The Potential of Tropical Agro-Industrial by-Products as a Functional Feed for Poultry

Document Type: Review Articles

Authors

Department of Animal Science, Faculty of Animal and Agricultural Science, Diponegoro University, Semarang Central Java, Indonesia

Abstract

Following the ban of synthetic antibiotics as antimicrobial agents and growth promoters, poultry nutritionists are now trying to find antibiotic substitutes. Agro-industrial by-products are abundant in tropical countries and have been used as the alternatives to conventional feedstuffs in poultry rations. These by-products are also known to contain several bioactive compounds such as oligosaccharides, phenolic compounds, certain fatty acids, vitamins, etc. The compounds may serve as antimicrobial agents, antioxidants and immune-modulators for poultry. Owing to this, agro-industrial by-products have a potential to become functional feeds that can promote the health and well-being of poultry. The potentials of some tropical agro-industrial by-products (e.g., palm kernel meal, rice bran, cassava meal, copra meal, banana peel meal, orange peels and pulp) and their derivative products as functional feeds for poultry are elaborated in the present review, and the possible mechanisms through which agro-industrial by-products may improve the health status of poultry will also be discussed. Future studies are needed to confirm the efficacy of agro-industrial residues and their derivative products in substituting the use of synthetic antibiotics in poultry rations.

Keywords


INTRODUCTION

Tropical countries are rich in plant resources that may be processed for food or other products. This processing activities (agro-industries) produce a large quantities of by-products that can ultimately lead to environmental problems. In response to the increased price of conventional feedstuffs (e.g., maize and soybean), there has been a rising interest to reutilize by-products from the agro-industries as feed ingredients in poultry rations. This may not only deal with environmental issues, but also reduce the cost of feed in poultry production (Kasapidou et al. 2015). Recently, there has been a global concern about antibiotic resistance both in poultry and human as consumers, leading to the ban of sub-therapeutic use of synthetic antibiotics as antimicrobial agents and growth promoters in poultry production (Sugiharto, 2016). It has been known that agro-industrial by-products are rich in bioactive components (e.g., oligosaccharides, phenolic compounds, certain fatty acids, vitamins, etc.) with beneficial effects on the health and well-being of poultry. These compounds may act as antimicrobials, antioxidants and immune-modulators (Esa et al. 2013; Abbasi et al. 2015; Ebrahimi et al. 2015; Kang and Kim, 2016), which are antibiotic properties. For the sustainable global poultry production, therefore, agro-industrial by-products need to be used not only as the alternatives to conventional feedstuffs, but also as safe antibiotic substitutes for poultry. Several tropical agro-industrial residues have been researched as functional feed ingredients for poultry, including palm kernel meal, rice bran, cassava meal, copra meal, banana peel meal, orange peels and pulp, etc. The detailed properties and nutraceutical effects of each by-product on poultry are elaborated in the present review. To suggest the potential of selected tropical agro-industrial by-products as functional feeds, some parameters on poultry have been taken into consideration when preparing this review, including immune competences, intestinal health (e.g., intestinal morphology and bacterial populations), physiological responses and production parameters. To prepare the review, literature search with focus on the functional properties of tropical agro-industrial by-products has been conducted. During the search, peer-reviewed journal articles in English were included, while conference proceedings and Ph D. dissertation were selectively included. Studies on humans, pigs and rodents were selectively cited to support the existing data on poultry. A number of scientific portals have been used for literature search, including Elsevier Science-Direct, EBSCO E-journal, Proquest Research Library, Cambridge University Press E-Journal, Springerlink E-Journal and Google Scholar. 

 

Definition of functional feed

Functional feed ingredients have recently attracted much attention as additives, following the withdrawal of sub therapeutic antibiotics from poultry feeds. Currently, there is no exact definition for the functional feed in poultry nutrition. On the basis of human nutrition, however, functional feed can be regarded as the whole feed, fortified, enriched or enhanced feed that have potentially health effects in addition to the basic nutrition (Hasler, 2002; Martirosyan and Singh, 2015). Hence, functional feed has to be able to promote the health and growth of poultry. Compared to conventional feed, functional feed have a similar appearance, but functional feed provides components with health- and growth-promoting effects (Cencic and Chingwaru, 2010). In addition to carbohydrates, proteins, fats, vitamins and minerals, functional feed may contain some biologically-active components including flavonoids, capsaicinoids, lignin, terpenoids, carotenoids, chlorophylls, stilbene, phenolic acids, fibres, sterols, polysaccharides, etc. needed for healthy growth of animals (Martirosyan and Singh, 2015). These bioactive components may occur in either the natural or the processed feeds (Syngai et al. 2016). Palm kernel meal is one of the example of natural feeds that is rich in β-mannan, capable of improving the growth performance and health of chickens (Zulkifli et al. 2003; Sundu et al. 2006). With regard to the processed feed, rice bran oil (extracted from rice bran, rich in essential fatty acids and unsaturated fatty acid) has been used as a functional feed ingredient to improve growth performance, total cholesterol in serum and the immune defense system of broiler chicks (Kang and Kim, 2016). The term of functional feed is often confusing with nutraceuticals, as both terms are usually used to describe health-promoting feed or its extracted components. Although the exact meaning of these terms has not been found, El Sohaimy (2012) inferred that nutraceuticalsis healthful products that are isolated or purified from feeds, and formulated and taken in dosage form (capsules, tinctures or tablets). On the other hand, functional feeds are products that are provided and consumed as conventional feeds, not in dosage form.  

 

Tropical agro-industrial waste as poultry feed ingredients

Agro-industrial waste refers to the by-product derived from the processing of agricultural products (Sindhu et al. 2002). Molasses, milk whey, wheat bran, cottonseed meal, cottonseed cake, groundnut cake, palm kernel meal, palm kernel cake, copra meal, banana peel meal, soybean hull, brewers grains (dried and bran), rice bran, rice husk, rice chaff, cassava pulp, cassava peeling, orange peels and pulp, maize bran, etc. are among the examples of agro-industrial by-products in general. Of the aforementioned agro-industrial by-products, molasses, palm kernel meal, copra meal, banana peel meal, rice bran, cassava pulp, orange peels and pulp are probably the most prominent examples of agro-industrial by-products in the tropical countries including Indonesia. Due to its abundant availability and low cost, nutritionists have now been encouraged to incorporate agro-industrial by-products in poultry nutrition, especially as an alternative to conventional feedstuffs (Abbasi et al. 2015; Kasapidou et al. 2015). Palm kernel meal (Zulkifli et al. 2003; Sundu et al. 2006), cassava pulp (Khempaka et al. 2009; Sugiharto et al. 2016) and fruit processing co-products such as orange peels and pulp (Abbasi et al. 2015; Kasapidou et al. 2015) are among the examples of agro-industrial waste being used as feed ingredients in poultry diets. However, there is a limitation in the use of agro-industrial waste as feed ingredients in poultry diets. For example, Khempaka et al. (2009) reported that cassava pulp may only be used as an energy source in poultry diet at maximum 8%. The inclusion level above 8% negatively impact the growth performance of broiler chicks. A high concentration of rice bran (above 20%) was also associated with a retarded growth rate in broiler chicks (Gallinger et al. 2004). In general, the high and low fibre and protein contents, respectively, as well as the presence of anti-nutritional factors and toxins, may limit the use of agro-industrial by-products as poultry diets (Sindhu et al. 2002; Gallinger et al. 2004; Khempaka et al. 2009). Of the methods available to improve the nutritional qualities, fermentation is a simple technique that can be exploited especially to lower fibre and increase protein contents of the agro-industrial waste, so that can be included in poultry diets at higher levels (Khempaka et al. 2014; Sugiharto et al. 2015; Sugiharto et al. 2016). For instance, fermentation can be a tool to produce functional feed ingredients for poultry. Recent studies revealed that fermentation of cassava pulp with the fungus Acremonium charticola decreased fibre (Sugiharto et al. 2015; Sugiharto et al. 2016) while the addition of urea as a nitrogen source increased protein content (Sugiharto et al. 2016) of cassava pulp. Consequently, the cassava pulp could be incorporated in broiler diets up to 24% without adversely affecting the nutritional and metabolic status of birds (Sugiharto et al. 2016). Apart from the nutritional improving effects, fermentation may produce health-beneficial properties for poultry. Indeed fermentation increased the content of lactic acid bacteria (LAB) (Sugiharto et al. 2015) and the antioxidant and antimicrobial properties in the pulp (Wen et al. 2013).

 

Tropical agro-industrial by-product as functional feed ingredients for poultry

In response to the global concern about antibiotic resistance both in human and farm animals, the use of functional feeds as the substitute for synthetic antibiotics in poultry diets has been encouraged. Apart from its use as the substitute for conventional feed ingredients, agro-industrial by-products have been reported to benefit the health of poultry, and therefore can serve as functional feed ingredients. For instance, Zulkifli et al. (2003) and Sundu et al. (2006) reported that palm kernel meal was able to improve the immune system, intestinal microbial ecosystem and thus chicken health. The beneficial impacts of either the cassava pulp on intestinal health (Khempaka et al. 2009) or the dried sweet orange (Citrus sinensis) pulp on humoral immunity and caecum microbial population (Abbasi et al. 2015) have also been reported. The detailed discussion about the use of each agro-industrial waste as functional feed ingredients will be elaborated in the following section.

 

Palm kernel meal

Palm kernel meal, also called palm kernel cake or palm kernel expeller, is an agro-industrial waste derived from the palm oil industry. This agro-industrial by-product has been used as feed ingredients to reduce the proportion of maize in poultry rations (Sundu et al. 2006; Alshelmani et al. 2016). Note that palm kernel meal contains 16.58% crude protein and 20.4 MJ/kg gross energy (Zulkifli et al. 2003). Due to its high content of β-mannan (a good source of prebiotics), feeding palm kernel meal has also been expected to improve the health of chickens (Sundu et al. 2006). Zulkifli et al. (2003) reported that feeding palm kernel meal reduced mortality rate and maintained the antibody titre for Newcastle disease (ND) in broiler chicks during a week period of heat stress. Concomitant with this, Soltan (2009) showed that feeding palm kernel cake increased antibody titre to ND vaccine and relative weights of immune organs of broilers such as spleen, bursa of fabricius and thymus. Moreover, Ugwu et al. (2008) reported an improvement in haematological indices (e.g., red blood cells, haemoglobin, packed cell volume and eosinophils) in broiler chicks fed palm kernel cake. With regard to gut health, Sundu et al. (2006) revealed that feeding palm kernel meal was able to reduce the load of pathogenic bacteria (Salmonella and Escherichia coli) and increase the population of non-pathogenic bacteria (Bifidiobacterium sp.) in the intestine of broiler chickens. In laying hens, feeding palm kernel meal increased the population of Lactobacilli and decreased growth of coliform/E. coli (Yusrizal et al. 2013). In these regard, palm kernel meal may serve as functional feed ingredients for poultry. In contrast to the above studies, Shakila and Sudhakar (2012) reported that feeding palm kernel meal had no significant effect on the humoral immune system (antibody titre to ND) of laying hens, although the treatment improved hen-day egg production and feed efficiency. Moreover, Navidshad et al. (2015) revealed that feeding palm kernel meal had no substantial effect on the intestinal bacteria population (Lactobacilli, E. coli, Enterococcus genus and Enterobacteriaceae family) of chicks. These divergent results might be due to the different types of chickens, nature of palm kernel meal and conditions of experiment (e.g., diets, environment, stage of production, etc.). So far, there is no exact recommendation on the proportion of palm kernel meal in poultry rations. Considering that palm kernel meal contains no anti-nutritional factors, Sundu et al. (2006) suggested that palm kernel meal can be included up to 40% in the poultry rations provided that the diet is balanced in amino acids and metabolisable energy. In some tropical countries, such as Indonesia and Malaysia, palm oil industries produce a huge amount of palm kernel meal throughout the entire year. Considering their abundant availability, good nutritional values and health-promoting properties, palm kernel meal may therefore be encouraged (especially for the palm oil producing countries) to be included in poultry rations to reduce feed cost and substitute the role of synthetic antibiotics. As mentioned above, fermentation may not only improve the nutrient values (so that increase the inclusion level of palm kernel meal in poultry rations), but also increase the functionality of feed or feed ingredients. In the study of Alshelmani et al. (2016), it was apparent that feeding palm kernel cake fermented by Paenibacillus polymyxa ATCC 842 decreased the number of Enterobacteriaceae and increased LAB in the intestine of broiler chickens. In respect to immune system, Chinajariyawong and Muangkeow (2011) reported that feeding Aspergillus wentii TISTR 3075 fermented palm kernel meal increased the relative weight of spleen of broiler chickens. However, the latter report was in contrast to Khin (2004) who reported that feeding palm kernel cake fermented with Aspergillus niger had an adverse effect on the weight of bursa of fabricius in broiler chicks. The different microorganisms used as a starter, the level of incorporation of fermented palm kernel meal and the study conditions might be responsible for these differences. Apart from the provision as a whole meal, palm kernel meal may be extracted to produce mannose and mannan-oligosaccharides that can serve as prebiotics for broiler chickens (Chen et al. 2015). The prebiotics extracted from palm kernel meal have been reported to reduce the number of potential pathogenic bacteria (Enterococcus, Enterobacter and E. coli) and promote the growth of beneficial bacteria (Lactobacillus and Bifidobacterium) and thus the health of the bird (Chen et al. 2015). Accordingly, Rezaei et al. (2015) reported that feeding oligosaccharides extracted from palm kernel expeller tended to increase Bifidobacterium and decrease Salmonella colonization in the intestine of broilers. This study also showed a positive treatment effect on the immune and health status of broiler, as indicated by the increased plasma immunoglobulin (Ig) A level and decreased heterophil and basophil counts.

 

Rice bran

Rice bran, a by-product of rice milling industry, has commonly been used as an energy source in poultry rations (Mu et al. 2011). This by-product contains 12.10% crude protein and 3165 kcal/kg gross energy (Supriyati et al. 2015). Due to its content in prebiotics and other phytochemicals/nutraceutical compounds (e.g., α, β, γ, δ-tocopherol, tocotrienols/vitamin E and γ-oryzanol; Esa et al. 2013), rice bran has also been reported to improve host’ health status through modulating intestinal homeostasis and mucosal immune system (Komiyama et al. 2011; Henderson et al. 2012; Kumar et al. 2012). However, its high content in phytate, an enzyme inhibitor (trypsin inhibitor), and fibre may limit the use of this feedstuff in poultry diets (Gallinger et al. 2004). To overcome these constraints, nutritionists employed fermentation. Not only improving the nutritional qualities and thus increasing the inclusion level of rice bran in the poultry rations (Supriyati et al. 2015), fermentation may also improve the functionality of rice bran for poultry. Fermentation increased phenolic compounds and antioxidant activity of rice bran (Oliveira et al. 2008). Indeed, report regarding the use of fermented rice bran to improve the health status of poultry is scarce, but in human, rice bran fermented with Lentinus edodes increased interferon (IFN)-γ production, which may be beneficial to healthy individuals (Choi et al. 2014). Concomitantly, in animal models it has been shown an anti-stress effect of fermented rice bran on spleen, thyroid and thymus gland, beneficial for enhanced immunity (Koh et al. 2002). Extraction of rice bran has been carried out to isolate the active compounds such as vitamin E and oryzanol responsible for the health of host. Inclusion of rice bran extract in poultry rations is believed to be more effective in improving poultry health than feeding rice bran as a whole stuff. Indeed, Kang et al. (2015) reported that dietary supplementation with rice bran extract increased the concentration of IgG and consequently the immune responses in broiler chickens. In weanling piglets, the extracted rice bran was able to increase the populations of Lactobacillus and reduce Salmonella counts in faeces (Hossain et al. 2016). Different from the previous studies, Zheng et al. (2017) revealed that the dietary supplementation with fermented (using Lactobacillus plantarum, Bacillus subtilis and Saccharomyces cerevisiae) rice bran extract failed to affect on the concentrations of IgA, IgG, and tumor necrosis factor (TNF)-α in the ileal mucosa of broiler chickens, even though it was beneficial for the growth performance of birds. The rice bran oil is another product from the rice bran extraction, which is rich in γ-oryzanol. Kang and Kim (2016) reported that dietary supplementation of rice bran oil improved both the production performance and the health status and immune response of broilers, as indicated by the increase in heterophils, lymphocytes and monocytes as well as the concentration of IgG. In laying hens, feeding rice bran oil tended to decrease heterophil to lymphocyte ratio (H/L ratio) which may indicate a better stress response in birds (Kim et al. 2016). Although it has widely been used in most tropical countries, no exact rule can be inferred with regard to the optimum inclusion level of rice bran in poultry rations. However, the inclusion level of 10% to 15% may not produce adverse effect on the performance of poultry especially broiler chickens (Mu et al. 2011; Supriyati et al. 2015). With regard to rice bran oil and rice bran extract, the use of both functional ingredients could be up to 20 g/kg in the poultry rations (Kang et al. 2015; Kang and Kim, 2016). Recently, rice bran has increasingly been used as functional foods for human consumption. The latter condition may consequently increase the demand and, thus price of rice bran. This increase in price, must therefore be considered by nutritionists when formulating poultry rations with rice bran.

 

Copra meal

Copra meal is a residue of the oil extraction from the endosperm of coconut. This tropical agro-industrial by-product contains 4247-5872 kcal/kg gross energy and high level of protein (15-25%) and carbohydrate (60%), and therefore the potential to be used as poultry feed ingredients. However, the low level of amino acid, particularly lysine and methionine, and its high level of fibre (major proportion of carbohydrate in copra meal) may limit its utilization in poultry diets (Sundu et al. 2009). To date, there is no exact recommendation upon the use of copra meal in poultry rations, however, Sundu et al. (2009) suggested that copra meal may be used up to 30% provided a balanced diet (in particularly amino acids and energy) is formulated. Fermentation has been conducted to improve the nutritional qualities of copra meal. Hatta and Sundu (2009) fermented copra meal with either Aspergillus niger or Trichoderma spp. and supplemented to broiler chickens fed a copra meal diet. They found that fermentation of copra meal with Trichoderma spp. could improve the performance of bird in a diet containing 30% copra meal. To date, report regarding the effect of raw and fermented copra meal on the health of poultry if scarce. Attempt has been conducted to produce or isolate bioactive components (prebiotics) that may be beneficial for the health of poultry by degrading the crude fibre content of copra meal (Sundu et al. 2009). Manno-oligosaccharides (MOS) have been produced by using endo-β-1,4-mannanase (produced by Aspergillus niger BK01) on copra meal (Cương et al. 2010) or on pretreated and defatted copra meal (Ghosh et al. 2015). In an in vitro study, this isolated MOS had prebiotic potentials as it more supported the growth of L. acidophilus and B. infantis than with standard inulin (Ghosh et al. 2015). In an in vivo study, Sundu et al. (2012) showed that mannan derived from copra was able to counteract the negative impact of E. coli infection and aflatoxin B1 contamination in terms of growth performance and health status of broiler chickens. In accordance with those findings, Ibuki et al. (2013) reported that mannanase-hydrolysed copra meal improved intestinal histology (hence the intestinal absorptive function) and positively affect the immune system of broiler chicks. Further, β-1,4-mannobiose derived from the copra meal was able to prevent Salmonella enteritidis infection in broilers by improving Salmonella enteritidis clearance and increasing IgA production (Ibuki et al. 2010). However, those authors did not observe any impact of treatment on the immune organ development of broilers. In pigs, the mannanase-hydrolyzed copra meal exerted an anti-inflammatory activity (i.e., decreased the mRNA levels of ileal interleukin [IL]-1β, IL-6, IL-17 and TNF-α) in the intestine, showing a beneficial effect alleviating the intestinal inflammation (Ibuki et al. 2014). As prebiotics, MOS isolated from copra meal may be administrated to broilers in combination with probiotics to obtain a symbiotic effect. Duarte et al. (2014) showed that the application of mannanase-hydrolyzed copra meal together with Bacillus cereus var. toyoi could improve the performance and duodenum and jejunum mucous morphometry of broilers, when compared to control group.

 

Cassava pulp

Cassava pulp is a by-product of tapioca industry that is abundant in most of tropical countries. Due to its high energy content (2484 kcal/kg), this by-product has been used as feed ingredient to partially replace the role of maize in poultry rations (Khempaka et al. 2009). However, the high fibre (14.6%) and low protein contents (2.02%) may limit the use of cassava pulp in poultry diets. Fermentation has been used to improve the nutritional values of cassava pulp and thereby to increase its incorporation level in poultry rations. Khempaka et al. (2014) fermented cassava pulp using Aspergillus oryzae and subsequently included the fermented cassava pulp up to 16% in broiler diet without any adverse effects on the performance and well-being of broiler chickens. This proportion was apparently higher when compared with the level of inclusion of dried (raw) cassava pulp in broiler rations (8%) (Khempaka et al. 2009). Also Sugiharto et al. (2016); Sugiharto et al. (2017a) and Sugiharto et al. (2017b) included 16% of cassava pulp fermented with the fungus Acremonium charticola in broiler ration without any negative effects. The cassava pulp is a good source of oligosaccharide (mannose) that may act as prebiotics. Kurdi and Hansawasdi (2015) showed that the oligosaccharide isolated from cassava pulp was capable of promoting the growth of Lactobacillus and Bifidobacterium in vitro. An in vivo study showed that the fibre isolated from cassava pulp reduced the population of E. coli in the faeces of rats (Osundahunsi et al. 2012). However, the role of cassava pulp and its isolated active components as functional feed for poultry has not adequately been studied. Feeding dried cassava pulp improved the intestinal health (Khempaka et al. 2009) and also increased the relative weight of immune organs (thymus and bursa of fabricius) of broiler chicks (Sugiharto et al. 2016). Concomitant with this, feeding cassava pulp fermented with A. charticola or Rhizopus oryzae increased the relative weight of thymus and bursa of fabricius, and lowered both the heterophil to lymphocyte (H/L) and albumin to globulin (A/G) ratios (Sugiharto et al. 2016). In another study, it was also reported the increased of the relative weight of spleen, ileum and cecum as well as a reduced oxidative stress, as indicated by a lower 2,2-diphenylpicrylhydrazyl (DPPH) % inhibition, in broilers fed cassava pulp fermented with A. charticola (Sugiharto et al. 2017a). It was also showed that cassava pulp fermented with A. charticola decreased the number of total coliform bacteria in the ileum and increased the concentration of butyric acid in the caeca of broilers (Sugiharto et al. 2017b). Owing to the aforementioned data, it may be suggested that it is safe to include up to 8% of raw cassava pulp and 16% of fermented cassava pulp as alternative to conventional feedstuffs and functional feed ingredients in the poultry rations.

 

Banana peel

Banana peel or banana skin is the outer covering of banana fruit. Besides banana-processing industries, banana peel is produced by the fritter vendors and household consumption. A number of studies have reported the use of banana peels in poultry rations to partially replace maize as a source of energy (Duwa et al. 2014; Abel et al. 2015; Blandon et al. 2015). Banana peel contains 10% crude protein and 2932 kcal/kg metabolizable energy (ME) (Blandon et al. 2015). So far, no specific recommendation for the optimum proportion of banana peel in the poultry rations can be found in the literatures, however, Blandon et al. (2015) reported that dietary inclusion of banana peel up to 25% did not have adverse effects on the performance of broiler chickens. The use of banana peel meal as a functional feed ingredient to improve the health status for poultry has not been adequately researched. In the literature search, only one study was found referring that the feeding banana peel meal increased the weight of spleen of 35-days old broiler chicks (Siyal et al. 2016). According to recent studies (Pereira and Maraschin, 2015; Hernández-Alcántara et al. 2016) the banana peel is a good source of prebiotics, antioxidants and pro-vitamin A due to its contents of carotenoids, phenolics and amine compounds. Moreover, banana peel extract presented antimicrobial activity against Porphyromonas gingivalis, Aggregatibacter actinomycetemcomitans (Kapadia et al. 2015) and Staphylococcus aureus (Guil-Guerrero et al. 2016). These properties in the banana peel may therefore be beneficial for the health and well-being of poultry. Zhang et al. (2004) had previously reported that arabinoxylans derived from banana peels induced a positive oxidative burst in macrophages (activate a macrophage cell line as an immune stimulator), and can thus promote the health of broiler chicks. However, data regarding the application of banana peel extract on the health of poultry is scarce.

 

Orange peel and pulp

Orange peel is a by-product of sweet orange processing industry that are abundant especially during the harvesting period. Oluremi et al. (2008) revealed that the peels of sweet oranges contain 2440-2890 kcal/kg gross energy and 7.44-10% crude protein and may therefore be used to substitute the role of maize in poultry diets. The latter authors further showed that sweet orange peels can be included in broiler rations up to 15% without any detrimental impacts on final weight. In addition to vitamin C and dietary fibre, orange peels possess high contents of carotenoids (Ernawita et al. 2017), phenols and hesperidin (Kasapidou et al. 2015), which are essential for stimulating the immune system. Orange peels also contains essential oils (terpens and aliphatic sesquiterpene) displaying antimicrobial activities against E. coli 0157:H7 and Salmonella typhirmurium (Callaway et al. 2008). These latter properties may be beneficial for maintaining the poultry intestinal health. Ebrahimi et al. (2015) further reported that dried orange peels increased the mean value for the hemagglutination inhibition test in broiler chicks on day 42. Indeed, the treatment also reduced the population of E. coli in the caecum of broilers. Conversely, Alefzadeh et al. (2016) reported no effect of dried orange peel powder on the immune organ weights and the population of E. coli and Lactobacillus in the intestine of broiler chickens. The different nature of orange peels and the condition of the studies might explain these divergent results. For some agro-industrial by-products, fermentation is one of the method not only to improve the nutritional qualities, but also to enhance the functionality of the products. With regard to the fermentation of orange peels, reports available in the literatures shows differently. For example, Oluremi et al. (2010) revealed that fermentation did not change the nutritive values of the sweet orange peels, and that its use in feeding during the starter period depressed the growth performance of broiler chicks. In a previous study, Oluremi et al. (2008) also reported that feeding fermented sweet orange peels to replace maize had depressed the feed intake and growth rate of broilers. The spontaneous (without fermentation starter) fermentation failed to decrease the fibre content in orange peels and therefore reduced the digestibility of broiler chicks (Oluremi et al. 2008; Oluremi et al. 2010). The benefits of orange peel extract has been shown, not only in the production parameters (Ebrahimi et al. 2014), but also to the health and well-being of poultry. Pourhossein et al. (2015) reported that feeding orange peel extract increased antibody titer response to sheep red blood cells, antibody titer responses to ND virus, avian Influenza (AI), infectious Bursal disease (IBD) and infectious Bronchitis virus (IBV) vaccines. The treatment also increased the concentrations of IgA and IgG, but did not affect the relative weights of spleen and bursa of Fabricius. An earlier study by Akbarian et al. (2013) showed that the orange peel extract (400 mg/kg) increased the weight of bursa of fabricius and reduced the number of coliform bacteria in the ileum and caecum of broiler chickens. Also, Pourhossein et al. (2012) reported that the orange peel extract was able to reduce E. coli and coliform counts and increase the population of Lactobacilli in the ileum of broilers. These studies were in accordance with an in vitro study showing the antibacterial activities of orange peel extract against E. coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, S. typhi, S. paratyphi A, S. paratyphi B, Shigella flexneri and Vibrio cholerae (Nisha et al. 2013). A recent study in Japanese quails further showed the usefulness of orange peels in improving the stress response of birds to unfavorable conditions, as indicated by the level of malondialdehyde, glutathione peroxidase activity and glutathione production in liver (Ciftci et al. 2016). Orange pulp is the other by-product of sweet orange processing industry especially from juice extraction. It contains 8.1% crude protein and 18.13 MJ gross energy/kg DM. It is also rich in carotenoids, phenolic acids, flavonoids, terpenoids and vitamin C (Ernawita et al. 2017). Several studies have reported the application of orange pulp in poultry rations. For instance, inclusion of up to 2% of dried sweet orange pulp in broiler diets improved feed intake and body weight gain, decreased liver and abdominal fat as well as serum triglyceride level in broilers, while also improving the immune responses (antibody titres against ND virus, IB virus and IBD virus) in treated vs. control groups (Abbasi et al. 2015). Moreover, the treatment was able to reduce the total aerobic bacteria counts and increase the numbers of E. coli and Lactobacillus. Similarly, feeding pigs with 150 g/kg of ensiled citrus pulp reduced the enterobacteria counts after two weeks of treatment (Moset et al. 2015). Pascoal et al. (2015) further reported that the use of citrus pulp together with soybean hulls was capable of increasing the number of goblet cells and the density of villi in the jejunum as well as reducing the number of E. coli in the intestine of piglets slaughtered at day 35. Different from the aforementioned data, a different result was reported by Mourão et al. (2008), in which the dietary inclusion of citrus pulp (10%) lowered the growth rate and reduced the carcass yield of broiler chickens. The different natures and levels of orange pulp inclusion as well as the different of experiment conditions may explain the divergent results among the above reported studies. Interestingly, incorporating of citrus pulp in broiler diets resulted in higher content of polyunsaturated fatty acid (good fatty acids) in the meat of broilers as compared to control (Mourão et al. 2008).

 

General mechanism of tropical agro-industrial by-product in improving the health status of poultry

It is generally believed that functional feed ingredients may alleviate the risk factors responsible for a number of diseases in poultry. The exact mechanism by which the tropical agro-industrial by-products acting as functional feeds protect the poultry from diseases remains unclear, but multiple reports describe an improvement of the immune defense system (Sundu et al. 2006; Soltan, 2009), the modulation of intestinal microbial populations (Sundu et al. 2006) and other physiological functions of poultry (Abbasi et al. 2015; Ebrahimi et al. 2015). It has been mentioned earlier that agro-industrial residues are good sources for oligosaccharides such as mannose, mannan, arabinoxylans, etc. (Chen et al. 2015; Kurdi and Hansawasdi, 2015; Rezaei et al. 2015), which can serve as prebiotics for poultry. These oligosaccharides may stimulate the growth of endogenous beneficial bacteria (e.g., bifid bacteria and lactobacilli) ensuring the intestinal microbial balance and enhanced immune defense of chicks. The detailed mechanisms through which prebiotics, which include the oligosaccharides, improve the gut microbial ecosystem and immune competence of poultry have intensively been reviewed elsewhere (Sugiharto, 2016). With regard to the role of prebiotics derived from agro-industrial residues on the physiological functions of poultry, data available in the literature are still limited. However, prebiotics may in general improve the morphology (perimeter and height of villi) and development of the intestine, and therefore improve digestion and absorption of nutrients (Oliveira et al. 2008; Ao and Choct, 2013). Prebiotics may also improve the hormonal regulation in poultry, as previously reported by Sohail et al. (2012) who found prebiotics (MOS) were able to alleviate the dramatic increased level of stress-related corticosterone in poultry (e.g., heat stress). Note that increased corticosterone compromises the physiological imbalance in poultry. It has been known that agro-industrial by-products contain several bioactive components (Esa et al. 2013) that may provide nutraceutical effects on poultry. Among the active components derived from the agro-industrial residues, γ-oryzanol derived from the rice bran oil has immune-stimulatory properties that may modulate the immune response of poultry against pathogenic microorganisms (Kang et al. 2015). Ghatak and Panchal (2012) reported that γ-oryzanol was able to improve immune competences of host through cellular and humoral mediated mechanisms. Further, γ-oryzanol may also promote the development of immune organs, such as thymus and spleen (Szczesniak et al. 2016). The latter workers further reported that γ-oryzanol has antioxidant potential and can therefore ameliorate the oxidative stress in poultry. To deal with the oxidative stress, γ-oryzanol may improve the body redox capacity of host (Zolali et al. 2015). The antibacterial and antioxidant capacities of agro-industrial by-products may in some extent be determined by the presence of phenolic compounds in the by-products (Hernández-Alcántara et al. 2016; Ernawita et al. 2017). The definite mechanism by which phenolic compounds exert their antimicrobial activities are largely unknown, but one possible mechanism may be that they disrupt the cytoplasmic membrane of bacteria resulting in loss of membrane integrity and morphological changes, resulting in bacterial cell lysis and death (Wu et al. 2016). Apart from the amelioration of oxidative stress, the antioxidant properties of phenolic compounds may improve the immune response of poultry. In mice, the phenolic compounds were capable of improving the immune system as indicated by the increased antibody titres and the percentage of protected animals after swine herpesvirus type 1 (SuHV-1) challenge (Fischer et al. 2010). Several mechanisms on how the phenolic compounds may be able to improve immune system of poultry have been suggested. One possible mechanism could be that phenolic compounds modulate the process of differentiation and activation of immune cells (Cuevas et al. 2013). Moreover, antioxidant properties of phenols may also prevent the destructive effect of free radicals on the immune functions of host (Brambilla et al. 2008).

 

CONCLUSION

Tropical agro-industrial by-products contain several bioactive compounds that may act as antimicrobial agents, antioxidants and immune-modulator. These properties may contribute to the role of agro-industrial by-products as functional feed ingredients in promoting the health and well-being of poultry. Future research is needed to confirm the potential of agro-industrial residues and their derivative products in substituting the use of synthetic antibiotics in poultry rations. Overall, given that the availability and price of the agro-industrial by-products may vary greatly across the regions, the use of such by-products as functional feed ingredients in poultry rations should therefore be adjusted according to the availability and cost of each by-product.

 

ACKNOWLEDGEMENT

Authors acknowledge the financial support provided by Diponegoro University, Semarang Central Java, Indonesia through non-tax state revenue (PNBP).

Abbasi H., Seidavi A., Liu W. and Asadpour L. (2015). Investigation on the effect of different levels of dried sweet orange (Citrus sinensis) pulp on performance, carcass characteristics and physiological and biochemical parameters in broiler chicken. Saudi J. Biol. Sci. 22, 139-146.

Abel F.A.S., Adeyemi O.A., Oluwole O.B., Oladunmoye O.O. and Ayo-Ajasa O.Y. (2015). Effects of treated banana peel meal on the feed efficiency, digestibility and cost effectiveness of broiler chickens diet. J. Vet. Sci. Anim. Husb. 3(1), 101-107.

Akbarian A., Golian A., Kermanshahi H., Farhoosh R., Raji A.R., de Smet S. and Michiels J. (2013). Growth performance and gut health parameters of finishing broilers supplemented with plant extracts and exposed to daily increased temperature. Spanish J. Agric. Res. 11, 109-119.

Alefzadeh T., Bouyeh M., van den Hoven R., Seidavi A., Laudadio V. and Tufarelli V. (2016). Effect of dietary dried orange (Citrus sinensis) peel powder and exogenous multi-enzymes on growth and carcass traits and ileal microflora of broiler chickens. Pakistan J. Zool. 48(6), 1891-1897.

Alshelmani M.I., Loha T.C., Food H.L., Sazilia A.Q. and Lau W.H. (2016). Effect of feeding different levels of palm kernel cake fermented by Paenibacillus polymyxa ATCC 842 on nutrient digestibility, intestinal morphology, and gut microflora in broiler chickens. Anim. Feed Sci. Technol. 216, 216-224.

Ao Z. and Choct M. (2013). Oligosaccharides affect performance and gut development of broiler chickens. Asian-Australasian J. Anim. Sci. 26(1), 116-121.

Blandon J.C., Hamady G.A.A. and Abdel-Moneim M.A. (2015). The effect of partial replacement of yellow corn by banana peels with and without enzymes on broiler’s performance and blood parameters. J. Anim. Poult. Sci. 4(1), 10-19.

Brambilla D., Mancuso C., Scuderi M.R., Bosco P., Cantarella G., Lempereur L., Di Benedetto G., Pezzino S. and Bernardini R. (2008). The role of antioxidant supplement in immune system, neoplastic, and neurodegenerative disorders: A point of view for an assessment of the risk/benefit profile. Nutr. J. 7, 29-35.

Callaway T.R., Carroll J.A., Arthington J.D., Pratt C., Edrington T.S., Anderson R.C., Galyean M.L., Ricke S.C., Crandall P. and Nisbet D.J. (2008). Citrus products decrease growth of E. coli 0157:H7 and Salmonella typhirmurium in pure culture and in fermentation with mixed ruminal microorganisms in vitro. Foodborne Pathog. Dis. 5(5), 621-627.

Cencic A. and Chingwaru W. (2010). The role of functional foods, nutraceuticals, and food supplements in intestinal health. Nutrients. 2, 611-625.

Chen W.L., Liang J.B., Jahromi M.F., Abdullah N., Ho Y.W. and Tufarelli V. (2015). Enzyme treatment enhances release of prebiotic oligosaccharides from palm kernel expeller. BioResources. 10(1), 196-209.

Chinajariyawong C. and Muangkeow N. (2011). Carcass yield and visceral organs of broiler chickens fed palm kernel meal or Aspergillus wentii TISTR 3075 fermented palm kernel meal. Walailak J. Sci. Technol. 8(2), 175-185.

Choi J.Y., Paik D.J., Kwon D.Y. and Park Y. (2014). Dietary supplementation with rice bran fermented with Lentinus edodes increases interferon-γ activity without causing adverse effects: A randomized, double blind, placebo controlled, parallel-group study. Nutr. J. 13, 35-41.

Ciftci M., Simsek U.G., Dalkilic B., Azman M.A., Yilmaz O., Mutlu S.I., Ozcelik M., Baykalir Y., Tonbak F. and Bahsi M. (2016). Effect of dietary orange peel extract on physiological, biochemical, and metabolic responses of Japanese quail reared under low ambient temperature. Turkish J. Vet. Anim. Sci. 40, 288-297.

Cuevas A., Saavedra N., Salazar L.A. and Abdalla D.S.P. (2013). Modulation of immune function by polyphenols: Possible contribution of epigenetic factors. Nutrients. 5, 2314-2332.

Cương D.B., Hoa N.T., Huyền L.T. and Thu D.T. (2010). Bioconversion of copra meal into prebiotic mannooligosaccharides using endo-β-1,4-mannanase producing by Aspergillus niger BK 01. J. Sci. Technol. 48(3), 43-49.

Duarte K.F., Ibuki M., Fukui K., Kato M., Santos E.T. and Junqueira O.M. (2014). Effect of hydrolyzed copra meal separately or in combination with Bacillus cereus var. toyoi on growth performance of broiler chickens. Acta Sci. Anim. Sci. 36(4), 373-377.

Duwa H., Saleh B., Lamido M. and Saidu A. (2014). Growth, haematological and serum biochemical indices of broiler chickens fed banana peel meal as replacement for maize in the semi-arid zone of Nigeria. Online J. Anim. Feed Res. 4(5), 121-126.

Ebrahimi A., Qotbi A.A.A., Seidavi A. and Bahar V. (2014). The effects of dietary supplementation of Citrus sinensis peel extract on production and quality parameters of broiler chicken. J. Appl. Anim. Res. 42(4), 445-450.

Ebrahimi A., Santini A., Alise M., Pourhossein Z., Miraalami N. and Seidavi A. (2015). Effect of dried Citrus sinensis peel on gastrointestinal microbiota and immune system traits of broiler chickens. Italian J. Anim. Sci. 14(4), 4194.

El Sohaimy S.A. (2012). Functional foods and nutraceuticals-modern approach to food science. World Appl. Sci. J. 20(5), 691-708.

Ernawita, Wahyuono R.A., Hesse J., Hipler U.C., Elsner P. and Böhm V. (2017). In vitro lipophilic antioxidant capacity, antidiabetic and antibacterial activity of citrus fruits extracts from Aceh, Indonesia. Antioxidants. 6, 1-11. 

Esa N.M., Ling T.B. and Peng L.S. (2013). By-products of rice processing: An overview of health benefits and applications. J. Rice Res. 1, 107.

Fischer G., Paulino N., Marcucci M.C., Siedler B.S., Munhoz L.S., Finger P.F., Vargas G.D., Hübner S.O., Vidor T. and Roehe P.M. (2010). Green propolis phenolic compounds act as vaccine adjuvants, improving humoral and cellular responses in mice inoculated with inactivated vaccines. Mem. Inst. Oswaldo Cruz. 105(7), 908-913.

Gallinger C.I., Suárez D.M. and Irazusta A. (2004). Effects of rice bran inclusion on performance and bone mineralization in broiler chicks. J. Appl. Poult. Res. 13, 183-190.

Ghatak S.B. and Panchal S.J. (2012). Investigation of the immunomodulatory potential of oryzanol isolated from crude rice bran oil in experimental animal models. Phytother. Res. 26, 1701-1708.

Ghosh A., Verma A.K., Tingirikari J.R., Shukla R. and Goyal A. (2015). Recovery and purification of oligosaccharides from copra meal by recombinant endo-β-mannanase and deciphering molecular mechanism involved and its role as potent therapeutic agent. Mol. Biotechnol. 57(2), 111-127.

Guil-Guerrero J.L., Ramos L., Moreno C., Zúñiga-Paredes J.C., Carlosama-Yepez M. and Ruales P. (2016). Antimicrobial activity of plant-food by-products: A review focusing on the tropics. Livest. Sci. 189, 32-49.

Hasler C.M. (2002). Functional foods: benefits, concerns and challenges-a position paper from the American council on science and health. J. Nutr. 132(12), 3772-3781.

Hatta U. and Sundu B. (2009). Effects of Copra Meal Fermented by Aspergillus niger and Trichoderma spp. on Performance of Broiler. Pp. 54 in Proc. 1st Int. Semin. Anim. Indust. Bogor Agricultural University, Bogor, Indonesia.

Henderson A.J., Kumar A., Barnett B., Dow S.W. and Ryan E.P. (2012). Consumption of rice bran increases mucosal immunoglobulin A concentrations and numbers of intestinal Lactobacillus spp. J. Med. Food. 15(5), 469-475.

Hernández-Alcántara A.M., Totosaus A. and Perez-Chabela M.L. (2016). Evaluation of agro-industrial co-products as source of bioactive compounds: fiber, antioxidants and prebiotic. AUCFT. 20(2), 3-16.

Hossain M.M., Park J.W., Nyachoti C.M. and Kim I.H. (2016). Effects of extracted rice bran supplementation on growth performance, nutrient digestibility, diarrhea score, blood profiles, and fecal microbial shedding in comparison with apramycin (antibiotic growth promoter) in weanling pigs. Canadian J. Anim. Sci. 96(4), 495-503.

Ibuki M., Fukui K., Kanatani H. and Mine Y. (2014). Anti-inflammatory effects of mannanase-hydrolyzed copra meal in a porcine model of colitis. J. Vet. Med. Sci. 76(5), 645-651.

Ibuki M., Kovacs-Nolan J., Fukui K., Kanatani H. and Mine Y. (2010). Analysis of gut immune-modulating activity of β-1,4-mannobiose using microarray and real-time reverse transcription polymerase chain reaction. Poult. Sci. 89, 1894-1904.

Ibuki M., Yamauchi K. and Fukui K. (2013). Effect of dietary mannanase-hydrolysed copra meal on growth performance and intestinal histology in broiler chickens. J. Anim. Physiol. Anim. Nutr. 98(4), 636-642.

Kang H.K. and Kim C.H. (2016). Effects of dietary supplementation with rice bran oil on the growth performance, blood parameters, and immune response of broiler chickens. J. Anim. Sci. Technol. 58, 12-19.

Kang H.K., Kim J.H., Kim C.H., Jeon I.S. and Hwangbo J. (2015). Effect of dietary supplementation with rice bran extract on the growth performance, blood parameters of broiler chickens.Pp.37-42 in Proc.20th European Symp. Poult. Nutr., Prague, Czech Republic.

Kapadia S.P., Pudakalkatti P.S. and Shivanaikar S. (2015). Detection of antimicrobial activity of banana peel (Musa paradisiaca) on Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans: An in vitro study. Contemp. Clin. Dent. 6(4), 496-499.

Kasapidou E., Sossidou E. and Mitlianga P. (2015). Fruit and vegetable co-products as functional feed ingredients in farm animal nutrition for improved product quality. Agriculture. 5, 1020-1034.

Khempaka S., Molee W. and Guillaume M. (2009). Dried cassava pulp as an alternative feedstuff for broilers: Effect on growth performance, carcass traits, digestive organs, and nutrient digestibility. J. Appl. Poult. Res. 18, 487-493.

Khempaka S., Thongkratok R., Okrathok S. and Molee W. (2014). An evaluation of cassava pulp feedstuff fermented with A. oryzae, on growth performance, nutrient digestibility and carcass quality of broilers. J. Poult. Sci. 51, 71-79.

Khin H.S. (2004). Evaluation of solid state fermentation by Aspergillus niger to improve the nutritive value of palm kernel cake for broilers. Ph D. Thesis. University of Putra Malaysia, Selangor Darul Ehsan, Malaysia.

Kim C.H., Park S.B., Kang M.G. and Ku H. (2016). Effects of graded levels of rice bran oil on laying performance, blood parameters and egg yolk cholesterol in HyLine laying hens. Korean J. Poult. Sci. 43, 89-96.

Koh J.H., Yu K.W. and Suh H.J. (2002). Biological activities of Saccharomyces cerevisiae and fermented rice bran as feed additives. Lett. Appl. Microbiol. 35, 47-51.

Komiyama Y., Andoh A., Fujiwara D., Ohmae H., Araki Y., Fujiyama Y., Mitsuyama K. and Kanauchi O. (2011). New prebiotics from rice bran ameliorate inflammation in murine colitis models through the modulation of intestinal homeostasis and the mucosal immune system. Scandinavian J. Gastroenterol. 46(1), 40-52.

Kumar A., Henderson A., Forster G.M., Goodyear A.W., Weir T.L., Leach J.E., Dow S.W. and Ryan E.P. (2012). Dietary rice bran promotes resistance to Salmonella enterica serovar typhimurium colonization in mice. BMC Microbiol. 12, 71-78.

Kurdi P. and Hansawasdi C. (2015). Assessment of the prebiotic potential of oligosaccharide mixtures from rice bran and cassava pulp. LWT - Food Sci. Technol. 63, 1288-1293.

Martirosyan D.M. and Singh J. (2015). A new definition of functional food by FFC: What makes a new definition unique? Funct. Foods Health Dis. 5(6), 209-223.

Moset V., Piquer O., Cervera C., Fernández C.J., Hernández P. and Cerisuelo A. (2015). Ensiled citrus pulp as a byproduct feedstuff for finishing pigs: nutritional value and effects on intestinal microflora and carcass quality. Spanish J. Agric. Res. 13(3), e0607.

Mourão J.L., Pinheiro V.M., Prates J.A., Bessa R.J., Ferreira L.M., Fontes C.M. and Ponte P.I. (2008). Effect of dietary dehydrated pasture and citrus pulp on the performance and meat quality of broiler chickens. Poult. Sci. 87(4), 733-743.

Mu K.S., Kasim A.B., Ideris A. and Saad C.R. (2011). Effect of fermented rice bran, bio-converted byproducts on performance of broiler chickens. J. Anim. Vet. Adv. 10, 2990-2995.

Navidshad B., Liang J.B., Jahromi M.F., Akhlaghi A. and Abdullah N. (2015). A comparison between a yeast cell wall extract (Bio-Mos®) and palm kernel expeller as mannan-oligosac-charides sources on the performance and ileal microbial population of broiler chickens. Italian J. Anim. Sci. 14(1), 3452-3467.

Nisha S.N., Swedha A. and Rahaman J.S.N. (2013). Antibacterial activity of Citrus sinensis peel against enteric pathogens. Int. J. Pharma. Res. Bio. Sci. 2, 1-13.

Oluremi O.I.A., Mou P.M. and Adenkola A.Y. (2008). Effect of fermentation of sweet orange (Citrus sinensis) fruit peel on its maize replacement value in broiler diet. Livest. Res. Rural Dev. 20(2), 1-6.

Oluremi O.I.A., Okafor F.N., Adenkola A.Y. and Orayaga K.T. (2010). Effect of fermentation of sweet orange (Citrus sinensis) fruit peel on its phytonutrients and the performance of broiler starter. Int. J. Poult. Sci. 9(6), 546-549.

Oliveira M.C., Rodrigues E.A., Marques R.H., Gravena R.A., Guandolini G.C. and Moraes V.M.B. (2008). Performance and morphology of intestinal mucosa of broilers fed mannanoligosaccharides and enzymes. Arq. Bras. Med. Vet. Zootec. 60(2), 442-448.

Osundahunsi O.F., Williams A.O. and Oluwalana I.B. (2012). Prebiotic effects of cassava fibre as an ingredient in cracker-like products.Food Funct. 3(2), 159-163.

Pascoal L.A.F., Thomaz M.C., Watanabe P.H., dos Santos Ruiz U., Amorim A.B., Daniel E. and da Silva S.Z. (2015). Purified cellulose, soybean hulls and citrus pulp as a source of fiber for weaned piglets. Sci. Agric. 72(5), 400-410.

Pereira A. and Maraschin M. (2015). Banana (Musa spp.) from peel to pulp: Ethnopharmacology, source of bioactive compounds and its relevance for human health. J. Ethnopharmacol. 160, 149-163.

Pourhossein Z., Qotbi A.A.A. and Seidavi A. (2012). Investigation on the effect of different levels of Citrus sinensis extract on gastrointestinal microbial population in commercial broilers. African J. Microbiol. Res. 6, 6370-6378.

Pourhossein Z., Qotbi A.A.A., Seidavi A., Laudadio V., Centoducati G. and Tufarelli V. (2015). Effect of different levels of dietary sweet orange (Citrus sinensis ) peel extract on humoral immune system responses in broiler chickens. Anim. Sci. J. 86, 105-110.

Rezaei S., Jahromi M.F., Liang J.B., Zulkifli I., Farjam A.S., Laudadio V. and Tufarelli V. (2015). Effect of oligosaccharides extract from palm kernel expeller on growth performance, gut microbiota and immune response in broiler chickens. Poult. Sci. 94, 2414-2420.

Shakila S. and Sudhakar R.P. (2012). The utilization of palm kernel meal in laying hen diet. Indian J. Poult. Sci. 47, 79-83.

Sindhu A.A., Khan M.A., Mahr-Un-N. and Sarwar M. (2002). Agro-industrial by-products as a potential source of livestock feed. Int. J. Agric. Biol. 4(2), 307-310.

Siyal F.A., Wagan R., Bhutto Z.A., Tareen M.H., Arain M.A., Saeed M., Brohi S.A. and Soomro R.N. (2016). Effect of orange and banana peels on the growth performance of broilers. Adv. Anim. Vet. Sci. 4(7), 376-380.

Sohail M.U., Hume M.E., Byrd J.A., Nisbet D.J., Ijaz A., Sohail A., Shabbir M.Z. and Rehman H. (2012). Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult. Sci. 91, 2235-2240.

Soltan M.A. (2009). Growth performance, immune response and carcass traits of broiler chicks fed on graded levels of palm kernel cake without or with enzyme supplementation. Livest. Res. Rural Dev. 21(3), 1-7.

Sugiharto S., Yudiarti T. and Isroli I. (2015). Functional properties of filamentous fungi isolated from the Indonesian fermented dried cassava, with particular application on poultry. Mycobiology. 43(4), 415-422.

Sugiharto S., Yudiarti T. and Isroli I. (2016). Haematological and biochemical parameters of broilers fed cassava pulp fermented with filamentous fungi isolated from the Indonesian fermented dried cassava. Livest. Res. Rural Dev. 28(4), 1-9.

Sugiharto S. (2016). Role of nutraceuticals in gut health and growth performance of poultry. J. Saudi Soc. Agric. Sci. 15, 99-111.

Sugiharto S., Yudiarti T., Isroli I., Widiastuti E. and Putra F.D. (2017a). Effects of feeding cassava pulp fermented with Acremonium charticola on growth performance, nutrient digestibility and meat quality of broiler chicks. South African. J. Anim. Sci. 47(2), 130-138.

Sugiharto S., Yudiarti T., Isroli I., Widiastuti E. and Putra F.D. (2017b). Intestinal microbial ecology and hematological parameters of broiler fed cassava waste pulp fermented with Acremonium charticola. Vet. World. 10(3), 324-330.

Sundu B., Hatta U. and Chaudhry A.S. (2012). Potential use of beta-mannan from copra meal as a feed additive for broilers. World’s Poult. Sci. J. 68, 707-716.

Sundu B., Kumar A. and Dingle J. (2009). Feeding value of copra meal for broilers. World’s Poult. Sci. J. 65, 481-491.

Sundu B., Kumar A. and Dingle J. (2006). Palm kernel meal in broiler diets: effect on chicken performance and health. World’s Poult. Sci. J. 62(2), 316-325.

Supriyati T., Haryati T., Susanti T. and Susana I.W.R. (2015). Nutritional value of rice bran fermented by Bacillus amyloliquefaciens and humic substances and its utilization as a feed ingredient for broiler chickens. Asian Australian J. Anim. Sci. 28(2), 231-238.

Syngai G.G., Gopi R., Bharali R., Dey S., Lakshmanan G.M.A. and Ahmed G. (2016). Probiotics - the versatile functional food ingredients. J. Food Sci. Technol. 53(2), 921-933.

Szczesniak K.A., Ostaszewski P., Ciecierska A. and Sadkowski T. (2016). Investigation of nutriactive phytochemical-gamma-oryzanol in experimental animal models. J. Anim. Physiol. Anim. Nutr. 100, 601-617.

Ugwu S.O.C., Onyimonyi A.E. and Ozonoh C.I. (2008). Comparative performance and hematological indices of finishing broilers fed palm kernel cake, bambara and rice husk as partial replacement for maize. Int. J. Poult. Sci. 7(3), 299-303.

Wen Y.L., Yan L.P. and Chen C.S. (2013). Effects of fermentation treatment on antioxidant and antimicrobial activities of four common Chinese herbal medicinal residues by Aspergillus oryzae. J. Food Drug Anal. 21, 219-226.

Wu Y., Bai J., Zhong K., Huang Y., Qi H., Jiang Y. and Gao H. (2016). Antibacterial activity and membrane-disruptive mechanism of 3-p-trans-coumaroyl-2-hydroxyquinic acid, a novel phenolic compound from pine needles of Cedrus deodara, against Staphylococcus aureus. Molecules. 21, 1084-1092.

Yusrizal Y., Angel R., Adrizal A., Wanto B.E., Fakhri S. and Yatno Y. (2013). Feeding native laying hens diets containing palm kernel meal with or without enzyme supplementations. 2. Excreta nitrogen, ammonia, and microbial counts. J. Appl. Poult. Res. 22, 269-278.

Zheng L., Duarte M.E., Park I. and Kim S.W. (2017). Supplemental effects of fermented rice bran extracts on growth performance, bone characteristics, and immune response of broiler chickens. J. Anim. Sci. 95(2), 75-76.

Zhang P., Wampler J.L., Bhunia A.K., Burkholder K.M., Patterson J.A. and Whistler R.L. (2004). Effects of arabinoxylans on activation of murine macrophages and growth performance of broiler chicks. Cereal Chem. 60, 46-50.

Zolali E., Asgharian P., Hamishehkar H., Kouhsoltani M., Khodaii H. and Hamishehkar H. (2015). Effects of gamma oryzanol on factors of oxidative stress and sepsis induced lung injury in experimental animal model. Iran J. Basic Med. Sci. 18(12), 1257-1263.

Zulkifli I., Ginsos J., Liew P.K. and Gilbert J. (2003). Growth performance and Newcastle disease antibody titres of broiler chickens fed palm-based diets and their response to heat stress during fasting. Archiv für Geflügelkunde. 67(3), 125-130.