Prevalence and subtypes of ciprofloxacin-resistant Campylobacter spp. in commercial poultry flocks before, during, and after treatment with fluoroquinolones

Antimicrobial Agents and Chemotherapy

Volumn 49, Issue 2, 2005, Pages 690-698

  Humphrey, Tom J ^a   Jørgensen, Frieda ^b   Frost, Jennifer A ^c   Wadda, Haddy ^c   Domingue, Gil ^d   Elviss, Nicola C ^b   Griggs, Deborah J ^e   Piddock, Laura J V ^e  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

^d Avigen Ltd   (United Kingdom)

^e UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; DIFLOXACIN; ENROFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT;

ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ISOLATION; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CHICKEN; CONTROLLED STUDY; DRUG SENSITIVITY; FOOD CHAIN; FOOD CONTAMINATION; GRAM NEGATIVE INFECTION; HERD; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POULTRY FARMING; PRIORITY JOURNAL;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOPHAGE TYPING; CAMPYLOBACTER; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CHICKENS; CIPROFLOXACIN; COLONY COUNT, MICROBIAL; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; FECES; FLUOROQUINOLONES; GREAT BRITAIN; POULTRY DISEASES; SEROTYPING;

EID: 12944300320     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.49.2.690-698.2005     Document Type: Article

References (45)

1. Adak, G. K., S. M. Long, and S. J. O'Brien. 2002. Trends in indigenous foodborne disease and deaths, England and Wales: 1992 to 2000. Gut 51:832-841.
2. Anonymous. 2000. Compendium of datasheets for veterinary products 2000-2001, p. 68 and 203. National Office of Animal Health Ltd., Enfield, United Kingdom.
3. Avrain, L., F. Humbert, R. L'Hospitalier, P. Sanders, C. Vernozy-Rozand, and I. Kempf. 2003. Antimicrobial resistance in Campylobacter from broilers: association with production type and antimicrobial use. Vet. Microbiol. 96:267-276.
4. Berrang, M. E., R. J. Buhr, J. A. Cason, and J. A. Dickens. 2001. Broiler carcass contamination with Campylobacter from feces during defeathering. J. Food Prot. 64:2063-2066.
5. Best, E. L., E. J. Powell, C. Swift, K. A. Grant, and J. A. Frost. 2003. Applicability of a rapid duplex real-time PCR assay for speciation of Campylobacter jejuni and Campylobacter coli directly from culture plates. FEMS Microbiol. Lett. 229:237-241.
6. Bolton, F. J., D. R. A. Wareing, M. B. Skirrow, and D. N. Hutchinson. 1992. Identification and biotyping of campylobacters, p. 151-161. In G. R. Board, D. Jones, and F. A. Skinner (ed.), Identification methods in applied and environmental microbiology. Blackwell Scientific Publications, Oxford, United Kingdom.
7. Campylobacter Sentinel Surveillance Scheme Collaborators. 2002. Ciprofloxacin resistance in Campylobacter jejuni: case-case analysis as a tool for elucidating risks at home and abroad. J. Antimicrob. Chemother. 50:561-568.
8. Communicable Disease Surveillance Centre. 2002. Antimicrobial resistance in 2000: England and Wales. [Online.] http://www.hpa.org.uk/infections/ topics_az/antimicrobial_resistance/amr.pdf. Accessed 18 December 2003.
9. Endtz, H. P., G. J. Ruijs, B. van Klingeren, W. H. Jansen, T. van der Reyden, and R. P. Mouton. 1991. Quinolone resistance in campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J. Antimicrob. Chemother. 27:199-208.
10. Engberg, J., F. M. Aarestrup, D. E. Taylor, P. Gerner-Smidt, and I. Nachamkin. 2001. Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg. Infect. Dis. 7:24-34.
11. Food and Drug Administration. 2002. Enrofloxacin for poultry; notice of hearing. Fed. Regist. 67:7700-7701.
12. Food Standards Agency. 2003. UK wide survey of salmonella and campylobacter contamination of fresh and frozen chicken on retail sale. [Online.] http://www.foodstandards.gov.uk/multimedia/pdfs/campsalmsurv.pdf. Accessed 27 November 2003.
13. Food Standards Agency. 2003. Food Standards Agency strategy for control of campylobacter in chickens. Food Standards Agency Consultation document. [Online.] http://www.foodstandards.gov.uk/multimedia/pdfs/campyloconsult0603e. pdf. Accessed 18 December 2003.
14. Frost, J. A., A. N. Oza, R. T. Thwaites, and B. Rowe. 1998. Serotyping scheme for Campylobacter jejuni and Campylobacter coli based on direct agglutination of heat-stable antigens. J. Clin. Microbiol. 36:335-339.
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. Gaunt, P. N., and L. J. V. Piddock. 1996. Ciprofloxacin resistant Campylobacter spp. in humans: an epidemiological and laboratory study. J. Antimicrob. Chemother. 37:747-757.
17. Gillespie, I. A., S. J. O'Brien, J. A. Frost, G. K. Adak, P. Horby, A. V. Swan, M. J. Painter, and K. R. Neal. 2002. A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg. Infect. Dis. 8:937-942.
18. 17a. Griggs, D. J., M. M. Johnson, J. A. Frost, T. Humphrey, F. Jørgensen, and L. J. V. Piddock. 2005. Incidence and mechanism of ciprofloxacin resistance in Campylobacter spp. isolated from commercial poultry flocks in the United Kingdom before, during, and after fluoroquinolone treatment. Antimicrob. Agents Chemother. 49:699-707.
19. Guerrant, R. L., T. Van Gilder, T. S. Steiner, N. M. Thielman, L. Slutsker, R. V. Tauxe, T. Hennessy, P. M. Griffin, H. DuPont, R. B. Sack, P. Tarr, M. Neill, I. Nachamkin, L. B. Reller, M. T. Osterholm, M. L. Bennish, and L. K. Pickering. 2001. Practice guidelines for the management of infectious diarrhea. Clin. Infect. Dis. 32:331-351.
20. Health Protection Agency. 2003. Campylobacter spp. Laboratory reports of faecal isolates England & Wales, 1986-2001. [Online.] http://www.hpa.org.uk/ infections/topics_az/campy/data_ew.htm. Accessed 18 December 2003.
21. Hein, I., C. Schneck, M. Knogler, G. Feierl, P. Plesss, J. Kofer, R. Achmann, and M. Wagner. 2003. Campylobacter jejuni isolated from poultry and humans in Styria, Austria: epidemiology and ciprofloxacin resistance. Epidemiol. Infect. 130:377-386.
22. Hong, Y., M. E. Berrang, T. Liu, C. L. Hofacre, S. Sanchez, L. Wang, and J. J. Maurer. 2003. Rapid detection of Campylobacter coli, C. jejuni, and Salmonella enterica on poultry carcasses by using PCR-enzyme-linked immunosorbent assay. Appl. Environ. Microbiol. 69:3492-3499.
23. Humphrey, T. J. 1995. Techniques for the isolation of campylobacters from food and the environment, p. 79-83. In Proceedings of a WHO meeting, April 1994. World Health Organization, Geneva, Switzerland.
24. Jacobs-Reitsma, W. F., C. A. Kan, and N. M. Bolder. 1994. The induction of quinolone resistance in Campylobacter bacteria in broilers by quinolone treatment. Lett. Appl. Microbiol. 18:228-231.
25. Jorgensen, 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 Microbiol. 76:151-164.
26. Kramer, J. M., J. A. Frost, F. J. Bolton, and D. R. Wareing. 2000. Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. J. Food Prot. 63:1654-1659.
27. McDermott, P., S. Bodeis, F. Aerestrup, S. Brown, M. Traczewski, P. Fedorka-Cray, M. Wallace, I. Critcheley, C. Thornsberry, S. Graff, R. Flamm, J. Beyer, D. Shortridge, L. J. V. Piddock, and V. Ricci. 2004. Development of a standardized susceptibility test for Campylobacter with quality control ranges for ciprofloxacin, doxifloxacin, erythromycin, gentamicin and meropenem. Microb. Drug Resist. 10:124-131.
28. McDermott, P. F., S. M. Bodeis, L. L. English, D. G. White, R. D. Walker, S. Zhao, S. Simjee, and D. D. Wagner. 2002. Ciprofloxacin resistance in Campylobacter jejuni evolves rapidly in chickens treated with fluoroquinolones. J. Infect. Dis. 185:837-840.
29. Moore, J. E., M. Crowe, N. Heaney, and E. Crothers. 2001. Antibiotic resistance in Campylobacter spp. isolated from human faeces (1980-2000) and foods (1997-2000) in Northern Ireland: an update. J. Antimicrob. Chemother. 48:455-457.
30. Nachamkin, I., H. Ung, and M. Li. 2002. Increasing fluoroquinolone resistance in Campylobacter jejuni, Pennsylvania, USA, 1982-2001. Emerg. Infect. Dis. 8:1501-1503.
31. Neimann, J., J. Engberg, K. Molbak, and H. C. Wegener. 2003. A case-control study of risk factors for sporadic campylobacter infections in Denmark. Epidemiol. Infect. 130:353-366.
32. Newell, D. G., J. A. Frost, B. Duim, J. A. Wagenaar, R. H. Madden, and S. L. W. On. 2000. New developments in the subtyping of Campylobacter species, p. 27-44. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter. ASM Press, Washington, D.C.
33. Newell, D. G., J. E. Shreeve, M. Toszeghy, G. Domingue, S. Bull, T. Humphrey, and G. Mead. 2001. Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abattoirs. Appl. Environ. Microbiol. 67:2636-2640.
34. Newell, D. G., and C. Fearnley. 2003. Sources of Campylobacter colonization in broiler chickens. Appl. Environ. Microbiol. 69:4343-4351.
35. Oza, A. N., J. P. McKenna, S. W. McDowell, F. D. Menzies, and S. D. Neill. 2003. Antimicrobial susceptibility of Campylobacter spp. isolated from broiler chickens in Northern Ireland. J. Antimicrob. Chemother. 52:220-223.
36. Rodrigues, L. C., J. M. Cowden, J. G. Wheeler, D. Sethi, P. G. Wall, P. Cumberland, D. S. Tompkins, M. J. Hudson, J. A. Roberts, and P. J. Roderick. 2001. The study of infectious intestinal disease in England: risk factors for cases of infectious intestinal disease with Campylobacter jejuni infection. Epidemiol. Infect. 127:185-193.
37. Smith, K. E., J. M. Besser, C. W. Hedberg, F. T. Leano, J. B. Bender, J. H. Wicklund, B. P. Johnson, K. A. Moore, M. T. Osterholm, et al. 1999. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. N. Engl. J. Med. 340:1525-1532.
38. Thwaites, R. T., and J. A. Frost. 1999. Drug resistance in Campylobacter jejuni, C. coli, and C. lari isolated from humans in north west England and Wales, 1997. J. Clin. Pathol. 52:812-814.
39. Unicomb, L., J. Ferguson, T. V. Riley, and P. Collignon. 2003. Fluoroquinolone resistance in campylobacter absent from isolates, Australia. Emerg. Infect. Dis. 9:1482-1483.
40. Uyttendaele, M., R. Schukkink, B. van Gemen, and X. Debevere. 1996. Comparison of the nucleic acid amplification system of NASBA and agar isolation for detection of pathogenic campylobacter in naturally contaminated poultry products. J. Food Prod. 59:683-687.
41. van Boven, M., K. T. Veldman, M. C. de Jong, and D. J. Mevius. 2003. Rapid selection of quinolone resistance in Campylobacter jejuni but not in Escherichia coli in individually housed broilers. J. Antimicrob. Chemother. 52:719-723.
42. Wheeler, J. G., D. Sethi, J. M. Cowden, P. G. Wall, L. C. Rodrigues, D. S. Tompkins, M. J. Hudson, P. J. Roderick, et al. 1999. Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. BMJ 318:1046-1050.
43. World Health Organization. 1998. The use of quinolones in food animals and potential impact on human health. Report of a WHO meeting, Geneva, Switzerland, 2 to 5 June 1998. [Online.] http://www.who.int/emc-documents/ zoonoses/docs/whoemczdi9810.pdf. Accessed 18 December 2003.
44. World Health Organization. 2000. The increasing incidence of human campylobacteriosis. Report and proceedings of a WHO consulation of experts, Copenhagen, Denmark, 21 to 25 November 2000. [Online.] http://www.who.int/emc- documents/zoonoses/docs/whocdscsraph20017.pdf. Accessed 18 December 2003.
45. Yang, C., Y. Jiang, K. Huang, C. Zhu, and Y. Yin. 2003. Application of real-time PCR for quantitative detection of Campylobacter jejuni in poultry, milk and environmental water. FEMS Immunol. Med. Microbiol. 38:265-271.