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FROM THE ACADEMY Position Paper

Position of the Academy of and Dietetics: Vegetarian Diets

ABSTRACT POSITION STATEMENT It is the position of the Academy of Nutrition and Dietetics that appropriately planned It is the position of the Academy of Nutrition vegetarian, including vegan, diets are healthful, nutritionally adequate, and may provide and Dietetics that appropriately planned fi vegetarian, including vegan, diets are bene ts for the prevention and treatment of certain . These diets are healthful, nutritionally adequate, and may appropriate for all stages of the life cycle, including pregnancy, lactation, infancy, provide health benefits in the prevention childhood, adolescence, older adulthood, and for athletes. -based diets are more and treatment of certain diseases. These environmentally sustainable than diets rich in animal products because they use fewer diets are appropriate for all stages of the life cycle, including pregnancy, lactation, infancy, natural resources and are associated with much less environmental damage. Vegetar- childhood, adolescence, older adulthood, ians and vegans are at reduced risk of certain health conditions, including ischemic and for athletes. Plant-based diets are more heart , type 2 , , certain types of , and . Low environmentally sustainable than diets rich intake of saturated and high intakes of , , whole , , soy in animal products because they use fewer fi natural resources and are associated with products, nuts, and (all rich in ber and ) are characteristics of much less environmental damage. vegetarian and vegan diets that produce lower total and low-density lipoprotein levels and better serum glucose control. These factors contribute to reduc- tion of chronic disease. Vegans need reliable sources of B-12, such as fortified or supplements. J Acad Nutr . 2016;116:1970-1980.

EGETARIAN AND VEGAN VEGETARIAN DIETS IN intake from vegetables, fruits, whole dietary patterns can be quite PERSPECTIVE grains, and .3 In the 2015-2020 diversebecauseofthevari- Trends among Vegetarians Dietary Guidelines for Americans, ety of choices available vegetarian diets are recommended as V According to a nationwide poll in 2016, and the different factors that moti- one of three healthful dietary patterns, vate people to adopt such patterns. approximately 3.3% of American adults and plans are provided for those People choose to adopt a vegetarian are vegetarian or vegan (never eat following lacto-ovo-vegetarian and fi diet for many reasons, such as meat, poultry, or sh), and about 46% of vegan diets.4 The National School 1 compassion toward animals, a desire vegetarians are vegan. The same poll Lunch Program, while not requiring to better protect the environment, to revealed that 6% of young adults (18 to vegetarian options per se, requires lower their risk of chronic diseases, or 34 years) are vegetarian or vegan, schools to increase availability of fruits, to therapeutically manage those dis- while only 2% of those 65 years or older vegetables, and whole grains in current eases. A well-planned vegetarian diet are vegetarian. Sales of alternative meal patterns in the school menu. containing vegetables, fruits, whole meat products reached $553 million in Those following a vegetarian diet now grains, legumes, nuts, and seeds can 2012, an 8% increase in 2 years. It was have technological support. To date, provide adequate nutrition. Vege- observed that 36% of survey responders while no online nutrition food tracker tarian diets are devoid of flesh foods sought vegan meat alternatives, largely exists strictly for vegetarian diets, some (such as meat, poultry, wild game, from among the 18- to 44-year-old age allow clients to select vegetarian and 1,2 , and their products). The group. While whole plant foods serve vegan plans. These applications for mo- most commonly followed vegetarian best as dietary staples, some processed bile devices allow vegetarians to discover fi diets are shown in Figure 1.The and forti ed foods, such as nondairy nutritional needs, track intake, and adoption of a vegetarian diet may beverages, meat analogs, and breakfast locate restaurants and markets where cause a reduced intake of certain , can contribute substantially to vegan foods are available. The online ; however, deficiencies can the intake of vegetarians. tracking tool at www.SuperTracker.usda. be readily avoided by appropriate Plant-based diets, including vege- gov is a part of the US Department of planning. tarian and vegan diets, are becoming Agriculture Choose My Plate program.5 well accepted, as further evidenced by fi many nonpro t and government NUTRITION CONSIDERATIONS institutions highlighting this dietary FOR VEGETARIANS choice. The American Institute for 2212-2672/Copyright ª 2016 by the Cancer Research encourages a plant- Academy of Nutrition and Dietetics. based diet, suggesting Americans Vegetarian, including vegan, diets http://dx.doi.org/10.1016/j.jand.2016.09.025 consume two-thirds of their dietary typically meet or exceed recommended

1970 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS ª 2016 by the Academy of Nutrition and Dietetics. FROM THE ACADEMY

nonvegetarians, and tissue levels Concerns about the status of Type of diet Nature of diet (all are of EPA and DHA can be significantly vegetarians have led to questions of fl devoid of esh foods) lower.10,11 bioavailability of non- iron from The clinical relevance of reduced EPA plant foods. Non-heme iron absorption Vegetarian May or may not include and DHA status among vegetarians and depends upon physiological need and egg or vegans is unknown.11,12 Long-chain n-3 is regulated in part by iron stores. Its products. fatty acids are important for the absorption can vary greatly, depending development and maintenance of the upon both the meal composition and Lacto-ovo- Includes eggs and dairy brain, retina, and cell membranes and the iron status of the individual. vegetarian products. favorably impact pregnancy outcomes Bioavailability of non-heme iron is and risk for impacted by the ratio of inhibitors, Lacto- Includes dairy (CVD) and other chronic diseases.6,13,14 such as phytates and polyphenolics, vegetarian products, but not Yet, vegetarian and vegan children do and enhancers, such as , citric egg products. not appear to experience impairment acid, and other organic acids.19 in visual or mental development, and In a recent review, non-heme iron Ovo- Includes eggs and egg vegetarian and vegan adults experi- absorption was seen to vary from 1% to vegetarian products, but no ence reduced risk for CVD.10,11,15 23%, depending upon iron status and dairy. ALA is endogenously converted to dietary enhancers and inhibitors.20 EPA and DHA, but the process is A newly developed regression equa- Vegan Excludes eggs and somewhat inefficient and is affected by tion enables iron absorption to be dairy products, and sex, dietary composition, health status, predicted from serum ferritin levels may exclude . and age. High intakes of linoleic acid and dietary modifiers. Diet had a 11,13 Raw vegan Based on vegetables, (LA) may suppress ALA conversion. greater effect on iron absorption when A ratio of LA/ALA not exceeding 4:1 serum ferritin levels were low.20 , nuts and seeds, has been suggested for optimal Nonheme iron absorption can be as legumes, and conversion.7,10,14 much as 10 times greater in iron- sprouted grains. The The for ALA deficient individuals compared with amount of uncooked are 1.6 g/day and 1.1 g/day, for men and iron-replete individuals. food varies from 75% women, respectively.4 For vegetarians The Dietary Reference Intake to 100%. and vegans, it may be prudent to assigned to iron for vegetarians in 2001 ensure somewhat higher intakes of was 80% more than that for non- Figure 1. Types of vegetarian diets. ALA.8,10 The most concentrated plant vegetarians. This derives from the sources of n-3 fatty acids are seeds assumption that the bioavailability of (flax, chia, camelina, canola, and iron from a vegetarian diet is 10%, protein intakes, when caloric intakes 8,10 6-8 ), , and their oils. Evi- whereas that from a nonvegetarian diet are adequate. The terms complete dence suggests that n-3 needs of is 18%.21 These assumptions were and incomplete are misleading in rela- healthy individuals can be met with based on very limited data using tion to plant protein. Protein from a ALA alone, and that endogenous syn- single-meal absorption studies variety of plant foods, eaten during the thesis of EPA and DHA from ALA is involving that were atypical of course of a day, supplies enough of all sufficient to keep levels stable over what most vegetarians consume in indispensable (essential) amino acids 11,14 7 many years. Low-dose micro- Western countries. when caloric requirements are met. based DHA supplements are We now know that individuals can The regular use of legumes and soy available for all vegetarians with adapt and absorb non-heme iron more products will ensure an adequate pro- increased needs (eg, pregnant or effectively.22 The magnitude of the tein intake for the vegetarian, as well as 9 lactating women) or with reduced effect of enhancers and inhibitors of providing other essential nutrients. conversion ability (eg, those with iron absorption can diminish with Fruitarian diets are normally low in hypertension or diabetes).10 time.23 Individuals are able to adapt to protein and other nutrients. Protein low intakes of iron over time and can needs at all ages, including those for reduce iron losses.24 In one study, total athletes, are well achieved by balanced Iron fi 7,8 iron absorption signi cantly increased vegetarian diets. Vegetarians generally consume as by almost 40% after 10 weeks of much iron as, or slightly more than, consuming the low-bioavailability n-3 Fatty Acids .16 Despite having similar diet.22 While a-linolenic acid (ALA) intakes of iron intakes,17 the iron stores of vege- Individuals with low iron status can vegetarians and vegans are similar to tarians are typically below those of substantially increase their iron those of nonvegetarians, dietary nonvegetarians. Lower serum ferritin absorption from diets with moderate to intakes of the long-chain n-3 fatty levels may be an advantage because high iron bioavailability. The absorp- acids, (EPA) and elevated serum ferritin levels have tion process appears to adapt effec- (DHA), are independently been associated with tively in the case of Western lower in vegetarians and typically the risk of developing metabolic vegetarians because their hemoglobin absent in vegans.10,11 Compared with syndrome.18 values and most other measures of iron

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status are similar to those values seen nutrient. Foods that are fortified with 7 ’ in nonvegetarians. Intakes of lacto-ovo-vegetarians typi- include cow s milk, some cally meet or exceed calcium recom- nondairy milks, fruit juices, breakfast mendations, while calcium intakes of cereals, and . Eggs may also provide some vitamin D. Mushrooms Compared with nonvegetarian control vegans vary widely and sometimes fall 7 treated with ultraviolet light can be groups, studies show adult vegetarians below recommendations. Bioavail- significant sources of vitamin D.36,37 have dietary zinc intakes that are ability of calcium from plant foods, Both vitamin D-2 and vitamin D-3 are similar or somewhat lower, and serum which is related to oxalate content of used in supplements and to fortify zinc concentrations that are lower but foods and, to a lesser degree, phytate foods. Vitamin D-3 (cholecalciferol) within the normal range.7,25 There do and fiber, is an important consideration. may be of plant or animal origin, while not appear to be any adverse health Fractional absorption from high-oxalate vitamin D-2 (ergocalciferol) is pro- consequences in adult vegetarians that vegetables, such as spinach, beet greens, duced from the ultraviolet irradiation are attributable to a lower zinc status, and Swiss chard, may be as low 5%. Thus, of ergosterol from yeast. At low doses, possibly due to homeostatic mecha- these cannot be considered good vitamin D-2 and vitamin D-3 appear to nisms that allow adults to adapt to a sources of calcium, despite their high be equivalent, but at higher doses vegetarian diet. Overt zinc deficiency is calcium content. In comparison, ab- vitamin D-2 appears to be less effective not evident in Western vegetarians. For sorption from low-oxalate vegetables, than vitamin D-3.36 If sun exposure and the most at-risk members of the such as kale, turnip greens, Chinese 31 intake of fortified foods are insufficient population (older adults, children, cabbage, and bok choy, is about 50%. to meet needs, vitamin D supplements and pregnant and lactating women), Absorption from calcium-set are recommended, especially for the there is insufficient evidence to deter- (made with a calcium salt) and from older adults.35,36,38 Because vitamin D mine whether zinc status is lower in most fortified plant milks is similar to influences a large number of metabolic vegetarians compared with non- that from cow’s milk, at approximately 32,33 pathways beyond bone meta- vegetarians.25 Zinc sources for the 30%. Other plant foods, such as bolism,35,38 some experts recommend vegetarian include soy products, white beans, almonds, tahini, figs, and daily intakes of vitamin D of 1,000 to legumes, grains, cheese, seeds, and oranges, provide moderate amounts of 2,000 IU, or even more. nuts. Food preparation techniques, calcium with somewhat lower such as soaking and sprouting beans, bioavailability (about 20%). Comparing forms of calcium used for fortification, grains, nuts, and seeds, as well as Vitamin B-12 leavening bread, can reduce binding of bioavailability of calcium-citrate- malate can be at least 36%, while Vitamin B-12 is not a component of zinc by and increase zinc 7,39 34 plant foods. Fermented foods (such bioavailability.26 Organic acids, such as others are about 30%. Registered die- as ), nori, spirulina, chlorella citric acid, also can enhance zinc titian nutritionists (RDNs) and nutrition algae, and unfortified absorption to some extent.26 and dietetics technicians, registered (NDTRs) can help clients meet calcium cannot be relied upon as adequate or 39,40 needs by encouraging regular con- practical sources of B-12. Vegans Iodine sumption of good calcium sources and, must regularly consume reliable sour- — fi Because plant-based diets can be low when necessary, low-dose calcium ces meaning B-12 forti ed foods or — in iodine, vegans who do not consume supplements. B-12 containing supplements or they key vegan sources of iodine, such as could become deficient, as shown in iodized salt or sea vegetables, may be case studies of vegan infants, children, at risk for iodine deficiency.7,27 The Vitamin D and adults.8,39 Most vegetarians should iodine content of sea vegetables varies Vitamin D status depends on sunlight include these reliable B-12 sources widely and some may contain sub- exposure and intake of vitamin because 1 cup of milk and one egg per stantial amounts of iodine.28 Intakes Defortified foods or supplements.35 day only provides about two-thirds of should not exceed the Tolerable Upper The extent of cutaneous vitamin D the Recommended Dietary Allowance Intake Level of 1,100 mg for adults.29 production after sunlight exposure is (RDA).7,39,40 Vegan women of child-bearing age highly variable and is dependent on a Early symptoms of a severe B-12 should supplement with 150 mg/day number of factors, including the time deficiency are unusual fatigue, tingling iodine.27,29 Sea salt, kosher salt, and of day, season, latitude, air pollution, in the fingers or toes, poor cognition, salty , such as tamari, are skin pigmentation, sunscreen use, poor digestion, and failure to thrive in generally not iodized,7 and iodized salt amount of clothing covering the skin, small children. A subclinical B-12 defi- is not used in processed foods. Dairy and age.35,36 Low vitamin D intakes ciency results in elevated homocyste- products may contain iodine, although have been reported in some vegetar- ine. People with little or no B-12 intake amounts can vary considerable.7 ians and vegans, as well as low plasma may feel healthy; however, long-term Although foods such as , or serum 25-hydroxyvitamin D levels, subclinical deficiency can lead to cruciferous vegetables, and sweet the latter especially when the blood stroke, , and poor bone potatoes contain natural goitrogens, was collected in the winter or spring, health.7,8,41 Laboratory tests to assess these foods have not been associated and especially in those living at high vitamin B-12 status include serum with thyroid insufficiency in healthy latitudes.36 Dietary and supplemental methylmalonic acid, serum or plasma people, provided that iodine intake is sources of vitamin D are commonly B-12, and serum holo-transcobalamin adequate.7,8,29,30 required to meet the needs of this (Holo-TC or Holo-TCII).8,39,41

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The normal mechanism for B-12 was highest (28.8) in meat eaters and reduced risk of heart disease.56 The absorption is via the intrinsic factor, lowest in those who avoided all animal vegetarian diet was especially benefi- which becomes saturated at about half products (23.6).47 Similarly, in the cial for healthy weight and the RDA and requires 4 to 6 hours EPIC-Oxford Study, researchers found individuals, but less effective for obese before further absorption.40 Hence, the highest mean BMI among meat individuals, underscoring the impor- fortified foods are best eaten twice eaters (24.4) and the lowest among tance of early dietary intervention for during the course of a day. A second vegans (22.5).48 In the Swedish long-term risk reduction.56 absorption mechanism is passive Mammography Cohort study, re- In the Adventist Health Study-2 of diffusion at a rate of 1%, allowing less- searchers found that the prevalence 73,308 Seventh-day Adventists, re- frequent consumption of large supple- of overweight or obesity was 40% searchers found that vegetarians had mental doses. Recommendations based among omnivores and 25% among a 13% and 19% decreased risk for on large doses have been made (eg, vegetarians.49 developing CVD and ischemic heart 500 to 1,000 mg cyanocobalamin several Research indicates that therapeutic disease, respectively, compared with times per week).8,39 use of a vegetarian diet is effective for nonvegetarians.15 A previous analysis The four forms of B-12 are differen- treating overweight and may perform from the EPIC study found that vege- tiated by their attached groups. better than alternative omnivorous di- tarian groups had a 32% lower risk of Cyanocobalamin is most commonly ets for the same purpose. Two meta- hospitalization or from heart used in fortified foods and supple- analyses of intervention trials showed disease.53 ments because of its stability. Methyl- that adoption of vegetarian diets was Vegetarians enjoy a lower risk of cobalamin and adenosylcobalamin are associated with greater heart disease by regularly consuming a forms used in the body’s enzymatic compared with control diet groups.50,51 variety of vegetables, fruit, whole reactions; these are available in sup- A vegan diet with structured group grains, legumes, and nuts. Low-fat plement forms that appear to be no support and behavioral therapy vegan and vegetarian diets, combined more effective than cyanocobalamin compared with the National Choles- with other lifestyle factors, including and may require higher doses than the terol Education Program diet, was not smoking and weight reduction, RDA. Hydroxocobalamin is the form associated with significantly greater have been shown to reverse athero- used effectively for injections.8,42 weight loss after 1 and 2 years.52 sclerosis.61 Risk factors for coronary heart disease, such as total and low- CVD, Including Hyperlipidemia, density lipoprotein cholesterol levels, THERAPEUTIC VEGETARIAN body weight, and body fat, improve DIETS AND CHRONIC DISEASE Ischemic Heart Disease, and Hypertension within a short time on a vegetarian Provided that adequate nutrition edu- diet, even without the use of Vegetarian diets are associated with a 61 cation is given, a therapeutic vege- 15,53 cholesterol-lowering drugs. tarian diet performs as well as reduction in the risk of CVD. Compared with nonvegetarians, omnivorous diets in terms of adher- Vegetarian diets improve several vegetarians have a lower prevalence of 43 modifiable heart disease risk factors, ence. As with implementation of any 54 hypertension. Results of the EPIC- diet, employing a variety of counseling including abdominal obesity, blood Oxford study showed vegans have the pressure,55 serum lipid profile,56 and strategies, including motivational 42,57 lowest systolic and diastolic blood interviewing, frequent sessions, cook- blood glucose. They also decrease pressure levels and the lowest rate of fl ing demonstrations, and incentives, markers of in ammation such as hypertension of all diet groups (vegans, can improve nutrition-related out- C-reactive protein, reduce oxidative vegetarians, fish eaters, and meat stress, and protect from atherosclerotic 62 comes when using a vegetarian diet 58 eaters). Data from the Adventist therapeutically. plaque formation. Consequently, Health Study-2 confirmed that vegans vegetarians have reduced risk of have the lowest blood pressure levels developing and dying from ischemic and the least hypertension of all vege- Overweight and Obesity 15,53,59 heart disease. tarians, and significantly less than the With more than two-thirds the Amer- Vegan diets seem to be most bene- meat eaters.55 A meta-analysis ican population overweight or obese ficial in improving heart disease risk 44 55,57 60 comparing blood pressure from more and numbers increasing, RDNs factors. The EPIC-Oxford study than 21,000 people around the world should be aware of the evidence to revealed that those who consumed a found that those who follow a vege- fi support the use of vegetarian and vegan diet ate the most ber, the least tarian diet have systolic blood pressure vegan diets for achieving and main- total fat and , and had the about 7 mm Hg lower and diastolic taining a healthy weight. A healthy healthiest body weights and choles- blood pressure 5 mm Hg lower than body weight is associated with terol levels compared with omnivores 45 study participants who consume an improved cardiovascular function and other vegetarians. A meta-analysis omnivorous diet.63 and sensitivity,46 as well as of 11 randomized controlled trials helping to reduce the risk of other found that those participants assigned chronic diseases.45 to a vegetarian diet experienced a Diabetes Plant-based dietary patterns are also substantial reduction in total, low- Compared with meat eaters, lacto-ovo- associated with lower density lipoprotein, and high-density vegetarians and vegans have lower risk (BMI; calculated as kg/m2). In the lipoprotein cholesterol, which corre- of . The Adventist Adventist Health Study-2, mean BMI sponded with an approximately 10% Health Study-2 reported that meat

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eaters had more than twice the preva- the vegan group.71 In a 24-week ran- observed between processed red meat lence of diabetes compared with lacto- domized controlled trial in patients consumption and risk of colorectal ovo-vegetarians and vegans, even after with type 2 diabetes, those on an cancer.81 Processed meat consumption correcting for BMI.47 Among those who isocaloric vegetarian diet reported was also seen to increase the risk of were free of diabetes, the Adventist greater improvements of insulin dying from cancer.82 In a systematic Health Study found that the odds of sensitivity, reduction in visceral fat, review and meta-analysis of 26 epide- developing diabetes were reduced by and a reduction in inflammatory miological studies, the relative risk of 77% for vegans and by 54% for lacto- markers than those on a conventional colorectal adenomas was 1.27 per daily ovo-vegetarians compared with non- diabetic diet.72 100-g intake of red meat and 1.29 per vegetarians (adjusting for age). When According to a meta-analysis of six daily 50-g intake of processed meat.83 BMI and other confounding factors controlled clinical trials, vegetarian were adjusted for, the association diets were associated with improved remained strong. Vegans were 62% less glycemic control in people with type Bone studies have reported that vege- 73 likely to develop diabetes, while lacto- 2 diabetes. Vegetarian and vegan tarians have either similar or slightly 64 ovo-vegetarians were 38% less likely. dietary patterns characterized by reduced bone density levels fi nutrient-dense, high- ber plant foods compared with omnivores, with Prevention. In the past 2 decades, lower the risk of type 2 diabetes and vegans typically having the lowest prospective observational studies and serve as effective therapeutic tools in levels.84 While the differences are clinical trials have provided significant the management of type 2 diabetes. relatively modest, they appear not to evidence that diets rich in whole be of clinical significance, provided the grains, fruits, vegetables, legumes, Cancer nutrients of concern are adequately fi seeds, and nuts, and lower in re ned Results from the Adventist Health provided. grains, red or processed meats, and Study-2 revealed that vegetarian diets Vegetarian diets are associated with -sweetened beverages, reduce the are associated with a lower overall several factors that promote bone risk of diabetes and improve glycemic cancer risk, and especially a lower health, including high intakes of vege- control and blood lipids in patients tables and fruits; an abundant supply 65 risk of gastrointestinal cancer. Further- with diabetes. Whole- intake more, a vegan diet appeared to confer of , , , has been consistently associated with a a greater protection against overall vitamin C; and a relatively low acid lower risk of diabetes, even after load.36 Conversely, they can compro- 66 cancer incidence than any other adjusting for BMI. Legumes, which 74 mise bone health when low in calcium, dietary pattern. Recently, vegan diets 36 are low glycemic index foods, may were reported to confer about a vitamin D, vitamin B-12, and protein. fi provide bene t for diabetes by 35% lower risk of .75 EPIC-Oxford reported a 30% increase in reducing postprandial glucose levels A meta-analysis of seven studies re- fracture risk of vegans as a group, but after consumption of a meal as well as ported vegetarians having an 18% no increase in fracture risk in lacto- after a subsequent meal, known as the lower overall cancer incidence than ovo-vegetarians compared to non- “ ”67 second-meal effect. A meta- nonvegetarians.59 vegetarians. However, when only > analysis demonstrated that higher in- Epidemiologic studies have consis- vegans with calcium intakes 525 mg/ takes of fruit or vegetables, particularly day were included in the analysis, dif- tently shown that a regular consump- 84 green vegetables, were associated with tion of fruit, vegetables, legumes, or ferences in fracture risk disappeared. fi a signi cant reduction in risk of type 2 whole grains is associated with a The Adventist Health Study-2 reported 68 ’ diabetes. In the Nurses Health Study reduced risk of certain .76 A vast that more frequent intakes of legumes I and II, greater consumption, array of phytochemicals, such as sul- and meat analogs reduced risk of hip especially walnuts, was associated with fracture, with a greater protective ef- 69 foraphane, ferulic acid, genistein, 85 a lower risk of diabetes. Conversely, indole-3-carbinol, curcumin, epi- fect than that of meat. Protein has a red and processed meats are strongly fi neutral or slightly positive impact on gallocatechin-3-gallate, diallyldisul de, 36 associated with increased fasting resveratrol, lycopene, and quercetin bone health. Inadequate intakes of glucose and insulin concentrations and found in vegetables, legumes, fruits, D and B-12 have been linked diabetes risk.70 Potential etiologies for to low bone mineral density, increased spices, and whole grains may provide 36 the association of meat and diabetes protection against cancer.77,78 These fracture risk, and osteoporosis. include saturated , advanced phytochemicals are known to interfere To achieve and maintain excellent glycation end products, nitrates/ with a number of cellular processes bone health, vegetarians and vegans nitrites, heme iron, trimethylamine involved in the progression of cancer.79 are well advised to meet the RDA for all N-oxide, branched amino acids, and nutrients, particularly calcium, vitamin 70 Vegetarians typically consume endocrine disruptor chemicals. higher levels of fiber compared with D, vitamin B-12, and protein, and to consume generous servings of vegeta- other diets. The EPIC study involving 10 36 Treatment. In a randomized clinical European countries reported a 25% bles and fruits. trial comparing a low-fat vegan diet to reduction in risk of colorectal cancer a diet based on the American Diabetes for the highest intake of dietary VEGETARIAN DIETS Association guidelines, greater im- fiber compared with the lowest.80 THROUGHOUT THE LIFE CYCLE provements in glycemic control, blood On the other hand, in two large US Well-planned vegan, lacto-vegetarian, lipids, and body weight were seen in cohorts, a positive association was and lacto-ovo-vegetarian diets are

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appropriate, and they satisfy the in pregnancy).8,89 Pregnant and years have been suggested.7,95 While nutrient needs and promote normal lactating vegetarians may benefit from dietary factors may limit absorption of growth at all stages of the life cycle, direct sources of EPA and DHA derived iron and zinc, deficiencies of these including pregnancy and lactation, from microalgae.8,91 are uncommon in vegetarian infancy, childhood, adolescence, older children in industrialized countries.98 adulthood, and for athletes. Infants, Children, and Iron and zinc status of children on Adolescents very restricted plant-based diets Pregnant and Lactating Women should be monitored. Supplemental Exclusive breastfeeding is recom- iron and zinc may be needed in such fi 94 Limited research indicates that where mended for the rst 6 months. If cases.98 food access is adequate, vegetarian breastfeeding is not possible, commer- Vitamin B-12 intake of vegan infants pregnancy outcomes, such as birth cial infant formula should be used as and children should be assessed and fi weight and pregnancy duration, are the primary beverage for the rst year. fortified foods and/or supplements similar to those in nonvegetarian Complementary foods should be rich in used as needed to insure adequacy.7 pregnancy.7,86,87 Use of a vegetarian energy, protein, iron, and zinc, and may diet in the first trimester resulted in include hummus, tofu, well-cooked lower risk of excessive gestational legumes, and mashed .8 Full Older Adults in one study.88 Maternal fat, fortified , or dairy milk can Nutrient intakes of older vegetarians diets high in plant foods may reduce be started as early as 1 year of age for appear to be similar to or better than the risk of complications of pregnancy, toddlers who are growing normally those of older nonvegetarians,7 such as gestational diabetes.88,89 and eating a variety of foods.95 Vege- although past research suggested The Academy of Nutrition and tarian children and teens are at lower lower zinc intakes and a greater inci- Dietetics’ position and practice papers risk than their nonvegetarian peers for dence of poor iron status among veg- on “Nutrition and Lifestyle for a overweight and obesity. Children and etarians.86,99 Caloric needs generally Healthy Pregnancy Outcome”90,91 pro- adolescents with BMI values in the decrease with age, while requirements vide appropriate guidance for pregnant normal range are more likely to also be for some nutrients increase; thus, it is vegetarians. Special consideration is within the normal range as adults, important that all older people choose required for iron, zinc, vitamin B-12, resulting in significant disease risk nutrient-dense diets. Some evidence and EPA/DHA.87,89 reduction.96 Other benefits of a vege- suggests that protein is used less effi- Depending on dietary choices, preg- tarian diet in childhood and adoles- ciently with aging, which may translate nant vegetarians may have higher iron cence include greater consumption of to higher protein requirements.100 intakes than nonvegetarians and are fruits and vegetables, fewer sweets and Thus, it is important for older vegetar- more likely to use iron supplements.92 salty snacks, and lower intakes of total ians and vegans to include protein-rich Because of the potential for inade- and saturated fat.97 Consuming foods such as legumes and soy foods in quate intakes and the adverse effects of balanced vegetarian diets early in life their diets. Meat analogs may be help- iron deficiency, a low-dose (30 mg) can establish healthful lifelong habits.8 ful as protein sources. Older people iron supplement is recommended The peak age of onset for the most synthesize vitamin D less efficiently, in pregnancy.93 The recommended common eating disorders is in the and are likely to require supplements, amount of iron could be provided via a adolescent years. Eating disorders have especially if sun exposure is limited.35 prenatal supplement, a separate iron a complex etiology and prior use of a The higher calcium recommendations supplement, or a combination of these. vegetarian or vegan diet does not for older adults may be met more There is insufficient evidence that zinc appear to increase the risk of an eating easily when fortified foods, such as intake and status in vegetarian preg- disorder, though some with pre- plant milks, are included. The require- nancies differ from nonvegetarian existing disordered eating may choose ment for vitamin B-6 increases with pregnancies.87,89 Due to the increased these diets to aid in their limitation of aging, and may be higher than current zinc requirements of pregnancy and food intake.7,8 RDAs for older people. Atrophic the lower bioavailability in diets based Nutrients that may require attention gastritis is common among people over on high-phytate grains and legumes, in the planning of nutritionally the age of 50 years and can result in increasing zinc intake and using food adequate diets for young vegetarians decreased absorption of vitamin B-12 preparation techniques that improve include iron, zinc, vitamin B-12, and for from animal products. Therefore, many bioavailability are recommended.7,8,29 some, calcium and vitamin D. Mean older people, regardless of diet, require Pregnant and lactating vegetarians protein intakes of vegetarian children vitamin B-12 supplements. need regular and adequate dietary and/ generally meet or exceed recommen- or supplemental sources of vitamin dations.7 Protein needs of vegan chil- B-12.7,8,89,91 dren may be slightly higher than those ENVIRONMENTAL ISSUES Infants of vegetarian women have of nonvegan children because of dif- Plant-based diets are more environ- lower plasma DHA concentrations and ferences in protein digestibility and mentally sustainable than diets rich in breast milk of vegetarians is lower in composition.7 Recommen- animal products because they use fewer DHA.7,8 These n-3 fatty acids can be dations of 30% to 35% more protein for natural resources and are associated synthesized to some extent from 1- to 2-year-old vegans, 20% to 30% with considerably less environmental a-linolenic acid, but conversion rates more for 2 to 6 year olds, and 15% to damage.101-105 The current worldwide are low (though somewhat enhanced 20% more for children older than 6 consumption of diets high in meat and

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www.vndpg.org The Dietetic Practice Group (VNDPG) member benefits include professional information on vegetarian nutrition, RDN resources, and quarterly newsletters. www.vegetariannutrition.net VNDPG’s consumer website provides a blog with evidence-based vegetarian nutrition plus RDN resources for consumers. www.vrg.org The Vegetarian Resource Group provides nutrition information, recipes, meal plans, and recommended readings for vegetarian nutrition. www.PCRM.org The Physicians Committee for Responsible promotes preventive medicine through innovative programs and offers free patient educational materials. www.veganhealth.org This website offers evidence-based recommendations covering the nutritional features of plant-based diets. www.nutritionfacts.org This website provides brief, referenced video clips and articles on numerous aspects of vegetarian nutrition. www.vegweb.com VegWeb offers vegetarian recipes, community, and a blog. www.vegetarian-nutrition.info Vegetarian Nutrition Info provides topical articles, resources, and news. Figure 2. Professional and consumer websites for vegetarian nutrition, food, and related topics. Many of these sites provide high- quality educational materials upon which the registered nutritionist (RDN); nutrition and dietetics technician, registered; and other health care practitioners can rely. These sites supply patient or client education regarding vegetarian nutrition throughout the life cycle, nutrients of interest, meal plans, and plant-based substitutions for nonvegetarian ingredients.

dairy products is considered by some as the United States is a result of pollution production has a greater potential to unsustainable.101,103,105 The systematic from animal farms.109 Animal agricul- reduce greenhouse gas emissions than review conducted by the Scientific ture is associated with land degrada- “technological mitigation or increased Committee of the Dietary Guidelines for tion, air pollution, loss of biodiversity, productivity measures.”105 Americans provides evidence that diets and global warming.104,110 Meat pro- The use of antibiotics in farm animals higher inplant foods and lower in animal duction makes a significant contribu- as growth promoters and for the pre- foods (like a vegetarian diet) are associ- tion to anthropogenic carbon dioxide vention and treatment of animal dis- ated with lower environmental dam- emissions and anthropogenic methane eases has generated antibiotic-resistant age.106 Many scientists are calling for a and nitrous oxide production.101,103,111 . This antibiotic resistance can substantial reduction of livestock prod- Using calculations based on 210 com- be transmitted to through an- ucts in the diet of humans as a major way mon foods, greenhouse gas emissions imal food consumption and is now a to reverse climate change.105 Compared from consuming a vegetarian diet were major problem, causing with omnivorous diets, vegetarian diets found to be 29% lower than from the illnesses that are difficult to treat, and utilize less water and fossil fuel resources use of a nonvegetarian diet,112 while a resulting in increased morbidity, mor- and use lower amounts of pesticides and vegan diet can have >50% lower tality, and health care costs.105,114 fertilizers.107 Substituting beans for greenhouse emissions compared to a in the diet would significantly reduce the nonvegetarian diet.102 environmental footprint worldwide. To While new technologies for animal ROLES, RESPONSIBILITIES, AND produce 1 kg protein from kidney beans farming are available, a recent study RESOURCES FOR THE RDN AND requires 18 times less land, 10 times less found that greenhouse gas emissions NDTR water, 9 times less fuel, 12 times less from the production and consumption Vegan and vegetarian diets can provide fertilizer, and 10 times less pesticide in of animal products were reduced significant health benefits compared comparison to producing 1 kg protein only 9% due to a more efficient with nonvegetarian diets. Ensuring from beef.108 In addition, beef production livestock production.113 The authors energy balance; nutritional adequacy; generates considerably more manure concluded that cuts in greenhouse gas and a focus on a variety of vegetables, waste than from any other animal food emissions necessary to meet the global legumes, fruits, whole grains, nuts, and production.108 temperature target “imply a severe seeds, can maximize these benefits. According to the US Environmental constraint on the long-term global Nutrition and dietetics practitioners Protection Agency, about 70% of all consumption of animal food.”113 Others can play key roles in educating vege- water pollution in rivers and lakes in have suggested that reducing animal tarians about sources of specific

1976 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS December 2016 Volume 116 Number 12 FROM THE ACADEMY

nutrients and foods useful in the vegetarian diets provide adequate ed. Sudbury, MA: Jones and Bartlett; management of specific chronic dis- nutrient intakes for all stages of the 2011. eases. In order to effectively counsel on lifecycle and can also be useful in the 8. Davis B, Melina V. Becoming Vegan: Comprehensive Edition. Summertown, the adoption and implementation of a therapeutic management of some TN: Book Publishing Co; 2014. vegetarian or vegan diet, RDNs and chronic diseases. Overall nutrition, as 9. Messina V. Nutritional and health bene- NDTRs must have adequate knowledge assessed by the Alternative Healthy fits of dried beans. Am J Clin Nutr. and access to educational materials to Eating Index, is typically better on 2014;100(suppl 1):437S-442S. facilitate healthful recommendations. vegetarian and vegan diets compared 10. Saunders AV, Davis BC, Garg ML. Omega- The US Department of Agriculture’s with omnivorous diets. While some 3 polyunsaturated fatty acids and vege- tarian diets. Med J Aust. 2013;199 ChooseMyPlate allows for lacto-ovo- vegetarian diets may be low in certain (4 suppl):S22-S26. vegetarian and vegan menus, listing nutrients, such as calcium and vitamin 11. Sanders TA. DHA status of vegetarians. beans and peas, nuts and seeds, and B-12, this can be remedied by appro- Prostaglandins Leukot Essent Fatty Acids. soy products as plant-based choices in priate planning. Compared to nonveg- 2009;81(2-3):137-141. the protein food group, as well as eggs etarian diets, vegetarian diets can 12. Sarter B, Kelsey KS, Schwartz TA, et al. for ovo-vegetarians.115 Fortified soy provide protection against many Blood docosahexaenoic acid and eicosa- ’ pentaenoic acid in vegans: Associations milk is listed as an alternative for cow s chronic diseases, such as heart disease, with age and gender and effects of an milk and calcium-fortified foods (jui- hypertension, type 2 diabetes, obesity, algal-derived omega-3 fatty acid sup- ces, cereals, breads, , and and some cancers. Furthermore, a plement. Clin Nutr. 2015;34(2):212-218. almond milk), as well as kale, are sug- vegetarian diet could make more con- 13. Gibson RA, Muhlhausler B, Makrides M. gested as calcium choices.116,117 Vegan servative use of natural resources and Conversion of linoleic acid and alpha- linolenic acid to long-chain poly- food guides, all modeled on the US cause less environmental degradation. unsaturated fatty acids (LCPUFAs), with Department of Agriculture’s Choose- Greater educational resources are a focus on pregnancy, lactation and the fi MyPlate, are available online, and available today, and RDNs and NDTRs rst 2 years of life. Matern Child Nutr. 2011;7(suppl 2):17-26. include specifications regarding sour- have more current information on 14. Rosell MS, Lloyd-Wright Z, Appleby PN, ces of calcium, vitamin B-12, iodine, vegetarian diets to better assist the et al. Long-chain n-3 polyunsaturated and n-3 fatty acids (www.vrg.org/ general public and vegetarian clients in fatty acids in plasma in British meat- nutshell/MyVeganPlate.pdf; www. making well-informed decisions about eating, vegetarian, and vegan men. Am becomingvegan.ca/food-guide; www. their nutritional health. J Clin Nutr. 2005;82(2):327-334. theveganrd.com/food-guide-for-vegans). 15. Orlich MJ, Singh PN, Sabaté J, et al. Vegetarian dietary patterns and mortal- Evidence-based RDN consumer and References ity in Adventist Health Study 2. JAMA professional resources are available 1. Stahler C. How often do Americans eat Intern Med. 2013;173(13):1230-1238. through the Vegetarian Nutrition vegetarian meals? And how many adults 16. Van Dokkum W. Significance of iron in the US are vegetarian? The Vegetarian Dietetic Practice Group’s website bioavailability for iron recommendations. Resource Group website. http://www. Biol Trace Elem Res. 1992;35(1):1-11. (www.vegetariannutrition.net). These vrg.org/nutshell/Polls/2016_adults_veg. resources are regularly updated and htm. Accessed June 23, 2016. 17. Rizzo NS, Jaceldo-Siegl K, Sabate J, Fraser GE. Nutrient profiles of vegetarian provide information on critical nutri- 2. Hoek AC, Luning PA, Weijzen P, and nonvegetarian dietary patterns. ents and lifecycle issues in plant-based Engels W, Kok FJ, de Graaf C. Replace- J Acad Nutr Diet. 2013;113(12):1610- ment of meat by meat substitutes. A 1619. diets. survey on person- and product-related Figure 2 lists useful websites that factors in consumer acceptance. Appe- 18. Park SK, Ryoo JH, Kim MG, Shin JY. As- tite. 2011;56(3):662-673. sociation of serum ferritin and the promote and encourage appropriate development of in 3. American Institute for Cancer Research. evidence-based recommendations and middle-aged Korean men: A 5-year Recommendations for cancer preven- follow-up study. Diabetes Care. food choices for both the RDN and tion. http://www.aicr.org/reduce-your- 2012;35(12):2521-2526. clientele. Further recommendations cancer-risk/recommendations-for-can cer-prevention/recommendations_04_ 19. Craig WJ. Iron status of vegetarians. Am J can be found at the Evidence Analysis ¼ fi plant_based.html?gclid CJ6__O7dpboCF Clin Nutr. 1994;59(5 suppl):1233S- Library, a free bene t to all Academy of cid4AodhkMAIA. Accessed June 23, 1237S. Nutrition and Dietetics members. In 2016. 20. Collings R, Harvey LJ, Hooper L, et al. The addition, all RDNs have ethical obliga- 4. US Department of Agriculture, US absorption of iron from whole diets: A tions to respect vegetarian dietary Department of Health and Ser- systematic review. Am J Clin Nutr. vices. 2015-2020 Dietary Guidelines for 2013;98(1):65-81. patterns as they would any other di- Americans.8th ed. Washington, DC: US etary pattern. fi 21. Food and Nutrition Board, Institute of Government Printing Of ce; 2015. Medicine. Iron. In: Dietary References http://health.gov/dietaryguidelines/2015. Intake for , Vitamin K, Arsenic, Accessed June 23, 2016. Boron, , Copper, Iodine, Iron, CONCLUSIONS 5. US Department of Agriculture. Super- , , , Silicon, Interest in and appreciation for plant- Tracker. https://www.supertracker.usda. and Zinc.Washington,DC:The gov/default.aspx. Accessed June 23, National Academies Press; 2001:290-393. based diets continue to grow in the 2016. United States and other parts of 22. Hunt JR, Roughead ZK. Adaptation of 6. Institute of Medicine. Dietary reference iron absorption in men consuming diets the world as governmental agencies intakes for energy, , fiber, with high or low iron bioavailability. Am and various health and nutrition orga- fat, fatty acids, cholesterol, protein, and J Clin Nutr. 2000;71(1):94-102. nizations promote the regular use amino acids. http://www.nap.edu/ 23. Armah SM, Carriquiry A, Sullivan D, download.php?record_id¼10490. of plant foods. Abundant choices in Cook JD, Reddy MB. A complete diet- Accessed June 23, 2016. based algorithm for predicting the marketplace facilitate following 7. Mangels R, Messina V, Messina M. The nonheme iron absorption in adults. a plant-based diet. Well-designed Dietitian’s Guide to Vegetarian Diets. 3rd J Nutr. 2013;143(7):1136-1140.

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24. Hunt JR, Roughead ZK. Nonheme-iron The National Academies Press; 2011. 52. Turner-McGrievy GM, Barnard ND, absorption, fecal ferritin excretion, and www.nap.edu/download.php?record_id¼ Scialli AR. A two-year randomized blood indexes of iron status in women 13050. Accessed June 23, 2016. weight loss trial comparing a vegan diet consuming controlled lactoovovege- 39. Norris, J. recommendations. to a more moderate low-fat diet. Obesity. tarian diets for 8 weeks. Am J Clin Nutr. www.veganhealth.org/b12/rec. Accessed 2007;15(9):2276-2281. 1999;69(5):944-952. June 23, 2016. 53. Crowe FL, Appleby PN, Travis RC, Key TJ. 25. Foster M, Samman S. Vegetarian diets 40. Food and Nutrition Board, Institute of Risk of hospitalization or death from across the lifecycle: Impact on zinc Medicine. Dietary Reference Intakes for ischemic heart disease among British intake and status. Adv Food Nutr Res. 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Tang AL, Walker KZ, Wilcox G, Strauss BJ, Health; 1998. tematic review. Ann Nutr Metab. Ashton JF, Stojanovska L. Calcium 46. Schindler TH, Cardenas J, Prior JO. Rela- 2012;60(4):233-240. absorption in Australian osteopenic tionship between increasing body 60. Bradbury KE, Crowe FL, Appleby PN, post-menopausal women: An acute weight, insulin resistance, inflammation, Schmidt JA, Travis RC, Key TJ. Serum comparative study of fortified soymilk to adipocytokine , and coronary cir- concentrations of cholesterol, apolipo- cows’ milk. Asia Pac J Clin Nutr. culatory function. J Am Coll Cardiol. protein A-I and apolipoprotein B in a 2010;19(2):243-249. 2006;47(6):1188-1195. total of 1694 meat-eaters, fish-eaters, 33. Zhao Y, Martin BR, Weaver CM. Calcium 47. Tonstad S, Butler T, Yan R, Fraser GE. vegetarians and vegans. 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66. Aune D, Norat T, Romundstad P, Nutrition (EPIC): An observational study. 94. Breastfeeding and the use of human Vatten LJ. and refined grain Lancet. 2003;361(9368):1496-1501. milk. Pediatrics. 2012;129(3):e827-e841. consumption and the risk of type 2 dia- 81. Bernstein AM, Song M, Zhang X, et al. 95. Mangels AR, Messina V. Considerations betes: A systematic review and dose- Processed and unprocessed red meat in planning vegan diets: Infants. JAm response. Eur J Epidemiol. 2013;28(11): and risk of colorectal cancer: Analysis by Diet Assoc. 2001;101(6):670-677. 845-858. tumor location and modification by 96. Sabaté J, Wien M. Vegetarian diets and 67. Brighenti F, Benini L, Del Rio D, et al. time. PLoS One. 2015;10(8):e0135959. prevention. Am J Clin Colonic fermentation of indigestible 82. Rohrmann S, Overvad K, Bueno-de- Nutr. 2010;91(5):1525S-1529S. http:// contributes to the Mesquita HB, et al. Meat consumption ajcn.nutrition.org/content/91/5/1525S. second-meal effect. 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EPA Number 821B01001. https://www3. change mitigation and health effects of 115. US Department of Agriculture. All about epa.gov/npdes/pubs/cafo_proposed_env_ varied dietary patterns in real-life settings the protein foods group. http://www. assess_ch1-3.pdf. Published January 2001. throughout North America. Am J Clin Nutr. choosemyplate.gov/protein-foods. Upda- Accessed September 14, 2016. 2014;100(suppl 1):490S-495S. ted July 29, 2016. Accessed September 14, 2016. 110. Machovina B, Feeley KJ, Ripple WJ. 113. Cederberg C, Hedenus F, Wirsenius S, Biodiversity conservation: The key is Sonesson U. Trends in greenhouse gas 116. US Department of Agriculture. All about reducing meat consumption. Sci Total emissions from consumption and pro- the dairy group. http://www.choose Environ. 2015;536:419-431. duction of animal food products—Impli- .gov/dairy. Updated July 29, 111. Ripple WJ, Smith P, Haberl H, cations for long-term climate targets. 2016. Accessed September 14, 2016. Montzka SA, McAlpine C, Boucher DH. Animal. 2013;7(2):330-340. 117. US Department of Agriculture. Non- Ruminants, climate change and climate 114. Economou V, Gousia P. Agriculture and dairy sources of calcium. http://www. policy. Nat Climate Change.2014;4(1):2-5. food animals as a source of choosemyplate.gov/dairy-calcium-sources. 112. Soret S, Mejia A, Batech M, Jaceldo- antimicrobial-resistant bacteria. Infect Updated January 12, 2016. Accessed Siegl K, Harwatt H, Sabate J. Climate Drug Resist. 2015;8:49-61. September 14, 2016.

This Academy of Nutrition and Dietetics position was adopted by the House of Delegates Leadership Team on October 18, 1987 and reaffirmed on September 12, 1992; September 6, 1996; June 22, 2000; June 11, 2006; and March 19, 2012. This position is in effect until December 31, 2021. Position papers should not be used to indicate endorsement of products or services. All requests to use portions of the position or republish in its entirety must be directed to the Academy at [email protected]. Authors: , MS, RD (Consultant, , Canada); Winston Craig, PhD, MPH, RD (Andrews University, Berrien Springs, MI); Susan Levin, MS, RD, CSSD (Physicians Committee for Responsible Medicine, Washington, DC). STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors. FUNDING/SUPPORT There is no funding to disclose. Reviewers: and Environmental Nutrition dietetic practice group (Melissa Altman-Traub, MS, RDN, LDN, Community College of Phila- delphia, Philadelphia, PA); Catherine Conway, MS, RDN, CDN, CDE (YAI/National Institute for People with Disabilities, New York, New York); Sharon Denny, MS, RD (Academy Knowledge Center, Chicago, IL); Sarah Picklo Halabu, RDN, LDN, CDE (Academy Publications and Resources, Chicago, IL); D. Enette Larson-Meyer, PhD, RD, CSSD (University of Wyoming, Laramie, WY); Mark E. Rifkin, MS, RD (Academy Policy Initiatives & Advocacy, Washington, DC); Tamara Schryver, PhD, MS, RD (The Schwan Food Company, Minneapolis, MN); Alison Steiber, PhD, RD (Academy Research, International and Scientific Affairs, Chicago, IL); Vegetarian Nutrition dietetic practice group (John Westerdahl, PhD, MPH, RD, CNS, FAND, Bragg Health Foundation, Santa Barbara, CA). Academy Positions Committee Workgroup: Mary Ellen E. Posthauer, RDN, CD, LD, FAND (chair) (MEP Healthcare Dietary Services, Inc, Evansville, IN); Ainsley Malone, MS, RD, LD, CNSC, FAND, FASPEN (American Society for Parenteral and Enteral Nutrition, New Albany, OH); Joan Sabate, MD, DrPH (content advisor) (Loma Linda University, Loma Linda, CA). The authors thank the reviewers for their many constructive comments and suggestions. The reviewers were not asked to endorse this position or the supporting paper.

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