Why focus on micronutrients?

Deficiency in micronutrients is often termed as ‘hidden hunger’ as the effects may not be evident with clinical signs^{(Reference Stevens, Beal and Mbuya10)} (at least not in the early stages of deficiency). Globally it has been estimated that 56 % of children aged 6–59 months (equivalent to 372 million children) and 69 % of non-pregnant women of reproductive age (equivalent to 1·2 billion women) are deficient in at least one micronutrient (iron, zinc, and/or folate)^{(Reference Stevens, Beal and Mbuya10)}. This analysis was based on biomarkers of nutrient status using data from nationally-representative surveys^{(Reference Stevens, Beal and Mbuya10)} but as it did not include some micronutrients with a high prevalence of deficiency, such as iodine, these figures may be an underestimate. The fact that iodine was not included in the estimates may relate to the difficulties in assessing iodine status in an individual^{(Reference Zimmermann and Andersson11)}.

Animal foods are rich sources of many micronutrients – as an example, in the UK one portion of milk (200 g glass) would provide 43 % of iodine, 33 % of calcium, 40 % of riboflavin, and 107 % of vitamin B₁₂ recommendations for a female adult, while one chicken egg would provide 19 % of the iodine, 23 % of the selenium and vitamin B₂ recommendations, and 83 % of vitamin B₁₂ recommendations (Table 1)^(12,13) . Young women are a key population group when considering the potential impact of a transition to a plant-based diet (see later) and Table 1 shows that one portion each of milk, yoghurt and cheese (i.e. three portions of dairy products per day), would provide 161 % of vitamin B₁₂, 87 % of calcium, 86 % of iodine and 79 % of vitamin B₂ recommendations for a female adult⁽¹³⁾.

Table 1. Content of selected at-risk micronutrients in milk, dairy products and eggs and the proportion of the female adult Reference Nutrient Intake (RNI) provided by one portion

Nutrient composition data taken from UK Composition of Food⁽¹²⁾; median value calculated from food items within the food group.

At a population level, animal foods contribute the majority of the total intake of various micronutrients (n 11 shown in Table 2). Animal products contribute over half of total intake of calcium, iodine, selenium, zinc, and vitamin B₁₂ for at least one age group (Table 2), based on data from the UK National Diet and Nutrition Survey (NDNS)^(1,14) . Total animal products contribute approximately 80 % of vitamin B₁₂ intake and 60–70 % of iodine intake across all age groups (Table 2). Total animal product contribution to micronutrient intake may mask the picture, as some animal foods are particularly relevant for certain micronutrients. Figure 1 shows a breakdown of animal foods into (i) milk and dairy products, (ii) meat and meat products, (iii) fish and fish products, and (iv) eggs and egg dishes, as contributors to total intake of seven at-risk micronutrients in children and adults (19–64 years). Milk and dairy products contribute over 30 % of adult calcium, iodine, vitamin B₁₂ intake, and over 25 % of vitamin B₂. Meat is a major source (contributing over 25 %) of selenium, zinc, and vitamin B₁₂, while fish (with its lower popularity in the UK diet) provides a smaller proportion of micronutrient intake, but contributes at least 10 % of iodine, selenium and vitamin B₁₂ intake (Figure 1). Eggs and egg dishes also contribute a relatively small proportion of micronutrient intake, but contribute around 10 % of iodine and selenium intake (Figure 1).

Table 2. Contribution of animal products to total intake of micronutrients in UK children and adults

Data are from Years 9–11 (2016/17–2018/19) of the NDNS report⁽¹⁾, except for B_12, which is taken from the report from Years 1–4⁽¹⁴⁾.

Figure 1. Contribution of animal-foods to total intake of at-risk micronutrients in children and adults. Data are from Years 9–11 (2016/17–2018/19) of the National Diet and Nutrition Survey report⁽¹⁾, except for vitamin B₁₂, which is taken from the report from Years 1–4.⁽¹⁴⁾

The provision of a range of micronutrients from animal-source foods underlines the importance of considering the effect of a transition to a plant-based diet on these micronutrients; many of these are already nutrients of concern, particularly in young women (see later), as intake is low and therefore the risk of nutrient deficiency is of public-health importance. In addition, the use of substitute products (e.g. milk/meat alternatives) may be an important factor when considering the nutrients most at risk – for some nutrients, such as calcium, many alternative food products are fortified to match the nutrient content values in their animal-product equivalent, but for others, such as iodine, this is not the case^{(Reference Nicol, Thomas and Nugent15)} (discussed later).

Priority micronutrients for vulnerable populations: women of reproductive age

From a public-health perspective, when considering the effects of a transition to plant-based diets, the focus should be on micronutrients that are already of concern in terms of low intake and risk of deficiency. Dietary data in NDNS show that for girls 11–18 years and women 19–64 years, a considerable, and in some cases very high, proportion have intakes of key micronutrients below the LRNI (Table 3). For example, 16 % of 11–18-year-old girls and 9 % of adult women have intakes below the LRNI for calcium, and 28 % and 12 % of girls and adult women, respectively, have intakes below the LRNI for iodine^{( 1)} . Even considering potential inaccuracies associated with dietary assessment, it is likely that a considerable proportion of women of childbearing age have low intake of iron, iodine, calcium and vitamin B₂ (Table 3). This is supported by the NDNS data on biomarkers, which shows that for young women in particular, status is suboptimal. For example, for women aged 16–49 years, iodine status is below the threshold set for adequacy (urinary iodine concentration 98 µg/l⁽¹⁾, threshold > 100 µg/l), and for women 19–64 years old, 15 % and 55 % have biomarkers of iron (plasma ferritin) and vitamin B₂ (erythrocyte glutathione reductase activation coefficient, EGRAC) respectively that are outside of the reference ranges⁽²⁶⁾. Taken together, the low intake and status in young women are of concern and transition to a plant-based diet could further reduce the intake of key micronutrients that is already low in vulnerable groups. In addition, teenage girls and young women are groups that are more likely to use plant-based alternative products (which may not be fortified), and to follow a vegan/plant-based diet^{(Reference Alae-Carew, Green and Stewart28)}. Research using NDNS data from 2008–2019 has shown that females are significantly more likely to be consumers of plant-based alternatives than males (OR 1·46 95 % CI 1·27, 1·67)^{(Reference Alae-Carew, Green and Stewart28)}. The data also show that 25–39-year-olds are more likely to have used plant-based alternatives than those 11–23 years or 75+ years^{(Reference Alae-Carew, Green and Stewart28)}.

Table 3. Proportion with intake below lower reference nutrient intake (LRNI) for micronutrients at risk in young women of childbearing age

Data are from Years 9–11 (2016/17–2018/19) of the NDNS report⁽¹⁾, except for B_12, which is taken from the report from Years 1–4⁽¹⁴⁾.

NR: not reported for this age group in the NDNS Years 9–11 tables.

Concern around micronutrient deficiency in populations tends to focus on women and children. This is because they are vulnerable to the effects of deficiency as many micronutrients (e.g. vitamin B₂, calcium, iron and iodine) are vital for processes including growth and development, and are particularly important for foetal development during the first 1000 d of life^{(Reference McCarthy, Murray and Kiely29,Reference Velasco, Bath and Rayman30)} and prior to pregnancy for the optimisation of stores. Therefore, a reduced intake of these micronutrients when women of childbearing age follow a plant-based diet may have public-health implications. For example, vitamins B₂ and B₁₂ are vital during pregnancy and deficiency of these vitamins has been linked to negative child outcomes^{(Reference Pentieva, Caffrey and Duffy31)}. Adequate iodine is essential during pregnancy to produce the thyroid hormones that are required for brain and neurological development, and deficiency can alter brain structure^{(Reference Jansen, Korevaar and Mulder32)}. It has been shown that even mild-to-moderate iodine deficiency in early pregnancy is associated with lower child IQ and reading scores at age 8–9 years^{(Reference Bath, Steer and Golding33,Reference Levie, Korevaar and Bath34)} . Therefore, iodine deficiency during pregnancy is a considerable public-health issue and it is estimated that up to 50 % of UK pregnant women are iodine deficient^{(Reference Bath and Rayman35)}.

While deficiencies of some micronutrients, such as iron and vitamin B₁₂, are widely recognised as an issue for those consuming a vegan or predominantly plant-based diet, other micronutrients are often overlooked. Two such overlooked nutrients are iodine and vitamin B₂, perhaps because there are (incorrect) assumptions that intake is generally adequate within populations, and that deficiency is not a problem in high-income countries such as the UK^{(Reference Duffy, McNulty and Ward36,Reference Bath and Rayman37)} . That may be one of the reasons for the lack of fortification with these nutrients in plant-based alternative products, especially considering that milk and dairy products are the main source of both iodine and vitamin B₂ in the UK diet⁽¹⁾.

Plant sources of micronutrients

For some micronutrients, such as iron, zinc and calcium, certain plant foods may be considered as a suitable food source, but for others, such as vitamin B₁₂ and iodine, this is not the case. In the case of vitamin B₁₂, there are no reliable plant sources and the only reasonable source on a vegan diet would therefore be fortified foods or nutritional supplements^{(Reference Niklewicz, Hannibal and Warren20,Reference Niklewicz, Smith and Smith38)} . Seaweed is a rich plant-based source of iodine, but it is not a reliable source because it has a highly variable iodine concentration, even within the same seaweed species^{(Reference Teas, Pino and Critchley39)}, and therefore the content consumed by the consumer would be unknown^{(Reference Aakre, Solli and Markhus40)}. Some species of seaweed, including the brown seaweed kelp, can have a very high iodine concentration and should not be taken as a source of iodine, particularly during pregnancy, owing to the risk of iodine excess^{(Reference Farebrother, Zimmermann and Andersson41,Reference Zimmermann and Delange42)} . Iodised salt is a common source of iodine in many countries, and one that would be acceptable on a plant-based diet (within the restrictions of salt intake for cardiovascular health^(43,44) ). However, iodised retail salt is not widely available in all countries in Europe, including in the UK^{(Reference Bath, Button and Rayman45)}, Ireland^{(Reference Shaw, Nugent and McNulty46)} and Norway^{(Reference Carlsen, Andersen and Dahl47)}; as such, shifts to a plant-based diet in these countries may have a considerable impact on iodine intake, where there is no food fortification policy and diets are more reliant on animal-source foods. Plant-based foods contain variable amounts of selenium, and that is largely dependent on the soil concentration and conditions^{(Reference Rayman48)}. Brazil nuts are often cited as a good plant-based source but the selenium content is highly variable and can lead to excess selenium intake if consumed frequently^{(Reference Rayman48)}; furthermore Brazil nuts contain small, and variable, amounts of radioactive radium^{(Reference Koeder and Keller49)} and they also contain barium^{(Reference Lemire, Fillion and Barbosa50,Reference Duarte, Reis and Rogero51)} , therefore it has been suggested that they should not be eaten daily (i.e. as if they were a supplement) in order to provide selenium.

Even for those micronutrients where there are plant-based sources (such as iron and calcium), there should be consideration of the bioavailability, and the presence of inhibitors or enhancers in the context of a plant-based diet. For example, non-haem iron is found in plant-based foods and has variable absorption as it is dependent on individual body stores, and the balance of enhancers (e.g. muscle tissues and ascorbic acid) and inhibitors (e.g. phytates, polyphenols, calcium) in the diet^{(Reference Brittenham and Fairweather-Tait52,Reference Hurrell and Egli53)} . Iodine uptake into the thyroid gland can be competitively inhibited by dietary goitrogens, which are found in plant foods, including cruciferous vegetables such as, kale, broccoli and cabbage^{(Reference Di Dalmazi and Giuliani54)}. Generally, goitrogens are not of concern unless intake of these foods is extreme, or if iodine intake is very low^{(Reference Zimmermann55)}, however, there is a lack of data and research as to whether goitrogens could be a concern when consuming a vegan, or predominantly planted based, diet where the ratio of goitrogens to iodine could be high.

Plant-based alternative products as a source of micronutrients

Long before the trend for using alternatives to cows’ milk, there has been a decline in milk consumption in the UK. The National Food Survey (1942–2000) and later the Family Food Survey shows a 41 % reduction in milk intake between the 1970s and 2010s; milk consumption in 1974 was 2978 ml/person/week (or around 425 ml/person/day), compared to 1745 ml/person/week in 2019 (249 ml/person/day)⁽⁵⁶⁾. Since the early 2000s, there has been an increase in the use of plant-based milk alternatives (e.g. soy, oat and coconut drinks). In the UK, 6·7 % were consumers of plant-based alternatives in 2008–2011, which had increased to 13·2 % by 2018–2019^{(Reference Alae-Carew, Green and Stewart28)}. To achieve the necessary reductions in animal-source foods to meet dietary recommendations, such as EAT-Lancet or Net Zero goals, consumers may use plant-based alternatives that can easily be substituted in the diet. Indeed, the UK Eatwell Guide includes dairy alternatives in the section on dairy products⁽⁵⁷⁾, but the micronutrient profile of these alternative products may not be the same as cows’ milk^{(Reference Nicol, Thomas and Nugent15)}. For example, many plant-based milk alternatives are currently fortified to match the micronutrient profile of cows’ milk for some nutrients (such as calcium), but they are not always fortified with iodine or vitamins B₁₂ or B₂ ^{(Reference Nicol, Thomas and Nugent15)}. In a 2020 UK market survey, 63 % of milk alternatives were fortified calcium, compared with just 20 % fortified with iodine, and 29 % with vitamin B₂ ^{(Reference Nicol, Thomas and Nugent15)}. Furthermore, when plant-based drinks were fortified, the median value of iodine and vitamin B₁₂ was lower than that of cows’ milk (at 75 % and 48 % respectively), whereas the calcium and vitamin B₂ content was similar^{(Reference Nicol, Thomas and Nugent15)}. On the other hand, many milk alternatives are fortified with vitamin D, meaning that their concentration is greater than that of UK cows’ milk^{(Reference Nicol, Thomas and Nugent15)}. Data from other countries shows a similar picture of a lack of micronutrient fortification, particularly iodine in plant-based alternative products^{(Reference Craig and Fresán58–Reference Khalil and Herter-Aeberli64)}. The plant-based alternative market is constantly changing and expanding, and therefore risk of deficiency of certain nutrients may change as brands fortify their products.

Besides milk alternatives, there are an increasing number of products that are sold as alternatives to other dairy products (e.g. yoghurt and cheese), or to meat or fish, though these products are less likely to be fortified than milk alternatives^{(Reference Nicol, Thomas and Nugent15)}. For example, in 2020, just 6 % of the yoghurt alternatives were iodine fortified (v. 72 % with calcium), and none of the cheese alternatives were fortified with iodine (compared to 55 % fortified with calcium)^{(Reference Nicol, Thomas and Nugent15)}. In the 2020 survey, none of the fish alternatives were fortified with iodine, vitamin D or vitamin B₁₂. Some fish alternatives include kelp as an ingredient, which may provide some iodine, though there are no data on the concentration of iodine in these products, nor the bioavailability of iodine.

Milk and dairy products contribute 51 % and 33 % of the total iodine intake of UK children (4–10 years) and adults, respectively (Table 2). UK milk has a relatively high iodine concentration (approximate content of 413 µg/kg) compared to the value from milk in other countries^{(Reference Tattersall, Peiris and Arai65)}. By contrast, milk-alternative drinks that are not fortified with iodine have a low iodine concentration – approximately 2 % of that of cows’ milk (at 7·3 µg/kg)^{(Reference Bath, Hill and Infante66)}. As the market data shows that most milk-alternative drinks are not fortified with iodine, the rise in popularity of these products may place consumers at risk of iodine deficiency. Indeed, data from the National Diet and Nutrition Survey (Years 7–9; 2014–2017) shows that consumers of milk-alternatives were classified as iodine deficient and had a lower iodine intake than consumers of cows’ milk^{(Reference Dineva, Rayman and Bath67)}. As these results were based on data from before 2017, the majority of the milk-alternatives on the market would not have been fortified with iodine and therefore highlights the risk associated with unfortified alternatives. If the consumer replaced three portions of cows’ milk products per day with milk/dairy alternatives, iodine intake would reduce from 124 µg/d to 84 µg/d if two of the three portions were iodine-fortified, or just 2·6 µg/d if all products were unfortified^{(Reference Nicol, Thomas and Nugent15)}; overall complete substitution of cows’ milk products with unfortified alternatives would reduce iodine intake by 97·8 %^{(Reference Nicol, Thomas and Nugent15)}.

At the population level, using data from the NDNS, the effect of substituting cows’ milk with plant-based milk alternatives has been modelled, with varying degrees of iodine fortification of milk alternatives (from none, to 45 µg/100 ml)^{(Reference Nicol, Nugent and Woodside68)}. The modelling showed that complete replacement with an unfortified plant-based milk alternative would increase the risk of iodine insufficiency (proportion with intake < LRNI) across both children and females aged 11–18 (from 20 % to 48 %) and 19–49 years (from 13 % to 33 %). By contrast, substitution with a plant-based milk alternative fortified to either 22·5 µg/100 g or 27·4 µg/100 g (the value that corresponds to the average fortification on the UK market^{(Reference Nicol, Thomas and Nugent15)}) had minimal impact on iodine intake in all population groups, but fortification at 45 µg/100 g resulted in an increase in the proportion above the tolerable upper limit in children. Importantly, the impact on risk of iodine insufficiency was even greater when considering the current market situation – i.e. based on the probability of consumers being able to select an iodine-fortified drink. The modelling study therefore emphasises the need for a greater proportion of the market to be fortified with iodine, so as not to negatively affect population iodine intake as these products become more popular. From this modelling exercise, fortification of milk alternatives should be fortified with ≥ 22·5 and < 45 μg iodine/100 ml to avoid a negative impact on iodine intake in the population if there was a transition to plant-based alternatives^{(Reference Dineva, Rayman and Bath67 , Reference Nicol, Nugent and Woodside68)}.

Potential solutions to providing adequate micronutrients on a plant-based diet