Utilization of Moringa oleifera in ruminant nutrition (Review article)

Abstract

The present review provides information regarding the nutritional importance of bioactive components of Moringa (Moringa oleifera) for ruminants. Moringa leaves have high quality of protein balanced with its amino acids, thus the leaves are the most part used as a source of protein, however; it is well known for high ruminal degradability of protein and organic matter. Moreover, in comparison with leaves of other shrubs like leucaena, moringa leaves containing around 200g/kg DM crud protein (CP), thus it cannot consider as a potent source of high protein supplement. Despite the CP content, every part of moringa plant is containing several bioactive components and found to have specific nutritional characteristics. Many studies have shown that the leaf, seeds, root, flower, bark and gum exhibit several activities including antimicrobial, antioxidant, anthelmintic. Thus it can suggested that moringa has more nutritional mode of action; thereby improve the ruminal degradability, digestion, health and production performance of the animals. So the whole tree is recommended to be planted extensively and studied for further nutritional research aspects.

Full text

3rd. International conference "Sustainable Development of Livestock's Production Systems"
(sdlps2017)" from 7-9 November, 2017. Department of Animal production, Faculty of Agriculture,
Alexandra University, Egypt)"
Utilization of Moringa oleifera in ruminant nutrition (Review article)
Y.A. Soltana*, A.S. Morsyb, N.M. Hashema, S.M. Sallama
aAlexandria University, Faculty of Agriculture, Animal and fish Production Department, Alexandria, Egypt
bCity of Scientific Research and Technological Applications, Arid Lands Cultivation Research Institute,
Livestock Research Department, New Borg El-Arab, Alexandria, Egypt
* Corresponding author. Tel: +201203307920; Fax: +203-5922780
E-mail address:uosra_eng@yahoo.com (Y.A. Soltan)
Abstract
The present review provides information regarding the nutritional importance of
bioactive components of Moringa (Moringa oleifera) for ruminants. Moringa leaves have
high quality of protein balanced with its amino acids, thus the leaves are the most part
used as a source of protein, however; it is well known for high ruminal degradability of
protein and organic matter. Moreover, in comparison with leaves of other shrubs like
leucaena, moringa leaves containing around 200g/kg DM crud protein (CP), thus it
cannot consider as a potent source of high protein supplement. Despite the CP content,
every part of moringa plant is containing several bioactive components and found to have
specific nutritional characteristics. Many studies have shown that the leaf, seeds, root,
flower, bark and gum exhibit several activities including antimicrobial, antioxidant,
anthelmintic. Thus it can suggested that moringa has more nutritional mode of action;
thereby improve the ruminal degradability, digestion, health and production performance
of the animals. So the whole tree is recommended to be planted extensively and studied
for further nutritional research aspects.
1. Introduction
Feed deficiencies are one of the most serious problems worldwide and it
represents a challenge for ruminant livestock productivity in many developing countries.
In this regard, forage legume browses seem promising in overcoming the limitations of
feed sources as they can be grown by small scale farmers and contain higher amounts of
protein than grasses (Soltan et al., 2012). Even though these legumes are useful as feed
alternatives to low quality diets, the potential of their bioactive components in terms of
animal nutrition is still limited (Cieslak et al., 2013). Moringa (Moringa oleifera) is a
popular multipurpose legume tree, small, fast growing, evergreen, or deciduous tree that
usually grows up to 10 or 12 m in height (Mishra et al., 2011). It can tolerate
unfavourable environmental conditions of many developing countries of Asia, Africa and
Latin America. Moringa is well known to have nutritional and pharmacological
properties (Soliva et al., 2005). Many parts of moringa tree were found to have various

industrial and medicinal applications thus it is known as ‘tree of life’ or ‘the miracle tree’
(Soliva et al., 2005; FAO, 2014; Shah et al., 2016).
Moringa leaves are the most part that attracted the attention of ruminant's
nutritionists as a source of protein, due to the optimal balanced composition of their
amino acid, and high digestible protein content (Babiker et al., 2017). It considered as
alternative to soybean meal and rapeseed meal as protein sources for ruminants (Soliva et
al., 2005). Leaves also were used as a protein supplement and found to improve the
growth performance of growing lambs, milk yield and composition of sheep and goats
(Babiker et al., 2017). On other side, moringa leaves are not suggested as a source of
rumen-protected protein due to the high ruminal degradability of its protein (Soliva et al.,
2005). In addition, the leaves containing around 200g/kg DM crud protein (CP), thus it
considered as a poor undegradable protein supplement for ruminants (Kakengi et al., 2005)
in comparison with other shrubs like leucaena leaves (containing CP from 270 to 350g/kg
DM) (Soltan et al., 2017). In other side, many parts of moringa are recommended to use
as supplementation when minerals or vitamins are limited or unavailable (FAO, 2014). In
addition, various phytochemicals with high potency as antifertility, cardiotonic, anti-
cancerous, antianthelmintic, antitubercular, antispasmodic, abortifacient, nantilithic, anti-
inflammatory, and antimicrobial properties were presented in moringa leaves as well as
in other parts of moringa tree (Sholapur and Patil 2013; Wang et al., 2016). These
phytochemicals including saponins, terpenoids, tannins, quercetin, kaempferol, sterols,
anthraquinones, glucosinolates, isothiocyanates, glycoside compounds and glycerol-1-9-
octadecanoate Table 1 (Berkovich et al., 2013; Shah et al., 2016; Saini et al. 2016; El-
Desoky et al., 2017). Despite considerable interest in the use of moringa as a source of
protein for ruminants, there is no elaborate information on the effects of its
phytochemicals in ruminant's performance. Therefore in order to more accurately
describe moringa tree feeding value for ruminants, a closer look on the possible effects of
its bioactive compounds on ruminal fermentation as well as animal health are discussed
in this review.
2. Moringa plantation
Moringa oleifera is a perennial evergreen tree of 2.5–10 m in height, when
matured, the fruit becomes brown and has 10–50 seeds inside (Vlahof et al., 2002).
Moringa originated in India, but has spread to many semiarid, tropical, and subtropical
areas of other countries of the world, because it tend to be sensitive to drought and winds,
and can be grown widely with a temperature around 25–35◦ C (Gopalakrishnan et al.,
2016). It tolerates a wide range of soil conditions, but prefers a neutral to slightly acidic
(pH 6.3 to 7.0), well-drained sandy or loamy soil (Thurber et al., 2010). Under intensive
farming conditions, a very high biomass production of moringa leaves over 100 ton of
dry matter (DM)/ha can be achieved (Foidl et al., 2002). This makes moringa viable as a
potential nutraceuticalany where in the world (Gopalakrishnan et al., 2016). Thus, a
large-scale of moringa cultivation has been initiated in many countries (Makkar and
Becker, 1996). For example moringa has been introduced to Egypt over the last few years
and is grown on in a various land use patterns (Abd El Baky and El Baroty, 2013).

Table 1. Moringa oleifera bioactive constituents
Moringa part
Bioactive component*
Leaves
9,12,15-Octadecatrienoic acid, Rhamanose, Pterygospermin, Isothiocyanates.
4-(4'-O-acetyl-a-Lrhamnopyranosyloxy)benzyl isothiocyanate, Glycoside
niazirin, niazirinin and three mustard oil glycosides, 4-[4’-O-acetyl- α -L-
rhamnosyloxy) benzyl] isothiocyanate, niaziminin, vitamins (A, B and E,
ascorbic acid), Folates, 2, 6-dihexadecanoate, tetraacetyl-D-xylonic nitrile,
phytol and isobenzofuran-1-one 3-acetic acid, flavonol glycosides (glucosides,
rutinosides, malonyl glucosides), quercetin (kaempferol), amino acids
(Arginine, Histidine, Lysine, Tryptophan, Phenylanaline, Methionine
Threonine, Leucine, Isoleucine, Valine), Oxalic acid, and minerals (Fe, Ca,
Cu, Mg, P, S), Omega-3 and omega-6 polyunsaturated fatty acids
Seeds
Riseofulvin, dechlorogriseofulvin, 8-dihydroramulosin and mullein, Crude
protein, Crude fat, carbohydrate, methionine, cysteine, 4-(α-L-
rhamnopyranosyloxy) benzylglucosinolate, benzylglucosinolate, moringyne,
mono-palmitic, di-oleic triglyceride, folates, amino acids (Arginine, Histidine,
Lysine, Tryptophan, Phenylanaline, Methionine Threonine, Leucine,
Isoleucine, Valine), Oxalic acid, minerals (Fe, Ca, Cu, Mg, P, S), linoleic acid,
linolenic acid and oleic acid.
Roots
4-(α-L-rhamnopyranosyloxy)-benzylglucosinolate and benzylglucosinolate,
glucotropaeolin, Folates
Flowers
D-mannose, D-glucose, protein, ascorbic acid, polysaccharide, Carotenoids
(all-E-luteoxanthin, 13-Z -lutein, all-E-zeaxanthin,and 15-Z-b-carotene),
Omega-3 and omega-6 polyunsaturated fatty acids
Pods
Nitriles, isothiocyanate, thiocarbanates, 0-[2’-hydroxy-3’-(2’’-heptenyloxy)]
propylundecanoate, 0-ethyl-4-[( α -1-rhamnosyloxy)-benzyl] carbamate,
methyl-p-hydroxybenzoate and β-sitosterol, Carotenoids (all-E-luteoxanthin,
13-Z -lutein, all-E-zeaxanthin,and 15-Z-b-carotene), Omega-3 and omega-6
polyunsaturated fatty acids
Bark
4-(α-L-rhamnopyranosyloxy)-benzylglucosinolate
Stem
4-hydroxymellein, vanillin, β-sitosterone, octacosanic acid and β-sitosterol
Gum
L-arabinose, D-galactose, D-glucuronic acid, L-rhamnose, D-mannose, D-
xylose and leucoanthocyanin
* Cited from Berkovich et al. (2013), Shah et al. (2016), Saini et al. (2016) and El-Desoky
et al., (2017)
3. Moringa oleifera antimicrobial bioactive compounds
Antimicrobial activity against opportunistic diseases is the most studied property
of moringa (Wang et al., 2016). Especially with the development of drug resistance
among many virulently pathogenic bacteria which happened by the indiscriminate use of
antibacterial drugs, moringa was found to be a valuable natural source of antimicrobial
agents against these resistant microbes (Wang et al., 2016). Both Gram-negative and
Gram-positive bacteria were found to be sensitive by several antibacterial components of
moringa. Different leaf extracts of moringa showed different inhibition patterns against
Bacillus cereus, Bacillus subtilis, Staphylococcus aureus, Sarcinalutea, Escherichia coli,
Acid fast Mycobacterium phlei, Enterobacter aerogenes, Klebsiella pneumonia,

Pseudomonas aeruginosa and Providencia stuartii (Wang et al., 2016). Many bioactive
components exist in leaves thought to be responsible of the antibacterial activity,
specifically; these compounds include glucosinolates, rhamanose, pterygospermin, and
isothiocyanates. 4-(4'-O-acetyl-a-Lrhamnopyranosyloxy) benzyl isothiocyanate (Shah et
al., 2016).
Parts other than leaves exhibited also a strong antibacterial activity against
Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, Cladosporium
cladosporioides and Penicillium sclerotigenum (Oluduro et al., 2010) due to the high
content of 4-(α-L-rhamnopyranosyloxy)benzyl isothiocyanate, methyl N-4-(α-L-
rhamnopyranosyloxy)benzyl carbamate, and 4-(β-D-glucopyranosyl-1→4-α-L-
rhamnopyranosyloxy)-benzyl thiocarboxamide of moringa seed. Moringa pods and
flowers could effectively inhibit three strains of Vibrio cholera, Vibrio vulnificus and
Vibrio mimicus (Brilhante et al., 2015). Moringa roots and root barks were confirmed by
early observations against gram-positive and gram-negative bacteria like Staphylococcus
aureus, Escherichia coli, Salmonella gallinarum and Pseudomonas aeruginosa due to
containing 4-(α-L-rhamnopyranosyloxy)-benzylglucosinolate and benzylglucosinolate
(Dewangan et al., 2010).
Moringa seeds exhibited high antifungal activity against the both human and plant
pathogenic fungi like Trichophyton rubrum, Trichophyton mentagrophytes,
Epidermophyton floccosum and Microsporum canis (Chuang et al., 2007). A thermo-
stable protein named chitin-binding protein (Mo-CBP3) was isolated from the seeds of
Moringa and found to have antifungal activity against Fusarium solani, Fusarium
oxysporum, Colletotrichum musae and Colletotrichum gloesporioides (Batista et al.,
2014). Zhao et al. (2012) isolated the active antifungal components of moringa seeds and
identified them as riseofulvin, dechlorogriseofulvin, 8-dihydroramulosin and mellein.
By reviewing the studies discussed in this section, it can speculated that however
numerous antibacterial compounds have been isolated from every part of moringa tree,
but no information are available concerning the effects of these components on ruminal
microbial ecosystem, just a few studies suggested that moringa affected the ruminal
fermentation through its tannin and saponins content, however no specific bioactive
components were subjected to any laboratory determinations. When taking into account
that the rumen comprises a diverse, symbiotic population of bacteria, fungi and protozoa
which play a key role in the feed utilization by ruminants (Forsberg and Cheng, 1992).
Thus including moringa in ruminates diets would affect the activity of the ruminal
microbes, and as a consequence ruminal fermentation, digestibility and the allover animal
performance not only through its protein content but also buy these bioactive
components.
4. Moringa oleifera and ruminal fermentation and degradability
The major results of the ruminal fermentation are short chain fatty acids (SCFAs),
ammonia (NH3), methane (CH4), CO2 and microbial protein (Marhaeniyanto1 and
Susanti, 2014). Moringa leaves was found to be methanogen inhibitor, thus it was
suggested to be an alternative to replace critical antibiotics feed additives to alternate the
ruminal fermentation pathways (Soliva et al., 2005), however no information are
available concerning the effects of moringa against ruminal methanogens. Soltan et al.

(2014) evaluated the dose (10, 100, and 1000 µg/ 500 mg dry matter diet) response
effects of the ethanolic extracts of Moringa oleifera leaves and root bark as natural
alternatives to monensin for sheep diets on rumen CH4, extracts of Moringa leaves (all
doses) and root bark at (10 and 1000 µg) presented similarity in CH4 reduction with
monensin and the authors concluded that moringa leaves, root bark could be used as
effective natural intervention to monensin in sheep diets, not only to reduce CH4
production but also to enhance the ruminal efficiency of dietary nutrient use. Similarly,
Soliva et al. (2005) found that the in vitro degradability of organic matter of diets
containing moringa leaves or its extract were similar or even higher compared to those
containing rapeseed meal or soybean meal. Methane production was inhibited by 17% (P
< 0.05) with the complete moringa leaves diet as compared to the diets containing
rapeseed meal or soybean meal. Similarly, Dey et al. (2014) reported an achievement of
methane reduction combined with increases in total gas production and degradability of
organic matter in vitro by wheat straw supplemented with Moringa oleifera leaves in
buffalo diet. The authors of the studies discussed in this section suggested that such
effects might relate to existence of saponins or tannins in moringa leaves.
In other side, Hoffmann et al. (2003) found that the in vitro incubation of
aqueous extract of moringa seeds with pure carbohydrates at a concentration of 1 mg/ ml
reduced the degradation of the total true protein using the dot blot assay which able to
directly detect true protein in rumen fluid samples. The total protein degradation was thus
delayed by approximately 9 h. When fermented along with wheat straw, leaf protein was
almost entirely protected during 12 h of fermentation. The degradation of soy proteins
was retarded by at least 4 ± 6 h, depending on the protein band. The authors concluded
that a new substance, which is neither a tannin nor a saponin, is the responsible of these
effects and can considered as an alternative to replace critical synthetic feed additives
(such as antibiotics) for high yielding dairy cows. There is evidence that the positive
effects of leaves of moringa on the ruminal fermentation might not related to the protein
content. Recently, Babiker et al. (2017) replaced alfalfa with moringa leaves in the diets
of lactating ewes and goats; they concluded that, although the protein of alfalfa was
tended to be higher than that of moringa leaves, the latter positively affected the milk
yield, composition and quality and growth performance of kids and lambs. Moreover,
moringa leaves resulted in an increase of the total antioxidant capacity and vitamin C in
milk and serum of goats and ewes compared with alfalfa diet. The authors suggested that
this could be due to the high antioxidant activity present in moringa leaves and to the
presence of adequate macro- and micro-minerals, vitamins which enhance the efficiency
of rumen microbial growth, fermentation, and absorption of moringa nutrients such as
minerals, vitamins and protein by the goats, which are essential for milk production and
quality. Thus it can be suggested that the high antioxidant activity of moringa could lead
to better utilization of feed nutrients in ruminant diets.
5. Moringa oleifera antioxidant activity
Ruminal microbes are predominantly strictly anaerobes with less developed
antioxidant capacity than facultative anaerobic and aerobic microbes (Morsy et al., 2015).
Thus antioxidants supplementations in ruminant diets (like mimosine) would lessen
oxidative stress, consequently promote more nutrients channelled towards optimal

microbial growth and a consequence better microbial protein synthesis (Soltan et al.,
2017). Moringa leaves are well known to have potent antioxidant activity against free
radicals, prevent oxidative damage to major biomolecules and provide significant
protection against oxidative damage (Sreelatha and Padma, 2009). Seeds and leaves of
moringa were found to have potential source of natural antioxidants and high antioxidant
activity higher than alpha Tocopheryl (Shah et al., 2016). The leaves contain up to 8%
natural antioxidants on dry matter basis due to containing ascorbic acid and flavonoids
which possess the antioxidant activity (Nadeem et al., 2013). El-Desoky et al. (2017)
reported that moringa leaves extract contained high amounts of compounds with
antioxidant activity, they were ascorbic acid (9.60% l-(+)-ascorbic acid 2, 6-
dihexadecanoate), tetraacetyl-D-xylonic nitrile, phytol and isobenzofuran-1-one 3-acetic
acid. The leaves also containing, high amount of quercetin and kaempferol was found to
be in the range of 0.07–1.26 and 0.05–0.67 %, respectively which posses high antioxidant
activity, moreover these two componants have been confirmd to decrease cell viability of
the human cancer (KB). (Saini et al., 2016). Anwar et al. (2003) characterized different
antioxidants of moringa leaves and found them effective in the inhibition of
autooxidation and to enhance the oxidative stability of sunflower oil for 90 days at
ambient storage temperature. Moringa leaf extract enhanced the storage stability of butter
stored at refrigeration temperature for three months with acceptable sensory
characteristics (Nadeem et al., 2013). The antioxidant potential of seed extracts of
moringa also was investigated by Lalas and Tsaknis (2002) and they reported that seeds
are rich in phenolic antioxidants (7–8% on dry mass basis) and they recommend the
stabilization of vegetable oils by the seed extract of moringa. The enrichment of moringa
in these phenolic components leads to add another property to this miraculous tree as an
anthelmintic activity for ruminants.
6. Moringa oleifera anthelmintic activity
Ruminant production remains limited by the gastrointestinal nematodes (GINs) in
many developing countries (Mortensen et al., 2003). For example, Haemonchus
contortus, it sucks blood voraciously inside the goat’s abomasum and causes severe
anemia, anasarca and causing acute mortality (Mortensen et al., 2003). Recently,
Moringa oleifera seed ethanolic and aqueous extracts were found to have multiple
mechanisms in killing the Haemonchus contortus eggs and infective stage larvae (L3s),
which then limit the likelihood of developing anthelmintic resistance (Cabardo Jr and
Portugaliza, 2017). Similar study was done using aqueous and ethanolic leaf extracts of
moringa confirmed the validity of leaves to suppress activities of Haemonchus contortus
eggs and larvae (L1 and L2) (Tayo et al., 2014). On the whole, Moringa oleifera shows
high potential in the control of parasites, which could inhibit the spread of related
diseases (Cabardo Jr and Portugaliza, 2017). An in vivo study found that supplementation
of moringa leaves may suppress the burden of strongyle worms in naturally infected West
West African Dwarf goats (Asaolu et al., 2012) and cross-bred Xhosa lop eared goats
(Moyo et al., 2013). These studies describe the potential use of moringa seeds, leaves and
gum extracts in controlling nematode parasites through containing potential secondary
metabolites (tannins, saponins, alkaloids, isophlaphoiods) responsible for over 90% egg
hatch inhibition. Tannins have attracted most attention for their effect on internal

nematodes in ruminants, not only directly through their antiparasitic activity but might
also act indirectly by increasing host resistance (Hoste et al., 2006). Tannins are known to
reduce the motility of the L3s of Haemonchus contortus, which may indicate paralysis
and interference to neuromuscular coordination of the larvae (Hoste et al., 2006).
Saponins are reported as an excellent source of cytotoxic and anthelmintic constituents
that warrant its isolation and purification for new drug development (Ali et al., 2011).
The ability of moringa seeds to reduce helminth eggs is not only thought the
gastrointestinal tract of ruminants but also in the water purifying process from helminth
parasite and their eggs (Wang et al., 2016). Seeds are used in water purification for a long
time in underdeveloped countries. The mechanism of moringa seeds as water purifying
agents was shown by the flocculent protein from moringa seed forming flocculate
particles in suspension in water (Pramanik et al., 2016). In many developing countries all
over the world, irrigation water is widely used in urban farming, which can get polluted
by the helminth parasite and their eggs. Therefore, moringa seeds were used to reduce
helminth eggs and turbidity in irrigation water (Sengupta et al., 2012).
7. Other activates of Moringa oleifera
Other components were detected in moringa like lactogogue, which made of
phytosterols, acts as a precursor for hormones required for reproductive growth. Moringa
is rich in phytosterols like stigmasterol, sitosterol and kampesterol which are precursors
for hormones. These phytochemicals alongside with high amino acids content can
enhance the estrogen excretion, which in turn stimulates the proliferation of the
mammary gland ducts to produce milk (Gopalakrishnan et al., 2016). Recently, moringa
leaves as a supplement in ruminant diets was found to enhance milk yield and
composition as well as minimizing the oxidative damage of milk and serum of ewes and
goats (Babiker et al., 2017). Moringa can be considered as good source of amino acids,
leaves, pods and flowers have 440, 300 and 310 g/kg DM amino acids, respectively
(Gopalakrishnan et al., 2016). Moringa also was recommended as a source of minerals,
because it can provide 7 times more vitamin C than oranges, 10 times more vitamin A
than carrots, 17 times more calcium than milk, 9 times more protein than yoghurt, 15
times more potassium than bananas and 25 times more iron than spinach (Rockwood et
al., 2013). Moreover, the seeds are rich in linoleic acid, linolenic acid and oleic acid;
these fatty acids have the ability to control cholesterol. Moringa seed oil presented around
76% of these fatty acids, making it ideal for use as a substitute for olive oil (Lalas and
Tsaknis). Thus, milk low in cholesterol could be obtained by feeding lactating animals on
moringa leaves. The reduced cholesterol content in milk of ewes and goats fed with
moringa leaves could be ascribed to its functional effect of phenolic acids and antioxidant
activity (Babiker et al., 2017). The unique combination of moringa active components
leading to occur several other activities including coagulant, biosorbent, antihypertensive,
antitumor, anticancer, antidiabetic, antipyretic, anti-asthmatic, cardiac and circulatory
stimulant, analgesic, antipyretic, wound healing (Shah et al., 2016). All of these activities
should positively affect the animal health and production as a consequence.

8. Conclusion
In conclusion, every part of Moringa oleifera, nearly all parts of this tree are full
of several bioactive components with different activities, thus we can speculated that
moringa affect the ruminant production by various mechanism of actions (e.g.
antimicrobial and antioxidant), thus it can be used in the development of promising
natural feed additives for ruminants. In contrast to the dietary antibiotics, residual of
these bioactive components in the milk produced by animals fed with moringa probably
has a benefit for human health. Thus Moringa oleifera tree needs to be widely cultivated
in most of the areas where climatic conditions favor its optimum growth like Egypt.
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