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Original Investigation |

Effect of Legumes as Part of a Low Glycemic Index Diet on Glycemic Control and Cardiovascular Risk Factors in Type 2 Diabetes Mellitus:  A Randomized Controlled Trial FREE

David J. A. Jenkins, MD, PhD; Cyril W. C. Kendall, PhD; Livia S. A. Augustin, PhD; Sandra Mitchell, RD; Sandhya Sahye-Pudaruth, RD; Sonia Blanco Mejia, MD; Laura Chiavaroli, MSc; Arash Mirrahimi, MSc; Christopher Ireland, BSc; Balachandran Bashyam, PhD; Edward Vidgen, BSc; Russell J. de Souza, ScD; John L. Sievenpiper, MD; Judy Coveney, RD; Lawrence A. Leiter, MD; Robert G. Josse, MD
[+] Author Affiliations

Author Affiliations: Clinical Nutrition and Risk Factor Modification Center (Drs Jenkins, Kendall, Augustin, Blanco Mejia, Bashyam, de Souza, and Sievenpiper, Mss Mitchell, Sahye-Pudaruth, Chiavaroli, and Coveney, and Mssrs Mirrahimi, Ireland, and Vidgen), Division of Endocrinology and Metabolism (Drs Leiter and Josse), Keenan Research Center of the Li Ka Shing Knowledge Institute (Drs Jenkins, Leiter, and Josse), St Michael's Hospital, Toronto, Ontario, Canada; Departments of Nutritional Sciences (Drs Jenkins, Kendall, Augustin, Blanco Mejia, Bashyam, Leiter, and Josse, Ms Chiavaroli, and Mr Mirrahimi) and Medicine (Drs Jenkins, Leiter, and Josse), Faculty of Medicine, University of Toronto, Toronto; College of Pharmacy and Nutrition (Dr Kendall), University of Saskatchewan, Saskatoon, Saskatchewan, Canada; and Departments of Clinical Epidemiology and Biostatistics (Dr de Souza) and Pathology and Molecular Medicine (Dr Sievenpiper), Faculty of Health Sciences, McMaster University, Hamilton, Ontario.


Arch Intern Med. 2012;172(21):1653-1660. doi:10.1001/2013.jamainternmed.70.
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Published online

Background Legumes, including beans, chickpeas, and lentils, are among the lowest glycemic index (GI) foods and have been recommended in national diabetes mellitus (DM) guidelines. Yet, to our knowledge, they have never been used specifically to lower the GI of the diet. We have therefore undertaken a study of low-GI foods in type 2 DM with a focus on legumes in the intervention.

Methods A total of 121 participants with type 2 DM were randomized to either a low-GI legume diet that encouraged participants to increase legume intake by at least 1 cup per day, or to increase insoluble fiber by consumption of whole wheat products, for 3 months. The primary outcome was change in hemoglobin A1c (HbA1c) values with calculated coronary heart disease (CHD) risk score as a secondary outcome.

Results The low-GI legume diet reduced HbA1c values by −0.5% (95% CI, −0.6% to −0.4%) and the high wheat fiber diet reduced HbA1c values by −0.3% (95% CI, −0.4% to −0.2%). The relative reduction in HbA1c values after the low-GI legume diet was greater than after the high wheat fiber diet by −0.2% (95% CI, −0.3% to −0.1%; P < .001). The respective CHD risk reduction on the low-GI legume diet was −0.8% (95% CI, −1.4% to −0.3%; P = .003), largely owing to a greater relative reduction in systolic blood pressure on the low-GI legume diet compared with the high wheat fiber diet (−4.5 mm Hg; 95% CI, −7.0 to −2.1 mm Hg; P < .001).

Conclusion Incorporation of legumes as part of a low-GI diet improved both glycemic control and reduced calculated CHD risk score in type 2 DM.

Trial Registration clinicaltrials.gov Identifier: NCT01063361

Figures in this Article

Low glycemic index (GI) foods have been shown to improve glycemic control in patients with type 2 diabetes mellitus (DM).1,2 Legumes, also known as pulses (dried beans, chick peas, and lentils), were the first class of foods recognized as having low GI values3 and have been recommended in many national DM guidelines.46 However, few studies have assessed the effect of legumes in DM,7 even fewer have documented the quantity used to improve glycemic control, and none have reported their effect on cardiovascular risk.8 Not only are legumes good sources of slowly digested starch, but they are also relatively high in fiber and vegetable protein. Both fiber, notably viscous fiber, and also vegetable protein, specifically legume protein containing the 7S globulin fraction, are known to lower serum cholesterol levels.912 Furthermore, increased intakes of fiber9 and substitution of vegetable for animal proteins, as occur with increased legume consumption, have been associated with reductions in blood pressure (BP).13 In this respect, consumption of legumes, especially in the context of hypocaloric diets, also resulted in lower BP in patients without DM.1417 The potential for reduction in coronary heart disease (CHD) risk factors in patients with type 2 DM by a dietary change, such as increased legume consumption, aimed at improving glycemic control is particularly relevant at a time when pharmacologic approaches to achieve improved glycemic control have not resulted in improved cardiovascular outcomes in the short term.18

We have therefore tested the effect on glycemic control, serum lipid levels, and BP of emphasizing increased legume intake as part of a low-GI diet in the treatment of type 2 DM.

PARTICIPANTS

Participants were recruited from newspaper and public transport advertisements as well as hospital clinics. A total of 121 participants were eligible and randomized (Figure). Recruitment took place from February 16, 2010, to May 11, 2011, with the last study visit on August 8, 2011. Eligible participants had been diagnosed as having type 2 DM for at least 6 months, were taking a stable dose of oral antihyperglycemic agents for at least the previous 2 months, and had hemoglobin A1c (HbA1c) values that were 6.5% to 8.5% of total hemoglobin both at initial screening and at the visit 1 week prior to commencing the study (Figure). (To convert HbA1c to a proportion of total hemoglobin, multiply by 0.01.) No participants had clinically significant cardiovascular, renal (creatinine level >1.70 mg/dL [>150 μmol/L]) or liver disease (alanine aminotransferase level >3 times the upper limit of normal [10-40 U/L, or 0.17-0.68 μkat/L]) or a history of cancer (Table 1).

Place holder to copy figure label and caption
Graphic Jump Location

Figure. Flowchart of participants through the trial. HbA1c indicates hemoglobin A1c; ITT, intention to treat.

Table Graphic Jump LocationTable 1. Baseline Characteristics of Study Participants
PROTOCOL

The study followed a randomized, parallel design with 2 treatment arms of 3 months' duration consisting of (1) a low-GI diet emphasizing legume consumption and (2) a high wheat fiber diet emphasizing high wheat fiber foods. After stratification by sex and HbA1c value (HbA1c value ≤7.1% of total hemoglobin), participants were randomized by a statistician (E.V.)who was geographically separate from the study center. Neither the dietitians nor the participants could be blinded, but equal emphasis was placed on the potential importance for health of both diets. The analytical technicians were blinded to treatment, as was the statistician, up to analysis of the primary outcome.

Participants attended the research center for screening and at week −1, baseline (week 0), and weeks 2, 4, 8, 10, and 12 of the study. At each visit, they were weighed, waist circumference was measured at the level of the umbilicus when standing, and a fasting blood sample was taken. Seated BP was measured in triplicate with an automatic sphygmomanometer (model HEM 907 XL; Omron Healthcare Inc), and 7-day food records covering the week prior to each visit were discussed with the dietitian. If participants experienced symptoms of hypoglycemia and observed capillary blood glucose levels lower than 63 mg/dL and providing hypoglycemia was not explained by specific circumstances, such as missed meals or increased physical activity, antihyperglycemic medications were reduced by the participants' physician according to a predetermined protocol previously sent to the participants' physician. (To convert blood glucose levels to millimoles per liter, multiply by 0.0555.) If HbA1c values rose above 8.5% of total hemoglobin on 2 successive occasions, participants were withdrawn from the study and referred back to their physician.

The study was approved by the research ethics board of St Michael's Hospital and the University of Toronto, Toronto, Ontario, Canada, and written consent was obtained from all participants.

DIETARY INTERVENTIONS

Participants were provided with a checklist of 15-g carbohydrate portions of recommended foods and the quantities they were expected to consume daily (eTable 1 and eTable 2). The target legume consumption was 1 cup per day (approximately 190 g per day, or 2 servings per day) of cooked beans, chickpeas or lentils, while a high wheat fiber diet was achieved by consumption of whole wheat and whole grain carbohydrate foods (whole wheat breakfast cereals, breads, brown rice, etc). Adherence to the diet was assessed from 7-day food records at the week zero visit and the mean of the last 3 visits (weeks 8, 10, and 12); 109 participants provided complete dietary and blood data for the 3-month study, and 114 also provided at least 1 data point during the last month of the study and were therefore classified as completers (Figure). At the conclusion of the study, participants were contacted and asked to rate their gastrointestinal symptoms before and at the end of the study on a scale of 0 to 6, where 0 was none, 3 was moderate, and 6 was excessive. Forty-four participants in the low-GI legume diet arm and 46 in the high wheat fiber diet arm responded.

ENERGY REQUIREMENTS

Energy requirements were calculated for each participant using the Harris-Benedict equation with allowance for light physical activity (ie, light exercise 1-3 days per week).19,20

BIOCHEMICAL AND DIETARY ANALYSES

The HbA1c value was analyzed within 24 hours using whole blood collected in EDTA Vacutainer tubes (Vacutainer; Becton, Dickinson and Co) in the hospital routine analytical laboratory by a turbidometric inhibition latex immunoassay (TINIA Roche Diagnostics) with a coefficient of variation between assays of 3% to 4%. Blood glucose and serum lipid levels were also measured in the hospital routine analytical laboratory using a Random Access Analyzer and Beckman reagents (SYNCHRON LX Systems; Beckman Coulter), with a coefficient of variation of 1.6% to 2.3% for blood glucose level and 1.3% to 3.0% for total cholesterol, triglycerides, and high-density lipoprotein cholesterol (HDL-C) levels. The low-density lipoprotein cholesterol (LDL-C) level was calculated by the method of Friedewald et al21 {LDL-C level = total cholesterol –[(triglycerides/5) × (HDL-C level)]}.

Diet records were analyzed using a computer program (ESHA Food Processor SQL, version 10.1.1) based on US Department of Agriculture data22 and international GI tables23 using the bread scale (for glucose scale, multiply values by 0.71)24 with additional GI measurements made on local foods (Glycemic Index Laboratories).

STATISTICAL ANALYSES

Results are expressed as means ± SEM or 95% confidence intervals (CIs). The absolute CHD risk score was calculated using the Framingham risk equation.25 Any patient who met inclusion criteria, including an HbA1c value of at least 6.5% of total hemoglobin at the week −1 visit, and provided week 0 measurements was included in the analysis (n = 121). The mean of weeks −1 and 0 time was taken as baseline, and weeks 8, 10 and 12 were selected as end of study to allow for stabilization of HbA1c values as the main outcome. Treatment differences in physical and biochemical measures were assessed using all available data, and a repeated measures mixed (random effects) model accounting for time of assessment (SAS statistical software, version 9.2; SAS Institute Inc).The response variable was change from baseline, with diet and week as the main fixed-effects and patient identification nested in diet. There was no adjustment for baseline. An additional term representing an autoregression covariance assumption was included in the model for body weight since a significant time trend was observed over the 12-week treatment (specifically, over the 8- to 12-week period).

Multiple imputation (taking the mean of 5 sets of randomly imputed values) was used for Table 2 and Table 3 to generate data for those who dropped out or had missing values. Two participants were randomized but did not start, provided no data, and were unaware of their randomization and hence were not included in the analysis (modified intention to treat), nor were 8 participants whose week −1 HbA1c values were lower than 6.5% of total hemoglobin. Differences in gastrointestinal symptom scores were assessed by 2 sample t tests and within-treatment changes for other variables were assessed by paired t test (2-tailed) using data derived by multiple imputation. Changes in medication use were assessed by the likelihood ratio χ2 test.

Table Graphic Jump LocationTable 2. Daily Nutritional Profile at Baseline and End of Study for 121 Participants Consuming Either High Wheat Fiber or Low–Glycemic Index (GI) Legume Dietsa
Table Graphic Jump LocationTable 3. Mean Study Measurements and Significance of Treatment Differences for Modified Intention-to-Treat Analysis in 121 Participantsa

Fifty-six of 60 participants (93.3%) completed the low-GI legume diet arm (ie, provided ≥1 blood sample in the final month), compared with a similar proportion, 58 of 61 (95.1%) completing the high wheat fiber diet arm. Participants did not differ significantly in baseline blood lipids levels, BP, or anthropometry (Table 1).

Dietary variables at baseline were different between treatments for saturated and polyunsaturated fats, as a percentage of total energy, on the low-GI legume diet relative to variables on the high wheat fiber diet (1.0%; P = .03 and −0.8%; P = .03, respectively), although the clinical significance of these differences is doubtful. During the study, there were also many similarly small statistically significant changes in dietary variables following increased legume consumption (Table 2). The absolute GI reduction on the low-GI legume diet was −14 GI units (95% CI, −16 to −13; P < .001), and the relative GI reduction compared with the high wheat fiber diet was −18 GI units (95% CI, −20 to −16; P < .001).

GLYCEMIC CONTROL AND BODY WEIGHT

Oral antihyperglycemic medication dosages increased in 2 participants (both receiving the high wheat fiber treatment) and decreased in 3 participants based on the participants' physicians' decision owing to decreased blood glucose levels (1 in the high wheat fiber diet arm and 2 in the low-GI legume diet arm). Changes in medication were not different between treatments (P = .85).

The mean HbA1c value fell by −0.5% absolute HbA1c value (95% CI for change, −0.6% to −0.4%; P = .001) on the low-GI legume diet and by −0.3% absolute HbA1c value (95% CI, −0.4% to −0.2%; P < .001) on the high wheat fiber diet (Table 3). The relative HbA1c reduction on the low-GI legume diet was −0.2% of total hemoglobin (95% CI, −0.3% to −0.1%; P < .001) (Table 3) and remained significant after adjustment for body weight change (P = .005). Significant reductions in body weight were also seen on both the low-GI legume and high wheat fiber diets (−2.7 kg; 95% CI, −3.5 to −1.9 kg; and −2.0 kg; 95% CI, −2.5 to −1.5 kg, respectively; P < .001 for both comparisons) (Table 3). The treatment difference in body weight was also significant (P = .002), together with a significant reduction in waist circumference on the low-GI legume diet compared with the high wheat fiber diet (−1.4 cm; 95% CI, −2.3 to −0.4 cm; P = .007).

SERUM LIPID LEVELS

Lipid-lowering medications were decreased in 4 participants (1 in the high wheat fiber diet arm, 3 in the low-GI legume diet arm) and increased in 1 participant in the high wheat fiber diet arm, with no significant treatment difference (P = .21).

The low-GI legume diet produced significant decreases in total cholesterol level (−8 mg/dL; 95% CI, −13 to −4 mg/dL; P < .001) and triglyceride levels (−22 mg/dL; 95% CI, −30 to −13 mg/dL; P < .001) with no significant change in HDL-C level (−1 mg/dL; 95% CI, −2 to 0 mg/dL; P = .19). Meanwhile, the high wheat fiber diet resulted in a significant increase in HDL-C level (2 mg/dL; 95% CI, 1 to 3 mg/dL; P = .004). (To convert total cholesterol and HDL-C and LDL-C to millimoles per liter, multiply by 0.0259; to convert triglyceride to millimoles per liter, multiply by 0.0113.)

The relative reduction in total cholesterol level (−8 mg/dL; 95% CI, −13 to −2 mg/dL; P = .005) was greater in the low-GI legume diet arm, as was the reduction in HDL-C level (−2 mg/dL; 95% CI, −3 to −1 mg/dL; P < .001) owing to the rise in HDL-C level in the high wheat fiber diet arm. No other lipid treatment differences were significant (Table 3).

BP AND HEART RATE

Both BP and heart rate were reduced on the low-GI legume diet relative to the high wheat fiber diet (systolic BP, −4.5 mm Hg; 95% CI, −7.0 to −2.1 mm Hg; P < .001; diastolic BP, −3.1 mm Hg; 95% CI, −5.0 to −1.6 mm Hg; P < .001); and heart rate (−3.1 beats per minute [bpm]; 95% CI, −4.7 to −1.5 bpm; P < .001) (Table 3).

CHD RISK

Calculated absolute CHD risk was reduced after low-GI legume consumption relative to the high wheat fiber diet (−0.8%; 95% CI, −1.4% to −0.3%; P = .003). The relative CHD risk reduction was not significant (P = .27) (Table 3).

ADVERSE EVENTS

There were no serious adverse events recorded. One participant in the low-GI legume diet arm experienced chest pain related to a spontaneous pleural effusion and temporally discontinued antihyperglycemic medications, and a further participant experienced heartburn. No patient was withdrawn from the study owing to repeated HbA1c values greater than 8.5% of total hemoglobin.

GASTROINTESTINAL SYMPTOMS

Self-reported gastrointestinal symptoms were similar between groups at baseline and showed similar changes on treatment in symptom scores (abdominal pain, bloating, flatus, or bowel habit) between the legume and high-fiber arms (eTable 3).

Increased legume consumption as part of a low-GI diet lowered HbA1c values, BP, heart rate, and estimated absolute CHD risk. These data provide support for the use of legumes as a specific food option to lower the dietary GI in type 2 DM and for the recommendations to increase low-GI food consumption by many national diabetes associations.46

This is the first study, to our knowledge, to promote the use of legumes specifically as the major focus of a low-GI diet for the treatment of DM and to report the quantities of legumes consumed. A previous meta-analysis of studies that included legumes as part of low-GI or high fiber interventions in type 2 DM demonstrated a 0.48% reduction in HbA1c values,8 similar to the 0.5% reduction observed with the low-GI legume diet in the current study. The US Food and Drug Administration has proposed a reduction of 0.3% to 0.4% in HbA1c value as therapeutically meaningful.26 The 1% and 0.67% absolute reductions in HbA1c values in the UKPDS27 and ADVANCE28 studies, respectively, resulted in 37% and 21% reductions in microvascular complications.

Use of wheat fiber as a positive control may have minimized the treatment difference. It is true that the increase in fiber intake was modest, but the baseline was already high at 16.6 g per 1000 kcal. The high wheat fiber diet resulted in a significant 0.3% reduction in HbA1c values, a significant rise in HDL-C levels, and reductions in body weight, waist circumference, fasting blood glucose and triglyceride levels, and CHD risk. These data are in line with the findings from cohort studies, which have observed strong associations between cereal fiber intake and reductions in DM incidence and cardiovascular events.2931 However, it is difficult to explain the increase in the HDL-C level. To our knowledge, an increased HDL-C level has not previously been associated with increased wheat fiber intake.32 Furthermore, the lack of association between change in the HDL-C level and legume consumption on the low-GI legume diet (r = −0.02; n = 56; P = .86) does not support an effect of beans in lowering the HDL-C level.

To our knowledge, this trial is the first to demonstrate a BP reduction with legume consumption in type 2 DM. This reduction was all the more remarkable since the mean starting BP was already in the acceptable range at 122/72 mmHg. Increased plant food and plant protein consumption has been associated with lower BP, as seen with the DASH diet.33,34 Consumption of baked beans in an analysis of the NHANES data was associated with lower BP,35 and trials of bean-enriched diets, specifically the use of lupins, have also demonstrated a reduction in BP,1416 although not all studies of bean consumption have shown this effect.17

The exact mechanisms for the BP reduction associated with bean intake are not known. Peptides digested from proteins, notably from casein (lactopeptides), may be absorbed and have antihypertensive effects.36 Other protein sources may also produce antihypertensive peptides.37 Beans specifically are good sources of potassium and magnesium, which may reduce BP38,39 and by virtue of their low GI are likely to result in lower postprandial insulin levels, associated with reduced salt retention and lower BP.40,41 Acarbose, which converts dietary carbohydrates into a slow-release, low-GI form, has also been associated with a reduced incidence of hypertension and CHD events in prediabetic participants in the STOP NIDDM trial.42 In addition to the potential direct beneficial effects of vegetable protein and fiber, there is also the potential displacement value of vegetable protein foods in reducing animal protein foods, which are higher in saturated fat and cholesterol, as has been shown for increased soy consumption.43

To our knowledge, this study is also the first to assess the effect of bean consumption on heart rate and indeed one of the few to determine the effect of any dietary intervention. Previous studies have suggested that increased heart rate is associated with increased CHD risk.34 Relatively little work has been done recently with this simple measurement to define the dose-response relation of heart rate to CHD risk; however, earlier studies suggest a doubling of CHD risk for every increase of 10 bpm.44

The study weaknesses include the relatively small changes observed in glycemic control, blood lipid levels, and BP compared with the control arm. However, the use of an effective control diet (positive control) may have minimized the opportunity to see treatment differences. Furthermore, this study was ad libitum in nature, with self-reported diet records and likely underreporting of food intake, as evidenced by the relatively low caloric intakes.

These findings linking legume consumption to both improved glycemic control and reduced CHD risk are particularly important because type 2 DM is increasing most rapidly in the urban environments of populations in which bean intake has traditionally been high (eg, India, Latin America, the Pima Indians of Arizona).45,46 Support for the continued use of such foods in traditional bean-eating communities, together with their reintroduction into the Western diet, could therefore be justified even if the effect on glycemia is relatively small, given the magnitude of the problem and the need for acceptable dietary options, especially those options that may also have a BP and cardiovascular advantage.

In conclusion, legume consumption of approximately 190 g per day (1 cup) seems to contribute usefully to a low-GI diet and reduce CHD risk through a reduction in BP. This effect of legumes seems analogous to that seen with acarbose, which also transforms the dietary carbohydrate into a more slowly digested low-GI form and has been associated with a reduced rate of hypertension and CHD events in prediabetic individuals.42

Correspondence: David J. A. Jenkins, MD, PhD, Department of Nutritional Sciences, University of Toronto, 150 College St, Toronto, ON M5G 2M4, Canada (NutritionProject@smh.ca).

Accepted for Publication: July 2, 2012.

Published Online: October 22, 2012. doi:10.1001/2013.jamainternmed.70

Author Contributions: Drs Jenkins, Kendall, and Augustin and Mr Vidgen had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Jenkins and Kendall. Acquisition of data: Augustin, Mitchell, Sahye-Pudaruth, Blanco Mejia, Chiavaroli, Mirrahimi, Ireland, and Coveney. Analysis and interpretation of data: Jenkins, Kendall, Augustin, Bashyam, Vidgen, de Souza, Sievenpiper, Leiter, and Josse. Drafting of the manuscript: Jenkins. Critical revision of the manuscript for important intellectual content: Jenkins, Kendall, Augustin, Mitchell, Sahye-Pudaruth, Blanco Mejia, Chiavaroli, Mirrahimi, Ireland, Bashyam, Vidgen, de Souza, Sievenpiper, Leiter, Coveney, and Josse. Statistical analysis: Vidgen and de Souza. Obtained funding: Jenkins and Kendall. Administrative, technical, and material support: Kendall, Augustin, Chiavaroli, Mirrahimi, Ireland, and Bashyam. Study supervision: Jenkins, Kendall, Augustin, Leiter, and Josse.

Conflict of Interest Disclosures: Dr Jenkins has served on the Scientific Advisory Board of Sanitarium Company, Agri-Culture and Agri-Food Canada (AAFC), Canadian Agriculture Policy Institute (CAPI), California Strawberry Commission, Loblaw Supermarket, Herbal Life International, Nutritional Fundamental for Health, Pacific Health Laboratories, Metagenics, Bayer Consumer Care, Orafti, Dean Foods, Kellogg’s, Quaker Oats, Procter & Gamble, Coca-Cola, NuVal Griffin Hospital, Abbott, Pulse Canada, Saskatchewan Pulse Growers, and Canola Council of Canada; received honoraria for scientific advice from Sanitarium Company, Orafti, the Almond Board of California, the American Peanut Council, International Tree Nut Council Nutrition Research and Education Foundation and the Peanut Institute, Herbal Life International, Pacific Health Laboratories, Nutritional Fundamental for Health, Barilla, Metagenics, Bayer Consumer Care, Unilever Canada and Netherlands, Solae, Oldways, Kellogg’s, Quaker Oats, Procter & Gamble, Coca-Cola, NuVal Griffin Hospital, Abbott, Canola Council of Canada, Dean Foods, California Strawberry Commission, Haine Celestial, Pepsi, and Alpro Foundation; has been on the speakers panel for the Almond Board of California; received research grants from Saskatchewan Pulse Growers, the Agricultural Bioproducts Innovation Program (ABIP) through the Pulse Research Network (PURENet), Advanced Food Materials Network (AFMNet), Loblaw, Unilever, Barilla, Almond Board of California, Coca-Cola, Solae, Haine Celestial, Sanitarium Company, Orafti, International Tree Nut Council Nutrition Research and Education Foundation and the Peanut Institute, the Canola and Flax Councils of Canada, Calorie Control Council, Canadian Institutes of Health Research, Canada Foundation for Innovation, and the Ontario Research Fund; and received travel support to meetings from the Solae, Sanitarium Company, Orafti, AFMNet, Coca-Cola, The Canola and Flax Councils of Canada, Oldways Preservation Trust, Kellogg’s, Quaker Oats, Griffin Hospital, Abbott Laboratories, Dean Foods, the California Strawberry Commission, American Peanut Council, Herbal Life International, Nutritional Fundamental for Health, Metagenics, Bayer Consumer Care, AAFC, CAPI, Pepsi, Almond Board of California, Unilever, Alpro Foundation, International Tree Nut Council, Barilla, Pulse Canada, and the Saskatchewan Pulse Growers. Dr Jenkins' wife is a director of Glycemic Index Laboratories, Toronto, Ontario, Canada. Dr Kendall has received research grants, travel funding, consultant fees, or honoraria or has served on the scientific advisory board for Abbott, AFMNet, Almond Board of California, American Peanut Council, American Pistachio Growers, Barilla, California Strawberry Commission, Canadian Institutes of Health Research, Canola Council of Canada, Danone, General Mills, Hain Celestial, International Tree Nut Council, Kellogg’s, Loblaw Brands Ltd, Oldways, Orafti, Paramount Farms, Pulse Canada, Saskatchewan Pulse Growers, Solae, and Unilever. Mr Vigden has been a consultant for ABIP through the PURENet and the Saskatchewan Pulse Growers. Dr de Souza is a coapplicant on unrestricted research grants awarded to Dr Jenkins from Coca-Cola and the Calorie Control Council and is a recipient of a postdoctoral research fellowship from the Canadian Institutes of Health Research. Dr Sievenpiper has received several unrestricted travel grants to present research at meetings from The Coca-Cola Company and is a coinvestigator on an unrestricted research grant from The Coca-Cola Company. Dr Sievenpiper has also received travel funding and honoraria from Archer Daniels Midland, the International Life Sciences Institute (ILSI) North America, and Abbott Laboratories; and research support, consultant fees, and travel funding from Pulse Canada. Ms Chiavaroli holds a casual clinical research coordinator position at Glycemic Index Laboratories. Dr Augustin and Mss Mitchell, Sahye-Pudaruth, and Coveney and Mr Ireland received funding from Saskatchewan Pulse Growers, Pulse Canada, and AAFC.

Funding/Support: This work was supported by ABIP through the PURENet and the Saskatchewan Pulse Growers. Dr Jenkins receives salary support as a Canada Research Chair from the federal government of Canada.

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Lovati MR, Manzoni C, Corsini A, Granata A, Fumagalli R, Sirtori CR. 7S globulin from soybean is metabolized in human cell cultures by a specific uptake and degradation system.  J Nutr. 1996;126(11):2831-2842
PubMed
Jenkins DJ, Wong JM, Kendall CW,  et al.  The effect of a plant-based low-carbohydrate (“Eco-Atkins”) diet on body weight and blood lipid concentrations in hyperlipidemic subjects.  Arch Intern Med. 2009;169(11):1046-1054
PubMed   |  Link to Article
Belski R, Mori TA, Puddey IB,  et al.  Effects of lupin-enriched foods on body composition and cardiovascular disease risk factors: a 12-month randomized controlled weight loss trial.  Int J Obes (Lond). 2011;35(6):810-819
PubMed   |  Link to Article
Hermsdorff HH, Zulet MA, Abete I, Martínez JA. A legume-based hypocaloric diet reduces proinflammatory status and improves metabolic features in overweight/obese subjects.  Eur J Nutr. 2011;50(1):61-69
PubMed   |  Link to Article
Abete I, Parra D, Martinez JA. Legume-, fish-, or high-protein-based hypocaloric diets: effects on weight loss and mitochondrial oxidation in obese men.  J Med Food. 2009;12(1):100-108
PubMed   |  Link to Article
Lee YP, Mori TA, Puddey IB,  et al.  Effects of lupin kernel flour-enriched bread on blood pressure: a controlled intervention study.  Am J Clin Nutr. 2009;89(3):766-772
PubMed   |  Link to Article
Gerstein HC, Miller ME, Genuth S,  et al; ACCORD Study Group.  Long-term effects of intensive glucose lowering on cardiovascular outcomes.  N Engl J Med. 2011;364(9):818-828
PubMed   |  Link to Article
Shetty PS, Henry CJ, Black AE, Prentice AM. Energy requirements of adults: an update on basal metabolic rates (BMRs) and physical activity levels (PALs).  Eur J Clin Nutr. 1996;50:(suppl 1)  S11-S23
PubMed
Harris J, Benedict F. A Biometric Study of Basal Metabolism in Man. Washington, DC: Carnegie Institute of Washington; 1919. Publication No. 279
Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge.  Clin Chem. 1972;18(6):499-502
PubMed
US Department of Agriculture.  Composition of Foods, Agriculture Handbook No. 8: The Agriculture Research Service. Washington, DC: US Dept of Argiculture; 1992
Atkinson FS, Foster-Powell K, Brand-Miller JC. International tables of glycemic index and glycemic load values: 2008.  Diabetes Care. 2008;31(12):2281-2283
PubMed   |  Link to Article
International Standards Organisation.  ISO 26642-2010: Food Products: Determination of the Glycaemic Index (GI) and Recommendation for Food Classification. Geneva, Switzerland: International Standards Organisation; 2010
Anderson KM, Wilson PW, Odell PM, Kannel WB. An updated coronary risk profile: a statement for health professionals.  Circulation. 1991;83(1):356-362
PubMed   |  Link to Article
US Food and Drug Administration.  Guidance for industry: diabetes mellitus: developing drugs and therapeuticbiologics for treatment and prevention. http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm071624.pdf. Accessed June 12, 2012
Stratton IM, Adler AI, Neil HA,  et al.  Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study.  BMJ. 2000;321(7258):405-412
PubMed   |  Link to Article
Patel A, MacMahon S, Chalmers J,  et al; ADVANCE Collaborative Group.  Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes.  N Engl J Med. 2008;358(24):2560-2572
PubMed   |  Link to Article
Salmerón J, Manson JE, Stampfer MJ, Colditz GA, Wing AL, Willett WC. Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women.  JAMA. 1997;277(6):472-477
PubMed   |  Link to Article
Liu S, Willett WC, Stampfer MJ,  et al.  A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease in US women.  Am J Clin Nutr. 2000;71(6):1455-1461
PubMed
Meyer KA, Kushi LH, Jacobs DR Jr, Slavin J, Sellers TA, Folsom AR. Carbohydrates, dietary fiber, and incident type 2 diabetes in older women.  Am J Clin Nutr. 2000;71(4):921-930
PubMed
Jenkins DJ, Kendall CW, McKeown-Eyssen G,  et al.  Effect of a low-glycemic index or a high-cereal fiber diet on type 2 diabetes: a randomized trial.  JAMA. 2008;300(23):2742-2753
PubMed   |  Link to Article
Sacks FM, Svetkey LP, Vollmer WM,  et al; DASH-Sodium Collaborative Research Group.  Effects on blood pressure of reduced dietary sodium and the Dietary Approaches to Stop Hypertension (DASH) diet.  N Engl J Med. 2001;344(1):3-10
PubMed   |  Link to Article
Elliott P, Stamler J, Dyer AR,  et al.  Association between protein intake and blood pressure: the INTERMAP Study.  Arch Intern Med. 2006;166(1):79-87
PubMed   |  Link to Article
Papanikolaou Y, Fulgoni VL III. Bean consumption is associated with greater nutrient intake, reduced systolic blood pressure, lower body weight, and a smaller waist circumference in adults: results from the National Health and Nutrition Examination Survey 1999-2002.  J Am Coll Nutr. 2008;27(5):569-576
PubMed
Boelsma E, Kloek J. Lactotripeptides and antihypertensive effects: a critical review.  Br J Nutr. 2009;101(6):776-786
PubMed   |  Link to Article
Vermeirssen V, Van Camp J, Verstraete W. Bioavailability of angiotensin I converting enzyme inhibitory peptides.  Br J Nutr. 2004;92(3):357-366
PubMed   |  Link to Article
Chobanian AV, Bakris GL, Black HR,  et al; Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. National Heart, Lung, and Blood Institute; National High Blood Pressure Education Program Coordinating Committee.  Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure.  Hypertension. 2003;42(6):1206-1252
PubMed   |  Link to Article
Joffres MR, Reed DM, Yano K. Relationship of magnesium intake and other dietary factors to blood pressure: the Honolulu Heart Study.  Am J Clin Nutr. 1987;45(2):469-475
PubMed
DeFronzo RA, Cooke CR, Andres R, Faloona GR, Davis PJ. The effect of insulin on renal handling of sodium, potassium, calcium, and phosphate in man.  J Clin Invest. 1975;55(4):845-855
PubMed   |  Link to Article
Friedberg CE, van Buren M, Bijlsma JA, Koomans HA. Insulin increases sodium reabsorption in diluting segment in humans: evidence for indirect mediation through hypokalemia.  Kidney Int. 1991;40(2):251-256
PubMed   |  Link to Article
Chiasson JL, Josse RG, Gomis R, Hanefeld M, Karasik A, Laakso M. STOP-NIDDM Trial Research Group.  Acarbose treatment and the risk of cardiovascular disease and hypertension in patients with impaired glucose tolerance: the STOP-NIDDM trial.  JAMA. 2003;290(4):486-494
PubMed   |  Link to Article
Jenkins DJ, Mirrahimi A, Srichaikul K,  et al.  Soy protein reduces serum cholesterol by both intrinsic and food displacement mechanisms.  J Nutr. 2010;140(12):2302S-2311S
PubMed   |  Link to Article
Singh BN. Increased heart rate as a risk factor for cardiovascular disease.  Eur Heart J. 2003;5:(suppl G)  G3-G9
Link to Article
Brand JC, Snow BJ, Nabhan GP, Truswell AS. Plasma glucose and insulin responses to traditional Pima Indian meals.  Am J Clin Nutr. 1990;51(3):416-420
PubMed
 Trends in diabetes prevalence among American Indian and Alaska Native children, adolescents, and young adults: 1990-1998. www.cdc.gov/diabetes. Accessed May 15, 2012

Figures

Place holder to copy figure label and caption
Graphic Jump Location

Figure. Flowchart of participants through the trial. HbA1c indicates hemoglobin A1c; ITT, intention to treat.

Tables

Table Graphic Jump LocationTable 1. Baseline Characteristics of Study Participants
Table Graphic Jump LocationTable 2. Daily Nutritional Profile at Baseline and End of Study for 121 Participants Consuming Either High Wheat Fiber or Low–Glycemic Index (GI) Legume Dietsa
Table Graphic Jump LocationTable 3. Mean Study Measurements and Significance of Treatment Differences for Modified Intention-to-Treat Analysis in 121 Participantsa

References

Brand-Miller J, Hayne S, Petocz P, Colagiuri S. Low-glycemic index diets in the management of diabetes: a meta-analysis of randomized controlled trials.  Diabetes Care. 2003;26(8):2261-2267
PubMed   |  Link to Article
Ludwig DS. The glycemic index: physiological mechanisms relating to obesity, diabetes, and cardiovascular disease.  JAMA. 2002;287(18):2414-2423
PubMed   |  Link to Article
Jenkins DJ, Wolever TM, Taylor RH, Barker HM, Fielden H. Exceptionally low blood glucose response to dried beans: comparison with other carbohydrate foods.  Br Med J. 1980;281(6240):578-580
PubMed   |  Link to Article
Mann JI, De Leeuw I, Hermansen K,  et al; Diabetes and Nutrition Study Group (DNSG) of the European Association.  Evidence-based nutritional approaches to the treatment and prevention of diabetes mellitus.  Nutr Metab Cardiovasc Dis. 2004;14(6):373-394
PubMed   |  Link to Article
Bantle JP, Wylie-Rosett J, Albright AL,  et al; American Diabetes Association.  Nutrition recommendations and interventions for diabetes: a position statement of the American Diabetes Association.  Diabetes Care. 2008;31:(suppl 1)  S61-S78
PubMed   |  Link to Article
Misra A, Sharma R, Gulati S,  et al; National Dietary Guidelines Consensus Group.  Consensus dietary guidelines for healthy living and prevention of obesity, the metabolic syndrome, diabetes, and related disorders in Asian Indians.  Diabetes Technol Ther. 2011;13(6):683-694
PubMed   |  Link to Article
Simpson HC, Simpson RW, Lousley S,  et al.  A high carbohydrate leguminous fibre diet improves all aspects of diabetic control.  Lancet. 1981;1(8210):1-5
PubMed   |  Link to Article
Sievenpiper JL, Kendall CW, Esfahani A,  et al.  Effect of non-oil-seed pulses on glycaemic control: a systematic review and meta-analysis of randomised controlled experimental trials in people with and without diabetes.  Diabetologia. 2009;52(8):1479-1495
PubMed   |  Link to Article
Vuksan V, Jenkins DJ, Spadafora P,  et al.  Konjac-mannan (glucomannan) improves glycemia and other associated risk factors for coronary heart disease in type 2 diabetes: a randomized controlled metabolic trial.  Diabetes Care. 1999;22(6):913-919
PubMed   |  Link to Article
Anderson JW, Story L, Sieling B, Chen WJ, Petro MS, Story J. Hypocholesterolemic effects of oat-bran or bean intake for hypercholesterolemic men.  Am J Clin Nutr. 1984;40(6):1146-1155
PubMed
Anderson JW, Johnstone BM, Cook-Newell ME. Meta-analysis of the effects of soy protein intake on serum lipids.  N Engl J Med. 1995;333(5):276-282
PubMed   |  Link to Article
Lovati MR, Manzoni C, Corsini A, Granata A, Fumagalli R, Sirtori CR. 7S globulin from soybean is metabolized in human cell cultures by a specific uptake and degradation system.  J Nutr. 1996;126(11):2831-2842
PubMed
Jenkins DJ, Wong JM, Kendall CW,  et al.  The effect of a plant-based low-carbohydrate (“Eco-Atkins”) diet on body weight and blood lipid concentrations in hyperlipidemic subjects.  Arch Intern Med. 2009;169(11):1046-1054
PubMed   |  Link to Article
Belski R, Mori TA, Puddey IB,  et al.  Effects of lupin-enriched foods on body composition and cardiovascular disease risk factors: a 12-month randomized controlled weight loss trial.  Int J Obes (Lond). 2011;35(6):810-819
PubMed   |  Link to Article
Hermsdorff HH, Zulet MA, Abete I, Martínez JA. A legume-based hypocaloric diet reduces proinflammatory status and improves metabolic features in overweight/obese subjects.  Eur J Nutr. 2011;50(1):61-69
PubMed   |  Link to Article
Abete I, Parra D, Martinez JA. Legume-, fish-, or high-protein-based hypocaloric diets: effects on weight loss and mitochondrial oxidation in obese men.  J Med Food. 2009;12(1):100-108
PubMed   |  Link to Article
Lee YP, Mori TA, Puddey IB,  et al.  Effects of lupin kernel flour-enriched bread on blood pressure: a controlled intervention study.  Am J Clin Nutr. 2009;89(3):766-772
PubMed   |  Link to Article
Gerstein HC, Miller ME, Genuth S,  et al; ACCORD Study Group.  Long-term effects of intensive glucose lowering on cardiovascular outcomes.  N Engl J Med. 2011;364(9):818-828
PubMed   |  Link to Article
Shetty PS, Henry CJ, Black AE, Prentice AM. Energy requirements of adults: an update on basal metabolic rates (BMRs) and physical activity levels (PALs).  Eur J Clin Nutr. 1996;50:(suppl 1)  S11-S23
PubMed
Harris J, Benedict F. A Biometric Study of Basal Metabolism in Man. Washington, DC: Carnegie Institute of Washington; 1919. Publication No. 279
Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge.  Clin Chem. 1972;18(6):499-502
PubMed
US Department of Agriculture.  Composition of Foods, Agriculture Handbook No. 8: The Agriculture Research Service. Washington, DC: US Dept of Argiculture; 1992
Atkinson FS, Foster-Powell K, Brand-Miller JC. International tables of glycemic index and glycemic load values: 2008.  Diabetes Care. 2008;31(12):2281-2283
PubMed   |  Link to Article
International Standards Organisation.  ISO 26642-2010: Food Products: Determination of the Glycaemic Index (GI) and Recommendation for Food Classification. Geneva, Switzerland: International Standards Organisation; 2010
Anderson KM, Wilson PW, Odell PM, Kannel WB. An updated coronary risk profile: a statement for health professionals.  Circulation. 1991;83(1):356-362
PubMed   |  Link to Article
US Food and Drug Administration.  Guidance for industry: diabetes mellitus: developing drugs and therapeuticbiologics for treatment and prevention. http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm071624.pdf. Accessed June 12, 2012
Stratton IM, Adler AI, Neil HA,  et al.  Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study.  BMJ. 2000;321(7258):405-412
PubMed   |  Link to Article
Patel A, MacMahon S, Chalmers J,  et al; ADVANCE Collaborative Group.  Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes.  N Engl J Med. 2008;358(24):2560-2572
PubMed   |  Link to Article
Salmerón J, Manson JE, Stampfer MJ, Colditz GA, Wing AL, Willett WC. Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women.  JAMA. 1997;277(6):472-477
PubMed   |  Link to Article
Liu S, Willett WC, Stampfer MJ,  et al.  A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease in US women.  Am J Clin Nutr. 2000;71(6):1455-1461
PubMed
Meyer KA, Kushi LH, Jacobs DR Jr, Slavin J, Sellers TA, Folsom AR. Carbohydrates, dietary fiber, and incident type 2 diabetes in older women.  Am J Clin Nutr. 2000;71(4):921-930
PubMed
Jenkins DJ, Kendall CW, McKeown-Eyssen G,  et al.  Effect of a low-glycemic index or a high-cereal fiber diet on type 2 diabetes: a randomized trial.  JAMA. 2008;300(23):2742-2753
PubMed   |  Link to Article
Sacks FM, Svetkey LP, Vollmer WM,  et al; DASH-Sodium Collaborative Research Group.  Effects on blood pressure of reduced dietary sodium and the Dietary Approaches to Stop Hypertension (DASH) diet.  N Engl J Med. 2001;344(1):3-10
PubMed   |  Link to Article
Elliott P, Stamler J, Dyer AR,  et al.  Association between protein intake and blood pressure: the INTERMAP Study.  Arch Intern Med. 2006;166(1):79-87
PubMed   |  Link to Article
Papanikolaou Y, Fulgoni VL III. Bean consumption is associated with greater nutrient intake, reduced systolic blood pressure, lower body weight, and a smaller waist circumference in adults: results from the National Health and Nutrition Examination Survey 1999-2002.  J Am Coll Nutr. 2008;27(5):569-576
PubMed
Boelsma E, Kloek J. Lactotripeptides and antihypertensive effects: a critical review.  Br J Nutr. 2009;101(6):776-786
PubMed   |  Link to Article
Vermeirssen V, Van Camp J, Verstraete W. Bioavailability of angiotensin I converting enzyme inhibitory peptides.  Br J Nutr. 2004;92(3):357-366
PubMed   |  Link to Article
Chobanian AV, Bakris GL, Black HR,  et al; Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. National Heart, Lung, and Blood Institute; National High Blood Pressure Education Program Coordinating Committee.  Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure.  Hypertension. 2003;42(6):1206-1252
PubMed   |  Link to Article
Joffres MR, Reed DM, Yano K. Relationship of magnesium intake and other dietary factors to blood pressure: the Honolulu Heart Study.  Am J Clin Nutr. 1987;45(2):469-475
PubMed
DeFronzo RA, Cooke CR, Andres R, Faloona GR, Davis PJ. The effect of insulin on renal handling of sodium, potassium, calcium, and phosphate in man.  J Clin Invest. 1975;55(4):845-855
PubMed   |  Link to Article
Friedberg CE, van Buren M, Bijlsma JA, Koomans HA. Insulin increases sodium reabsorption in diluting segment in humans: evidence for indirect mediation through hypokalemia.  Kidney Int. 1991;40(2):251-256
PubMed   |  Link to Article
Chiasson JL, Josse RG, Gomis R, Hanefeld M, Karasik A, Laakso M. STOP-NIDDM Trial Research Group.  Acarbose treatment and the risk of cardiovascular disease and hypertension in patients with impaired glucose tolerance: the STOP-NIDDM trial.  JAMA. 2003;290(4):486-494
PubMed   |  Link to Article
Jenkins DJ, Mirrahimi A, Srichaikul K,  et al.  Soy protein reduces serum cholesterol by both intrinsic and food displacement mechanisms.  J Nutr. 2010;140(12):2302S-2311S
PubMed   |  Link to Article
Singh BN. Increased heart rate as a risk factor for cardiovascular disease.  Eur Heart J. 2003;5:(suppl G)  G3-G9
Link to Article
Brand JC, Snow BJ, Nabhan GP, Truswell AS. Plasma glucose and insulin responses to traditional Pima Indian meals.  Am J Clin Nutr. 1990;51(3):416-420
PubMed
 Trends in diabetes prevalence among American Indian and Alaska Native children, adolescents, and young adults: 1990-1998. www.cdc.gov/diabetes. Accessed May 15, 2012

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Supplemental Content

Jenkins DJA, Kendall CWC, Augustin LSA, et al. Effect of legumes as part of a low glycemic index diet on glycemic control and cardiovascular risk factors in type 2 diabetes mellitus: a randomized controlled trial. Arch Intern Med.. doi:10.1001/2013.jamainternmed.70.

eTable 1. Foods for the high wheat fiber diet: carbohydrate choices

eTable 2. Foods for the low glycemic index–legume diet: carbohydrate choices

eTable 3. Gastrointestinal symptoms

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