4.1. Main Findings and Their Significance
This systematic review provides a comprehensive overview on nutrient intake and status of adults following a predominantly plant-based diet as compared to those following a dietary pattern containing meat. The outcomes are summarized in
Table 2.
For energy and macronutrients, we found that energy intake was similar across dietary patterns. Compared to meat-eaters, average protein, EPA and DHA intake was lower in vegetarians and particularly vegans, yet intake of fiber, PUFA, total n-3 fatty acids and ALA was higher in plant-based dietary patterns. Except for EPA and DHA, mean intake of energy and macronutrients of plant-based diets was within the recommendations. In meat-eaters, mean intake of fiber, PUFA and ALA were below recommendations
For micronutrients, vegetarians and vegans generally had lower vitamin B12, vitamin D and iodine intake and status and higher rates of bone turnover markers compared to meat-eaters. Mean iron and zinc intakes were inadequate in vegetarians and vegans due to higher requirements because of lower bioavailability of these micronutrients in plant-based diets. On the other hand, compared to meat-eaters, folate, vitamin E and magnesium intakes were higher in vegetarians and vegans, and vitamin B1, B6 and C intakes were especially higher in vegans. In meat-eaters, mean intake of vitamin E and D was inadequate. Mean calcium intakes were slightly above the EAR for all dietary patterns. Furthermore, mean intakes of vitamin A, B2, niacin and phosphorus were adequate and similar among all dietary patterns.
Our findings imply that plant-based dietary patterns can increase the risk of inadequate intake and status of certain nutrients, which are mainly present or more bioavailable in animal foods (EPA/DHA, vitamin B12, D, iodine, iron, zinc, calcium), but can improve the intake of other nutrients, which are abundant in plant foods. Conversely, meat-eaters are more at risk of inadequate intake of nutrients that are more present in plant foods (fiber, PUFA, ALA, vitamin E, folate, magnesium). However, the inadequate fiber, vitamin E and magnesium intake in more than 25% of the studies in vegetarians indicates that intake of plant-foods may be suboptimal in some populations. Public health strategies are needed to provide guidance and facilitate behavior change to help populations transition to a nutritionally balanced plant-based diet.
4.2. Strenghts and Limitations of This Review
The current review is the first systematic review aiming to quantify the differences in nutrient intake and status among different dietary patterns in adults, including meat-eaters, vegetarians, and vegans. A strength of this literature review was that we applied common definitions for the different dietary patterns across all studies to ensure a consistent interpretation of the data. Likewise, for comparability and consistency, we only included studies that used biomarkers and cut-off levels as applied by the IOM and WHO to assess nutritional status and deficiencies. The restriction of the studies to the years 2000–2020 increases the possibility of data being reflective of the current situation, thereby increasing the validity of this study. The findings of our review may help public health authorities and policy makers to develop practical guidance to consumers to help them transitioning to more healthy and sustainable diets, which should consist of a variety of nutrient-dense plant foods.
A major limitation of our review was that we could not provide reliable estimations on the adequacy of dietary nutrient intakes. The prevalence of inadequacy depends on the shape and variation of the usual intake distribution. Therefore, to evaluate the adequacy of dietary intake in a population, ideally the proportion of the population with usual intakes below the EAR should be determined [
59]. However, most studies did not provide this information. Instead, we compared mean or median intakes with the EAR (or the lower bound of the AMDR) to indicate (in)adequacy of nutrient intakes in the population. It can be assumed that if mean intake is at or below this level, a substantial proportion of the population will have intakes less than the requirement and is therefore at risk of deficiency. For ALA and fiber, for which only an Adequate Intake (AI) level is available (i.e., based on nutrient intake of a group of healthy people, who are assumed to be adequate), it is not possible to make any assumptions about the prevalence of inadequacy if mean intakes are below the AI, because actual requirements for these nutrients are unknown. Only, when mean intake is above the AI, prevalence of inadequate intakes can be assumed to be low [
59].
Another limitation of this review is that the vast majority of studies was conducted in developed, Western countries, mostly in Europe or North America. An exception was the evaluation of vitamin B12, for which a larger part of studies was conducted in Asia. Therefore, our results are mostly applicable to Western populations. The lack of studies from low- and middle-income countries (in particular from Africa) may be explained by the exclusion of studies that assessed habitual, monotonous plant-based diets from populations living in poverty and food insecure situations. These diets are largely consisting of staple foods and lack nutrient-rich plant foods, while food intake is generally limited and therefore the risk of nutrient inadequacies is high for all nutrients [
2].
Lastly, we did not detect major differences between studies that assessed intake from foods only or from foods and supplements (except for vitamin B12 and D). This may be explained by heterogeneity in the proportion of supplement users across studies, as well as dose and type of vitamin and minerals used. Moreover, from the included studies it was not clear whether intake from fortified foods was considered, which may have led to an underestimation of micronutrient intakes.
4.3. Findings on Energy and Macronutrients
Whereas some studies have suggested that energy intake in people consuming plant-based diets is lower compared to that of meat-eaters [
32,
33,
43], our review showed that mean energy intake was similar and adequate among different dietary patterns.
Despite a somewhat lower average protein intake in the plant-based dietary patterns, all studies reported protein intakes within the level of the adequate macronutrient distribution range. Because the overall protein quality of a vegan or vegetarian diet is estimated to be about 80% and 90% compared to the diet of meat-eaters (i.e., mainly due to the lower digestibility of plant proteins) [
60,
61], it has been suggested that dietary protein requirements of vegetarians and vegans should be increased by about 20% [
61,
62]. The mean protein intakes found in our review would still exceed such a potentially increased requirement (i.e., 12% E instead of 10% E). However, WHO and IOM do not specify increased protein requirements for vegetarians and vegans because diverse plant-based diets consisting of different plant proteins with complementary amino acid profiles can provide all essential amino acids and the lower digestibility of plant proteins can be improved through processing and preparation methods [
60,
63]. Nevertheless, for older adults it can be difficult to obtain sufficient protein from plant-based diets, due to increased protein needs and reduced overall food intake [
64,
65].
The higher intakes of fiber, PUFA, total n-3 fatty acids (mainly ALA) in plant-based dietary patterns (with the highest intakes in vegan diets) can be explained by the higher intake of plant foods in general, which are rich in these nutrients. While PUFA, n-3 fatty acid and ALA intakes were above the lower AMDR, in about one-third of the studies in vegetarians, fiber intake was below the recommendations, suggesting that not all vegetarians consume sufficient plant foods. However, EPA and DHA intake of vegetarians and vegans was far below the lower AMDR (i.e., 250 mg/d EPA and DHA) because of the absence of fish and seafood from the diet. While eggs can supply some EPA and DHA [
66], algae are the only direct plant source of long-chain n-3 fatty acids, but are usually only consumed in small amounts [
67,
68]. Furthermore, EPA and DHA can also be synthesized in the body from ALA, however, the capacity for conversion remains generally limited (i.e., <10%) [
66]. The latter is confirmed by consistent observations of lower EPA and DHA status in vegans and vegetarians compared to meat-eaters and may suggest the need for supplements or fortified foods. Conversely to vegetarians and vegans, meat-eaters’ EPA and DHA intake was in line with the AMDR, but their average fiber, PUFA and ALA intakes failed to meet the lower AMDR or AI. Therefore, meat-eaters would benefit from higher intakes of plant foods such as whole grain products, pulses, nuts, seeds, and some plant oils.
4.4. Findings on Micronutrients
Our review showed that intake and/or status of vitamin B12, D, calcium, iron, and zinc may not be sufficient in plant-based diets as these are low, lacking or have a low bioavailability in plant foods.
Most studies in vegans and half of the studies in vegetarians indicated that vitamin B12 intake was inadequate, which was confirmed by a high mean prevalence of vitamin B12 deficiency among vegans (44%) and vegetarians (32%). Our findings are in line with those of earlier reviews [
10,
12,
69]. Vitamin B12 is only present in animal foods, while fermented soy products (e.g., miso, tempeh), shiitake mushrooms, algae and unfortified nutritional yeast contain analogues of vitamin B12, which have been reported to be inactive and may even block the absorption of true vitamin B12 when intake is low [
70]. For an adequate vitamin B12 supply, vegans rely on regular use of fortified foods or supplements. Vegetarians can obtain vitamin B12 from dairy and eggs but may also benefit from fortified foods or supplemental vitamin B12 when intake of animal-based foods is limited.
Vitamin D is naturally present only in a few foods, particularly fatty fish, eggs, meat, mushrooms treated with UV-light and algae [
71], which explains why highest vitamin D intakes were seen in pesco-vegetarians with regular fish consumption. However, mean vitamin D intakes (also when intake from supplements was considered) were far below the EAR in all dietary patterns and therefore vitamin D fortified foods or supplements are generally recommended [
72]. While vitamin D can also be synthesized in the skin upon exposure to sunlight, this may be insufficient during winter in areas of higher latitude (around > 40 °N, e.g., Madrid, Beijing) and for people with dark skin or limited sun exposure [
72], as illustrated by the high prevalence of vitamin D deficiency in a small study among Finnish vegans and vegetarians (67% and 33%) [
46].
Calcium intake was lower in vegans compared to vegetarians and meat-eaters. However, for all dietary patterns, one third or more of studies reported intakes below the EAR, suggesting that inadequate intakes may occur in the general population. While dairy foods are important sources of calcium, green leafy vegetables, beans, pulses, seeds, nuts and grains are plant foods that are high in calcium, too [
70]. It is important to note that calcium absorption may be reduced by phytates and oxalates from plant foods, as well as by insufficient dietary protein intake and low vitamin D status [
70]. When habitual calcium intakes are low, calcium absorption is upregulated [
70] and PTH production is increased, which stimulates tubular calcium reabsorption and bone resorption [
73]. Our review found significantly higher levels of PTH and bone turnover markers in vegans and vegetarians and lower BMD of the lumbar spine in vegans, suggesting greater bone resorption as compared to meat-eaters. Our findings are in line with two recent systematic reviews and meta-analysis, which found that vegetarians and vegans had lower lumbar spine, femoral neck, and whole-body BMDs than omnivores [
74,
75]. Bone formation and resorption is not only influenced by calcium intake, but also other nutrients such as vitamin D, magnesium, and protein. Therefore, biomarkers on bone health are no direct measure for calcium status, but they can be used to evaluate the overall effect of nutritional intake of different dietary patterns on bone metabolism [
73].
Despite similar or higher intakes of iron in vegetarians and vegans as compared to meat-eaters, vegetarians and vegans, particularly women, had lower iron status than meat-eaters, and higher prevalence of iron deficiency and anemia. These findings have been confirmed in previous reviews [
9,
76] and can be explained by the fact that iron bioavailability in a plant-based diet is substantially lower (i.e., ~10%) compared to a diet with meat and fish containing heme iron (18%) [
19]. Heme iron is more efficiently absorbed (15–40%) than non-heme iron (1–15%) [
19] which is inhibited by phytates, polyphenols and proteins from milk and eggs [
77]. Because of the lower bioavailability of iron from plant-based diets, IOM estimates that dietary requirement of iron is 1.8 times higher for vegetarians and vegans [
19]. Notably, vegetarians had a lower mean iron intake than vegans. A possible explanation could be that dairy, unlike protein-rich plant foods, does not contain iron. Therefore, vegetarians who use dairy foods as their major protein source, should be educated to include other iron rich foods in their diet [
71]. In addition, absorption of iron from plant-foods can be improved by consumption of vitamin C rich fruits and vegetables [
77].
Like iron, zinc absorption from plant-based diets can be reduced due to the higher amount of phytate and fiber. Therefore, dietary requirements for vegetarians and vegans can be increased by up to 50% in high phytate diets as suggested by IOM [
14,
19]. While mean zinc intakes were similar across dietary patterns, vegans and vegetarians failed to meet the bioavailability-adjusted EAR which was confirmed by lower zinc status and higher prevalence of deficiency, particularly in vegans. Our findings are in line with those of earlier reviews and meta-analysis showing a lower zinc intake and status in vegetarians and vegans, particularly in women, compared to meat-eaters [
14,
78]. However, there are no reported adverse health consequences in adult vegetarians with lower zinc status, suggesting that the efficiency of zinc utilization may be increased in vegetarians on the longer term [
14].
The few studies reporting on iodine indicated a lower intake and status in plant-based diets compared to meat-eaters. Iodine content of animal-based foods is usually higher than in plant-based foods, with fish and dairy as richest sources of iodine [
79]. Marine algae are a very concentrated source of iodine, but their iodine content can vary a lot and consumption can lead to excessive intake [
80,
81]. Because of the limited number of foods with iodine, consumption of iodized table salt and foods produced with iodized salt (e.g., bread, bouillon cubes and seasonings) is recommended by WHO regardless of dietary pattern [
82].
We also found that plant-based as compared to meat-containing dietary patterns provided a better supply of some micronutrients, including folate, vitamin E and magnesium, with highest intakes in vegans. Mean intake of folate and magnesium was adequate in vegans and vegetarians, while in 38–57% of the studies meat-eaters failed to meet the requirements. For vitamin E, vegans had an adequate intake, but 43% and 64% of the studies showed inadequate intakes in vegetarians and meta-eaters, respectively. Vitamin E intake in the diet often corresponds with PUFA intake. However, due to higher PUFA intakes, more vitamin E is needed to protect PUFA in cell membranes and plasma lipoproteins from oxidation by free radicals [
83]. This may explain why a higher vitamin E intake in vegans was not reflected in a higher vitamin E status.
The intake of vitamin B1,B6 and C was higher in vegans, yet intakes were generally above the EAR across all dietary patterns. Good sources of vitamin B1 and B6 are wholegrains, pulses, nuts and seeds but also meat and fish [
19,
83], while fruits and vegetables are the major sources of vitamin C.
For vitamin A, B2, niacin and phosphorus, mean intakes were well above the EAR and similar across dietary patterns. For vitamin A, intakes may have been overestimated for plant-based diets as factors to convert carotenoids to retinol were not described in all studies. A study from the UK that estimated inadequate intakes of total vitamin A based on different conversion factors, showed that the prevalence of inadequate vitamin A intake increased from 3–8% when using 1:6 factor for beta-carotene conversion (RE) to 9–22% in vegetarians and 20–37% in vegans when using 1:12 factor for beta-carotene conversion (RAE) [
84]. While the limited data in our review did not show any presence of vitamin A deficiency in vegetarians and vegans, more research with recent validated biomarkers of vitamin A status may help to conclude which conversion factor will be relevant.
4.5. Implications for Public Health and Recommendations
A shift to a diet with more plant foods and less animal foods can improve the intake of fiber, PUFA, folate, vitamin B1, B6, C, E, and magnesium and subsequently benefit health outcomes. In particular, intake of fiber, PUFA, folate and vitamin E was found to be inadequate in meat-eaters compared to vegetarians and vegans in the current review.
On the other hand, careful planning is needed to consume a nutritious plant-based diet as there is a risk of inadequate intakes of EPA, DHA, vitamin B12, D, calcium, iron, zinc, and iodine (of which vitamin D and calcium are also of concern in meat-eaters). In addition, in the case of vegetarian diets, intakes of fiber and vitamin E may be insufficient when foods rich in these nutrients are not consumed in adequate amounts.
Therefore, in the transition to more healthy plant-based diets, health authorities will need to educate consumers to adopt a diverse diet with foods rich in these nutrients and facilitate behavior change. In addition, for vitamin B12, which is absent in plant foods, and for vitamin D and iodine, which can naturally only be found in a limited number of foods, additional public health strategies are needed, including food fortification and universal salt iodization. For iron, zinc and possibly calcium and provitamin A carotenoids, guidance should include advice to improve the bioavailability and bioconversion of these nutrients to avoid deficiencies (e.g., to consume vitamin C rich foods with meals to improve iron absorption). Industry can play a role in designing nutritious products and recipes that can help to increase the nutrient intake and bioavailability of these nutrients. Supplementation can be an alternative strategy, and our review showed that mean vitamin B12 intake and status was higher and adequate in studies that considered supplement use. However, for vitamin D, intakes in most studies remained inadequate, even when intake from supplements was considered. Additionally, mean intakes of other micronutrients did hardly differ between studies that assessed intake from foods only or from foods and supplements. This may be explained by heterogeneity in use, dose, and type of micronutrients among studies. Therefore, supplement use may not always be the preferred strategy to improve micronutrient intake as they are possibly used by a select group of people, who are health conscious and can afford them.