from the association

Position of the American Dietetic Association: Vegetarian Diets

ABSTRACT This American Dietetic Association (ADA) position paper includes the It is the position of the American Di- authors’ independent review of the literature in addition to systematic etetic Association that appropriately review conducted using the ADA’s Evidence Analysis Process and informa- planned vegetarian diets, including tion from the Evidence Analysis Library. Topics from the Evidence Analysis total vegetarian or vegan diets, are Library are clearly delineated. The use of an evidence-based approach healthful, nutritionally adequate, and provides important added benefits to earlier review methods. The major may provide health benefits in the advantage of the approach is the more rigorous standardization of review prevention and treatment of certain criteria, which minimizes the likelihood of reviewer bias and increases the diseases. Well-planned vegetarian di- ease with which disparate articles may be compared. For a detailed descrip- ets are appropriate for individuals tion of the methods used in the evidence analysis process, access ADA’s during all stages of the life cycle, in- Evidence Analysis Process at http://adaeal.com/eaprocess/. cluding pregnancy, lactation, infancy, Conclusion Statements are assigned a grade by an expert work group childhood, and adolescence, and for based on the systematic analysis and evaluation of the supporting research athletes. A vegetarian diet is defined evidence. Grade IϭGood; Grade IIϭFair; Grade IIIϭLimited; Grade as one that does not include meat (in- IVϭExpert Opinion Only; and Grade VϭNot Assignable (because there is cluding fowl) or seafood, or products no evidence to support or refute the conclusion). containing those foods. This article Evidence-based information for this and other topics can be found at reviews the current data related to https://www.adaevidencelibrary.com and subscriptions for nonmembers are key nutrients for vegetarians includ- available for purchase at https://www.adaevidencelibrary.com/store.cfm. ing protein, n-3 fatty acids, iron, zinc, iodine, calcium, and vitamins D and B-12. A vegetarian diet can meet cur- cals. The variability of dietary practices or products containing these foods. rent recommendations for all of these among vegetarians makes individual The eating patterns of vegetarians nutrients. In some cases, supplements assessment of dietary adequacy essen- may vary considerably. The lacto-ovo- or fortified foods can provide useful tial. In addition to assessing dietary ad- vegetarian eating pattern is based on amounts of important nutrients. An ev- equacy, food and nutrition profession- grains, vegetables, fruits, legumes, idence-based review showed that veg- als can also play key roles in educating seeds, nuts, dairy products, and eggs. etarian diets can be nutritionally ad- vegetarians about sources of specific The lacto-vegetarian excludes eggs equate in pregnancy and result in nutrients, food purchase and prepara- as well as meat, fish, and fowl. The positive maternal and infant health tion, and dietary modifications to meet vegan, or total vegetarian, eating pat- outcomes. The results of an evidence- their needs. tern excludes eggs, dairy, and other based review showed that a vegetar- J Am Diet Assoc. 2009;109: animal products. Even within these ian diet is associated with a lower risk 1266-1282. patterns, considerable variation may of death from ischemic heart disease. exist in the extent to which animal Vegetarians also appear to have lower POSITION STATEMENT products are excluded. low-density lipoprotein cholesterol lev- It is the position of the American Di- Evidence-based analysis was used els, lower blood pressure, and lower etetic Association that appropriately to evaluate existing research on types rates of hypertension and type 2 diabe- planned vegetarian diets, including of vegetarian diets (1). One question tes than nonvegetarians. Furthermore, total vegetarian or vegan diets, are for evidence-analysis was identified: vegetarians tend to have a lower body healthful, nutritionally adequate, and What types of vegetarian diets are mass index and lower overall cancer may provide health benefits in the pre- examined in the research? The com- rates. Features of a vegetarian diet vention and treatment of certain dis- plete results of this evidence-based that may reduce risk of chronic disease eases. Well-planned vegetarian diets analysis can be found on the Ameri- include lower intakes of saturated fat are appropriate for individuals during can Dietetic Association’s Evidence and cholesterol and higher intakes of all stages of the lifecycle, including Analysis Library (EAL) Web site fruits, vegetables, whole grains, nuts, pregnancy, lactation, infancy, child- (www.adaevidencelibrary.com) and soy products, fiber, and phytochemi- hood, and adolescence, and for athletes. are summarized below. EAL Conclusion Statement: The two VEGETARIAN DIETS IN PERSPECTIVE most common ways of defining vege- 0002-8223/09/10907-0019$36.00/0 A vegetarian is a person who does not tarian diets in the research are vegan doi: 10.1016/j.jada.2009.05.027 eat meat (including fowl) or seafood, diets: Diets devoid of all flesh foods;

1266 Journal of the AMERICAN DIETETIC ASSOCIATION © 2009 by the American Dietetic Association and vegetarian diets: Diets devoid of erations, concern for the environ- ketplace with new levels of fortifica- all flesh foods, but also include egg ment, and animal welfare factors. tion. These products and dietary sup- (ovo) and/or dairy (lacto) products. Vegetarians also cite economic rea- plements, which are widely available in However, these very broad cat- sons, ethical considerations, world supermarkets and natural foods stores, egories mask important variations hunger issues, and religious beliefs as can add substantially to vegetarians’ within vegetarian diets and dietary their reasons for following their cho- intakes of key nutrients such as cal- practices. These variations within sen eating pattern. cium, iron, zinc, vitamin B-12, vitamin vegetarian diets make absolute cat- D, riboflavin, and long-chain n-3 fatty egorization of vegetarian dietary acids. With so many fortified products practices difficult and may be one of Consumer Trends available today, the nutritional status the sources of unclear relationships In 2006, based on a nationwide poll, of the typical vegetarian today would between vegetarian diets and other approximately 2.3% of the US adult be expected to be greatly improved Fair. population (4.9 million people) consis- from that of a vegetarian 1 to 2 decades؍factors. Grade II In this article, the term vegetarian tently followed a vegetarian diet, ago. This improvement would be will be used to refer to people choosing stating that they never ate meat, fish, enhanced by the greater awareness a lacto-ovo-, lacto-, or vegan vegetarian or poultry (2). About 1.4% of the US among the vegetarian population of diet unless otherwise specified. adult population was vegan (2). In what constitutes a balanced vegetarian Whereas lacto-ovo-, lacto-, and 2005, according to a nationwide poll, diet. Consequently older research data vegan-vegetarian diets are those 3% of 8- to 18-year-old children and may not represent the nutritional sta- most commonly studied, practitioners adolescents were vegetarian; close to tus of present-day vegetarians. may encounter other types of vegetar- 1% were vegan (3). ian or near-vegetarian diets. For ex- Many consumers report an interest ample, people choosing macrobiotic in vegetarian diets (4) and 22% report Health Implications of Vegetarian Diets diets typically describe their diet as regular consumption of meatless sub- Vegetarian diets are often associated vegetarian. The macrobiotic diet is stitutes for meat products (5). Addi- with a number of health advantages, based largely on grains, legumes, and tional evidence for the increasing in- including lower blood cholesterol levels, vegetables. Fruits, nuts, and seeds terest in vegetarian diets includes the lower risk of heart disease, lower blood are used to a lesser extent. Some peo- emergence of college courses on vege- pressure levels, and lower risk of hy- ple following a macrobiotic diet are tarian nutrition and on animal rights; pertension and type 2 diabetes. Vege- not truly vegetarian because they eat the proliferation of Web sites, period- tarians tend to have a lower body mass limited amounts of fish. The tradi- icals, and cookbooks with a vegetar- index (BMI) and lower overall cancer tional Asian-Indian diet is predomi- ian theme; and the public’s attitude rates. Vegetarian diets tend to be lower nantly plant based and is frequently toward ordering a vegetarian meal in saturated fat and cholesterol, and lacto-vegetarian although changes of- when eating away from home. have higher levels of dietary fiber, mag- ten occur with acculturation, includ- Restaurants have responded to this nesium and potassium, vitamins C and ing greater consumption of cheese interest in vegetarian diets. A survey E, folate, carotenoids, flavonoids, and and a movement away from a vege- of chefs found that vegetarian dishes other phytochemicals. These nutri- tarian diet. A raw foods diet may be a were considered “hot” or “a perennial tional differences may explain some of vegan diet, consisting mainly or ex- favorite” by 71%; vegan dishes by 63% the health advantages of those follow- clusively of uncooked and unproc- (6). Fast-food restaurants are begin- ing a varied, balanced vegetarian diet. essed foods. Foods used include fruits, ning to offer salads, veggie burgers, However, vegans and some other vege- vegetables, nuts, seeds, and sprouted and other meatless options. Most uni- tarians may have lower intakes of vita- grains and beans; in rare instances versity foodservices offer vegetarian min B-12, calcium, vitamin D, zinc, and unpasteurized dairy products and options. long-chain n-3 fatty acids. even raw meat and fish may be used. Recently, outbreaks of food-borne ill- Fruitarian diets are vegan diets ness associated with the consumption based on fruits, nuts, and seeds. Veg- New Product Availability of domestically grown and imported etables that are classified botanically The US market for processed vegetar- fresh fruits, sprouts, and vegetables as fruits like avocado and tomatoes ian foods (foods like meat analogs, that have been contaminated by Sal- are commonly included in fruitarian nondairy milks, and vegetarian en- monella, Escherichia coli, and other diets; other vegetables, grains, beans, trees that directly replace meat or micro-organisms have been seen. and animal products are excluded. other animal products) was estimated Health advocacy groups are calling for Some people will describe them- to be $1.17 billion in 2006 (7). This stricter inspection and reporting proce- selves as vegetarian but will eat fish, market is forecast to grow to $1.6 bil- dures and better food-handling prac- chicken, or even meat. These self-de- lion by 2011 (7). tices. scribed vegetarians may be identified The availability of new products, in- in research studies as semivegetarians. cluding fortified foods and convenience Individual assessment is required to foods, would be expected to have an NUTRITION CONSIDERATIONS FOR accurately evaluate the nutritional impact on the nutrient intake of vege- VEGETARIANS quality of the diet of a vegetarian or a tarians who choose to eat these foods. Protein self-described vegetarian. Fortified foods such as soy milks, meat Plant protein can meet protein re- Common reasons for choosing a analogs, juices, and breakfast cereals quirements when a variety of plant vegetarian diet include health consid- are continually being added to the mar- foods is consumed and energy needs

July 2009 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1267 are met. Research indicates that an development. The bioconversion of sorption have been short term, there assortment of plant foods eaten over ␣-linolenic acid (ALA), a plant-based is evidence that adaptation to low in- the course of a day can provide all n-3 fatty acid, to EPA is generally less takes takes place over the long term, essential amino acids and ensure ad- than 10% in humans; conversion of and involves both increased absorp- equate nitrogen retention and use in ALA to DHA is substantially less (14). tion and decreased losses (27,28). In- healthy adults; thus, complementary Vegetarians, and particularly vegans, cidence of iron-deficiency anemia proteins do not need to be consumed tend to have lower blood levels of EPA among vegetarians is similar to that at the same meal (8). and DHA than nonvegetarians (15). of nonvegetarians (12,29). Although A meta-analysis of nitrogen bal- DHA supplements derived from mi- vegetarian adults have lower iron ance studies found no significant dif- croalgae are well absorbed and posi- stores than nonvegetarians, their se- ference in protein needs due to the tively influence blood levels of DHA, rum ferritin levels are usually within source of dietary protein (9). Based on and also EPA through retroconver- the normal range (29,30). the protein digestibility-corrected sion (16). Soy milk and breakfast amino acid score, which is the stan- bars, fortified with DHA, are now dard method for determining protein available in the marketplace. Zinc quality, other studies have found that The Dietary Reference Intakes rec- The bioavailability of zinc from vege- although isolated soy protein can ommend intakes of 1.6 and 1.1 g ALA tarian diets is lower than from nonveg- meet protein needs as effectively as per day, for men and women, respec- etarian diets, mainly due to the higher animal protein, wheat protein eaten tively (17). These recommendations phytic acid content of vegetarian diets alone, for example, may result in a may not be optimal for vegetarians (31). Thus, zinc requirements for some reduced efficiency of nitrogen utiliza- who consume little if any DHA and vegetarians whose diets consist mainly tion (10). Thus, estimates of protein EPA (17) and thus may need addi- of phytate-rich unrefined grains and le- requirements of vegans may vary, de- tional ALA for conversion to DHA and gumes may exceed the Recommended pending to some degree on dietary EPA. Conversion rates for ALA tend Dietary Allowance (26). Zinc intakes of choices. Food and nutrition profes- to improve when dietary n-6 levels vegetarians vary with some research sionals should be aware that protein are not high or excessive (14). Vege- showing zinc intakes near recommen- needs might be somewhat higher tarians should include good sources of dations (32) and other research finding than the Recommended Dietary Al- ALA in their diet, such as flaxseed, zinc intakes of vegetarians signifi- lowance in those vegetarians whose walnuts, canola oil, and soy. Those cantly below recommendations (29,33). dietary protein sources are mainly with increased requirements of n-3 Overt zinc deficiency is not evident in those that are less well digested, such fatty acids, such as pregnant and lac- Western vegetarians. Due to the diffi- as some cereals and legumes (11). tating women, may benefit from culty in evaluating marginal zinc sta- Cereals tend to be low in lysine, an DHA-rich microalgae (18). tus, it is not possible to determine the essential amino acid (8). This may be possible effect of lower zinc absorption relevant when evaluating diets of in- from vegetarian diets (31). Zinc sources dividuals who do not consume animal Iron include soy products, legumes, grains, protein sources and when diets are The iron in plant foods is nonheme cheese, and nuts. Food preparation relatively low in protein. Dietary ad- iron, which is sensitive to both inhibi- techniques, such as soaking and justments such as the use of more tors and enhancers of iron absorption. sprouting beans, grains, and seeds as beans and soy products in place of Inhibitors of iron absorption include well as leavening bread, can reduce other protein sources that are lower phytates, calcium, and the polypheno- binding of zinc by phytic acid and in- in lysine or an increase in dietary pro- lics in tea, coffee, herb teas, and cocoa. crease zinc bioavailability (34). Organic tein from all sources can ensure an Fiber only slightly inhibits iron absorp- acids, such as citric acid, can also en- adequate intake of lysine. tion (19). Some food preparation tech- hance zinc absorption to some extent Although some vegan women have niques such as soaking and sprouting (34). protein intakes that are marginal, beans, grains, and seeds, and the leav- typical protein intakes of lacto-ovo- ening of bread, can diminish phytate vegetarians and of vegans appear to levels (20) and thereby enhance iron Iodine meet and exceed requirements (12). absorption (21,22). Other fermentation Some studies suggest that vegans Athletes can also meet their protein processes, such as those used to make who do not consume key sources of needs on plant-based diets (13). miso and tempeh, may also improve iodine, such as iodized salt or sea veg- iron bioavailability (23). etables, may be at risk for iodine de- Vitamin C and other organic acids ficiency, because plant-based diets n-3 Fatty Acids found in fruits and vegetables can are typically low in iodine (12,35). Sea Whereas vegetarian diets are gener- substantially enhance iron absorp- salt and kosher salt are generally not ally rich in n-6 fatty acids, they may tion and reduce the inhibitory effects iodized nor are salty seasonings such be marginal in n-3 fatty acids. Diets of phytate and thereby improve iron as tamari. Iodine intake from sea veg- that do not include fish, eggs, or gen- status (24,25). Because of lower bio- etables should be monitored because erous amounts of algae generally are availability of iron from a vegetarian the iodine content of sea vegetables low in eicosapentaenoic acid (EPA) diet, the recommended iron intakes varies widely and some contain sub- and docosahexaenoic acid (DHA), for vegetarians are 1.8 times those of stantial amounts of iodine (36). fatty acids important for cardiovascu- nonvegetarians (26). Foods such as soybeans, cruciferous lar health as well as eye and brain Whereas many studies of iron ab- vegetables, and sweet potatoes con-

1268 July 2009 Volume 109 Number 7 tain natural goitrogens. These foods has shown that calcium availability is not regularly consuming reliable have not been associated with thyroid substantially less when tricalcium sources of vitamin B-12 (12,46,47). insufficiency in healthy people pro- phosphate is used to fortify the soy Lacto-ovo-vegetarians can obtain ad- vided iodine intake is adequate (37). beverage (40). Fortified foods such as equate vitamin B-12 from dairy foods, fruit juices, soy milk, and rice milk, eggs, or other reliable vitamin B-12 and breakfast cereals can contribute sources (fortified foods and supple- Calcium significant amounts of dietary cal- ments), if regularly consumed. For Calcium intakes of lacto-ovo-vegetar- cium for the vegan (41). Oxalates in vegans, vitamin B-12 must be ob- ians are similar to, or higher than, some foods, such as spinach and tained from regular use of vitamin those of nonvegetarians (12), whereas Swiss chard, greatly reduce calcium B-12-fortified foods, such as fortified intakes of vegans tend to be lower absorption, making these vegetables soy and rice beverages, some break- than both groups and may fall below a poor source of usable calcium. Foods fast cereals and meat analogs, or Red recommended intakes (12). In the Ox- rich in phytate may also inhibit cal- Star Vegetarian Support Formula nu- ford component of the European Pro- cium absorption tritional yeast; otherwise a daily vita- spective Investigation into Cancer min B-12 supplement is needed. No and Nutrition (EPIC-Oxford) study, unfortified plant food contains any the risk of bone fracture was similar Vitamin D significant amount of active vitamin for lacto-ovo-vegetarians and meat Vitamin D has long been known to B-12. Fermented soy products cannot eaters, whereas vegans had a 30% play a role in bone health. Vitamin D be considered a reliable source of ac- higher risk of fracture possibly due to status depends on sunlight exposure tive B-12 (12,46). their considerably lower mean cal- and intake of vitamin D–fortified Vegetarian diets are typically rich cium intake (38). Diets rich in meat, foods or supplements. The extent of in folacin, which may mask the hema- fish, dairy products, nuts, and grains cutaneous vitamin D production fol- tological symptoms of vitamin B-12 produce a high renal acid load, lowing sunlight exposure is highly deficiency, so that vitamin B-12 defi- mainly due to sulfate and phosphate variable and is dependent on a num- ciency may go undetected until after residues. Calcium resorption from ber of factors, including the time of neurological signs and symptoms bone helps to buffer this acid load, day, season, latitude, skin pigmenta- may be manifest (47). Vitamin B-12 resulting in increased urinary losses tion, sunscreen use, and age. Low vi- status is best determined by measur- of calcium. A high sodium intake can tamin D intakes (42), low serum 25- ing serum levels of homocysteine, also promote urinary calcium losses. hydroxyvitamin D levels (12), and methylmalonic acid, or holotransco- On the other hand, fruits and vegeta- reduced bone mass (43) have been re- balamin II (48). bles rich in potassium and magne- ported in some vegan and macrobiotic sium produce a high renal alkaline groups who did not use vitamin D load which slows bone calcium resorp- supplements or fortified foods. VEGETARIAN DIETS THROUGHOUT THE tion, and decreases calcium losses in Foods that are fortified with vita- LIFE CYCLE the urine. In addition, some studies min D include cow’s milk, some show that the ratio of dietary calcium brands of soy milk, rice milk, and or- Well-planned vegan, lacto-vegetarian, to protein is a better predictor of bone ange juice, and some breakfast cere- and lacto-ovo-vegetarian diets are ap- health than calcium intake alone. als and margarines. Both vitamin D-2 propriate for all stages of the life cycle, Typically, this ratio is high in lacto- and vitamin D-3 are used in supple- including pregnancy and lactation. Ap- ovo-vegetarian diets and favors bone ments and to fortify foods. Vitamin propriately planned vegan, lacto-vege- health, whereas vegans have a ratio D-3 (cholecalciferol) is of animal ori- tarian, and lacto-ovo-vegetarian diets of calcium to protein that is similar to gin and is obtained through the ultra- satisfy nutrient needs of infants, chil- or lower than that of nonvegetarians violet irradiation of 7-dehydrocholes- dren, and adolescents and promote nor- (39). Many vegans may find it is eas- terol from lanolin. Vitamin D-2 mal growth (49-51). Figure 1 provides ier to meet their calcium needs if cal- (ergocalciferol) is produced from the specific suggestions for meal planning cium-fortified foods or dietary supple- ultraviolet irradiation of ergosterol for vegetarian diets. Lifelong vegetari- ments are utilized (39). from yeast and is acceptable to veg- ans have adult height, weight, and Low-oxalate greens (eg, bok choy, ans. Although some research sug- BMIs that are similar to those who be- broccoli, Chinese cabbage, collards, gests that vitamin D-2 is less effective came vegetarian later in life, suggest- and kale) and fruit juices fortified than vitamin D-3 in maintaining se- ing that well-planned vegetarian diets with calcium citrate malate are good rum 25-hydroxyvitamin D levels (44) in infancy and childhood do not affect sources of highly bioavailable calcium other studies find that vitamin D-2 final adult height or weight (53). Vege- (50% to 60% and 40% to 50%, respec- and vitamin D-3 are equally effective tarian diets in childhood and adoles- tively), while calcium-set tofu, and (45). If sun exposure and intake of cence can aid in the establishment of cow’s milk have good bioavailability fortified foods are insufficient to meet lifelong healthful eating patterns and of calcium (about 30% to 35%), and needs, vitamin D supplements are can offer some important nutritional sesame seeds, almonds, and dried recommended. advantages. Vegetarian children and beans have a lower bioavailability adolescents have lower intakes of cho- (21% to 27%) (39). The bioavailability lesterol, saturated fat, and total fat and of calcium from soy milk fortified with Vitamin B-12 higher intakes of fruits, vegetables, and calcium carbonate is equivalent to The vitamin B-12 status of some veg- fiber than nonvegetarians (54,55). Veg- cow’s milk although limited research etarians is less than adequate due to etarian children have also been re-

July 2009 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1269 EAL Conclusion Statement: No research A variety of menu planning approaches can provide adequate nutrition for vegetarians. was identified that focused on the birth The Dietary Reference Intakes are a valuable resource for food and nutrition professionals. outcomes of vegan vs omnivorous .Not Assignable؍Various food guides (41,52) can be used when working with vegetarian clients. In addition, the mothers. Grade V following guidelines can help vegetarians plan healthful diets: ● Choose a variety of foods, including whole grains, vegetables, fruits, legumes, nuts, seeds, Micronutrient Intake. Based on 10 stud- and, if desired, dairy products, and eggs. ies (58-60,63-69), two of which were ● Minimize intake of foods that are highly sweetened, high in sodium, and high in fat, conducted in the United States (64,65), especially saturated fat and trans-fatty acids. only the following micronutrients had ● Choose a variety of fruits and vegetables. lower intake among vegetarians than ● If animal foods such as dairy products and eggs are used, choose lower-fat dairy products nonvegetarians: and use both eggs and dairy products in moderation. ● Use a regular source of vitamin B-12 and, if sunlight exposure is limited, of vitamin D. ● vitamin B-12; ● vitamin C; Figure 1. Suggestions for planning vegetarian meals. ● calcium; and ● zinc. ported to be leaner and to have lower Macronutrient and Energy Intake. Four Vegetarians did not meet dietary serum cholesterol levels (50,56). primary research studies were identi- standard (in at least one country) for: fied that examined maternal macro- ● vitamin B-12 (in the United King- nutrient intake during lacto-ovo- or Pregnant and Lactating Women dom); lacto- vegetarian pregnancy (58-61). ● iron (in the United States, for both The nutrient and energy needs of None focused on pregnant vegans. vegetarians and omnivores); pregnant and lactating vegetarian EAL Conclusion Statement: Limited re- ● folate (in Germany, though lower women do not differ from those of search on non-US populations indi- rate of deficiency than among omni- nonvegetarian women with the excep- cates that the macronutrient intake vores); and tion of higher iron recommendations of pregnant vegetarians is similar to ● zinc (in the United Kingdom). for vegetarians. Vegetarian diets can that of nonvegetarians with the fol- ؍be planned to meet the nutrient needs lowing exceptions (as percentages of EAL Conclusion Statement: Grade III of pregnant and lactating women. Ev- energy intake): Limited. idence-based analysis of the research literature was used to evaluate exist- Micronutrient Bioavailability. Six studies ● pregnant vegetarians receive statis- ing research on vegetarian pregnancy (five non-US, one with combined US tically lower levels of protein than (57). Seven questions for evidence- and non-US samples; all but one of pos- pregnant nonvegetarians; and analysis were identified: itive quality) were identified that ex- ● pregnant vegetarians receive statis- amined the bioavailability of different tically higher levels of carbohydrates ● micronutrients in vegetarian vs non- How do macronutrient and energy than pregnant nonvegetarians. intake in pregnant vegetarians dif- vegetarian pregnant women (58,63,64, fer from intakes in pregnant omni- 66,67,69). Of the micronutrients exam- vores? It is important to note, however, ined in the research, only serum B-12 ● Are birth outcomes different for that none of the studies report a clin- levels were significantly lower in non- mothers who maintain a vegetarian ically significant difference in macro- vegan-vegetarians than nonvegetar- vs an omnivorous diet during preg- nutrient intake. In other words, none ians. In addition, one study reported nancy? of the studies report a protein defi- that lower B-12 levels are more likely ● ciency in pregnant vegetarians. to be associated with high serum total ؍ How do macronutrient and energy intake in pregnant vegans differ Grade III Limited. homocysteine in lacto-ovo-vegetarians from intakes in pregnant omnivores? EAL Conclusion Statement: No research than low meat eaters or omnivores. ● Are birth outcomes different for was identified that focused on macro- Whereas zinc levels were not signifi- mothers who maintain a vegan vs nutrient intakes among pregnant veg- cantly different between nonvegan- -Not Assignable. vegetarians and nonvegetarians, vege؍an omnivorous diet during preg- ans. Grade V nancy? tarians who have a high intake of ● What are patterns of micronutrient Birth Outcomes. Four cohort studies calcium may be at risk for zinc defi- intake among pregnant vegetarians? were identified that examined the rela- ciency (because of the interaction be- ● What is the bioavailability of differ- tionship between maternal macronu- tween phytate, calcium, and zinc). ent micronutrients in pregnant veg- trient intake during pregnancy and Based on limited evidence, plasma fo- etarians? birth outcomes such as birth weight late levels may actually be higher ● What are birth outcomes associated and length (59-62). None of the studies among some vegetarian groups than with the micronutrient intake of focused on pregnant vegans. nonvegetarians. ؍maternal vegetarian diets? EAL Conclusion Statement: Limited re- EAL Conclusion Statement: Grade III search on non-US populations indi- Limited. The complete results of this evidence- cates that there are no significant based analysis can be found on the EAL health differences in babies born to Micronutrients and Birth Outcome EAL Con- Web site (www.adaevidencelibrary.com) nonvegan vegetarian mothers vs non- clusion Statement: Limited evidence Limited. from seven studies (all outside the؍and are summarized below. vegetarians. Grade III

1270 July 2009 Volume 109 Number 7 United States) indicated that the mi- with ALA, a DHA precursor, in preg- take of vitamin B-12 should receive a cronutrient content of a balanced ma- nancy and lactation has not been vitamin B-12 supplement (51). Zinc ternal vegetarian diet does not have shown to be effective in increasing in- intake should be assessed and zinc detrimental outcomes for the health fant DHA levels or breast milk DHA supplements or zinc-fortified foods of the child at birth (58-63,69). There concentration (74,75). used when complementary foods are may be, however, a risk for a false introduced if the diet is low in zinc or positive diagnosis of Down syndrome mainly consists of foods with low zinc in the fetus when maternal serum Infants bioavailability (76). free beta-human chorionic gonadotro- Growth of young vegetarian infants pin and alpha fetoprotein levels are receiving adequate amounts of breast used as markers in vegetarian moth- milk or commercial infant formula is Children -Limited. normal. When solid foods are intro- Growth of lacto-ovo-vegetarian chil؍ers. Grade III Nutrition Considerations. Results of evi- duced, provision of good sources of en- dren is similar to that of their nonveg- dence-based analysis suggest that ergy and nutrients can ensure normal etarian peers (50). Little information vegetarian diets can be nutritionally growth. The safety of extremely re- about the growth of nonmacrobiotic adequate in pregnancy and can lead strictive diets such as fruitarian and vegan children has been published. to a positive birth outcome (57). raw foods diets has not been studied Some studies suggest that vegan chil- Key nutrients in pregnancy include in children. These diets can be very dren tend to be slightly smaller but vitamin B-12, vitamin D, iron, and low in energy, protein, some vita- within the normal ranges of the stan- folate whereas key nutrients in lacta- mins, and some minerals and cannot dards for weight and height (58). Poor growth in children has primarily been tion include vitamin B-12, vitamin D, be recommended for infants and chil- seen in those on very restricted calcium, and zinc. Diets of pregnant dren. diets (77). and lactating vegetarians should con- Breastfeeding is common in vege- Frequent meals and snacks and the tain reliable sources of vitamin B-12 tarian women, and this practice should be supported. The breast milk use of some refined foods (such as for- daily. Based on recommendations for of vegetarian women is similar in tified breakfast cereals, breads, and pregnancy and lactation, if there is composition to that of nonvegetarians pasta) and foods higher in unsatur- concern about vitamin D synthesis and is nutritionally adequate. Com- ated fats can help vegetarian children because of limited sunlight exposure, mercial infant formulas should be meet energy and nutrient needs. Av- skin tone, season, or sunscreen use, used if infants are not breastfed or erage protein intakes of vegetarian pregnant and lactating women should are weaned before 1 year of age. Soy children (lacto-ovo, vegan, and macro- use vitamin D supplements or vita- formula is the only option for non- biotic) generally meet or exceed rec- min D–fortified foods. No studies breastfed vegan infants. Other prep- ommendations (12). Vegan children included in the evidence-analysis ex- arations including soymik, rice milk, may have slightly higher protein amined vitamin D status during veg- and homemade formulas should not needs because of differences in pro- etarian pregnancy. Iron supplements be used to replace breast milk or com- tein digestibility and amino acid com- may be needed to prevent or treat mercial infant formula. position (49,78) but these protein iron-deficiency anemia, which is com- Solid foods should be introduced in needs are generally met when diets mon in pregnancy. Women capable of the same progression as for nonveg- contain adequate energy and a vari- becoming pregnant as well as women etarian infants, replacing strained ety of plant foods. in the periconceptional period are ad- meat with mashed or pureed tofu, le- Food guides for vegetarian children ␮ vised to consume 400 g folate daily gumes (pureed and strained if neces- have been published elsewhere (12). from supplements, fortified foods, or sary), soy or dairy yogurt, cooked egg both. Zinc and calcium needs can be yolk, and cottage cheese. Later, met through food or supplement around 7 to 10 months, foods such as Adolescents sources as identified in earlier sec- cubed tofu, cheese, or soy cheese and Growth of lacto-ovo-vegetarian and tions on these nutrients. bite-size pieces of veggie burgers can nonvegetarian adolescents is similar DHA also plays a role in pregnancy be started. Commercial, full-fat, forti- (50). Earlier studies suggest that veg- and lactation. Infants of vegetarian fied soy milk or pasteurized cow’s etarian girls reach menarche slightly mothers appear to have lower cord milk can be used as a primary bever- later than nonvegetarians (79); more and plasma DHA than do infants of age starting at age 1 year or older for recent studies find no difference in nonvegetarians (70). Breast milk a child who is growing normally and age at menarche (53,80). DHA is lower in vegans and lacto-ovo- eating a variety of foods (51). Foods Vegetarian diets appear to offer vegetarians than in nonvegetarians that are rich in energy and nutrients some nutritional advantages for ado- (71). Because of DHA’s beneficial ef- such as legume spreads, tofu, and lescents. Vegetarian adolescents are fects on gestational length, infant vi- mashed avocado should be used when reported to consume more fiber, iron, sual function, and neurodevelopment, the infant is being weaned. Dietary folate, vitamin A, and vitamin C than pregnant and lactating vegetarians fat should not be restricted in chil- nonvegetarians (54,81). Vegetarian and vegans should choose food dren younger than 2 years. adolescents also consume more fruits sources of DHA (fortified foods or eggs Guidelines for dietary supplements and vegetables, and fewer sweets, from hens fed DHA-rich microalgae) generally follow those for nonvegetar- fast foods, and salty snacks compared or use a microalgae-derived DHA sup- ian infants. Breastfed infants whose to nonvegetarian adolescents (54,55). plement (72,73). Supplementation mothers do not have an adequate in- Key nutrients of concern for adoles-

July 2009 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1271 cent vegetarians include calcium, vi- ian diets and exercise. The position of ence in risk persists even after adjust- tamin D, iron, zinc, and vitamin B-12. American Dietetic Association and Di- ment for BMI, other aspects of a veg- Being vegetarian does not cause etitians of Canada on nutrition and etarian diet may be responsible for disordered eating as some have sug- athletic performance provides addi- the risk reduction, above and beyond gested although a vegetarian diet tional information specific to vegetar- that which would be expected due to may be selected to camouflage an ex- ian athletes (90). Research is needed on lower BMI. isting eating disorder (82). Because of the relation between vegetarian diet EAL Conclusion Statement: A vegetar- this, vegetarian diets are somewhat and performance. Vegetarian diets that ian diet is associated with a lower risk more common among adolescents meet energy needs and contain a vari- of death from ischemic heart disease. .Good؍with eating disorders than in the gen- ety of plant-based protein foods, such Grade I eral adolescent population (83). Food as soy products, other legumes, grains, and nutrition professionals should be nuts, and seeds, can provide adequate Blood Lipid Levels. The lower risk of aware of young clients who greatly protein without the use of special foods death from ischemic heart disease limit food choices and who exhibit or supplements (91). Vegetarian ath- seen in vegetarians could be ex- symptoms of eating disorders. letes may have lower muscle creatine plained in part by differences in blood With guidance in meal planning, concentration due to low dietary creat- lipid levels. Based on blood lipid lev- vegetarian diets can be appropriate ine levels (92,93). Vegetarian athletes els in one large cohort study, the in- and healthful choices for adolescents. participating in short-term, high-inten- cidence of ischemic heart disease was sity exercise and resistance training estimated to be 24% lower in lifelong may benefit from creatine supplemen- vegetarians and 57% lower in lifelong Older Adults tation (91). Some, but not all research vegans compared to meat eaters (97). With aging, energy needs decrease suggests that amenorrhea may be more Typically, studies find lower total cho- but recommendations for several nu- common among vegetarian than non- lesterol and low-density lipoprotein trients, including calcium, vitamin D, vegetarian athletes (94,95). Female (LDL) cholesterol levels in vegetari- and vitamin B-6 are higher. Intakes vegetarian athletes may benefit from ans (100, for example). Intervention diets that include adequate energy, of micronutrients, especially calcium, studies have demonstrated a reduc- higher levels of fat, and generous zinc, iron, and vitamin B-12, decline tion in total and LDL-cholesterol lev- amounts of calcium and iron. in older adults (84). Studies indicate els when subjects switched from their that older vegetarians have dietary usual diet to a vegetarian diet (101, intakes that are similar to nonveg- for example). Although evidence is etarians (85,86). VEGETARIAN DIETS AND CHRONIC limited that a vegetarian diet is asso- Older adults may have difficulty DISEASE ciated with higher high-density li- with vitamin B-12 absorption from Cardiovascular Disease (CVD) poprotein cholesterol levels or with food, frequently due to atrophic gas- Evidence-based analysis of the re- higher or lower triglyceride levels, a tritis, so vitamin B-12-fortified foods search literature is being used to vegetarian diet is consistently associ- or supplements should be used be- evaluate existing research on the re- ated with lower LDL cholesterol lev- cause the vitamin B-12 in fortified lationship between vegetarian di- els. Other factors such as variations foods and supplements is usually etary patterns and CVD risk factors well-absorbed (87). Cutaneous vita- (96). Two evidence analysis questions in BMI and foods eaten or avoided min D production decreases with ag- have been completed: within the context of a vegetarian diet ing so that dietary or supplemental or lifestyle differences could partially explain the inconsistent results with sources of vitamin D are especially ● What is the relationship between a important (88). Although current rec- regard to blood lipid levels. vegetarian diet and ischemic heart Factors in a vegetarian diet that ommendations for protein for healthy disease? could have a beneficial effect on blood older adults are the same as those for ● How is micronutrient intake in a lipid levels include the higher amounts younger adults on a body weight basis vegetarian diet associated with of fiber, nuts, soy, and plant sterols and (17), this is a controversial area (89). CVD risk factors? Certainly older adults who have low lower levels of saturated fat. Vegetari- energy requirements will need to con- Ischemic Heart Disease. Two large co- ans consume between 50% and 100% sume concentrated sources of protein. hort studies (97,98) and one meta- more fiber than nonvegetarians and Older adults can meet protein needs analysis (99) found that vegetarians vegans have higher intakes than lacto- on a vegetarian diet if a variety of were at lower risk of death from isch- ovo-vegetarians (12). Soluble fiber has protein-rich plant foods, including le- emic heart disease than nonvegetar- been repeatedly shown to lower total gumes and soy products, are eaten ians. The lower risk of death was seen and LDL cholesterol levels and to re- daily. in both lacto-ovo-vegetarians and veg- duce risk of coronary heart disease (17). ans (99). The difference in risk per- A diet high in nuts significantly lowers sisted after adjustment for BMI, total and LDL cholesterol levels (102). Athletes smoking habits, and social class (97). Soy isoflavones may play a role in re- Vegetarian diets can also meet the This is especially significant because ducing LDL cholesterol levels and in needs of competitive athletes. Nutri- the lower BMI commonly seen in veg- reducing the susceptibility of LDL to tion recommendations for vegetarian etarians (99) is one factor that may oxidation (103). Plant sterols, found in athletes should be formulated with con- help to explain the lower risk of heart legumes, nuts and seeds, whole grains, sideration of the effects of both vegetar- disease in vegetarians. If this differ- vegetable oils, and other plant-based

1272 July 2009 Volume 109 Number 7 foods reduce cholesterol absorption and Hypertension ventist nonvegetarians (125). In the lower LDL cholesterol levels (104). A cross-sectional study and a cohort Adventist Health Study, age-adjusted study found that there was a lower risk for developing diabetes was two- Factors Associated with Vegetarian Diets rate of hypertension among vegetari- fold greater in nonvegetarians, com- that May Affect Risk of CVD. Other fac- ans than nonvegetarians (97,98). pared with their vegetarian counter- tors in vegetarian diets may impact Similar findings were reported in parts (98). Although obesity increases CVD risk independent of effects on Seventh-day Adventists (Adventists) the risk of type 2 diabetes, meat and cholesterol levels. Foods that feature in Barbados (116) and in preliminary processed meat intake was found to prominently in a vegetarian diet that results from the Adventist Health be an important risk factor for diabe- may offer protection from CVD in- Study-2 cohort (117). Vegans appear tes even after adjustment for BMI clude soy protein (105), fruits and to have a lower rate of hypertension (126). In the Women’s Health Study, vegetables, whole grains, and nuts than do other vegetarians (97,117). the authors also observed positive as- (106,107). Vegetarians appear to con- Several studies have reported sociations between intakes of red sume more phytochemicals than do lower blood pressure in vegetarians meat and processed meat and risk of nonvegetarians because a greater compared to nonvegetarians (97,118) diabetes after adjusting for BMI, total percentage of their energy intake although other studies reported little energy intake, and exercise (127). A comes from plant foods. Flavonoids difference in blood pressure between significantly increased risk of diabe- and other phytochemicals appear to vegetarians and nonvegetarians tes was most pronounced for frequent have protective effects as antioxi- (100,119,120). At least one of the consumption of processed meats such dants, in reducing platelet aggrega- studies reporting lower blood pres- as bacon and hot dogs. Results re- tion and blood clotting, as anti-in- sure in vegetarians found that BMI mained significant even after further flammatory agents, and in improving rather than diet accounted for much adjustment for dietary fiber, magne- endothelial function (108,109). Lacto- of the age-adjusted variation in blood sium, fat, and glycemic load (128). In ovo-vegetarians have been shown to pressure (97). Vegetarians tend to a large cohort study, the relative risk have significantly better vasodilation have a lower BMI than nonvegetar- for type 2 diabetes in women for every responses, suggesting a beneficial ef- ians (99); thus, vegetarian diets’ in- one-serving increase in intake was fect of vegetarian diet on vascular en- fluence on BMI may partially account 1.26 for red meat and 1.38 to 1.73 for dothelial function (110). for reported differences in blood pres- processed meats (128). Evidence analysis was conducted sure between vegetarians and non- In addition, higher intakes of vege- to examine how the micronutrient vegetarians. Variations in dietary in- tables, whole-grain foods, legumes, makeup of vegetarian diets might be take and lifestyle within groups of and nuts have all been associated related to CVD risk factors. vegetarians may limit the strength of with a substantially lower risk of in- EAL Conclusion Statement: No re- conclusions with regard to the rela- sulin resistance and type 2 diabetes, search meeting inclusion criteria tionship between vegetarian diets and improved glycemic control in ei- were identified that examined the mi- and blood pressure. ther normal or insulin-resistant indi- cronutrient intake of a vegetarian Possible factors in vegetarian diets viduals (129-132). Observational diet and CVD risk factors. Grade that could result in lower blood pres- studies have found that diets rich in Not Assignable. sure include the collective effect of whole-grain foods are associated with؍V Not all aspects of vegetarian diets various beneficial compounds found improved insulin sensitivity. This ef- are associated with reduced risk for in plant foods such as potassium, fect may be partly mediated by signif- heart disease. The higher serum ho- magnesium, antioxidants, dietary fat, icant levels of magnesium and cereal mocysteine levels that have been re- and fiber (118,121). Results from the fiber in the whole-grain foods (133). ported in some vegetarians, appar- Dietary Approaches to Stop Hyper- Persons with elevated blood glucose ently due to inadequate vitamin B-12 tension study, in which subjects con- may experience an improvement in intake, may increase risk of CVD sumed a low-fat diet rich in fruits, insulin resistance and lower fasting (111,112) although not all studies vegetables and dairy, suggest that blood glucose levels after they have support this (113). substantial dietary levels of potas- consumed whole grains (134). People Vegetarian diets have been suc- sium, magnesium, and calcium play consuming about three servings per cessfully used in treatment of CVD. A an important role in reducing blood day of whole-grain foods are 20% to regimen that used a very low-fat pressure levels (122). Fruit and vege- 30% less likely to develop type 2 dia- (Յ10% of energy) near vegan (limited table intake was responsible for about betes than low consumers (Ͻ3 serv- nonfat dairy and egg whites allowed) one-half of the blood pressure reduc- ings per week) (135). diet along with exercise, smoking ces- tion of the Dietary Approaches to In the Nurses’ Health Study, nut sation, and stress management, was Stop Hypertension diet (123). In ad- consumption was inversely associ- shown to reduce blood lipid levels, dition, nine studies report that con- ated with risk of type 2 diabetes after blood pressure, and weight, and im- sumption of five to 10 servings of fruit adjustment for BMI, physical activ- prove exercise capacity (114). A near- and vegetables significantly lowers ity, and many other factors. The risk vegan diet high in phytosterols, vis- blood pressure (124). of diabetes for those consuming nuts cous fiber, nuts, and soy protein has five or more times a week was 27% been shown to be as effective as a lower than those almost never eating low-saturated fat diet and a statin for Diabetes nuts, whereas the risk of diabetes for lowering serum LDL-cholesterol lev- Adventist vegetarians are reported to those consuming peanut butter at els (115). have lower rates of diabetes than Ad- least five times a week (equivalent to

July 2009 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1273 5 oz peanuts/week) was 21% lower tional study of 37,875 adults, meat- strongly associated with a reduced than those who almost never ate pea- eaters had the highest age-adjusted risk of some cancers (108,145,146). In nut butter (129). mean BMI and vegans the lowest, contrast, among survivors of early Because legumes contain slowly di- with other vegetarians having inter- stage breast cancer in the Women’s gested carbohydrate and have a high mediate values (140). In the EPIC- Healthy Eating and Living trial, the fiber content, they are expected to im- Oxford Study, weight gain over a adoption of a diet enhanced by addi- prove glycemic control and reduce in- 5-year period, among a health-con- tional daily fruit and vegetable serv- cident diabetes. In a large prospective scious cohort, was lowest among ings did not reduce additional breast study, an inverse association was those who moved to a diet containing cancer events or mortality over a seen between the intake of total le- fewer animal foods (141). In a large 7-year period (147). gumes, peanuts, soybeans, and other cross-sectional British study, it was Fruit and vegetables contain a com- legumes by Chinese women, and the observed that those people who be- plex mixture of phytochemicals, pos- incidence of type 2 diabetes mellitus, came vegetarian as adults did not dif- sessing potent antioxidant, antiprolif- after adjustment for BMI and other fer in BMI or body weight compared erative, and cancer-protective activity. factors. The risk of type 2 diabetes to those who were life-long vegetari- The phytochemicals can display addi- was 38% and 47% lower, for those ans (53). However, those who have tive and synergistic effects, and are consuming a high intake of total le- been following a vegetarian diet for at best consumed in whole foods gumes and soybeans, respectively, least 5 years typically have a lower (148-150). These phytochemicals inter- compared to a low intake (132). BMI. Among Adventists in Barbados, fere with several cellular processes in- In a prospective study, the risk of the number of obese vegetarians, who volved in the progression of cancer. type 2 diabetes was 28% lower for had followed the diet for more than 5 These mechanisms include the inhibi- women in the upper quintile of vege- years, was 70% less than the number tion of cell proliferation, inhibition of table, but not fruit intake, compared of obese omnivores whereas recent DNA adduct formation, inhibition of to the lower quintile of vegetable in- vegetarians (following the diet Ͻ5 phase 1 enzymes, inhibition of signal take. Individual vegetable groups years) had body weights similar to transduction pathways and oncogene were all inversely and significantly omnivores (116). A low-fat vegetarian expression, induction of cell cycle arrest associated with the risk of type 2 di- diet has been shown to be more effec- and apoptosis, induction of phase 2 en- abetes (131). In another study, con- tive in long-term weight loss for post- zymes, blocking the activation of nu- sumption of green leafy vegetables menopausal women than a more clear factor-kappaB, and inhibiting an- and fruit, but not fruit juice, was as- conventional National Cholesterol giogenesis (149). sociated with a lower risk of diabetes Education Program diet (142). Vege- According to the recent World Can- (136). tarians may have a lower BMI due to cer Research Fund report (143), fruit Fiber-rich vegan diets are charac- their higher consumption of fiber- and vegetables are protective against terized by a low glycemic index and a rich, low-energy foods, such as fruit cancer of the lung, mouth, esophagus, low to moderate glycemic load (137). and vegetables. and stomach, and to a lesser degree In a 5-month randomized clinical some other sites. The regular use of trial, a low-fat vegan diet was shown legumes also provides a measure of to considerably improve glycemic con- Cancer protection against stomach and pros- trol in persons with type 2 diabetes, Vegetarians tend to have an overall tate cancer (143). Fiber, vitamin C, with 43% of subjects reducing diabe- cancer rate lower than that of the carotenoids, flavonoids, and other phy- tes medication (138). Results were general population, and this is not tochemicals in the diet are reported to superior to those obtained from fol- confined to smoking-related cancers. exhibit protection against various can- lowing a diet based on American Dia- Data from the Adventist Health cers. Allium vegetables may protect betes Association guidelines (individ- Study revealed that nonvegetarians against stomach cancer and garlic pro- ualized based on body weight and had a substantially increased risk for tects against colorectal cancer. Fruits lipid concentrations; 15%-20% pro- both colorectal and prostate cancer rich in the red pigment lycopene are tein; Ͻ7% saturated fat; 60% to 70% compared with vegetarians, but there reported to protect against prostate carbohydrate and monounsaturated were no significant differences in risk cancer (143). Recently, cohort studies fat; Յ200 mg cholesterol). of lung, breast, uterine, or stomach have suggested that a high intake of cancer between the groups after con- whole grains provided substantial pro- trolling for age, sex, and smoking tection against various cancers (151). Obesity (98). Obesity is a significant factor in- Regular physical activity provides sig- Among Adventists, about 30% of creasing the risk of cancer at a num- nificant protection against most of the whom follow a meatless diet, vegetar- ber of sites (143). Because the BMI of major cancers (143). ian eating patterns have been associ- vegetarians tends to be lower than Although there is such a variety of ated with lower BMI, and BMI in- that of nonvegetarians, the lighter potent phytochemicals in fruit and creased as the frequency of meat body weight of the vegetarians may vegetables, human population studies consumption increased in both men be an important factor. have not shown large differences in and women (98). In the Oxford Vege- A vegetarian diet provides a variety cancer incidence or mortality rates tarian Study, BMI values were higher of cancer-protective dietary factors between vegetarians and nonvegetar- in nonvegetarians compared with (144). Epidemiologic studies have ians (99,152). Perhaps more detailed vegetarians in all age groups for both consistently shown that a regular food consumption data are needed be- men and women (139). In a cross-sec- consumption of fruit and vegetables is cause the bioavailability and potency

1274 July 2009 Volume 109 Number 7 of phytochemicals depends on food wards breast cancer (160). On the gand stimulates osteoclastic activity preparation, such as whether the veg- other hand, meat consumption has and recruitment of new osteoclasts to etables are cooked or raw. In the case been linked in some, but not all, stud- promote bone resorption and buffer- of prostate cancer, a high dairy intake ies with an increased risk of breast ing of the proton load (169). may lessen the chemoprotective effect cancer (161). In one study, breast can- An increased fruit and vegetable of a vegetarian diet. Use of dairy and cer risk increased by 50% to 60% for consumption has a positive effect on other calcium-rich foods have been each additional 100 g/day of meat con- the calcium economy and markers of associated with an increased risk of sumed (162). bone metabolism (170). The high po- prostate cancer (143,153,154), al- tassium and magnesium content of though not all studies support this fruits, berries, and vegetables, with finding (155). Osteoporosis their alkaline ash, makes these foods Red meat and processed meat con- Dairy products, green leafy vegeta- useful dietary agents for inhibiting sumption is consistently associated bles, and calcium-fortified plant foods bone resorption (171). Femoral neck with an increase in the risk of colorec- (including some brands of ready-to- and lumbar spine BMD of premeno- tal cancer (143). On the other hand, eat cereals, soy and rice beverages, pausal women was about 15% to 20% the intake of legumes was negatively and juices) can provide ample calcium higher for women in the highest quar- associated with risk of colon cancer in for vegetarians. Cross-sectional and tile of potassium intake compared nonvegetarians (98). In a pooled anal- longitudinal population-based studies with those in the lowest quartile ysis of 14 cohort studies, the adjusted published during the past 2 decades (172). risk of colon cancer was substantially suggest no differences in bone min- Dietary potassium, an indicator of reduced by a high intake of fruit and eral density (BMD), for both trabecu- net endogenous acid production and vegetable vs a low intake. Fruit and lar and cortical bone, between omni- fruit and vegetable intake, was shown vegetable intakes were associated vores and lacto-ovo-vegetarians (163). to exert a modest influence on mark- with a lower risk of distal colon can- Although very little data exist on ers of bone health, which over a life- cer, but not with proximal colon can- the bone health of vegans, some stud- time may contribute to a decreased cer (156). Vegetarians have a sub- ies suggest that bone density is lower risk of osteoporosis (173). stantially greater intake of fiber than among vegans compared with non- High protein intake, especially an- nonvegetarians. A high fiber intake is vegetarians (164,165). The Asian imal protein, can produce increased thought to protect against colon can- vegan women in these studies had calciuria (167,174). Postmenopausal cer, although not all research sup- very low intakes of protein and cal- women with diets high in animal pro- ports this. The EPIC study involving cium. An inadequate protein and low tein and low in plant protein revealed 10 European countries reported a calcium intake has been shown to be a high rate of bone loss and a greatly 25% reduction in risk of colorectal associated with bone loss and frac- increased risk of hip fracture (175). cancer in the highest quartile of di- tures at the hip and spine in elderly Although excessive protein intake etary fiber intake compared to the adults (166,167). In addition, vitamin may compromise bone health, evi- lowest. Based upon these findings, D status is compromised in some veg- dence exists that low protein intakes Bingham and colleagues (157) con- ans (168). may increase the risk of low bone in- cluded that in populations with a low Results from the EPIC-Oxford study tegrity (176). fiber intake, doubling the fiber intake provide evidence that the risk of bone Blood levels of undercarboxylated could reduce the colorectal cancer by fractures for vegetarians is similar to osteocalcin, a sensitive marker of vi- 40%. On the other hand, a pooled that of omnivores (38). The higher risk tamin K status, are used to indicate analysis of 13 prospective cohort of bone fracture in vegans appeared to risk of hip fracture (177), and predict studies reported a high dietary fiber be a consequence of a lower calcium BMD (178). Results from two large, intake was not associated with a de- intake. However, the fracture rates of prospective cohort studies suggest an creased risk of colorectal cancer after the vegans who consumed over 525 mg inverse relationship between vitamin accounting for multiple risk factors calcium/day were not different from the K (and green, leafy vegetable) intake (158). fracture rates in omnivores (38). Other and risk of hip fracture (179,180). Soy isoflavones and soy foods have factors associated with a vegetarian Short-term clinical studies suggest been shown to possess anti-cancer diet, such as fruit and vegetable con- that soy protein rich in isoflavones de- properties. Meta-analysis of eight sumption, soy intake, and intake of vi- creases spinal bone loss in postmeno- studies (one cohort, and seven case tamin K-rich leafy greens must be con- pausal women (181). In a meta-analy- control) conducted in high-soy-con- sidered when examining bone health. sis of 10 randomized controlled trials, suming Asians showed a significant Bone has a protective role in main- soy isoflavones demonstrated a signifi- trend of decreasing risk of breast can- taining systemic pH. Acidosis is seen cant benefit on spine BMD (182). In a cer with increasing soy food intake. In to suppress osteoblastic activity, with randomized controlled trial, postmeno- contrast, soy intake was unrelated to the gene expression of specific matrix pausal women receiving genistein ex- breast cancer risk in studies con- proteins and alkaline phosphatase ac- perienced significant decreases in uri- ducted in 11 low-soy-consuming tivity diminished. Prostaglandin pro- nary excretion of deoxypyridinoline (a Western populations (159). However, duction by the osteoblasts increases marker of bone resorption), and in- controversy remains regarding the synthesis of the osteoblastic receptor creased levels of serum bone-specific al- value of soy as a cancer-protective activator of nuclear factor kappaB li- kaline phosphatase (a marker of bone agent, because not all research sup- gand. The acid induction of receptor formation) (183). In another meta-anal- ports the protective value of soy to- activator of nuclear factor kappaB li- ysis of nine randomized controlled tri-

July 2009 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1275 als on menopausal women, soy isofla- protective factor, whereas meat in- permitted to provide substitute foods vones significantly inhibited bone take may increase the risk of divertic- for children who are medically certi- resorption and stimulated bone forma- ulitis (190). In a cohort study of 800 fied as having a special dietary need tion compared to placebo (184). women aged 40 to 69 years, nonveg- (195). Some public schools regularly To promote bone health, vegetari- etarians were more than twice as feature vegetarian choices, including ans should be encouraged to consume likely as vegetarians to suffer from vegan, menu items and this seems to foods that provide adequate intakes gallstones (191), even after control- be more common than in the past al- of calcium, vitamin D, vitamin K, po- ling for obesity, sex, and aging. Sev- though many school food programs tassium, and magnesium; adequate, eral studies from a research group in still have limited options for vegetar- but not excessive protein; and to in- Finland suggest that fasting, followed ians (196). Public schools are allowed clude generous amounts of fruits and by a vegan diet, may be useful in the to offer soy milk to children who bring vegetables and soy products, with treatment of rheumatoid arthritis a written statement from a parent or minimal amounts of sodium. (192). guardian identifying the student’s special dietary need. Soy milks must meet specified standards to be ap- Renal Disease PROGRAMS AND AUDIENCES AFFECTED proved as substitutes and schools Long-term high intakes of dietary Special Supplemental Nutrition Program must pay for expenses that exceed protein (above 0.6 g/kg/day for a per- for Women, Infants, and Children federal reimbursements (197). son with kidney disease not undergo- The Special Supplemental Nutrition ing dialysis or above the Dietary Ref- Program for Women, Infants, and erence Intake for protein of 0.8 g/kg/ Children is a federal grant program Feeding Programs for Elderly Adults day for people with normal kidney that serves pregnant, postpartum, The federal Elderly Nutrition Pro- function) from either animal or vege- and breastfeeding women; infants; gram distributes funds to states, ter- tables sources, may worsen existing and children up to age 5 years who ritories, and tribal organizations for a chronic kidney disease or cause renal are documented as being at nutri- national network of programs that injury in those with normal renal tional risk with family income below provide congregate and home-deliv- function (185). This may be due to the federal standards. This program pro- ered meals (often known as Meals on higher glomerular filtration rate as- vides vouchers to purchase some Wheels) for older Americans. Meals sociated with a higher protein intake. foods suitable for vegetarians includ- are often provided by local Meals on Soy-based vegan diets appear to be ing infant formula, iron-fortified in- Wheels agencies. A 4-week set of veg- nutritionally adequate for people fant cereal, vitamin C–rich fruit or etarian menus has been developed for with chronic kidney disease and may vegetable juice, carrots, cow’s milk, use by the National Meals on Wheels slow progression of kidney disease cheese, eggs, iron-fortified ready-to- Foundation (198). Similar menus (185). eat cereal, dried beans or peas, and have been adapted by individual pro- peanut butter. Recent changes to this grams including New York City’s De- program promote the purchase of partment for the Aging which has Dementia whole-grain breads and cereals, allow preapproved a 4-week set of vegetar- One study suggests that vegetarians the substitution of canned beans for ian menus (199). are at lower risk of developing demen- dried beans, and provide vouchers for tia than nonvegetarians (186). This purchasing fruits and vegetables reduced risk may be due to the lower (193). Soy-based beverages and cal- Corrections Facilities blood pressure seen in vegetarians or cium-set tofu that meet specifications Court rulings in the United States to the higher antioxidant intake of can be substituted for cow’s milk for have granted prison inmates the right vegetarians (187). Other possible fac- women and for children with medical to have vegetarian meals for certain tors reducing risk could include a documentation (193). religious and medical reasons (200). lower incidence of cerebrovascular In the federal prison system, vegetar- disease and possible reduced use of ian diets are only provided for in- postmenopausal hormones. Vegetari- Child Nutrition Programs mates who document that their diet is ans can, however, have risk factors The National School Lunch Program a part of an established religious for dementia. For example, poor vita- allows nonmeat protein products in- practice (201). Following review and min B-12 status has been linked to an cluding certain soy products, cheese, approval by the chaplaincy team, the increased risk of dementia apparently eggs, cooked dried beans or peas, yo- inmate can participate in the Alterna- due to the hyperhomocysteinemia gurt, peanut butter, other nut or seed tive Diet Program either through self- that is seen with vitamin B-12 defi- butters, peanuts, tree nuts, and seeds selection from the main line that in- ciency (188). to be used (194). Meals served must cludes a nonflesh option and access to meet the 2005 Dietary Guidelines for the salad/hot bar or through provision Americans and provide at least one of nationally recognized, religiously Other Health Effects of Vegetarian Diets third of the Recommended Dietary certified processed foods (202). If In a cohort study, middle-aged vege- Allowance for protein, vitamins A and meals are served in prepared trays, tarians were found to be 50% less C, iron, calcium, and energy. Schools local procedures are developed for the likely to have diverticulitis compared are not required to make modifica- provision of nonflesh foods (201). In with nonvegetarians (189). Fiber was tions to meals based on food choices of other prisons, the process for obtain- considered to be the most important a family or a child although they are ing vegetarian meals and the type of

1276 July 2009 Volume 109 Number 7 meal available varies depending on ● Instruct clients about the prepara- Vegetarian Nutrition Dietetic Practice where the prison is located and the tion and use of foods that frequently Group type of prison (201). Although some are part of vegetarian diets. The http://vegetariannutrition.net prison systems provide meatless al- growing selection of products aimed ternatives, others simply leave meat Andrews University Nutrition Department at vegetarians may make it impos- off the inmate’s tray. http://www.vegetarian-nutrition.info sible to be knowledgeable about all such products. However, practitio- Center for Nutrition Policy and Promotion ners working with vegetarian cli- Military/Armed Forces http://www.mypyramid.gov/tips_resources/ ents should have a basic knowledge The US Army’s Combat Feeding Pro- vegetarian_diets.html of preparation, use, and nutrient gram, which oversees all food regula- Food and Nutrition Information Center content of a variety of grains, tions, provides a choice of vegetarian http://www.nal.usda.gov/fnic/pubs/bibs/gen/ beans, soy products, meat analogs, menus including vegetarian Meals, vegetarian.pdf and fortified foods. Ready-to-Eat (203,204). ● Be familiar with local sources for Mayo Clinic purchase of vegetarian foods. In http://www.mayoclinic.com/health/ some communities, mail order Other Institutions and Quantity Food vegetarian-diet/HQ01596 sources may be necessary. Service Organizations Medline Plus, Vegetarian Diet ● Work with family members, partic- Other institutions, including colleges, http://www.nlm.nih.gov/medlineplus/ ularly the parents of vegetarian universities, hospitals, restaurants, vegetariandiet.html children, to help provide the best and publicly funded museums and possible environment for meeting parks, offer varying amounts and Seventh-day Adventist Dietetic nutrient needs on a vegetarian diet. types of vegetarian selections. Re- Association ● If a practitioner is unfamiliar with sources are available for vegetarian http://www.sdada.org/plant.htm vegetarian nutrition, he/she should quantity food preparation. The Vegan Society (vitamin B-12) assist the individual in finding http://www.vegansociety.com/food/nutrition/ someone who is qualified to advise ROLES AND RESPONSIBILITIES OF FOOD b12/ the client or should direct the client AND NUTRITION PROFESSIONALS to reliable resources. The Vegetarian Resource Group Nutrition counseling can be highly http://www.vrg.org beneficial for vegetarian clients who Qualified food and nutrition profes- manifest specific health problems re- The Vegetarian Society of the United sionals can also play key roles in ensur- lated to poor dietary choices and for Kingdom ing that the needs of vegetarians are vegetarians with existing clinical con- http://www.vegsoc.org/health met in foodservice operations, includ- ditions that require additional di- ing child nutrition programs, feeding etary modifications (eg, diabetes, hy- Figure 2. Useful Web sites concerning vege- programs for the elderly, corrections fa- perlipidemia, and kidney disease). tarian diets. cilities, the military, colleges, universi- ties, and hospitals. This can be accom- Depending on the client’s knowledge Qualified food and nutrition profes- plished through development of level, nutrition counseling may be sionals can help vegetarian clients in useful for new vegetarians and for in- the following ways: guidelines specifically addressing the dividuals at various stages of the life needs of vegetarians, creation and im- cycle including pregnancy, infancy, ● Provide information about meeting plementation of menus acceptable to childhood, adolescence, and for the el- requirements for vitamin B-12, cal- vegetarians, and the evaluation of derly. Food and nutrition profession- cium, vitamin D, zinc, iron, and n-3 whether or not a program meets the als have an important role in provid- fatty acids because poorly planned needs of its vegetarian participants. ing assistance in the planning of vegetarian diets may sometimes healthful vegetarian diets for those fall short of these nutrients. CONCLUSIONS who express an interest in adopting ● Give specific guidelines for plan- vegetarian diets or who already eat a ning balanced lacto-ovo-vegetarian Appropriately planned vegetarian diets vegetarian diet, and they should be or vegan meals for all stages of the have been shown to be healthful, nutri- able to give current accurate informa- life cycle. tionally adequate, and may be benefi- tion about vegetarian nutrition. In- ● Supply information about general cial in the prevention and treatment of formation should be individualized measures for health promotion and certain diseases. Vegetarian diets are depending on type of vegetarian diet, disease prevention. appropriate for all stages of the life cy- age of the client, food preparation ● Adapt guidelines for planning bal- cle. There are many reasons for the ris- skills, and activity level. It is impor- anced lacto-ovo-vegetarian or vegan ing interest in vegetarian diets. The tant to listen to the client’s own de- meals for clients with special dietary number of vegetarians in the United scription of his or her diet to ascertain needs due to allergies or chronic dis- States is expected to increase during which foods can play a role in meal ease or other restrictions. the next decade. Food and nutrition planning. Figure 1 provides meal ● Be familiar with vegetarian options professionals can assist vegetarian cli- planning suggestions. Figure 2 pro- at local restaurants. ents by providing current, accurate in- vides a list of Web resources on vege- ● Provide ideas for planning optimal formation about vegetarian nutrition, tarian diets. vegetarian meals while traveling. foods, and resources.

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1280 July 2009 Volume 109 Number 7 145. Khan N, Afaq F, Mukhtar H. Cancer che- Slimani N, Norat T, Clavel-Chapelon F, ranges during the winter in Finland. JAm moprevention through dietary antioxi- Kesse E, Nieters A, Boeing H, Tjønneland Diet Assoc. 2000;100:434-441. dants: Progress and promise. Antioxid Re- A, Overvad K, Martinez C, Dorronsoro M, 169. Krieger NS, Frick KK, Bushinsky DA. dox Signal. 2008;10:475-510. Gonzalez CA, Key TJ, Trichopoulou A, Mechanism of acid-induced bone resorp- 146. Béliveau R, Gingras D. Role of nutrition in Naska A, Vineis P, Tumino R, Krogh V, tion. Curr Opin Nephrol Hypertens. 2004; preventing cancer. Can Fam Physician. Bueno-de-Mesquita HB, Peeters PH, 13:423-436. 2007;53:1905-1911. Berglund G, Hallmans G, Lund E, Skeie G, 170. New SA. Intake of fruit and vegetables: 147. Pierce JP, Natarajan L, Caan BJ, Parker Kaaks R, Riboli E; European Prospective Implications for bone health. 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July 2009 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1281 Bonaiuto M, D’Anna R, Cannata ML, Cor- prospective study of diet and the risk of 220) Federal Register. September 12, 2008; rado F, Adamo EB, Wilson S, Squadrito F. symptomatic diverticular disease in men. 73:52903-52908. Effects of the phytoestrogen genistein on Am J Clin Nutr. 1994;60:757-764. 198. Four-week vegetarian menu set for Meals bone metabolism in osteopenic postmeno- 191. Pixley F, Wilson D, McPherson K, Mann J. on Wheels Sites. The Vegetarian Resource pausal women: A randomized trial. Ann Effect of vegetarianism on development of Group Web site. http://www.vrg.org/fsupdate/ Intern Med. 2007;146:839-847. gall stones in women. Br Med J (Clin Res fsu974/fsu974menu.htm. Posted May 18,1998. 184. Ma DF, Qin LQ, Wang PY, Katoh R. Soy Ed). 1985:291:11-12. Accessed July 10,2008. isoflavone intake inhibits bone resorption 192. Muller H, de Toledo FW, Resch KL. Fasting 199. Vegetarian menus. New York City Depart- and stimulates bone formation in meno- followed by vegetarian diet in patients with ment for the Aging Web site. http://www. pausal women: Meta-analysis of randomized rheumatoid arthritis: A systematic review. nyc.gov/html/dfta/downloads/pdf/menu_ controlled trials. Eur J Clin Nutr. 2008;62: Scand J Rheumatol. 2001;30:1-10. vegetarian.pdf. Accessed January 19, 2009. 155-161. 193. Special Supplemental Nutrition Program 200. Ogden A, Rebein P. Do prison inmates have a 185. Bernstein AM, Treyzon L, Li Z. Are high- for Women, Infants, and Children (WIC): right to vegetarian meals? Vegetarian Jour- protein, vegetable-based diets safe for kid- Revisions in the WIC Food Packages; In- nal Mar/Apr 2001. The Vegetarian Resource ney function? A review of the literature. terim Rule. Federal Register. 7CFR, Part Group Web site. http://www.vrg.org/journal/ J Am Diet Assoc. 2007;107:644-650. 246, Dec. 6, 2007;72:68966-69032. vj2001mar/2001marprison.htm. Posted Jan- 186. Giem P, Beeson WL, Fraser GE. The inci- 194. Modification of the “Vegetable Protein uary 16,2001. Accessed July 10,2008. dence of dementia and intake of animal Products” requirements for the National 201. Prison regulations by jurisdiction. Prison products: Preliminary findings from the School Lunch Program, School Breakfast Vegetarian Project Web site. http://www. Adventist Health Study. Neuroepidemiol- Program, Summer Food Service Program assistech.info/prisonvegetarian/index.html. ogy. 1993;12:28-36. and Child And Adult Care Food Program. 187. Luchsinger JA, Mayeux R. Dietary factors (7 CFR 210,215,220,225,226) Federal Reg- Accessed July 10,2008. and Alzheimer’s disease. Lancet Neurol. ister. March 9, 2000;65:12429-12442. 202. Federal Bureau of Prisons. Program state- 2004;3:579-587. 195. Accommodating children with special ment. Religious beliefs and practices. US 188. Haan MN, Miller JW, Aiello AE, Whitmer needs in the School Nutrition Programs. Dept of Justice Web site. http://www.bop.gov/ RA, Jagust WJ, Mungas DM, Allen LH, US Department of Agriculture, Food and policy/progstat/5360_009.pdf. Posted Decem- Green R. Homocysteine, B vitamins, and Nutrition Service Web site. http://www. ber 31,2004. Accessed July 10,2008. the incidence of dementia and cognitive im- fns.usda.gov/cnd/Guidance/special_dietary_ 203. Special briefing on Objective Force Warrior pairment: Results from the Sacramento needs.pdf. Posted Fall 2001. Accessed July and DoD Combat Feeding Program. May Area Latino Study on Aging. Am J Clin 10,2008. 23,2002. US Department of Defense Web Nutr. 2007;85:511-517. 196. Healthy school lunches. 2007 school lunch site. http://www.defenselink.mil/transcripts/ 189. Gear JS, Ware A, Fursdon P, Mann JI, report card. Physicians Committee for Re- transcript.aspx?transcriptidϭ3459. Ac- Nolan DJ, Broadribb AJ, Vessey MP. sponsible Medicine Web site. http://www. cessed July 10,2008. Symptomless diverticular disease and in- healthyschoollunches.org/reports/report2007_ 204. Combat feeding directorate improves meals. take of dietary fibre. Lancet. 1979;1:511- card.html. Posted August 2007. Accessed US Dept of Defense Web site. http://www. 514. July 10,2008. defenselink.mil/transformation/articles/ 190. Aldoori WH, Giovannucci EL, Rimm EB, 197. Fluid milk substitutions in the School Nu- 2006-05/ta051506c.html. Accessed July 10, Wing AL, Trichopoulos DV, Willett WC, A trition Programs. (7CFR Parts 210 and 2008.

American Dietetic Association (ADA) position adopted by the House of Delegates Leadership Team on October 18, 1987, and reaffirmed on September 12, 1992; September 6, 1996; June 22, 2000; and June 11, 2006. This position is in effect until December 31, 2013. ADA authorizes republication of the position, in its entirety, provided full and proper credit is given. Readers may copy and distribute this paper, providing such distribution is not used to indicate an endorsement of product or service. Commercial distribution is not permitted without the permission of ADA. Requests to use portions of the position must be directed to ADA headquarters at 800/877-1600, ext. 4835, or [email protected]. Authors: Winston J. Craig, PhD, MPH, RD (Andrews University, Berrien Springs, MI); Ann Reed Mangels, PhD, RD, LDN, FADA (The Vegetarian Resource Group, Baltimore, MD). Reviewers: Pediatric Nutrition and Sports, Cardiovascular, and Wellness Nutrition dietetic practice groups (Catherine Conway, MS, RD, YAI/National Institute for People with Disabilities, New York, NY); Sharon Denny, MS, RD (ADA Knowledge Center, Chicago, IL); Mary H. Hager, PhD, RD, FADA (ADA Government Relations, Washington, DC); Vegetarian Nutrition dietetic practice group (Virginia Messina, MPH, RD, Nutrition Matters, Inc., Port Townsend, WA); Esther Myers, PhD, RD, FADA (ADA Scientific Affairs, Chicago, IL); Tamara Schryver, PhD, MS, RD (General Mills, Bloomington, MN); Elizabeth Tilak, MS, RD (WhiteWave Foods, Inc, Broomfield, CO); Jennifer A. Weber, MPH, RD (ADA Government Relations, Washington, DC). Association Positions Committee Workgroup: Dianne K. Polly, JD, RD, LDN (chair); Katrina Holt, MPH, MS, RD; Johanna Dwyer, DSc, RD (content advisor). 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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