Effects of Replacement of Soybean Meal by Fermented Cottonseed Meal on Growth Performance, Serum Biochemical Parameters and Immune Function of Yellow-feathered Broilers

  • Tang, J.W. (Institute of Plant Protection and Microbiology, Zhejiang Academy of Agriculture Sciences) ;
  • Sun, H. (College of Animal Sciences, Zhejiang University) ;
  • Yao, X.H. (Institute of Plant Protection and Microbiology, Zhejiang Academy of Agriculture Sciences) ;
  • Wu, Y.F. (Institute of Plant Protection and Microbiology, Zhejiang Academy of Agriculture Sciences) ;
  • Wang, X. (Institute of Plant Protection and Microbiology, Zhejiang Academy of Agriculture Sciences) ;
  • Feng, J. (College of Animal Sciences, Zhejiang University)
  • Received : 2011.10.21
  • Accepted : 2011.12.27
  • Published : 2012.03.01


The study was conducted to examine the effects of partially replacing soybean meal (SBM) by solid-state fermented cottonseed meal (FCSM) on growth performance, serum biochemical parameters and immune function of broilers. After inoculated with Bacillus subtilis BJ-1 for 48 h, the content of free gossypol in cottonseed meal was decreased from 0.82 to 0.21 g/kg. A total of 600, day-old male yellow-feathered broilers were randomly divided into four groups with three replicates of 50 chicks each. A corn-SBM based control diet was formulated and the experimental diets included 4, 8 or 12% FCSM, replacing SBM. Throughout the experiment, broilers fed 8% FCSM had higher (p<0.05) body weight gain than those fed 0, 4 and 12% FCSM. The feed intake in 8% FCSM group was superior (p<0.05) to other treatments from d 21 to 42. On d 21, the concentration of serum immunoglobin M in the 4% and 8% FCSM groups, as well as the content of complements (C3, C4) in 8% FCSM group were greater (p<0.05) than those in the SBM group. Besides, birds fed 8% FCSM had increased (p<0.05) serum immunoglobin M, immunoglobulin G and complement C4 levels on d 42 compared with bird fed control diet. No differences (p>0.05) were found between treatments regarding the serum biochemical parameters and the relative weights of immune organs. In conclusion, FCSM can be used in broiler diets at up to 12% of the total diet and an appropriate replacement of SBM with FCSM may improve growth performance and immunity in broilers.


Bacillus subtilis;Fermented Cottonseed Meal;Growth Performance;Immune Function;Serum Parameters;Yellow-feathered Broiler


  1. Ao, X., T. X. Zhou, H. J. Kim, S. M. Hong and I. H. Kim. 2011. Influence of fermented red ginseng extract on broilers and laying hens. Asian-Aust. J. Anim. Sci. 24:993-1000.
  2. AOAC. 1999. Official methods of analysis. 16th ed. Association of Official Analytical Chemists, Washington, DC, USA.
  3. AOCS. 2009. Official methods and recommended practices of the AOCS. 6th ed. American Oil Chemists Society, Chicago, IL, USA.
  4. Amartey, S. A., P. C. J. Leung, N. Baghaei-Yazdi, D. J. Leak and B. S. Hartley. 1999. Fermentation of a wheat straw acid hydrolysate by Bacillus stearothermophilus T-13 in continuous culture with partial cell recycle. Process Biochem. 34:289-294.
  5. Azman, M. A. and M. Yilmaz. 2005. The growth performance of broiler chicks fed with diets containing cottonseed meal supplemented with lysine. Rev. Med. Vet. 156:104-106.
  6. Chen, C. C., Y. C. Shih, P. W. S. Chiou and B. Yu. 2010. Evaluating nutritional quality of single stage- and two stage-fermented soyben meal. Asian-Aust. J. Anim. Sci. 23:598-606.
  7. Chen, K. L., W. L. Kho, S. H. You, R. H. Yeu, S. W. Tang and C. W. Hsieh. 2009. Effects of Bacillus subtilis var. natto and Saccharomyces cerevisiae mixed fermented feed on the enhanced growth performance of broilers. Poult. Sci. 88:309-315.
  8. Chiang, G., W. Q. Lu, X. S. Piao, J. K. Hu, L. M. Gong and P. A. Thacker. 2010. Effects of feeding solid-state fermented rapeseed meal on performance, nutrent digestibility, intestinal ecology and intestinal morphology of broiler chickens. Asian-Aust. J. Anim. Sci. 23:263-271.
  9. Dodds, A. W. and S. Law. 1998. The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and a2-macroglobulin. Immunol. Rev. 166:15-26.
  10. Feng, J., X. Liu, Z. R. Xu, Y. Y. Liu and Y. P. Lu. 2007a. Effects of Aspergillus oryzae 3.042 fermented soybean meal on growth performance and plasma biochemical parameters in broilers. Anim. Feed Sci. Technol. 134:235-242.
  11. Feng, J., X. Liu, Z. R. Xu, Y. P. Lu and Y. Y. Liu. 2007b. Effect of fermented soybean meal on intestinal morphology and digestive enzyme activities in weaned piglets. Dig. Dis. Sci. 52:1845-1850.
  12. Feng, J., W. Q. Ma, H. H. Niu, X. M. Wu, Y. Wang and J. Feng. 2009. Effects of zinc glycine chelate on growth hematological, and immunological characteristics in broilers. Biol. Trace Elem. Res. 133:203-211.
  13. Fritts, C. A., J. H. Kersey, M. A. Motl, E. C. Kroger, F. Yan, J. Si, Q. Jiang, M. M. Campos, A. L. Waldroup and P. W. Waldroup. 2000. Bacillus Subtilis C-3102 (Calsporin) improves live performance and microbiological status of broiler chickes. J. Appl. Poult. Res. 9:149-155.
  14. Gamboa, D. A., M. C. Calhoun, S. W. Kuhlmann, A. U. Haq and C. A. Bailey. 2001. Use of expander cottonseed meal in broiler diets formulated on a digestible amino acid basis. Poult. Sci. 80:789-794.
  15. Gao, D., Y. Cao and H. Li. 2010. Antioxidant activity of peptide fractions derived from cottonseed protein hydrolysate. J. Sci. Food Agric. 90:1855-1860.
  16. Gessesse, A. and G. Mamo. 1999. High-level xylanase production by an alkaliphilic Bacillus sp. by using solid-state fermentation. Enzyme Microb. Technol. 25:68-72.
  17. Grigorova, R. and J. R. Norris. 1990. Methods in microbiology, Volume 22: Techiques in Microbial Ecology. Academic Press, New York, New York.
  18. Heckert, R. A., I. Estevez, E. Russek-Cohen and R. Pettit-Riley. 2002. Effects of density and perch availability on the immune status of broilers. Poult. Sci. 81:451-457.
  19. Henry, M. H., G. M. Pesti and T. P. Brown. 2001. Pathology and histopathology of gossypol toxicity in broiler chicks. Avian Dis. 45:598-604.
  20. Henry, M. H., G. M. Pesti, R. Bakalli, J. Lee, R. T. Toledo, R. R. Eitenmiller and R. D. Phillips. 2001. The performance of broiler chicks fed diets containing extruded cottonseed meal supplemented with lysine. Poult. Sci. 80:762-768.
  21. Hermes, I. H., N. R. Asker, M. T. Shulkamy and M. El Sherskl. 1983. The effect of using different levels of decorticated cottonseed meal on performance of chicks: I. Growth and feed efficiency of starting chicks. Ann. Agric. Sci. Ain Shams University, Egypt. 28:1415-1428.
  22. Mountzouris, K. C., P. Tsitrsikos, I. Palamidi, A. Arvaniti, M. Mohnl, G. Schatzmayr and K. Fegeros. 2010. Effects of probiotic inclusion levles in broiler nutrition on growth performance, nutrient digestibility, plasma immunolobulins, and cecal microflora composition. Poult. Sci. 89:58-67.
  23. Morgan, B. P., K. J. Marchbank, M. P. Longhi, C. L. Harris and A. M. Gallimore. 2005. Complement: central to innate immunity and bridging to adaptive responses. Immunol. Lett. 97:171-179.
  24. Ilyas, A., M. Hirabayashi, T. Matsui, H. Yano, T. Kikushima, M. Takebe and K. Hayakawa. 1995. The note on the removal of phytic acid in soybean meal using Aspergillus usamii. Asian-Aust. J. Anim. Sci. 8:135-138.
  25. Kim, B. N., J. L. Yang and Y. S. Song. 1999. Physiological functions of chongkukjang. Food Ind. Nutr. 4:40-46.
  26. Kim, H. W., E. J. Ko, S. D. Ha, K. B. Song, S. K. Park, D. H. Chung, K. S. Youn and D. H. Bae. 2005. Physical, mechanical, and antimicrobial properties of edible film produced from defatted soybean meal fermented by Bacillus subtilis. J. Microbiol. Biotechnol. 15:815-822.
  27. Mushtaq, T., M. Sarwar, G. Ahmad, M. A. Mirza, T. Ahmad, M. Athar, M. M. H. Mushtaq and U. Noreen. 2009. Influence of pre-press solvent-extracted cottonseed meal supplemented with exogenous enzyme and digestible lysine on performance, digestibility, carcass and immunity responses of broiler chickens. J. Anim. Physiol. Anim. Nutr. 93:253-262.
  28. NRC. 1994. Nutrient requirements of poultry. 9th rev. ed. National Academy Press, Washington, DC, USA.
  29. Paton, A. W., R. Morona and J. C. Paton. 2006. Designer probiotics for prevention of enteric infections. Nat. Rev. Microbiol. 4:193-200.
  30. SAS Institute. 1998. SAS/STAT user's guide: Statistics. Version 7.0. SAS Institute Inc., Cary, NC.
  31. Sterling, K. G., E. F. Costa, M. H. Henry, G. M. Pesti and R. I. Bakalli. 2002. Responses of broiler chickens to cottonseed- and soybean meal-based diets at several protein levels. Poult. Sci. 81:217-226.
  32. Terlabie, N. N., E. Sakyi-Dawson and W. K. Amoa-Awua. 2006. The comparative ability of four isolates of Bacillus subtilis to ferment soybeans into dawadawa. Int. J. Food Microbiol. 106:145-152.
  33. Wang, T., Y. M. Fu, J. L. Lv, H. S. Jiang, Y. P. Li, C. Y. Chen and C. M. Zuo. 2003. Effects of mini-peptides on the growth performance and the development of small intestines in weaning piglets. Anim. Husbandry Vet. Med. 35:4-8.
  34. Wang, J. F., Y. H. Zhu and D. F. Li. 2004. In vitro fermentation of various fiber and starch sources by pig fecal inocula. J. Anim. Sci. 82:2615-2622.
  35. Watkins, S. E., J. T. Skinner, M. H. Adams and P. W. Waldroup. 1993. An evaluation of low-gossypol cottonseed meal in diets for broiler chickens: 1. Effect of cottonseed meal level and lysine supplementation. J. Appl. Poult. Res. 2:221-226.
  36. Watkins, S. E., J. T. Skinner, M. H. Adams and P. W. Waldroup. 1994. An evaluation of low-gossypol cottonseed meal in diets for broiler chickens: 2. Influence of assigned metabolizable energy values and supplementation with essential amino acids on performance. J. Appl. Poult. Res. 3:7-16.
  37. Watkins, S. E. and P. W. Waldroup. 1995. Utilization of high protein cottonseed meal in broiler dites. J. Appl. Poult. Res. 4:310-318.
  38. Weng, X. Y. and J. Y. Sun. 2006. Biodegradation of free gossypol by a new strain of Candida tropicalis under solid state fermentation: Effects of fermentation parameters. Process Biochem. 41:1663-1668.
  39. Xu, F. Z., L. M. Li, J. P. Xu, K. Qian, Z. D. Zhang and Z. Y. Liang. 2011. Effects of fermented rapeseed meal on growth performance and serum parameters in ducks. Asian-Aust. J. Anim. Sci. 24:678-684.
  40. Yu, F., W. C. McNabb, T. N. Barry and P. J. Moughan. 1996. Effect of heat treatment upon the chemical composition of cottonseed meal and upon the reactivity of cottonseed condensed tannins. J. Sci. Food Agric. 72:263-272.<263::AID-JSFA653>3.0.CO;2-1
  41. Zhang, W. J., J. Y. Sun and X. Yang. 2006a. Effect of selected fungi on the reduction of gossypol levels and nutritional value during solid substrate fermentation of cottonseed meal. J. Zhejiang Univ. Sci. B. 7:690-695.
  42. Zhang, W. J., Z. R. Xu, J. Y. Sun and X. Yang. 2006b. A study on the reduction of gossypol levels by mixed culture solid substrate fermentation of cottonseed meal. Asian-Aust. J. Anim. Sci. 19:1314-1321.
  43. Zhang, W. J., Z. R. Xu, S. H. Zhao, J. Y. Sun and X. Yang. 2007. Development of a microbial fermentation process for detoxification of gossypol in cottonseed meal. Anim. Feed Sci. Technol. 135:176-186.

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