{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T03:02:10Z","timestamp":1787022130654,"version":"build-2736575974"},"reference-count":44,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2023,8,30]],"date-time":"2023-08-30T00:00:00Z","timestamp":1693353600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"\n Staphylococcus pseudintermedius<\/jats:italic>\n is an important cause of clinical infections in small-animal-veterinary medicine. Evolutionary changes of strains using multilocus sequence typing (MLST) have been observed among\n S<\/jats:italic>\n .\n pseudintermedius<\/jats:italic>\n in European countries and the United States. However, there are limited or no studies on the detection of methicillin resistant\n Staphylococcus pseudintermedius<\/jats:italic>\n (MRSP) and predominating MLST strains in South Africa. Therefore, this study aimed to determine the molecular epidemiology of\n S<\/jats:italic>\n .\n pseudintermedius<\/jats:italic>\n in South Africa. Twenty-six, non-duplicate, clinical isolates from dogs were obtained as convenience samples from four provinces in South Africa. The Kirby Bauer disk diffusion test was used to determine antimicrobial susceptibility. We used Resfinder and the Comprehensive Antibiotic Resistance Database (CARD) to detect antimicrobial resistance genes. Virulence genes were identified using the virulence factor database and Basic Local Alignment Search Tool (BLASTN) on Geneious prime. geoBURST analysis was used to study relationships between MLST. Finally, the maximum likelihood phylogeny was determined using Randomized Axelerated Maximum Likelihood (RAxML). Twenty-three isolates were confirmed as\n S<\/jats:italic>\n .\n pseudintermedius<\/jats:italic>\n of which 14 were MRSP. In addition to \u03b2-lactam antimicrobials, MRSP isolates were resistant to tetracycline (85.7%), doxycycline (92.8%), kanamycin (92.8%), and gentamicin (85.7%). The isolates harbored antimicrobial resistance genes (\n tetM<\/jats:italic>\n ,\n ermB<\/jats:italic>\n ,\n drfG<\/jats:italic>\n ,\n cat<\/jats:italic>\n ,\n aac(6\u2019)-Ie-aph(2\u201d)-Ia<\/jats:italic>\n ,\n ant(6)-Ia<\/jats:italic>\n , and\n aph(3\u2019)-III<\/jats:italic>\n ) and virulence genes (\n AdsA<\/jats:italic>\n ,\n geh<\/jats:italic>\n ,\n icaA<\/jats:italic>\n , and\n lip)<\/jats:italic>\n . MLST analysis showed that ST2228, ST2229, ST2230, ST2231, ST2232, ST2318, ST2326 and ST2327 are unique sequence types in South Africa. Whereas, previously reported major STs including ST45, ST71, ST181, ST551 and ST496 were also detected. The geoBURST and phylogenetic analysis suggests that the isolates in South Africa are likely genetically related to isolates identified in other countries. Highly resistant MRSP strains (ST496, ST71, and ST45) were reported that could present challenges in the treatment of canine infections in South Africa. Hence, we have gained a better understanding of the epidemiology of MRSP in the African continent, the genes involved in resistance and virulence factors associated with these organisms.\n <\/jats:p>","DOI":"10.1371\/journal.pone.0290645","type":"journal-article","created":{"date-parts":[[2023,8,30]],"date-time":"2023-08-30T13:29:42Z","timestamp":1693402182000},"page":"e0290645","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":11,"title":["The molecular epidemiology and antimicrobial resistance of Staphylococcus pseudintermedius canine clinical isolates submitted to a veterinary diagnostic laboratory in South Africa"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4378-2976","authenticated-orcid":true,"given":"Lufuno","family":"Phophi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed","family":"Abouelkhair","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebekah","family":"Jones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maryke","family":"Henton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel N.","family":"Qekwana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4490-7347","authenticated-orcid":true,"given":"Stephen A.","family":"Kania","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,8,30]]},"reference":[{"issue":"1","key":"pone.0290645.ref001","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1089\/mdr.2016.0250","article-title":"Clonal Complexes and Antimicrobial Susceptibility Profiles of Staphylococcus pseudintermedius Isolates from Dogs in the United States","volume":"24","author":"R Videla","year":"2018","journal-title":"Microb Drug Resist Larchmt N"},{"issue":"4","key":"pone.0290645.ref002","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.diagmicrobio.2016.05.008","article-title":"Human infections due to Staphylococcus pseudintermedius, an emerging zoonosis of canine origin: report of 24 cases","volume":"85","author":"R Somayaji","year":"2016","journal-title":"Diagn Microbiol Infect Dis"},{"key":"pone.0290645.ref003","first-page":"43","article-title":"Coagulase-Positive and Coagulase-Negative Staphylococci Animal Diseases","author":"F Marsilio","year":"2018","journal-title":"In: Pet-to-Man Travelling Staphylococci: A World in Progress. Elsevier Inc."},{"issue":"12","key":"pone.0290645.ref004","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1009961","article-title":"From canines to humans: Clinical importance of Staphylococcus pseudintermedius","volume":"17","author":"KC Carroll","year":"2021","journal-title":"PLoS Pathog"},{"key":"pone.0290645.ref005","article-title":"Systematic review on global epidemiology of methicillin-resistant Staphylococcus pseudintermedius: Inference of population structure from multilocus sequence typing data","volume":"7","author":"TP Dos Santos","year":"2016","journal-title":"Frontiers in Microbiology. Frontiers Media S.A"},{"issue":"1","key":"pone.0290645.ref006","first-page":"14","article-title":"Molecular characteristics of new clonal complexes of Staphylococcus pseudintermedius from clinically normal dogs","volume":"38","author":"JI Han","year":"2017"},{"issue":"1","key":"pone.0290645.ref007","doi-asserted-by":"crossref","DOI":"10.1186\/s12917-019-1990-x","article-title":"Identification and molecular epidemiology of methicillin resistant Staphylococcus pseudintermedius strains isolated from canine clinical samples in Argentina","volume":"15","author":"P Gagetti","year":"2019","journal-title":"BMC Vet Res"},{"issue":"8","key":"pone.0290645.ref008","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1111\/j.1863-2378.2011.01398.x","article-title":"Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: Indirect evidence of zoonotic transmission","volume":"58","author":"NC Paul","year":"2011","journal-title":"Zoonoses Public Health"},{"issue":"3\u20134","key":"pone.0290645.ref009","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.vetmic.2011.03.026","article-title":"The role of mecA and blaZ regulatory elements in mecA expression by regional clones of methicillin-resistant Staphylococcus pseudintermedius","volume":"151","author":"CC Black","year":"2011","journal-title":"Vet Microbiol"},{"issue":"6","key":"pone.0290645.ref010","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1002\/mbo3.258","article-title":"Methicillin\u2010resistant Staphylococcus pseudintermedius (MRSP) from healthy dogs in Norway\u2013occurrence, genotypes and comparison to clinical MRSP","volume":"4","author":"EE Kjellman","year":"2015","journal-title":"MicrobiologyOpen"},{"issue":"8","key":"pone.0290645.ref011","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1002\/iub.1289","article-title":"Critical Review Penicillin-binding Protein 2a of Methicillin-resistant Staphylococcus aureus","volume":"66","author":"J Fishovitz","year":"2014","journal-title":"IUBMB Life"},{"key":"pone.0290645.ref012","first-page":"117","volume-title":"AIMS Microbiology","author":"MU Okwu","year":"2019"},{"issue":"4","key":"pone.0290645.ref013","article-title":"Burden and predictors of Staphylococcus aureus and S. pseudintermedius infections among dogs presented at an academic veterinary hospital in South Africa","author":"DN Qekwana","year":"2017","journal-title":"PeerJ"},{"issue":"DEC","key":"pone.0290645.ref014","doi-asserted-by":"crossref","first-page":"3055","DOI":"10.3389\/fmicb.2018.03055","article-title":"Evolution of the population structure of Staphylococcus pseudintermedius in France","volume":"9","author":"M Bergot","year":"2018","journal-title":"Front Microbiol"},{"issue":"2","key":"pone.0290645.ref015","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.cimid.2014.01.003","article-title":"Prevalence and characterization of Staphylococcus aureus and Staphylococcus pseudintermedius isolated from companion animals and environment in the veterinary teaching hospital in Zambia, Africa","volume":"37","author":"JH Youn","year":"2014","journal-title":"Comp Immunol Microbiol Infect Dis"},{"issue":"10","key":"pone.0290645.ref016","doi-asserted-by":"crossref","first-page":"e01599","DOI":"10.1128\/genomeA.01599-17","article-title":"Complete Genome Sequences of Three Staphylococcus pseudintermedius Strains Isolated from Botswana","volume":"6","author":"MA Abouelkhair","year":"2018","journal-title":"Genome Announc"},{"key":"pone.0290645.ref017","doi-asserted-by":"crossref","first-page":"620491","DOI":"10.3389\/fvets.2021.620491","article-title":"Molecular Epidemiology of Clinical and Colonizing Methicillin-Resistant Staphylococcus Isolates in Companion Animals","volume":"8","author":"H Rynhoud","year":"2021","journal-title":"Front Vet Sci"},{"issue":"1","key":"pone.0290645.ref018","first-page":"1","article-title":"Patterns and predictors of antimicrobial resistance among Staphylococcus spp","volume":"13","author":"DN Qekwana","year":"2017","journal-title":"from canine clinical cases presented at a veterinary academic hospital in South Africa. BMC Vet Res"},{"key":"pone.0290645.ref019","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.vetmic.2017.11.018","article-title":"Clonal diversity and geographic distribution of methicillin-resistant Staphylococcus pseudintermedius from Australian animals: Discovery of novel sequence types","volume":"213","author":"KA Worthing","year":"2018","journal-title":"Vet Microbiol"},{"key":"pone.0290645.ref020","volume-title":"Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement","author":"JB Patel","year":"2015"},{"key":"pone.0290645.ref021","article-title":"Assessment of disk diffusion and E-test methods to determine antimicrobial activity of cefalotin and vancomycin on clinical isolates of Staphylococcus aureus","author":"M Rezaeifar","year":"2016"},{"key":"pone.0290645.ref022","unstructured":"CASFM_2013.pdf [Internet]. [cited 2023 Jun 1]. Available from: https:\/\/www.sfm-microbiologie.org\/wp-content\/uploads\/2020\/07\/CASFM_2013.pdf."},{"key":"pone.0290645.ref023","unstructured":"Clinical and Laboratory Standard Institute (CLSI). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals [Internet]. 5th-CLSI VET01S ed. 2020 [cited 2023 Jun 29]. Available from: https:\/\/clsi.org\/media\/m1gppkx2\/vet01sed5_sample.pdf."},{"key":"pone.0290645.ref024","first-page":"170","article-title":"Clinical and Laboratory Standards Institute","year":"2018","journal-title":"Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animalsVET08."},{"issue":"D1","key":"pone.0290645.ref025","doi-asserted-by":"crossref","first-page":"D535","DOI":"10.1093\/nar\/gkw1017","article-title":"Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center","volume":"45","author":"AR Wattam","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"pone.0290645.ref026","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1093\/nar\/gki008","article-title":"VFDB: A reference database for bacterial virulence factors","volume":"33","author":"L Chen","year":"2005","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"pone.0290645.ref027","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1128\/JCM.02421-12","article-title":"Multilocus Sequence Typing for Characterization of Staphylococcus pseudintermedius","volume":"51","author":"SM Solyman","year":"2013","journal-title":"J Clin Microbiol"},{"issue":"1","key":"pone.0290645.ref028","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2105-13-87","article-title":"PHYLOViZ: Phylogenetic inference and data visualization for sequence based typing methods","volume":"13","author":"AP Francisco","year":"2012","journal-title":"BMC Bioinformatics"},{"issue":"5","key":"pone.0290645.ref029","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: Multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"RC Edgar","year":"2004","journal-title":"Nucleic Acids Res"},{"issue":"9","key":"pone.0290645.ref030","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"A. Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"issue":"1","key":"pone.0290645.ref031","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1186\/1297-9716-45-70","article-title":"Enhanced adherence of methicillin-resistant Staphylococcus pseudintermedius sequence type 71 to canine and human corneocytes","volume":"45","author":"F Latronico","year":"2014","journal-title":"Vet Res"},{"issue":"1","key":"pone.0290645.ref032","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13028-015-0129-8","article-title":"Epidemiology of methicillin resistant Staphylococcus pseudintermedius in guide dogs in Finland","volume":"57","author":"T Gr\u00f6nthal","year":"2015","journal-title":"Acta Vet Scand"},{"issue":"1","key":"pone.0290645.ref033","doi-asserted-by":"crossref","DOI":"10.36303\/JSAVA.2022.93.1.505","article-title":"Prevalence of methicillin resistance in Staphylococcus pseudintermedius isolates from dogs with skin and ear infections in South Africa","volume":"93","author":"CD Prior","year":"2022","journal-title":"J S Afr Vet Assoc"},{"issue":"1","key":"pone.0290645.ref034","first-page":"1","article-title":"Patterns of antimicrobial, multidrug and methicillin resistance among Staphylococcus spp. isolated from canine specimens submitted to a diagnostic laboratory in Tennessee","volume":"18","author":"J Lord","year":"2022","journal-title":"USA: a descriptive study. BMC Vet Res"},{"issue":"4","key":"pone.0290645.ref035","first-page":"1021","article-title":"Antimicrobial resistance in Staphylococcus pseudintermedius and the molecular epidemiology of methicillin-resistant S. pseudintermedius in small animals in Finland","volume":"72","author":"T Gr\u00f6nthal","year":"2017","journal-title":"J Antimicrob Chemother"},{"issue":"2","key":"pone.0290645.ref036","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1128\/JCM.01288-15","article-title":"Changes in the population of methicillin-resistant Staphylococcus pseudintermedius and dissemination of antimicrobial-resistant phenotypes in the Netherlands","volume":"54","author":"B Duim","year":"2016","journal-title":"J Clin Microbiol"},{"key":"pone.0290645.ref037","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.vetmic.2018.09.013","article-title":"Comparative genomics of phenotypic antimicrobial resistances in methicillin-resistant Staphylococcus pseudintermedius of canine origin","volume":"225","author":"A Wegener","year":"2018","journal-title":"Vet Microbiol"},{"issue":"2","key":"pone.0290645.ref038","article-title":"Characterization of agr Groups of Staphylococcus pseudintermedius Isolates from Dogs in Texas","volume":"4","author":"V. Little S","year":"2019","journal-title":"mSphere"},{"issue":"12","key":"pone.0290645.ref039","doi-asserted-by":"crossref","DOI":"10.3390\/microorganisms7120702","article-title":"Investigation on Antibiotic-Resistance, Biofilm Formation and Virulence Factors in Multi Drug Resistant and Non Multi Drug Resistant Staphylococcus pseudintermedius","volume":"7","author":"G Meroni","year":"2019","journal-title":"Microorganisms"},{"key":"pone.0290645.ref040","doi-asserted-by":"crossref","first-page":"44","DOI":"10.3389\/fcimb.2012.00044","article-title":"Comparative genomics of the Staphylococcus intermedius group of animal pathogens","volume":"2","author":"NL Ben Zakour","year":"2012","journal-title":"Front Cell Infect Microbiol"},{"key":"pone.0290645.ref041","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1038\/nrmicro3161","article-title":"Adhesion, invasion and evasion: The many functions of the surface proteins of Staphylococcus aureus","volume":"12","author":"TJ Foster","year":"2014","journal-title":"Nature Reviews Microbiology"},{"issue":"9","key":"pone.0290645.ref042","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0204450","article-title":"Characterization of a leukocidin identified in Staphylococcus pseudintermedius","volume":"13","author":"MA Abouelkhair","year":"2018","journal-title":"PLoS ONE"},{"key":"pone.0290645.ref043","doi-asserted-by":"crossref","first-page":"109119","DOI":"10.1016\/j.vetmic.2021.109119","article-title":"Genomic insights into the emergence and spread of methicillin-resistant Staphylococcus pseudintermedius in veterinary clinics","volume":"258","author":"B Papi\u0107","year":"2021","journal-title":"Vet Microbiol"},{"key":"pone.0290645.ref044","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.vetmic.2017.07.025","article-title":"Changes in the population structure of canine methicillin-resistant Staphylococcus pseudintermedius in Poland","volume":"208","author":"M Kizerwetter-\u015awida","year":"2017","journal-title":"Vet Microbiol"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0290645","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,30]],"date-time":"2023-08-30T13:30:03Z","timestamp":1693402203000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0290645"}},"subtitle":[],"editor":[{"given":"Kunyan","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,8,30]]},"references-count":44,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8,30]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0290645","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,30]]}}}