Application of a group II campylobacter bacteriophage to reduce strains of campylobacter jejuni and campylobacter coli colonizing broiler chickens

Journal of Food Protection

Volumn 72, Issue 4, 2009, Pages 733-740

  El Shibiny, Ayman ^a,b   Scott, Andrew ^a   Timms, Andrew ^a   Metawea, Yasser ^a,c   Connerton, Phillippa ^a   Connerton, Ian ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b SUEZ CANAL UNIVERSITY   (Egypt)

^c Benha University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

AVES; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; GALLUS GALLUS;

EID: 64749083080     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-72.4.733     Document Type: Article

References (46)

1. Adams, M. H. 1959. Bacteriophages. Interscience Publishers Inc., New York.
2. Allen, V. M, S. A. Bull, J. E. Corry, G. Domingue, F. Jørgensen, J. A. Frost, R. Whyte, A. Gonzalez, N. Elviss, and T. J. Humphrey. 2007. Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation. Int. J. Food Microbiol. 113:54-61.
3. Atterbury, R., E. Dillon, C. Swift, P. Connerton, J. Frost, C. Dodd, C. Rees, and I. Connerton. 2005. Correlation of Campylobacter bac-teriophage with reduced presence of hosts in broiler chicken ceca. Appl. Environ. Microbiol. 71:4885-4887.
4. Atterbury, R. J., P. L. Connerton, C. E. Dodd, C. E. Rees, and 1. F. Connerton. 2003. Isolation and characterization of Campylobacter bacteriophages from retail poultry. Appl. Environ. Microbiol. 69: 4511-4518.
5. Atterbury, R. J., P. L. Connerton, C. E. Dodd, C. E. Rees, and I. F. Connerton. 2003. Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl. Environ. Microbiol. 69:6302-6306.
6. Barrow, P. A. 2001. The use of bacteriophages for treatment and prevention of bacterial disease in animals and animal models of human infection. J. Chem. Technol. Biotechnol. 76:677-682.
7. Brüssow, H. 2007. Phage therapy: the Western perspective, p. 159-192. In S. McGrath and D. van Sinderen (ed.), Bacteriophage genetics and molecular biology. Caister Academic Press, Norfolk, UK.
8. Connerton, I. F., P. L. Connerton, P. Barrow, B. S. Seal, and R. J. Atterbury. 2008. Bacteriophage therapy and Campylobacter, p. 679-693. In I. Nachamkin, C. M. Szymanski, and M. J. Blaser (ed.), Campylobacter, 3rd ed. ASM Press, Washington, DC.
9. Connerton, P. L., and I. F. Connerton. 2005. Microbial treatments to reduce pathogens in poultry meat, p. 414-432. In G. C. Mead (ed.), Food safety control in the poultry industry. Woodhead Publishing Limited, Cambridge, and CRC Press LLC, Boca Raton, FL.
10. Connerton, P. L., C. M. Loc Carrillo, C. Swift, E. Dillon, A. Scott, C. E. Rees, C. E. Dodd, J. Frost, and I. F. Connerton. 2004. Longitudinal study of Campylobacter jejuni bacteriophages and their hosts from broiler chickens. Appl. Environ. Microbiol. 70:3877-3883.
11. Corry, J. E. L., and H. I. Atabay. 2001. Poultry as a source of Cam-pylobacter and related organisms. J. Appl. Microbiol. 90:96S-114S.
12. Coward, C, A. J. Grant, C. Swift, J. Philp, R. Towler, M. Heydarian, J. A. Frost, and D. J. Maskell. 2006. Phase-variable surface structures are required for infection of Campylobacter jejuni by bacterio-phages. Appl. Environ. Microbiol. 72:4638-4647.
13. El-Shibiny, A., P. L. Connerton, and 1. F. Connerton. 2005. Enumeration and diversity of campylobacters and bacteriophages isolated during the rearing cycles of free-range and organic chickens. Appl. Environ. Microbiol. 71:1259-1266.
14. El-Shibiny, A., P. L. Connerton, and I. F. Connerton. 2007. Cam-pylobacter succession in broiler chickens. Vet. Microbiol. 125:323-332.
15. Frost, J. A., J. M. Kramer, and S. A. Gillanders. 1999. Phage typing of Campylobacter jejuni and Campylobacter coli and its use as an adjunct to serotyping. Epidemiol. Infect. 123:47-55.
16. 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.
17. Grajewski, B. A., J. W. Kusek, and H. M. Gelfand. 1985. Development of a bacteriophage typing scheme for Campylobacter jejuni and Campylobacter coli. Epidemiol. Infect. 104:403-414.
18. Greer, G. G. 2005. Bacteriophage control of foodborne bacteria. J. Food Prot. 68:1102-1111.
19. Hansen, V. M., H. Rosenquist, D. L. Baggesen, S. Brown, and B. B. Christensen. 2007. Characterization of Campylobacter phages including analysis of host range by selected Campylobacter Penner serotypes. BMC Microbiol. 7:90.
20. Hudson, J. A., C. Billington, G. Carey-Smith, and G. Greening. 2005. Bacteriophages as biocontrol agents in food. J. Food Prot. 68: 426-437.
21. Jacobs-Reitisma, W., U. Lyhs, and J. Wagenaar. 2008. Campylobac-ter in the food supply, p. 627-644. In I. Nachamkin, C. M. Szy-manski, and M. J. Blaser (ed.), Campylobacter, 3rd ed. ASM Press, Washington, DC.
22. Jørgensen, F., R. Bailey, S. Williams, P. Henderson, D. R. Wareing, F. J. Bolton, J. A. Frost, L. Ward, and T. J. Humphrey. 2002. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. Int. J. Food Micro-biol. 76:151-164.
23. Kasman, L. M., A. Kasman, C. Westwater, J. Dolan, M. G. Schmidt, and J. S. Norris. 2002. Overcoming the phage replication threshold: a mathematical model with implications for phage therapy. J. Virol. 76:5557-5564.
24. Loc Carrillo, C, R. J. Atterbury, A. El-Shibiny, P. L. Connerton, E. Dillon, A. Scott, and I. F. Connerton. 2005. Bacteriophage therapy to reduce Campylobacter jejuni colonisation of broiler chickens. Appl. Environ. Microbiol. 71:6554-6563.
25. Loc Carrillo, C. M., P. L. Connerton, T. Pearson, and I. F. Connerton. 2007. Free-range layer chickens as a source of Campylobacter bac-teriophage. Antonie Leeuwenhoek 92:275-284.
26. Mead, G. C. 2005. The use of probiotics to control foodborne pathogens in poultry, p. 216-236. In G. C. Mead (ed.), Food safety control in the poultry industry. Woodhead Publishing Limited, Cambridge, and CRC Press LLC, Boca Raton, FL,
27. Park, S. C, I. Shimamura, M. Fukunaga, K. I. Mori, and T. Nakai. 2000. Isolation of bacteriophages specific to a fish pathogen, Pseu-domonas plecoglossicida, as a candidate for disease control. Appl. Environ. Microbiol. 66:1416-1422.
28. Payne, R. J., and V. A. Jansen. 2001. Understanding bacteriophage therapy as a density-dependent kinetic process. J. Theor. Biol. 208: 37-48.
29. Payne, R. J., and V. A. Jansen. 2003. Pharmacokinetic principles of bacteriophage therapy. Clin. Pharmacokin. 42:315-325.
30. Reich, F., V. Atanassova, E. Haunhorst, and G. Klein. 2008. The effects of Campylobacter numbers in caeca on the contamination of broiler carcasses with Campylobacter. Int. J. Food Microbiol. 127: 116-120.
31. Ribot, E. M., C. Fitzgerald, K. Kubota, B. Swaminathan, and T. J. Barrett. 2001. Rapid pulsed-tield gel electrophoresis protocol for subtyping of Campylobacter jejuni. J. Clin. Microbiol. 39:1889-1894.
32. Rivoal, K., C. Ragimbeau, G. Salvat, P. Colin, and G. Ermel. 2005. Genomic diversity of Campylobacter coli and Campylobacter jejuni isolates recovered from free-range broiler farms and comparison with isolates of various origins. Appl. Environ. Microbiol. 71:6216-6227.
33. Rosenquist, H., N. L. Nielsen, H. M. Sommer, B. Norrung, and B. B. Christensen. 2003. Quantitative risk assessment of human cam-pylobacteriosis associated with thermophilic Campylobacter species in chickens. Ini. J. Food Microbiol. 83:87-103.
34. Sails, A. D., D. R. A. Wareing, F. J. Bolton, A. J. Fox, and A. Curry. 1998. Characterisation of 16 Campylobacter jejuni and C coli typing bacteriophages. J. Med. Microbiol. 47:123-128.
35. Salama, S., F. J. Bolton, and D. N. Hutchinson. 1989. Improved method for the isolation of Campylobacter jejuni and Campylobacter coli bacteriophages. Lett. Appl. Microbiol. 8:5-7.
36. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Scott, A. E., A. R. Timms, P. L. Connerton, A. El-Shibiny, and I. F. Connerton. 2007. Bacteriophage influence Campylobacter jejuni types populating broiler chickens. Environ. Microbiol. 9:2341-2353.
38. Scott, A. E., A. R. Timms, P. L. Connerton, C. Loc Carrillo, K. A. Radzum, and I. F. Connerton. 2007. Genome dynamics of Campylo-bacter jejuni in response to bacteriophage predation. PLoS Pathog. 3:el 19.
39. Sklar, I. B., and R. D. Joerger. 2001. Attempts to utilize bacteriophage to combat Salmonella enterica serovar Enteritidis infection in chickens. J. Food Saf. 21:15-30.
40. Smith, H. W., M. B. Huggins, and K. M. Shaw. 1987. The control of experimental Escherichia coli diarrhoea in calves by means of bacteriophages. J. Gen. Microbiol. 133:1111-1126.
41. Snedecor, G. W., and W. G. Cochran. 1989. Statistical methods, 8th ed. Iowa State University Press, Ames.
42. Sulakvelidze, A., Z. Alavidze, and J. G. Morris. 2001. Bacteriophage therapy. Antimicrob. Agents Chemother. 45:649-659.
43. Summers, W. C. 2001. Bacteriophage therapy. Annu. Rev. Microbiol. 55:437-451.
44. Wagenaar, J., M. van Bergen, M. Mueller, T. Wassenaar, and R. Carl-ton. 2005. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet. Microbiol. 109:275-283.
45. Wagenaar, J. A., W. Jacobs-Reitisma, M. Hofshagen, and D. Newell. 2008. Poultry colonization with Campylobacter and its control at the primary production level, p. 667-678. In I. Nachamkin, C. M. Szy-manski, and M. J. Blaser (ed.), Campylobacter, 3rd ed. ASM Press, Washington, DC.
46. Weld, R. J.. C. Butts, and J. A. Heinemann. 2004. Models of phage growth and their applicability to phage therapy. J. Theor. Biol. 227: 1-11.