{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T07:27:22Z","timestamp":1791358042195,"version":"4.3.1"},"reference-count":96,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2021,10,3]],"date-time":"2021-10-03T00:00:00Z","timestamp":1633219200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Staphylococcus aureus is a commensal resident of the skin and nasal cavities of humans and can cause various infections. Some toxigenic strains can contaminate food matrices and cause foodborne intoxications. The present study aimed to provide relevant information (clonal complex lineages, agr types, virulence and antimicrobial resistance-associated genes) based on DNA microarray analyses as well as the origins and dissemination of several circulating clones of 60 Staphylococcus aureus isolated from food matrices (n = 24), clinical samples (n = 20), and nasal carriers (n = 16) in northern Algeria. Staphylococcus aureus were genotyped into 14 different clonal complexes. Out of 60 S. aureus, 13 and 10 isolates belonged to CC1-MSSA and CC97-MSSA, respectively. The CC 80-MRSA-IV was the predominant S. aureus strain in clinical isolates. The accessory gene regulator allele agr group III was mainly found among clinical isolates (70.4%). Panton\u2013Valentine leukocidin genes lukF\/lukS-PV were detected in 13.3% of isolates that all belonged to CC80-MRSA. The lukF\/S-hlg, hlgA, and hla genes encoding for hemolysins and leucocidin components were detected in all Staphylococcusaureus isolates. Clinical and food isolates harbored more often the antibiotic resistance genes markers. Seventeen (28.3%) methicillin-resistant Staphylococcus aureus carrying the mecA gene localized on a SCCmec type IV element were identified. The penicillinase operon (blaZ\/I\/R) was found in 71.7% (43\/60) of isolates. Food isolates belonging to CC97-MSSA carried several antibiotic resistance genes (blaZ, ermB, aphA3, sat, tetM, and tetK). The results of this study showed that all clones were found in their typical host, but interestingly, some nasal carriers had isolates assigned to CC705 thought to be absent in humans. The detection of MRSA strains among food isolates should be considered as a potential public health risk. Therefore, controlling the antibiotics prescription for a rational use in human and animal infections is mandatory.<\/jats:p>","DOI":"10.3390\/pathogens10101276","type":"journal-article","created":{"date-parts":[[2021,10,8]],"date-time":"2021-10-08T21:26:20Z","timestamp":1633728380000},"page":"1276","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria"],"prefix":"10.3390","volume":"10","author":[{"given":"Rachid","family":"Achek","sequence":"first","affiliation":[{"name":"Faculty of Nature and Life and Earth Sciences, Djilali-Bounaama University, Soufay, Khemis-Miliana 44225, Algeria"},{"name":"Laboratory of Food Hygiene and Quality Assurance System, High National Veterinary School, Oued Smar, Algiers 16059, Algeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8585-4237","authenticated-orcid":false,"given":"Hosny","family":"El-Adawy","sequence":"additional","affiliation":[{"name":"Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, 07743 Jena, Germany"},{"name":"Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 35516, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helmut","family":"Hotzel","sequence":"additional","affiliation":[{"name":"Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9651-5495","authenticated-orcid":false,"given":"Ashraf","family":"Hendam","sequence":"additional","affiliation":[{"name":"Climate Change Information Center, Renewable Energy and Expert Systems (CCICREES), Agricultural Research Center, 9 Algamaa Street, Giza 12619, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Herbert","family":"Tomaso","sequence":"additional","affiliation":[{"name":"Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6612-0043","authenticated-orcid":false,"given":"Ralf","family":"Ehricht","sequence":"additional","affiliation":[{"name":"Leibniz Institute of Photonic Technology (IPHT), 07745 Jena, Germany"},{"name":"InfectoGnostics Research Campus Jena e. V., 07743 Jena, Germany"},{"name":"Institute of Physical Chemistry, Friedrich Schiller University Jena, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heinrich","family":"Neubauer","sequence":"additional","affiliation":[{"name":"Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ibrahim","family":"Nabi","sequence":"additional","affiliation":[{"name":"Faculty of Sciences, Yahia Far\u00e8s University, Urban Pole, M\u00e9d\u00e9a 26000, Algeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9639-5208","authenticated-orcid":false,"given":"Taha Mossadak","family":"Hamdi","sequence":"additional","affiliation":[{"name":"Laboratory of Food Hygiene and Quality Assurance System, High National Veterinary School, Oued Smar, Algiers 16059, Algeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Monecke","sequence":"additional","affiliation":[{"name":"Leibniz Institute of Photonic Technology (IPHT), 07745 Jena, Germany"},{"name":"InfectoGnostics Research Campus Jena e. V., 07743 Jena, Germany"},{"name":"Institute for Medical Microbiology and Virology, Dresden University Hospital, 01307 Dresden, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1007\/s10142-005-0019-7","article-title":"Understanding the rise of the superbug: Investigation of the evolution and genomic variation of Staphylococcus aureus","volume":"6","author":"Lindsay","year":"2006","journal-title":"Funct Integr Genom."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Tristan, A., Rasigade, J.P., Ruizendaal, E., Laurent, F., Bes, M., Meugnier, H., Lina, G., Etienne, J., Celard, M., and Tattevin, P. (2012). Rise of CC398 lineage of Staphylococcus aureus among Infective endocarditis isolates revealed by two consecutive population-based studies in France. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0051172"},{"key":"ref_3","first-page":"63","article-title":"Staphylococcus aureus and food poisoning","volume":"2","author":"Baron","year":"2003","journal-title":"Genet. Mol. Res."},{"key":"ref_4","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":"Foster","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.mib.2013.11.004","article-title":"Staphylococcus aureus toxins","volume":"17","author":"Otto","year":"2014","journal-title":"Curr Opin Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Palavecino, E.L. (2014). Clinical, epidemiologic, and laboratory aspects of methicillin-resistant Staphylococcus aureus infections. Methods Mol. Biol., 661\u2013664.","DOI":"10.1007\/978-1-62703-664-1_1"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.2217\/fmb.15.35","article-title":"Multiple-locus variable number tandem repeat analysis is superior to spa typing and sufficient to characterize MRSA for surveillance purposes","volume":"10","author":"Bosch","year":"2015","journal-title":"Future Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"El-Adawy, H., Ahmed, M., Hotzel, H., Monecke, S., Schulz, J., Hartung, J., Ehricht, R., Neubauer, H., and Hafez, H.M. (2016). Characterization of methicillin-resistant Staphylococcus aureus isolated from healthy turkeys and broilers using DNA microarrays. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.02019"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1186\/s12866-016-0789-1","article-title":"Characterization of Staphylococcus aureus isolates from raw milk sources in Victoria, Australia","volume":"16","author":"McMillan","year":"2016","journal-title":"BMC Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.vetmic.2007.05.016","article-title":"Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle","volume":"125","author":"Monecke","year":"2007","journal-title":"Vet. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.ijantimicag.2011.09.030","article-title":"Meticillin-resistant Staphylococcus aureus (MRSA): Global epidemiology and harmonisation of typing methods","volume":"39","author":"Stefani","year":"2012","journal-title":"Int J. Antimicrob Agents."},{"key":"ref_12","first-page":"205","article-title":"Improved understanding of factors driving methicillin-resistant Staphylococcus aureus epidemic waves","volume":"5","author":"Chatterjee","year":"2013","journal-title":"Clin. Epidemiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"711","DOI":"10.3201\/eid1105.040866","article-title":"Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs","volume":"11","author":"Ruimy","year":"2005","journal-title":"Emerg Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1089\/vbz.2010.0072","article-title":"The emergence of Staphylococcus aureus ST398","volume":"11","author":"Smith","year":"2011","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_15","first-page":"49","article-title":"Panton-Valentine leukocidin positive sequence type 80 methicillin-resistant Staphylococcus aureus carrying a staphylococcal cassette chromosome mec type IVc is dominant in neonates and children in an Algiers hospital","volume":"36","author":"Djoudi","year":"2013","journal-title":"New Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.micres.2009.03.005","article-title":"Molecular characterization of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus isolates in Egypt","volume":"165","author":"Enany","year":"2010","journal-title":"Microbiol Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1186\/1471-2180-13-2","article-title":"Molecular characterization of methicillin-resistant Panton-valentine leukocidin positive Staphylococcus aureus clones disseminating in Tunisian hospitals and in the community","volume":"13","author":"Mariem","year":"2013","journal-title":"BMC Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1128\/JCM.44.1.108-118.2006","article-title":"Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States","volume":"44","author":"Tenover","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e43037","DOI":"10.1371\/journal.pone.0043037","article-title":"The molecular epidemiology of the highly virulent ST93 Australian community Staphylococcus aureus strain","volume":"7","author":"Coombs","year":"2012","journal-title":"PLoS ONE"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.ijmm.2009.11.002","article-title":"Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species","volume":"300","author":"Cuny","year":"2010","journal-title":"Int J. Med. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1949","DOI":"10.1099\/mic.0.2007\/015289-0","article-title":"Staphylococcus aureus host specificity: Comparative genomics of human versus animal isolates by multi-strain microarray","volume":"154","author":"Sung","year":"2008","journal-title":"Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.3201\/eid1112.050428","article-title":"Methicillin-resistant Staphylococcus aureus in pig farming","volume":"11","author":"Voss","year":"2005","journal-title":"Emerg Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"978","DOI":"10.3201\/eid0908.030089","article-title":"Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: Worldwide emergence","volume":"9","author":"Vandenesch","year":"2003","journal-title":"Emerg Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1056\/NEJMoa042683","article-title":"Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles","volume":"352","author":"Miller","year":"2005","journal-title":"N Engl J. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1111\/j.1469-0691.2010.03273.x","article-title":"High prevalence of methicillin-resistant Staphylococcus aureus clone ST80-IV in hospital and community settings in Algiers","volume":"17","author":"Antri","year":"2011","journal-title":"Clin. Microbiol Infect."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1186\/s12879-019-4245-3","article-title":"Methicillin-resistant Staphylococcus aureus (MRSA) in East Africa: Red alert or red herring?","volume":"19","author":"Wangai","year":"2019","journal-title":"BMC Infect. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1089\/mdr.2013.0136","article-title":"Staphylococcus aureus nasal carriage among patients and health care workers in S\u00e3o Tom\u00e9 and Pr\u00edncipe","volume":"20","year":"2014","journal-title":"Microb Drug Resist."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e89716","DOI":"10.1371\/journal.pone.0089716","article-title":"Molecular epidemiology and antimicrobial susceptibility of clinical Staphylococcus aureus from healthcare institutions in Ghana","volume":"9","author":"Egyir","year":"2014","journal-title":"PloS one."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1186\/1471-2334-12-286","article-title":"Characterization of methicillin-susceptible and -resistant staphylococci in the clinical setting: A multicentre study in Nigeria","volume":"12","author":"Shittu","year":"2012","journal-title":"BMC Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1002\/nmi2.53","article-title":"In vitro characterization of representative clinical South African Staphylococcus aureus isolates from various clonal lineages","volume":"2","author":"Oosthuysen","year":"2014","journal-title":"New Microbe New Infect."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Abdulgader, S.M., Shittu, A.O., Nicol, M.P., and Kaba, M. (2015). Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Africa: A systematic review. Front. Microbiol., 6.","DOI":"10.3389\/fmicb.2015.00348"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Lozano, C., Gharsa, H., Ben Slama, K., Zarazaga, M., and Torres, C. (2016). Staphylococcus aureus in animals and food: Methicillin resistance, prevalence and population structure. A Review in the African Continent. Microorganisms., 4.","DOI":"10.3390\/microorganisms4010012"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.vetmic.2011.11.009","article-title":"Prevalence, antibiotic resistance, virulence traits and genetic lineages of Staphylococcus aureus in healthy sheep in Tunisia","volume":"156","author":"Gharsa","year":"2012","journal-title":"Vet. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.cmi.2014.12.001","article-title":"Staphylococcus aureus complex from animals and humans in three remote African regions","volume":"21","author":"Schaumburg","year":"2015","journal-title":"Clin. Microbiol Infect."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Agabou, A., Ouchenane, Z., Ngba Essebe, C., Khemissi, S., Chehboub, M.T.E., Chehboub, I.B., Sotto, A., Dunyach-Remy, C., and Lavigne, J.P. (2017). Emergence of nasal carriage of ST80 and ST152 PVL+ Staphylococcus aureus isolates from livestock in Algeria. Toxins., 9.","DOI":"10.3390\/toxins9100303"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7450","DOI":"10.3168\/jds.2015-9432","article-title":"Staphylococci in cattle and buffaloes with mastitis in Dakahlia Governorate, Egypt","volume":"98","author":"Gwida","year":"2015","journal-title":"J. Dairy Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"E369","DOI":"10.1111\/1469-0691.12199","article-title":"Molecular epidemiology of Staphylococcus aureus strains isolated from inpatients with infected diabetic foot ulcers in an Algerian University Hospital","volume":"19","author":"Djahmi","year":"2013","journal-title":"Clin. Microbiol Infect."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"890","DOI":"10.3168\/jds.2019-16583","article-title":"Short communication: Diversity of staphylococci isolated from sheep mastitis in northern Algeria","volume":"103","author":"Achek","year":"2020","journal-title":"J. Dairy Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.smallrumres.2018.10.015","article-title":"Phenotypic characterization of staphylococci causing mastitis in goats and microarray-based genotyping of Staphylococcus aureus isolates","volume":"169","author":"Akkou","year":"2018","journal-title":"Small Ruminant Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"6876","DOI":"10.3168\/jds.2018-16208","article-title":"Emergence of methicillin-resistant Staphylococcus aureus (MRSA) ST8 in raw milk and traditional dairy products in the Tizi Ouzou area of Algeria","volume":"102","author":"Titouche","year":"2019","journal-title":"J. Dairy Sci."},{"key":"ref_41","unstructured":"Denis, F., Ploy, M.C., Martin, C., Bingen, E., and Quentin, R. (2011). Bact\u00e9riologie M\u00e9dicale: Techniques Usuelles, Elsevier Masson SAS. [3rd ed.]."},{"key":"ref_42","unstructured":"Council, N.M. (2004). Microbiological Procedures for the Diagnosis of Bovine Udder Infection and Determination of Milk Quality, National Mastitis Council NMC Inc.. [4th ed.]."},{"key":"ref_43","first-page":"24","article-title":"Biochemical and molecular analysis of Staphylococcus aureus clinical isolates from hospitalized patients","volume":"9041636","author":"Karmakar","year":"2016","journal-title":"Can. J. Infect. Dis Med. Microbiol."},{"key":"ref_44","unstructured":"ISO (2003). Microbiology of food and animal feeding stuffs \u2014 Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) \u2014 Part 1: Technique using Baird-Parker agar medium, ISO."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1614","DOI":"10.1111\/j.1469-0691.2010.03311.x","article-title":"Matrix-assisted laser desorption ionization time-of-flight mass spectrometry, a revolution in clinical microbial identification","volume":"16","author":"Bizzini","year":"2010","journal-title":"Clin. Microbiol Infect."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1911","DOI":"10.1128\/JCM.00389-14","article-title":"Multiplex real-time PCR assay for rapid detection of methicillin-resistant staphylococci directly from positive blood cultures","volume":"52","author":"Wang","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1111\/j.1469-0691.2005.01243.x","article-title":"Rapid genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolates using miniaturised oligonucleotide arrays","volume":"11","author":"Monecke","year":"2005","journal-title":"Clin. Microbiol Infect."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1008","DOI":"10.1128\/JCM.03022-15","article-title":"Detecting Staphylococcus aureus virulence and resistance genes: A comparison of whole-genome sequencing and DNA microarray technology","volume":"54","author":"Ruffing","year":"2016","journal-title":"J. Clin. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1111\/j.1574-695X.2008.00426.x","article-title":"Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition","volume":"53","author":"Monecke","year":"2008","journal-title":"FEMS Immunol Med. Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1101\/gr.092759.109","article-title":"Circos: An information aesthetic for comparative genomics","volume":"19","author":"Krzywinski","year":"2009","journal-title":"Genome Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1093\/jac\/dkp378","article-title":"Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain","volume":"64","author":"Lozano","year":"2009","journal-title":"J. Antimicrob Chemother."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Mairi, A., Touati, A., Pantel, A., Zenati, K., Martinez, A.Y., Dunyach-Remy, C., Sotto, A., and Lavigne, J.P. (2019). Distribution of toxinogenic methicillin-resistant and methicillin-susceptible Staphylococcus aureus from different ecological niches in Algeria. Toxins., 11.","DOI":"10.3390\/toxins11090500"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1128\/AEM.01110-08","article-title":"Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats","volume":"75","author":"Pu","year":"2009","journal-title":"Appl Environ. Microbiol."},{"key":"ref_54","first-page":"199","article-title":"Staphylococcus aureus-associated skin and soft tissue infections: Anatomical localization, epidemiology, therapy and potential prophylaxis","volume":"409","author":"Olaniyi","year":"2017","journal-title":"Curr Top. Microbiol Immunol."},{"key":"ref_55","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_56","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":"Journal of clinical microbiology"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"127","DOI":"10.3389\/fmicb.2012.00127","article-title":"Methicillin-Resistant Staphylococcus aureus Associated with Animals and Its Relevance to Human Health","volume":"3","author":"Pantosti","year":"2012","journal-title":"Frontiers in microbiology"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1007\/s10096-010-0884-4","article-title":"Molecular fingerprinting of Staphylococcus aureus from bone and joint infections","volume":"29","author":"Luedicke","year":"2010","journal-title":"Eur J. Clin. Microbiol Infect. Dis."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Monecke, S., Coombs, G., Shore, A.C., Coleman, D.C., Akpaka, P., Borg, M., Chow, H., Ip, M., Jatzwauk, L., and Jonas, D. (2011). A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0017936"},{"key":"ref_60","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_61","doi-asserted-by":"crossref","first-page":"2767","DOI":"10.3389\/fmicb.2018.02767","article-title":"Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity","volume":"9","author":"Wu","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.vetmic.2015.01.007","article-title":"Host-specificity of Staphylococcus aureus causing intramammary infections in dairy animals assessed by genotyping and virulence genes","volume":"176","author":"Blum","year":"2015","journal-title":"Vet. Microbiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1007\/s10096-017-3161-y","article-title":"Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: Molecular characterisation by microarray technology","volume":"37","author":"Jamil","year":"2018","journal-title":"European Journal of Clinical Microbiology & Infectious Diseases"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"7151","DOI":"10.1128\/AEM.00561-11","article-title":"Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany","volume":"77","author":"Fessler","year":"2011","journal-title":"Appl Environ. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2797","DOI":"10.1128\/AEM.07470-11","article-title":"Commercially distributed meat as a potential vehicle for community-acquired methicillin-resistant Staphylococcus aureus","volume":"78","author":"Ogata","year":"2012","journal-title":"Appl Environ. Microbiol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1111\/j.1469-0691.2012.03881.x","article-title":"Methicillin-resistant Staphylococcus aureus among companion and food-chain animals: Impact of human contacts","volume":"18","author":"Petinaki","year":"2012","journal-title":"Clin. Microbiol Infect."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s10096-008-0660-x","article-title":"A portrait of Staphylococcus aureus from the other side of the Mediterranean Sea: Molecular characteristics of isolates from Western Algeria","volume":"28","author":"Bekkhoucha","year":"2009","journal-title":"Eur J. Clin. Microbiol Infect. Dis"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.diagmicrobio.2008.02.010","article-title":"Characterization of ST80 Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus clone in Tunisia","volume":"77","author":"Mastouri","year":"2013","journal-title":"Diagn Microbiol Infect. Dis."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"3514","DOI":"10.1128\/JCM.00966-08","article-title":"Genetic lineages of community-associated methicillin-resistant Staphylococcus aureus in Kuwait hospitals","volume":"46","author":"Udo","year":"2008","journal-title":"J. Clin. Microbiol"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2514","DOI":"10.1093\/jac\/dks245","article-title":"Shift in dominant hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) clones over time","volume":"67","author":"Knight","year":"2012","journal-title":"J. Antimicrob Chemother."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"00305","DOI":"10.1128\/mBio.00305-11","article-title":"Staphylococcus aureus CC398: Host adaptation and emergence of methicillin resistance in livestock","volume":"3","author":"Price","year":"2012","journal-title":"mBio."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"255","DOI":"10.3201\/eid1302.060924","article-title":"Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe","volume":"13","author":"Witte","year":"2007","journal-title":"Emerg Infect. Dis"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"521","DOI":"10.3390\/antibiotics4040521","article-title":"Livestock-associated MRSA: The impact on humans","volume":"4","author":"Cuny","year":"2015","journal-title":"Antibiotics."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/j.tim.2015.03.007","article-title":"Staphylococcus aureus infections: Transmission within households and the community","volume":"23","author":"Knox","year":"2015","journal-title":"Trends Microbiol."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Herron-Olson, L., Fitzgerald, J.R., Musser, J.M., and Kapur, V. (2007). Molecular correlates of host specialization in Staphylococcus aureus. PLoS ONE., 2.","DOI":"10.1371\/journal.pone.0001120"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1007\/s10096-009-0752-2","article-title":"Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers","volume":"28","author":"Monecke","year":"2009","journal-title":"Eur J. Clin. Microbiol Infect. Dis."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1128\/JCM.00887-07","article-title":"Overlapping population structures of nasal isolates of Staphylococcus aureus from healthy Dutch and American individuals","volume":"46","author":"Melles","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.fm.2016.10.020","article-title":"Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy","volume":"62","author":"Basanisi","year":"2017","journal-title":"Food Microbiol."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Woolhouse, M., Ward, M., van Bunnik, B., and Farrar, J. (2015). Antimicrobial resistance in humans, livestock and the wider environment. Philos Trans. R Soc. Lond B Biol Sci, 370.","DOI":"10.1098\/rstb.2014.0083"},{"key":"ref_80","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_81","doi-asserted-by":"crossref","first-page":"515","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_82","doi-asserted-by":"crossref","first-page":"3274","DOI":"10.3168\/jds.2018-15317","article-title":"Staphylococcus aureus related to bovine mastitis in Switzerland: Clonal diversity, virulence gene profiles, and antimicrobial resistance of isolates collected throughout 2017","volume":"102","author":"Morach","year":"2019","journal-title":"J. Dairy Sci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.femsle.2005.09.005","article-title":"An outbreak of staphylococcal food poisoning caused by enterotoxin H in mashed potato made with raw milk","volume":"252","author":"Mathisen","year":"2005","journal-title":"FEMS Microbiol Lett."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1128\/CMR.13.1.16","article-title":"Exotoxins of Staphylococcus aureus","volume":"13","author":"Dinges","year":"2000","journal-title":"Clin. Microbiol Rev."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Arciola, C.R., Campoccia, D., Ravaioli, S., and Montanaro, L. (2015). Polysaccharide intercellular adhesin in biofilm: Structural and regulatory aspects. Front. Cell Infect. Microbiol., 5.","DOI":"10.3389\/fcimb.2015.00007"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.micpath.2013.05.002","article-title":"Biofilm formation and dispersal of Staphylococcus aureus under the influence of oxacillin","volume":"62","author":"Mirani","year":"2013","journal-title":"Microb Pathog."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1089\/fpd.2014.1885","article-title":"Molecular characterization, antibiotic resistance, and virulence factors of methicillin-resistant Staphylococcus aureus strains isolated from imported and domestic meat in Korea","volume":"12","author":"Kim","year":"2015","journal-title":"Foodborne Pathog Dis."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.fm.2016.03.004","article-title":"Prevalence, antimicrobial susceptibility and molecular typing of methicillin-resistant Staphylococcus aureus (MRSA) in bulk tank milk from southern Italy","volume":"58","author":"Parisi","year":"2016","journal-title":"Food Microbiol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1046\/j.1469-0691.2003.00531.x","article-title":"Prevalence of methicillin-resistant Staphylococcus aureus in eight African hospitals and Malta","volume":"9","author":"Kesah","year":"2003","journal-title":"Clin. Microbiol Infect."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.medmal.2014.01.006","article-title":"Emergence of the European ST80 clone of community-associated methicillin-resistant Staphylococcus aureus as a cause of healthcare-associated infections in Eastern Algeria","volume":"44","author":"Alioua","year":"2014","journal-title":"Med. Mal. Infect."},{"key":"ref_91","first-page":"e129","article-title":"Molecular characterization of methicillin-resistant Staphylococcus aureus isolates in Algeria","volume":"59","author":"Ouchenane","year":"2011","journal-title":"Pathologie Biologie"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1016\/j.medmal.2011.09.010","article-title":"Emergence of vancomycin-resistant Staphylococcus aureus identified in the Tlemcen university hospital (North-West Algeria)","volume":"41","author":"Rebiahi","year":"2011","journal-title":"Med. Mal. Infect."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.14202\/vetworld.2019.1195-1203","article-title":"Antimicrobial resistance of Escherichia coli isolates from cattle in Eastern Algeria","volume":"12","author":"Barour","year":"2019","journal-title":"Vet. World."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Benrabia, I., Hamdi, T.M., Shehata, A.A., Neubauer, H., and Wareth, G. (2020). Methicillin-resistant Staphylococcus aureus (MRSA) in poultry species in Algeria: Long-term study on prevalence and antimicrobial resistance. Vet. Sci., 7.","DOI":"10.3390\/vetsci7020054"},{"key":"ref_95","first-page":"121","article-title":"Infections caused by community-associated methicillin-resistant Staphylococcus aureus European clone (ST80) in Slovenia between 2006 And 2013","volume":"55","author":"Dermota","year":"2016","journal-title":"Zdr Varst."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1128\/JCM.01381-07","article-title":"Epidemiology of european community-associated methicillin-resistant Staphylococcus aureus clonal complex 80 type IV strains isolated in Denmark from 1993 to 2004","volume":"46","author":"Larsen","year":"2008","journal-title":"J. Clin. Microbiol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/10\/1276\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:09:03Z","timestamp":1760166543000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/10\/1276"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,3]]},"references-count":96,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2021,10]]}},"alternative-id":["pathogens10101276"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10101276","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,3]]}}}