Vegetarian diets and children”2

TAB Sanders and Sheela Reddy

ABSTRACT The diets and growth ofchildren reared on veg- infants and toddlers fed inappropriate vegetarian diets (5, 6) as
etarian diets are reviewed. Excessive bulk combined with low well as deficiencies of iron, vitamin B- 1 2, and vitamin D.
energy density can be a problem for children aged 5 y and can The adequacy of most diets is judged by the foods included in
lead to impaired growth. Diets that have a high content of phytate the diet, whereas vegetarian diets are defined by what foods are
and other modifiers of mineral absorption are associated with an excluded. Problems are more likely to arise ifthe variety of foods
increased prevalence of rickets and iron-deficiency anemia. Vita- making up the diet is restricted and particularly when the con-
mm B- I 2 deficiency is a real hazard in unsupplemented or un- sumption of dairy products is low. Vegetarian diets that contain
fortified vegan and vegetarian diets. It is suggested that vegans reasonable amounts of milk products and eggs are less likely to
and vegetarians should use oils with a low ratio of linoleic to be inadequate than vegan diets. As a rule, the greater the variety
linolenic acid in view of the recently recognized role of doco- of foods that make up the diet, the better the chances that all the
sahexaenoic acid in visual functioning. If known pitfalls are nutrients will be provided.

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avoided, the growth and development of children reared on both In Western developing countries, economic factors do not play
vegan and vegetarian diets appears normal. Am J Cliii Nutr as major a role in restricting food choice as they do in other
1994;59(suppl):l 1765-815. developing countries. For example, there is clear evidence that
the growth of infants reared on vegetarian diets is retarded com-
pared with those eating mixed diets in India, where poverty, in-
KEY WORDS Vegetarian, vegan, growth, vitamin B-12,
testinal infestation, and high parity are common, and that these
vitamin D
infants are also at increased risk of anemia (7). On the other hand,
when people of Indian origin migrate to developed countries and
Introduction maintain their vegetarian dietary practices but consume more
dairy products, the impact of the vegetarian diet on growth is
The popularity of vegetarianism has increased greatly over the more limited (8, 9).
past few years because of concerns about animal welfare, the Most reviews on the influence of vegetarian diets on children
environment, and healthy eating. Although vegetarianism is a have focused on studies of white populations such as Seventh-
relatively recent phenomenon in the West, it has been practiced day Adventists, commune-dwelling vegetarians, or ethical veg-
in Asia for centuries, especially by followers of the Hindu reli- etarians. In the United Kingdom there is a large ethnic minority
gion. The health and diet of adult Western vegetarian groups has ( one million) of Indian origin. One subethnic group, the
been extensively studied and generally appears to be good (I). Gujarati population, are predominantly Hindu and are lifelong
Although strict vegetarian or vegan diets, in view of their low vegetarians. The Gujarati population originates from the northern
saturated fat and high fiber contents, may offer certain advantages Indian state of Gujarat although many immigrated from East
to the health of adults, their adequacy for children has been a Africa. The other major subgroups in the United Kingdom orig-
moot point (2). More recently, the adoption of vegetarian diets mate from the Punjab or Bengal, are not vegetarians, and follow
has been associated with eating disorders in female teenagers, either the Muslim or Sikh religions. Comparisons could be made
which lead to disorders of menstruation (3). Widdowson and between these different groups to study the lifelong effects of
McCance (4), in their classic experiment carried out at the end vegetarian diets.
of World War II, clearly demonstrated that children will grow Studies on the growth and development of vegetarians are con-
and develop quite normally on a diet consisting of plenty of bread founded by the different reasons for following the diets. Vege-
and vegetables with minimal amounts of milk and meat. There tarianism may be associated with different lifestyles and attitudes
is no doubt that a properly selected vegetarian diet can meet all toward health as well as toward the use of health care facilities.
the requirements of growing children, yet many health profes- For example, some ethical vegetarians will refuse to be immu-
sionals still remain concerned about the adequacy of vegetarian nized against polio, tuberculosis, and pertussis on the grounds
diets. that the antisera are prepared from animals. Childhood illnesses
Risk of nutrient deficiency is greatest during periods of phys-
iological stress and accelerated growth. Problems of dietary in- From the Department of Nutrition and Dietetics, Kings College, Uni-
adequacy are more likely to occur in children than in adults, as versity of London.
their requirements relative to body weight are greater and they 2 Reprints not available. Address correspondence to TAB Sanders,
are unable to exert the same degree of control over what they eat Department of Nutrition and Dietetics, Kings College, University of
compared with adults. Severe malnutrition has been reported in London, Campden Hill Road, London, England W8 7AH.

1 l76S Am J Clin Nutr l994:59(suppl):l 1765-815. Printed in USA. © 1994 American Society for Clinical Nutrition
 VEGETARIAN CHILDREN ll77S

can cause growth faltering and thus influence growth indepen- It seems almost certain that lower birth weights in the vege-
dent of diet. tarian population are due to diet. Although deficiencies of micro-
Meat and fish provide several nutrients that are scarce or absent nutrients may have an important influence on early pregnancy,
from common foods of plant origin and these include iodine, they are not believed to affect birth weight because of the effi-
taurine, vitamin B-l2, vitamin D, and long-chain polyunsaturated ciency of the placenta in extracting micronutrients from the cir-
fatty acids such as eicosapentaenoic (20:5n-3) and docosahexa- culation. Nevertheless, factors that influence placental develop-
enoic acid (DHA) (22:6n-3). Meat and fish also make a signif- ment and blood flow could influence birth weight. Energy intake
icant contribution to protein intake although protein requirements is believed to be a major factor that influences birth weight. En-
are easily met by vegetarian diets especially if they are derived ergy intakes are low in Hindu vegetarian women. Moreover, 5ev-
from a variety of dietary sources. Meat is an important source of eral studies showed that women with habitually low energy in-
iron in the diet and the heme form is particularly well absorbed. takes gave birth to heavier babies when given additional food
Iron intakes of vegetarians are strongly dependent on the iron energy (16). The practice of fasting in Hindu women could lead
content of staple foods, with wheat being far superior to rice. to decreased availability of glucose for the fetus. However, there
Plant foods contain a number of substances that modify the ab- is no evidence to suggest that energy intakes are lower in Hindu
sorption of several minerals such as iron, zinc, and calcium. vegetarians compared with Muslim women (17).
These modifiers occur in higher concentrations in the unrefined It is possible that lower birth weight of infants born to vege-
cereals that are favored by many vegetarians. This adds another tarian women is related to poor nutritional status for iron, folate,
dimension to the problem as some vegetarian groups are against or vitamin B-l2, which will be discussed later. Whether or not
processing food and advocate the consumption of raw food. lower birth weight in the vegetarian population is of any patho-
These vegetarian groups, particularly those who eat large physiological significance is unclear.
amounts of unrefined, unleavened cereals (eg, brown rice and
chapatis) may have problems with the absorption of certain mm-

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erals. This may lead to iron-deficiency anemia and rickets. This Growth
problem can also occur in individuals who consume small
amounts of fish and meat and thus is not a problem specific for Gujarati children tend to be an average of 3 cm shorter than
white children (9). However, Asian children born in the United
vegetarians.
Kingdom are taller than those born in East Africa, India,
This paper reviews the nutritional adequacy of vegan and veg-
etarian diets for children and identifies the conditions under Pakistan, or Bangladesh. This may be attributed to improved nu-

which nutritional deficiency can arise. It also looks at the influ- trition and a low incidence of infectious diseases (I 8). The

ence of vegetarian diets on growth and considers some new de-

growth of the white Seventh-day Adventist (SDA) vegetarian
velopments in essential-fatty-acid nutrition. population appears virtually indistinguishable from that of white
omnivores (19, 20). Lower growth rates particularly in the first
5 y of life have been reported in children reared on vegan (21,
Birth weight 22) and macrobiotic diets (14). Despite lower rates of growth in
the first 5 y of life, catch up growth occurs by the age of 10 y
The duration of pregnancy is a4-5 d shorter in Hindu vege-
tarians and both an earlier onset of labor and cesarian sections
(Table 1) ( 14, 24). Height is normal in vegan children but there
are more common in Hindus than in the white population in the is still a tendency for them to be lighter in proportion to their
height than children consuming mixed diets. The lower rates of
United Kingdom (10, 1 1). Sudden-infant-death syndrome is less
common among the Asian subpopulation in the United Kingdom
growth observed in some vegetarian children aged < 5 y can be

(1 1 ). Babies born to Hindus are lighter than those born to

attributed to low energy intakes. The bulky nature and low energy
Muslims or whites even when adjustments are made for gesta- density of some vegetarian diets restricts the amount of food

tional age and maternal frame size. It has been suggested that
this might reflect poor nutritional status, especially zinc and cop- TABLE 1
per status, but measurements of serum concentrations of these Anthropometric measurement of 20 vegan children
minerals failed to show evidence of deficiency (12). We recently
confirmed the shorter duration of pregnancy and that birth Mean Range
weight, head circumference, and length are all lower in the Hindu
Height
vegetarian population even after correcting for gestational age,
Percent standard for age (%)‘ 100.7 89.7- 1 10.8
sex of infant, parity, smoking habits, maternal age, and height Median centile for age 55 <3->97
(13). The mean adjusted birth weight was 240 g lighter in the Weight 95.5 77-119
Hindu vegetarian population compared with the nonvegetarian Percent standard for age’
white population. This is greater than the 190 g difference that Median centile for age 35 3-88
was previously reported for Hindu subjects in the United King- Head circumference (cm) 53.9 51-55.5
dom. Lower birth weights have also been reported in white pop- Median centile for age 94 50- >97
Biceps skinfold thickness (mm) 2.1 1.8-2.9
ulations who consume macrobiotic diets, which are predomi-
Triceps skinfold thickness (mm) 2.7 1.9-3.7
nantly vegetarian (14). However, it is uncertain whether the
Median centile for age <3 <3
lower birth weight in those communities is associated with a
Subscapular skinfold thickness (mm) 5.2 3.6-5.9
shorter duration of pregnancy. Dagnelie (14) noted that macro-
Median centile for age 25 <3-50
biotic subjects who consumed fish more than once a week gave Age (y) 9.5 5.8-12.8
birth to babies who were 1 80 g heavier. We also reported a
tendency for lower birth weights in the vegan population (15). ‘ Standards from reference 23.
 ll78S SANDERS AND REDDY

TABLE 2 Most vegan children are breast-fed well into the second year
Weights of food making up the daily diet of 18 vegan children’ of life and problems of nutritional inadequacy are only likely to
occur if the infants are prematurely weaned onto an unsuitable
Food Weight
breast-milk substitute (2). Many of the potential hazards of vegan
g diets can be avoided by the use of fortified soya milks in the
Bread 137 postweaning period. The diets consumed by vegan and vegetar-
Breakfast cereals 33 ian schoolchildren are usually similar to those consumed by
Other cereals 63 adults. Tables 2 and 3 show the typical nutrient composition
Cakes and biscuits 21 consumed by British vegan children compared with other chil-
Fats 29
dren of the same age consuming mixed diets. The vegan diets
Vegetables 88
were based around whole-meal bread as a staple and contained
Potatoes 162
Other root vegetables plenty of soy products (24). This clearly illustrates the similarity
42
Leafy vegetables 34 of vegan diets and mixed diets with respect to nutrient content.
Pulses, including soya milk 239
Fresh fruit 216
Dried fruit 13 Iron-deficiency anemia
Nuts 25
Sugar 4 The Asian vegetarian population has a higher incidence of
Jam 5 iron-deficiency anemia compared with the general population
Confectionary 5 (24). Infants and pregnant women are most susceptible with in-
Fruit juice and soft drinks 238 cidences being highest in those who rely on rice as a staple of
Others 205 their diet rather than wheat (28). A prevalence as high as 40%
(hemoglobin < 1 10 gIL) was found in Asian infants aged 22 mo

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I Number of foods making up diet, .i(range) = 55 (30-84).
(29). Iron-deficiency anemia in infancy is associated with late
weaning practices. It has also been reported in macrobiotic veg-
energy that can be consumed. Children aged > 5 y are able to etarians (30). However, iron intakes appear to be high in vege-
exert their own food preferences and are able to forage for food tarians and vegans whose staple food is whole-meal bread. He-
in the home. Energy intakes in older vegan children are similar moglobin concentrations are generally normal in both SDA and
to those of children consuming mixed diets. British vegans and vegetarians. Serum femtin concentrations are
Weight, in particular the proportion of body fat, is a good low in vegetarian women of childbearing age (3 1 ) and this may
predictor of the rate of sexual maturation. Adipose tissue plays mean that infants born to vegetarians have lower stores of iron.
an important role in the peripheral aromatization of androgens to
form estrogens. It would be predicted, therefore, that age of men- TABLE 3
arche might be delayed in children reared on vegetarian diets. A Nutrient density of the vegan children’s diets compared with British
later age of menarche has indeed been noted in SDA vegetarian omnivorous children, excluding supplements
girls (25). In our own studies age of menarche was slightly higher
in children reared as vegans or vegetarians (between 13 and 15 Omnivourous
Vegan children children aged
y of age, TAB Sanders, unpublished observations, 1992) but cer-
aged 6-13 y’ 7-12 y2
tainly not as high as > 16 y, seen in China and in the past century
in Europe. Energy (percent of RDA)3 (%) 83 ± 15.7 82
Protein (gIMJ) 7.4 ± 1.22 7.3
Fat (gIMJ) 8.3 ± 1.52 9.8
Dietary intakes Carbohydrate (gIMJ) 35.3 ± 8.79 32.1
Fiber(g/MJ) 5.2 ± 1.05 2.2
Calcium(mgIMJ) 64.3 ± 11.5 95.2
Numerous studies have measured nutrient intakes in white
Iron (mg/Mi) 3.0 ± 1.71 1.4
vegan and vegetarian children (19-22, 24). However, individuals
Zinc (mg/Mi) 1.0 ± 0.20 0.9
who are able to keep an accurate dietary inventory are generally
Copper (mgfMJ) 0.23 ± 0.03 0.23
well educated and informed and therefore may not be truly rep-
Vitamin A (REIMJ) 130 ± 48.1 88
resentative of the vegan or vegetarian populations. A major dif- Thiamin (mgIMJ) 0.23 ± 0.05 0.15
ference between white vegan and vegetarian groups and those Riboflavin (mgfMJ) 0.24 ± 0.1 17 0.20
following Asian vegetarian or macrobiotic diets is the use of Niacin (NEIMJ) 3.33 ± 0.72 3.36
bread as a dietary staple and the use of soy products in the white Vitamin B6 (mgIMJ) 0.19 ± 0.045 0.16
vegan and vegetarian groups. There are few qualitative differ- Vitamin B12 (.tgIMJ) 0.31 ± 0.281 0.39
ences in the diets of both white vegans and vegetarians compared Total folate (igIMJ) 35 ± 7. 1 18
with omnivores with the exception of the intakes of vitamin B-
Biotin (igIMJ) 2.6 ± 0.70 1.9
Vitamin C (mg/MJ) 13 ± 5.8 9.1
12 and, in vegans, calcium. The intake of all other essential nu-
Vitamin D (pg/MJ) 0.26 ± 0. 14 0.21
trients is similar or greater in vegan or vegetarian children than
Vitamin E (mg/MJ) I .05 ± 0. 193 0.60
in children reared on mixed diets. Fat intakes tend to be slightly
‘i±SD:n= 18.
lower, providing 30-35% of dietary energy, in vegan and veg-
etarian children and carbohydrate intakes are higher, 55% of 2 , 194.
dietary energy. 3 Recommended daily amount from reference 26.
 VEGETARIAN CHILDREN 1 l79S

Kim et al (32) found that low birth weight and inadequate ges- hormone production and increases the catabolism of vitamin
tational weight were strongly associated with anemia in the first D (46).
trimester. Scholl et al (33) found that low femtin concentrations A high prevalence of rickets has also been noted in children
( < I 2 pgfL) in early pregnancy are associated with an increased reared on macrobiotic diets (47, 48). However, rickets is not a
risk of prematurity and low birth weight. The use of iron supple- problem in SDA vegetarians and vegans. It seems likely that, as
ments during pregnancy may be desirable in these groups. in Asian rickets, the high phytate content of the macrobiotic diet
is a contributing factor in the development of rickets.

Vitamin B-12 deficiency

n-3 Fatty acids
The incidence of megaloblastic anemia resulting from corn-
DHA (22:6n-3) is believed to play an important role in the
bined vitamin B-12 and folate deficiency in Asian vegetarians is
retina and in the central nervous system (49). DHA is found
three times higher than the UK national average (34). Megalo-
predominantly in meat and fish and in small amounts in eggs and
blastic anemia may be precipitated during pregnancy and babies
milk but is absent from frequently consumed foods of plant ori-
may also be prone to develop severe vitamin B-12 deficiency,
gin. It can be synthesized to a limited extent from linolenic acid
particularly if breast-fed with milk of low vitamin B- 12 content
(18:3n-3) but this is subject to competitive inhibition from lin-
(35). Megaloblastic anemia is rarely encountered in white vegans
oleic acid (I 8:2n-6) (50). Lower proportions of DHA have been
and vegetarians because of their high intakes of folate. Conse-
found in both plasma and umbilical cord artery phospholipids
quently, vitamin B-12 deficiency usually presents with neurolog-
from vegetarians compared with omnivores ( 1 5). This is not un-
ical signs and symptoms in infants (36, 37). Many vegans are
expected because lower proportions of these fatty acids are found
aware of the need to supplement their diets with vitamin B-12
in the plasma phospholipids of vegetarians. Lower concentrations
but intakes are often too low. Vegetarians may also need to con-
of DHA were also found in the milk of vegan mothers compared

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sider supplementing their diets with vitamin B-l 2. Many pro-
with omnivore control subjects and the erythrocyte lipids of the
cessed foods are fortified with vitamin B-l2 but these foods are
infants also contained a lower proportion of DHA than infants
not necessarily acceptable to ethical vegetarians. Both vegans
breast-fed by omnivorous mothers or those bottle-fed with a cow
and vegetarians clearly need to be vigilant to avoid vitamin B-
milk formula. Recent studies have shown that preterm infants
12 deficiency.
deprived of DHA also show abnormalities in visual and cortical
functions (5 1 ). It is uncertain whether the size of changes re-
ported in vegans and vegetarians are sufficient to result in marked
Rickets
changes in physiological functioning. However, differences in
maternal diet result in infants being born with different stores of
Cases of rickets affecting both vegetarian and nonvegetarian
essential fatty acids.
groups in the Asian ethnic minority in the United Kingdom have
Many vegetarian and particularly vegan diets are rich in lino-
been reported for > 30 y (38). ‘ ‘Asian rickets’ ‘ differs from vita-
leic acid and have a high ratio of linoleic to linolenic acid. Such
mm D deficiency because it is found not only in infancy but
a diet inhibits conversion ofa-linolenic acid ( 18:3n-3) to DHA.
throughout childhood and adolescence (39). In a formal assess-
It might be appropriate to recommend vegans to use soybean or
ment of the prevalence of nutritional rickets, Holmes et al (40)
canola oils instead of sunflower, safflower, or corn oils for cook-
found that 30% of Asian children had clinical rickets compared
ing as these oils have lower ratios of linoleic to a-linolenic acid.
with 4% of white children. Significantly lower concentrations of
25-hydroxycholecalciferol were found in Asians compared with
whites; concentrations < 1 2.5 nmolIL occurred in 33% of Asian Conclusion
girls and 22% of Asian boys (4 1 ). From seasonal measurements
of the plasma concentrations of vitamin D, it is clear that Asians Several hazards of vegetarian diets have been identified. These
do not accumulate stores of vitamin D during the summer months include iron deficiency anemia, vitamin B- 1 2 deficiency, rickets,
because of limited exposure to sunlight (42). The prevalence of and a bulky diet that can restrict energy intake in the first few
Asian rickets appears to have declined (43). The exact reason for years of life. However, these known pitfalls are easily avoided.
the decline remains unknown. Although general health and development appears to be normal
Factors known to influence rickets are the dietary intake of in vegetarians there may be subtle differences compared with
vitamin D, exposure to sunlight, and the availability of dietary omnivores. There is no evidence to suggest that neural function
calcium. Naturally occurring dietary sources of vitamin D are or intellectual function are impaired because of a lower intake of
limited and are confined to liver and oily fish, although several n-3 fatty acids. Impaired psychomotor development has been
foods such as margarine and breakfast cereals are fortified with reported in previously malnourished macrobiotic infants but a
the vitamin. Although skin pigmentation may decrease the ca- follow-up study reported higher than average intelligence quo-
pacity to synthesize vitamin D, rickets is uncommon in the Afro- tients in older macrobiotic children (52), which confirmed an
Caribbean subpopulation. Modifiers of calcium absorption, eg, earlier observation made on a different macrobiotic community
phytic acid, contributed by unrefined cereals, particularly in (53). This, however, may reflect the high educational status of
chaptis (unleavened breads), have been implicated as a cause of the parents. Furthermore, the educational attainment of children
Asian rickets, and the reduction of dietary phytic acid has been born to Asian parents in the United Kingdom is above average
shown to promote healing (44). Heath (45) proposed that high (54). However, this does not rule out the possibility that there
phytate diets increased vitamin D requirements. It is known that may be subtle differences in visual or neural functioning and
low availability of calcium from the diet increases parathyroid studies in this area are warranted. U
1 1 80S SANDERS AND REDDY

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