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Luminal Fermentation and Colonocyte Metabolism in a Rat Model of Enteral Nutrition

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Abstract

Large intestinal fermentation and nutrient metabolism in colonocytes were investigated in a rat model of enteral feeding. Male Wistar rats (240–280 g) were submitted to 7 or 14 days of treatment: intragastric feeding (elemental formula) versus oral feeding (isocaloric and isonitrogenous diet, containing 5% purified cellulose) in the control group. Fermentation products and bacterial populations were analyzed in cecal contents. Colonic cells were isolated and tested for their capacities to metabolize [1-14C] butyrate and [U-14C]glutamine. After 7 days of enteral nutrition, short-chain fatty acid concentrations represented 52% of those measured in the control group, but colonocyte metabolism remained unchanged. After 14 days of enteral nutrition, short-chain fatty acid concentrations were still decreasing, although bacterial counts remained unchanged. In parallel, ammonia and lactate concentrations were significantly increased. The capacities to utilize butyrate and glutamine in colonocytes were only slightly affected. However, there was a dramatic increase in the ratio of β-OH-butyrate to acetoacetate fluxes, suggesting a more reduced redox mitochondrial state associated with enteral feeding.

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References

  1. Lo CW, Walker WA: Changes in the gastrointestinal tract during enteral or parenteral feeding. Nutr Rev 47:193-198, 1989

    Google Scholar 

  2. Jackson WD, Grand RJ: The human intestinal response to enteral nutrients: a review. J Am Coll Nutr 10:500-509, 1991

    Google Scholar 

  3. Suchner U, Senftleben U, Eckart T, Scholz MR, Beck K, Murrh, Enzenbach R, Peter K: Enteral versus parenteral nutrition: effect on gastrointestinal function and metabolism. Nutrition 12:13-22, 1996

    Google Scholar 

  4. Bowling TE, Silk DBA: Hormonal responses to enteral feeding and the possible role of Peptide YY in the pathogenesis of enteral feeding related diarrhoea. Clin Nutr 15:307-310, 1996

    Google Scholar 

  5. Riachi G, Ducrotte P, Guedon C, Bouteloup C, Denis P, Colin R, Lerebours E: Duodenojejunal motility after oral and enteral nutrition in humans: a comparative study. J Parenter Enteral Nutr 20:150-155, 1996

    Google Scholar 

  6. O'Keefe SJD, Lee RB, Anderson FP, Gennings C, Abou-Assi S, Clore J, Heuman D, Chey W: Physiological effects of enteral and parenteral feeding on pancreaticobiliary secretion in humans. Am J Physiol Gastrointest Liver Physiol 284:27-36, 2003

    Google Scholar 

  7. Bowling TE, Silk DBA: Colonic responses to enteral tube feeding. Gut 42:147-151, 1998

    Google Scholar 

  8. McFarlane GT, Cummings JH: The colonic flora, fermentation, and large bowel digestive function. In The Large Intestine, Physiology, Pathophysiology, and Disease. SF Phillips, JH Pemberton, RG Shorter (eds). New York, Raven Press, 1991, pp 51-92

    Google Scholar 

  9. Scheppach W: Effect of short chain fatty acids on gut morphology and function. Gut Suppl 1:S35-S38, 1994

    Google Scholar 

  10. Mortensen PB, Clausen MR: Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol 31(suppl 216):132-148, 1996

    Google Scholar 

  11. Roediger WE: Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83:424-429, 1982

    Google Scholar 

  12. Ardawi MSM, Newsholme EA: Fuel utilization in colonocytes of the rat. Biochem J 231:713-719, 1985

    Google Scholar 

  13. Darcy-Vrillon B, Morel MT, Cherbuy C, Bernard F, Posho L, Blachier F, Meslin JC, Duée PH: Metabolic characteristics of pig colonocytes after adaptation to a high fiber diet. J Nutr 123:234-243, 1993

    Google Scholar 

  14. Colomb V, Darcy-Vrillon B, Jobert A, Guihot G, Morel MT, Corriol O, Ricour C, Duée PH: Parenteral nutrition modifies glucose and glutamine metabolism in rat isolated enterocytes. Gastroenterology 112:429-436, 1997

    Google Scholar 

  15. Bergmeyer HU: Methods of Enzymatic Analyses, 3rd ed, vols. 1–4. New York, Academic Press, 1974

    Google Scholar 

  16. Dropsy G, Boy J: Détermination de l'ammoniémie (méthode automatique par dialyse). Ann Biol Clin 19:313-317, 1961

    Google Scholar 

  17. Guérin-Danan C, Chabanet C, Pedone C, Popot F, Vaissade P, Boulez C, Szylit O, Andrieux C: Milk fermented with yogurt cultures and Lactobacillus casei compared with yogurt and gelled milk: influence on intestinal microflora in healthy infants. Am J Clin Nutr 67:111-117, 1998

    Google Scholar 

  18. Djouzi Z, Andrieux C: Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. Br J Nutr 78:313-324, 1997

    Google Scholar 

  19. Cherbuy C, Darcy-Vrillon B, Morel MT, Pégorier JP, Duée PH: Effect of germ-free state on the capacities of isolated rat colonocytes to metabolize n-butyrate, glucose, and glutamine. Gastroenterology 109:1890-1899, 1995

    Google Scholar 

  20. Williamson DH, Bates MW, Page MA, Krebs HA: Activities of enzymes involved in acetoacetate utilization in adult mammalian tissues. Biochem J 121:41-47, 1971

    Google Scholar 

  21. Ardawi MSM, Newsholme EA: Maximum activities of some enzymes of glycolysis, the tricarboxylic acid cycle and ketone body and glutamine utilization pathways in lymphocytes of the rat. Biochem J 208:743-748, 1982

    Google Scholar 

  22. Wyatt GM, Horn M, Gee JM, Johnson IT: Intestinal microflora and gastrointestinal adaptation in the rat in response to non-digestible dietary polysaccharides. Br J Nutr 60:197-207, 1988

    Google Scholar 

  23. Andrieux C, Gadelle D, Leprince C, Sacquet E: Effects of some poorly digestible carbohydrates on bile acid bacterial transformations in the rat. Br J Nutr 62:103-119, 1989

    Google Scholar 

  24. Le Blay G, Michel C, Blottière H, Cherbut C: 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, 1999

    Google Scholar 

  25. Gibson GR, Roberfroid MB: Dietary modulation of the human colonic microbiota introducing the concept of prebiotics. J Nutr 125:1401-1412, 1995

    Google Scholar 

  26. Salyers AA, Kuritza AP, McCarthy RE: Influence of dietary fiber on the intestinal environment. Proc Soc Exp Biol Med 180:415-421, 1985

    Google Scholar 

  27. Crowther JS, Drasar BS, Goddard P, Hill MJ, Johnson K: The effect of a chemically defined diet on the faecal flora and faecal steroid concentration. Gut 14:790-793, 1973

    Google Scholar 

  28. Bounous G, Devroede GJ: Effects of elemental diet on human fecal flora. Gastroenterology 66:210-214, 1974

    Google Scholar 

  29. Bornside GH, Cohn I, Jr: Stability of normal human fecal flora during a chemically defined, low residue liquid diet. Ann Surg 181:58-60, 1975

    Google Scholar 

  30. Ducluzeau R, Ladire M, Laplace JP: Evolution of caecal microbial flora after surgical isolation of the large intestine in the pig. Ann Inst Pasteur/Microbiol 137:123-128, 1986

    Google Scholar 

  31. Miller TL, Weaver GA, Wolin MJ: Methanogens and anaerobes in a colon segment isolated from the normal fecal stream. Appl Environ Microbiol 48:449-450, 1984

    Google Scholar 

  32. Firmansyah A, Penn D, Lebenthal E: Isolated colonocyte metabolism of glucose, glutamine, n-butyrate, and β-hydroxybutyrate in malnutrition. Gastroenterology 97:622-629, 1989

    Google Scholar 

  33. Williamson DH, Lund P, Krebs HA: The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem J 103:514-527, 1967

    Google Scholar 

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Babakissa, C., Colomb, V., Andrieux, C. et al. Luminal Fermentation and Colonocyte Metabolism in a Rat Model of Enteral Nutrition. Dig Dis Sci 48, 1339–1345 (2003). https://doi.org/10.1023/A:1024115411253

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