Recent advances in the incorporation of leaf meals in broiler diets

S Sugiharto, T Yudiarti, I Isroli, E Widiastuti, H I Wahyuni and T A Sartono

Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University, Semarang, Central Java, Indonesia
sgh_undip@yahoo.co.id

Abstract

The increase in feed price has been a serious problem in broiler industry as it may increase broiler production cost. Attempt has been carried out to reduce the feed cost by for example partly replacing the conventional-expensive protein-rich feed ingredients with the alternative protein-rich feedstuffs. Among the alternatives, leaf meals containing high content of protein have been incorporated in broiler diets. Besides being rich in protein, leaf meals also contain a wide variety of biological active components that may serve as growth-promoting and health-improving agents for broiler chickens. Yet, the high contents of fibre and anti-nutritional factors may limit the inclusion levels of leaf meals in broiler diets. To obtain the benefits of bioactive compounds in leaf meals with no detrimental effects on the production traits of broilers, dietary supplementation of enzymes and fermentation have been conducted. This review provided a comprehensive view regarding the recent advances in the application of leaf meals in broiler diets.

Keywords: duckweed, green leaf, growth, health

Introduction

Feed has been a major cost in modern broiler production, accounting about 70% of the total production cost (Sugiharto 2019). The increase in feed price may therefore imply in the increase in total production cost and thus decrease the profit margin of broiler industry. Attempt has recently been taken to reduce the cost of feed, including the incorporation of agro-industrial by-products in broiler diets as an energy source (Sugiharto et al 2018a; Sugiharto 2019; Sugiharto and Rajitkar 2019). However, some limitations may exist when using the agro-industrial by-products as the ingredients in broiler rations. The high and low contents of fibre and protein in the by-products may limit the digestibility and thus inclusion level of such by-products (Sugiharto et al 2018a). In addition to the agro-industrial by-products, the application of leaf meal as the ingredient in broiler feeds has also been conducted (Abdulsalam et al 2015; Aroche et al 2018; Mustafa 2019). Compared to agro-industrial by-products, the content of crude protein in leaf meal is much higher (Tesfaye et al 2013; Sugiharto et al 2018a). This may be beneficial in reducing the proportion of the conventional-expensive protein-rich feed ingredients in broiler rations.

It has been known that some particular foliages contain a number of bioactive compounds that are beneficial for the health of chickens (Rama Rao et al 2019). These compounds include vitamins, phenolic acids, flavonoids, isothiocyanates, tannins as well as saponins (Vergara-Jimenez et al 2017). In this regard, the use of leaf meal in rations may not only reduce the cost of feeds, but also elicit the health-promoting effect on broiler chickens. Apart from their benefits, the use of leaf meals in broiler diets may be limited by their high content of crude fibre (Santoso and Sartini 2001; Ubua et al 2019). In general, broiler chickens showed low tolerance to dietary fibre, and therefore feeding diets containing high levels of leaf meal may impose in compromised nutrient digestibility and thus alleviated growth performance of broilers (Buragohain 2016). To deal with the latter problem, dietary supplementation of enzymes (fibre-degrading enzymes) (Fasuyi and Akindahunsi 2009; Oloruntola et al 2016) and fermentation has been conducted to particularly degrade the fibre and hence increase the incorporation levels of leaf meal (Mandey et al 2015; Santoso et al 2015). The present review provided a comprehensive view concerning the recent advances in the application of leaf meal in broiler rations.

Nutritional properties and potential of leaf meals as feed ingredients for broiler chickens

In generally speaking, leaf meals may be defined as the dried and ground products of plant leaf. The products may be used for human consumption as well as livestock feeds. In broilers, the potential of leaf meal as feed ingredients has long been studied (Wyllie and Chamanga 1979). Today, due to the increase in feed price particularly for the protein-rich feed ingredients, the incorporation of leaf meal in broiler diets is encouraged (Oloruntola et al 2019; Sebola et al 2019; Ubua et al 2019). This could be understood as the majority of leaf meals contain considerable levels of crude protein (Table 1). Previously, Onyimonyi and Ernest (2009) used papaya leaf meal to partially reduce the proportion of groundnut cake, which is rich in protein, in broiler rations. Likewise, Tesfaye et al (2013) used Moringa olifera leaf meal as an alternative protein source to reduce the use of soybean meal in broiler rations. In addition to protein, most of leaf meals contain high amounts of ash (Table 1), and therefore could be a good source of minerals for poultry. It should, however, be noted that the minerals contents of leaf meal may vary across the plant leaf. Tsega and Tamir (2009) provided an example that sweet potato leaf meal contains high concentration of Ca, but has low concentration of P. In the latter case, dietary supplementation of P should be conducted to achieve the ideal ratio of Ca to P in broiler rations. Apart from the potential of leaf meal as an alternative protein source, study showed that application of leaf meal in broiler diets is often limited by the high content of crude fibre in the foliage (Table 1). Tesfaye et al (2013) suggested that the increased fibre content in rations with the increased levels of leaf meal may consequently depress feed intake and thus growth performance of broilers. The fibre may increase the bulkiness in the gastrointestinal tract and thereby reduce feed consumption (Buragohain 2016).

In addition to the species of plants, the nutritional qualities of leaf meal may also be determined by the maturity stage of leaf. Sebola et al (2019) noticed that compared to mature leaf, young leaf of Moringa oleifera had considerable higher organic matter and crude protein, and lower crude fibre, crude fat and ash contents. Hence, the stage of maturity of the foliage should be considered when formulating broiler rations using leaf meal as it may influence the nutritional contents of diets. Indeed, the different nutritional contents may also exist within the species of plant. For example, Kagya-Agyemang et al (2007) showed that Gliricidia sepium leaf meal contained 18.2% crude protein and 12.9% crude fibre, while Oloruntola (2018) found that such leaf meal contained 24.4% crude protein and 12.5% crude fibre. The variation of crude protein content in Gliricidia sepium leaf meal may be due to the differences in the nature of plants, age, water, temperature/climate and soil conditions where the plants are grown.

Functional properties of leaf meal

The role of functional feeds or feed ingredients is becoming noticeable during the post-antibiotic era. With their active components, the functional feeds may exert beneficial impacts on the health and production traits of broiler chickens (Sugiharto et al 2018a). Among the sources of functional properties, green leaf have been known to naturally contain numerous active compounds that are beneficial for the health and wellbeing of both humans and animals. These bioactive components include phenols, flavonoids, alkaloids, saponins, tannins, terpenoids, steroids, etc. Mashayekhi et al (2018) revealed that phenolic compounds in the eucalyptus leaf can act as antioxidants, antimicrobial agent, appetite enhancer, growth promoter and immunostimulator. Also, polyphenols in summer-autumn tea leaf improved the oxidative status and immune competences of broiler chickens in the study of Wang et al (2018). Study by Ouyang et al (2016) showed the efficacy of alfalfa flavonoids in improving the antioxidative status and fatness in broiler chickens. Likewise, Kamboh et al (2016) demonstrated that plant flavonoids (genistein and hesperidin) improved the immune competences and antioxidant status of broiler chicks. With regard to saponin, Manjaniq et al (2017) exhibited that saponin in Moringa leaf meal was responsible for protecting the erythrocytes from destruction (caused by the free radicals or reactive oxygen species) as well as stimulating the erythrocytes production in broiler chickens. In line with this, Zhang et al (2017) showed that saponins derived from mango leaf improved growth performance, meat characteristics and plasma lipid profile of broilers. In term of alkaloids, study by Santoso (2018) showed that feeding Sauropus androgynus leaf meal rich in alkaloid was beneficial in improving the growth performance of broilers. In agreement, Alagbe (2017) reported that Polyalthia longifolia leaf meal containing 0.51% alkaloids may be employed as an antibiotic substitute for improving the growth performance of broilers. Another active compound that is largely found in green leaf is condensed tannins, which is valuable in protecting the chicks from infectious diseases and improving their growth performance (Alagbe 2017; Hidanah et al 2018; Sebola et al 2019). In general, there are a great variation in the types and levels of active components within and among the species of plant leaf (Alagbe 2017; Sebola et al 2019). Both genetic and environmental factors may determine the types and levels of the bioactive compounds in the plant leaf (Makita et al 2016). Also, the age or degree of maturation affects the concentration of bioactive compounds in the leaf (Sebola et al 2019). To optimize the role of leaf meals in improving the health and production traits of broilers, it is therefore crucial to select the leaf according to its species, origin and degree of maturation before being included in broiler rations.

Extraction and isolation of specific component have widely been practiced from the green leaf. This is necessary as green leaf contain wide spectrum or mixed of active compounds (Alagbe 2017; Sebola et al 2019). The extraction and isolation are generally expected to obtain particular compound with certain functional effect on chickens. Oke et al (2017) extracted phenolic compound (oleuropein) from olive leaf and supplemented in the drinking water of broilers. They found that such treatment improved broiler growth performance under thermal stress. In line with this, Zhang et al (2017) found that saponins extracted from the mango leaf was attributed to the improved growth performance, meat characteristics and plasma lipid profiles of broiler chickens. In practice, supplementation of the active compounds should be conducted regularly in broiler chickens. This because the active components are rapidly metabolized and not accumulated in the body of broilers. Moreover, the chicks cannot synthesise these active components, and therefore dietary supplementation of these components is necessary.

Anti-nutritional factors in leaf meals

The presence of anti-nutritional factors such as tannin, alkaloids, saponins, flavonoids, cyanide, oxalate, phytate, etc. has been a great concern when incorporating leaf meals into broiler diets as they may negatively affect the nutrient digestibility and utilization of broiler chicks (Kagya-Agyemang et al 2007; Buragohain 2016). Buragohain (2016) revealed that the presence of tannin in Tithonia diversifolia leaf meal was attributed to the decreased feed intake and nutrient digestibility in broilers. Tannin may bind protein and digestive enzymes to be a complex form that are not readily digestible (Buragohain 2016). This consequently reduces the protein digestibility and utilization. The presence of tannin in leaf meals may also damage the mucosa of enterocytes and interrupt the metabolic processes leading to compromised growth performance of broilers. However, the effect of tannin seems to be ambiguous as many studies exhibited the improving effect of tannin on the health and growth performance of broilers (Alagbe 2017; Hidanah et al 2018; Sebola et al 2019). The similar condition is observed for saponins in leaf meals, in which feeding leaf meal rich in saponins could improve the health and growth of broilers (Zhang et al 2017). Conversely, the presence of saponins in leaf meals may act as anti-nutritional factors for broiler chickens (Peiretti 2018). According to Chamorro et al (2019), administration of moderate amounts of phenolic compounds and other secondary plant metabolites (such as tannin and saponins) may positively affect the health and production performance of broilers, whereas the high levels of such compounds negatively affect the nutrient utilization of broilers. In this regard, study to optimize the level of leaf meals in broiler rations is necessary to obtain the functional properties of leaf meals without compromising the growth of broilers.

Some methods may be conducted to reduce the anti-nutritional factors in leaf meal. Among the methods, sundrying has been reported to reduce the anti-nutritional factors content in leaf meal (Fasuyi et al 2008). Other methods such as cooking, autoclaving, dehulling, soaking, toasting and using the anti-nutritional binding agents may also be carried out to reduce the contents of anti-nutritional factors in leaf meals (Medugu et al 2012). Moreover, fermentation may also be conducted to reduce the anti-nutritional factors in leaf meals (Santoso et al 2015; Sugiharto and Ranjitkar 2019).

Leaf meals as feedstuffs for broiler chickens

A number of works has incorporated leaf s in broiler diets (Table 2). The incorporation of leaf meal is primarily subjected to reduce the use of protein-rich feed ingredients in broiler rations and, hence, reduce the cost of feeds. The other is to take the advantages from the bioactive components in leaf meal to improve the growth performance of broiler chicks. Rahman and Yang (2018) noted that supplementation of pineapple (Ananas comosus) leaf powder up to 3% in diets was able to improve the growth performance of broiler chicks. It seemed that leaf meals increased the production and activities of digestive enzymes as well as improved the intestinal morphology (villi development) of broilers resulting in improved nutrient digestibility and utilization (Mariana et al 2018; Mustafa 2019). The improvement of intestinal microbial ecosystem, immune responses and physiological conditions of chicks may also be attributed to the increased growth rate in broilers fed with leaf meals (Fasuyi et al 2008; Liaqat et al 2016; Rahman and Yang 2018; Mustafa 2019).

In general, the response of broilers in term of production performance to dietary leaf meal seems variable, depending on the types of leaf meal and levels of incorporations. Moringa oleifera may be included at the levels up to 20% to improve the growth rate of broilers (Alnidawi et al 2016), while Alchornea cordifolia leaf meal can only be included at 10% in rations without any deleterious effect on broiler performance (Oloruntola et al 2015). Different form the above mentioned leaf, Tithonia diversifolia leaf meal (Buragohain 2016) and Summer-autumn tea leaf powder (Wang et al 2018) may only be included in broiler rations at maximum of 4% and 2%, respectively, as higher levels of inclusion resulted in depressed nutrient utilization and thus compromised growth performance of broilers. In addition to the fibre content, the presence of anti-nutritional factors, nutritional composition of the whole diets, age of chicks, environmental factors, etc. may limit the use of leaf meal in broiler rations. To increase the dietary inclusion levels of leaf meal, the use of exogenous enzyme in concomitant with leaf meal may be conducted. Oloruntola et al (2016) reported that the use of exogenous enzymes improved the nutrient utilization of Alchornea cordifolia leaf meal by broiler chickens. The latter authors further suggested that the exogenous enzymes may work synergistically with the digestive enzymes of chicks to degrade the polysaccharides, protein and anti-nutritional factors resulting in increased nutritional values of leaf meal. The presence of the exogenous enzymes may also compensate the activity of endogenous enzymes that are inhibited by the presence of anti-nutritional factors such as tannin in leaf meal. In accordance with this, Fasuyi and Akindahunsi (2009) demonstrated that the use of enzyme such as Roxazyme G2 (containing cellulase, glucanase and xylanase) may increase the nutritional benefits of Amaranthus cruentus leaf meal as well as increase the incorporation levels of the leaf meal up to 25% in broiler rations. The use of enzymes may thereby increase the economical values of leaf meal in broiler production. From the economical point of view, the application of exogenous enzymes in conjunction with dietary leaf meal should, however, be practiced with caution as enzyme supplementation may increase the cost of broiler production. Indeed, Martens et al (2012) suggested that enzymes are not suitable for the smallholder broiler producers because of the cost and limited availability of enzymes in the market especially in the rural area.

It is generally believed that feeding of leaf meal may reduce the cost of feed in broiler production. Yet, the economic benefits seems to depend on the local circumstances. This is because some plants may grow well in certain place but not in other particular place. The season/climate and soil condition may determine the production and nutritional qualities of leaf meal, while the competition with the human needs may affect the supply of leaf meal for broiler production.

Due to the latter competition, the use of, for example, water spinach ( Ipomoea aquatica) and taro (Colocasia esculenta) leaves in broiler rations is limited. Note that in some countries such as Indonesia, water spinach and taro leaves have traditionally been used as foodstuffs (vegetables). Other factor that may limit the use of particular leaf meals as broiler feed ingredients is the high cost of production of leaf meal. In this regard, Sońta et al (2019) noticed that high cost is needed for harvesting and processing of fresh duckweed into duckweed meal.

Leaf meal as functional feedstuffs for broiler chickens

In the post-antibiotic era, effort has been intensified to search the alternative stuffs for in-feed antibiotics. The use of leaf meal has been reported to improve the health status and physiological conditions of broilers in farms (Table 3). Hence, there is potential to use leaf meal as the alternative to in-feed antibiotics for broiler chickens. Several active ingredients in leaf meal are most likely to involve, either alone or in conjunction, in improving the immune competences of broilers. Among the active compounds, phenols have been reported to promote the immune organ development as well as stimulate the immune system of chicks (Kamboh et al 2015). Phenols may also serve as antimicrobial agents and antioxidants that eventually protect the immune system of broilers from the dangerous effect of reactive oxygen species (free radicals) (Mahmoud et al 2013; Kamboh et al 2015). With regard to tannins, although at high level it may act as anti-nutritional factors, in moderate level this compound has been reported to improve the immune competence, intestinal microbial ecology and gut health for broiler chicks (Huang et al 2018). Other active compound in plant leaf, such as flavonoids, may also contribute in improving the health of broilers. Kamboh et al (2016) showed that dietary supplementation of plant flavonoids increased the immune organ indices as well as improved the humoral immunity by elevating the numbers of intestinal intraepithelial lymphocyte and antibody titre against New castle diseases and avian influenza virus. The treatment with flavonoids also reduced lipid peroxidation in the liver and improved the antioxidative status of broilers (Kamboh et al 2016; Rama Rao et al 2019). Note that the increased antioxidant capacity is essential for broilers, as the low antioxidant capacity may be associated with cellular damage, immune system deterioration and metabolic disturbances. Eventually, it is difficult to infer that the health-improving effects of leaf meal depend only on one active compound, but rather on combined effect of several compounds as contain mixed of active compounds.

Recently, treatment with leaf meal may be exploited to alleviate the harmful effect of toxin contamination on the growth performance of broilers. For examples, Prakoso et al (2018) incorporated 5% of Sauropus androgynus leaf meal in broiler diets and found that the treatment increased the final body weight of broilers contaminated with aflatoxin. It was most likely that phenolic compounds in could act as antitoxin or deactivate the toxin (inhibit the toxin activity) and thereby alleviating the negative effect of aflatoxin in broiler chickens (Prakoso et al 2018). In addition to the antitoxin activity, green leaf may also be used as therapeutic agents for bacterial infections in broiler chickens. For example, Suryani et al (2014) and Sharma et al (2016) used Morinda citrifolia leaf extract and neem leaf extract, respectively, to reduce the prevalence of colibacillosis in broiler chickens. The antibacterial properties and immunomodulatory effects of the bioactive compounds in the green leaf seems to be attributable to the therapeutic effects of the leaf (Sharma et al 2016). Different from the above reports, Balami et al (2018) showed that feeding of Moringa oleifera leaf meal neither protected the liver from pathological damage nor prevented the lipid peroxidation in broilers following the challenge with variant strains of infectious bursal disease virus (vIBDV). It was not clear what the particular compound in the leaf meal that was expected to protect the liver from the infection in the latter study, but the relatively low level of the active compounds in the leaf meal as compared to that in extract may be the reason for such above divergent results. Taken together, to improve the therapeutic effects of the leaf, it is better to extract the leaf before being included in the diets or drinking water of broilers (Suryani et al 2014; Sharma et al 2016).

Recently, there has been a trend to use leaf meal in combination with other active ingredients to further improve the functional effects of green leaf on broiler chickens. In our previous study, we combined Moringa oleifera leaf powder and garlic powder, and found that such combination better reduced the number of Enterobacteriaceae in the ileum as well as decreased the fat deposition in the abdomen of broilers, when compared with the use of Moringa leaf powder or garlic powder alone (Sugiharto et al 2018b). Likewise, the combination of guava leaf meal and olive oil improved performance and health of broiler chickens as compared to control (Mahmoud et al 2013). The combination of neem leaf meal and ginger extract was also reported to improve the immune status and growth performance of broilers (Rahman et al 2015). Moreover, Abujradah et al (2018) demonstrated that the combination of neem leaf meal, garlic and probiotics boosted immune responses of broiler chickens. It was most likely that the combination may result in positive synergistic effect on the immune system of broilers.

In addition to the improved health and wellbeing of chicks, feeding leaf meal was also noticed to improve the product qualities of broiler. Mustafa (2019) reported that dietary incorporation of 1% Eucalyptus camaldulensis leaf meal improved the sensory evaluation such as flavour and juiciness of thigh and breast meats of broilers. The feeding treatment also produced less hardness and thiobarbituric acid reactive substances (TBARS) in the thigh and breast meats of broiler compared to control. In line with this, Onyimonyi and Ernest (2009) showed that dietary inclusion of 2% papaya leaf meal in finisher diets improved carcass and organoleptic traits of broiler meats. Dietary inclusion of papaya leaf meal has also been shown to reduce lipid peroxidation and increased antioxidant activity of broiler breast meats (Ebrahimi et al 2015). Moreover, feeding of Sauropus androgynous leaf meal reduced fat deposition in abdomen, liver and carcass (Santoso and Sartini 2001). The phenolic compounds in plant leaf seems to be responsible for the reduced oxidative susceptibility and hence improved the sensory and nutritional characteristics of broiler meats (Starčević et al 2015). In term of fat deposition, the phenolic compounds in leaf meal may serve as a lipid-lowering agent (by inhibiting the synthesis of lipid) and thereby reduce fat deposition in the body of broilers (Santoso and Sartini 2001; Starčević et al 2015). However, it should be noted that different types of leaf meal may exert different impacts on broiler meat traits due to a vast variety on types and levels of phenolic compounds across the plant leaf.

Fermented leaf meal for broiler chickens

Fermentation has widely been conducted to deal with the problems related to the high fibre and anti-nutrition contents in feedstuffs (Sugiharto and Rajitkar 2019). The method has also been carried out in plant leaf not only to increase the inclusion levels of leaf in broiler diets (Syahruddin et al 2011; Has et al 2013; Mandey et al 2015), but also to increase and/or produce the biological active compounds with health-improving effects for broilers (Cao et al 2012). Table 4 shows some examples of the fermented plant leaf used in broiler diets. Indeed, feeding fermented plant leaf improved feed digestibility (Has et al 2013), intestinal ecology and function and antioxidant capacity of broilers (Zhang et al 2015). The decreased fibre and anti-nutritional factors and the increased protein contents in plant leaf due to fermentation was attributed to the improved feed utilization and thus increased the levels of plant leaf inclusion in broiler diets. In addition to the role of bioactive compounds in plant leaf, the live microbes and their metabolites produced during fermentation may also play a substantial role in improving the intestinal functions and thus nutrient utilisation by the birds (Sugiharto and Rajitkar 2019).

In general, although fermentation has been associated with the increased protein and amino acid contents, such technique has often been attributed to the decreased total phenols and thus antioxidant activity of the substrates (Sugiharto et al 2018c). Fermentation has also been reported to decrease the content of flavonoids in the substrates (Cao et al 2012). Several factors may be responsible for the reduced antioxidative components in the substrates during fermentation, including the nature of substrates, species and strains of microbes used as starter inoculum and other environmental factors. Taken together, to obtain the benefits of fermentation in terms of nutritional improvement without having deleterious effect on the antioxidative properties, the selection of particular plant leaf and types of microbes as starter inoculum is crucial.

Conclusions

• Several studies have shown the benefits of dietary incorporation of leaf meal on the production performance and health status of broilers.
  
  
• Such benefits may be attributed to the high contents of protein and bioactive compounds in the leaf meal.
  
  
• The responses of broilers to dietary leaf meal in term particularly of growth performance are variable, depending on the types of plant leaf meal and levels of inclusion.
  
  
• The contents of fibre and anti-nutritional factors may suppress the nutrient utilisation of leaf meal and thus growth performance of broilers.
  
  
• Dietary supplementation of fibre-degrading enzymes and fermentation may be conducted to increase the digestibility and utilization of leaf meal by broiler chicks.

Acknowledgments

The study was supported by Diponegoro University, Semarang Central Java, Indonesia through non-tax state revenue.

Conflict of interests

We have no conflict of interest.

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Received 12 June 2019; Accepted 26 June 2019; Published 2 July 2019

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