szmtag Vitamin and Mineral Status in a Vegan Diet (31.08.2020)
DÄ internationalArchive35-36/2020Vitamin and Mineral Status in a Vegan Diet

Original article

Vitamin and Mineral Status in a Vegan Diet

Dtsch Arztebl Int 2020; 117: 575-82. DOI: 10.3238/arztebl.2020.0575

Weikert, C; Trefflich, I; Menzel, J; Obeid, R; Longree, A; Dierkes, J; Meyer, K; Herter-Aeberli, I; Mai, K; Stangl, G I; Müller, S M; Schwerdtle, T; Lampen, A; Abraham, K

Background: In Germany, public interest in a vegan diet is steadily growing. There are, however, no current data on the macro- and micronutrient status of vegans.

Methods: In a cross-sectional study entitled “The Risks and Benefits of a Vegan Diet” (RBVD), we investigated the dietary intake, basic laboratory parameters, vitamin status, and trace-element status of 36 vegans and 36 persons on an omnivorous diet. Each group consisted of 18 men and 18 women aged 30–60.

Results: Nearly all the vegans and one-third of the persons on a mixed diet had consumed supplements in the previous 4 weeks. Vegans and non-vegans had similar energy intake but differed in the intake of both macronutrients (e.g., dietary fiber) and micronutrients (e.g., vitamins B12, B2, D, E, and K, as well as folate, iodine, and iron). There were no intergroup differences in the biomarkers of vitamin B12, vitamin D, or iron status. The ferritin values and blood counts indicated iron deficiency in four vegans and three non-vegans. Measurements in 24-hour urine samples revealed lower calcium excretion and markedly lower iodine excretion in vegans compared to non-vegans; in one-third of the vegans, iodine excretion was lower than the WHO threshold value (<20 µg/L) for severe iodine deficiency.

Conclusion: Vitamin B12 status was similarly good in vegans and non-vegans, even though the vegans consumed very little dietary B12. This may be due to the high rate of supplementation. The findings imply a need to also assure adequate iodine intake in the population, especially among persons on a vegan diet.

LNSLNS

In recent years, the interest in a vegan diet, avoiding all foods of animal origin, has been growing steadily in Germany. The results of market research surveys indicate that currently approximately 6 million German citizens follow a vegetarian diet (vegetarians) and almost 1 million a vegan diet (vegans) (1, 2). Data of the 7-day Adventist Health Study from the US describe positive effects of these types of diets against the development of obesity, hypertension (lacto-ovo vegetarians: relative risk [RR] 0.45; 95% confidence intervals: [0.44; 0.47]; vegans: RR 0.25 [0.22; 0.28]); diabetes (lacto-ovo vegetarians RR: 0.39 [0.36; 0.42]; vegans RR: 0.22 [0.18; 0.28]) (3) and cardiovascular mortality in males (lacto-ovo vegetarians RR 0.77 [0.59; 0.99]; vegans RR 0.58 [0.38; 0.89]) (4, 5). In addition, a recent review with meta-analysis has shown that a vegetarian diet is associated with a reduced risk of ischemic heart disease (RR: 0.75 [0.68; 0.82]) and cancer (RR: 0.92 [0.87; 0.98]), and a vegan diet with a decreased risk of cancer (RR: 0.85 [0.75; 0.95]) compared to an omnivorous diet, even after adjusting for key confounding factors, such as smoking and body mass index (6). Thus, a meat-free diet would be desirable from the perspective of the health of the entire population. Furthermore, reduced consumption of foods of animal origin could contribute to ensuring food security in the future (7) and combating climate change (8).

However, risks associated with a purely vegan diet are under discussion as well. In its vegan diet position paper, the German Nutrition Society (DGE, Deutsche Gesellschaft für Ernährung) describes the following substances as critical nutrients: vitamin B12, vitamin B2 (riboflavin) and vitamin D, protein (essential amino acids), long-chain n-3 fatty acids, as well as calcium and the trace elements iron, iodine, zinc, and selenium (9). By contrast, a vegan diet is expected to ensure a good supply of vitamin C, vitamin E, thiamine and folate, the minerals magnesium and potassium, as well as dietary fiber and secondary plant compounds (9, 10). The lower intake of saturated fatty acids and cholesterol is also regarded as beneficial (10). Up-to-date data on the intake of micronutrients and macronutrients among vegans in Germany are currently not available. Thus, the aim of this cross-sectional study of the German Federal Institute for Risk Assessment (BfR, Bundesinstitut für Risikobewertung) was to provide first insights into the current micronutrient status in a vegan diet compared to an omnivorous diet.

Methods

Study design

The 72 participants of the study “Risks and Benefits of a Vegan Diet“ (RBVD) were recruited in Berlin at the BfR in the period from January to July 2017 (Figure 1) (11). The sample size for this study is based on the power calculation for the primary research question (bone health in vegans compared to omnivores). The observed differences in bone health are part of a further planned publication. The study was approved by the Ethics Committee of Charité—Universitätsmedizin Berlin (no. EA4/121/16).

Flowchart of the study “Risks and Benefits of a Vegan Diet“ (RBVD); BMI, body mass index
Figure 1
Flowchart of the study “Risks and Benefits of a Vegan Diet“ (RBVD); BMI, body mass index

Dietary habits were recorded using three-day weighed food protocol. With the help of the German Nutrient Database (BLS, Bundeslebensmittelschlüssel) Version 3.02, the mean daily intake of macronutrients and micronutrients was calculated (12). Information about age, educational attainment, and lifestyle factors was collected using tablet-based questionnaires. Height and body weight, waist circumference, and blood pressure were measured using a standardized method (eMethods, eTable 1).

Overview of the methods used to determine the biochemical parameters
eTable 1
Overview of the methods used to determine the biochemical parameters

Determination of the micronutrient status using biomarkers

From all participants in the study, 60 mL of blood was obtained. On the same day, a differential blood count was performed and lipid, HbA1c, glucose, liver enzyme, creatinine, homocysteine, (highly sensitive) C-reactive protein, ferritin, and zinc levels were determined in a certified routine laboratory (Labor 28 GmbH, Berlin, Germany). In a 24-hour urine sample, urine creatine and calcium concentrations were determined. All other biochemical analyses were performed on samples stored at a temperature of −80 °C (eTable 1).

The vitamin B12 indicator (4cB12), calculated from the concentrations of holotranscobalamin, vitamin B12, homocysteine, and methylmalonic acid, was used to assess the vitamin B12 status (13).

Statistical analysis

The statistical software suite SAS Enterprise Guide Version 7.13 was used for the analysis of the data (eMethods).

Results

Characteristics of study participants

36 vegans and 36 omnivores aged between 30 and 57 years participated in the study. The vegan participants had followed their diet between 1.6 years and 20.2 years. General characteristics of the study participants and important lifestyle factors are summarized in Table 1. Almost all vegans and a third of the omnivores had taken dietary supplements within the preceding four weeks (Figure 2, eTables 2 and 3). A comparison of basic biochemical data revealed significantly lower concentrations of total cholesterol and LDL cholesterol among vegans compared to omnivores (Table 3).

Supplement use among the participants of the cross-sectional RBVD study within the preceding four weeks
Figure 2
Supplement use among the participants of the cross-sectional RBVD study within the preceding four weeks
Characteristics of the participants in the cross-sectional RBVD study by diet
Table 1
Characteristics of the participants in the cross-sectional RBVD study by diet
Status of biochemical basic data and selected vitamins and minerals of the participants in the cross-sectional RBVD study by diet
Table 3
Status of biochemical basic data and selected vitamins and minerals of the participants in the cross-sectional RBVD study by diet
Mean daily intake of vitamins and minerals through supplements in the RBVD study
eTable 2
Mean daily intake of vitamins and minerals through supplements in the RBVD study
Vitamin and mineral status depending on the intake of dietary supplements
eTable 3
Vitamin and mineral status depending on the intake of dietary supplements

Macro- and micronutrient intake

Despite the almost identical energy intake, differences between vegans and omnivores were observed with respect to both macronutrients and micronutrients. Of note is the considerably higher intake of dietary fiber, vitamin E, vitamin K, and folate as well as iron and the very low intake of vitamin B12, vitamin D, and iodine among vegans compared to omnivores (Table 2).

Daily energy intake as well as macronutrient and micronutrient intake of participants in the cross-sectional RBVD study by diet, based on three-day weighed food records without taking supplement use into account
Table 2
Daily energy intake as well as macronutrient and micronutrient intake of participants in the cross-sectional RBVD study by diet, based on three-day weighed food records without taking supplement use into account

Micronutrient status (blood and urine)

Among vegans, lower concentrations of vitamin B2, vitamin B3, vitamin E (alpha-tocopherol), vitamin A, selenoprotein P, and zinc in blood as well as a reduced excretion of iodine and calcium in 24-hour urine samples compared to omnivores was observed. By contrast, folate and vitamin K1 blood levels were higher among vegans. Yet, no differences between vegans and omnivores were found with respect to median vitamin B12, 25-hydroxy vitamin D and ferritin concentrations (Table 3). In four vegans and three omnivores, however, signs of latent to manifest iron deficiency (lower ferritin levels and blood count changes) were observed. With respect to the vitamin B12 status, the B12 indicator (4cB12) revealed a mild deficiency in two vegans and one omnivore, as well as increased levels in four vegans. The Spearman correlation coefficient for the association between the duration of vegan diet and 4cB12 was 0.30 (p = 0.07).

Riboflavin levels below the reference range were measured in 13 vegans (36%) and 5 omnivores (14%).

Parathyroid hormone (PTH) was measured as an important parameter of calcium, phosphate, and vitamin D metabolism. Ten vegans and three omnivores showed elevated PTH levels (>65 pg/mL). The comparison of calcium excretion found that the excretion in vegans with elevated PTH levels was lower compared to vegans without elevated PTH levels (p = 0.02). There was no correlation between duration of a vegan diet and calcium excretion (r = −0.02, p = 0.88 according to Spearman). With regard to 25-hydroxy vitamin D levels, plasma concentrations of <30 nmol/L (<12 ng/mL) were measured in 12 vegans and 8 omnivores, while plasma levels of <50 nmol/L (<20 ng/mL) were measured in 15 vegans and 19 omnivores. Supplement users showed higher 25-hydroxy vitamin D plasma concentrations (eTable 3).

Iodine excretion was lower in vegans compared to omnivores. Only 8% of vegans and 25% of omnivores achieved iodine excretion of ≥100 µg/L. 31% of the vegans excreted less than 20 µg/L. When viewed alone, the screening parameter thyroid-stimulating hormone (TSH) was found abnormal in two vegans and two omnivores with values of >4mU/L.

Discussion

The focus of our study was on vitamin B12, vitamin B2 and vitamin D as well as calcium and the trace elements iron, iodine, zinc, and selenium, since these have been critically discussed with respect to a vegan diet.

Studies on the nutritional status of vegans are very rare (14, 15, 16, 17, 18). In addition, most of these studies only collected data on the intake of macronutrients and micronutrients using dietary food records. Only two of these studies—Elorinne et al. from Finnland and Schüpbach et al. from Switzerland—also looked at specific blood parameters (16, 18) (eTable 4).

Overview of the most relevant studies on macronutrient and micronutrient intake and on the status of macronutrients and micronutrients in the blood of vegans and omnivores
eTable 4
Overview of the most relevant studies on macronutrient and micronutrient intake and on the status of macronutrients and micronutrients in the blood of vegans and omnivores
Potentially critical vitamins and minerals in a vegan diet and a selection of food items of plant origin, typically containing large amounts of these vitamins and minerals
eTable 5
Potentially critical vitamins and minerals in a vegan diet and a selection of food items of plant origin, typically containing large amounts of these vitamins and minerals

Most vegans are aware that a vegan diet is associated with the risk of vitamin B12 deficiency and vitamin B12 is by far their most frequently taken supplement. Based on the vitamin B12 indicator findings, our study did not observe an increased risk of vitamin B12 deficiency among the vegan participants. Most likely, this is due to the high rate of vitamin B12 supplementation among vegans (92%). However, the proportion of dietary supplement users in our study appears to be high compared to those in recent studies from Germany (19, 20) (74% and 81% supplementation rate, respectively) and Denmark (17) (2/3 supplementation rate); only the data of the Finnish cross-sectional study are comparable (supplementation rate of 91%) (16). On the other hand, increased B12 indicator values were found in four vegan participants. Against the backdrop of recent studies about the association between the intake of vitamin B12 supplements and an increased lung cancer risk (21, 22), the intake of vitamin B12 supplements, which was previously regarded as safe, may need to be re-evaluated.

Vitamin B2 is present in larger amounts in animal products; in addition, its absorption from foods of plant origin is lower. In line with our results, recently conducted cross-sectional studies (14, 16, 17) have shown that the absorbed amounts of vitamin B2 tend to be lower in vegans. In the Swiss study (18), vitamin B2 deficiency was diagnosed based on B2 blood levels in one quarter of vegans and 14% der omnivores. However, little is known as yet about the clinical relevance of B2 levels below the cut-off value; further studies are needed to shed light on this question.

Most of the required amount of vitamin D is produced by sun-exposure–dependent endogenous synthesis and only a minor proportion is contributed by nutrition. Since the intake of vitamin D is mainly from animal products, the lower vitamin D uptake among vegans is not surprising. With a vitamin D supplementation rate of 50% among vegans, the rate in our study is rather high compared to other studies (19, 20). Comparable data are only known from the Finnish study which found that serum levels of vitamin D in vegans were 34% lower compared to omnivores, even though in the Finnish study the vitamin D supplementation rate among vegans was with 68% even higher than in our study (16). Without supplementation, a significantly greater proportion of vegans had subnormal 25-hydroxy vitamin D levels compared to omnivores, highlighting the importance of supplementation, especially in a vegan diet.

For many years, calcium deficiency due to the lack of intake of dairy products was regarded as a key risk in vegans (23). Recent studies on calcium uptake have shown conflicting results, with significant differences between vegans and omnivores in some studies (14, 15, 18) and similar calcium intake amounts in others ([16] and in our study). The observation that calcium intake among vegans is higher in recent years compared to older studies is usually attributed to the intake of fortified foodstuffs. However, the evaluation of calcium intake is also more reliable when it includes the corresponding biomarkers. In this context, the lower calcium excretion and the increased PTH levels of nearly every third vegan participant in our study may be interpreted as evidence of a physiological response to low calcium intake.

Especially in the evaluation of iron intake, the importance of using biomarkers is obvious. The bioavailability of iron depends very much on the source of iron, but also on the simultaneous intake of certain secondary plant compounds or of vitamin C. Divalent heme iron from animal products is absorbed two to three times better than trivalent iron from plants. Vitamin C facilitates the absorption of iron, while the simultaneous intake of phytic acid (for example from pulses and grains) or of polyphenols (tea or coffee) reduce the absorption of iron. Iron deficiency is one of the risks associated with a vegan or plant-based diet which is commonly mentioned (9). Signs of iron deficiency were noted in 11% of the vegan participants, which is in line with the results of the two comparable cross-sectional studies from Finnland and Switzerland (16, 18). However, we also observed insufficient iron intake in 8% of the omnivores which is comparable to the findings in the Swiss study (18).

Corresponding to the lower intake of iodine according to the weighed food protocols, iodine excretion in urine was far below the WHO cut-off value for undersupply of iodine (100 µg/L) in three-quarters of the omnivores and almost all vegans (24). Only 5 vegans supplemented iodine (Figure 2, eTable 3). In line with the findings of low iodine intake (16, 17) and iodine undersupply (16, 18, 25) in other recent studies, the results of our study suggest that it is challenging to ensure adequate iodine intake in vegans as there seems to be a lack of awareness of this potential deficiency. Individual monitoring of iodine intake based on iodine excretion is usually not practicable. In line with the literature (26), our study also showed that TSH is not a very sensitive marker—in only four participants with significantly decreased iodine excretion, TSH levels were found increased. Since iodine deficiency is a major cause for the development of goiter, it would need to be considered whether regular clinical assessments of the thyroid should be performed by ultrasound scans (18, 25). Due to the limited availability of natural iodine sources for vegans, it may also be appropriate to recommend iodine supplementation.

In contrast to the study by Schüpbach et al. which found that almost half of the vegans were deficient in zinc (18), we observed lowered zinc concentrations (<60 µg/dL) only in two vegans in our study.

Since selenium has numerous effects on the immune system, thyroid function and the cardiovascular system, and probably also influences carcinogenesis (27, 28), adequate supply of selenium should be ensured. In our study, we used selenoprotein P to assess the selenium status, in addition to the total blood selenium concentrations. As a selenium transport protein, selenoprotein P appears to be well suited as a biomarker to assess the selenium status, especially in patients with low selenium intake (29). Vegans showed lower selenoprotein P levels compared to the omnivores in our study, but also compared to the selenoprotein P levels in the largest European study on nutrition and cancer (The European Prospective Investigation into Cancer and Nutrition, EPIC) in which a representative number of selenoprotein P measurements was performed (30). The results indicate a lower selenium intake in vegans compared to omnivores and are consistent with the results of the Finnish cross-sectional study (16). Most studies, however, used the plasma concentration of selenium, a parameter for which we found no difference in our study. Based on the current recommendations for selenium intake, considering 60–70 µg/d as adequate (31), a normal selenium intake is assumed with serum concentrations of >50 µg/L. Selenium supplementation carries the risk of overdosing. According to EFSA, an intake of 300 µg selenium per day is considered acceptable in adults (32).

While vitamin K intake was generally good in both groups, vegans were found to have higher concentrations of vitamin K1 compared to omnivores. Further studies are needed to better understand this finding. Here, the discussion focuses on the positive effect of higher vitamin K1 concentrations on bone health as well as a lower risk of type 2 diabetes and cardiovascular disease (33, 34, 35).

A special strength of our study is the excellent comparability between vegans and omnivores which was achieved by matching the subjects for age and sex, by the short recruitment period, and by the inclusion criterion of a BMI below 30 kg/m2. Furthermore, our study is notable for its elaborate dietary assessment, using three-day weighed food protocols, and for measuring a wide range of biomarkers. Limitations of our study include: With 72 participants, it is a rather small cross-sectional study with local data collection in the Berlin area. In addition, participants were mainly selected through postings on notice boards (convenience sample). Therefore, the possibility that these participants were particularly health-conscious cannot be excluded. However, since the same recruitment strategy was used for vegans and omnivores and a BMI ≥ 30 kg/m2 was chosen as an exclusion criterion, it can be assumed that the level of health consciousness was similar in both groups. Thus, no major differences between the two groups were present with regard to lifestyle characteristics. Consequently, the results of our study provide first insights into the current vitamin and mineral status in vegans versus omnivores in the German population.

Further studies, preferably with longitudinal design and a larger number of participants, are needed to, on the one hand, obtain up-to-date information about the nutritional and health status of a vegan population and, on the other hand, evaluate potential long-term health risks and protective effects.

Acknowledgement

We thank all participants for their participation in the study. We also thank Elektra Polychronidou for her great commitment in the recruitment of the participants and the conduct of the study. We thank Corinna Genrich and Christel Rozycki for their fast processing of the biospecimens. We extend our thanks to Dr. Mark Lohmann and his expert group for their support in developing the lifestyle questionnaire and Dr. Oliver Lindtner and his expert group for their support in collecting the nutritional data using weighed food protocols. Our special thanks goes to Clarissa Lage-Barbosa and Marjolein Haftenberger (Robert Koch Institute) for their support in analyzing the weighed food protocols.

Conflict of interest statement

The authors declare that no conflict of interest exists.

Manuscript received on 15 November 2019, revised version accepted on 11 May 2020

Translated from the original German by Ralf Thoene, MD.

Corresponding author
Prof. Dr. med. Cornelia Weikert, MPH
Bundesinstitut für Risikobewertung (BfR)
Abteilung Lebensmittelsicherheit
Max-Dohrn-Straße 8–10
10589 Berlin, Germany
cornelia.weikert@bfr.bund.de

Cite this as:
Weikert C, Trefflich I, Menzel J, Obeid R, Longree A, Dierkes J, Meyer K,
Herter-Aeberli I, Mai K, Stangl GI, Müller SM, Schwerdtle T, Lampen A, Abraham K: Vitamin and mineral status in a vegan diet. Dtsch Arztebl Int 2020; 117: 575–82. DOI: 10.3238/arztebl.2020.0575

Supplementary material

eMethods, eTables:
www.aerzteblatt-international.de/20m0575

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German Federal Institute for Risk Assessment, Department of Food Safety, Berlin, Germany:
Prof. Dr. med. Cornelia Weikert, Iris Trefflich, Dr. rer. medic. Juliane Menzel, Alessa Longree, Prof. Dr. vet. med. Dr. rer. nat. Alfonso Lampen, PD Dr. med. Klaus Abraham
Department of Clinical Chemistry and Laboratory Medicine, Saarland University Hospital, Homburg/Saar, Germany: Prof. Dr. rer. med. Rima Obeid
Department of Clinical Medicine, Center for Nutrition, University of Bergen, Bergen, Norway:
Prof. Dr. oec. troph. Jutta Dierkes
BEVITAL AS, Bergen, Norway: Dr. rer. nat. Klaus Meyer
Laboratory of Human Nutrition, Institute of Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland: Dr. rer. nat. Isabelle Herter-Aeberli
Medical Department of Endocrinology, Diabetes and Metabolic Medicine, Charité-Universitätsmedizin Berlin, Berlin, Germany: Prof. Dr. med. Knut Mai
Clinical Research Unit, Berlin Institute of Health (BIH), Berlin, Germany: Prof. Dr. med. Knut Mai
Charité-Center for Cardiovascular Research (CCR), Berlin, Germany: Prof. Dr. med. Knut Mai
DZHK (German Center for Cardiovascular Research), Berlin site, Berlin, Germany: Prof. Dr. med. Knut Mai
Institute of Agricultural and Nutritional Science, Martin Luther University Halle-Wittenberg, Halle, Germany: Prof. Dr. oec. troph. Gabriele I. Stangl
Department of Food Chemistry, Institute of Nutritional Science, University of Potsdam, Nuthetal, Germany: Dr. rer. nat. Sandra M. Müller, Prof. Dr. rer. nat. Tanja Schwerdtle
TraceAge DFG Research Unit on Interactions of Essential Trace Elements in Healthy and Diseased Elderly, Potsdam-Berlin-Jena, Germany: Prof. Dr. rer. nat. Tanja Schwerdtle
Flowchart of the study “Risks and Benefits of a Vegan Diet“ (RBVD); BMI, body mass index
Figure 1
Flowchart of the study “Risks and Benefits of a Vegan Diet“ (RBVD); BMI, body mass index
Supplement use among the participants of the cross-sectional RBVD study within the preceding four weeks
Figure 2
Supplement use among the participants of the cross-sectional RBVD study within the preceding four weeks
Key messages
Characteristics of the participants in the cross-sectional RBVD study by diet
Table 1
Characteristics of the participants in the cross-sectional RBVD study by diet
Daily energy intake as well as macronutrient and micronutrient intake of participants in the cross-sectional RBVD study by diet, based on three-day weighed food records without taking supplement use into account
Table 2
Daily energy intake as well as macronutrient and micronutrient intake of participants in the cross-sectional RBVD study by diet, based on three-day weighed food records without taking supplement use into account
Status of biochemical basic data and selected vitamins and minerals of the participants in the cross-sectional RBVD study by diet
Table 3
Status of biochemical basic data and selected vitamins and minerals of the participants in the cross-sectional RBVD study by diet
Overview of the methods used to determine the biochemical parameters
eTable 1
Overview of the methods used to determine the biochemical parameters
Mean daily intake of vitamins and minerals through supplements in the RBVD study
eTable 2
Mean daily intake of vitamins and minerals through supplements in the RBVD study
Vitamin and mineral status depending on the intake of dietary supplements
eTable 3
Vitamin and mineral status depending on the intake of dietary supplements
Overview of the most relevant studies on macronutrient and micronutrient intake and on the status of macronutrients and micronutrients in the blood of vegans and omnivores
eTable 4
Overview of the most relevant studies on macronutrient and micronutrient intake and on the status of macronutrients and micronutrients in the blood of vegans and omnivores
Potentially critical vitamins and minerals in a vegan diet and a selection of food items of plant origin, typically containing large amounts of these vitamins and minerals
eTable 5
Potentially critical vitamins and minerals in a vegan diet and a selection of food items of plant origin, typically containing large amounts of these vitamins and minerals
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