Extended Spectrum β-Lactamase (ESBL) producing Enterobacteriaceae started to appear in the 1980s, and have since emerged as some of the most significant hospital-acquired infections with Escherichia coli and Klebsiella being main players. More than 100 different ESBL types have been described, the most widespread being the CTX-M β-lactamase enzymes (blaCTX-M genes). This study focuses on the zoonotic dissemination of ESBL bacteria, mainly CTX-M type, in the southern coastal region of France. We found that the level of general antibiotic resistance in single randomly selected E. coli isolates from wild Yellow-legged Gulls in France was high. Nearly half the isolates (47,1%) carried resistance to one or more antibiotics (in a panel of six antibiotics), and resistance to tetracycline, ampicillin and streptomycin was most widespread. In an ESBL selective screen, 9,4% of the gulls carried ESBL producing bacteria and notably, 6% of the gulls carried bacteria harboring CTX-M-1 group of ESBL enzymes, a recently introduced and yet the most common clinical CTX-M group in France. Multi locus sequence type and phylogenetic group designations were established for the ESBL isolates, revealing that birds and humans share E. coli populations. Several ESBL producing E. coli isolated from birds were identical to or clustered with isolates with human origin. Hence, wild birds pick up E. coli of human origin, and with human resistance traits, and may accordingly also act as an environmental reservoir and melting pot of bacterial resistance with a potential to re-infect human populations.
References
[1]
Bonnet R (2004) Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 48: 1–14.
[2]
Sorum H, Sunde M (2001) Resistance to antibiotics in the normal flora of animals. Vet Res 32: 227–241.
[3]
Livermore DM, Canton R, Gniadkowski M, Nordmann P, Rossolini GM, et al. (2007) CTX-M: changing the face of ESBLs in Europe. J Antimicrob Chemother 59: 165–174.
[4]
Gordon DM, Cowling A (2003) The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149: 3575–3586.
[5]
？sterblad M, Norrdahl K, Korpimaki E, Huovinen P (2001) Antibiotic resistance. How wild are wild mammals? Nature 409: 37–38.
[6]
Sj？lund M, Bonnedahl J, Hernandez J, Bengtsson S, Cederbrant G, et al. (2008) Dissemination of multidrug-resistant bacteria into the Arctic. Emerg Infect Dis 14: 70–72.
[7]
Dolejska M, Cizek A, Literak I (2007) High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from Black-headed Gulls in the Czech Republic. J Appl Microbiol 103: 11–19.
[8]
Middleton JH, Ambrose A (2005) Enumeration and antibiotic resistance patterns of fecal indicator organisms isolated from migratory Canada geese (Branta canadensis). J Wildl Dis 41: 334–341.
[9]
Costa D, Poeta P, Saenz Y, Vinue L, Rojo-Bezares B, et al. (2006) Detection of Escherichia coli harbouring extended-spectrum beta-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J Antimicrob Chemother 58: 1311–1312.
[10]
Poeta P, Radhouani H, Igrejas G, Goncalves A, Carvalho C, et al. (2008) Seagulls of the Berlengas natural reserve of Portugal as carriers of fecal Escherichia coli harboring CTX-M and TEM extended-spectrum beta-lactamases. Appl Environ Microbiol 74: 7439–7441.
[11]
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.
[12]
Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66: 4555–4558.
[13]
Escobar-Páramo P, Grenet K, Le Menac'h A, Rode L, Salgado E, et al. (2004) Large-Scale Population Structure of Human Commensal Escherichia coli Isolates. Appl Environ Microbiol 70: 5698–5700.
[14]
Goossens H, Ferech M, Vander Stichele R, Elseviers M (2005) Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet 365: 579–587.
[15]
Galas M, Decousser JW, Breton N, Godard T, Allouch PY, et al. (2008) Nationwide study of the prevalence, characteristics, and molecular epidemiology of extended-spectrum-beta-lactamase-produci？ngEnterobacteriaceae in France. Antimicrob Agents Chemother 52: 786–789.
[16]
Crowley B, Ratcliffe G (2003) Extended-spectrum beta-lactamases in Enterobacter cloacae: underestimated but clinically significant! J Antimicrob Chemother 51: 1316–1317.
[17]
Gordon DM, Clermont O, Tolley H, Denamur E (2008) Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol 10: 2484–2496.
[18]
Lau SH, Reddy S, Cheesbrough J, Bolton FJ, Willshaw G, et al. (2008) Major uropathogenic Escherichia coli strain isolated in the northwest of England identified by multilocus sequence typing. J Clin Microbiol 46: 1076–1080.
[19]
Tartof SY, Solberg OD, Manges AR, Riley LW (2005) Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing. J Clin Microbiol 43: 5860–5864.
[20]
Johnson TJ, Wannemuehler Y, Johnson SJ, Stell AL, Doetkott C, et al. (2008) Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens. Appl Environ Microbiol 74: 7043–7050.
[21]
Moulin-Schouleur M, Reperant M, Laurent S, Bree A, Mignon-Grasteau S, et al. (2007) Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45: 3366–3376.
[22]
Melhus ？ (1996) Juhlin's medium: a selective and differential medium for gram-negative rods. Med Microbiol Lett 5: 74–81.
[23]
Kahlmeter G (2007) The Swedish Reference Group for Antibiotics (SRGA) and its subcommittee on methodology (SRGA-M).
[24]
Pitout JD, Hossain A, Hanson ND (2004) Phenotypic and molecular detection of CTX-M-beta-lactamases produced by Escherichia coli and Klebsiella spp. J Clin Microbiol 42: 5715–5721.
[25]
Pitout JD, Thomson KS, Hanson ND, Ehrhardt AF, Moland ES, et al. (1998) beta-Lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob Agents Chemother 42: 1350–1354.
[26]
Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L (2003) Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob Agents Chemother 47: 3724–3732.
[27]
Higgins J, Hohn C, Hornor S, Frana M, Denver M, et al. (2007) Genotyping of Escherichia coli from environmental and animal samples. J Microbiol Methods 70: 227–235.
