{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T04:23:17Z","timestamp":1790310197487,"version":"4.1.0"},"reference-count":80,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2019,12,18]],"date-time":"2019-12-18T00:00:00Z","timestamp":1576627200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002428","name":"Austrian Science Fund","doi-asserted-by":"publisher","award":["FWF-P29304-B22"],"award-info":[{"award-number":["FWF-P29304-B22"]}],"id":[{"id":"10.13039\/501100002428","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>The present study was conducted from July to August 2018 on milk samples taken at dairy farms in the Northern Province and Kigali District of Rwanda in order to identify Staphylococcus spp. associated with bovine intramammary infection. A total of 161 staphylococcal isolates originating from quarter milk samples of 112 crossbred dairy cattle were included in the study. Antimicrobial susceptibility testing was performed and isolates were examined for the presence of various resistance genes. Staphylococcus aureus isolates were also analyzed for the presence of virulence factors, genotyped by spa typing and further phenotypically subtyped for capsule expression using Fourier Transform Infrared (FTIR) spectroscopy. Selected S. aureus were characterized using DNA microarray technology, multi-locus sequence typing (MLST) and whole-genome sequencing. All mecA-positive staphylococci were further genotyped using dru typing. In total, 14 different staphylococcal species were detected, with S. aureus being most prevalent (26.7%), followed by S. xylosus (22.4%) and S. haemolyticus (14.9%). A high number of isolates was resistant to penicillin and tetracycline. Various antimicrobial and biocide resistance genes were detected. Among S. aureus, the Panton\u2013Valentine leukocidin (PVL) genes, as well as bovine leukocidin (LukM\/LukF-P83) genes, were detected in two and three isolates, respectively, of which two also carried the toxic shock syndrome toxin gene tsst-1 bovine variant. t1236 was the predominant spa type. FTIR-based capsule serotyping revealed a high prevalence of non-encapsulated S. aureus isolates (89.5%). The majority of the selected S. aureus isolates belonged to clonal complex (CC) 97 which was determined using DNA microarray based assignment. Three new MLST sequence types were detected.<\/jats:p>","DOI":"10.3390\/antibiotics9010001","type":"journal-article","created":{"date-parts":[[2019,12,20]],"date-time":"2019-12-20T09:50:33Z","timestamp":1576835433000},"page":"1","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":31,"title":["Characterization of Antibiotic and Biocide Resistance Genes and Virulence Factors of Staphylococcus Species Associated with Bovine Mastitis in Rwanda"],"prefix":"10.3390","volume":"9","author":[{"given":"Fruzsina Ir\u00e9n","family":"Ant\u00f3k","sequence":"first","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8527-1472","authenticated-orcid":false,"given":"Rosa","family":"Mayrhofer","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helene","family":"Marbach","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean Claude","family":"Masengesho","sequence":"additional","affiliation":[{"name":"New Vision Veterinary Hospital, Musanze, Rwanda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helga","family":"Keinprecht","sequence":"additional","affiliation":[{"name":"New Vision Veterinary Hospital, Musanze, Rwanda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vedaste","family":"Nyirimbuga","sequence":"additional","affiliation":[{"name":"New Vision Veterinary Hospital, Musanze, Rwanda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Otto","family":"Fischer","sequence":"additional","affiliation":[{"name":"New Vision Veterinary Hospital, Musanze, Rwanda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Lepuschitz","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Hygiene, Austrian Agency for Health and Food Safety, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Werner","family":"Ruppitsch","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Hygiene, Austrian Agency for Health and Food Safety, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7384-0594","authenticated-orcid":false,"given":"Monika","family":"Ehling-Schulz","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea T.","family":"Fe\u00dfler","sequence":"additional","affiliation":[{"name":"Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universit\u00e4t Berlin, 10115 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6303-8212","authenticated-orcid":false,"given":"Stefan","family":"Schwarz","sequence":"additional","affiliation":[{"name":"Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universit\u00e4t Berlin, 10115 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Monecke","sequence":"additional","affiliation":[{"name":"Leibniz Institute of Photonic Technology (IPHT), 07743 Jena, Germany"},{"name":"InfectoGnostics Research Campus, 07743 Jena, Germany"},{"name":"Institute for Medical Microbiology and Hygiene, Technical University of Dresden, 01307 Dresden, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ralf","family":"Ehricht","sequence":"additional","affiliation":[{"name":"Leibniz Institute of Photonic Technology (IPHT), 07743 Jena, Germany"},{"name":"InfectoGnostics Research Campus, 07743 Jena, Germany"},{"name":"Friedrich Schiller University Jena, Institute of Physical Chemistry, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tom","family":"Grunert","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joachim","family":"Spergser","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1401-2961","authenticated-orcid":false,"given":"Igor","family":"Loncaric","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,12,18]]},"reference":[{"key":"ref_1","unstructured":"Mendez-Vilas, A. (2011). War against mastitis: Current concepts on controlling bovine mastitis pathogens. Science against Microbial Pathogens: Communicafing Current Research and Technological Advances, World Scientific."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1645","DOI":"10.1007\/s11250-017-1372-y","article-title":"Current status of cattle production system in Nyagatare District-Rwanda","volume":"49","author":"Mazimpaka","year":"2017","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_3","unstructured":"(2019, October 11). Laenderdaten Info. Available online: https:\/\/www.laenderdaten.info\/Afrika\/Ruanda\/bevoelkerungswachstum.php."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2018","DOI":"10.3168\/jds.S0022-0302(01)74645-0","article-title":"Sensitivity and specificity of somatic cell count and California Mastitis Test for identifying intramammary infection in early lactation","volume":"84","author":"Sargeant","year":"2010","journal-title":"J. Dairy Sci."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Mpatswenumugabo, J.P., Bebora, L.C., Gitao, G.C., Mobegi, V.A., Iraguha, B., Kamana, O., and Shumbusho, B. (2017). Prevalence of subclinical mastitis and distribution of pathogens in dairy farms of Rubavu and Nyabihu Districts, Rwanda. J. Vet. Med., 1\u20138.","DOI":"10.1155\/2017\/8456713"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"567","DOI":"10.17221\/7138-VETMED","article-title":"Prevalence of mastitis pathogens in milk from clinically healthy cows","volume":"58","author":"Cervinkova","year":"2013","journal-title":"Vet. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4102\/jsava.v86i1.1228","article-title":"Bovine mastitis prevalence and associated risk factors in dairy cows in Nyagatare District, Rwanda","volume":"86","author":"Iraguha","year":"2015","journal-title":"J. S. Afr. Vet. Assoc."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1017\/S002202999600194X","article-title":"Patterns of clinical mastitis manifestations in Danish organic dairy herds","volume":"64","author":"Vaarst","year":"1997","journal-title":"J. Dairy Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1007\/s11250-017-1290-z","article-title":"Assessment of antibiotic use in farm animals in Rwanda","volume":"49","author":"Manishimwe","year":"2017","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/microbiolspec.ARBA-0010-2017","article-title":"Antimicrobial resistance among staphylococci of animal origin","volume":"6","author":"Schwarz","year":"2018","journal-title":"Microbiol. Spectr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"865","DOI":"10.4269\/ajtmh.14-0607","article-title":"High prevalence of antimicrobial resistance among common bacterial isolates in a tertiary healthcare facility in Rwanda","volume":"92","author":"Ntirenganya","year":"2015","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4102\/jsava.v88i0.1464","article-title":"Comparison of cow-side diagnostic tests for subclinical mastitis of dairy cows in Musanze district, Rwanda","volume":"88","author":"Iraguha","year":"2017","journal-title":"J. S. Afr. Vet. Assoc."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Ndahetuye, J.B., Persson, Y., Nyman, A.K., Tukei, M., Ongol, M.P., and B\u00e5ge, R. (2019). Aetiology and prevalence of subclinical mastitis in dairy herds in peri-urban areas of Kigali in Rwanda. Trop. Anim. Health Prod., 1\u20138.","DOI":"10.1007\/s11250-019-01905-2"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1089\/mdr.2007.713","article-title":"Aminoglycoside resistance in members of the Staphylococcus sciuri group","volume":"13","author":"Hauschild","year":"2007","journal-title":"Microb. Drug Resist."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1007\/s11250-013-0455-7","article-title":"Prevalence of subclinical mastitis in dairy farms in urban and peri-urban areas of Kampala, Uganda","volume":"46","author":"Persson","year":"2014","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1007\/s11250-017-1424-3","article-title":"Prevalence of bovine subclinical mastitis and antibiotic susceptibility patterns of major mastitis pathogens isolated in Unguja island of Zanzibar, Tanzania","volume":"50","author":"Suleiman","year":"2018","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.vetmic.2008.09.015","article-title":"Coagulase-negative staphylococci-emerging mastitis pathogens","volume":"134","author":"Taponen","year":"2009","journal-title":"Vet. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4102\/jsava.v85i1.950","article-title":"Mastitogenic bacteria isolated from dairy cows in Kenya and their antimicrobial sensitivity","volume":"85","author":"Gitau","year":"2014","journal-title":"J. S. Afr. Vet. Assoc."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.tvjl.2014.11.001","article-title":"Identification, typing, ecology and epidemiology of coagulase negative staphylococci associated with ruminants","volume":"203","author":"Vanderhaeghen","year":"2015","journal-title":"Vet. J."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4962","DOI":"10.3168\/jds.2009-2184","article-title":"Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci","volume":"92","author":"Thorberg","year":"2009","journal-title":"J. Dairy Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"35","DOI":"10.4236\/ojvm.2014.44005","article-title":"High prevalence of subclinical mastitis and multidrug resistant Staphylococcus aureus are a threat to dairy cattle production in Kiboga District (Uganda)","volume":"4","author":"Kasozi","year":"2014","journal-title":"Open J. Vet. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3271","DOI":"10.5897\/AJMR2014.6998","article-title":"Antibiotic resistance trend of Staphylococcus aureus isolated between 2010 and 2012 from mastitis cases in Azawak Zebu in Niger","volume":"8","author":"Duprez","year":"2014","journal-title":"Afr. J. Microbiol. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1093\/jac\/dkq021","article-title":"Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis","volume":"65","author":"Scott","year":"2010","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_24","first-page":"2433","article-title":"Bovine mastitis in Finland 2001\u2014prevalence, distribution of bacteria, and antimicrobial resistance","volume":"87","author":"Haveri","year":"2010","journal-title":"J. Dairy Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.bjm.2016.10.011","article-title":"Correlation of phenotypic tests with the presence of the blaZ gene for detection of beta-lactamase","volume":"48","author":"Ferreira","year":"2017","journal-title":"Braz. J. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1016\/j.ijantimicag.2018.07.026","article-title":"Detection and characterization of methicillin-resistant and susceptible coagulase-negative staphylococci in milk from cows with clinical mastitis in Tunisia","volume":"52","author":"Klibi","year":"2018","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2797","DOI":"10.1128\/AAC.46.9.2797-2803.2002","article-title":"Frequency of disinfectant resistance genes and genetic linkage with \u03b2-lactamase transposon Tn552 among clinical staphylococci","volume":"46","author":"Sidhu","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4363","DOI":"10.1128\/JCM.43.9.4363-4368.2005","article-title":"Widespread distribution of disinfectant resistance genes among staphylococci of bovine and caprine origin in Norway","volume":"43","author":"Bjorland","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1128\/AAC.02140-15","article-title":"High prevalence of biocide resistance determinants in Staphylococcus aureus isolates from three African countries","volume":"60","author":"Coelho","year":"2016","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.vetmic.2016.06.004","article-title":"Heavy metal and disinfectant resistance genes among livestock-associated methicillin-resistant Staphylococcus aureus isolates","volume":"191","author":"Lauzat","year":"2016","journal-title":"Vet. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/j.rvsc.2016.02.009","article-title":"Dissemination of metal resistance genes among animal methicillin-resistant coagulase-negative staphylococci","volume":"105","author":"Butaye","year":"2016","journal-title":"Res. Vet. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0378-1135(97)00172-7","article-title":"Prevalence of capsular serotypes among Staphylococcus aureus isolates from cows with mastitis in the United States","volume":"51","author":"Guidry","year":"1997","journal-title":"Vet. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"846","DOI":"10.1128\/JCM.38.2.846-850.2000","article-title":"Capsule expression by bovine isolates of Staphylococcus aureus from Argentina: Genetic and epidemiologic analyses","volume":"38","author":"Sordelli","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"K\u00fcmmel, J., Stessl, B., Gonano, M., Walcher, G., Bereuter, O., Fricker, M., Grunert, T., Wagner, M., and Ehling-Schulz, M. (2016). Staphylococcus aureus entrance into the dairy chain: Tracking S. aureus from dairy cow to cheese. Front. Microbiol., 1603.","DOI":"10.3389\/fmicb.2016.01603"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"15968","DOI":"10.1038\/s41598-018-34371-1","article-title":"Distinct phenotypic traits of Staphylococcus aureus are associated with persistent, contagious bovine intramammary infections","volume":"8","author":"Grunert","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.2217\/fmb.10.147","article-title":"Staphylococcus aureus adaptation to the host and persistence: Role of loss of capsular polysaccharide expression","volume":"5","author":"Tuchscherr","year":"2010","journal-title":"Future Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"512","DOI":"10.3168\/jds.2015-9589","article-title":"Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer","volume":"99","author":"Boss","year":"2016","journal-title":"J. Dairy Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2130","DOI":"10.1128\/JCM.01940-09","article-title":"Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans","volume":"48","author":"Hata","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"511","DOI":"10.3389\/fmicb.2017.00511","article-title":"Molecular characterization of Staphylococcus aureus isolated from bovine mastitis and close human contacts in South African dairy herds: Genetic diversity and inter-species host transmission","volume":"8","author":"Schmidt","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.vetmic.2018.08.003","article-title":"New host shift from human to cows within Staphylococcus aureus involved in bovine mastitis and nasal carriage of animal\u2019s caretakers","volume":"223","author":"Akkou","year":"2018","journal-title":"Vet. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Asiimwe, B.B., Baldan, R., Trovato, A., and Cirillo, D.M. (2017). Prevalence and molecular characteristics of Staphylococcus aureus, including methicillin resistant strains, isolated from bulk can milk and raw milk products in pastoral communities of South-West Uganda. BMC Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2524-4"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"127","DOI":"10.3389\/fcimb.2017.00127","article-title":"Molecular characteristics of Staphylococcus aureus causing bovine mastitis between 2014 and 2015","volume":"7","author":"Li","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1007\/s10096-017-2904-0","article-title":"Characterisation of Staphylococcus aureus isolates from bloodstream infections, Democratic Republic of the Congo","volume":"36","author":"Vandendriessche","year":"2017","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1111\/j.1469-0691.2011.03534.x","article-title":"Virulence factors and genotypes of Staphylococcus aureus from infection and carriage in Gabon","volume":"17","author":"Schaumburg","year":"2011","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.jgar.2013.05.006","article-title":"Prevalence of nasal carriage and diversity of Staphylococcus aureus among inpatients and hospital staff at Korle Bu Teaching Hospital, Ghana","volume":"1","author":"Egyir","year":"2013","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1186\/s12941-016-0171-z","article-title":"Molecular characterization of Staphylococcus aureus isolates from various healthcare institutions in Nairobi, Kenya: A cross sectional study","volume":"15","author":"Omuse","year":"2016","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.3389\/fmicb.2015.01160","article-title":"An assessment on DNA microarray and sequence-based methods for the characterization of methicillin-susceptible Staphylococcus aureus from Nigeria","volume":"6","author":"Shittu","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Seni, J., Bwanga, F., Najjuka, C.F., Makobore, P., Okee, M., Mshana, S.E., Kidenya, B.R., Joloba, M.L., and Kateete, D.P. (2013). Molecular Characterization of Staphylococcus aureus from patients with surgical site infections at Mulago Hospital in Kampala, Uganda. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0066153"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1111\/1469-0691.12690","article-title":"New epidemiology of Staphylococcus aureus infection in Africa","volume":"20","author":"Schaumburg","year":"2014","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12917-018-1558-1","article-title":"Characterization of Staphylococcus aureus isolated from milk samples of dairy cows in small holder farms of North-Western Ethiopia","volume":"14","author":"Mekonnen","year":"2018","journal-title":"BMC Vet. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1271\/bbb.68.981","article-title":"Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: Structures, pore-forming mechanism, and organization of the genes","volume":"68","author":"Kaneko","year":"2004","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"37759","DOI":"10.1038\/srep37759","article-title":"LukMF\u2032 is the major secreted leukocidin of bovine Staphylococcus aureus and is produced in vivo during bovine mastitis","volume":"6","author":"Vrieling","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/1297-9716-43-42","article-title":"Leukocidin genes lukF-P83 and lukM are associated with Staphylococcus aureus clonal complexes 151, 479 and 133 isolated from bovine udder infections in Thuringia, Germany","volume":"43","author":"Schlotter","year":"2012","journal-title":"Vet. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.fm.2017.01.017","article-title":"East and West African milk products are reservoirs for human and livestock-associated Staphylococcus aureus","volume":"65","author":"Jans","year":"2017","journal-title":"Food Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.vetmic.2014.09.020","article-title":"Evaluation of biofilm formation using milk in a flow cell model and microarray characterization of Staphylococcus aureus strains from bovine mastitis","volume":"174","author":"Snel","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"33","DOI":"10.3201\/eid1202.050962","article-title":"Sequencing and staphylococci identification","volume":"12","author":"Mellmann","year":"2006","journal-title":"Emerg. Infect. Dis."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.vetmic.2013.11.022","article-title":"Identification and characterization of methicillin-resistant Staphylococcus aureus (MRSA) from Austrian companion animals and horses","volume":"168","author":"Loncaric","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"6256","DOI":"10.3168\/jds.2015-9715","article-title":"Diversity and antimicrobial susceptibility profiling of staphylococci isolated from bovine mastitis cases and close human contacts","volume":"98","author":"Schmidt","year":"2015","journal-title":"J. Dairy Sci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1128\/AAC.44.2.231-238.2000","article-title":"Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis","volume":"44","author":"Martineau","year":"2000","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1093\/jac\/43.1.5","article-title":"Host range of the ermF rRNA methylase gene in bacteria of human and animal origin","volume":"43","author":"Chung","year":"1999","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"58086","DOI":"10.18632\/oncotarget.19491","article-title":"Dissemination of macrolides, fusidic acid and mupirocin resistance among Staphylococcus aureus clinical isolates","volume":"8","author":"Liu","year":"2017","journal-title":"Oncotarget"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"4746","DOI":"10.1128\/AAC.00627-12","article-title":"New MLS B resistance gene erm(43) in Staphylococcus lentus","volume":"56","author":"Schwendener","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"6133","DOI":"10.1128\/AAC.02949-14","article-title":"The novel macrolide-lincosamide-streptogramin B resistance gene erm(44) is associated with a prophage in Staphylococcus xylosus","volume":"58","author":"Wipf","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/j.vetmic.2015.03.027","article-title":"Identification of ABC transporter genes conferring combined pleuromutilin-lincosamide-streptogramin A resistance in bovine methicillin-resistant Staphylococcus aureus and coagulase-negative staphylococci","volume":"177","author":"Wendlandt","year":"2015","journal-title":"Vet. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1093\/jac\/dkt015","article-title":"Detection and new genetic environment of the pleuromutilin-lincosamide-streptogramin a resistance gene lsa(e) in methicillin resistant Staphylococcus aureus of swine origin","volume":"68","author":"Li","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1128\/AAC.43.5.1062","article-title":"Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci","volume":"43","author":"Lina","year":"1999","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1093\/jac\/dkt482","article-title":"Identification of a novel vga(E) gene variant that confers resistance to pleuromutilins, lincosamides and streptogramin A antibiotics in staphylococci of porcine origin","volume":"69","author":"Li","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1093\/jac\/dkh457","article-title":"Nucleotide sequence and organization of the multiresistance plasmid pSCFS1 from Staphylococcus sciuri","volume":"54","author":"Kehrenberg","year":"2004","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1128\/AAC.50.4.1156-1163.2006","article-title":"Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates","volume":"50","author":"Kehrenberg","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"4444","DOI":"10.1128\/JCM.00868-06","article-title":"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","volume":"44","author":"Schnellmann","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"3052","DOI":"10.1128\/AEM.02260-10","article-title":"Virulence and resistance determinants of German Staphylococcus aureus ST398 isolates from nonhuman sources","volume":"77","author":"Tenhagen","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/S0378-1135(98)00234-X","article-title":"Tetracycline resistance in Staphylococcus spp. from domestic animals","volume":"63","author":"Schwarz","year":"1998","journal-title":"Vet. Microbiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"964","DOI":"10.1111\/j.1469-0691.2008.02073.x","article-title":"Usefulness of mec-associated direct repeat unit (dru) typing in the epidemiological analysis of highly clonal methicillin-resistant Staphylococcus aureus in Scotland","volume":"14","author":"Goering","year":"2008","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2261","DOI":"10.1128\/JCM.00581-13","article-title":"Rapid and reliable identification of Staphylococcus aureus capsular serotypes by means of artificial neural network-assisted Fourier-transform infrared spectroscopy","volume":"51","author":"Grunert","year":"2013","journal-title":"J. Clin. Microbiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.syapm.2016.03.003","article-title":"High-resolution subtyping of Staphylococcus aureus strains by means of Fourier-transform infrared spectroscopy","volume":"39","author":"Johler","year":"2016","journal-title":"Syst. Appl. Microbiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1111\/j.1469-0691.2008.01986.x","article-title":"DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from Eastern Saxony","volume":"14","author":"Monecke","year":"2008","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2365","DOI":"10.1128\/JCM.00262-14","article-title":"Bacterial whole-genome sequencing revisited: Portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes","volume":"52","author":"Leopold","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"e01166-17","DOI":"10.1128\/genomeA.01166-17","article-title":"Draft genome sequence of a community-acquired methicillin-resistant Staphylococcus aureus USA300 isolate from a river sample","volume":"5","author":"Lepuschitz","year":"2017","journal-title":"Genome Announc."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"9467","DOI":"10.1038\/s41598-018-27781-8","article-title":"Characterization of a community-acquired-MRSA USA300 isolate from a river sample in Austria and whole genome sequence based comparison to a diverse collection of USA300 isolates","volume":"8","author":"Lepuschitz","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_80","first-page":"497","article-title":"One world, one health: Humans, animals and the environment are inextricably linked\u2014A fact that needs to be remembered and exploited in our modern approach to health","volume":"6","author":"Hoal","year":"2013","journal-title":"EMBO Rep."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/1\/1\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:43:13Z","timestamp":1760190193000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/1\/1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,18]]},"references-count":80,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,1]]}},"alternative-id":["antibiotics9010001"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics9010001","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,18]]}}}