Animal Feed Science and Technology 260 (2020) 114338

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Animal Feed Science and Technology

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Review article

Review of Moringa oleifera as forage meal (leaves plus stems)

T
intended for the feeding of non-ruminant animals
Manuel Valdivié-Navarroa,1, Yordan Martínez-Aguilarb,1, Odrey Mesa-Fleitasa,
Aroldo Botello-Leónc, Cesar Betancur Hurtadod, Borja Velázquez-Martíe,*
a
Instituto de Ciencia Animal, Carretera Central, km. 47½, San José de las Lajas, Mayabeque, Cuba
b
Departamento de Ciencia y Producción Agropecuaria, Escuela Agrícola Panamericana, Valle de Yeguare, San Antonio de Oriente 96, Honduras
c
Carrera de Zootecnia, Facultad de Ciencias Agrarias, Universidad Técnica "Luis Vargas Torres" de Esmeraldas, Esmeraldas, Ecuador
d
Departamento de Ciencias Pecuarias, Facultad de Medicina Veterinaria y Zootecnia, Universidad de Córdoba, Carrera 6 No 76-103, Montería,
230002, Colombia
e
Departamento de Ingeniería Rural y Agroalimentaria, Universitat Politècnica de Valencia, Camino de Vera s/n, 46022 Valencia, Spain

A R T IC LE I N F O ABS TRA CT

Keywords: A review of the chemical composition of the Moringa oleifera forage meal (leaves plus stems) and
Moringa the possibilities of safe use in the feeding of non-ruminant animals was made. The forage meal
Biomass obtained from Moringa oleifera at 35 to 60 days from regrowth and cut at 5 to 40 cm height from
Chemical composition the soil has good protein concentration, and its amino acid content is similar to the alfalfa forage
Secondary metabolite
meal. In addition, the moringa forage meal has a high content of crude fiber (CF), neutral de-
Bioactive substance
tergent fiber (NDF), acid detergent fiber (ADF), and acid detergent lignin (ADL), which must
Animal feed
cause a low content of metabolizable energy (ME) for poultry and pigs. Apparently, the con-
tribution of secondary metabolites and bioactive substances at low concentrations does not harm
the growth performance and quality of the final product. Moreover, we recommend favorable
levels of inclusion in the diets of poultry, pigs and rabbits.

1. Introduction

The tree of Moringa oleifera Lam. is a forage plant whose leaves and stems, obtained from continuous cuts, has been used as meal
or pellets in animal feeding with 88 to 92% dry matter (DM) (Valdivié et al., 2016b). This feed can be handled easily in feed mills,
efficiently and with positive economic impact, very similar as it is done internationally with alfalfa forage meal and other forage
plants with more than 15% crude protein (CP). It is necessary to establish an efficient sowing, cultivation and harvesting system,
(Padilla et al., 2016), which allows to have abundant biomass, with a little variable chemical composition and high quality.
The fields of M. oleifera intended for animal consumption are cut mechanically or manually, depending on the surface to be cut
every day and the availability or not of harvesting machines (Pérez et al., 2010; Padilla et al., 2016). Also, the height of cut commonly
ranges between 5 and 40 cm (Pérez et al., 2010; Mendieta-Araica et al., 2013; Basra et al., 2015; Ramos-Trejo et al., 2015; Dao et al.,
2017).
Also, the wide variability in the chemical composition of the moringa forage meal is directly influenced by the planting densities,
length of establishment period, cutting frequency, cutting height, drying method, genotype of the plant and other environmental and

⁎
Corresponding author.
E-mail address: borvemar@dmta.upv.es (B. Velázquez-Martí).
1
All Authors contributed equally to this manuscript.

https://doi.org/10.1016/j.anifeedsci.2019.114338
Received 6 February 2019; Received in revised form 18 July 2019; Accepted 25 October 2019
0377-8401/ © 2019 Published by Elsevier B.V.
M. Valdivié-Navarro, et al. Animal Feed Science and Technology 260 (2020) 114338

human variations (Sánchez et al., 2006a; Jongrungruangchok et al., 2010; Joshi and Mehta, 2010; Ogbe and Affiku, 2011; Leone
et al., 2015a, 2015b; Padilla et al., 2016; Savón et al., 2017). Our aim in this review was to inform the basic chemical composition,
the amino acid content and the characterize of their secondary metabolites and main bioactive substances in the forage meal obtained
from M. oleifera (leaves plus stems), cut at a height of 5 to 40 cm from the soil, with regrowth age between 35 and 60 days, as well as
to recommend the safe inclusion levels in balanced feeds, which generate a positive economic impact and which do not damage the
health, viability, growth, reproduction and production of animals.
The Moringa oleifera is a fast-growing softwood tree that can reach 12 m in height, which belongs to the Moringaceae monogeneric
family, which includes another 12 species and is native to the foothills of the Himalayas, north of India, Pakistan and Nepal (Paliwal
and Sharma, 2011; Sharma et al., 2011; Roloff et al., 2009). It is grown in arid and semi-arid regions of India, Pakistan, Afghanistan,
Saudi Arabia, and also grows in African countries such as Ghana, Nigeria, Ethiopia, East Africa and Malawi (Ramachandran et al.,
1980; Agbogidi and Ilondu, 2012; Nouman et al., 2014) and other countries belonging to the American continent such as Nicaragua,
Cuba, Guatemala, Paraguay, Venezuela, Brazil, Argentina, Ecuador (Ayerza, 2011; Sánchez et al., 2006b; Valdes et al., 2017).
Research on the nutritional characterization of Moringa oleifera in Cuba was developed by Ly et al. (2016); Valdivié et al. (2016);
García and Macias (2014); Caro et al. (2018) and in Brazil by Macambira et al. (2018). The climate of these two regions, San José de
Las Lajas and Caraúbas, where these investigations were developed were different, which could influence the nutritional composition
of the Moringa oleifera. At the Institute of Animal Science (ICA), located at San José de Las Lajas, Mayabeque, Cuba, the study was
carried out with a typical red ferralitic soil, of rapid desiccation and uniform profile (Hernández et al., 1999), the climate is tropical,
in winter there is much less rain than in summer, the average temperature is 24.0 °C, the approximate average rainfall is 1558 mm.
However, in Caraúbas, Brazil, the climate is very hot and semi-arid, with an average rainfall of 734 mm/year. Its rainy season is from
February to May. The average annual temperatures are: maximum: 32 °C, average: 27 °C and minimum: 22 °C. Average annual
relative humidity is 66% and sunshine time is 2 700 h/year.
On this subject, Aslam et al. (2005); Asante et al. (2014) and Dania et al. (2014) noted that the nutritional composition of Moringa
oleifera varies in different places. The tree that is grown in India has slightly different nutritional components than those in Nigeria
(Aslam et al., 2005). In turn, Asante et al. (2014) studied the nutritive composition of the leaves of Moringa oleifera from two semi-
deciduous ecological localities and the Savannah regions, which showed that the latter was less nutritious than the previous one and
attributed it to the high temperatures in the Savannah regions, at higher temperatures, the proteins and enzymes become denatured
and this could be the cause of the difference in nutrient content. Also, soil is an important factor that defines the nutrient content and
the strength of the plant . Likewise, the circumference of the stem and the vegetative growth of the moringa increased with the
application of bird manure. The general nutritional attributes of the plant remain the same, although there is variability of nutrients.

2. Growth conditions

The Moringa oleifera, grows mainly in regions with tropical or subtropical dry to humid climates, annual rainfall of 760–2500 mm,
requires less than 800 mm of irrigation. It grows on any type of soil, where the heavy and saturated water clayey stands out, with a pH
between 4.5 and 8.0 (Palada, 1996; Nouman et al., 2014). It can grow at altitudes between 0–1800 masl, although better results are
obtained below 600 masl (F/FRED, 1994). Moringa has a wide range of adaptation to different temperatures (F/FRED, 1994; Palada,
1996; Nouman et al., 2014; Valdes et al., 2017). The temperature requirement for the cultivation of Moringa oleifera is between 18
and 28 °C (Palada, 1996; Nouman et al., 2014). In Central America, this plant is located in areas with average temperatures that vary
between 6 and 38 °C, although it is able to withstand low temperatures, but not below 2–3 °C. In addition, it is important to bear in
mind that once the temperatures fall below 10 °C, the flowering process is affected, so in these cases the dispersion should depend on
the vegetative cuttings. In its natural habitat, average annual temperatures show large fluctuations, during the coldest months, it is
between −1 °C and +3 °C, while in the warmer months it is 38 °C–48 °C (Valdes et al., 2017).
The cultivation of Moringa oleifera is mainly done through sowing and cutting, traditionally, seeds are preferred in Sudan, while
vegetative propagation is common in India, Indonesia and in some areas of West Africa (Palada, 1996). The seeds germinate in two
weeks, a maximum depth of 2 cm, when sowing is done in the nursery, the seedlings can be transplanted when they reach about
30 cm, from 3 to 6 weeks after germination (Ojiako et al., 2011).
Number of seeds per kg of 3000–9000, depending on the variety, with a germination rate of 80%–90% for ideal storage conditions
(3 °C, 5%–8% humidity); however, the rate of germination is reduced to 7.5% after three months (Roloff et al., 2009; Morton, 1991).
It is preferred to cut when the availability of seeds is scarce and/or when work is not a limiting factor. When hardwoods 1–2 m long,
4–16 cm in diameter (Palada, 1996) of adult trees are planted, during the rainy season, during the year, the roots that in a few months
reach a considerable size (Jahn et al., 1986).

3. Bromatological composition

The fresh forage of M. oleifera cut at a height of 5 to 40 cm from the soil and between 35 and 60 days of regrowth contains
between 15.20 and 22.60% DM, with an average of 17.99% (Valdivié et al., 2017), although as is known, drying ensures a greater
concentration of nutrients; thus in moringa forage meal with a DM between 88.24 to 88.85% (Safwat et al., 2014; Ly et al., 2016; Caro
et al., 2018), the CP oscillate between 15.31 and 22.66%, with an average value of 20.20% and a coefficient of variation of 10.10%
(Table 1). This variability has been associated with multiple factors mainly related to the leaves and stems, such as genetic variety,
soil fertility, cultivation methods, temperature, humidity, photoperiod, environmental radiation conditions, loss of leaves during
handling and drying of green forage, loss of dust during milling (depending on quality and type of mill), lab errors and deterioration

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M. Valdivié-Navarro, et al. Animal Feed Science and Technology 260 (2020) 114338

Table 1
Chemical composition of the Moringa oleifera forage meal (leaves plus stems) (dry basis).
Source: taken from Pérez et al. (2010); Nouman et al. (2014); Ramos-Trejo et al. (2015); Padilla et al. (2016); Rodríguez et al. (2016); Savón et al.
(2017); Valdivié et al. (2017); Macambira et al. (2018); Méndez et al. (2018)
Composition, % n Values SD ± CV % Minimum Maximum

DM in natura 12 17.96 0.99 4.71 15.05 22.60

CP 31 20.20 2.04 10.10 15.31 22.66
Ethereal extract 7 3.10 1.00 32.29 1.80 4.16
Ashes 19 10.31 1.85 17.95 6.49 14.16
Nitrogen-free extract 5 44.94 8.93 19.87 31.25 52.59
Organic matter 19 89.69 1.86 2.07 85.84 93.51
CF 18 30.02 8.92 29.72 14.50 44.32
NDF 18 48.29 10.18 21.08 33.31 66.34
ADF 16 35.36 7.62 21.54 22.23 45.94
ADL 14 9.32 2.33 25.01 5.43 13.66
Cellulose 13 26.76 8.81 32.92 11.30 43.98
Hemicellulose 6 11.74 2.01 17.08 8.97 15.08
Calcium 14 1.66 0.72 43.41 0.99 3.00
Total phosphorus 14 0.40 0.10 24.38 0.21 0.61

SD: standard deviation CV: coefficient of variation.

during storage (Sánchez et al., 2006a; Jongrungruangchok et al., 2010; Joshi and Mehta, 2010; Ogbe and Affiku, 2011; Leone et al.,
2015a, 2015b; Padilla et al., 2016).
Moringa oleifera leaf meal contains more CP than M. oleifera forage meal (leaves plus stems) because the first one does not have the
stem (Makkar and Becker, 1997; Falowo et al., 2018; Méndez et al., 2018). In this sense, Olugbemi et al. (2010); Ayssiwede et al.
(2011), and Moyo et al. (2011) found that CP value varies between 27 and 30% when worked with M. oleifera leaf meal without
stems.
However, M. oleifera forage meal (leaves plus stems) is considered a good source of protein when compared to other grass forages
(NRC, 2007; Bahamondes et al., 2016; Lemenager et al., 2016) and it has the same the level of the best-recognized protein forages
such as the alfalfa forage meal (15–22.7% CP) (NRC, 2012; Heuzé et al., 2016; Sun et al., 2018), hence this alternative feed could be
used daily as a partial substitute of corn and soy cake and as a total substitute for alfalfa forage meal in the diets of poultry, pigs,
rabbits and other non-ruminant species. On the other hand, the ethereal extract of moringa forage meal is low. Although it has a high
coefficient of variability (Table 1), its contribution of digestible energy (DE) or metabolizable energy should not be high for poultry,
pigs and other animals, as well as its contribution of acids fatty acids (Leeson and Summers, 2009; Aly et al., 2016).
Authors such as Makkar and Becker (1996), 1997; Al-Masri (2003); Sánchez et al. (2006a) and Sánchez et al. (2006b) have
reported that moringa forage meal has a good concentration of ashes, although with wide chemical variability (Table 1). In this sense,
the calcium content oscillates in high values from 0.99 to 3.00%, which is very favorable for laying hens, however when this meal is
included in high concentrations in the diets can cause a mineral imbalance (mainly with the phosphorus) in growing animals or meat
producers (Leeson and Summers, 2009). Likewise, the total phosphorus contents in moringa forage meal is acceptable from 0.21 to
0.61% taking as reference other traditional feeds (Moyo et al., 2011; Rostagno et al., 2011; Falowo et al., 2018), however, its
composition in available phosphorus is not high (Valdivié et al., 2016a, 2017), it will be necessary to specify the contributions of
inorganic phosphorus in non-ruminant animal diets fed with moringa forage meal.
As in with most forages, the components of the fiber (CF, NDF, ADF, ADL, cellulose and hemicellulose) are relatively high in M.
oleifera forage meal done from leaves plus stems. This have from 14.50 to 44.32% CF, from 33.31 to 66.34% NDF, from 22.23 to
45.91% ADF and from 5.43 to 13.66% ADL (Table 1). For ruminants and herbivores, the fiber components of M. oleifera leaves are
more accessible to the action of rumen microorganisms and microbial enzymes, have a high rate of ruminal degradation, less ruminal
retention and cause a higher consumption voluntary, because the leaves have less vascular tissue and sclerenchyma, as well as less
lignin than grasses and other traditional forages (Kholif et al., 2015).
Several papers have shown the positive role of fiber in the diets of non-ruminant animals; the fiber has been attributed digestive,
antimicrobial, immune functions and regulators of harmful lipids (Martínez et al., 2015; Savón, 2016). In this sense, in rabbits, fiber is
essential to live, because of its role in cecotrophy (de Blas et al., 2015), in replacement laying pullets (from 10 to 16 weeks) high fiber
levels are used to modify the GIT and prepare them for egg laying (Martínez et al., 2015) and in sows in gestation and lactation it is
acceptable the fiber in a balanced diet to improve the farrowing process, body condition, milk production and piglet health (van der
Peet-Schwering et al., 2003).
However, high levels of dietary fiber may increase digestible energy loss, reduce mineral availability, and influence negatively the
bioproductive indicators (Mateos et al., 2012). In this sense, the fibrous components in the moringa forage meal cause that their
contribution of digestible energy, ME or net energy is poor for non-ruminant species such as poultry and pigs, because structural
carbohydrates are poorly digested and absorbed in the stomach and small intestine, they can also reduce digestion and absorption of
other feeds that make up the diet due to their physical and chemical properties (Yu et al., 2016; Valdivié et al., 2017).

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M. Valdivié-Navarro, et al. Animal Feed Science and Technology 260 (2020) 114338

Table 2
Amino acid content of the forage meals from Moringa oleifera (Supergenius variety and Pernambuco cultivar) and alfalfa (dry basis).
Amino acids, % Alfalfa forage meal1 Moringa oleifera, Supergenius variety2 Moringa oleifera, Pernambuco cultivar3

CP 17.50 17.18 18.08

Methionine 0.25-0.27 0.24 0.31
Cystine 0.18-0.23 0.40 0.22
Methionine plus cystine 0.43-0.50 0.64 0.53
Lysine 0.69-0.73 0.51 0.93
Threonine 0.70-0.73 0.49 0.77
Tryptophan 0.24-0.38 0.15 0.37
Arginine 0.71-0.72 1.20 0.99
Isoleucine 0.68-0.83 0.49 0.77
Leucine 1.21-1.30 0.87 1.51
Valina 0.86-0.97 0.63 0.97
Histidine 0.35-0.37 0.24 0.38
Phenylalanine 0.84-0.91 0.58 1.01
Glycine 0.80-0.82 0.72 0.90
Serina 0.77-0.80 0.53 0.74
Proline 0.79-1.33 0.67 0.86
Alanine 0.86-0.93 0.73 1.09
Aspartic acid 1.87-1.88 1.03 1.53
Glutamic acid 1.47-1.78 2.12 2.03

Heuzé et al. (2016)1; Valdivié et al. (2017)1; Macambira et al. (2018)3.

4. Contribution of amino acids

Table 2 shows the contribution of amino acids from the forage meal of Moringa oleifera, Supergenius variety and Pernambuco
cultivar, cut at 55 day of regrowth at a height of 40 cm from the soil with 17.18 and 18.08% CP, respectively, compared with the
alfalfa forage meal with 17.5% CP.
The forage meal obtained from Moringa oleifera (Supergenius variety) produced in Cuba has more cystine, methionine plus cystine
and arginine than the Pernambuco cultivar produced in Brazil, however the latter has more lysine, threonine, tryptophan, isoleucine,
leucine, valine, histidine, phenylalanine, serine, proline, alanine and aspartic acid (Table 2), which could be associated to multiple
causes, maybe the non-appearance of the main stem in the Pernambuco cultivar could influence this result. However, more analysis is
required to have a better idea of the average amino acid balance and its range of normal variation in some countries.
Moreover, Moringa oleifera (Supergenius variety) forage meal has more cystine, sulfur amino acids and arginine than the alfalfa
forage meal, but less concentration for the other amino acids, as occurred with the Pernambuco cultivar. In addition, Pernambuco
cultivar has more lysine and arginine than alfalfa forage meal, while in the rest of the amino acids the difference was minimal, which
indicate that moringa forage meal is similar or better in its contribution of amino acids (Table 2).
These results demonstrate the protein and amino acid (arginine, lysine and sulfur amino acids) potential of moringa forage meal,
which is important for non-ruminant animals in all productive stages. In this sense, dietary substitution of alfalfa forage meal by
moringa forage meal could increase the contributions of some essential amino acids; therefore, arginine participates in the synthesis
of proteins, nitric oxide, polyamines and creatine as well as reduces platelet aggregation and monocyte adhesion in humans and
animals (Sikalidis, 2015). Moreover, the sulfur amino acids improves the egg weight and albumen/yolk ratio in laying hens and it is
indispensable to growth and development non-ruminant animals (Safaa et al., 2008; Martínez et al., 2017). Likewise, from the
practical point of view, the lysine (mainly Pernambuco cultivar) could stimulus egg production and breast yield in poultry; also, it has
been shown that it has a central role in the absorption of calcium and production of hormones, enzymes and antibodies (Liao et al.,
2015).

5. Secondary metabolites and bioactive compounds

The young forages (leaves plus stems) of M. oleifera from 35 to 60 days of regrowth have moderate amounts of secondary
metabolites and bioactive compounds with pharmacological, nutraceutical and growth promoting properties, which are concentrated
in the leaves, petioles and to a lesser extent in the stems (Makkar and Becker, 1997; Bennett et al., 2003; Amaglo et al., 2010; Moyo
et al., 2011; Ogbe and Affiku, 2011; Mbikay, 2012; Nouman et al., 2014; Leone et al., 2015a, 2015b; Tanwar et al., 2018).
The concentrations of these secondary metabolites and bioactive compounds in the leaves plus stems of M. oleifera are variable
and appear indistinctly in the chemical analyzes, which is attributed to several causes such as genetic variations of the plants, state of
growth-development-maturity of the plants, different cultivation techniques, agroclimatic differences between countries or regions,
type and intensity of solar radiation, attack of pests-diseases, drying methods, types of mills (loss of dust during milling), damage
during storage, leaf: forage stem ratio, incorrect sampling method and effects of laboratories and chemical analysts (Sánchez et al.,
2006a; Joshi and Mehta, 2010; Ogbe and Affiku, 2011; Förster et al., 2015; Leone et al., 2015a, 2015b).
The total polyphenols are quantified in the forages (leaves plus stems) and leaves of M. oleifera at concentrations ranging between
1.13 and 4.43% with an average of 2.89% (Gupta et al., 1989; Makkar and Becker, 1996, 1997; Moyo et al., 2011; Leone et al., 2015a,

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2015b). Tannins expressed in the form of tannic acid are also detected at concentrations ranging between 1.2 and 2.19% (Makkar and
Becker, 1996, 1997; Ogbe and Affiku, 2011), Moyo et al. (2011) found very low values (0.31%). Tannins are polyphenols of plants,
which have the ability to form complex bonds with metal ions and with macromolecules such as proteins and polysaccharides
(Arbenz and Avérous, 2015; Marín et al., 2015), hence a high concentration of this secondary metabolite can reduce the efficiency in
the use of feed and decrease the gain of body weight in broiler and other non-ruminant species (Dei et al., 2007; Aguilar et al., 2013).
Nevertheless, this is not the case with the leaves and forages (leaves plus stems) of M. oleifera when is consumed at relatively high
concentrations, as have been indicated by the investigations of Valdivié et al. (2016) and Valdivié et al. (2017).
Flavonoids are the main phenolic compounds of M. oleifera leaves and both flavonoids and phenolic acids from the forages of M.
oleifera contribute to use this plant as nutraceutical (Leone et al., 2015a, 2015b). The main flavonoids found in the leaves of M.
oleifera are different types of quercetin, kaempfenol, and apigenin; as well as glycosylated flavonoids derived from the condensation
of kaempferol with rhamnose and glucose (Anwar et al., 2007; Leone et al., 2015a, 2015b).
Saponins are glycosides that include steroid saponins and triterpenoid saponins (Dei et al., 2007; Munafo and Gianfagna, 2015)
which, at high concentrations in feed, can reduce feed intake and growth of chickens and other non-ruminant animals (Dei et al.,
2007; Bartoš et al., 2016; Nesseim et al., 2017). The reduction of feed intake is associated with the pungent and irritating taste of
saponins (Siddiqui et al., 2017; Salehi et al., 2018). Although the saponins can cause hypocholesterolemia, because it binds to
cholesterol in feeds and limits or prevents their absorption (Tanwar et al., 2018). Also, this secondary metabolite has hemolytic
activity (Vo et al., 2017) and their complexes with proteins can reduce the digestibility of proteins (Gemede and Ratta, 2014). The
concentrations of saponins determined in the leaves and forages (leaves plus stems) of M. oleifera are moderate, with values ranging
between 1.6 and 8.1% with an average of 4.9% (Makkar and Becker, 1996, 1997; Ogbe and Affiku, 2011).
Plants contain organic phosphorus compounds called phytates, which are linked to calcium, iron, magnesium or zinc, amino acids
of proteins and other compounds (Leeson and Summers, 2009; Muhammad et al., 2011; Falowo et al., 2018), which are indigestible
in the gastro-intestinal tract (GIT) of non-ruminant animals and therefore not absorbed because these animals do not synthesize
phytase enzymes (Bernal et al., 2006). The leaves and forages (leaves plus stems) of M. oleifera contain important amounts of
phytates, ranging between 2.1 and 3.1%, with an average value of 2.56% (Gupta et al., 1989; Makkar and Becker, 1997; Ogbe and
Affiku, 2011; Leone et al., 2015a, 2015b), in consequence, it is recommended to incorporate phytase enzymes in diets containing
leaves or fodder meal of M. oleifera, to increase the digestibility and absorption of nutrients and to reduce feeding costs, as indicated
by Bernal et al. (2006), when they using other feeding systems without moringa forage meal.
Naturally, oxalate binds with calcium to form calcium oxalate crystals. When these crystals reach the kidneys, they form the so-
called stones, which block the renal tubules, causing severe pain (Vinaiphat et al., 2017; Alelign and Petros, 2018). In the leaves and
forages (leaves plus stems) of M. oleifera, calcium oxalate appears as crystals in the cells of the plant (Radek and Savage, 2008) at
concentrations ranging between 0.45 and 4.1%, with an average of 2.42% (Gupta et al., 1989; Ogbe and Affiku, 2011; Nouman et al.,
2014). Moringa leaves contain only insoluble oxalates, which are excreted in feces and animals cannot assimilate (Stevens et al.,
2015), thus they are not harmful to the kidney.
The inhibitors of trypsin and chymotrypsin prevent the functioning of these enzymes, deteriorating the digestion of proteins,
depressing growth and causing a thickening of the pancreas (Leeson and Summers, 2009; Kostekli and Karakaya, 2017). Fortunately,
in the leaves and forages (leaves plus stems) of M. oleifera, most analyzes indicate that these protease inhibitors are absent (Makkar
and Becker, 1996, 1997), however, in a study by Ogbe and Affiku (2011) were at a relatively low level (3.00%).
Hydrogen cyanide (HCN) has an affinity for metal ions of Fe and Cu, being toxic when ingested in important quantities, as it reacts
with iron in the blood, preventing the oxygenation of the organism and causing death by asphyxia (Bernal et al., 2006). It also reacts
with the Cu of some enzymes, interfering with normal metabolism. According to Gupta et al. (1989) its presence in the leaves and
forages (leaves plus stems) of M. oleifera is null or reduced (from 5 to 6 mg/kg of HCN).
The adverse effect of HCN is counteracted through physical, biological and nutritional methods (Nambisan, 2011). However, in
the liver, HCN at low concentrations has positive effects, because in the presence of sulfur it forms thiocyanates and isothiocyanates
(Castanheiro et al., 2016), which are related to the peroxidase system and the metabolism of glutamine with beneficial effects such as
isothiocyanates which have bactericidal properties (Keppler et al., 2017), its contact with the peroxidase system contributes to reduce
the formation of free radicals and glutamine favors the proliferation of the T-lymphocytes and as a consequence phagocytosis in-
creases (Lushchak, 2014; Amorati and Valgimigli, 2015).
The leaves of M. oleifera have rhamnose, a sugar that contributes to the synthesis of glucosinolate called glucomoringin (Fahey
et al., 2001; Bennett et al., 2003; Amaglo et al., 2010). The glucosinolates of the moringa leaves were considered by Doerr et al.
(2009) as responsible for its acrid-pungent flavor. Some glucosinolates have been shown to be harmful so they are not accepted at
high levels; values that can be detrimental to fertility of sows are those that are above 4 μmol of glucosinolates/g in the diet and
8 mmol of daily feed (Makkar and Becker, 1997).
The presence of substances with documented pharmacological activity, such as salicylic acid and ferulic acid, were recently
identified in the M. oleifera leaves by Leone et al. (2015a), who found concentrations ranging from 0.14 to 0.33 mg of salicylic acid
per 100 g and from 304 to 427 mg of ferulic acid per 100 g. Salicylic acid is the main metabolite of aspirin, identified as an anti-
inflammatory that seems to be involved in the prevention of some types of cancer (Dachineni et al., 2016), while ferulic acid inhibits
the promotion of tumors, reduces cholesterol and triglycerides of serum and liver and also functions as a hepatoprotective (Kesh
et al., 2013).
According with Moyo et al. (2011) and Folorunso et al. (2012) the Moringa oleifera leaves are rich in other substances with
recognized antioxidant properties, such as Beta-carotenes (from 68 to 285 mg/kg with an average of 174 mg/kg), vitamin C (from
2200 to 9670 mg/kg with an average of 7231 mg/kg) and vitamin E (1100 mg/kg). It is known that vitamin C is an essential nutrient

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M. Valdivié-Navarro, et al. Animal Feed Science and Technology 260 (2020) 114338

Table 3
Recommended inclusion levels of Moringa oleifera forage meal (leaves plus stems).
Source: taken from García and Macias (2014); Valdivié et al. (2014); Valdivié and Ponce
de León (2015); Almeida et al. (2016); Ly et al., 2016; Valdivié et al. (2016a); Mireles
et al. (2017); Valdivié et al. (2017); Caro et al. (2018); Macambira et al. (2018).
Animals Inclusion levels (%)

Laying hens
Replacements pullets, 0–8 weeks 10
Replacements pullets, 9–18 weeks 20
Layings, 20–25 weeks 20
Layings, +26 weeks 10
Ducks
Starter 20
Grower 30
Finisher 40
Broilers
Starter, 1–7 days 0
Grower, 8–35 days 5
Finisher, +36 days 10
Camperos chicks
Starter, 1–28 days 20
Grower, 29–57 days 20
Finisher, 58–70 days 20
Rabbits
Growth-fattening 30
Reproduction 35
Pigs
Gestanting Sows, 6–16 weeks 40
Lactacting sows 15
Lactating, from the first meal to the weaning 15
Grower, 28–75 days 20
Growing pigs, 20–115 kg 20

for humans and not essential for farm animals, because ruminal microorganisms synthesize vitamin C and birds and pigs synthesize
vitamin C in the liver (Achilonu et al., 2018). However, vitamin C is an antioxidant component of plasma and extracellular fluids that
surround the lung, lens and retina, as well as protect the phagocytic cells involved in the defense against invasion of pathogens. In
cases of stress, it is advisable to use ingredients rich in vitamin C (Blaszczak et al., 2019). In addition, vitamin E is an essential to farm
animals and is the main lipid‐soluble antioxidant; it protects unsaturated fatty acids (MUFA and PUFA) against chemical reactions
with reactive oxygen and nitrogen species (ROS and RNS), prevents membrane destabilization and cellular dysfunction (Zingg, 2019),
it is therefore important to use ingredients, and supplements rich in this vitamin.
In the forages (leaves plus stems) and leaves of M. oleifera no lectins have been detected resins and only very little presence of
mucilage (Makkar and Becker, 1996, 1997). According to Velázquez-Zavala et al. (2016), another group of substances with diverse
medicinal properties can appear in the leaves and barks of the stems of M. oleifera, although they do not mention the concentrations
found in those parts of the plant.
The contribution of secondary metabolites and bioactive substances from the Moringa oleifera forage meal does not cause damage
when used at appropriate levels of diets for non-ruminant animals (Makkar and Becker, 1996, 1997; Valdivié et al., 2017) and it can
promote nutraceutical properties when its use levels are adjusted (Mbikay, 2012; Leone et al., 2015a, 2015b; Nkukwana et al., 2015).

6. Safe levels of use in the feeding of non-ruminant animals

During the last years, several articles have been published, showing the possibility of including safe levels of moringa forage meal,
in balanced feed for poultry, pigs and rabbits without damage health, survival, mortality, growth rate, efficiency of feed use, egg
production and reproduction, with a positive economic impact, by significantly reducing feed and production costs.
The inclusion levels considered safe for feed intended for non-ruminant animals are shown in Table 3. In the diets for ducks, it is
recommended the dietary inclusion with 20, 30 and 40% of moringa forage meal during the starter, grower and finisher, respectively
to increase the carcass plus edible viscera yields and reduce the cost to produce one kg of carcass (Valdivié et al., 2014). Also, the
inclusion with 20% of moringa forage meal in the diets of Camperos broiler chickens or chickens of low potential of growth, that
weigh between 1500 and 1600 g to the 42 days old, show economic feasibility and good growth performance from the birth until the
sacrifice (Valdivié et al., 2017). However, in broiler chickens with high growth potential, it is not recommended to use this alternative
meal during the first 7 days old, due to the development insufficient of the GIT of these poultry. New findings showed that it is safe to
include 5% in diets from 8 to 35 days old and up to 10% in diets for chickens over 36 days old, because the birds had a normal
development during the feeding phases and there was no higher mortality (Almeida et al., 2016; Valdivié et al., 2017; Macambira
et al., 2018).
The White Leghorn chicks from 0 to 8 and 9 to 18-week-old stage accept diets up to 10 and 20% of moringa forage meal, without

6
M. Valdivié-Navarro, et al. Animal Feed Science and Technology 260 (2020) 114338

effecting batch uniformity and viability, respectively, being inclusion levels safe and economically attractive (Valdivié et al., 2017).
Likewise, young laying hens from 20 to 25-week-old stage admit an inclusion of up to 20% of moringa forage meal with a significant
reduction in the feed cost and an increase the yolk color (Valdivié et al., 2017). Also, in laying hen diets that reach or surpass the
laying peak (26 or more weeks old) the use from 5 to 10% of moringa forage meal (leaves plus stems) has no modifies the growth
performance and reduce the cost to produce one egg (Valdivié et al., 2016a).
New studies have found the possibility of including the moringa forage meal up to 40% in diets for pregnant sows from 6 to 16
weeks, since it does not affect the sow weight and the development of the fetus. In addition, levels of use of 15% in diets for breeding
sows during lactation have been observed, without damaging the production of milk and the growth of piglets. Likewise, 15% and
20% of moringa are considered safe in diets for lactating piglets from the start of feed intake until weaning at 28 days old and for
weaned piglets, from 28 to 75 days old, respectively. In growing pigs this feed has a good acceptability and does not depress the
weight gain and the feed intake (García and Macias, 2014; Ly et al., 2016; Mireles et al., 2017; Caro et al., 2018). In broiler rabbits,
according to Valdivié and Ponce de León (2015) and Caro et al. (2018) dietary inclusion from 25 to 30% of moringa forage meal
(leaves plus stems), in industrial or artisan feed for are very safe, since the use of this feed did not depress the body weight, viability,
feed intake and feed conversion. Maybe this product can completely replace the alfalfa forage meal in the classic rabbit diets.

7. Conclusions

The forage meal from Moringa oleifera (leaves plus stems) from 35 to 60 days of regrowth and cut at a height of 5 to 40 cm from
the soil has a good protein contents and their amino acid concentration is similar to that of the alfalfa forage meal, also has high
content of fibrous compounds, hence its contribution of DE or ME for poultry and pigs must be low.
The concentration of secondary metabolites and bioactive substances of the M. oleifera forage meal (leaves plus stems) does not
cause damage when used at appropriate levels, in diets for non-ruminant animals and may evident nutraceutical properties, when
their use levels are adjusted. The safe inclusion levels of M. oleifera forage meal were identified in the present review for the diets of
ducks, chickens, broiler chickens, replacement laying pullets, laying hens, pigs, and rabbit.

Declaration of Competing Interest

None.

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