Cited by 170Antibiotic Resistance in BacteriaAntibiotic Use and ResistanceSalmonella and Campylobacter epidemiology

Sharing more than friendship – transmission of NDM-5 ST167 and CTX-M-9 ST69 Escherichia coli between dogs and humans in a family, Finland, 2015

Open access
Grönthal, Thomas, Österblad, Monica, Eklund, Marjut, Jalava, Jari, Nykäsenoja, Suvi, Pekkanen, Katariina, Rantala, Merja·2018·Eurosurveillance

Abstract

Introduction: Carbapenemase-producing Enterobacteriaceae (CPE) have rarely been reported in dogs, and never in animals in Finland. However, in April 2015, two meropenem-resistant Escherichia coli were identified from two dogs in one family. Both dogs suffered from chronic otitis externa . Methods: Epidemiological and molecular investigations (pulsed-field gel electrophoresis (PFGE), multilocus sequence typing) were conducted to investigate the source of infection and transmission routes. Results: In both dogs and one family member New Delhi metallo-beta-lactamase (NDM-5)-producing multidrug-resistant ST167 E. coli was found. Whole genome sequencing confirmed that the isolates were identical or only had one or two allelic differences. Additionally, the dogs and humans of the family carried an identical extended-spectrum beta-lactamase (ESBL) CTX-M-group 9 E. coli ST69 strain, indicating interspecies transmission. While the original source remains unclear, human-to-canine transmission is possible. No carbapenems had been administered to the dogs, but exposure to numerous other antimicrobials likely sustained the bacteria and supported its propagation in the canine host. Conclusion: To our knowledge, canine clinical NDM-5 E. coli in Europe, and confirmed CPE transmission between dogs and humans have not been previously reported. The screening of veterinary Enterobacteriaceae isolates for carbapenem resistance is highly recommended.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.2807/1560-7917.es.2018.23.27.1700497

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Dog owners who did not consider obesity to be a disease were more likely to have obese dogs.

    “Dog owners who did not consider obesity to be a disease, maybe because the facial features of their pets fit the concept of baby schema [87], were more likely to have obese dogs [97].”

    From A One Health Perspective on the Human-Companion Animal Relationship with Emphasis on Zoonotic Aspects. (2020) · cites this paper as [97]

    The Results (Epidemiological investigation and Case presentations; page unavailable) describe two dogs, their owners, and the dogs’ ear infections. The Discussion addresses antibiotic-resistant E. coli transmission. Searches for obesity as a disease and for owners’ perceptions of canine weight found no passage addressing the claimed association. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 34

  1. [1]Shaikh S Fatima J Shakil S Rizvi SM Kamal MA Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi J Biol Sci. 2015; 22(1): 90- 101. 10.1016/j.sjbs.2014.08.002 25561890 PMC4281622 · DOI · Paper page
  2. [2]Meletis G Carbapenem resistance: overview of the problem and future perspectives. Ther Adv Infect Dis. 2016; 3(1): 15- 21. 10.1177/2049936115621709 26862399 PMC4735501 · DOI
  3. [3]Wang Q Zhang Y Yao X Xian H Liu Y Li H Risk factors and clinical outcomes for carbapenem-resistant Enterobacteriaceae nosocomial infections. Eur J Clin Microbiol Infect Dis. 2016; 35(10): 1679- 89. 10.1007/s10096-016-2710-0 27401905 · DOI
  4. [4]Lee CR Lee JH Park KS Kim YB Jeong BC Lee SH Global Dissemination of Carbapenemase-Producing Klebsiella pneumoniae: Epidemiology, Genetic Context, Treatment Options, and Detection Methods. Front Microbiol. 2016; 7: 895. 10.3389/fmicb.2016.00895 27379038 PMC4904035 · DOI
  5. [5]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(3-4): 290- 7. 10.1016/j.vetmic.2014.02.001 24629777 · DOI
  6. [6]Woodford N Wareham DW Guerra B Teale C Carbapenemase-producing Enterobacteriaceae and non-Enterobacteriaceae from animals and the environment: an emerging public health risk of our own making? J Antimicrob Chemother. 2014; 69(2): 287- 91. 10.1093/jac/dkt392 24092657 · DOI
  7. [7]McLaughlin M Advincula MR Malczynski M Qi C Bolon M Scheetz MH Correlations of antibiotic use and carbapenem resistance in enterobacteriaceae. Antimicrob Agents Chemother. 2013; 57(10): 5131- 3. 10.1128/AAC.00607-13 23836188 PMC3811461 · DOI
  8. [11]Garcia LS, Isenberg HD. Clinical microbiology procedures handbook. 3rd ed. Washington, DC: ASM Press; 2010.
  9. [15]Österblad M Kirveskari J Hakanen AJ Tissari P Vaara M Jalava J Carbapenemase-producing Enterobacteriaceae in Finland: the first years (2008-11). J Antimicrob Chemother. 2012; 67(12): 2860- 4. 10.1093/jac/dks299 22855858 · DOI
  10. [18]Lau SH Reddy S Cheesbrough J Bolton FJ Willshaw G Cheasty T Major uropathogenic Escherichia coli strain isolated in the northwest of England identified by multilocus sequence typing. J Clin Microbiol. 2008; 46(3): 1076- 80. 10.1128/JCM.02065-07 18199778 PMC2268376 · DOI
  11. [19]Mulvey MR Soule G Boyd D Demczuk W Ahmed R Multi-provincial Salmonella Typhimurium Case Control Study Group Characterization of the first extended-spectrum beta-lactamase-producing Salmonella isolate identified in Canada. J Clin Microbiol. 2003; 41(1): 460- 2. 10.1128/JCM.41.1.460-462.2003 12517894 PMC149628 · DOI
  12. [20]Nyberg SD Osterblad M Hakanen AJ Huovinen P Jalava J The Finnish Study Group For Antimicrobial Resistance Detection and molecular genetics of extended-spectrum beta-lactamases among cefuroxime-resistant Escherichia coli and Klebsiella spp. isolates from Finland, 2002-2004. Scand J Infect Dis. 2007; 39(5): 417- 24. 10.1080/00365540601105731 17464864 · DOI
  13. [21]Haanperä M Forssten SD Huovinen P Jalava J Typing of SHV extended-spectrum beta-lactamases by pyrosequencing in Klebsiella pneumoniae strains with chromosomal SHV beta-lactamase. Antimicrob Agents Chemother. 2008; 52(7): 2632- 5. 10.1128/AAC.01259-07 18458132 PMC2443882 · DOI
  14. [22]Pérez-Pérez FJ Hanson ND Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol. 2002; 40(6): 2153- 62. 10.1128/JCM.40.6.2153-2162.2002 12037080 PMC130804 · DOI
  15. [23]Zankari E Hasman H Cosentino S Vestergaard M Rasmussen S Lund O Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012; 67(11): 2640- 4. 10.1093/jac/dks261 22782487 PMC3468078 · DOI · Paper page
  16. [24]Carattoli A Zankari E García-Fernández A Voldby Larsen M Lund O Villa L In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014; 58(7): 3895- 903. 10.1128/AAC.02412-14 24777092 PMC4068535 · DOI · Paper page
  17. [25]Ljungquist O Ljungquist D Myrenås M Rydén C Finn M Bengtsson B Evidence of household transfer of ESBL-/pAmpC-producing Enterobacteriaceae between humans and dogs - a pilot study. Infect Ecol Epidemiol. 2016; 6(1): 31514. 10.3402/iee.v6.31514 27330043 PMC4916256 · DOI
  18. [27]Berrazeg M Diene S Medjahed L Parola P Drissi M Raoult D New Delhi Metallo-beta-lactamase around the world: an eReview using Google Maps. Euro Surveill. 2014; 19(20): 20809. 10.2807/1560-7917.ES2014.19.20.20809 24871756 · DOI
  19. [31]Päivärinta M Pohjola L Fredriksson-Ahomaa M Heikinheimo A Low Occurrence of Extended-Spectrum β-lactamase-Producing Escherichia coli in Finnish Food-Producing Animals. Zoonoses Public Health. 2016; 63(8): 624- 31. 10.1111/zph.12277 27215423 · DOI
  20. [32]Österblad M Norrdahl K Korpimäki E Huovinen P Antibiotic resistance. How wild are wild mammals? Nature. 2001; 409(6816): 37- 8. 10.1038/35051173 11343104 · DOI
  21. [33]Jalava JVN, Miettinen S, Pelkonen S, Rantala M. Prevalence of third-generation cephalosporinresistant Escherichia coli and their resistance mechanisms in dogs in Finland, P1107 abstract. 22nd ECCMID Conference; 31 March – 3 April 2012; London, UK; 2012.
  22. [34]Abraham S O’Dea M Trott DJ Abraham RJ Hughes D Pang S Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats. Sci Rep. 2016; 6(1): 35527. 10.1038/srep35527 27767038 PMC5073282 · DOI
  23. [35]Liu X Thungrat K Boothe DM Occurrence of OXA-48 Carbapenemase and Other β-Lactamase Genes in ESBL-Producing Multidrug Resistant Escherichia coli from Dogs and Cats in the United States, 2009-2013. Front Microbiol. 2016; 7: 1057. 27462301 PMC4939299
  24. [36]Hérivaux A Pailhoriès H Quinqueneau C Lemarié C Joly-Guillou ML Ruvoen N First report of carbapenemase-producing Acinetobacter baumannii carriage in pets from the community in France. Int J Antimicrob Agents. 2016; 48(2): 220- 1. 10.1016/j.ijantimicag.2016.03.012 27424597 · DOI
  25. [37]Yousfi M Touati A Mairi A Brasme L Gharout-Sait A Guillard T Emergence of Carbapenemase-Producing Escherichia coli Isolated from Companion Animals in Algeria. Microb Drug Resist. 2016; 22(4): 342- 6. 10.1089/mdr.2015.0196 26741510 · DOI
  26. [38]González-Torralba A Oteo J Asenjo A Bautista V Fuentes E Alós JI Survey of Carbapenemase-Producing Enterobacteriaceae in Companion Dogs in Madrid, Spain. Antimicrob Agents Chemother. 2016; 60(4): 2499- 501. 10.1128/AAC.02383-15 26824947 PMC4808160 · DOI
  27. [39]Shaheen BW Nayak R Boothe DM Emergence of a New Delhi metallo-β-lactamase (NDM-1)-encoding gene in clinical Escherichia coli isolates recovered from companion animals in the United States. Antimicrob Agents Chemother. 2013; 57(6): 2902- 3. 10.1128/AAC.02028-12 23587948 PMC3716147 · DOI
  28. [40]Melo LC Boisson MN Saras E Médaille C Boulouis HJ Madec JY OXA-48-producing ST372 Escherichia coli in a French dog. J Antimicrob Chemother. 2017; 72(4): 1256- 8. 28039279
  29. [41]Stolle I Prenger-Berninghoff E Stamm I Scheufen S Hassdenteufel E Guenther S Emergence of OXA-48 carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in dogs. J Antimicrob Chemother. 2013; 68(12): 2802- 8. 10.1093/jac/dkt259 23833179 · DOI
  30. [42]Yousfi M Mairi A Bakour S Touati A Hassissen L Hadjadj L First report of NDM-5-producing Escherichia coli ST1284 isolated from dog in Bejaia, Algeria. New Microbes New Infect. 2015; 8: 17- 8. 10.1016/j.nmni.2015.09.002 26566444 PMC4600852 · DOI
  31. [43]Yong D Toleman MA Giske CG Cho HS Sundman K Lee K Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009; 53(12): 5046- 54. 10.1128/AAC.00774-09 19770275 PMC2786356 · DOI
  32. [45]Kantele A Mero S Kirveskari J Lääveri T Fluoroquinolone antibiotic users select fluoroquinolone-resistant ESBL-producing Enterobacteriaceae (ESBL-PE) - Data of a prospective traveller study. Travel Med Infect Dis. 2017; 16: 23- 30. 10.1016/j.tmaid.2017.01.003 28153711 · DOI
  33. [46]Yang P Xie Y Feng P Zong Z blaNDM-5 carried by an IncX3 plasmid in Escherichia coli sequence type 167. Antimicrob Agents Chemother. 2014; 58(12): 7548- 52. 10.1128/AAC.03911-14 25246393 PMC4249565 · DOI
  34. [47]Kumarasamy KK Toleman MA Walsh TR Bagaria J Butt F Balakrishnan R Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis. 2010; 10(9): 597- 602. 10.1016/S1473-3099(10)70143-2 20705517 PMC2933358 · DOI · Paper page

Cited by

Sorted by citations

Authors
Grönthal, T., Österblad, M., Eklund, M., Jalava, J., Nykäsenoja, S., Pekkanen, K., & Rantala, M.
Affiliations
  • University of Helsinki (FI)
  • Finnish Institute for Health and Welfare (FI)
  • Herttoniemi Hospital (FI)
Venue
Eurosurveillance
Published
2018-07-05
Volume
23
Issue
27
ISSN
  • 1025-496X (ISSN-L)
  • 1560-7917
OpenAlex
W2824121307
Cited by
170
References
3
Citations by year
2026: 5 · 2025: 21 · 2024: 33 · 2023: 19 · 2022: 36 · 2021: 19 · 2020: 22 · 2019: 12 · 2018: 3
FWCI
5.29
Type
journal article
Language
en
Open access
Locations
  • Eurosurveillance (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Työväentutkimus Vuosikirja (submittedVersion)
  • STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
  • WOS
Funders
  • Helsingin Yliopisto
  • Alfred Kordelinin Säätiö
  • Suomen Kulttuurirahasto
  • Eläinlääketieteen Tutkimuksen Tukisäätiö
  • Suomen Eläinlääketieteen Säätiö
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Keywords
carbapenemase-producing Enterobacteriaceae, New Delhi metallo-beta-lactamase, CTX-M-9, interspecies transmission, dogs, chronic otitis externa, antimicrobial resistance, extended-spectrum beta-lactamase, family outbreak, Finland
MeSH terms
Whole Genome Sequencing, Animals, beta-Lactamases, Dogs, Escherichia coli, Escherichia coli Infections, Finland, Humans, Carbapenems, Polymerase Chain Reaction, Electrophoresis, Gel, Pulsed-Field, Friends, Pets, Multilocus Sequence Typing

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review