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The estimated increase in world population will lead to a deterioration in global food security, aggravated in developing countries by hidden hunger resulting from protein deficiency. Plant proteins derived from grains and seeds provide nutritionally balanced diets, improve health status, reduce poverty, enhance food security, and contain several functional compounds. The evidence on the nutritional and functional properties of underutilized grains, their incorporation into functional foods, and the role of their proteins and bioactive peptides is summarized herein.
underutilized grains
functional foods
bioactive peptides
nutritional composition
enzymatic hydrolysis
gastrointestinal digestion
health benefits
1. Introduction to Underutilized Grains
In recent years, the continuous and concerning rise in world population and the consequent increase in food demand have challenged global food security. To aid with this global crisis, international organizations, governments, industries, and consumers are claiming sustainable, nutrient-rich and calorically efficient foods as an alternative or complement to animal products, and also reducing their associated negative-environmental impacts [1]. Food insecurity is higher in developing countries, where most people suffer from hidden hunger resulting from protein deficiencies [2]. This malnutrition problem can be addressed by exploring plant proteins as a sustainable and cost-affordable source of protein for a healthy diet [3]. Among plant proteins, those derived from grains and seeds have been recognized as the poor man’s meat, providing nutritionally balanced diets, improving health status, reducing poverty, and enhancing food security in low-income populations [4]. In addition to their nutritional role as a staple source of macro- and micro-nutrients, whole grain and seed proteins contain functional compounds such as bioactive peptides that play an important role in the prevention/management of various chronic disorders such as obesity, type 2 diabetes, cardiovascular disease, and cancer [5].
Grain- and seed-enriched proteins include wheat, brown rice, maize, millet, cornmeal, oatmeal, amaranth, buckwheat, couscous, teff, quinoa, flax, chia, and pumpkin, as well as sunflower seeds, peanuts, walnuts, almonds, cashews, dates, kiwi, and cumin. Cereal grains (Gramineae family) contain approximately 70–72% carbohydrates, 7–15% protein and 1–12% lipids, providing a significant source of energy in most diets when consumed as whole grains or in their refined form. Wheat, rice, and maize represent the major cereal crops sustaining over 50% of the worldwide caloric demand [6]. However, although these cereal grains constitute an important part of many diets, they are deficient in one or more essential amino acids as well as in some vitamins, minerals, and phytochemicals. To ensure access to nutritional grain-derived foods that meet human protein needs, approaches such as biofortification or supplementation have been implemented. On the other hand, in recent years, the interest has been focused on underutilized grains such as pseudocereals that traditionally have been used in rural areas as staple crops to provide essential amino acids, micronutrients and/or phytonutrients but the cultivation of which is limited and tied to cultural ancestry, and the agro-ecological and climate characteristics of their places of origin [7].
2. Nutritional Value of Underutilized Grains as the Basis for the Development of Functional Foods
The nutritional composition of food provides values based on energy and is a measure of essential nutrients, including protein, carbohydrates, fat, fiber, vitamins, and minerals. Functional foods proffer healthful benefits beyond basic nutrient requirements due to their physiologically active components. It has been suggested that these foods support or contribute to the control of several health conditions [8]. Functional food products are being increasingly developed using several grains and seeds, which are usually consumed for their higher fiber and protein contents. Also, this is connected to the functional and nutritional properties of whole grains, which include the three critical parts of grains, that is, the bran, the germ, and the endosperm, as opposed to refined grains containing only the endosperm [9]. To go further within this perspective, Table 1 captures an updated overview of the nutritional properties, biological activity, and physicochemical and techno-functional features of underutilized grains incorporated into functional foods. The recent advances with respect to these attributes will be discussed below for each grain species, also considering the sensorial characteristics of the developed functional foods.
Table 1. Nutritional, biological and techno-functional impact of the incorporation of underutilized grains in functional foods.
ABTS: 2,2′-azinobis(3-ethylbenzothiazoline-6-sulphonic acid) diammonium salt; ACE: angiotensin converting enzyme; AGEs: Advanced glycation end products; DPPH: 2,2-diphenyl-1-picryl-hydrazyl; FRAP: ferric reducing antioxidant power; MDA: malondialdehyde; MUFAs: monounsaturated fatty acids; ORAC: oxygen radical antioxidant capacity; PUFAs: polyunsaturated fatty acids; SFA: saturated fatty acids.
2.1. Amaranth
Amaranth is rich in various nutrients and bioactive molecules such as high-quality protein, unsaturated fats, dietary fiber, tocopherols, phenolic compounds, flavonoids, carotenoids, polyphenols, vitamins, and minerals. The elevated presence of phytochemicals makes amaranth a natural antioxidant-rich food [12]. Its leaves are rich in protein (17.9 g/kg), calcium (44.2 mg/100 g), iron (13.6 mg/100 g), zinc (3.8 mg/100 g), vitamin A (3.3 mg/100 g), and vitamin C (25.4 mg/100 g) on a dry weight basis [10]. Numerous health benefits have been linked to this pseudocereal, given its proposed hypo-cholesterolemic and anti-tumorigenic effects, immunomodulatory activity, anti-allergic action, impact on hepatic and glycemic function, and activity against celiac disease as a gluten-free product [15][46]. Its content in protein and various essential amino acids, especially lysine, are reportedly very high in comparison with other cereal grains [15].
This rich profile of amaranth has prompted a plethora of studies targeting its use in functional food products (Table 1). Cárdenas-Hernández et al. [17] reported a loss of antioxidant capacities in terms of ferric reducing antioxidant power (FRAP) and oxygen radical absorbance capacity (ORAC) after cooking amaranth-fortified elbow-type pasta, alongside the reduction of its luminosity values and the cooking time as compared to semolina pasta. The other merits of this development included the increase of protein, crude fiber, and ash contents in flour and dry leaves pasta, as well as iron, zinc, magnesium, and potassium in dry leaves pasta [17]. A more recent study showed that fortification of cassava pasta with amaranth could reduce cooking time and gruel solid loss while increasing its fiber, protein, β-carotene, iron, and zinc contents. Interestingly, the research was meant to present a healthy food choice to micronutrient-deficient consumers in low- and middle-income countries by combining a biofortified crop with leafy vegetables [10]. Earlier, semolina pasta enriched with digested and undigested amaranth proteins showed antihypertensive effects in a rat model, whereas it also reduced optimum cooking time and cooking loss [13]. However, the sensorial property was negatively impacted, especially the acceptability index. In the production of spaghetti pasta, a mixture of amaranth, sorghum, and wholesome sesame significantly increased protein, ash, fat, fiber, calcium, magnesium, and zinc, but also the contents of alkaloids, total phenolic, flavonoids, and 2,2′-diphenyl-1-picrylhydrazyl (DPPH) and FRAP activities relative to wheat flour, referred to as control pasta [21].
Apart from pasta kinds, cookies are popular types of food product intended for biofortification. In a study where enriched cookies were supplemented with hydrolyzed amaranth and fed to mice, angiotensin-converting enzyme (ACE) inhibition was found in serum, and the blood pressure of hypertensive rats was also reduced [11]. Hence, this study suggested the suitability of cookies as incorporation vehicles for amaranth antihypertensive hydrolyzates based on the enriched cookies’ ability to release in vivo ACE inhibitors that could pass through the murine bloodstream, while still presenting acceptable sensory properties. Following this research, a similar study in which functional cookies were enriched with amaranth showed an increase of total protein, ash, and flavonoid contents, including higher antioxidant capacity [12]. In addition, the microbiological quality and sensorial acceptability were not negatively affected. This premise is suggestive of amaranth flour being an optimum alternative for fortification of functional ingredients.
Puffed snacks and muffins are other functional foods that have been targeted with amaranth. Regarding their nutritional composition, their higher protein, iron, zinc, and dietary fiber, as well as increased total phenolics, flavonoid content and antioxidant (2,2′-azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), and DPPH) activities have been described in puffed snacks and muffins enriched with amaranth, respectively [14][15]. Moreover, the color and texture of the muffins were improved; this research developed out of the need for gluten-free functional foods to act against risks associated with celiac disease [15].
When it comes to bread, Olagunju and colleagues [16] reported that the nutritional status of multigrain bread improved after fortification with amaranth due to the increase in ash, fiber, and protein contents. Although the carbohydrate content was reduced, the product displayed hydroxyl radical scavenging ability, Fe2+ chelation, and inhibition of Fe2+-induced lipid peroxidation, coupled to an increase of α-amylase and α-glucosidase inhibitory abilities, and a decrease in glycaemic indices in comparison to white-flour bread [16]. Moreover, the combination of amaranth with other grains to produce functional bread could be significant. For example, when amaranth, quinoa, and chia were incorporated in fresh bread manufacturing, there was a significant increase in the protein, ash, and lipid contents [47]. The crumbs were also firmer than wheat bread, and the loaf-specific volume decreased, while similar calorie values were observed between the control and the fortified bread. Although the sensorial acceptability was similar between both products, the functional and nutritional values of the optimized bread were far superior to that of the control.
It is also possible to formulate beverages with amaranth proteins, as reported by two independent studies. In the study of Malgor and colleagues [18], amaranth lemon sorbet was developed directed to vegan and celiac consumers. These authors found, on one hand, increased foaming properties and, on the other hand, that antithrombotic peptides were released from amaranth protein after simulated gastrointestinal digestion of the beverage. Also, the functional sorbet rheology exerts the desired stability during a two-month storage, and it evinces acceptable sensory characteristics such as creaminess, airiness, and healthiness [18]. Amaranth-based beverages with good nutritional quality like that of skimmed milk with high-value proteins, soluble fiber, lipids, and carbohydrates have been also developed [19]. Amaranth proteins in the fractions of 11S and P globulins displayed the propensity of interacting to form aggregates and increase viscosity, thereby contributing to the physical stability of the beverage. Indeed, this functional drink exhibited more advantages than did plant-based milk products earlier developed [48].
2.2. Buckwheat
Belonging to the Polygonaceae family, buckwheat grains are rich in high flavonoids, dietary fiber, essential minerals, vitamins (e.g., B1, C, and E), and quality protein contents [49]. Apart from its gluten-free status, the proteins of buckwheat are rich in essential arginine and lysine amino acids and present excellent nutritional quality with high digestibility and bioavailability of amino acids. Also, buckwheat flavonoids such as rutin and quercetin exhibit high antioxidant activity [49]. This remarkable nutritional profile makes buckwheat protein a suitable source for functional food products.
Due to its protein, flavonoids, and rutin contents, buckwheat flour was used in bread production and found to increase iron content while the porosity and specificity of loaf volume became reduced [22]. Likewise, tartary buckwheat (F. tartaricum) and chia were combinedly used in bread manufacture resulting in an increased amount of protein, insoluble dietary fibers, ash, alpha-linolenic acid, and in vitro antioxidant power, parallel to reduced energy and carbohydrate contents [28].
Buckwheat has been also used to formulate functional biscuits. Zieliński and colleagues [23][24] performed extensive works regarding the utilization of buckwheat in functional biscuits aimed at inhibition of ACE and anti-advanced glycation end products (AGEs). They were able to characterize the total phenolic compounds that include p-coumaric, sinapic, syringic, vanillic, protocatechuic acids, kaempherol, quercetin, apigenin, and orientin, and could partially correlate ACE inhibitory activity with the content of total phenolic compounds. Indeed, they observed a decrease in ACE inhibition, which was reverted by simulated gastrointestinal digestion, whereas higher anti-AGEs activity, antioxidant/reducing capacity and total phenolics contents were found following simulated digestion of biscuits [23][24]. It is thus inferred that the bio-accessible phenolic antioxidant compounds contributed to the inhibitory activity of biscuits against AGEs formation. An increase in dietary fiber content and antioxidant capacity has been also reported in functional deserts in which buckwheat by-products and derived melanin were incorporated [27]. Further complementing the functional role of this grain, it has recently been shown that tartary buckwheat supplementation for 12 weeks can attenuate serum oxidative and inflammatory responses, modulate gut microbiota and colonic short-chain fatty acids, and improve lipid metabolism of high-fat-diet-fed rats, like the effect displayed by an oat-supplemented diet [50].
Common buckwheat (F. esculentum Moench) and tartary buckwheat were comparatively studied for their cooking, textural, sensorial, and antioxidant activities in the noodling process [26]. They showed low and high concentrations of total phenolics and flavonoids in both grain sources, respectively, and correspondingly exhibition of low and high antioxidant capacities (FRAP, ABTS, and DPPH). On the other hand, the common buckwheat made the noodles’ tensility higher, but reduced adhesiveness whereas tartary buckwheat offered lower tensility and increased adhesiveness [26].
Functional beef burgers incorporated with buckwheat and quinoa showed an increase in magnesium, phosphorus, iron, and zinc contents in comparison with control burgers while their oil absorption and water holding capacity were significantly reduced when compared with soy protein and bread crumb-based control burgers [25]. Although the control burgers had higher protein and ash contents and lower carbohydrate content, the quinoa and buckwheat burgers showed higher levels of several minerals, increased sensory acceptance, and increased shelf-life stability [25]. Authors suggested that the replacement of soy protein and bread crumbs with buckwheat and quinoa flour is feasible when formulating beef burgers with improved nutritious and sensorial qualities, while gluten-sensitive and celiac consumers may obtain a beef burger alternative.
2.3. Chia
Chia (S. hipanica L.) grains are included in the group of alternative food products that have attracted the interest of both consumers and the food industry in recent years because of its nutritional quality, functional effects, and proposed health benefits ranging from cardiovascular health to chemopreventive properties against chronic disorders. Chia belongs to the Lamiaceae family, and its seeds have high dietary fiber (35%), lipids (40%), high-quality protein (19%), natural minerals, antioxidants, vitamins, and polyphenol and tocopherol contents [51].
Due to its rich nutritional profile, Alcântara Brandão et al. [29] reported that chia, as well as its seed blends and derived flours, increased the protein and dietary fiber contents of manufactured functional cookies, sensorial properties and acceptability of which were positively affected at purchase intention. A year later, sweet cookies incorporated with defatted chia flour were observed to increase their polyphenol content and antioxidant capacity (FRAP and ABTS) [34]. In this study, although lesser amounts of polyphenols were released from the food matrix during gastrointestinal digestion and absorbed through the intestinal barrier by passive diffusion, there was a greater release of polyphenols and antioxidant activity during colonic fermentation, thus establishing its potential prebiotic effects [34].
The richness of polyphenols and polyunsaturated fatty acids (PUFA) in chia cannot be diminished. In the formulation of beef burgers, chia seeds and goji puree were evaluated for their effects on the fatty acid profile, lipid peroxidation, total phenols, and antioxidant capacity of cooked beef burgers [30]. An increase in polyphenol bio-accessibility and antioxidant capacities (ORAC, ABTS, DPPH), as well as a reduction of malondialdehyde (MDA) values were found after simulated gastrointestinal digestion.
The use of chia in bread manufacture is another area for functional food development. Recently, chia seeds and kinako flour were utilized in the improvement of lipid profile in bread [31]. The authors reported an increase in PUFA content, with special attention to linolenic acid, and reduced contents of saturated fatty acid (SFA) and monounsaturated fatty acids (MUFAs). Similar results were obtained for incorporation of chia flour, which provided an increased amount of linoleic acid, protein, lipids, and minerals content and a reduced glycaemic index in comparison to wheat-based bread [20]. Moreover, Verdú et al. [37] studied the techno-functional effects of chia seed flour on the bread-making process and found a reduction of water activity and an equal amount of moisture compared to the control along with an improvement of gas retention in the dough, thereby cutting the time required to reach maximum dough development.
Functional yogurts are popular among consumers of functional foods. Hence, the study of Kowaleski et al. [32] developed yogurt formulations with enhanced nutritional properties and favoring probiotic effects by using strawberries and chia seeds supplementation. Earlier, another group of researchers used chia seed extract to fortify yogurt, and its radical scavenging activity and protection against lipopolysaccharide (LPS)-induced damage was increased in human colon cells [33]. Moreover, these in vitro effects were demonstrated in parallel to the acceleration of fermentation rate and growth of lactic acid and improvement of syneresis and water-holding capacity [33]. Hence, it is suggested that a set type of yogurt can benefit from chia supplementation, which enhances the growth of lactic acid bacteria, the physicochemical properties, and the health benefits of the final product.
Other functional food ingredients and products such as pineapple jam [35], cake [36], kulfi dessert [38], corn tortillas [39], and gluten-free noodles [40] have been also formulated or developed whilst incorporating chia or its by-products. From these studies, it may be inferred that adding chia components to a set type of functional products allows the enhancement of their nutritional profile, physicochemical properties, and the health benefits of the final product (Table 1). As an example, gluten-free noodles were developed with increased protein, fat, phytic acid, and phytate phosphorus contents along with several micronutrients, while there was also an increase in antioxidant activity, total phenolic content, and a significant rise in volume and weight.
2.4. Lupin
Lupins (Lupinus albus L.) are distinguished by their high-quality protein and dietary fiber contents, which are associated with cholesterol-lowering activity. Their seeds are enriched with high levels of total unsaturated fatty acids and contain vitamins such as thiamine, niacin, riboflavin, and tocopherols, as well as minerals including iron, zinc, and manganese [41]. When processed into flour and protein isolates, lupins are rich in antioxidants like polyphenolic tannins and flavonoids [52]. When compared with soybean and other legumes, lupins have lower levels of anti-nutritional components such as phytate and saponins. Besides, the amounts of lysine, isoleucine, leucine, phenylalanine, and tyrosine in lupin are in the optimal range of reference protein for adults according to the Food and Agricultural Organization (FAO) standards [41].
Studies summarized in Table 1 have found that proteins and dietary fiber contents of lupins have the potential to increase the nutritional quality and modify the technological properties of bread and other baked products when wheat flour is supplemented by lupin flour. This serves as the backdrop for the supplementation of wheat flour with lupin flour in biscuits production [41]. The authors reported an increase in protein, lipid, fiber, and ash contents, and a reduction in carbohydrate content compared with the control biscuits made of wheat flour. There was also a rise in all amino acid content, and increased quality scores.
Lupin flour can be used to formulate both functional baked products [53] and other non-baked foods like dairy products [54], pasta [55], and meat products [56]. Hence, in beef sausage lupin incorporation, increased dietary fiber and reduced fat content were reported after cooking [43]. Moreover, the meat emulsion stability increased, the cooking loss decreased, and there was a greater adhesiveness in the final product. In sweet-cookie formulation with lupin seed extract, low values of water activity and moisture content were obtained while higher firmness but a reduced impact on the shape parameters as well as lightness were observed in the finished cookies [42].
2.5. Quinoa
Quinoa (Chenopodium quinoa) has been grown for more than five millennia and it is a good source of starch, vitamins, minerals, protein, fat, dietary fiber, and polyphenols [57]. Quinoa seed has a high protein quality (average percentage~14 to 18%) due to its elevated concentrations of lysine and histidine amino acids, while is a rich source of digestible plant protein for celiac and gluten-sensitive consumers [58]. It also contains high amounts of micronutrients including magnesium, calcium, zinc, copper, iron, niacin, and α- carotene [25].
In functional bread development, quinoa flour has been used with the result of increased yellowness and increased contents of vitamins, minerals, essential amino acids, protein, dietary fiber, Mg, Fe, and P, while reducing the starch content, lightness, and redness of the finished products [44][45]. The implication is that both nutritional qualities and the sensory and physico-chemical properties of bread may be enhanced by the incorporation of quinoa and its products. Following this line of thought, a mix of quinoa and buckwheat flour was used for the formulation of functional beef burgers [25]. This study found increased shelf-life stability, increased contents of magnesium, phosphorus, iron, and zinc, as well as reduced oil absorption and water holding capacity, in comparison with control burgers made of soy protein and breadcrumbs.
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