Veterinary World

     Open access and peer reviewed journal  

ISSN (Online): 2231-0916


Home l Editorial board l Instructions for authors l Reviewer guideline l Open access policy l Archives l FAQ

Open Access

Research (Published online: 23-11-2016)

20. Value added by Spirulina platensis in two different diets on growth performance, gut microbiota, and meat quality of Japanese quails - Mohamed S. Yusuf, Marwa A. Hassan, Mohamed M. Abdel-Daim, Adel S. El nabtiti, Ali Meawad Ahmed, Sherief A. Moawed, Ahmed Kamel El-Sayed and Hengmi Cui

Veterinary World, 9(11): 1287-1293



   doi: 10.14202/vetworld.2016.1287-1293


Mohamed S. Yusuf: Institute of Epigenetics and Epigenomics, Yangzhou University, Yangzhou, 225009 Jiangsu, China; Department of Nutrition and Clinical Nutrition, Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Marwa A. Hassan: Department of Animal Hygiene, Zoonoses and Behavior, Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Mohamed M. Abdel-Daim: Department of Pharmacology, Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Adel S. El nabtiti: Department of Animal Wealth Development, Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Ali Meawad Ahmed: Department of Food Hygiene, Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Sherief A. Moawed: Department of Animal Wealth Development, (Biostatistics) Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Ahmed Kamel El-Sayed: Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Suez Canal University, 41522 Ismailia, Egypt;

Hengmi Cui: Institute of Epigenetics and Epigenomics, Yangzhou University, Yangzhou, 225009 Jiangsu, China;


Received: 06-08-2016, Accepted: 14-10-2016, Published online: 23-11-2016


Corresponding author: Hengmi Cui, e-mail:

Citation: Yusuf MS, Hassan MA, Abdel-Daim MM, El nabtiti AS, Ahmed AM, Moawed SA, El-Sayed AK, 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(11): 1287-1293.

Aim: The growth promoting effect of the blue-green filamentous alga Spirulina platensis (SP) was observed on meat type Japanese quail with antibiotic growth promoter alternative and immune enhancing power.

Materials and Methods: This study was conducted on 180 Japanese quail chicks for 4 weeks to find out the effect of diet type (vegetarian protein diet [VPD] and fish meal protein diet [FMPD])- Spirulina dose interaction (1 or 2 g/kg diet) on growth perfor-mance, gut microbiota, and sensory meat quality of growing Japanese quails (1-5 weeks old).

Results: Data revealed improvement (p<0.05) of weight gain, feed conversion ratio and European efficiency index due to 1, 2 g (SP)/kg VPD, and 2 g (SP)/kg FMPD, respectively. There was a significant decrease of ileum mean pH value by 1 g (SP)/kg VPD. Concerning gut microbiota, there was a trend toward an increase in Lactobacilli count in both 1; 2 g (SP)/kg VPD and 2 g (SP)/kg FMPD. It was concluded that 1 or 2 g (SP)/kg vegetarian diet may enhance parameters of performance without obvious effect on both meat quality and gut microbiota. Moreover, 1 and/or 2 g (SP) may not be invited to share fish meal based diet for growing Japanese quails.

Conclusion: Using of SP will support the profitable production of Japanese quails fed vegetable protein diet.

Keywords: isocaloric, isonitrogenous, meat quality, performances, quails, spirulina.

1. Franciosini, M.P., Casagrande-Proietti, P., Forte, C., Beghelli, D., Acuti, G., Zanichelli, D., Bosco, A., Castellini, C. and Trabalza-Marinucci, M. (2016) Effects of oregano (Origanum vulgare L.) and rosemary (Rosmarinus officinalis L.) aqueous extracts on broiler performance, immune function and intestinal microbial population. J. Appl. Anim. Res., 44(1): 474-479.
2. Frehner, M. Paulus, C. Philipps, P. and Gadient, M. (2015) Use of Organic Acids and Essential Oils in Animal feeding, Google Patents.
3. Yusuf, M.S., Nabtiti, A.S.E. and Cui, H. (2016) Effects of NENP vs LELP diets on some laying and reproductive performance parameters of Japanese Quail's hens. J. Adv. Agric. Technol., 3(2): 132-135.
4. Hassan, M.A., Yusuf, M.S., Kilany, O.E., Khalil, H. A., Hanafy, A.M. and Hassan, A.M. (2015) Evaluation of essential oil mixture overuse on gut health and some immune parameters in laying Japanese Quail (Coturnix Coturnix japonica). Int. Proc. Chem. Biol. Environ. Eng., 89: 14-22.
5. Khan, Z., Bhadouria, P. and Bisen, P. (2005) Nutritional and therapeutic potential of Spirulina. Curr. Pharm. Biotechnol., 6(5): 373-379.
6. Thormar, H. (2012) Patented non-antibiotic agents as animal feed additives. Rec. Pat. Food Nutr. Agric., 4(2): 155-168.
7. Huili, W., Xiaokai, Z., Meili, L., Dahlgren, R.A., Wei, C., Jaiopeng, Z., Chengyang, X., Chunlei, J., Yi, X., Xuedong, W., Li, D. and Qiyu, B. (203) Proteomic analysis and qRT-PCR verification of temperature response to Arthrospira (Spirulina) platensis. PLoS One, 8(12): e83485.
PMid:24349519 PMCid:PMC3861494
8. Abdel-Daim, M.M. (2014) Pharmacodynamic interaction of Spirulina platensis with erythromycin in Egyptian Baladi bucks (Capra hircus). Small Rumin. Res., 120(2): 234-41.
9. Alvarenga, R.R., Rodrigues, P.B., Cantarelli, V.S., Zangeronimo, M.G., Silva, J.W.Jr., Silva, L.R., Santos, L.M., Pereira, L.J. and Ribeiro, R. (2011) Energy values and chemical composition of Spirulina (Spirulina platensis) evaluated with broilers. Rev. Bras. Zootec., 40(5): 992-996.
10. Shanmugapriya, B., Babu, S.S., Hariharan, T., Sivaneswaran, S. and Anusha, M.B. (2015) Dietary administration of Spirulina platensis as probiotics on growth performance and histopathology in broiler chicks. Int. J. Rec. Sci. Res., 6(2): 2650-3.
11. El-Tarabany, M.S. (2015) Impact of temperature-humidity index on egg-laying characteristics and related stress and immunity parameters of Japanese quails. Int. J. Biometeorol., 60(7): 957-964.
12. NRC. (1994) Nutrient Requirements of Poultry. 9th ed. National Academy Press, Washington, DC.
13. Filho, J., da Silva, J.H.V., Costa, F.G.P., Albino, L.F.T., Melo, T.S., de Lacerda, P.B., Dantas, G.M., Soares, R.P. (2012) Requirement for maintenance and gain of crude protein for two genotypes of growing quails. Rev. Bras. Zootec., 41: 2048-2054.
14. García-Ortega, A., Kissinger, K.R. and Trushenski, J.T. (2016) Evaluation of fish meal and fish oil replacement by soybean protein and algal meal from Schizochytrium limacinum in diets for giant grouper Epinephelus lanceolatus. Aquaculture, 452: 1-8.
15. Levine, R.B. and Horst, G.P. (2015) method for improving feed efficiency and increasing growth rates in animals. Us Patent 20,150,181,909.
16. Commision, E., (2001) 2nd Opinion on Anti-Microbial Resistance. Available from: out203_en.pdf. [Last cited on 2009 Feb 11].
17. Kaoud, H.A. (2015) Effect of Spirulina platensis as a dietary supplement on broiler performance in comparison with prebiotics. Sci. Arena Publ. Spec. J. Biol. Sci., 1(2): 1-6.
18. 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 J. Multidisc. Res., 1(2): 149-155.
19. Kumar, V., Tirumalai, P.S., Singh, A., Bhatnagar, A.K., Shrivastavaet, J.N. (2013) Natural compounds from algae and Spirulina platensis & its antimicrobial activity. Indo Glob. J. Pharm. Sci., 3(3): 212-223.
20. Ramadan, M.F., Selim, M., Asker, M. and Zeinab, K.L. (2008) Functional bioactive compounds and biological activities of Spirulina platensis lipids. Czech. J. Food Sci., 26(3): 211-226.
21. Sarada, D.V.L., Kumar, C.H. and Rengasamy, R. (2011) Purified Cphycocyanin from Spirulina platensis (Nordstedt) geitler: A novel and potent agent against drug resistant bacteria. World J. Microbiol. Biotechnol., 27: 770-783.
22. Challouf, R., Rafika, C., Lamia, T., Rym, B.D., Omeya, E.A., Ali, Y., Khamissa, G., Jihen, B.A., Hela, O. and Ouada, H.B. (2011) Evaluation of cytotoxicity and biological activities in extracellular polysaccharides released by cyanobacterium Arthospira platensis. Braz. Arch. Biol. Technol., 54(4): 831-838.
23. Kulandaivel, S., Prakash, R., Anitha, R. and Arunnagendran, N. (2007) Antibacterial activity of Spirulina platensis and Oscillatoria sp. J. Plant Appl. Microbiol., 1(1): 127-129.
24. Mala, R., Sarijini, M., Saravanababu, S. and Umadevi, G. (2009) Screening for antimicrobial activity of crude extracts of Spirulina platensis. J. Cell Tissue Res., 93(3): 1951-1955.
25. Sudha, S.S. R. Karthic, J. Rengaramanujam and Athulya (2011) Antimicrobial activity of Spirulina platensis and Aphanothece sp. on selected clinical bacterial isolates and its Antioxidant activity. South Asian J. Biol. Sci., 1: 87-98.
26. Pradhan, J., Das, B.K., Sahu, S., Marhual, N.P., Swain, A.K., Mishra, B.K. and Eknath, A.E. (2012) Traditional antibacterial activity of freshwater microalga Spirulina platensis to aquatic pathogens. Aqua Res., 43(9): 1287-1295.
27. Rania, M.A.A. and Taha, H.M. (2008) Antibacterial and antifungal activity of cyanobacteria and green microalgae. Evaluation of medium components by placket-burman design for antimicrobial activity of Spirulina platensis. Glob. J. Biotechnol. Biochem., 3(1): 22-31.
28. Sivakumar, J. and Santhanan, P. (2011) Antipathogenic activity of Spirulina platensis. Rec. Res. Sci. Technol., 3(4): 158-161.
29. Yusuf, M.S., Mahmoud, M.M.A., Samy, H.M. and Ibrahim, M.T. (2014) Effect of lactose, yeast and organic acids mixture supplementation on laying performance of Japanese quails (Coturnix coturnix japonica). Glob. Anim. Sci. J., 2(1): 123-138.
30. Babadzhanov, A.S., Abdusamatova, N., Yusupova, F.M., Fayzullavea, N., Ezhlumyan, L.G. and Mailkova, M.K. (2004) Chemical composition of Spirulina platensis cultivated in Uzbekistan. Chem. Nat. Compd., 40(3): 276-279.
31. Mata, T.M., Martins, A.A. and Caetano, N.S. (2010) Microalgae for biodiesel production and other applications: A review. Renew. Sustain. Energy Rev., 14(1): 217-232.
32. Sánchez, M., Bernal-Castillo, J., Van Niel, J., Rozo, C. and Rodríguez, I. (2003) Spirulina (Arthrospira): An edible microorganism: A review. Univ. Sci., 8(1): 7-24.
33. Yamani, K., Rashwan, A. and Magdy, M. (1997) Effects of copper, zinc and tafla dietary supplementation on broiler performance. In: International Conference on Animal, Poultry, Rabbit Production and Health, Cairo, (Egypt). p2-4.
34. Demeterová, M. (2009) Performance of chickens fed diets containing full-fat soybean and natural humic compounds. In Folia Veterinaria. University of Veterinary Medicine.
35. Al-Natour, M.Q. and Alshawabkeh, K.M. (2005) Using varying levels of formic acid to limit growth of Salmonella gallinarum in contaminated broiler feed. Asian Aust. J. Anim. Sci., 18(3): 390-395.
36. Khaldari, M., Pakdel, A., Yegane, H.M., Javaremi, A.N. and Berg, P. (2010) Response to selection and genetic parameters of body and carcass weights in Japanese quail selected for 4-week body weight. Poult. Sci., 89(9): 1834-1841.
37. Hassan, M.A., Yusuf, M.S., Kilany, O.E., Khalil, H.A., Hanafy, A.M. and Hassan, A.M. (2015) Evaluation of Essential Oil Mixture Overuse on Gut Health and Some Immune Parameters in Laying Japanese Quail (Coturnix Coturnix japonica).
38. Herigstad, B., Hamilton, M. and Heersink, J. (2001) How to optimize the drop plate method for enumerating bacteria. J. Microbiol. Methods, 44(2): 121-129.
39. Snedecor, G.W. and Cochran, W.G. (1989) Statistical Methods. 8th ed. Iowa State University Press, Ames. p503.
40. Duncan, D.B. (1955) Multiple range and multiple F Tests. Biometrics, 11(1): 1-42.
41. Kaur, S., Mandal, A.B., Singh, K.B. and Kadam, M.M. (2008) The response of Japanese quails (heavy body weight line) to dietary energy levels and graded essential amino acid levels on growth performance and immuno-competence. Livest. Sci., 117(2): 255-262.
42. Varkoohi, S., Moradi Shahr Babak, M., Pakdel, A., Nejati Javaremi, A., Zaghari, M. and Kause, A. (2010) Response to selection for feed conversion ratio in Japanese quail. Poult. Sci., 89(8): 1590-1598.
43. Nikodémusz, E., Páskai, P., Tóth, L. and Kozák, J. (2010) Effect of dietary Spirulina supplementation on the reproductive performance of farmed pheasants. Technical Articles-Poultry Industry, p1-2.
44. Toyomizu, M., Sato, K., Taroda, H., Kato, T. and Akiba, Y. (2001) Effects of dietary Spirulina on meat colour in muscle of broiler chickens. Br. Poult. Sci., 42(2): 197-202.
45. Ross, E. and Dominy, W. (1990) The nutritional value of dehydrated, blue-green algae (Spirulina plantensis) for poultry. Poult. Sci., 69(5): 794-800.
46. Holman, B. and Malau-Aduli, A. (2013) Spirulina as a livestock supplement and animal feed. J. Anim. Physiol. Anim. Nutr., 97(4): 615-623.
47. Hossain, M., Bhuiyan, M. and Iji, P. (2015) Nutritive value of vegetable protein diets for broiler chickens and selection of diets containing different vegetable or animal proteins. World's Poult. Sci. J., 71(01): 15-26.
48. Razafindrajaona, J. Rakotozandriny, JN, Rakotozandrindrainy, R, Tsivingaina, A, Ramapiherika, KD and Randria, J (2008) Influence de l'incorporation dans les provendes de la spiruline de Madagascar (Spirulina platensis var. Toliarensis) sur la croissance des poulets de chair. In: International Symposium on Spirulina - Toliara Sud-Ouest de Madagascar.
49. Alali, W., Hofacre, C.L., Mathis, G.F. and Batal, A.B. (2011) Effect of plant-based protein meal use in poultry feed on colonization and shedding of Salmonella Heidlberg in broiler birds. Agric. Food Anal. Bacteriol. J., 1: 45-53.
50. Radhakrishnan, L., Kadirvel, R. and Vijayakumar, R. (2001) Replacement of fishmeal with vegetable protein sources in broiler diets. Indian J. Poult. Sci., 36(3): 300-304.
51. Li, E. and Anderson, G. (1983) Amino acids in the regulation of food intake. Nutr Abstr Rev Clin Nutr. 53: 171-181.
52. Rogers, Q. and Leung, P. (1973) The influence of amino acids on the neuroregulation of food intake. Fed. Proc., 2: 1709-1719.
53. Acar, N., Patterson, P. and Barbato, G. (2001) Appetite suppressant activity of supplemental dietary amino acids and subsequent compensatory growth of broilers. Poult. Sci., 80(8): 1215-1222.
54. Pimentel, D. and Pimentel, M. (2003) Sustainability of meat-based and plant-based diets and the environment. Am. J. Clin. Nutr., 78(3): 660S-663S.
55. Edmonds, M.S. and Baker, D.H. (1987) Comparative effects of individual amino acid excesses when added to a corn-soybean meal diet: Effects on growth and dietary choice in the chick. J. Anim. Sci., 65(3): 699-705.
56. Latshaw, J. (1993) Dietary lysine concentrations from deficient to excessive and the effects on broiler chicks. Br. Poult. Sci., 34(5): 951-958.
57. Ozdemir, G., Karabey, N.U., Dalay, M.C. and Pazarbasi, S. (2004) Antibacterial activity of volatile component and various extracts of Spirulina platensis. Phytother. Res., 18(9): 754-757.
58. Kim, D.H., Park, M.H., Choi, Y.J., Chung, K.W., Park, C.H., Jang, E.J., An, H.J., Yu, B.P. and Chung, H.Y. (2013) Molecular study of dietary heptadecane for the anti-inflammatory modulation of NF-kB in the aged kidney. PLoS One, 8(3): e59316.
59. Yuan, J.H. and Austic, R. (2001) The effect of dietary protein level on threonine dehydrogenase activity in chickens. Poult. Sci., 80(9): 1353-1356.
60. Nelson, D.L. and Cox, M.M. (2011) Princípios de bioquímica de lehninger. In: Principios de Bioquimica de Lehninger. Artmed, Porto Alegre.
61. Singh, K.S. and Panda, B. (1992) Poultry Nutrition. Kalyani Publishers, New Delhi, India. p57-61.
62. Thongsong, B., Kalandakanond-Thongsong, S. and Chavananikul, V. (2008) Effects of the addition of probiotic containing both bacteria and yeast or an antibiotic on performance parameters, mortality rate and antibiotic residue in broilers. Thai J. Vet. Med., 38(1): 17-26.
63. Bhowmik, D., Dubey, J. and Mehra, S. (2009) Probiotic efficiency of Spirulina platensis - Stimulating growth of lactic acid bacteria. World J. Dairy Food Sci., 4(2): 160-163.
64. Bónai, A., Zotte, A.D., Kametler, L., Vántus, V., Morsy, W.A., Matics, Z., Dal Bosco, A., Szendrő, Z. and Kovács, M. (2012) Dietary Supplementation of Spirulina (Arthrospira platensis) And Thyme (Thymus Vulgaris). Part 2: Effect On Gastrointestinal Growth, Caecal Microbiota and Fermentation in Rabbits. World Rabbit Science Association Proceedings 10th World Rabbit Congress-September 3-6, 2012-Sharm El-Sheikh-Egypt. p707-711.
65. Mariey, Y.A., Samak, H.R. and Ibrahem, M.A. (2012) Effect of using Spirulina platensis algae as a feed additive for poultry diets: 1-productive and reproductive performances of local laying hens. Egypt. Poult. Sci., 32(1): 201-215.