Botanical description, geographic distribution and chemical composition of M. oleifera

M. oleifera Lam. or Moringa pterygosperma Gaertner is a shrub belonging to the family Moringaceae, cultivated for its leaves, flowers and fruits with many nutritional, medicinal and industrial potentialities. This tree, native to India, has been introduced in all tropical and subtropical regions (Price, 2007; Atakpama et al., 2014) and has become naturalized in many African countries. Still called mouroungue, ben ailé, neverdié, horseradish tree; M. oleifera is a small, fast-growing, perennial (Bosch, 2017) deciduous tree that can reach 7 to 12 m in height (Foidl et al., 2001).

The stem is brittle with a cork bark, whitish gray, with drooping branches; the leaves are pale green and bipinnate or more often tripinnate with opposite and ovoid leaves (Pandey et al., 2011). They are 6.5 to 60 cm long, 4 to 6 pairs of pinnae and elliptic to Tableobovate leaflets (Bosch, 2017) (Figure 1a). The fragrant, bisexual and zygomorphous flowers have five free petals, oblong-spatulate, 1 to 2 cm long, unequal, white or cream and finely veined (Figure 1b). The fruit of Moringa oleifera is a pendulous and elongated capsule, 10 to 50 cm long, brown in color becoming dark brown when ripe (Bosch, 2017). The fruits form pods with three lobes which, when dry, open in three parts (Figure 1c). Each pod contains between 12 and 35 seeds (Foidl et al., 2001). Seeds, globose, 1 to 1.5 cm in diameter bear three thin wings (Bosch, 2017).

 

 

Sterols, glycosides, alkaloids, triterpenoids, flavonoids, anthraquinones, carotenoids and tannins have been identified in the stem bark and flowers of M. oleifera. The seeds are oleaginous, revealing a very high fatty acid profile. They have the same health benefits as olive oil (Anwar et al., 2007). The leaves of M. oleifera contain negligible proportions of anti-nutritional factors (Kavitha et al., 2012). The average composition of some parts of M. oleifera is established in Table 1.

 

The review article was written using secondary data analysis. Information on searching databases such as Agora, Hinari, Google Scholar, various journals, books, articles were used during redaction of biological properties and immunomodulatory effect of M. oleifera in animal and human nutrition.

 

Biological activities of M. oleifera

Anti-anaphylactic activity

The anti-anaphylactic effect of the ethanolic seed extract was studied in a murine model of systemic anaphylactic shock induced by compound 48/80. Passive cutaneous anaphylaxis activated by the anti-IgE antibody was also used to evaluate the effect of the extract (Mahajan and Mehta, 2007). The study showed, on the one hand, that administered one hour before the injection of compound 48/80, the ethanolic extract of M. oleifera at doses of 0.001 to 1 g / kg completely inhibits the induced anaphylactic shock; on the other hand, the extract significantly inhibits  the  passive  cutaneous  anaphylaxis activated by the anti-IgE antibody at a dose of 1 g / kg (Mahajan and Mehta, 2007).

Antiulcer activity

The root extract of M. oleifera have been used in the treatment of ulcerative colitis in mice (Gholap et al., 2012). Leaf extracts also produced a significant reduction in stress-induced gastric ulcers and duodenal ulcers induced by cysteamine (Devaraj et al., 2007). Debnath and Guha (2007) also reported an anti-ulcer effect of the aqueous extract of M. oleifera leaves on adult albino Holtzman rats. Indeed, according to these authors, treatment with M. oleifera for 14 days on ulcerated rats decreased the average ulcer index, increased the number of enterochromaffin cells and the content of 5-hydroxytryptamine. The alcoholic leaves extract of M. oleifera Lam. has shown ulcer protective effect as dose dependently against pylorus-ligation, ethanol, cold restraint stress, and aspirin induced gastric ulcer in rats. The said extract of M. oleifera Lam. was found to decrease ulcer and acid pepsin secretion (Verma et al., 2012).

Antithyroid activity

Tahiliani and Kar (2000) studied the role of M. oleifera leaf extract in the regulation of thyroid hormones in Swiss adult rats and found that it plays an inhibitory role in the peripheral conversion of tetraidothyoronin (T4) into triiodothyronine (T3). In addition, at low concentrations, this extract can be used to control hyperthyroidism (Tahiliani and Kar, 2000).

Hepatoprotective activity

Various studies have reported that ethanolic extracts of seeds and leaves of M. oleifera have hepatoprotective action. Indeed, Pari and Kumar (2002) evaluated the hepatoprotective effect of the ethanolic extract of M. oleifera leaves on hepatic lesions induced by antituberculous drugs such as isoniazid, rifampicin and pyrazinamide in rats. Thus, oral administration of the extract has shown an important protective action made evident by its effect on the levels of alanine aminotransferase, aspartate aminotransferase, alkaline phosphatase and bilirubin in serum, also on lipid levels and lipid peroxidation in the liver. This observation was completed by a histopathological examination of the liver.

The seed extract of M. oleifera also exerts a hepatoprotective effect against liver fibrosis induced by the oral administration of 20% carbon tetrachloride (CCl4). Indeed, the administration of Moringa seed extract decreased the  CCl4-induced  elevation  of  serum  aminotransferase activity and the level of globulin (Hamza, 2010).

Anti-inflammatory activity

Several parts of the Moringa plant have shown anti-inflammatory activity. The anti-inflammatory activity of the methanolic extract of M. oleifera leaves has been demonstrated using tests induced by carrageenan and histamine (Adepapo et al., 2014). N'diaye et al. (2002) showed that M. oleifera root extract has anti-inflammatory activity in carrageenan-induced paw edema in rats using indomethacin, a potent anti-inflammatory drug (10 mg / kg). In fact, at a dose of 750 mg / kg, the aqueous root extract of M. oleifera significantly inhibited the development of edema at 1, 3 and 5 hours (53.5, 44.6 and 51.1% respectively).

Alcohol extract from M. oleifera seeds has also shown anti-inflammatory activity against ovalbumin-induced respiratory tract inflammation in guinea pigs (Mahajan and Mehta, 2007). Bioactive compounds in M. oleifera pods can contribute to anti-inflammatory activity to improve the pathogenesis of chronic inflammatory diseases (Muangnoi et al., 2012).

Antidiabetic activities

The use of M. oleifera as a therapeutic agent against diabetes has been explored. Studies have shown that in rats with type 2 diabetes, leaves of M. oleifera significantly reduce glucose concentration. Leaves are indeed a powerful source of polyphenols, responsible for hypoglycemic activity. M. oleifera also has an enhancing effect on glucose intolerance that can be mediated by quercetin-3-glucoside and fibers contained in leaf powder (Ndong et al., 2007). The aqueous extract of M. oleifera leaves at doses of 100, 200 and 300 mg / kg body weight showed a reduction of 33.29; 40.69 and 44.06% of the glycemia of alloxan-induced diabetic albino rats (Edoga et al., 2013). At the same doses, Manohar et al. (2012) showed the antihyperglycaemic activity of the aqueous extract of M. oleifera leaves on normal rabbits and diabetic alloxan-induced rabbits. Moringa fruit lower serum cholesterol, phospholipids, triglycerides, LDL (Low Density Lipoprotein), VLDL (Very Low Density Lipoprotein) and reduce lipid profile in cholesterol-positive rabbits elevated and then increase the excretion of fecal cholesterol (Mehta et al., 2003).

Antitumor activities

M. oleifera has several bioactive compounds with antitumor activity. Niazimicin, niaziminine and beta-sitosterol-3-o-beta-D-glucopyranoside have indeed shown an antitumor action. Studies have explored the chemopreventive and antiproliferative potential of M. oleifera against chemical carcinogenesis, as well as its role in epithelial ovarian cancer. In addition, M. oleifera seed extracts have effects on enzymes metabolizing hepatic carcinogen (Bharali et al., 2003; Bose, 2007). The leaf extract of M. oleifera has shown potential cytotoxic effects on cell lines of human multiple myeloma (Parvathy and Umamaheshwari, 2007; Soha et al., 2019).

Antioxidant activities

Exploration of M. oleifera as a potential source of antioxidants has yielded positive results (Chumark et al., 2008). The content of phenolic compounds present in the leaves confers a scavenging property of free radicals, whereas the ethanolic fraction has considerable properties of metal chelation which can protect against DNA cleavage (Verma et al., 2009; Sreelatha and Padma, 2009; Singh et al., 2009). Seed powder showed a reduction in tissue arsenic concentration, providing protection against oxidative stress (Gupta et al., 2007). M. oleifera seeds have been shown to be superior for trapping free radicals relative to palm oil (Ogbunugafor et al., 2011). Aqueous-methanol extract of M. oleifera leaves has antioxidant capacity (Okumu et al., 2016).

Diuretic and antiurolithic activities

Studies indicate that the M. oleifera wood root has anti-urolithic activity (Dubey et al., 2013). One study also revealed an anti-lithiolithic property of the aqueous and alcoholic extracts of the bark of the M. oleifera root (Karadi et al., 2006). Indeed, both extracts significantly lowered the levels of urinary excretion and renal retention of oxalate, calcium and phosphate.

Hypocholesterolemic and cardioprotective activities

The Moringa root bark contains the moringinine alkaloid, which by its effect on the sympathetic nervous system stimulates cardiac function (Duke, 2001). The effects may also be due to the prevention of hyperlipidemia. He demonstrated that M. oleifera prevents hyperlipidemia due to iron deficiency in male Wistar rats (Ndong et al., 2007). A study comparing M. oleifera leaf extract with antenolol (a selective β1-receptor antagonist used for cardiovascular diseases) reported the leaf extract of M. oleifera as a hypolipidemic, lowering of body weight, heart weight, serum triglyceride and cholesterol levels in experimental animals (Ara et al., 2008).

M. oleifera also has a cardioprotective role in isoproterenol-induced myocardial infarction. Treatment with M. oleifera has been reported to have cardioprotective cardioprotective effects in male Wistar albino rats on enzymatic biochemical parameters including superoxide dismutase, catalase, glutathione peroxidase, lactate dehydrogenase, and creatine kinase (Farooq et al., 2012). It has also been shown that this compound lowers cholesterol levels in rats fed a high-fat diet (Ghasi et al., 2000).

Antihypertensive activities

Several bioactive compounds in M. oleifera leaves exert a direct effect on blood pressure and can thus be used for the stabilization of blood pressure. The compounds of M. oleifera leading to an antihypertensive effect include nitrile, mustard oil glycosides and thiocarbamate glycosides present in Moringa leaves (Anwar et al., 2007). Moringa leaves contain b-sitosterol, a bioactive phytoconstituent with a cholesterol lowering effect.

Antiasthmatic activity

The alkaloid of the Moringa plant showed a similarity with ephedrine in terms of activity. Thus, it can be used in the treatment of asthma. The seeds of M. oleifera have shown a potential effect in the management of bronchial asthma. Patients showed significant relief from the severity of asthma symptoms in addition to improved respiratory function (Agarwal and Mehta, 2008).

Immunomodulatory activity

The immunomodulatory action of the methanolic extract of M. oleifera was studied in an experimental model of immunity. Neutrophil adhesion assays, cyclophosphamide-induced neutropenia, and carbon clearance assay were used to study cellular immunity. Humoral immunity was tested by lethality testing in mice, estimation of serum immunoglobulin levels, and indirect haemagglutination assay in animals. The study showed that M. oleifera stimulates both the cell-mediated and the humoral-mediated immune system at lower doses (Sudha et al., 2010). Several studies concluded that, the inclusion of M. oleifera in chicken diets resulted in better growth performance, immune response and antioxidative status (Khan et al., 2017; Oghenebrorhie and Oghenesuvwe, 2016; Yeung et al., 2019). Cui et al. (2018) reported that dietary M. Oleifera supplementation can act as ROS scavenger to improve the antioxidant capacity by activating the antioxidant enzymes and reducing the level of oxidative enzymes in broilers. Moussa et al. (2017) have reported that the inclusion of dietary M. Oleifera could improve the immune response of chickens. Furthermore, El-Deep et al. (2019) reported that M.  oleifera  supplementation of  broiler's  diet  would also modulate the immune response by regulating mRNA expression levels of the innate immune response mediators, such as IL2 and IL6, and alleviating the degenerative changes that occurred in live tissue following HS.

Spasmolytic activity

The roots as well as the ethanol extract of the leaves showed an antispasmodic action, perhaps through the blocking of calcium channels. The spasmolytic activity exhibited by the constituents of the plant provides a solid base for traditional uses of the plant in gastrointestinal motility disorders (Anwar et al., 1994).

Radioprotective activity

A radioprotective effect was observed in the methanolic extract of M. oleifera leaves in irradiated Swiss albino mice. In fact, pretreatment with the methanolic extract of M. oleifera leaves considerably reduces the percentage of aberrant cells in the bone marrow after irradiation with gamma whole body radiation in animals. Pretreatment with the methanolic extract of M. oleifera leaves confers significant radiative protection to bone marrow chromosomes in irradiated mice (Rao et al., 2001).

Antinociceptive activity

Several studies have shown that M. oleifera has analgesic activity. This activity was indeed demonstrated using the acetic acid induced convulsion test and the Eddy hot plate test for peripheral and central analgesic actions respectively using albino mice. The ethanolic leaf extract of M. oleifera showed significant analgesic activity at 100, 200, 400 mg / kg in both tests compared to the control group (Bhattacharya et al., 2014).

The antimigraine potential of the alcoholic fraction of leaf sap of M. oleifera that is traditionally used in the treatment of migraine has been studied. The study showed that Moringa can be used effectively in the treatment and management of migraine (Upadhye et al., 2012). The fresh leaf sap and ethanol extract of Moringa oleifera leaves were administered orally at varying doses to mice and were tested for antinociceptive activities using three models: acetic acid-induced convulsion, licking of the formalin-induced paw and tail stroke test using analgesiometer. The study showed significant antinociceptive activity of M. oleifera (Upadhye et al., 2011).

Healing activity

The aqueous extract of M. oleifera leaves and the ethyl acetate   extract   of   dried  leaves  were  found  to   have  significant healing potential. For the study, 10% of the extract was applied to excision, incision and dead space (granuloma) models in the rat as an ointment (Rathi et al., 2006; Hukkeri et al., 2006). The polysterols and phenolic compounds in these extracts promote healing activity (Dubey et al., 2013). 

Antimicrobial activities and antihelminthic effects

Various components of M. oleifera have inhibitory activity against several microorganisms. The seeds of M. oleifera because of some active ingredients they contain: antimicrobial isothiocyanates and glucomoringin is a potent antibacterial and antifungal agent (Padla et al., 2012; Galuppo et al., 2013; Jeon et al., 2014). Moreover Dougnon et al. (2011) have shown that the ethanolic extract of M. oleifera leaves has antibacterial activity against Staphylococcus aureus strains.

A range of antimicrobial activity has been observed from susceptibility of B. stearothermophilus to resistance to Pseudomonas aeruginosa (Ali et al., 2004). In addition to the antibacterial activity of M. oleifera oils, antifungal activity has also been demonstrated (Chuang et al., 2007). Comparative comparison of the antibacterial and antifungal efficacy of the M. oleifera vapor distillate revealed maximal inhibition of E. coli followed by S. aureus, Klebsiella pneumoniae, P. aeruginosa and Bacillus subtilis. Of the fungi, Aspergillus niger was the most inhibited, followed by Aspergillus oryzae, Aspergillus terreus and Aspergillus nidulans (Prashith et al., 2010).

Alcohol extracts from leaves, seeds and flowers showed antimicrobial activity against E. coli, Klebsiella pneumoniae, Enterobacter species, Proteus mirabilis, P. aeruginosa, Salmonella typhi, Streptococcus aureus, and Candida albicans (Nepolean et al., 2009). In vitro antifungal activity has been observed against dermatophytes such as Trichophyton rubrum, Trichophyton mentagrophytes, Epidermophyton floccosum and Microsporum canis, including some species of Aspergillus and Penicillium (Ayanbimpe et al., 2009). 

Recent discoveries have revealed cyanobactericidal potential in seeds (Lürling and Beekman, 2010). It has also been reported that ethanolic extracts of M. oleifera leaves inhibit the Indian worm Pheritima posthuma (Rastogi et al., 2009).

Antiplasmodial activity

In vitro studies have shown an antiprotozoal effect of M.oleifera (Köhler et al., 2002). Soluble seed extract lectin showed larvicidal activity by delaying larval development and promoting mortality in Aedes aegypti, probably due to its haemagglutinating activity (Coelho et al., 2009; Ferreira et al., 2009).

Cerebroprotective and depressive activities of the Central Nervous System (CNS)

The root extract exhibits CNS depressive activity. Studies using the aqueous extract of M. oleifera root on penicillin-induced convulsion, locomotor behavior, cerebral serotonin (5-HT), dopamine (DA) and norepineprine (NE) were studied in rat. The extract improved the imbalance between 5-HT, DA and NE (Ray et al., 2003). The brain-protective effect of M. oleifera leaf extract against brain damage and oxidative stress in the animal model of focal ischemic stroke was studied. The study demonstrated that M. oleifera leaf extract is a potential neuroprotectant that is cheap and easy to approach (Kirisattayakul et al., 2013).

Other pharmacological effects of M. oleifera

Work on the leaves of M. oleifera has shown that they can serve as a strengthening of the immune system against viral damage and especially in people living with HIV / AIDS (Lipipun et al., 2003). Flowers and leaves are used to treat inflammation, muscle disease, hysteria, tumors, enlarged spleen, and reduced serum cholesterol (Siddhuraju and Becker, 2003). 

The different researches on M. oleifera have come to justify the various uses and virtues that endogenous populations have lent to it for centuries. Given the different nutrients and properties of this miracle tree, it would benefit from being considered in the efforts to contain cases of bacterial resistance increasingly frequent and why not in the prevention and fight against avian pathologies of origin viral disease like Newcastle disease. Also, several investigations are needed to corroborate the main mechanisms of Moringa as an immunostimulatory agent.

 

The authors have not declared any conflict of interests.

The authors thank the Research Unit in Applied Microbiology and Pharmacology of Natural Substances (U.R.M.A.Pha), which give access to their library for the provision of documents and information necessary for the writing of this review paper.