A review on health benefits, antimicrobial and antioxidant properties of Bambara groundnut (Vigna subterranean)

ABSTRACT Bambara groundnut (Vigna subterranean) is an African legume that belongs to the family and subfamily of Fabaceae and Faboidea, respectively. It is becoming one of the most utilized legumes after being underutilized for many years in Africa. It is the third most significant legume after groundnut (Arachis hypogaea) and cowpea (Vigna hypogea). Bambara groundnut (BGN) is a complete food because of its richness in nutritional properties such as crude fiber, iron, protein, carbohydrate, fat and minerals. Moreover, BGN possesses antioxidants properties as it contains phytochemicals, such as tannins, flavonoids and phytic acids which possess health benefits for humans such as preventing diabetes, stroke, atherosclerosis, heart disease, cancer, Alzheimer and cardiovascular diseases. In addition, these phytochemicals extend the shelf life of food products and have antimicrobial properties which can inhibit microbial growth. This paper highlights the current findings on BGN nutritional composition, health benefits, antimicrobial and antioxidant properties. Therefore, it is advisable for food industry to exploit BGN grain to its full potential to tackle challenges of food security and nutrition globally.


Introduction
Bambara groundnut (Vigna subterranean) is a legume belonging to the family and subfamily of Fabaceae and Faboidea, respectively. [1]Bambara groundnut is a legume indigenous to Africa and it is believed that its origin is between west and central Africa. [2]It grows in the wild in northern Nigeria and eastwards to southern Sudan and is currently grown across tropical Africa and to a smaller range in tropical portions of America, Asia, and Australia. [3]Bambara groundnut (BGN) is the third most significant legume after groundnut (Arachis hypogaea) and cowpea (Vigna hypogea). [4,5]It plays a crucial socio-economic impact in the semi-arid regions globally and contains sufficient protein.Therefore, if combined with some native protein sources, it could help improve the nutritional issues globally. [6,7]ambara groundnut grain is a proper healthy food due to its high iron (4.9-48 mg/100 g) and protein contents (18.0-24.0%)when compared to other legume products, with great amount of amino acids content, fiber (5.0-12%), fat (5.0-7.0%),carbohydrate (57.43-63.09%)calcium(95.8-99 mg/100 g), potassium (1144-1935 mg/100 g), and sodium (2.9-12.0mg/100 g). [7,8]Bambara groundnuts diverse nutritional composition suggests that it can meet dietary needs of people globally. [9]Its high protein content maintains a greater focus on improving procedures for processing its grains and expanding food applications. [9]16] Bambara groundnut thrives at temperatures ranging from 20 o C to 28°C and grows to maturity in three to five months.The plant is extremely versatile and can withstand extreme weather conditions than other crops.It thrives in well-drained soil and may even thrive in low-nutrient soil, with a pH range of 5.0 to 6.5.It is not susceptible to total crop failure resulting from rainfall scarcity or other unpredictable weather conditions. [17,18]Given these factors, BGN can improve malnutrition and poverty in this period of global warming and food security threats globally, particularly in places with severe water problems. [8,19]ambara groundnut variants include the red seed with huge kernels that mature late and has a high production rate.The seven types of BGN seeds from various landraces are depicted in Figure 1.The black-colored seed matures quicker than other cultivars and often has a one seed in a tiny to mediumsized kernel.The cream/brown eye produces sizable kernel.The cream/no eye has a relatively little kernels and pods, produces mostly one seed and has low productivity.The speckled or spotted variety has a strong purple color, small kernels, and primarily one-seeded pods.Finally, the brown variety contains medium to big kernels that varies in color from pale to dark brown. [21]his review focuses on health benefits, antioxidant and antimicrobial properties of BGN since it has been identified as a possible source of bioactive components.It is crucial to promote BGN so that its biologically active compounds can be used to improve health and nutrition.This is because of the growing interest and attention in plant-based nutraceutical properties for various health promotion.

Figure 1.
Seven different color types of BGN seeds: black, red, cream/black eye, cream/brown eye, cream with no eye, purple, and brown color (A to G), respectively. [20].
Consumption of foods such as BGN which is rich in flavonoids has shown to help prevent some chronic diseases and provide therapeutic effects.Bambara groundnuts components haven't been used as an ingredient in the production of nutraceuticals and functional foods despite their abundance of phytochemicals, diversity of physiologically active components, and rich nutritional profile.

Utilizations of Bambara groundnut
Legumes have long been a staple food of low-cost meals around the globe.Thus, it is important that their low levels of intake be elevated. [22,23]Plant protein contributes about 64% of the world's protein supply for human beings, with cereals accounting for 44% -50% and legumes for 10% -15%.Legumes are rich in unprocessed protein, valuable for urban and rural inhabitants, particularly in developing countries. [18]fter being picked and dried, BGN is processed and consumed in a variety of ways (Table 1).After being grilled or boiled for almost an hour, picked fresh grains are eaten as snacks. [9,31]Boiling dry grains makes them a functional food.Furthermore, after scorching or roasting, BGN can be eaten matured and consumed as a snack or as porridge. [9,32]Dry grains are hard to ground because of their stiff and closely fitting grain coats.[35] Bambara groundnut is roasted and ground in Eastern Africa, and the powder is utilized to produce relish, soup, and coffee.The powder is also utilized to make a thin or hard porridge. [36,37]Figure 2 indicates various food products produced from BGN.
Interestingly, several tribes in Africa utilize BGN as traditional remedy for various ailments.For instance, in Senegal, BGN grains are crushed and mixed with water to treat vision problems and nausea and vomiting in pregnant women in South Africa, [34] as well as nausea and diarrhea in Kenya. [38]In Ghana, white BGN grains are blended with Guinea fowl meat to treat diarrhea, whereas children with diarrhea are treated by mixing black BGN grains with water. [39]Joint pains, bone decalcification, stomach pains, sore throats and amoebic dysentery are treated by BGN in Cameroon. [39]Bambara groundnut is utilized to treat sexually transmitted infections by the Ibo people of Nigeria. [40]It aids in digestion due to its laxative qualities.It helps to breastfeed mothers to produce more milk and is given to new mothers to cure their wounds. [2,7]Kaempferol, an antioxidant found in BGN, lowers the risk of numerous longlasting diseases, including malignancy. [9,41]ble 1.Various foods products of Bambara groundnut produced in selected African countries.

Country
Product name and processing of the product References South Africa "Tshipupu" in Tshivenda-(Soup or porridge is made by boiling and stirring BGN) [24]   Nigeria "Okpa"-BGN is steamed into pudding [25] Kenya "Njugumawe"-BGN grains are soaked, then cooked with maize, crushed and fried into a stew maize [24]  Zimbabwe "Matakura"-BGN grains are boiled to prepare Matakura [26] Zambia "Ntoyo or Katoy"-BGN is ground into flour to bake bread [24,27]  Ghana "Koose"-A paste of fried BGN grains "Tubani"-BGN powder is mixed with water to make a stiff paste [8,28]   Botswana "Ditloo"-BGN is boiled and salted, and then eaten as a snack "Dikgobe"-A porridge prepared by boiled BGN grains mixed with dry maize [8,28]   Cameroon "Akara"-It is made by rolling BGN grain paste into balls and fried immediately in oil BGN grains are milled into powder, other times following roasting to prepare a porridge BGN flour is also mixed with maize flour to enrich traditional meals.[29,30]   Sudan Dried grains powder is utilized to prepare a stiff porridge [8]  Mali BGN grain powder is incorporated with sorghum or millet powder to prepare croquettes and grilled bread [8]   Tanzania Ground roasted BGN grains are roasted to prepare a soup or stiff porridge [8]   BGN = Bambara groundnut

Nutritional profile and health benefits of Bambara groundnut
The BGN grains have proteins, fat, carbohydrates, and ash (Table 2), which serve as a major source of nutrients in developing countries.Bambara groundnut is a balance food product for a nutritionally balanced diet because it has enough crude fiber, proteins, carbohydrates, fats and minerals. [46]ompared to other legumes, BGN contains high protein quality and has an excellent balance of essential amino acids such as tryptophan, lysine, valine, threonine, isoleucine, and phenylalanine, with relatively high lysine (8.5%) and methionine (6.4%). [47,48]laleke et al. [48] found 2.84% of total crude protein in cream testa BGN.Therefore, due to ongoing studies on therapeutic benefits of BGN grain and its high protein content, its consumption is expected to rise in future.Polyunsaturated fatty acid makes up most of the oil. [49]The grains of BGN contain 5.8% level of crude fat and is a source of healthy fat for low-fat diet food formulations. [50]Okpuzor et al. [51] stated that BGN is composed of polyunsaturated fatty acids (linolenic & linoleic acids) and saturated fatty acids (stearic and palmitic).
Dietary fiber in BGN decreases blood pressure and serum cholesterol and protects against cardiovascular diseases. [52]Bambara groundnut contains oligosaccharides carbohydrates such as raffinose   (0.4 g/mg) and stachyose (1.6 g/mg), which cause flatulence. [44,50]It also contains reducing sugars (3.6 g/mg).Its chemical makeup of legume starch is characterized by high amylopectin concentration, [53,54] indicating that BGN is rich in energy.BGN grains are abundant in minerals such as iron, phosphorus, potassium, magnesium, sodium and calcium as shown in Table 3.
Iron contributes to the synthesis of proteins myoglobin and hemoglobin by functioning as an oxygen transporter, thereby reducing chances of getting diseases such as anemia, physical weakness, and fatigue. [55,58]Phosphorus assists in the development of bones, proper functioning of kidneys and formation of cells.Potassium helps to adjust the human's body acid-alkaline balance. [59]Calcium is significant for blood coagulation, contraction of muscles, and the metabolic activity of certain enzymes.Magnesium activates many enzyme systems.Water-soluble vitamins, including niacin, riboflavin and thiamine is essential for carbohydrate, lipid, and protein metabolism. [51]ambara groundnut also has vitamin C (1.170.20 mg/100 g), vitamin E (3. 180.15 mg/100 g) and vitamin A (26.050.14 mg/100 g). [9,40]However, the mineral composition of BGN grains might vary depending on the variety of the grain.For example, Kaptso et al. [42] found significant difference in phosphorus content of black and white BGN flours, with the white variety having lower content (216.8 mg/100 g) than the black variety (231.9 mg/100 g).Furthermore, several studies reported significant difference of mineral composition in different BGN accessions from wide geographical areas. [55,60,61]These variations might be due to environmental factors and crop management.
Bambara groundnut grains have a lot of amino acids, which are the building blocks of protein and are molecules with amino (-NH 2 ) and carboxyl (COOH) group. [62]Amino acids are essential for metabolism, anabolism, and neuron transmission in human body.They assist in curing injury, tissue regeneration, nutrients transportation and storage, cell structuring, body strengthening and the creation of arteries. [62,63]Amino acids are divided into two groups, essential and non-essential amino acids.Bambara groundnut has a lot of essential amino acids (Table 4).Human cells cannot synthesize essential amino acids, that is why their consumption via food is critical.However, nonessential amino acids can be produced by human bodies. [66]mino acids are commonly used to complement the nutritional content of some food products.For example, lysine and methionine are not available in some grains but are present in BGN. [67,68]herefore, BGN can be utilized to complement the amino acids content of such products when introduced.Amino acids are also used as flavoring agent in food because they are sweet, salty, sour, and bitter or possess umami taste. [69]For example, BGN contains great amounts of glutamic acid (2.56 g/100 g) that can be utilized as a flavoring substance in food products. [8,62,64]Bambara groundnut is rich in lysine and glutamic acid and contains considerable quantities of phenylalanine, aspartic acid, leucine, valine, arginine, and isoleucine.

Antimicrobial activities of Bambara groundnut
[72] The section also addresses unanswered questions about bioactivity and sustainability of legume additives and compounds as anti-microbes, bioavailability, influence on microbiological cells and metabolic process and pathogenicity production. [73]Table 5 shows the ability of BGN to fight several foodborne pathogens.
Different authors have reported an increase in inhibition of gram-negative bacteria such as Klebsiella pneumonia, Klebsiella aerogenes, and Pseudomonas aeruginosa, as well as gram-positive bacteria such as Escherichia coli, Candida albicans, Staphylococcus aureus, Bacillus aureus, and Aspergillus Niger with an increase in BGN grain extracts. [16,24,72,74,75]Moreover, Udeh et al. [76] states that the anti-microbiological properties of BGN are also dependent on the concentration of the extract and the variety of the legume.The ability of BGN grains extract to inhibit microbial growth is due to polyphenols such as flavonoids, anthocyanins and tannins in the hulls of BGN grains that exhibit antimicrobiological and antioxidant potentials. [72,77]arris [24] found antibacterial action of raw BGN extract and no antibacterial action in BGN milk and yogurt extracts; possibly indicating that phytochemical concentration was lower than in a raw BGN.The author further concluded that incorporating food products with high BGN hulls can improve their antioxidant and anti-microbiological properties.Moreover, Alakali et al. [78] found an elevation of total plate count in beef patties incorporated with BGN powder for the first 14 storages days of the samples.However, after 14 days of storage to 21 days, the elevation of total plate in untreated beef patties was substantially greater than of treated patties with BGN powder.
Significant polyphenolic compounds in legumes can be found in the roots and seeds, depending on a particular product. [79]Many polyphenolic compounds in legumes have been thoroughly investigated and linked with antimicrobial activity against extensive range of microbes.Chelation of crucial micro minerals such as iron and zinc, suppression of cell surface microbiological enzymes and straight

Staphylococcus aureus Candida albicans Pseudomonas aeruginosa
Growth inhibition [24]  forward intervention in microbiological activity are processes that are widely recognized as liable for polyphenols' antimicrobial capability. [80,81]Moreover, polyphenol compounds present in BGN such as tannins and flavonoid have been reported to possess antimicrobial activities. [72,82]ntimicrobial activity has also been discovered in proteinase inhibitors found in plants, especially legumes.Plant-derived substances that protect from pests and pathogens have great prospects for application as anti-microbiological agents in products.These substances work by inhibiting enzyme activity in response to proteinases generated by phytopathogenic microbes attacking them. [83,84]itohy et al. [85] determined the impact of chickpea, broad bean, and soybean proteins extracted and esterified with methanol that they inhibited microbial development.By utilizing the agar, a concentrated-dependent suppression area was noted against gram-positive (Bacillus subtilis and Staphylococcus aureus) and gram-negative (Pseudomonas aeruginosa, and Escherichia coli) bacterial upon adding methylated proteins at concentrations between 0.1 and 10 mg/ml.Similarly, Kanatt et al. [86] found growth inhibition against Bacillus cereus, Staphylococcus aureus, Escherichia coli, and Pseudomonas fluorescens by chickpea, mung, and pigeon pea extracts at concentration of 0.05%.

Natural antioxidants of Bambara groundnut
Natural antioxidants are substances that are utilized to prevent fat oxidation from occurring, as well as to prolong shelf-life of food. [87]Moreover, natural antioxidants protect food from spoilage due to oxidation, which may lead to lipid rancidity or alterations of color in products. [88]Despite their lower efficiency, natural antioxidants are well tolerated by consumers and are safe for consumption.Moreover, other natural substances possess greater antioxidant potential compared to artificial compounds and others have beneficial impacts on processed meat sensory attributes. [89,90]ambara groundnut has natural antioxidants such as flavonoids and phenolic, as well as DPPH and ferric reducing antioxidant power (Table 6).Thus, the shelf life of products containing fats can be extended due to availability of such substances.Natural antioxidants from BGN grains also help to [ 64,112,113]   CVDs = Cardiovascular diseases maintain health. [114]Antioxidant qualities of BGN are influenced by different ways of processing, crop variant and assay methodologies.The availability of phenolic substances in the grains is responsible for these qualities.Oyeyinka et al. [90] found that antioxidant activities of BGN decrease significantly after the removal of hulls.Furthermore, Xu and Chang [114] reported that most phenolic substances which are contained in hulls are mostly accountable for antioxidant activities.The reason for this is presumable due to the uneven distribution of phenolic compounds in plants.For instance, the seed coats of grains have greater concentrations of phenolic compounds than those present in the inner portions. [115,116]Most research on antioxidant activities of BGN utilized entire grain or grains without hulls which probably lowered the levels of antioxidants tested.Therefore, extracting phenolic compounds from the grains and determining antioxidant activities is essential.Bambara groundnut contains variety of phytochemicals with different physiological active constituents; therefore BGN constituents should be utilized as an additive in the production of nutraceuticals and functional foods. [117]Dried grains are an excellent source of phenolic compounds and they can contribute to antioxidants consumption in other foods.Phenolic compounds in legumes can attach to proteins, minerals and amino acids that lack some of their electrons, therefore lowering the digestibility of crucial minerals and possibly improving the uptake of the nutrients . [118,119]Phenolic compound possess health benefits due to several biological processes by acting as free radical scavenger, reducing potential, chain breaking agent and changing of signal transduction pathways. [120]Flavonoids, often vitamin P, are a type of aromatic secondary metabolites from plants.Plants primarily utilize them to make essential pigments that are vital in forming color. [121,122]nthocyanidins, flavones, flavanols, and flavan-3-ols are among flavonoids found in BGN grains. [116]erric reducing antioxidant power (FRAP) of legumes such as BGN grains demonstrates their potential to decrease ferric ions (Fe 3+) to ferrous ions (Fe 2+ ) while changing the color from yellow to blue-green. [123,124]In general, the existence of components that disrupt the free radical chains by acting as hydrogen-donor indicates FRAP. [119]The 1,1-diphenyl-2-picryl hydrazyl radical (DPPH) of legumes is a steady nitrogen-centered free radical donor that is mostly utilized to determine the scavenging activity of plant extracts.Extracts that possess antioxidant potential to alter DPPH color from violet to yellow, due to their ability of donating electrons to a steady DPPH radical. [119,125]yeyinka et al. [16] found comparatively greater DPPH activity in maroon and black BGN grains aqueous extract, due to possibly greater amount of protic flavonoids in them than in brown BGN grains. [126]In addition, the differences in composition of the BGN grains may affect how differently the hydrogen atoms are donated to DPPH, which could be possibly account for variations in antioxidant content across varied BGN grains extract. [72]Chinnapun and Sakorn [127] discovered a new substance in BGN grains that was classified as luteolin glycoside (C 20 H 18 O 9 ), which inhibited DPPH radical in them.
However, the quantity of antioxidant properties of the same or different BGN cultivars as well as other legumes vary depending on various factors such as legume breed, soil characteristics, growing parameters and solvents used for extracting samples. [13,128]Total phenolic and flavonoid content of BGN grains are more reliant on their coat color.Therefore, the darker the seed coat, the higher its antioxidant properties and the lighter the seed coat, the lower its antioxidant properties. [96,129]For instance, Adedayo et al. [96] found higher flavonoid, phenolic and FRAP content of Black BGN variety compared to red and brown variety.Similar trends were also reported by Oyeyinka et al. [16] for maroon, black, brown, and maroon BGN grains.Furthermore, Malik and Kapoor [130] found that 70% acetone was the most effective solvent for extracting antioxidant properties of varieties of Indian lentils compared to pure methanol and 80% acetone.Similarly, Yusnawan and Kristiono [128] found that 70% acetone generated higher flavonoid and phenolic content, as well as antioxidant activity of Mungbean varieties, compared to 70% methanol and 70% ethanol.Tsamo et al. [77] found a range of total phenolic content (0.75-17.71 mg GAE/g) and total flavonoids content (0.01-2.51 mg GAE/g) in 21 BGN landraces.Since BGN grains contain considerable amount of phytochemicals, it is essential to further explore their utilization and how new processing techniques affect their phytochemical composition. [116]

Limitation of Bambara groundnut production
In underdeveloped areas, BGNs are essential part of people's diet by supplementing the shortage of protein in grains, stems, and tubers.Nevertheless, owing to the emergence of difficult to cook phenomena while storing at extreme conditions (above 26°C) and relative humidity (above 75°C) as is prevalent in African countries, limits the use of BGN. [26,131]Two mechanisms occur at those temperatures, (1) lignification (the binding among branched-chain amino acids and liberated polyphenols in the cells results in lignin production and promotes cell wall strengthening), [131,132] (2) pectin-phytase: phytase results in hydrolysis of positive charged phytate when stored, freeing bivalent charged ions.At the same time, pectin methyl esterase destroys the methyl esters of pectin, releasing liberated carboxyl group, that prefer to bind with bivalent positively charged ions.Therefore, the cell wall is solidified by the formation on non-soluble magnesium and calcium pectate compounds prevents cell detachment and weakens upon cooking. [8,132]135] Individuals in affluent areas that have energy supplies and cutting-edge technology to use grains do not consider difficult-to-cook phenomena to be problematic because they can afford various products rich in protein. [26,136]Challenging to cook BGN grains need more time (3 to 4 h) to be boiled and thus elevated heat so that they can be consumable.However, since most villagers are dependent on firewood for cooking, the longer boiling durations needed for BGN grains processing are not sustainable based on expenses and power usage.The need for fuel wood in several African areas keeps rising, rising in land usage, and cutting down of trees have limited their availability, forcing people to fetch firewood far away from their homes. [131,137]urthermore, difficult to cook BGN also display difficult to mill qualities and difficult to cook issues owing to the solid bonding among husks and cotyledons due to gums and mucilage at the interaction. [131,138]Another impediment to the utilization of this significant legume is the low production of BGN in African countries. [139,140]Lack of modern equipment for post-harvest processes such as the removal of hulls, have also led to its under-use. [141,142]Altogether, these undesirable physical features contribute to reduction in BGN utilization and reduces its application in various food products and increases its economic costs. [26,137]lutions to limitations of Bambara groundnut and future scope Difficult to cook occurrence in BGN grains can be managed by storing them at lower temperatures in refrigerators.However, individuals living in poor areas cannot access such ideal conditions. [26]urning difficult to cook BGN grains to consumable and nutrient-rich products; efficient and effective preparation methods are needed. [9,143]For instance, chemical procedures (cooking aids), biological procedures (germinating and fermenting), and physical procedures (milling, to roasting, and canning) are all utilized when processing legumes. [131]Although these procedures minimize cooking time, Annan et al. [144] found that most participants during sensory evaluation indicated that processing methods change the taste and texture of products.Due to BGN hard to cook phenomena which is a constraint for its utilization, understanding advanced science using various fourth industrial revolution technologies, including green technology is essential. [145]hus, to promote the use of BGN in areas with a shortage of resources, appropriate techniques to shorten cooking duration, conserving power and grinding qualities should be designed and deployed in local circumstances. [26]Developing and promoting of local preparation procedures that can reduce existing post-harvest costs will be essential to the wide utilization of BGN. [26,146]Those procedures should conform to the standards for competence, digestion of nutrients, and customer satisfaction requirements. [26]As a result, it is critical to learn from and improve on procedures which have proven successful in preparing difficult to cook grains. [26,147]etween 1999 and 2018 there was a decline in the production of BGN which also resulted in lessyielding cultivars and low standards grains. [140,143]Therefore, initiating studies on breeding and the advancement of cultivars with improved agricultural methods targeting to improve yields is required.In future, trials to breed cultivars would be vital to examine local techniques, appropriateness, and personal participation of farming community to permit them to suggest viable lines to satisfy their urgent needs. [26]Bambara groundnut is a climate smart plant because of thriving in different agricultural soils and varied climate conditions. [8,147]Therefore, investors, sponsors, or departments of agriculture should assist farmers with funding to plant a lot of BGN crops by increasing labor and farming equipment.To improve the utilization of BGN, food manufacturers with advanced fourth industrial revolution equipment machinery should collaborate with farmers to improve the availability of the product in the market.

Conclusion
Although BGN is an underutilized legume crop, its diverse nutritional profile demonstrates that it has the potential to satisfy dietary requirements of people, as well as fighting food insecurity and malnutrition around the globe.Its high protein content keeps a stronger emphasis on creating better methods for producing its grains and expanding food applications.From this research, it is apparent that BGN has bioactive phytochemical substances that prevent diabetes, stroke, atherosclerosis, heart disease, cancer, Alzheimer and cardiovascular diseases.Furthermore, BGN grain can be utilized in food industry as a preservative because of its antioxidant and antimicrobial properties.However, difficult-to-cook phenomena of BGN is a major constraint for its utilization, therefore, it is recommended to utilize biological and physical procedures to minimize cooking time.Furthermore, extensive research on advanced processing technologies such as high pressure processing should be explored.

Disclosure statement
No potential conflict of interest was reported by the author(s).

Table 2 .
Nutritional profile of various types of Bambara groundnut grains, flour and grain coat.

Table 4 .
Amino acids content of Bambara groundnut grains.

Table 5 .
Antimicrobial activities of Bambara groundnut grains and against crucial foodborne pathogens.

Table 6 .
Phytochemicals of Bambara groundnut grains and their health benefits.