Authors:
Seyda Cengiz Department of Microbiology, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey

Search for other papers by Seyda Cengiz in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-1273-2941
,
Sitkican Okur Department of Surgery, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey

Search for other papers by Sitkican Okur in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-2620-897X
,
Cihan Oz Department of Microbiology, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey

Search for other papers by Cihan Oz in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-3547-5965
,
Ferda Turgut Department of Surgery, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey

Search for other papers by Ferda Turgut in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-2956-7548
,
Burak Gumurcinler Department of Surgery, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey

Search for other papers by Burak Gumurcinler in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-2922-7279
,
Nur Selcen Sevuk Department of Microbiology, Faculty of Veterinary Medicine, Istanbul University-Cerrahpasa, 34320, Istanbul, Turkey

Search for other papers by Nur Selcen Sevuk in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-1593-8793
,
Ayse Ilgin Kekec Department of Microbiology, Faculty of Veterinary Medicine, Istanbul University-Cerrahpasa, 34320, Istanbul, Turkey

Search for other papers by Ayse Ilgin Kekec in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-0821-8376
,
Haluk Cepoglu Vetmemorial Veterinary Clinic, 34734, Istanbul, Turkey

Search for other papers by Haluk Cepoglu in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-8948-1204
,
Umit Sevimli Pendik Veterinary Control Institute, Istanbul, 34890, Turkey

Search for other papers by Umit Sevimli in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-1504-4685
, and
Mehmet Cemal Adiguzel Department of Microbiology, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey
Veterinary Vaccine and Biological Product Development Application and Research Center, Ataturk University, 25240, Erzurum, Turkey

Search for other papers by Mehmet Cemal Adiguzel in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-2385-9649
Restricted access

Abstract

Objectives

Methicillin-resistant Staphylococcus (MRS) has originated, spread extensively, and become a prominent source of bacterial infections in both human and animal.

Methods

We report the prevalence, genetic diversity, and antimicrobial resistance pattern of Staphylococcus pseudintermedius and Staphylococcus aureus strains isolated from dogs and cats with eye discharges.

Results

A total of 12 (6.0%) coagulase-positives staphylococci were identified as (6/200, 3%) S. aureus and (6/200, 3%) S. pseudintermedius. The phenotypic methicillin resistance of S. aureus and S. pseudintermedius were 50.0% (3/6) and 16.7% (1/6), respectively. None of the isolates showed biofilm formation in the microtiter plate assay. The highest resistance (50.0%) for S. pseudintermedius strains was detected against clindamycin and tetracycline. 67.0% of S. aureus isolates were resistant to penicillin-G. The PCR analysis conducted for detection of mecA gene indicated that only one S. aureus isolated from a cat was mecA gene positive. Phylogenetic analysis based on repetitive sequence-based PCR (rep-PCR) showed that all strains were typable and generated PCR products ranging from 800 bp to 4,400 bp. The lineages ST241 and the novel ST2361 in multi-locus sequence typing (MLST) analysis were detected in one methicillin-susceptible S. pseudintermedius and methicillin-resistant S. pseudintermedius of dogs, respectively. In addition, the lineages ST4155 and ST7217 of two methicillin-resistant S. aureus strains of cats were connected epidemiologically to previously reported cases.

Conclusions

These results indicate epidemiologically related strains (ST241, ST4155, and ST7217) transferring between animals and humans. Therefore, the strategies to combat the widespread MRS should be based on collaboration between human and veterinary medicine under the One Health concept.

  • 1.

    Soimala T, Lübke-Becker A, Hanke D, Eichhorn I, Feßler AT, Schwarz S, et al. Molecular and phenotypic characterization of methicillin-resistant Staphylococcus pseudintermedius from ocular surfaces of dogs and cats suffering from ophthalmological diseases. Vet Microbiol 2020; 244, 108687.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Morris DO, Loeffler A, Davis MF, Guardabassi L, Weese JS. Recommendations for approaches to meticillin‐resistant staphylococcal infections of small animals: diagnosis, therapeutic considerations and preventative measures. Clinical consensus guidelines of the world association for veterinary dermatology. Vet Dermatol 2017; 28: 304–e69.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Thomson P, García P, Miles J, Isla D, Yáñez C, Santibáñez R, et al. Isolation and identification of Staphylococcus species obtained from healthy companion animals and humans. Vet Sci 2022; 9: 79.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Gentile D, Allbaugh RA, Adiguzel MC, Kenne DE, Sahin O, Sebbag L. Bacterial cross-contamination in a veterinary ophthalmology setting. Front Vet Sci 2020: 1141.

    • Search Google Scholar
    • Export Citation
  • 5.

    Mouney MC, Stiles J, Townsend WM, Guptill L, Weese JS. Prevalence of methicillin‐resistant Staphylococcus spp. in the conjunctival sac of healthy dogs. Vet Ophthalmol 2015; 18, 123126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Varges R, Penna B, Martins G, Martins R, Lilenbaum W. Antimicrobial susceptibility of Staphylococci isolated from naturally occurring canine external ocular diseases. Vet Ophthalmol 2009; 12: 216220.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Feßler AT, Scholtzek AD, Schug AR, Kohn B, Weingart C, Schink AK, et al. Antimicrobial and biocide resistance among feline and canine Staphylococcus aureus and Staphylococcus pseudintermedius isolates from diagnostic submissions. Antibiotics 2022; 11: 127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Walther B, Hermes J, Cuny C, Wieler LH, Vincze S, Abou Elnaga Y, et al. Sharing more than friendship—nasal colonization with coagulase-positive staphylococci (CPS) and co-habitation aspects of dogs and their owners. PLoS One 2012; 7, e35197.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Sing A, Tuschak C, Hörmansdorfer S. Methicillin-resistant Staphylococcus aureus in a family and its pet cat. N Engl J Med 2008; 358: 12001201.

    • Search Google Scholar
    • Export Citation
  • 10.

    Hemeg HA. Determination of phylogenetic relationships among methicillin-resistant Staphylococcus aureus recovered from infected humans and companion animals. Saudi J Biol Sci 2021; 28: 20982101.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Tabatabaei S, Najafifar A, Badouei MA, Salehi TZ, Tamai IA, Khaksar E, et al. Genetic characterisation of methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in pets and veterinary personnel in Iran: new insights into emerging methicillin-resistant S. pseudintermedius (MRSP). J Glob Antimicrob Resist 2019; 16: 610.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Garcia-Vallvé S, Palau J, Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol Biol Evol 1999; 16: 11251134.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Schwarz S, Feßler AT, Loncaric I, Wu C, Kadlec K, Wang Y, et al. Antimicrobial resistance among staphylococci of animal origin. Microbiol Spectr 2018; 6: 614.

    • Search Google Scholar
    • Export Citation
  • 14.

    Baran A, Oz C, Cengiz S, Adiguzel MC. Genomic characterization, antimicrobial resistance profiles, enterotoxin, and biofilm production of methicillin-resistant Staphylococcus aureus isolated from clinical and animal products origins in Eastern Turkey. Pesq Vet Bras 2022; 42: e06991.

    • Search Google Scholar
    • Export Citation
  • 15.

    CLSI. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, 5th ed. Wayne, PA, USA: CLSI Supplement VET01S; Clinical and Laboratory Standards Institute, 2020.

    • Search Google Scholar
    • Export Citation
  • 16.

    Becker K, van Alen S, Idelevich EA, Schleimer N, Seggewiß J, Mellmann A, et al. Plasmid-encoded transferable mecB-mediated methicillin resistance in Staphylococcus aureus. Emerg Infect Dis 2018; 24: 242.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Schwendener S, Cotting K, Perreten V. Novel methicillin resistance gene mecD in clinical Macrococcus caseolyticus strains from bovine and canine sources. Sci Rep 2017; 7, 43797.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, et al. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecALGA251. Clin Microbiol Infect 2012; 18: 395400.

    • Search Google Scholar
    • Export Citation
  • 19.

    Horie H, Yamahata N, Takahashi N, Yoshida A, Katabami K, Sato H, et al. Enhancement of antimicrobial activities of antibiotics by combination with epigallocatechin gallate against methicillin-resistant Staphylococcus aureus. J Hum Nurs Stud 2009; 7: 1926.

    • Search Google Scholar
    • Export Citation
  • 20.

    Krapf M, Müller E, Reissig A, Slickers P, Braun SD, Müller E, et al. Molecular characterisation of methicillin-resistant Staphylococcus pseudintermedius from dogs and the description of their SCCmec elements. Vet Microbiol 2019; 233: 196203.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Sahin O, Shen Z, Zhang Q. Methods to study antimicrobial resistance in Campylobacter jejuni. Methods Mol Biol 2017; 1512: 2942.

  • 22.

    Sasaki T, Tsubakishita S, Tanaka Y, Sakusabe A, Ohtsuka M, Hirotaki S, et al. Multiplex-PCR method for species identification of coagulase-positive staphylococci. J Clin Microbiol 2010; 48: 765769.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Lade H, Park JH, Chung SH, Kim IH, Kim JM, Joo HS, et al. Biofilm formation by Staphylococcus aureus clinical isolates is differentially affected by glucose and sodium chloride supplemented culture media. J Clin Med 2019; 8: 1853.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    EUCAST. Breakpoint tables for interpretation of MICs and zone diameters. European Committee on Antimicrobial Susceptibility Testing (EUCAST) 2022: 3338.

    • Search Google Scholar
    • Export Citation
  • 25.

    Švec P, Pantůček R, Petráš P, Sedláček I, Nováková D. Identification of Staphylococcus spp. using (GTG) 5-PCR fingerprinting. Syst Appl Microbiol 2010; 33: 451456.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Albufera U, Bhugaloo-Vial P, Issack MI, Jaufeerally-Fakim Y. Molecular characterization of Salmonella isolates by REP-PCR and RAPD analysis. Infect Genet Evol 2009; 9: 322327.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Solyman SM, Black CC, Duim B, Perreten V, Van Duijkeren E, Wagenaar JA, et al. Multilocus sequence typing for characterization of Staphylococcus pseudintermedius. J Clin Microbiol 2013; 51: 306310.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    LoPinto AJ, Mohammed HO, Ledbetter EC. Prevalence and risk factors for isolation of methicillin‐resistant Staphylococcus in dogs with keratitis. Vet Ophthalmol 2015; 18: 297303.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Kaliamurthy J, Kalavathy CM, Parmar P, Nelson Jesudasan CA, Thomas PA. Spectrum of bacterial keratitis at a tertiary eye care centre in India. Biomed Res Int 2013; 2013, 181564.

    • Search Google Scholar
    • Export Citation
  • 30.

    Göçmen H, Tamakan H, Şükür H, Esendal ÖM. Investigation of multidrug resistance among Staphylococcus species isolated from cats and dogs. Atatürk Univ J Vet Sci 2020; 15: 156166.

    • Search Google Scholar
    • Export Citation
  • 31.

    Adiguzel MC, Schaefer K, Rodriguez T, Ortiz J, Sahin O. prevalence, mechanism, genetic diversity, and cross-resistance patterns of methicillin-resistant Staphylococcus isolated from companion animal clinical samples submitted to a veterinary diagnostic laboratory in the midwestern United States. Antibiotics 2022; 11: 609.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Shariati A, Dadashi M, Chegini Z, van Belkum A, Mirzaii M, Khoramrooz SS, et al. The global prevalence of daptomycin, tigecycline, quinupristin/dalfopristin, and linezolid-resistant Staphylococcus aureus and coagulase–negative staphylococci strains: a systematic review and meta-analysis. Antimicrob Resist Infect Control 2020; 9: 120.

    • Search Google Scholar
    • Export Citation
  • 33.

    Asanin J, Misic D, Aksentijevic K, Tambur Z, Rakonjac B, Kovacevic I, et al. Genetic profiling and comparison of human and animal methicillin-resistant Staphylococcus aureus (MRSA) isolates from Serbia. Antibiotics 2019; 8: 26.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Wegener A, Broens EM, Zomer A, Spaninks M, Wagenaar JA, Duim B. Comparative genomics of phenotypic antimicrobial resistances in methicillin-resistant Staphylococcus pseudintermedius of canine origin. Vet Microbiol 2018; 225: 125131.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Cong Y, Yang S, Rao X. Vancomycin resistant Staphylococcus aureus infections: a review of case updating and clinical features. J Adv Res 2020; 21: 169176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Argudín MA, Roisin S, Nienhaus L, Dodémont M, De Mendonça R, Nonhoff C, et al. Genetic diversity among Staphylococcus aureus isolates showing oxacillin and/or cefoxitin resistance not linked to the presence of mec genes. Antimicrob Agents Chemother 2018; 62: e00091–18.

    • Search Google Scholar
    • Export Citation
  • 37.

    Tyson GH, Ceric O, Guag J, Nemser S, Borenstein S, Slavic D, et al. Genomics accurately predicts antimicrobial resistance in Staphylococcus pseudintermedius collected as part of Vet-LIRN resistance monitoring. Vet Microbiol 2021; 254, 109006.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Lozano C, Rezusta A, Ferrer I, Pérez-Laguna V, Zarazaga M, Ruiz-Ripa L, et al. Staphylococcus pseudintermedius human infection cases in Spain: dog-to-human transmission. Vector-Borne Zoonotic Dis 2017; 17: 268270.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Zakošek Pipan M, Švara T, Zdovc I, Papić B, Avberšek J, Kušar D, et al. Staphylococcus pseudintermedius septicemia in puppies after elective cesarean section: confirmed transmission via dam’s milk. BMC Vet Res 2019; 15: 18.

    • Search Google Scholar
    • Export Citation
  • 40.

    Venugopal N, Mitra S, Tewari R, Ganaie F, Shome R, Rahman H, et al. Molecular detection and typing of methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci isolated from cattle, animal handlers, and their environment from Karnataka, Southern Province of India. Vet World 2019; 12: 1760.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Rahman MM, Amin KB, Rahman SMM, Khair A, Rahman M, Hossain A, et al. Investigation of methicillin-resistant Staphylococcus aureus among clinical isolates from humans and animals by culture methods and multiplex PCR. BMC Vet Res 2018; 14: 16.

    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
The author instructions are available in PDF.
Please, download the file from HERE

 

Senior editors

Editor-in-Chief: Prof. Dóra Szabó (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Managing Editor: Dr. Béla Kocsis (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Co-editor: Dr. Andrea Horváth (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Editorial Board

  • Prof. Éva ÁDÁM (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Sebastian AMYES (Department of Medical Microbiology, University of Edinburgh, Edinburgh, UK.)
  • Dr. Katalin BURIÁN (Institute of Clinical Microbiology University of Szeged, Szeged, Hungary; Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary.)
  • Dr. Orsolya DOBAY (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Ildikó Rita DUNAY (Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-von-Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany)
  • Prof. Levente EMŐDY(Department of Medical Microbiology and Immunology, University of Pécs, Pécs, Hungary.)
  • Prof. Anna ERDEI (Department of Immunology, Eötvös Loránd University, Budapest, Hungary, MTA-ELTE Immunology Research Group, Eötvös Loránd University, Budapest, Hungary.)
  • Prof. Éva Mária FENYŐ (Division of Medical Microbiology, University of Lund, Lund, Sweden)
  • Prof. László FODOR (Department of Microbiology and Infectious Diseases, University of Veterinary Medicine, Budapest, Hungary)
  • Prof. József KÓNYA (Department of Medical Microbiology, University of Debrecen, Debrecen, Hungary)
  • Prof. Yvette MÁNDI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Károly MÁRIALIGETI (Department of Microbiology, Eötvös Loránd University, Budapest, Hungary)
  • Prof. János MINÁROVITS (Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary)
  • Prof. Béla NAGY (Centre for Agricultural Research, Institute for Veterinary Medical Research, Budapest, Hungary.)
  • Prof. István NÁSZ (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Kristóf NÉKÁM (Hospital of the Hospitaller Brothers in Buda, Budapest, Hungary.)
  • Dr. Eszter OSTORHÁZI (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Rozália PUSZTAI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Peter L. RÁDY (Department of Dermatology, University of Texas, Houston, Texas, USA)
  • Prof. Éva RAJNAVÖLGYI (Department of Immunology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary)
  • Prof. Ferenc ROZGONYI (Institute of Laboratory Medicine, Semmelweis University, Budapest, Hungary)
  • Prof. Joseph G. SINKOVICS (The Cancer Institute, St. Joseph’s Hospital, Tampa, Florida, USA)
  • Prof. Júlia SZEKERES (Department of Medical Biology, University of Pécs, Pécs, Hungary.)
  • Prof. Mária TAKÁCS (National Reference Laboratory for Viral Zoonoses, National Public Health Center, Budapest, Hungary.)
  • Prof. Edit URBÁN (Department of Medical Microbiology and Immunology University of Pécs, Pécs, Hungary; Institute of Translational Medicine, University of Pécs, Pécs, Hungary.)

 

Editorial Office:
Akadémiai Kiadó Zrt.
Budafoki út 187-187, A/3, H-1117 Budapest, Hungary

Editorial Correspondence:
Acta Microbiologica et Immunologica Hungarica
Institute of Medical Microbiology
Semmelweis University
P.O. Box 370
H-1445 Budapest, Hungary
Phone: + 36 1 459 1500 ext. 56101
Fax: (36 1) 210 2959
E-mail: amih@med.semmelweis-univ.hu

 Indexing and Abstracting Services:

  • Biological Abstracts
  • BIOSIS Previews
  • CAB Abstracts
  • CABELLS Journalytics
  • Chemical Abstracts
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Referativnyi Zhurnal
  • SCOPUS
  • Science Citation Index Expanded

2023  
Web of Science  
Journal Impact Factor 1.3
Rank by Impact Factor Q4 (Immunology)
Journal Citation Indicator 0.31
Scopus  
CiteScore 2.3
CiteScore rank Q3 (Infectious Diseases)
SNIP 0.389
Scimago  
SJR index 0.308
SJR Q rank Q3

Acta Microbiologica et Immunologica Hungarica
Publication Model Hybrid
Submission Fee none
Article Processing Charge 1100 EUR/article (only for OA publications)
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 fee 2025 Online subsscription: 772 EUR / 848 USD
Print + online subscription: 860 EUR / 944 USD
Subscription Information Online subscribers are entitled access to all back issues published by Akadémiai Kiadó for each title for the duration of the subscription, as well as Online First content for the subscribed content.
Purchase per Title Individual articles are sold on the displayed price.

Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
Year of
Foundation
1954
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 1217-8950 (Print)
ISSN 1588-2640 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Mar 2024 172 1 1
Apr 2024 87 0 0
May 2024 116 0 0
Jun 2024 104 0 1
Jul 2024 82 1 1
Aug 2024 138 0 0
Sep 2024 55 0 0