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Research article

Clinical Microbiology and Biomedical Sciences

Therapeutic Effects of Bacteriophages Against Salmonella gallinarum Infection in Chickens

Sung Sik Hong 1, Jipseol Jeong 2, Jinju Lee 2, Suk Kim 2, Wongi Min 2 and Heejoon Myung 1, 3*

1Department of Bioscience and Biotechnology, Hankuk University of Foreign Studies, Yong-In 449-791, Republic of Korea, 2Department of Veterinary Medicine, Gyungsang National University, Jin-Ju 660-701, Republic of Korea, 3Bacteriophage Bank of Korea, Yong-In 449-791, Republic of Korea

Received: April 26, 2013; Accepted: June 18, 2013

J. Microbiol. Biotechnol. 2013; 23(10): 1478-1483

Published October 28, 2013 https://doi.org/10.4014/jmb.1304.04067

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

In this study the isolation and characterization of three bacteriophages (ST4, L13, and SG3) infecting Salmonella gallinarum were carried out. They were further tested for their in vivo efficacy in phage therapy. All three phages belong to the Siphoviridae family with isometric heads and non-contractile tails. They have a broad host range among serovars of Salmonella enterica. The burst sizes were observed to be 1670, 80, and 28 for ST4, L13, and SG3, respectively. The in vivo efficacy of the phages was tested in chickens. Layer chickens were challenged with S. gallinarum, whereas contact chickens were cohabited without direct challenge. Each bacteriophage was orally inoculated in the form of feed additives. Mortality was observed and S. gallinarum was periodically re-isolated from the livers, spleens, and cecums of the chickens. Bacterial re-isolation from the organs and mortality decreased significantly in both challenged and contact chickens treated with the bacteriophages compared with untreated chickens serving as the control. The three bacteriophages may be effective alternatives to antibiotics for the control of fowl typhoid disease in chickens.

Keywords

Salmonella gallinarum, fowl typhoid, phage therapy, animal experiment

References

  1. Barrow PA, Freitas Neto OC. 2011. Pullorum disease and fowl typhoid - new thoughts on old diseases: a review. Avian Pathol. 40: 1-13.
    Pubmed CrossRef
  2. Basnet HB, Kwon HJ, Cho SH, Kim SJ, Yoo HS, Park YH, et al. 2008. Reproduction of fowl typhoid by respiratory challenge with Salmonella gallinarum. Avian Dis. 52: 156-159.
    Pubmed CrossRef
  3. Davies RH. 2005. Pathogen populations on poultry farms, pp. 101-135. In Mead G (ed.). Food Safety Control in the Poultry Industry. Woodhead Publishing Ltd., Cambridge, UK.
    Pubmed CrossRef
  4. De Lappe N, Doran G, O’Connor J, O’Hare C, Cormican M. 2009. Characterization of bacteriophages used in the Salmonella enterica serovar Enteritidis phage-typing scheme. J. Med. Microbiol. 58: 86-93.
    Pubmed CrossRef
  5. Hong J, Kim KP, Heu S, Lee SJ, Adhya S, Ryu S. 2008. Identification of host receptor and receptor-binding module of a newly sequenced T5-like phage EPS7. FEMS Microbiol. Lett. 289: 202-209.
    Pubmed CrossRef
  6. Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, et al. 2008. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Animal Health Res. Rev. 9: 201215.
    Pubmed CrossRef
  7. Kang HW, Kim JW, Jung TS, Woo GJ. 2013. Wksl3, a new biocontrol agent for Salmonella enterica serovars Enteritidis and typhimurium in foods: characterization, application, sequence analysis, and oral acute toxicity study. Appl. Environ. Microbiol. 79: 1956-1968.
    Pubmed CrossRef
  8. Kim SH, Park JH, Lee BK, Kwon HJ, Shin JH, Kim J, et al. 2012. Complete genome sequence of Salmonella bacteriophage SS3e. J. Virol. 86: 10253-10254.
    Pubmed CrossRef
  9. Lim TH, Lee DH, Lee YN, Park JK, Youn HN, Kim MS, et al. 2011. Efficacy of bacteriophage therapy on horizontal transmission of Salmonella gallinarum on commercial layer chickens. Avian Dis. 55: 435-438.
    Pubmed CrossRef
  10. Lu TK, Collins JJ. 2009. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc. Nat. Acad. Sci. USA 106: 4629-4634.
    Pubmed CrossRef
  11. Lu TK, Koeris MS. 2011. The next generation of bacteriophage therapy. Curr. Opin. Microbiol. 14: 524-531.
    Pubmed CrossRef
  12. Mi dzybrodzki R, Borysowski J, Weber-D browska B, Fortuna W, Letkiewicz S, Szufnarowski K, et al. 2012. Clinical aspects of phage therapy. Adv. Virus Res. 83: 73-121.
  13. Sambrook J, Russell DW. 2006. Purification of bacteriophage lambda particles by centrifugation through a glycerol step gradient. CSH Protocols 2006:10.1101/pdb.prot3969.
    CrossRef
  14. Shivaprasad HL. 2000. Fowl typhoid and pullorum disease. Rev. Sci. Tech. 19: 405-424.
    Pubmed
  15. Tiwari BR, Kim S, Kim J. 2012. Complete genomic sequence of Salmonella enterica serovar Enteritidis phage SE2. J. Virol. 86: 7712.
    Pubmed CrossRef
  16. Turner D, Hezwani M, Nelson S, Salisbury V, Reynolds D. 2012. Characterization of the Salmonella bacteriophage vB_SenS-Ent1. J. Gen. Virol. 93: 2046-2056.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(10): 1478-1483

Published online October 28, 2013 https://doi.org/10.4014/jmb.1304.04067

Copyright © The Korean Society for Microbiology and Biotechnology.

Therapeutic Effects of Bacteriophages Against Salmonella gallinarum Infection in Chickens

Sung Sik Hong 1, Jipseol Jeong 2, Jinju Lee 2, Suk Kim 2, Wongi Min 2 and Heejoon Myung 1, 3*

1Department of Bioscience and Biotechnology, Hankuk University of Foreign Studies, Yong-In 449-791, Republic of Korea, 2Department of Veterinary Medicine, Gyungsang National University, Jin-Ju 660-701, Republic of Korea, 3Bacteriophage Bank of Korea, Yong-In 449-791, Republic of Korea

Received: April 26, 2013; Accepted: June 18, 2013

Abstract

In this study the isolation and characterization of three bacteriophages (ST4, L13, and SG3)
infecting Salmonella gallinarum were carried out. They were further tested for their in vivo
efficacy in phage therapy. All three phages belong to the Siphoviridae family with isometric
heads and non-contractile tails. They have a broad host range among serovars of Salmonella
enterica. The burst sizes were observed to be 1670, 80, and 28 for ST4, L13, and SG3,
respectively. The in vivo efficacy of the phages was tested in chickens. Layer chickens were
challenged with S. gallinarum, whereas contact chickens were cohabited without direct
challenge. Each bacteriophage was orally inoculated in the form of feed additives. Mortality
was observed and S. gallinarum was periodically re-isolated from the livers, spleens, and
cecums of the chickens. Bacterial re-isolation from the organs and mortality decreased
significantly in both challenged and contact chickens treated with the bacteriophages
compared with untreated chickens serving as the control. The three bacteriophages may be
effective alternatives to antibiotics for the control of fowl typhoid disease in chickens.

Keywords: Salmonella gallinarum, fowl typhoid, phage therapy, animal experiment

References

  1. Barrow PA, Freitas Neto OC. 2011. Pullorum disease and fowl typhoid - new thoughts on old diseases: a review. Avian Pathol. 40: 1-13.
    Pubmed CrossRef
  2. Basnet HB, Kwon HJ, Cho SH, Kim SJ, Yoo HS, Park YH, et al. 2008. Reproduction of fowl typhoid by respiratory challenge with Salmonella gallinarum. Avian Dis. 52: 156-159.
    Pubmed CrossRef
  3. Davies RH. 2005. Pathogen populations on poultry farms, pp. 101-135. In Mead G (ed.). Food Safety Control in the Poultry Industry. Woodhead Publishing Ltd., Cambridge, UK.
    Pubmed CrossRef
  4. De Lappe N, Doran G, O’Connor J, O’Hare C, Cormican M. 2009. Characterization of bacteriophages used in the Salmonella enterica serovar Enteritidis phage-typing scheme. J. Med. Microbiol. 58: 86-93.
    Pubmed CrossRef
  5. Hong J, Kim KP, Heu S, Lee SJ, Adhya S, Ryu S. 2008. Identification of host receptor and receptor-binding module of a newly sequenced T5-like phage EPS7. FEMS Microbiol. Lett. 289: 202-209.
    Pubmed CrossRef
  6. Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, et al. 2008. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Animal Health Res. Rev. 9: 201215.
    Pubmed CrossRef
  7. Kang HW, Kim JW, Jung TS, Woo GJ. 2013. Wksl3, a new biocontrol agent for Salmonella enterica serovars Enteritidis and typhimurium in foods: characterization, application, sequence analysis, and oral acute toxicity study. Appl. Environ. Microbiol. 79: 1956-1968.
    Pubmed CrossRef
  8. Kim SH, Park JH, Lee BK, Kwon HJ, Shin JH, Kim J, et al. 2012. Complete genome sequence of Salmonella bacteriophage SS3e. J. Virol. 86: 10253-10254.
    Pubmed CrossRef
  9. Lim TH, Lee DH, Lee YN, Park JK, Youn HN, Kim MS, et al. 2011. Efficacy of bacteriophage therapy on horizontal transmission of Salmonella gallinarum on commercial layer chickens. Avian Dis. 55: 435-438.
    Pubmed CrossRef
  10. Lu TK, Collins JJ. 2009. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc. Nat. Acad. Sci. USA 106: 4629-4634.
    Pubmed CrossRef
  11. Lu TK, Koeris MS. 2011. The next generation of bacteriophage therapy. Curr. Opin. Microbiol. 14: 524-531.
    Pubmed CrossRef
  12. Mi dzybrodzki R, Borysowski J, Weber-D browska B, Fortuna W, Letkiewicz S, Szufnarowski K, et al. 2012. Clinical aspects of phage therapy. Adv. Virus Res. 83: 73-121.
  13. Sambrook J, Russell DW. 2006. Purification of bacteriophage lambda particles by centrifugation through a glycerol step gradient. CSH Protocols 2006:10.1101/pdb.prot3969.
    CrossRef
  14. Shivaprasad HL. 2000. Fowl typhoid and pullorum disease. Rev. Sci. Tech. 19: 405-424.
    Pubmed
  15. Tiwari BR, Kim S, Kim J. 2012. Complete genomic sequence of Salmonella enterica serovar Enteritidis phage SE2. J. Virol. 86: 7712.
    Pubmed CrossRef
  16. Turner D, Hezwani M, Nelson S, Salisbury V, Reynolds D. 2012. Characterization of the Salmonella bacteriophage vB_SenS-Ent1. J. Gen. Virol. 93: 2046-2056.
    Pubmed CrossRef