Abstract
Cardiovascular disease (CVD) is a leading cause of death among adults while associated comorbidities like diabetes further increase risks of CVD-related complications and mortality. Strategies to prevent and manage CVD risk, such as dietary change, are a key component for CVD and diabetes prevention and management. Pulses, defined as the dried edible seeds of plants in the legume family, have received attention for their superior nutritional composition as high-fiber, low–glycemic index foods and have been studied for their potential to reduce CVD and diabetes risk. Both observational and experimental studies conducted among adults with and without diabetes have provided support for pulses in their ability to improve lipid profiles, glycemic control, and blood pressure, all of which are major modifiable risk factors of CVD. These capabilities have been attributed to various mechanisms associated with the nutrient and phytochemical composition of pulses. Overall, this evidence provides support for the consumption of pulses as an important dietary strategy to reduce risk of CVD for those living with and without diabetes.
Keywords: blood pressure, cardiovascular disease, diabetes, glycemic response, lipid profile, pulses
“Pulses are a rich source of micronutrients, . . ., which contribute to their ability to improve diet quality.”
Introduction
Diabetes and Cardiovascular Disease
Diabetes is a highly prevalent disease with approximately 425 million individuals diagnosed worldwide as of 2017.1 This number is only expected to grow, with >629 million cases projected by 2045, making it an epidemic and serious public health concern.1 While both type 1 diabetes (T1D) and type 2 diabetes (T2D) are becoming increasingly prevalent, 90% of cases are T2D, which occurs primarily later in life and is linked to modifiable lifestyle-related risk factors.2 Diabetes leads to hyperglycemia, impaired insulin secretion, and insulin resistance, often causing microvascular and macrovascular complications.3 This consequently imposes serious threats to cardiovascular health, making diabetes a major risk factor for cardiovascular disease (CVD).
CVD is currently the leading cause of death worldwide, accounting for 31% of deaths in 2016.4 CVD is defined as a group of disorders that affect the heart and blood vessels, including coronary heart disease (CHD), cardiomyopathy, stroke, and heart failure. While nonmodifiable risk factors for CVD exist such as age, ethnicity, and family history, there are also major modifiable risk factors, including obesity, smoking, dyslipidemia, hypertension, and T2D.3,5
T2D can cause CVD-related complications and increase CVD mortality by 2- to 4-fold6 making it crucial to determine effective T2D prevention and management strategies. Although pharmaceuticals are often primary treatment options, adherence to a healthy lifestyle, including diet, has also been associated with lower risks of CVD incidence and CVD-related mortality in adults with T2D.7-9 For example, a prospective study of patients with diabetes or CVD showed that consumption of a high-quality diet significantly reduced CVD mortality risk by 35%.10 Within dietary components, pulses have garnered scientific interest for their role in the prevention and management of diabetes and CVD, largely due to their superior nutritional composition.11,12 This review will summarize observational and experimental studies that have examined the role of pulses in reducing CVD risk and CVD risk biomarkers in adults with diabetes.
Pulses
Pulses are defined as the dried edible seeds of plants in the legume family and include dry peas, chickpeas, lentils, and dry beans.13 Pulses are a rich source of micronutrients, including folate, potassium, iron, niacin, and riboflavin, which contribute to their ability to improve diet quality.13 As a source of protein, pulses provide 17% to 40% of protein per dry weight with high amounts of lysine, which is typically lower in other plant-based protein sources.14-16 Pulses are also considered a low glycemic index (GI) food due to their high content of dietary fiber, slowly digestible carbohydrate, and resistant starch.17 They are naturally low in fat, providing heart healthy mono- and polyunsaturated fats as well as plant sterols.14,16 Finally, pulses are a source of bioactive phytochemical compounds, including phytate, lectins, and polyphenols such as tannins, flavonoids, and phenolic acids.14,18 These superior nutritional characteristics of pulses have prompted interest and scientific study into their potential health benefits.
Pulse consumption is recommended by the American Heart Association and the Canadian Heart and Stroke Foundation as dietary components to improve cardiovascular health and to prevent CVD.19,20 Pulse consumption is also included in the clinical practice guidelines of the American Diabetes Association21 and Diabetes Canada22 for nutrition therapy and lifestyle management of diabetes. The United States Dietary Guidelines further highlight pulses as a component of a healthy eating pattern23 and the recently released Canadian Dietary Guidelines recommend more frequent consumption of plant-based protein sources, including legumes, as a foundation for healthy eating.24 Despite these recommendations and potential health benefits, pulse consumption is low in North America with studies estimating that only 8% of Americans25 and 13% of Canadians26 consume pulses on any given day. To improve public awareness of pulses and their health benefits, the United Nations declared 2016 the International Year of Pulses, highlighting the nutritional, environmental, and economical benefits that pulses provide.27
Observational Studies
Observational studies have examined pulse consumption in relation to risks of CVD and diabetes. Although some of these studies have indirectly examined pulses as part of an overall dietary pattern or as part of legumes (which can also include soybeans, peanuts, and fresh beans),28 they have provided insight into the potential health benefits of a diet containing pulses.
Pulse Consumption and CVD Risk
Pulse consumption and CVD risk has frequently been examined in the context of the Mediterranean diet, a high-quality dietary pattern that has received attention for its contribution to the management and prevention of CVD and diabetes.29,30 Characterized not only by legumes (which include pulses) but also by fruits, vegetables, nuts, fish, and olive oil, the Mediterranean diet has been recommended by the American Heart Association and the American Diabetes Association as a diet for improvement of CVD and diabetes risk.30,31
The Mediterranean diet has been associated with reduced CVD risk in a number of observational studies as well as in studies summarized in meta-analyses. In one meta-analysis of 11 prospective studies, high adherence to the Mediterranean diet was related to a 19% reduced risk of CVD (relative risk [RR] 0.81, 95% CI 0.74-0.88).32 This was confirmed in a larger meta-analysis of 20 prospective studies which also found that high adherence to the Mediterranean diet (20 g legumes per day) was associated with a reduced risk of CVD by 24% (RR 0.76, 95% CI 0.68-0.83) as well as reduced risks of CHD by 28% (RR 0.72, 95% CI 0.60-0.86), myocardial infarction by 33% (RR 0.67; 95% CI 0.54-0.83), and stroke by 24% (RR 0.76, 95% CI 0.60-0.96).33 The Mediterranean diet has also been studied for improving other CVD-related risk factors as well as mortality. For example, one prospective cohort study suggested that high adherence to the Mediterranean diet may be related to a decreased burden of carotid atherosclerotic plaque.34 Another example includes the European Prospective Investigation into Cancer and Nutrition (EPIC) study, which showed that higher adherence to the Mediterranean diet was significantly related to reduced risk of total mortality by 14% of which 9.7% was explained by legume consumption (median 9.13 g/d for males and 6.66 g/d for females).35
Observational studies have also more directly examined pulses in relation to risk of CVD and associated conditions, primarily as components of legumes or as beans specifically. For example, in the National Health and Nutrition Examination Survey (NHANES) Epidemiological Follow-up Study, consumption of legumes ≥4 times per week was associated with an 11% reduced risk of CVD (RR 0.89, 95% CI 0.80-0.98).36 More recently, the Isfahan Cohort study found that consumption of >3 servings of legumes/week was associated with a 34% reduced CVD risk (hazard ratio [HR] 0.66, 95% CI 0.45-0.98) in older but not middle-aged adults.37 Legume consumption was also identified as the most important dietary predictor among older adults in Japan, Sweden, Greece, and Australia in the Food Habits in Later Life prospective study.38 The study followed 785 adults ≥70 years old for up to 7 years and found legumes to be the only food group significantly related to survival. More specifically, results showed a 7% to 8% reduction in mortality risk for every 20 g increase in daily legume intake with (RR 0.92, 95% CI 0.85-0.99) or without (RR 0.93, 95% CI 0.87-0.99) controlling for ethnicity.38 Legume intake (including beans, black beans, lentils, peas, chickpeas, and black-eyed peas) was also examined in the Prospective Urban Rural Epidemiology (PURE) study, which followed 135 335 adults aged 35 to 70 years in 18 countries without CVD. After a median follow-up of 7.4 years, results showed that legume intake more than once per day was inversely associated with cardiovascular mortality (HR 0.72, 95% CI 0.57-0.92) and total mortality (HR 0.59, 95% CI 0.51-0.67).39
Other observational studies have focused on specific pulses such as beans and risk of CVD-related measures. For example, an analysis of NHANES data showed that bean consumption (in the past 24 hours) was associated with reduced risks of increased waist size by 41% (odds ratio [OR] 0.59, 95% CI 0.41-0.85), obesity by 39% (OR 0.61, 95% CI 0.38-0.99), and elevated systolic blood pressure by 47% (OR 0.53, 95% CI 0.29-0.96).40 Beans were also the focus of a prospective study in which consumption of one daily serving (1/3 cup) of beans by survivors of a myocardial infarction significantly reduced their risk of a recurrent myocardial infarction by 38% (OR 0.62, 95% CI 0.45-0.88).41 Another study among Japanese men and women found that 4.5 servings of beans per week was related to reduced risks of CVD by 16% (HR 0.84, 95% CI 0.74-0.95) and total mortality by 10% (HR 0.90, 95% CI 0.84-0.96).42
Meta-analyses have further summarized how pulse consumption relates to CVD risk. For example, one meta-analysis of 5 prospective cohort studies found that consumption of 4 servings of legumes per week was associated with a 14% reduced risk of total ischemic heart disease (RR 0.86, 95% CI 0.78-0.94).43 Similarly, a larger meta-analysis of 14 prospective cohort studies found that 3 to 4 servings of legumes per week was associated with a 10% reduction in risks of CVD and CHD (RR 0.90, 95% CI 0.84-0.97).44 Finally, legume consumption (amount not reported) was related to a reduced risk of all-cause mortality by 7% (RR 0.93, 95% CI 0.87-0.99) but not CVD risk in another meta-analysis of 6 prospective cohort studies.45
Pulse Consumption and Diabetes Risk
Observational studies have also investigated pulse consumption in relation to T2D risk. Similar to the CVD studies aforementioned, pulses have been indirectly studied as a component of the Mediterranean diet. A meta-analysis of 10 prospective studies that included European and non-European participants summarized a 23% reduction in T2D risk associated with high adherence to the Mediterranean diet (RR 0.77, 95% CI 0.66-0.89).46 This was confirmed in a subsequent meta-analysis of 8 prospective studies conducted in Mediterranean and Southern European countries, in which high adherence to the Mediterranean diet was associated with a 13% reduced risk of T2D (RR 0.87, 95% CI 0.82-0.93).47 Legumes were also identified, along with wholegrain cereals and fruits, to have the greatest predictive contribution to risk of 10-year incidence of diabetes with medium (OR 0.51, 95% CI 0.30-0.88) and high (OR 0.38, 95% CI 0.16-0.88) adherence to the Mediterranean diet in a large prospective study conducted in Athens.48 Another prospective cohort study by Martinez-Gonzalez et al49 showed that the highest Mediterranean diet adherence (31 g legumes per day) was related to an 83% reduced risk of T2D (incidence rate ratio [IRR] 0.17, 95% CI 0.04-0.75). The Mediterranean diet has been further studied in relation to diabetes risk among a Mediterranean population at risk for CVD in the prospective assessment of the PREvencion con DIeta MEDiterranea (PREDIMED) study that also reported a correlation between high Mediterranean diet adherence (34.6 g legumes per day) and a 35% decreased T2D incidence (HR 0.65, 95% CI 0.43-0.96).50 This study also reported a significantly lower risk of diabetes incidence (HR 0.55, 95% CI 0.32-0.93) when a half serving of legumes (30 g) substituted similar servings of foods rich in protein (eg, eggs) or carbohydrates (eg, white bread).50
Other observational studies that have focused more directly on pulses have also reported inverse associations with diabetes risk. For example, the China Health and Nutrition Survey study found that participants who consumed legumes had healthier dietary trajectory scores associated with a significantly lower HbA1c (glycated hemoglobin) by 1.64 (95% CI −3.17 to −0.11) along with a nonsignificant 14% lower risk of diabetes (OR 0.86, 95% CI 0.44-1.67).51 Furthermore, the Shanghai Women’s Health Study reported a reduced T2D risk in relation to intake of total legumes (including soy, peanuts, and pulses; RR 0.62, 95% CI 0.51-0.74) as well as non-soy and non-peanut legumes but including pulses (RR 0.76, 95% CI 0.64-0.90).52 India’s third National Family Health Survey also showed that diabetes risk among women (but not men) was reduced with daily (OR 0.71, 95% CI 0.59-0.87) and weekly (OR 0.66, 95% CI 0.54-0.80) legume consumption.53 The RODAM Study among Ghanaian migrants throughout Ghana and Europe found that higher adherence to a diet containing legumes was related to reduced T2D risk (OR 0.66, 95% CI 0.48-0.90).54 Finally, an Iranian study in Tehran showed that consumption of fiber from legumes was inversely associated with risk of metabolic syndrome (OR 0.73, 95% CI 0.53-0.99).55
In contrast, other studies have not found significant associations between legume intake and diabetes risk. For example, the prospective Third Indian Migration Study did not find a significant relationship between legume consumption and fasting blood glucose or measures of insulin resistance.56 Similarly, a meta-analysis conducted by Afshin et al43 did not find a significant association between legume consumption (4 weekly servings) and diabetes risk (RR 0.78, 95% CI 0.50-1.24) although there was a significant inverse association with total ischemic heart disease by 14% (RR 0.86, 95% CI 0.78-0.94). Overall, observational studies have provided useful information about the role of diet in CVD and diabetes risk and although inconsistencies exist, the incorporation of pulses into the diet has been shown to associate with disease risk reductions. This has rationalized the need for experimental studies to further examine the effect of pulse consumption on risk of CVD and diabetes.
Experimental Studies
Experimental studies have followed observational studies to examine the effects of pulse consumption on biomarkers of CVD risk. Pulses have been studied in different participant groups, including healthy, overweight, obese, and hypercholesterolemic adults as well as adults with insulin resistance or T2D. Studies have also examined pulses in multiple formats such as whole foods incorporated into the diet, as components of healthy dietary patterns, as part of low to moderate GI diets or as flours or extracts. Finally, multiple CVD biomarkers have been examined with some studies focusing on circulating lipids and other studies focusing on glycemic response.
Effect of Pulse Consumption on Circulating Lipids in Adults Without Diabetes
Circulating lipids are common biomarkers measured in studies that examine the effects of pulse consumption on CVD risk, with glucose and insulin also measured in some studies. Among adults of varying body weight (normal, overweight, obese), pulses have been examined as whole foods incorporated into the diet (Supplemental Table 1). The earliest study that examined the effect of beans on circulating lipids was conducted by Anderson et al57 and it found that 115 g of dried pinto and navy beans consumed as cooked beans or bean soup for 21 days significantly decreased total cholesterol, low-density lipoprotein (LDL) cholesterol, and glucose when compared with a nutrient-matched, lower-fiber control diet consumed for 7 days in 10 adult hypercholesterolemic males living on a metabolic ward. Soon thereafter, Shutler et al58 reported on the effects of consuming one can of baked beans (450 g per day) in tomato sauce for 14 days in 13 healthy males and found that total cholesterol was significantly decreased but high-density lipoprotein (HDL) cholesterol, triglycerides (TG), fasting glucose, and insulin did not change when compared with consuming spaghetti in tomato sauce. Two other early studies in healthy males found that a mixed legume diet (120 g per day) significantly decreased LDL cholesterol (but not total, very-low-density lipoprotein [VLDL] or HDL cholesterol or TG) compared with a legume-free diet for 30 to 35 days in 20 healthy males59 and for 6-7 weeks in 9 healthy males.60 More recently, studies have been conducted in overweight and obese adults such as one randomized, crossover study where consumption of 2 servings (150 g dry weight) of pulses (beans, peas, chickpeas, or lentils) incorporated into snacks, salads, soups, and meals for 2 months was compared with a pulse-free control diet in 87 overweight adults.61 Results showed that the pulses significantly reduced total cholesterol by 8.3% and LDL cholesterol by 7.9% compared with the control diet, but did not significantly affect HDL cholesterol, TG, C-reactive protein, fasting glucose, or insulin.61 Another randomized, crossover study in 47 overweight adults showed that consumption of a diet containing canned chickpeas, chickpea bread, and chickpea shortbread biscuits (2 servings, 140 g per day) for 5 weeks caused significant reductions in total cholesterol by 3.9% and LDL cholesterol by 4.6% but did not significantly change HDL cholesterol or TG when compared with a wheat-based diet (wholemeal bread, high-fiber wheat breakfast cereals, and shortbread biscuits).62 A similar subsequent study also found that the same 5-week chickpea intervention consumed by 27 overweight adults significantly decreased total cholesterol by 0.25 mmol/L and LDL cholesterol by 0.20 mmol/L but did not significantly change HDL cholesterol, TG, glucose, or insulin compared to the same wheat-based control diet.63 Finally, the effect of incorporating 5 cups of pulses per week (lentils, chickpeas, yellow split peas, navy beans) into the diet of 40 overweight and obese adults with metabolic risk factors for 8 weeks on fasting and postprandial biomarkers was examined in another study.64 Results showed that the pulse diet significantly increased HDL cholesterol by 4.5% and C-peptide by 12.3% but did not affect total or LDL cholesterol, TG, glucose (fasting or postprandial), fasting insulin, HbA1c or C-reactive protein, in comparison with an energy-restricted pulse-free diet.64 Postprandial effects of the pulse diet on insulin were sex dependent with insulin area under the curve (AUC) decreased in females and increased in males.64
Effect of pulses on serum lipids have further been examined in experimental studies as components of various dietary patterns, such as in a randomized, crossover study of 46 overweight women who consumed a 4-week diet rich in brown beans (86 g/day), chickpeas (82 g/day), and kernel-based barley products or a control diet of similar macronutrient composition without legumes or barley.65 Results showed that the legume-based diet significantly decreased serum total and LDL cholesterol, apolipoprotein B, diastolic blood pressure, the Framingham cardiovascular risk estimate and γ-glutamyl transferase, but did not significantly affect HDL cholesterol, TG, apolipoprotein A1, glucose, insulin or C-reactive protein.65 Another study, using a parallel-arm design, examined the effect of a diet based on the New Zealand National Heart Foundation guidelines without or with pulses (2 servings per day) and wholegrain foods (4 servings per day) for 18 months in 108 obese adults as part of a weight-loss program.66 Results showed that although the inclusion of pulses and wholegrain foods did not significantly change body weight (or glucose or blood pressure), it did significantly decrease total and LDL cholesterol, and waist circumference66. Weight loss was also examined, this time with 30% caloric restriction, in 30 overweight or obese adults using a parallel-arm design with legumes (4 weekly servings [160-235 g] cooked lentils, chickpeas, peas, or beans) or without legumes (control).67 Results showed that the caloric-restricted legume diet caused a significant decrease in body weight and BMI, as well as total and LDL cholesterol, complement 3, C-reactive protein, and systolic blood pressure; however, it did not significantly affect HDL cholesterol, TG, glucose, insulin, or tumor necrosis factor–α (TNF-α).67 Another study included 123 obese adults (some with T2D) who consumed pulses (½ cup per day for the first week followed by ½ cup at each meal) as part of a high-fiber, bean-rich diet for 16 weeks and results showed significant decreases in total and LDL cholesterol in comparison with a control low-carbohydrate diet, although no significant differences were found for body weight, HDL cholesterol, TG, glucose, or HbA1c.68 Beans were also the focus in a study by Finley et al,69 which examined the effects of daily consumption of a bean entrée (½ cup (130 g) of canned pinto beans) or an isocaloric chicken soup entrée for 12 weeks in 2 groups of participants including 40 obese adults with pre–metabolic syndrome and 40 normal or overweight, healthy adults. Results showed that the bean entrée significantly decreased total, LDL and HDL cholesterol in both participant groups but did not significantly affect VLDL cholesterol, TG, or glucose in either participant group, all compared with the isocaloric chicken soup entrée.69
In contrast to these studies, other studies have not found significant improvements in serum lipids from pulse consumption. For example, no significant changes were observed in total, LDL or HDL cholesterol, TG, or glucose when obese men (n = 35) consumed legumes 4 days per week for 8 weeks; however, systolic blood pressure significantly decreased compared with a legume-free control diet.70 Similarly, serum lipids were not significantly different between 8 weeks consumption of ½ cup of cooked beans or legumes/day (as part of a high-fiber, high-carbohydrate, energy-restricted diet) and a moderately high-protein, energy-restricted diet in 83 overweight or obese women, although body weight, total body fat, and diastolic blood pressure significantly decreased more with the moderately high-protein diet.71 Finally, a parallel-arm intervention study of 5 weekly meals with or without 750 mL of pulses for 16 weeks did not significantly affect circulating lipids, glucose, blood pressure, or inflammatory biomarkers in 134 overweight or obese women with components of metabolic syndrome.72 Overall, these studies that have included pulses as components of various dietary patterns not only reveal inconsistent results for serum lipids but also vary in their study designs, participants, and specific treatments examined.
In addition to normal weight, overweight, and obese adults, the effects of pulse consumption on circulating lipids has also been assessed in adults who are hypercholesterolemic and/or have impaired glucose tolerance (Supplemental Table 1). For example, an early study showed that consumption of 90 g of cooked or raw field bean flour for 30 days mixed into various foods significantly decreased serum total and VLDL cholesterol, TG, total cholesterol/HDL cholesterol, LDL cholesterol/HDL cholesterol as well as glucose and insulin while increasing HDL cholesterol and glucagon compared with a control flour in 40 adult males with borderline-high or high cholesterol.73 LDL cholesterol was also significantly decreased by the cooked and raw bean flour compared with the control flour, however only in the participants with high cholesterol.73 Another study also focused on beans using a randomized, crossover design in 23 hypercholesterolemic adults and showed that ½ cup of baked navy beans/day for 8 weeks significantly reduced total cholesterol by 5.6% but did not significantly affect LDL or HDL cholesterol, TG, glucose, insulin, HbA1c, homeostatic model assessment for insulin resistance (HOMA-IR), or C-reactive protein when compared to ½ cup of canned carrots.74 Another randomized, crossover study in 23 hypercholesterolemic obese adults investigated the effect of yellow pea flours in the form of whole yellow pea flour muffins or fractionated yellow pea flour muffins (50 g dry yellow peas per day) on serum lipids and glucose, insulin, and postprandial blood glucose compared with control wheat flour muffins, each consumed for 4 weeks.75 Results showed that both forms of the yellow pea flour muffins significantly reduced insulin and HOMA-IR, but did not significantly change lipid profiles compared to the control.75 Other studies have examined pulse consumption in adults with impaired glucose tolerance including one by Winham et al,76 who studied 16 adults with mild insulin resistance who consumed ½ cup of pinto beans, black-eyed peas, or carrots per day for 8 weeks using a randomized, crossover study design. Although the pinto beans significantly reduced total and LDL cholesterol compared with the carrot control, the same was not found for the black-eyed peas.76 Another study by Zhang et al77 was also conducted in insulin-resistant (n = 28) and insulin-sensitive (n = 36) men who consumed a daily legume diet (250 g cooked pinto, navy, kidney, lima, and black beans) or a healthy American diet as a control for 4 weeks each. The legume diet caused significant reductions in total and LDL cholesterol compared with the control diet in all participants with more effects in the insulin sensitive (decreased total cholesterol, LDL cholesterol, total cholesterol/HDL cholesterol, and LDL cholesterol/HDL cholesterol) than the insulin resistant (decreased HDL cholesterol and TG/HDL cholesterol) participants.77
Overall, experimental studies that have examined the lipid-lowering effects of pulses as whole foods or as part of dietary patterns in adults of varying body weight status and/or with hypercholesterolemia and/or impaired glucose tolerance have provided varying support for reduced risk of CVD. Most of these studies also included fasting glucose and/or insulin in their outcome measures; however, other studies have focused on glycemic response in the fasting or more often postprandial state as their primary outcomes.
Effect of Pulse Consumption on Glycemic Response in Adults Without Diabetes
Experimental studies have frequently examined the effects of pulses on fasting or postprandial glycemic response as their primary outcome measure. These studies are relevant since hyperglycemia can increase CVD risk by causing endothelial dysfunction and microvascular damage78 while control of postprandial blood glucose can help prevent and manage both diabetes and CVD.79,80 As mentioned, the majority of the previously summarized experimental studies that focused on circulating lipids also included measures of fasting glucose and/or insulin57,58,61,63-77; however only a few showed significant improvements.57,64,73,75 The following studies have examined the effects of consuming pulses in multiple formats (whole, pureed, powdered, pulse flours, pulse fractions) on fasting and/or postprandial glycemic response as their primary outcome.
In normal and overweight adults, pulses have been examined for their glycemic effects as whole foods and compared with carbohydrate controls (Supplemental Table 2). The first comprehensive comparison study of this kind was completed by Jenkins et al81 in which groups of 5-10 healthy adults consumed 8 different pulses and 24 common carbohydrate foods in 50 g available carbohydrate (AC) portions. Postprandial glycemic response showed that blood glucose peak rise and AUC were significantly lower for the pulses compared to the other carbohydrate foods. Another study by Nestel et al82 focused on chickpeas and examined their acute (3 hours) and chronic (6 weeks) effects in 19 overweight women. The acute study showed that chickpeas significantly decreased postprandial glucose at 30 and 60 minutes as well as insulin and HOMA at 120 minutes, compared to wheat cereal or white bread. However, the chronic study did not show any effects of the chickpea diet (140 g canned chickpeas, and bread and biscuits baked with 30% chickpea flour) on fasting or postprandial glucose, insulin, or HOMA compared with the wheat-based diet (wheat cereal, and bread and biscuits made from whole-grain flour).82
Whole pulses have also been studied for their glycemic effects when consumed in combination with high-GI foods such as in one study by Mollard et al,83 who found chickpeas, lentils, and navy beans (44% of energy) in a pasta meal significantly decreased glucose AUC compared to a control pasta meal in 24 healthy males. Postprandial glucose AUC was also significantly decreased when chickpeas (½ cup) were consumed with white rice (½ cup) compared to white rice alone in 12 healthy women.84 The same study also showed significantly decreased glucose at 60 and 90 minutes when chickpeas or black beans were consumed and at 120 minutes when black beans were consumed (all combined with white rice) compared with white rice alone.84 Another study focused on the replacement of AC in rice or potatoes with lentils on postprandial glycemic response in 24 healthy adults.85 Results showed that glucose maximum concentration (Cmax) and AUC were significantly decreased by replacing half of the AC from rice or potato with large green (P = 0.057 for rice AUC), small green and red lentils; and insulin Cmax and AUC were significantly decreased by replacing half of the potato AC with all 3 lentil types.85
Pulses processed in various ways (ie, boiled, pureed, powdered, flour, fractions) have also been examined for their glycemic effects in healthy adults (Supplemental Table 2). An early study investigated the acute effect of a breakfast meal containing red lentils processed in 4 ways (boiled for 20 or 60 minutes; or boiled for 20 minutes and then blended; or boiled for 20 minutes, blended and then dried and ground into a powder) compared to a white bread control, all containing 50 g AC.86 Results showed that compared to the white bread, red lentils decreased blood glucose response in all formats except as a dried powder, which may be due to a more rapid carbohydrate release.86 A decade later, another study focused on the effects of processing, this time with red kidney beans (boiled or autoclaved or precooked flour with cell-enclosed starch or precooked flour with free starch) as well as lentils (as a precooked flour with free starch) and a control white wheat bread, each providing 30 g AC.87 Results showed that processing was not relevant since all red kidney bean treatments as well as the lentils significantly reduced peak glucose compared to the control. Peak insulin was also significantly reduced by all red kidney bean treatments (significantly more for the boiled) compared to the control and the lentils.87 Another randomized, crossover study that focused on powdered spray-dried pulses (100 g of chickpeas, large green lentils or whole green peas) found no significant effects on glucose, insulin or HOMA-IR compared with powdered potato flakes when consumed for 28 days by 21 healthy males.88 Pulses (navy beans, lentils, chickpeas) in their whole, pureed, and powdered forms were also investigated for their acute glycemic effects in three randomized, crossover studies of 12 to 17 healthy males by Anderson et al.89 Results showed that the processed forms did not affect the ability of navy beans to significantly decrease postprandial peak glucose or for the lentils and chickpeas to significantly decrease postprandial (0-120 minutes) mean glucose, all compared with the control whole wheat flour.89 Another acute study focused on chickpea hummus in 3 doses (28, 112, and 259 g) alone or with 50 g of AC from white bread in 10 healthy adults.90 Results showed that only hummus alone (not combined with white bread) significantly reduced postprandial glucose AUC at all 3 doses and insulin AUC at the 28 and 112 g doses, compared with the white bread control.90
Pulses as components of meals have also been investigated for their glycemic responses such as in one study that compared a breakfast burrito containing whole lentils (84.6 g), blended lentils (84.6 g) or no lentils in 12 healthy adults.91 Blood glucose average and AUC were significantly decreased by the blended but not the whole lentils, compared with the lentil-free burrito, indicating a differential effect related to processing.91 Another acute, randomized, crossover study looked at the effect of chickpeas in a bread made from 25% or 35% chickpea flour compared with whole wheat bread and white bread in 13 healthy females.92 Glucose Cmax was significantly decreased by both chickpea breads compared with white bread while glucose AUC was decreased by the 35% chickpea bread compared with both whole wheat and white bread and by the 25% chickpea bread compared with white bread.92 Chickpeas were also examined in breads made from chickpea flour or extruded chickpea flour in replacement of wheat flour and compared with a white bread control in 11 healthy adults.93 Glucose AUC did not significantly change but glucose was decreased at 90 minutes by the chickpea flour bread and at 120 minutes by the extruded chickpea flour bread, and insulin AUC was increased by the chickpea flour bread, all compared with the white bread.93
In addition to providing acute glycemic benefits, pulses have been shown to exert glycemic benefits that persist even after a subsequent meal to indicate a second meal effect.94 For example, the aforementioned Anderson et al89 study included an ad libitum pizza meal in their study design and found that consuming whole navy beans in tomato sauce before the meal significantly reduced postprandial mean glucose after the meal, compared with whole wheat flour in tomato sauce in 17 healthy males. Smith et al95 also included an ad libitum pizza meal in their study of 19 healthy males who consumed tomato soup with yellow pea fiber (10 g or 20 g), yellow pea protein (10 g or 20 g) or a control tomato soup. Postprandial glucose before the pizza meal (0-30 min) was significantly decreased by the 10 g and 20 g yellow pea protein but not the fiber treatments and postprandial glucose after the pizza meal (50-120 min) was decreased by the 20 g yellow pea protein compared with the 10 g yellow pea fiber and the control tomato soup.95 Peas were examined in another study of 15 healthy males that also included an ad libitum pizza meal and showed that consumption of pea protein (10 g) combined with pea hull fiber (7 g) and yellow peas alone (406 g), all in tomato sauce, significantly reduced pre-pizza meal postprandial glucose AUC (compared with both control noodles and the pea fiber alone in tomato sauce) and the yellow peas significantly reduced postprandial glucose after the meal at 155 min (compared with the pea hull fiber).96 Finally, a second meal-type effect was demonstrated by Nilsson et al97 who showed that consuming brown beans (compared with white wheat bread, 35 g available starch) in an evening meal significantly decreased glucose and insulin AUC after a standardized breakfast meal the following morning.
Overall, these studies in adults without diabetes provide evidence that pulses in multiple formats, including whole pulses, boiled pulses, pureed pulses, powdered pulses, pulse flours, and pulse fractions alone or in mixed meals can improve the glycemic response, which in turn can contribute toward a reduction in CVD risk.
Effect of Pulse Consumption on Serum Lipids and Glycemic Response in Adults With Diabetes
The effects of pulse consumption on circulating lipids and glycemic response have also been investigated in adults living with diabetes, as part of a low- to moderate-GI diet, as components of healthy dietary patterns or as whole foods incorporated into the diet (Supplemental Table 3). Among the studies that examined pulses as part of low- to moderate-GI diets, Rizkalla et al98 used a randomized, crossover design to compare the effects of a pulse-containing (lentils, haricot beans, chickpeas, mung beans) and low-GI (GI < 45) diet to a high-GI (GI > 60) diet for 4 weeks each in 12 obese males with T2D. Results showed that the pulse-containing, low-GI diet caused significant reductions in total and LDL cholesterol, free fatty acids, apolipoprotein B and plasminogen activator inhibitor-1 (PAI-1) compared with the high-GI diet.98 The pulse-containing, low-GI diet also significantly decreased fasting and postprandial glucose AUC and HbA1c, and improved whole-body peripheral insulin sensitivity (measured through a euglycemic-hyperinsulinemic clamp).98 In a larger study, Jenkins et al99 used a parallel-arm study design to examine the effect of consuming at least 1 cup of legumes (beans, chickpeas, lentils)/day in a low-GI diet compared to a high–wheat fiber control diet for 3 months in 121 overweight or obese adults with T2D. Results showed that the low-GI pulse diet significantly reduced total and HDL cholesterol, TG, and CHD risk score as well as fasting glucose, HbA1c, systolic and diastolic blood pressure, all compared with the control diet.99 In another study, Jimenez-Cruz et al100 assessed the effects of consuming pinto beans at breakfast and dinner as part of a moderate-GI (GI = 60), higher dietary fiber (53 g per day) diet, compared with a high-GI (GI = 72), lower dietary fiber (30 g per day) diet for 3 weeks in 8 adults with T2D. Results showed that the pinto bean–containing, moderate-GI, higher dietary fiber diet caused significant reductions in total and LDL cholesterol but did not affect HDL cholesterol, TG, or glucose when compared with the high-GI, lower dietary fiber diet.100 These studies reinforce the idea that pulse consumption in low-GI diets can improve serum lipids and glycemic response in adults with diabetes.
Pulses have also been examined in adults with T2D as components of other healthy dietary patterns. For example, an early study by Simpson et al101 used a randomized, crossover design to compare the effects of a 6-week diet high in leguminous and cereal fiber (with the legumes mainly from dried red kidney, haricot, and butter beans) to a control low-carbohydrate diet in 27 adults with diabetes (18 T2D, 9 T1D). Results showed that the leguminous diet significantly decreased total cholesterol in all participants and LDL cholesterol in the T2D participants, and increased HDL cholesterol in the T1D participants and the HDL cholesterol/LDL cholesterol ratio in the T2D participants.101 In another randomized, crossover study of 31 adults with T2D, Hosseinpour-Niazi et al102 assessed the consumption of a Therapeutic Lifestyle Change (TLC) diet with or without pulses for 8 weeks. Inclusion of pulses in the TLC diet involved replacing 2 servings of red meat with ½ cup of cooked legumes (lentils, chickpeas, peas, or beans) for 3 days each week. Results showed that the TLC diet with pulses caused significant reductions in LDL cholesterol and TG (but not total cholesterol) as well as glucose and insulin compared to the TLC diet without pulses.102 Another study by Barnard et al. (2006)103 focused on the effects of a vegan diet (n = 49) containing legumes, fruits, and grains in comparison with the American Diabetes Association control diet (n = 50) for 22 weeks in adults with T2D. Results showed no significant differences in circulating lipids; however, a subgroup analyses showed significantly decreased total and LDL cholesterol among participants whose lipid-controlling medications did not change during the study in the vegan diet (n = 39) and in the control diet (n = 41) and significantly decreased HbA1c among participants whose diabetes medications did not change during the study in the vegan diet (n = 24) and in the control diet (n = 33).103
Finally, pulses have been examined for their lipid lowering effects in adults with T2D as whole foods incorporated into the diet. For example, Shams et al104 conducted a randomized, crossover study in 30 adults with T2D who consumed cooked lentils (50 g) as a breakfast meal, which was found to significantly reduce total cholesterol and glucose but not LDL cholesterol or TG when compared with a control breakfast with bread and cheese.
The glycemic response from pulses has also been studied in adults with diabetes such as in an early study that compared lentils with 3 other carbohydrates (potato, rice, and spaghetti) in a conventional mixed meal in 8 adults with T2D.105 The lentil meal significantly reduced postprandial glucose and insulin compared with the potato but not compared with the rice or spaghetti meal.105 Another study in 9 adults with T2D demonstrated that yellow peas consumed in a mixed meal significantly decreased glucose and insulin (P = .0514) AUC when compared with potatoes or a combination of yellow peas and potatoes.106 Finally, Thompson et al107 studied the acute glycemic effect of 50 g AC from red kidney, black, and pinto beans combined with ½ cup of white rice in 17 adults with T2D. When compared with a control white rice meal, all 3 bean meals significantly reduced postprandial glucose at 90, 120, and 150 minutes and the black and pinto beans significantly reduced glucose AUC.107
Overall, these 9 studies in adults with T2D have examined the effects of pulses as part of a low-GI diet, as components of other healthy dietary patterns and as whole foods on circulating lipids, glycemic response, and other CVD risk biomarkers. Results provide support that pulses incorporated into the diet can improve markers of CVD and diabetes risk therefore providing evidence for a feasible dietary strategy.
Meta-analyses of the Effects of Pulses on Serum Lipids and Glycemic Response
Meta-analyses have strengthened the literature on the effect of pulses on circulating lipids, glycemic response and other CVD risk factors by combining data from multiple studies (Supplemental Table 4). For example, one meta-analysis from the Cochrane Library combined data from 11 randomized controlled trials (RCTs), including 52 044 healthy, or hypercholesterolemic, overweight, or obese adults with hypertension, or sedentary adults with metabolic syndrome, or adults with high risk of colorectal cancer.108 The studies, which ranged in duration from 3 months to 8 years, were included if they examined at least 2 components of the Mediterranean diet (high monounsaturated/saturated fat ratio [olive oil]; high consumption of legumes; fish; grains and cereals; and/or fruits and vegetables; moderate consumption of milk and dairy products; low to moderate consumption of red wine; and/or low consumption of meat and meat products).108 Results showed overall significant reductions in total cholesterol by 0.16 mmol/L (95% CI −0.26 to −0.06), LDL cholesterol by 0.07 mmol/L (95% CI −0.13 to −0.01) and a further significant reduction in total cholesterol by 0.23 mmol/L (95% CI −0.27 to −0.20) in a subgroup analysis of studies that specifically described the intervention as a Mediterranean diet.108
Another large meta-analysis combined data from 50 studies (35 RCTs, 13 cross-sectional and 2 prospective studies) that examined the effects of a Mediterranean diet of varying regimens in 534 906 healthy or overweight or obese and/or hypercholesterolemic adults with or without T2D.109 For the experimental studies, there were significant reductions in waist circumference by 0.42 cm (95% CI −0.82 to −0.02), TG by 0.07 mmol/L (95% CI −0.12 to −0.02), systolic blood pressure by 2.35 mm Hg (95% CI −3.51 to −1.18), diastolic blood pressure by 1.58 mm Hg (95% CI −2.02 to −1.13), blood glucose by 0.22 mmol/L (95% CI −0.32 to −0.11) and HOMA-IR by 0.45 (95% CI −0.74 to −0.16) as well as a significant increase in HDL cholesterol by 0.03 mmol/L (95% CI 0.01-0.05).109 For the observational studies, high adherence to the Mediterranean diet was significantly related to decreased TG by 0.11 mmol/L (95% CI −0.18 to −0.04), blood glucose by 0.22 mmol/L (95% CI −0.35 to −0.09), HOMA-IR by 0.87 (95% CI −1.15 to −0.59) and increased HDL cholesterol by 0.06 mmol/L (95% CI 0.03-0.09).109
Pulse consumption has also been more directly examined in meta-analyses such as one that combined 11 RCTs that included a total of 187 healthy, hyperlipidemic, hypercholesterolemic adults or adults with T2D. Results showed that consumption of 46 to 150 g pulses per day significantly decreased total cholesterol by 7.2% (95% CI −5.8% to −8.6%), LDL cholesterol by 6.2% (95% CI −2.8% to −9.5%), and TG by 16.6% (95% CI −11.8% to −21.5%).110 Another meta-analysis of 10 RCTs including 268 participants with normal, borderline-high, or high cholesterol showed similar results, reporting that consumption of 80 to 440 g pulses per day for 3 to 8 weeks significantly decreased total cholesterol by 0.31 mmol/L (95% CI −0.42 to −0.19), LDL cholesterol by 0.21 mmol/L (95% CI −0.30 to −0.12), and TG by 0.21 mmol/L (95% CI −0.43 to 0.002; P = .05) and increased HDL cholesterol by 0.02 mmol/L (95% CI −0.42 to 0.09; P = .05).111
More recently, a meta-analysis that focused on pulses combined data from 26 RCTs with 1037 hyperlipidemic or normolipidemic adults with and without diabetes, found that consuming a median of 130 g pulses per day in either a whole food, a flour incorporated into baked foods or a combination of the 2 resulted in a 5% reduction in LDL cholesterol (−0.17 mmol/L; 95% CI −0.25 to −0.09), but not in non-HDL cholesterol or apolipoprotein B.112
Finally, the glycemic benefits of pulse consumption have also been summarized through a meta-analysis by Sievenpiper et al,113 which combined data from 41 RCTs of adults with or without diabetes that examined dietary pulses alone (11 RCTs, n = 253), pulses as part of a low-GI diet (19 RCTs, n = 762) and pulses as part of a high-fiber diet (11 RCTs, n = 641). Results showed that pulses alone (average 152.1 g per day) significantly decreased fasting glucose (standardized mean difference [SMD] of 0.82 mmol/L; 95% CI −1.36 to −0.27) and insulin (SMD of 0.49 mmol/L; 95% CI: −0.93 to −0.04).113 Pulses as part of a low-GI diet significantly decreased glycated proteins (SMD of 0.28; 95% CI −0.42 to −0.14) and pulses as part of a high-fiber diet significantly decreased fasting glucose (SMD of 0.32; 95% CI −0.49 to −0.15) and glycated proteins (SMD of 0.27; 95% CI −0.45 to −0.09).113
Collectively, these meta-analyses provide extensive combined evidence to support a role for pulses as components of the Mediterranean diet or as whole foods incorporated in the diet in reducing CVD risk by improving lipid profiles and glycemic control.
Mechanisms of Action of How Pulses Can Improve Circulating Lipids and Glycemic Response
The lipid-lowering effects of pulses have been attributed to multiple pulse components, including dietary fiber, resistant starch, protein, and bioactive phytochemicals. For example, the soluble and insoluble fiber content of pulses has been proposed to disrupt enterohepatic circulation, preventing the reabsorption of bile acids by binding them in the intestinal lumen and promoting their excretion.114 This can then cause an increase in hepatic production and cholesterol saturation of bile acids, which can decrease circulating cholesterol. This idea is supported by early human studies in which consumption of 120 g legumes per day by healthy males for 30 to 35 days59 or 6 to 7 weeks60 was shown to decrease LDL cholesterol and increase cholesterol saturation of bile, hepatic cholesterol synthesis, biliary lipid secretion, and fecal acidic sterols.59,60
The resistant starch content of pulses may also contribute to the ability of pulses to improve circulating lipids through fermentation by colonic bacteria into short chain fatty acids such as propionate and butyrate, which in turn can inhibit endogenous cholesterol synthesis.115 Propionate has also been shown to inhibit fatty acid synthesis in cell culture and animal models116,117; however, specific mechanisms have not been extensively studied in humans.
Pulse proteins have also been examined for their effects on circulating lipids. For example, glutamine, an amino acid high in fava beans, peas, and lentils, can increase postmeal energy expenditure and fat oxidation, contributing to a reduction in serum lipids.118 In addition, legume 7S globulin, a storage protein in pulses that was isolated from cowpeas and adzuki beans and fed with a high-cholesterol diet to rodents caused reductions in non-HDL cholesterol by increasing fecal fat and cholesterol excretion.119,120 Similarly, the 7S globulin of soybeans reduced apolipoprotein B synthesis in HepG2 cells.121
Finally, bioactive phytochemical components of pulses show potential to influence lipid profiles. For example, phenolics present in extracts of adzuki bean and moth beans inhibited pancreatic lipase, an enzyme needed for TG absorption.122 Pancreatic lipase was also inhibited by flavonoids identified as the most common phenolic in 20 different lentil cultivars.123 A recent study also provides support for the role of pulse phytochemicals with their examination of whole pinto beans and a supplement of pinto bean hulls (markedly higher in total phenolic content) in a saturated fat–rich diet on cholesterol metabolism and molecular mechanisms in a hamster model.124 Results showed that both the whole pinto beans and pinto bean hulls significantly decreased non-HDL cholesterol compared with control (by 31.9% and 53.6%, respectively) and also caused hepatic mechanistic changes, including lower liver cholesterol, higher fecal cholesterol, and higher expressions of cholesterol metabolic enzymes.124
The glucose-lowering effects of pulses, like their lipid-lowering effects, have also been attributed to numerous pulse components including dietary fiber, resistant starch, and phytochemicals. For example, pulse fiber has been shown to reduce postprandial glycemic response by delaying carbohydrate digestion and glucose absorption.114 Pulse-derived fibers also stimulate cholecystokinin secretion, a hormone that also slows gastric emptying and can delay glucose absorption.125 The resistant starch content of pulses may also be responsible as demonstrated in healthy rats who had significantly decreased non-fasting plasma glucose after being fed mung bean starch compared with high-GI wheat starch for 5 weeks.126 The idea of a slow release by the carbohydrates in legumes has early support from studies by Jenkins et al127,128 that demonstrate an improved second meal effect and the relevance of a prolonged rate of glucose absorption to glucose and insulin metabolism. Finally, phenolic compounds in pulses may affect starch digestion by directly interacting with starch or inhibiting starch-digesting enzymes. For example, Zhang et al123 found that pulse flavonoids inhibit α-glucosidase, which can delay glucose absorption. Inhibition of α-glucosidase was also demonstrated in another study by extracts of mung, moth, and adzuki beans.122
Together, pulse fibers, resistant starch, proteins, and bioactive compounds all have the potential to contribute to the lipid-lowering and glycemic benefits of pulses. These have been predominantly studied in cell culture and animal models warranting further study among humans to improve understanding of the lipid-lowering and glucose-lowering mechanisms of pulses.
Effect of Pulse Consumption on Blood Pressure
In addition to lipids and glycemic response, blood pressure has been recognized as an important biomarker of CVD. Hypertension, defined by chronic elevations in blood pressure, is considered one of the strongest risk factors of CVD129 and 73.6% of American adults with diabetes are hypertensive.130 Research suggests that controlled blood pressure significantly reduces the risk for macrovascular effects and all-cause mortality.131
Pulses have been examined in multiple studies for their potential in reducing blood pressure, as was summarized in a meta-analysis of 8 RCTs that were ≥3 weeks in duration and conducted in healthy (n = 103), overweight or obese (n = 215) adults, as well as adults with metabolic syndrome (n = 119) and diabetes (n=121) with and without hypertension132 (Supplemental Table 5). Results summarized that a median dose of 162 g of pulses per day (in whole or powdered form) caused significant reduction in systolic (but not diastolic) blood pressure by 2.25 mm Hg (95% CI −4.22 to −0.28) and mean arterial blood pressure by 0.75 mm Hg (95% CI −1.44 to −0.06).132 While studies focusing on pulses and blood pressure as a primary outcome are limited, the promising results from this meta-analysis rationalize the need for further study on pulses and blood pressure as a means to reduce CVD risk.
Mechanisms of Action of How Pulses Can Reduce Blood Pressure
The blood pressure–lowering effects of pulses could be due to various components of pulses such as phytochemicals, dietary fiber, potassium, and magnesium. A polyphenol extract from lentils was shown to prevent angiotensin-II-induced hypertension in a rat model by decreasing intracellular reactive oxygen species and mean artery pressure.133 Another lentil study used a metabolomics approach to show an attenuation of blood pressure in spontaneously hypertensive rats that was attributed to 7 specific metabolites; 2 of which were shown to modulate nitric oxide synthase activity.134 Although not directly studied, the dietary fiber, potassium, and magnesium content of pulses may also help reduce blood pressure,120 identifying a need for further mechanistic studies to support this promising biological effect of pulses.
Summary
Observational and experimental studies have shown the potential for pulses, as components of dietary patterns or alone, to reduce CVD-related biomarkers and CVD risk. While inconsistencies exist, studies are heterogenous in their design, duration, participant characteristics, and treatments, which may bring about these variable results. This suggests the continued need for well-designed studies to further elucidate the benefits of pulse consumption in mitigating risks of CVD in adults with diabetes. Similarly, while the disease risk reducing potential of pulses has been attributed to numerous pulse properties, conducting human-based mechanistic studies may provide insight into the physiological role that pulses can play in disease risk reduction. In conclusion, pulses have been shown to influence lipid profiles, glycemic control, and blood pressure, therefore providing a potential dietary tool for disease risk reduction, which may be particularly beneficial among adults with diabetes.
Supplemental Material
Supplemental material, AJLM-19-0104-Table_1-Lipids-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Supplemental material, AJLM-19-0104-Table_2-Glycemic-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Supplemental material, AJLM-19-0104-Table_3-LipidsGlycemic_in_T2D-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Supplemental material, AJLM-19-0104-Table_4-MetaAnalyses-LipidsGlycemic-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Footnotes
Declaration of Conflicting Interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical Approval: Not applicable, because this article does not contain any studies with human or animal subjects.
Informed Consent: Not applicable, because this article does not contain any studies with human or animal subjects.
Trial Registration: Not applicable, because this article does not contain any clinical trials.
Supplemental Material: Supplemental material for this article is available online.
ORCID iD: Alison M. Duncan
https://orcid.org/0000-0003-4748-6645
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Supplementary Materials
Supplemental material, AJLM-19-0104-Table_1-Lipids-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Supplemental material, AJLM-19-0104-Table_2-Glycemic-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Supplemental material, AJLM-19-0104-Table_3-LipidsGlycemic_in_T2D-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
Supplemental material, AJLM-19-0104-Table_4-MetaAnalyses-LipidsGlycemic-REVISED-2020.03.12 for The Role of Pulses in Cardiovascular Disease Risk for Adults With Diabetes by Patricia K. Lukus, Katarina M. Doma and Alison M. Duncan in American Journal of Lifestyle Medicine
