
Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125 14011412.CrossRefGoogle ScholarPubMed
Gibson, GR & Wang, X (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. Journal of Applied Bacteriology 74 667674.Google Scholar
He, F, Ouwehand, AC, Hashimoto, H, Isolauri, E, Benno, Y & Salminen, S (2001) Adhesion of Bifidobacterium spp. to human intestinal mucus. Microbiology and Immunology 45 259262.CrossRefGoogle ScholarPubMed
Kleessen, B, Hartmann, L & Blaut, M (2001) Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. British Journal of Nutrition 86 291300.CrossRefGoogle ScholarPubMed
Kleessen, B, Kroesen, AJ, Buhr, HJ & Blaut, M (2002) Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls. Scandinavian Journal of Gastroenterology 37 10341041.Google Scholar
Kleessen, B, Noack, J & Blaut, M (1999) Distribution of viable and non-viable bacteria in the gastrointestinal tract of gnotobiotic and conventional rats. Microbial Ecology in Health and Disease 11 218225.CrossRefGoogle Scholar
Kleessen, B, Sykura, B, Zunft, H-J & Blaut, M (1997) Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. American Journal of Clinical Nutrition 65 13971402.Google Scholar
Korshunov, UM, Sinitsyna, NA, Gindoman, GA & Pinegin, BV (1985) Correction of intestinal microflora in chemotherapeutic dysbacteriosis using bifidobacterial and lactobacterial autologous strains. Journal of Microbiology, Epidemiology and Immunobiology 62, 2025 [in Russian].Google Scholar
Kruse, H-P, Kleessen, B & Blaut, M (1999) Effects of inulin on faecal bifidobacteria in human subjects. British Journal of Nutrition 82 375382.Google Scholar
Laboisse, C, Jarry, A, Branka, JE, Merlin, D, Bou-Hanna, C & Vallette, G (1996) Recent aspects of the regulation of intestinal mucus secretion. Proceedings of the Nutrition Society 55 259264.Google Scholar
Langendijk, PS, Schut, F, Jansen, GJ, Raangs, GC, Kamphuis, GR, Wilkinson, MHF & Welling, GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Applied and Environmental Microbiology 61 30693075.Google Scholar
Macfarlane, S, Cummings, JH & Macfarlane, GT (2000) Bacterial populations on the rectal mucosa in healthy and colitic subjects. Gastroenterology 118, Suppl. 2, A101 (Abstr 678).CrossRefGoogle Scholar
Manz, W, Amann, R, Ludwig, W, Vancanneyt, M & Schleifer, K-H (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142 10971106.CrossRefGoogle ScholarPubMed
Matsuo, K, Ota, H, Akamatsu, T, Sugiyama, A & Katsuyama, T (1997) Histochemistry of the surface mucous gel layer of the human colon. Gut 40 782789.Google Scholar
Meslin, JC, Andrieux, C, Sakata, T, Beaumatin, P, Bensaada, M, Popot, F, Szylit, O & Durand, M (1993) Effects of galacto-oligosaccharide and bacterial status on mucin distribution in mucosa and on large intestine fermentation in rats. British Journal of Nutrition 69 903912.Google Scholar
Meslin, JC, Fontaine, N & Andrieux, C (1999) Variations of mucin distribution in the rat intestine, caecum and colon: effect of the bacterial flora. Comparative Biochemistry and Physiology A 123 235239.CrossRefGoogle ScholarPubMed
Poxton, IR, Brown, R, Sawyer, A & Ferguson, A (1997) Mucosa-associated bacterial flora of the human colon. Journal of Medical Microbiology 46 8591.CrossRefGoogle ScholarPubMed
Prosky, L, Asp, N-G, Schweizer, TF, De Vries, J & Furda, I (1988) Determination of insoluble, soluble, and total dietary fiber in foods and food products: interlaboratory study. Journal of the Association of Analytical Chemists 71 10171023.Google Scholar
Rhodes, JM (1997) Mucins and inflammatory bowel disease. Quarterly Journal of Medicine 90 7982.Google Scholar
Roberfroid, MB, Van Loo, JA & Gibson, GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. Journal of Nutrition 128 1119.CrossRefGoogle ScholarPubMed
Romeis, R (1989) Polysaccharide and mucous substances. In Microscopic Technique, pp. 439444 [Böck, P, editor]. Munich, Vienna, Baltimore: Urban & Schwarzenberg.Google 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 on fermentable fibre, gut microbes and luminal trophic factors. British Journal of Nutrition 58 95103.CrossRefGoogle ScholarPubMed
Satchithanandam, S, Vargofcak-Apker, M, Calvert, RJ, Leeds, AR & Cassidy, MM (1990) Alteration of gastrointestinal mucin by fiber feeding in rats. Journal of Nutrition 120 11791184.CrossRefGoogle ScholarPubMed
Sekine, K, Toida, T, Saito, M, Kuboyama, M & Kawashima, T (1985) A new morphologically characterized cell wall preparation (whole peptidoglucan) from Bifidobacterium infantis with a higher efficacy on the regression of an established tumor in mice. Cancer Research 45 13001307.Google Scholar
Schmidt-Wittig, U, Enss, M-L, Coenen, M, Gärtner, K & Hedrich, HJ (1996) Response of rat colonic mucosa to a high fiber diet. Annals of Nutrition and Metabolism 40 343350.Google Scholar
Sghir, A, Chow, JM & Mackie, RI (1998) Continuous culture selection of bifidobacteria and lactobacilli from human faecal samples using fructooligosaccharide as selective substrate. Journal of Applied Microbiology 85 769777.Google Scholar
Sharma, R & Schumacher, U (1995) Morphometric analysis of intestinal mucins under different dietary conditions and gut flora in rats. Digestive Diseases and Sciences 40 25322539.CrossRefGoogle ScholarPubMed
Sharma, R, Schumacher, U, Ronaasen, V & Coates, M (1995) Rat intestinal mucosal responses to a microbial flora and different diets. Gut 36 209214.CrossRefGoogle ScholarPubMed
Tappenden, KA, Drozdowski, LA, Thomson, ABR & McBurney, MI (1998) Short-chain fatty acid-supplemented total parenteral nutrition alters intestinal structure, glucose transporter 2 (GLUT2) mRNA and protein, and proglucagon mRNA abundance in normal rats. American Journal of Clinical Nutrition 68 118125.Google Scholar
Van Loo, J, Coussement, P, De Leenheer, L, Hoebregs, H & Smits, G (1995) On the presence of inulin and oligofructose as natural ingredients in the Western diet. Critical Reviews in Food Science and Nutrition 35 525552.Google Scholar
Van Loo, J, Cummings, J, Delzenne, N, Englyst, H, Franck, A, Hopkins, M, Kok, N, Macfarlane, G, Newton, D, Quigley, M, Roberfroid, M, Van Vliet, T & Van den Heuvel, E (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). British Journal of Nutrition 81 121132.Google ScholarPubMed
Wang, X & Gibson, GR (1993) Effect of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. Journal of Applied Bacteriology 75 373380.CrossRefGoogle ScholarPubMed
Wilcoxon, F & Wilcox, RA (1964) Some Rapid Approximate Statistical Procedures. New York: Lederle Laboratories.Google Scholar
Zar, JH (1984) Biostatistical Analysis, 2nd ed., New York: Prentice-Hall.Google Scholar