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Introduction
Quinoa is an ancestral grain, native to countries in the Andean region 1) and it is currently being cultivated in other countries such as the United States, China, and France due to its importance in global food security. It is recognized for its resistance to different environmental conditions, biological diversity, nutritional potential, pest resistance, soil conservation, and its positive impact on the economy of local communities 1,2. Quinoa is a plant-based food known for its high protein content, excellent amino acid profile, essential fatty acids, lipids, fiber, vitamins, and minerals 3,4. When compared to other traditional cereals like wheat and rice, quinoa demonstrates superior nutritional content 5. The FAO and several studies highlight the nutritional potential of quinoa, particularly its ability to support lactic fermentations and the development of new products 6 thanks to its balance of essential amino acids, antioxidant content (flavonoids, polyphenols, and phytosterols), as well as its abundance of vitamins and minerals such as calcium and zinc 7. These characteristics have sparked research and innovation efforts in various fields focused on this versatile pseudocereal 8. Indeed, research and innovation efforts are evident in the cultivation of quinoa and grain, from different sectors according to the works reviewed in the Scopus database during the last 5 years, in the agricultural sector (36%), in biochemistry (9.1%), engineering (9.1%), and others to a lesser extent, mainly for crop improvement, development of new products, and evaluation of their functionality, demonstrating ample opportunities. In the field of new product development, research has been conducted on the fermentation process to enhance beneficial effects in sourdough bread-making 9 and quinoa-based beverages 10,11. It is evident that this pseudocereal can be explored and is susceptible to fermentation with lactic acid bacteria, to enhance organoleptic properties and encourage the development of gluten- and lactose-free foods 9-12, a viable alternative that improves nutritional and functional properties 3,13,14, providing added value to food preparations. Fermentation can generate bioactive peptides due to the balanced essential amino acid profile, increasing total phenolic content and antioxidant capacity 7,15,16.
Nutritional and functional properties of quinoa
Quinoa has high nutritional value due to its protein, mineral, vitamin, and carbohydrate content 17. It also contains bioactive compounds that are important components in the fermentation process. This pseudocereal has a high protein content, ranging from 12.9% to 16.5%, which is higher than some cereals (Oats: 11.6%, Rice: 7.5% and 9.1%, Corn: 10.2% and 13.4%, Wheat: 14.3% and 15.4%, Barley: 10.8% and 11%) (8,18). In terms of its essential amino acid composition, quinoa stands out for its high lysine content and a very complete amino acid profile 18,19. Most cereals are deficient in essential amino acids such as threonine, lysine, and tryptophan 20. Table 1 describes the amino acid profile of some pseudocereals, showing that quinoa has a high content of arginine (14.0 g/100 g of protein), proline (9.4 g/100 g of protein), and lysine (6.9 g/100 g of protein) compared to other pseudocereals. Furthermore, the lysine content exceeds the FAO/WHO recommended value (5.5 g/100 g of protein) 21,22. In fact, according to FAO recommendations, quinoa provides over 180% of the recommended daily intake of essential amino acids for adult nutrition 8. Its amino acid composition is considered balanced and capable of meeting human needs, and it is even comparable to the amino acid profile of milk 23. Quinoa protein is also digestible and biologically available 8,21,23.
Table 1 Composition of essential amino acids.
| Amino Acid | Quinoa | Kañiwa | Kiwicha | Amaranth |
|---|---|---|---|---|
| (g/100 g crude protein) | ||||
| Val | 4.6 | 4.2 | 3.8 | 5.1 |
| Thr | 3.9 | 3.3 | 3.3 | 4.5 |
| Ser | 4.9 | 3.9 | 5.0 | 5.6 |
| Pro | 9.4 | 3.2 | 3.4 | 4.8 |
| Methionine | 3.1 | 3.0 | 3.0 | - |
| Phe+Tyr | 8.2 | - | - | 6.6 |
| Met+Cys | 4.2 | - | - | 5.6 |
| Lys | 6.9 | 5.3 | 5.3 | 6.1 |
| Leu | 6.6 | 6.1 | 5.4 | 6.0 |
| Ile | 3.5 | 3.4 | 3.2 | 3.8 |
| His | 3.2 | 2.7 | 2.4 | 3.4 |
| Gly | 3.8 | 5.2 | 7.4 | 5.9 |
| Glx | 9.9 | 13.6 | 15.6 | 16.0 |
| Asx | 9.2 | 7.9 | 7.4 | 7.7 |
| Arg | 14.0 | 8.3 | 8.2 | 9.3 |
| Ala | 9.3 | 4.1 | 3.6 | 4.3 |
| Try | - | 0.9 | 1.1 | - |
Note: Not detected (-)
The starch content of quinoa ranges from 30 to 70% 25, with a low glycemic index generation and smaller granules. The fiber content (10%) is higher than that of some cereals, and it has a low FODMAP (fructose, fructans) content. Regarding lipid content, pseudocereals exhibit unsaturated fatty acids in higher percentages than some cereals, with lipid contents ranging from 2 to 10%, where 89.4% are unsaturated fatty acids, and 54.2 to 58.3% are polyunsaturated fatty acids 8. Vitamins are significantly higher in comparison to other typical cereals, meeting the population’s vitamin needs, such as folate and vitamin B in their natural form. Quinoa is rich in phenolic compounds (flavonoids, polyphenols, and phytosterols) with high antioxidant potential 16. However, like all grains, including pseudocereals, quinoa contains antinutrients such as phytic acid, which reduces mineral availability. Other antinutritional components present in quinoa are saponins 8.
Lactic acid fermentation
Lactic acid bacteria are gram-positive, non-spore-forming microorganisms, deficient in cytochrome and catalase-negative, aerotolerant, acid-tolerant, and strictly fermentative, producing lactic acid as the primary end metabolic product of carbohydrate fermentation 26. Eleven genera have been recognized: Carnobacterium, Enterococcus, Lactococcus, Lactobacillus, Lactosphaera, Leuconostoc, Oenococcus, Pediococcus, Streptococcus, Vagococcus, and Weissella. These genera are divided into two groups: homofermentative and heterofermentative 27. In homofermentation, one molecule of glucose is converted into two molecules of lactic acid 28. In heterofermentation, lactic acid, carbon dioxide, and ethanol are produced in equal amounts. The genera Pediococcus, Streptococcus, Lactococcus, and Vagococcus are exclusively homofermentative, while Lactobacillus can be both homofermentative and heterofermentative. The other genera are all heterofermentative 27. The kinetics of the homofermentative process depend on the culture, substrate, nutritional and/or physicochemical characteristics of the matrix, and applied pre-treatments 29,30. Some studies report that lactic acid bacteria require fermentable carbohydrates, free amino acids, peptides, and vitamins for their growth 31. The basic indicators that should be evaluated in the process are shown in Figure 1.
The intracellular pH of most microorganisms remains close to neutrality, but lactic acid fermenting bacteria can tolerate a low pH. However, only some can proliferate at pH values below 4.6 28. These microorganisms can even decrease their growth rate, achieving a stable process, which is evident when there is a decrease in metabolic activity in terms of sugar consumption and acid production 32.
In lactic acid fermentation, there is an increase in acidity, but it depends on the substrate in the medium, fermentation time, and oxygenation. Various studies report that some strains can switch from homofermentative to mixed acid fermentation due to the composition of the medium 31. Regarding the functionality of probiotics, it is considered that these microorganisms can provide health benefits when present in high concentrations of 10 8 to 109 per gram of product, as long as these viable and available 33.
Substrate for lactic acid fermentation
Suitable raw materials as substrates for fermentation must have the required physical and chemical characteristics for the growth of microorganisms 34. An important compound is water content, as its availability will determine the growth of lactic acid bacteria. Salt or sugar influence water availability, and sugars allow for the production of organic acids, B vitamins, and amino acids. It is worth noting that in homofermentations, lactic acid bacteria derive energy solely from carbohydrate fermentation, requiring enzymes such as cellulases and amylases, among others 35. Seeds have a high nutritional content necessary for germination and are primarily composed of carbohydrates, usually in the form of starch along with some free sugars. Seeds also contain minerals, vitamins, sterols, and other microbial growth factors, including lactic acid bacteria, which are selective and demanding. Therefore, seeds are suitable for fermentation if a prior treatment such as soaking or boiling in water is performed. Starch- and protein-rich seeds have been widely used to generate fermented products by yeast and lactic acid bacteria. Furthermore, very few grains are consumed directly without undergoing any processing. Examples include rice, soybeans, corn, and other seeds that are often fermented to enhance their sensory acceptance 35,36. In countries like Asia and Africa, cereals are fermented and mixed with legumes to improve protein content. Additionally, grains naturally harbor microbiota that competes for nutrients 7.
Lactic acid bacteria (LAB) can adapt to different substrates, and quinoa can be a good alternative for fermentation 7,37,38. In fact, fermentation controls the growth of pathogens, and lactic acid bacteria act as bioconservatives due to the production of metabolites such as bacteriocins, which are antibacterial organic acids 3,7,22.
Fermentation of quinoa
In accordance with the consumer trend towards functional and gluten-free foods 6,39,40, numerous studies have been conducted to evaluate the nutritional composition, functionality, technological and sensory characteristics of fermented quinoa products. This process depends on various factors such as the grains used, strains, time, temperature, and pH 11,16
As shown in Table 2, fermented quinoa doughs have been evaluated with Weissella cibaria, Weissella confusa, Leuconostoc spp., and Lactobacillus plantarum rich in exopolysaccharides 41. These microorganisms have been fermented in a mixed manner with Lactobacillus plantarum and yeasts 42, spontaneously by lactic acid bacteria and yeasts 43, with buckwheat and inoculated with Lactobacillus paracasei and Pediococcus pentosaceus 44 for use as technological improvers in bread development or to enhance the nutritional content of other gluten-free products. Some evaluated products include gluten-free bread with quinoa fermented by Lactobacillus plantarum 38 and by Lactobacillus sanfranciscensis 45, fermented quinoa beverages with Lactobacillus plantarum, Lactobacillus acidophilus, Bifidobacterium sp., Bifidobacterium longum spp. infantis, and Streptococcus thermophilus 16,46,47, fermented soy and quinoa extracts with Lactobacillus casei Bianchi et al., 50, muffins made with oat flour, corn starch, wheat flour, and quinoa sourdough inoculated with Lactobacillus plantarum 46, and fermented quinoa pasta with Lactobacillus plantarum 47.
Table 2 Studies on fermented quinoa.
| Fermentation Substrate | Strain | Results | References |
|---|---|---|---|
| Quinoa dough | Strain C20: Lactobacillus plantarum JCM1149 Strain JC5: Lactobacillus plantarum 1 | The fermentation by LAB favored obtaining gluten-free baked products, higher nutritional content than traditional bread, improvements in the textural characteristics, reducing the hardness of the product for better consumer acceptance. | 48 |
| Quinoa flour | lactobacillus plantarum ATCC 8014 | Fermentation quinoa flour leads to a sourdough nutritional enrichment and an improvement of its rheological features. The production of acids and the drop of the pH lead further to a bigger bioavailability of minerals, increasing their values at least twice. | 46 |
| Amaranth and Quinoa Flours | Weissella cibaria and Lactobacillus plantarum | The W. cibaria strain (C43-11), was able to produce a considerable amount of Exopolysaccharides (EPS) mainly in the presence of pseudocereals amaranth or quinoa and to hydrolyze proteins during fermentation. | 41 |
| Fermented quinoa beverages | Bifidobacterium sp., Lactobacillus acidophilus, and Streptococcus thermophilus | It was shown that the fermentation process significantly increased proteins and total phenolic content and antioxidation activity in the products. Sensory evaluation showed that the overall acceptability of quinoa-based fermented. | 49 |
| Extracts of quinoa and soy | L. casei | Potentially synbiotic beverage based on aqueous extracts of quinoa and soy with appropriate nutritional, rheological, and sensory characteristics. | 50 |
| Chia, quinoa and hemp seed flour | Lactobacillus sanfranciscensis W2 | Increase of firmness and porosity in sourdough for gluten-free bread. | 45 |
| Red quinoa previously crushed | Lactiplantibacillus plantarum CECT 220, Bifidobacterium longum subsp. infants CECT 4551 | in vitro gastrointestinal digestion. High concentration levels of probiotics (10 6 - 10 8 CFU/ mL) in short fermentation periods (6h). | 16 |
| Quinoa flour | Lactobacillus plantarum 299v ® (Probi Mage, Sweden). | Phytate reduction between 61.8% and 64.4%. | 51 |
| Quinoa | Lactobacillus plantarum | Significant increase in essential amino acids, free fatty acids, | 42 |
| Pasta made with quinoa sourdough | Lactobacillus plantarum CRL 1964 | Increased bioavailability of vitamins (B 2 and B 9) and minerals (Calcium, iron and Magnesium) | 47 |
| Amaranth, buckwheat and quinoa flour | lactic acid bacteria | Gluten free sourdough | 43 |
| Cooked quinoa seeds. | Lactobacillus paracasei A1 2.6 and Pediococcus pentosaceus GS.B. | Increase in phenolic compounds (Flavonoids, Lignans, phenolic acids) and tyrosols. | 44 |
| Quinoa flour | Lactic acid bacteria strains, previously isolated from quinoa: Lactobacillus plantarum, Lactobacillus rossiae, Pediococcus pentosaceus | Lactic acid bacteria produced peptides with antioxidant activity and protein hydrolysis in fermented quinoa flour. | 13 |
Effect of fermentation on the nutritional properties of quinoa products
Fermentation can lead to an increase in protein content and availability, as well as fatty acids. Quinoa has a high protein content 3,4. Table 2 shows that lactic acid fermentation allows for the development of gluten-free bread and pasta with high amino acid contents 9,47. Ceballos-González et al. 38 reported that fermentation of quinoa and wheat for the production of soft bread increased soluble protein content. In another study, the differences between protein hydrolysis and lipid production during quinoa fermentation with different strains were compared. Yeast, L. plantarum, and a combination of both for fermentation and found that different strains of microorganisms increase the protein hydrolysis index in quinoa. While yeast fermentation is more favorable for protein conversion in the pseudocereal, different types of fermentation improved the content of free fatty acids and increased functional lipids such as phospholipids. In fact, yeast is more favorable than L. plantarum in terms of improving the nutrition of fermented quinoa 42.
It is also possible to reduce and digest different antinutritional components of quinoa that cause food intolerance through fermentation 52. Ayub et al. 51, identified that fermentation of quinoa at 37°C with L. plantarum for the development of a beverage significantly reduced phytate concentration by 61.8% and 64.4% for two types of fermentation.
Probiotic microorganisms can remain viable in fermented quinoa beverages. In the study by Cerdá Bernad et al. 16, a fermented red quinoa beverage was developed, and fermentation allowed for the production of a beverage with high concentrations of functional microorganisms even after in vitro digestion. High levels of probiotics (106 to 108 CFU/mL) were found in short fermentation periods of quinoa inoculated with Lactiplantibacillus plantarum CECT 220 and Bifidobacterium longum subsp. infantis CECT 4551 after 6 hours, with high viability and functionality after gastrointestinal digestion.
Several studies have demonstrated the effect of quinoa fermentation on the bioavailability and increase of antioxidants. For example, high concentrations of phenols have been reported 13,16,53, improved bioavailability of polyphenols 54, and increased antioxidant capacity in fermented quinoa beverages 16.
Furthermore, regarding vitamins, improvements in the concentration of water-soluble vitamins have been identified. High concentrations of vitamin B have been reported, and certain strains of lactic acid bacteria (Lb. plantarum, Lactococcus rossiae, Lb. fermentum, Lactococcus buchneri, Lactococcus hilgardii, and Lb. brevis strains) have a high capacity to produce vitamin B, including riboflavin (B2), folates (B9), and cobalamin (B12) 15,55. Fermentation also increases the availability of other micronutrients such as iron, zinc, and calcium 56.
Finally, an additional nutritional property is the production of exopolysaccharides, which can have a favorable effect on human health and help prevent various diseases 34. It is worth noting that strains of the Lactobacillus genus are recognized for their production of this compound 48.
Effect of Fermentation on Technological and Sensory Characteristics of Quinoa Products
Fermentation of quinoa for the development of bread, pasta, soups, and beverages can also improve organoleptic characteristics due to the development of favorable aromas 7. The modification of starch and proteins, influenced by organic acids produced during fermentation, favor textural properties such as dough firmness and starch viscosity 38. Jagelaviciute and Cizeikiene 45, in the development of quinoa, chia, and hemp seed bread with sourdough inoculated with L. sanfranciscensis, observed that although the volume of the bread was affected by the flours used, fermented quinoa bread achieved an acceptable porosity and a decrease in hardness compared to the non-fermented control. Consumer acceptance testing also showed that fermented quinoa bread increased the overall acceptability of the bread. Rizzello et al. 13 studied the production of bread with 20% fermented quinoa sourdough, primarily fermented by L. plantarum, and their results demonstrated a final volume and crumb cell area similar to the control, with a decrease in hardness.
Furthermore, fermented quinoa with Lactobacillus spp. produces exopolysaccharides 41,53, which are important for improving food qualities in terms of rheological and functional properties, acting as natural thickeners. According to Chis et al. 46, in the development of muffins using oat flour, corn starch, wheat flour, and quinoa sourdough with spontaneous fermentation, viscous properties increased due to the possible production of exopolysaccharides, but elasticity decreased.
Conclusions
It is widely recognized that quinoa is a food with high nutritional potential due to its protein, lipid, bioactive, and vitamin content. It is a plant matrix that can be utilized in the development of various products. The review found that quinoa is susceptible to fermentation, as the nutritional content of the substrate should be rich in free amino acids, vitamins, and peptides to promote the growth of lactic acid bacteria. However, it is important to highlight that lactic acid fermentation depends on various factors that can affect the process. For instance, if the pH of the substrate is below 4.6, it would hinder the growth of certain fermenting bacteria. Additionally, the time and temperature employed are also crucial factors.
Lactic acid fermentation of quinoa for product development can enhance nutritional properties by increasing amino acids, essential fatty acids, phenols, improving the bioavailability of polyphenols, and increasing B-complex vitamins. Furthermore, it results in the production of exopolysaccharides that can enhance the techno-functional properties of the products. Ultimately, it is concluded that fermenting quinoa, whether in its seed form or different products or by-products, offers nutritional, functional, and sensory advantages. This presents an opportunity for the industry and consumers who seek gluten-free, more nutritious products that meet desired sensory characteristics.
