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Special | DGE Position “Vegan Diet” with written permission of Umschau Zeitschriftenverlag GmbH, Wiesbaden.Reproduction and dissemination – also partial – applicable to all media only Copyright! Corrected version Vegan Diet (Erratum) Position of the German Nutrition Society (DGE) Margrit Richter, Heiner Boeing, Dorle Grünewald-Funk, Helmut Heseker, Anja Kroke, Eva Leschik-Bonnet, Helmut Oberritter, Daniela Strohm, Bernhard Watzl 1 for the German Nutrition Society (DGE) Abstract is female, young, educated and wealthy, lives in a city and follows a On the basis of current scientific literature, the German Nutrition Society (DGE) has “healthy lifestyle” [1, 2]. developed a position on the vegan diet. With a pure plant-based diet, it is difficult or impossible to attain an adequate supply of some nutrients. The most critical Vegetarian diets nutrient is vitamin B . Other potentially critical nutrients in a vegan diet include 12 protein resp. indispensable amino acids, long-chain n-3 fatty acids, other vitamins Depending on the form of vegetar- (riboflavin, vitamin D) and minerals (calcium, iron, iodine, zinc and selenium). The ianism (• Table 1), either selected DGE does not recommend a vegan diet for pregnant women, lactating women, in- animal foods (e.g. eggs or milk) are fants, children or adolescents. Persons who nevertheless wish to follow a vegan diet consumed, or animal foods and ad- should permanently take a vitamin B supplement, pay attention to an adequate ditives are totally avoided, including 12 intake of nutrients, especially critical nutrients, and possibly use fortified foods or foods where animal components are dietary supplements. They should receive advice from a nutrition counsellor and added during the production pro- their supply of critical nutrients should be regularly checked by a physician. cess. A vegan diet is a very strict Keywords: vegan diet, critical nutrients, vitamin B form of vegetarian diets. Vegans 12 exclusively consume plant-based foods and reject all kinds of animal foods, sometimes including honey, Introduction as well as articles of daily use made of animal body parts – such as fur Background and leather [2]. The principle reasons The vegan diet is exclusively restric- for a vegetarian diet are ethical (e.g. ted to the consumption of plant-based rejection of intensive livestock far- foods. As with other forms of vegeta- ming), as well as ecological aspects, rian diets, it is becoming increasingly sustainability and health aspects. popular among the population of the According to current knowledge, Western world. It is not known precise- the risk of nutrition-related disea- ly how many individuals in Ger- ses is determined by food compo- many adhere to a vegan diet. The sition, particularly the balance bet- data vary between 0.1% and 1% of ween animal and plant-based foods, Citation: the population, corresponding to as well as the degree of processing. Richter M, Boeing H, Grüne- between 81,000 and 810,000 indivi- Epidemiological studies have shown wald-Funk D, Heseker H, Kroke duals. Excluding animal foods from that a high intake of red meat and, A, Leschik-Bonnet E, Oberritter H, the diet is usually a conscious and particularly, meat products in- Strohm D, Watzl B for the voluntary decision [1, 2]. A vegan creases the risk of many disea- German Nutrition Society (DGE) diet as part of a “Western” lifestyle ses (e.g. certain cancer sites [5–7]), (2016) Vegan diet. Position of the differs from a “traditional” plant- whereas high levels of dietary fibre- German Nutrition Society (DGE). based diet, which is mostly practiced rich cereal products, vegetables and Ernahrungs Umschau 63(04): 92– in developing countries, where it fruit can decrease the risk of many dis- 102. Erratum in: 63(05): M262 is often accompanied by restricted eases (e.g. cardiovascular diseases [8], food availability and low energy in- and type 2 diabetes mellitus [9]). This article is available online: take, due to low incomes and lev- DOI: 10.4455/eu.2016.021 els of education [3]. In Western 1 Complete information on the authors can be countries, the typical vegetarian found on p. 99. Ernaehrungs Umschau international | 4/2016 92 Vegetarian diets often have a more a comparable diet with a low level ble-rich diets such as vegetarian favourable composition with res- of meat. However, it can be assu- diets (• Table 1) are associated with pect to these foods than the mixed med that a plant-based diet (with or good supplies of some vitamins diet which is conventional in Ger- without low levels of meat) is as- (vitamin C, vitamin E, thiamine many considering the supply sociated to a reduced risk of nutri- and folate [14, 16–23]), minerals of nutrients and other beneficial tion-related diseases in comparison (magnesium and potassium [14, phytochemicals. A meta-analysis with the currently conventional 17–19]), dietary fibre and phyto- of observational studies found that German diet. chemicals [24, 25]. In comparison persons adhering to a vegetarian to a mixed diet, all vegetarian diets diet exhibited a lower risk of met- contain, for example, lower levels abolic and cardiovascular diseases Nutrient intake in of saturated fatty acids and choles- than persons not on a vegetarian vegan nutrition terol [14, 24, 25]. diet. The risks of ischaemic heart The risk of an inadequate supply of disease and cancer were also lower The mixed diet recommended by the nutrients or of nutritional deficiency [10]. However, within the different DGE contains low levels of meat and progressively increases as the selec- studies, it is important to consider meat products, as well as fish. The tion of foods becomes more restric- which reference groups are used animal-based foods in this diet con- tive and the diet becomes less varied. and whether other differences in tribute to the supply of the nutrients This applies in principle to all forms lifestyle were considered in the protein resp. essential amino acids, as of nutrition. Adequate nutrition can statistical analysis. There is evi- well as long chain n-3 fatty acids (ei- be achieved for vegetarians who dence that some of the investigated cosapentaenoic acid [EPA] and doco- eat no meat or meat products, but groups had very different lifestyles, sahexaenoic acid [DHA]), vitamin D, consume other animal foods, e.g. so that the lower risk of disease is riboflavin, vitamin B12 (cobalamin), milk, dairy products and eggs. In a presumably not only due to nutri- calcium, iron, iodine, zinc and sele- vegan diet, the most critical nutri- tional differences [11]. In an ana- nium. As vegetarian diets (• Table 1) ent is vitamin B . Potentially critical 12 lysis of two prospective studies, avoid several or even all of these nutrients in a vegan diet moreover persons adhering to a vegetarian foods, an adequate supply of these include protein resp. indispensable diet (pesco, ovo-lacto vegetarians nutrients may be difficult. Adequate amino acids, as well as long-chain and vegans) were compared with supply of these nutrients must be en- n-3 fatty acids (EPA and DHA), other 2 persons on a high vegetable mixed sured by a well-directed selection of vitamins (riboflavin, vitamin D ) and diet, containing low levels of meat plant-based foods. Alternative sour- minerals (calcium, iron, iodine, zinc 3 and meat products. There were ces of nutrients for vegans are sum- and selenium) [14, 25, 29]. no differences between the two marised in • Table 2. An overview of the functions and signs groups with respect to mortality Only a few studies have investi- of deficiencies for the potentially criti- [12]. These results indicate that we gated the nutritional physiological cal nutrients can be found in the refe- cannot currently assume a health quality of restrictive diets such as rence values for nutrient intake [30]. advantage of vegetarians in com- the vegan diet and compared these parison with persons consuming with other diets [13–15]. Vegeta- Foods that are eaten Foods that are avoided Pesco vegetarians plant-based foods, fish, eggs, milk and Meat and all products derived thereof dairy products Ovo-lacto vegetarians plant-based foods, eggs, milk and dairy meat, fish (including other aquatic ani- products mals) and all products derived thereof Lacto vegetarians plant-based foods, milk and dairy meat, fish (including other aquatic ani- products mals), eggs and all products derived thereof Ovo vegetarians plant-based foods, eggs meat, fish (including other aquatic ani- mals), milk and dairy products and all products derived thereof Vegans plant-based foods all animal foods, also honey Tab. 1: Forms of vegetarianism resp. vegetarian oriented diets (mod. from: [4]) Ernaehrungs Umschau international | 4/2016 93 Special | DGE Position “Vegan Diet” b Potentially Vegetable nutrient source Comments on the vegan diet a critical nutrient Protein legumes, nuts, cereals (whole-grain), oil seeds, • If a variety of vegetable protein sources, such as cereals, legumes and potatoes, are distributed potatoes specifically combined and consumed over the day [83] along with adequate energy intake [84], protein requirements can be covered over the day (e.g. cereals + legumes, soya pro- [85, 86]. It is unclear whether this is also possible for toddlers. According to Young and Pellett, ducts and/or oil seeds). normal growth is indeed possible in children if they receive an exclusively plant-based diet and if different protein sources are combined [83]. On the other hand, Krajcovicova-Kudlackova et al. considered that the requirements for indispensable amino acids cannot be exclusively covered by plant protein in phases of high requirements, such as growth, as the protein quality of plant protein is lower than that of animal protein [87]. • By well-directed combining different sources of plant protein, the protein quality of daily protein intake can be increased, as can the intake of all indispensable amino acids [88, 89]. • Infants and children require relatively more indispensable amino acids in protein than adults do [90]. During growth, it is therefore essential to ensure that intake of protein and of indispensable amino acids as well as energy intake are adequate. Long-chain food fortified with oil from microalgae • With a strict vegan diet, there is hardly any intake of eicosapentaenoic acid (EPA) or docosa- n-3 fatty acids hexaenoic acid (DHA). Moreover, conversion of the n-3 fatty acid α-linolenic acid (ALA; e.g. from flaxseed, walnuts, rape or their oils) to EPA and DHA is limited [91]. • Oils from microalgae contain DHA [92–94]. Microalgal oils from the microalgae Ulkenia and Schizochytrium have been approved as Novel Foods [95, 96]. Vitamin D Some mushrooms (e.g. common mushrooms, A unique characteristic of vitamin D is that it cannot only be obtained from food, but can also be chanterelles), foods fortified with vitamin D synthesised by the human body itself if the skin is exposed to sunlight (UVB) [30]. Riboflavin Oil seeds, nuts, legumes, various types of vege- table (e.g. broccoli, kale) and whole-grain cereals Vitamin B Foods fortified with vitamin B • If fortified foods are strictly excluded in a vegan diet, hardly any vitamin B is consumed. 12 12 12 • As a result of bacterial fermentation, plant-based foods, such as sauerkraut, may contain traces of vitamin B . However, it is unclear whether this form of vitamin B can be utilised 12 12 in the human body. Moreover, the levels are so low that adequate intake is not possible [2]. • Shiitake mushrooms contain vitamin B , although the quantities may vary greatly [97]. 12 Sea algae such as nori may also contain vitamin B . Attention must then be paid to the 12 declared moderate content of iodine. However, these foods are unsuited to be the sole source of vitamin B , as the bioavailability is unclear resp. the vitamin B is in an inactive 12 12 form [97–102]. • Spirulina and other products with cyanobacteria marketed as natural sources of vitamin B12 for persons adhering to a vegan diet contain no cobalamin in a form that is active in the human body and are therefore unsuited for fulfilling requirements [102]. • Vegans cannot ensure their supply of vitamin B12 with conventional foods, including fermented foods. An adequate supply of vitamin B can only be ensured by taking a 12 vitamin B supplement [32, 33]. 12 Calcium Vegetables (e.g. broccoli, kale, rocket), nuts (e.g. hazelnuts and Brazil nuts), legumes, soya meat replacement products (“textured soya protein”), tofu, mineral water (calcium-rich, > 150 mg/L), foods fortified with calcium Iron legumes, oil seeds, nuts, whole-grain cereals • Simultaneous consumption of foods rich in vitamin C or other organic acids improves and various types of vegetable (e.g. spinach, iron bioavailability [2]. black salsify) • Substances such as phytates and polyphenols (e.g. in tea and coffee) may reduce iron absorption [2, 103]. Black tea and coffee should not be drunk directly before, during or after meals of high iron content. • As generally recommended, it is particularly important that pregnant women and lacta- ting women should take an iron supplement if they are known to suffer from iron de- ficiency. Iodine • Iodinated and fluoridated table salt as well as • The Federal Institute for Risk Assessment considers that dried algal products of iodine con- foods prepared thereof (as generally recom- tent > 20 mg/kg are harmful to health and advises against their consumption [104]. mended) • Goitrogenic substances in plant-based foods, such as cabbage plants, soya beans and sweet • Sea salt fortified with sea algae and of defined io- potatoes, may decrease the bioavailability of iodine, which may be important if iodine intake dine content, or occasional consumption of sea is very low [2]. algae of moderate iodine content, e.g. nori • As generally recommended, it is particularly important that pregnant women and lactating women should take iodine supplements, after consulting a physician and considering their individual iodine intake. Zinc Whole-grain, legumes, oil seeds, nuts Preparation procedures such as sour dough fermentation and germination improve bio- availability [2]. Selenium Cabbage (e.g. broccoli, white cabbage), bulb The content in plant-based foods is highly dependent on the area of culture, as it depends vegetables (e.g. garlic, onions), mushrooms, on the selenium content in the soil [2]. asparagus and legumes, Brazil nuts Ernaehrungs Umschau international | 4/2016 94 ▸ Tab. 2: Potential critical nutrients in a vegan diet and vegetable nutrient sources a For reference values for the intake of these nutrients, see [30] and URL: www.dge.de/wissenschaft/referenzwerte/ b Aside from the comments here on taking dietary supplements, vegans, like the general population, should comply with the recommendations on vitamin K administration to neonates (oral administration of 3 x 2 mg vitamin K) and on vitamin D administration to infants (daily 10 μg vi- tamin D) and for the intake of folic acid supplements by women intending to get pregnant (daily 400 μg synthetic folic acid); folic acid intake should start not later than 4 weeks before the start of the pregnancy and continue until the end of the first trimester of pregnancy [30]. Vitamin B12 ception is an independent risk fac- for these groups at risk. Case re- tor for complications during preg- ports show that the supply of vita- Vitamin B is solely produced by nancy (miscarriage, pre-eclamp- min B and iodine of infants whose 12 12 microorganisms. The form that is sia) and for negative effects on mothers were on a vegan diet was available to the human body oc- the neonate (low birth weight, not adequately guaranteed and that curs almost exclusively in animal neural tube defect) [38–41]. If the they developed neurological disor- foods (• Table 2) [2]. Thus a vegan mother is on a strict vegan diet ders and megaloblastic anaemia or diet increases the risk of vitamin B without dietary supplements and goitre [46, 47, 52, 56]. 12 deficiency (unless a vitamin B the neonate is exclusively breast- Nutrient supply in a vegan diet 12 supplement is used) [31]. Several fed, vitamin B12 deficiency and its in pregnancy was investigated studies on vegans who took no vi- consequences (neurological dis- in a systematic review. The stu- tamin B supplements have found orders, megaloblastic anaemia) dies were heterogenous, with re- 12 that the prevalence of low vita- could already be observed in the spect to both their methodology min B supply resp. vitamin B first months of life [42–54]. and their results. Some of the 12 12 deficiency was up to 86%, depen- Vitamin B12 supply can be asses- studies were rated as being of poor ding on the parameters examined sed with several biomarkers. These quality. Bearing in mind these [32, 33]. include blood concentrations of limitations, the authors concluded Vitamin B participates in the vitamin B , holotranscobalamin that a freely chosen vegetarian or 12 12 regulation of homocysteine con- (HTC), serum methylmalonic acid vegan diet without financial restric- centrations and methionine me- (MMA) and plasma homocys- tions is safe during pregnancy, if nu- tabolism, as well as haematopoie- teine. None of these biomarkers is trient supply is observed and nutrient sis and the metabolism of fatty suitable as the sole parameter to deficits are compensated for [3]. acids and amino acids. Low serum evaluate vitamin B supply [55]. For population groups with spe- 12 concentrations of vitamin B12 are cial requirements for nutrient associated with high plasma con- supply, a well-directed selection of centrations of homocysteine. High Population groups with foods and modes of preparation is plasma homocysteine concentra- special requirements for necessary, i.e. high quality, nutri- tions have been considered to be a nutrient supply ent dense foods, preparation and risk factor for cardiovascular dis- administration appropriate to age. eases [34–36]. Protracted low vita- In persons on a vegan diet, there are Particularly in phases of growth min B intake can also impair cell difficulties with the supply of some or of increased requirements for 12 function and DNA synthesis and nutrients (• Table 2), and this may nutrients, the intake and supply may lead to megaloblastic anaemia have unfavourable consequences of nutrients should be regularly or neurological disorders [37]. for health, particularly for peo- checked by a nutrition counsel- As the liver store of vitamin B ple in sensitive phases of life (e.g. lor or physician. If intake is ina- 12 is relatively large and the reuti- growth). Therefore special attention dequate, this can be optimised by lisation rate through enterohe- is required for pregnant and lacta- patic circulation is high, clinical ting women on a vegan diet, as well symptoms of deficiency only be- as children from infants through come evident after some years of the growth phase up to adolescence 2 Aside from vitamin D intake in food, vitamin vitamin B -free nutrition. Thus, who adhere to or who are given a D can also be produced in the human body by 12 UVB light exposure (sunlight). The synthe- vegans should regularly have their vegan diet. These special population sis of vitamin D in skin depends on various vitamin B supply checked. Neo- groups are at greater risk of nutri- 12 factors, e.g. the dose and wavelength of UVB nates depend on the mother recei- tional deficiencies [30].There are exposure and the area of the exposed skin, the ving adequate vitamin B12 intake currently no conclusive studies skin type and the age [26, 27]. 3 during pregnancy and lactation. with persons on a vegan diet that Among these vitamins and minerals, vitamin There is preliminary evidence that might allow a comprehensive D and iodine should be regarded as critical nu- vitamin B deficiency before con- evaluation of the supply situation trients in the general population, iron and cal- 12 cium only in specific population groups [28]. Ernaehrungs Umschau international | 4/2016 95
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