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Dietary carbohydrates and insulin action in humans

Published online by Cambridge University Press:  09 March 2007

Thomas M. S. Wolever
Thomas M. S. Wolever*
Affiliation:
Department of Nutritional Sciences, Faculty of Medicine, University of Toronto, Canada and Division of Endocrinology and Metabolism, and Clinical Nutrition and Risk Factor Modification Centre, St Michael's Hospital, Toronto, Canada
*
*Corresponding author: T. M. S. Wolever, fax +1 416 978 5882, email thomas.wolever@utoronto.ca
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Abstract

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The metabolic syndrome represents a vicious cycle whereby insulin resistance leads to compensatory hyperinsulinaemia, which maintains normal plasma glucose but may exacerbate insulin resistance. Excess insulin secretion may eventually reduce β-cell function due to amyloid deposition, leading to raised blood glucose and further deterioration of β-cell function and insulin sensitivity via glucose toxicity. Reducing postprandial glucose and insulin responses may be a way to interrupt this process, but there is disagreement about the dietary approach to achieve this. Glucose and insulin responses are determined primarily by the amount of carbohydrate consumed and its rate of absorption. Slowly absorbed, low glycaemic-index (GI) foods are associated with increased HDL cholesterol and reduced risk of type 2 diabetes. There is some evidence that low-GI foods improve insulin sensitivity in humans, although studies using established techniques (glucose clamp or frequently sampled intravenous glucose tolerance test) have not been done. Low carbohydrate diets have been suggested to be beneficial in the treatment of the metabolic syndrome because of reduced postprandial insulin. However, they may increase fasting glucose and impair oral glucose tolerance — effects which define carbohydrate intolerance. The effects of low carbohydrate diets on insulin sensitivity depend on what is used to replace the dietary carbohydrate, and the nature of the subjects studied. Dietary carbohydrates may affect insulin action, at least in part, via alterations in plasma free fatty acids. In normal subjects a high-carbohydrate/low-GI breakfast meal reduced free fatty acids by reducing the undershoot of plasma glucose, whereas low-carbohydrate breakfasts increased postprandial free fatty acids. It is unknown if these effects occur in insulin-resistant or diabetic subjects. Thus further work needs to be done before a firm conclusion can be drawn as to the optimal amount and type of dietary carbohydrate for the treatment of the metabolic syndrome.

Keywords

DietHumansCarbohydrateInsulin sensitivityInsulin secretionGlycaemic index
Type
Research Article
Information
British Journal of Nutrition , Volume 83 , Issue S1 , June 2000 , pp. S97 - S102
Copyright
Copyright © The Nutrition Society 2000

References

Beck-Nielsen, H, Pedersen, O & Lindskov, HO (1980) Impaired cellular insulin binding and insulin sensitivity induced by high-fructose feeding in normal subjects. American Journal of Clinical Nutrition 33, 273–278.CrossRefGoogle ScholarPubMed
Beebe, C (1999) Diets with a low glycemic index: not ready for practice yet! Nutrition Today 34, 82–86.CrossRefGoogle Scholar
Boden, G, Chen, X, Ruiz, J, White, JV & Rossetti, L (1994) Mechanisms of fatty acid-induced inhibition of glucose uptake. Journal of Clinical Investigation 93, 2438–2446.CrossRefGoogle ScholarPubMed
Borkman, M, Campbell, LV, Chisholm, DJ & Storlien, LH (1991) Comparison of the effects on insulin sensitivity of high carbohydrate and high fat diets in normal subjects. Journal of Clinical Endocrinology and Metabolism 72, 432–437.CrossRefGoogle ScholarPubMed
Brand-Miller, J & Foster-Powell, K (1999) Diets with a low glycemic index: from theory to practice. Nutrition Today 34, 64–72.CrossRefGoogle Scholar
Chen, M, Bergman, RN & Porte, D (1988) Insulin resistance and β-cell dysfunction in aging: the importance of dietary carbohydrate. Journal of Clinical Endocrinology and Metabolism 67, 951–957.CrossRefGoogle ScholarPubMed
Chiasson, JL, Josse, RG, Leiter, LA, Mihic, M, Nathan, DM, Palmason, C, Cohen, RM & Wolever, TMS (1996) The effect of acarbose on insulin sensitivity in subjects with impaired glucose tolerance. Diabetes Care 19, 1190–1193.CrossRefGoogle ScholarPubMed
Collier, GR, Greenberg, GR, Wolever, TMS & Jenkins, DJA (1988) The acute effect of fat on insulin secretion. Journal of Clinical Endocrinology and Metabolism 66, 323–326.CrossRefGoogle ScholarPubMed
Cutler, DL, Gray, CG, Park, SW, Hickman, MG, Bell, JM & Kolterman, OG (1995) Low-carbohydrate diet alters intracellular glucose metabolism but not overall glucose disposal in exercise-trained subjects. Metabolism 44, 1264–1270.CrossRefGoogle Scholar
Daly, ME, Vale, C, Walker, M, Alberti, KGMM & Mathers, JC (1997) Dietary carbohydrates and insulin sensitivity: a review of the evidence and clinical implications. American Journal of Clinical Nutrition 66, 1072–1085.CrossRefGoogle ScholarPubMed
Dengel, DR, Pratley, RE, Hagberg, JM, Rogus, EM & Goldberg, AP (1996) Distinct effects of aerobic exercise training and weight loss on glucose homeostasis in obese sedentary men. Journal of Applied Physiology 81, 318–325.CrossRefGoogle ScholarPubMed
Frayn, KN & Kingman, SM (1995) Dietary sugars and lipid metabolism in humans. American Journal of Clinical Nutrition 62, 250S-261S.CrossRefGoogle ScholarPubMed
Fraze, E, Donner, CC, Swislocki, ALM, Chiou, Y-AM, Chen, Y-DI & Reaven, GM (1985) Ambient plasma free fatty acid concentrations in noninsulin-dependent diabetes mellitus: evidence for insulin resistance. Journal of Clinical Endocrinology and Metabolism 61, 807–811.CrossRefGoogle ScholarPubMed
Frost, G, Keogh, B, Smith, D, Akinsanya, K & Leeds, A (1996) The effect of low-glycemic carbohydrates on insulin and glucose response in vivo and in vitro in patients with coronary heart disease. Metabolism 45, 669–672.CrossRefGoogle ScholarPubMed
Frost, G, Leeds, A, Trew, G, Margara, R & Dornhorst, A (1998) Insulin sensitivity in women at risk of coronary heart disease and the effect of a low glycemic diet. Metabolism 47, 1245–1251.CrossRefGoogle ScholarPubMed
Frost, G, Leeds, AA, Doré, CJ, Madeiros, S, Brading, S & Dornhorst, D (1999) Glycaemic index as a determinant of serum HDL-cholesterol concentration. Lancet 353, 1045–1048.CrossRefGoogle ScholarPubMed
Fukagawa, NK, Anderson, JW, Hageman, G, Young, VR & Minaker, KL (1990) High-carbohydrate, high-fiber diets increase peripheral insulin sensitivity in healthy young and old adults. American Journal of Clinical Nutrition 52, 524–528.CrossRefGoogle ScholarPubMed
Gannon, MC, Nuttall, FQ, Neil, BJ & Westphal, SA (1988) The insulin and glucose responses to meals of glucose plus various proteins in type II diabetic subjects. Metabolism 37, 1081–1088.CrossRefGoogle ScholarPubMed
Garg, A, Grundy, SM & Unger, RH (1992) Comparison of effects of high and low carbohydrate diets on plasma lipoproteins and insulin sensitivity in patients with mild NIDDM. Diabetes 41, 1278–1285.CrossRefGoogle ScholarPubMed
Goodpaster, BH, Kelley, DE, Wing, RR, Meier, A & Thaete, FL (1999) Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 48, 839–847.CrossRefGoogle ScholarPubMed
Hughes, VA, Fiatarone, MA, Fielding, RA, Ferrara, CM, Elahi, D & Evans, WJ (1995) Long-term effects of a high-carbohydrate diet and exercise on insulin action in older subjects with impaired glucose tolerance. American Journal of Clinical Nutrition 62, 426–433.CrossRefGoogle ScholarPubMed
Jenkins, DJA, Wolever, TMS, Vuksan, V, Brighenti, F, Cunnane, SC, Rao, AV, Jenkins, A, Buckley, G, Patten, R, Singer, W, Corey, P & Josse, RG (1989) ‘Nibbling versus gorging’: metabolic advantages of increased meal frequency. New England Journal of Medicine 321, 929–934.CrossRefGoogle ScholarPubMed
Kiens, B & Richter, EA (1996) Types of carbohydrate in an ordinary diet affect insulin action and muscle substrates in humans. American Journal of Clinical Nutrition 63, 47–53.CrossRefGoogle Scholar
Luscombe, ND, Noakes, M & Clifton, PM (1999) Diets high and low in glycemic index versus high monounsaturated fat diets: effects on glucose and lipid metabolism in NIDDM. European Journal of Clinical Nutrition 53, 473–478.CrossRefGoogle ScholarPubMed
Oppert, JM, Nadeau, A, Tremblay, A, Despres, JP, Theriault, G & Bouchard, C (1997) Negative energy balance with exercise in identical twins: plasma glucose and insulin responses. American Journal of Physiology 272, E248-E254.Google ScholarPubMed
Pan, XR, Li, GW, Hu, YH, Wang, JX, Yang, WY, An, ZX, Hu, ZX, Lin, J, Xiao, JZ, Cao, HB, Liu, PA, Jiang, XG, Jiang, YY, Wang, JP, Zheng, H, Zhang, H, Bennett, PH & Howard, BV (1997) Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance. The Da Qing IGT and Diabetes Study. Diabetes Care 20, 537–544.CrossRefGoogle Scholar
Paolisso, G, Tataranni, PA, Foley, JE, Bogardus, C, Howard, BV & Ravussin, E (1995) A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 38, 1213–1217.CrossRefGoogle ScholarPubMed
Parillo, M, Rivellese, AA, Ciardullo, AV, Capaldo, B, Giacco, A, Genovese, S & Riccardi, G (1992) A high-monounsaturated-fat/low-carbohydrate diet improves peripheral insulin sensitivity in non-insulin-dependent diabetic patients. Metabolism 41, 1373–1378.CrossRefGoogle ScholarPubMed
Porte, D (1991) Beta-cells in type II diabetes mellitus. Diabetes 40, 166–180.CrossRefGoogle ScholarPubMed
Purnell, JQ & Brunzell, JD (1997) The central role of dietary fat, not carbohydrate, in the insulin resistance syndrome. Current Opinion in Lipidology 8, 17–22.CrossRefGoogle Scholar
Randle, PJ, Hales, CN, Garland, PB & Newsholme, EA (1963) The glucose fatty-acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1, 785–789.CrossRefGoogle ScholarPubMed
Reaven, GM (1997) Do high carbohydrate diets prevent the development or attenuate the manifestations (or both) of syndrome X? A viewpoint strongly against. Current Opinion in Lipidology 8, 23–27.CrossRefGoogle ScholarPubMed
Rossetti, L, Giaccari, A, DeFronzo, RA (1990) Glucose toxicity. Diabetes Care 13, 610–630.CrossRefGoogle ScholarPubMed
Salmerón, J, Ascherio, A, Rimm, ER, Colditz, GA, Spiegelman, D, Jenkins, DJ, Stampfer, MJ, Wing, AL & Willett, WC (1997) Dietary fiber, glycemic load, and risk of NIDDM in men. Diabetes Care 20, 545–550.CrossRefGoogle ScholarPubMed
Salmerón, J, Manson, JE, Stampfer, MJ, Colditz, GA, Wing, AL & Willett, WC (1997) Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women. Journal of the American Medical Association 277, 472–477.CrossRefGoogle ScholarPubMed
Swanson, JE, Laine, DC, Thomas, W & Bantle, JP (1992) Metabolic effects of dietary fructose in healthy subjects. American Journal of Clinical Nutrition 55, 851–856.CrossRefGoogle ScholarPubMed
Swinburn, BA, Boyce, VL, Bergman, RN, Howard, BV & Bogardus, C (1991) Deterioration in carbohydrate metabolism and lipoprotein changes induced by modern, high fat diet in Pima Indians and Caucasians. Journal of Clinical Endocrinology and Metabolism 73, 156–165.CrossRefGoogle ScholarPubMed
Tasman-Jones, C (1993) Effect of dietary fiber and fiber-rich foods on structure of the upper gastrointestinal tract. In CRC Handbook of Dietary Fiber in Human Nutrition, 2nd edn, pp. 355–357 [Spiller, GA , editor]. Boca Raton, FL: CRC Press.Google Scholar
Thorburn, AW, Storlien, LH, Jenkins, AB, Khouri, S & Kraegen, EW (1989) Fructose-induced in vivo insulin resistance and elevated plasma triglyceride levels in rats. American Journal of Clinical Nutrition 49, 1155–1163.CrossRefGoogle Scholar
Welch, IM, Bruce, C, Hill, SE & Read, NW (1987) Duodenal and ileal lipid suppresses postprandial blood glucose and insulin responses in man: possible implications for the dietary management of diabetes mellitus. Clinical Science 72, 209–216.CrossRefGoogle ScholarPubMed
Wolever, TMS (1995) Short-chain fatty acids and carbohydrate metabolism. In Physiological and Clinical Aspects of Short-Chain Fatty Acids, pp. 483–493 [JH, Cummings, JL, Rombeau and T, Sakata, editors]. Cambridge, UK: Cambridge University Press.Google Scholar
Wolever, TMS & Brand, Miller J (1995) Sugars and blood glucose control. American Journal of Clinical Nutrition 62, 212S-227S.CrossRefGoogle ScholarPubMed
Wolever, TMS, Bentum-Williams, A & Jenkins, DJA (1995) Physiologic modulation of plasma FFA concentrations by diet: metabolic implications in non-diabetic subjects. Diabetes Care 18, 962–970.CrossRefGoogle Scholar
Wolever, TMS & Bolognesi, C (1996) Prediction of glucose and insulin responses of normal subjects after consuming mixed meals varying in energy, protein, fat, carbohydrate and glycemic index. Journal of Nutrition 126, 2807–2812.Google ScholarPubMed
Wolever, TMS & Chiasson, J-L (2000) Acarbose raises serum butyrate in humans with impaired glucose tolerance British Journal of Nutrition(in press).Google Scholar
Zhou, Y-P & Grill, VE (1994) Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. Journal of Clinical Investigation 93, 870–876.CrossRefGoogle ScholarPubMed