Comparative Analysis of ESBL-Positive Escherichia coli Isolates from Animals and Humans from the UK, The Netherlands and Germany

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Wu, Guanghui ^a   Day, Michaela J ^b   Mafura, Muriel T ^a   Nunez Garcia, Javier ^a   Fenner, Jackie J ^a   Sharma, Meenaxi ^a   van Essen Zandbergen, Alieda ^c   Rodríguez, Irene ^d,g   Dierikx, Cindy ^c   Kadlec, Kristina ^e   Schink, Anne Kathrin ^e   Wain, John ^b,f   Helmuth, Reiner ^d   Guerra, Beatriz ^d   Schwarz, Stefan ^e   Threlfall, John ^b   Woodward, Martin J ^a,h   Woodford, Neil ^b   Coldham, Nick ^a   Mevius, Dik ^c  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

^b PUBLIC HEALTH ENGLAND   (United Kingdom)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^e FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^f UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^g HOSPITAL RAMÓN Y CAJAL   (Spain)

^h UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BETA LACTAMASE; BETA LACTAMASE CTX M; BETA LACTAMASE OXA 1; CEFOTAXIME; EXTENDED SPECTRUM BETA LACTAMASE; UNCLASSIFIED DRUG;

AAC GENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BLA CTX M GROUP 1 GENE; BLA OXA 1 LIKE GENE; CATB3 GENE; CATTLE; CHICKEN MEAT; DOG; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ESCHERICHIA COLI; GENETIC VARIABILITY; GERMANY; MICROARRAY ANALYSIS; MPH GENE; MRX GENE; MULTILOCUS SEQUENCE TYPING; NETHERLANDS; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; UNITED KINGDOM;

ANIMAL FEED; ANIMALS; BETA-LACTAMASES; CATTLE; CHICKENS; DOGS; DRUG RESISTANCE; ESCHERICHIA COLI; GERMANY; GREAT BRITAIN; HUMANS; MICROARRAY ANALYSIS; MULTILOCUS SEQUENCE TYPING; NETHERLANDS; SPECIES SPECIFICITY; VIRULENCE;

EID: 84884650083     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075392     Document Type: Article

References (45)

1. Russo TA, Johnson JR, (2003) Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5: 449-456. doi:10.1016/S1286-4579(03)00049-2. PubMed: 12738001.
2. HPA website. Available: http://www.hpa.org.uk/web/HPAwebFile/HPAweb_C/1296686942137 Accessed 2013 Aug. 23.
3. Coque TM, Baquero F, Canton R, (2008) Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill 13(47):: 19044,19021958.
4. Schwaber MJ, Carmeli Y, (2007) Mortality and delay in effective therapy associated with extended-spectrum beta-lactamase production in Enterobacteriaceae bacteraemia: A systematic review and meta-analysis. J Antimicrob Chemother 60: 913-920. doi:10.1093/jac/dkm318. PubMed: 17848376.
5. Lau SH, Kaufmann ME, Livermore DM, Woodford N, Willshaw GA, et al. (2008) UK epidemic Escherichia coli strains A-E, with CTX-M-15 β-lactamase, all belong to the international O25:H4-ST131 clone. J Antimicrob Chemother 62: 1241-1244. doi:10.1093/jac/dkn380. PubMed: 18779256.
6. Livermore DM, Hawkey PM, (2005) CTX-M: changing the face of ESBLs in the UK. J Antimicrob Chemother 56: 451-454. doi:10.1093/jac/dki239. PubMed: 16006451.
7. Hawkey PM, Jones AM, (2009) The changing epidemiology of resistance. J Antimicrob Chemother 64 (Suppl 1):: i3-10. doi:10.1093/jac/dkp256. PubMed: 19675017.
8. Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM, (2005) β-Lactamases among extended-spectrum β-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 56: 115-121. doi:10.1093/jac/dki190. PubMed: 15941775.
9. Hunter PA, Dawson S, French GL, Goossens H, Hawkey PM, et al. (2010) Antimicrobial-resistant pathogens in animals and man: prescribing, practices and policies. J Antimicrob Chemother 65 (Suppl 1):: i3-17. doi:10.1093/jac/dkp433. PubMed: 20045808.
10. Liebana E, Batchelor M, Hopkins KL, Clifton-Hadley FA, Teale CJ, et al. (2006) Longitudinal farm study of extended-spectrum β-lactamase-mediated resistance. J Clin Microbiol 44: 1630-1634. doi:10.1128/JCM.44.5.1630-1634.2006. PubMed: 16672386.
11. Liebana E, Gibbs M, Clouting C, Barker L, Clifton-Hadley FA, et al. (2004) Characterization of β-lactamases responsible for resistance to extended-spectrum cephalosporins in Escherichia coli and Salmonella enterica strains from food-producing animals in the United Kingdom. Microb Drug Resist 10: 1-9. doi:10.1089/107662904323047745. PubMed: 15140388.
12. Roest HI, Liebana E, Wannet W, van Duynhoven Y, Veldman KT, et al. (2007) [Antibiotic resistance in Escherichia coli O157 isolated between 1998 and 2003 in The Netherlands]. Tijdschr Diergeneeskd 132: 954-958. PubMed: 18225714.
13. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, et al. (2011) Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 17: 873-880. doi:10.1111/j.1469-0691.2011.03497.x. PubMed: 21463397.
14. Vincent C, Boerlin P, Daignault D, Dozois CM, Dutil L, et al. (2010) Food reservoir for Escherichia coli causing urinary tract infections. Emerg Infect Dis 16: 88-95. doi:10.3201/eid1601.091118. PubMed: 20031048.
15. Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, et al. (2007) Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002-2004. Emerg Infect Dis 13: 838-846. doi:10.3201/eid1306.061576. PubMed: 17553221.
16. Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD, (2008) Community-onset extended-spectrum β-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect 57: 441-448. doi:10.1016/j.jinf.2008.09.034. PubMed: 18990451.
17. Tängdén T, Cars O, Melhus A, Löwdin E, (2010) Foreign travel is a major risk factor for colonization with Escherichia coli producing CTX-M-type extended-spectrum β-lactamases: a prospective study with Swedish volunteers. Antimicrob Agents Chemother 54: 3564-3568. doi:10.1128/AAC.00220-10. PubMed: 20547788.
18. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, et al. (2011) Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis 17: 1216-1222. doi:10.3201/eid1707.110209. PubMed: 21762575.
19. Randall LP, Clouting C, Horton RA, Coldham NG, Wu G, et al. (2011) Prevalence of Escherichia coli carrying extended-spectrum β-lactamases (CTX-M and TEM-52) from broiler chickens and turkeys in Great Britain between 2006 and 2009. J Antimicrob Chemother 66: 86-95. doi:10.1093/jac/dkq396. PubMed: 21098542.
20. Snow LC, Warner RG, Cheney T, Wearing H, Stokes M, et al. (2012) Risk factors associated with extended spectrum β-lactamase Escherichia coli (CTX-M) on dairy farms in North West England and North Wales. Prev Vet Med 106: 225-234. doi:10.1016/j.prevetmed.2012.03.009. PubMed: 22552330.
21. Schink AK, Kadlec K, Schwarz S, (2011) Analysis of bla(CTX-M)-carrying plasmids from Escherichia coli isolates collected in the BfT-GermVet study. Appl Environ Microbiol 77: 7142-7146. doi:10.1128/AEM.00559-11. PubMed: 21685166.
22. Wu G, Mafura M, Carter B, Lynch K, Anjum MF, et al. (2010) Genes associated with Escherichia coli isolates from calves with diarrhoea and/or septicaemia. Vet Rec 166: 691-692. doi:10.1136/vr.b4791. PubMed: 20511653.
23. Anjum MF, Mafura M, Slickers P, Ballmer K, Kuhnert P, et al. (2007) Pathotyping Escherichia coli by using miniaturized DNA microarrays. Appl Environ Microbiol 73: 5692-5697. doi:10.1128/AEM.00419-07. PubMed: 17630299.
24. Batchelor M, Hopkins KL, Liebana E, Slickers P, Ehricht R, et al. (2008) Development of a miniaturised microarray-based assay for the rapid identification of antimicrobial resistance genes in Gram-negative bacteria. Int J Antimicrob Agents 31: 440-451. doi:10.1016/j.ijantimicag.2007.11.017. PubMed: 18243668.
25. Geue L, Schares S, Mintel B, Conraths FJ, Müller E, et al. (2010) Rapid microarray-based genotyping of enterohemorrhagic Escherichia coli serotype O156:H25/H-/Hnt isolates from cattle and clonal relationship Analysis. Appl Environ Microbiol 76: 5510-5519. doi:10.1128/AEM.00743-10. PubMed: 20581183.
26. Bonnet R, (2004) Growing group of extended-spectrum β-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 48: 1-14. doi:10.1128/AAC.48.1.1-14.2004. PubMed: 14693512.
27. Dierikx CM, van Duijkeren E, Schoormans AH, van Essen-Zandbergen A, Veldman K, et al. (2012) Occurrence and characteristics of extended-spectrum-β-lactamase- and AmpC-producing clinical isolates derived from companion animals and horses. J Antimicrob Chemother 67: 1368-1374. doi:10.1093/jac/dks049. PubMed: 22382469.
28. Simpson's Diversity Index. Available: http://www.countrysideinfo.co.uk/simpsons.htm. Accessed 2013 Aug. 23.
29. Wirth T, Falush D, Lan R, Colles F, Mensa P,et al (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60: 1136-1151. doi:10.1111/j.1365-2958.2006.05172.x. PubMed: 16689791.
30. Nataro JP, Kaper JB, (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11: 142-201. PubMed: 9457432.
31. Dho-Moulin M, Fairbrother JM, (1999) Avian pathogenic Escherichia coli (APEC). Vet Res 30: 299-316. PubMed: 10367360.
32. Cloeckaert A, Baucheron S, Flaujac G, Schwarz S, Kehrenberg C, et al. (2000) Plasmid-mediated florfenicol resistance encoded by the floR gene in Escherichia coli isolated from cattle. Antimicrob Agents Chemother 44: 2858-2860. doi:10.1128/AAC.44.10.2858-2860.2000. PubMed: 10991873.
33. Coque TM, Novais A, Carattoli A, Poirel L, Pitout J, et al. (2008) Dissemination of clonally related Escherichia coli strains expressing extended-spectrum β-lactamase CTX-M-15. Emerg Infect Dis 14: 195-200. doi:10.3201/eid1402.070350. PubMed: 18258110.
34. Mesko Meglic K, Koren S, Palepou MF, Karisik E, Livermore DM, et al. (2009) Nationwide survey of CTX-M-type extended-spectrum β-lactamases among Klebsiella pneumoniae isolates in Slovenian hospitals. Antimicrob Agents Chemother 53: 287-291. doi:10.1128/AAC.00746-08. PubMed: 19001116.
35. Dhanji H, Doumith M, Rooney PJ, O'Leary MC, Loughrey AC, et al. (2011) Molecular epidemiology of fluoroquinolone-resistant ST131 Escherichia coli producing CTX-M extended-spectrum β-lactamases in nursing homes in Belfast, UK. J Antimicrob Chemother 66: 297-303. doi:10.1093/jac/dkq463. PubMed: 21131323.
36. Dhanji H, Murphy NM, Akhigbe C, Doumith M, Hope R, et al. (2011) Isolation of fluoroquinolone-resistant O25b:H4-ST131 Escherichia coli with CTX-M-14 extended-spectrum β-lactamase from UK river water. J Antimicrob Chemother 66: 512-516. PubMed: 21172781.
37. Pitout JD, Campbell L, Church DL, Gregson DB, Laupland KB, (2009) Molecular characteristics of travel-related extended-spectrum-β-lactamase-producing Escherichia coli isolates from the Calgary Health Region. Antimicrob Agents Chemother 53: 2539-2543. doi:10.1128/AAC.00061-09.
38. Pitout JD, Gregson DB, Church DL, Elsayed S, Laupland KB, (2005) Community-wide outbreaks of clonally related CTX-M-14 β-lactamase-producing Escherichia coli strains in the Calgary health region. J Clin Microbiol 43: 2844-2849. doi:10.1128/JCM.43.6.2844-2849.2005. PubMed: 15956407.
39. Pitout JD, Laupland KB, (2008) Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8: 159-166. doi:10.1016/S1473-3099(08)70041-0. PubMed: 18291338.
40. (BIOHAZ) EPoBH (2011) Scientific Opinion on the public health risks of bacterial strains producing extended-spectrum β-lactamases and/or AmpC β-lactamases in food and food-producing animals EFSA Journal 9: 2322.
41. Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH, (2012) Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 18: 646-655. doi:10.1111/j.1469-0691.2012.03850.x. PubMed: 22519858.
42. Stokes MO, Cottell JL, Piddock LJV, Wu G, Wootton M, et al. (2012) Detection and Characterisation of blaCTX-M-14 IncK pCT like plasmid vectors in Escherichia coli isolates from humans, turkeys and cattle in England and Wales. J Antimicrob Chemother 67(7):: 1639-44.
43. Wu G, AbuOun M, Hackl E, La Ragione RM, Fookes M, et al. (2010) Epidemic multidrug-resistant (MDR-AmpC) Salmonella enterica serovar Newport strains contain three phage regions and a MDR resistance plasmid. Environ Microbiol Rep 2: 228-235. doi:10.1111/j.1758-2229.2009.00095.x. PubMed: 23766073.
44. Wu G, Carter B, Mafura M, Liebana E, Woodward MJ, et al. (2008) Genetic diversity among Escherichia coli O157:H7 isolates and identification of genes linked to human infections. Infect Immun 76: 845-856. doi:10.1128/IAI.00956-07. PubMed: 18070900.
45. Wu G, Ehricht R, Mafura M, Stokes M, Smith N, et al. (2012) Escherichia coli isolates from extraintestinal organs of livestock animals harbour diverse virulence genes and belong to multiple genetic lineages. Vet Microbiol 160: 197-206. doi:10.1016/j.vetmic.2012.05.029. PubMed: 22766078.