Journal of Human Nutrition and Dietetics (1992), 5, 11-21

The growth and development of vegan children

T. A. B. Sanders* and Joan Manning Department of Nutrition and Dietetics, King's College London, Campden Hill Road, London W8 7AH

The results of prospective study on the growth and diets, estimated from 7-day weighed food intake records, of 20 life vegan children (aged 5.8-12.8 years) are presented. The growth and development of the children were normal but they tended to be lighter in weight and exceptionally lean compared with standards. Heights were around the median of the Tanner-Whitehouse standards but were lower than the medians recently proposed by the Department of Health. Energy intakes were similar to those reported i n children of the same age in the general population, but dietary fibre intakes were very high which may have influenced the digestible energy. Sugar provided an average 15.6% of the dietary energy and this was supplied mainly by fruit and fruit juice. Mean fat intakes were close to the dietary reference values. Daily intakes of essential nutrients generally met the amounts recommended, with the exceptions of calcium and vitamin BIZ. Many children received supplementary sources of vitamin BI2 and only two children had intakes below the lower recommended nutrient intake. Intakes of saturated fatty acids were low and those of linoleic acid were high. The ratio of linoleic/a-linolenic acid was high. As docosahexaenoic acid is absent from vegan diets, it is suggested that vegans should use oils with a lower ratio of linoleic/a-linolenic acid. Future studies should also consider the influence of a vegan diet on retinal function. None of the children was immunized against whooping cough and 11 had not been immunized against polio: 16 of the children had suffered from whooping cough. Future studies need to take into account factors other than diet when assessing the health of vegans. The results of this study show that children can be successfully reared on a vegan diet providing sufficient care is taken to avoid the known pitfalls of a bulky diet and vitamin BIZ deficiency.

Key words: diet, growth, polyunsaturated fatty acids, vegans, vegetarianism, vitamin BIZ.

Introduction

The popularity of vegetarianism has in- creased greatly over the past few years with growing concerns about animal wel- fare, the environment and healthy eating. While strict vegetarian or vegan diets may offer certain advantages to the health of

'To whom correspondence should be ad- dressed.

adults, in view of their low saturated fat and high fibre contents (Sanders, 1978), their adequacy for children has been a moot point (Jacob & Dwyer, 1988).

In 1978 we began a prospective study on the growth and development of children born to vegan mothers (Sanders et al., 1978a, 1978b; Hughes, 1979; Sanders & Purves, 1981). In this paper we report on the dietary habits and development of the children in 1987-88.

11

12 T. A. B. Sanders and J. Manning

Methods

Twenty-seven vegan families who had been the subjects of earlier research (San- ders & Purves, 1981; Roshanai, 1983) were contacted by letter. Twelve families re- plied: one family was not willing to partici- pate, two families were no longer vegans, nine families agreed to take part in the study.

The families were visited at home by J.M. and a structured interview was car- ried out with the parents and children. The children were weighed in minimum in- door clothing on electronic bathroom scales that had been calibrated and their heights without shoes recorded with a portable stadiometer. Chest and head cir- cumference measurements were made and biceps, triceps and subscapular skinfold thickness were measured using Harpenden callipers. Photographs of all but two of the children were taken. The parents and children were given clear instructions on how to record foodintake. Each family was provided with a Soehlne electronic dietary balance (accurate to 1 g) and a food record diary. Food wrappers, recipes and the composition of packed lunches were re- quested where applicable. The families were asked to keep a weighed food-intake record for each child for a minimum of five consecutive days including a weekend. The families returned their diaries and the scales by post. They were reimbursed their postage expenses and sent photographs of their children.

Anthropometric measurements were compared with the Tanner and White- house standards and the centiles for height and weight were estimated using charts obtained from Creaseys Ltd (Castlemead, Herts SG14 1LH). Samples of hair were obtained from the children and analysed for heavy metals and trace elements by atomic absorption spectroscopy (Bio- labs; Weymouth Street, London). Nutrient intakes were calculated from the weighed food intake data using the FOODTABS computer program (T.A.B. Sanders, unpub- lished). This program uses the McCance and Widdowson data base (Paul & South- gate, 1978; Paul et al., 1979; Tan et al., 1985;

Holland et al., 1988, 1989) as well as supplementary information obtained from manufacturers.

Results

General health Twenty children (mean age 9.5 years, range 5.8-12.8 years) were studied. The general health of the children appeared good and all the children were registered with a general practitioner. Eight of the nine families, however, reported that they preferred to seek advice from an alterna- tive practitioner (homeopath or herbalist). Nineteen out of 20 of the children were registered with a dentist and 18 of these visited regularly. Two children had miss- ing teeth, two decayed teeth and nine had dental fillings. The mean decayed, missing or filled (DMF) index was 1.2 (S.E. 0.38).

None of the children had been vacci- nated against whooping cough and 16 had suffered from whooping cough. Only nine children had been immunized against po- lio. Nine children received vitamin BI2 supplements regularly.

All of the children had been breast-fed from birth, on average for 15.5 months (range 3 months-8 years). Three children received cows' milk or cow's milk infant formula at 1 week, 2 years and 5 years respectively.

One child WRS educated at home, one at a music school and all the others attended state schools. No behavioural problems were reported by the parents. Most of the children (17) took packed lunches to school, but four also had school lunches, usually chips and beans. Other food con- sumed away from the home included crisps, nuts and fruit, cakes, biscuits, jelly and sandwiches. Fifteen of the children did not mind eating non-vegan foods but five were upset by the thought and two of these claimed it made them physically ill.

The children were asked whether they had eaten any food of animal origin and if so what food and how often. The usual reason for eating non-vegan food was to be sociable. The quantities eaten were small

Growth and development of vegan children 13

Table 1. Anthropometric measurement on 20 vegan children

Height Mean 96 standard for age 100.7 Median centile for age 55

Mean % standard for age Median centile for age 35 Mean head circumference (cm) 53.9 Median centile for age 94 Mean Biceps skinfold (mm) 2.1

Median centile for age (3

Weight 95.5

Triceps skinfold Mean (mm) 2.7

Subscapular skinfold Mean (mm) 5.2 Median centile for age 25 Age (years) 9.5

Range

89.7- 110.8 (3-97

77-119 3-88

51-55.5 50- >97

1.8-2.9

1.9-3.7 all <3

3.6-5.9 (3-50 5.8-12.8

and were infrequently consumed [from once a week to 2-3 times a year). Cake, milk, biscuits, ice-cream, egg, chocolate and jelly were the non-vegan foods most commonly consumed.

Potato crisps were the favourite snack food, followed by sweets, fruit and health bars [i.e. muesli bars). Snack foods were part of the daily diet of 13 of the children.

The average age of the parents was 41 years [range 33-50). The mothers had been vegans for 16 years on average [s.d. 9.4 years). The parents in seven families drank moderate amounts of alcohol and in two families, the parents smoked cigarettes. The families bought their food in bulk from supermarkets as well as from special- ity shops. They all purchased wholegrain cereals and grew some of their own vege- tables. Six families always purchased or- ganic and pesticide-free foods. Eight of the families claimed to avoid food additives.

Anthropometric measurements The growth and development of the chil- dren were normal and their heights and weights were generally inside the normal range for children of their age [Table 1). However, there was a tendency for the children to be lighter in weight compared

with standards, although their heights were on average around the median. This tendency for the children to be smaller in stature was more marked in the boys than amongst the girls, and this was noted when the children were under the age of five years. One child was mildly malnourished at the age of 13 months-on resurveying her at age 8 years, she had caught up and was on the 75th percentile for weight and height for her age. The children were all exceptionally lean and this was reflected in their low skinfold thickness measure- ments. In contrast to the rest of their bodies, their head circumferences were high.

Dietary intakes The diets of the children consisted mainly of wholemeal bread, other cereals, pota- toes, soya products and fresh fruit and vegetables [Table 2). The weight of foods consumed was relatively high and the energy density was on average 1.15 kcal/g [range 0.93-1.37; s.e. 0.029). Table 3 shows the intakes of proximate nutrients. Fat provided on average 31.5% of the dietary energy. The intake of saturated fatty acids was very low in the children, but the intake of linoleic acid was high. Conse- quently the average polyunsaturated/satu-

14 T. A. B. Sanders and J. Manning

Table 2. Weights of food making up the daily diet of 18 vegan children

Bread Breakfast cereals Other cereals Cakes end biscuits Fats Vegetables Potatoes Other root vegetables Leafy vegetables Pulses, including soya milk Fresh fruit Dried fruit Nuts Sugar Jam Confectionery Fruit juice and soft drinks Other

g 137

33 63 21 29 88

162 42 34

239 216

13 25 4 5 5

238 205

Number of foods making up diet 55 (30-84)

rated ratio was 1.89. The ratio of n-6/n-3 fatty acids was also high, 44:l. Sugar provided on average 15.6% of the energy intake.

Table 4 shows the intakes of nutri- ents/1000 kcal compared with intakes of children of the same age estimated from 7- day weighed food intake records in North London reported by Nelson et aJ. (1990) eating mixed diets (the same software was

used to calculate nutrient intakes in that study). Comparisons of energy intakes are made in this case with the 1979 rec- ommended daily amounts (Department of Health and Social Security, 1979). The vegan diets provided greater amounts of most nutrients with the notable exceptions of fat, calcium and vitamin BIZ. The vegan diets provided large amounts of dietary fibre. Total energy intakes were similar to those reported in non-vegetarian children.

Comparisons of the intakes with esti- mated energy requirements and dietary guidlines are shown in Table 5. Compared with the recent WHO (1990) guidelines, intakes of sugar and polyunsaturated fat and total fat exceeded the upper limits recommended for the population. None of the children had intakes of vitamin D that approached the UK recommendation- although a dietary source may not be necessary if exposure to sunlight is ade- quate. The diets of the majority of children provided intakes below the recommended nutrient intakes (RNI) for calcium and vitamin B,2.

Table 6 shows the contribution made by different food groups to the intakes of selected nutrients. Cereals provided most of the energy, protein, carbohydrates, fibre, calcium and iron. Fats provided almost half the vitamin E intake and margarine about 20% of the vitamin A intake. Nuts and pulses provided useful amounts of

Table 3. Daily nutrient intakes of 18 vegan children aged 5.8-12.8 years

Mean Range

Energy (MJ) 7.20 5.60-10.48 Energy (kcal) 1720 1340-2500 Per cent EAR (DOH, 1991) 95 69-136 Protein % energy 12.4 9.2-16.9 Fat O h energy 31.5 22,O-45.5 Saturated fatty acid % energy 4.8 3.1-6.9 Linoleic acid % energy 8.8 4.35-13.41 Linolenic acid % energy 0.2 0.15-0.46 Polyunsaturated/Saturated ratio 2 -89 1.26-2.50 Carbohydrate % energy 55.6 43.8-65.6 Sugar % energy 15.6 8.2-26.5

23.5-52.3 Dietary fibre (g) 36.9

Growth and development of vegan children 15

Table 4. Nutrient density of the vegan children’s diets compared with those of British omnivorous children excluding supplements

British Vegan children*

children 7-12 yrs (n=18) s.d. (n=194)

Energy Oh RDA (DHSS, 1979)

Protein (g/1000 kcal) Fat (g/1000 kcal) Carbohydrate (g/lOOO kcal) Fibre (g/1000 kcal) Calcium (mg/1000 kcal) Iron (mg/1000 kcal) Zinc (mg/1000 kcal) Copper (rng/1000 kcal) Vitamin A (r.e./1000 kcal) Thiamin (rng/lOOO kcal) Riboflavin (rng/1000 kcal) Niacin (n.e./1000 kcal) Vitamin B, (mg/1000 kcal) Vitamin B,2 (&lo00 kcal) Total folate @g/1000 kcal) Biotin (pg/1000 kcal) Vitamin C (rng/1000 kcal) Vitamin D @g/1000 kcal) Vitamin E (mg/lOOO kcal]

83

31.0 35.0

21.8

12.6 4.3 0.96

0.98 1.00 14.0 0.79 1.3

146 10.9 54 1.1 4.4

148

270

546

15.7 82

5.12 6 30.8 6.4 41.1

4.42 9.2

7.1 5.7 0.85 3.9 0.14 0.96

0.22 0.64 0.49 0.82 3.02 14.1 0.19 0.66 1.18 1.64

29.6 77 2.95 7.9 24.2 38.2 0.60 0.9 0.81 2.5

36.9 135

48.3 400

202 370

‘Source: Nelson et 01. (1990).

protein, fibre, calcium and iron. Carrots provided 60% of the vitamin A intake. Fruit and fruit juice provided most of the vitamin C intake followed by potatoes and other vegetables. Very little of the sugar was provided by confectionery, sugars and preserves; most was provided by fruit (both fresh and dried) and soft drinks, mainly fruit juice. Potatoes were the most impor- tant source of potassium in the diet.

Table 7 shows the results of the hair mineral analyses. The results were gener- ally inside the reference ranges for the laboratory. One child had a slightly ele- vated level of lead in his hair. However, his father had a metal workshop in the garden and it is possible that the lead was not of dietary origin (e.g. solder) as his sister had normal levels of lead in her hair.

Discussion

This prospective study of the growth and

development of children reared as vegans is unique. Other studies of vegan children have been cross-sectional (O’Connell et al., 1989) and have involved the inclusion of children who have not been vegans for life. The families studied lived independently inside the general community, unlike some other studies which have looked at commune dwelling vegetarians. Neverthe- less, the families in our study differed from the general population in respects other than that of diet. These have implications for health. This was highlighted by the low proportion of children who have been immunized against whooping cough and polio. All the children were registered with a general practitioner and the low uptake of immunization was for ethical reasons as vaccines are usually raised in animals. It is noteworthy that the majority of the children had suffered from whoop- ing cough which, although rarely fatal, is associated with significant long-term mor- bidity.

16 T. A. B. Sanders and J. Manning

Table 5. Comparison of the nutrient intakes of the vegan children with dietary guidelines (DHSS, 1991)

Number out of 18

Energy (Estimated Average Requirement Protein< RNI Fat>30% energy Fat>35% energy Saturated fat>lo% energy Polyunsaturated fatty acids>lo% energy Sugars>lO% energy CalciumcRNI Calcium<LRNI IrontRNI ZinctRNI ZinctLRNI Vitamin A<RNI Vitamin AtLRNI Thiamin < R NI RiboflavintRNI Riboflavin< LRNI NiacintRNI Vitamin B,<RNI Vitamin B,,<RNI Vitamin B,,<LRNI FolatetRNI

16 0

11 3 0 5

17 17

1 0 9 0 2 0 0 6 0 0 0 9 (3)’ 2 (1)’ 0

*including supplements. RN1:recommended nutrient intake. LRNI: lower recommended nutrient intake.

Height is believed to be a good indicator of nutritional status, but diet is not the only environmental factor influencing height. Childhood illness can also cause growth faltering and this may have a permanent effect on growth. The growth and develop- ment of the children appeared to be within the normal range but there was a tendency for the children to be lighter in weight and shorter in stature compared with children on mixed diets. The tendency for the children to be short in height compared with standards was also noted when the children were under the age 5 (Sanders & Purves, 1981). In contrast to height, the head circumference was greater than the 90th centile. The Department of Health (1989a) found that children on mixed diets tended to be taller and heavier compared with the Tanner-Whitehouse standards which were based on measurements made on children in the 1960s. The vegan chil- dren were around the 50th centile for

height using these standards. The Depart- ment of Health (1991) has recently pro- posed new standards for height and weight which allow for the increase in average height and weight in the general popula- tion. If the vegan children are compared with those, then there is certainly a ten- dency for them to be shorter in stature.

In the present study it should be noted that the children were exceptionally lean. Weight and, in particular, the proportion of body fat is a good predictor of the rate of maturation. Adipose tissue plays an impor- tant role in the peripheral aromatization of androgens to form oestrogens. It would be predicted therefore that sexual maturation would be delayed in girls. This may be advantageous in that an early age of men- arche is well-known to be associated with an increased risk of breast cancer in later life.

The lower proportion of body fat in the children cannot be explained by low en-

Tab

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1.6

1.2

6.0

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4.7

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2.8

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16.6

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18

Table 7. Trace minerals in hair of 18 vegan children (mg/kg) aged 5.8-12.8 years

T. A. B. Sanders and J. Manning

Normal Mean s.d. range

Iron Calcium Zinc Chromium Manganese Selenium Nickel Cobalt Lead Mercury Cadmium Arsenic Aluminium

27 16 183 0.78 1.28 2.08 0.53 0.20 6.46 0.42 0.15 0.10 3.49

2.1 1.0 14.1 0.028 0.098 0.066 0.039 0.029 0.94 0.085 0.017 0.009 0.589

20-60 10-40 150-240 0.6-1.5 1.0-2.6 1.5-4.0 0.4-1.4 0.1-0.7 €15 (2 (0.5 (2 (10

ergy intakes as their energy intakes were similar to children on mixed diets. This tendency for leanness in vegans has been previously reported (Sanders et al., 1978b) and again there is little evidence to suggest that vegans have lower intakes of food energy than omnivores (Roshanai & San- ders, 1984; Sanders & Key, 1987). The diets of the vegan children contained large amounts of dietary fibre. This may have decreased the digestibility of fat and other energy-providing nutrients (British Nutri- tion Foundation, 1990).

Low serum vitamin BI2 concentrations have been reported both in vegans (San- ders et al., 1978a) and vegetarians (Reddy & Sanders, 1990) and in children reared on macrobiotic diets (Dagnelie et a]., 1989; Specker et al., 1990 Miller et al., 1991). The latter two reported increased urinary ex- cretion of methyl malonic acid in macro- biotic vegetarians which is consistent with an inadequate intake of the vitamin. A number of isolated cases of dietary vitamin B,* deficiency have been reported in ve- gans. Deficiency mainly presents as the more insidious neurological symptoms which can lead to peripheral neuropathy and optic nerve damage rather than as megaloblastic anaemia because of their high intakes of folate. Small amounts of vitamin B,,-like material is present in some plant foods, but is not biologically

active (Herbert, 1988). Fortified foods con- taining cyanocobalamin are, however, used by many vegans in the U.K. Most of the families were aware of the need to use food supplemented with vitamin B,, and generally the diets of the children pro- vided insufficient amounts of the vitamin. However, all but a few had adequate intakes if the contribution made by supple- ments were included. There is clearly a need for vegans to be vigilant in avoiding dietary vitamin BI2 deficiency.

Iron intakes were reassuringly high. The availability of iron from plant sources is generally low, but it would be enhanced by the high intakes of vitamin C provided by the vegan diets. Reddy & Sanders (1990) found low serum ferritin levels in vegetar- ians compared with omnivores. However, both vegetarian and vegan diets are able to sustain normal haemoglobin concentra- tions (Sanders et al., 1978a; Reddy & San- ders, 1990).

Calcium intakes almost without excep- tion were below the amounts rec- ommended by most authorities (National Research Council, 1989; Department of Health, 1991). However, they were gener- ally above the lower recommended nutri- ent intake (Department of Health, 1991). Besides milk products, there are few other rich sources of calcium. Fortunately, some soya milks, such as Plamil, are fortified with calcium. Dark green, leafy vegetables are often recommended as a good source of calcium but they are rarely eaten in suffici- ent quantity to make a significant contribu- tion to total intake. Cereals and pulses [particularly soya milk) were the most important sources of calcium in the vegan diets. Although the availability of calcium is reduced by the presence of phytates in cereals, the process of leavening bread destroys the phytate. The results of this study support the earlier conclusion drawn by Widdowson & McCance (1954) that children will grow and develop quite nor- mally on a diet consisting of plenty of bread and vegetables with minimal amounts of milk and meat.

The value of hair analyses for the assess- ment of mineral status has been ques- tioned (Fairweather-Tate, 1988). However,

Growth and development of vegan children 19

it was reassuring that the concentrations of essential and toxic minerals were inside the laboratory normal range.

It is of interest to compare the dietary intakes of the children with recent dietary guidelines. A decrease in ‘free’ or ‘extrin- sic’ sugars to less than 10% of the energy intake (WHO, 1990; Department of Health, 1991) have been advocated in order to avoid dental caries and obesity but also because sugar is regarded as a source of ‘empty calories’. From a practical stand- point, it is difficult to define, in the cur- rency of food, what is meant by the term ‘intrinsic’ sugar as defined by the Depart- ment of Health (1989b), especially as the ‘extrinsic’ sugar in fruit becomes, intrinsic sugar when it is chewed in the mouth! Similarly, the term ‘free sugar‘ is ambig- uously defined by the WHO (1990) as ‘including monosaccarides, disaccharides and other short-chain sugars produced by refining carbohydrates’. This begs several questions. Is the sugar in unsweetened apple juice free sugar? Is the sugar in bananas, dates and raisins free?

The total sugar intakes of the vegan children were high. However, only a small fraction was derived from ‘added sugars’, i.e. confectionary, jam and table sugar. Indeed vegans tend to avoid white sugar as animal charcoal is sometimes used to bleach it. Despite their high sugar intakes, the children generally had good teeth and the level of dental caries was low. More- over, there certainly was no evidence to suggest that their high sugar intake was causing obesity. In fact the opposite was true, the children were very lean. The desirability of decreasing the intake of sugar in these children is questionable as the foods that provided the sugar also supplied several other useful nutrients. Indeed, it would be more appropriate to advise them against consuming sugary snacks (including fruit) too frequently be- tween meals as frequency of consumption is more strongly related to risk of dental caries than the total quantity of sugar in the diet (Curzon,. 1988).

The Department of Health and Social Security (1984), WHO (1990) and Depart- ment of Health (1991) have recommended

reductions in total fat and saturated fatty acid intake. The rationale for imposing these limits is the association of obesity with high fat intakes and the relationship between high intakes of saturated fatty acids and coronary heart disease in adults. Total fat intakes were lower in the vegan children than in children on mixed diets and those of saturated fatty acid were particularly low. On the other hand, the intake of polyunsaturated fatty acids was relatively high. Moreover, the ratio of linoleic/linolenic acid was high and this is likely to inhibit conversion of a-linolenic acid (18: 3n -3) to docosahexaenoic acid (22:6n-93). This may be important as docosahexaenoic acid is absent from vegan diets (Roshanai & Sanders, 1984). Previous studies (Sanders et al., 1978b; Sanders & Younger, 1981; Roshanai, 1983) have re- ported reduced levels of docosahexaenoic acid in plasma, erthrocyte and platelet phospholipids of vegans compared with controls. Similar differences have also been noted in the Hindu vegetarians (Reddy & Sanders, 1987). Docosahexaenoic acid (22:6n-3) is believed to play an important role in the retina and in the central nervous system. It has been argued that docosahexaenoic acid might be condi- tionally essential for the premature infant. Primates fed on diets containing a high ratio of linoleic/linolenic acid show im- paired visual function (Neuringer et al., 1984) and this change is accompanied by a reduction in docosahexaenoic acid (22: 6n - 3) in blood lipids. However, re- versing the biochemical abnormality did not correct the impaired visual function (Connor et al., 1991). Uauy et al (1990) reported abnormal electro-retinograms in pre-term infants fed diets devoid of a- linolenic acid or its derivatives. The chil- dren in this study were all breast-fed. Lower levels of docosahexaenoic acid were found in the milk of vegan mothers com- pared with omnivore controls (Sanders et a]., 1978b) and the erythrocyte lipids of the infants also contained a lower proportion of 22 : 6n - 3 than infants breast-fed by omnivorous mothers or those bottle fed on cow’s milk formula (Sanders & Naismith, 1979).

20

It has been alleged that low levels of docosahexaenoic acid in brain may affect learning ability. Although we undertook no formal assessment of intelligence and cognitive skills, the children did not ap- pear to have any learning problems and were doing well at school. Some were exceptionally bright and had received mu- sic scholarships. However, it might be appropriate to recommend vegans to use soyabean or rapeseed oils instead of sun- flower, safflower or corn oils for cooking as these oils have lower ratios of a-linolenic/ linoleic acid.

In future, we hope to confirm whether sexual maturity occurs later in children reared on vegan diets and to carry out tests relating to visual function.

T. A. B. Sanders and J. Manning

Acknowledgments

The authors wish to thank the parents and children, Mrs Kathleen Jannaway and John Strettle, for their co-operation in the study, the Vegetarian Society for a grant and Dr John Howard and Dr Stephen Davies for the hair analyses.

References

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MS acccepted October 1991