Research Open Access
Like 0



Carbapenem-resistant Enterobacteriaceae pose a serious threat to public health worldwide, and the role of companion animals as a reservoir is still unclear.


This 4-month prospective observational study evaluated carriage of carbapenem-resistant Enterobacteriaceae at admission and after hospitalisation in a large referral hospital for companion animals in Switzerland.


Rectal swabs of dogs and cats expected to be hospitalised for at least 48 h were taken from May to August 2018 and analysed for the presence of carbapenem-resistant Enterobacteriaceae using selective agar plates. Resistant isolates were further characterised analysing whole genome sequences for resistance gene and plasmid identification, and ad hoc core genome multilocus sequence typing.


This study revealed nosocomial acquisition of harbouring the carbapenemase gene , the pAmpC cephalosporinase gene as well as quinolone resistance associated with and mutations in the topoisomerases II (GyrA) and IV (ParC). The and genes were identified on a 51 kb IncX3 plasmid and on a 47 kb IncI1 plasmid. All isolates belonged to sequence type ST410 and were genetically highly related. This clone was detected in 17 of 100 dogs and four of 34 cats after hospitalisation (21.6%), only one of the tested animals having tested positive at admission (0.75%). Two positive animals were still carriers 4 months after hospital discharge, but were negative after 6 months.


Companion animals may acquire carbapenemase-producing during hospitalisation, posing the risk of further dissemination to the animal and human population and to the environment.


Article metrics loading...

Loading full text...

Full text loading...



  1. Hooper DC, Jacoby GA. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci. 2015;1354(1):12-31.  https://doi.org/10.1111/nyas.12830  PMID: 26190223 
  2. Fernandes R, Amador P, Prudêncio C. β-lactams: chemical structure, mode of action and mechanisms of resistance. Rev Med Microbiol. 2013;24(1):7-17.  https://doi.org/10.1097/MRM.0b013e3283587727 
  3. Patel G, Bonomo RA. "Stormy waters ahead": global emergence of carbapenemases. Front Microbiol. 2013;4:48.  https://doi.org/10.3389/fmicb.2013.00048  PMID: 23504089 
  4. Nordmann P, Gniadkowski M, Giske CG, Poirel L, Woodford N, Miriagou V, et al. Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect. 2012;18(5):432-8.  https://doi.org/10.1111/j.1469-0691.2012.03815.x  PMID: 22507110 
  5. Poirel L, Potron A, Nordmann P. OXA-48-like carbapenemases: the phantom menace. J Antimicrob Chemother. 2012;67(7):1597-606.  https://doi.org/10.1093/jac/dks121  PMID: 22499996 
  6. Poirel L, Stephan R, Perreten V, Nordmann P. The carbapenemase threat in the animal world: the wrong culprit. J Antimicrob Chemother. 2014;69(7):2007-8.  https://doi.org/10.1093/jac/dku054  PMID: 24576948 
  7. Stolle I, Prenger-Berninghoff E, Stamm I, Scheufen S, Hassdenteufel E, Guenther S, et al. Emergence of OXA-48 carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in dogs. J Antimicrob Chemother. 2013;68(12):2802-8.  https://doi.org/10.1093/jac/dkt259  PMID: 23833179 
  8. Melo LC, Boisson MN, Saras E, Médaille C, Boulouis HJ, Madec JY, et al. OXA-48-producing ST372 Escherichia coli in a French dog. J Antimicrob Chemother. 2017;72(4):1256-8. PMID: 28039279 
  9. Liu X, Thungrat K, Boothe DM. Occurrence of OXA-48 carbapenemase and other beta-lactamase genes in ESBL-producing multidrug resistant Escherichia coli from dogs and cats in the United States, 2009-2013. Front Microbiol. 2016;7:1057. PMID: 27462301 
  10. Yousfi M, Touati A, Mairi A, Brasme L, Gharout-Sait A, Guillard T, et al. Emergence of carbapenemase-producing Escherichia coli isolated from companion animals in Algeria. Microb Drug Resist. 2016;22(4):342-6.  https://doi.org/10.1089/mdr.2015.0196  PMID: 26741510 
  11. Gentilini F, Turba ME, Pasquali F, Mion D, Romagnoli N, Zambon E, et al. Hospitalized pets as a source of carbapenem-resistance. Front Microbiol. 2018;9(2872):2872.  https://doi.org/10.3389/fmicb.2018.02872  PMID: 30574124 
  12. Pires J, Novais A, Peixe L. Blue-carba, an easy biochemical test for detection of diverse carbapenemase producers directly from bacterial cultures. J Clin Microbiol. 2013;51(12):4281-3.  https://doi.org/10.1128/JCM.01634-13  PMID: 24108615 
  13. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0, 2019. Växjö: EUCAST; 2019. Available from: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_9.0_Breakpoint_Tables.pdforg
  14. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 26th ed. CLSI document M100- S27. Wayne, PA: CLSI; 2017.
  15. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12(1):402.  https://doi.org/10.1186/1471-2164-12-402  PMID: 21824423 
  16. Reynolds ME, Phan HTT, George S, Hubbard ATM, Stoesser N, Maciuca IE, et al. Occurrence and characterization of Escherichia coli ST410 co-harbouring blaNDM-5, blaCMY-42 and blaTEM-190 in a dog from the UK. J Antimicrob Chemother. 2019;74(5):1207-11.  https://doi.org/10.1093/jac/dkz017  PMID: 30753576 
  17. Evans BA, Amyes SG. OXA β-lactamases. Clin Microbiol Rev. 2014;27(2):241-63.  https://doi.org/10.1128/CMR.00117-13  PMID: 24696435 
  18. Liu Y, Feng Y, Wu W, Xie Y, Wang X, Zhang X, et al. First report of OXA-181-producing Escherichia coli in China and characterization of the isolate using whole-genome sequencing. Antimicrob Agents Chemother. 2015;59(8):5022-5.  https://doi.org/10.1128/AAC.00442-15  PMID: 26014927 
  19. Qin S, Cheng J, Wang P, Feng X, Liu HM. Early emergence of OXA-181-producing Escherichia coli ST410 in China. J Glob Antimicrob Resist. 2018;15:215-8.  https://doi.org/10.1016/j.jgar.2018.06.017  PMID: 30393155 
  20. Overballe-Petersen S, Roer L, Ng K, Hansen F, Justesen US, Andersen LP, et al. Complete nucleotide sequence of an Escherichia coli sequence type 410 strain carrying blaNDM-5 on an IncF multidrug resistance plasmid and blaOXA-181 on an IncX3 plasmid. Genome Announc. 2018;6(5):e01542-17.  https://doi.org/10.1128/genomeA.01542-17  PMID: 29437102 
  21. Bitar I, Dagher C, Salloum T, Araj G, Tokajian S. First report of an Escherichia coli from Lebanon carrying an OXA-181 carbapenemase resistance determinant. J Glob Antimicrob Resist. 2018;12:113-4.  https://doi.org/10.1016/j.jgar.2018.01.002  PMID: 29353076 
  22. Pulss S, Semmler T, Prenger-Berninghoff E, Bauerfeind R, Ewers C. First report of an Escherichia coli strain from swine carrying an OXA-181 carbapenemase and the colistin resistance determinant MCR-1. Int J Antimicrob Agents. 2017;50(2):232-6.  https://doi.org/10.1016/j.ijantimicag.2017.03.014  PMID: 28666753 
  23. Zurfluh K, Poirel L, Nordmann P, Klumpp J, Stephan R. First detection of Klebsiella variicola producing OXA-181 carbapenemase in fresh vegetable imported from Asia to Switzerland. Antimicrob Resist Infect Control. 2015;4(1):38.  https://doi.org/10.1186/s13756-015-0080-5  PMID: 26448862 
  24. Feng Y, Yang P, Xie Y, Wang X, McNally A, Zong Z. Escherichia coli of sequence type 3835 carrying blaNDM-1, blaCTX-M-15, blaCMY-42 and blaSHV-12. Sci Rep. 2015;5(1):12275.  https://doi.org/10.1038/srep12275  PMID: 26194736 
  25. Sugawara Y, Akeda Y, Sakamoto N, Takeuchi D, Motooka D, Nakamura S, et al. Genetic characterization of blaNDM-harboring plasmids in carbapenem-resistant Escherichia coli from Myanmar. PLoS One. 2017;12(9):e0184720.  https://doi.org/10.1371/journal.pone.0184720  PMID: 28910381 
  26. Bitar I, Piazza A, Gaiarsa S, Villa L, Pedroni P, Oliva E, et al. ST405 NDM-5 producing Escherichia coli in Northern Italy: the first two clinical cases. Clin Microbiol Infect. 2017;23(7):489-90.  https://doi.org/10.1016/j.cmi.2017.01.020  PMID: 28159670 
  27. Akiba M, Sekizuka T, Yamashita A, Kuroda M, Fujii Y, Murata M, et al. Distribution and relationships of antimicrobial resistance determinants among extended-spectrum-cephalosporin-resistant or carbapenem-resistant Escherichia coli isolates from rivers and sewage treatment plants in India. Antimicrob Agents Chemother. 2016;60(5):2972-80.  https://doi.org/10.1128/AAC.01950-15  PMID: 26953207 
  28. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M, Røder BL, et al. Escherichia coli sequence type 410 is causing new international high-risk clones. MSphere. 2018;3(4):e00337-18.  https://doi.org/10.1128/mSphere.00337-18  PMID: 30021879 
  29. Schaufler K, Semmler T, Wieler LH, Wöhrmann M, Baddam R, Ahmed N, et al. Clonal spread and interspecies transmission of clinically relevant ESBL-producing Escherichia coli of ST410--another successful pandemic clone? FEMS Microbiol Ecol. 2016;92(1):fiv155.  https://doi.org/10.1093/femsec/fiv155  PMID: 26656065 
  30. Piazza A, Comandatore F, Romeri F, Pagani C, Floriano AM, Ridolfo A, et al. First report of an ST410 OXA-181 and CTX-M-15 coproducing Escherichia coli clone in Italy: a whole-genome sequence characterization. Microb Drug Resist. 2018;24(8):1207-9.  https://doi.org/10.1089/mdr.2017.0366  PMID: 29473791 
  31. Wohlwend N, Endimiani A, Francey T, Perreten V. Third-generation-cephalosporin-resistant Klebsiella pneumoniae isolates from humans and companion animals in Switzerland: spread of a DHA-producing sequence type 11 clone in a veterinary setting. Antimicrob Agents Chemother. 2015;59(5):2949-55.  https://doi.org/10.1128/AAC.04408-14  PMID: 25733505 
  32. Federal Office of Public Health (FOPH) and Federal Food Safety and Veterinary Office. Swiss Antibiotic Resistance Report 2018. Usage of Antibiotics and Occurrence of Antibiotic Resistance in Bacteria from Humans and Animals in Switzerland. November 2018; FOPH publication number: 2018-OEG-87. Bern: FOPH; 2018. Available from: https://www.bag.admin.ch/dam/bag/de/dokumente/mt/star/swiss-antibiotic-resistance-report-2018.pdf

Data & Media loading...

Submit comment
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error