Seaweed (edible algae) is not a staple food in the Western diet, despite occasional use as a traditional ingredient in coastal areas. High nutritional value, combined with the expansion of the health-food industry, has led to a resurgence of seaweed in the British diet. While seaweed could be useful in tackling dietary iodine insufficiency, consumption of some species and sources of seaweed has also been associated with risks, such as toxicity from high iodine levels, or accumulation of arsenic, heavy metals and contaminants. The current retail level of seaweed and edible algae in the UK market, either as whole foods or ingredients, was evaluated with particular focus on labelling and iodine content. Seaweed-containing products (n = 224) were identified. Only 22 products (10%) stated information regarding iodine content and another 40 (18%) provided information sufficient to estimate the iodine content. For these products, the median iodine content was 110 μg/g (IQR 21–503) and 585 μg per estimated serving (IQR 105–2520). While calculations for iodine exposure per serving relied on assumptions, 26 products could potentially lead to an iodine intake above the (European) tolerable adult upper level of 600 μg/day. In the context of the data presented, there is scope to improve product labelling (species, source, processing, content). 3129 foods Foods Foods Multidisciplinary Digital Publishing Institute (MDPI) PMC5302319 5302319 5302319 28231201 10.3390/foods4020240 Emergence of Seaweed and Seaweed-Containing Foods in the UK: Focus on Labeling, Iodine Content, Toxicity and Nutrition Bouga Maria 1 Combet Emilie 1 * Smith Christopher J Academic Editor 1 1 Human Nutrition, School of Medicine, College of Medical, Veterinary and life Sciences, University of Glasgow, Glasgow G31 2ER, UK; E-Mail: Maira.Bouga@glasgow.ac.uk * Author to whom correspondence should be addressed; E-Mail: emilie.combetaspray@glasgow.ac.uk ; Tel.: +44-141-201-8527. For example, the iodine content of seaweed varies from 16 μg/g in some Nori species ( Porphyra tenera ) to 8165 μg/g in Icelandic Fingered tangle [ 5 ]. Meanwhile, inorganic arsenic concentration is found to be low in kelp species, one of the most common edible seaweed category, and within the Tolerable Daily Intake level of 2 μg/kg body weight, set by the World Health Organisation (WHO) [ 6 ]. Overall, there is lack of data regarding seaweed availability and consumption in the British diet, with limited consumer knowledge on the product(s) [ 7 ]. Recent coverage in the UK media also advocated for a seaweed-based diet, in response to low iodine intake in the population, which is potentially harmful, since it may lead to over-exposure to the nutrient [ 24 ]. Retail availability and intake or iodine-rich foods are essential for individuals to meet their daily iodine requirements (140 μg, equivalent to two portions of fish per week, and dairy to the equivalent of one glass (drinks, in cereals), plus a cheese serving per day). The product lists of all UK grocery retailers were searched, with the exception of those that did not have an online shop. Twenty nine different retailers, which all have an online shop, were included in the survey. Product selections available for purchase were searched with the keywords “seaweed”, “sea vegetable”, “Ascophyllum”, “Laminaria”, “lava bread”, “miso soup”, “Arame”, “Kombu”, “kelp”, “algal” and “Dulse”. 2.2. Identification of Products’ Iodine Information All products’ packaging was checked for information relative to their iodine content. All products’ labels which detailed iodine content were recorded in the database. Iodine content of each type calculated as median when more than one value was present There are currently five unauthorized claims in the European register on nutrition and health claims [ 43 ], pertaining to the use of seaweed for the management of blood glucose and insulin levels, body detoxification and appetite and hunger control [ 43 ]. Seaweed is a good iodine source and its contribution to the daily iodine intake of the UK population should be further explored. Accurate laboratory analysis is needed to define seaweed products’ iodine content. Iodine should be considered for analysis, as very high concentrations might cause toxicity and adverse effects but safe levels might be able to help reduce the iodine insufficiency in the UK population. There should be careful consideration on iodine levels in products using seaweed as a functional food. Inclusion of nutrient-dense ingredients in specific food formulation will also drive a need to revise food composition table, which may considerably skew the iodine content for some food groups and render dietary assessment difficult. 4.3. Iodine was only labelled in a minority of the food products with limited provision of the necessary information to accurately calculate iodine content in others. At the moment, there are no rules regarding iodine and/or seaweed labelling in food products, making it difficult to retrieve information about the contribution of products containing iodine and seaweed on the daily iodine intake, as well as estimating their suitability regarding toxicity. This lack of information and the impact of processing on seaweed content limits our analysis and also highlights the need for the products to display iodine content. Conclusions The present study identified a wide range of seaweed containing products sold in the UK grocery market. The lack of information regarding the seaweed type used, its source and iodine content makes it difficult to formulate safe conclusions regarding the safety and suitability of these products and is a potential issue for high iodine exposure, especially for consumers who are pregnant. Further information on the source of seaweed (and derived information on water quality) and information on how it was processed will also enhance the ability to assess potential exposure to contaminants and toxic compounds.

The world population is continuously growing, so it is important to keep producing food in a sustainable way, especially in a way that is nutritious and in a sufficient quantity to overcome global needs. Seaweed grows, and can be cultivated, in seawater and generally does not compete for arable land and freshwater. Thus, the coastal areas of the planet are the most suitable for seaweed production, which can be an alternative to traditional agriculture and can thus contribute to a reduced carbon footprint. There are evolving studies that characterize seaweed's nutritional value and policies that recognize them as food, and identify the potential benefits and negative factors that may be produced or accumulated by seaweed, which are, or can be, dangerous for human health. Seaweeds have a high nutritional value along with a low caloric input and with the presence of fibers, proteins, omega 3 and 6 unsaturated fatty acids, vitamins, and minerals. Moreover, several seaweed sub-products have interesting features to the food industry. Therefore, the focus of this review is in the performance of seaweed as a potential alternative and as a safe food source. Here described is the nutritional value and concerns relating to seaweed consumption, and also how seaweed-derived compounds are already commercially explored and available in the food industry and the usage restrictions to safeguard them as safe food additives for human consumption. Excess dietary iodine may lead to thyrotoxicosis and could be associated with hyperthyroidism [ 190 , 191 ]. So, ingestion of seaweeds, namely brown ones, that have higher contents of I, must have some precautions since the daily intake of more than 1100 µg (tolerable upper intake level for adults) may cause harmful effects [ 158 , 186 ]. Above the specific features and geographical and environmental factors, iodine has been reported to vary with age and condition of the seaweed, with iodine concentration dropping when the seaweed is no longer growing. In line with this, according to an individual’s iodine-related pathologies, and knowing that seaweed consumption may benefit an individual’s health, prevention of excessive iodine intake may include the disclosure of iodine content and the provision of cooking instructions on seaweeds’ product labeling to ensure consumer safety. Another issue of seaweed ingestion is the chemical toxicity associated with the absorption and bioaccumulation of heavy metals from the environment, such as lead, mercury, cadmium and arsenic (inorganic arsenic) [ 195 ]. These values on seaweeds depend on the external contamination, which has led to inconsistency in research findings. For instance, the maximum level for inorganic arsenic is 3 mg/kg (dry weight), for iodine is 2000 mg/kg (dry weight), for cadmium 0.5 mg/kg (dry weight), for mercury 0.1 mg/kg (dry weight) and for lead 5 mg/kg (dry weight) [ 59 , 201 ]. Additionally, dried seaweeds have to be submitted to microbiological tests, as Salmonella sp. (0 in 25 g of product) and Staphylococcus aureus (<100/g of product) [ 61 , 201 , 202 ]. Algae are one of the best approaches to address the nutritional deficiencies found in some of the current “western” daily meals, due to its wide range of constituents: minerals (iron and calcium), protein (with all essential amino acids), vitamins and fibers. Therefore, under the Commission Recommendation (EU) 2018/464, the monitoring of the concentration of metals and iodine in seaweed and their derivative products is also advised [ 209 ]. Meanwhile, in the United States of America, seaweeds’ application in the food industry is regulated by FDA, within the Department of Health and Human Services (title 21, chapter 1B, part 182) [ 210 ]. However, the legislation differs between countries, namely in the mandatory monitoring and the concentration limits accepted for seaweed compounds [ 211 ]. 3.1. Regarding food security, the responsible European authorities considered E . cava phlorotannins safe for human consumption, establishing a threshold of daily intake according to the age of the consumer [ 275 , 277 ] 3.3. Pigments Among chlorophyll, and other accessory pigments (such as carotenoids) and phycobilins, there are light-harvesting compounds characteristic of certain seaweed groups. Seaweeds are categorized taxonomically according to the main accessory pigments that they possess [ 25 ]. However, there is a need for supervision of the negative impact of the seaweeds in the human diet, such as the excessive intake of iodine and arsenic, so there is a need to control the seaweed nutritional quality and the negative factors of seaweeds that is also required in regular agriculture. The commercial sub-products of seaweeds, mainly the polysaccharides, have been under inspection and have restricted orders and directives to be considered food-safe ingredients. Species Calcium Copper Iodine Iron Magnesium Manganese Phosphorus Zinc Potassium Sodium Ochrophyta, Phaeophyceae (brown seaweed) Fucus vesiculosus 725–3000 <0.5 14.50–26 29–11 670–994 3.7–5.50 100–315 3.71 2500–4322 1800–5469 Saccharina japonica 225–910 0.25–0.40 130–690 1.19–43 550–757 0.13–0.65 150–300 0.89–1.63 4350–5951 2532–3260 Sargassum fusiforme 1860 ND 43.6 88.6 687 ND ND 1.35 ND ND Undaria pinnatifida 331–1380 0.19–2.0 22–30 1.54–30 277–680 0.27–0.56 235–450 0.94–4.03 864–6810 1600–7000 Rhodophyta (red seaweed) Chondrus crispus 420–1300 <0.5–0.76 24.5 4–20 600–900 1.32–2.2 135–240 7.14 1350–3184 1200–4270 Palmaria palmata 250–1200 <0.5 10–100 7.30–50 120–610 0.41–1.14 210–235 2.86 2800–9000 320–2500 Neopyropia tenera 390 0.63 1.7 10–11 565 3 ND 2–3 3500 3627 Chlorophyta (green seaweed) Caulerpa lentilifera 780–1874 0.11–2.20 ND 9.30–21.40 630–1650 7.90 700–1142 2.6–3.5 700–1142 8917 Ulva lactuca 840–1600 0.71 0.43 66–180 2700 2.6 140–220 ND 2800 700 life-10-00140-t008_Table 8 Table 8 Food and Drug Administration (FDA) and European Food Safety Authority (EFSA) specific limitations of

<b>Background:</b> Seaweed has a high potential for nourishing the future planet. However, besides being beneficial, it also contains adverse components; this poses the question whether consumption of seaweed foods overall contributes beneficially or detrimentally to human health, and hence if their consumption should be promoted or restricted. <b>Methods:</b> This study evaluated the impact of substituting regular foods with seaweed foods in the diet, both in terms of nutritional quality (<i>via</i> iodine and sodium) and food safety (<i>via</i> arsenic, cadmium, lead, and mercury). Food consumption data from the Netherlands and Portugal (adults aged >18 years) were used, in which 10% of the amounts of pasta, bacon, and lettuce consumed were replaced by seaweed-derived products made from kelp (<i>Saccharina latissima</i>). Using Monte Carlo Risk Assessment software (MCRA), long-term nutrient intake and exposure to contaminants were assessed. The results obtained for the Netherlands and Portugal were compared with data from Japan, a country that has a high natural consumption of seaweed. <b>Results:</b> This low-tier risk-benefit study reveals that an increased seaweed consumption (as assessed by the 10% replacement with seaweed products) has no consequences in terms of intake of sodium and exposure to cadmium, lead, and mercury, and the associated (absence of) adverse health aspects. The alternative scenario almost doubled the mean iodine intake in the Netherlands (to 300 μg/day) and Portugal (to 208 μg/day) and increased the average exposure to arsenic levels in the Netherlands (to 1.02 μg/kg bw/day) and Portugal (to 1.67 μg/kg bw/day). <b>Conclusion:</b> The intake of iodine and exposure to arsenic in the Netherland and Portugal were certainly higher due to the modeled increase of seaweed foods. If seaweed consumption increases close to the 10% substitution, the public health consequences thereof may trigger further research. Conclusion: The intake of iodine and exposure to arsenic in the Netherland and Portugal were certainly higher due to the modeled increase of seaweed foods. If seaweed consumption increases close to the 10% substitution, the public health consequences thereof may trigger further research. Seaweed can contain high concentrations of iodine and can be considered as “rich in” iodine according to Regulation EU 1924/2006 ( 11 , 12 ). Globally, the elimination of iodine deficiency is regarded as a major public health challenge ( 13 – 16 ). Iodine deficiency results in inadequate thyroid hormone production causing a range of adverse health effects, including impaired growth and development in children and in the offspring of deficient mothers, cretinism, goiter, and thyroid cancer ( 17 ). Previous studies investigating iodine status in Portuguese pregnant women and school-aged children reported intakes well below the adequacy recommendation of WHO ( 13 , 14 ). Verkaik-Kloosterman et al. reported that the iodine intake among the Dutch population (7–69 years) seems adequate due to fortification of bread with iodized salt, although iodine intake has decreased since the period before 2008 ( 16 ). Contrary, high iodine intake exceeding the upper tolerable intake levels may lead to iodine toxicity and can have negative health effects such as impaired thyroid function, goiter, and hyperthyroidism ( 9 , 18 ). Moreover, seaweed contains the essential micronutrient sodium. The intake of sodium is, in general, much higher than recommended and should be limited. Additionally, although the EU has no regulation on the maximum level of iodine in algae food products, France has set a limit of 5 mg/kg dry matter and Germany warns about damage to health for algae food products with more than 20 mg/kg dry matter algae ( 27 ). As seaweeds contain both nutrients and contaminants, it poses the question whether consumption of these foods has a beneficial or detrimental effect on human health and whether consumption should be promoted or restricted. This is the domain of risk-benefit assessment in food safety and nutrition, an emerging field in food safety risk assessment ( 28 – 32 ). With a low tier risk-benefit analysis, we examine the change in intake of selected dietary nutrients (iodine and sodium) and chemical contaminants [total-arsenic (organic and inorganic arsenic) (t-arsenic), i-arsenic, cadmium, lead, and mercury]. A rough comparison is made with established health-based guidance values (HBGVs) or benchmark dose lower confidence limit (BMDLs) by EFSA or FAO/WHO Joint Expert Committee on Food Additives (JECFA). The results obtained for the Netherlands and Portugal are compared with dietary intake data from Japan, a country with a high natural consumption of seaweed. Guidance Values The resulting usual daily intake and exposure for iodine, sodium, and chemical contaminants in the Netherlands, Portugal, and Japan were compared with the most recent evaluations of HBGV's, as published by EFSA and JECFA (FAO/WHO Joint Expert Committee on Food Additives). For sodium and iodine, HBGV's, which are the dietary references values, are set in mg/day and μg/day, respectively. b Exceeding safe and adequate intake of 2000 mg/day (EFSA) . c Exceeding BMDL of 0.3-8 ug/kg bw/day i-arsenic (BMDL01,EFSA) . d At risk or exceeding BMDL of 0.63 (f) ug/kg bw/day lead, (BMDL10,EFSA) . e At risk for exceeding HBGV of 0,19 ug/kg bw/day MeHg [(P),TWI,EFSA] . Table 6 The intake of selected nutrients (iodine and sodium) and exposure to contaminants (arsenic, cadmium, b Exceeding safe and adequate intake of 2000 mg/day (EFSA) . c Exceeding BMDL of 0.3-8 ug/kg bw/day i-arsenic , (BMDL01,EFSA) . d At risk or exceeding BMDL of 0.63 (f) ug/kg bw/day lead, (BMDL10,EFSA) . e At risk for exceeding HBGV of 0,19 ug/kg bw/day MeHg [(P),TWI,EFSA] . Table 7 Outcome of the assessment for the intake of selected nutrients (iodine and sodium) and exposure to contaminants (arsenic, cadmium, lead, and mercury) for Japan a .