Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Effect of Bacillus amyloliquefaciens-based Direct-fed Microbial on Performance, Nutrient Utilization, Intestinal Morphology and Cecal Microflora in Broiler Chickens

  • Lei, Xinjian (College of Animal Science and Technology, Gansu Agricultural University) ;
  • Piao, Xiangshu (State Key Laboratory of Animal Nutrition, Ministry of Agriculture Feed Industry Certre, China Agricultural University) ;
  • Ru, Yingjun (College of Animal Science and Technology, Gansu Agricultural University) ;
  • Zhang, Hongyu (State Key Laboratory of Animal Nutrition, Ministry of Agriculture Feed Industry Certre, China Agricultural University) ;
  • Peron, Alexandre (Danisco Animal Nutrition) ;
  • Zhang, Huifang (College of Animal Science and Technology, Gansu Agricultural University)
  • Received : 2014.05.07
  • Accepted : 2014.08.01
  • Published : 2015.02.01
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Abstract

The present study was conducted to evaluate the effect of the dietary supplementation of Bacillus amyloliquefaciens-based direct-fed microbial (DFM) on growth performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. A total of two hundred and eighty eight 1-d-old Arbor Acres male broilers were randomly allocated to one of four experimental treatments in a completely randomized design. Each treatment was fed to eight replicate cages, with nine birds per cage. Dietary treatments were composed of an antibiotic-free basal diet (control), and the basal diet supplemented with either 15 mg/kg of virginiamycin as antibiotic growth promoter (AGP), 30 mg/kg of Bacillus amyloliquefaciens-based DFM (DFM 30) or 60 mg/kg of Bacillus amyloliquefaciens-based DFM (DFM 60). Experimental diets were fed in two phases: starter (d 1 to 21) and finisher (d 22 to 42). Growth performance, nutrient utilization, morphological parameters of the small intestine and cecal microbial populations were measured at the end of the starter (d 21) and finisher (d 42) phases. During the starter phase, DFM and virginiamycin supplementation improved the feed conversion ratio (FCR; p<0.01) compared with the control group. For the finisher phase and the overall experiment (d 1 to 42) broilers fed diets with the DFM had better body weight gain (BWG) and FCR than that of control (p<0.05). Supplementation of virginiamycin and DFM significantly increased the total tract apparent digestibility of crude protein (CP), dry matter (DM) and gross energy during both starter and finisher phases (p<0.05) compared with the control group. On d 21, villus height, crypt depth and villus height to crypt depth ratio of duodenum, jejunum, and ileum were significantly increased for the birds fed with the DFM diets as compared with the control group (p<0.05). The DFM 30, DFM 60, and AGP groups decreased the Escherichia coli population in cecum at d 21 and d 42 compared with control group (p<0.01). In addition, the population of Lactobacillus was increased in DFM 30 and DFM 60 groups as compared with control and AGP groups (p<0.01). It can be concluded that Bacillus amyloliquefaciens-based DFM could be an alternative to the use of AGPs in broilers diets based on plant protein.

Keywords

References

  1. Aliakbarpour, H. R., M. Chamani, G. Rahimi, A. A. Sadeghi, and D. Qujieq. 2012. The Bacillus subtilis and lactic acid bacteria probiotics influences intestinal mucin gene expression, histomorphology and growth performance in broilers. Asian Australas. J. Anim. Sci. 25:1285-1293. https://doi.org/10.5713/ajas.2012.12110
  2. Alloui, M. N., W. Szczurek, and S. Swiatkiewicz. 2013. The usefulness of prebiotics and probiotics in modern poultry nutrition: A review. Ann. Anim. Sci. 13:17-32.
  3. An, B. K., B. L. Cho, S. J. You, H. D. Paik, H. I. Chang, S. W. Kim, C. W. Yun, and C. W. Kang. 2008. Growth performance and antibody response of broiler chicks fed yeast derived $\beta$-glucan and single-strain probiotics. Asian Australas. J. Anim. Sci. 21:1027-1032. https://doi.org/10.5713/ajas.2008.70571
  4. AOAC. 1990. Official Methods of Analysis. 16th ed. Association of Official Analytical Chemists, Washington, DC, USA.
  5. Baruzzi, F., L. Quintieri, M. Morea, and L. Caputo. 2011. Antimicrobial compounds produced by Bacillus spp. and applications in food. Science against microbial pathogens: Communicating Current research and technological advances (Ed. A. M. Vilas). City, Spain. 1102-1111.
  6. Castanon, J. I. R. 2007. History of the use of antibiotic as growth promoters in European poultry feeds. Poult. Sci. 86:2466-2471. https://doi.org/10.3382/ps.2007-00249
  7. Chichlowski, M., J. Croom, B. W. McBride, G. B. Havenstein, and M. D. Koci. 2007. Mebabolic and physiological impact of probiotics or direct-fed-microbials on poultry: a brief review of current knowledge. Int. J. Poult. Sci. 6:694-704. https://doi.org/10.3923/ijps.2007.694.704
  8. Choct, M. 2009. Managing gut health through nutrition. Br. Poult. Sci. 50:9-15. https://doi.org/10.1080/00071660802538632
  9. Deng, W., X. F. Dong, J. M. Tong, and Q. Zhang. 2012. The probiotic Bacillus licheniformis ameliorates heat stressinduced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poult. Sci. 91:575-582. https://doi.org/10.3382/ps.2010-01293
  10. Fan, Y., J. Croom, V. L. Christensen, B. L. Black, A. R. Bird, L. R. Daniel, B. W. McBride, and E. J. Eisen. 1997. Jejunal glucose uptake and oxygen consumption in turkey poults selected for rapid growth. Poult. Sci. 76:1738-1745. https://doi.org/10.1093/ps/76.12.1738
  11. Ferreira, C. L., S. salminen, L. Grzeskowiak, M. A. Brizuela, L. Sanchez, H. Carneiro, and M. Bonnet. 2011. Terminology concepts of probiotic and prebiotic and their role in human and animal health. Rev. Salud Anim. 33:137-146.
  12. Fioramonti, J., V. Theodorou, and L. Bueno. 2003. Probiotics:what are they? What are their effects on gut physiology? Best Pract. Res Cl. Gastroenterol. 17:711-724. https://doi.org/10.1016/S1521-6918(03)00075-1
  13. Fuller, R. F. 1989. Probiotic in man and animals. J. Appl. Bacteriol. 66:365-378. https://doi.org/10.1111/j.1365-2672.1989.tb05105.x
  14. Gaskins, H. R., C. T. Collier, and D. B. Anderson. 2002. Antibiotics as growth promotants: Mode of action. Anim. Biotechnol. 13:29-42. https://doi.org/10.1081/ABIO-120005768
  15. Geng, W., M. Cao, C Song, H. Xie, L. Liu, C. Yang, J. Feng, W. Zhang, Y. Jin, Y. Du, and S. Wang. 2011. Complete genome sequence of Bacillus amyloliquefaciens LL3, which exhibits glutamic acid-independent production of poly-$\gamma$-glutamic acid. J. Bacteriol. 193:3393-3394. https://doi.org/10.1128/JB.05058-11
  16. Hong, H. A., L. H. Duc, and S. M. Cutting. 2005. The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev. 29:813-835. https://doi.org/10.1016/j.femsre.2004.12.001
  17. Huyghebaert, G., R. Ducatelle, and F. V. Immerseel. 2011. An update alternatives to antimicrobial growth promoters for broilers. Vet. J. 187:182-188. https://doi.org/10.1016/j.tvjl.2010.03.003
  18. Isolauri, E., Y. Sutas, P. Kankaanpaa, H. Arvilommi, and S. Salminen. 2001. Probiotics: effects on immunity. Am. J. Clin. Nutr. 73:444S-450S.
  19. Jayaraman, S., G. Thangavel, H. Kurian, R. Mani, R. Mukkalil, and H. Chirakkal. 2013. Bacillus subtilis PB6 improves intestinal health of broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Poult. Sci. 92:370-374. https://doi.org/10.3382/ps.2012-02528
  20. Jerzsele, A., K. Szeker, R. Csizinszky, E. Gere, C. Jakab, J. J. Mallo, and P. Galfi. 2012. Efficacy of protected sodium butyrate, a protected blend of essential oils, their combination, and Bacillus amyloliquefaciens spore suspension against artificially induced necrotic enteritis in broilers. Poult. Sci. 91:837-843. https://doi.org/10.3382/ps.2011-01853
  21. Keeney, K. M. and B. B. Finlay. 2011. Enteric pathogen exploitation of the microbiota-generated nutrient environment of the gut. Curr. Opin. Microbiol. 14:92-98. https://doi.org/10.1016/j.mib.2010.12.012
  22. Li, P. F., X. S. Piao, Y. J. Ru, X. Han, L. F. Xue, and H. Y. Zhang. 2012. Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response and intestinal health. Asian Australas. J. Anim. Sci. 25:1617-1626. https://doi.org/10.5713/ajas.2012.12292
  23. Maruta, K., H. Miyazaki, Y. Tadano, S. Masuda, A. Suzuki, H. Takahashi, and M. Takahashi. 1996. Effects of Bacillus subtilis C-3102 intake on fecal flora of sows and on diarrhea and mortality rate of their piglets. Anim. Sci. Technol. 67:403-409.
  24. Montagne, L., J. R. Pluske, and D. J. Hampson. 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young nonruminant animals. Anim. Feed Sci. Technol. 108:95-117. https://doi.org/10.1016/S0377-8401(03)00163-9
  25. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC, USA.
  26. Onderci, M., N. Sahin, K. Sahin, G. Cikim, A. Aydin, I. Ozercanand, and S. Aydin. 2006. Efficacy of supplementation of $\alpha$-amylase-producing bacterial culture on the performance, nutrient use, and gut morphology of broiler chickens fed a corn-based diet. Poult. Sci. 85:505-510. https://doi.org/10.1093/ps/85.3.505
  27. SAS. Institute. 1999. SAS User's Guide: Statistics (Version 8.01). SAS Inst. Inc., Cary, NC, USA.
  28. Shamoto, K. and K. Yamauchi. 2000. Recovery responses of chick intestinal villus morphology to different refeeding procedures. Poult. Sci. 79:718-723. https://doi.org/10.1093/ps/79.5.718
  29. Sharifi, S. D., A. Dibamehr, H. Lotfollahian, and B. Baurhoo. 2012. Effects of flavomycin and probiotic supplementation to diets containing different sources of fat on growth performance, intestinal morphology, apparent metabolizable energy, and fat digestibility in broiler chickens. Poult. Sci. 91:918-927. https://doi.org/10.3382/ps.2011-01844
  30. Song, J., K. Xiao, Y. L. Ke, L. F. Jiao, C. H. Hu, Q. Y. Diao, B. Shi, and X. T. Zhou. 2014. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier interity of broilers subjected to heat stress. Poult. Sci. 93:581-588. https://doi.org/10.3382/ps.2013-03455
  31. Williams, C. H., D. J. David, and O. Lismaa. 1962. The determination of chromic oxide in faeces sample by atomic absorption spectrophotometry. J. Agric. Sci. 59:381-385. https://doi.org/10.1017/S002185960001546X
  32. Wu, B. Q., T. Zhang, L. Q. Guo, and J. F. Lin. 2011. Effect of Bacillus subtilis $KD_1$ on broiler intestinal flora. Poult. Sci. 90:2493-2499. https://doi.org/10.3382/ps.2011-01529

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