Effects of Bacteriophage Supplementation on Egg Performance, Egg Quality, Excreta Microflora, and Moisture Content in Laying Hens

  • Zhao, P.Y. (Department of Animal Resource and Science, Dankook University) ;
  • Baek, H.Y. (Department of Animal Resource and Science, Dankook University) ;
  • Kim, I.H. (Department of Animal Resource and Science, Dankook University)
  • Received : 2012.01.11
  • Accepted : 2012.04.04
  • Published : 2012.07.01


An experiment was conducted to evaluate the effects of bacteriophage supplementation on egg performance, egg quality, excreta microflora, and moisture content in laying hens. A total of 288 Hy-line brown commercial laying hens (36-wk-old) were randomly allotted to 4 treatments in this 6-wk trial and dietary treatments included: i) CON, basal diet; ii) T1, CON+0.020% bacteriophage; iii) T2, CON+0.035% bacteriophage; iv) T3, CON+0.050% bacteriophage. There were 6 replicates for each treatment with 6 adjacent cages (2 hens/cage). Laying hens in T2 and T3 treatments had higher (p<0.05) egg production than those in CON and T1 treatments during wk 0 to 3. In addition, egg production in T1, T2, and T3 treatments was increased (p<0.05) compared with that in CON treatment during wk 4 to 6. At wk 4 and 5, birds in T2 group had higher (p<0.05) HU than those in CON. In addition, at wk 5 and 6, HU in birds fed T1 and T3 diets was greater (p<0.05) than those fed CON diet. E. coli and Salmonella spp. concentrations in excreta were decreased (p<0.05) by T1, T2, and T3 treatments. However, egg weight, egg shell color, yolk height, yolk color unit, egg shell strength, egg shell thickness, egg gravity, and excreta moisture content were not influenced by dietary treatments during the entire experimental period. In conclusion, bacteriophage supplementation has beneficial effects on egg production, egg albumen, and excreta microflora concentration in laying hens.


Bacteriophage;Egg Production;Egg Albumen;Excreta Microflora;Laying Hens


Supported by : Rural Development Administration, Agriculture and Forestry, Ministry for Food, Agriculture, Forestry and Fisheries


  1. Anonymous. 1988. Salmonella Enteritidis phage type 4: Chicken and egg. The Lancet 332:720-722.
  2. Araujo, E., M. Pacheco, R. F. Boni, Y. S. K. Fonseca, D. S. Gelli, S. A. Fernandes and A. T. Tavechio. 1995. Surtos alimentares por Salmonella enteritidis associados ao consumo de alimentos a base de ovos em Sorocaba, SP. Hig Aliment. 9:24-26.
  3. Barrow, P. A., J. F. Tucker and J. M. Simpson. 1987. Inhibition of colonization of the chicken alimentary tract with Salmonella typhimurium gram-negative facultatively anaerobic bacteria. Epidemiol. Infect. 98:311-322.
  4. Barrow, P. A. and Margaret A. Lovell. 1991. Experimental infection of egg‐laying hens with Salmonella enteritidis phage type 4. Avian Pathol. 20:335-348.
  5. Barrow, P., M. A. Lovell and A. Berchieri Jr. 1998. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clin. Diagn. Lab. Immunol. 5:294-298.
  6. Berchieri, Jr., A., M. A. Lovell and P. A. Barrow. 1991. The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella typhimurium. Res. Microbiol. 142:541-549.
  7. Codex Alimentarius Commission. 2001. Codex Alimentarius: Food Hygiene-Basic Texts. 2nd ed. Joint FAO/WHO Food Standards Programme, Rome, Italy.
  8. De Reu, K., K. Grijspeerdt, W. Messens, M. Heyndrickx, M. Uyttendaele, J. Debevere and L. Herman. 2006. Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including Salmonella Enteritidis. Int. J. Food Microbiol. 112:253-260.
  9. Eisen, E. J., B. B. Bohren and H. E. McKean. 1962. The Haugh Unit as a measure of egg albumen quality. Poult. Sci. 41:1461-1468.
  10. Fiorentin, L., N. D. Vieira and W. Barioni Junior. 2005. Use of lytic bacteriophages to reduce Salmonella Enteritidis in experimentally contaminated chicken cuts. Braz. J. Poult. Sci. 7:255-260.
  11. Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck, R. Gast, T. J. Humphrey and F. Van Immerseel. 2009. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol. Rev. 33:718-738.
  12. Gast, R. K. 1994. Understanding Salmonella Enteritidis in laying chickens: The contributions of experimental infections. Int. J. Food Microbiol. 21:107-116.
  13. Goode, D., V. M. Allen and P. A. Barrow. 2003. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 69:5032-5036.
  14. Hempe, J. M., R. C. Lauxen and J. E. Savage. 1998. Rapid determination of egg weight and specific gravity using a computerized data collection system. Poult. Sci. 67:902-907.
  15. Hogue, A., P. White, J. Guard-Petter, W. Schlosser, R. Gast, E. Ebel, J. Farrar, T. Gomez, J. Madden, M. Madison, A. M. McNamara, R. Morales, D. Parham, P. Sparling, W. Sutherlin and D. Swerdlow. 1997. Epidemiology and control of egg-associated Salmonella Enteritidis in the United States of America. Rev. Sci. Tech. 16:542-553.
  16. Huff, W. E., G. R. Huff, N. C. Rath, J. M. Balog, H. Xie, Jr. P. A. Moore and A. M. Donoghue. 2002. Prevention of Escherichia coli respiratory infection in broiler chickens with bacteriophage (SPR02). Poult. Sci. 81:437-441.
  17. Huff, W. E., G. R. Huff, N. C. Rath, J. M. Balog and A. M. Donoghue. 2003. Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Escherichia coli respiratory infection. Poult. Sci. 82:1108-1112.
  18. Humphrey, T. J. 1993. Salmonella enteritidis P.T.4 infections in chickens. In WHO Consultation on control of Salmonella infections in animals: Prevention of food-borne Salmonella infections in man. Jena, Germany, 21-26, December.
  19. Humphrey, T. J. 2006. Are happy chickens safer chickens? Poultry welfare and disease susceptibility. Br. Poult. Sci. 47:379-390.
  20. Kaku, M., J. Peresi, A. T. Tavechio, A. S. Fernandes, A. B. Batista, I. Castanheira, G. Garcia, K. Irino and D. Gelli. 1995. Surto alimentar por Salmonella enteritidis no Noroeste do Estado de Sao Paulo, Brasil. Rev. Saude Publica. 29:127-131.
  21. Lee, N. and D. L. Harris. 2001. The effect of bacteriophage treatment as preharvest intervention strategy to reduce the rapid dissemination of Salmonella typhimurium in pigs. Proc. Am. Assoc. Swine Vet. pp. 555-557.
  22. Messens, W., K. Grijspeerdt and L. Herman. 2005. Eggshell penetration by Salmonella: A review. Worlds Poult. Sci. J. 61:71-85.
  23. McGrath, S., G. F. Fitzgerald and D. van Sinderen. 2004. Starter cultures: Bacteriophage. Cheese Chemistry, Physics and Microbiology 1:163-189.
  24. NRC. 1994. Nutrient requirements of poultry. 9th Revised Edition. National Academy Press. Washington, DC, USA.
  25. Okamura, M., M. Sonobe, S. Obara, T. Kubo, T. Nagai, M. Noguchi, K. Takehara, and M. Nakamura. 2010. Potential egg contamination by Salmonella enterica serovar Typhimurium definitive type 104 following experimental infection of pullets at the onset of lay. Poult. Sci. 89:1629-1634.
  26. Rodrigue, D. C., R. V. Tauxe and B. Rowe. 1990. International increase in Salmonella Enteritidis: A new pandemic? Epidemiol. Infect. 105:21-27.
  27. SAS. 1996. SAS user's guide. Release 6.12 edition. SAS Institute. Inc. Cary NC, USA.
  28. Shivaprasad, H. L., J. F. Timoney and S. Morales. 1990. Pathogenesis of Salmonella enteritidis infection in laying chickens. I. Studies on egg taansmission, clinical signs, fecal shedding, and serologic responses. Avian Dis. 34:548-557.
  29. Shivaprasad, H. L. 2000. Fowl typhoid and pullorium disease. Rev. Sci. Tech. 19:405-424.
  30. Sklar, I. B. and R. D. Joerger. 2001. Attempts to utilize bacteriophages to Attempts to utilize bacteriophages to combat Salmonella enterica serovar Enteritidis in chickens Salmonella enterica serovar Enteritidis in chickens. J. Food Saf. 21:15-29.
  31. Snoeyenbos, G. H. 1991. Pullorium disease. In Disease of poultry, ed. Calnek, B. W., Iowa State University Press, Ames, 73-86.
  32. St Louis, M. E., D. L. Morse, M. E. Potter, T. M. DeMelfi, J. J. Guzewich, R. V. Tauxe and P. A. Blake. 1988. The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. J. Am. Med. Assoc. 259:2103-2107.
  33. Swabe, J. M., L. Sterrenberg and N. E. van de Poll. 2001. Van zaadje tot karbonaadje: Betrokkenen over de volksgezondheidsrisico's van de veehouderij. Rathenau Instituut, The Hague, The Netherlands.
  34. Takata, T., J. Liang, H. Nakano and Y. Yoshimura. 2003. Invasion of Salmonella Enteritidis in the tissues of reproductive organs in laying Japanese quail: An immunocytochemical study. Poult. Sci. 82:1170-1173.
  35. Toro, H., S. B. Price, A. S. McKee, F. J. Hoerr, J. Krehling, M. Perdue and L. Bauermeister. 2005. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis. 49:118-124.
  36. Van Immerseel, F., F. Haesebrouck and R. Ducatelle. 2011. The importance of digestive health and nutritional strategies to control Salmonella. Proceedings of the International Symposium on Avian Salmonellosis, 28-30, June.
  37. Vege, P., A. Cloeckaert and P. Barrow. 2005. Emergence of Salmonella epidemics: The problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistence in orther major serotypes. Vet. Res. 36:267-288.
  38. Whichard, J. M., N. Sriranganathan and F. W. Pierson. 2003. Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. J. Food Prot. 66:220-225.

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