Introduction

The number of people adopting a vegetarian eating pattern is increasing and can be estimated to be 2% to 5% of the adult population in Europe (http://en.wikipedia.org/wiki/Vegetarianism_by_country#Europe). Besides religious reasons and health considerations, concerns about global warming and sustainable food production are important motivators to adopt a vegetarian diet. One kilogramme of greenhouse gas emissions is associated with the production of 162 g protein from wheat and 32 g protein from milk, but only 10 g protein from meat [28]. Moreover, about 6 to 7 kg of soy protein are needed to produce 1 kg of animal protein [28]. Many of these vegetarians are young parents who want their children to share their eating pattern. This article intends to give the paediatrician insight on the health effects of vegetarianism in children, i.e. which diets carry a risk for deficiencies and how to monitor them and in which situations individualised counselling by a knowledgeable dietician is recommended.

Definitions [1, 2]

Vegetarianism is defined by not eating animal flesh foods, 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 lacto-ovo-vegetarianism, which includes milk, cheese and eggs. In contrast, veganism excludes all animal-derived food; hence, vegans do not consume dairy products or eggs. Raw food diets are based on non-cooked plant foods, using grounding and fermentation for enhancing digestibility. Fruitarians consume a diet limited to fruits and nuts. Other diets, like a macrobiotic diet, are part of a lifestyle philosophy. A macrobiotic diet favours locally produced foods with minimal processing—aiming at a balance between “yin” and “yang” products—and includes fowl or fish once or twice weekly but excludes dairy products.

Health effects of a vegetarian diet

Benefits

Whereas former publications tended to highlight the risks, a growing body of evidence is showing the long-term benefits of a vegetarian diet [39]. Meta-analyses from large cohort studies in adults show that vegetarians have a lower body mass index and lower mortality from ischaemic heart disease than omnivorous persons [15, 46, 48]. This protective effect is linked to a high consumption of unrefined vegetable products, such as whole grains, legumes, nuts, fruits and vegetables. The same health effect can probably be obtained by a prudent omnivorous diet, limiting the intake of meat combined with a high intake of whole plant foods, a dietary pattern, which is called “flexitarian” [6]. Studies in vegetarian children and with intermediary end points such as serum lipids and cholesterol are limited and yield conflicting results. Some studies show lower serum cholesterol [18], whereas others do not confirm this finding [29, 47].

Growth and development

Descriptive cohort studies have demonstrated an identical growth and weight evolution in lacto(-ovo)-vegetarian children and adolescents compared to their omnivorous peers, whereas vegan children tend to be leaner and smaller [7, 12, 21, 30, 32, 40, 41, 43, 49].

Eating disorders and vegetarianism

An association between vegetarianism and disordered eating behaviour has repeatedly been described in adolescents [17, 35, 37]. There is, however, no proof that a vegetarian diet predisposes to eating disorders. In most patients, signs of an eating disorder are present before the change to a vegetarian or vegan diet [33]. As a consequence, it is important for the clinician to be alert and to explore the reasons for adopting a vegetarian diet in adolescents, as it can be a method of concealing disordered eating behaviour. The majority of vegetarian adolescents, however, do not have an eating disorder [24].

Nutritional concerns

Vitamin B12

Animal products are the only reliable dietary source of vitamin B12 or cobalamin. The cobalamins present in algae and seaweeds have been shown to be non-active analogues of vitamin B12 [50]. The Recommended Dietary Allowance for cobalamin is 2.4 μg/day for adults, 2.6 μg/day for pregnant and lactating women and ranges from 0.7 μg/day for toddlers to 2 μg/day during adolescence [51]. Dairy products contain less cobalamin (0.3–0.4 μg/100 g) than eggs (0.9–1.4 μg/100 g) or meat and fish (3 and 33 μg/100 g). However, bioavailability of cobalamin from dairy products is higher than from meat, fish or eggs [50].

As vitamin B12 is an essential cofactor in DNA and RNA synthesis, deficiency symptoms will manifest first in organs with rapid cell turnover such as bone marrow and intestine. Moreover, it is indispensable for the maintenance of the nervous system [8]. Vitamin B12 deficiency results in haematological (megaloblastic anaemia) and neurological disorders (neurodevelopmental delay and regression, neuropsychiatric disorders). The haematological signs can be absent in the case of high folate levels; one third of vitamin B12-deficient adults do not display megaloblastic anaemia [4]. As neurologic damage by vitamin B12 deficiency can be irreversible [22], prevention is of utmost importance. Since current laboratory methods also measure non-active cobalamin analogues, serum levels within the lower normal range do not exclude a deficiency. Vitamin B12 is an essential cofactor for methionine synthase-converting homocysteine and also in the conversion of methylmalonyl-coenzyme A to succinyl-coenzyme A (Fig. 1). The metabolites of these enzymes will increase in case of vitamin B12 deficiency even before the presence of overt clinical symptoms. The measurement of increased homocysteine and methylmalonic acid concentrations in urine and plasma are more expensive but more sensitive methods to detect vitamin B12 deficiency [13].

Fig. 1
figure 1

Role of vitamin B12

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Whereas vegans have a much higher risk of developing vitamin B12 deficiency, it is not excluded in lacto-vegetarians. All persons consuming fish or meat less than once weekly are at risk of vitamin B12 deficiency. High methylmalonic acid levels in blood and urine and elevated levels of homocysteine, markers of functional vitamin B12 deficiency, have been described in vegetarians consuming limited amounts of dairy products [6, 22]. Infants breastfed by vegan mothers can develop vitamin B12 deficiency between the age of 2 and 12 months due to their limited body reserve at birth even in the absence of signs of the deficiency in the mother [25, 36]. Prevention is possible by consuming fish or meat once or twice weekly, by consuming supplemented food (e.g. supplemented soy products or cereals) or by a vitamin B12 supplement. Overdosing with vitamin B12 has not been described.

Proteins

Protein quality reflects the content and relative proportion of indispensable amino acids and is lower for plant-derived proteins than animal proteins. Protein quality of a given food is expressed as the protein digestibility corrected amino acid score (PDCAAS) [11]. This score depends on the limiting indispensable amino acid (in milligrammes per gramme protein) divided by the requirement for this amino acid for a pre-school child (in milligrammes per gramme protein), corrected for digestibility [53]. Table 1 summarises the PDCAAS for different food protein sources. Lysine is the limiting amino acid for cereals such as wheat, corn and rice, methionine for legumes such as soy and lentils. Whereas former advice on healthy vegetarian diets stressed the importance of combining different plant protein sources in one meal, later research indicates that variation in plant protein sources can be dispersed over a longer period of time [53]. The PDCAAS can be calculated not only for a specific food, but also for a diet. The PDCAAS probably underestimates true protein quality because the amount of the limiting indispensable amino acid from one source will be supplemented by another [44, 52]. Nevertheless, it remains a practical method for estimating whether or not a diet covers protein needs. As a vegan diet has a PDCAAS of 75–77%, protein requirements for vegans can be estimated to be 1.3 times those for omnivores [26].

Table 1 PDCAAS percentage for different food protein sources [44]
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In developed countries where a large variety of plant protein sources are available, protein needs are generally met, also in vegan children and adolescents. Infants on a vegan diet however, if not breastfed, are at risk for protein malnutrition [16]. Non-supplemented plant-derived milk substitutes based on cereal, nut or legume extracts are often wrongly referred to as rice “milk”, almond “milk” or soy “milk”. They should be properly named rice “drink”, almond “drink” and soy “drink” as their nutritional value is not comparable to milk. It can be argued to reserve the term “soy milk” for fully supplemented adapted soy formula, enriched with methionine, iron, zinc, calcium and vitamins, compliant with the regulations on infant formula.

“Tofu” (pressed soya curd), “tempeh” (fermented soybeans) and “seitan” (processed wheat gluten extract) are part of traditional Asian vegetarian diets for centuries. As vegetarianism is becoming more popular in Western countries, the food industry has developed meat substitutes based on soy protein isolates (textured soy protein), on mycoprotein and egg white (Quorn ®) or on other plant protein sources such as lupin flour (Lopino®). These substitutes are processed in a growing number of convenience chicken- or beef-style products [10, 42]. These meat substitutes contain in general less saturated fat and less cholesterol than meat, but are not good sources of iron and contain no vitamin B12 unless supplemented.

Calcium, vitamin D and bone health

Sufficient calcium intake during childhood is important for obtaining lifelong normal bone mineral density. Rickets has been described in vitamin D-sufficient toddlers on a calcium-deficient diet, consuming large amounts of non-supplemented soy drink [20]. Bone mineral density and risk for bone fractures was found to be similar in omnivores and lacto-vegetarians [3, 31]. The higher risk of bone fracture described in vegans appears to be associated with a low mean calcium intake. Low bone mineral density has also been described in adolescents consuming a macrobiotic diet low in calcium since young age [34].

In adults, calcium intake in lacto-vegetarians is equivalent or higher than calcium intake in omnivores, while calcium intake in vegans is often lower than recommended [19, 45]. Vegan adults who consume >525 mg calcium daily do not show higher fracture rates than omnivores [3].

Green vegetables low in oxalate, such as broccoli, Chinese cabbage, collards and kale, are good sources of calcium. In contrast, calcium in nuts, dried beans and vegetables with high oxalate content such as spinach has a low bioavailability [1]. Calcium-fortified soy drink, rice drink, cereals or fruit juices are alternative calcium sources.

Sunlight exposure induces vitamin D synthesis in the skin. A good dietary source of vitamin D, such as fortified dairy products, soy drinks or cereals, is important for those not regularly exposed to sunlight, persons living at high latitudes (especially in winter time), users of sun-blocking agents and dark-skinned people [1]. Plasma concentrations of 25-OH-vitamin D were found to be lower in vegans than in lacto-vegetarians, both having lower levels than meat and fish eaters [5]

Fat and fatty acids

The intake of essential fatty acids (EFA), linoleic acid (18:2n-6) and linolenic acid (18:3n-3), has to be ascertained by the diet. These EFA are transformed into long-chain poly-unsaturated fatty acids such as eicosapentaenoic acid (EPA; 20:5n-3), docosahexaenoic acid (DHA) and arachidonic 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 and DHA were found to be lower in vegetarians compared to non-vegetarians [38]. In order to restore n-6/n-3 balance, regular consumption of micro-algae (rich in DHA) and of walnuts, canola oil or flaxseed oil (rich in α-linolenic acid) is recommended.

Iron and zinc

Iron deficiency is not more common in vegetarians than in non-vegetarians, despite the fact that non-heme iron is less bioavailable than heme-bound iron. Vitamin C, in fruits and vegetables, enhances iron absorption and counteracts the inhibitory effects of phytates [1].

Due to the higher phytate content, zinc from vegetarian diets has a low bioavailability. Nevertheless, overt zinc deficiency has not been documented in Western vegetarians [14].

Practical advice on vegetarian child nutrition

Vegetarian diets can provide adequate nutrition for children, when parents and caregivers are knowledgeable [1, 2, 9, 23, 26]. Several health agencies have developed information systems on healthy diets such as the vegetarian food pyramid [27]. Age-adapted points of special attention are summarised in Tables 2, 3 and 4. As in all infants, children and adolescents, monitoring of weight evolution, growth and psychomotor evolution is indicated and part of the nutritional evaluation. Vegetarian diets can be as variable as omnivorous ones, hence it is important to take a detailed dietary history and to start from this information to give appropriate advice. Referral to a dietician interested in and acquainted with vegetarian diets can be indicated. In general, a well-balanced lacto-ovo-vegetarian diet can satisfy all nutritional needs of the growing child, whereas a vegan diet has at least to be supplemented with vitamin B12, with special attention to adequate intakes of calcium and zinc and energy-dense foods containing enough high-quality protein for young children [1, 2, 9, 23, 26]. The more restricted the diet and the younger the child, the greater the risk for deficiencies [16].

Table 2 Nutritional advice in vegetarian infants (0–12 months)
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Table 3 Nutritional advice in vegetarian toddlers/preschool children
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Table 4 Nutritional advice in vegetarian adolescents
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