Vegetarian Diets in the Prevention and Management of Diabetes and Its Complications Roman Pawlak

■ IN BRIEF Epidemiological studies have found a lower prevalence of type 2 diabetes among vegetarians compared to nonvegetarians. This reduced risk is likely a function of improved weight status, higher intake of dietary fiber, and the absence of animal protein and heme iron in the diet. Interventional studies have shown that vegetarian diets, especially a vegan diet, are effective tools in glycemic control and that these diets control plasma glucose to a greater level than do control diets, including diets traditionally recommended for patients with diabetes (e.g., diets based on carbohydrate counting). Vegetarian diets are associated with improvement in secondary outcomes such as weight reduction, serum lipid profile, and blood pressure. Studies indicate that vegetarian diets can be universally used in type 2 diabetes prevention and as tools to improve blood glucose management.

iet plays an important role diets exclude all meats and animal in diabetes prevention and products. Dmanagement. According to There are additional variations the American Diabetes Association within each of the above categories. (ADA), a variety of eating patterns For example, some individuals who are acceptable for the management consider themselves vegans do not eat of diabetes (1). The impacts of veg- honey or other bee products, whereas etarian eating patterns on the risk of others just limit their dietary exclu- type 2 diabetes, glycemic control, and sions to dairy products and eggs. In prevention of diabetes comorbidities addition, plant-based diets are an have been the focus of several recent eating pattern that mainly includes research studies. unrefined foods of plant origin but Vegetarian diets encompass several may include small amounts of meats, diet types, including semi-vegetarian mainly white meat. (flexitarian), pesco-vegetarian, Vegetarian diets have been asso- lacto-vegetarian, ovo-vegetarian, ciated with improvements in many lacto-ovo-vegetarian, vegan, and raw- modifiable heart disease risk factors, food vegan diets. Semi-vegetarians including serum lipid profile, serum East Carolina University–Nutrition Science, include small amounts of meat, glucose concentration, and systolic Greenville, NC mainly from fish and poultry. and diastolic blood pressure (2–5). Corresponding author: Roman Pawlak, Pesco-vegetarians ingest some fish, Consequently, vegetarians have been [email protected] in addition to foods of animal and shown to have a lower risk of hospital- https://doi.org/10.2337/ds16-0057 plant origin. Milk and dairy prod- ization or death from ischemic heart ucts are ingested by lacto-vegetarians; disease (6). Furthermore, vegetarian ©2017 by the American Diabetes Association. Readers may use this article as long as the work ovo-vegetarians include eggs; and lacto- diets have been shown to regress is properly cited, the use is educational and not ovo-vegetarians ingest both dairy arterial stenosis among heart dis- for profit, and the work is not altered. See http:// creativecommons.org/licenses/by-nc-nd/3.0 products, including milk, and eggs. ease patients (7). These diets are also for details. Individuals who adhere to vegan associated with reduced risk of other

82 SPECTRUM.DIABETESJOURNALS.ORG pa w l a k health conditions, including type 2 women (OR 0.25 [95% CI 0.15– Diabetes Association. The trial lasted diabetes, some types of cancer, diver- 0.42] for diabetes and OR 0.73 [95% for 12 weeks. Although A1C signifi- ticular disease, and cataracts (8–11). CI 0.56–0.95] for IFG). The odds for cantly decreased in both groups, the This manuscript is a review of the premenopausal women were not sta- improvement was greater among par- impact of vegetarian diets on diabe- tistically significant for either diabetes ticipants in the vegan group (–0.5%, tes. The specific objectives included: (OR 0.26 [95% CI 0.06–1.21]) or P <0.01 vs. –0.2%, P <0.05). This 1) assessment of the incidence of type IFG (OR 0.60 [95% CI 0.35–1.04]). difference became greater when the 2 diabetes among vegetarians in com- Vegetarians living in North analysis was restricted to patients parison to nonvegetarians, 2) review America also have lower odds of with the highest rate of compliance of the impact vegetarian diets have on being diagnosed with type 2 dia- to the respective diets (–0.9% in the type 2 diabetes management/blood betes, according to results from the vegan group and –0.3% in the con- glucose control and treatment, and 3) Adventist Health Study 2 (8), which ventional group, P = 0.010). evaluation of the influence of vegetar- included 15,200 men and 26,187 The beneficial effects of vegetar- ian diets on diabetes comorbidities. women. Compared to nonvege- ian diets described above indicate FROM RESEARCH TO PRACTICE Vegetarian Diets and Incidence tarians, vegans had the lowest risk that these diets might be effective in of Type 2 Diabetes (OR 0.381 [95% CI 0.236–0.617]), diabetes management and treatment. followed by semi-vegetarians (OR The effect of vegetarian diets on This conclusion is supported by find- 0.486 [95% CI 0.312–0.755]) and the risk of developing type 2 diabe- ings reported by Barnard et al. (16), in lacto-ovo-vegetarians (OR 0.618 tes has been assessed in a few large a study with 99 individuals with type [95% CI 0.503–0.760]). This trend studies with individuals of different 2 diabetes. Participants were divided was similar among both black and sexes, ethnic backgrounds, and geo- into group 1, with 49 people between nonblack participants. graphical locations. In a recent study, 33 and 82 years of age who were Agrawal et al. (12) reported an asso- Vegetarian Diets in Type 2 assigned to a vegan diet, and group ciation between the consumption of Diabetes Management and 2, with 50 people between 27 to 80 a vegetarian diet and the occurrence Blood Glucose Control and years of age who were assigned to fol- of type 2 diabetes in a nationally rep- Treatment low a diet recommended by the ADA resentative sample of 156,317 East Results of a meta-analysis (14) that based on carbohydrate counting. The Indian participants who were 20–49 assessed the impact of vegetarian di- first group was advised to consume years of age. Individuals who adhered ets on plasma glucose suggested that vegetables, fruits, whole-grain cereals, to any type of vegetarian diet except such diets are effective in blood glu- and beans. The amounts of calories for vegan had statistically significant cose management. The analyses were and carbohydrates consumed were lower odds of diabetes (odds ratio based on six interventional studies not limited. Carbohydrates consti- [OR] 0.67 [95% CI 0.58–0.76], involving 255 individuals. Five of tuted ~75% of consumed calories, P <0.01 for lacto-vegetarians; OR the studies assessed the effect of a with the remainder provided by fat 0.70 [95% CI 0.51–0.96], P = 0.03 vegan diet, whereas the sixth assessed (10%) and protein (15%). for lacto-ovo-vegetarians; and OR a lacto-ovo-vegetarian diet. The study Participants in both groups 0.77 [95% CI 0.60–0.98], P = 0.03 periods varied from 4 to 74 weeks reduced their caloric intake from for semi-vegetarians). The association (average 23.7 weeks). Adhering to a 1,759 ± 468 to 1,425 ± 427 kcal/day for vegans was not statistically signifi- vegan or vegetarian diet resulted in (P <0.0001) in the vegan group and cant (OR 0.91 [95% CI 0.61–1.36], a statistically significant lower mean from 1,846 ± 597 to 1,391 ± 382 P = 0.643). A1C (–0.39 percentage points [95% kcal/day (P <0.0001) in the control The results described by Agrawal CI –0.62 to –0.15], P = 0.001) com- group. Protein intake among vegans et al. are consistent with findings pared to A1C among participants dropped from 77 ± 27 to 51 ± 16 g/day from another Asian study from from control diets. No heterogeneity (P <0.0001), whereas in the control Taiwan (13). This study included was observed among study results group it decreased from 85 ± 27 to 4,384 individuals who were Buddhist (P = 0.389 for heterogeneity). 73 ± 23 g/day (P <0.002). Similarly, volunteers. The reported analyses Since the meta-analysis described fat intake fell in both groups from 72 were sex and age specific. Vegetarian above was published, Lee et al. (15) ± 28 to 30 ± 19 g/day (P <0.0001) in men had statistically significant lower published results of a study in which the experimental group and from 73 odds for both diabetes (OR 0.49 they assessed the impact of a brown ± 35 to 52 ± 21 g/day (P <0.0001) in [95% CI 0.28–0.89]) and impaired rice–based vegan diet on glycemic the control group. Conversely, carbo- fasting glucose (IFG; OR 0.66 [95% control among 46 Korean patients hydrate intake increased from 205 ± CI 0.46–0.95]). A similar pattern and 47 control participants who used 69 to 251 ± 70 g/day (P <0.0001) in was observed for postmenopausal a diet recommended by the Korean the vegan group and from 213 ± 70

VOLUME 30, NUMBER 2, SPRING 2017 83 FROM RESEARCH TO PRACTICE / PERSPECTIVES ON MEAL PLANNING to 165 ± 51 g/day (P <0.0001) in the control group. Before switching to a vegan diet After switching to a vegan diet After 22 weeks, individuals as- signed to consume the high-carbo- hydrate vegan diet lowered their A1C from an average of 8.0 to 7.1% Average monthly decrease in creatinine (12.6%). A1C in the control group clearance before vegan diet: 1.48 mL/min dropped from 7.9 to 7.4% (6.8%) in Average monthly decrease in creatinine the same time period. Moreover, 21 clearance while on vegan diet: 0.13 mL/min of the 49 participants (43%) in the

vegan group reduced their doses of Creatinine Cearance medication prescribed for blood glu- Average diastolic pressure: Average diastolic pressure: 130.9 mmHg cose control, compared to 26% of 128.1 mmHg individuals in the control group. Vegetarian Diets and Diabetes Comorbidities ■ FIGURE 1. Creatinine clearance before and after adoption of an amino acid– Vegetarian diets have been associated supplemented vegan diet. Reprinted from ref. 18 with permission of S. Karger AG, with reduced risk of several diabetes Basel. comorbidities. In one of the most recent studies, Bunner et al. (17) The average monthly decrease in this study had a reduction in protein- showed that individuals consuming creatinine clearance before adoption uria which, consistent with results a vegan diet supplemented with vi- of the vegan diet was 1.48 mL/min. of Barsotti et al. (18), indicated an tamin B12 (1,000 µg of methylco- After switching to a vegan diet, improvement in kidney function. balamin/day) had a reduced risk of the decrease in creatinine clearance Discussion diabetes-related neuropathy pain. At markedly decreased to 0.13 mL/min. The prevalence of diabetes is on the end of the 20-week intervention Urine protein levels decreased from the rise, both in the United States with the vegan diet and vitamin B12 5.2 to 2.8 g/day, mean cholesterol and worldwide. According to the supplement, participants experienced decreased from 254 to 165 mg/dL, International Diabetes Federation a decrease of 9.1 points on a pain and average blood glucose decreased (20), ~415 million individuals world- questionnaire (from 22.6 at baseline from 166 to 131 mg/dL. wide have diabetes. This number is to 13.5 at 20 weeks). In contrast, the The findings of Barsotti et al. projected to increase to 642 million decrease among participants in the (18) were confirmed in a newer by 2040. In the United States, the control group, who also received a study involving 25 vegan Buddhist number of individuals with diabe- vitamin B12 supplement but did not monks and 25 nonvegetarian con- tes increased from ~20.8 million in consume a vegan diet, was 0.9 points trol subjects in Thailand (19). All 2005 to ~29.1 million in 2012 (21). during the same time period. assessed parameters of renal func- Epidemiological studies (5,12,13) Intriguing findings were reported tion, including blood urea nitrogen comparing the prevalence of type 2 by Barsotti et al. (18) in a study (BUN), BUN-to-creatinine ratio, diabetes among vegetarians and non- involving patients diagnosed with urinary protein content, and serum vegetarians have shown that vegetari- diabetic neuropathy and renal fail- creatinine, were improved among ans have a lower risk. Thus, it is log- ure (varying in degree from mild to the vegan participants compared ical to conclude that promotion and significant). After the adoption of a to their nonvegetarian counter- adoption of a vegetarian diet may help strict vegan diet supplemented with parts. For example, mean urinary in controlling the diabetes epidemic. protein, the progression of kidney protein among vegans was 1.4 The lower risk of type 2 diabetes insufficiency was halted. The average mg/dL, compared to 5.2 mg/dL among vegetarians may be explained ingested protein intake before the among control subjects. Figure 1 in part by improved weight status (i.e., experiment was 1.2 g/kg/day. After illustrates creatinine clearance before lower BMI) (8). However, the lower switching to a vegan diet, protein and after adoption of the vegan diet. risk also may be explained by higher intake decreased to 0.3 g/kg/day. Results of the study by Barnard et amounts of ingested dietary fiber and Within 15 months prior to switching al. (16) showed that a vegan diet plant protein, the absence of meat- to the vegan diet, creatinine clearance improved traditional cardiovascular and egg-derived protein and heme decreased from 40.9 to 15.6 mL/min. disease (CVD) risk factors (Table 1). iron, and lower intake of saturated After ~1 year on a meatless diet, cre- In addition to the improvement in fat (22–27). Most studies report the atinine clearance was 13.6 mL/min. CVD risk factors, participants in lowest risk of type 2 diabetes among

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TABLE 1. Effect of a Vegan Diet on Traditional CVD Risk the control group by 30% (95% CI Factors. –50 to –14, P <0.001). These findings highlight several benefits of follow- Risk Factor Baseline After 22 Weeks of Vegan Diet ing a vegetarian diet for patients with diabetes, from improvement in glyce- Body weight (kg) 97 91.1 mic control to amendment of factors BMI (kg/m2) 33.9 31.8 important in preventing diabetes Systolic blood pressure (mmHg) 123.8 120 complications. Diastolic blood pressure (mmHg) 77.9 72.8 No statistically significant reduc- tion in risk of type 2 diabetes was Total cholesterol (mg/dL) 187 159.3 found for vegan participants from LDL cholesterol (mg/dL) 104.4 88 the study by Agrawal et al. (12). The Triglycerides (mg/dL) 148.1 119.7 reason why these findings differed

Adapted from ref. 16. from the results of other studies is not FROM RESEARCH TO PRACTICE clear, although the authors suggested individuals who adhere to vegan diets. medications and insulin doses. For a few possible explanations. First, This may be explained by the fact that example, Barnard et al. (16) reported vegan diets in India might differ vegans, in contrast to ovo- and lac- that up to 43% of their experimen- from vegan diets in Western coun- to-ovo-vegetarians, do not ingest eggs. tal group altered their medication. In tries. For example, Indian vegans may Two separate meta-analyses (28,29) comparison, 26% of the control group eat greater amounts of butter or ghee linked egg consumption with a higher assigned to a carbohydrate counting– (clarified butter). Also, only 26 par- risk of type 2 diabetes. based dietary method altered their ticipants from the vegan group were The studies included in the medications. Similarly, in a study by diagnosed with type 2 diabetes. Thus, meta-analysis that assessed the impact Kahleova et al. (30), 43% of partici- the study may not have had adequate of vegetarian diets on plasma glucose pants in the experimental group and statistical power. showed that vegetarian diets not only 5% of participants in the control In addition to the studies that improved glycemic control, they did group reduced their diabetes medica- assessed the impact of vegetarian diets so to a greater level than did control tions (P <0.001). on the risk of type 2 diabetes and gly- diets, including diets based on car- The findings reported by Kahleova cemic control, several studies assessed bohydrate counting (14). Also, these et al. (30) deserve special consider- the impact of plant-based diets on diets were associated with an improve- ation. In this study, 74 participants risk of type 2 diabetes. Plant-based ment of secondary outcomes, such as were randomly assigned to either an diets are mainly composed of plant weight reduction, serum lipid pro- experimental or a control diet group. foods and may or may not contain file, and systolic and diastolic blood The former consisted of a vegetarian small amounts of meat. For exam- pressure. Furthermore, when supple- diet, whereas the latter was a conven- ple, analyses based on a combined mented with vitamin B12, a vegan tional diabetic diet. Although the sample of >200,000 participants, diet used in a study by Bunner et al. two diets were isocaloric with 500 of which 16,162 developed type 2 (17) showed that it may be helpful kcal restriction, individuals from the diabetes, from the Nurses’ Health in reducing neuropathy pain among experimental group lost more body Study, Nurses’ Health Study II, and diabetes patients. The respective stud- weight (mean –6.2 kg [95% CI –6.6 Health Professionals Follow-Up ies were conducted in Brazil, Czech to –5.3] vs. mean –3.2 kg [95% CI Study showed a 34% risk reduction Republic, and the United States –3.7 to –2.5) and had greater improve- among participants in extreme deciles (14). The newest study that assessed ments in insulin sensitivity (30% of a healthful plant-based diet index a brown rice–based vegetarian diet [95% CI 24.5–39] vs. 20% [95% (HR [adjusted for BMI] 0.66 [95% on glucose control was conducted in CI 14–25], P = 0.04). Furthermore, CI 0.61–0.72, P <0.001 for the trend) South Korea (15). The unidirectional compared to baseline, A1C was sta- (25). outcomes suggest that vegetarian diets tistically significantly lower only in Vegetarians have been shown to can improve blood glucose control the experimental group (–0.65 ± 1%, have a high prevalence of vitamin regardless of cultural food choices or P = 0.002 vs. –0.21 ± 1.1%). Also, B12 deficiency (31). In addition, met- product availability due to geograph- markers of oxidative stress improved formin therapy increases the risk of ical locations. in the experimental group. For exam- vitamin B12 deficiency (32,33). Poor The improvement in glycemic ple, superoxide dismutase increased vitamin B12 status is associated with control found in some individuals in the experimental group by 49% hyperhomocysteinemia (34), which assigned to vegetarian/vegan diets (95% CI 44.7–57.4, P <0.001), com- in turn has been shown to increase have resulted in decreases in diabetes pared to baseline, but it decreased in risk of several diabetes complications,

VOLUME 30, NUMBER 2, SPRING 2017 85 FROM RESEARCH TO PRACTICE / PERSPECTIVES ON MEAL PLANNING including retinopathy, neuropathy, ing vegetarian, and especially vegan, Rather, these participants were living bone fractures, and CVD (34–37). diets resulted in discontinuation of in their respective communities and Thus, it would be prudent to rou- medication or insulin therapy. Given may only have received basic instruc- tinely monitor vitamin B12 status that vegetarian diets result in better tion regarding vegetarian/vegan meal and to prescribe supplementation as plasma glucose control than a diet planning from dietetic or other health needed for patients with diabetes who based on carbohydrate counting, professionals. Similarly, plant-based adopt a vegetarian lifestyle. patients find them easier to adhere to, diets had generally good adherence Vegetarian diets also increase and they are associated with reduc- during worksite interventional man- risk of a deficiency of a few addi- tion in risk of developing diabetes agement programs for type 2 diabetes tional nutrients, such as iron (38). comorbidities, recommending these (48). These findings indicate some Vegetarians also have lower intake diets to patients with diabetes may patients with diabetes may find veg- and status of the long-chain omega-3 result in better dietary adherence and etarian or plant-based diets easier to fatty acids EPA and DHA than their better health outcomes. The ADA accept than many clinicians may fear. nonvegetarian counterparts (39). now endorses vegetarian diets as one A healthy, vegetarian diet is Some studies also have documented option for patients with diabetes (1). composed of a variety of unrefined low vitamin D levels and low intake In addition, the Canadian Diabetes foods, including grain products such of calcium (mainly among veg- Association has issued a statement in as bread, cereal, and pasta; fruits, ans) (40–42). The potential impact support of the use of plant-based diets including berries (e.g., blueberries and of compromised vitamin D, iron, for the management of type 2 dia- raspberries) and avocados; vegetables, and calcium levels on diabetes risk, betes (47). Because vegetarian diets especially legumes and green leafy diabetes management, and the devel- improve glycemic control, patients vegetables; and nuts and seeds. These opment of diabetes comorbidities is adopting such a diet should have plant foods, with few exceptions (e.g., not clear. However, adequate intake their medication and insulin doses potatoes and dates), tend to improve of the long-chain omega-3 fatty acids adjusted to prevent hypoglycemia. glycemic control and reduce the risk EPA and DHA has been associated It is important to note that of diabetes complications (49–51). with some benefits for patients with patients with diabetes find it easier to Traditional meat-containing dishes diabetes, including reduction of adhere to a vegetarian diet, mainly a can easily be made vegetarian with albuminuria, improvement in renal vegan diet, than to a diet based on the use of meat analogues such as soy function, and risk reduction of dia- carbohydrate counting and that there meat substitutes. Vegetarian substi- betic retinopathy (43–45). These is a higher degree of compliance with tutes for burgers, sausages, hot dogs, fatty acids also have been associated vegetarian diets than with alterna- crumbles, strips, “meatballs,” and a with a lower risk of CVD incidence tive diets. Such findings have been variety of other foods are available and mortality among patients with reported in more than one study. in regular grocery stores. Patients diabetes (46). Algal EPA and DHA For example, in the study by Lee et willing to adopt a vegan diet can supplements (oils derived from al. (15) the mean compliance score substitute dairy products with soy algae) are available in health foods (maximum score of 10) during the products, including soymilk, tofu, stores. These supplements are suit- intervention period was 9.2 ± 1.6 in and tempeh. able for both vegetarians and vegans. the vegan group and 8.2 ± 1.5 in the Patients also can be referred to Considering the risk of these nutri- conventional diet group (P = 0.002). existing resources to guide them in ent deficiencies, patients should These findings are important in light adopting a healthy, vegetarian diet. be referred to a registered dietitian of the common assumption that Such resources may include online nutritionist (RDN) for dietary con- patients will be unwilling to adopt information from the ADA, the sultation to discuss effective ways to a vegan or vegetarian diet. Although USDA, and the Vegetarian Research maintain adequate status of these this assumption may hold true for Group (52–54). Patients can also find nutrients. some patients, anecdotal evidence online search engines that list vege- The studies reviewed above indi- indicates that even many patients tarian restaurants (55,56). In addition cate that vegetarian diets can be used who are advanced in age are willing to meal-planning guides and websites universally in type 2 diabetes preven- to adopt such diets when advised by that list vegetarian restaurants, many tion and as tools to improve blood their physician. ethnic restaurants, especially Middle glucose management. In addition It is equally important to point Eastern and Mexican restaurants, to the published studies, substantial out that, in most of the studies that offer a variety of meatless dishes. unpublished anecdotal evidence is assessed the impact of vegetarian or Again, to successfully implement available in support of the effective- vegan diets on glycemic control in a healthy vegetarian eating plan, ness of vegetarian diets in diabetes patients with diabetes, participants patients can be referred to an RDN, management. In many cases, adopt- were not provided ready-to-eat meals. who can assist them in meal planning

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