Authors:
Aleksandra TrościańczykFaculty of Veterinary Medicine, Sub-Department of Veterinary Microbiology, Institute of Biological Bases of Animal Diseases, University of Life Sciences, Akademicka 12, 20-033, Lublin, Poland

Search for other papers by Aleksandra Trościańczyk in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-6400-2131
,
Aneta NowakiewiczFaculty of Veterinary Medicine, Sub-Department of Veterinary Microbiology, Institute of Biological Bases of Animal Diseases, University of Life Sciences, Akademicka 12, 20-033, Lublin, Poland

Search for other papers by Aneta Nowakiewicz in
Current site
Google Scholar
PubMed
Close
,
Sebastian GnatFaculty of Veterinary Medicine, Sub-Department of Veterinary Microbiology, Institute of Biological Bases of Animal Diseases, University of Life Sciences, Akademicka 12, 20-033, Lublin, Poland

Search for other papers by Sebastian Gnat in
Current site
Google Scholar
PubMed
Close
,
Magdalena WójcikDepartment of Genetics and Microbiology, Maria Curie-Skłodowska University, Lublin, Poland

Search for other papers by Magdalena Wójcik in
Current site
Google Scholar
PubMed
Close
,
Sylwia Wdowiak-WróbelDepartment of Genetics and Microbiology, Maria Curie-Skłodowska University, Lublin, Poland

Search for other papers by Sylwia Wdowiak-Wróbel in
Current site
Google Scholar
PubMed
Close
, and
Michał KalitaDepartment of Genetics and Microbiology, Maria Curie-Skłodowska University, Lublin, Poland

Search for other papers by Michał Kalita in
Current site
Google Scholar
PubMed
Close
Restricted access

Abstract

The aim of the study was to assess the incidence, resistance, virulence, and genotypic characteristics of Staphylococcus spp. residing in the gastrointestinal tract of dogs and cats, as a group of animals causing potential contamination of the urban space. A high percentage of strains resistant to penicillin (58%), oxacillin (9%) and tetracycline (60%) were found. All isolates resistant to penicillin, kanamycin, or chloramphenicol carried genes responsible for individual resistance (blaZ, aph(3′)-IIIa, and cat (pC194)/cat (pC223), respectively. The mecA gene was detected in 45% of the oxacillin-resistant Staphylococcus pseudintermedius strains. The amplification of DNA fragments surrounding rare restriction sites analysis demonstrated high heterogeneity of genotypic profiles correlating with phenotypic resistance profiles. Multilocus sequence typing analysis classified the methicillin-resistant S. pseudintermedius strains as ST71, ST890, and the totally new ST1047. The presence of a high level of resistance among Staphylococcus strains may suggest a potential risk of transfer of these bacteria between companion animals and humans.

  • Aarestrup, F. M., Agersø, Y., Ahrens, P., Jørgensen, J. C., Madsen, M. and Jensen, L. B. (2000): Antimicrobial susceptibility and presence of resistance genes in staphylococci from poultry. Vet. Microbiol. 74, 353364.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bannoehr, J., Ben Zakour, N. L., Waller, A. S., Guardabassi, L., Thoday, K. L., van den Broek, A. H. M. and Fitzgerald, J. R. (2007): Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. J. Bacteriol. 189, 86858692.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Becker, K., Roth, R. and Peters, G. (1998): Rapid and specific detection of toxigenic Staphylococcus aureus: use of two multiplex PCR enzyme immunoassays for amplification and hybridization of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene. J. Clin. Microbiol. 36, 25482553.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Beever, L., Bond, R., Graham, P. A., Jackson, B., Lloyd, D. H. and Loeffler, A. (2015): Increasing antimicrobial resistance in clinical isolates of Staphylococcus intermedius group bacteria and emergence of MRSP in the UK. Vet. Rec. 176, 172.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Blaiotta, G., Fusco, V., Ercolini, D., Pepe, O. and Coppola, S. (2010): Diversity of Staphylococcus species strains based on partial kat (catalase) gene sequences and design of a PCR-restriction fragment length polymorphism assay for identification and differentiation of coagulase-positive species (S. aureus, S. delphini, S. hyicus, S. intermedius, S. pseudintermedius, and S. schleiferi subsp. coagulans). J. Clin. Microbiol. 48, 192201.

    • Search Google Scholar
    • Export Citation
  • CLSI, Clinical and Laboratory Standards Institute (2012): Performance Standards for Antimicrobial Susceptibility Testing; Twenty-second Informational Supplement. CLSI Document M100-S22, Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, USA.

    • Search Google Scholar
    • Export Citation
  • CLSI, Clinical and Laboratory Standards Institute (2013a): Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Approved Standard. 4th edition, CLSI document Vet 01-A4. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, USA.

    • Search Google Scholar
    • Export Citation
  • CLSI, Clinical and Laboratory Standards Institute (2013b): Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Second Informational Supplement. CLSI Document Vet 01-S2, Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, USA.

    • Search Google Scholar
    • Export Citation
  • Duim, B., Verstappen, K. M., Broens, E. M., Laarhoven, L. M., van Duijkeren, E., Hordijk, J., de Heus, P., Spaninks, M., Timmerman, A. J. and Wagenaar, J. A. (2016): Changes in the population of methicillin-resistant Staphylococcus pseudintermedius and dissemination of antimicrobial-resistant phenotypes in The Netherlands. J. Clin. Microbiol. 54, 283288.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Epstein, C. R., Yam, W. C., Peiris, J. S. M. and Epstein, R. J. (2009): Methicillin-resistant commensal staphylococci in healthy dogs as a potential zoonotic reservoir for community-acquired antibiotic resistance. Infect. Genet. Evol. 9, 283285.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • European Medicines Agency, European Surveillance of Veterinary Antimicrobial Consumption. (2018): Sales of Veterinary Antimicrobial Agents in 30 European Countries in 2016, EMA/275982/2018.

    • Search Google Scholar
    • Export Citation
  • Frank, L. A., Kania, S. A., Kirzeder, E. M., Eberlein, L. C. and Bemis, D. A. (2009): Risk of colonization or gene transfer to owners of dogs with methicillin-resistant Staphylococcus pseudintermedius. Vet. Dermatol. 20, 496501.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Frank, M. G., Keniston, A., Madinger, N., Price C. and Bessesen, M. T. (2015): Staphylococcus intermedius group infections in humans: report of four cases and a literature review. JMM Case Rep. 2, (4).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Garbacz, K., Żarnowska, S., Piechowicz, L. and Haras, K. (2013): Pathogenicity potential of Staphylococcus pseudintermedius strains isolated from canine carriers and from dogs with infection signs. Virulence 4, 255259.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • García-Alvarez, L., Holden, M. T. G., Lindsay, H., Webb, C., Brown, D. F. J., Curran, M. D., Walpole, E., Brooks, K., Pickard, D. J., Teale, C., Parkhill, J., Bentley, S. D., Edwards, G. F., Girvan, E. K., Kearns, A. M., Pichon, B., Hill, R. L. R., Larsen, A. R., Skov, R. L., Peacock, S. J., Maskell, D. J. and Holmes, M. A. (2011): Methicillin-resistant Staphylococcus aureus with a novel mec A homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect. Dis. 11, 595603.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Grönthal, T., Eklund, M., Thomson, K., Piiparinen, H., Sironen, T. and Rantala, M. (2017): Antimicrobial resistance in Staphylococcus pseudintermedius and the molecular epidemiology of methicillin-resistant S. pseudintermedius in small animals in Finland. J. Antimicrob. Chemother. 72, 10211030.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kizerwetter-Świda, M., Chrobak-Chmiel, D., Rzewuska, M. and Binek, M. (2017): Changes in the population structure of canine methicillin-resistant Staphylococcus pseudintermedius in Poland. Vet. Microbiol. 208, 106109.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Latronico, F., Moodley, A., Nielsen, S. S. and Guardabassi, L. (2014): Enhanced adherence of methicillin-resistant Staphylococcus pseudintermedius sequence type 71 to canine and human corneocytes. Vet. Res. 45, 70.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lautz, S., Kanbar, T., Alber, J., Lämmler, C., Weiss, R., Prenger-Berninghoff, E. and Zschöck, M. (2006): Dissemination of the gene encoding exfoliative toxin of Staphylococcus intermedius among strains isolated from dogs during routine microbiological diagnostics. J. Vet. Med. B Infect. Dis. Vet. Public Health 53, 434438.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B., Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T. and Monnet, D. L. (2012): Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Martineau, F., Picard, F. J., Lansac, N., Menard, C., Roy, P. H., Ouellette, M. and Bergeron, M., (2000): Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis. Antimicrob. Agents Chemother. 44, 231238.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Morris, D. O., Rook, K. A., Shofer, F. S. and Rankin, S. C. (2006): Screening of Staphylococcus aureus, Staphylococcus intermedius, and Staphylococcus schleiferi isolates obtained from small companion animals for antimicrobial resistance: a retrospective review of 749 isolates (2003–04). Vet. Dermatol. 17, 332337.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nowakiewicz, A., Ziółkowska, G., Zięba, P., Gnat, S., Trościańczyk, A. and Adaszek, Ł. (2017): Characterization of multidrug resistant E. faecalis strains from pigs of local origin by ADSRRS-fingerprinting and MALDI-TOF MS; Evaluation of the compatibility of methods employed for multidrug resistance analysis. PloS One. 12, e0171160.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nowakiewicz, A., Ziółkowska, G., Zięba, P., Gnat, S., Wojtanowicz-Markiewicz, K. and Trościańczyk, A. (2016): Coagulase-positive Staphylococcus isolated from wildlife: identification, molecular characterization and evaluation of resistance profiles with focus on a methicillin-resistant strain. Comp. Immunol. Microbiol. Infect. Dis. 44, 2128.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Oliveira, D. C. and de Lencastre, H. (2002): Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 46, 21552161.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Perreten, V., Kadlec, K., Schwarz, S., Grönlund Andersson, U., Finn, M., Greko, C., Moodley, A., Kania, S. A., Frank, L. A., Bemis, D. A., Franco A., Iurescia, M., Battisti, A., Duim, B., Wagenaar, J. A., van Duijkeren, E., Weese, J. S., Fitzgerald, J. R., Rossano, A. and Guardabassi, L. (2010): Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J. Antimicrob. Chemother. 65, 11451154.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Reygaert, W. C. (2013): Antimicrobial mechanisms of Staphylococcus aureus. In: Nendez-Vilas, A. (ed) Microbial Pathogens and Strategies for Combating Them: Science, Technology and Education, Formatex Research Center, Spain. pp. 297310.

    • Search Google Scholar
    • Export Citation
  • Sasaki, T., Kikuchi, K., Tanaka, Y., Takahashi, N., Kamata, S. and Hiramatsu, K. (2007): Methicillin-resistant Staphylococcus pseudintermedius in a veterinary teaching hospital. J. Clin. Microbiol. 45, 11181125.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Schnellmann, C., Gerber, V., Rossano, A., Jaquier, V., Panchaud, Y., Doherr, M. G., Thomann, A., Straub, R. and Perreten, V. (2006): Presence of new mecA and mph(C) variants conferring antibiotic resistance in Staphylococcus spp. isolated from the skin of horses before and after clinic admission. J. Clin. Microbiol. 44, 44444454.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Solyman, S. M., Black, C. C., Duim, B., Perreten, V., van Duijkeren, E., Waganaar, J. A., Eberlein, L. C., Sadeghi, L. N., Videla, R., Bemis, D. A. and Kania, S. A. (2013): Multilocus sequence typing for characterization of Staphylococcus pseudintermedius. J. Clin. Microbiol. 51, 306310.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Stegmann, R., Burnens, A., Maranta, C. A. and Perreten, V. (2010): Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J. Antimicrob. Chemother. 65, 20472048.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Strommenger, B., Kettlitz, C., Werner, G. and Witte, W. (2003): Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J. Clin. Microbiol. 41, 40894094.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • van de Klundert, J. A. M. and Vliegenthart, J. S. (1993): PCR detection of genes for aminoglycoside-modifying enzymes. In: Persing, D. H., Smith, T. F., Tenover, F. C. and White, T. J. (eds) Diagnostic Molecular Microbiology. Principles and Applications, American Society for Microbiology, Washington D.C. pp. 547552.

    • Search Google Scholar
    • Export Citation
  • Ventrella, G., Moodley, A., Grandolfo, E., Parisi, A., Corrente, M. and Bounavoglia, D. (2017): Frequency, antimicrobial susceptibility and clonal distribution of methicillin-resistant Staphylococcus pseudintermedius in canine clinical samples submitted to a veterinary diagnostic laboratory in Italy: a 3-year retrospective investigation. Vet. Microbiol. 211, 103106.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yoon, J. W., Lee, K.-J., Lee, S.-Y., Chae, M.-J., Park, J.-K., Yoo, J.-H. and Park, H.-M. (2010): Antibiotic resistance profiles of Staphylococcus pseudintermedius isolates from canine patients in Korea. J. Microbiol. Biotechnol. 20, 17641768.

    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Author information is available in PDF.
Please, download the file from HERE.

The manuscript preparation instructions is available in PDF.
Please, download the file from HERE.

Senior editors

Editor-in-Chief: Mária BENKŐ

Managing Editor: András SZÉKELY

Editorial Board

  • Béla DÉNES (National Food Chain Safety Office, Budapest Hungary)
  • Edit ESZTERBAUER (Veterinary Medical Research Institute, Budapest, Hungary)
  • Hedvig FÉBEL (National Agricultural Innovation Centre, Herceghalom, Hungary)
  • László FODOR (University of Veterinary Medicine, Budapest, Hungary)
  • Balázs HARRACH (Veterinary Medical Research Institute, Budapest, Hungary)
  • Peter MASSÁNYI (Slovak University of Agriculture in Nitra, Nitra, Slovak Republic)
  • Béla NAGY (Veterinary Medical Research Institute, Budapest, Hungary)
  • Tibor NÉMETH (University of Veterinary Medicine, Budapest, Hungary)
  • Zsuzsanna NEOGRÁDY (University of Veterinary Medicine, Budapest, Hungary)
  • Alessandra PELAGALLI (University of Naples Federico II, Naples, Italy)
  • Kurt PFISTER (Ludwig-Maximilians-University of Munich, Munich, Germany)
  • László SOLTI (University of Veterinary Medicine, Budapest, Hungary)
  • József SZABÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Péter VAJDOVICH (University of Veterinary Medicine, Budapest, Hungary)
  • János VARGA (University of Veterinary Medicine, Budapest, Hungary)
  • Štefan VILČEK (University of Veterinary Medicine in Kosice, Kosice, Slovak Republic)
  • Károly VÖRÖS (University of Veterinary Medicine, Budapest, Hungary)
  • Herbert WEISSENBÖCK (University of Veterinary Medicine, Vienna, Austria)
  • Attila ZSARNOVSZKY (Szent István University, Gödöllő, Hungary)

ACTA VETERINARIA HUNGARICA
Institute for Veterinary Medical Research
Centre for Agricultural Research
Hungarian Academy of Sciences
P.O. Box 18, H-1581 Budapest, Hungary
Phone: (36 1) 467 4081 (ed.-in-chief) or (36 1) 213 9793 (editor) Fax: (36 1) 467 4076 (ed.-in-chief) or (36 1) 213 9793

Indexing and Abstracting Services:

  • Biological Abstracts
  • BIOSIS Previews
  • CAB Abstracts
  • Chemical Abstracts
  • Current Contents: Agriculture, Biology and Environmental Sciences
  • Elsevier Science Navigator
  • Focus On: Veterinary Science and Medicine
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Science Citation Index
  • Science Citation Index Expanded (SciSearch)
  • SCOPUS
  • The ISI Alerting Services
  • Zoological Abstracts

 

2021  
Web of Science  
Total Cites
WoS
1040
Journal Impact Factor 0,959
Rank by Impact Factor Veterinary Sciences 103/144
Impact Factor
without
Journal Self Cites
0,876
5 Year
Impact Factor
1,222
Journal Citation Indicator 0,48
Rank by Journal Citation Indicator Veterinary Sciences 106/168
Scimago  
Scimago
H-index
36
Scimago
Journal Rank
0,313
Scimago Quartile Score Veterinary (miscellaneous) (Q2)
Scopus  
Scopus
Cite Score
1,7
Scopus
CIte Score Rank
General Veterinary 79/183 (Q2)
Scopus
SNIP
0,610

2020  
Total Cites 987
WoS
Journal
Impact Factor
0,955
Rank by Veterinary Sciences 101/146 (Q3)
Impact Factor  
Impact Factor 0,920
without
Journal Self Cites
5 Year 1,164
Impact Factor
Journal  0,57
Citation Indicator  
Rank by Journal  Veterinary Sciences 93/166 (Q3)
Citation Indicator   
Citable 49
Items
Total 49
Articles
Total 0
Reviews
Scimago 33
H-index
Scimago 0,395
Journal Rank
Scimago Veterinary (miscellaneous) Q2
Quartile Score  
Scopus 355/217=1,6
Scite Score  
Scopus General Veterinary 73/183 (Q2)
Scite Score Rank  
Scopus 0,565
SNIP  
Days from  145
submission  
to acceptance  
Days from  150
acceptance  
to publication  
Acceptance 19%
Rate

 

2019  
Total Cites
WoS
798
Impact Factor 0,991
Impact Factor
without
Journal Self Cites
0,897
5 Year
Impact Factor
1,092
Immediacy
Index
0,119
Citable
Items
59
Total
Articles
59
Total
Reviews
0
Cited
Half-Life
9,1
Citing
Half-Life
9,2
Eigenfactor
Score
0,00080
Article Influence
Score
0,253
% Articles
in
Citable Items
100,00
Normalized
Eigenfactor
0,09791
Average
IF
Percentile
42,606
Scimago
H-index
32
Scimago
Journal Rank
0,372
Scopus
Scite Score
335/213=1,6
Scopus
Scite Score Rank
General Veterinary 62/178 (Q2)
Scopus
SNIP
0,634
Acceptance
Rate
18%

 

Acta Veterinaria Hungarica
Publication Model Hybrid
Submission Fee none
Article Processing Charge 1100 EUR/article
Printed Color Illustrations 40 EUR (or 10 000 HUF) + VAT / piece
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 2022 Online subsscription: 710 EUR / 892 USD
Print + online subscription: 824 EUR / 1028 USD
Subscription fee 2023 Online subsscription: 732 EUR / 892 USD
Print + online subscription: 848 EUR / 1028 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 Veterinaria Hungarica
Language English
Size A4
Year of
Foundation
1951
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 0236-6290 (Print)
ISSN 1588-2705 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Jun 2022 0 0 0
Jul 2022 2 0 0
Aug 2022 12 0 0
Sep 2022 32 0 0
Oct 2022 7 0 0
Nov 2022 12 1 2
Dec 2022 0 0 0