Eur J Pediatr (2011) 170:1489–1494 DOI 10.1007/s00431-011-1547-x

REVIEW

Clinical practice Vegetarian infant and child nutrition

Myriam Van Winckel & Saskia Vande Velde & Ruth De Bruyne & Stephanie Van Biervliet

Received: 24 July 2011 /Accepted: 27 July 2011 /Published online: 13 September 2011 # Springer-Verlag 2011

Abstract The aim of this review is to give insight on the adult population in Europe (http://en.wikipedia.org/wiki/ benefits and risks of , with special emphasis on Vegetarianism_by_country#Europe). Besides religious rea- vegetarian child nutrition. This eating pattern excluding meat sons and health considerations, concerns about global and fish is being adopted by a growing number of people. A warming and sustainable production are important vegetarian has been shown to be associated with lower motivators to adopt a vegetarian diet. One kilogramme of mortality of ischaemic heart disease and lower prevalence of greenhouse gas emissions is associated with the production obesity. Growth in children on a vegetarian diet including of 162 g protein from wheat and 32 g protein from , has been shown to be similar to omnivorous peers. but only 10 g protein from meat [28]. Moreover, about 6 to Although vegetarianism in adolescents is associated with 7 kg of soy protein are needed to produce 1 kg of animal eating disorders, there is no proof of a causal relation, as the protein [28]. Many of these vegetarians are young parents eating disorder generally precedes the exclusion of meat from who want their children to share their eating pattern. This the diet. A well-balanced lacto-ovo-vegetarian diet, including article intends to give the paediatrician insight on the health dairy products, can satisfy all nutritional needs of the growing effects of vegetarianism in children, i.e. which diets carry a child. In contrast, a vegan diet, excluding all animal food risk for deficiencies and how to monitor them and in which sources, has at least to be supplemented with vitamin B12, situations individualised counselling by a knowledgeable with special attention to adequate intakes of calcium and zinc dietician is recommended. and energy-dense containing enough high-quality protein for young children. The more restricted the diet and the younger the child, the greater the risk for deficiencies. Definitions [1, 2]

Keywords Vegetarianism . Child nutrition . Vitamin B12 . Vegetarianism is defined by not eating animal flesh foods, Protein quality which means that meat and fish are excluded from the diet. Respecting this prerequisite, vegetarian diets can be as diverse as conventional diets. The most common variant is Introduction lacto-ovo-vegetarianism, which includes milk, cheese and . In contrast, excludes all animal-derived The number of people adopting a vegetarian eating pattern food; hence, vegans do not consume dairy products or eggs. is increasing and can be estimated to be 2% to 5% of the Raw food diets are based on non-cooked foods, using grounding and fermentation for enhancing digestibility. M. Van Winckel (*) : S. Vande Velde : R. De Bruyne : Fruitarians consume a diet limited to and nuts. Other S. Van Biervliet diets, like a macrobiotic diet, are part of a lifestyle Department of Paediatrics, Division of Paediatric Gastroenterology philosophy. A macrobiotic diet favours locally produced and Nutrition, University Hospital Ghent, foods with minimal processing—aiming at a balance 3K12D, De Pintelaan 185, “ ” “ ” — 9000 Ghent, Belgium between yin and yang products and includes fowl or e-mail: [email protected] fish once or twice weekly but excludes dairy products. 1490 Eur J Pediatr (2011) 170:1489–1494

Health effects of a vegetarian diet pregnant and lactating women and ranges from 0.7 μg/day for toddlers to 2 μg/day during adolescence [51]. Dairy Benefits products contain less cobalamin (0.3–0.4 μg/100 g) than eggs (0.9–1.4 μg/100g)ormeatandfish(3and33μg/100 g). Whereas former publications tended to highlight the risks, a However, bioavailability of cobalamin from dairy products is growing body of evidence is showing the long-term higher than from meat, fish or eggs [50]. benefits of a vegetarian diet [39]. Meta-analyses from large As vitamin B12 is an essential cofactor in DNA and cohort studies in adults show that vegetarians have a lower RNA synthesis, deficiency symptoms will manifest first in body mass index and lower mortality from ischaemic heart organs with rapid cell turnover such as bone marrow and disease than omnivorous persons [15, 46, 48]. This intestine. Moreover, it is indispensable for the maintenance protective effect is linked to a high consumption of of the nervous system [8]. Vitamin B12 deficiency results in unrefined products, such as whole , haematological (megaloblastic anaemia) and neurological , nuts, fruits and . The same health effect disorders (neurodevelopmental delay and regression, neu- can probably be obtained by a prudent omnivorous diet, ropsychiatric disorders). The haematological signs can be limiting the intake of meat combined with a high intake of absent in the case of high folate levels; one third of vitamin whole plant foods, a dietary pattern, which is called B12-deficient adults do not display megaloblastic anaemia “flexitarian” [6]. Studies in vegetarian children and with [4]. As neurologic damage by vitamin B12 deficiency can intermediary end points such as serum lipids and choles- be irreversible [22], prevention is of utmost importance. terol are limited and yield conflicting results. Some studies Since current laboratory methods also measure non- show lower serum cholesterol [18], whereas others do not active cobalamin analogues, serum levels within the confirm this finding [29, 47]. lower normal range do not exclude a deficiency. Vitamin

B12 is an essential cofactor for methionine synthase- Growth and development converting homocysteine and also in the conversion of methylmalonyl-coenzyme A to succinyl-coenzyme A Descriptive cohort studies have demonstrated an identical (Fig. 1). The metabolites of these enzymes will increase growth and weight evolution in lacto(-ovo)-vegetarian in case of vitamin B12 deficiency even before the presence children and adolescents compared to their omnivorous of overt clinical symptoms. The measurement of increased peers, whereas vegan children tend to be leaner and smaller homocysteine and methylmalonic acid concentrations in [7, 12, 21, 30, 32, 40, 41, 43, 49]. urine and plasma are more expensive but more sensitive

methods to detect vitamin B12 deficiency [13]. Eating disorders and vegetarianism Whereas vegans have a much higher risk of developing

vitamin B12 deficiency, it is not excluded in lacto-vegetarians. An association between vegetarianism and disordered All persons consuming fish or meat less than once weekly eating behaviour has repeatedly been described in adoles- are at risk of vitamin B12 deficiency. High methylmalonic cents [17, 35, 37]. There is, however, no proof that a acid levels in blood and urine and elevated levels of vegetarian diet predisposes to eating disorders. In most homocysteine, markers of functional vitamin B12 deficiency, patients, signs of an eating disorder are present before the have been described in vegetarians consuming limited change to a vegetarian or vegan diet [33]. As a conse- amounts of dairy products [6, 22]. Infants breastfed by vegan quence, it is important for the clinician to be alert and to mothers can develop vitamin B12 deficiency between the age explore the reasons for adopting a vegetarian diet in of 2 and 12 months due to their limited body reserve at birth adolescents, as it can be a method of concealing disordered even in the absence of signs of the deficiency in the mother eating behaviour. The majority of vegetarian adolescents, [25, 36]. Prevention is possible by consuming fish or meat however, do not have an eating disorder [24]. once or twice weekly, by consuming supplemented food (e.g. supplemented soy products or ) or by a

Nutritional concerns vitamin B12 supplement. Overdosing with vitamin B12 has not been described. Vitamin B12 Proteins Animal products are the only reliable dietary source of vitamin B12 or cobalamin. The cobalamins present in algae Protein quality reflects the content and relative proportion and seaweeds have been shown to be non-active analogues of indispensable amino acids and is lower for plant-derived of vitamin B12 [50]. The Recommended Dietary Allowance proteins than animal proteins. Protein quality of a given food for cobalamin is 2.4 μg/day for adults, 2.6 μg/day for is expressed as the protein digestibility corrected amino acid Eur J Pediatr (2011) 170:1489–1494 1491

Fig. 1 Role of vitamin B12 methionine tetrahydrofolate

5,10-methyleentetrahydrofolate Vit B12 methioninesynthase

5-methyltetrahydrofolaat Methyleentetrahydrofolate homocysteine reductase

succinylcoënzyme A Vit B cystathione- - 12 synthase

Methylmalonylcoënzyme-A- Vit B dysmutase 12 cysteine

cystathionine -ketobutyraat D-methylmalonylcoënzyme AL-methylmalonylcoënzyme A

Methylmalonic acid score (PDCAAS) [11]. This score depends on the limiting In developed countries where a large variety of plant indispensable amino acid (in milligrammes per gramme protein sources are available, protein needs are generally protein) divided by the requirement for this amino acid for a met, also in vegan children and adolescents. Infants on a pre-school child (in milligrammes per gramme protein), vegan diet however, if not breastfed, are at risk for corrected for digestibility [53]. Table 1 summarises the protein malnutrition [16]. Non-supplemented plant- PDCAAS for different food protein sources. Lysine is the derived milk substitutes based on , nut or limiting amino acid for cereals such as wheat, corn and rice, extracts are often wrongly referred to as rice “milk”, methionine for legumes such as soy and lentils. Whereas almond “milk” or soy “milk”. They should be properly former advice on healthy vegetarian diets stressed the named rice “drink”, almond “drink” and soy “drink” as importance of combining different plant protein sources in their nutritional value is not comparable to milk. It can be one meal, later research indicates that variation in plant argued to reserve the term “” for fully supplemented protein sources can be dispersed over a longer period of time adapted soy formula, enriched with methionine, iron, [53]. The PDCAAS can be calculated not only for a specific zinc, calcium and vitamins, compliant with the regulations on food, but also for a diet. The PDCAAS probably under- infant formula. estimates true protein quality because the amount of the “” (pressed soya curd), “” (fermented ) limiting indispensable amino acid from one source will be and “seitan” (processed extract) are part of supplemented by another [44, 52]. Nevertheless, it remains a traditional Asian vegetarian diets for centuries. As vegetarian- practical method for estimating whether or not a diet covers ism is becoming more popular in Western countries, the food protein needs. As a vegan diet has a PDCAAS of 75–77%, industry has developed meat substitutes based on soy protein protein requirements for vegans can be estimated to be 1.3 isolates (textured soy protein), on mycoprotein and white times those for omnivores [26]. ( ®) or on other plant protein sources such as lupin flour (Lopino®). These substitutes are processed in a growing Table 1 PDCAAS percentage for different food protein sources [44] number of convenience chicken- or beef-style products [10, 42]. These meat substitutes contain in general less Protein source PDCAAS % Limiting amino acid saturated fat and less cholesterol than meat, but are not Egg 118 good sources of iron and contain no vitamin B12 unless Milk, cheese 121 supplemented. Meat, fish 92 Branched amino acids Calcium, vitamin D and bone health Soy 91 Methionine, cysteine Corn 52 Lysine Rice 44 Lysine Sufficient calcium intake during childhood is important for Wheat 42 Lysine obtaining lifelong normal bone mineral density. Rickets has been described in vitamin D-sufficient toddlers on a 1492 Eur J Pediatr (2011) 170:1489–1494

Table 2 Nutritional advice in vegetarian infants (0–12 months) rice drink, cereals or juices are alternative calcium –Breastfed? sources. • lacto-vegetarian mother (consumingmeatorfishlessthanonceweekly): Sunlight exposure induces vitamin D synthesis in the check vitamin B12 serum level/urinary methylmalonic acid skin. A good dietary source of vitamin D, such as fortified

• vegan mother: supplement mother and child with vitamin B12 dairy products, soy drinks or cereals, is important for those –Bottlefed? not regularly exposed to sunlight, persons living at high • rice drinks, non-adapted soy drinks and almond drinks are not latitudes (especially in winter time), users of sun-blocking suitable milk substitutes, even if calcium-supplemented agents and dark-skinned people [1]. Plasma concentrations • infant formula or soy formula are indicated of 25-OH-vitamin D were found to be lower in vegans than –Weaning food? in lacto-vegetarians, both having lower levels than meat and • ensure continued breastfeeding or at least 400 ml of infant formula fish eaters [5] as source of protein and calcium • pureed legumes or tofu can be used from 6 months Fat and fatty acids • consider an iron supplement in breastfed infants from 6 months onwards The intake of essential fatty acids (EFA), linoleic acid • ensure sufficient caloric density of meals by adding oil, rich in (18:2n-6) and linolenic acid (18:3n-3), has to be ascertained linolenic acid (flaxseed, canola, rapeseed or nut oil) by the diet. These EFA are transformed into long-chain • check parents’ knowledge on preparation of foods and their access to a variety of foods poly-unsaturated fatty acids such as eicosapentaenoic acid • ask the parents to hold a 7-day food diary and refer to a dietician for (EPA; 20:5n-3), docosahexaenoic acid (DHA) and arach- evaluation idonic acid (AA; 20:4n-6). As for omnivores consuming little or no fish, vegetarians tend to consume a lot of n-6 but marginal amounts of n-3 fatty acids. Blood levels of EPA calcium-deficient diet, consuming large amounts of non- and DHA were found to be lower in vegetarians compared supplemented soy drink [20]. Bone mineral density and risk to non-vegetarians [38]. In order to restore n-6/n-3 balance, for bone fractures was found to be similar in omnivores and regular consumption of micro-algae (rich in DHA) and of lacto-vegetarians [3, 31]. The higher risk of bone fracture walnuts, canola oil or flaxseed oil (rich in α-linolenic acid) described in vegans appears to be associated with a low is recommended. mean calcium intake. Low bone mineral density has also been described in adolescents consuming a macrobiotic diet Iron and zinc low in calcium since young age [34]. In adults, calcium intake in lacto-vegetarians is equiva- Iron deficiency is not more common in vegetarians than in lent or higher than calcium intake in omnivores, while non-vegetarians, despite the fact that non-heme iron is less calcium intake in vegans is often lower than recommended bioavailable than heme-bound iron. Vitamin C, in fruits and [19, 45]. Vegan adults who consume >525 mg calcium daily vegetables, enhances iron absorption and counteracts the do not show higher fracture rates than omnivores [3]. inhibitory effects of phytates [1]. Green vegetables low in oxalate, such as broccoli, Due to the higher phytate content, zinc from vegetarian Chinese cabbage, collards and kale, are good sources of diets has a low bioavailability. Nevertheless, overt zinc calcium. In contrast, calcium in nuts, dried beans and deficiency has not been documented in Western vegetarians vegetables with high oxalate content such as spinach [14]. has a low bioavailability [1]. Calcium-fortified soy drink,

Practical advice on vegetarian child nutrition Table 3 Nutritional advice in vegetarian toddlers/preschool children

• ensure sufficient calcium intake (dairy products or calcium- Vegetarian diets can provide adequate nutrition for supplemented drinks) children, when parents and caregivers are knowledge- • check on sufficient caloric density of meals • limit raw non-processed foods (lower digestibility compared to Table 4 Nutritional advice in vegetarian adolescents cooked/fermented products, more difficult to ingest because of not fully developed oral motor mastication skills) • enquire about the reasons for becoming a vegetarian, evaluate weight • advice grinding nuts (prevent choking) concerns and body image, check on growth curve • vegan diet: ask the parents to hold a 7-day food diary and refer to a • provide adequate information sources (food guides, recipes, …)on dietician for evaluation healthy vegetarian diets

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