Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T12:05:10.512Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of dietary propionate on hepatic glucose production, whole-body glucose utilization, carbohydrate and lipid metabolism in normal rats

Published online by Cambridge University Press:  09 March 2007

Josette Boillot ,
Catherine Alamowitch ,
Anne-Marie Berger ,
Jing Luo ,
Françoise Bruzzo ,
Francis R. J. Bornet  and
Gerard Slama
Josette Boillot
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
Catherine Alamowitch
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
Anne-Marie Berger
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
Jing Luo
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
Françoise Bruzzo
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
Francis R. J. Bornet
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
Gerard Slama
Affiliation:
Department of Diabetes, INSERM U 341 and Pierre & Marie Curie University, Hôtel-Dieu Hospital, I Place du Parvis de Notre Dame, 75004 Paris, France
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.

Increased intake of dietary fibres is associated with several beneficial effects on carbohydrate and lipid metabolism. The colonic fermentation of dietary fibres produces short-chain fatty acids (SCFA; acetate, propionate and butyrate). Some authors have suggested that SCFA could be partly responsible for the effects of dietary fibres. The purpose of the present study was to test the effects of one of the SCFA, propionate. The effects of moderate amounts of dietary propionate on insulin sensitivity and hepatic glucose production were studied in male Sprague-Dawley rats. Two groups of twenty-one adult rats were fed for 3 weeks on a diet containing 78 g propionate/kg (P) or 78 g/kg of a poorly fermentable cellulose (control group; C). Feed intake, body weight, fasting plasma glucose, insulin, free fatty acids, alanine, lactate, glycerol and β-hydroxybutyrate levels were measured weekly in anaesthetized rats. At the end of the feeding period basal hepatic glucose production (BHGP) was measured with a primed continuous infusion of [3−3H]glucose and the in vivo insulin sensitivity in rats was quantified by the euglycaemic-hyperinsulinaemic clamp technique (0.6 and 2 U/kg per h). At that time fasting plasma glucose measured in anaesthetized rats was significantly lower in group P than in group C: 7·7 (SE 0·2) v. 8.5 (SE 0·2) mmol/l respectively (P < 0·002); plasma insulin levels were not significantly different. Neither the BHGP (mg/min per kg; C 14·8 (SE 1·3), P 15·1 (SE 1·3); n 7, not significant) nor the basal metabolic clearance (ml/min per kg; 8·9 (SE 08) v. 9·9 (SE 1·1); not significant) were different between treatments. Hepatic glucose production and glucose utilization at the two insulin concentrations (approximately 500 and 1500 mU/l respectively, n 7) did not differ significantly between the two groups. These results show that dietary propionate chronically ingested by normal rats could decrease fasting glycaemia, but from our findings, no effect on hepatic glucose production and whole-body glucose utilization could be clearly demonstrated.

Keywords

Fatty acidsGlucoseInsulinLiverPropionate
Type
Hepatic metabolism in rats
Information
British Journal of Nutrition , Volume 73 , Issue 2 , February 1995 , pp. 241 - 251
Copyright
Copyright © The Nutrition Society 1995

References

Anderson, J. W. (1986) Dietary fiber and diabetes. In Dietary Fiber: Basic and Clinical Aspects, pp. 151–167 [Vahouny, G. V. and Kritchevsky, D., editors]. New York: Plenum Press.Google Scholar
Anderson, J. W. & Bridges, S. R. (1984) Short chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hmatocytes (41958). Proceedings of the Society for Experimental Biology and Medicine 177, 372–376.CrossRefGoogle Scholar
Anderson., J. W. & Chen., W. L. (1979) Plant fiber: carbohydrate and lipid metabolism. American Journal of clinical Nutrition 32, 346–363.Google Scholar
Bär, A. (1990) Factorial calculation model for the estimation of the physiological caloric value of polyols. In Caloric Evaluation of Carbohydrates, pp. 209–257 [Hosoya, N., editor]. Tokyo: Japan Association of Dietetics and Enriched Foods.Google Scholar
Blair, J. B., Cook, D. E. & Lardy, H. A. (1973) Interaction of propionate and lactate in the perfused rat liver. Journal of Biological Chemistry 248, 3608–3614.CrossRefGoogle ScholarPubMed
Bornet, F. (1987) Effets des fibres alimentaires sur la digestion et le métabolisme des glucides (Effects of dietary fibres on carbohydrate metabolism and digestion). In Les Fibres Alimentaires pp. 1–39 [Thibault, J. F. and Rouau, X., editors]. Paris: Apria.Google Scholar
Chan, T. M. & Freedland, R. A. (1972) The effect of propionate on the metabolism of pyruvate and lactate in the perfused rat liver. Biochemical Journal 127, 539–543.CrossRefGoogle Scholar
Chen, W. J. L. & Anderson, J. W. (1986) Hypocholesterolemic effects of soluble fibres. In Dietary Fiber: Basic and Clinical Aspects, pp. 275–286 [Vahouny, G. V. and Kritchwsky, D., editors]. New York: Plenum Press.CrossRefGoogle Scholar
Chen, W. L., Anderson, J. W. & Jennings, D. (1984) Propionate may mediate the hypocholesterolemic effects of certain soluble plant fibers in cholesterol-fed rats. Proceedings of the Society for Experimental Biology and Medicine 175, 215–218.CrossRefGoogle ScholarPubMed
Cummings, J. H. (1983) Fermentation in the human large intestine: evidence and implication for health. Lancet i, 161–166.Google Scholar
Cummings, J. H., Pomare, E. W., Branch, W. J., Naylor, C. P. E. & Macfarlane, G. T. (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 1221–1227.Google Scholar
Gutmann, I. & Wahlefeld, A. W. (1974) L(+)lactate determination with lactate dehydrogenase and NAD. In Methods of Enzymatic Analysis, pp. 1464–1468 [Berjpeyer, H. U., editor]. New York: Academic Press.Google Scholar
Jenkins, D. J. A., Wolever, T. M. S., Nineham, R., Sarson, D. L., Bloom, S. R., Ahern, J., Alberti, K. G. M. M. & Hockaday, T. D. (1980) Improved glucose tolerance four hours after taking guar with glucose. Diabetologia 19, 21–24.Google Scholar
Katz, J., Rostami, H. & Dunn, A. (1974) Evaluation of glucose turnover, body mass and recycling with reversible and irreversible tracers. Biochemical Journal, 142, 161–170.CrossRefGoogle ScholarPubMed
Keys, J. A., Van Soest, P. J. & Young, E. P. (1969) Comparative digestibility of forage cellulose and hemicellulose in ruminants and non ruminants. Journal of Animal Science 29, 11–15.CrossRefGoogle Scholar
Leturque, A., Bumol, A. F., Ferré, P. & Girard, J. (1984) Pregnancy induced insulin resistance in rat: impaired suppression of glucose production and impaired stimulation of glucose utilization. American Journal of Physiology 246, E25–31.Google Scholar
Leturque, A., Gilbert, M. & Girard, J. (1981) Glucose turnover during pregnancy in anaesthetized post-absorptive rats. Biochemical Journal, 196, 633–636.CrossRefGoogle ScholarPubMed
Livesey, G. & Elia, M. (1988) Estimation of energy expenditure, net carbohydrate utilization, and net fat oxidation and synthesis by indirect calorimetry: evaluation of errors with special reference to the detailed composition of fuels. American Journal of Clinical Nutrition 47, 608–628.CrossRefGoogle Scholar
McNeil, N. I., Cummings, J. H. & James, W. P. T. (1978) Short chain fatty acid absorption by the human large intestine. Gut, 19, 819–822.CrossRefGoogle ScholarPubMed
Nyman, M., Asp, N. G., Cummings, J. H. & Wiggens, H. (1986) Fermentation of dietary fibre in the intestinal tract: comparison between man and rat. British Journal of Nutrition 55, 487–496.Google Scholar
Oberholzer, V. G., Levin, B., Burgess, E. A. & Young, W. F. (1967) Methylmalonic aciduria. An inborn error of metabolism leading to chronic metabolic acidosis. Archives of Disease in Childhood 42, 492–504.CrossRefGoogle ScholarPubMed
Pénicaud, L., Kande, J., LeMagnen, J. & Girard, J. (1985) Insulin action during fasting and refeeding in rat determined by euglycaemic clamp. American Journal of Physiology 249, E514–518.Google Scholar
Randle, P. J., Garland, P. B., Hales, C. N. & Newsholme, E. A. (1963) The glucose-fatty acid cycle: Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet i, 785–789.CrossRefGoogle Scholar
Ruppin, H., Bar-Meir, S., Soergel, K. H., Wood, C. M. & Schmitt, M. G. (1980) Absorption of short chain fatty acids by the colon. Gastroenterology 78, 1500–1507.CrossRefGoogle ScholarPubMed
Skutches, C. L., Holroyde, C. P., Myers, R. N., Paul, P. & Reichard, G. A. (1979) Plasma acetate turnover and oxidation. Journal of Clinical Investigation 64, 708–713.Google Scholar
Somogyi, M. J: (1945) Determination of blood sugar. Journal of Biological Chemistry 160, 69–73.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, 420–430.Google Scholar
Todesco, T., Venketshwer Rao, A., Bosello, O. & Jenkins, D. J. A. (1991) Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. American Journal of Clinical Nutrition 54, 860–865.CrossRefGoogle ScholarPubMed
Venter, C. S. & Vorster, H. H. (1989) Possible metabolic consequences of fermentation in the colon for humans. Medical Hypotheses 29, 161–166.CrossRefGoogle ScholarPubMed
Venter, C. S., Vorster, H. H. & Cummings, J. H. (1990 a) Effects of dietary propionate on carbohydrate and lipid metabolism in healthy volunteers. American Journal of Gastroenterology 85, 549–553.Google ScholarPubMed
Venter, C. S., Vorster, H. H. & Van Der Nest, D. G. (1990 b) Comparison between physiological effects of konjac-glucomannan and propionate in baboons fed ‘western’ diets. Journal of Nutrition 120, 1046–1053.Google Scholar
Verdonk, C. A., rizza, R. A. & Gerich, J. E. (1981) Effects of plasma glucose concentration on glucose utilization and clearance in normal man. Diabetes 30, 535–537.Google Scholar
Vorster, H. H., Venter, C. S., Van Eeden, T. S., Silvis, N., Huisman, H. W., Van Ryssen, J. C. J. & Walker, A. R. P. (1988) Benefits from supplementation of the current recommended diabetic diet with gel fibre. International Clinical Nutrition Review 8, 140–146.Google Scholar
Wieland, O. (1974) Glycerol, UV method. In Methods of Enzymatic Analysis, pp. 1404–1408 [Bergmeyer, H. U., editor]. New York: Academic Press.Google Scholar
Wolever, T. M. S., Brighenti, F., Royall, D., Jenkins, A. L. & Jenkins, D. J. A. (1989) Effect of rectal infusion of short chain fatty acids in human subjects. American Journal of Gastroenterology 84, 1027–1033.Google Scholar
Williamson, D. H. (1974) L-Alanine determination with alanine dehydrogenase. In Methods of Enzymatic Analysis, pp. 1679–1682 [Bergmeyer, H. U., editor]. New York: Academic Press.CrossRefGoogle Scholar
Williamson, D. H. & Mellanby, J. (1974) D(-)(3)-Hydroxybutyrate. In Methods of Enzymatic Anafysis pp. 1836–1839 [Bergmeyer, H. U., editor]. New York: Academic Press.CrossRefGoogle Scholar