Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University, Semarang, Central Java, Indonesia (50275) firstname.lastname@example.org
The availability of alternative antimicrobial- and growth-promoting agents are of importance for sustainable broiler production following the global retraction of in-feed antibiotics. Microalgae Spirulina and Chlorella have been shown to improve the growth performance of broiler chickens. These microalgae may also improve immune responses, intestinal morphology and the microbial ecosystem and antioxidative status of broilers. Also, Spirulina and Chlorella may serve as therapeutic agents for broiler chickens. The present review provides the recent advances in the applications of microalgae Spirulina and Chlorella in broiler production as well as the mechanisms through which the microalgae exert the positive effects.
Keywords: antibiotic substitute, broilers, health, microalgae
To maximize the genetic potential for growth, broiler chickens have traditionally been reared with antibiotics incorporated in feed. Antibiotics may control the microbial population in the intestine and hence maintain the health and promote the growth rate of broilers (Sugiharto 2016). Apart from the benefits of in-feed antibiotics on broilers, a number of studies have shown the potential threat of in-feed antibiotics on the health of humans as consumers of broiler products. This is associated with the phenomenon of antimicrobial resistance in humans (Sugiharto 2016; Sugiharto and Ranjitkar 2019). The latter problems have consequently encouraged the authorities to ban the use of antibiotics in broiler diets in most countries. Beyond the food safety reason, the removal of antibiotics from diets has adversely affected the growth performance and health status of broilers. During the post-antibiotic era, the outbreak of bacterial infections have frequently been reported. This may result in the increase in morbidities and mortalities. The antibiotic retraction has also been reported to retard the growth rate of broilers in commercial farms. Considering the crucial functions of growth-promoting and health-improving agents in broiler production, any alternatives to substitute the role of in-feed antibiotics are thereby of importance for the sustainable broiler production. Several alternatives have been proposed to substitute the role of in-feed antibiotics for broilers including probiotics, prebiotics, synbiotics, herbs, vitamins, antioxidants, enzymes and fatty acids (Sugiharto 2016). These bioactive components may improve the intestinal microbial ecosystem, morphology and immune system of broiler chicks. Such improvement may eventually exert the positive impacts on the health and growth performance of broilers. In addition to the above mentioned alternatives, microalgae Spirulina and Chlorella, which are the two most studied microalgae, have also been used as substitutes for in-feed antibiotics for broiler chickens (Sugiharto and Lauridsen 2016; Sugiharto et al 2018). Studies showed that the administration of Spirulina resulted in improved production performance and intestinal health in broiler chickens (Jamil et al 2015; Kaoud 2015; Sugiharto et al 2018). Likewise, feeding Chlorella was attributed to the improved growth rate, immune responses and intestinal microbial ecosystem of broilers (Kang et al 2013; An et al 2016; Sugiharto and Lauridsen 2016; El-Abd and Hamouda 2017; Abdelnour et al 2019). The present review provides the recent advances in the use of microalgae Spirulina and Chlorella in broiler production as well as the mechanisms through which the microalgae exert the positive effects on broiler chicks.
Nutritional compositions of microalgae Spirulina and Chlorella
Microalgae have long been known as a good source of nutrients both for humans and animals. Proximate analysis showed that Spirulina contains high amount of protein and it may therefore widely be used as a protein supplement. Soni et al (2017) documented that Spirulina contains 60-70% protein, which is much higher than that of conventional dietary protein source for broilers (i.e., soy bean meal contains about 40% protein). In term of quality, Spirulina contains a complete list of essential amino acids (Sharoba et al 2014). This may therefore encourage the nutritionist to use Spirulina as protein supplement for poultry (Alvarenga et al 2011; Sugiharto et al 2018). It should however be noticed that not all protein in Spirulina can be utilised by the chicks, as some of the total protein in this microalgae (nearly 10%) is non-protein nitrogen (Devi et al 1981). In addition to protein, Spirulina has also been reported to be rich in vitamins, minerals, pigments, chlorophyll, essential fatty acids, polysaccharides and phenolic compounds (Karkos et al 2011; Beheshtipour et al 2013; Holman and Malau-Aduli 2013). The analysed chemical composition of microalgae Spirulina has been reported by two authors (Table 1). It is apparent that there is a significant variation in the chemical composition of Spirulina. Several factors may account for the variation, including climatic factors, light intensity, aeration, culture condition and stress (Soni et al 2017).
Table 1. Chemical composition of microalgae Spirulina (% dry basis)
Chemical Sharoba Sugiharto compositions et al (2014) et al (2018)
Crude protein 62.8 52.4
Crude fat 6.93 0.63
Crude fibre 8.12 34.2
Crude ash 7.47 11.9
In line with Spirulina, Chlorella is also rich in crude protein (Kang et al 2013), and could therefore be used to enrich the protein content of broiler feeds. Chlorella is also a good source of essential amino acids, vitamins, minerals and chlorophyll as well as several bioactive substances that may positively affect broiler chickens (Abdelnour et al 2019). As in the case with Spirulina, there is also a variation in the chemical composition of Chlorella. For example, Kang et al (2013) reported that that Chlorella has 60.6% crude protein, 12.8% fat, 13.0% crude fibre and 4.50% ash. Different from the above proximate data, Sugiharto et al (2010) previously showed that Chlorella contained 55.3% crude protein, 10.3% crude fat and 5.80% crude fibre. As with other microalgae, particularly Spirulina, climate, light intensity, aeration, culture condition, stress, as well as post-harvesting management may be responsible for the differences in chemical composition and quality of Chlorella (Sugiharto et al 2010; Soni et al 2017).
Apart from the high nutritional contents of Spirulina and Chlorella, dietary supplementation of such microalgae to broiler chickens should be conducted with caution as long term administration of microalgae Spirulina may negatively affect erythropoiesis. Our previous study showed that feeding microalgae Spirulina for the whole period of rearing (35 days) decreased the levels of erythrocytes, haemoglobin and haematocrit in broiler chickens (Sugiharto et al 2018). The presences of microcystin (Iwasa et al 2002) and cyanotoxins (Roy-Lachapelle et al 2017) in the microalgae may be attributed to the disruption of liver where the erythrocytes and haemoglobin are partly produced.
Immune-enhancing properties of microalgae Spirulina and Chlorella for broilers
Many properties must be possessed by feeds in order for them to be used as alternatives for in-feed antibiotics for chickens, one of which is their capacity to improve the immune function, which may be expected to result in better health status of broiler chicks. The microalgae Spirulina and Chlorella are among the examples of bioactive materials possessing immune-enhancing properties for both humans and animals. A previous study showed that dietary administration of Chlorella resulted in higher levels of plasma immunoglobulin (IgA and IgG) in broiler chickens (Kang et al 2013). The modulation capacity of Chlorella was also reported on the immune response of broiler chicks by An et al (2016), in which feeding dried Chlorella vulgaris increased the serum levels of IgG and IgM. Likewise, Kang et al (2016) documented that feeding Chlorella by‐product increased the plasma concentrations of IgG, IgM and IgA. In respect to Spirulina, dietary supplementation of this microalga was attributed to the higher antibody response against sheep red blood cells (SRBC) in broiler chickens as reported by Mirzaie et al (2018). Similar to the latter report, an earlier study by Qureshi et al (1996) documented a beneficial impact of feeding Spirulina on the second humoral response against SRBC antigen when compared with the control. The potential of Spirulina in improving the immunity of broilers has also been reported by Lokapirnasari et al (2015), in which treatment with Spirulina increased the number of leukocytes and thus the protective capacity of broiler chicks. Likewise, Jamil et al (2015) revealed that treatment with Spirulina resulted in increased numbers of leukocytes in broiler chicks. The latter treatment was also associated with improved blood indices in broilers (ie: increased total erythrocytes and haemoglobin, and decreased erythrocyte sedimentation rate). A recent study by Fathi et al (2018) further showed that feeding Spirulina platensis resulted in higher relative weight of immune organs (bursa, thymus and spleen) in broiler chickens. In accordance with this, Kumari et al (2019) showed that Spirulina administration increased the bursal index in broiler chickens vaccinated with infectious bursal diseases (IBD) vaccine, suggesting that microalga supplementation may alleviate the immunosuppression by IBD. Corresponding to the chicken studies, a study in humans showed that administration of Chlorella enhanced the activity of natural killer cells and produced cytokines such as interferon (INF)-γ, interleukin (IL)-12 and IL-1β (Kwak et al 2012). The latter condition may eventually increase the immune cells and activities of macrophages (Kang et al 2013). In line with this, Spirulina was used as immune enhancer in rabbits, increasing the CD4+/CD8+ in the serum (Seyidoglu et al 2017).
The mechanism through which the green algae Spirulina and Chlorella improve the immune system of broilers is definitely unknown but some possible mechanisms may be proposed. Seyidoglu et al (2017) noted that polysaccharides (particularly β-glucan) and phycocyanin in Spirulina improved the development and maturation of leukocytes, which is a pivotal part of the immune defence of broilers. The phycocyanin also had an anti-inflammatory effect controlling the release of histamine by mast cells to prevent the excessive immune responses by the animals (Karkos et al 2011). Barkia et al (2019) also documented that omega-3 fatty acids in Chlorella may serve as an anti-inflammatory agent, thus improving the host immune responses. In support to the latter study, Sugiharto and Lauridsen (2016) pointed out that omega-3 fatty acids in Chlorella increased the production of secretory IgA in the intestine of broiler chickens. A very recent study by Abdelnour et al (2019) further confirmed that omega-3 fatty acids in Chlorella vulgaris were capable of modulating the immune system of broilers. The latter workers also suggested that antioxidant content in microalgae may contribute to the improvement in the immune functions of broilers. This inference was supported by other authors revealing that selenium (Rezvani et al 2012) and zinc (Jamil et al 2015), which are antioxidant minerals, content in Chlorella and Spirulina play a substantial role in increasing the cellular immune system of broiler chickens. Many phenolic compounds in microalgae Spirulina and Chlorella exert anti-inflammatory effect, thereby improving immune competences of animals (Finamore et al 2017). Moreover, β-carotene and vitamin B12 seemed also to possess immunomodulatory properties that can improve the immune responses of broilers (Abdelnour et al 2019). It is also most likely that both Spirulina and Chlorella have a direct effect on the development (Fathi et al 2018) and stimulation (Abou-Zeid et al 2015) of the lymphatic tissues of broiler chickens. It is generally understood that nutritional status is in parallel with the immune status, hence nutritional deficiency is often attributed to the compromised immune function in animals. Apart from their biologically active compounds as discussed above, microalgae Spirulina and Chlorella may also be exploited to compensate nutritional deficiencies, thus improving the immune system of broilers (Karkos et al 2011). Indeed, the remarkably high content of protein in the microalgae can help to cover the nutritional deficiencies in feeds of broiler chickens.
Microbial-modulating properties of microalgae Spirulina and Chlorella for broilers
In most conditions, phytochemicals have been used as antimicrobial agents to control the growth of pathogenic microorganisms. Spirulina is known to produce extracellular metabolites possessing antimicrobial activity. Owing to this, Spirulina platensis has been used to inhibit the growth of gram positive (such as Staphylococcus aureus,Bacillus subtilis and B. pumulis) and gram negative (Escherichia coli, Pseudomonas aeruginosa, and Proteus vulgaris) bacteria (Finamore et al 2017). In an in vivo study, Sugiharto et al (2018) have recently reported that feeding Spirulina platensis decreased the numbers of coliforms in the ileum and caecum of broiler chickens. Similarly, Shanmugapriya et al (2015) and Fathi et al (2018) reported the decreased number of E. coli in the intestine of broilers with feeding of Spirulina platensis. In line with Spirulina, a study by Hussein et al (2018) showed the antimicrobial activity of Chlorella vulgaris against gram negative (Enterobacter, Proteus, and Escherichia coli) and gram positive (Staphylococcus aureus, Lactobacillus acidophilus, and Streptococcus pyogenes) bacteria. In an in vivo study, feeding dried Chlorella powder decreased the number of E. coli and Salmonella in the intestine of broiler chickens (Rubel et al 2019). In contrast to the antibacterial effect, microalgae Spirulina and Chlorella may be used as prebiotics that can increase the populations of the beneficial microorganisms in the intestine of broiler chickens. The latter conditions may beneficially improve the intestinal health, functions and ecology/morphology that in turn improve the digestion and absorption of nutrients (Sugiharto 2016). The study by Kang et al (2013) showed that feeding Chlorella increased the population of lactic acid bacteria in the intestine of broiler chickens. Likewise, Janczyk et al (2009) noticed the increased numbers ofLactobacilli spp. in the crop and caecum of layers by feedingChlorella vulgaris. Moreover, dietary incorporation of fermented Chlorella vulgaris increased the number of lactic acid bacteria in the caecum of laying hens (Zheng et al 2012). Furthermore, Kang et al (2016) noticed the increased counts of Lactobacillus and decreased E. coli and Salmonella in the caecal digesta of broilers fed Chlorella by‐product. In line with Chlorella, dietary supplementation of Spirulina platensis increased the populations of lactic acid bacteria and yeast in the intestine of broilers (Sugiharto et al 2018). Feeding microalga Spirulina platensis has also been reported to increase the numbers of Lactobacillus in the intestine (Fathi et al 2018) and caecum of broiler chickens (Park et al 2018). In Japanese quails, the microalgae Spirulina supplementation also increased the population of Lactobacilli in the intestine (Yusuf et al 2016). In support to the in vivo study an in vitro study also showed the growth-promoting effect of Spirulina platensis onLactobacillus acidophilus (Bhowmik et al 2009),Lactococcus lactis, Streptococcus thermophilus, Lactobacillus casei, Lactobacillus acidophilus and Lactobacillus bulgaricus (Gupta et al 2017).
To function as prebiotics, the components such as microalgae must be able to support the growth of the beneficial bacteria particularly in the host intestine (Sugiharto 2016). Recently, Abdelnour et al (2019) suggested that the high contents of fibrous wall materials (β-glucans) and chlorophyll in the microalgae may provide substrates for the growth of lactic acid bacteria. The latter authors further suggested that phloroglucinol and apigenin may also promote the growth of beneficial bacteria in the intestine of animals. Apart from the antibacterial activities (against pathogenic microorganisms), phenolic compounds in the microalgae Spirulina and Chlorella may also act to support the growth of probiotic microorganisms that are favourable for the health of broiler chickens (Finamore et al 2017).
Antioxidant properties of microalgae Spirulina and Chlorella for broilers
Stress is one of the main factors affecting the health and productivity of poultry. To alleviate the detrimental effect of stress, poultry farmers have commonly used synthetic antioxidants. Yet, the latter practice may pose to carcinogenic effects on the consumers when used at an excessive extent (Sugiharto 2019). In this concern, the search for the natural-based antioxidants may be crucial. Besides plants and herb preparations, microalgae Spirulina and Chlorella have been used as natural antioxidants for poultry. A recent study by Mirzaie et al (2018) showed that Spirulina platensis may be used to alleviate the adverse effect of heat stress in broiler chickens. In the latter study, feeding Spirulina platensis decreased the concentration of corticosterone and increased the levels of antioxidant enzymes (i.e., superoxide dismutase and glutathione peroxidase) in broilers exposed to heat stress, and hence the oxidative damage may be avoided as reflected by the decreased malondialdehyde (MDA) levels in serum. In line with this, Zeweil et al (2016) also documented that feeding Spirulina platensis increased the tissue levels of glutathione peroxidase and decreased MDA of broiler chickens. Also, Fathi et al (2018) noticed that dietary inclusion of Spirulina platensis decreased the heterophils to lymphocyte (H/L) ratio of broiler chickens, which is the indicator of stress condition in vertebrate animals. Moreover, feeding Spirulina ( Arthrospira) platensis remarkably increased the serum activities of superoxide dismutase and glutathione peroxidase enzymes (Park et al 2018). With regard to Chlorella, Subhani et al (2018) reported that dietary supplementation of Chlorella pyrenoidosa increased total antioxidant capacity (TAC) and catalase activity in the liver of broiler chickens. In line with this, El-Abd et al (2018) reported that dietary inclusion of Chlorella vulgaris decreased the serum level of MDA.
A number of factors may contribute to the antioxidative activities of microalgae Spirulina and Chlorella in broiler chickens, including β-carotene, astaxanthin, lutein, bioactive peptides, phenolic compounds, phycocyanin and sulfated polysaccharides (Barkia et al 2019). Also, lycopene and phycobiliproteins in the microalgae may serve as antioxidant agents that could neutralize the excessive free radicals and thus prevent oxidative damage (Bhalamurugan et al 2018). Furthermore, Moradi kor et al (2016) pointed out that Chlorella may increase selenium level in the blood and thereby improve the antioxidative status of chickens.
Growth-promoting properties of microalgae Spirulina and Chlorella for broilers
The global retraction of antibiotics from broiler diets has enforced poultry nutritionists to search the alternatives for growth-promoting agents for broiler chickens. Many alternatives have actually been proposed, one of which is microalgae Spirulina and Chlorella. Feeding Spirulina has been reported to improve the growth performance of broiler chickens in the studies of Jamil et al (2015), Kaoud (2015), Abou-Zeid et al (2015), Shanmugapriya et al (2015), El-Hady and El-Ghalid (2018), Fathi et al (2018), Park et al (2018) and Kumari et al (2019). In accordance, Chlorella supplementation has been attributed to the improved growth performance of broiler chickens in the studies of Han et al (2002), Zheng et al (2012), Kang et al (2013), Abou-Zeid et al (2015), An et al (2016) and Rubel et al (2019). The definite reasons by which the microalgae improved the growth performance of broiler chickens are largely unknown, but some possible mechanisms could be proposed. Microalgae Spirulina may improve the development and morphological structure of the digestive tract resulting in increased apparent total tract digestibility of dry matter and protein (Park et al 2018). This may consequently improve the growth performance of broilers. It has also been suggested that dietary Spirulina supplementation improved the microbial balance in the intestine resulting in better digestion and nutrient absorption by broiler chickens (El-Hady and El-Ghalid 2018). Similar with this, Kang et al (2013) noted that Chlorella accelerated the growth and development of the digestive tract of the young chicks, which hence improved the nutrient digestion and utilization of chicks at the later age. Feeding Chlorella may also improve the morphology of the intestines, such as increased villus height (Kang et al 2016), leading to the increased area of nutrient absorption by the chicks.
Recently, El-Abd et al (2018) reported that feeding Chlorella vulgaris increased the concentration of haemoglobin of broiler chickens. Considering the function of haemoglobin in transporting oxygen for cellular metabolism (energy production), the increased haemoglobin concentration may consequently increase the growth rate of broiler chickens. Moreover, the improved antioxidative and health status when feeding microalgae Chlorella or Spirulina) may also help to promote the growth rate of broilers (by alleviating the energy used for maintenance and recovery) (Kang et al 2013; 2016; El-Abd et al 2018; Abdelnour et al 2019). Also, the presences of some essential amino acids in Spirulina (El-Hady and El-Ghalid 2018) and growth promoting components in the Chlorella such as S-nucleotide adenosyl peptide complex (Han et al 2002) seem to positively affect the digestibility and growth performance of broiler chickens.
Therapeutic properties of microalgae Spirulina and Chlorella for broilers
Besides being used as a food/feed ingredient, the microalgae Spirulina and Chlorella have been documented to have a therapeutic potential for humans (Sigamani et al 2016; Barkia et al 2019). In broiler chickens, Chlorella pyrenoidosa has been exploited to counteract the hepatotoxic impacts of Aflatoxin B1 (Subhani et al 2018). With regard to Spirulina, the study assessing the therapeutic effect of such microalga on broiler chickens is not available in the literature, but a study in ducks showed that feeding Spirulina may alleviate the toxic effect of arsenic. The therapeutic mechanisms of microalgae Spirulina and Chlorella have not been definitely explained, but the presence of some bioactive constituents such as phycocyanin, active peptides, linolenic acid, carotene, tocopherols and phenolic compounds seemed to exert pharmaceutical effects of the microalgae (Sigamani et al 2016; Barkia et al 2019). Overall, the therapeutic properties of microalgae Spirulina and Chlorella need to be intensively explored.
Microalgae Spirulina and Chlorella can improve the growth performance of broiler chickens.
The microalgae may also improve immune responses, intestinal morphology and the microbial ecosystem and antioxidative status of broilers.
The microalgae Spirulina and Chlorella may serve as therapeutic agents for broiler chickens.
Abdelnour S A, Abd El-Hack M E, Arif M, Khafaga A F and Taha A E 2019 The application of the microalgae Chlorella spp. as a supplement in broiler feed. World’s Poultry Science Journal, 75, 305-318. https://doi.org/10.1017/S0043933919000047
Abou-Zeid A E, El-Damarawy S Z, Mariey Y A and El-Mansy M M 2015 Effect of using Spirulina platensis and/or Chlorella vulgaris algae as feed additives on productive performance of broiler chicks. Journal of Animal and Poultry Production Mansoura University, 6, 623-634.
Alvarenga R R, Rodrigues P B, Cantarelli V, Zangeronimo M G, Da Silva Junior J W, Da Silva L R, Dos Santos L M and Pereira L J 2011 Energy values and chemical composition of spirulina ( Spirulina platensis) evaluated with broilers. Brazilian Journal of Animal Science, 40, 992-996. https://doi.org/10.1590/S1516-35982011000500008
An B-K, Kim K-E, Jeon J-Y and Lee K W 2016 Effect of dried Chlorella vulgaris and Chlorella growth factor on growth performance, meat qualities and humoral immune responses in broiler chickens. SpringerPlus. 5, 718. https://doi.org/10.1186/s40064-016-2373-4
Barkia I, Saari N and Manning S R 2019 Microalgae for high-value products towards human health and nutrition. Marine Drugs, 17, 304. https://doi.org/10.3390/md17050304
Beheshtipour H, Mortazavian A M, Mohammadi R, Sohrabvandi S and Khosravi - Darani K 2013 Supplementation of Spirulina platensis and Chlorella vulgaris Algae into probiotic fermented milks. Comprehensive Reviews in Food Science and Food Safety, 12, 144-154. https://doi.org/10.1111/1541-4337.12004
Bhalamurugan G L, Valerie O and Mark L 2018 Valuable bioproducts obtained from microalgal biomass and their commercial applications: A review. Environmental Engineering Research, 23, 229-241. https://doi.org/10.4491/eer.2017.220
Bhowmik D, Dubey J and Mehra S 2009 Probiotic efficiency of Spirulina platensis - stimulating growth of lactic acid bacteria. World Journal of Dairy & Food Science, 4, 160-163.
Devi M A, Subbulakshmi G, Devi K M and Venkataraman L V 1981 Studies on the proteins of mass-cultivated, blue-green alga ( Spirulina platensis). Journal of Agricultural and Food Chemistry, 29, 522-525. https://doi.org/10.1021/jf00105a022
El-Abd N M and Hamouda R A E 2017 Improved productivity and health of broiler chicken by micro green alga Chlorella vulgaris. Asian Journal of Poultry Science, 11, 57-63. https://doi.org/10.3923/ajpsaj.2017.57.63
El-Hady A M A and El-Ghalid O A H 2018 Spirulina platensis Algae (SPA): A novel poultry feed additive. Effect of SPA supplementation in broiler chicken diets on productive performance, lipid profile and calcium-phosphorus metabolism. 6th Mediterranean Poultry Summit, Torino, Italy, 18-20 June 2018.
Fathi M A, Namra M M M, Ragab M S and Aly M M M 2018 Effect of dietary supplementation of algae meal ( Spirulina platensis) as growth promoter on performance of broiler chickens. Egyptian Poultry Science, 38, 375-389.
Finamore A, Palmery M, Bensehaila S and Peluso I 2017 Antioxidant, immunomodulating, and microbial-modulating activities of the sustainable and ecofriendly Spirulina. Oxidative Medicine and Cellular Longevity, http://dx.doi.org/10.1155/2017/3247528
Gupta S, Gupta C, Garg A P and Prakash D 2017 Prebiotic efficiency of blue green algae on probiotics microorganisms. Journal of Microbiology and Experimentation, 4, 00120. http://dx.doi.org/10.15406/jmen.2017.04.00120
Han J G, Kang G G, Kim J K and Kim S H 2002 The present status and future of Chlorella. Food Science and Indusrty, 6, 64-69.
Holman B W B and Malau-Aduli A E O 2013 Spirulina as a livestock supplement and animal feed. Journal of Animal Physiology and Animal Nutrition, 97, 615-623. https://doi.org/10.1111/j.1439-0396.2012.01328.x
Hussein J H, Naji S S and Al-Khafaji N M S 2018 Antibacterial properties of the Chlorella vulgaris isolated from polluted water in Iraq. Journal of Pharmaceutical Sciences and Research, 10, 2457-2460.
Islam M S, Awal M A, Mostofa M, Begum F, Khair A and Myenuddin M 2009 Effect of Spirulina on biochemical parameters and reduction of tissue arsenic concentration in arsenic induced toxicities in ducks. International Journal of Poultry Science, 8, 69-74. https://doi.org/10.3923/ijps.2009.69.74
Iwasa M, Yamamoto M, Tanaka Y, Kaito M and Adachi Y 2002 Spirulina associated hepatotoxicity. The American Journal of Gastroenterology, 97, 3212-3213. https://doi.org/10.1111/j.1572-0241.2002.07145.x
Jamil A B M R, Akanda R, Rahman M, Hossain A and Islam S 2015 Prebiotic competence of spirulina on the production performance of broiler chickens. Journal of Advanced Veterinary and Animal Research, 2, 304-309. http://dx.doi.org/10.5455/javar.2015.b94
Janczyk P, Halle B and Souffrant W B 2009 Microbial community composition of the crop and ceca contents of laying hens fed diets supplemented with CLV vulgaris. Poultry Science, 88, 2324-2332. http://dx.doi.org/10.3382/ps.2009-00250
Kang H K, Park S B and Kim C H 2017 Effects of dietary supplementation with a chlorella by-product on the growth performance, immune response, intestinal microflora and intestinal mucosal morphology in broiler chickens. Journal of Animal Physiology and Animal Nutrition, 101, 208-214. https://doi.org/10.1111/jpn.12566
Kang H K, Salim H M, Akter N, Kim D W, Kim J H, Bang H T, Kim M J, Na J C, Hwangbo J, Choi H C and Suh O S 2013 Effect of various forms of dietary Chlorella supplementation on growth performance, immune characteristics, and intestinal microflora population of broiler chickens. Journal of Applied Poultry Research, 22, 100-108. https://doi.org/10.3382/japr.2012-00622
Kaoud H A 2012 Effect of Spirulina platensis as a dietary supplement on broiler performance in comparison with prebiotics. Scientific Journal of Applied Research, 1, 44-48.
Karkos P D, Leong S C, Karkos C D, Sivaji N and Assimakopoulos D A 2011 Spirulina in clinical practice: evidence-based human applications. Evidence-Based Complementary and Alternative Medicine. https://doi.org/10.1093/ecam/nen058
Kumari P, Nehra V, Lather D, Kundu P and Narang G 2019 Effect of Spirulina on growth and bursal index of infectious bursal disease vaccinated chickens. Haryana Veterinarian, 58, 70-72.
Kwak J H, Baek S H, Woo Y, Han J K, Kim B G, Kim O Y and Lee J H 2012 Beneficial immunostimulatory effect of short-term Chlorella supplementation: enhancement of Natural Killer cell activity and early inflammatory response (Randomized, double-blinded, placebo-controlled trial). Nutrition Journal, 11: 53. http://www.nutritionj.com/content/11/1/53
Lokapirnasari W P, Yulianto A B, Legowo D and Agustono 2016 The effect of Spirulina as feed additive to myocardial necrosis and leukocyte of chicken with avian influenza (H5N1) virus infection. Procedia Chemistry, 18, 213-217. https://doi.org/10.1016/j.proche.2016.01.033
Mirzaie S, Zirak-Khattab F, Hosseini S A and Donyaei-Darian H 2018 Effects of dietary Spirulina on antioxidant status, lipid profile, immune response and performance characteristics of broiler chickens reared under high ambient temperature. Asian Australasian Journal of Animal Sciences, 31, 556-563. https://doi.org/10.5713/ajas.17.0483
Moradi kor N, Akbari M and Olfati A 2016 The effects of different levels of Chlorella microalgae on blood biochemical parameters and trace mineral concentrations of laying hens reared under heat stress condition. International Journal of Biometeorology, 60, 757-762. https://doi.org/10.1007/s00484-015-1071
Park J H, Lee S I and Kim I H 2018 Effect of dietary Spirulina (Arthrospira) platensis on the growth performance, antioxidant enzyme activity, nutrient digestibility, cecal microflora, excreta noxious gas emission, and breast meat quality of broiler chickens. Poultry Science, 97, 2451-2459. http://dx.doi.org/10.3382/ps/pey093
Qureshi M A, Garlich J D and Kidd M T 1996 Dietary Spirulina platensis enhances humoral and cell-mediated immune functions in chickens. Immunopharmacology and Immunotoxicology, 18, 465-476. https://doi.org/10.3109/08923979609052748
Rezvani M, Shivazad M, Zaghari M and Moravej H 2012 A survey on Chlorella vulgaris effect’s on performance and cellular immunity in broilers. International Journal of Agricultural Science and Research, 3, 9-15.
Roy-Lachapelle A, Solliec M, Bouchard M F and Sauvé S 2017 Detection of cyanotoxins in algae dietary supplements. Toxins, 9m 76. https://doi.org/10.3390/toxins9030076
Rubel Md Z U, Beg Md A H, Begum M and Anjum N 2019 Effects of dietary supplement of dried Chlorella powder as an alternative to antibiotic on growth performance and health status of broiler chicken. International Journal of Biosciences, 14, 255-263. http://dx.doi.org/10.12692/ijb/14.4.255-263
Seyidoglu N, Galip N, Budak F and Uzabaci E 2017 The effects of Spirulina platensis (Arthrospira platensis) and Saccharomyces cerevisiae on the distribution and cytokine production of CD4+ and CD8+ T-lymphocytes in rabbits. Austral Journal of Veterinary Sciences, 49, 185-190. http://australjvs.cl/index.php/amv/article/view/601
Shanmugapriya B, Babu S S, Hariharan T, Sivaneswaran S, Anusha M B and Raja P U 2015 Synergistic effect of Spirulina platensis on performance and gut microbial load of broiler chicks. Indo - Asian Journal of Multidisciplinary Research, 1, 149-155.
Sharoba A M 2014 Nutritional value of spirulina and its use in the preparation of some complementary baby food formulas. Journal of Agroalimentary Processes and Technology, 20, 330-350.
Sigamani S, Ramamurthy D and Natarajan H 2016 A review on potential biotechnological applications of microalgae. Journal of Applied Pharmaceutical Science, 6, 179-184. https://doi.org/10.7324/JAPS.2016.60829
Soni R A, Sudhakar K, Rana R S 2017 Spirulina-From growth to nutritional product: A review. Trends in Food Science & Technology, 69, 157-171. https://doi.org/10.1016/j.tifs.2017.09.010
Subhani Z, Shahid M, Hussain F and Khan J A 2018 Efficacy of Chlorella pyrenoidosa to ameliorate the hepatotoxic effects of Aflatoxin B1 in broiler chickens. Pakistan Veterinary Journal, 38, 13-18. https://doi.org/10.29261/pakvetj/2018.003
Sugiharto S 2016 Role of nutraceuticals in gut health and growth performance of poultry. Journal of the Saudi Society of Agricultural Sciences, 15, 99-111. https://doi.org/10.1016/j.jssas.2014.06.001
Sugiharto S 2019 A review of filamentous fungi in broiler production. Annals of Agricultural Sciences, 64, 1-8. https://doi.org/10.1016/j.aoas.2019.05.005
Sugiharto S and Lauridsen C 2016 Dietary Chlorella supplementation effect on immune responses and growth performances of broiler chickens exposed to post hatch holding time. Livestock Research for Rural Development, 28(7). http://www.lrrd.org/lrrd28/7/sugi28119.html
Sugiharto S and Ranjitkar S 2019 Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology and immune responses: A review. Animal Nutrition, 5, 1-10. https://doi.org/10.1016/j.aninu.2018.11.001
Sugiharto S, Henckel P and Lauridsen C 2010 Fatty acids profile of meat, mucosal sIgA concentration and production index of broiler as a response to Chlorella sp. administration in the diet. Journal of the Indonesian Tropical Animal Agriculture, 35, 172-178. https://doi.org/10.14710/jitaa.35.3.172-178
Sugiharto S, Yudiarti T, Isroli I and Widiastuti E 2018 Effect of feeding duration of Spirulina platensis on growth performance, haematological parameters, intestinal microbial population and carcass traits of broiler chicks. South African Journal of Animal Science, 48, 98-107. http://dx.doi.org/10.4314/sajas.v48i1.12
Yusuf M S, Hassan M A, Abdel-Daim M M, El Nabtiti A S, Ahmed A M, Moawed S A, El-Sayed A K and Cui H 2016 Value added by Spirulina platensis in two different diets on growth performance, gut microbiota, and meat quality of Japanese quails, Veterinary World, 9, 1287-1293. http://dx.doi.org/10.14202/vetworld.2016.1287-1293
Zeweil H, Abaza I M, Zahran S M, Ahmed M H, AboulEla H M, Saad A A 2016 Effect of Spirulina platensis as dietary supplement on some biological traits for chickens under heat stress condition. Asian Journal of Biomedical and Pharmaceutical Sciences, 6, 8-12.
Zheng L, Oh S T, Jeon J Y, Moon B H, Kwon H S, Lim S U, An B K and Kang C W 2012 The dietary effects of fermented Chlorella vulgaris (CBT) on production performance, liver lipids and intestinal microflora in laying hens. Asian Australasian Journal of Animal Sciences, 25, 261-266. http://dx.doi.org/10.5713/ajas.2011.11273
20 views0 comments