Investigations of the distribution and persistence of salmonella and ciprofloxacin-resistant escherichia coli in Turkey hatcheries in the UK

Zoonoses and Public Health

Volumn 60, Issue 4, 2013, Pages 296-303

  Mueller Doblies, D ^a   Clouting, C ^a   Davies, R H ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Antimicrobial; Escherichia coli; Fluoroquinolones; Hatchery; Resistance; Salmonella; Turkey

Indexed keywords

AMIKACIN; AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; APRAMYCIN; CEFOTAXIME; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; ENROFLOXACIN; FURAZOLIDONE; GENTAMICIN; NALIDIXIC ACID; NEOMYCIN; STREPTOMYCIN; SULFADIAZINE; SULFAMERAZINE; SULFATHIAZOLE; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; BREEDING; ESCHERICHIA COLI; HATCHERY; NONHUMAN; PRIORITY JOURNAL; SALMONELLA; SEROTYPE; TURKEY (BIRD); UNITED KINGDOM;

ANIMALS; ANTI-BACTERIAL AGENTS; CIPROFLOXACIN; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FOOD MICROBIOLOGY; GREAT BRITAIN; POULTRY DISEASES; SALMONELLA INFECTIONS, ANIMAL; TURKEYS;

ESCHERICHIA COLI; SALMONELLA;

EID: 84876795676     PISSN: 18631959     EISSN: 18632378     Source Type: Journal    
DOI: 10.1111/j.1863-2378.2012.01524.x     Document Type: Article

References (46)

1. Andrews, J. M., 2001: Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother.48(Suppl. 1), 5-16.
2. Anonymous, 2003: Regulation (EC) No. 2160/2003 of the European Parliament and of the Council of 17 November 2003 on the control of Salmonella and other specified food-borne zoonotic agents.
3. Anonymous, 2008: Commission Regulation (EC) No. 584/2008 of 20 June 2008 implementing Regulation (EC) No. 2160/2003 of the European Parliament and of the Council as regards a Community target for the reduction of the prevalence of Salmonella enteritidis and Salmonella typhimurium in turkeys.
4. Anonymous, 2009a: Commission Regulation (EC) No. 213/2009 of 18 March 2009 amending Regulation (EC) No. 2160/2003 of the European Parliament and of the Council and Regulation (EC) No. 1003/2005 as regards the control and testing of Salmonella in breeding flocks of Gallus gallus and turkeys.
5. Anonymous, 2009b: BSAC Methods for Antimicrobial Susceptibility Testing. http://www.bsac.org.uk/Resources/BSAC/Version%20%2010.2%202011%20final%20May%202011.pdf. (accessed on 27 July 2011).
6. Anonymous, 2009c: Scientific Opinion of the Panel on Biological Hazards on a request from European Commission on Quantitative estimation of the impact of setting a new target for the reduction of Salmonella in breeding hens of Gallus gallus. EFSA J.1036, 1-68.
7. Anonymous, 2009d: Zoonoses: National Control Programmes for the reduction of Salmonella. http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/zoonoses/ncp.htm. (accessed on 26 July 2011).
8. Anonymous, 2010: Commission Regulation (EU) No 200/2010 of 10 March 2010 implementing Regulation (EC) No 2160/2003 of the European Parliament and of the Council as regards a Union target for the reduction of the prevalence of Salmonella serotypes in adult breeding flocks of Gallus gallus.
9. Anonymous, 2011a: Commission Regulation (EU) No 517/2011 of 25 May 2011 implementing Regulation (EC) No 2160/2003 of the European Parliament and of the Council as regards a Union target for the reduction of the prevalence of certain Salmonella serotypes in laying hens of Gallus gallus and amending Regulation (EC) No 2160/2003 and Commission Regulation (EU) No 200/2010.
10. Anonymous, 2011b: Zoonoses Report United Kingdom 2009. http://www.defra.gov.uk/publications/files/pb13571-zoonoses2009-110125.pdf. last accessed 26/07/2011.
11. Bailey, J. S., N. A. Cox, L. C. Blankenship, and N. J. Stern, 1992: Hatchery contamination reduces the effectiveness of competitive exclusion treatments to control Salmonellae colonization of broiler chicks. Poult. Sci.71(Suppl. 1), 6.
12. Bailey, J. S., N. A. Cox, and M. E. Berrang, 1994: Hatchery-acquired salmonellae in broiler chicks. Poult. Sci.73, 1153-1157.
13. Bailey, J. S., R. J. Buhr, N. A. Cox, and M. E. Berrang, 1996: Effect of hatching cabinet sanitation treatments on Salmonella cross-contamination and hatchability of broiler eggs. Poult. Sci.75, 191-196.
14. Berrang, M. E., 1999: Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: a review. J. Appl. Poult. Res.8, 499-504.
15. Betancor, L., M. Pereira, A. Martinez, G. Giossa, M. Fookes, K. Flores, P. Barrios, V. Repiso, R. Vignoli, N. Cordeiro, G. Algorta, N. Thomson, D. Maskell, F. Schelotto, and J. A. Chabalgoity, 2010: Prevalence of Salmonella enterica in poultry and eggs in Uruguay during an epidemic due to Salmonella enterica serovar Enteritidis. J. Clin. Microbiol.48, 2413-2423.
16. Christensen, J. P., D. J. Brown, M. Madsen, J. E. Olsen, and M. Bisgaard, 1997: Hatchery-borne Salmonella enterica serovar Tennessee infections in broilers. Avian Pathol.26, 155-168.
17. Cox, N. A., J. S. Bailey, J. M. Mauldin, and L. C. Blankenship, 1990: Presence and impact of Salmonella contamination in commercial broiler hatcheries. Poult. Sci.69, 1606-1609.
18. Crespo, R., J. S. Jeffrey, R. P. Chin, G. Senties-Cue, and H. L. Shivaprasad, 2004: Phenotypic and genotypic characterization of Salmonella arizonae from an integrated turkey operation. Avian Dis.48, 344-350.
19. Davies, R. H., and C. Wray, 1994: Evaluation of a rapid cultural method for identification of salmonellas in naturally contaminated veterinary samples. J. Appl. Bacteriol.77, 237-241.
20. Davies, R. H., R. A. Nicholas, I. M. McLaren, J. D. Corkish, D. G. Lanning, and C. Wray, 1997: Bacteriological and serological investigation of persistent Salmonella enteritidis infection in an integrated poultry organisation. Vet. Microbiol.58, 277-293.
21. Davies, R., E. Liebana, and M. Breslin, 2003: Investigation of the distribution and control of Salmonella enterica serovar Enteritidis PT6 in layer breeding and egg production. Avian Pathol.32, 225-237.
22. EFSA, 2008a: Analysis of the baseline survey on the prevalence of Salmonella in turkey flocks in the EU, 2006-2007. Part B: factors related to Salmonella flock prevalence and distribution of Salmonella serovars. EFSA J.198, 1-224.
23. EFSA, 2008b: The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents, Antimicrobial Resistance and Foodborne Outbreaks in the European Union in 2006. http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1178671312912.htm, (accessed on 26 July 2011).
24. EFSA, 2008c: Report of the Task Force on Zoonoses Data Collection on the Analysis of the baseline survey on the prevalence of Salmonella in turkey flocks, part A. EFSA J.134, 1-91.
25. Grimont, P. A. D., and F.-X. Weill, 2007: Antigenic formulae of the Salmonella Serovars, 9th edn. Pasteur Institute, Paris. Available at: http://www.pasteur.fr/ip/portal/action/WebdriveActionEvent/oid/01s-000036-089, (accessed on 07 February 2012).
26. Hammerum, A. M., and O. E. Heuer, 2009: Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clin. Infect. Dis.48, 916-921.
27. Hopper, S. A., and S. Mawer, 1988: Salmonella enteritidis in a commercial layer flock. Vet. Rec.123, 351.
28. Kim, A., Y. J. Lee, M. S. Kang, S. I. Kwag, and J. K. Cho, 2007: Dissemination and tracking of Salmonella spp. in integrated broiler operation. J. Vet. Sci.8, 155-161.
29. Lister, S. A., 1988: Salmonella enteritidis infection in broilers and broiler breeders. Vet. Rec.123, 350.
30. Litrup, E., M. Torpdahl, B. Malorny, S. Huehn, H. Christensen, and E. M. Nielsen, 2010: Association between phylogeny, virulence potential and serovars of Salmonella enterica. Infect. Genet. Evol.10, 1132-1139.
31. Mathew, A. G., R. Cissell, and S. Liamthong, 2007: Antibiotic resistance in bacteria associated with food animals: a United States perspective of livestock production. Foodborne Pathog. Dis.4, 115-133.
32. Mueller-Doblies, D., A. R. Sayers, J. J. Carrique-Mas, and R. H. Davies, 2009: Comparison of sampling methods to detect Salmonella infection of turkey flocks. J. Appl. Microbiol.107, 635-45.
33. Nesse, L. L., K. Nordby, E. Heir, B. Bergsjoe, T. Vardund, H. Nygaard, and G. Holstad, 2003: Molecular analyses of Salmonella enterica isolates from fish feed factories and fish feed ingredients. Appl. Environ. Microbiol.69, 1075-1081.
34. O'Brien, J. D., 1988: Salmonella enteritidis infection in broiler chickens. Vet. Rec.122, 214.
35. Olesiuk, O. M., V. L. Carlson, G. H. Snoeyenbos, and C. F. Smyser, 1969: Experimental Salmonella typhimurium infection in two chicken flocks. Avian Dis.13, 500-508.
36. O'Regan, E., T. Quinn, J. G. Frye, J. M. Pages, S. Porwollik, P. J. Fedorka-Cray, M. McClelland, and S. Fanning, 2010: Fitness costs and stability of a high-level ciprofloxacin resistance phenotype in Salmonella enterica serotype enteritidis: reduced infectivity associated with decreased expression of Salmonella pathogenicity island 1 genes. Antimicrob. Agents Chemother.54, 367-374.
37. Pedersen, T. B., J. E. Olsen, and M. Bisgaard, 2008: Persistence of Salmonella Senftenberg in poultry production environments and investigation of its resistance to desiccation. Avian Pathol.37, 421-427.
38. Poppe, C., 2000: Salmonella infections in the domestic fowl. In: Wray, C., and A. Wray (eds), Salmonella in Domestic Animals, pp. 107. CABI Publishing, Wallingford, UK.
39. Prescott, J. F., 2008: Antimicrobial use in food and companion animals. Anim. Health Res. Rev.9, 127-133.
40. Shivaprasad, H. L., J. F. Timoney, S. Morales, B. Lucio, and R. C. Baker, 1990: Pathogenesis of Salmonella enteritidis infection in laying chickens. I. Studies on egg transmission, clinical signs, fecal shedding, and serologic responses. Avian Dis.34, 548-557.
41. Silbergeld, E. K., J. Graham, and L. B. Price, 2008: Industrial food animal production, antimicrobial resistance, and human health. Annu. Rev. Public Health29, 151-169.
42. Taylor, N. M., R. H. Davies, A. Ridley, C. Clouting, A. D. Wales, and F. A. Clifton-Hadley, 2008: A survey of fluoroquinolone resistance in Escherichia coli and thermophilic Campylobacter spp. on poultry and pig farms in Great Britain. J. Appl. Microbiol.105, 1421-1431.
43. Threlfall, E. J., T. Cheasty, A. Graham, and B. Rowe, 1997: Antibiotic resistance in Escherichia coli isolated from blood and cerebrospinal fluid: a 6-year study of isolates from patients in England and Wales. Int. J. Antimicrob. Agents9, 201-205.
44. Timoney, J. F., H. L. Shivaprasad, R. C. Baker, and B. Rowe, 1989: Egg transmission after infection of hens with Salmonella enteritidis phage type 4. Vet. Rec.125, 600-601.
45. Wassenaar, T. M., and P. Silley, 2008: Antimicrobial resistance in zoonotic bacteria: lessons learned from host-specific pathogens. Anim. Health Res. Rev.9, 177-186.
46. Wilkins, M. J., S. A. Bidol, M. L. Boulton, M. G. Stobierski, J. P. Massey, and B. Robinson-Dunn, 2002: Human salmonellosis associated with young poultry from a contaminated hatchery in Michigan and the resulting public health interventions, 1999 and 2000. Epidemiol. Infect.129, 19-27.