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American Journal of Neuroscience 3 (1): 17-24, 2012 ISSN1948-9900 2012 Science Publications
Moringa Oleifera Leaves Extract Attenuates Male Sexual Dysfunction
1,3Thawatchai Prabsattroo, 2,3Jintanaporn Wattanathorn,3 4 2 3 13, Sitthichai Iamsa-ard,, Supaporn Muchimapura and, Wipawee Thukhammee
1Department of Physiology and Graduate School
(Neuroscience Program), Faculty of Medicine,2Department of Physiology, Faculty of Medicine,3Intergrative Complementary Alternative Medicine
Research and Development Group, 4Department of
Anatomy, Faculty of Medicine, Khon Kaen University,Khon Kaen, Thailand
Abstract: Problem statement: At present, the novel agent that is effective, cheap and easy to approach for treating
male sexual dysfunction is required due to the current poor therapeutic efficacy. Though Moringa oleifera is
reputed for aphrodisiac activity in traditional folklore, no scientific evidence is available. Therefore, we aimed to
determine the effect ofM.oleifera leaves extract on male sexual behaviors in animal model of sexual dysfunction.
Moreover, the possible underlying mechanisms were also investigated. Approach: Male Wistar rats, weighing
200-250 g, had been orally given M.oleifera leaves extract at doses of 10, 50 and 250 mg kg -1 BW once daily at 30
min before the exposure to 12-h immobilization stress for 14 days. They were assessed male sexual behaviors
including mounting, intromission and ejaculation numbers and latencies after single administration and every 7
days until the end of experiment. To further investigate the possible mechanisms of action, we also determined
serum testosterone level of all rats at the end of experiment together with the determination of suppression effect of
the plant extract on MAOB and PDE-5 activities. Results: The results showed that after single administration, rats
subjected to M.oleifera extract at dose of 10 mg kg -1 BW significantly enhanced mounting number. When the
treatment was prolonged to 7 days rats subjected to the low dose of extract showed the enhanced intromission
number whereas rats subjected to high dose of extract showed the enhanced mounting number. Our data also
showed no significant change in serum testosterone level. However, the extract could also suppress MAOB and
PDE-5 activities. Taken all together, the extract could enhance male sexual desire and performance via the
suppression of MAOB and PDE-5 activities. Conclusion: M.oleifera can be the potential sexual enhancer
particularly for acute and short term application. However, further researches are necessary.
Key words: Numerous health products, scientific evidence, sexual enhancer particularly, Erectile Dysfunction
(ED), harvested during, room temperature
INTRODUCTION
Sexual dysfunction has been recognized as one of the
important social and biological relationship in human life. This
condition affects the sexual life of millions of men worldwide.
The prevalence of male sexual dysfunction is increased as the
age advanced (Wattanathorn etat., 2012; Moreira et al, 2006).
Therefore, the sexual dysfunction is still increasing its
prevalence and importance. Sexual dysfunction caused by
various factors including stress. Despite the importance of
sexual dysfunction, the therapeutic efficacy is still not in
satisfaction level. The most well known drug used nowadays
appears to target only at intromission phase, the main problem
in Erectile Dysfunction (ED) which is the most commonly
found sexual dysfunction. However, sexual dysfunction refers
to a problem during any phase of the sexual response cycle.
Therefore, the searching for new agent targeting at numerous
phases of sexual response cycle which is more cheap has
gained much concentration.
Moringa oleifera Lam. or Drumstick tree, a plant in a
family of Moringaceae, is widely cultivated in Thailand. Both
leaves and fruit of this tree are edible. It is believed to be
miracle herbs because it can be used not only as food but also
as medicine which can cure
Corresponding Author: Jintanaporn Wattanathorn, Department of Physiology, Faculty of Medicine and Integrative Complementary Alternative
Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
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Am J . Neuroscience 3 (1): 17-24, 2012numerous ailments. The leaves ofM.oleifera have been used as
used as antiulcer, diuretic, anti-inflammatory and for wound
healing (Kirtikar and Basu, 1935; Caceres etal., 1992; Udupa
et al, 1994; Pal et a l , 1995). Moreover, it has been used to
enhance male sexual functions including libido, improve
sperm quality and anti-erectile dysfunction. Nowadays,
numerous health products of M.oleifera are available in the
market and claimed for the effect on male sexual functions as
mentioned earlier, no scientific evidence was observed until
now. Therefore, the current study aimed to determine the effect
ofM.oleifera leaves extract on male sexual behaviors and the
possible underlying mechanism in sexual dysfunction rats
induced by stress.
MATERIALS AND METHODS
Plant material: The fresh Moringa oleifera Lam
(Moringaceae) were harvested during November to December,
2010 from the Khon Kaen province Thailand. The plant
specimen was authenticated by Associate Professor Dr. Panee
Sirisa-ard, Faculty of Pharmaceutical Sciences, Chiangmai
University, Thailand. The voucher specimen was kept at
Integrative Complementary Alternative Medicine Research
and Development Group, Khon Kaen University, Khon Kaen,
Thailand.
Plant material preparation: The fresh leaves were
immediately cleaned, than cut into small pieces and dried at the
temperature less than 50C. The dried plant material was
ground into fine coarse powder and extracted with 50%
alcoholic. After that evaporation of solvent in rotary evaporator
affords a crude extract of the soluble components and filtrate
was lyophilized. The percent yield of extract was 17.49%. The
extract contained total phenolic compounds at concentration of
86.73-93.60.51 mg of GAE/g extract. The extracts were
stored at -25C in a dark bottle until used. The crude extract
was suspended in distilled water.
Animals: Healthy male Wistar rats (200-250 g) were obtained
from National Animal Center, Salaya, Nakorn Pathom and
were housed in group of 6 per cage in standard metal cages at
222C on 10:14 h light-dark cycle. All animals were given
access to food and water ad labium The experiments were
performed to minimize animal suffering in accordance with the
internationally accepted principles for laboratory use and care
of European Community (EEC directive of 1986;
86/609/EEC).The experimental protocols were approved by
the Institutional Animal Care and Use Committee.
Stress procedure: The restraint stress was performed during
the light cycle from 6.00 a.m. to 6.00 p.m. The restrainer was
made of transparent perforated plastic tube, 20 cm long and 7
cm in diameter. The rats were put into the restrainer, head first
and once in, the tubes were closed with plexiglass lids. The
animals fit tightly into the restrainers and it was not possible
for them to turn around. None stressed control rats were at thesame time briefly handled and returned to their home cages.
Evaluation of sexual behaviors: Male Wistar rats of proven
fertility were randomly divided into 4 groups of 6 animals each
as following; (1) Vehicle plus stress (2)- (4) M.oleifera plus
stress. Rats in group 1 were administered with distilled water
which used as vehicle for the plant extract then expose to the
12 h-restraint stress whereas rats in group (2)-(4) were
administered with the plant extract at doses of 10, 50 and 250
mg kg-1 BW plus stress exposure as mentioned earlier.
All substances treatments were administered 45 m prior
to the 12 h-restraint stress exposure. The treatment and the
stress-exposure were performed once daily and the sexual
behaviors assessments were performed blindly. The animals
were allowed to rest in order to refresh the animals 3 h after the
removal from restraint cage and then they were assessed the
sexual behaviors between 9.00 p.m. to 12.00 a.m. at roomtemperature 26-28C after single dose,1 and 2 weeks of
treatment. In order to assess the sexual behaviors, estrous
female rats were paired with male treated with single or
repeated doses of extract. Female rats were induced to estrous
by sequential administration of estradiol benzoate (Sigma, St.
Louis, MO) at dose of 2 ^g kg-1 BW and progesterone (Sigma,
St.Louis, MO) at dose of 500 ^g kg-1 BW were injected before
the determination of copulatory behaviors via subcutaneous
route 48 h and 6 h respectively. Sexual behaviors were
monitored in a separate room for 3 h in a clear plastic box via
blind observer 30 min at the start of first hour whereas the
whole duration of observation (3h) was recorded by digital
video recording. The assessed sexual parameters were
including the following parameters:Mounting number: The number of mounts without
intromission from the time of introduction of the female until
ejaculation:
Intromission number: The number of intromissions fromthe time of introduction of the female until ejaculation
Mount latency: The time interval between theintroductions of the female to the first mount by the male
Intromission latency: The interval from the time ofintroduction of the female to the first intromission by the
male
Ejaculation number: The number of ejaculation whichcharacterized by longer, deeper pelvic thrusting and slow
dismount followed by a period of inactivity
Ejaculation latency: The time interval between the firstintromission and ejaculation
Determination of testosterone level: Separate groups of
animals were used for the measurement of plasma testosterone
level of rats subjected to 12-h immobilization stress. At the end
of 14-day experimental period, the rat blood samples were
collected and kept on ice and then centrifuged immediately at
2000*g at 4C for 15 min. The obtained plasma was kept
at-80C until analysis. Testosterone levels were measured
using a commercially available radioimmunoassay (RIA) kit
(TESTO-CT2, Cisbio International, France).
Determination of monoamine oxidase type B inhibition:
The inhibitory action of the plant extract on monoamine
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Am J . Neuroscience 3 (1): 17-24, 2012oxidase type B was determined by incubating a series of
concentrations of the test samples in the reaction mixture
including rat brain homogenates. In brief, 2.75 mL Tris buffer
(0.1 M, pH 7.4) and 100 ^L of 0.1 M benzylamine was mixed
in quartz cuvette which was placed in double beam
spectrophotometer and followed by the addition of 150 ^L
solution of brain homogenate to initiate the enzymatic reaction.
The change in absorbance was recorded at wavelength of 249.5
nm for 5 min against the blank containing Tris buffer and
5-hydroxytryptamine (Xu et al., 2005).
Determination of Phosphodiesterase (PDE) activity:
Testis was collected from healthy Wistar male rat in order to
Determine Phosphodiesterase Enzyme (PDE) activity. The
testis was washed with PBS and weighted before cut to small
pieces. Then, it was homogenized with 5 volumes of lysate
RIPA buffer. The testicular solution was centrifuged at
14,000*g for 15 min at 4C and the supernatant was collected
and used as PDE substrate. M.oleifera leaves extract at the
various concentrations ranging from 2, 10, 100, 500, 2000 mg
mL-1 were prepared together with the positive control sildenafil
at dose of 10 mg mL-1. The standard curve was prepared from
PDE (testicular lysate) at the various concentrations. The
experiment was divide into 7 groups as following (1) control
group (untreated group), (2-6) M.oleifera leaves extract treated
groups at the various concentrations (2, 10, 100, 500, 2000 mg
ml) and (7) positive control (10 mg mL-1 of sildenafil citrate).
PDE-Glo Phosphodiesterase assays were performed in a
white 96-well microplate. In brief, phosphodiesterase substrate
or testicular lysate was incubated with cGMP. Then, PDE
reaction solutions were added and incubated for 20 min at
room temperature. The cGMP in the mixture then drives a
kinase reaction leading to a reduction of ATP levels. Following
the kinase reaction, an Kinase Glo reagent was added and
reactions were mixed and incubated for 10 min at room
temperature. Luminescence was measured using a SpectraMax
L microplate luminometer (MSD AT (US) Inc). The
luminescent signal produced is directly related to the amount of
ATP remaining and correlates with phosphodiesterase activity.
Statistic analysis: All data were expressed as meanSEM
value. The significant differences among various groups were
compared by ANOVA and followed by Duncan's test. The
statistical difference was regarded at p
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as mean SEM (n = 6 group )
Fig. 2: Effect ofM.oleifera leaves extract (10, 50, 250 mg kg 1 BW) on mount number. Data were presented as mean SEM (n = 6
group-1). * p
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Fig. 6: Effect ofM.oleifera leaves extract (10, 50, 250 mg kg 1 BW) on ejaculation number. Data were presented as mean SEM (n
= 6 group-1).
Fig. 5:Effect ofM.oleifera leaves extract (10, 50, 250 mg kg 1 BW) on ejaculation latency. Data were presented as mean SEM (n
= 6 group-1)
Baseline Single dose Day 7 Day 14D Vehicle + stress n M.oleifera 10 mg kg"1 BW + stress
M.oleifera 50 mg kgi BW + stress M.oleifera 250 mg kg i BW + stress
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SEM (n = 6 group-1)
Fig. 7: Effect ofM.oleifera leaves extract (0, 2, 10, 100, 500, 2000 g ml-1) and Sildenafil citrate (10 g mL-1) on phosphodiesterase
(PDE) activity. Data were presented as mean SEM. a aa p
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Effect of M.oleifera leaves extract on monoamine oxidase
type B (MAOB) activity: The effect of M.oleifera leaves
extract on MAOb activity was evaluated and the results wereshown in Fig. 8. Our data clearly revealed that the extract at
concentration of 50,100, 250, 500 and 1000 mg mL-1 could
significantly suppress MAOB activity (p-value
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Project of Thailand, Office of the Higher Education
Commission, through the Food and Functional Food Research
Cluster of Khon Kaen University, Integrative Complementary
Alternative Medicine Research and Development Group, Khon
Kaen University. Moreover, we also would like to express our
sincere thank to Associate Professor Bungorn Sripanidkulchai,
Director of Center for Research and Development of Herbal
Health Product, Khon Kaen University for her kindly
management through Functional Food Cluster and Associate
Professor Panee Sirisa-ard for her authentication.
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Bagatell, C.J., J.R. Heiman, J.E. Rivier and W.J. Bremner,
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Gingel, K. Tang, L.A. Turner and M.E. Price et al, 1998.
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2171. DOI: 10.1016/S0022-5347(01)63299-3 Caceres, A., A.
Saravia, S. Rizzo, L. Zabala, E.D. Leon and F. Nave, 1992.
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(92)90049-W Dominguez, J.M. and E.M. Hull, 2005.
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Physiol. Behav., 86: 356-368. PMID: 16135375 Glover, V., M.
Sandler, F. Owen and G.J. Riley, 1977. Dopamine is a
monoamine oxidase B substrate in man. Nature, 265: 80-81.
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Indian Medicinal Plants. 2nd Edn., Lalit Mohan Basu,
Allahabad.
Moreira, E.D., S.C. Kim, D. Glasser and C. Gingell, 2006.
Sexual activity, prevalence of sexual problems and
associated help-seeking patterns in men and women aged
40-80 years in Korea: data from the Global Study of
Sexual Attitudes and Behaviors (GSSAB). J. Sex Med., 3:
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Moreland, R.B., I. Goldstein and A. Traish, 1998.
Sildenafil, a novel inhibitor of phosphodiesterase type 5
in human corpus cavernosum smooth muscle cells. Life
Sci., 62: 309-318. PMID: 9600334
Pal, S.K., P.K. Mukherjee and B.P. Saha, 1995. Studies on the
antiulcer activity of Moringa oleifera leaf extract on
gastric ulcer models in rats. Phytother Res., 9: 463-465.
DOI: 10.1002/ptr.2650090618 Seftel, A.D., R.J. Mack,
A.R. Secrest and T.M. Smith, 2004. Restorative increases
in serum testosterone levels are significantly correlated to
improvements in sexual functioning. J. Androl., 25:
963-972. PMID: 15477371 Udupa, S.L., A.L. Udupa and
D.R. Kulkarni, 1994. Studies on anti-inflammatory and
wound healing properties of Moringa oleifera and Aegle
marmelos. Fitoterapia, 65: 119-123. Wang, C., G.
Cunningham, A. Dobs, A. Iranmanesh and A.M.
Matsumoto et al., 2004. Long-term testosterone gel
(AndroGel) treatment maintains beneficial effects on
sexual function and mood, lean and fat mass and bone
mineral density in hypogonadal men. J. Clin. Endocrinol.Metab., 89: 2085-2098. DOI: 10.1210/jc.2003-032006
Wattanathorn, J., P. Pangphukiew, S. Muchimapura, K.
Sripanidkulchai and B. Sripanidkulchai, 2012.
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10.2844/ajabssp.2012.114.120 Xu, Y., B.S. Ku, H.Y.
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10.1016/j.ejphar.2005.06.002PHYTOTHERAPY RESEARCHPhytother.
Res. 21, 17-25 (2007)
Published online 6 November 2006 in Wiley InterScience unci Juciivc
(www.interscience.wiley.com) DOI: 10.1002/ptr.2023 0,1"
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Copyright 2006 John Wiley & Sons, Ltd.
REVIEWARTICLE
Moringa oleifera: A Food Plant with MultipleMedicinal Uses
Farooq Anwar1, Sajid Latif1, Muhammad Ashraf2 and Anwarul Hassan Gilani3*1Department of Chemistry, University of Agriculture, Faisalabad-38040, Pakistan 'Department of Botany, University of Agriculture, Faisalabad-38040,
Pakistan3Department of Biological and Biomedical Sciences, Aga Khan University Medical College, Karachi-74800, Pakistan
Mor inga oleiferaLam (Moringaceae) is a highly valued plant, distributed in many countries of the tropics and
subtropics. It has an impressive range of medicinal uses with high nutritional value. Different parts of this plant contain
a profile of important minerals, and are a good source of protein, vitamins, -carotene, amino acids and various
phenolics. The Moringaplant provides a rich and rare combination of zeatin, quercetin, j3- sitosterol, caffeoylquinic acid
and kaempferol. In addition to its compelling water purifying powers and high nutritional value, M. oleiferais very
important for its medicinal value. Various parts of this plant such as the leaves, roots, seed, bark, fruit, flowers and
immature pods act as cardiac and circulatory stimulants, possess antitumor, antipyretic, antiepileptic,
antiinflammatory, antiulcer, antispasmodic, diuretic, antihypertensive, cholesterol lowering, antioxidant, antidiabetic,hepatoprotective, antibacterial and antifungal activities, and are being employed for the treatment of different ailments
in the indigenous system of medicine, particularly in South Asia. This review focuses on the detailed phytochemical
composition, medicinal uses, along with pharmacological properties of different parts of this multipurpose tree.
Copyright 2006 John Wiley & Sons, Ltd.
Keywords: Moringa oleifera; phytomedicine; food plant; medicinal uses; pharmacological properties; natural coagulant.
INTRODUCTION
Moringa oleifera Lam (syn. M. ptreygosperma Gaertn.) is one of
the best known and most widely distributed and naturalized species
of a monogeneric family Moringaceae (Nadkarni, 1976;
Ramachandran et al., 1980). The tree ranges in height from 5 to 10
m (Morton, 1991). It is found wild and cultivated throughout theplains, especially in hedges and in house yards, thrives best under
the tropical insular climate, and is plentiful near the sandy beds of
rivers and streams (The Wealth of India, 1962; Qaiser, 1973). It
can grow well in the humid tropics or hot dry lands, can survive
destitute soils, and is little affected by drought (Morton, 1991). It
tolerates a wide range of rainfall with minimum annual rainfall
requirements estimated at 250 mm and maximum at over 3000 mm
and a pH of 5.0-9.0 (Palada and Changl, 2003).
Moringa oleifera, native of the western and sub- Himalayan
tracts, India, Pakistan, Asia Minor, Africa and Arabia (Somali et
al., 1984; Mughal et al., 1999) is now distributed in the
Philippines, Cambodia, Central America, North and South
America and the Caribbean Islands (Morton, 1991). In some parts
of the worldM. oleifera is referred to as the 'drumstick tree' or the'horse radish tree', whereas in others it is known as the
* Correspondence to: Professor Anwarul Hassan Gilani, Department of
Biological and Biomedical Sciences, Aga Khan University Medical College,
Karachi-74800, Pakistan. E-mail:[email protected]
kelor tree (Anwar and Bhanger, 2003). While in the Nile valley,
the name of the tree is 'Shagara al Rauwaq', which means 'tree for
purifying' (Von Maydell, 1986). In Pakistan, M. oleifera is locally
known as 'Sohanjna' and is grown and cultivated all over the
country (Qaiser, 1973; Anwaret al., 2005).
Moringa oleifera is an important food commodity which has
had enormous attention as the 'natural nutrition of the tropics'. The
leaves, fruit, flowers and immature pods of this tree are used as ahighly nutritive vegetable in many countries, particularly in India,
Pakistan, Philippines, Hawaii and many parts of Africa (D'souza
and Kulkarni, 1993; Anwar and Bhanger, 2003; Anwar et al.,
2005). Moringa leaves have been reported to be a rich source of
-carotene, protein, vitamin C, calcium and potassium and act as a
good source of natural antioxidants; and thus enhance the shelf-life
of fat containing foods due to the presence of various types of
antioxidant compounds such as ascorbic acid, flavo- noids,
phenolics and carotenoids (Dillard and German, 2000; Siddhuraju
and Becker, 2003). In the Philippines, it is known as 'mother's best
friend' because of its utilization to increase woman's milk
production and is sometimes prescribed for anemia (Estrella et al.,2000; Siddhuraju and Becker, 2003).
A number of medicinal properties have been ascribed to various
parts of this highly esteemed tree (Table 1). Almost all the parts of
this plant: root, bark, gum, leaf, fruit (pods), flowers, seed and seed
oil have been used for various ailments in the indigenous medicine
of South Asia, including the treatment of inflammation and
infectious diseases along with cardiovascular, gastrointestinal,
hematological and hepatorenal disorders
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18 F. ANWARET AL.
Copyright 2006 John Wiley & Sons, Ltd. Phytother. Res. 21, 17-25 (2DOI: 10.100
Table 1. Some common medicinal uses of different parts ofMoringa oleiferaMedicinalUses
Antilithic,rubefacient,vesicant,carminative,antifertility,anti-inflammatory,stimulantinparalyticafflictions;actasacardiac/circulatorytonic,usedasa
laxative,abortifacient,treatingrheumatism,inflammations,articularpains,
lowerbackorkidneypainandconstipation,
Purgative,appliedaspoulticetosores,rubbedonthetemplesfor
headaches,usedforpiles,fevers,sorethroat,bronchitis,eyeandear
infections,scurvyandcatarrh;leafjuiceisbelievedtocontrolglucose
levels,appliedtoreduceglandularswelling
Rubefacient,vesicantandusedtocureeyediseasesandforthetreatment
ofdeliriouspatients,preventenlargementofthespleenandformationof
tuberculousglandsoftheneck,todestroytumorsandtohealulcers.The
juicefromtherootbarkisputintoearstorelieveearachesandalsoplaced
inatoothcavityasapainkiller,andhasanti-tubercularactivity
Usedfordentalcaries,andisastringentandrubefacient;Gum,mixedwith
sesameoil,isusedtorelieveheadaches,fevers,intestinalcomplaints,
dysentery,asthmaandsometimesusedasanabortifacient,andtotreat
syphilisandrheumatism
Highmedicinalvalueasastimulant,aphrodisiac,abortifacient,cholagogue;
usedtocureinflammations,musclediseases,hysteria,tumors,and
enlargementofthespleen;lowertheserumcholesterol,phospholipid,
triglyceride,VLDL,LDLcholesteroltophospholipidratioandatherogenic
index;decreaselipidprofileofliver,heartandaortain
hypercholesterolaemicrabbitsandincreasedtheexcretionoffaecal
cholesterol
Seedextractexertsitsprotectiveeffectbydecreasingliverlipidperoxides,
antihypertensivecompoundsthiocarbamateandisothiocyanateglycosids
havebeenisolatedfromtheacetatephaseoftheethanolicextractof
Mo r i nga pods
(The Wealth of India, 1962; Singh and Kumar, 1999; Morimitsu et
al., 2000; Siddhuraju and Becker, 2003).
The seeds ofMoringa are considered to be antipyretic, acrid,
bitter (Oliveira et al., 1999) and reported to show antimicrobial
activity (The Wealth of India, 1962). The seed can be consumed
fresh as peas; or pounded, roasted, or pressed into sweet,
non-desiccating oil, commercially known as 'Ben oil' of high
quality. The unique property is the ability of its dry, crushed seed
and seed press cake, which contain polypeptides, to serve as natu-
ral coagulants for water treatment (Ndabigengesere and Narasiah,
1998).
So far no comprehensive review has been compiled from the
literature encompassing the efficacy of this plant in all dimensions.Its versatile utility as a medicine, functional food, nutraceutical and
water purifying potential motivated us to bridge the information
gap in this area, and to write a comprehensive review on the
medicinal, phytochemical and pharmacological attributes of this
plant of high economic value.
PHYTOCHEMISTRY
Moringa oleifera is rich in compounds containing the simple
sugar, rhamnose and a fairly unique group of compounds called
glucosinolates and isothiocyanates (Fahey et al., 2001; Bennett et
al., 2003). The stem bark has been reported to contain twoalkaloids, namely moringine and moringinine (Kerharo, 1969).
Vanillin, -sitosterol [14], -sitostenone, 4-hydroxymellin and
octacosanoic acid have been isolated from the stem ofM. oleifera
(Faizi et al., 1994a).
Purified, whole-gum exudate from M. oleifera has been found to
contain L-arabinose, -galactose, -glucuronic acid, and L-rhamnose,
-mannose and -xylose, while a homogeneous, degraded-gum
polysaccharide consisting of L-galactose, -glucuronic acid and
L-mannose has been obtained on mild hydrolysis of the whole gum
with acid (Bhattacharya et al., 1982).
Flowers contain nine amino acids, sucrose, D-glucose, traces of
alkaloids, wax, quercetin and kaempferat; the ash is rich in
potassium and calcium (Ruckmani et al., 1998). They have also
been reported to contain some flavonoid pigments such as
alkaloids, kaempherol, rhamnetin, isoquercitrin and kaempferitrin
(Faizi et al., 1994a; Siddhuraju and Becker, 2003).
Antihypertensive compounds thiocarbamate and isothiocyanateglycosides have been isolated from the acetate phase of the ethanol
extract ofMoringa pods (Faizi et al., 1998). The cytokinins have
been shown to be present in the fruit (Nagaret al., 1982). A new
0-ethyl-4-(a-L-rhamnosyloxy)benzyl carbamate [11]
Plantpart References Root The Wea l t h o f I nd ia , 1962;Padmaraoe t a l . ,
1996;Dahot,1988;
Ruckmani e t a l . , 1998
Morton,1991;Fuglie,2001;
Makonnen e t a l . , 1997;
The Wea l t h o f I nd ia ,
1962;Dahot,1988
Bhatnagar e t a l . , 1961;
Siddhuraju and Becker,
2003
Leave
Stembark
GumFuglie,2001
Nair and Subramanian,
1962;Bhattacharya e t a l . ,
1982; Dahot, 1998;
Siddhuraju and Becker,
2003;Mehta e t a l . , 2003
Flower
Seed Faizi e t a l ., 1998; Lalas
andTsaknis,2002
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ORINGA OLEIFERA 19
Copyright 2006 John Wiley & Sons, Ltd.
together with seven known bioactive compounds, 4(a-
L-rhamnosyloxy)-benzyl isothiocyanate [3], niazimicin [4], 3-
O-(6'- O-oleoyl--D -glucopyranosyl)- -sitosterol [15],
^-sitosterol-3-O-^-D-glucopyranoside [16], niazirin
[12] , ^-sitosterol [14] and glycerol-1-(9-octadecanoate)[13] have been isolated from the ethanol extract of the Moringaseed (Guevara et al., 1999). Figure 1 shows the structures of
selected phytochemicals fromMoringa.
Lately, interest has been generated in isolating hormones/growth
promoters from the leaves of M. oleifera. Nodulation of
black-gram (Vigna munga L.)
14: R= H
15: R= 6'-0-oleoyl-P-D-glucop5Tanosyl 16: R =
P-D-glucopyranosylFiqure 1. Structures of selected phytochemicals from Moringa: niazinin A [1], 4-(4'-0-acetyl-a-L-rhamnopyranosyloxy)benzyl isoth- iocyanate [2],4-(-L-rhamnopyranosyloxy)benzyl isothiocyanate [3], niazimicin [4], 4-(a-L-rhamnopyranosyloxy)benzyl glucosinolate [5], benzyl isothiocyanate [6], aglyconofdeoxy-niazimicine(N-benzyl,S-ethylthioformate) [7],pterygospermin [8],niaziminin [9 + 10], 0-ethyl-4-(a-L-rhamnosyloxy)benzylcarbamate [11],niazirin [12],glycerol-1-(9-octadecanoate) [13],^-sitosterol [14],3-0-(6'-0-oleoyl- -D-glucopyranosyl)-3-sitosterol [15],^-sitosterol-3-O-^-D-glucopyranoside [16].
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20 F. ANWARET AL.
Copyright 2006 John Wiley & Sons, Ltd.
has been shown to increase vigorously with the application of an
aqueous-ethanol extract (Bose, 1980) of M. oleifera leaves,
although the nature of the active ingredient is still unknown.
Moringa leaves act as a good source of natural antioxidant due to
the presence of various types of antioxidant compounds such as
ascorbic acid, flavonoids, phenolics and carotenoids (Anwaret al.,
2005; Makkar and Becker, 1996). The high concentrations of
ascorbic acid, oestrogenic substances and -sitosterol [16], iron,
calcium, phosphorus, copper, vitamins A, B and C, a-tocopherol,
riboflavin, nicotinic acid, folic acid, pyridoxine, -carotene,
protein, and in particular essential amino acids such as methionine,
cystine, tryptophan and lysine present in Moringa leaves and pods
make it a virtually ideal dietary supplement (Makkar and Becker,
1996).The composition of the sterols of Moringa seed oil mainly
consists of campesterol, stigmasterol, -sitosterol, A5-avenasterol
and clerosterol accompanied by minute amounts of
24-methylenecholesterol, A7-campestanol, stigmastanol and
28-isoavenasterol (Tsaknis et al., 1999; Anwar and Bhanger, 2003;
Anwaret al., 2005; Table 2). The sterol composition of the major
fractions ofMoringa seed oil differs greatly from those of most of
the conventional edible oils (Rossell, 1991). The fatty acid com-
position ofM. oleifera seed oil reveals that it falls in the category
of high-oleic oils (C18:1, 67.90%-76.00%). Among the other
component fatty acids C16:0 (6.04%- 7.80%), C18:0
(4.14%-7.60%), C20:0 (2.76%-4.00%), and C22:0 (5.00%-6.73%)
are important (Tsaknis etal., 1999; Anwar and Bhanger, 2003;
Anwar et al., 2005). Moringa oleifera is also a good source ofdifferent tocopherols (a-, y-and 5-); the concentration of those is
reported to be 98.82-134.42, 27.90-93.70, and 48.0071.16 mg/kg,
respectively (Anwar and Bhanger, 2003; Tsaknis et al., 1999).
MEDICINAL USES AND PHARMACOLOGICAL
PROPERTIES
Moringa oleifera also has numerous medicinal uses, which have
long been recognized in the Ayurvedic and
Unani systems of medicine (Mughal et al., 1999). The medicinal
attributes (Table 1) and pharmacological activities ascribed to
various parts ofMoringa are detailed below.
Antihypertensive, diuretic and cholesterol lowering
activities
The widespread combination of diuretic along with lipid and blood
pressure lowering constituents make this plant highly useful in
cardiovascular disorders. Moringa leaf juice is known to have a
stabilizing effect on blood pressure (The Wealth of India, 1962;
Dahot, 1988). Nitrile, mustard oil glycosides and thiocarbamate
glycosides have been isolated from Moringa leaves, which were
found to be responsible for the blood pressure lowering effect
(Faizi et al., 1994a; 1994b; 1995). Most of these compounds,
bearing thiocarbamate, carbamate or nitrile groups, are fully
acetylated glycosides, which are very rare in nature (Faizi et al.,
1995). Bioassay guided fractionation of the active ethanol extract
of Moringa leaves led to the isolation of four pure compounds,
niazinin A [1], niazinin [1] B, niazimicin [4] and niazinin A + B
which showed a blood pressure lowering effect in rats mediatedpossibly through a calcium antagonist effect (Gilani et al., 1994a).
Another study on the ethanol and aqueous extracts of whole
pods and its parts, i.e. coat, pulp and seed revealed that the blood
pressure lowering effect of seed was more pronounced with
comparable results in both ethanol and water extracts indicating
that the activity is widely distributed (Faizi et al., 1998).
Activity-directed fractionation of the ethanol extract of pods ofM.
oleifera has led to the isolation of thiocarbamate and
isothiocyanate glycosides which are known to be the hypotensive
principles (Faizi et al., 1995). Methyl p- hydroxybenzoate and
-sitosterol (14), investigated in the pods ofM. oleifera have also
shown promising hypotensive activity (Faizi et al., 1998).
Moringa roots, leaves, flowers, gum and the aqueous infusion of
seeds have been found to possess diuretic activity (Morton, 1991;Caceres et al., 1992) and such diuretic components are likely to
play a complementary
Table 2. Sterol composition (grams per 100 g of fatty acids) of the M. oleiferaoilsSterol AnwarandBhanger,
2003
LalasandTsaknis,
2002
Tsaknis e t a l . , 1999
Cholesterol Notreported 0.10 0.13
Brassicasterol Notreported 0.05 0.06
24-methylenecholesterol 1.49 0.08 0.88
Campesterol 16.00 15.29 15.13
Campestanol Notreported 0.33 0.35
A7-campestanol 0.50 Notreported Notreported
Stigmasterol 19.00 23.06 16.87
Ergostadienol Notreported 0.35 0.39
Clerosterol 1.95 1.22 2.52
Stigmastanol 1.00 0.64 0.86
^-sitosterol 46.65 43.65 50.07
A -avenasterol 0.96 Notdetected 1.11
A5-avenasterol 10.70 11.61 8.84
28-isoavenasterol 0.50 0.25 1.40
A7,14
Stigmastadienol Notreported 0.39 Notreported
A,
Stigmastanol Notreported 0.85 0.44
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ORINGA OLEIFERA 21
Copyright 2006 John Wiley & Sons, Ltd.
role in the overall blood pressure lowering effect of this plant.
The crude extract of Moringa leaves has a significant
cholesterol lowering action in the serum of high fat diet fed rats
which might be attributed to the presence of a bioactive
phytoconstituent, i.e. -sitosterol (Ghasi et al., 2000). Moringafruit has been found to lower the serum cholesterol, phospholipids,
triglycerides, low density lipoprotein (LDL), very low density
lipoprotein (VLDL) cholesterol to phospholipid ratio, atherogenic
index lipid and reduced the lipid profile of liver, heart and aorta in
hypercholesteremic rabbits and increased the excretion of fecal
cholesterol (Mehta et al., 2003).
Antispasmodic, antiulcer and hepatoprotective
activities
M. oleifera roots have been reported to possess anti- spasmodic
activity (Caceres et al., 1992). Moringa leaves have been
extensively studied pharmacologically and it has been found that
the ethanol extract and its constituents exhibit antispasmodic
effects possibly through calcium channel blockade (Gilani et al.,
1992; 1994a; Dangi et al., 2002). The antispasmodic activity of the
ethanol extract of M. oleifera leaves has been attributed to the
presence of 4-[a-(L-rhamnosyloxy) benzyl]- o-methyl
thiocarbamate [3] (trans), which forms the basis for its traditional
use in diarrhea (Gilani et al., 1992). Moreover, spasmolytic
activity exhibited by different constituents provides
pharmacological basis for the traditional uses of this plant in
gastrointestinal motility disorder (Gilani et al., 1994a).
The methanol fraction of M. oleifera leaf extract showed
antiulcerogenic and hepatoprotective effects in rats (Pal et al.,
1995a). Aqueous leaf extracts also showed antiulcer effect (Pal et
al., 1995a) indicating that the antiulcer component is widely
distributed in this plant.Moringa roots have also been reported to
possess hepatoprotective activity (Ruckmani et al., 1998). The
aqueous and alcohol extracts from Moringa flowers were also
found to have a significant hepatoprotective effect (Ruckmani et
al., 1998), which may be due to the presence of quercetin, a well
known flavonoid with hepato- protective activity (Gilani et al.,
1997).
Antibacterial and antifungal activities
Moringa roots have antibacterial activity (Rao et al., 1996) and are
reported to be rich in antimicrobial agents. These are reported to
contain an active antibiotic principle, pterygospermin [8], which
has powerful antibacterial and fungicidal effects (Ruckmani et al.,1998). A similar compound is found to be responsible for the
antibacterial and fungicidal effects of its flowers (Das et al., 1957).
The root extract also possesses antimicrobial activity attributed to
the presence of 4-a-L-rhamnosyloxy benzyl isothiocyanate [3]
(Eilert et al., 1981). The aglyc- one of deoxy-niazimicine
(N-benzyl, S-ethyl thiofor- mate) [7] isolated from the chloroform
fraction of an ethanol extract of the root bark was found to be
responsible for the antibacterial and antifungal activities (Nikkon
et al., 2003). The bark extract has been shown to possess antifungal
activity (Bhatnagaret al., 1961), while the juice from the stem bark
showed antibacterial effect against Staphylococcus aureus (Mehta
et al., 2003). The fresh leaf juice was found to inhibit the growth of
microorganisms (Pseudomonas aeruginosa and Staphylococcus
aureus), pathogenic to man (Caceres et al., 1991).
Antitumor and anticancer activities
Makonnen et al. (1997) found Moringa leaves to be a potential
source for antitumor activity. O-Ethyl-
4-(a-L-rhamnosyloxy)benzyl carbamate [11] together with
4(a-L-rhamnosyloxy)-benzyl isothiocyanate [3], niazimicin [4] and
3-O-(6'-O-oleoyl-^-D-glucopyranosyl)- -sitosterol [15] have been
tested for their potential antitumor promoting activity using an in
vitro assay which showed significant inhibitory effects on Epstein-Barr virus-early antigen. Niazimicin has been proposed to be a
potent chemopreventive agent in chemical car- cinogenesis
(Guevara et al., 1999). The seed extracts have also been found to
be effective on hepatic carcinogen metabolizing enzymes,
antioxidant parameters and skin papillomagenesis in mice (Bharali
et al., 2003). A seed ointment had a similar effect to neomycin
against Staphylococcus aureus pyodermia in mice (Caceres and
Lopez, 1991).
It has been found that niaziminin [9 + 10], a thio- carbamate
from the leaves of M. oleifera, exhibits inhibition of
tumor-promoter-induced Epstein-Barr virus activation. On the
other hand, among the isothiocyanates, naturally occurring
4-[(4'-O-acetyl-a-i-rhamnosyloxy) benzyl] [2], significantly
inhibited tumor-promoter- induced Epstein-Barr virus activation,suggesting that the isothiocyano group is a critical structural factor
for activity (Murakami et al., 1998).
Other diverse activities
Moringa oleifera has also been reported to exhibit other diverse
activities. Aqueous leaf extracts regulate thyroid hormone and can
be used to treat hyperthyroidism and exhibit an antioxidant effect
(Pal et al., 1995a; 1995b; Tahiliani and Kar, 2000). A methanol
extract of M. oleifera leaves conferred significant radiation
protection to the bone marrow chromosomes in mice (Rao et al.,
2001). Moringa leaves are effective for the regulation of thyroid
hormone status (Tahiliani and Kar, 2000).
A recent report showed that M. oleifera leaf may be applicableas a prophylactic or therapeutic anti-HSV (Herpes simplex virus
type 1) medicine and may be effective against the
acyclovir-resistant variant (Lipipun et al., 2003). Table 1 depicts
some common medicinal uses of different parts of this plant. The
flowers and leaves also are considered to be of high medicinal
value with anthelmintic activity (Bhattacharya et al., 1982). An
infusion of leaf juice was shown to reduce glucose levels in rabbits
(Makonnen et al., 1997).
Moringa oleifera is coming to the forefront as a result of
scientific evidence that Moringa is an important source of naturally
occurring phytochemicals and this provides a basis for future
viable developments. Different parts of M. oleifera are also
incorporated in various marketed health formulations, such as
Rumalaya andSeptilin (the Himalaya Drug Company, Bangalore, India),
Orthoherb (Walter Bushnell Ltd, Mumbai, India), Kupid Fort
(Pharma Products Pvt. Ltd, Thayavur, India) and Livospin
(Herbals APS Pvt. Ltd, Patna, India), which are reputed as
remedies available for a variety of human health disorders (Mehta
et al., 2003).
Moringa seeds have specific protein fractions for skin and hair
care. Two new active components for the cosmetic industry have
been extracted from oil cake. Purisoft consists of peptides of the
Moringa seed. It protects the human skin from environmental
influences and combats premature skin aging. With dual activity,
antipollution and conditioning/strengthening of hair, the M.
oleifera seed extract is a globally acceptable innovative solution
for hair care (Stussi et al., 2002).
WATER PURIFYING ATTRIBUTES OF M.
OLEIFERA SEED
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22 F. ANWARET AL.
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Moringaseeds as coagulant
Moringa seeds are one of the best natural coagulants discovered so
far (Ndabigengesere and Narasiah, 1998). Crushed seeds are a
viable replacement of synthetic coagulants (Kalogo et al., 2000).
In Sudan, seed crude extract is used instead of alum by rural
women to treat the highly turbid Nile water because of a traditional
fear of alum causing gastrointestinal disturbances and Alzheimer's
disease (Crapper et al., 1973; Milleret al., 1984; Martyn et al.,
1989; Muyibi, 1994).
Moringa seeds are very effective for high turbidity water and
show similar coagulation effects to alum (Muyibi and Evison,
1995b). The coagulation effectiveness of M. oleifera varies
depending on the initial turbidity and it has been reported that M.
oleifera could reduce turbidity by between 92% and 99% (Muyibi
and Evison, 1995b). Moringa seeds also have softening properties
in addition to being a pH correctant (alkalinity reduction), as well
as exhibiting a natural buffering capacity, which could handle
moderately high to high alkaline surface and ground waters. The
Moringa seeds can also be used as an antiseptic in the treatment of
drinking water (Obioma and Adikwu, 1997).
Ongoing research is attempting to characterize and purify the
coagulant components of Moringa seeds (Ndabigengesere et al.,
1995; Gassenschmidt et al., 1995). It is believed that the seed is an
organic natural polymer (Jahn, 1984). The active ingredients are
dimeric proteins with a molecular weight of about 1300 Da and an
iso-electric point between 10 and 11 (Ndabigengesere et al., 1995).
The protein powder is stable and totally soluble in water.
Moringa coagulant protein can be extracted by water or salt
solution (commonly NaCl). The amount and effectiveness of the
coagulant protein from salt and water extraction methods vary
significantly. In crude form, the salt extract shows a better
coagulation performance than the corresponding water extract
(Okuda et al., 1999). This may be explained by the presence of ahigher amount of soluble protein due to the salting-in
phenomenon. However, purification of the M. oleifera coagulant
protein from the crude salt extract may not be technically and
economically feasible.
The coagulation mechanism of the M. oleifera coagulant protein
has been explained in different ways. It has been described as
adsorption and charge neutralization (Ndabigengesere et al., 1995;
Gassenschmidt et al., 1995) and interparticle bridging (Muyibi and
Evison, 1995a). Flocculation by inter-particle bridging is mainly
characteristic of high molecular weight polyelectrolytes. Due to
the small size of the M. oleifera coagulant protein (6.5-13 kDa), a
bridging effect may not be considered as the likely coagulation
mechanism. The high positive charge (pI above 10) and small size
may suggest that the main destabilization mechanism could beadsorption and charge neutralization.
Microbial elimination with Moringaseeds
Moringa seeds also possess antimicrobial properties (Olsen, 1987;
Madsen et al., 1987). Broin et al. (2002) reported that a
recombinant protein in the seed is able to flocculate Gram-positive
and Gram-negative bacterial cells. In this case, microorganisms
can be removed by settling in the same manner as the removal of
colloids in properly coagulated and flocculated water (Casey,
1997). On the other hand, the seeds may also act directly upon
microorganisms and result in growth inhibition. Antimicrobial
peptides are thought to act by disrupting the cell membrane or byinhibiting essential enzymes (Silvestro et al., 2000; Suarez et al.,
2003). Sutherland et al. (1990) reported that Moringa seeds could
inhibit the replication of bacteriophages. The antimicrobial effects
of the seeds are attributed to the compound 4(a-L-rhamnosyloxy)
benzyl isothiocynate (Eilert et al., 1981).
Moringaseeds as biosorbent
Moringa seeds could be used as a less expensive bio- sorbent for
the removal of cadmium (Cd) from aqueous media (Sharma et al.,
2006). The aqueous solution of Moringa seed is a heterogeneous
complex mixture having various functional groups, mainly low
molecular weight organic acids (amino acids). These amino acids
have been found to constitute a physiologically active group of
binding agents, working even at a low concentration, which
because of the ability to interact with metal ions is likely to
increase the sorption of metal ions (Brostlap and Schuurmans,
1988). The proteineous amino acids have a variety of structurally
related pH dependent properties, generating a negatively charged
atmosphere and play an important role in the binding of metals
(Sharma et al., 2006).
FUTURE PROSPECTS
So far numerous studies have been conducted on different parts of
M. oleifera, but there is a dire need to isolate and identify new
compounds from different parts of the tree, which have possible
antitumor promoters as well as inhibitory properties. Although
preliminary studies are under way in different laboratories to use
the antispasmodic, antiinflammatory, antihypertensive and diuretic
activities ofM. oleifera seed, these studies should be extended to
humans in view of the edible nature of the plant. Moringa roots and
leaves have been used traditionally to treat constipation. Studies to
verify these claims need to be carried out in the light of the reported
antispasmodic activities, which are contrary to its medicinal use as
a gut motility stimulant. Earlier studies on the presence of a
combination of spasmogenic and spasmolytic constituents in
different plants used for constipation (Gilani et al., 2000; 2005a;Bashiret al., 2006) might be of some guidance in designing experi-
ments in which the presence of antispasmodic constituents at
higher doses are explained as a possible mode to offset the
side-effects usually associated with high dose of laxative therapy.
Similarly, the known species differences in the pharmacological
actions of medicinal plants (Ghayur et al., 2005; Ghayur and
Gilani, 2006) may also be taken into account when planning
studies involving contradictory results.
Food plants are considered relatively safe as they are likely to
contain synergistic and/or side effect neutralizing combinations of
activities (Gilani and Atta-ur- Rahman, 2005). Moringa oleifera,
known to be rich in multiple medicinally active chemicals, may be
a good candidate to see if it contains effect enhancing and/or
side-effects neutralizing combinations. Medicinal plants arerelatively rich in their contents of calcium channel blockers
(CCBs) which are known to possess a wide variety of
pharmacological activities such as antihyper- tensive,
hepatoprotective, antiulcer, antiasthmatic, anti- spasmodic and
antidiarroeal (Stephens and Rahwan, 1992; Gilani et al., 1994b;
1999; 2005b; Yaeesh et al., 2006; Ghayur et al., 2006) and it
remains to be seen whether such activities reported to be present in
Moringa oleifera have a direct link with the presence of CCBs.
Niazimicin, a potent antitumor promoter in chemical
carcinogenesis is present in the seed; its inhibitory mechanism on
tumor proliferation can be investigated by isolating more pure
samples. The mechanism of action ofM. oleifera as prophylactic
or therapeutic anti- HSV medicines for the treatment of HSV-1
infection also needs to be examined.
The available information on the -, - and y- tocopherol
content in samples of various parts of this edible plant is very
limited. -Carotene and vitamins A and C present in M. oleifera,
serve as an explanation for their mode of action in the induction of
antioxidant profiles, however, the exact mechanism is yet to be
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ORINGA OLEIFERA 23
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elucidated. -Carotene of M. oleifera leaves exerts a more
significant protective activity than silymarin against anti-
tubercular induced toxicity. It would be interesting to see if it also
possesses hepatoprotective effect against other commonly used
hepatotoxic agents such as CCl4 and galactosamine, which areconsidered more suitable models and close to human viral hepatitis
(Gilani and Janbaz, 1995; Yaeesh et al., 2006).
Although Moringa leaves are considered a best protein source,
it still has to be shown whether or not this protein source could
compete with the more common protein sources in highly
productive growing or milk- producing ruminants.
Many studies have also been conducted on the performance of
Moringa seeds as an alternative coagulant, coagulant aid and in
conjunction with alum for treating waste water. Therefore, it is
important to identify the active constituents ofMoringa seed for a
better understanding of the coagulation mechanism. Reports on the
antimicrobial effects of the protein purified from M. oleifera are
very rare.
Since this plant naturally occurs in varying habitats, it is naive to
expect a great magnitude of variation in the concentration andcomposition of chemical ingredients in different parts of the tree.
However, the extent to which the chemical composition varies in
populations adapted to varying habitats is not known. Thus,
detailed studies are required to examine this aspect.
In view of its multiple uses, the M. oleifera plant needs to be
widely cultivated in most of the areas where climatic conditions
favor its optimum growth. In this way, a maximum yield of its
different useable parts could be achieved to derive the maximal
amount of commodities of a multifarious nature for the welfare of
mankind.
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