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Table of Contents
REVIEW ARTICLE
Year : 2022  |  Volume : 8  |  Issue : 3  |  Page : 314-338

Pharmacological, ethnomedicinal, and evidence-based comparative review of Moringa oleifera Lam. (Shigru) and its potential role in the management of malnutrition in Tribal Regions of India, especially Chhattisgarh


1 Department of Kaumarabhritya - Balaroga, Shri NPA Government Ayurveda College, Raipur, Chhattisgarh, India
2 Department of Natural Chemistry, Madurai Kamraj University, Madurai, Tamil Nadu, India
3 Drug Testing Lab Avam Anushandhan Kendra, Department of AYUSH, Chhattisgarh, India
4 Department of Dravya Guna, Shri NPA Government Ayurveda College, Raipur, Chhattisgarh, India
5 Department of Biotechnology, National Institute of Technology, Raipur, Chhattisgarh, India

Date of Submission22-Jun-2021
Date of Acceptance28-Jun-2021
Date of Web Publication11-Mar-2022

Correspondence Address:
Dr. Prashant Kumar Gupta
Department of Kaumarabhritya - Balaroga, Shri NPA Government Ayurveda College, Raipur, Chhattisgarh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/wjtcm.wjtcm_69_21

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  Abstract 


Moringa oleifera Lam. (Shigru) (Moringaceae family) is a traditional medicine used for control of diabetes, obesity, asthma, and cardiac, liver, gastrointestinal, infective, and brain disorders, such as depression and Alzheimer's disease. In Ayurvedic literature, Shigru is among few drugs having Balya (nourishing) as well as Medohara (antiobesity) property. This review focuses on valid connections between the properties documented in ancient literature and current pharmacological knowledge of Moringa, including pharmacological actions, phytochemistry, botanical description, and how Moringa can tackle malnutrition in India, especially Chhattisgarh. All information about M. oleifera was obtained from electronic scientific databases such as PubMed, Web of Science, Scopus, ScienceDirect, Elsevier, Google Scholar, Traditional Knowledge Digital Library, and Indian Traditional Books (Ancient Ayurveda literatures, The Wealth of India, and The Ayurvedic Formulary of India), postgraduate/doctoral thesis, and googling the keyword M. oleifera. M. oleifera have anti-oxidant, antimicrobial, anti-diabetic, anti-obesity, anti-inflammatory, cardioprotective, hepatoprotective, neuroprotective, gastroprotective, wound-healing properties and it can potentially tackle malnutrition. This review describes the key information related to botanical description of M. oleifera, phytochemistry, pharmacological actions, clinical studies, toxicological studies, better utilization as food therapeutics, and ethnobotanical and evidence-based comparative review of M. oleifera. M. oleifera can effectively tackle malnutrition in India, especially Chhattisgarh. The authors emphasize the need for future in-depth ethnopharmacological lead-based research and clinical studies to expand M. oleifera pharmacological activities, clinical efficacy, and safety.

Keywords: Ethnobotanical practices, ethnomedicine, Moringa oleifera, phytochemicals, pharmacological action


How to cite this article:
Sonewane K, Chouhan SS, Rajan M, Chauhan NS, Rout OP, Kumar A, Baghel GS, Gupta PK. Pharmacological, ethnomedicinal, and evidence-based comparative review of Moringa oleifera Lam. (Shigru) and its potential role in the management of malnutrition in Tribal Regions of India, especially Chhattisgarh. World J Tradit Chin Med 2022;8:314-38

How to cite this URL:
Sonewane K, Chouhan SS, Rajan M, Chauhan NS, Rout OP, Kumar A, Baghel GS, Gupta PK. Pharmacological, ethnomedicinal, and evidence-based comparative review of Moringa oleifera Lam. (Shigru) and its potential role in the management of malnutrition in Tribal Regions of India, especially Chhattisgarh. World J Tradit Chin Med [serial online] 2022 [cited 2022 Oct 3];8:314-38. Available from: https://www.wjtcm.net/text.asp?2022/8/3/314/339345




  Introduction Top


Worldwide, Moringa oleifera is a gossip plant for its health values. M. oleifera (family - Moringaceae) is native to South Asia and has 13 species worldwide. M. oleifera is a short, fast-growing, easily cultivated, evergreen, tropical, deciduous, angiosperm tree.[1],[2] Owing to its strong tolerating nature against the worst atmospheric conditions (drought/mild frost), it has been cultivated throughout the world.[3] It has low demand for soil nutrients, needs no much care, does not shed leaves in the dry season, tolerates a wide range of rainfall, called as “Miracle Tree” or “Nebedaye” (never die).[4],[5]

For thousands of years, M. oleifera is known for its medicinal values also. In Ayurveda, M. oleifera is named as Shigru, and few synonyms such as “Akshiv” (healthy for eyes), “Mochak” (trouble shooter), and “Shobhanjan” are also been used depending on its medicinal utility. Its Patra (leaves), Pushpa (flowers), Phala (fruits), and Beeja (seeds) are used [Table 1], and in many parts of Africa and India, it is used as a food. M. oleifera leaves were used by Indian warriors to enhance energy and pain and stress relief during the war.[5],[8]
Table 1: Parts of Moringa oleifera (Shigru) plant and their uses

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It has antioxidant, anticancerous, antidiabetic, hepatoprotective, antiobesity, antimicrobial, anti-inflammatory, immunomodulatory, and cardioprotective actions. M. oleifera leaf contains more Vitamin A than a carrot, 12 times Vitamin C than oranges, much potassium than a banana, higher iron than spinach, and 17 times the calcium of milk.[1],[9],[10]

Indian classical medicine texts such as Charak-Samhita, Sushruta-Samhita, Ashtanga-Sangaha, and Nighantoos (a particular type of Sanskrit glossary, containing brief annotations of difficult words grouped into thematic categories) have also described various medicinal properties of Shigru (M. oleifera) such as Deepan (appetizers), Rochan, Sangrahi (absorbant), Chakshushya, Brimhan, Krimihar (anthelminthic), Vishnashanam (detoxicants), Medohar (antiobesity), Shophaghnam (anti-inflammatory), Pramehahar (antidiabetic), and Shulaghna (pain killer).[6],[11],[12],[13],[14] Honey is advised as adjuvant to Shigru (M. oleifera) for good palatability and synergistic effect[15] [Table 1].

Malnutrition is a major problem in developing countries, resulting in mental and physical health consequences. Globally, 155 million children under 5 years of age are suffering from stunting, while 41 million are overweight or obese, and about 45% of below 5 years of age deaths are linked to under-nutrition. M. oleifera can have a potential role in the management of all types of malnutrition, i.e., undernutrition and obesity.

This review focuses on valid connections between the properties documented in ancient literature and current pharmacological knowledge of M. oleifera including botanical description, phytochemistry, pharmacological actions, clinical studies, toxicological studies, in silico studies, ethnobotanical practices, patents, formulations, and evidence-based practices. The current study also discussed the potential role of M. oleifera in tackling malnutrition (both under- and over-nutrition) and better human utilization of M. oleifera in tribal regions of Chhattisgarh, India. A brief about phytochemistry, pharmacology, traditional uses, ethnomedicinal comparison, and malnutrition management capacity of M. oleifera is depicted in [Figure 1].
Figure 1: Phytochemistry, pharmacology, traditional uses, ethnomedicinal comparison, and malnutrition management capacity of Moringa oleifera

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  Species Distribution, Production, and Cultivation Top


M. oleifera is native to Himalayan foothills countries such as India and Bangladesh, but commercially, it is cultivated extensively in Middle Eastern, African, and Asian countries.[16] India is the largest producer of M. oleifera fruits (pods). It is distributed in Assam, Gujarat, Punjab, Jammu and Kashmir, Kerala, Madhya Pradesh, Maharashtra, Chhattisgarh, Odisha, Rajasthan, and Uttar Pradesh, whereas Andhra Pradesh, a southern state of India, is a major producer followed by Karnataka and Tamil Nadu.[8]


  Brief Botanical Description of Moringa oleifera Top


M. oleifera is a short, slender, deciduous, perennial, dicotyledonous tree. It grows up to 8-m high and 60-cm diameter at breast height. Its wood is soft, the stem is brittle-corky, and the bark is whitish-gray, while the leaves are feathery, pale green, tri-pinnate with opposite ovate leaflet. Flowers are fragrant, white or creamy blossoms throughout the year. Its fruit pods are large, pendulous, distinctive, slightly constricted at intervals, gradually tapering to a point. Unripe green pods are somewhat fleshy, fibrous, and grayish when mature. Seeds are trigonous, winged, and blackish in color. M. oleifera tree grows well in a temperature range of 25°C–35°C, direct sunlight, altitude of 500 m, and slightly acidic to alkaline soil.[8],[17] Chhattisgarh is geographically and environmentally similar to the above conditions hence, best conducive for M. oleifera cultivation.


  Phytochemistry Top


Major phytochemicals of M. oleifera are carotenoids, flavonoids, phenolic compounds, tocopherols, ascorbic acid, folate, polyunsaturated fatty acids, amino acids, alkaloids, tannins, saponins that have therapeutic potential [Figure 2]. M. oleifera leaves contain a significant amount of copper (Cu), zinc (Zn), magnesium (Mg), iron (Fe), calcium (Ca), potassium (K), beta-carotene (Vitamin A), Vitamin B (folic acid, pyridoxine, and nicotinic acid), Vitamin C, Vitamin D, and Vitamin E [Figure 3]. M. oleifera is a good source of proteins and lipids. The crude protein content of Indian M. oleifera seed is equivalent to soya bean and higher than peanuts, and its crude lipid content is considerably higher than soya bean but slightly lower than peanuts.[1],[8],[18],[19] Different classes of chemical constituents of M. oleifera are summarized in [Table 2].
Figure 2: Major phytoconstituents of Moringa oleifera

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Figure 3: Major elements and vitamins present in M. Oleifera.

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Table 2: Different classes of chemical constituents of Moringa oleifera

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  Pharmacological Actions Top


Detail pharmacological actions of the M. oleifera are summarized in [Table 3].
Table 3: Detailed pharmacological activities of Moringa oleifera

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Antiobesity action

The M. oleifera ethanolic extract showed antiobesity activity in obese female Wistar rats at a dose of 600 mg/kg/p.o. by downregulating mRNA expression of leptin and resistin while upregulating adiponectin gene expression.[29] The methanolic extract of M. oleifera leaves reduced the level of liver biomarkers (total cholesterol [TC], triglycerides, low-density lipoprotein [LDL], very LDL), body weight, organ weight, and atherogenic index in high fat-induced obesity in Wistar albino rats at doses of 200 and 400 mg/kg/p.o.[30] The polyphenol extract of M. oleifera leaves (100 and 200 mg/kg/p.o.) reduces lipid markers in male Wistar rats through inhibiting HMG CoA reductase activity and fecal bile acid binding.[31] M. oleifera significantly inhibits the expression of adipogenesis molecules, lipid metabolism mediators and unregulated thermogenesis in an in-vitro adipose stem cell study.[82] Details are given in [Table 3].

Antimicrobial activity

Phytochemicals such as flavonoids, tannins, steroids, benzyl glucosinolate, benzyl isothiocyanate, alkaloids, and saponins are responsible for the antimicrobial activity of M. oleifera. Methanolic extracts of M. oleifera (20%, 40%, and 60% concentration) showed inhibitory effects of 16, 18, 18 mm diameter on Staphylococcus aureus standard strain (ATCC25923) and 16, 17, 19 mm diameter on Klebsiella pneumoniae standard strain (ATCC35637). Aqueous extract of M. oleifera (20%, 40%, and 60%) had inhibitory effects of 18, 19, 21 mm diameter on Proteus vulgaris (NCTC8196) strain. Antibacterial activity against clinically isolated Staphylococcus saprophyticus, S. aureus, and Escherichia coli from urinary tract infected patients was also observed.[83] The aqueous, ethanol, and methanol extract of M. oleifera leaves exhibited antibacterial activity against Gram-positive bacteria S. aureus, Gram-negative bacteria E. coli, and Pseudomonas aeruginosa at the concentrations of 30, 60, 90, and 120 mg/ml.[84] The moringin-conjugated α-cyclodextrin complex showed antimicrobial activity against the S. aureus reference strains (ATCC 25923, ATCC6538, and ATCC BAA-977). This complex exhibited bacteriostatic effects (Minimum inhibition capacity (MIC) =0.5 mg/ml) and bactericidal effects (Minimum bactericidal concentration (MBC) =1 mg/ml) against the S. aureus reference strains.[28] The ethanol extract of M. oleifera seed at low and hot temperature is shown to be bioactive against 92% and 90% of the vibrio species strains (isolated from the hemolymph of Litopenaeus vannamei shrimp), respectively, at an MIC value of 32 μg/ml.[85] The iron oxide nanoparticles via a composite of Psidium guajava-M. oleifera leaf extract at 10 μg/ml inhibit the growth of E. coli and S. aureus bacterial strains with an inhibition zone of 25.2 and 30.3 mm, respectively.[23]

Cardiovascular activity

Active components niazinin A, niazinin B, niazimicin, as well as thiocarbamate and isothiocyanate glycoside in M. oleifera displayed antihypertensive activity, which leads to cardioprotection. The hydroalcoholic extract of M. oleifera (200 mg/kg/p.o.) exhibited cardioprotection in the isoproterenol-induced myocardial infarct Wistar rats through biochemical enzymes modulation. This shows antioxidant, anti-peroxidative, and myocardial preservative properties.[33] Dietary supplementation with M. oleifera seed powder (750 mg/kg/day/p.o.) corrects aging-induced endothelial dysfunction by upregulating Nitric Oxide (NO) and Endothelium-Derived Hyperpolarizing Factor (EDHF) signaling in the aorta and mesenteric artery respectively in Wistar rats.[36] Details are given in [Table 3].

Antioxidant action

M. oleifera leaf extract showed the highest 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging and ferric-reducing antioxidant power (FRAP) total reducing power activities with IC50 values of 1.02 ± 0.13 mg/ml and 0.99 ± 0.06 mM Fe2+/g respectively; the leaf and root extracts have ABTS radical scavenging activities with the IC50 values of 1.36 ± 0.02 and 1.24 ± 0.03 mg/ml.[86] Isolated polypeptide (<3.5 kDa) from M. oleifera seeds showed strong antioxidant activity.[18] The methanol extract of M. oleifera leaves displayed free radical scavenging activity with an IC50 value of 49.30 μg/ml in DPPH assay and 11.73 μg/ml in ABTS assay.[22] M. oleifera leaf acetone extract exhibited antioxidant property with IC50values of 5.18, 2.66, and 2.44 μg/ml for DPPH, FRAP, and ABTS respectively.[87]

Antidiabetic activity

Ethanolic extract of M. oleifera (500 mg/kg/p.o.) showed antihyperglycemic activity through carbohydrase inhibition and glucose fiber binding in an in vivo and in situ study. It also inhibits alpha-amylase, thus inhibiting the absorption of glucose.[37] M. oleifera leaf powder (20 gm/day) supplemented with local traditional meal in Saharawi refugee camp of southwestern Algeria ameliorates postprandial glucose response in diabetic subjects.[38] Other antidiabetic studies are compiled in [Table 3].

Anti-inflammatory activity

Alkaloids, flavonoids, phenols, moringin, beta-sitosterol, carotenoids, and vanillin present in M. oleifera are responsible for anti-inflammatory action. M. oleifera root extract compounds like aurantiamide acetate and 1,3-dibenzyl urea 5, inhibited the production of tumor necrosis factor (TNF)-alpha and interleukin (IL)-2 leading to inflammation control through stabilization of mast cells. The methanolic extract of M. oleifera (250 mg/kg/p.o.) for 6 weeks in streptozotocin-induced diabetic male Wistar strain rats showed anti-inflammatory activity by improving TNF-α and IL-6.[40] In vitro study by protein denaturation method in the ethanolic flower extract of M. oleifera (100–500 μg/ml), showed significant inhibition of denaturation of egg albumin in a dose-dependent manner.[88]

Wound-healing property

M. oleifera showed wound-healing activity on incision, excision, and dead space wound models in rats.[42]

Antiasthmatic action

Ethanol extract of M. oleifera seeds showed antiasthmatic action through inhibition of immediate hypersensitive reaction, histamine release, and infiltration of various inflammatory cells (eosinophil and monocyte) in bronchoalveolar lavage in induced airway inflammation of guinea pigs.[45]

Neuroprotective action

Vitamin C and Vitamin E present in M. oleifera play an important role in improving memory in patients with Alzheimer's disease. M. oleifera leaf alcoholic extract (250 mg/kg/p.o.) is effective in the experimental Alzheimer rat model by altering monoamine levels and electrical activity.[47] Methanolic extract of M. oleifera leaves at a dose of 50, 100, and 200 mg/kg/p.o. showed potent nootropic activity (enhancement of memory or other cognitive functions) in scopolamine-induced cognitive dysfunction albino mice.[48] The M. oleifera leaf extract (300 mg/kg/p.o.) reduced serum aluminum concentration and showed ameliorative effects against aluminum-induced neurohistopathological changes in the temporal cortex of albino Wistar rats.[49] M.oliefera 70% ethonolic seed extract (500 mg/kg/p.o.) showed neuroprotective effects in both the acute and chronic stages of ischemic stroke by promoting hippocampal neurogenesis and synaptic plasticity as well as improving cholinergic function.[89] The glucomoringin isothiocyanate (0.313–10 μg/ml) isolated from M. oleifera seed abrogated oxidative stress-induced neurodegeneration through Nrf2 and NFkB signaling pathways in neuroblastoma SHSY5Y (ATCC® CRL-2266™) cell line.[50]

Cross-kingdom regulation

The miRNA endogenous to one species may impact the biological process of another distantly related species. miRNAs are capable of fine-tuning mammalian gene expression, and the polyphenols from the M. oleifera plant are suggestive to regulate endogenous mammalian miRNA levels in high-throughput sequencing analysis. M. oleifera mRNA highlighted the role of mol-miR168a (M. oleifera gene) in the active regulation of SIRT1 (human gene). SIRT1 acts as a transcription factor in the regulation of P53. Both SIRT1 and P53 regulate metabolism, stress signaling, cellular regulation, and genome stability. Moringin isothiocyanate (0.5 μM) pretreatment inhibits the expression of genes involved in mitophagy in the stem cells of the human periodontal ligament. It downregulates the proapoptotic gene BAX and caspases (CASP1 FC: −1.43, CASP4 FC: −0.18, CASP6 FC: −1.34, CASP7 FC: −0.46, CASP8 FC: −0.65) which implies the inactivation of the apoptotic process along with upregulation of antiapoptotic genes BCL2L12 and MCL1.[53]

Anticancerous action

M. oleifera crude aqueous leaf extract (0.1–10 mg/ml) induces cell cycle arrest and apoptosis in human liver hepatocellular carcinoma (HepG2) cells.[55] Moringin (16.4 μM) from M. oleifera seeds inhibits growth and induces apoptosis of human neuroblastoma cells (SH-SY5Y) and arrests cell cycle through the modulation of NF-κB- and apoptotic-related factors.[56] M. oleifera extract (0.01%–0.25%) exerts its cytotoxic effect in the human lung adenocarcinoma cell line (A549) by affecting mitochondrial viability and inducing apoptosis in a ROS-dependent manner.[57] Kaempferol (flavonoid) was found to exhibit anticancer activity through different modes of action including antiproliferation, apoptosis induction, cell cycle arrest, anti-metastasis or anti-angiogenesis activities, generation of reactive oxygen species, modulation of multiple molecular targets including P53, STAT3, and activation of caspases.[90] M. oleifera stem bark extract-mediated AgNPs (15.6, 31.25, 65.5, 125, and 250 μg/ml) exhibit excellent anticancer activity against the human cervical carcinoma (HeLa cell) cell line.[58]

Antidiarrheal action

The hydroalcoholic extract of M. oleifera leaves (100, 250, and 500 mg/kg/p.o.) showed antidiarrheal activity mediated through inhibition of hypersecretion and gastrointestinal motility in castor oil-induced diarrhea model of albino mice and Wistar rats.[59] M. oleifera leaf extract (400 mg/kg/p.o.) modulate murine intestinal immunity in hymenolepiasis nana (parasite)-infected Swiss albino mice.[60] Tannins, saponins, and flavonoids play an important role in antidiarrheal action.

Immunomodulatory action

Methanolic extract of M. oleifera plant stimulates humoral and cellular immunity through the increase in white blood cells (WBCs), levels of serum immunoglobulins in mice and adhesions of neutrophils, and increase in the phagocytic index in carbon clearance test. The methanolic extract of M. oleifera (250 and 750 mg/kg, p.o.) stimulates both cellular and humoral immune response in bovine Pasteurella multocida-infected mice.[62] The aqueous extract of M. oleifera leaves (300 mg/kg/p.o.) activates cellular immunity in herpes simplex virus type-1 infected BALB/c mice.[63] The hydroalcoholic extract of M. oleifera substantially enhanced cellular immune response, humoral immune response, neutrophil index, and phagocytic activity at doses of 100 and 200 mg/kg body weight in cyclophosphamide-induced immunosuppressed animals.[91] Vitamin A, B, and C, iron, calcium, potassium, proteins, saponins, flavonoids, carotenoids, phytates, and phenolic compounds or increased production of growth factors may be responsible for immune-modulatory action.

Analgesic and antipyretic action

The M. oleifera alcoholic extract (30 mg/kg) showed analgesic activity in Wistar albino rats.[66] Methanolic extract of the root of M. oleifera (0.35–0.70 g/kg/i.p.) produced analgesia in Swiss mice and also potentiated the analgesic action of morphine and pethidine.[67] The ethanol extract of M. oleifera leaves (250, 500, and 750 mg/kg) revealed antinociceptive activity in normal and CFA-induced Sprague–Dawley male arthritis rats in a dose-dependent manner.[68] The hydroalcoholic M. oleifera bark extract (100 mg/kg/p.o.) in rabbits against E. coli-induced pyrexia.[70]

Gastroprotective and antiulcer action

The M. oleifera leaves extract (500 mg/kg, p.o.) increased the healing of gastric ulcers and prevented the development of experimentally induced gastric ulcers and duodenal ulcers in albino Wistar rats.[71] The isothiocyanate-enriched Moringa seed extract (150 mg/kg/p.o.) alleviates ulcerative colitis symptoms through Nrf2-mediated anti-inflammatory/antioxidant signaling pathway in C57BL/6J mice.[72]

Hepatoprotective action

M. oleifera extract was found to be liver protective against paracetamol-induced hepatic injury in the rat model.[73] Gastrodigenin rhamnopyranoside and 1-O-(4-hydroxymethyphenyl)-alpha-L-rhamnopyranoside from M. oleifera seed is a liver protective agent in ICR mice and L02 cell model.[74]

Other actions

The cream prepared from M. oleifera leaves extract reduces unwanted sebum secretion from the sebaceous gland in healthy human male volunteers.[76] Ethanolic leaf extract of M. oleifera (50, 100, or 200 mg/kg) is effective in benign prostatic hyperplasia (BPH) in testosterone-induced BPH through enhancement of antioxidant defense mechanisms in male Sprague–Dawley rats.[78] M. oleifera stem extract (1 mg/ml) alleviated lens opacification, reduced reactive oxygen species generation, increased glutathione content, and elevated superoxide dismutase and catalase activities in cultured mouse lenses.[77] The polyphenolic-rich M. oleifera leaf extract (200 mg/kg/p.o.) showed radioprotective effects against mobile phone electromagnetic radiation-induced infertility in Wistar rats.[79] The M. oleifera leaf extract (250 and 500 mg/kg) increases folliculogenesis in polycystic ovary syndrome in 3-month-old Wistar strain.[80] It has great potential as a natural preservative.[92] M. oleifera possesses anticholinesterase action against mammalian acetylcholinesterase enzyme sourced from brain homogenate of male F344 rat strain.[93] M. oleifera leaf extract ameliorates the adverse effects of salt loading on the blood cells (RBCs and WBCs) in salt-loaded albino mice model.[81] M. oleifera leaf Ext. can overcome the negative impact of herbicides (pendimethalin) when added to water used for agriculture.[94] M. oleifera contains dimeric cationic proteins that absorb and neutralize colloidal charges in turbid water; hence, it exhibits water purification action.[95] M. oleifera is equally beneficial in bovines, as it increases the gene expression of casein in bovine mammary epithelial cells.[54]


  Traditional Ayurveda Uses of Moringa oleifera Top


In Ayurveda, Rasayana means a substance, which ameliorates Jara (senility) and Vyadhi (disease).[96] According to Acharya Charak, Rasayana imparts Tarunam vayah (youth ness and antiaging), Deha Bala (body strength), Indriya Bala (strength to organs especially sensory and motor), Ayu (life), Medha (intelligence), Smriti (memory), Prabha (complexion), and so on.[97] In 16th century book Rajnighantoo, Raktashigru (a type of M. oleifera) is described as Rasayan.[13] Krimiharam, Krimighna, and Kriminashanam (antimicrobial and anthelminthic) have widely been used for the action of Shigru.[11],[13],[14],[98] According to Vangasen Samhita, Shigru (M. oleifera) - Vidang (Embalia ribes) decoction has krimihar (anti-microbial) property. Shigru (M. oleifera) has Medohar (antiobesity) and Hridya (cadiotonic) property.[11],[14] In Sushrut Samhita, Shigrutail (oil extract from M. oleifera seed) is indicated for Prameh (diabetes) disease.[98] The terms such as Shophaghna, Shwayathunashak, Shothjeet, and Shwayathuhar came from the actions of Shigru,[11],[12],[14] which are near to anti-inflammatory action.[19],[36] The terms such as Vranaghna, Vrandoshnut, Vranhar, and Vidradhihar concerning Shigru matche with the wound-healing action.[6],[11],[12],[13]

Shigruphal (fruit of M. oleifera) also has a Shwashar (reduces dyspnea) effect,[11] similar to the antiasthmatic effect.[99] In Sushrut Samhita, Shiroroghar (capable of relieving ailments involving head and neck) property of Shigrutail (oil extract from M. oleifera seeds) is mentioned.[98] Shigru has Angavyathahar and Shulaghna properties, which are similar to the analgesic property.[11],[13] In Charak-Samhita, Shigru comes under Svedopag Gana (sweat generator) so indicated as Jwaraghna (antipyretic). Shigru is indicated in Pliharog (liver and spleen disorders). A detailed comparison between the pharmacological properties documented in ancient literature and current pharmacological knowledge of M. oleifera (Shigru) is provided in [Table 4] and a brief structural and pharmacological description of major phytoconstituent of M. oleifera is given in [Table 5].
Table 4: Pharmacological effects of Moringa oleifera (Shigru) in comparison to modern medical science

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Table 5: Major phytoconstituents of Moringa oleifera and its pharmacological values

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  Clinical Trials on Moringa oleifera Top


Two clinical trials performed in India showed an improvement in nutritional status in children. In a study, performed among preschool (Anganwadi) children (30 each in control and treated group) in the rural area of Bangalore suffering from Grade I and Grade II protein–energy malnutrition (PEM), M. oleifera was administered orally for 60 days. At the end of the study, 70% of children with Grade II PEM improved to Grade I, and 60% of children with Grade I PEM got a significant improvement in their nutritional status.[104] In another study, 6–9-month-old infants were supplemented with 10 g M. oleifera leaf powder for 3 months. After 3 months, the mean change in body weight and hemoglobin (Hb, gm%) in the treatment group was higher than the control group.[105]

A community based interventional study done at Tanzania showed anemia prevalence reduction among children supplemented with M. oleifera.[106] Significant improvement in platelet count (in low-dose group), an increase in mean Hb value, and mean corpuscular Hb concentration after using M. oleifera leaf powder in 0.038 mg/kg and 0.077 mg/kg divided group (10 each) healthy volunteers was observed.[107]

A randomized, double-blind, placebo-controlled study in anemic women (Hb 8–12 g/dl), M. oleifera aqueous leaf extract (1400 mg capsule, orally) daily for 3 weeks as add-on therapy with ferrous sulfate (200 mg/tablet) was administered in 35 women (16–49 years) divided into 17 treated and 18 of control showed a significant increase of mean of Hb, red distribution wide, serum ferritin, and mean corpuscular Hb concentration in Moringa-treated group whereas the platelets count were significantly lower (P < 0.05) than those of control group.[108]

M. oleifera is found to improve nutritional status among women as well. 32 (94%) among 34 reproductive-aged females supplemented with M. Oleifera for 3 months showed rise in Hemoglobin levels (1.8 g/dl on average). Overall, 94% of cases showed an increase in Hb g% level (1.8 g/dl on average) after the intervention.[109] M. oleifera is effective for improving obesity among women as well. In a study, 15 obese females between 45 and 55 years with a body mass index (BMI) of 29–34 kg/m2 were supplemented with M. oleifera leaf extract (400 mg) hard gelatin capsule for 8 weeks showed a significant reduction of the average BMI, TC, and LDL compared to the baseline values.[32] M. oleifera can prevent postmenopausal complications in women suggested by a study done in 90 postmenopausal women supplemented with 7 gm M. oleifera leaf powder and 9 gm amaranth powder for 3 months. Data revealed that supplementation significantly improved blood biomarkers of antioxidants (serum retinol, serum ascorbic acid, serum Glutathione, and superoxide dismutase) and reduced blood biomarkers of oxidative stress (malondialdehyde).[110] M. oleifera leaf powder was found helpful for mean glycemic meal response and increased insulin secretion although taste acceptance was a limiting factor.[38]

Nutritional value of M. oleifera was also examined among human immunodeficiency virus (HIV)-infected patients. A single-blind randomized controlled trial in HIV-infected patients concluded that M. oleifera leaf extract supplementation may represent a readily available and effective local solution to improve BMI and serum albumin level in people leaving with HIV undergoing antiretroviral therapy.[111] A double-blind placebo clinical trial using a single oral dose of a nutritional supplement containing M. oleifera leaf saponin revealed that it can stimulate the production of nitric oxides, which enhances the cardiovascular and physical fitness of sports participants.[112]


  Toxicological Studies of Moringa oleifera Top


A study conducted in rat model indicated that oral administration of M. oleifera-dried leaf powder up to 2000 mg/kg showed no clinical or gross pathological changes, indicating oral toxicity (LD50) of the M. oleifera dried leaf powder is higher than 2000 mg/kg,[113] while in another study, male Wistar albino mice were administered M. oleifera aqueous leaf extract orally in various doses of 400–6400 mg/kg showed no mortality while post-treatment dullness and reduced locomotion were observed in doses 3200 mg/kg and beyond. LD50 was estimated to be 1585 mg/kg.[114] M. oleifera leaf extract found genotoxic at supra-supplementation levels of 3000 mg/kg body weight in animal study. However, its intake is safe at levels ≤1000 mg/kg body weight.[115] A subchronic toxicity study of M. oleifera on 30 Balb mice received 1000 mg/kg dried leaf powder for 90 days showed no adverse effect.[116]

Oral intake of M. oleifera root and root extracts are possibly unsafe due to the presence of a toxic substance called spirochin; hence, consumption of root extract should be avoided for human uses. Safety evaluation studies on M. oleifera have shown no toxicity when consumed in large quantities and no adverse effect reported even on daily use in the meal. Toxicological studies of M. oleifera are summarized in [Table 6].
Table 6: Toxicological studies of Moringa oleifera

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  In Silico Studies of Moringa oleifera Top


In silico is a broad term that denotes “anything which is performed on computer or via computer simulations about biological experiments.” The bioinformatics tools used for in silico studies of M. oleifera are molecular docking software PyRx 0, 8, ligand docking, and binding site analysis with pyMOL and LigPlus software, PubChem compound database, and protein target prediction database Pharmmapper and Chemmapper.[118] M. oleifera in silico screening showed that niazimicin (active constituent of M. oleifera) has greater potential as a glycosyltransferase inhibitor than other existing inhibitors based on its binding affinity and intermolecular interactions with the target site.[119] In an another in silico study, β-sitosterol, ellagic acid, and aurantiamide acetate present in M. oleifera showed promising affinity as an anti-HIV candidate using CXCR4 as a target receptor.[120] In silico study of antimicrobial peptides from M. oleifera leaves exhibits activity against Gram-negative and Gram-positive bacteria, fungi, and specific biological activity against S. aureus, P. aeruginosa, E. coli, Klebsiella sp., Saccharomyces cerevisiae, Candida albicans, and Alternaria brassicicola.[121] In-silico study confirms that M. oleifera coagulant protein (MOCP) derived from crude seed extract of M. oleifera (MOCE) checks water and soil pollutants through molecular interactions. Study advocates prospective use of MOCE for large scale treatment of drinking water and industrial effluents.[122] and after comparison between monomeric and dimeric forms of MOCP, it was suggested that oligomerization does not affect the biological activity of a protein.[123]


  Patents and Current Market Formulations of Moringa oleifera Top


Globally, a total of 10,613 patent application and 1744 patent grants are available on “Google patent” regarding M. oleifera on dated March 27, 2020, out of which US office (US) have 689 patents grants, China office (CN) 422 grants, European Patent (EP) office 199 grants, and so on. In 2019, nearly, 331 applications for patents were received while 41 patents were granted related to M. oleifera.[124] Patents granted for medicinal, health, or cosmetic properties of M. oleifera are summarized in [Table 7]. Shigru is used in various Ayurvedic medicines as a main or side ingredient. These medicines have a wide base of therapeutic uses ranging from skin disorders, neuronal disorders, pain, cardiac disorders, malnutrition, and so on.[125] Main Ayurvedic formulations (classical and marketed) of M. oleifera are summarized in [Table 8].
Table 7: Patents related to medicinal/health/cosmetic uses of Moringa oleifera[124]

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Table 8: Classical and marketed formulations containing Moringa oleifera as an ingredient

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  Potential in Tackling Malnutrition Top


Malnutrition refers to deficiencies, excess, or imbalances in a person's intake of energy and/or nutrients. Lack of access to a variety of foods is the major cause of micronutrient malnutrition in low socioeconomic rural populations because they consume most of food directly from their farms. Hence, high nutrient dietary diversification through promoting locally available/grown food products can be a long-term, cost-effective, and sustainable solution to malnutrition.

M. oleifera has almost all the essential nutrients required for well-being. M. oleifera leaf has a high iron and calcium content, so it may help to treat anemia and calcium deficient disorders[126] hence, can be co-administered with standard care. M. oleifera has the potential as a home-based remedy for nutritional disorders, especially in limited health facility areas. Among the recent efforts in the developing world, M. oleifera leaf powder is being used as a food fortifier to combat malnutrition.

M. oleifera is rich in all essential amino acids, which are building blocks for proteins that are necessary for all cell growth in undernutrition. M. oleifera is equally helpful in managing obesity because of the abundance of secondary metabolites, principally polyphenols and 4 unique Moringa isothiocyanates.[30] Isothiocyanates are the main antiobesity and antidiabetic bioactivities that regulate rate-limiting steps in liver gluconeogenesis, leading to direct or indirect increase in insulin signaling and sensitivity. It reduces plasma insulin, leptin, resistin, and cholesterol.[26] The role of M. oleifera in the management of malnutrition is shown in [Figure 4].
Figure 4: Diagrammatic presentation of direct and indirect role of Moringa oleifera in management of under nutrition, obesity, diabetes, and heart disorder

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According to Ayurveda, Shigru is among the few drugs that have the Balya as well as Medohara effect,[11] although both attributes look functionally opposite to each other.


  Chhattisgarh Province of India and Moringa. oleifera Top


Malnutrition in Chhattisgarh has been a concern, as the recent National Family Health Survey (NFHS)-3 data showed that the prevalence of stunting is 53%, underweight is 48%, and wasting is 24%. One in every four children less than 3 years of age suffers from wasting due to acute undernutrition. Two-thirds of adolescent girls suffer from anemia. Consequently, malnutrition leads to communicable and noncommunicable diseases. The tribal population of Chhattisgarh has a high level of malnutrition; citing women and children are worst affected. An underweight, anemic, teenager contends with early pregnancy along with restricted prenatal nutrition and healthcare, resulting in delivering a low birth-weight baby, which later in life develops into a stunted and underweight adolescent.

M. oleifera tree easily grows in home gardens. It is short, easy to cultivate, grows quickly, and does not shed leaves in the dry season. M. oleifera leaf powder can be stored at home for up to 6 months under recommended storage conditions; hence, it is easily consumable throughout the year even by low-income families. Moringa is well adaptable to the central Indian climate; hence, Chhattisgarh is best conducive for Moringa tree cultivation. It occupies a considerable part of the food plate in Indian states such as Orissa and Chhattisgarh. Edible parts such as M. oleifera pods are consumed by the local people in tribal areas of Bilaspur district, situated in the eastern part of Chhattisgarh. Traditional agroforestry for M. oleifera is practiced at Bastar region of Chhattisgarh.

“Poshan Vatika scheme” was launched in tribal-dominated districts of Chhattisgarh to raise the nutrition levels of people, especially women and children. Scheme incorporates cultivation of green leafy vegetables and drumsticks in kitchen gardens or Poshan vatikas. Chhattisgarh government launched an ambitious “The Narva, Guruva, Ghurva, and Baadi” program in the state, under which Baadi (horticulture within or near home) is Nutri-garden having fruits, vegetables, and other crops for household consumption and the government is encouraging M. oleifera cultivation in the kitchen baadi. Under the supervision of Directorate, AYUSH Chhattisgarh, the “Ayurved Gram” in Chhattisgarh promotes awareness about Moringa uses and distributes Moringa-based ready-to-use products in the Bastar region to manage malnutrition.

Some misconceptions passed on by oral traditions in rural Chhattisgarh and Eastern Maharashtra that M. oleifera should not be consumed if anyone is under any treatment, second, M. oleifera and bitter gourd (Momordica charantia) should not be cooked together. An extensive vernacular literature search was conducted to get the reference for such information with no fruitful results but further search and research is needed to examine this casuistry. It can be better tackled by using proper Information Education Communication material and community-level awareness.

During the flowering season of M. oleifera, an ethnobotanical practice of putting branches of seed pods of Cassia occidentalis (local name Dhandhani) over previously nonflowering (Virgin) M. oleifera tree surprisingly results in flowering/fruiting to same nonflowering M. oleifera [Figure 5]a and [Figure 5]b. These ethnobotanical practices need further botanical research.
Figure 5: (a) Nonflowering Moringa plant covered with branches of Cassia occidentalis (dated: January 26, 2020). (b) Moringa oleifera starts flowering after practice of putting branches of Cassia occidentalis (dated February 21, 2020)

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  Roadmap for Better Utilization of Moringa oleifera in Local Setups Top


To increase the acceptability of Moringa-fortified food products, a sweet excipient can be used to overcome its bitter taste. The addition of M. oleifera germinated seed flour to commonly used wheat/rice flour can increase the protein content of the final product. Roasting can increase protein, calcium, zinc, lipids, carbohydrates, fiber, and ash content while Vitamin A and B1 are significantly decreased. Fermentation and germination can increase amino acids in M. oleifera; hence, it is advisable to educate local tribal people about such tricks of nutri-addition. Complementing M. oleifera with other foods rich in sulfur amino acids or lysine can improve the nutritional property.

There is a need for policy shift from just promotion of M. oleifera benefits to health markers-based intensified public health initiatives and awareness programs, especially in malnutrition-hit districts of Chhattisgarh. A comprehensive pool policy involving departments such as health and family welfare, horticulture, agriculture, forestry, and AYUSH along with traditional health practitioners and local preachers can effectively reduce malnutrition and improve health parameters. Primary health centers should be involved for better results.

We, at our hospital, are providing M. oleifera seeds to every patient visiting the pediatric outpatient department with advice to plant it at his or her residential vicinity. In addition, we promote the slogan “A Moringa pod a day…keeps the disease away.” Other ways of using M. oleifera as a main food source and food fortificants are summarized in [Table 9].
Table 9: Ways of using Moringa oleifera as a main food source and food fortifier

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M. oleifera can be used to improve hand hygiene as well. In an interesting study conducted in the School of Hygiene and Tropical Medicine, M. oleifera dried or wet powder was compared with nonmedicated liquid soap for their activity on hands artificially contaminated with E. coli. Not less than 4 g of M. oleifera powder in the dry and wet application had the same effects as nonmedicated soap used for hand wash on E. coli. Hence, hand wash with wet/dry M. oleifera powder could be a good locally available option for hand hygiene.[127]


  Conclusion Top


This review provided a summary of phytochemistry, pharmacological actions, phytochemical analytical, in silico studies, patents, clinical studies, tradition Ayurveda uses, and toxicological studies of M. oleifera. The above attempt for evidence-based comparative review concludes similarities in classical and modern pharmacological actions of M. oleifera (Shigru). Preclinical studies discovered that M. oleifera holds anti-inflammatory, analgesic, anticancer, antioxidant, antipyretic, antiulcer, gastroprotective, hepatoprotective, cardiovascular, antiobesity, antiepileptic, antiasthmatic, antidiabetic, antiallergic, antiurolithiasis, diuretic, anthelmintic, antimicrobial, nootropic, wound-healing, and immunomodulatory properties. These vast ranges of activities may be ascribed due to phytoconstituents present in its bark, flower, leaf, pod, seed, and stem of M. oleifera. It could be a panacea remedy for malnutrition in developing countries of the African and South Asia subcontinent. It can effectively tackle malnutrition in India, especially Chhattisgarh. Various ways of incorporating M. oleifera as the main food source and as a potential food fortifier have been suggested. Multiple nutri-addition tricks are also suggested for nutrition fortification. The present study can open up new meadows for research and can provide better conceptual leads for future Moringa researches. The authors emphasize the need for future in-depth ethnopharmacological-leads-based research and clinical studies to expand M. oleifera pharmacological activities, clinical efficacy, and safety.

Acknowledgments

We thanks Prof. Brij Mohan Singh and Prof. Kishor Patwardhan, faculty of Ayurveda, Banaras Hindu University for guiding conceptual structuring and pre-submission review; Dr. Rupendra Chandrakar, Reader, Government Ayurved College, Raipur, for giving additional information about ethno-botanical practices of M. oleifera in Chhattisgarh region; Dr. Rashmi Sahu, Postgraduate student, Government Ayurved College, Raipur, for technical support, Dr. Sandeep Patwardhan, Bangalore, for grammatical correction and paper formatting. Authors are grateful to their parent institution for providing the library facility and support for this work.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Abstract
Introduction
Species Distribu...
Brief Botanical ...
Phytochemistry
Pharmacological ...
Traditional Ayur...
Clinical Trials ...
Toxicological St...
In Silico...
Patents and Curr...
Potential in Tac...
Chhattisgarh Pro...
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