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1 From the Department of Food and Nutrition, Umeå University, Umeå, Sweden.
2 Supported by grants from the Faculty of Social Sciences, Umeå University; the Swedish Institute; the Swedish Foundation for Healthcare Science and Allergy Research; the Swedish Nutrition Foundation; and the JC Kempes Memorial Fund. 3 Address reprint requests to CL Larsson, Department of Food and Nutrition, Umeå University, SE-901 87 Umeå, Sweden. E-mail: christel.larsson{at}kost.umu.se.
ABSTRACT
Background: Adolescents sometimes become vegetarian for ethical rather than health reasons. This may result in health problems caused by lack of interest in and knowledge of nutrition.
Objective: We compared the dietary intake and nutritional status of young Swedish vegans and omnivores.
Design: The dietary intakes of 30 vegans (15 males and 15 females; mean age: 17.5 ± 1.0 y) and 30 sex-, age-, and height-matched omnivores were assessed with the use of a diet-history interview and validated by the doubly labeled water method and by measuring nitrogen, sodium, and potassium excretion in urine. Iron status and serum vitamin B-12 and folate concentrations were measured in blood samples.
Results: The diet-history method underestimated energy intake by 13% and potassium intake by 7% compared with the doubly labeled water method and 24-h urine excretion, respectively. Reported dietary nitrogen and sodium intakes agreed with the 24-h urinary excretion measure. Vegans had higher intakes of vegetables, legumes, and dietary supplements and lower intakes of cake and cookies and candy and chocolate than did omnivores. Vegans had dietary intakes lower than the average requirements of riboflavin, vitamin B-12, vitamin D, calcium, and selenium. Intakes of calcium and selenium remained low even with the inclusion of dietary supplements. There was no significant difference in the prevalence of low iron status among vegans (20%) and omnivores (23%). Two vegans with low intakes of vitamin B-12 had low serum concentrations.
Conclusion: The dietary habits of the vegans varied considerably and did not comply with the average requirements for some essential nutrients.
Key Words: Adolescents • diet-history method • dietary intake • folate • iron • nutritional status • vegan • vegetarian • omnivore • vitamin B-12 • Sweden
INTRODUCTION
In the early 20th century, few people accepted vegetarian foods as sufficient for a healthy diet, although many realized that eating more vegetables was necessary for good health (1). In the middle of the 20th century, a Scandinavian author, Are Waerland (2), strongly emphasized the importance of a lactovegetarian diet, physical activity, and abstinence from alcohol and tobacco in restoring good health to the body. Waerland advocated a diet characterized by high intakes of water, vegetables, fruit, and berries; limited intakes of dairy products, salt, and spices; and the exclusion of meat, fish, eggs, coffee, tea, sugar, white flour, alcohol, and tobacco (2). This diet and lifestyle were endorsed to promote health and to avoid and cure diseases. Ethical concerns were not a major issue.
A well-planned and varied vegetarian diet is perfectly consistent with good health and can potentially reduce the risk of many chronic diseases (3). However, care must be taken during times of extra nutritional demand, such as adolescence, to ensure sufficient intake of energy, calcium, iron, and vitamins B-12 and D (4). Approximately 5% of Swedish students aged 16–20 y eat a vegetarian school lunch, and 0.1% eat vegan food (5). Consumption of vegan school lunches is more common in some areas of Sweden than in others. For example, in the northern town Umeå, 2% of 16–20-y-olds were reported to eat a vegan school lunch (5). Vegetarianism may be a fad with some adolescents, but for others it is based on a strong conviction that lasts for years or even a lifetime. Young people choose to adhere to a vegetarian diet for many reasons, but ethical and ecologic concerns appear to be a more common motivation than health (6). Consequently, some young vegetarians may have limited nutritional interest and knowledge and poor meal planning. There is a risk that meat and other animal products are excluded without being replaced by nutritionally equivalent vegetarian foods. In these cases, the overall dietary intake may not comply with the daily nutritional needs of the adolescents. The concern increases with more restrictive food choices and would most likely be greater for vegans than for other types of vegetarians.
The aim of this study was to assess the dietary intake and nutritional status of a group of Swedish vegans aged 16–20 y living in Umeå, Sweden, by using a validated diet-history (DH) method and blood samples to compare the results with those for sex-, age-, and height-matched omnivores.
SUBJECTS AND METHODS
Subjects
Volunteers were recruited through advertising and visits to schools in the Umeå area. The subjects had to be 16–20 y of age and in good health, with no chronic diseases. Vegans were defined as people eating food of plant origin only and were included in the study if they had consumed a vegan diet for 6 mo and were planning to continue. Omnivores were defined as people eating food of both plant and animal origin and were included if they had consumed an omnivorous diet for their entire life and were planning to continue this diet. In total, 65 vegetarians and 272 omnivores were interviewed. Thirty vegans were eligible for inclusion. Thereafter, 30 omnivores were matched by sex, age (±6 mo), and height (±3.5 cm). Each participant gave written, informed consent, and the study was approved by the Research Ethics Committee of the Medical Faculty, Umeå University, Umeå, Sweden.
Dietary assessment
Each respondent was asked about customary food intake during 2 separate 1–2-h DH interviews (1–2 wk apart) during August 1997–June 1998. The aim was to construct a typical eating pattern for the preceding 3 mo. Portion sizes of foods were described in terms of household measures, standard weights of food items, 3-dimensional food models, or portion photographs of known weights (7). The reported food, beverage, and dietary supplement intakes were entered in the dietary analysis program Stor MATs 4_03e (Rudans Lättdata, Västerå, Sweden), which uses the Swedish food composition database (version 2_97; National Food Administration, Uppsala, Sweden). Recipes and information on nutritional content were entered for composite foods and dietary supplements not listed in the food database. The calculated vitamin and mineral intakes were compared with average requirements for groups and lowest recommended intakes for individuals, according to the Nordic Nutrition Recommendations (8). Body weight was measured with a scale to the nearest 0.1 kg while the subjects were wearing light underwear, and height was measured to the nearest 0.5 cm.
Validity of the dietary assessment
Energy expenditure determined by the doubly labeled water (DLW) method and measurement of nitrogen, sodium, and potassium excretion in 24-h urine collections were used to validate reported energy and nutrient intakes (9). The total energy expenditure of 32 subjects (16 vegans and 16 matched omnivores) was measured during 14 d with the use of the DLW method (10). To validate reported nutrient intakes, nitrogen, sodium, and potassium excretion was measured in all subjects by using four 24-h urine collections per person (11). Sodium and potassium in urine were determined by flame atomic absorption spectrophotometry (Perkin-Elmer model 5000; Norwalk, CT), according to routine clinical laboratory procedures, and urine collections with para-aminobenzoic acid recovery between 50% and 85% were adjusted by a linear regression method (12). We previously described the validity of the DH (13).
The reported intakes of energy, nitrogen, sodium, and potassium were divided by the respective biological markers to detect under- or overestimation in the DH (10). Measured energy expenditure, nitrogen in urine divided by the excretion factor 0.81 (11), and sodium in urine (14–16) were used as biological markers for reported energy, nitrogen, and sodium intakes, respectively. The measured potassium in urine divided by the excretion factor—0.73 for lactovegetarians and 0.77 for omnivores (15)—was used as the biological marker for potassium intake, because potassium in feces was not measured (14).
Nutritional assessments
After the DH interviews, 3 fasting venous blood samples (1 wk apart) were taken. Hemoglobin, serum iron and ferritin, total-iron-binding capacity, transferrin saturation, and immune cell concentrations were measured to enable classification of the subjects' iron status. Three blood samples were required to accurately determine ferritin (17). Before each blood sample was taken, the subjects completed a short questionnaire about the last time they had eaten, infections, antibiotic treatment, dieting, and stress. One fasting venous blood sample for measuring vitamin B-12 and folate in serum was taken at the same time as the first sample for iron-status classification.
All blood samples were analyzed according to standard methods used at the Clinical Chemistry Department, University Hospital of Umeå, Umeå, Sweden. Hemoglobin was measured by using cyanmethemoglobin and an absorbance measurement on a sample in EDTA-containing tubes. Iron was measured by a colorimetric assay, ferritin by an immunoturbidimetric assay, and total-iron-binding capacity by an alkaline buffer–reductant solution from Roche Diagnostics (Indianapolis). Iron status was classified as normal, early negative iron balance, iron depletion, iron-deficient erythropoiesis, or iron deficiency anemia, according to definitions by Herbert (18). Vitamin B-12 and folate were analyzed with the Quantaphase II B12/Folate Radioassay (Bio-Rad Scandinavia Inc, Upplands Väsby, Sweden). Adequate blood concentrations of vitamin B-12 and folate were defined as within 95–568 pmol/L and 3.4–47 nmol/L, respectively.
Statistical analyses
Data are expressed as means ± SDs and means with 95% CIs. Differences between measurements and groups were analyzed with the use of the Mann-Whitney U test. A two-tailed P value of <0.05 was considered statistically significant. All statistical analyses were performed with SPSS (version 10.0; SPSS, Inc, Chicago).
RESULTS
Subjects
The present paper reports dietary data on 60 age-, sex-, and height-matched adolescents with a mean age of 17.5 ± 1.0 y, living in Umeå, Sweden. Male vegans weighed less than male omnivores (70.9 ± 5.0 and 65.9 ± 7.0 kg, respectively) and had a lower body mass index [BMI (in kg/m2); 22.0 ± 1.3 and 20.5 ± 2.1, respectively], P < 0.01. There was no significant difference in body weight and BMI between female omnivores (weight: 60.1 ± 8.8 kg; BMI: 21.1 ± 2.7) and female vegans (weight: 65.6 ± 10.6 kg; BMI: 23.1 ± 4.0). The vegans had been consuming a vegan diet for a mean of 1.7 y (range: 0.5–3.5 y) and a vegetarian diet for 2.8 y (range: 0.7–4.0 y). All 30 vegans reported ethical reasons as their primary motivation for being vegan; 4 also mentioned health reasons.
Validity of the dietary assessment
There was no significant difference in the validity of reported energy, nitrogen, or potassium intakes between the dietary groups (Table 1). However, the validity of reported sodium intake was significantly lower for female vegans than for female omnivores (P < 0.05). The DH method underestimated energy intake by -1.93 MJ/d (95% CI: -2.89, -0.97 MJ/d) compared with the DLW method. Potassium intake was also underestimated by -419 mg/d (95% CI: -689, -149 mg/d) compared with the biological marker. However, the DH method showed good agreement for the biological marker of urinary nitrogen excretion, with a mean difference of 0.31 g/d (95% CI: -0.23, 0.85 g/d). The DH method also showed good agreement for sodium intake and urinary sodium excretion, with a mean difference of -198 mg/d (95% CI: -538, 141 mg/d).
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TABLE 1 . Validation of reported intakes of energy, nitrogen, sodium, and potassium in 30 vegans and 29 omnivores with the use of the doubly labeled water method and 24-h urine collections1
Dietary intake
Female vegans had significantly higher daily intakes of rice (55 ± 47 g), legumes (300 ± 213 g), vegetables (325 ± 284 g), whole-wheat bread (101 ± 59 g), and dietary supplements and lower intakes of cake and cookies (13 ± 16 g) and candy and chocolate (32 ± 51 g) than did female omnivores. Male vegans had significantly higher daily intakes of legumes (335 ± 185 g), vegetables (307 ± 127 g), nuts and seeds (8 ± 10 g), juice (272 ± 263 g), and dietary supplements and lower intakes of cereals (9 ± 16 g) and candy and chocolate (22 ± 13 g) than did male omnivores. No significant difference was observed between groups for daily consumption of fruit and berries (161 ± 146 g); white bread (71 ± 72 g); pizza, pie, and pastries (22 ± 32 g); chips and popcorn (16 ± 18 g); soft drinks (326 ± 321 g); and alcoholic beverages (111 ± 139 g).
Both vegans and omnivores obtained a large portion of energy from between-meal snacks: 33% and 40%, respectively. Female vegans obtained more energy from lunch (22%) and less from snacks (33%) than did female omnivores (18% and 40%), and male vegans obtained more energy from breakfast than did male omnivores (21% and 15%, respectively), P < 0.05. Vegans had lower dietary intakes (excluding supplements) of protein, saturated fat, cholesterol, disaccharides, riboflavin, niacin, vitamin B-12, vitamin D, calcium, phosphorus, zinc, and selenium than did omnivores (Tables 2 and 3). On the other hand, vegans obtained a higher percentage of total energy from carbohydrates than did omnivores and had higher intakes of polyunsaturated fat, monosaccharides, dietary fiber, folate, vitamin C, vitamin E, and magnesium. Furthermore, female vegans had lower intakes of total and monounsaturated fat and a higher intake of iron than did female omnivores. Male vegans had lower intakes of alcohol and sodium than did male omnivores.
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TABLE 2 . Dietary intake of macronutrients (excluding supplements) of 30 vegans and 30 omnivores1
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TABLE 3 . Dietary intake of vitamins and minerals (excluding supplements) of 30 vegans and 30 omnivores1
The dietary intake (excluding supplements) of the omnivores as a group was adequate for all nutrients, except selenium for females (Table 3). Vegans had dietary intakes (excluding supplements) that were lower than the average requirements of riboflavin (males only), vitamin B-12, vitamin D (females only), calcium, and selenium (Table 3). Intakes of calcium and selenium remained low for vegans even after inclusion of intake from dietary supplements. A significantly larger number of vegans than omnivores used dietary supplements (26, or 87%, compared with 13, or 43%), and there was no significant sex difference in either dietary group. Aside from multivitamin and mineral supplements, 11 vegans (37%) and no omnivores consumed vitamin B-12 supplements, and 6 vegans (20%) and no omnivores consumed calcium supplements. Excluding multimineral supplements, 3 (10%) of the omnivores and no vegans consumed iron supplements.
The individual intakes (including supplements) of 19 vegans (11 females) were below the lowest recommended intake level for one or several nutrients. Five vegans had a low intake of vitamin A, 5 of riboflavin, 11 of vitamin B-12, 7 of vitamin D, 1 of iron (<6.5 mg/d), 7 of calcium, 1 of zinc, and 17 of selenium. One female omnivore had a low intake of selenium.
Nutritional assessment
Six (20%) female vegans and 7 (23%) female omnivores were classified as having low iron status (Table 4). Three vegans had low vitamin B-12 concentrations in blood; as a group, vegans had lower vitamin B-12 and higher folate concentrations than did omnivores (P < 0.01). Both dietary groups had iron-status variables and vitamin B-12 and folate concentrations within the reference range, according to the Clinical Chemistry Department, University Hospital of Umeå, Umeå, Sweden.
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TABLE 4 . Iron-status, vitamin B-12, and folate assessment of female vegans and omnivores1
DISCUSSION
In accordance with other findings (19), male vegans weighed less and had a lower BMI than male omnivores; in contrast, no significant differences were seen between female vegans and omnivores in the present study.
Validity of the dietary assessment
Energy intake was underreported (compared with measured energy expenditure) by 14% of vegans and 12% of omnivores (Table 1; 13). Thus, subjects underreporting energy intake probably had a higher than reported intake of nutrients; the opposite would be true for subjects overreporting energy intake. A possible explanation for the lower reported-to-measured sodium ratio of female vegans is that the salt content of vegan food items and dishes in the food database is lower than is actually the case. Potassium intake was underreported by 4% among vegans and 10% among omnivores, but even without adjusting reported intake to account for underestimation, the potassium intake was above the lowest recommended intake level of the Nordic Nutrition Recommendations for all subjects.
Dietary intake and nutritional assessment
The higher intake of vegetables and legumes among vegans than among omnivores confirms the results of another study of lactoovovegetarian adolescents (20). However, the lactoovovegetarians in that study ate less legumes and nuts (78 ± 73 g/d) and vegetables (242 ± 147 g/d) and more sweets (149 ± 190 g/d) than did the vegans in the present study, suggesting a healthier diet among the Swedish vegans. A possible explanation for the lower intake of candy and chocolate and cake and cookies among female vegans than among female omnivores is that these food items often contain animal products and that the range of comparable vegan products is limited. In contrast with previous findings (21–24), the vegans and omnivores in our study consumed similar amounts of alcoholic beverages. One exception was that male vegans had a lower intake of alcohol (g/d) than did male omnivores. The observation that vegans and omnivores had similar intakes of fruit and berries; white bread; pizza, pie, and pastries; chips and popcorn; soft drinks; and alcoholic beverages may indicate that in this respect, young "ethical vegans" differ from the vegetarians who participated in previous studies, who probably were more health conscious (24). Also, the high SDs of the food intake values in the present study imply heterogeneous intakes, especially among female vegans, indicating that some young vegans have good food habits and others do not.
Energy intake from snacks was higher than recommended (25); these findings confirm those of a dietary survey of 731 adolescents living in Umeå, Sweden (26). The lower intake of protein among vegans than among omnivores was consistent with results from previous studies (27–30). A low protein intake was reported to decrease urinary excretion of calcium (31–33), but a recent study showed no association between intake of protein and calcium absorption (34). The finding of lower intakes of total and saturated fat and cholesterol among vegans than among omnivores was in agreement with findings from other studies (27–30). Together with higher intakes of polyunsaturated fat and dietary fiber among vegans, this has health benefits, at least as far as ischemic heart disease is concerned.
The higher prevalence of supplement use among vegans than among omnivores verifies previous results (24,35). To prevent intakes that are lower than the average requirements of riboflavin (for males), vitamin B-12, vitamin D (for females), calcium, and selenium, the vegans were dependent on supplements. A study of 76 vegetarians (44 males, aged 27 y) showed that 73% of the males had nonacceptable urinary riboflavin content, and the mean intake of 50 subjects was 56% of the recommended allowance (36). However, riboflavin need not be a problem in a well-planned vegan diet because there are several vegan dietary sources, such as cornflakes, corn, spinach, and lentil sprouts (37). The vegans in the present study had an intake of vitamin B-12 from diet that was lower than the average requirement, and long-term vegans are advised to include vitamin B-12–fortified foods or dietary supplements in their diets (38). The differences in concentrations of vitamin B-12 and folate between the vegans and omnivores confirm findings of other studies (39,40). One of the 3 vegans with low vitamin B-12 concentrations took B-12-supplements, indicating a failure in absorption rather than low intake. A possible explanation is a lack or insufficient amounts of intrinsic factor needed for absorption (38,41). Female vegans had dietary intakes of vitamin D that were lower than the average requirement, but the vitamin is also obtained via endogenous production when skin is exposed to ultraviolet light. If exposure to sunlight is inadequate, which may be the case in northern Sweden between November and February, fortified foods such as soy drinks and some cereals or supplements of vitamin D may be needed for vegans (37). Vegans had a lower intake of calcium than did omnivores, which confirms previous findings for female vegans (42) but is in contrast to those for male vegans (27). Vegans in the present study relied on dietary supplements and calcium-fortified fluids to make up 35% of their calcium intake; omnivores obtained 69% of their calcium from milk products. Vegans need to replace milk products with calcium-rich vegan foods such as semolina, tofu, and fortified soy drinks and consume sizable servings of leafy green vegetables such as kale and broccoli (37,43). The dietary intake of selenium in Sweden is estimated to be 10–70 µg/d because of low selenium content in the soil, and the lowest levels have been found in vegan diets comprising mostly locally grown products (44). Supplementation of animal foods with selenium has led to increased concentrations in meat, milk, and cheese (45,46), indicating underestimated values of selenium content in these and possibly other food items included in the database. By eating products grown outside Sweden, such as lentils, nuts, and cereals (47), grown on selenium-rich soil, vegans may increase selenium intake.
Female vegans had a higher iron intake (excluding supplements) than female omnivores, which does not support a previous finding (28). However, intake was similar when including supplements. Low iron status was as frequent among omnivores as among vegans, despite the vegans' intake of nonheme iron only, which has a lower absorption rate than does heme iron (48), and higher intakes of dietary fiber and possibly phytic acid, which decrease the bioavailability of iron (8,47). This result is in agreement with one previous study (28) but not with others (29,49). The prevalence of low iron status was similar to results of other Swedish studies on adolescents (50,51). Only females had low iron status because their intakes were lower and their iron requirements higher than those of males (8). Iron bioavailability may be increased by combining iron intake with intake of food items high in vitamin C and by decreasing intake of phytic acid, through, for instance, yeast fermentation of whole-wheat flours when baking bread, and by minimizing intake of the tannins found in tea and coffee (37).
For 11 of the 20 individuals with nutrient intakes lower than the average requirements, energy intake was validated with DLW. Five of these had a reported energy intake/measured energy expenditure value of <0.80, indicating underreporting as a likely explanation for the low intake. However, the low intake of iron of one female vegan could not be explained by underreporting because it was confirmed by a low iron status.
The vegan diet of adolescents was very heterogeneous and did not comply with the average requirements for riboflavin, vitamin B-12, vitamin D, calcium, and selenium when supplements were excluded from the calculations. Intakes of calcium and selenium remained lower than the average requirements even after inclusion of supplements. The prevalence of insufficient iron status was as high among omnivores (23% of females) as among vegans (20% of females), indicating a female rather than a vegan problem. It is important for adolescents in general and vegetarians in particular to receive knowledge, both theoretical and practical, about how to combine and prepare a healthy diet.
ACKNOWLEDGMENTS
We thank all the adolescents who participated and Linda Hagfors and Maria Hedström for valuable help with data entry.
REFERENCES