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1 From the Department of Medicine, Division of Gastroenterology and Endocrinology, University of Göttingen, Germany.
2 Address reprint requests to G Schäfer, Department of Medicine, Division of Gastroenterology and Endocrinology, University of Göttingen, Robert-Koch-Strasse 40, 37075 Göttingen, Germany. E-mail: gschfer{at}med.uni-goettingen.de.
ABSTRACT
Background: Data on the blood glucose response of diabetic patients to mixed meals containing food both rich in fiber and with a low glycemic index, such as dried peas, is scarce. Thus, the extent to which type 2 diabetic patients should take into account low-glycemic, high-fiber foods for their daily carbohydrate intake is uncertain.
Objective: We compared the glycemic and insulinemic responses to 3 different meals based on dried peas, potatoes, or both in patients with type 2 diabetes undergoing dietary treatment.
Design: The meals, prepared according to local recipes and consumed at weekly intervals in random order at lunchtime, contained comparable amounts of carbohydrate, fat, protein, and water. The carbohydrate source of the meals differed and was supplied from either dried peas (meal 1), potatoes (meal 3), or a combination thereof (meal 2). Peripheral and venous blood was sampled over 180 min.
Results: The increases in postprandial plasma glucose and insulin concentrations were delayed and significantly smaller after the pea meal than after the potato meal. The areas under the glucose curve were 164 ± 40, 257 ± 57, and 381 ± 40 mmol • 180 min/L for meals 1, 2, and 3, respectively (P < 0.01). The areas under the insulin curve were 13.8 ± 4.3, 15.4 ± 3.9, and 31.2 ± 6.9 nmol • 180 min/L, respectively (P = 0.0514).
Conclusion: These findings suggest that carbohydrates in dried peas may be largely disregarded in carbohydrate counting and that type 2 diabetic patients should probably increase their consumption of low-glycemic, high-fiber foods at the expense of high-glycemic, low-fiber foods.
Key Words: Postprandial glycemia • dried peas • potatoes • type 2 diabetes • dietary carbohydrate • glycemic index • insulin secretion
INTRODUCTION
Maintenance of near-normal blood glucose concentrations is one of the major goals of medical nutrition therapy and is an integral part of diabetes management (1). A balance between food intake, (endogenous or exogenous) insulin or oral antidiabetic medication, and the level of physical activity may help in achieving this goal (2). Although dietary proteins and fats can also modify postprandial glycemia, the carbohydrate load of a meal is the primary determinant in postprandial blood glucose excursions. Therefore, knowledge of the carbohydrate content of foods and calculating the amount contained in meals (carbohydrate counting) are useful tools in the self-management of diabetes. However, there are differences in the digestibility and absorbability of different types of carbohydrates by the gastrointestinal tract (3). The postprandial glycemic response to different foods may vary despite equal amounts of total absorbable carbohydrates (4, 5). The concept of the glycemic index (GI; 5–7) was established to account for these differences. The varying fiber content of foods may also cause fluctuations in the absorption of dietary carbohydrate (8). Patients with type 2 diabetes who increased their fiber intake (9) and included more foods with a low GI in their diet had improved blood glucose regulation and lipid metabolism (10, 11). The extent to which low-glycemic, high-fiber foods, such as dried peas, should be accounted for in carbohydrate counting is uncertain. The full carbohydrate content of legumes is sometimes listed in dietary guidelines given to patients with type 2 diabetes. Some guidelines, however, take into account legume carbohydrates in part or do not list them at all. We therefore studied the glycemic and insulinemic responses to 3 different mixed meals containing either dried peas, potatoes, or both as carbohydrate sources, in type 2 diabetic patients undergoing dietary treatment.
SUBJECTS AND METHODS
Subjects
The study comprised 9 patients with type 2 diabetes, 6 men and 3 women, who followed a meal plan recommended by a dietitian. Patients with a fasting blood glucose concentration < 7.2 mmol/L and a hemoglobin concentration > 135 (men) or 125 (women) g/L were eligible for the study. Patients treated with oral antidiabetic drugs, insulin, ß-blockers, corticosteroids, or other drugs with a potential influence on blood glucose concentrations were excluded, as were patients with a history of gastrointestinal tract surgery or gastrointestinal disease. The mean (± SEM) age of the patients was 61 ± 3 y (range: 48–75 y). The mean body mass index (BMI; in kg/m2) was 29.9 ± 1.7 (range: 23.1–39.6). The average glycated hemoglobin value at the first study visit was 6.3% (range: 5.6–6.9%).
Study design
This randomized crossover study was conducted on 3 different days separated by weekly intervals. After consuming a standard breakfast at 0800 and a snack at 1000, type 2 diabetic patients received 1 of 3 different mixed meals in random order at 1230. The isoenergetic meals contained comparable amounts of carbohydrate, protein, fat, and water. The carbohydrate sources were either dried peas (Pisum sativum), potatoes (Solanum tuberosum, var. Granola), or both. The details of the test meals are shown in Table 1. Nutrient data were calculated by using food-composition tables (12). Meals were freshly prepared according to traditional recipes and a standardized procedure. Dried peas (yellow whole seeds) were presoaked overnight and cooked until soft. We served 3 different meals: meal 1 had peas as the only carbohydrate source, meal 2 had peas and potatoes as the carbohydrate sources (two-thirds and one-third of the carbohydrate content, respectively), and meal 3 had potatoes as the only carbohydrate source. Cooked carrots, celery, and sausages were mixed with the peas in meals 1 and 2. Meal 3 was served with cooked carrots and celery separately, together with fried lean pork and gravy. The patients also drank small servings of tea to compensate for differences in water content between the meals. The meals were consumed over 10–17 min.
View this table:
TABLE 1 . Composition of the 3 test meals1
Blood samples were collected 15 and 0 min before meal ingestion (baseline) and then 30, 60, 90, 120, 150, and 180 min after meal ingestion (postprandial values). Venous blood was taken from an antecubital vein for the measurement of serum insulin concentrations, and fingertip capillary blood was used for the measurement of plasma glucose concentrations. Between study days, the patients went about their everyday lives without any change in the degree of physical activity. Informed consent was obtained from each patient before enrolment, and the study design was approved by the Faculty of Medicine Ethics Committee, Georg-August-University, Göttingen, Germany.
Laboratory analyses
Venous blood samples were collected in serum monovettes, and capillary blood was collected into heparin-containing microvettes (Sarstedt, Nürnbrecht, Germany). Venous blood was centrifuged immediately at 3500 x g for 15 min at 4 °C, and serum for insulin measurement was portioned and frozen at -20 °C. Insulin was quantified by using a commercial radioimmunoassay (Pharmacia, Uppsala, Sweden). Blood collected in the microvettes was stored at 4 °C until completion of sample collection on each study day. Plasma glucose concentrations were then measured immediately by using the glucose oxidase method with a Hitachi 917 Automatic Analyzer (Boehringer Mannheim, Mannheim, Germany).
Statistics
Plasma glucose and serum insulin responses were calculated as incremental areas above the preprandial concentrations and are expressed as means ± SEMs. One-way analysis of variance with subsequent Tukey’s multiple comparison test was performed for statistical analysis. Student’s unpaired t test (two-tailed) was used for the BMI-subgroup analysis of increases from baseline at 60 min for plasma glucose and serum insulin. The results are presented as means ± SDs. All analyses were done by using GRAPHPAD PRISM 2.00 software for PCs (GraphPad Software Inc, San Diego). A value of P < 0.05 was considered significant.
RESULTS
Mean plasma glucose and serum insulin responses are presented in Figure 1. On each test day, plasma glucose (6.9 ± 0.5, 6.6 ± 0.5, and 6.7 ± 0.8 mmol/L) and serum insulin (125 ± 22, 127 ± 23, and 126 ± 13 pmol/L) concentrations were not significantly different before the consumption of meals 1, 2, and 3, respectively. Marginal, intermediate, or distinct initial increases in plasma glucose concentration (glucose30 min) occurred after ingestion of meals 1, 2, and 3 (0.3 ± 0.2, 1.3 ± 0.2, and 2.6 ± 0.5 mmol/L, respectively; P = 0.0002). Mean increases from baseline at 60 min (glucose60 min) of 1.1 ± 0.3, 2.0 ± 0.4, and 4.1 ± 0.3 mmol/L, respectively, were calculated (P < 0.0001).
FIGURE 1. . Mean (± SEM) plasma glucose and serum insulin concentrations in patients with type 2 diabetes in response to the ingestion of mixed meals containing peas (; meal 1), potatoes (; meal 3), or both (; meal 2) as carbohydrate sources. n = 9.
The serum insulin curves ran roughly parallel to the plasma glucose curves. Mean initial increases (insulin30 min) were 49 ± 21, 68 ± 13, and 131 ± 37 pmol/L after meals 1, 2, and 3, respectively (P = 0.0826). Mean increases from baseline at 60 min (insulin60 min) were 84 ± 29, 119 ± 29, and 255 ± 41 pmol/L, respectively (P = 0.0037). After meal 3, a major difference was noted in the insulin curve, which did not decrease in parallel with the glucose curve. Rather, the 60-min insulin peak remained at approximately the same concentration up to 120 min.
At these time points, the insulinemic responses showed marked interindividual variations, as is evident from the broad SEM ranges (Figure 1). Differences between the patients’ BMIs may have been responsible for these variations. Four subjects had a BMI < 30, and 5 subjects had a BMI > 30. Subgroup analysis showed no significant differences between baseline serum insulin concentrations before meal 1 (100 ± 29 compared with 138 ± 13 pmol/L), meal 2 (93 ± 32 compared with 126 ± 17 pmol/L), or meal 3 (119 ± 29 compared with 115 ± 6 pmol/L) in those with a BMI < 30 (n = 4) compared with those with a BMI ≥ 30 (n = 5), respectively (P > 0.05). In response to meals 1, 2, or 3, increases in plasma glucose or in serum insulin from baseline at 60 min did not differ significantly between the BMI subgroups. However, the insulinemic response of subjects with a BMI > 30 was, on average, twice that of subjects with a BMI < 30; the respective ratio for the glycemic response was 0.8:1.
The results shown in Figure 1 are shown as incremental areas under the curve (AUCs) for plasma glucose and serum insulin responses 120 and 180 min postprandially in Figure 2. On average, meal 3 (potatoes) elicited a response 3.3 and 2.3 times higher than did meal 1 (dried peas) for the 120- and 180-min incremental AUCs for glucose (P < 0.05 each). Incremental AUCs for insulin at 120 and 180 min were 2.7 (P < 0.05) and 2.3 (P = 0.0514) times higher after meal 3 than after meal 1. Significant differences between respective means were found except for the 180-min insulin AUCs (P = 0.0514).
FIGURE 2. . Mean (± SEM) incremental areas under the curve (AUCs) for plasma glucose and serum insulin calculated over 120- and 180-min periods in patients with type 2 diabetes after the ingestion of mixed meals containing peas (meal 1), potatoes (meal 3), or both (meal 2) as carbohydrate sources. Bars with different letters are significantly different, P < 0.05 (ANOVA). n = 9.
DISCUSSION
One aim of the dietary recommendations given to patients with diabetes mellitus is to help them avoid marked postprandial hyperglycemia. The importance of these recommendations is strengthened by the fact that postprandial blood glucose concentrations have been shown to be directly associated with cardiovascular disease in type 2 diabetic patients (13). Therefore, calculation of the carbohydrate content of meals may help these patients achieve well-balanced daily blood glucose profiles. In our department, we generally recommend that middle-aged, moderately overweight type 2 diabetic patients eat a total of 36 g carbohydrates at lunchtime; therefore, we chose this amount for the meals in our study.
The main rationale for conducting the study was to collect supporting data for practical dietary guidelines. It therefore seemed reasonable to offer "normal" mixed meals that were prepared according to popular traditional recipes and hence adapted to the participants’ usual eating habits. In addition, the test meals were not given in the morning after an overnight fast, as in several previous studies (6, 7, 14–16), but at the usual lunchtime. Although this time period might not be ideal for a standardized experimental setting, it was chosen to better reflect the real-life situation. After fixed breakfasts and snacks on each study day, prelunch concentrations of plasma glucose and serum insulin did not differ significantly between the participants. Absolute values and interindividual differences were consistent with the ranges observed before breakfast in type 2 diabetic patients who had fasted overnight (7). Prelunch glucose concentrations also did not differ significantly from those measured before breakfast in fasting subjects who self-monitored their glucose concentrations with home glucose meters. This finding, in combination with the finding of glycated hemoglobin values in a therapeutically desirable range, led us to assume that our study participants were not markedly insulin resistant or insulin deficient.
The glycemia observed after consumption of 36 g carbohydrate from dried peas was only about one-third of the glycemia observed after ingestion of 36 g carbohydrate as potatoes. Concerning practical dietary recommendations for carbohydrate exchange, it seems advisable to count 30 g dried peas as one-third of a carbohydrate unit. If the total carbohydrate content of dried peas is counted, it might lead to hypoglycemia in patients receiving antidiabetic drugs. Total disregard of the carbohydrate content, however, would probably result in higher than expected blood glucose concentrations if dried peas were consumed together with other carbohydrate sources. Dietary education programs should therefore make diabetic patients aware of these facts. Bearing this in mind, it seems reasonable to recommend that type 2 diabetic patients, especially those receiving dietary treatment only, should increase their consumption of dried peas (and probably other legumes). It is important to note, however, that traditional legume-based stews are often cooked with sausage or bacon and therefore contain a high amount of fat. Dietary recommendations should include suggestions for lean exchanges, if not for all patients, then at least for diabetic patients with a BMI of 30 or above.
Most of the findings on glycemic responses to legumes have focused on the responses to beans, lentils, and chickpeas (17). Dried pea seeds have been used in only a few studies, and the GI is reported to be 33 (mean values of 22, 31, and 47) (17). The reported GI for potatoes also varies considerably, ranging from 47 to 82 (17). This variation may be due to the fact that the carbohydrate content of potatoes is actually lower than food-composition tables suggest (18). When the carbohydrate content was directly assessed, an average GI of > 78 was calculated for 3 different potato varieties (18). Although the calculation of GIs was not an objective of the present study, our findings may nevertheless provide some comparative values.
Attenuated glycemic responses after ingestion of legumes have been attributed to their high-fiber content, their high amylose-amylopectin ratio in starch, their antinutrient content, or a combination thereof (7, 8, 19). Thirty grams of isolated pea fiber have been reported to markedly reduce the incremental AUC for glucose after a 50-g glucose load in healthy subjects (20). The total fiber content of the meals offered in the present study differed somewhat and was not adjusted (by adding isolated fibers) to maintain the typical character of the meals. Generally, diets with fiber contents of 5 g/meal and providing 15 g/d or 1.7 g/MJ are considered low in fiber; meals that contain 3 times these amounts are considered to be high in fiber (21–23). In the present study, meal 3 had a medium fiber content (10.9 g/meal, or 5.3 g/MJ), and the maximum ratio between fiber amounts was only 1.6 (meal 1 compared with meal 3). Thus, we did not expect these differences to have a major effect on the results. The data presented suggest that digestion and absorption of the potato starch was not substantially affected by the presence of peas, because the glycemic responses (glucose60 min, AUC120 min, and AUC180 min) measured after meal 2 agreed well with values obtained arithmetically by adding two-thirds of the responses to meal 1 and one-third of the responses to meal 3.
The finding of parallel glycemic and insulinemic responses in the present study is consistent with observations from a previous investigation that assessed insulinemic indexes and GIs for mixed meals in type 2 diabetic patients (7) and healthy subjects (15). By contrast, this finding does not concur with results reported by Indar-Brown et al (16), who found inconsistencies between insulinemic and glycemic responses in both healthy persons and type 2 diabetic patients after the ingestion of ethnic foods. In contrast with the study designs chosen by Bornet et al (7), Chew et al (15), and us, the study by Indar-Brown et al (16) did not require all subjects to consume all 5 meals. Interindividual differences in insulinemic responses may have contributed to the discrepancy mentioned.
Bornet et al (7) suggested that the presence of protein was responsible for the differences seen in insulinemic responses to starch-rich foods eaten alone or in a mixed meal. Our study design did not make a distinction between carbohydrate- and protein-induced insulin secretion. Because the meals were designed to be about equal in nutrient composition, proteins were not presumed to affect the results. When 10, 30, or 50 g protein was added to 50-g glucose loads in type 2 diabetic patients, the insulinemic response increased significantly only after the meals containing 30 or 50 g protein (24). Thus, we do not believe that the somewhat lower protein content of meal 2 (25 g) than of meals 1 and 3 (30 g) in our study was responsible for the observed differences in the insulinemic responses.
The insulinemic response varied greatly between the study participants. Hyperinsulinemia due to insulin resistance is a well-known feature of obesity; thus, differences in body weight might explain the variability observed. The BMI in our study participants varied within a broad range (subjects ranged from being of normal weight to being severely obese). On the basis of a cutoff BMI of 30, the insulinemic response was more pronounced in the obese subjects. Differences in b cell function might have also contributed to the variations in insulinemic responses. However, as shown by the values for percentage of glycated hemoglobin, the study participants had excellent glycemic control without the use of oral antidiabetic drugs; therefore, it seems unlikely that the variations in insulinemic responses were due to b cell exhaustion in some patients.
Hyperinsulinemia (in fasting and nonfasting states) might be a risk factor for cardiovascular disease (25). An increase in the consumption of low-glycemic, low-insulinemic foods (eg, dried peas) is advisable for obese persons, especially for those who have diabetes. However, as mentioned above, the importance of consuming a low-fat diet should be stressed.
In conclusion, our study showed that dried peas as a carbohydrate source in a normal mixed meal elicit significantly lower glycemic and insulinemic responses than do potatoes in patients with type 2 diabetes. We suggest that two-thirds of the carbohydrate content of dried peas be disregarded by type 2 diabetic patients when carbohydrate counting.
ACKNOWLEDGMENTS
GS analyzed the data and wrote the manuscript. US designed the experiment, adjusted the composition of and prepared the meals, and collected and analyzed the data. UR obtained patient information, collected samples, and assisted with the writing of the manuscript. GR and UL conceived the study and interpreted the data. The study was not supported by any organization or sponsor; thus, the authors had no financial or personal interests to disclose.
REFERENCES