View More View Less
  • 1 University of Veterinary Medicine, Vienna, Austria
  • | 2 University of Veterinary Medicine Vienna, Austria
Open access

In the past, the horizontal transfer of antimicrobial resistance genes was mainly associated with conjugative plasmids or transposons, whereas transduction by bacteriophages was thought to be a rare event. In order to analyze the likelihood of transduction of antimicrobial resistance in the field of clinical veterinary medicine, we isolated phages from Escherichia coli from a surgery suite of an equine clinic. In a pilot study, the surgery suite of a horse clinic was sampled directly after surgery and subsequently sampled after cleaning and disinfection following a sampling plan based on hygiene, surgery, and anesthesia. In total, 31 surface sampling sites were defined and sampled. At 24 of these 31 surface sampling sites, coliphages were isolated. At 12 sites, coliphages were found after cleaning and disinfection. Randomly selected phages were tested for their ability of antimicrobial resistance transduction. Ten of 31 phages were detected to transfer antimicrobial resistance. These phages most often transduced resistance to streptomycin, encoded by the addA1 gene (n = 9), followed by resistance to chloramphenicol by cmlA (n = 3) and ampicillin (n = 1). This is, to the best of our knowledge, the first report on antimicrobial resistance-transferring bacteriophages that have been isolated at equine veterinary clinics.

  • 1.

    Walther B , Janssen T, Gehlen H, Vincze S, Borchers K, Wieler L, Barton A, Lübke-Becker A: Infection control and hygiene management in equine hospitals. Berl Munch Tierarztl Wochenschr 127, 486497 (2014)

    • Search Google Scholar
    • Export Citation
  • 2.

    Isgren CM , Salem SE, Archer DC, Worsman FCF, Townsend NB: Risk factors for surgical site infection following laparotomy: Effect of season and perioperative variables and reporting of bacterial isolates in 287 horses. Equine Vet J 49, 3944 (2017)

    • Search Google Scholar
    • Export Citation
  • 3.

    Galuppo LD , Pascoe JR, Jang SS, Willits NH, Greenman SL: Evaluation of iodophor skin preparation techniques and factors influencing drainage from ventral midline incisions in horses. J Am Vet Med Assoc 215, 963969 (1999)

    • Search Google Scholar
    • Export Citation
  • 4.

    Walther B , Lübke-Becker A, Stamm I, Gehlen H, Barton A, Janssen T, Wieler L, Guenther S: Suspected nosocomial infections with multi-drug resistant E. coli, including extended-spectrum beta-lactamase (ESBL)-producing strains, in an equine clinic. Berl Munch Tierarztl Wochenschr 127, 421427 (2014)

    • Search Google Scholar
    • Export Citation
  • 5.

    Ahmed MO , Williams NJ, Clegg PD, van Velkinburgh JC, Baptiste KE, Bennett M: Analysis of risk factors associated with antibiotic-resistant Escherichia coli. Microb Drug Resist 18, 161168 (2012)

    • Search Google Scholar
    • Export Citation
  • 6.

    Racklyeft D , Love D: Bacterial infection of the lower respiratory tract in 34 horses. Aust Vet J 78, 549559 (2000)

  • 7.

    Johns IC , Adams EL: Trends in antimicrobial resistance in equine bacterial isolates: 1999–2012. Vet Rec 176, 334 (2015)

  • 8.

    Boerlin P , Reid-Smith RJ: Antimicrobial resistance: its emergence and transmission. Anim Health Res Rev 9, 115126 (2008)

  • 9.

    Normark BH , Normark S: Evolution and spread of antibiotic resistance. J Intern Med 252, 91106 (2002)

  • 10.

    Kenzaka T , Tani K, Nasu M: High-frequency phage-mediated gene transfer in freshwater environments determined at single-cell level. ISME J 4, 648659 (2010)

    • Search Google Scholar
    • Export Citation
  • 11.

    Muniesa M , Colomer-Lluch M, Jofre J: Could bacteriophages transfer antibiotic resistance genes from environmental bacteria to human-body associated bacterial populations? Mob Genet Elements 3, e25847 (2013)

    • Search Google Scholar
    • Export Citation
  • 12.

    Shousha A , Awaiwanont N, Sofka D, Smulders FJ, Paulsen P, Szostak MP, Humphrey T, Hilbert F: Bacteriophages isolated from chicken meat and the horizontal transfer of antimicrobial resistance genes. Appl Environ Microbiol 81, 46004606 (2015)

    • Search Google Scholar
    • Export Citation
  • 13.

    Soucy SM , Huang J, Gogarten JP: Horizontal gene transfer: building the web of life. Nat Rev Genetics 16, 472482 (2015)

  • 14.

    Furusawa T , Iwano H, Hiyashimizu Y, Matsubara K, Higuchi H, Nagahata H, Niwa H, Katayama Y, Kinoshita Y, Hagiwara K, Iwasaki T, Tanji Y, Yokota H, Tamura Y: Phage therapy is effective in a mouse model of bacterial equine keratitis. Appl Environ Microbiol 82, 53325339 (2016)

    • Search Google Scholar
    • Export Citation
  • 15.

    Abedon ST , Kuhl SJ, Blasdel BG, Kutter EM: Phage treatment of human infections. Bacteriophage 1, 6685 (2011)

  • 16.

    ISO, N. ISO 10705-2 (2000): Water quality – detection and enumeration of bacteriophages Part 2: enumeration of somatic coliphages, 1112.

    • Search Google Scholar
    • Export Citation
  • 17.

    Sullivan MB , Coleman ML, Weigele P, Rohwer F, Chisholm SW: Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3, s144 (2005)

    • Search Google Scholar
    • Export Citation
  • 18.

    ISO, N ISO 20776-1 (2006): Clinical laboratory testing and in vitro diagnostic test systems – Susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices. – Part 1 Reference method for testing the invitro acitivity of antimicrobial agents against rapidly growing aerobic bacteria involved in infectious diseases.

    • Search Google Scholar
    • Export Citation
  • 19.

    Williams A , Christley RM, McKane SA, Roberts VL, Clegg PD, Williams NJ: Antimicrobial resistance changes in enteric Escherichia coli of horses during hospitalisation: resistance profiling of isolates. Vet J 195, 121126 (2013)

    • Search Google Scholar
    • Export Citation
  • 20.

    Langsrud S , Sundheim G, Borgmann-Strahsen R: Intrinsic and acquired resistance to quaternary ammonium compounds in food-related Pseudomonas spp. J Appl Microbiol 95, 874882 (2003)

    • Search Google Scholar
    • Export Citation
  • 21.

    Shousha A , Paulsen P, Sofka D, Hilbert M, Dinhopl N, Hilbert F: Tenazität von antibiotikaresistenzübertragenden Bakteriophagen. 16. Fachtagung für Fleisch- und Geflügelfleischhygiene. 1.-2. März, Berlin (2016)

    • Search Google Scholar
    • Export Citation
  • 22.

    Maidhof H , Guerra B, Abbas S, Elsheikha HM, Whittam TS, Beutin L: A multiresistant clone of shiga toxin-producing Escherichia coli O118: (H16) is spread in cattle and humans over different European countries. Appl Environ Microbiol 68, 58345842 (2002)

    • Search Google Scholar
    • Export Citation
  • 23.

    Chen S , Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott PF, Ayers S, Meng J: Characterization of multiple- antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 70, 17 (2004)

    • Search Google Scholar
    • Export Citation
  • 24.

    Van TT , Chin J, Chapman T, Tran LT, Coloe PJ: Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol 124, 217223 (2008)

    • Search Google Scholar
    • Export Citation
The author instruction is available in PDF.
Please, download the file from HERE.

Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita

Editor(s)-in-Chief: Heimesaat, Markus M.

Vice Editor(s)-in-Chief: Fuchs, Anja

Editorial Board

Chair of the Editorial Board:
Jeffrey S. Buguliskis (Thomas Jefferson University, USA)

  • Jörn Albring (University of Münster, Germany)
  • Stefan Bereswill (Charité - University Medicine Berlin, Germany)
  • Dunja Bruder (University of Megdeburg, Germany)
  • Jan Buer (University of Duisburg, Germany)
  • Jeff Buguliskis (Thomas Jefferson University, USA)
  • Edit Buzas (Semmelweis University, Hungary)
  • Charles Collyer (University of Sydney, Australia)
  • Renato Damatta (UENF, Brazil)
  • Ivelina Damjanova (Semmelweis University, Hungary)
  • Maria Deli (Biological Research Center, HAS, Hungary)
  • Olgica Djurković-Djaković (University of Belgrade, Serbia)
  • Jean-Dennis Docquier (University of Siena, Italy)
  • Anna Erdei (Eötvös Loránd University, Hungary)
  • Zsuzsanna Fabry (University of Washington, USA)
  • Beniam Ghebremedhin (Witten/Herdecke University, Germany)
  • Nancy Guillen (Institute Pasteur, France)
  • Georgina L. Hold (University of Aberdeen, United Kingdom)
  • Ralf Ignatius (Charité - University Medicine Berlin, Germany)
  • Zsuzsanna Izsvak (MDC-Berlin, Germany)
  • Achim Kaasch (University of Cologne, Germany)
  • Tamás Laskay (University of Lübeck, Germany)
  • Oliver Liesenfeld (Roche, USA)
  • Shreemanta Parida (Vaccine Grand Challenge Program, India)
  • Matyas Sandor (University of Wisconsin, USA)
  • Ulrich Steinhoff (University of Marburg, Germany)
  • Michal Toborek (University of Miami, USA)
  • Mary Jo Wick (University of Gothenburg, Sweden)
  • Susanne A. Wolf (MDC-Berlin, Germany)


Dr. Dunay, Ildiko Rita
Magdeburg, Germany

Indexing and Abstracting Services:

  • PubMed Central
  • Scopus
  • ESCI
  • CABI


CrossRef Documents 23
WoS Cites 708
Wos H-index 27
Days from submission to acceptance 219
Days from acceptance to publication 176
Acceptance Rate 70%



European Journal of Microbiology and Immunology
Publication Model Gold Open Access
Submission Fee none
Article Processing Charge 928 EUR/article
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription Information Gold Open Access
Purchase per Title  

European Journal of Microbiology and Immunology
Language English
Size A4
Year of
per Year
per Year
Founder Akadémiai Kiadó
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Aug 2021 0 4 1
Sep 2021 0 10 10
Oct 2021 0 11 8
Nov 2021 0 10 11
Dec 2021 0 13 7
Jan 2022 0 8 5
Feb 2022 0 0 0