Аннотация

Seaweed has a unique chemical composition with an abundance of bioactive substances. In Russia, brown seaweed grows in the coastal areas of the Pacific Ocean (Far East) and the seas of the Arctic Ocean.
This review focuses on the therapeutic and nutritional potential of functional components of brown seaweed. It was based on a systematic analysis of research and review articles published from 2010 to 2023 and indexed in Scopus, Web of Science, and eLIBRARY.RU. Our particular interest was in seaweed’s bioactive components such as polysaccharides, phenolic compounds, vitamins, lipids and fatty acids, proteins, peptides, and amino acids.
Compounds extracted from brown seaweed exhibit antioxidant, antiglycemic, antitumoral, neuroprotective, anti-inflammatory, anticoagulant, antibacterial, and immunostimulating properties. Brown seaweed and its derivatives are used as structural modifiers, antioxidants, preservatives, moisture-retaining agents, and sources of vitamins and minerals in the development of functional and preventive food products. They are also used as ingredients in meat, dairy, bakery and flour products, as well as in food additives and beverages, to provide potential health benefits and essential nutrients.
Studies have proven the functional effectiveness of food products containing brown seaweed and its derivatives. The incorporation of seaweed components into functional foods could contribute to global food security. More research is needed to develop new competitive products based on seaweed and to investigate them for the presence of substances hazardous to humans and the environment.

Ключевые слова

Brown seaweed, bioactive substances, bioactivity, functional foods, functional ingredients, essential nutrients

ВВЕДЕНИЕ

Nowadays, there is an increasing interest in the production of healthy food products, with special attention paid to balanced therapeutic and functional products. This is associated with their positive impact on human health and preventative action against various diseases. Food formulators focus on the use of novel and renewable sources of commercial food raw materials that are rich in bioactive substances with therapeutic potential. Brown seaweed is a promising source of bioactive components since it has a high growth rate, a large increase in biomass, and an abundance of fermentable carbohydrates. In addition, seaweed does not need fresh water for cultivation.

Based on pigmentation, seaweeds belong to three different groups: Phaeophyta (brown algae), Chlorophyta (green algae), and Rhodophyta (red algae) [1–3]. Brown seaweeds, which number over 2000 species, have predominated in global seaweed production (some of the most common of them are shown in Fig. 1) [4]. From 1950 to 2019, seaweed production annually increased by 11% to reach about 35 million tons [5]. In 2019, two main brown seaweeds (Laminaria saccharina and Undaria pinnatifida) accounted for about 47% of global seaweed production [6].

In Russia, brown seaweeds grow in the coastal zone of the seas of the Arctic Ocean and in the coastal waters of the Pacific Ocean in the Far East [7, 8]. Commercial stocks of brown seaweeds in the Arctic Ocean basin (the White and Barents Seas) are represented by the families of laminaria (L. saccharina, Laminaria digitata, Laminaria hyperborea, Alaria esculenta) and fucus (Fucus vesiculosus, Fucus distichus, Fucus serratus, Ascophyllum nodosum) [9]. Their total reserves exceed 900 000 tons. L. saccharina is commercially cultivated on the littoral of the White and Barents Seas. The Far-Eastern seas are home to over 160 species of brown seaweed, with their total reserves estimated at 25–28 million tons. In the coastal waters of the Peter the Great Gulf (the Sea of Japan), near the coast of Primorsky Krai, Laminaria japonica is cultivated in special engineering structures (seaweed plantations), with an annual yield of 600–800 tons.

Brown seaweeds are rich in carbohydrates, proteins, polyunsaturated fatty acids, and dietary fibers (Table 1), while being very low in lipids [10]. They are a plant source of vitamins, minerals (micro- and macronutrients), bioactive molecules and enzymes, as well as iodine [11]. These components may vary in content depending on the conditions of seaweed growth: temperature, water salinity, light exposure, degree of surfacing, depth of growth, type of substrate, and other factors [12, 13]. These changes are associated with the influence of external factors on the processes of photosynthesis, respiration, and permeability of seaweed shells [14–16].

Seaweeds are consumed in small quantities and therefore cannot be considered a major source of energy. However, brown seaweeds are a source of extracts rich in nutrients and bioactive substances. They have high potential for use as food additives and/or ingredients to enhance the nutritional and biological value of food products.

In this review, we analyzed and systematized data on the therapeutic and nutritional potential of the functional components of brown seaweeds. In the first part, we described their bioactive components, including polysaccharides, dietary fibers, phenolic compounds, pigments, lipids (fatty acids), proteins, peptides, amino acids, vitamins, and minerals. Based on current scientific publications, we evaluated possible uses of these compounds in the treatment and prevention of various diseases. The second part of the review is devoted to the use of bioactive substances extracted from brown seaweeds in food technologies for the production of foods with functional and preventative action.

ОБЪЕКТЫ И МЕТОДЫ ИССЛЕДОВАНИЯ

This study was carried out in the Chemistry and Technology of Marine Bioresources Laboratory at Murmansk State Technical University. We systematized data from original research articles and reviews on seaweeds, their bioactive components, as well as their nutritional and therapeutic potential and applications. For this, we employed a number of methods. First, bibliometric analysis was performed to determine the relevance of literature sources and clean the data of irrelevant or repeated sources. Then, the key scientific publications selected were exposed to in-depth analysis and systematization. A logical search strategy was employed for exploratory analysis to select publications covering the entire range of research problems, from the description of properties of brown seaweeds to their consumption [23]. The search terms (keywords) were broad to provide maximum coverage and included various combinations with the term “brown seaweed”. The search was limited to publications from 2010 to 2023 on three databases: Web of Science, Scopus, and eIBRARY.RU. The publication citation ranking was used to select publications from the generated list for in-depth analysis.

РЕЗУЛЬТАТЫ И ИХ ОБСУЖДЕНИЕ

Bioactive components of brown seaweeds and their therapeutic potential. Brown seaweeds have a unique chemical composition and are rich in various bioactive substances () with physiological activity in vitro and in vivo [24, 25]. The main components of brown seaweeds are represented by minerals, including microelements, and organic substances, including proteins, free amino acids, lipids (fatty acids), pigments, polyphenolic substances, structural carbohydrates (alginic acids, fucoidan, cellulose), and spare carbohydrates (mannitol, laminarin). This composition results from complex metabolic processes occurring in seaweed.

Functional components extracted from brown seaweed have high potential in treating a number of chronic diseases due to their antioxidant, anticoagulant, antiglycemic, antitumorous, and neuroprotectant activities [26–32] (Fig. 3). These properties are key to potential nutraceutical and therapeutic applications of brown seaweeds [33, 34].

Figure 3 shows the main components of brown seaweeds that have biological activity and are widely used in various technologies.

Polysaccharides. Seaweed is an important source of polysaccharides, which are more diverse than those in land plants [35, 36]. Most carbohydrates in seaweed are sulfated and unsulfated polysaccharides. Brown seaweed is rich in polysaccharides such as laminarin, alginate, and fucoidan, which consist of monosaccharides such as glucose, rhamnose, galactose, fucose, xylose, mannose, as well as glucuronic and mannuronic acids [24, 37].

According to clinical studies, seaweed-derived bioactive components are effective in the prevention and treatment of COVID-19. Sulfated polysaccharides and polyunsaturated fatty acids obtained from seaweed also exhibit immunostimulating and antitumorous effects [33, 37, 38].

Alginates (or alginic acid) (Figs. 4a and b), which are part of cell membranes, are the most common polysaccharide in brown seaweeds. Some of them contain up to 70% of alginic acid on dry basis [39]. Alginates can be obtained by chemical extraction, by microwave radiation, ultrasonic extraction, or a combination of enzymatic and traditional chemical extraction [40]. Alginates are extracted from such genera as Laminaria, Ecklonia, Ascophyllum, Durvillaea, Lessonia, Macrocystis, Sargassum, and Turbinaria [41]. Laminaria and Macrocystis are currently the main sources of alginates [42]. Alginates are widely used in the food and pharmaceutical industries to prevent bowel diseases and regulate blood sugar levels. Placebo-controlled studies in humans have shown that alginates have a positive effect on the appetite by increasing a feeling of fullness and reducing energy consumption by the body while maintaining its functionality [43–46].

Alginates are also able to form hydrogels in the presence of metal cations. They are widely used in the food and pharmaceutical industries due to their high waterholding capacity and good adsorption properties [32].

Fucoidan (Fig. 4c) is a fucose-containing sulfated cell wall polysaccharide that protects brown seaweed against environmental impacts. Its content and composition vary depending on the species, as well as the season and stage of seaweed growth [47, 48]. Fucoidan can be extracted by conventional chemical, microwave, ultrasonic, or enzyme extraction [49]. Saccharina latissima and Fucus evanescens are the most suitable sources of fucoidans [50].

Brown seaweed-derived fucoidan is the most promising anticancer agent due to its powerful antitumor activity against various types of cancer [51]. Also, fucoidan has a hypoglycemic effect and is therefore used to treat diabetes mellitus and prevent its complications [46, 52].

Fucoidan extracted from brown seaweed can also be used in aquaculture as a functional bioactive component in the diets of both fish and shellfish [53].

Laminarin. Beta-glucan (β-glucan), which is a polymer of glucose, is contained in the cell walls of plants, cereals, fungi, seaweed, and some species of bacteria [54]. Brown seaweed is the main source of laminarin (or laminaran), a type of β-(1→3)-glucan containing β-(1→6)-related branches (Fig. 4d) [55]. Laminarin was first discovered in kelp species [56]. It belongs to dietary fibers and is not digested in the upper gastrointestinal tract. Laminarin helps reduce the risk of colon cancer, obesity, and diabetes [47]. Oxidation and reduction processes enhance the antitumorous, antioxidant, and anti-inflammatory properties of laminarin [32]. In 2020, the beta-glucan market amounted to $403.8 million, and it is estimated to grow annually by 7.6% to reach $628.3 million by 2026 [57].

Dietary fibers. The human gut microbiota plays an enormous role in general health and disease prevention. Numerous current studies are aiming to strengthen the immune system with the help of the gut microbiota and to treat a number of diseases, such as diabetes, cancer, and obesity [58]. Polysaccharides obtained from brown seaweed have been found effective in stimulating the gut microorganisms. Seaweeds contain 25–70% of total dietary fibers, of which 50–80% are soluble fibers [59]. Laminarin and fucoidan are typical soluble dietary fibers in brown seaweeds, while cellulose belongs to insoluble dietary fibers [60]. Sulfated polysaccharides, which are dietary fibers in seaweeds, are rarely found in terrestrial plants [61].

Dietary fibers have a prebiotic effect on human health. Brown seaweeds of the genera Ecklonia, Sargassum, Laminaria, Ascophyllum, Fucus, Undaria, Saccorhiza, and Porphyra have this effect due to the presence of polysaccharides, including dietary fibers (carbohydrates) which are not digested by human digestive enzymes. On the other hand, they are a nutrient substrate that stimulates the growth of beneficial microbiota (e.g., Lactobacillus, Bifidobacterium, and Faecalibacterium) [62, 63]. The prebiotic potential of seaweed has been confirmed by studies using a human colon model in vitro [17, 64]. As prebiotic compounds, dietary fibers induce an immune response by increasing the microbial activity of the gastrointestinal tract. This leads to fermentation and production of short-chain fatty acids, which, in turn, has several positive physiological effects. Seaweed’s dietary fibers have antioxidant, anti-inflammatory, anticoagulant, and antiviral activities [65–68]. Ajanth Praveen et al. reviewed the structure of various seaweed polysaccharides, new methods their extraction and purification, as well as their immunomodulatory effects on the gut microbiota [69].

Dietary fibers of brown seaweed are widely used in food technology, mainly as thickeners, emulsifiers, gelling agents, and prebiotics [70]. Sulfated polysaccharides (dietary fiber) have been shown to play an important role in enhancing seaweed’s antioxidant, immunomodulatory, anticarcinogenic, antiviral, and antimicrobial activities [41]. Dietary fibers extracted from brown seaweed show an excellent ability to swell and retain water due to the hydrophilic characteristics of sulfated polysaccharides [71]. This property is used in the production of meat products.

Phenolic compounds are among the most important bioactive components of seaweed. They include phenolic acids, tannins, flavonoids, catechins, and phlorotannins. Their composition varies depending on the type of seaweed. Brown seaweed contains mainly phlorotannins, which are complex polymers made up of phloroglucin links (1,3,5-trihydroxybenzene). Polyphenols account for 2 to 30% of seaweed’s dry weight. Phenolic compounds in brown seaweed have been shown to have antihyperlipidemic and antihyperglycemic effects [72, 73]. Phlorotannins exhibit antioxidant, anti-inflammatory, antimicrobial, cytotoxic, and antitumorous activities [74, 75]. They can also be used as anti-aging agents [76]. Phlorotannins play a major role in cell wall creation and perform protective functions [56].

People with prediabetes, overweight, and obesity are recommended to consume extracts of brown seaweeds (Ascophyllum nodosum and Fucus vesiculosus), which contribute to a significant reduction in body weight, waist circumference, and overall fat mass, as well as have beneficial effects on insulin secretion [77]. Numerous studies have shown a positive effect of phlorotannins and polysaccharides from Silvetia compressa on the growth of probiotic bacteria and therefore the human microbiota [78]. The therapeutic effects and possible applications of polysaccharides and phenolic compounds from brown seaweeds are shown in Table 2.

Pigments. There are three groups of pigments in seaweed: chlorophylls, carotenoids, and phycobiliprote- ins [94, 95]. Brown seaweed contains chlorophylls “a”, “c1 and c2”, and fucoxanthin (Fig. 5), which give the cells the brown color, as well as β-carotene, neofucoxanthin, and other carotenoids [96]. Chlorophyll pigments have positive effects on human health. In particular, they contribute to chelation with some chemical carcinogens and mutagens, lower the risk of cancer, and exhibit high antioxidant activity [95]. Pigments can be extracted from seaweed by solvent extraction, liquid extraction under pressure, or microwave extraction [97].

Fucoxanthin is among the most common carotenoids in brown seaweed. It is absent in terrestrial plants [26]. Fucoxanthin exhibits strong antioxidant action against oxidative stress [45]. It is safe to use and has no side effects. Fucoxanthin protects the cardiovascular system and has anti-inflammatory, anti-cancerous, and neuroprotective effects. Furthermore, it is an effective chelator of toxic and heavy metals [98]. Fucoxanthin’s antioxidant activity is associated with its neuroprotective, photoprotective, and hepatoprotective effects [26].

Lipids, fatty acids. Fatty acids with two or more double bonds are necessary for normal cell function, and they play a key role in cellular and tissue metabolism, regulating membrane fluidity, electron and oxygen transport, as well as temperature adaptation [99].

Lipids of seaweed mainly contain fatty acids with a long carbohydrate chain. Some brown seaweeds have a high content of total lipids in the range of 10–20 wt%. In particular, lipids account for 11.91 ± 2.00 wt% in Dictyota bartayresii, 10.80 ± 0.99 wt% in Dictyota dichotoma, 11.73 ± 0.49 wt% in Spatoglossum macrodontum, 12.8, 13.4, and 10.9 wt% (in April, May, and July, respectively) in Costaria costata, and 15.59 wt% (January) in Cystoseira hakodatensis [100]. Essential fatty acids and polyunsaturated fatty acids are found in large quantities in brown seaweed [101]. The main omega-3 polyunsaturated fatty acids are eicosapentaenoic acid (20:5 n-3), stearidonic acid (18:4 n-3), and α-linolenic acid (18:3 n-3), while the main omega-6 polyunsaturated fatty acid is arachidonic acid (20:4 n-6). Polyunsaturated fatty acids account for 51.28% of all fatty acids in Saccharina japonica. Arachidonic acid (C20:4 n-6) varies from 10.55% (Undaria pinnatifida) to 14.87% (Sargassum horneri), and eicosapentaenoic acid ranges from 8.36% (C. costata) to 13.04% (Saccharina japonica) [102].

The content of eicosapentaenoic acid is also high in A. nodosum (6.85%) and S. latissima (4.67%) [19]. Sargassum pallidum extract contains n-6 polyunsaturated fatty acids (41.3%) with C18 and C20 carbon atoms and such n-3 polyunsaturated fatty acids as α-linolenic (18:2; 7.8%), stearidonic (18:4; 7.3%), and eicosapentaenoic (20:5; 3.5%) acids Since the human body has a low ability to synthesize docosahexaenoic acid from linoleic acid, high intake of long-chain fatty acids and more unsaturated forms of linoleic acid (eicosapentaenoic and docosahexaenoic acids) is recommended to prevent cardiovascular disease [100].

Lipids containing n-6 and n-3 long-chain fatty acids are known to prevent atherosclerosis [103]. The lipid complex of S. pallidum introduced into the diet may have a hypolipidemic effect, restoring the liver’s lipid metabolism and esterifying function, as well as regulating the lipoprotein content in plasma. The combined action of n-3 and n-6 polyunsaturated fatty acids in S. pallidum’s lipid complex has an antioxidant effect on

the organism [104]. S. japonica’s lipid complex reduces dyslipidemia and hypercholesterolemia, as well as normalizes the ratio of fatty acids in total lipids of blood plasma and erythrocyte membranes due to the presence of various polyunsaturated fatty acids [105].

Proteins, peptides, and amino acids. The protein content in brown seaweed ranges from 5.00 to 19.66%. For example, Chnoospora minima, Dictyota menstrualis, Padina gymnospora, and Sargassum vulgare contain from 10 to 15% of protein dry weight. Brown seaweed contains all essential amino acids in the quantities recommended by the Food and Agriculture Organization of the United Nations (FAO). Its levels of aspartic and glutamic amino acids, which give seaweed a unique taste and aroma, are higher than those in red or green seaweed [4, 47, 101, 106]. Peptides derived from seaweed are known to exhibit antioxidant properties. They are also effective in treating cardiovascular diseases and diseases associated with metabolic syndrome [47].

Glycoproteins obtained from brown seaweed have unique biological properties. For example, glycoprotein isolated from U. pinnatifida has an antioxidant effect and is active against inflammatory diseases and Alzheimer’s disease due to cholinesterase inhibition [106, 107]. This glycoprotein inhibits the formation of toxic β-amyloid peptides by inhibiting β-secretase. In addition, it does not exhibit cytotoxicity in primary hippocampal cells and protects the cells from natural death. This glycoprotein was also shown to inhibit inflammatory mediators and nitric oxide, so it can be used as a dietary supplement to prevent inflammatory pathologies. Glycoprotein isolated from the brown seaweed Laminaria japonica has an antiproliferative effect on HT-29 colon cancer cells [108]. Glycoprotein was also shown to stimulate gastrointestinal cell growth in mice [109].

Brown seaweeds contain lectins, glycoproteins capable of reversibly and specifically binding to sugar residues [110]. Lectins are capable of specific recognition and can bind sugars (lactose, mannose, galactose, N-acetylgalactosamine, and N-acetylglucosamine) by non-covalent interactions. Lectin-carbohydrate interactions play an important role in such biological processes as cell adhesion, agglutination, opsonization, complement activation, and phagocytosis. Due to the specificity of mannose binding, lectins from brown seaweed are used to decipher and characterize complex mannose-containing glycans from the glycocalyx covering both normal and transformed cells. Lectins are also widely used as effective agents against the human immunodeficiency virus [111].

Seaweed lectins, often called phycolectins, are similar to plant lectins, but they also differ in some physical and chemical properties and have a unique carbohydrate specificity [112]. Phycolectins are monomeric proteins with a low molecular weight and an isoelectric point (pI) in the range of 4 to 6 [113]. Over 800 lectins from seaweeds have now been identified, of which 61% are from red seaweed, 22% from green seaweed, and 17% from brown seaweed. However, only about 40 lectins have been identified, purified, and sequenced [114].

Seaweed lectins are attracting attention because of their antiviral activity. Lectins can prevent the virus’s invasion into host cells and spreading there. This is where they differ from most traditional antiviral agents which block the life cycle of a virus once it has entered the cell. In addition, lectins act as surface markers for tumor cell recognition, transmembrane signal transduction, cell adhesion, mitotic apoptosis, and cytotoxicity. Therefore, lectins can be used in cancer diagnosis and therapy [110].

Noteworthily, the consumption of brown seaweed that has not undergone deep processing can reduce the availability and digestibility of protein due to high contents of soluble fibers and polyphenols. For use in food, the protein of brown seaweed should be separated from non-protein components [115, 116]. Proteins can be extracted from seaweed by using enzymes, microwaves, ultrasound, pulsed electric fields, or supercritical fluids [4]. Enzymes that decompose polysaccharides are used to release flavor components that impart umami flavor, such as peptides and amino acids [117].

Vitamins. Seaweed contains both water- and fatsoluble vitamins. Brown seaweed is an excellent source of vitamins A, B₁, B₂, B₃, B₁₂, C, D, E, as well as pantothenic and folic acids.

Brown seaweed is rich in vitamins B₁ and B₂. In particular, U. pinnatifida and S. japonica contain 0.3 and 0.24 mg B₁/100 g dry weight, respectively, as well as 1.35 and 0.85 mg of B₂/100 g dry weight, respectively [118, 119]. According to [120], U. pinnatifida has even higher contents of vitamins B₁ and B₂, namely 5 mg of B₁/100 g dry weight and 11.7 mg of B₂/100 g dry weight. Vitamins B₁ and B₂ are contained in smaller amounts in Eisenia arborea, namely 0.06–0.12 and 0.65– 0.92 mg/100 g dry weight, respectively [121]. Brown seaweed is also rich in vitamin C. Its contents in U. pinnatifida, S. latissima, and F. vesiculosus are 14.58, 61, and 40.9–51.7 mg/100 g dry weight, respectively [122–124].

Brown seaweed has a higher content of α-tocopherol, as well as β- and γ-tocopherols, compared to red and green seaweeds containing only α-tocopherol. The largest amount of vitamin E was found in Macrocystis pyrifera (132.77 mg/100 g) [119]. In Durvillaea antarctica and U. pinnatifida, the content of vitamin E amounted to 84.0 ± 0.5 mg/kg dry weight and 0.63 mg/100 g dry weight, respectively [125, 126].

Seaweed contains only provitamins of vitamin A. The brown seaweed S. japonica has a high content of β-carotene with vitamin A activity (2.99 mg/100 g dry weight calculated as 481 IU/100 g dry weight) [119]. According to [126], the content of vitamin A in U. pinnatifida is 4.73 IU/kg dry weight.

The bioavailability of vitamins is primarily related to their solubility, which ensures their absorption in the intestine. The bioavailability and absorption of some seaweed fat-soluble vitamins depends on whether they are taken with fat-containing foods or not. Fat-soluble vitamins are absorbed in the same way as dietary lipids [119]. Also, vitamins that are bound to fiber or some other carbohydrates in foods are less available than those taken in pure form.

Seaweeds are an important source of antioxidants since they can generate necessary compounds for protection against oxidation [127, 128]. Antioxidant activity is determined by several factors, such as the antioxidant’s internal chemical activity against radicals, the location and reactivity of radicals, the antioxidant’s concentration and interaction with other antioxidants, etc. Antioxidant compounds in seaweed include vitamin E (α-tocopherol), vitamin C (ascorbic acid), vitamin B₁, and nicotinic acid [119, 129]. Vitamins with strong antioxidant capacity can act as therapeutic agents to protect against cancer [51, 130].

Seaweed is the only non-animal source of vitamin B₁₂, which is important for vegetarians. Cobalamin is not synthesized in higher plants and is not required for their metabolism, so vegetables and fruits are low in this vitamin. Vitamin B₁₂ deficiency is a common consequence of vegetarian and vegan diets that leads to pernicious anemia, a disease characterized by impaired hematopoiesis. Vitamin B₁₂ is present in brown seaweeds of the genera Ascophyllum and Laminaria. Vitamin B₁₂ also slows down the aging process [131, 132].

Vitamin E found in seaweed is a strong antioxidant that prevents the formation of free radicals. As reported in [133], vitamin E improves the condition of blood vessels and reduces their damage. Vitamin E has also been shown to lower the risk of lung and cervix uteri cancer by interacting with genotoxic radicals, reducing mutagenic activity, inhibiting the formation of carcinogenic nitrosamines, and protecting cell membranes from peroxidation [134, 135]. α-tocopherol is able to bind free radicals through the phenol group and plays an important role in the oxidation of biological membranes, lipoproteins, and fatty deposits, controlling or reducing lipid levels [136].

Ascorbic acid contained in seaweed is another effective antioxidant [119]. Due to its ability to neutralize free radicals, it is believed to play an important role in preventing cancer. In addition, ascorbic acid has prooxidant properties [137]. Several studies have established a correlation between vitamin C intake and lower incidence of stomach cancer [134, 138, 139]. They have also found a possible association with a decreased risk of developing cancer of the oral cavity, pharynx, lungs, and gallbladder in men. Vitamin C intake helps lower blood pressure in patients with hypertension, hyperlipidemia, and diabetes. A combination of vitamin C with other antioxidants (vitamin E, β-carotene) can provide a synergistic antihypertensive effect [140].

Minerals. Seaweed can accumulate micro- and macronutrients contained in seawater, which gave rise to the term “marine organic drugs”. Brown seaweed absorbs minerals better than green or red seaweed due to its high content of alginic acid and its salts [141]. In brown seaweed, minerals and micronutrients account for 14– 45% dry weight, depending on seasonal and climatic variations [142]. The mineral content in seaweed is up to 36% dry weight, which is 10–100 times higher than that of fruits and vegetables. Thus, seaweed can make an important contribution to the daily mineral intake [143].

Brown seaweeds Laminaria digitata, U. pinnatifida, and F. vesiculosus are rich in minerals that are thought to improve glycemic control. These minerals include potassium (K; 2–15% dry weight), calcium (Ca; 0.1– 3.0% dry weight), and magnesium (Mg; 0.1–1.5% dry weight) [31, 122, 144, 145]. These seaweeds also contain zinc (Zn) and chromium (Cr) in the amounts of 0.004– 0.020 and 0.02–0.05%, respectively, due to improved circulating glucose levels [31, 122, 145–147].

According to scientific estimates, about one-third of the world’s population is at risk of zinc deficiency, especially children under the age of five who need zinc to support their growth [148]. Zinc exhibits therapeutic effects in several chronic diseases, such as atherosclerosis, some cancers, autoimmune diseases, Alzheimer’s and other neurodegenerative disorders, diabetes, depression, Wilson’s disease, as well as aging [149]. Chromium is required for energy production from blood sugar, as well as for insulin function and lipid metabolism [150]. A daily intake of one gram of U. pinnatifida can meet the recommended physiological requirement for chromium [143].

Seaweed is one of the most important sources of calcium and phosphorus. It contains large amounts of Ca, Mg, Na, P, Zn, and I. Compared to other mineral-rich foods, seaweed contains more Ca, Cr, I, Fe, Mg, P, Se, Zn, K, and Na. However, it has a lower copper content compared to other foods such as raw meat or mushrooms [151]. The content of calcium in the brown seaweeds A. nodosum (575.0 mg/100 g raw weight) and L. digitata (364.7 mg/100 g raw weight) exceeds that of whole milk (115.0 mg/100 g raw weight). Thus, these seaweeds can be used as a source of calcium to prevent or treat osteoporosis in growing children, as well as in pre- and postmenopausal women. In addition, the non-digestible prebiotic carbohydrates in seaweed can increase calcium absorption and bioavailability [152–154]. F. vesiculosus also contains Ca and Mg in much higher concentrations than many other products. Particularly, its Ca values (2.175 mg per 100 g dry weight) are almost 20 times as high as in whole milk, while its Mg concentration (994 mg per 100 g) is about 5 times as high as in peanuts. The iron (Fe) content in F. vesiculosus can reach 49– 52 mg per 100 g dry weight, so this seaweed may be useful in providing daily iron intake and preventing iron deficiency anemia [141, 154].

It has also been shown that one gram of seaweed can cover up to 57.6 % of the recommended daily intake of selenium, with the brown seaweeds M. pyrifera and S. japonica having the highest content [143].

Brown seaweeds are able to accumulate higher concentrations of sodium (Na) ranging from 0.4 to 9% dry weight and potassium (K) ranging from 2 to 15% dry weight than green seaweeds. The Na/K ratio in brown seaweeds is quite low (0.3–1.5), so they can support human cardiovascular health by reducing blood pressure [155].

Mg and Ca play a key role in the health of bones and teeth. In addition, Mg is also involved in cellular metabolism and enzyme systems, while Ca is involved in the regulation of heartbeat, nerve impulse transmission, muscle contraction, blood clotting, and activation of insulin and thyroid hormone calcitonin [156]. Brown seaweeds have been shown to contain higher amounts of calcium than tofu or cabbage [143].

Brown seaweeds are a source of iodine, especially in the genus Laminaria, which can accumulate iodine in amounts exceeding its content in seawater more than 30 000 times [157]. Iodine content in different seaweeds consumed as food can vary significantly (from 0.1 to 30 mg/g dry weight). Iodine is an important trace element necessary for the production of thyroid hormones thyroxine and triiodothyronine, which stimulate both metabolic regulation and normal development of the body. The bioavailability of iodine from brown seaweed is quite high, ranging from 31 to 90%, as shown by in vivo studies. However, excessive iodine intake can cause thyroid disorders and lead to both hyperthyroidism and hypothyroidism [158].

Uses of brown seaweeds in food technology. Among brown seaweeds, F. evanescens, S. japonica, S. latissima, L. digitata, and U. pinnatifida have the largest application in the food industry [159].

Seaweed is obtained in their natural habitat or grown on special farms. The world production of brown seaweed increased from 13 000 tons in 1950 to 16.4 million tons in 2019. Its average annual growth in 1950–2019 was higher than the growth of global aquaculture of all species. In 2019, the brown seaweeds Laminaria saccharina and U. pinnatifida accounted for 47.3% of the world’s seaweed production [5]. The world market for seaweed products amounted to $4.7 billion in 2021 and is expected to reach $6.4 billion by 2026, with an average annual growth of 6.3% [160].

Seaweed is mainly cultivated and processed in East and Southeast Asia, where it is commonly used as a food product. Although it is a traditional product in the coastal communities, many countries consider seaweed a niche or a novel product and therefore consume it in small quantities. Functionally, seaweed is consumed:
– as part of vegetarian diet, as well as in therapeutic or preventative nutrition;
– as a seaweed-based food additive;
– for gastronomic purposes in exotic dishes of oriental cuisine;
– as organic, ecological bio-products, whose production is environmentally-friendly and reduces emissions of greenhouse gases; and
– in social nutrition as an affordable balanced product for the growing population, etc.

In addition to nutritional purposes, seaweed is also used to produce feed for farm animals (including aquaculture), pharmaceuticals and nutraceuticals, cosmetics, textiles, biofertilizers/biostimulants, bio-packing, biofuels, etc. [159, 161–163].

Brown seaweeds are widely used as a functional ingredient in food production to improve health and reduce the risk of developing diet-related diseases [24]. Due to their physical and chemical properties, as well as biological activity, brown seaweeds can be used for nutraceutical purposes [152]. Brown seaweeds and their components (polysaccharides, protein extracts, etc.) are increasingly used in food technologies [164–167]. Many regions where the use of seaweed is limited for various reasons are showing interest in functional foods, including seaweed products [168, 169]. The functional roles and uses of bioactive components of brown seaweeds in food products are shown in Table 3.

In 2021, the global market of functional foods reached more than $180 billion, and it is expected to grow by almost 3% per year in 2022–2027 [179].

Noteworthily, consumers are conditioned to use traditional, familiar products. Therefore, people in those countries where seaweed is not commonly used as a food and is not part of traditional cuisine are neophobic towards this product [176, 184]. However, seaweed is often used in sophisticated, trendy cuisine due to its unique sensory properties. Its chemical composition and functional effects also contribute to its growing popularity [191].

The main types of products where seaweed or seaweed-derived bioactive substances are used as functional ingredients are reviewed below.

Meat products. Modern meat products containing bioactive ingredients have a balance of nutritional and functional properties [35, 192].

F. vesiculosus is rich in phlorotannins, polyphenolic compounds with high antioxidant activity. F. vesiculosus extracts are used as natural preservatives in pork chops to protect their lipids and proteins from oxidation during storage [193].

Extracts of the brown seaweeds A. nodosum, F. vesiculosus, and Bifurcaria bifurcata, which are high in natural antioxidants, provide chilled pâté of lean pork liver with oxidative stability similarly to the synthetic antioxidant tert-butyl-4-hydroxytoluene [194].

Replacing sodium chloride with edible seaweed (Himanthalia elongata and U. pinnatifida) in meat sausages can lower the risk of chronic diseases by reducing the salt content [195].

Alginates are widely used as thickening and stabilizing agents to reduce the fat content in various restructured meat products. Their stabilizing properties are due to their ability to form complexes with proteins [42]. Replacing pork speck with sodium alginate in meat sausages decreases the fat content and the energy value of the final product [182].

The addition of dietary fiber derived from seaweed can clearly improve the quality, nutritional properties, and taste characteristics of processed meat products [4]. Seaweeds can also enhance the ability of sausages to bind water/lipids and contribute to a thinner and denser gel-like matrix of meat protein [196]. The addition of laminarin and fucoidan significantly delays lipid oxidation in pork chops during storage [197]. Further, dietary fiber derived from brown seaweed can be a real alternative to phosphates in the production of meat sausages [198]. Phosphate-free sausages treated with dietary fiber have an improved quality profile, which meets the demand for healthier meat products. Dietary fiber improves the texture of phosphate-free sausages and effectively slows down lipid oxidation during storage.

Dairy products. Bioactive components of brown seaweeds (H. elongata, Laminaria ochroleuca, U. pinnatifida) are used in the production of various dairy products to improve their quality indicators. In particular, phenolic compounds exhibit antioxidant properties and can therefore increase the antioxidant activity of cheese when added to the milk clot. Introducing dehydrated seaweed can also enhance the retention of whey in the milk clot and has a positive effect on the color and texture of cheese [199].

Alginate oligosaccharides have a potential antifungal effect against certain yeasts that cause milk spoilage. In yogurt starter culture, alginate oligosaccharides extracted from Laminaria hyperborea decreased the growth of microorganisms Candida parapsilosis, Debaryomyces hansenii, and Meyerozyma guilliermodii. Thus, these oligomers can ensure safe storage of dairy and milk-containing products whose shelf life is reduced by yeast [200].

The use of bioactive food foam containing sodium alginate can replace fat and sugar in ice cream. Such functional products can benefit consumers who are overweight, obese, or have other weight-related complications [201].

Bakery and flour products. In bakery and flour products (bread, noodles, cakes, cookies, etc.), seaweed is usually used in the form of fine powder [202–204]. Seaweed forms stable mixtures and emulsions with dough, improving the functional properties of the end products. Added to bakery and flour products, seaweed decreased the color values of lightness, redness, and yellowness [205].

When added to bread, polyphenol-rich brown seaweeds (A. nodosum and F. vesiculosus) significantly reduce carbohydrate digestion compared with the control bread. However, the heat treatment of seaweed in bread during baking lowers its polyphenol content, which may reduce the seaweed’s ability to inhibit carbohydrates digestion in vitro [206].

Bread made from flour enriched with fucoidan extracted from the brown seaweed U. pinnatifida has a significantly high specific volume and softer crumb. Its improved quality is associated with a high production of CO₂ during proofing. Fucoidan’s antitumorous activity in vitro is preserved even after baking [207]. The brown seaweed F. vesiculosus can be added to bread as a natural antioxidant, as well as to increase its nutritional value. The addition of F. vesiculosus powder increased the longitudinal viscosity of the dough, which decreased its sponginess at the end of proofing, compared to a typical wheat bread formulation [208].

Food additives are used to achieve a certain technological or sensory effect [209]. The growing consumer interest in natural products has led to an increased demand for natural food additives among food and beverage manufacturers. These additives are believed to have health benefits and are used as functional ingredients and natural sources of soluble dietary fiber.

Seaweed has a naturally salty taste due to its high content of minerals such as potassium, which can be used as a healthy substitute for sodium to reduce the risk of cardiovascular disease [95].

Food hydrocolloids produced from brown seaweed are biopolymers that are widely used as thickeners (in soups, gravies, salad dressings, sauces, and fillings), moisture-holding agents, stabilizers, emulsifiers, and gelling agents (in jam, jelly, marmalade, restructured foods, and low-fat products) [42, 166]. The global hydrocolloid market amounted to $9.7 billion in 2020 and is estimated to reach $13.36 billion by 2026 [210].

3D food printing is a new technology that can produce any food product a consumer might desire. For example, it can be used to develop a product with the exact nutritional value, the most beneficial nutrients, and without the ingredients a consumer is allergic to. It can even predict or personalize the taste, color, shape, and size of the food product [211]. Hydrocolloids are added to facilitate extrusion during 3D printing. Sodium alginate determines rheological properties and therefore is widely used in 3D food printing [212].

Drinks. Brown seaweed components are added to provide drinks with functional properties. For example, fucoidan, a water-soluble polysaccharide, is added to beverages such as tea, coffee, fruit drinks, etc. Fucoidanrich seaweed is non-toxic and has antioxidant activity. Functional tea was developed from the brown seaweed Sargassum binderi. It was supplemented with lemon essence to mask the seaweed’s unpleasant taste and smell and thus improve its consumer acceptance [213]. Another example is a functional pasteurized apple drink, in which fucoidan obtained from the brown seaweed F. vesiculosus exhibited biological activity as an antimicrobial agent against Listeria monocytogenes and Salmonella enterica serovar Typhimurium [214].

ВЫВОДЫ

The production of functional food products based on brown seaweeds has enormous potential due to their unique biochemical composition. Brown seaweeds are rich in polysaccharides, dietary fiber, proteins, vitamins, minerals, and other nutrients, which contributes to high consumer interest. A number of authoritative in vitro studies have proven the effectiveness of food products based on brown seaweeds. Developing new competitive products is an important step in promoting seaweeds further and making them commercially viable. Also, more studies are needed to determine the safety of brown seaweeds during their harvesting, cultivation, and processing, including the environmental impact. In particular, new functional foods based on brown seaweeds should be thoroughly examined for the presence of pollutants, allergens, heavy metals or other substances that may pose a risk to both humans and the environment.

The incorporation of seaweeds into functional foods and a daily diet could potentially contribute to global food security in the future.

Вклад авторов

All the authors contributed equally to the study and bear equal responsibility for the information published in this article.

КОНФЛИКТ ИНТЕРЕСОВ

The authors declare no conflict of interest.

БЛАГОДАРНОСТИ

The study was performed at the Laboratory of Chemistry and Technology of Marine Bioresources established with the financial support of the Russian Ministry of Science and Higher Education (Agreement No. 075-032021-088/4). S.R. Derkach thanks the Russian Science Foundation (Project No.22-16-20046) and the Ministry of Education and Science of the Murmansk Region (Agreement No. 103) for their support.

ФИНАНСИРОВАНИЕ

This research was funded by the Russian Science Foundation (RSF) (Project No. 21-73-00191 “Obtaining polyelectrolyte complexes based on underutilized biopolymers of marine origin for biomedical purposes”).

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