A survey of fluoroquinolone resistance in Escherichia coli and thermophilic Campylobacter spp. on poultry and pig farms in Great Britain

Journal of Applied Microbiology

Volumn 105, Issue 5, 2008, Pages 1421-1431

  Taylor, N M ^a   Davies, R H ^b   Ridley, A ^b   Clouting, C ^b   Wales, A D ^b   Clifton Hadley, F A ^b  

^a UNIVERSITY OF READING   (United Kingdom)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Broiler; Campylobacter; Escherichia coli; Fluoroquinolone; Pig; Poultry; Resistance; Turkey

Indexed keywords

ANTIBIOTICS; FARMS; MAMMALS;

BROILER; CAMPYLOBACTER SPP; CAMPYLOBACTERS; E. COLI; FLUOROQUINOLONES; PIG; PIG FARMS; POULTRY FARMS; RESISTANCE; TURKEY;

ESCHERICHIA COLI;

CIPROFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; COLIFORM BACTERIUM; FECES; INFECTIOUS DISEASE; PIG; POULTRY; PUBLIC HEALTH; THERMOPHILIC BACTERIUM;

ANTIBIOTIC RESISTANCE; ARTICLE; CAMPYLOBACTER; CHICKEN; CONTROLLED STUDY; ESCHERICHIA COLI; FECES CULTURE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PIG FARMING; POULTRY FARMING; SENSITIVITY AND SPECIFICITY; SWINE; THERMOPHILIC BACTERIUM; TURKEY (BIRD); UNITED KINGDOM;

EURASIA; EUROPE; UNITED KINGDOM; WESTERN EUROPE;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER; ESCHERICHIA COLI; SUIDAE;

EID: 54049123736     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2008.03877.x     Document Type: Article

References (57)

1. Aarestrup, F.M. Wegener, H.C. (1999) The effects of antibiotic usage in food animals on the development of antimicrobial resistance of importance for humans in Campylobacter and Escherichia coli. Microbes Infect 1, 639 644.
2. Acar, J.F. Goldstein, F.W. (1997) Trends in bacterial resistance to fluoroquinolones. Clin Infect Dis 24 (Suppl. 1 S67 S73.
3. Achtman, M., Heuzenroeder, M., Kusecek, B., Ochman, H., Caugant, D., Selander, R.K., Vaisanen-Rhen, V., Korhonen, T.K. et al. (1986) Clonal analysis of Escherichia coli O2:K1 isolated from diseased humans and animals. Infect Immun 51, 268 276.
4. Al-Mustafa, Z.H. Al-Ghamdi, M.S. (2000) Use of norfloxacin in poultry production in the eastern province of Saudi Arabia and its possible impact on public health. Int J Environ Health Res 10, 291 299.
5. Amara, A., Ziani, Z. Bouzoubaa, K. (1995) Antibioresistance of Escherichia coli strains isolated in Morocco from chickens with colibacillosis. Vet Microbiol 43, 325 330.
6. Anon (2005a) DANMAP 2004 - Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark. Søborg : Danish Institute for Food and Veterinary Research.
7. Anon (2005b) MARAN-2004 - Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in the Netherlands in 2004. Lelystad : CIDC-Lelystad.
8. Bager, F. Helmuth, R. (2001) Epidemiology of resistance to quinolones in Salmonella. Vet Res 32, 285 290.
9. Baquero, F. (1996) Trends in antibiotic resistance of respiratory pathogens: an analysis and commentary on a collaborative surveillance study. J Antimicrob Chemother 38 (Suppl. A 117 132.
10. Bengtsson, B., Franklin, A., Greko, C. Pringle, M. (2005) SVARM 2004, Swedish Veterinary Antimicrobial Resistance Monitoring. Uppsala, Sweden : The National Veterinary Institute (SVA).
11. Boes, J., Nersting, L., Nielsen, E.M., Kranker, S., Enoe, C., Wachmann, H.C. Baggesen, D.L. (2005) Prevalence and diversity of Campylobacter jejuni in pig herds on farms with and without cattle or poultry. J Food Prot 68, 722 727.
12. van Boven, M., Veldman, K.T., de Jong, M.C.M. Mevius, D.J. (2003) Rapid selection of quinolone resistance in Campylobacter jejuni but not in Escherichia coli in individually housed broilers. J Antimicrob Chemother 52, 719 723.
13. Cherifi, A., Contrepois, M., Picard, B., Goullet, P., Orskov, I., Orskov, F. De Rycke, J. (1991) Clonal relationships among Escherichia coli serogroup 06 isolates from human and animal infections. FEMS Microbiol Lett 64, 225 230.
14. Cherifi, A., Contrepois, M., Picard, B., Goullet, P., Orskov, I. Orskov, F. (1994) Clonal relationships among Escherichia coli serogroup O78 isolates from human and animal infections. J Clin Microbiol 32, 1197 1202.
15. Cooke, E.M., Kumar, P.J., Shooter, R.A., Rousseau, S.A. Foulkes, A.L. (1970) Hospital food as a possible source of Escherichia coli in patients. Lancet 1, 436 437.
16. Davies, R.H., Teale, C.J., Wray, C., McLaren, I.M., Jones, Y.E., Chappell, S. Kidd, S. (1999) Nalidixic acid resistance in salmonellae isolated from turkeys and other livestock in Great Britain. Vet Rec 144, 320 322.
17. Delsol, A.A., Sunderland, J., Woodward, M.J., Pumbwe, L., Piddock, L.J. Roe, J.M. (2004) Emergence of fluoroquinolone resistance in the native Campylobacter coli population of pigs exposed to enrofloxacin. J Antimicrob Chemother 53, 872 874.
18. Endtz, H.P., Ruijs, G.J., van Klingeren, B., Jansen, W.H., van der Reyden, T. Mouton, R.P. (1991) Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother 27, 199 208.
19. Engberg, J., Neimann, J., Nielsen, E.M., Aarestrup, F.M. Fussing, V. (2004) Quinolone-resistant Campylobacter infections in Denmark: risk factors and clinical consequences. Emerg Infect Dis 10, 1056 1063.
20. Gallay, A., Prouzet-Mauleon, V., Kempf, I., Lehours, P., Labadi, L., Camou, C., Denis, M., de Valk, H. et al. (2007) Campylobacter antimicrobial drug resistance among humans, broiler chickens, and pigs, France. Emerg Infect Dis 13, 259 266.
21. Gaunt, P.N. Piddock, L.J. (1996) Ciprofloxacin resistant Campylobacter spp. in humans: an epidemiological and laboratory study. J Antimicrob Chemother 37, 747 757.
22. Ge, B.L., McDermott, P.F., White, D.G. Meng, J.H. (2005) Role of efflux pumps and topoisomerase mutations in fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother 49, 3347 3354.
23. Giraud, E., Leroy-Setrin, S., Flaujac, G., Cloeckaert, A., Dho-Moulin, M. Chaslus-Dancla, E. (2001) Characterization of high-level fluoroquinolone resistance in Escherichia coli O78:K80 isolated from turkeys. J Antimicrob Chemother 47, 341 343.
24. Gootz, T.D. Martin, B.A. (1991) Characterization of high-level quinolone resistance in Campylobacter jejuni. Antimicrob Agents Chemother 35, 840 845.
25. Griggs, D.J., Johnson, M.M., Frost, J.A., Humphrey, T., Jorgensen, F. Piddock, L.J.V. (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.
26. Guevremont, E., Higgins, R. Quessy, S. (2004) Characterization of Campylobacter isolates recovered from clinically healthy pigs and from sporadic cases of campylobacteriosis in humans. J Food Prot 67, 228 234.
27. Gupta, A., Nelson, J.M., Barrett, T.J., Tauxe, R.V., Rossiter, S.P., Friedman, C.R., Joyce, K.W., Smith, K.E. et al. (2004) Antimicrobial resistance among Campylobacter strains, United States, 1997-2001. Emerg Infect Dis 10, 1102 1109.
28. Hanninen, M.-L. Hannula, M. (2007) Spontaneous mutation frequency and emergence of ciprofloxacin resistance in Campylobacter jejuni and Campylobacter coli. J Antimicrob Chemother 60, 1251 1257.
29. Harvey, R.B., Anderson, R.C., Young, C.R., Swindle, M.M., Genovese, K.J., Hume, M.E., Droleskey, R.E., Farrington, L.A. et al. (2001) Effects of feed withdrawal and transport on cecal environment and Campylobacter concentrations in a swine surgical model. J Food Prot 64, 730 733.
30. Hopkins, K.L., Davies, R.H. Threlfall, E.J. (2005) Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. Int J Antimicrob Agents 25, 358 373.
31. Kassenborg, H.D., Smith, K.E., Vugia, D.J., Rabatsky-Ehr, T., Bates, M.R., Carter, M.A., Dumas, N.B., Cassidy, M.P. et al. (2004) Fluoroquinolone-resistant Campylobacter infections: eating poultry outside of the home and foreign travel are risk factors. Clin Infect Dis 38, S279 S284.
32. Kern, W.V., Oethinger, M., Jellen-Ritter, A.S. Levy, S.B. (2000) Non-target gene mutations in the development of fluoroquinolone resistance in Escherichia coli. Antimicrob Agents Chemother 44, 814 820.
33. Kramer, J.M., Frost, J.A., Bolton, F.J. Wareing, D.R. (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.
34. Levy, S.B., FitzGerald, G.B. Macone, A.B. (1976) Spread of antibiotic-resistant plasmids from chicken to chicken and from chicken to man. Nature 260, 40 42.
35. Linton, A.H. (1977) Animal to man transmission of Enterobacteriaceae. R Soc Health J 97, 115 118.
36. Linton, A.H. (1986) Flow of resistance genes in the environment and from animals to man. J Antimicrob Chemother 18 (Suppl. C 189 197.
37. Mammeri, H., Van de Loo, M., Poirel, L., Martinez-Martinez, L. Nordmann, P. (2005) Emergence of plasmid-mediated quinolone resistance in Escherichia coli in Europe. Antimicrob Agents Chemother 49, 71 76.
38. McDermott, P.F., Bodeis, S.M., English, L.L., White, D.G., Walker, R.D., Zhao, S.H., Simjee, S. Wagner, D.D. (2002) Ciprofloxacin resistance in Campylobacter jejuni evolves rapidly in chickens treated with fluoroquinolones. J Infect Dis 185, 837 840.
39. Moore, J.E., McLernon, P., Wareing, D., Xu, J. Murphy, P.G. (2002) Characterisation of fluoroquinolone-resistant Campylobacter species isolated from human beings and chickens. Vet Rec 150, 518 520.
40. National Committee for Clinical Laboratory Standards 1997) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, 4th edn. Approved standard, NCCLS document M7-A4, 17 (2) (ISBN 1-56238-309-4). Wayne, PA : NCCLS.
41. Nijsten, R., London, N., van den Bogaard, A. Stobberingh, E. (1994) Resistance in faecal Escherichia coli isolated from pig farmers and abattoir workers. Epidemiol Infect 113, 45 52.
42. Norstrom, M., Hofshagen, M., Stavnes, T., Schau, J., Lassen, J. Kruse, H. (2006) Antimicrobial resistance in Campylobacter jejuni from humans and broilers in Norway. Epidemiol Infect 134, 127 130.
43. Osterlund, A., Hermann, M. Kahlmeter, G. (2003) Antibiotic resistance among Campylobacter jejuni/coli strains acquired in Sweden and abroad: a longitudinal study. Scand J Infect Dis 35, 478 481.
44. Oza, A.N., McKenna, J.P., McDowell, S.W.J., Menzies, F.D. Neill, S.D. (2003) Antimicrobial susceptibility of Campylobacter spp. isolated from broiler chickens in Northern Ireland. J Antimicrob Chemother 52, 220 223.
45. Padungton, P. Kaneene, J.B. (2003) Campylobacter spp. in human, chickens, pigs and their antimicrobial resistance. J Vet Med Sci 65, 161 170.
46. Piddock, L.J. (1995) Quinolone resistance and Campylobacter spp. J Antimicrob Chemother 36, 891 898.
47. Randall, L.P., Ridley, A.M., Cooles, S.W., Sharma, M., Sayers, A.R., Pumbwe, L., Newell, D.G., Piddock, L.J.V. et al. (2003) Prevalence of multiple antibiotic resistance in 443 Campylobacter spp. isolated from humans and animals. J Antimicrob Chemother 52, 507 510.
48. Rautelin, H., Renkonen, O.V. Kosunen, T.U. (1991) Emergence of fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli in subjects from Finland. Antimicrob Agents Chemother 35, 2065 2069.
49. Siemer, B.L., Nielsen, E.M. On, S.L. (2005) Identification and molecular epidemiology of Campylobacter coli isolates from human gastroenteritis, food, and animal sources by amplified fragment length polymorphism analysis and Penner serotyping. Appl Environ Microbiol 71, 1953 1958.
50. Sjogren, E., Kaijser, B. Werner, M. (1992) Antimicrobial susceptibilities of Campylobacter jejuni and Campylobacter coli isolated in Sweden: a 10-year follow-up report. Antimicrob Agents Chemother 36, 2847 2849.
51. Smith, K.E., Besser, J.M., Hedberg, C.W., Leano, F.T., Bender, J.B., Wicklund, J.H., Johnson, B.P., Moore, K.A. et al. (1999) Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. N Engl J Med 340, 1525 1532.
52. Stern, N.J. Robach, M.C. (2003) Enumeration of Campylobacter spp. in broiler feces and in corresponding processed carcasses. J Food Prot 66, 1557 1563.
53. Threlfall, E.J., Cheasty, T., Graham, A. Rowe, B. (1998) 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 Agents 9, 201 205.
54. Van den Bogaard, A.E. Stobberingh, E.E. (2000) Epidemiology of resistance to antibiotics: links between animals and humans. Int J Antimicrob Agents 14, 327 335.
55. Webber, M. Piddock, L.J.V. (2001) Quinolone resistance in Escherichia coli. Vet Res 32, 275 284.
56. Yan, M.G., Sahin, O., Lin, J. Zhang, Q.J. (2006) Role of the CmeABC efflux pump in the emergence of fluoroquinolone-resistant Campylobacter under selection pressure. J Antimicrob Chemother 58, 1154 1159.
57. Zhang, Q., Lin, J. Pereira, S. (2003) Fluoroquinolone-resistant Campylobacter in animal reservoirs: dynamics of development, resistance mechanisms and ecological fitness. Anim Health Res Rev 4, 63 71.