A comprehensive review on beneficial dietary phytochemicals in common traditional Southern African leafy vegetables

Abstract Regular intake of sufficient amounts of certain dietary phytochemicals was proven to reduce the incidence of noncommunicable chronic diseases and certain infectious diseases. In addition, dietary phytochemicals were also reported to reduce the incidence of metabolic disorders such as obesity in children and adults. However, limited information is available, especially on dietary phytochemicals in the commonly available traditional leafy vegetables. Primarily, the review summarizes information on the major phytochemicals and the impact of geographical location, genotype, agronomy practices, postharvest storage, and processing of common traditional leafy vegetables. The review also briefly discusses the bioavailability and accessibility of major phytochemicals, common antinutritive compounds of the selected vegetables, and recently developed traditional leafy vegetable‐based food products for dietary diversification to improve the balanced diet for the consumers. The potential exists for better use of traditional leafy vegetables to sustain food security and to improve the health and well‐being of humans.

Moringa oleifera, belonging to the family moringaceae, is another popular traditional vegetable in the Southern African region.
It has been identified as a sustainable crop to fight food insecurity (Tshetlhane, 2016 is similar to that of orange, eggplant, spinach, red cabbage, and peanuts which is remarkably lower than levels noted in cereals (Leone et al., 2015). The, salicylic acid concentration in M. oleifera leaves was similar to the levels found in some commercial fruits and vegetables such as nectarine, pineapple, tomato, and asparagus (Leone et al., 2015). Presence of different isomers of chlorogenic acid [3acyl, 4-acyl, and 5-acyl p-coumaroylquinic (pCoQA), caffeoylquinic (CQA), and feruloylquinic acids (FQA), a single isomer of 3,5-diCQA, 3-CQA-glycoside, and two regional isomers of the (3′ and 4′) glycosides of 4-CQA] was reported in M. ovalifolia leaves obtained from Namibia, in the southern region of Africa (Makita et al., 2017).

| Carotenoids
Amaranthus hybridus leaf contains 1136 mg/kg total carotenoids and 184 mg/kg β-carotene Ibrahim et al. (2015), and the composition was comparable to baby spinach (Bergquist, 2006). It is also well known that β-carotene is a precursor for vitamin A and it shows higher antioxidant properties which provide protection against free radical attack and thereby reducing the incidence of cataracts and cardiovascular disease, enhancing the immune response, and reducing the risk of degenerative diseases such as cancer and muscular, degenerative diseases (Krinsky, 1993 Spider flower, which includes Cleome gynandra, C. monophylla and C. hirta, (Capparaceae family), is also a commonly consumed traditional vegetable in the southern African region (Jansen van Rensburg et al., 2007). Cleome hirta, a commonly consumed leafy vegetable in Zimbabwe (Codd, Kers, Killick, Tölken, & Marsh, 1970), contains 131.705 mg/kg DW of β-carotene (Agea et al., 2014).
Corchorus trilocularis L, known as the member of Jew's mallow (Tiliaceae family) (Jansen van Rensburg et al., 2007), was reported to contain 54.43 mg/kg Dw (Agea et al., 2014). Jew's mallow is commonly consumed by the African communities from Limpopo, Gauteng, and Mpumalanga provinces in South Africa.
Moringa leaves are also recommended as a higher source of β-carotene, and the content of β-carotene in moringa leaves was higher than in orange, carrots, and melon, which are known as the primary vegetable sources of β-carotene (Leone et al., 2015).
Cowpea leaves are a rich source of source of β-carotene, and it contributes to 22.55% of the total carotenoid content and lutein contributes only 4.14% to the total carotenoid content (Mduma, 2010).
Furthermore, the total carotenoid content in Brassica rapa subsp.

| Glucosinolates
Glucosinolates are also secondary plant metabolites and popular in the food industry because of their health benefits owing to their antioxidant, antimicrobial, and nutraceutical properties (Förster, Ulrichs, older leaves showed 3 mg/g DW, which showed the glucosinolate content declined with increasing leaf maturity (Bennett et al., 2003).
However, no detailed reports of the glucosinolate profile in B. rapa chinensis grown in South Africa are available.

| IMPAC T OF G EOG R APHI C AL LO C ATI ON , G ENOT YPE , AND AG RONOMY PR AC TI CE S ON D IE TARY PHY TOCHEMIC AL S
Geographical locations, environmental factors, and agronomic practices can affect the composition and the content of phytochemicals in fresh produce (Tiwari & Cummins, 2013 (Leone et al., 2015). The said authors commented that the β carotene content of moringa leaves obtained from Chad and Algeria was similar to the levels found in South African moringa leaves, but the concentrations were lower than that noted in the leaves from India. Also, a comparative study conducted by Ndhlala et al. (2014) clearly demonstrated that the total phenolic and flavonoid content of moringa cultivars grown in different geographical regions contained differ between the locations. Cultivars obtained from Thailand (TOT5169) and South Africa (Silver Hill (SH)) showed higher total phenolic content of approximately 1500 mg/kg based on dry weight. It is also noteworthy that the variation in total phenolic content between the cultivars Silver Hill South Africa and Limpopo. Cultivar Limpopo showed significantly lower total phenolic content than the cv. Silver Hill (Ndhlala et al., 2014). Based on the investigations conducted by Ndhlala et al. (2014), Thailand cultivars TOT4100; TOT4951 and cv.
Limpopo from South Africa showed higher flavonoid catechin content around 40 mg/kg. The antioxidant scavenging activity was also noted to vary among the cultivars investigated, and cv. CHM Silver Hill (South Africa) showed the highest activity (32.56 EC50 (μg/ml)) (Ndhlala et al., 2014). However, the correlation between the antioxidant activity and the phytochemical components in moringa cultivars needs to be established.
The phytochemical composition can also vary with a genotype and between different accessions (Kebwaro, 2013). Considering the total phenolic compounds in five spider plant (C. gynandra) accessions, it was evident that UGSF accession contained higher total phenol content (14,070 mg/kg) and quercetin (37,090 mg/kg) (Kebwaro, 2013). Furthermore, the maturity stages after plating or the related flowering stage also influenced the phytochemical content in traditional vegetables (Kebwaro, 2013). Rutin content differed among amaranth species at the stage of blossoming (Kalinova & Dadakova, 2009;Martirosyan, 2001). Light quality such as higher UV-B radiation can also favor the accumulation of rutin and rutin glucosidase in plants (Suzuki, Honda, & Mukasa, 2005). The concentrations of flavonol, quercetin, kaempferol, and isorhamnetin between the varieties of Cowpea leaves varied remarkably (Mduma, 2010). Variety Dakawa contained higher amounts of quercetin (654.8 mg/kg) compared with var. Ex-Iseke (585.8 mg/kg) (Mduma, 2010). Also the concentrations of kaempferol (224.5 mg/kg) and isorhamnetin (117.8 mg/kg) were higher in var. Ex-Iseke than in var. Dakawa (Mduma, 2010). to southern Namibia and in southwestern Angola (Ananias, 2015;Dyer, 1975). In Namibia, M. ovalifolia leaves obtained from two sites showed a higher total phenolic content (Okaukuejo 168681.6 mg/ kg and Tsumeb 151088.5 mg/kg) on a dry weight basis and antioxidant reducing power (Ananias, 2015). According to the reports of Ananias (2015) (Saini, Sivanesan, & Keum, 2016) than the African indigenous moringa (Coppin, Xu, Chen, & Wu, 2013). It is also noteworthy that the flavone, apigenin, was identified in major moringa cultivars of M. oleifera from Pakistan (Saini et al., 2016 (Kebwaro, 2013). Moreover, the organic farming improves the glucosinolates and phenolics in the plant parts compared to the inorganic farming mainly due to the "stimulation of biotic stress" (Francisco et al., 2016). Also, based on several reports, it is evident that low N application rate favors the accumulation of total phenolic and flavonoid contents in crops (Stefanelli, Goodwin, & Jones, 2010;Zhu, Lin, Jin, Zhang, & Fang, 2009). Francisco et al. (2016), using the hypothesis of Bryant, Chapin, and Klein (1983) in their review, explained that lower availability of N causes lower N uptake by the crop and inhibits the production of N-based secondary metabolites (e.g., alkaloids) and thereby increases the availability of carbon that can be used for the flavonoid biosynthesis.

| EFFEC T OF P OS THARVE S T S TOR AG E AND PRO CE SS ING OPER ATI ON ON PHY TOCHEMIC AL S IN TR ADITIONAL LE AF Y VEG E TAB LE S
Recently, Amaranth spp. Brassica rapa subsp. chinensis have become popular at formal markets and supermarkets as ethnic commodities.
Bi-orientated polypropylene packaging containing 4.3% O 2 and 7.3% CO 2 A. cruentus, 5.6% O 2 and 6.7% CO 2 for S. reflexum, and 2% O 2 and 7% CO 2 for B. rapa subsp. Chinensis helped to retain the phytochemicals (total phenols and flavonoids) at the market shelf temperature 10°C (Mampholo et al., 2013(Mampholo et al., , 2015. The packaging at the low temperature at the market shelf significantly extended the shelf life up to 8 days for A. cruentus and up to 10 days for B. chinensis and S. reflexum (Mampholo et al., 2013(Mampholo et al., , 2015. It is well known that cooking practices (thermal processes) can affect polyphenols by oxidation in traditional leafy vegetables (Kebwaro, 2013). The changes in phytochemical composition during thermal processing greatly depend on the temperature and duration (time) (Kebwaro, 2013). Cleome gynandra leaves boiled for 15 min in water retained 71.42% flavonoids, 37.62% total phenolic compounds, and 51.05% tannin (an antinutritive compound) (Kebwaro, 2013).
Drying is the most common method adopted in food preservation to store traditional leafy vegetables, and sun drying is a popular method used by the rural communities (Mduma, 2010). Exposure of the leafy vegetable to direct sunlight can favor rapid degradation of β-carotene. Therefore, solar dryers are recommended so that the vegetables can be dried in solar cabinets (Mduma, 2010).

Higher levels of carotenoids were lost in amaranthus and cowpea
leaves during the open sun-drying process compared to solar drying (Svanberg, 2007). The direct sun-drying method was reported to result in 58% loss of β-carotene in cowpea leaves (Ndawula, Kabasa, & Byaruhanga, 2004). However, solar drying improved the retention β carotene in amaranth, cassava, and pumpkin leaves compared to the amount retained after direct sun drying (Mduma, 2010). The oxidation process of β carotene by the enzymes peroxidase and lipoxygenase (Gökmen, 2010) continues during the drying process, unlike in blanching (Gökmen, 2010;Mduma, 2010). Use of antioxidants such as ascorbic acid could improve the retention of β-carotene during drying. Also, the solar dryer reduced the drying time by 50% and improved the color, texture, and nutritional properties and could be adopted to preserve the β-carotene in traditional leafy vegetables (Bala, Mondol, Biswas, Chowdury, & Janjal, 2003;Mduma, 2010).  (Potisate et al., 2015).
Blanching is a beneficial process in food processing that inactivates enzymes (peroxidase and lipoxygenase) that are involved in carotenoid destruction through oxidation (Mduma, 2010). Blanching enabled the retention of 15% of β-carotene in cowpea leaves (Ndawula et al., 2004). The canning process involves a higher temperature (100 • C) and longer duration (1 h), and it was reported to convert 75% of transβ-carotene to 13 or 9 isomers that are not absorbed by the body (Van het Hof, Gärtner, West, & Tijburg, 1998).

The aforesaid authors indicated that mild heating such as steam-
ing was demonstrated to improve the extractability of β-carotene from vegetables as well as its bioavailability. Dehydration of leafy vegetables also favors the loss of β-carotene mainly by increasing the surface area (Mduma, 2010). Extensive cutting or chopping or grinding also favors the destruction of β-carotene and polyphenols in vegetables (Abid, Jabbar, & Wu, 2013), therefore blanching prior to the cutting or chopping process (Bohn, 2014).
Using sunflower oil or red palm oil during cooking improved the accessibility of β-carotene content by 39-94% of traditional vegetables such as amaranth, sweet potato, pumpkin, and cassava leaves (Hedren, Mulokozi, & Svanberg, 2002). It was also reported that generally leaves are subjected to a drying process prior to cooking and β-carotene decreased to 19.4% during drying (Ndawula et al., 2004). However, Medoua and Oldewage-Theron (2014) found that a 25-min cooking process with water to just cover the leaves decreased the total polyphenols to 58.33%, myricetin to 51.97%, and kaempferol to 40.86%, while among the three flavonols, quercetin was least affected (25.44% reduction). In order to improve the intake of moringa, Kiranawati and Nurjanah (2014) had developed moringa noodles. The sautéing cooked (cooking quickly in a minimal amount of fat over relatively high heat) moringa noodles improved the milk production in rats (Kiranawati & Nurjanah, 2014).

| B I OAVAIL AB ILIT Y OF D IE TARY PHY TOCHEMIC AL S
The beneficial effect of dietary phytochemicals depends on their bioavailability (absorption, distribution, metabolism, and excretion) which is mainly dependent on the structure of the phytochemical and food matrix. Furthermore, the term bioavailability can be defined according to Thilakarathna and Rupasinghe (2013) as the rate of absorption and the availability at the site of action is very important for a bioactive compound to be effective within biological systems and thus be "bioavailable." Based on this explanation, it is clear that the concentration of the compound and its metabolites at the site of action is more important than the concentration of a dietary phenolic compound in a particular food. Scalbert and Williamson (2000) and Thilakarathna and Rupasinghe (2013), in their reviews, reported that factors such as "class of phenolic compounds, complex structures of phenolic compounds, degree of polymerization and molecular weights, glycosylation, metabolic conversion process and interaction with colonic microflora" affect the bioavailability of the dietary phenolic compounds. As mentioned, recent research has focused on the impact of dietary polyphenols on the gut microbiota composition and the effect of gut microbiota on the biotransformation of phenolic compounds, their bioavailability, and human health (Ozdal et al., 2016). Flavanones showed higher bioavailability than flavonols and flavan-3-ols mainly due to the lesser degradation by the gut microflora and the greater bio-accessibility for intestinal absorption (Ozdal et al., 2016). Furthermore, the bioavailability of catechins (tea) was improved by supplementation with steamed rice.
Higher amounts of proline-rich proteins in the rice endosperm bind with the epigallocatechingallate and epicatechin gallate and convert them to nongallated catechins in the small intestines (Monobe, Ema, Tokuda, & Maeda-Yamamoto, 2011). The authors also mentioned in their research findings that the nongallated catechins are more readily absorbed than the gallated catechins. In some cases, the heating process can break the plant cell walls and thereby mediate the release of polyphenols during digestion (Bohn, 2014). Cutting and grinding of blanched vegetables can increase the bio-accessibility of polyphenols by increasing the surface area for the activity of the digestive enzymes (Abid et al., 2013). Bio-accessibility can be defined as the fraction of a compound that is available for the absorption by the gut (Alminger et al., 2014). Domestic cooking influences the bioavailability of naringenin, and chlorogenic acid increased amounts of theses phenolic compounds in human blood plasma compared to the consumption of fresh cherry tomatoes (Bugianesi, Salucci, Leonardi, & Maiani, 2005). However, higher temperature and processing time can negatively affect the naringenin and chlorogenic acid concentration in the vegetables (Bugianesi et al., 2005).
Bioavailability of quercetin is affected by the differences in its conjugated glycosides, but higher bioavailability of quercetin can be obtained from quercetin glucoside than quercetin rhamnoside and quercetin galactoside (Kasikci & Bagdatlioglu, 2016). Furthermore, quercetin bioavailability can be improved when quercetin is consumed as a cereal bar ingredient instead of a capsule (Egert et al., 2012). The authors explained that the manufacturing process helps to improve the homogeneous solid dispersion of quercetin in the presence of the ingredients of a cereal bar. Also, the presence of dietary fat (Kasikci & Bagdatlioglu, 2016;Lesser, Cermak, & Wolffram, 2004) and fructooligosaccharide (Matsukawa et al., 2009) in the food matrix was demonstrated to improve the bioavailability of quercetin.
The novel nano-encapsulation technology (Hu, Liu, Zhang, & Zeng, 2017), on the one hand, has been demonstrated to increase the bioavailability and to improve the interaction of polyphenols with the food matrix during digestion, especially by improving their solubility.
On the other hand, bioavailability of β-carotenes can be improved by a food processing method and pureed; thermally processed spinach was shown to influence the blood plasma response of β-carotene During freezing of B. rapa subsp. chinensis, typical blanching protocols are recommended prior to freezing in order to inactivate the myrosinase enzyme and thereby reducing the bioavailability of isothiocyanates. Myrosinase is heat sensitive (thermolabile) and denatures at 60 C for 10 min (Francisco et al., 2016;Van Eylen, Oey, Hendrickx, & Van Loey, 2007). Furthermore, food preparation methods such as chopping and grinding can affect the glucosinolate content due to the tissue damage-induced myrosinase activity that results in the production of isothiocyanates (Francisco et al., 2016).
Steaming for 15 min was shown to retain the glucosinolates to a great extent in brassica vegetables (Francisco et al., 2010).

| DE VELOPMENT OF FOOD PRODUC TS WITH TR ADITIONAL LE AF Y VEG E TAB LE S FOR D IE TARY D IVER S IFIC ATI ON
Nestlé included morogo (Amaranth) leaf to flavor their new line of Maggi two-minute noodles (Greve, 2015). Moringa dried leaf was used to fortify the noodles to improve the iron and dietary phytochemicals. Similarly, "moringa fortification was adopted to increase the nutrient level in children and incorporation of 20% moringa powder in cocoa powder" (Gopalakrishnan, Doriya, & Santhosh Kumar, 2016). Different percentages of moringa leaf powder tested in the chocolate fortification indicated that 20% moringa incorporation in cocoa powder was ideal (Gopalakrishnan et al., 2016). The addition of moringa powder to cocoa during chocolate production can help to reduce childhood obesity (Morsy, Mohamed Rayan, & Youssef, 2015). The said authors also demonstrated the production of rice extrudate products containing 2% Jew's mallow (C. olitorius L. Leaves) dried leaves for healthy snack food production. Production of health beverages including moringa leaf as an ingredient with beetroot leaves was also reported (Vanajakshi, Vijayendra, Varadaraj, Venkateswaran, & Agrawal, 2015). The authors demonstrated the fermented moringa leaves in a beetroot-based beverage containing 1:2 moringa leaf paste and beetroot showed 20.79% radical scavenging activity with a phenolic content of 5 mg/ml and 30-day shelf life at 4°C with a good viable lactic population at 6.5 pH.

| ANTIN UTRITIVE COMP OUNDS IN TR ADITIONAL LE AF Y VEG E TAB LE S
It is clearly evident, based on several research reports, that the traditional leafy vegetables contain non-nutrient or antinutrient bioactive phytochemicals. Some of these phytochemicals were found to pose some toxicity when consumed in large quantities or over a long period (Smith & Eyzaguirre, 2005).
Ascorbic acid favors the optimal acidic conditions, especially in the stomach and intestines for the absorption of iron and also acts as a chelating agent of ferric iron so that it is stable and in a soluble form, even at a higher pH (Bohn et al., 2008;Teucher et al., 2015). Also, ascorbic acid prevents the reduction in ferric iron to ferrous and the precipitation of ferric hydroxide (Bohn et al., 2008;Teucher et al., 2015). Conventional cooking of vegetables can reduce the phytic acid to some extent; however, methods such as soaking in an acid medium, lactic acid fermentation, and sprouting can help to reduce the phytic acid concentration (Bohn et al., 2008). Use of phytase enzymes can be recommended during food processing to reduce the phytate content; however, production of thermally stable phytase needs to be cost-effective and an efficient process for the food industry (Bohn et al., 2008).
Tannin is a group of phenolic compounds responsible for the astringent (bitter mouthfeel) sensory attribute (Egbuna & Chieneye, 2015). Tannin binds and precipitates proteins, amino acids, and alkaloids and thereby reduces their bioavailability (Egbuna & Chieneye, 2015). Tannin content in Amaranthus spp is higher around 157 mg/ kg, but in A. cruentus it is around 7.6 mg/kg, which explains the preferred traditional food preference of A. cruentus by the consumers.
Tannin content in C. gynandra (spider plant) from Zimbabwe, on the one hand, was reported to contain 190 mg/kg, and it is comparable to the amount found in commonly consumed lettuce (Chipurura, 2010). On the other hand, the different genotypes of C. gynandra, such as CGSKGP (Seke District, Zimbabwe), CGMRR (Marondera, Zimbabwe), and CGSKP (Seke District, Zimbabwe), had lower tannin content than the amounts (Chipurura, 2010). The tannin content between these genotypes varied from 230 to 490 mg/kg (Chipurura, 2010). However, A. hybridus contains 0.60 mg/kg oxalate, 4.12 mg/ kg phytate, and 0.20-0.19 mg/kg tannin (Agbaire, 2012). Some reports sates tannin or saponin were not detected in Amaranthus spp (Uusiku et al., 2010;). The difference in non-nutritive components can also vary according to geographical location, soil nutritional components, and abiotic stress experienced by the plants. Common antinutritive compounds are summarized in Table 4.

| CON CLUS ION
The review reemphasizes that the inclusion of traditional vegetables in a regular diet could provide many health benefits. However, it is evident that there is a significant knowledge gap in the quantifica- Generally, traditional vegetables are sold at the urban markets; therefore, the highly perishable nature of these vegetables affects their marketing. Therefore, adapting appropriate postharvest handling methodologies and the use of appropriate packaging are recommended to reduce the postharvest loss of freshly harvested traditional leafy vegetables in order to retain the dietary phytochemicals at the retailer's shelf during marketing. As boiling was recommended for the retention of phytochemicals and for the removal of antinutritive compounds, the vegetables need to be marketed in fresh form. It is also important to identify the harvestable maturity, cost-effective methods to enhance shelf life, and appropriate packaging for the traditional leafy vegetables. When developing new value-added processes for functional food products, it is also important to assess the loss of dietary phytochemicals.
Overall, it is important to promote the consumption of traditional leafy vegetables that possess a wide variety of health-promoting phytochemicals. Tremendous potential exists to establish improved crop production and food manufacturing practices to optimize the phytochemicals and introduce vegetable-based functional foods that could combat diseases and obesity while sustaining food security in the southern African region.

ACK N OWLED G M ENT
The authors wish to acknowledge the National Research Foundation grant (grant number 98352) for Phytochemical Food Network to Improve Nutritional Quality for Consumers.

CO N FLI C T O F I NTE R E S T
The authors declare that they have no conflict of interest.