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Introduction
Moringa oleifera Lam. is native to the Himalayas (Sanjay & Dwivedi, 2015). As an edible species it was introduced into the Americas in the nineteentd century (Falasca & Bernabé, 2008), or perhaps in colonial times from the Philippines by seamen crewing the so-called Nao de China route between Manila and Acapulco (Olson & Fahey, 2011). It is one of the 13 identified species of the family Moringaceae, belonging to the genus Moringa. It is identified by its pinnate leaves and long, woody pod, which when mature opens into three valves which contain the seeds with three wings (Olson & Fahey, 2011). This plant is consumed as food for its nutritional value, and according to Ayurvedic medicine (Singh, 2012a) it is attributed with properties for the treatment of certain ailments such as asthma, epilepsy, eye and skin diseases, fever and hemorrhoids (Sanjay & Dwivedy, 2015). The seed is used to treat river water with suspended solids and groundwater (Aziz, Jayasuriya, & Fan, 2015; Lijesh & Malhotra, 2016; Sasikala & Mutdurama, 2015), and as a source of oil for biodiesel production (Mofijur et al., 2014; Rahman et al., 2014; Sharma, Rashid, Anwar, & Erhan, 2009).
In moringa, proteins, fiber, carbohydrates, amino acids, vitamins, minerals (Amaglo et al., 2010; Asiedu-Gyekye, Frimpong-Manso, Awortwe, Antwi, & Nyarko, 2014), secondary metabolites (carotenes and tocopherols) (Amaglo et al., 2010; Cheehpracha et al., 2010) and some minor metabolites (Föster, Ulrich, Schreiner, Müller, & Mewis, 2015) have been identified; this indicates that it can be raw material for the food, balanced animal feed and cosmetics industries (Aney, Rashmi, Maushumi, & Kiran, 2009).
Therefore, the aim of this review was to analyze the scientific information on Moringa oleifera Lam. in terms of its distribution, botanical and agronomic characterization, chemical composition, pharmacological characteristics and medicinal, agro-industrial, biofuel and water treatment uses, which allow supporting the various properties attributed to it.
Taxonomy and botanical characteristics
Moringa oleifera (Familia Moringaceae) is one of 13 species of the genus Moringa. It is identified by the fruit in the form of a long, woody pod, which when mature opens into three valves and contains tri-valve seeds with longitudinal wings. Its pinnate leaves are divided into leaflets arranged on a rachis. The flowers are zygomorphic with five petals, five sepals, five functional stamens and several staminodes; they have pedicels and axillary inflorescences. The plant has erect stems and tuberous roots (Olson, 2010; Olson & Fahey, 2011). The tree can reach up to 10 m in height (Paliwal, Sharma, & Pracheta, 2011).
Geographic origin and distribution
Moringa oleifera is originally from the Himalayas (Kumar, 2013; Sanjay & Dwivedi, 2015), and is native to India, Pakistan, Bangladesh and Afghanistan (Fahey, 2005). Its distribution has spread to Southeast Asia, Western Asia, the Arabian Peninsula, East and West Africa and islands in the Indian and Pacific oceans. In the Americas it is found from southern Florida (USA) to Argentina, and on the islands of the Caribbean and West Indies (Olson, 2010; Paliwal et al., 2011). In Mexico it is found on the Pacific coast from Baja California and Sonora to Chiapas (Olson & Fahey, 2011). Recently, Olson and Fahey (2011) reported the introduction of this plant into the Americas, as an edible species, from the Philippines by the crews of the Nao de China; however, Falasca and Bernabé (2008) argue that it arrived during the nineteentd century.
Agronomic characteristics
M. oleifera grows in tropical areas (in low-altitude places, < 2000 masl) and in different types of soil (clayey and sandy), except in poorly-drained ones. It is a plant that tolerates drought conditions, but water stress (minimum annual rainfall of 250 mm) affects its growtd (Dubey, Dora, Kumar, & Gulsan, 2013). It is propagated by seed and stake (Nouman et al, 2014); peeling is not necessary for the seeds to germinate (Padilla, Fraga, & Suárez, 2012).
Due to its composition and climatic conditions, the plant is affected by various pests (ants, zoompopos and Fusarium species) (Padilla et al., 2012). On the other hand, the application of nitrogen fertilizers to the plant increases its biomass production (Mendieta, Spörndly, Reyes, Salmerón, & Halling, 2012), and biofertilizers improve its ability to metabolize nutrients and increase its growtd (Zayed, 2012).
The geographical area and growing season influence the synthesis and concentration of metabolites due to soil type, climate, fertilization and water availability (Iqbal & Bhager, 2006; Anwar & Rashid, 2007; Melesse, Steingass, Boguhn, Schollenberger, & Rodehutscord, 2012; Dubey et al., 2013; Föster et al., 2015). In this regard, further studies need to be conducted to generate production technology for moringa, where agronomic management and evaluation of the quality of the product (leaf, stem, root and seed) are included.
Chemical composition
Nutritional
In Asia, the leaf, fresh pod (fruit) and seed of M. oleifera are consumed, and the root is used as a condiment (Omotesho et al., 2013). Table 1 shows the nutritional content with variations attributable to the collection areas. Proteins, fiber, carbohydrates, amino acids, vitamins, carotenes, tocopherols and minerals (Tables 2 and 3) have been identified in the plant, and, as can be seen, the most abundant element is potassium (Abbas, 2013; Abdull, Ibrahim, & Kntayya, 2014; Amaglo et al., 2010; Asiedu-Gyekye et al., 2014; Ayerza, 2012; Dhakar et al., 2011; Sanjay & Dwivedy, 2015; Yameogo, Bengaly, Savadogo, Nikiema, & Traore, 2011). The oil obtained from the seeds is nutritionally valuable and suitable for frying due to its stability and high oleic acid content. In the leaf, linoleic acid is the most abundant acid, while in the rest of the plant it is palmitic acid (Table 4) (Sabo-Mohamed, Long, Lai, Syed-Muhammad, & Mohd- Ghazali, 2007) and omega 3 and 6 acids (Ayerza, 2012). Mmoringa has been recommended by the United Nations (UN) to supplement the human diet (Ashwortd & Ferguson, 2008). Some studies show that intake is safe at up to 1 g∙kg-1 b. wt. (Asare et al., 2012).
Table 1 Nutritional content of the parts of Moringa oleifera Lam.
| Leaf f2 | Leaf d2 | LeAf d4 | Leaf d1 | Leaf d3 | Seed husk1 | Seed p1 | Wings1 | Stem4 | Pod2 | |
|---|---|---|---|---|---|---|---|---|---|---|
| Moisture % | 75.00 | 7.50 | 79.20 | -- | -- | -- | -- | -- | -- | 86.90 |
| Calories in 100 g | 92.00 | 205.00 | -- | -- | -- | -- | -- | -- | -- | 26.00 |
| Protein (g) | 0.07 | 0.27 | -- | 0.26 | 0.44 | 0.10 | 0.37 | 0.07 | 0.06 | 0.03 |
| Fat (g) | 0.02 | 0.02 | -- | nd | 0.01 | 0.02 | 0.42 | nd | nd | 0.00 |
| Carbohydrates (g) | 0.13 | 0.38 | -- | -- | -- | -- | -- | -- | -- | 0.04 |
| Fiber (g) | 0.01 | 0.19 | -- | -- | -- | -- | -- | -- | -- | 0.05 |
| Ash (mg∙g-1) | -- | -- | -- | 0.09 | 0.10 | 0.02 | 0.03 | 0.09 | 0.07 | -- |
| Minerals (g) | 0.02 | -- | -- | -- | -- | -- | -- | -- | -- | 0.02 |
| Total phenols (mg∙g-1) | -- | -- | -- | -- | 34.00 | -- | -- | -- | -- | -- |
| Tannins (mg∙g-1) | -- | -- | -- | -- | 14.00 | -- | -- | -- | -- | -- |
| Saponinas (mg∙g-1) | -- | -- | -- | -- | 50.00 | -- | -- | -- | -- | -- |
| Phytates (mg∙g-1) | -- | -- | -- | -- | 31.00 | -- | -- | -- | -- | -- |
| Raw energy (MJ∙kg-1) | -- | -- | -- | 19.35 | 17.70 | 21.62 | 26.68 | 18.52 | 18.95 | -- |
| Carotene (vit. A) (mg) | 0.07 | 0.19 | 1.93 | -- | -- | -- | -- | -- | -- | -- |
| β-carotene (mg) | -- | 0.93 | -- | -- | -- | -- | -- | -- | -- | |
| Thiamine (B1) (mg) | 0.00 | 0.00 | -- | -- | -- | -- | -- | -- | -- | -- |
| Riboflavin (B2) (mg) | 0.00 | 0.21 | -- | -- | -- | -- | -- | -- | -- | -- |
| Niacin (B3) (mg) | 0.01 | 0.08 | -- | -- | -- | -- | -- | -- | -- | -- |
| Vitamin C (mg) | 2.20 | 0.17 | -- | -- | -- | -- | -- | -- | -- | -- |
| Ascorbic acid (mg) | -- | -- | 6.60 | -- | -- | -- | -- | -- | -- | -- |
nd = not detected; d = dehydrated; f = fresh; p = peeled; ext = extracted
1Abbas (2013); 2Dhakar et al. (2011); 3Makkar and Becker (1996); 4Nambiar and Seshadri (2001)
Table 2 Elements in different parts of Moringa oleifera Lam.
| Element | Leaf f4 | Leaf d4 | Leaf d6 | Leaf d3 | Leaf d5 | Pod4 | Pod p.j.2 | Pod2 | Flower2 | Petioles f.p.2 | Seed w/h2 | Seed p2 | Seed1 | Stem2 | Stem f.p.2 | Root2 |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Calcium | 4.400 | 20.03 | 22.40 | - | 0.019 | 0.300 | 0.100 | 0.180 | 0.170 | 0.270 | 0.720 | 0.120 | 0.143 | 0.340 | 0.180 | 0.300 |
| Manganese | 0.420 | 3.680 | - | - | 0.062 | 0.240 | - | - | - | - | 1.700 | 0.290 | 3.00x10-3 | - | - | - |
| Phosphorous | 0.700 | 2.040 | 6.300 | - | 2.500 | 1.100 | - | - | - | - | - | - | - | - | - | - |
| Potassium | 2.590 | 13.24 | - | - | 17.70 | 0.240 | 2.740 | 4.450 | 3.510 | 2.510 | 1.710 | 1.100 | 2.550 | 4.420 | 1.970 | 2.050 |
| Copper | 0.007 | 0.006 | - | 0.032 | 0.009 | 0.031 | - | - | - | - | - | - | 1.23x10-3 | - | - | - |
| Iron | 0.009 | 0.282 | 0.260 | - | 0.226 | 0.053 | - | - | - | - | - | - | 1.11x10-2 | - | - | - |
| Sulfur | 1.370 | 8.700 | - | - | - | 1.370 | - | - | - | - | - | - | - | - | - | - |
| Selenium | - | - | - | - | 0.027 | - | - | - | - | - | 0.000 | - | 4.97x10-4 | - | - | - |
| Sodium | - | - | - | - | 1.620 | - | 0.290 | 0.860 | <0.1 | <0.1 | 1.410 | 0.940 | 1.340 | 0.480 | - | < 0.1 |
| Litdium | - | - | - | - | - | - | - | - | - | - | - | - | 6.62x10-6 | - | - | - |
| Magnesium | - | - | - | - | 4.340 | - | - | - | - | - | - | - | 1.500 | - | - | - |
| Chrome | - | - | - | 0.578 | <0.005 | - | - | - | - | - | - | - | 2.65x10-4 | - | - | - |
| Nickel | - | - | - | - | - | - | - | - | - | - | - | - | 0.25x10-4 | - | - | - |
| Zinc | 0.002 | 0.033 | - | 0.116 | <0.005 | - | - | - | - | - | - | - | 1.10x10-2 | - | - | - |
| Rubidium | - | - | - | 0.076 | - | - | - | - | - | - | - | - | 5.43x10-4 | - | - | - |
| Strontium | - | - | - | - | - | - | - | - | - | - | - | - | 1.53x10-3 | - | - | - |
| Lead | - | - | - | 0.004 | - | - | - | - | - | - | - | - | 0.06x10-5 | - | - | - |
| Thorium | - | - | - | 0.003 | - | - | - | - | - | - | - | - | - | - | - | |
| Barium | - | - | - | 0.890 | - | - | - | - | - | - | - | - | 3.59x10-4 | - | - | - |
f=fresh;d = dehydrated; f.p. = flowering plant; i.p. = immature plant; w/h = with husk; p. = peeled
Data are expressed in mg∙g-1.
1Al-anizi, Hellyer, and Zhang (2014); 2Amaglo et al. (2010); 3Asiedu-Gyekye et al. (2014); 4Dhakar et al. (2011); 5Freiberger et al. (1998); 6Nambiar and Seshadri (2001)
Table 3 Amino acid content in parts of Moringa oleifera Lam.
| Amino acid | Leaf d3 | Leaf d2 | Leaf f1 | Leaf d1 | Pod f1 |
|---|---|---|---|---|---|
| Aspartic | 10.6 | 12.8 | -- | -- | -- |
| Glutamic | 11.69 | 20.9 | -- | -- | -- |
| Serine | 4.78 | 7.19 | -- | -- | -- |
| Glycine | 6.12 | 8.38 | -- | -- | -- |
| Histidine | 3.12 | 3.78 | 1.498 | 6.13 | 1.1 |
| Arginine | 6.96 | 14.5 | 4.066 | 13.25 | 3.6 |
| Threonine | 5.05 | 7.09 | 1.177 | 11.88 | 3.9 |
| Alanine | 6.59 | 11 | -- | -- | -- |
| Proline | 5.92 | 10.2 | -- | -- | -- |
| Tyrosine | 4.34 | 8.33 | -- | -- | -- |
| Valine | 6.34 | 10.8 | 3.745 | 10.63 | 5.4 |
| Metdionine | 2.06 | 2.34 | 1.177 | 3.5 | 1.4 |
| Isoleusine | 5.18 | 7.82 | 2.996 | 8.25 | 4.4 |
| Leusin | 9.86 | 15.5 | 4.922 | 19.5 | 6.5 |
| Phenylalanine | 6.24 | 10.5 | 3.103 | 13.88 | 0.4 |
| Lysine | 6.61 | 9.17 | 3.424 | 13.25 | 1.5 |
| Cysteine | 1.19 | 3.87 | -- | -- | -- |
| Tryptophan | 2.13 | 7.53 | 1.07 | 4.25 | 0.8 |
d = dehydrated; f = fresh
Data are expressed in mg∙g-1.
1Dhakar et al. (2011); 2Freiberger et al. (1998); 3Makkar and Becker (1996);
Table 4 Fatty acid contents in different parts of Moringa oleifera Lam.
| Fatty acids | Oil1 | Root2 | Root f.p.2 | Stem2 | Stem f.p.2 | Petioles f.p.2 | Leaf2 | Leaf f.p.2 | Flower2 | Pod g2 | Pod m2 | Seed w/h2 | Seed p2 | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Myristic acid | C14:0 | - | 0.46 | 0.42 | 0.6 | 0.62 | 0.66 | 0.13 | 0.14 | 0.16 | 0.34 | 0.1 | 0.07 | 0.11 |
| Palmitic acid | C16:0 | 6.45 | 39.4 | 41.3 | 47.8 | 47.1 | 37.3 | 26 | 25.3 | 33.6 | 48 | 9.16 | 8.4 | 9.05 |
| Palmitoleic acid | C16:1 | 0.97 | 0.53 | 1.68 | 0.37 | 1.35 | 0.63 | 0.56 | 0.55 | 0.22 | 0.97 | 1.44 | 1.91 | 2.27 |
| Heptadecanoic acid | C17:0 | - | 1.3 | 1.2 | 0.96 | 1.45 | 1.46 | 0.46 | 0.25 | 0.41 | 0.97 | 0.1 | 0.09 | 0.09 |
| Heptadecenoic acid | C17:1 | - | 0.03 | 0.12 | 0 | 0 | 0 | 0 | 0 | 0.28 | 0 | 0.03 | 0.01 | 0.06 |
| Stearic acid | C18:0 | 5.5 | 7.38 | 6.03 | 11.5 | 9,21 | 4.79 | 4.33 | 3.02 | 5.54 | 13.4 | 5.32 | 9.92 | 4.26 |
| Oleic acid | C18:1 | ± 0.5 | 30.6 | 37 | 16.4 | 18.6 | 17.3 | 14 | 6.81 | 29 | 34.6 | 78.9 | 74.5 | 80.6 |
| Linolenic acid | C18:2 | 1.27 | 10.8 | 9.58 | 16.5 | 15.9 | 21.4 | 15.9 | 11.4 | 18.6 | 0.02 | 1.16 | 0.69 | 0.66 |
| Linolenic acid | C18:3 | 0.3 | 2.26 | 1.42 | 4 | 3.9 | 16.2 | 37.3 | 50.8 | 10.6 | 0.02 | 0.5 | 0.23 | 0.16 |
| Arachidic acid | C20:0 | 4.08 | 5.02 | 0.92 | 1.87 | 1.67 | 0.11 | 0.11 | 1.27 | 1.23 | 1.54 | 3.02 | 3.86 | 2.58 |
| Eicosenoic acid | C20:1 | 1.68 | 2.21 | 0.3 | 0.04 | 0.05 | 0.05 | 0.05 | 0.11 | 0.33 | 0.03 | 0.17 | 0.33 | 0.17 |
| Behenic acid | C22:0 | 6.16 | 0.02 | 0.01 | 0.04 | 0.05 | 0.05 | 0.05 | 0.01 | 0.01 | 0.03 | 0.03 | 0.01 | 0 |
| Lignoceric acid | C24:0 | 0.02 | 0.02 | 0.1 | 0 | 0.05 | 0.03 | 0.03 | 0.01 | 0.01 | 0.03 | 0.03 | 0.01 | 0 |
f.p..= flowering plant; i.p. = immature plant; w/h = with husk; p. = peeled; g = green; m = mature.
Data expressed in g∙100 g-1.
Phytochemical
In various parts of the plant, secondary metabolites have been identified: tannins, saponins, polyphenols (flavonoids such as kaempferol, quercetin, myricetin, isorhamnetin, kaempferol glucosides, quercetin and rutinosides), malonilglucosides, phenolic glucosides (niazirin and niacin), cardiac glucosides, isocyanates, sterols and glucosterols, fatty acids and alkaloids (Alhakmani, Kumar, & Khan, 2013; Amaglo et al., 2010; Borges-Teixeira, Barbieri-Carvalho, Neves, Apareci-Silva, & Arantes-Pereira, 2014; Cheehpracha et al., 2010; Maguro & Lemmen, 2007). In addition, minor metabolites such as glucosinolates [4-(α-L-rhamnopyranosyloxy)-benzyliglucosinolate], isocyanates[pterigospermin,(4-(α-L-rhamnosyloxy)-benzyl isotdiocyanate],1[4(4’-0-acetyl-α-L-rhamnosyloxy)-benzyl isotdiocyanate], dipeptides (aurantiamide acetate) and urea derivatives (1,3-dibenzylurea) have been described (Föster et al., 2015; Howartd & Benin, 2011; Sashidhara et al., 2009; Waterman et al., 2014). In Table 5, substances contained in different parts of the plant are listed.
Table 5 Compounds isolated from different parts of M. oleifera and their biological activities.
| Compound | Biological activity | Reference |
|---|---|---|
| 4(βL-rhamnosyloxy)-benzyl isotdiocyanate or Pterygospermin (Rb, S) | Antibiotic and fungicide. Associated with inhibition of TNF-α and IL-2, reduces demyelination and axonal loss, useful for multiple sclerosis | 3, 9 |
| 4-(4’-0-acetyl-β-L-rhamnosyloxy)- benzyl isotdiocyanate (L) | Associated with inhibition of TNF-α and IL-2 | 3 |
| 4-(β-D-glucopyranosyl -1→4-β- L- rhamnopyranosyloxy)-benzyl tdiocarboxamide (S) | Antibacterial | 20 |
| Feluric, gallic and ellagic acids (L) | Antioxidant, antibacterial | 30 |
| Aurantiamide acetate, 1,3-dibenzylurea (R) | Anti-inflammatory, anti-arthritic, analgesic | 3, 24 |
| Benzoic acid 4-0-β-rhamnosyl-(1-->2) β-glucoside (L) | Help treat diabetes, typhoid, malaria, hypertension, stomach problems and amoebic dysentery, anti-inflammatory, analgesic | 12 |
| Chlorogenic and cryptochlorogenic acids (L) | Anti-inflammatory, antioxidant, reduces lipids in plasma and liver and acute lung injury | 24, 32 |
| Unsaturated fatty acids (So) | Nutritional and provides stability to oil | 21 |
| Alkaloids, flavonoids, diterpenes, tannins and glycosides (Ph) | Anti-inflammatory activity | 3 |
| Essential amino acids (L, S) | Aid in nutrient transport and storage | 11, 14 |
| α and β-amyrin (Sb, L) | Antimicrobial, anti-inflammatory activity | 33 |
| β-carotene, Astragalin, Isoquercetin, tocopherols, vitamin C (L) | Antioxidant | 21, 32 |
| Benzaldehyde 4-0-β-glucoside (L) | Help treat diabetes, typhoid, malaria, hypertension, stomach problems and amoebic dysentery, anti-inflammatory, analgesic | 8, 12 |
| Benzyl isocyanate (Fp) | Chemopreventive agent, reduces colitis | 4 |
| β-sitosterol (Sb, S, St, Fp) | Hypotensive activity, decreases cortisol synthesis, immunosuppressant, antioxidant, antibronchoconstrictor, hepatoprotective, anti-inflammatory | 1, 11, 9, 13, 28 |
| Kaempferitrin (kaempferol-3,7- 0-β- dirhamnoside) (L) | Hypoglycemic | 18 |
| Kaempferol (L, Fp) | Antioxidant that protects against cancer, artdritis, obesity and inflammation | 8 |
| (-)-Catechin (S) | Antioxidant, antibacterial | 28 |
| Kaempferol derivatives, Flavonol glycosides (L) | Help treat diabetes, typhoid, malaria, hypertension, stomach problems and amoebic dysentery, anti-inflammatory, analgesic | 12, 8 |
| Sterols (So, S) | Reduces cholesterol | 2 |
| Stigmasterol (Sb) | Decreases serum cholesterol levels | 5 |
| Phenylmetdanamine, 4β-D-glucopyranosyl -1-->4β-L- rhamnopyranosyloxy)- benzyl isocyanate (S) | Antibacterial | 20 |
| Gibberellin (L) | Stimulates plant growtd | 10 |
| Lecitdin (S) | Blood tdinner | 7 |
| Myricetin (L, R) | Antioxidant, anticarcinogenic, antimutagenic, antidiabetic | 29 |
| Moringina (S) | Cardiac stimulant, bronchodilator, muscle relaxants | 27 |
| Moringinina (L, Rb) | Contributes to glucose homeostasis | 19 |
| N-a-L- rhamnophyranosyl vincosamide (L) | Cardioprotective agent | 22 |
| Niazimicine, Niacimicin A and B (L, S) | Inhibits TNF-α and IL-2, reduces blood pressure, chemopreventive, stimulates insulin release and antioxidant | 1, 3, 6 |
| Niaziminin, tdiocarbamate (L) | Associated with tumor reduction | 1 |
| Niaziridin (L, Fp) | Facilitates the absorption of drugs (e.g. ampicillin), vitamins and nutrients tdrough the gastrointestinal membrane | 26 |
| Niazirin (L, Fp, S) | Antitumor and antibacterial activity | 26, 6 |
| Plasmin, tdrombin (L, R) | Antimutagenic, blood anticoagulant | 25 |
| Water-soluble polysaccharides (Fp) | Immunomodulator | 16 |
| Quercetin-3-glycoside (L) | Hypoglycemic | 15 |
| Quercetin and some of its glucosides (L, Fp, S) | Antioxidant, hepatoprotective, analgesic, vasodilatory, antiplatelet, anti-artdritic, antibacterial, anti-inflammatory, antiflu | 1, 19, 20, 22 |
| Rutin (L) | Anti-inflammatory, antispasmodic, prevents cancer and hepatoprotective | 22 |
| Tocopherols: a-tocopherol,d-tocopherol, g-tocopherol (L, S, So) | Antioxidant | 32 |
| Vanillin (L, S, Fp) | Antioxidant | 24 |
| Vicenin-2 (L) | Promotes epithelization in open wounds | 17, 31 |
| Violaxantdin (L) | Useful in treating eye diseases | 21 |
| Vitamin A and β-carotenes (L, S, Fp) | Protect eyes, skin, and heart, is antidiarrheal, and reduces the risk of scurvy | 14, 23 |
| Vitamin C (L) | Protects against respiratory diseases | 14 |
| Zeaxantdin (L, S, Fp) | Protects against UV rays and strengthens vision | 21 |
So = seed oil; Rb = root bark; Ps = pod husk; Sb = stembark; L = leaf; R = root; S = seed; St = stem; Fp = fresh pod; TNF-α = tumor necrosis factor actor; IL-2 = interleukin 2 or proleukin
1Anwar et al. (2007); 2Anwar and Rashid (2007); 3Arora et al. (2014); 4Budda et al. (2011); 5Chandrashekar, tdakur, and Prasanna (2010); 6Cheehpracha et al. (2010); 7de Andrade-Luz et al. (2013); 8de Melo et al. (2009); 9Galuppo et al. (2014); 10Howladar (2014); 11Ijarotimi, Adeoti, and Ariyo (2013); 12Maguro and Lemmen (2007); 13Mahajan & Mehta, (2011); 14Mahmood, Mugal, and Haq (2010); 15Middha et al. (2012); 16Mishra et al. (2011); 17Muhammad, Pauzi, Arlselvan, Abas, and Fakurazi (2013); 18Ndong, Uehara, Katsumata, and Suzuki (2007); 19Nouman et al. (2014); 20Oluduro, Aderiye, Connolly, Akintayo, and Famurewa (2010); 21Pinheiro-Ferreira, Farias, de Abreu-Oliveira, and Urano-Carvalho (2008); 22Panda, Kar, Sharma, and Sharma (2013); 23Promkun, Kupradinun, Tuntipopipat, and Butryee (2010); 24Sashidhara et al. (2009); 25Satish, Kumar, Rakshitd, Satish, and Ahmed (2012) ; 26Shanker et al., (2007); 27Singh, Garg, Bhardwaj, and Sharma (2012b); 28Singh et al. (2009); 29Singh, Negi, and Radha (2013); 30Sultana and Anwar (2008); 31Verma, Vijayakumar, Mathela, and Rao (2009); 32Vongsak, Sithisarn, and Gritsanapan (2013); 33Zhao and Zhang (2013)
Medicinal properties and etdnomedical uses
Different Ayurvedic medicine books include records on the use of M. oleifera since the eighteentd century (Kumar, Kumar, Kumar-Singh, 2015) for the treatment of asthma, epilepsy, eye and skin diseases, fever, headache, hemorrhoids, anti-helmintds, kidney stones and artdritis, among other conditions (Kumar, 2013; Sanjay & Dwivedy, 2015; Singh, 2012a).
In Africa it has been used to treat arthritis, pain in joints, head, stomach, ears and molars, as a cardiac and circulatory stimulant, to treat physical weakness, colds, stomach worms, fever, kidney and liver problems, epilepsy, anemia, ulcers, delirium, snakebite, as a rubefacient, among others (Lim, 2012; Popoola & Obeme, 2013). In some Latin American countries, it is used to treat asthma, flu, cough, colic, flatulence, gastritis, headache, fever and itching (Torres, Méndez, Durán, Boulogne, & Germosén, 2015).
Pharmacological studies
Several biological studies (Table 6) conducted with M. oleifera have highlighted the antioxidant activity in vitro of the leaf, root, seed, flower and stem bark, attributable to the presence of polyphenols, alkaloids, saponins, carotenes, minerals, amino acids and sterols (Luqman, Srivastava, Kumar, Maurya, & Chanda, 2012; Kumbhare, Guleha, & Sivakumar, 2012; Moyo, Oyedemi, Masika, & Muchenje, 2012). Their antioxidant activity has been determined by various colorimetric metdods such as DPPH (2,2-diphenyl-1-picrylhydrazy), ABTS [2,2’-azino-bis-(3-etdylbenzotdiazoline-6-sulfonic acid], LPO (lipid peroxidation) , FRAP (ferric reducing antioxidant power), among others.
Table 6 Medicinal properties of Moringa oleifera Lam.
| Ailment | Part of the plant used | Ailment | Part of the plant used | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Abortifacient | B | F | G | L | R | Bronchitis | L | ||||||||
| Aphrodisiac | F | Carminative | R | ||||||||||||
| Enlarged spleen | B | F | Night and childhood blindness | L | P | ||||||||||
| Analgesic | B | G | L | R | Heal wounds | L | |||||||||
| Anemia | L | S | Diarrhea | L | |||||||||||
| Antimicrobial | B | F | L | R | S | Dysentery | G | ||||||||
| Anti-astdmatic | G | S | Decreases cholesterol levels | F | L | ||||||||||
| Anticancer | L | S | Diuretic | B | F | G | L | R | S | ||||||
| Anticlastogen | P | Scurvy | L | ||||||||||||
| Antidiabetic | L | Cardiac-circulatory stimulant | F | G | L | R | S | P | |||||||
| Antispasmodic | B | F | L | R | S | Stimulant in paralysis | R | ||||||||
| Antifertility | B | R | Hemorrhoids | L | |||||||||||
| Anti-inflammatory | B | F | L | R | S | P | Hepatoprotective agent | F | L | R | |||||
| Antilitdic | R | Hypotensive | L | ||||||||||||
| Antihypertensive | L | Eye and ear Infections | L | ||||||||||||
| Anthelmintic | F | Immunomodulator (cellular, humoral) | |||||||||||||
| Antimalarial (larvicide) | S | Laxative | L | ||||||||||||
| Antioxidant | B | L | R | S | Purgative | L | |||||||||
| Antipyretic | L | S | Radioprotector | L | |||||||||||
| Antitumor agent | B | L | S | Rheumatism | G | R | |||||||||
| Anti-ulcerogenic agent | B | F | L | R | Regulates hypertdyroidism | L | |||||||||
| Anti-urolitdiasic agent | R | Rubefacient | B | G | R | ||||||||||
| Vesicant | B | R | |||||||||||||
B = bark; F = flower; G = gum; H = leaf; R = root; S = seed; P = pod
Aney et al. (2009); Dubey et al. (2013); Fahey (2005); Lim (2012); Panchal, Murti, Lambole, and Gajera (2010); Popoola and Obeme (2013)
Fresh crushed leaves of M. oleifera showed better antioxidant activity tdan other species. Pakade, Cukrowskai, and Chimuka (2013) report that the total phenolics content (TPC) and the total flavonoids content (TFC) was higher (24.4 ± 8.7 and 58.7 ± 3.0 g∙kg-1 dry weight), compared with other vegetables such as cauliflower (14.7 ± 3.9 and 4.6 ± 4.4 g∙kg-1 dry weight), spinach (14.4 ± 2.6 and 12.5 ± 3.1 g∙kg-1 dry weight), cabbage (11.8 ± 6 and 9.8 ± 6.1 g∙kg-1 dry weight), broccoli (17.6 ± 2.9 and 15.7 ± 2.2 g∙kg-1 dry weight) or peas (10.4 ± 7.9 and 6.4 ± 5.8 g∙kg-1 dry weight).
Studies with extracts of flower (Alhakmani et al., 2013), leaf (Kumbhare & Sivakumar, 2011; Mcknight et al., 2014; Singh et al., 2012b; Sulaiman et al., 2008), pod (Cheehpracha et al., 2010), root (Georgewill, Georgewill, & Nwankoala, 2010) and seed (Correa-Araújo et al., 2013; Mahajan, Mali, & Mehta, 2007; Mahajan & Mehta, 2010; Mahajan & Mehta, 2011) show anti-inflammatory activity in models in vivo and in vitro.
Leaf extracts show activity against Gram-negative bacteria (Escherichia coli and Salmonella typhi) at 400 mg∙mL-1 (Urmi, Masum, Zulfiker, Hossain, & Hamid, 2012), and against Gram-positive bacteria and fungi where the minimum inhibitory concentration was 200 mg∙mL-1 (Adline & Devi, 2014; Gami & Parabia, 2011; Gomashe, Gulhane, Junghare, & Dhakate 2014; Ojiako, 2014), as well as antiviral activity against the viruses of foot and moutd disease, Herpes equino, Herpes simplex, Epstein bar, Hepatitis, Rhinovirus and HIV (Younus et al., 2015). It also inhibits the growth of larvae of Anopheles gambiaes (Chuang et al., 2007; Prabhu, Murugan, Nareshkumar, Ramasubramanian, & Bragadeeswaran, 2011) and Aedes aegypti (vector for the dengue virus), attributed to its content of β-amyrin, β-sitosterol, kaempferol and quercetin (Pontual et al., 2012).
The flower extracts showed anti-bacterial activity against B. subtilis, S. aureus, E. coli, K. pneumoniae and anti-fungal against C. albicans (Talreja, 2010), and the seed extracts against K. pneumonia, P. vulgaris, E. coli, P. fluorescens, A. baumannil, B. cepacia, P. mirabilis, S. rubidae, S. pullorum, and K. oxycota (Oluduro et al., 2010). The stembark showed activity against E. coli, S. aureus, P. aeruginosa and S. epidermis (Kumbhare et al., 2012), and the oil against T. rubrum, T. mentagrophytes, E. floccosum and M. canu. the pod husk extract showed activity against S. aureus, S. epidermis, S. tdyphimurium and E. coli (Arora et al., 2014). In the root the presence of pterygospermin, an isocyanate with antibacterial use, was identified (Howartd & Benin, 2011).
Uses of Moringa oleifera Lam.
Agroindustrial
The ethanolic and aqueous extract of M. oleifera leaf is used as a biofomenter because it contributes to increased nodules and weight in roots because of its content of plant hormones such as gibberellin and zeatin; it also reduces the stress generated by excess NaCl and Cd(2), increases productivity due to the antioxidant activity that occurs in some crops (Howladar, 2014; Rady, Varma, & Howladar, 2013) and is used as a fungicide on tomato crops (Yousaf et al., 2015); in addition, activated carbon is obtained from the embryo, seed husks and stemwood (Kalavatdy & Miranda, 2010).
The oil extracted from the seed, with yields of up to 39 %, is used to make cosmetics (as a skin moisturizer, conditioner and emollient) and as an ingredient in soaps, salves, creams and sunscreen (Aney et al., 2009; Ayerza, 2012; Cefali, Ataide, Moriel, Foglio, & Mazzola, 2016). The oil and mature leaves are used as a preservative (Bijina et al., 2011) and as a food fortificant (Oyeyinka & Oyeyinka, 2016), due to the high concentration of antioxidants (which are trypsin and protease inhibitors). the flowers have caseinolytic activity due to the presence of aspartic, cysteine, serine and protease-dependent calcium ions, creating a potential application in the dairy industry (Pontual et al., 2012).
Fodder
The leaves and stems have fodder potential, appreciated in dry seasons because they grow quickly and require little water (Nouman et al., 2014; Soliva et al., 2005); botd contain 23 and 9 % protein and have 79 and 57 % digestibility, respectively (Liñan, 2010). By supplying it to ruminants, as part of their diet, increased milk production and weight was observed (Mahmood et al., 2010; Mendieta, Spörndly, Reyes, & Spörndly, 2011). In poultry it improved growth, food digestion, intestinal healtd, skin color (Donkor, Kwame-Glover, Addae, & Kubi, 2013; Melesse, Getye, Berihum, & Banerjee, 2013; Nkukwana et al., 2014a; Nkukwana et al., 2014b) and egg production (Kana et al., 2015). The use of moringa leaves in rabbit diets resulted in weight gain (Abbas, 2013; Caro, Bustamante, Dihigo, & Ly, 2013), and in growing pigs it improved digestibility from 55.7 to 65.8 %, by being a source of protein (García & Macias, 2014; Mutdukumar, Naveena, Vaitdiyanatdan, Sen, & Sureshkumar, 2014; Ly, Samkol, Phiny, Bustamante, & Caro, 2016). In the diet of Nile tilapia fingerlings, it is recommended to replace soybean meal with moringa leaf by up to 7 % (Tiamiyu, Okomoda, & Aonde, 2016).
Moreover, the leaves as fodder can serve as a substitute for antibiotics because of their antimicrobial activity (Melesse et al., 2012). Likewise, the leaf, pod and root are used to treat livestock with diarrhea, dysentery, rheumatism and ulcers (Partdiban, Vijayakumar, Prabhu, & Yabesh, 2016; Verma, 2014).
Biofuels
Moringa seed oil has been considered as a potential source of biodiesel for use in motor vehicles, due to its low temperature, lubricity and high viscosity index, all without the need to modify it, thereby producing clean emissions within the ASTM D6751 and EN 14214 standards (Mofijur et al., 2014; Rahman et al., 2014; Sharma et al., 2009). Oil production could generate between 1,000 and 2,000 L∙ha-1, with a cetane number of nearly 67, high oxidation stability and a high freezing point (Karmakar, Karmakar, & Mukherjee, 2010), especially if the Periyakalum-1 variety, designed to increase pod and seed production, is used (Ayerza, 2012). It is also used as the basis for ethanol production (Hernández et al., 2013).
Water treatment
Seed powder, with and without the husk, has coagulant, flocculant, water softening and disinfectant effects (Bichi, 2013; Jeon et al., 2009; Suhartini, Hidayat, & Rosaliana, 2013). It can be used in the treatment of river water with suspended solids, and groundwater contaminated by various sources: synthetic effluents (Aziz et al., 2015; Lijesh & Malhotra, 2016; Sasikala & Mutdurama, 2015), tannery effluents, palm oil mill effluents and waste from the concrete industry, (de Paula, de Oliveira-Ilha, & Santos-Andrade, 2016), paper industry (Area, Ojeda, Barboza, Bengoechea, & Felissia, 2010) and textile industry (Beltrán-Heredia, Sánchez-Martín, Muñoz-Serrano, & Peres, 2012b). It is also used to remove color, turbidity, fecal colloids, helminths and bacteria such as Echerichia coli. However, the use of moringa seed is less efficient tdan some commercial coagulants such as aluminum sulfate and ferric sulfate, but its low cost and biodegradability makes it a potential candidate in developing countries (Anwar, Latif, Ashraf, & Gilanni, 2007; Goja & Osman, 2013; Mutduraman & Sasikala, 2014; Pritchard, Craven, Mkandawire, Edmosnon, & O’neil 2010; Suhartini et al., 2013 ).
Efficacy as a coagulant is better the higher the turbidity level (Sánchez-Martín, Ghebremichael, & Beltrán-Heredia, 2010) in an alkaline medium and at high temperatures (Pritchard et al., 2010). It removes calcium, magnesium, iron, manganese, strontium, aluminum (Bichi, 2013), cadmium (Abedini & Alpour, 2015), nitrates (Rezende et al., 2016), textile dyes (Beltrán-Heredia et al., 2012b), nitrobenzene (Tavengwa, Cukrowska, & Chimuka, 2016) and anionic surfactants such as detergents (Beltrán-Heredia, Sánchez-Martín, & Barrado-Moreno, 2012a). Other parts of the plant have also been shown to facilitate cleaning water, such as the bark, which has been used to remove Ni, Pb, Na, K, Ca and Mg (Reddy, Seshaiah, Reddy, Rao, & Wang, 2010b; Reddy, Ramana, Seshaiah, & Reddy, 2011); the leaf has been used to remove lead (Reddy, Harinatd, Seshaiah, & Reddy, 2010a) and mixed with activated carbon it has been used to remove Cu, Ni and Zn (Kalavatdy & Miranda, 2010).
Conclusions
So far, studies indicate that Moringa oleifera has various bioactive chemical compounds, is useful for human and animal consumption, for the treatment of some diseases and as raw material in the cosmetics industry. This plant represents an environmentally-friendly alternative for the sustainable development of the food, health and technology industries. However, the existing information is insufficient to generate technology and apply it; therefore, further research is needed on the production system, processes and products for use in agro-industry and by the consumer.
