Resistance to critically important antimicrobials in Australian silver gulls (Chroicocephalus novaehollandiae) and evidence of anthropogenic origins

Journal of Antimicrobial Chemotherapy - Tập 74 Số 9 - Trang 2566-2574 - 2019
S.K. Mukerji1,2, Marc Stegger1,3, Alec Truswell1, Tanya Laird1, David Jordan4, Rebecca Abraham1, Ali Harb1, Mary Barton5, Mark O’Dea1, Sam Abraham1
1Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia
2School of Animal and Veterinary Sciences, The University of Adelaide, Roseworthy, South Australia, Australia
3Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark
4NSW Department of Primary Industries, Wollongbar, New South Wales, Australia
5School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia, Australia

Tóm tắt

Abstract Objectives Antimicrobial resistance (AMR) to critically important antimicrobials (CIAs) amongst Gram-negative bacteria can feasibly be transferred amongst wildlife, humans and domestic animals. This study investigated the ecology, epidemiology and origins of CIA-resistant Escherichia coli carried by Australian silver gulls (Chroicocephalus novaehollandiae), a gregarious avian wildlife species that is a common inhabitant of coastal areas with high levels of human contact. Methods Sampling locations were widely dispersed around the perimeter of the Australian continent, with sites separated by up to 3500 km. WGS was used to study the diversity and molecular characteristics of resistant isolates to ascertain their epidemiological origin. Results Investigation of 562 faecal samples revealed widespread occurrence of extended-spectrum cephalosporin-resistant (21.7%) and fluoroquinolone-resistant (23.8%) E. coli. Genome sequencing revealed that CIA-resistant E. coli isolates (n = 284) from gulls predominantly belonged to human-associated extra-intestinal pathogenic E. coli (ExPEC) clones, including ST131 (17%), ST10 (8%), ST1193 (6%), ST69 (5%) and ST38 (4%). Genomic analysis revealed that gulls carry pandemic ExPEC-ST131 clades (O25:H4 H30-R and H30-Rx) and globally emerging fluoroquinolone-resistant ST1193 identified among humans worldwide. Comparative analysis revealed that ST131 and ST1193 isolates from gulls overlapped extensively with human clinical isolates from Australia and overseas. The present study also detected single isolates of carbapenem-resistant E. coli (ST410-blaOXA-48) and colistin-resistant E. coli (ST345-mcr-1). Conclusions The carriage of diverse CIA-resistant E. coli clones that strongly resemble pathogenic clones from humans suggests that gulls can act as ecological sponges indiscriminately accumulating and disseminating CIA-resistant bacteria over vast distances.

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Tài liệu tham khảo

Viens, 2015, Is antimicrobial resistance a slowly emerging disaster?, Public Health Ethics, 8, 255

Mukerji, 2017, Development and transmission of antimicrobial resistance among Gram-negative bacteria in animals and their public health impact, Essays Biochem, 61, 23, 10.1042/EBC20160055

Abraham, 2014, Carbapenemase-producing bacteria in companion animals: a public health concern on the horizon, J Antimicrob Chemother, 69, 1155, 10.1093/jac/dkt518

Radhouani, 2014, Potential impact of antimicrobial resistance in wildlife, environment and human health, Front Microbiol, 5, 23, 10.3389/fmicb.2014.00023

Agersø, 2012, Prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail meat identified by selective enrichment and association with cephalosporin usage, J Antimicrob Chemother, 67, 582, 10.1093/jac/dkr507

Ewers, 2010, Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-β-lactamase-producing Escherichia coli among companion animals, J Antimicrob Chemother, 65, 651, 10.1093/jac/dkq004

Liakopoulos, 2016, The colistin resistance mcr-1 gene is going wild, J Antimicrob Chemother, 71, 2335, 10.1093/jac/dkw262

Stedt, 2015, Carriage of CTX-M type extended spectrum β-lactamases (ESBLs) in gulls across Europe, Acta Vet Scand, 57, 74, 10.1186/s13028-015-0166-3

Villa, 2015, IncA/C plasmid carrying blaNDM-1, blaCMY-16, and fosA3 in a Salmonella enterica serovar Corvallis strain isolated from a migratory wild bird in Germany, Antimicrob Agents Chemother, 59, 6597, 10.1128/AAC.00944-15

Vittecoq, 2017, VIM-1 carbapenemase-producing Escherichia coli in gulls from southern France, Ecol Evol, 7, 1224, 10.1002/ece3.2707

Smith, 2014, Antimicrobial resistant bacteria in wild mammals and birds: a coincidence or cause for concern?, Ir Vet J, 67, 8., 10.1186/2046-0481-67-8

Alonso, 2017, High frequency of B2 phylogroup among non-clonally related fecal Escherichia coli isolates from wild boars, including the lineage ST131, FEMS Microbiol Ecol, 93, fix016, 10.1093/femsec/fix016

Abraham, 2014, Salmonella enterica isolated from infections in Australian livestock remain susceptible to critical antimicrobials, Int J Antimicrob Agents, 43, 126, 10.1016/j.ijantimicag.2013.10.014

Abraham, 2015, First detection of extended-spectrum cephalosporin- and fluoroquinolone-resistant Escherichia coli in Australian food-producing animals, J Glob Antimicrob Resist, 3, 273, 10.1016/j.jgar.2015.08.002

Abraham, 2014, Phylogenetic and molecular insights into the evolution of multidrug-resistant porcine enterotoxigenic Escherichia coli in Australia, Int J Antimicrob Agents, 44, 105, 10.1016/j.ijantimicag.2014.04.011

Barlow, 2015, Prevalence and antimicrobial resistance of Salmonella and Escherichia coli from Australian cattle populations at slaughter, J Food Prot, 78, 912, 10.4315/0362-028X.JFP-14-476

Abraham, 2016, Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats, Sci Rep, 6, 35527, 10.1038/srep35527

Dolejska, 2016, High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the silver gull on Five Islands, Australia, J Antimicrob Chemother, 71, 63, 10.1093/jac/dkv306

Kidsley, 2018, Antimicrobial susceptibility of Escherichia coli and Salmonella spp. isolates from healthy pigs in Australia: results of a pilot national survey, Front Microbiol, 9, 1207., 10.3389/fmicb.2018.01207

2019, Performance Standards for Antimicrobial Susceptibility Testing—Twenty-Ninth Edition

Abraham, 2018, Dissemination and persistence of extended-spectrum cephalosporin-resistance encoding IncI1-blaCTXM-1 plasmid among Escherichia coli in pigs, ISME J, 12, 2352, 10.1038/s41396-018-0200-3

Seemann

Croucher, 2015, Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins, Nucleic Acids Research, 43, e15., 10.1093/nar/gku1196

Guindon, 2010, New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0, Syst Biol, 59, 307, 10.1093/sysbio/syq010

Price, 2013, The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx, Mbio, 4, e00377, 10.1128/mBio.00377-13

Sahl, 2016, NASP: an accurate, rapid method for the identification of SNPs in WGS datasets that supports flexible input and output formats, Microb Genom, 2, e000074.

Letunic, 2016, Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees, Nucleic Acids Res, 44, 242, 10.1093/nar/gkw290

Banerjee, 2014, A new clone sweeps clean: the enigmatic emergence of Escherichia coli sequence type 131, Antimicrob Agents Chemother, 58, 4997, 10.1128/AAC.02824-14

Nicolas-Chanoine, 2008, Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15, J Antimicrob Chemother, 61, 273, 10.1093/jac/dkm464

Tchesnokova, 2018, Rapid and extensive expansion in the U.S. of a new multidrug-resistant Escherichia coli clonal group, sequence type ST1193, Clin Infect Dis, 68, 334, 10.1093/cid/ciy525

Nüesch-Inderbinen, 2017, Clonal diversity, virulence potential and antimicrobial resistance of Escherichia coli causing community acquired urinary tract infection in Switzerland, Front Microbiol, 8, 2334, 10.3389/fmicb.2017.02334

2017

Johnson, 2012, Molecular epidemiological analysis of Escherichia coli sequence type ST131 (O25:H4) and blaCTX-M-15 among extended-spectrum-β-lactamase-producing E. coli from the United States, 2000 to 2009, Antimicrob Agents Chemother, 56, 2364, 10.1128/AAC.05824-11

Totsika, 2011, Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms, PLoS One, 6, e26578., 10.1371/journal.pone.0026578

Gibreel, 2012, Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from Northwest England, J Antimicrob Chemother, 67, 346, 10.1093/jac/dkr451

Coque, 2008, Dissemination of clonally related Escherichia coli strains expressing extended-spectrum β-lactamase CTX-M-15, Emerg Infect Dis, 14, 195, 10.3201/eid1402.070350

Tacão, 2017, mcr-1 and blaKPC-3 in Escherichia coli sequence type 744 after meropenem and colistin therapy, Portugal, Emerg Infect Dis, 23, 1419, 10.3201/eid2308.170162

Poirel, 2004, Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae, Antimicrob Agents Chemother, 48, 15, 10.1128/AAC.48.1.15-22.2004

Mairi, 2018, OXA-48-like carbapenemases producing Enterobacteriaceae in different niches, Eur J Clin Microbiol Infect Dis, 37, 587, 10.1007/s10096-017-3112-7

Lübbert, 2017, Environmental pollution with antimicrobial agents from bulk drug manufacturing industries in Hyderabad, South India, is associated with dissemination of extended-spectrum β-lactamase and carbapenemase-producing pathogens, Infection, 45, 479, 10.1007/s15010-017-1007-2

Stolle, 2013, Emergence of OXA-48 carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in dogs, J Antimicrob Chemother, 68, 2802, 10.1093/jac/dkt259

Roer, 2018, Escherichia coli sequence type 410 is causing new international high-risk clones, mSphere, 3, 10.1128/mSphere.00337-18

Ruzauskas, 2016, Detection of the mcr-1 gene in Escherichia coli prevalent in the migratory bird species Larus argentatus, J Antimicrob Chemother, 71, 2333, 10.1093/jac/dkw245

Mohsin, 2016, First description of plasmid-mediated colistin-resistant extended-spectrum β-lactamase-producing Escherichia coli in a wild migratory bird from Asia, Int J Antimicrob Agents, 48, 463, 10.1016/j.ijantimicag.2016.07.001

Guenther, 2011, Extended-spectrum β-lactamases producing E. coli in wildlife, yet another form of environmental pollution?, Front Microbiol, 2, 246, 10.3389/fmicb.2011.00246

Murray, 1964, Seasonal movements and habitats of the silver gull, Larus novaehollandiae Stephens, in south-eastern Australia, CSIRO Wildl Res, 9, 160, 10.1071/CWR9640160

Tizard, 2004, Salmonellosis in wild birds, Semin Avian Exot Pet Med, 13, 50, 10.1053/j.saep.2004.01.008

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Journal of Antimicrobial Chemotherapy

Tập 74 Số 9

2566-2574

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