Multi-Functional Application of Moringa Oleifera Lam. in Nutrition and Animal Food Products: A Review
Multi-Functional Application of Moringa Oleifera Lam. in Nutrition and Animal Food Products: A Review
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Review
A R T I C L E I N F O A B S T R A C T
Keywords: Research on the use of various parts of the Moringa oleifera Lam. plant (M. oleifera) as a nutritional and neu-
Moringa oleifera traceutical resource for human and animal diets has increased in recent years, emanating from the widespread
Functional bio-compounds use of the plant in traditional cuisines and medicinal remedies in several regions of the world. Analytical studies
Phytochemicals have identified M. oleifera as an important source of essential nutrients; rich in protein, essential amino acids,
Neutraceuticals
minerals, and vitamins, with a relatively low amount of antinutrients. It is also a rich source of other bio active
Livestock production
Fortification
compounds including flavonoids and phenolic compounds; with several studies detailing demonstrated in vitro
and in vivo functional properties, most substantially, antioxidant activities. Moringa oleifera consumption has
been reported to improve the health status, feed conversion efficiency, growth performance and product quality
of several livestock species, at dietary inclusion rates generally not exceeding 5% of total dry matter intake.
Fortification of processed foods with M. oleifera has been reported to increase nutritional value, some organo-
leptic properties, oxidative stability and product shelf life; with a notable need for further analytical and con-
sumer studies in the development of these products. There is a paucity of literature detailing clinical studies,
nutrient bioavailability, toxicity and the mode of action of the bioactive compounds to which the health claims
associated with M. oleifera consumption are attributed. Many of these are not yet fully understood; therefore
more research in these areas is required in order to fully utilize the potential benefits of this plant in human and
livestock nutrition.
⁎
Corresponding author.
E-mail address: vmuchenje@ufh.ac.za (V. Muchenje).
https://doi.org/10.1016/j.foodres.2017.12.079
Received 18 October 2017; Received in revised form 27 December 2017; Accepted 31 December 2017
Available online 04 January 2018
0963-9969/ © 2018 Elsevier Ltd. All rights reserved.
A.B. Falowo et al. Food Research International 106 (2018) 317–334
Food/Vegetable
d/Vege
Essential/Cooking oil Feed ingre
ingredients
Food fortificant Fodder
Medicine Antibiotic
Bio-preservatives
Antioxidant
Agriculture/Industry
ture/
Fertilizer/Manure
izer/M
Biogas/Biofuel
Cosmetics/perfume
Textile
Water purification
Wood
Wind breaker
Bio-pesticide
Fig. 1. Multi-functional application of Moringa oleifera plant in food systems and agro-processing.
health related diseases (Oyeyinka & Oyeyinka, 2016). Furthermore, the Table 1
application of M. oleifera in livestock feed as a source of protein, anti- Taxonomy of Moringa oleifera Lam.
biotic and antioxidant compounds has been reported in literature with
Kingdom Plantae
impressive success; including demonstrated to improve growth perfor-
mance, milk let down (the release of milk from the alveoli in the animal Subkingdom Viridiplantae
udder) and quality, meat oxidative stability and organoleptic quality as Infrakingdom Streptophyta
well as reducing the rate of microbial growth in meat products after Superdivision Embryophyta
Division Tracheophyta
processing and cold storage (Adeniji & Lawal, 2012; Mendieta-Araica,
Subdivision Spermatophytina
Sporndly, Reyes-Sanchez, & Sporndly, 2011; Moyo, Oyedemi, Masika, & Class Magnoliopsida
Muchenje, 2012; Mukumbo et al., 2014; Nkukwana et al., 2014; Superorder Rosanae
Nkukwana et al., 2014). The seeds of M. oleifera have also been used as Order Brassicales
Family Moringaceae
an effective coagulant and antimicrobial agent to remove hardness,
Genus Moringa
undesirable chemicals and biological contaminants in water (Saini, Species M. oleifera, M. arborea, M. borziana, M. concanensis
Sivanesan, & Keum, 2016). The bark of the plant is known to produce M. drouhardii, M. hildebrandtii, M. longituba
fibre which is a suitable raw material for the production of high alpha M. ovalifolia, M. peregrine, M. rivae, M. Ruspoliana
cellulose pulp for use in cellophane and textiles (Duke, 2001). Based on M. pygmaea, M. stenopetala
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A.B. Falowo et al. Food Research International 106 (2018) 317–334
and is surrounded by thick cork. The seeds are round or triangular in Table 2
shape with a brownish semi-permeable seed hull which is enclosed in Nutrient composition of Moringa oleifera Lam (dry basis).
long slender pods (Zhao & Zhang, 2013). Medicinally, most parts of this
Nutrient Content range (low–high)⁎
plant are used in the treatment of illness and production of drugs
against bacteria, fungi, virus and other pathogens in human beings. Leaf Seed Stem
Other products such as essential/cooking oil, green manure, biogas, and
Protein (g/100 g) 10.74a–30.29b 9.98c–51.80d 12.77e
bio-pesticide have been produced from the plant for human uses
Fat (g/100 g) 6.50b–20.00c 22.97g–38.67f 2.0e
(Fuglie, 1999; Paliwal, Sharma, & Pracheta, 2011). Particularly, the oil Crude fibre (g/100 g) 7.09h–35.00c 20.00c–22.93g –
from its seeds has been exploited as a solidifying agent in margarines Ash (g/100 g) 7.64a–10.71b 3.60j–5.00c 8.41e
and other foodstuffs containing solid and semi-solid fat, thus elim- Carbohydrate (g/100 g) 13.41c–63.11k 18.00c–40.09g –
inating hydrogenation processes (Francis & Becker, 2005; Makkar & K (mg/100 g) 120.96l–1845.00a 75.00f –
Ca (mg/100 g) 147.43l–7230.00a 751. 70f–2800.00g –
Becker, 1997). One kilogram of these seeds has been reported to pro-
P (mg/100 g) 300.00m 635.00f–5300.00g –
duce, on average, 400 mL of cooking oil (Mulugeta & Fekadu, 2014), Mg (mg/100 g) 322.50a–500.00b 45.00f –
indicating that a seed can produce up to 45% oil yield after processing. Fe (mg/100 g) 2.68l–49.00b 5.20f –
Presently, India is the largest producer of M. oleifera, meeting up to I (mg/100 g) 0.06l –
Zn (mg/100 g) 1.00b–3.10a 0.05f –
about 80% of global demand (Hutchinson, 2014). However, commer-
Mn (mg/100 g) 8.68b −45.00f –
cial production of the plant has spread to other parts of the world in- Vitamin A (beta-carotene) 13.48n–18.50b – –
cluding Africa, Asia, Central and South America. (mg/100 g)
Vitamin E (mg/100 g) 16.80n–77.00b – –
2.1. Nutritional composition of Moringa oleifera Vitamin C (mg/100 g) 245.13n 4.50f –
Vitamin B1 (mg/100 g) 0.05n 0.05f –
Vitamin B2 (mg/100 g) 0.80n 0.06f –
The recognition and utilization of M. oleifera products for dietary Vitamin B3 (mg/100 g) 220.00n 0.02f –
human and livestock purposes has been attributed to their high nutri- Total amino acid (g/100 g) − 76.40b 74.85j –
tional value and low anti-nutritional factors. Recent reports of the Total non-essential amino − 41.00b 40.37j –
acid (g/100 g)
analysed nutrient composition of the leaves, seeds and stems of the
Total essential amino acid − 35.40b 34.48j –
plant show that they are rich in protein, essential amino acids, minerals, (g/100 g)
vitamins and other bioactive compounds (Table 2) (Moyo et al., 2012; Total saturated fatty acid (%) − 58.00 b
– –
Valdez-Solana et al., 2015). Data on the nutrient composition of the Total monounsaturated fatty − 4.61b – –
roots is still scarce. On dry matter basis, the crude protein content of M. acid (%)
Total polyunsaturated fatty − 52.21b – –
oleifera leaf has been reported to be low as 10.74 g/100 g and high as
acid (%)
30.29 g/100 g. Crude fibre ranges from 7.09–35.0 g/100 g, carbohy-
drate 13.41–63.11 g/100 g, fat 6.50–20.00 g/100 g and ash References: a Valdez-Solana et al., 2015; b Moyo, Masika, Hugo, & Muchenje, 2011; c Aja
7.64–10.71 g/100 g. The nutritional analysis of M. oleifera seeds re- et al., 2013; d Ochi, Elbushra, Fatur, Abubakr, & Hafiz, 2015; e Shih, Chang, Kang, & Tsai,
vealed that they contain about 9.98–51.80 g/100 g crude protein, 2011; f Olagbemide & Philip, 2014; g Mabusela, Nkukwana, Mokoma, & Mucheje, 2018; h
17.26–20.00 g/100 g crude fibre, 3.36–18.00 g/100 g carbohydrate, Ogbe & Affiku, 2011; i Ogbe & Affiku, 2011; j Anhwange, Ajibola, & Oniye, 2004; k
Mbailao, Mianpereum, & Albert, 2014; l Asante, Nasare, Tom-Dery, Ochire-Boadu, &
38.67–43.60 g/100 g fat and 3.60–5.00 g/100 g ash (Table 2). The
Kentil, 2014; m Moyo et al., 2012; n El Sohaimy, Hamad, Mohamed, Amar, & Al-Hindi,
substantial variation in the nutritional composition may be due to 2015.
factors such as growth environment, stage of harvest, soil type and ⁎
Lowest reported values–highest reported values.
method of processing. The leaves and seeds contain appreciable
amounts of essential minerals, vitamins, amino acids, and fatty acids with digestion and absorption of other nutrients such as zinc, iron,
(Moyo et al., 2011). More than half (57%) of the M. oleifera leaf fatty calcium and magnesium when consumed in high quantities. According
acids has been classified as unsaturated fatty acids with α-Linolenic to Stevens et al. (2015) and Makkar and Becker (1996), the phytate and
acid having the highest value while the remaining are saturated fatty saponin content in M. oleifera seed (2.23%, 3.89%) and leaf (2.5%,
acids (43%) (Moyo et al., 2011). In addition, M. oleifera leaf has been 5.0%) was lower than those found in other legumes such as soya bean
reported to contain about 16–19 amino acids, of which 10 are classified meal. The saponin level in M. oleifera has been considered to be rela-
as essential amino acids namely threonine, tyrosine, methionine, valine, tively innocuous as the leaf is consumed by humans (4–50 g leaf
phenylalanine, isoleucine, leucine, histidine, lysine and tryptophan. powder) without any adverse effects (Makkar & Becker, 1996; Stohs &
The calcium, potassium, magnesium and iron content of M. oleifera Hartman, 2015). Similarly, the oxalate content in M. oleifera leaf
leaves has been observed to be higher compared with other plant (2.754 g/100 g) was reported to be lower compared to those found in
sources such as Vernomia anydalira, Manihot esculenta, Teiferia occi- Spinach leaf (12.57 g/100 g), Green amaranth leaf (10.05 g/100 g) and
dentalis, Talinum triangulare and Amaranthus spinosus (Moyo et al., 2011; Curry leaf (2.77 g/100 g) (Radek & Savage, 2008). The safety and
Nkafamiya, Osemeahon, Modibbo, & Aminu, 2010; Stevens, Ugese, toxicity aspect of applying various extracts of this plant in animals have
Otitoju, & Baiyeri, 2015). The amount of vitamins A, B, C and E in the also been reported with the threshold level 150 mg–2.0 g (Stohs &
M. oleifera leaf is reported to be high and can be used to combat mal- Hartman, 2015). So on this basis, consumption of M. oleifera appears
nutrition, especially among infants and nursing mothers (Oz, 2014). In nutritionally safer and healthier than above-mentioned common vege-
fact, the daily intake of 10 g of powdered M. oleifera dry leaves by tables.
malnourished children has been reported to improve their weight gain
and promote quick recovery after 6 months compared to control group
(Zongo, Zoungrana, Savadogo, & Traoré, 2013). Other parts of the M. 3. Moringa oleifera Lam. as a source of phytochemicals, natural
oleifera plant such as roots, stems, flowers and fruits have been reported antioxidants and as a neutraceutical
to have a rich proximate, fatty acids, mineral and vitamins profile (Shih
et al., 2011). The M. oleifera plant has important functional properties. It contains
Beside the above mentioned nutritional content, M. oleifera has been a huge array of bio-active compounds which are commonly referred to
found to contain a relatively low amount of antinutrients such as as secondary metabolites or phytochemicals. On estimate, more than
phytates, saponins, tannins and oxalates (Shih et al., 2011). These an- 200 compounds have been identified from M. oleifera (leaf, stem, root
tinutrients, though not necessarily toxic or deleterious, may interfere and seed) which can be classified into groups such as hydrocarbon,
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Table 3
Phytochemical constituents of fatty acid and ester class isolated from Moringa oleifera Lam.
N/S IUPC Molecular formula Extraction solvent Plant part Biological activity % Composition Ref.⁎
1 1,2-Benzenedicarboxylic acid, diethyl ester C12H14O4 ethyl acetate Leaf extract Antimicrobial 1.90 (1)
2 1,2-Benzenedicarboxylic acid, mono(2- C16H22O4 n-Hexane Leaf essential 5.09 (2)
ethylhexyl)ester oil
3 1,2-Benzenedicarboxylic acid, bis-2- C24H38O4 Ethyl acetate, Methanol Leaf extract Antimicrobial 2.23 (1)
ethylhexyl ester
4 2-Butenoic acid, 2-methoxy-3-methyl-, C7H12O3 Ethanol Leaf extract 1.17 (3)
methyl ester
6 cis-Vaccenic acid C18H34O2 Ethanol Leaf extract Anti-hypertensive 26.45 (3)
7 1,2,3-Cyclopentanetriol C5H10O3 Ethanol Leaf extract Antiviral 1.63 (3)
8 Diethyl phthalate C12H14O4 Aqueous ethanol Leaf extract Fragrance agent 0.33 (4)
9 Dibenzyl phthalate Dichloromethane Root extract 5.77 (5)
10 1,11 Diphenyl undecane C23H32 Dichloromethane Root extract 18.78 (5)
11 Di-3-phenyl propyl ether C18H22O Dichloromethane Root extract 0.48 (5)
12 N,N-dibenzyl undecanyl urea C26H38N2O Dichloromethane Root extract 5.69 (5)
13 2,5 Diethyl pyridine C9H13N Petroleum ether Root extract 2.42 (5)
14 Decanoic acid C10H20O2 Aqueous methanol Leaf extract 0.54 (4)
15 Dodecanoic acid C12H24O2 Aqueous methanol Leaf extract 0.32 (4)
16 Dimethyl-Propanedioic acid C5H8O4 Aqueous methanol Leaf extract 0.03 (5)
17 Ethyl hexadecanoate C18H30O2 Petroleum ether Root extract 2.05 (5)
18 (Z)-11-Eicosenoic acid, C20H38O2 Petroleum ether Root extract 3.01 (5)
(Z)-13-Eicosenoic acid Dichloromethane
19 (Z)-Hexyl oleate Aqueous methanol Leaf extract 8.66 (4)
20 Hexyl 3-methylbutanoate Aqueous methanol Leaf extract Flavoring agent 2.23 (4)
21 (Z)-3-Hexen-1-yl valerate Aqueous methanol Leaf extract 0.04 (4)
22 4-Hexenoic acid Aqueous methanol Leaf extract 0.36 (4)
23 2-Hexenoic acid Aqueous methanol Leaf extract 2.11 (4)
24 Hexadecanoic acid Aqueous methanol Leaf extract 1.15 (4)
25 Methyl palmitate Steam distillation Leaf essential Anti-inflammation 0.08 (6)
oil
26 Methyl lactate C4H8O3 Ethyl acetate Leaf extract 21.07 (1)
27 Methyl hexanoate Aqueous methanol Leaf extract Flavoring agent 0.28 (4)
28 Methyl (Z)-9-hexadecenoate C17H32O2 Dichloromethane Root extract 0.95 (5)
29 Methyl acetate Aqueous methanol Leaf extract 0.36 (4)
30 2-Methyl hexadecane C17H34 Petroleum ether Root extract 0.95 (5)
31 Mannitol,1,4-di-O-methyl-, tetraacetate C16H26O10 Ethanol Leaf extract 1.09 (3)
32 Methyl heptadecanoate C18H36O2 Dichloromethane Root extract 1.04 (5)
33 n-Hexadecanoic acid C16H32O2 Ethanol Leaf extract Antioxidant, pesticide and anti-
Steam distillation Leaf essential inflammation
n-Hexane oil
34 Octadecanoic acid C18H36O2 Ethanol Leaf extract Antibacterial action, lubricant, 4.91 (3)
Aqueous methanol cosmetics 0.26 (4)
Ethanol Seed extract (7)
35 (E)-6-Octadecenoic acid C18H34O2 Dichloromethane Root extract (5)
36 (E)-9-Octadecenoic acid Aqueous methanol Leaf extract 0.98 (4)
37 Octadecanoic acid, trimethylsilyl ester C21H44O2Si Seed extract (7)
38 Propyl 3-methylbutanoate C8H16O2 Aqueous methanol Leaf extract Flavoring agent 2.58 (4)
39 Palmitic acid C16H32O2 Ethyl acetate Leaf (extract) Antioxidant, pesticide, and 1.13 (1)
antimicrobial
40 Palmitoyl chloride C18H36O2 Ethanol Leaf extract Anticancer 1.56 (3)
41 Pentanoic acid C5H10O2 Aqueous methanol Leaf extract 0.98 (4)
42 Tetradecanoic acid C14H28O2 Ethanol Leaf extract Antioxidant, anti-cancer 2.21 (3)
Dichloromethane Root extract 0.27 (5)
43 Tertracosanoic acid C24H48O2 Petroleum ether Root extract 2.45 (5)
44 γ-Tocopherol C28H48O2 n-Hexane Leaf essential Antioxidant 3.38 (2)
oil
45 dl-α-Tocopherol C29H50O2 n-Hexane Leaf essential Anti-inflammatory and 3.52 (2)
oil antioxidant
46 Sulfurous acid, hexyl pentadecyl ester C21H44O3S n-Hexane Leaf essential 1.14 (2)
oil
47 Hexadecanoic acid, ethyl ester C18H36O2 n-Hexane Leaf essential Anticancer 0.15 (2)
oil
48 3-Methylbutanoic acid (CH3)2CHCH2CO2H Aqueous methanol Leaf extract 1.61 (4)
⁎
References: (1): Karthika, Ravishankar, Mariajancyrani, & Chandramohan, 2013; (2): Zhao & Zhang, 2013; (3): Bhattacharya et al., 2014; (4): Mukunzi et al., 2011; (5): Sana, Saleem,
& Faizi, 2015; (6): Chuang et al., 2007; (7): Sahab & Nawar, 2015.
ketones, fatty acids, alcohols, aldehydes, terpenes and others (Tables 3–7, Fig. 2). Basically, these phytochemicals are synthesized in plants
3–7). These compounds have been identified using GC–MS or HS-SPME partly as a response to ecological and physiological pressures such as
methods after extraction from solvents such as water, ethanol, hexane, pathogen and insect attack, UV radiation and wounding (Khoddami,
methanol, ethyl-acetate (Tables 3–7). Some of the detected phyto- Wilkes, & Roberts, 2013).
chemicals have been reported to be antioxidant, antimicrobial, anti- The natural antioxidants such as vitamin C, carotenoids, toco-
viral, antileukaemic, anti-otitis, antianemic, anti-inflammatory, anti- pherols, flavonoids and other phenolic compounds are known to be
fungal, anti-cancer, anti-ulcerative, and antipyretic in nature (Tables present in M. oleifera. According to Pakade, Cukrowska, and Chimuka
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Table 4
Phytochemical constituents of hydrocarbon class isolated from Moringa oleifera Lam.
N/S IUPC Molecular formula Extraction solvent Plant part Biological % Composition Ref.⁎
activity
⁎
References: (1): Sana et al., 2015; (2): Chuang et al., 2007; (3): Zhao & Zhang, 2013; (4): Mukunzi et al., 2011; (5): Sahab & Nawar, 2015; (6): Al-Asmari et al., 2015
(2013), the total phenolics and flavonoids content of M. oleifera leaf cauliflower (14.7 g/100 g and 4.6 g/100 g) and peas (10.4 g/100 g and
(31.9 g/100 g and 40.8 g/100 g) and flower (29.7 g/100 g and 36.1 g/ 6.6 g/100 g), respectively. Similarly, Falowo et al. (2017) and Subudhi
100 g) in dry basis was twice higher than those found in other vege- and Bhoi (2014) reported that, M. oleifera leaf has higher total phenolic
tables such as cabbage (11.8 g/100 g and 9.8 g/100 g), spinach (14.4 g/ and total flavonoid content than Brassica juncea and Bidens pilosa plants.
100 g and 12.5 g/100 g), broccoli (17.6 g g/100 g and 15.7 g/100 g), In all, the free radical-scavenging activity of M. oleifera leaf has been
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Table 5
Phytochemical constituents of alcohol class isolates from Moringa oleifera Lam.
N/S IUPC Molecular formula Extraction solvent Plant part Biological activity % Composition Ref.⁎
⁎
References: (1): Karthika et al., 2013; (2): Sana et al., 2015; (3): Mukunzi et al., 2011; (4): Zhao & Zhang, 2013; (5): Chuang et al., 2007; (6): Bhattacharya et al., 2014. (7) Falowo,
Muchenje, Hugo, Aiyegoro, & Fayemi, 2017
reported to be higher than the synthetic antioxidant counterparts such A study on the inclusion of aqueous ethanolic M. oleifera leaf extract
as butylated hydroxytoluene (BHT), rutin and ascorbic acid (Falowo, at 100 mg/kg and 200 mg/kg in mice diet was found to reduce hepa-
Muchenje, Hugo, & Charimba, 2016). totoxicity by decreasing the level of serum aspartate aminotransferase
As outlined in Tables 3–7, M. oleifera has numerous medicinal ap- (AST), alanine aminotransferase (ALT) and gammaglutamyl transpep-
plications in food systems for human use. It is traditionally utilized to tidase (GGT) as well as elevating the antioxidant enzymes in the liver
treat a wide variety of ailments such as skin diseases, respiratory dis- (Karthivashan, Arulselvan, Tan, & Fakurazi, 2015). This shows that, M.
tress, ear and dental infections, hypertension, diabetes, anemia, and oleifera can suppress the inflammation of liver tissues thereby preser-
cancer (Al-Asmari et al., 2015). Additionally, the pharmacological ac- ving them from damage. Moreso, Taha, Amin, and Sultan (2015) re-
tivities of M. oleifera (leaf, stem, seed and root) extracts have been well vealed that, the addition of aqueous ethanolic M. oleifera leaf extract at
described in many studies with outstanding results. For instance, the 500 mg/kg and 1000 mg/kg in mice diet significantly decreased mal-
addition of M. oleifera leaf, bark and root extract at 250 μg/mL or ondialdehyde (lipid peroxidation) and vascular congestion, and pro-
500 μg/mL to extracted human cultured cell lines have been demon- moted a well-organized architectural cell of urinary bladder compared
strated to inhibit the growth of breast (MDA-MB-231cell line), and to the control. This suggests that, M. oleifera can play an important role
colorectal (HCT cell line) cancers (Al-Asmari et al., 2015). Furthermore, in ameliorating and protecting the bladder from Cyclophosphamide
the extract of M. oleifera has been reported to be effective against the (CP) toxicity. Hannan et al. (2014) found that the administration of
growth of ovarian cancer cell in vitro and these effects has been at- ethanolic M. oleifera leaf extract (30 μg/mL) at every step of neuronal
tributed to the presence of bio-active compounds such as iso- development accelerated the early neuronal differentiation which fol-
thiocyanates, eugenol, D-allose, glucosinolates and hexadeconoic acid lows to the entire period of maturation when compared to the control
ethyl ester in the plant (Bose, 2007; Saralaya, Patel, Roy, & Patel, culture. This study revealed that M. oleifera can be used in the treatment
2010). of paralysis, epilepsy, nervous debility and other nerve disorders in
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Table 6
Phytochemical constituents of ketone class isolated from Moringa oleifera Lam.
N/S IUPC Molecular formula Extraction solvent Plant part Biological activity % Composition Ref.⁎
⁎
References: (1): Sana et al., 2015; (2): Mukunzi et al., 2011; (3): Karthika et al., 2013; (4): Chuang et al., 2007; (5): Sahab & Nawar, 2015.
323
Table 7
Phytochemical constituents of aldehydes class and other compounds isolated from Moringa oleifera Lam.
N/S IUPC Common name Molecular formular Extraction solvent Plant part Biological activity % Composition Ref.⁎
A.B. Falowo et al.
1 Hexanal Aldehydes Aqueous methanol Leaf extract Flavoring agents 0.36 (1)
2 2-Hexenal Aldehydes Aqueous methanol Leaf extract 1.02 (1)
3 (Z)-2-Heptenal Aldehydes Aqueous methanol Leaf extract 0.30 (1)
4 (E,E)-2,4-Hexadienal Aldehydes Aqueous methanol Leaf extract 0.67 (1)
5 (E,E)-2,4-Heptadienal Aldehydes Aqueous methanol Leaf extract 0.67 (1)
6 (E)-2-Butenal Aldehydes Aqueous methanol Leaf extract 2.05 (1)
7 2-Methyl furan Aldehydes Aqueous methanol Leaf extract Flavoring agent 0.61 (1)
8 Benzene acetaldehyde Acetaldehyde C8H8O Steam distillation Leaf essential oil 2.16 (2)
9 Benzaldehyde Aldehydes C7H6O Aqueous methanol Leaf extract Flavoring agent 5.12 (1)
Steam distillation Leaf essential oil 0.55 (2)
petroleum ether Root extract 0.17 (3)
10 Benzyl nitrile C8H7N Steam distillation Leaf essential oil Antibiotics and fragrances agent 1.10 (2)
11 Hepta thioureido-bis-1,1′-methylene amine C9H22N16S7 Petroleum ether Root extract 3.56 (3)
12 2-Amyl furan C9H14O Petroleum ether Root extract 0.32 (3)
13 Acetic acid Carboxylic acid C2H4O2 Aqueous methanol Leaf extract Anti-otitis 12.54 (1)
14 alpha-Himachalene Terpenoids C15H24 Aqueous methanol Leaf extract 1.74 (1)
15 beta-L-Rhamnofuranoside, 5-O-acetylthio-octyl- Glycoside C16H30O5S Ethanol Leaf extract Anti-inflammatory and 1.01 (4)
antioxidant
16 Benzyl isothiocyanate C8H7NS Dichloromethane Root extract Anticancer and antimicrobial 0.21 (3)
17 Benzene,1,3–5 dimethyl- C8H10 n-Hazane Essential oil 5.95 (5)
18 Benzene,(1-methylethyl)- C9H12 n-Hazane Essential oil 0.16 (5)
19 Benzene,1-ethyl-2,4-dimethyl- C10H14 n-Hazane Essential oil 2.55 (5)
20 beta-Ionone epoxide Terpenoids Aqueous methanol Leaf extract flavor and fragrance agents 0.65 (1)
21 1-β-Acetoxy furano-3-eudesmene C17H24O3 Petroleum ether Root extract 4.80 (3)
22 Benzamide C7H7ON Petroleum ether Root extract Anti-emetics 0.46 (3)
324
23 1-Chloro-2-methyl benzene C7H7Cl Dichloromethane Root extract 0.06 (3)
24 O-Cymene Terpenoids C10H14 Aqueous methanol Leaf extract 0.46 (1)
25 Citronellyl valerate Terpenoids Aqueous methanol Leaf extract Flavoring agent 0.44 (1)
26 3-Chloro-N-isochroman-1-ylmethylpropionamide Amide C13H16ClNO2 Ethanol Leaf extract 5.61 (4)
27 Cyclohexane, ethyl- C8H16 n-Haxane Leaf extract 0.43 (5)
28 Cyclohexane,1,3-dimethyl-, cis- C8H16 n-Haxane Leaf extract 0.78 (5)
29 Cyclohexane,1,4-dimethyl-, cis- C8H16 n-Haxane Leaf extract 0.14 (5)
30 3,4-Dichlorobenzonitrile Aromatic compound C7H3Cl2N Ethanol Leaf extract 2.21 (4)
31 Decyl-3-chlorobenzoate C17H25ClO2 Dichloromethane Root extract 12.0 (3)
32 4, 6 Dibromo 2 [4′,5′,6′ tribromo 2′ hydroxyp henoxy] phenol C12H5Br5O3 Ethanol Seed extract (6)
32 2 (2′,6′ Dimethoxyphenyl) 4,7 bis [4′(1″,1″dimethyl) phenoxy]1,10 C40H40N2O4 Ethanol Seed extract (6)
phenanthroline
33 1,10 Diphenyl decane C22H30 Petroleum ether Root extract 8.62 (3)
34 1–3 Dibenzyl-3-ethyl urea C17H20N2O Dichloromethane Root extract 2.51 (3)
35 Dimethyl sulfoxide Organosulfur compound C2H6OS Aqueous methanol Leaf extract Anti-inflamation 0.62 (1)
36 Dimethoate Organophosphate C5H12NO3PS2 n-Hexane Essential oil Insecticides 0.52 (5)
37 Dihydro actinidolide Terpenoid C11H16O2 Steam distillation Leaf essential oil Fragrance agent 1.21 (2)
38 D-allose Sugar Ethanol Leaf, root, seed Sweeteners and bulking agents; (7)
39 (E)-3,7-Dimethyl octa-2,6- dienyl-3-chlorobenzoate Organic compound C17H21Cl O2 Dichloromethane Root extract 4.65 (3)
40 Ethyl 2-hydroxypropanoate (lactate) Lactic acid C5H10O3 Ethyl acetate Leaf (extract) Food additives (8)
41 2-Ethyl-3,6-dimethylpyrazine Steam distillation Leaf essential oil Flavor and fragrance agents 0.12 (2)
42 Ethene 1,1′-bis–p-toulenyl sulfide C16H16S2 Petroleum ether Root extract 2.90 (3)
43 Ergosta-5,22-dien-3-ol, (3β,22E) C28H46O Dichloromethane Root extract 9.36 (3)
44 2,3-Epoxycarane Steam distillation Leaf essential oil 0.16 (2)
45 gamma-Sitosterol Steroid C29H50O Ethanol Leaf extract Anticancer and antioxidant 2.23 (4)
46 (E)-Geranyl acetone Terpenoid Aqueous methanol Leaf extract Flavoring agent 1.37 (1)
47 (E,E)-Farnesyl acetone Terpenoid Aqueous methanol Leaf extract 0.36 (1)
Farnesyl acetone Steam distillation Leaf essential oil 0.08 (2)
(continued on next page)
Food Research International 106 (2018) 317–334
Table 7 (continued)
N/S IUPC Common name Molecular formular Extraction solvent Plant part Biological activity % Composition Ref.⁎
48 Hexahydrofarnesyl acetone Terpenoid Aqueous methanol Leaf extract Flavor and fragrance agents 0.65 (1)
A.B. Falowo et al.
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69 2,6,6-Trimethylcyclohexa-1,3-dienecarbaldehyde Aldehyde Steam distillation Essential oil 0.05 (2)
⁎
References: (1): Mukunzi et al., 2011; (2): Chuang et al., 2007; (3): Sana et al., 2015; (4): Bhattacharya et al., 2014; (5): Zhao & Zhang, 2013; (6): Sahab & Nawar, 2015; (7): Al-Asmari et al., 2015; (8): Bose, 2007.
Food Research International 106 (2018) 317–334
A.B. Falowo et al. Food Research International 106 (2018) 317–334
H HO
OH
HO H
Phenethyl alcohol
Benzyl nitrile Acetic acid
Fig. 2. Chemical structure of representative bioactive phytochemicals reported from various parts of this plant.
there have not been many human clinical studies on the use of this plant biochemical parameters provide useful information for the evaluation
and further research in this area is needed to validate some of the health of the health status of birds and reflect many metabolic alterations of
claims attributed to M. oleifera use and consumption. organs and tissues (Makanjuola et al., 2014). Reports on the immune
responses of broiler chickens fed M. oleifera showed that it can increase
the production of red blood cells, white blood cells and the hea-
4. Dietary application of Moringa oleifera in livestock production
moglobin level in the blood system; as well as improve intestinal health
and products
by reducing the population of Escherichia coli and enhancing that of
Lactobacillus in the ileum (Stevens et al., 2015).
4.1. Livestock health and growth performance
Reportedly, the growth performance of broiler chickens fed M.
oleifera leaf meal (1, 3 and 5% of DM intake) showed significantly
Like some recently investigated plants such as Vachellia karroo
higher body weight, average daily gain and superior feed conversion
(Idamokoro, Masika, & Muchenje, 2016) and Cactus plant (Ben Salem &
ratio (i.e. number of units (kg) of feed used to produce a unit (kg) of
Smith, 2008), M. oleifera is rich in nutrients and bioactive compounds
meat) than birds fed the control diet, thereby improving growth per-
which offer great potential for its use as a livestock feed resource. The
formance (Nkukwana et al., 2014). On the contrary, Makanjuola et al.
leaf, seed and bark of M. oleifera are readily eaten by cattle, sheep,
(2014) and Onunkwo and George (2015) did not observe any sig-
goats, pigs, chickens and rabbits as an ingredient in the diet. The plant
nificant differences in the feed intake and body weight gain of broiler
has been used to improve the health status, growth performance, milk
chickens fed M. oleifera leaf meal included at 200, 400 and 600 g
production and meat quality of several livestock species. Serum
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Pregn-5,7-diene-3-ol-
Fig. 2. (continued)
respectively in 100 kg of feed when compared to control group. These the effect of M. oleifera seed, root and stem meal on livestock perfor-
studies revealed that M. oleifera leaf meal can be used as protein source mance, and more studies should be directed towards this area.
in poultry diets without causing any adverse effects on growth perfor-
mance.
Furthermore, the inclusion of M. oleifera leaf meal to replace cotton 4.2. Milk and Milk products
seed cake (CSC) at 25, 50, 75 and 100% in a ram diets has been found
not to affect the body weight gain compared to control diet (Adegun & In the face of increasing global food insecurity and malnutrition
Aye, 2013). In another study conducted by Ndemanisho, Kimoro, especially in developing countries, research on animal production and
Mrengeti, and Muhikambele (2007), average growth rate did not differ the development of food products that can improve economic growth
in goats fed CSC and M. oleifera Leaf meal based concentrates in rumen and human wellbeing in every society needs investigation. The utili-
fistulated goats. On the contrary, Moyo et al. (2012) found that goats zation of M. oleifera leaves to improve milk production and for value
fed diets containing 200 g of M. oleifera leaf had higher daily weight addition in milk products including cheese and yoghurt is now trending
gain and feed intake than those fed sunflower cake (SC) and the control (Gopalakrishnan et al., 2016; Oyeyinka & Oyeyinka, 2016). The use of
group. Moreover, Adeniji and Lawal (2012) found a significant increase M. oleifera as a fodder plant to improve livestock production can be
in feed intake and body weight gain of rabbits fed M. oleifera leaf at 20, attributed to the rich presence of minerals in the plant (Hekmat,
40 and 60% based diet in replacement of groundnut cake compared to Morgan, Soltani, & Gough, 2015), which are crucial for increased
rabbit on control diet. Mukumbo et al. (2014) also noted that pigs fed weight gain, milk yield and milk quality in ruminant animals
7.5% M. oleifera leaf based-diet showed higher average daily feed in- (Mendieta-Araica et al., 2011). Moringa oleifera is also known to be rich
takes and lower slaughter weight than the control group. In general, the in protein which is required to improve the microbial protein synthesis
increase in growth performance of livestock fed M. oleifera leaf diet has in the rumen vat of livestock (Soliva et al., 2005).
been attributed to its rich nutritional content, antioxidant and anti- Several studies on the use of M. oleifera as a replacement feedstuff to
microbial properties as well as the inherent natural enzyme which aid advance the yield and quality of milk of livestock such as goats
digestion of fibrous food in animals. (Babiker, Juhaimi, Ghafoor, & Abdoun, 2017), sheep (Babiker, Juhaimi,
Regarding M. oleifera seed, Ochi et al. (2015) reported significantly Ghafoor, Mohamed, & Abdoun, 2016) and cows (Cohen-Zinder et al.,
higher feed intake, feed efficiency and body weight gain in broilers fed 2016; Mendieta-Araica et al., 2011; Sarwatt, Milang'ha, Lekule, &
0.5% M. oleifera seed compared to control diet. However, at the in- Madalla, 2004) have been reported. In the study by Babiker et al.
clusion level higher than 0.5% M. oleifera seed in the diet, the same (2017), the replacement of alfalfa hay with 25% M. oleifera leaf powder
author found a lower feed intake, feed efficiency and body weight gain in a formulated diet for goats and ewes showed that, they had sig-
compared to control diet. This reduction in performance can be at- nificantly higher milk yield, milk fat, milk lactose and solid-non-fat
tributed to anti nutritional factors such as phytate which has been re- compared to the diet formulated with 40% alfalfa hay inclusion level.
ported to reduce bioavailability of minerals and decline digestibility of Furthermore, higher energy, catalase and serum content were also re-
starch and protein in animals (Reddy, Sathe, & Salunkhe, 1982; ported in milk of goats and ewes fed with M. oleifera leaf when com-
Thompson, 1993). Also, the administration of M. oleifera aqueous root pared to those fed with diets containing 40% alfalfa (Babiker et al.,
extracts at 5, 10 and 15 g/L to treat E. coli challenged broiler chicks 2017). According to Babiker et al. (2017), there was increase in the
during a nine day feeding trial revealed no significant difference in feed oxidative stability and vitamin C content of milk of goats and ewes that
intake, body weight gain and feed conversion ratio when compared to were fed with M. oleifera leaf (25% inclusion level) when compared to
chicks given commercial antibiotics (Abiodun, Adedeji, Taiwo, & those fed with Alfalfa hay. The high increase in the yield and quality of
Gbenga, 2015). However, there is still limited published literature on milk of goats and ewes fed with M. oleifera leaf when compared to those
fed with Alfalfa hay was attributed to the rich presence of micro
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nutrients including phosphorus, calcium, potassium and magnesium ground vegetables) were added to them or not (Hekmat et al., 2015;
(Babiker et al., 2017). Moyo et al. (2012) also attributed the presence of van Tienen et al., 2011). The reason for adding other food materials to
high anti-oxidant properties of M. oleifera leaf to be responsible for yoghurt fortified product is to suppress the colour intensity and herbal
improved productivity of livestock. smell of the leaf powder which may not be desirable to consumers.
In another related study, Mendieta-Araica et al. (2011) reported Hassan et al. (2016) reported that, the yoghurt made with 0.5% M.
that, cows fed with a formulated diet with 20% inclusion of M. oleifera oleifera inclusion rate had the highest score for taste and flavor com-
leaf had higher mean value of milk fat, total solids, non-fat solids, crude pared to the inclusion levels (1%, 1.5% and 2%) and control (without
protein and casein compared with those formulated with 20% soybean M. oleifera leaf powder). The study also observed that there were sig-
meal. Likewise, Sanchez, Sporndly, and Ledin (2006) reported an in- nificantly higher mean values of total solids, total protein, milk fat, total
crease in milk yield, milk fat and milk crude protein in cows fed with volatile fatty acids, diacetyl and acetaldehyde in the yoghurts made
2 kg or 3 kg dry matter (DM) M. oleifera leaf when compared to those with 0.5% M. oleifera leaf powder compared to those produced with
fed with Brachiaria brizantha hay alone. Khalel et al. (2014), used M. 1%, 1.5% and 2% inclusion rate and the control (without any Moringa
oleifera as a supplement feedstuff (20% and 40% inclusion level) in oleifera leaf powder). Furthermore, it was reported that yoghurt made
comparison with Trifolium alexandrium forage (40% inclusion level) in a with the addition of 0.5% M. oleifera leaf powder had higher mean
formulated; evaluating the milk yield and composition during lactation. values for all the 17 essential amino-acids that were identified in the
They reported that cows fed with the M. oleifera supplemented diets had product when compared with the other treatments and the control.
significantly higher (P ˂ 0.05) milk yield with 25% and 16% daily yield Howevera higher score was reported for the control treatment in terms
increase compared to those fed with Trifolium alexandrium hay. In ad- of colour and appearance as compared to the other treatments which
dition, there was increase (P ˂ 0.05) in total solids, solid non-fat, milk had 0.5%, 1%, 1.5% and 2% M. oleifera leaf powder inclusion.
fat, milk protein and ash of cows fed with M. oleifera ration compared to In another related study, Kuikman and O'Connor (2015) observed
those fed with the Trifolium alexandrium ration. that, the addition of fruits (banana, avocado and sweet-potato at
In a recent study, Cohen-Zinder et al. (2016) reported a significantly 250 mL per 1000 mL yoghurt) helped to boost the flavor and appear-
higher (P ˂ 0.05) milk yield, milk fat and milk energy composition for ance of yoghurt made with 1.7% inclusion of M. oleifera leaf powder. In
cows that were fed a diet formulated with M. oleifera leaf (44 g/kg DM that study, it was observed that, though the yoghurt made with M.
substitution rate) compared to the control diet formulated with wheat oleifera leaf powder may have higher nutritional content than the
hay. The increase in milk yield and quality as a result of M. oleifera leaf control (without M. oleifera), the resultant greenish colour and smell
supplement was attributed to the positive effect of the leaf in the rumen may be a major barrier to its acceptability by consumers. In line with
vat of ruminants, resulting to the increase in rumen microbial popula- this, Hekmat et al. (2015) also suggested that the addition of 5% sugar
tion that are found in the rumen environment (Sanchez et al., 2006). to yoghurt fortified with 0.5% M. oleifera leaf powder may boost the
Another possible reason for the increase in milk yield of cows fed with acceptability of the product in terms of flavor. However, they reported
M. oleifera leaves could be due to the fact that M. oleifera leaf possesses that at 1% M. oleifera leaf powder inclusion rate (plus 5% sugar); the
good rumen bypass attributes which is essential for animal productivity fortified yoghurt had a strong undesirable flavor which may hinder
(Sarwatt et al., 2004). The afore-mentioned studies are indicative of the consumer acceptability.
potential utilization of M. oleifera leaf as feed supplement in improving More research investigating other innovative techniques that can be
livestock productivity. employed to reduce the herbal smell and greenish colour resulting from
Research on the use of M. oleifera leaf extract as a functional food the inclusion of M. oleifera leaf powder in dairy products is needed for
additive to improve the nutritive value of foods such as bread, sauces, wider acceptability of these products. The use of flowers (Arise, Arise,
species, juices, biscuits, soup and dairy products (yoghurt and cheese) Sanusi, Esan, & Oyeyinka, 2014) and seeds (Ogunsina, Radha, &
among others is increasing (Mukunzi et al., 2011; Oyeyinka & Indrani, 2010) from M. oleifera instead of leaves could be utilized in
Oyeyinka, 2016). Several countries including Nigeria, Egypt, Ghana, order to reduce the smell and colour intensity in dairy products when
Malawi, Ethiopian and some East African countries have adopted the added as a fortificant (Oyeyinka & Oyeyinka, 2016), since they also
use of M. oleifera as food additives to improve the nutritional quality of have a substantial amount of protein and phyto-nutrients comparable to
some staple food (Hassan, Bayoumi, Abd El-Gawad, Enab, & Youssef, the leaves (Zaku, Emmanuel, Tukur, & Kabir, 2015). Another possible
2016). However, in this review, we shall be focusing on animal-sourced technique that can be adopted to suppress the smell and colour in-
foods, and in this section, on the utilization of M. oleifera leaf as nutrient tensity of M. oleifera leaf when used as additives in dairy products could
fortificant in dairy products. be the use of essential oil extracted from the plant parts. Essential oils
According to Oyeyinka and Oyeyinka (2016), the smell and greenish from M. oleifera possess important mirco-nutrients and phytochemicals
colour that may result due to the inclusion of M. oleifera leaf powder in (Anwar & Bhanger, 2003; Dahot & Memon, 1987; Farooq & Rashid,
dairy products may affect their acceptability by consumers. Some so- 2007) which can be used as fortificants for dairy products. Since es-
cieties where M. oleifera is highly utilized (as either food or food for- sential oils extracted from plant parts including leaves and flowers are
tificants) may have different perceptions in the scoring of the sensory colourless in most cases, they could be used as additives for dairy
attributes of dairy products fortified with M. oleifera leaf powder when products instead of the leaf extracts. Investigations on other innovative
compared to other places where these plant materials is not widely used techniques in removing the herbal smell and colour of M. oleifera leaf
as food or food additives. Hence, the inclusion of other food materials powder from dairy products without affecting their nutritional com-
such as banana, avocado and sweet potatoes among others have been position are worth researching.
recommended to improve their acceptability by consumers (Oyeyinka &
Oyeyinka, 2016). 4.3. Meat and meat quality
Yoghurt is a dairy food that is commonly consumed by people
worldwide. The use of M. oleifera leaf powder as condiments to boost its Fresh meat is a rich nutrient and moisture matrix ideal for the
nutritional quality has also been reported in literature (Babiker et al., growth and propagation of microorganisms, making it highly perish-
2017; Kuikman & O'Connor, 2015). However, the rate of inclusion of M. able and prone to spoilage (Zhou, Xu, & Liu, 2010). Microbial growth
oleifera leaf varies depending on the addition of other food materials and biochemical reactions are the main causative agents of spoilage,
(fruits, sugar or vegetables) to boost the product acceptability in terms resulting in deterioration of meat quality (Mills, 2004). The growth of
of colour, texture and taste (Oyeyinka & Oyeyinka, 2016). The inclusion microorganisms and associated release of metabolites results in de-
level of M. oleifera leaf powder in yoghurt ranges between 0.5%–3% composition and detectable deterioration of the organoleptic quality of
and this depends on whether fruits or other materials (e.g. sugar or meat (Ellis & Goodacre, 2001), while lipid oxidation is the main non-
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microbial cause of quality deterioration in muscle foods (Contini et al., research is needed on the mode of action of the various compounds and
2014; Gray, Gomaa, & Buckley, 1996). Both result in colour dete- their potentially synergistic effects.
rioration, off odour and flavors, nutrient losses, poor shelf life, and the A recent study by Cohen-Zinder et al. (2017) reported that, feeding
development of toxic compounds which can lead to food-borne illnesses lambs with a total mixed ration composed of 6.8% ensiled M. oleifera
(Ellis & Goodacre, 2001; Faustman, Sun, Mancini, & Suman, 2010). forage resulted in significantly lower shear force, as a result of in-
Lipid oxidation lowers the functional, sensory and nutritive values of creased sarcomere length, and lower intramuscular fat content.
meat and meat products; negatively impacting consumer acceptability Mukumbo et al. (2014) also reported lower intramuscular fat content in
(Bou, Guardiola, Tres, Barroeta, & Codony, 2004) as well as posing pigs fed diets containing 5 and 7.5% M. oleifera leaf meal, but no sig-
human health risks. The balance between pro-oxidants and antioxidants nificant difference in shear force in meat from pigs fed diets formulated
determines the oxidative stability of meat lipids (Pouzo, Descalzo, with 0–7.5% M. oleifera. Interestingly, higher levels of intramuscular fat
Zaritzky, Rossetti, & Pavan, 2016). Synthetic antioxidants, used ex- are typically correlated with lower shear force values and an increase in
tensively in the food industry to improve the shelf life, colour and flavor tenderness. The findings of these studies, however, suggest that, the
stability of meat products, have in some studies been implicated as a inclusion of M. oleifera leaves in diet had an effect on fat metabolism by
risk factor for degenerative diseases such as cancer (Hygreeva, Pandey, decreasing the intramuscular fat content without negatively affecting
& Radhakrishna, 2014). Recently, the safety of red and processed meat its tenderness. However, the mechanism of action for this effect is not
consumption came under intense scrutiny following the International yet fully understood and therefore requires further investigations.
Agency for Research on Cancer (IARC) evaluation on the carcinogeni- Cohen-Zinder et al. (2017) proposed that, dietary M. oleifera indirectly
city of red and processed meat, which attributed the formation of car- affects sarcomere length and consequently muscle fibre composition as
cinogenic compounds including N-nitroso-compounds (NOC), poly- well as the release of proteolytic enzymes from M. oleifera which pro-
cyclic aromatic hydrocarbons (PAH) and HAAs to processes and mote protein degradation in skeletal muscles. Consumer satisfaction of
additives used in curing, smoking, and high temperature cooking cooked meat depends largely on tenderness. Moyo et al. (2012) found
(grilling, pan frying, barbequing) (Bouvard et al., 2015). In line with that meat from goats supplemented with 200 g M. oleifera/day lost less
this, there is a growing demand for effective antioxidants from natural water during cooking, had tender meat and subsequently received
sources because they are increasingly viewed as being safer for human higher scores for aroma, juiciness and flavor by a consumer sensory
consumption (Falowo, Fayemi, & Muchenje, 2014). panel compared to the control diet.
As detailed in the previous sections and in numerous studies, M. Reports have it that most consumers' meat-purchasing decisions are
oleifera leaves possess immense nutritional value (Moyo et al., 2011; largely influenced by the colour (appearance) of meat (Mancini & Hunt,
Sánchez-Machado, Núñez-Gastélum, Reyes-Moreno, Ramírez-Wong, & 2005). A number of studies report meat colour enhancement as a result
López-Cervantes, 2010), polyphenolic content and antioxidant poten- of feeding M. oleifera leaves to livestock (Mukumbo et al., 2014; Shah
tial (Siddhuraju & Bekker, 2003; Sreelatha & Padma, 2009; Verma, et al., 2015; Wapi et al., 2013). The action of free radicals promotes the
Vijayakumar, Mathela, & Rao, 2009); as well as antimicrobial activity formation of metmyoglobin in meat, causing an unfavourable colour
(Jayawardana, Liyanage, Lalantha, Iddamalgoda, & Weththasinghe, change from red to brown (Falowo et al., 2014). Hence, enhanced
2015). Owing to its rich profile of polyphenols, tocopherols and car- colour retention can be attributed to the free-radical scavenging activity
otenoids, and reported antioxidant activity; many studies conducted on of M. oleifera leaves. Fat content and fatty acid profile also critically
the use of M. oleifera leaves and extracts to enhance meat quality have influences consumers' perceptions on meat quality. Dietary fatty acid
focused on their application as a natural antioxidant. The demand for (FA) consumption has come under increased scrutiny because saturated
natural alternatives to synthetic antioxidants used in the meat industry FAs have been implicated in aiding the increase of cardiovascular dis-
has grown in recent years (Falowo et al., 2014; Jayasena & Jo, 2013); eases, obesity and cancers (Nantapo et al., 2015), and has become an
due to their ability to prohibit lipid oxidation thereby enhancing meat influential factor affecting the selection and consumption of meat by
quality and shelf life. Since M. oleifera leaves are suitable for both consumers (Mukumbo & Muchenje, 2016). Further emphasis has been
human and animal consumption, they can be utilized to enhance meat placed on the balance between n-6 (linoleic acid, C18:2) and n-3 (li-
quality either through inclusion in animal diets or by direct applica- nolenic acid, C18:3) polyunsaturated fatty acids in food because the
tion/incorporation into meat products. It is well understood that animal ratio of n-6/n-3 has been identified as a risk factor for coronary heart
nutrition has a profound effect on the nutritional and chemical com- disease, formation of blood clots leading to heart attack and cancers
position of muscle tissue and on the aspects of meat quality such as pH, (Enser, 2001; Mukumbo & Muchenje, 2016; Wood et al., 2003). How-
colour, water holding capacity, tenderness, juiciness, flavor and aroma. ever, the use of M. oleifera in animal diet has helped to balance the ratio
A number of studies have assessed the effects of supplementation of M. of n-6 and n-3 in meat in an acceptable proportion for human con-
oleifera leaves in diets of various meat-producing animals as a means of sumption. Nkukwana et al. (2014) reported that, the dietary supple-
enhancing meat quality and safety (Table 8). Some limitations in the mentation of broiler chickens with M. oleifera (up to 5% of dry matter
bioavailability of polyphenols from natural antioxidants after con- intake) significantly increased n-3 content, reduced n-6/n-3 ratio in
sumption have been reported (Manach, Scalbert, Morand, Rémésy, & chicken breast meat.
Jiménez, 2004). Several studies have, however, found that meat from Research interest has recently turned towards the direct application
animals fed diets containing M. oleifera leaves had higher antioxidant or incorporation of M. oleifera into meat and meat products to improve
potential (Qwele et al., 2013) and lipid oxidative stability (Nkukwana physico-chemical properties, shelf life and nutritional value. The ap-
et al., 2014). This may be attributed in part to the high content of vi- plication of aqueous moringa leaf extract (MLE) has been reported to
tamin E in M. oleifera leaves, owing to the fact that dietary vitamin E inhibit lipid oxidation and enhance the colour of fresh beef (Shah et al.,
can be incorporated in the muscle tissue to improve lipid stability and 2015), raw and cooked pork patties (Muthukumar et al., 2014) during
meat quality. The findings of Descalzo et al. (2005) demonstrated the refrigerated storage. In these studies, an increase in redness (a*) was
important role of diet to be a significant avenue for the incorporation of observed with increasing MLE levels, attributed to the colour-stabilizing
vitamin E in muscle tissues. Moyo et al. (2012) reported increased ac- effect of antioxidant compounds in MLE preventing the oxidation of
tivity of the antioxidant enzymes superoxide dismutase and catalase, myoglobin to metmyoglobin. Unlike the dietary route, the direct ap-
and the non-enzymatic antioxidant reduced glutathione in liver from plication of M. oleifera extract to meat had no significant effect on the
goats supplemented with M. oleifera. This may be attributed to the shear force values of the meat. Strong antioxidant and antimicrobial
combined effects of phenolic compounds which have been found to activity of dry M. oleifera leaves was exhibited in chicken sausages
correspond with increased activity of these antioxidant enzymes. Since during 5 weeks of refrigerated storage (Jayawardana et al., 2015).
M. oleifera leaves contain multiple antioxidant compounds, more Sausages prepared with the inclusion of 0.5, 0.75 and 1% M. oleifera
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Table 8
Application of Moringa oleifera Lam. to enhance meat and meat product quality.
Animal species and age Mode and form of application Quantity and duration Sample analysed Effect on meat quality Ref.⁎
A. Dietary manipulation
Goats (8 months old) Supplementation (dried MO leaves) 200 g/day × 60 days LTL Increased total phenolic content and antioxidant activity, (1)
inhibited lipid oxidation
Goats (8 months old) Supplementation (dried MO leaves) 200 g/day × 60 days LTL Increased tenderness, reduced cooking loss, increased sensory (2)
quality
Pigs, 14 weeks old Formulated feed (dried MO leaves) 2.5, 5 and 7.5 g/100 g feed × 6 weeks LTL Increased shelf life, improved colour, reduced intramuscular (3)
fat content
Broilers (day old) Formulated feed (dried MO leaves) 1, 3 and 5 g/100 g feed × 5 weeks Chicken breast Increased n-3 PUFA content, reduced n-6/n-3 PUFA ratio, (4)
inhibited lipid oxidation
Lambs, 54 days old TMR (ensiled MO forage) 6.8% of TMR × 90 days LTL Increased tenderness (5)
B. Direct incorporation
330
Pork Moringa leaf extract (aqueous) 600 ppm × 9 days (raw) and 15 days (cooked) Raw and cooked (microwave, 4 min, 80 °C) Improved colour, inhibited lipid oxidation (6)
pork patties
Buffalo Moringa leaf extract (aqueous) 1%, 1.5% & 2%, cooked immediately Ground, cooked (10 min, 1600 °C) Increased water holding capacity, reduced cooking loss, (7)
lowered microbial TPC
Chicken Dried MO leaves 0.25, 0.5, 0.75 & 1 g/100 g meat × 5 weeks storage Chicken sausages Inhibited lipid oxidation, lowered microbial TPC (8)
at 4 °C
Beef Moringa leaf extract (aqueous) 0.1, 0.2 and 0.3 g MLE/L solution × 12 days at 4 °C Beef chunks Improved colour, inhibited lipid oxidation (9)
Beef Moringa leaf extract (ethanolic- 0.5 & 1 g/kg × 6 days storage at 4 °C Ground beef Lowered pH and inhibited lipid oxidation (10)
aqueous)
Beef Moringa leaf extract (ethanolic- 1 g/kg × 6 days storage at 4 °C Ground beef Reduced microbial TVC and LAB count (11)
aqueous)
MO: Moringa oleifera, LTL: Muscularis longissimus thoracis et lumborum; TMR: total mixed ration, PUFA: polyunsaturated fatty acid, MLE: Moringa leaf extract, TPC: total plate count, TVC: total viable count, LAB: lactic acid bacteria.
⁎
References: (1): Qwele et al., 2013; (2): Moyo, Masika, & Muchenje, 2012; (3) Mukumbo et al., 2014; (4): Nkukwana et al., 2014; (5): Cohen-Zinder et al., 2017; (6): Muthukumar, Naveena, Vaithiyanathan, Sen, & Sureshkumar, 2014; (7):
Hazra, Biswas, Bhattacharyya, Das, & Khan, 2012; (8): Jayawardana et al., 2015; (9): Shah, Bosco, & Mir, 2015; (10): Falowo et al., 2017; (11): Falowo et al., 2016.
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leaves had significantly lower TBARS, lower pH and correspondingly levels of above 15% could hamper the performance of laying birds
lower microbial Total Plate Counts compared to sausages treated with (Abou-Elezz, Sarmiento-Franco, Santos-Ricalde, & Solorio-Sanchez,
the synthetic antioxidant butylated hydroxytoluene (BHT) during sto- 2011; Kakengi et al., 2007; Olugbemi, Mutayoba, & Lekule, 2010).
rage (Jayawardana et al., 2015). Lower pH values of a product gen-
erally inhibit microbial growth and extend their shelf life. According to 5. Conclusion and future perceptive
Dahot (1998), M. oleifera leaves contain low weight proteins and pep-
tides with antibacterial and antifungal activity. Moringa oleifera leaves Current and ongoing research has revealed that M. oleifera Lam. is
also contain pterygospermin, a compound which dissociates into two an important plant that has multifunctional applications in human
molecules of benzyl isothiocyanate; which possesses antimicrobial nutrition, livestock production systems and products. Studies have de-
properties (Fahey, 2005). While some studies have reported that M. tailed the rich profile of essential nutrients and bioactive compounds in
oleifera leaf extract exhibited antimicrobial properties in raw (Falowo M. oleifera leaves, seeds and stems; alluding to the potential that the
et al., 2016) and cooked meat (Hazra et al., 2012), others found no addition of M. oleifera in diets and food products has to improve nu-
significant effect on pH and microbial counts, which may be due to the tritional status and wellbeing of consumers, especially pregnant and
binding of antimicrobial active compounds to food compounds. The nursing mothers. Similar information on the nutritional composition of
protein and fat contained in food can bind to and/or solubilize phenolic other plant-parts of interest, including the flowers, pods and roots is
compounds; reducing their availability for antimicrobial activity (El lacking. Historically, M. oleifera was first described as a medicinal herb
Abed et al., 2014). There is indeed a need for more studies to in- around 2000 BCE, and currently, a number of M. oleifera plant-based
vestigate the antimicrobial effect of M. oleifera leaf extracts in meat products such as food additives (leaf powder), nutraceutical (lip tea,
products which may be significantly different in food products than in drugs/capsules, essential oil) and functional foods (fortificant food e.g.
vitro. Insignificant antimicrobial activity may also be attributed to the bread, yoghurt and meat) have been developed for human and livestock
use of insufficient inclusion levels (Muthukumar et al., 2014). Higher consumption. The application of M. oleifera is regarded as safe and can
inclusion levels, however, may negatively impact on consumers' ac- provide consumers with healthy and functional food products.
ceptability of the product. Jayawardana et al. (2015) observed that the However, extensive research on its toxicity is required if M. oleifera is
inclusion of 0.5 g/100 g M. oleifera leaf extract was sufficient for in- going to be introduced as part of the daily diet for a large population.
hibition of lipid oxidation and microbial growth, while 0.75 and 1 g/ Additionally, consumption of M. oleifera also has been reported to boost
100 g M. oleifera leaf had a significant negative effect on sensory at- endogenous antioxidants and to fight excessive production of free ra-
tributes and texture of chicken sausages. There is ultimately a need to dicals. However, further research is needed to determine the bioavail-
conduct more research on the implications of M. oleifera incorporation ability of the nutrients and phytochemicals in M. oleifera once con-
on organoleptic properties and consumer acceptability. In the light of sumed. Its potential as a source of phytochemicals for the development
growing interest, utilizing the health-beneficial properties of M. oleifera of nanoparticles to combat human pathogens remains a rapid devel-
to enhance the functional value of meat products shows promise and oping area of research for scientists to exploit in human medicine. In
requires further clinical studies on the bioavailability of the bioactive this area, there is a need for more clinical studies and deeper research
compounds post-consumption. on the mode of action of the bioactive compounds. M. oleifera has
gained importance as a source of dietary ingredients in livestock and
4.4. Egg production and quality feed industry. The direct application of M. oleifera products as effective
natural antioxidant and antimicrobial agents to improve stability of
The utilization of eggs in the human diet plays a significant role in meat and meat products during processing and storage can provide an
tackling the issue of mal-nutrition. Eggs are a nutritionally complete alternative to synthetic antioxidants to meet the growing consumer
food and are affordable for both the rich and the poor in many societies. demand in this niche market. Despite positive results on the potential
Due to the increasing demand for eggs, the poultry industry seeks use of M. oleifera products in livestock diets to increase livestock health,
means of improving its production in terms of quantity and quality at a performance and product quality, there is yet a challenge of anti-nu-
low feed cost (Al-Harthi, El-Deek, Attia, Bovera, & Qota, 2009). Moringa tritional factors which could limit the inclusion level. However further
oleifera leaf meal is one of the plants that have been fingered to improve research on the utilization of enzyme additives (such as phytases) to
poultry production at a low cost input (Abbas, 2013). Recent studies enrich M. oleifera products should be considered in order to increase the
have shown that the inclusion of M. oleifera leaf powder in poultry diets inclusion level of M. oleifera and improve nutrient digestibility. Moreso,
improved the production and quality of eggs in poultry birds (Gakuya research focusing on effect of the M. oleifera plant on performance of
et al., 2014; Lu, Wang, Zhang, Wu, & Qi, 2016). The inclusion of 2.5% other livestock species and products (e.g. sheep and wool quality) and
and 5% of M. oleifera leaf powder in layer diet improved the egg other areas of the larger food system including environmental impact
number per week, egg weight, egg width, egg surface, yolk weight, yolk socioeconomic impact would be interesting as work little or no work
height, albumen weight and yolk ratio when compared to the control has been conducted and reported in this area.
diet (Ebenebe, Anigbogu, Anizoba, & Ufele, 2013). Kakengi et al.
(2007) reported significant increase (P ˂ 0.05) in egg weight when 5% Acknowledgements
M. oleifera leaf powder meal was used as a substitute to sun-flower seed
meal in layer diet. Likewise, Lu et al. (2016) showed that the inclusion The authors wish to thank the Govan Mbeki Research Development
of 5% level of M. oleifera leaf powder significantly improved the yolk Centre (GMRDC, Project ID: C262), University of Fort Hare, and the
colour and protein absorption without any adverse effects on the laying Department of Science and Technology/National Research Foundation
performance when compared to the control diet. However, the inclu- (Project ID: T359) for financial assistance.
sion of 1, 3 and 5% M. oleifera whole seed meal in layer hens' feed
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