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The Journal of Nutrition Vol. 128 No. 1 January 1998,
pp. 35-43
Department of Diabetes, INSERM U341, University of Pierre et Marie Curie, Hôtel-Dieu Hospital, 75004 Paris, France and * Laboratory of Nutrition INRA, 44026 Nantes, France
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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The aim of this study was to evaluate the effects of the chronic consumption of two starches, characterized by different glycemic indices and amylose-amylopectin content, on glucose metabolism in rat epididymal adipocytes. The two chosen starches were from mung bean (32% amylose) and cornstarch (0.5% amylose). The 
-amylase digestibility was higher for the waxy cornstarch than that of the mung bean starch (60 ± 4 vs. 45 ± 3%, mean ± SEM, respectively). The glycemic index of the waxy cornstarch diet (575 g starch /kg diet) was higher than that of the mung bean starch diet (107 ± 7 vs. 67 ± 5%, P < 0.01) when measured in vivo in two groups of normal rats (n = 9). In a subsequent study, normal and diabetic (streptozotocin-injected on d 2 of life) male Sprague-Dawley rats (18 per group) consumed a diet containing 575 g starch/kg diet as either waxy cornstarch or mung bean starch. After 3 wk, food intake, epididymal fat pad weights, and plasma glucose, insulin and triglyceride concentrations did not differ between diet groups. Adipocyte diameter was smaller in rats that consumed mung bean starch compared with those that consumed the waxy cornstarch diet (P < 0.01). The mung bean diet increased maximal insulin-stimulated 14C-glucose oxidation (% of basal values, P < 0.05). In contrast, incorporation of 14C-glucose into total lipids was significantly lower in rats that consumed the mung bean diet (P < 0.05). We conclude that in both normal and diabetic rats, the chronic replacement of a high glycemic index starch by a low glycemic index one in a mixed diet increases insulin-stimulated glucose oxidation, decreases glucose incorporation into total lipids and decreases epididymal adipocyte diameter. Thus, the type of starch mixed into the diet has important metabolic consequences at the cellular level in both normal and diabetic rats.
Improving postprandial hyperglycemic peaks is one of the main therapeutic targets in diabetic patients. It might also be of importance in glucose-intolerant or even in normal subjects. During the last 10 years, many tables of the glycemic index of foods have been published. Starchy foods represent the main candidate for reducing glycemic and insulinemic responses. However, coincidental with recommendations to increase the intake of starchy foods has been the recognition that the glycemic responses to all starches are not the same and that starches are not interchangeable (Bornet et al. 1989 In humans, the postprandial plasma glucose and insulin responses to 50 g carbohydrate as cooked potato are much higher than the responses to an equivalent load in the form of corn or rice (Crapo et al. 1977 One major reason for the lack of general acceptance of the possible nutritional value of using low glycemic index foods is the lack of understanding of mechanisms by which consistently low glycemic and insulinemic peaks confer long-term physiological benefits.
Recently, Lerer-Metzger et al. (1996)
Acute study
Characterization of starches.
A first set of experiment was designed to characterize the mung bean starch (cooked powdered Chinese noodles, Pagoda Brand, manufactured in the Republic of China, purchased from local Asian supermarkets in France, prepared by the INRA, Nantes; and donated by Dr. F. Bornet, Eridania Beghin-Say, Vilvoorde, Belgium), and the waxy cornstarch (prepared and donated by Cerestar). Previously, Bornet et al. (1989) In vitro digestibility ( Measurements of resistant starch.
Resistant starch is measured as the part of starch that escapes digestion and hydrolysis after incubation with Glycemic and insulinemic indices (test-meals).
Four test meals were administered to normal rats in our laboratory using four mixed diets with 575 g/kg starch as either mung beans, waxy corn, wheat or glucose. Twenty nondiabetic male Sprague-Dawley rats (body weight, 350 g, centre d'Elevage Robert Janvier, Le Genest St-Isle, France) were used. Approval to use laboratory animals was given by the French Ministry of Agriculture, and the protocol complied with the guide for the care and use of laboratory animals (NRC 1985). Rats were placed in individual cages and trained for 2 wk as follows: each morning a small amount of a powdered standard diet (semisynthetic diet no. 210, fabricated by the UAR, Usine d'Alimentation Rationnelle, Villemoisson-sur-Orge, France, Table 1) was introduced into the cage and removed after 20 min.
Chronic study
Animals and diet.
Eighteen normal and eighteen diabetic male Sprague-Dawley rats (Centre d'Elevage Robert Janvier) were used. Diabetes was induced by injecting rats with streptozotocin (Zanosar R, Upjohn, La Défence, France) on d 2 of life (100 mg/kg body weight in 5 mmol/L citrate buffer, pH 4.5) according to the method described by Bonner-Weir et al. (1981) Intraperitoneal glucose tolerance test.
Two tests were performed, before the start and 3 d before the end of the experimental period to verify that the diabetic rats were hyperglycemic. On the morning of the experiment, food was removed at 0800 h. At 1400 h, rats were anesthetized with pentobarbital. Blood samples were taken from the tip of the tail (time 0). A glucose challenge was given intraperitoneally, and other blood samples were taken at 15 and 50 min.
Preparation of isolated adipocytes.
Epididymal adipocytes were prepared and isolated according to the method described by Rodbell (1964) Glucose metabolism in epididymal adipocytes.
Glucose incorporation into total lipids and oxidation into CO2 in adipocytes were studied by incubating epididymal adipocytes in tubes capped with a rubber stopper fitted with a plastic central well (Lavau et al. 1979
Assessment of adipocyte volume and diameter.
Aliquots of adipocyte suspension were photographed under a light microscope. Adipocyte volume was measured by a semi-automatic method, as described by Lavau et al. (1977) Measurement of plasma glucose, insulin and lipid concentrations.
Plasma glucose was measured by the glucose oxidase technique with a Beckman glucose analyzer. Plasma insulin (Insulin RIA kits, CIS Bio International, Gif sur Yvette, France). Plasma triacylglycerols (Enzymatic triglyceride kit, BioMérieux, Marcy-l'Etoile, France), cholesterol (Labintest cholesterol kit, Labintest, Aix-en-Provence, France), phospholipids (Enzymatic phospholipid kits, BioMérieux) and free fatty acids (Enzymatic free fatty acids kits, Nefa C*, Unipath, Dardilly, France) were also measured.
Statistical analysis.
In the acute study, the glycemic index for each meal was calculated by dividing the area under the incremental curve above fasting glucose levels by that of the glucose meal. For the insulinemic area, the total area was used, because the time-0 value (measured on a separate day) was higher than the 30-min value. Comparison among the glycemic and insulinemic indices as well as glucose and insulin areas after the four different test meals was made by using one-way ANOVA. When the F test was significant, differences between all pairs of means were tested using Fisher's least significant difference procedure (Lellouch and Lazar 1974 Acute study
Characterization of starches.
The two starches were pure starches as shown in Table 2. The in vitro digestibility measured within 30 min was higher for waxy corn than for mung bean starch. The content of resistant starch was higher in the mung bean starch than in the waxy cornstarch. However, statistical difference was not determined because only duplicate assays existed.
Chronic study
Food intake, body and organ weights.
Both the mung bean and waxy cornstarch diets were well tolerated. Food intake and body weight of the diabetic rats were lower than those of the normal rats during wk 2 and 3 (P < 0.01), (Table 3). There were no differences between rats fed mung bean starch diet or waxy cornstarch diet in either diabetic or normal rats.
Intraperitoneal glucose tolerance test.
Plasma glucose responses were significantly higher, whereas plasma insulin responses were lower in rats that received streptozotocin compared with normal rats before the beginning of the experimental periods (P < 0.01, data not shown). These results are consistent with previous results from our laboratory (Lerer-Metzger et al. 1996 Cellularity of adipose tissue.
As shown in Table 3, diabetes had no effect on adipocyte diameter. The type of diet, however, affected the size of adipocytes. Rats fed the mung bean starch diet had smaller adipocytes than those fed the waxy cornstarch diet (P < 0.01).
Plasma glucose, insulin and lipid concentrations.
At the end of the experimental period, the diabetic rats were hyperglycemic (P < 0.005) compared with the nondiabetic rats (Table 4). Insulin, triacylglycerol, cholesterol, free fatty acid and phospholipid concentrations did not differ in normal and diabetic rats.These variables, measured in fed rats, were not significantly affected by diet treatment.
Glucose metabolism in adipocytes.
Basal conversion of glucose into total lipids in epididymal adipocytes was higher in the rats fed the waxy cornstarch diet than in those fed the mung bean starch diet, in both normal and diabetic rats (Table 5). Lipogenesis (both basal and maximal insulin stimulated) was higher due to the waxy cornstarch diet in both normal and diabetic rats (Fig. 2, Table 5).
Different carbohydrates produce different postprandial blood glucose and insulin responses in normal and diabetic subjects (Crapo et al. 1977 We thank F. Bornet (Eridania Beghin-Say) for his help in preparing the mung bean powder, B. Guy-Grand for agreeing to measure plasma lipids in his laboratory and M. Lavau for permitting us to make fat-cell size measurements in her laboratory.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
, Fontvieille et al. 1988, Lerer-Metzger et al. 1996).
and 1980). The lowest glycemic responses have been reported after consumption of dried legumes and peanuts (Bornet et al. 1989, Jenkins et al. 1981 and 1983). High amylose products, including rice (Miller et al. 1992, Goddard et al. 1984), muffins (Krezowski et al. 1987) and crackers (Behall et al. 1988), have been found to induce low blood glucose and insulin responses when compared with similar products high in amylopectin.
reported that a test meal of mung bean starch induced lower glycemic responses than the same amount of wheat starch in rats. Furthermore, replacing wheat starch with mung bean starch (570 g/kg) in a mixed diet for 5 wk resulted in lower plasma glucose and free fatty acid concentrations in normal but not in diabetic rats. A reduction in triacylglycerols and a decrease in adipocyte diameter were also found in both normal and diabetic rats. The mechanisms by which starches with different glycemic indices and amylose-amylopectin contents could modify lipid metabolism and adipocyte diameter in different ways have not been determined. To understand the underlying mechanisms, we decided to evaluate the effects of feeding for 3 wk a high or low glycemic index starchy diet on insulin-stimulated glucose metabolism in epididymal adipocytes of normal and diabetic rats. The starches used were cooked mung bean starch and waxy cornstarch because they are characterized by different glycemic responses and amylose-amylopectin contents. The mung bean starch contained 320 g amylose/kg starch and had a very low glycemic index (Bornet et al. 1989), whereas the waxy cornstarch contained 5 g amylose/kg starch (C* Top 12410 - Crestar - Benelux, Breda, Netherlands) and was expected to have a high glycemic index.
View this table:
Table 1.
Composition of standard diet
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
showed that the mung beans contain 97.6 g starch/100 g dry matter and <1 g fiber/100 g dry matter. In this study, we measured the total starch content of the two starches (14 samples of each) by an enzymatic method (Englyst et al. 1994).
-amylolysis).
The two starches were tested in vitro to investigate their susceptibility to -amylase, because it has been shown that the percentage of starch hydrolyzed in vitro within 30 min strongly correlates with the glycemic index of starch in humans (Bornet et al. 1989). Two aliquots of each of these diets (duplicate assay) were subjected after 1 min of sieving to -amylase hydrolysis with 3000 units of porcine pancreatic -amylase (166 U/g dry material) with constant stirring (30 rpm) in a phosphate buffer (5 mmol/L, pH 7) for 3 h at 37°C. Every 5 min, a 0.90-mL sample was mixed in 4.5 mL ethanol (80%) and 0.25 mol/L acetic acid and stored overnight at 4°C (Leclère et al. 1993). Samples were then centrifuged at 9000 × g for 10 min at 4°C. The soluble glucose in the supernatant was assayed using a sulfuric orcinol automatic method (Tollier and Robin 1979). Intra-assay reproductibility was 15% at 30 min and 4% at 180 min.
-amylase in vitro. It was measured by the method of Englyst et al. (1992) and the modified Berry method (Champ et al. 1992). After amylase treatment and alcohol washing, 5 mL of water was added to the residue. Samples were mixed, incubated for 30 min at 100°C and then cooled in ice water; 5mL of 4 mol/L KOH was added to disperse the resistant starch. After 30 min of magnetic stirring, 1 mL was added to 10 mL of 0.5 mol/L acetic acid containing 4 mmol/L CaCl2. Then 46.6 nkat of amyloglucosidase (AMG, 400 AGU, Novo Nordisk Bioindustries, UK) was added, and the samples were incubated for 30 min at 70°C. After neutralization and centrifugation, at 1000 × g for 5 min at 4°C, released glucose was determined by the glucose oxidase method (glucose GOD-PAP, Boehringer Mannheim, Germany) on an automatic analyzer (Beckman, Fullerton, CA).
View this table:
Table 2.
Characteristics of the two starches used
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Fig 1.
Postprandial plasma glucose and insulin concentrations (left panels) and areas under the response curves (right panels) in rats fed 2 g of a mixed diet containing 575 g starch/kg diet as either mung bean starch, waxy cornstarch, wheat starch or the same amount as glucose in normal Sprague-Dawley rats. Values are means ± SEM (n = 9). Blood samples were taken from the tip of the tail in pentobarbital-anesthetized rats. Plasma glucose and insulin concentrations at 0 min had been determined in the same rats on a separate day. *P < 0.05, **P < 0.005, waxy cornstarch-fed group vs. all other groups. Areas under the glucose and insulin response curves with different letter superscripts were significantly different, P < 0.05.
and Portha et al. (1989). Normal rats used as controls were injected with an equivalent volume of vehicle buffer.
20°C for further plasma glucose, insulin and lipid measurements. Epididymal fat pads, liver and kidneys were immediately removed and weighed.
. Minced epididymal fat pads were incubated under slow agitation for 60 min at 37°C with collagenase (EC 3.4.24.3 , type II, Sigma, St. Louis, MO) in Krebs-Ringer bicarbonate buffer, pH 7.4, containing 35 g/L bovine albumin (RIA grade, Sigma). Adipocytes were then filtered through a 250-µm nylon screen, washed three times in the same buffer and diluted in different proportions according to the study intended to achieve approximate respective concentrations of 109 and 4 × 108 cells/L. Two aliquots were taken for measurement of total lipid content, following the technique described by Dole and Meinertz (1960), to determine the adipocyte number in each experiment.
). The cells were incubated in triplicate for 1 h at 37°C at a final cellular concentration of 2% (v/v) in Krebs-Ringer bicarbonate buffer containing bovine serum albumin (35 g/L), glucose (6 mmol/L), D-[U-14C] glucose (14.8 MBq/L of final solution, Amersham International, Buckinghamshire, England) and insulin (0-1.7 nmol/L). The reaction was terminated by injecting 0.5 mL of sulfuric acid (0.25 mol/L) into the medium, which helps the liberation of CO2. The CO2 generated was trapped in 0.3 mL of hyamin 10-X (Packard Instruments, Downers Grove, IL) in the central well when the tubes were agitated (100 cycles/min) at room temperature. The central wells were removed for the determination of radioactivity from CO2. The total lipids from the incubated fat cells were extracted into n-heptane by the method of Dole and Meinertz (1960) and dried before radioactivity was counted. To determine glucose transport (Guerre-Millo et al. 1985), epididymal adipocytes were preincubated in Krebs-Ringer bicarbonate buffer containing bovine serum albumin (35 g/L), pyruvate(2 mmol/L) and insulin (0-1.7 nmol/L) for 30 min at 37°C. The final cellular concentration was 3.5% (v/v). Then, 22.2 kBq of D-[U-14 C] glucose (Amersham), was added to each tube and the incubation continued for 30 s. Glucose transport was stopped by centrifugation of the incubation mixture through 100 µL of silicon oil, and the radioactivity in the cell layer was counted.
View this table:
Table 3.
Characteristics of normal and diabetic rats after 3 wk of consuming a diet containing 575 g/kg mung bean
starch or waxy cornstarch1
. Mean cell diameter and volume were calculated using the formula of Goldrick (1967). The number of adipocytes was thus calculated after measurment of the total lipid content of the fat pads.
). Differences between starch contents of the two starches were determined by using unpaired Student's t test.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
) and those of others studying this type of diabetes (Bonner-Weir et al. 1981, Portha et al. 1989). After 3 wk of consuming the respective diets, the areas under the glucose response curves were higher in diabetic than in normal rats (P < 0.05), whereas those under the insulin response curves were lower in diabetic rats than in normal rats (P < 0.001) (curves not shown). The two diets, however, produced comparable plasma glucose and insulin responses to an intraperitoneal glucose challenge: in diabetic rats, the areas under the glucose response curves after mung bean and waxy cornstarch were 335 ± 35 versus 325 ± 43 mmol·min/L, respectively (P > 0.05). In normal rats the areas under the glucose response curves were 267 ± 21 vs. 150 ± 20 mmol·min/L, respectively (P = 0.057).
View this table:
Table 4.
Plasma glucose, insulin and lipid concentrations in normal and diabetic rats after 3 wk of consuming diets containing 575 g/kg mung bean starch or waxy cornstarch1
View this table:
Table 5.
Glucose incorporation into total lipids, oxidation and transport in epididymal adipocytes after 3 wk of consuming a diet containing 575 g/kg mung bean or waxy cornstarch in normal diabetic rats1
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Fig 2.
Biological effects of insulin (insulin-stimulated basal values): glucose-14C incorporated into lipids (A), converted into CO2 (B) and glucose transport (C) as a function of different insulin concentrations in the incubation medium in vitro in adipocytes isolated from normal and diabetic rats, after 3 wk of consuming mixed diets containing 575 g starch/kg as either mung bean or waxy cornstarch. Values are expressed as means ± SEM, n = 9. *P < 0.05, significant effects of cornstarch and diabetes.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, Järvi et al. 1995, Jenkins et al. 1981, Wolever et al. 1991). These results lead to the classification of carbohydrates according to their blood glucose response relative to glucose (Fontvieille et al. 1992) or to white bread (Wolever et al. 1992), which is called the glycemic index of carbohydrates. Several studies in humans also reported different responses after mixed meals with different glycemic indices (Behall et al. 1989, Goddard et al. 1984, Van Amelsvoort and Weststrate 1992). In this study, and for the first time, we showed that different starchy foods incorporated into a mixed meal gave different blood glucose responses in rats relative to glucose, i.e., different glycemic indices. When starches with different amylose-amylopectin ratios (waxy cornstarch, 5-995 g/kg; mung beans, 320-680 g/kg) were incorporated into a mixed meal, the meal with the high amylopectin starch (waxy cornstarch) showed a higher glycemic index than that of the low amylopectin starch (mung beans).
, Fontvielle et al. 1988, Jenkins et al. 1988 and 1992, Wolever et al. 1992) in diabetics or in patients with lipid disorders. Although the objectives in these studies were to maintain the same proportions of macronutrients and fiber in the tested diets (low or high glycemic index), in some cases this was not achieved. Some low glycemic index diets were higher in fiber and lower in fat than the high glycemic index diets, making the results difficult to interpret. Modest improvements mainly in plasma lipid concentrations were achieved in free-living individuals. Two studies have investigated the amylose content in the food as a factor in lowering blood glucose and insulin responses when given in chronic conditions in humans (Behall et al. 1989, Behall and Howe 1995). The authors found that the chronic consumption of high amylose foods normalized the insulin response of hyperinsulinemic subjects (Behall and Howe 1995) and even lowered glucose and insulin response curves of normal subjects (Behall et al. 1989).
found that the replacement of a high glycemic index starch incorporated into a mixed diet by a low glycemic index starch for 5 wk resulted in reduced plasma triglycerides and lessened adipocyte size. The cause of these results was questioned. In this study, a shorter period of time (3 wk) was used to measure insulin action in small sensitive adipocytes of younger rats. The replacement of the high glycemic index starch (waxy cornstarch/amylose, 0.5:100, wt/wt ) by a low glycemic index starch (mung beans/amylose, 32:100, wt/wt) led to small adipocytes, a result associated with both lowered basal and insulin-stimulated incorporation of glucose into total lipids in normal and diabetic rats. This decrease in insulin-stimulated lipogenesis probably was not due to a decrease in insulin action, because no difference was found when results were expressed as a percentage of basal values, indicating that insulin sensitivity of adipocytes did not interfere with lowering lipogenesis. The results observed were due mainly to decreased basal values. Nevertheless, reduced lipogenesis in adipocytes of mung bean-fed rats could be responsible for the observed change in adipocyte size.
). In this study, however, there were no differences in plasma insulin or glucose levels in either normal or diabetic rats after 3 wk of consuming either the high or low glycemic index starchy foods. These results confirm the findings of Byrnes et al. (1995) who found also that in normal rats, a high waxy cornstarch diet did not increase basal insulin levels if consumed for <9 wk. However, the effect of repeated low postprandial plasma insulin peaks in rats fed the mung bean starch diet, as well as the high peaks in those fed the waxy cornstarch diet (as shown in the present acute study) might play an important role in changing adipocyte size in the long term. Thus, variations in postprandial insulin levels cannot be excluded as a possible factor influencing adipocyte diameter.
) for a longer period (5 wk), the lower adipocyte diameter was accompanied by a marked tendency for lower epididymal fat pad weights, and plasma free fatty acids and triacylglycerols. Thus, changes in lipid metabolism at the cellular level seem to precede any change in plasma lipids.
showed that a low glycemic index diet consumed for 4 wk led to increased insulin-stimulated adipocyte glucose uptake. Adipocytes were taken by a presternal fat biopsy during a coronary artery bypass surgery. Increased peripheral insulin action at the cellular level in this study did not lead to a change in either plasma insulin or glucose responses at the basal values within the 3-wk study period. In normal rats, whole-body insulin resistance, measured by an intravenous glucose tolerance test, was found to be modified after 8 wk of consuming a high amylopectin starch diet. Insulin responses to an intravenous glucose load increased after 8 wk and were found to be 100% greater than those of rats fed the high amylose diet by 12 wk (Byrnes et al. 1995). There was no difference in glucose tolerance at any time. Wiseman et al. (1996) also showed that, in rats, whole-body insulin resistance induced by amylopectin starch consumed for 8 or 16 wk was nonreversible. Here again, changes in insulin action could occur early at the cellular level and might precede any modification of whole-body insulin action.
, fed a diet rich in resistant starch to rats for 6 wk and found a reduction in energy absorption and a decrease in epididymal fat pads. In this study, however, the amount of the resistant starch in the mung bean starch diet was about 10 g/100 g compared with the high values of 65 or 37 g/100 g inthe study of De Deckere et al. (1995). In addition, this study shows that after 3 wk of consuming the mung bean starch diet, there was no change in adipose tissue or whole-body weight. Thus, the amount of resistant starch in the low glycemic index diet could not be responsible for the observed results. Another factor to be considered is the rate of intestinal starch digestion. The -amylase digestibility in vitro of the two starches showed a slight difference. However, it is unclear whether the different rates of digestion could have different chronic effects on glucose and lipid metabolism at the cellular level. The only apparent main factor leading to the observed results was the consistently low postprandial glycemic and insulinemic peaks.
ACKNOWLEDGMENTS
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FOOTNOTES |
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Manuscript received 5 December 1996. Initial reviews completed 5 March 1997. Revision accepted 3 September 1997.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results
Discussion
References
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