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Evidence for altered control of glucose disposal after total colectomy

Published online by Cambridge University Press:  09 March 2007

M. Denise Robertson*
Affiliation:
Human Nutrition Research Centre, Department of Biological and Nutritional Sciences, University of Newcastle, Newcastle-upon-Tyne NE1 7RU, UK
Geoff Livesey
Affiliation:
Institute of Food Research, Colney Lane, Norwich NR4 7UA, UK
Shelagh M. Hampton
Affiliation:
School of Biological Science, University of Surrey, Guildford GU2 5XH, UK
John C. Mathers
Affiliation:
Human Nutrition Research Centre, Department of Biological and Nutritional Sciences, University of Newcastle, Newcastle-upon-Tyne NE1 7RU, UK
*
*Corresponding author: Dr M. Denise Robertson, present address Oxford Lipid Metabolism Group, Nuffield Dept Clinical Medicine, Radcliffe Infirmary, Oxford OX2 6HE, UK, fax +44 1865 224652, email denise.robertson@oxlip.ox.ac.uk
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Abstract

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Colonic fermentation of organic matter to short-chain fatty acids has been implicated in the improvement in insulin sensitivity achieved by feeding diets rich in complex carbohydrates. The present study assessed the potential role of the colon in determining postprandial glucose kinetics. Metabolic responses to a complex-carbohydrate test meal were determined in conjunction with a primed continuous infusion of D-[6,6-2H]glucose in a group of ileostomists and sex-matched controls. Glucose disposal (GD) was computed using non-steady-state kinetics on a single compartment model. Insulin sensitivity was derived using cumulative GD as the dependent variable, and time and the integrated insulin concentration as independent variables. The ileostomist group had a significantly higher postprandial plasma insulin concentration (P=0·034) compared with the control group, but no difference in the plasma glucose concentration. Total GD was similar in each group, although the insulin-dependent GD was substantially lower in the ileostomists (0·46 v. 0·13 mg glucose/min per pmol, P=0·015). The ileostomist group also showed a 50 % lower rate of glucose oxidation in the postprandial period (P=0·005), although the rate of non-oxidative GD was not significantly affected. The present study indicates that loss of the colon is associated with several characteristics of the insulin resistance syndrome, and favours a view that the colon has a role in the control of postprandial glucose.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Akanji, AO, Bruce, MA & Frayn, KN (1989) Effect of acetate infusion on energy expenditure and substrate oxidation rates in non-diabetic and diabetic subjects. European Journal of Clinical Nutrition 43, 107115.Google ScholarPubMed
Anderson, JW & Bridges, SR (1984) Short-chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hepatocytes. Proceedings of the Society for Experimental Biology and Medicine 177, 372376.CrossRefGoogle ScholarPubMed
Chambrier, C, Picard, S, Vidal, H, Cohen, R, Riou, JP & Beylot, M (1990) Interactions of glucagon and free fatty acids with insulin in control of glucose metabolism. Metabolism 39, 976984.CrossRefGoogle ScholarPubMed
Crouse, JR, Gerson, CD, DeCarli, LM & Lieber, CS (1968) Role of acetate in the reduction of plasma free fatty acids produced by ethanol in man. Journal of Lipid Research 9, 509512.CrossRefGoogle ScholarPubMed
Davidson, M (1979) The effect of ageing on carbohydrate metabolism: a review of the English literature and a practical approach to the diagnosis of diabetes mellitus. Metabolism 28, 688705.CrossRefGoogle Scholar
Department of Health (1994) Nutritional Aspects of Cardiovascular Disease. Report on Health and Social Subjects no. 46. London: HM Stationery Office.Google Scholar
Eissele, R, Goke, R, Willemer, S, Harthus, HP, Vermeer, H, Arnold, R & Goke, B (1992) Glucagon-like peptide-1 in cells in the gastrointestinal tract and pancreas of rat, pig and man. European Journal of Clinical Investigation 22, 283291.CrossRefGoogle Scholar
Englyst, HN & Cummings, JH (1988) An improved method for the measurement of dietary fibre as non-starch polysaccharides in plant foods. Journal of the Association of Official Analytical Chemists 71, 808814.Google ScholarPubMed
Hampton, SM; 1984 C-peptide of proinsulin: its diagnostic use and a possible physiological rolePhD Thesis. University of Surrey.Google Scholar
Hansen, CP, Andreasen, JJ & Holst, JJ (1997) The release of gastric inhibitory peptide, glucagon-like peptide 1 and insulin after oral glucose test in colectomized subjects. Scandinavian Journal of Gastroenterology 32, 473477.CrossRefGoogle Scholar
Heding, LG (1975) Radioimmunological determination of human C-peptide in serum. Diabetologia 11, 541548.CrossRefGoogle ScholarPubMed
Holland, B, Welch, AA, Urwin, ID, Buss, DH, Paul, AA & Southgate, DAT; (1991) McCance and Widdowson's The Composition of Foods. 5th ed. London: RSC/MAFF.Google Scholar
Jequier, E, Acheson, K & Schutz, Y (1987) Assessment of energy expenditure and fuel utilization in man. Annual Review of Nutrition 7, 187208.CrossRefGoogle ScholarPubMed
Laurent, C, Simoneau, C, Marks, L, Braschi, S, Champ, M, Charbonnel, B & Krempf, FM (1995) Effect of acetate and propionate on fasting hepatic glucose production in humans. European Journal of Clinical Nutrition 49, 484491.Google ScholarPubMed
Livesey, G, Faulks, R, Wilson, P, Brown, J, Roe, M, Newman, T, Taylor, K, Hampton, S & Greenwood, R (1997) Postprandial insulin sensitivity of glucose disposal measured with [6,62H]-D-glucose is markedly dependent on prior meal consumption. Proceedings of the Nutrition Society 56, 38A.Google Scholar
Livesey, G, Wilson, PDG, Dainty, JR, Brown, JC, Faulks, RM, Roe, MA, Newman, TA, Eagles, J, Mellon, FA & Greenwood, RH (1998) Simultaneous time-varying systematic appearance of oral and hepatic glucose in adults monitored with stable isotopes. American Journal of Physiology 275, E717E728.Google Scholar
Madsbad, S, Kehlet, H, Hilsted, J & Tronier, B (1983) Discrepancy between plasma C-peptide and insulin response to intravenous glucose. Diabetes 32, 436438.CrossRefGoogle ScholarPubMed
Matthews, DR, Hosker, JR, Rudenski, AS, Naylor, BA, Treacher, TF & Turner, RC (1985) Homeostasis model assessment: insulin resistance and B-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412419.CrossRefGoogle Scholar
Meyer, HU, Curchod, B, Maeder, F, Pachud, P, Jequier, E & Felber, JP (1980) Modifications of glucose storage and oxidation in non-obese diabetics, measured by continuous indirect calorimetry. Diabetes 29, 752756.CrossRefGoogle Scholar
Miyazaki, Y, Hirata, A, Murakami, H, Fukuoka, M, Agata, J, Higashiura, K, Masuda, A, Ura, N & Shimamoto, K (1998) Effects of aging on the insulin actions for the glucose metabolism and renal function in normotensives and essential hypertensives. American Journal of Hypertension 11, 10561064.CrossRefGoogle ScholarPubMed
Nauck, MA, Siemsgluss, J, Orskov, C & Holst, JJ (1996) Release of glucagon-like peptide 1(GLP-1[7-36 amide]), gastric inhibitory polypeptide (GIP) and insulin in response to oral glucose after upper and lower intestinal resections. Zeitschrift fur Gastroenterologie 34, 159166.Google ScholarPubMed
Printz, H, Reiter, S, Samedi, N, Ebrahimsade, S, Kirchner, R, Arnold, R & Goke, B (1998) GLP-1 release in man after large bowel resection or intrarectal glucose administration. Digestion 59, 689695.CrossRefGoogle ScholarPubMed
Randle, PJ, Garland, PB & Hales, CN (1963) The glucose-fatty acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet i, 785789.CrossRefGoogle Scholar
Reaven, GM (1988) Role of insulin resistance in human disease. Diabetes 37, 15951607.CrossRefGoogle ScholarPubMed
Reaven, G, Greensfield, M & Mondon, C (1982) Does insulin removal rate from the plasma decline with age?. Diabetes 31, 670673.CrossRefGoogle ScholarPubMed
Robertson, MD, Livesey, G, Morgan, LM, Hampton, SM & Mathers, JC (1999) The influence of the colon on postprandial glucagon-like peptide (7-36) amide concentration in man. Journal of Endocrinology 161, 2531.CrossRefGoogle ScholarPubMed
Robertson, MD & Mathers, JC (2000) Gastric emptying rate of solids is reduced in a group of ileostomists. Digestive Diseases and Sciences 45, 12871294.CrossRefGoogle Scholar
Steele, R (1959) Influence of glucose loading and of injected insulin on hepatic glucose output. Annals of the New York Academy of Sciences 82, 420430.CrossRefGoogle ScholarPubMed
Vaag, AA, Handberg, A, Skott, P, Richter, EA & Beck-Nielsen, H (1994) Glucose–fatty acid cycle operates in humans at the levels of both whole body and skeletal muscle during low and high physiological plasma insulin concentrations. European Journal of Endocrinology 130, 7079.CrossRefGoogle ScholarPubMed
Vaag, AA, Holst, JJ, Volund, A & Beck-Nielsen, H (1996) Gut incretin hormones in identical twins discordant for non-insulin dependent diabetes mellitus (NIDDM) – evidence for decreased glucagon-like peptide 1 secretion during oral glucose ingestion in NIDDM twins. European Journal of Clinical Endocrinology 135, 425432.CrossRefGoogle ScholarPubMed
Venter, CS, Vorster, HH & Cummings, JH (1990) Effect of dietary propionate on carbohydrate and lipid metabolism in healthy volunteers. American Journal of Gastroenterology 85, 549553.Google ScholarPubMed
Wieko, J & Sherman, WR (1976) Boroacetylation of carbohydrates. Correlations between structure and mass spectral behaviour in monoacetylhexose cyclic boronic esters. Journal of the American Chemical Society 98, 76317637.CrossRefGoogle Scholar
Wolever, TMS, Brighenti, F, Royall, D, Jenkins, AL & Jenkins, DJA (1989) Effect of rectal infusion of short chain fatty acids in human subjects. American Journal of Gastroenterology 84, 10271034.Google ScholarPubMed
Young, AM, Bogardus, C, Stone, K & Mott, DM (1988) Insulin response of components of whole body and muscle carbohydrate metabolism in humans. American Journal of Physiology 254, E231E236.Google ScholarPubMed