Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T13:41:20.491Z Has data issue: false hasContentIssue false

Fermentable carbohydrate modulates postprandial enteroglucagon and gastrin release in rats

Published online by Cambridge University Press:  09 March 2007

J. M. Gee
Affiliation:
Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA
W. Lee-Finglas
Affiliation:
Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA
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.

We studied the effects of a fermentable sugar-alcohol (lactitol) on the concentrations of enteroglucagon and gastrin in the blood of rats for 7·5 h after feeding. The control and treatment groups were fed on semi-purified diets containing either non-fermentable cellulose or lactitol respectively, at 100 g/kg. Compared with the cellulose-fed group, the animals fed with lactitol had higher levels of enteroglucagon (5−10 times higher than control; P < 0·05) and lower serum gastrin (70−80% of control; P< 0.·05) for several hours after the withdrawal of feed. In contrast, varying the level of dietary lipid (maize oil) over a range of 8−120 g/kg had no effect on the release of either peptide. These results suggest that poorly absorbed fermentable dietary carbohydrate stimulates postprandial plasma enteroglucagon and inhibits serum gastrin release in the rat. The mechanism is uncertain but an endocrine response by the colon to fermentation products seems probable.

Type
Fermentable carbohydrate and gut hormones
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

Andrews, P. C. & Ronner, P. (1985). Isolation and structures of glucagon and glucagon-like peptide from catfish pancreas. Journal of Biological Chemistry 260, 39103914.CrossRefGoogle ScholarPubMed
Baldissera, F. G. A. & Holst, J. J. (1984). Glucagon-related peptides in the human gastrointestinal mucosa. Diabetologia 26, 223228.CrossRefGoogle ScholarPubMed
Besterman, H. S., Mallinson, C. N., Modigliani, R., Christofides, N. D., Pera, A., Ponti, V., Sarson, D. L. & Bloom, S. R. (1983). The gut hormones in inflammatory bowel disease. Scandinavian Journal of Gastroenterology 18, 845852.CrossRefGoogle ScholarPubMed
Burley, V. J. & Blundell, J. E. (1990). Time course of the effects of dietary fibre on energy intake and satiety. In Dietary Fibre: Chemical and Biological Aspects, pp. 277281 [Southgate, D. A. T., Waldron, K.Johnson, I. T. and Fenwick, G. R. editors]. Cambridge: Royal Society of Chemistry.Google Scholar
Carles-Bonnet, C., Jarrousse, C., Niel, H., Martinez, J., Rolland, M. & Bataille, D. (1992). N-acetyl oxyntomodulin 30–37: pharmacokinetics and activity on gastric acid secretion. Naunyn-Schmiedebergs Archives of Pharmacology 345, 5765.CrossRefGoogle Scholar
Goodlad, R. A., Ratcliffe, B., Fordham, J. P., Ghatei, M. A., Domin, J., Bloom, S. R. & Wright, N. A. (1989). Plasma enteroglucagon, gastrin and peptide YY in conventional and germ-free rats re-fed with a fibre-free or fibre-supplemented diet. Quarterly Journal of Experimental Physiology 74, 437442.CrossRefGoogle ScholarPubMed
Grimble, G. K., Patil, D. H. & Silk, D. B. (1988). Assimilation of lactitol, and unabsorbed disaccharide in the normal human colon. Gut 29, 16661671.CrossRefGoogle ScholarPubMed
Heding, L. G. (1971). Radioimmunological determination of pancreatic and gut glucagon in plasma. Diabetologia 7, 1019.CrossRefGoogle ScholarPubMed
Holst, J. J. (1982). Evidence that enteroglucagon (II) is identical with the C-terminal sequence (residues 33–69) of glicentin. Biochemical Journal 87, 372378.Google Scholar
Holst, J. J. (1994). Glucagonlike peptide 1: a newly discovered gastrointestinal hormone. Gastroenterology 107, 18481855.CrossRefGoogle ScholarPubMed
Holst, J. J., Christiansen, J. & Kuhl, C. (1976). The enteroglucagon response to intrajejunal infusion of glucose, triglycerides and sodium chloride, and its relation to jejunal inhibition of gastric acid secretion in man. Scandinavian Journal of Gastroenterology 11, 297304.CrossRefGoogle ScholarPubMed
Inoue, K., Wiener, I., Fried, G. M., Lilja, P., Watson, L. C. & Thompson, J. C. (1982). Effect of colectomy on cholecystokinin and gastrin release. Annals of Surgery 196, 691694.CrossRefGoogle ScholarPubMed
Jacobs, L. R., Bloom, S. R. & Dowling, R. H. (1981). Response of plasma and tissue levels of enteroglucagon immunoreactivity to intestinal resection, lactation and hyperphagia. Life Sciences 29, 20032007.CrossRefGoogle ScholarPubMed
Johnson, I. T., Gee, J. M. & Brown, J. C. (1988). Plasma enteroglucagon and small bowel cytokinetics in rats fed soluble nonstarch polysaccharides. American Journal of Clinical Nutrition 47, 10041009.CrossRefGoogle ScholarPubMed
Kirkegaard, P., Moody, A. J., Holst, J. J., Loud, F. B., Olsen, P. Skov & Christiansen, J. (1982). Glicentin inhibits gastric acid secretion in the rat. Nature 297, 156157.CrossRefGoogle ScholarPubMed
Le Quellec, A., Kervran, A., Blache, P., Ciurana, A. J. & Bataille, D. (1992). Oxyntomodulin-like immunoreactivity: diurnal profile of a new potential enterogastrone. Journal of Clinical Endocrinology and Metabolism 74, 14051409.Google ScholarPubMed
Longo, W. E., Ballantyne, G. H., Savoca, P. E., Adrian, T. E., Bilchik, A. J. & Modlin, I. M. (1991). Short-chain fatty acid release of peptide YY in the isolated rabbit distal colon. Scandinavian Journal of Gastroenterology 2, 442448.CrossRefGoogle Scholar
Metzger, J., Chollet, C., Wermeille, M., Biollaz, J., Llull, J. B. & Lauterburg, B. H. (1988). Gastrointestinal absorption of lactitol and effect on blood lactate in healthy volunteers and patients with cirrhosis. European Journal of Clinical Pharmacology 35, 9799.CrossRefGoogle ScholarPubMed
Nilsson, O., Bilchik, A. J., Goldenring, J. R., Ballantyne, G. H., Adrian, T. E. & Modlin, I. M. (1991). Distribution and immunocytochemical colocalisation of peptide YY and enteroglucagon in endocrine cells of the rabbit colon. Endocrinology 129, 139148.CrossRefGoogle Scholar
Read, N. W., MacFarlane, A., Kinsman, R. I., Bates, T. E., Blackhall, N. W., Farrar, B. J., Moss, G., Morris, A. P., O'Neill, B., Welch, I., Lee, Y. & Bloom, S. R. (1984). Effect of infusion of nutrient solutions into the ileum on gastrointestinal transit and plasma levels of neurotensin and enteroglucagon. Gastroenterology 86,274280.CrossRefGoogle ScholarPubMed
Reilly, K. J., Frankel, W. L., Bain, A. M. & Rombeau, J. L. (1995). Colonic short chain fatty acids mediate jejunal growth by increasing gastrin. Gut 37, 8186.CrossRefGoogle ScholarPubMed
Roberge, J. N. & Brubaker, P. L. (1991). Secretion of proglucagon-derived peptides in response to intestinal luminal nutrients. Endocrinology 128, 31693174.CrossRefGoogle ScholarPubMed
Ryberg, B., Axelson, J., Hakanson, R., Sundler, F. & Mattson, H. (1990). Trophic effects of continuous infusion of (leu15)−gastrin−17 in the rat. Gastroenterology 98, 3338.CrossRefGoogle ScholarPubMed
Sasaki, I., Tuchiya, T., Naito, H., Funayama, Y., Toda, M., Suzuki, Y., Sato, T. & Ohneda, A. (1987). Effect of ileo-jejunal transposition on intestinal adaptation after total colectomy in dogs. Tohoku Journal of Experimental Medicine 151, 419428.CrossRefGoogle ScholarPubMed
Schjoldager, B., Mortensen, P. E., Myhre, J., Christiansen, J. & Holst, J. J. (1989). Oxyntomodulin from distal gut. Role in regulation of gastric and pancreatic functions. Digestive Diseases and Sciences 34, 14111419.CrossRefGoogle ScholarPubMed
Schwartz, S. E., Levine, R. A., Singh, A., Scheidecker, J. R. & Track, N. S. (1982). Sustained pectin ingestion delays gastric emptying. Gastroenterology 83, 812817.CrossRefGoogle ScholarPubMed
Singh, P., Rae-Venter, B., Townsend, C. M., Khalil, T. & Thompson, J. C. (1985). Gastrin receptors in normal and malignant gastrointestinal mucosa: age associated changes. American Journal of Physiology 249, G761G769.Google ScholarPubMed
Sircar, B.,Johnson, L. R. & Lichtenberger, L. M. (1980). Effect of chemically defined diets on antral and serum gastrin levels in rats. American Journal of Physiology 238, G376–G383.Google ScholarPubMed
Spiller, R. C., Trotman, I. F., Adrian, T. E., Bloom, S. R., Misiewicz, J. J. & Silk, D. B. A. (1988). Further characterisation of the ‘ileal brake’ reflex in man - effect of ileal infusion of partial digests of fat, protein, and starch on jejunal motility and release of neurotensin, enteroglucagon and peptide YY. Gut. 29, 10421051.CrossRefGoogle ScholarPubMed
Unger, R. H., Ohneda, A., Valverde, I., Eisentraut, A. M. & Exton, J. (1968). Characterization of the responses of circulating glucagon-like immunoreactivity to intraduodenal and intravenous administration of glucose. Journal of Clinical Investigation 41, 4865.CrossRefGoogle Scholar
van Velthuisen, J. A. (1979). Food additives derived from lactose: lactitol and lactitol palmitate. Journal of Agricultural and Food Chemistry 27, 680686.CrossRefGoogle Scholar
Wang, Z., Wang, R. M., Owji, A. A., Smith, D. M., Ghatei, M. A. & Bloom, S. R. (1995). Glucagon-like peptide-1 is a physiological incretin in rat. Journal of Clinical Investigation 95, 417421.CrossRefGoogle ScholarPubMed
Wong, K., Bearshall, K., Waters, C. M., Calam, J. & Poston, G. J. (1991). Postprandial hypergastrinaemia in patients with colorectal cancer. Gut 32, 13521354.CrossRefGoogle ScholarPubMed