OBJECTIVES: The objective of this study was to investigate the silver gull as an indicator of environmental contamination by salmonellae and carbapenemase-producing Enterobacteriaceae (CPE) in south-east Australia. METHODS: A total of 504 cloacal samples were collected from gull chicks at three nesting colonies in New South Wales, Australia [White Bay (n = 144), Five Islands (n = 200) and Montague Island (n = 160)] and were examined for salmonellae and CPE. Isolates were tested for carbapenemase genes and susceptibility to 14 antibiotics. Clonality was determined by PFGE and MLST. Genetic context and conjugative transfer of the carbapenemase gene were determined. RESULTS: A total of 120 CPE of 10 species, mainly Escherichia coli (n = 85), carrying the gene blaIMP-4, blaIMP-38 or blaIMP-26 were obtained from 80 (40%) gulls from Five Islands. Thirty percent of birds from this colony were colonized by salmonellae. Most isolates contained the gene within a class 1 integron showing a blaIMP-4-qacG-aacA4-catB3 array. The blaIMP gene was carried by conjugative plasmids of variable sizes (80-400 kb) and diverse replicons, including HI2-N (n = 30), HI2 (11), A/C (17), A/C-Y (2), L/M (5), I1 (1) and non-typeable (6). Despite the overall high genetic variability, common clones and plasmid types were shared by different birds and bacterial isolates, respectively. CONCLUSIONS: Our data demonstrate a large-scale transmission of carbapenemase-producing bacteria into wildlife, likely as a result of the feeding habits of the birds at a local waste depot. The isolates from gulls showed significant similarities with clinical isolates from Australia, suggesting the human origin of the isolates. The sources of CPE for gulls on Five Islands should be explored and proper measures applied to stop the transmission into the environment.

Central European Institute of Technology University of Veterinary and Pharmaceutical Sciences Brno Palackeho tr 1 3 612 42 Brno Czech Republic Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary and Pharmaceutical Sciences Brno Palackeho tr 1 3 612 42 Brno Czech Republic

Central European Institute of Technology University of Veterinary and Pharmaceutical Sciences Brno Palackeho tr 1 3 612 42 Brno Czech Republic Department of Infectious Diseases and Microbiology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Palackeho tr 1 3 612 42 Brno Czech Republic

Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary and Pharmaceutical Sciences Brno Palackeho tr 1 3 612 42 Brno Czech Republic

Office of Environment and Heritage PO Box 1967 Hurstville NSW 2220 Australia

Small Animal Specialist Hospital Richardson Place 1 1 North Ryde NSW 2113 Australia

Veterinary Research Institute Hudcova 296 70 621 00 Brno Czech Republic

Zobrazit více v PubMed

Cornaglia G, Giamarellou H, Rossolini GM. Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect Dis 2011; 11: 381–93. PubMed

Zhao WH, Hu ZQ. IMP-type metallo-β-lactamases in Gram-negative bacilli: distribution, phylogeny, and association with integrons. Crit Rev Microbiol 2011; 37: 214–26. PubMed

Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 2011; 17: 1791–8. PubMed PMC

Hu L, Zhong Q, Shang Y et al. . The prevalence of carbapenemase genes and plasmid-mediated quinolone resistance determinants in carbapenem-resistant Enterobacteriaceae from five teaching hospitals in central China. Epidemiol Infect 2014; 142: 1972–7. PubMed PMC

Hong JS, Kim JO, Lee HB. Characteristics of metallo-β-lactamase-producing Pseudomonas aeruginosa in Korea. Infect Chemother 2015; 47: 33–40. PubMed PMC

Peirano G, Lascols C, Hackel M et al. . Molecular epidemiology of Enterobacteriaceae that produce VIMs and IMPs from the SMART surveillance program. Diagn Microbiol Infect Dis 2014; 78: 277–81. PubMed

Leung GH, Gray TJ, Cheong EY et al. . Persistence of related blaIMP-4 metallo-β-lactamase producing Enterobacteriaceae from clinical and environmental specimens within a burns unit in Australia—a six-year retrospective study. Antimicrob Resist Infect Control 2013; 2: 35. PubMed PMC

Guerra B, Fischer J, Helmuth R. An emerging public health problem: acquired carbapenemase-producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Vet Microbiol 2014; 171: 290–7. PubMed

Palmgren H, Aspan A, Broman T et al. . Salmonella in black-headed gulls (Larus ridibundus); prevalence, genotypes and influence on Salmonella epidemiology. Epidemiol Infect 2006; 134: 635–44. PubMed PMC

Iveson JB, Shellam GR, Bradshaw SD et al. . Salmonella infections in Antarctic fauna and island populations of wildlife exposed to human activities in coastal areas of Australia. Epidemiol Infect 2009; 137: 858–70. PubMed

Smith GC, Carlile N. Habitat use by silver gulls Larus novaehollandiae in the Sydney-Wollongong region, New South Wales. Wetlands (Australia) 1992; 11: 33–46.

Smith GC, Carlile N. Food and feeding ecology of breeding silver gulls (Larus novaehollandiae) in urban Australia. Colonial Waterbirds 1993; 16: 9–17.

Grimont P, Weill F. Antigenic Formulae of the Salmonella Serovars. 9th edn Paris, France: WHO Collaborating Centre for Reference and Research on Salmonella, 2007.

Anderson ES, Ward LR, Saxe MJ et al. . Bacteriophage-typing designations of Salmonella typhimurium. J Hyg (Lond) 1977; 78: 297–300. PubMed PMC

Ward LR, de Sa JD, Rowe B. A phage-typing scheme for Salmonella enteritidis. Epidemiol Infect 1987; 99: 291–4. PubMed PMC

Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fourth Informational Supplement M100-S24. CLSI, Wayne, PA, USA, 2014.

Dunne MW, Hardin DJ. Use of several inducer and substrate antibiotic combinations in a disk approximation assay format to screen for AmpC induction in patient isolates of Pseudomonas aeruginosa, Enterobacter spp., Citrobacter spp., and Serratia spp. J Clin Microbiol 2005; 43: 5945–9. PubMed PMC

Giske CG, Gezelius L, Samuelsen Ø et al. . A sensitive and specific phenotypic assay for detection of metallo-β-lactamases and KPC in Klebsiella pneumoniae with the use of meropenem disks supplemented with aminophenylboronic acid, dipicolinic acid and cloxacillin. Clin Microbiol Infect 2011; 17: 552–6. PubMed

Diancourt L, Passet V, Verhoef J et al. . Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 2005; 43: 4178–82. PubMed PMC

Wirth T, Falush D, Lan R et al. . Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006; 60: 1136–51. PubMed PMC

Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66: 4555–8. PubMed PMC

Espedido BA, Partridge SR, Iredell JR. blaIMP-4 in different genetic contexts in Enterobacteriaceae isolates from Australia. Antimicrob Agents Chemother 2008; 52: 2984–7. PubMed PMC

Maher D, Taylor DE. Host range and transfer efficiency of incompatibility group HI plasmid. Can J Microbiol 1993; 39: 581–7. PubMed

Carattoli A, Bertini A, Villa L et al. . Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 2005; 63: 219–28. PubMed

Garcia-Fernandez A, Fortini D, Veldman K et al. . Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 2009; 63: 274–81. PubMed

Powling J. National Enteric Pathogens Surveillance Scheme, Human Annual Report 1996–2010. Victoria: Microbiological Diagnostic Unit, University of Melbourne, 2010.

Rabsch W, Andrews HL, Kingsley RA et al. . Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun 2002; 70: 2249–55. PubMed PMC

Australian Group on Antimicrobial Resistance. The Evolution of Carbapenemases in Enterobacteriaceae in Australia. Updated 20 October 2014. http://www.agargroup.org/files/AGAR_Carbapenemase_evolution%20Final.pdf.

Dahmen S, Metayer V, Gay E et al. . Characterization of extended-spectrum β-lactamase (ESBL)-carrying plasmids and clones of Enterobacteriaceae causing cattle mastitis in France. Vet Microbiol 2013; 162: 793–9. PubMed

Fischer J, Rodriguez I, Baumann B et al. . blaCTX-M-15-carrying Escherichia coli and Salmonella isolates from livestock and food in Germany. J Antimicrob Chemother 2014; 69: 2951–8. PubMed

Izdebski R, Baraniak A, Fiett J et al. . Clonal structure, extended-spectrum β-lactamases, and acquired AmpC-type cephalosporinases of Escherichia coli populations colonizing patients in rehabilitation centers in four countries. Antimicrob Agents Chemother 2013; 57: 309–16. PubMed PMC

Guo S, Wakeham D, Brouwers HJ et al. . Human-associated fluoroquinolone-resistant Escherichia coli clonal lineages, including ST354, isolated from canine feces and extraintestinal infections in Australia. Microbes Infect 2015; 17: 266–74. PubMed

Sidjabat HE, Townell N, Nimmo GR et al. . Dominance of IMP-4-producing Enterobacter cloacae amongst carbapenemase-producing Enterobacteriaceae in Australia. Antimicrob Agents Chemother 2015; 59: 4059–66. PubMed PMC

Lo WU, Cheung YY, Lai E et al. . Complete sequence of an IncN plasmid, pIMP-HZ1, carrying blaIMP-4 in a Klebsiella pneumoniae strain associated with medical travel to China. Antimicrob Agents Chemother 2013; 57: 1561–2. PubMed PMC

Antibiotic-resistant Escherichia coli from treated municipal wastewaters and Black-headed Gull nestlings on the recipient river

VIM-1-producing Enterobacter asburiae with mobile colistin resistance genes from wastewaters

Phylogenomic analysis of a global collection of Escherichia coli ST38: evidence of interspecies and environmental transmission?

Hospital and community wastewater as a source of multidrug-resistant ESBL-producing Escherichia coli

Interspecies Transmission of CMY-2-Producing Escherichia coli Sequence Type 963 Isolates between Humans and Gulls in Australia

Genomic Analysis of an I1 Plasmid Hosting a sul3-Class 1 Integron and blaSHV-12 within an Unusual Escherichia coli ST297 from Urban Wildlife

Urban Wildlife Crisis: Australian Silver Gull Is a Bystander Host to Widespread Clinical Antibiotic Resistance

Epidemic HI2 Plasmids Mobilising the Carbapenemase Gene blaIMP-4 in Australian Clinical Samples Identified in Multiple Sublineages of Escherichia coli ST216 Colonising Silver Gulls

Carbapenemase-Producing Gram-Negative Bacteria from American Crows in the United States

Escherichia coli Sequence Type 457 Is an Emerging Extended-Spectrum-β-Lactam-Resistant Lineage with Reservoirs in Wildlife and Food-Producing Animals

Wildlife Is Overlooked in the Epidemiology of Medically Important Antibiotic-Resistant Bacteria

Characterization of the Complete Nucleotide Sequences of IMP-4-Encoding Plasmids, Belonging to Diverse Inc Families, Recovered from Enterobacteriaceae Isolates of Wildlife Origin

Characterization of the Complete Nucleotide Sequences of IncA/C2 Plasmids Carrying In809-Like Integrons from Enterobacteriaceae Isolates of Wildlife Origin