Glycemic Index of Local Foods and Diets: The Mediterranean Experience
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1 May 2003: (II)S56 S60 Glycemic Index of Local Foods and Diets: The Mediterranean Experience Gabriele Riccardi, M.D., Gennaro Clemente, M.D., and Rosalba Giacco, M.D. The Mediterranean diet is a healthful eating pattern associated with the prevention of coronary heart disease (CHD). Its main features are moderate intake of total fat (predominantly monounsaturated fat), low consumption of saturated fat and cholesterol-rich foods, and high intake of starch. Although this type of diet has bene cial effects on lipid metabolism, its high carbohydrate content might not be ideal for patients with diabetes or other conditions associated with insulin resistance (e.g., metabolic syndrome), who are known to be at particular risk of CHD. We therefore evaluated the glycemic response to starchy foods based on wheat (typical of the Italian diet) in patients with type 2 diabetes and identi ed certain characteristics of foods explaining their effects on postprandial glucose response. We found that spaghetti and potato dumplings, because of their low blood glucose response, represent a valid alternative to other starchy foods typical of the Mediterranean diet. Food structure plays an important role in determining the accessibility of starch to digestion, thus in uencing the postprandial blood glucose response, which modulates plasma insulin and lipid levels. Key words: glycemic index, ber, diabetes, Mediterranean diet 2003 International Life Sciences Institute doi: /nr.2003.may.S56 S60 Introduction The Mediterranean diet represents a healthful eating pattern associated with the prevention of coronary heart diseases (CHD), the major cause of premature death and disability in industrialized countries. 1 The main features of this dietary model are a moderate intake of total fat with liberal intake of monounsaturated fat and low intake of saturated fat and cholesterol and a high consumption of foods rich in starch. 2 Although this type of diet has bene cial effects on lipid metabolism, its high carbohydrate content might not be ideal for diabetic patients, who are known to be at particularly high risk for CHD. A diet high in carbohydrate can have detrimental effects on glycemic control in patients with diabetes, particularly people treated with insulin or people who have more severe forms of type 2 diabetes. 3 7 Moreover, this type of diet may exacerbate metabolic abnormalities associated with insulin resistance (i.e., metabolic syndrome) and increase the risk of diabetes in the general population. Not all carbohydrate-rich foods are equally hyperglycaemic; different postprandial blood glucose responses to isoglucidic amounts of various carbohydratecontaining foods have been observed in healthy subjects and people with diabetes. Carbohydrate-rich foods are therefore classi ed as foods with high or low glycemic index (GI) Few studies report the blood glucose response to carbohydrate-rich foods typically consumed in the Mediterranean area. This information could be relevant not only to plan diabetes diets but also to improve the metabolic pro le of individuals with metabolic syndrome and, possibly, to reduce the risk of type 2 diabetes in the general population. Current data published on the GI of foods do not take into account the traditional eating habits of the Mediterranean populations and can only be of marginal help in the selection of foods with bene cial effects on lipid metabolism and minimal hyperglycemic activity. 13 Our goal in this review is to determine the glycemic response to starchy foods based on wheat that are typically consumed in the Mediterranean area in patients with type 2 diabetes and the importance of some selected characteristics of foods explaining their lower postprandial blood glucose response. Dr. Riccardi is with the Department of Clinical and Experimental Medicine, Federico II University, Medical School, Naples, Italy. Drs. Clemente and Giacco are with the Institute of Food Science and Technology of National Research Council, Avellino, Italy. Glucose Response to Starch-rich Foods Typically Consumed in Mediterranean Regions In type 2 diabetics, we evaluated plasma glucose response to 50 g of available carbohydrate contained in S56 Nutrition Reviews, Vol. 61, No. 5
2 three starch-rich foods: 65 g of spaghetti, 90 g of white bread, or 285 g of potatoes; each was consumed in random order within a standard meal. 14 When spaghetti was replaced in the standard meal by an isoglucidic portion of bread, the glycemic response, evaluated for 5 hours after the meal, increased by as much as 68%; when spaghetti was replaced by potatoes, the glycemic response was 48% higher (Figure 1). These differences cannot be accounted for by variations in any of the food constituents known to in uence blood glucose metabolism because the amounts of total carbohydrate as well as of dietary ber were similar in the three test meals. Results of this study suggest that the use of the exchange system based merely on total carbohydrate content of foods is of limited value in the dietary treatment of patients with diabetes. Instead, knowledge of the glycemic index may aid the selection of food items more appropriate for the diabetic diet. The results of this study are particularly relevant because, unlike most other studies on this subject, the evaluation of the glycemic response of the different foods was performed within a composite meal, which is more applicable to everyday life. We also examined some characteristics of foods in relation to their effects on postprandial blood glucose response of other starch-rich foods typical of the Mediterranean diet. In type 2 diabetic patients we evaluated plasma glucose responses to 50 g available carbohydrate provided by 90 g of white bread and an equivalent amount of carbohydrate provided by three different starchy foods frequently consumed in Italy: 85 g pizza, 165 g potato dumplings (gnocchi), and 60 g hard toasted bread. These foods have similar nutrient composition but are prepared with different technologic processes. 15 Figure 1. Blood glucose rise above baseline after each of the three test meals: spaghetti ; white bread ; and potatoes ; *P 0.05, **P 0.025, ***P 0.01 versus spaghetti. Figure 2. Blood glucose rise above baseline after white bread ; hard toasted bread ; pizza ; and potato dumplings ; *P 0.05, **P 0.01 potato dumplings versus white bread. Pizza and hard toasted bread, which are prepared with leavened white wheat our, elicited a blood glucose response similar to that of white bread. The GI of the test foods, using the white bread scale, was 114% for pizza and 104% for hard toasted bread. By contrast, potato dumplings, a typical potato and wheat food often used as a substitute for pasta, reduced glycemia during the whole postprandial period (glycemic index 74% on bread scale or 52% on the glucose scale) (Figure 2). Pizza and hard toasted bread are subject to very different cooking processes; pizza is rapidly cooked at very high temperatures and consumed immediately after baking, whereas hard toasted bread undergoes two thermal treatments (i.e., one for baking bread and a second one for drying at less than 200 until the product is completely toasted and its structure becomes very hard and brittle). Our results suggest that these different cooking processes do not modify either starch digestibility or glycemic response and thus consumption of pizza or hard toasted bread instead of bread has no signi cant in uence on postprandial blood glucose concentrations. A similar conclusion has been reached using a more international type of pizza in type 1 diabetic patients. 16 An unexpected nding was that potato dumplings elicited a signi cantly reduced plasma glucose response compared with the other foods tested. Our observation of a GI of 74% is far lower than the value previously reported by us for freshly boiled potatoes of the same cultivar. 14 This nding suggests that the low rate of carbohydrate digestion observed for this food is due to the particular way it is prepared (i.e., potato dumplings are made with boiled potatoes mixed with wheat our in proportion of approximately 60:40 while they are still hot; dumplings are then boiled again for approximately 5 minutes in salted water and Nutrition Reviews, Vol. 61, No. 5 S57
3 consumed). To explain the different effects of the test foods on postprandial glucose metabolism, food characteristics (i.e., viscosity, resistant starch and ber content, and physical structure of food) able to reduce a-amylase accessibility and therefore to in uence blood glucose response were evaluated. In our study, neither viscosity nor variations in resistant starch, sugars, or dietary ber justi ed the reduced GI of potato dumplings. Scanning electron microscopy showed that potato dumplings had a compact structure similar to that observed in other low-gi starchy foods (Figure 3). This is consistent with a reduction of the rate of starch accessibility owing to a combination of compact form and need for protein digestion to free trapped starch granules. 17 By contrast, for leavened foods the high porosity caused by the entrapment of gas bubbles that expand during cooking greatly increases the surface exposed to enzyme activity. On the basis of this observation, one can hypothesize that unleavened types of breads, which are consumed in some Mediterranean regions (e.g., Sardinia, Israel, and Lebanon), might also have a lower GI than conventional types of bread consumed in most Western countries. This hypothesis deserves testing. Figure 3. Ultrastructure of boiled potato and potato dumplings by scanning electron microscopy (1 cm 40 mm). Potato dumplings show a more compact structure than boiled potato. Low Glycemic Response to Fiber-rich Foods: Mechanisms of Action All soluble ber rich foods have a low GI, in general less than 50% compared with starch-rich foods. It is believed that their low glycemic potential is due to their high viscosity, which prolongs nutrient digestion and absorption in the small intestine. 18 For this reason different types of viscous ber (e.g., guar, glucomannan, and pectin, etc.) have been added to starchy products (e.g., bread, crispbread, spaghetti, and crackers, etc.) and tested in diabetic patients Experimental and clinical data have recently identi- ed several mechanisms other than viscosity to explain the hypoglycemic activity of soluble ber: delayed gastric emptying, increased colonic fermentation, limited access of starch to digestive enzymes owing to the physical structure of the food To evaluate the role that each mechanism plays, at least in acute conditions, type 2 diabetic patients were randomly allocated to four test diets every other week; each diet was consumed for 24 hours. The diets differed only in their content of soluble ber: natural guar, which is viscous and causes intestinal fermentation; hydrolyzed guar, which causes intestinal fermentation but is not viscous; and natural soluble ber, which is viscous, causes intestinal fermentation, and entraps starch granules to make them less accessible to the action of digestive enzymes. Basically, the four diets consisted of a control diet with low soluble ber content (30 g of total ber), a control diet plus 10 g natural guar (total ber content 40 g), a control diet plus 10 g hydrolyzed guar (total ber content 40 g), and a natural ber rich diet (total ber content 43 g). Plasma glucose, insulin, free fatty acid (FFA), and triglyceride concentrations, gastric emptying by ultrasonographic method, intestinal fermentation by exhaled H 2 (breath test), and plasma acetate levels were evaluated at breakfast and lunch during each diet. The results of this study showed that the three high- ber diets, although similar in nutrient composition and containing the same amount of soluble ber, induced different postprandial plasma glucose responses in type 2 diabetic patients. In particular, whereas the diet based on natural ber rich foods reduced the glycemic response by 40% (P 0.02) compared with the control diet, the diet enriched with either guar or hydrolyzed guar had no signi cant effect. In addition, only the natural ber rich diet lowered postprandial plasma insulin by 30% (P 0.02) and FFA by 53% (P 0.04) and reduced postprandial plasma triglyceride concentrations by approximately 48% (P ) compared with the control diet (Figure 4). Both the natural ber rich diet and the guar diet had a greater consistency (higher viscosity) and a slower gastric emptying rate compared with the control diet, but S58 Nutrition Reviews, Vol. 61, No. 5
4 Figure 4. Metabolic effects of a high soluble ber diets in relation to the most important mechanisms of action evaluated. FFA free fatty acids, TG triglycerides. only the natural ber rich diet increased plasma acetate concentrations ( 270%, P 0.04). In addition, in the natural ber rich diet, starch accessibility was reduced as a consequence of the physical structure of the foods consumed (e.g., beans, vegetables, and apples). 26 Our study con rms that viscous ber in a meal slows gastric emptying rate but this effect is not always associated with changes in postprandial glycemia. In fact, both the guar-enriched diet and the diet made up of natural ber rich foods reduced the gastric emptying rate by 48% and 52%, respectively, compared with the control diet, but only the natural ber rich diet was effective in reducing postprandial plasma glucose concentrations. These observations therefore do not support gastric emptying rate as a major mechanism for the hypoglycemic activity of soluble ber. Because the diet composed of natural ber rich foods and the guar-rich diets contained similar amounts of soluble viscous ber, and meal consistency was roughly the same for both diets, it might be argued that viscosity is not, in physiologic conditions, the most important mechanism of the hypoglycemic activity of soluble ber. Colonic fermentation, owing to its production of hydrogen and short-chain fatty acids (e.g., acetate, propionate, and butyrate), has also been proposed to contribute to the hypoglycemic activity of dietary ber All four experimental diets increased both breath hydrogen and plasma acetate in the postprandial period. Whereas breath hydrogen was not signi cantly different, postprandial plasma acetate concentrations were approximately four times higher after the natural ber rich diet than after the control diet. This supports the hypothesis that the hypoglycemic effect of the natural ber rich diet could at least be partly mediated by the increased plasma acetate concentrations. 30 Compared with the guar and hydrolyzed guar diets, the diet with natural ber rich foods had a different physical structure, which might also play an important role in the hypoglycemic effect of ber. Different from ber-supplemented foods, the ber naturally contained in foods surrounds the carbohydrate granules to form a physical barrier that protects the carbohydrate from the action of digestive enzymes. The low carbohydrate accessibility induces a delay in both the digestive and absorptive processes associated with a low glycemic response. The importance of food structure in in uencing the postprandial metabolic response is further supported by studies that have evaluated the metabolic effect of a food consumed under different physical forms (e.g., whole, milled, or mashed), showing marked differences in the glycemic response. 26,31,32 In acute conditions, therefore, gastric emptying or viscosity does not in uence the hypoglycemic activity of ber within the context of a mixed meal, whereas it is modulated by acetate production in the colon by bacterial fermentation. Moreover, the physical structure of natural foods can also in uence the carbohydrate accessibility to digestive enzymes with subsequent major effects on the digestibility of foods. Conclusion Many carbohydrate-rich foods consumed in the Mediterranean diet have a low GI. Legumes, fruit, and vegetables are traditionally consumed at each meal in this region. Foods such as spaghetti or potato dumplings, although not particularly rich in ber, also have a low GI. A better understanding of the mechanisms able to lower the postprandial blood glucose response might help to create new carbohydrate-rich foods with a low GI. Traditional Mediterranean foods that have undergone appropriate food technology processes may be useful if in- Nutrition Reviews, Vol. 61, No. 5 S59
5 cluded in the diet. To achieve a substantial increase in the range of staple foods with a low GI, intercultural gastronomic exchanges should be promoted. 1. Keys A, Menotti A, Karvonen MJ, et al. The diet and 15 year death rate in Seven Countries Study. Am J Epidemiol. 1986;124: Giacco R, Riccardi G. Comparison of current eating habits in various Mediterranean countries. In: Spiller GA, ed. The Mediterranean Diets in Health and Disease New York: Van Nostrand Reinhold; 1991: Coulston AM, Hoolenbeck CB, Swislocki AML, Chen YD, Reaven GM. Deleterious metabolic effects of high carbohydrate, sucrose containing diets in patients with NIDDM. Am J Med. 1987;82: Garg A, Bonanome A, Grundy SM, Zhang ZJ, Ungher RH. Comparison of a high carbohydrate diet with a high monounsaturated fat diet in patients with non-insulin-dependent diabetes mellitus. N Engl J Med. 1988;319: Parillo M, Giacco R, Ciardullo AV, Rivellese AA, Riccardi G. Does a high carbohydrate diet have different effects in NIDDM patients treated with diet alone or hypoglycemic drugs? Diabetes Care. 1996; 19: Rivellese A, Giacco R, Genovese S, et al. Effects of changing amount of carbohydrate in diet on plasma lipoproteins and apolipoproteins in type II diabetic patients. Diabetes Care. 1990;13: Salmeron J, Ascherio A, Rimm EB, et al. Dietary ber, glycemic load, and risk of NIDDM in men. Diabetes Care. 1997;20: Jenkins DJ, Wolever TM, Taylor RH, et al Glycemic index of foods: a physiological basis for carbohydrates exchange. Am J Clin Nutr. 1981;34: Jenkins DJA, Wolever TMS, Taylor RH, Barker HM, Fielden H, Gassull MA. Lack of effect of re ning on the glycemic response to cereals. Diabetes Care. 1981;4: Jenkins DJ, Wolever TM, Jenkins AL, et al. The glycaemic index of food tested in diabetic patients: a new basis for carbohydrate exchange favouring the uses of legumes. Diabetologia. 1983;24: Foster-Powell K, Brand J. International tables of glycemic index. Am J Clin Nutr. 1995;62:871s 893s. 12. Wolever TM, Jenkins DJ, Vuksan V, Josse RG, Wong GS, Jenkins AL. Glycemic index of foods in individual subjects. Diabetes Care. 1990;13: Foster-Powell K, Holt SH, Brand-Miller JC. International table of glycemic index and glycemic load values: Am J Clin Nutr. 2002;76: Parillo M, Giacco R, Riccardi G, Pacioni D, Rivellese A. Different glycaemic responses to pasta, bread, and potatoes in diabetic patients. Diabet Med. 1985;2: Giacco R, Brighenti F, Parillo M, et al. Characteristics of some wheat-based foods of the Italian diet in relation to their in uence on postprandial glucose metabolism in type 2 diabetic patients. Br J Nutr. 2001;85: Ahern JA, Gatcomb PM, Held NA, Petit WA Jr, Tamborlane WW. Exaggerated hyperglycemia after a pizza meal in well-controlled diabetes. Diabetes Care. 1993;16: Monge L, Cortassa G, Mussino G, Carta Q. Glycoinsulinaemic response, digestion and intestinal absorption of the starch contained in two types of spaghetti. Diabetes Nutr Metab. 1990;3: Wursch P, Pi-Sunyer FX. The role of viscous soluble ber in the metabolic control in diabetes. A review with special emphasis on cereals rich in beta-glucan. Diabetes Care. 1997;20: Jenkins DJ, Wolever TM, Nineham R, et al. Guar crispbread in the diabetic diet. Br J Med. 1978;2: Jenkins DJ, Wolever TM, Taylor RH, Barker HM, Fielden H, Jenkins AL. Effect of guar crispbread with cereal products and leguminous seeds on blood glucose concentrations of diabetics. BMJ. 1980;281: Gatti, E, CatenazzoG, Camisasca E, Torri A, Denegri E, Sirtori CR. Effects of guar enriched pasta in the treatment of diabetes and hyperlipidemia. Ann Nutr Metab. 1984;28: Giacco R, Brighenti F, Parillo M, et al. Are bene cial metabolic effects of bre enriched foods preserved when consumed within a composite meal? Diabetes Nutr Metab. 1998;11: Kong MFSC, MacDonald IA, Tattersall RB. Gastric emptying in diabetes. Diabet Med. 1996;13: Thorburn A, Muir J, Proietto J. Carbohydrate fermentation lowers hepatic glucose output in healthy subjects. Metabolism. 1993;42: Wursh P, Del Vedovo S, Koellreutter B. Cell structure and starch nature as key determinants of the digestion rate of starch in legume. Am J Clin Nutr. 1986;43: Golay A, Coulston AM, Hollenbeck CB, Kaiser LL, Wursch P, Reaven GM. Comparison of metabolic effects of white beans processed into different physical forms. Diabetes Care. 1986;9: Wolever TM, Brighenti F, Royall D, Jenkins DJ. Effect of rectal infusion of short chain fatty acids in humans subjects. Am J Gastroenterol. 1989;84: Todesco T, Rao AV, Bosello, Jenkins DJA. Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. Am J Clin Nutr. 1991;54: Wolever TMS, Chiasson JL. Acarbose raises serum butyrate in human subjects with impaired glucose tolerance. Br J Nutr. 2000;84: Brighenti F, Castellani G, Benini L, et al. Effect of neutralized and native vinegar on blood glucose and acetate response to a mixed meal in healthy subjects. Eur J Clin Nutr. 1995;49: Liljeberg H, Granfeldt Y, Bjorck I. Metabolic responses to starch in bread containing intact kernels versus milled our. Eur J Clin Nutr. 1992;46: O Dea K, Nestel R, Autonoff L. Physical factors in uencing postprandial glucose and insulin responses to starch. Am J Clin Nutr. 1980;33: S60 Nutrition Reviews, Vol. 61, No. 5
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