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Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Review

Bacteriophage therapy to combat bacterial infections in poultry

Authors: Andrzej Wernicki, Anna Nowaczek, Renata Urban-Chmiel

Published in: Virology Journal | Issue 1/2017

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Abstract

Infections in poultry are an economic and health problem in Europe and worldwide. The most common infections are associated with salmonellosis, colibacillosis, campylobacteriosis, and others. The prevalence of Campylobacter-positive poultry flocks in European countries varies from 18% to 90%. In the United States, the prevalence of infected flocks is nearly 90%. A similar percentage of infection has been noted for salmonellosis (about 75–90%) and E. coli (90–95%). The occurence of Clostridium perfringens is a major problem for the poultry industry, with some estimates suggesting colonization of as many as 95% of chickens, resulting in clinical or subclinical infections. In the US, annual economic losses due to Salmonella infections run from $1.188 billion to over $11.588 billion, based on an estimated 1.92 million cases. Similar costs are observed in the case of other types of infections. In 2005 economic losses in the the poultry industry due to mortalities reached 1,000,000 USD.
Infections caused by these pathogens, often through poultry products, are also a serious public health issue.
The progressive increase in the number of multi-drug resistant bacteria and the complete ban on the use of antibiotics in livestock feed in the EU, as well as the partial ban in the US, have led to the growth of research on the use of bacteriophages to combat bacterial infections in humans and animals.
The high success rate and safety of phage therapy in comparison with antibiotics are partly due to their specificity for selected bacteria and the ability to infect only one species, serotype or strain. This mechanism does not cause the destruction of commensal bacterial flora. Phages are currently being used with success in humans and animals in targeted therapies for slow-healing infections. They have also found application in the US in eliminating pathogens from the surface of foods of animal and plant origin. At a time of growing antibiotic resistance in bacteria and the resulting restrictions on the use of antibiotics, bacteriophages can provide an alternative means of eliminating pathogens.
Literature
1.
go back to reference Atterbury RJ. The age of phage. Poult Int. 2006;45:18–22. Atterbury RJ. The age of phage. Poult Int. 2006;45:18–22.
2.
go back to reference Sulakvelidze A, Alavidze Z, Glenn Morris Jr J. Bacteriophage therapy. Antimicrob Agents Ch. 2001;45:649–59.CrossRef Sulakvelidze A, Alavidze Z, Glenn Morris Jr J. Bacteriophage therapy. Antimicrob Agents Ch. 2001;45:649–59.CrossRef
3.
go back to reference Summers W. Bacteriophage research: early history. In: Kutter E, Sulakvelidze A, editors. Bacteriophages biology and applications. Boca Raton: Crc Press; 2005. p. 5–27. Summers W. Bacteriophage research: early history. In: Kutter E, Sulakvelidze A, editors. Bacteriophages biology and applications. Boca Raton: Crc Press; 2005. p. 5–27.
4.
go back to reference Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK, Sullivan MB, Rumnieks J, Prangishvili D, Lavigne R, Kropinski AM, Klumpp J, Gillis A, Enault F, Edwards RA, Duffy S, Clokie MRJ, Barylski J, Ackermann HW, Kuhn JH. Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol. 2016;4:1095–9.CrossRef Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK, Sullivan MB, Rumnieks J, Prangishvili D, Lavigne R, Kropinski AM, Klumpp J, Gillis A, Enault F, Edwards RA, Duffy S, Clokie MRJ, Barylski J, Ackermann HW, Kuhn JH. Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol. 2016;4:1095–9.CrossRef
6.
go back to reference Adriaenssens EM, Krupovic M, Knezevic P, Ackermann HW, Barylski J, Brister JR, Clokie MRC, Duffy S, Dutilh BE, Edwards RA, Enault F, Jang HB, Klumpp J, Kropinski AM, Lavigne R, Poranen MM, Prangishvili D, Rumnieks J, Sullivan MB, Wittmann J, Oksanen HM, Gillis A, Kuhn JH. Taxonomy of prokaryotic viruses: 2016 update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol. 2017; doi: 10.1007/s00705-016-3173-4. Adriaenssens EM, Krupovic M, Knezevic P, Ackermann HW, Barylski J, Brister JR, Clokie MRC, Duffy S, Dutilh BE, Edwards RA, Enault F, Jang HB, Klumpp J, Kropinski AM, Lavigne R, Poranen MM, Prangishvili D, Rumnieks J, Sullivan MB, Wittmann J, Oksanen HM, Gillis A, Kuhn JH. Taxonomy of prokaryotic viruses: 2016 update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol. 2017; doi: 10.​1007/​s00705-016-3173-4.
7.
go back to reference Ackermann HW. Bacteriophage taxonomy. Microbiol Aust. 2011;32:90–4. Ackermann HW. Bacteriophage taxonomy. Microbiol Aust. 2011;32:90–4.
9.
go back to reference Ackermann HW. Frequency of morphological phage descriptions in the year 2000. Arch Virol. 2001;146:843–57.CrossRefPubMed Ackermann HW. Frequency of morphological phage descriptions in the year 2000. Arch Virol. 2001;146:843–57.CrossRefPubMed
10.
go back to reference Leverentz B, Conway WS, Janisiewicz W, Camp MJ. Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. J Food Protect. 2004;67:1682–6.CrossRef Leverentz B, Conway WS, Janisiewicz W, Camp MJ. Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. J Food Protect. 2004;67:1682–6.CrossRef
11.
go back to reference Brüssow H, Kutter E. Phage ecology. In: Kutter E, Sulakvelidze A, editors. Bacteriophages biology and applications. Boca Raton: Crc Press; 2005. p. 128–63. Brüssow H, Kutter E. Phage ecology. In: Kutter E, Sulakvelidze A, editors. Bacteriophages biology and applications. Boca Raton: Crc Press; 2005. p. 128–63.
12.
go back to reference Hyman P, Abedon ST. Bacteriophage (overview). In: Schaechter M, editor. Desk encyclopedia of microbiology. 2nd ed. Oxford: Elsevier; 2009. p. 166–82. Hyman P, Abedon ST. Bacteriophage (overview). In: Schaechter M, editor. Desk encyclopedia of microbiology. 2nd ed. Oxford: Elsevier; 2009. p. 166–82.
13.
go back to reference Skurnik M, Strauch E. Phage therapy: facts and fiction. Int J Med Microbiol. 2006;2(96):5–14.CrossRef Skurnik M, Strauch E. Phage therapy: facts and fiction. Int J Med Microbiol. 2006;2(96):5–14.CrossRef
14.
go back to reference Rakhuba DV, Kolomiets EI, Szwajcer Dey E, Novik GI. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol. 2010;59:145–55.PubMed Rakhuba DV, Kolomiets EI, Szwajcer Dey E, Novik GI. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol. 2010;59:145–55.PubMed
15.
go back to reference Domingo-Calap P, Georgel P, Bahram S. Back to the future: bacteriophages as promising therapeutic tools. HLA. 2016;87:133–40.CrossRefPubMed Domingo-Calap P, Georgel P, Bahram S. Back to the future: bacteriophages as promising therapeutic tools. HLA. 2016;87:133–40.CrossRefPubMed
16.
go back to reference Guttman B, Raya R, Kutter E. Basic phage biology. In: Kutter E, Sulakvelidze A, editors. Bacteriophages biology and applications. Boca Raton: Crc Press; 2005. p. 29–66. Guttman B, Raya R, Kutter E. Basic phage biology. In: Kutter E, Sulakvelidze A, editors. Bacteriophages biology and applications. Boca Raton: Crc Press; 2005. p. 29–66.
17.
go back to reference Abedon ST. Phages, ecology, evolution. In: Bacteriophage ecology: population growth, evolution, and impact of bacterial viruses. Cambridge: Cambridge University Press; 2008. p. 1–30.CrossRef Abedon ST. Phages, ecology, evolution. In: Bacteriophage ecology: population growth, evolution, and impact of bacterial viruses. Cambridge: Cambridge University Press; 2008. p. 1–30.CrossRef
18.
go back to reference Hagens S, Loessner MJ. Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr Pharm Biotechnol. 2010;11:58–68.CrossRefPubMed Hagens S, Loessner MJ. Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr Pharm Biotechnol. 2010;11:58–68.CrossRefPubMed
19.
go back to reference EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). EU summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J. 2015; doi: 10.2903/j.efsa.2015.4036. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). EU summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J. 2015; doi: 10.​2903/​j.​efsa.​2015.​4036.
20.
go back to reference Urban-Chmiel R, Wernicki A, Stęgierska D, Dec M, Dudzic A, Puchalski A. Isolation and characterization of Lytic properties of Bacteriophages specific for M. Haemolytica strains. PLoS One. 2015;10:1–11.CrossRef Urban-Chmiel R, Wernicki A, Stęgierska D, Dec M, Dudzic A, Puchalski A. Isolation and characterization of Lytic properties of Bacteriophages specific for M. Haemolytica strains. PLoS One. 2015;10:1–11.CrossRef
22.
go back to reference Chibber S, Kumari S. Application of therapeutic phages in medicine. In: Kurtböke I, editor. Bacteriophages. Rijeka: InTech; 2012. p. 139–58. Chibber S, Kumari S. Application of therapeutic phages in medicine. In: Kurtböke I, editor. Bacteriophages. Rijeka: InTech; 2012. p. 139–58.
23.
go back to reference Kutateladze M, Adamia R. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol. 2010;28:591–5.CrossRefPubMed Kutateladze M, Adamia R. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol. 2010;28:591–5.CrossRefPubMed
24.
go back to reference Biswas B, Adhya S, Washart P, Paul B, Trostel AN, Powell B, Carlton R, Merril CR. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium [erratum in infection and immunity 2002,70,1664]. Infect Immun. 2002;70:204–10.CrossRefPubMedPubMedCentral Biswas B, Adhya S, Washart P, Paul B, Trostel AN, Powell B, Carlton R, Merril CR. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium [erratum in infection and immunity 2002,70,1664]. Infect Immun. 2002;70:204–10.CrossRefPubMedPubMedCentral
25.
go back to reference Weber-Dąbrowska B, Mulczyk M, Górski A. Bacteriophage therapy of bacterial infections: an update of our Institute’s experience. Arch Immunol Ther Exp. 2000;48:547–51. Weber-Dąbrowska B, Mulczyk M, Górski A. Bacteriophage therapy of bacterial infections: an update of our Institute’s experience. Arch Immunol Ther Exp. 2000;48:547–51.
26.
go back to reference Barrow P, Lovell M, Berchieri A Jr. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clin Vaccine Immunol. 1998;5:294–8. Barrow P, Lovell M, Berchieri A Jr. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clin Vaccine Immunol. 1998;5:294–8.
27.
go back to reference Sklar IB, Joerger RD. Attempts to utilize bacteriophages to combat Salmonella enterica serovar Enteritidis in chickens. J Food Saf. 2001;21:15–29.CrossRef Sklar IB, Joerger RD. Attempts to utilize bacteriophages to combat Salmonella enterica serovar Enteritidis in chickens. J Food Saf. 2001;21:15–29.CrossRef
28.
go back to reference Fiorentin L, Vieira ND, Barioni W Jr. Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathol. 2005;34:258–63.CrossRefPubMed Fiorentin L, Vieira ND, Barioni W Jr. Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathol. 2005;34:258–63.CrossRefPubMed
29.
go back to reference Atterbury RJ, Van Bergen MA, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol. 2007;73:4543–9.CrossRefPubMedPubMedCentral Atterbury RJ, Van Bergen MA, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol. 2007;73:4543–9.CrossRefPubMedPubMedCentral
30.
go back to reference Andreatti Filho RL, Higgins JP, Higgins SE, Gaona G, Wolfenden AD, Tellez G, Hargis BM. Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo. Poult Sci. 2007;86:1904–9.CrossRefPubMed Andreatti Filho RL, Higgins JP, Higgins SE, Gaona G, Wolfenden AD, Tellez G, Hargis BM. Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo. Poult Sci. 2007;86:1904–9.CrossRefPubMed
31.
go back to reference Torro H, Price SB, McKee S, Hoerr FJ, Krehling J, Perdue M, Bauermeister L. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis. 2005;49:118–24.CrossRef Torro H, Price SB, McKee S, Hoerr FJ, Krehling J, Perdue M, Bauermeister L. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis. 2005;49:118–24.CrossRef
32.
go back to reference Lim TH, Lee DH, Lee YN, Park JK, Youn HN, Kim MS, Lee HJ, Yang SY, Cho YW, Lee JB, Park SY, Choi IS, Song CS. Efficacy of bacteriophage therapy on horizontal transmission of Salmonella Gallinarum on commercial layer chickens. Avian Dis. 2011;55:435–8.CrossRefPubMed Lim TH, Lee DH, Lee YN, Park JK, Youn HN, Kim MS, Lee HJ, Yang SY, Cho YW, Lee JB, Park SY, Choi IS, Song CS. Efficacy of bacteriophage therapy on horizontal transmission of Salmonella Gallinarum on commercial layer chickens. Avian Dis. 2011;55:435–8.CrossRefPubMed
33.
go back to reference Wagenaar JA, Van Bergen MAP, Mueller MA, Wassenaar TM, Carlton RM. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol. 2005;109:275–83.CrossRefPubMed Wagenaar JA, Van Bergen MAP, Mueller MA, Wassenaar TM, Carlton RM. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol. 2005;109:275–83.CrossRefPubMed
34.
go back to reference Miller RW, Skinner J, Sulakvelidze A, Mathis GF, Hofacre CL. Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens. Avian Dis. 2010;54:33–40.CrossRefPubMed Miller RW, Skinner J, Sulakvelidze A, Mathis GF, Hofacre CL. Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens. Avian Dis. 2010;54:33–40.CrossRefPubMed
35.
go back to reference Ahmadi M, Amir Karimi Torshizi M, Rahimi S, Dennehy JJ. Prophylactic Bacteriophage administration more effective than post-infection Administration in Reducing Salmonella enterica serovar Enteritidis shedding in quail. Frontiers Microb. 2016; 7: art. 1253 doi: doi: 10.3389/fmicb.2016.01253. Ahmadi M, Amir Karimi Torshizi M, Rahimi S, Dennehy JJ. Prophylactic Bacteriophage administration more effective than post-infection Administration in Reducing Salmonella enterica serovar Enteritidis shedding in quail. Frontiers Microb. 2016; 7: art. 1253 doi: doi: 10.​3389/​fmicb.​2016.​01253.
36.
go back to reference Borie C, Sanchez ML, Navarro C, Ramírez S, Morales MA, Retamales J, Robeson J. Aerosol spray treatment with bacteriophages and competitive exclusion reduces Salmonella enteritidis infection in chickens. Avian Dis. 2009;53:250–4.CrossRefPubMed Borie C, Sanchez ML, Navarro C, Ramírez S, Morales MA, Retamales J, Robeson J. Aerosol spray treatment with bacteriophages and competitive exclusion reduces Salmonella enteritidis infection in chickens. Avian Dis. 2009;53:250–4.CrossRefPubMed
37.
go back to reference Lim TH, Kim MS, Lee DH, Lee YN, Park JK, Youn HN, Lee HJ, Yang SY, Cho YW, Lee JB, Park SY, Choi IS, Song CS. Use of bacteriophage for biological control of Salmonella Enteritidis infection in chicken. Res Vet Sci. 2012;93:1173–8.CrossRefPubMed Lim TH, Kim MS, Lee DH, Lee YN, Park JK, Youn HN, Lee HJ, Yang SY, Cho YW, Lee JB, Park SY, Choi IS, Song CS. Use of bacteriophage for biological control of Salmonella Enteritidis infection in chicken. Res Vet Sci. 2012;93:1173–8.CrossRefPubMed
38.
go back to reference Huff WE, Huff GR, Rath NC, Balog JM, Xie H, Moore PA Jr, Donoghue AM. Prevention of Escherichia coli respiratory infection in broiler chickens with bacteriophage (SPR02). Poult Sci. 2002;81:437–41.CrossRefPubMed Huff WE, Huff GR, Rath NC, Balog JM, Xie H, Moore PA Jr, Donoghue AM. Prevention of Escherichia coli respiratory infection in broiler chickens with bacteriophage (SPR02). Poult Sci. 2002;81:437–41.CrossRefPubMed
39.
go back to reference Huff WE, Huff GR, Rath NC, Donoghue AM. Critical evaluation of bacteriophage to prevent and treat colibacillosis in poultry. J Ark Acad Sci. 2009;63:93–8. Huff WE, Huff GR, Rath NC, Donoghue AM. Critical evaluation of bacteriophage to prevent and treat colibacillosis in poultry. J Ark Acad Sci. 2009;63:93–8.
40.
go back to reference Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Esherichia coli respiratory infection. Poultry Sci. 2003;82:1108–12.CrossRef Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Esherichia coli respiratory infection. Poultry Sci. 2003;82:1108–12.CrossRef
41.
go back to reference Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Therapeutic efficacy of bacteriophage and Baytril (enrofloxacin) individually and in combination to treat colibacillosis in broilers. Poult Sci. 2004;83:1944–7.CrossRefPubMed Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Therapeutic efficacy of bacteriophage and Baytril (enrofloxacin) individually and in combination to treat colibacillosis in broilers. Poult Sci. 2004;83:1944–7.CrossRefPubMed
42.
go back to reference Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Prevention of Escherichia coli infection in broiler chickens with a bacteriophage aerosol spray. Poult Sci. 2002b;81:1486–91.CrossRefPubMed Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Prevention of Escherichia coli infection in broiler chickens with a bacteriophage aerosol spray. Poult Sci. 2002b;81:1486–91.CrossRefPubMed
43.
go back to reference Oliveira A, Sereno R, Azeredo J. In vivo efficiency evaluation of a phage cocktail in controlling severe colibacillosis in confined conditions and experimental poultry houses. Vet Microbiol. 2010;146:303–8.CrossRefPubMed Oliveira A, Sereno R, Azeredo J. In vivo efficiency evaluation of a phage cocktail in controlling severe colibacillosis in confined conditions and experimental poultry houses. Vet Microbiol. 2010;146:303–8.CrossRefPubMed
44.
go back to reference El-Gohary FA, Huff WE, Huff GR, Rath NC, Zhou ZY, Donoghue AM. Environmental augmentation with bacteriophage prevents colibacillosis in broiler chickens. Poultry Sci. 2014;93:2788–92.CrossRef El-Gohary FA, Huff WE, Huff GR, Rath NC, Zhou ZY, Donoghue AM. Environmental augmentation with bacteriophage prevents colibacillosis in broiler chickens. Poultry Sci. 2014;93:2788–92.CrossRef
45.
go back to reference Loc-Carrillo C, Atterbury RJ, Connerton PL, Wassenaar TM, Carlton RM. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microb. 2005;71:6554–63.CrossRef Loc-Carrillo C, Atterbury RJ, Connerton PL, Wassenaar TM, Carlton RM. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microb. 2005;71:6554–63.CrossRef
46.
go back to reference Atterbury RJ, Dillon E, Swift C, Connerton PL, Frost JA, Dodd CER, Rees CED, Connerton IF. Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl Environ Microbiol. 2005;71:4885–7.CrossRefPubMedPubMedCentral Atterbury RJ, Dillon E, Swift C, Connerton PL, Frost JA, Dodd CER, Rees CED, Connerton IF. Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl Environ Microbiol. 2005;71:4885–7.CrossRefPubMedPubMedCentral
47.
go back to reference El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I. Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Protect. 2009;72:733–40.CrossRef El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I. Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Protect. 2009;72:733–40.CrossRef
48.
go back to reference Carvalho CM, Gannon BW, Halfhide DE, Santos SB, Hayes CM, Roe JM, Azeredo J. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiol. 2010;10:232–42.CrossRefPubMedPubMedCentral Carvalho CM, Gannon BW, Halfhide DE, Santos SB, Hayes CM, Roe JM, Azeredo J. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiol. 2010;10:232–42.CrossRefPubMedPubMedCentral
49.
go back to reference Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim Health Res Rev. 2008;9:201–15.CrossRefPubMed Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim Health Res Rev. 2008;9:201–15.CrossRefPubMed
50.
go back to reference Zimmer M, Scherer S, Loessner MJ. Genomic analysis of Clostridium perfringens bacteriophage phi3626, which integrates into guaA and possibly affects sporulation. J Bacteriol. 2002;184:4359–68.CrossRefPubMedPubMedCentral Zimmer M, Scherer S, Loessner MJ. Genomic analysis of Clostridium perfringens bacteriophage phi3626, which integrates into guaA and possibly affects sporulation. J Bacteriol. 2002;184:4359–68.CrossRefPubMedPubMedCentral
51.
go back to reference Zimmer M, Vukov N, Scherer S, Loessner MJ. The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl Environ Microbiol. 2002;68:5311–7.CrossRefPubMedPubMedCentral Zimmer M, Vukov N, Scherer S, Loessner MJ. The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl Environ Microbiol. 2002;68:5311–7.CrossRefPubMedPubMedCentral
52.
go back to reference Bigot B, Lee WJ, McIntyre L, Wilson T, Hudson JA, Billington C, Heinemann JA. Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol. 2011;28:1448–52.CrossRefPubMed Bigot B, Lee WJ, McIntyre L, Wilson T, Hudson JA, Billington C, Heinemann JA. Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol. 2011;28:1448–52.CrossRefPubMed
53.
go back to reference Bren L. Bacteria-eating virus approved as food additive. FDA Consum. 2007;41:20–2.PubMed Bren L. Bacteria-eating virus approved as food additive. FDA Consum. 2007;41:20–2.PubMed
55.
go back to reference Krylov VN, Tolmachova TO, Akhverdyan VZ. DNA homology in species of bacteriophages active on Pseudomonas Aeruginosa. Arch Virol. 1993;131:141–51.CrossRefPubMed Krylov VN, Tolmachova TO, Akhverdyan VZ. DNA homology in species of bacteriophages active on Pseudomonas Aeruginosa. Arch Virol. 1993;131:141–51.CrossRefPubMed
56.
go back to reference Wright A1, Hawkins CH, Anggård EE, Harper DR. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas Aeruginosa; a preliminary report of efficacy. Clin Otolaryngol. 2009;34:349–57.CrossRefPubMed Wright A1, Hawkins CH, Anggård EE, Harper DR. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas Aeruginosa; a preliminary report of efficacy. Clin Otolaryngol. 2009;34:349–57.CrossRefPubMed
57.
go back to reference Kutter E1, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST, et al. Curr Pharm Biotechnol. 2010;11:69–86.CrossRefPubMed Kutter E1, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST, et al. Curr Pharm Biotechnol. 2010;11:69–86.CrossRefPubMed
Metadata
Title
Bacteriophage therapy to combat bacterial infections in poultry
Authors
Andrzej Wernicki
Anna Nowaczek
Renata Urban-Chmiel
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0849-7

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