{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:55:56Z","timestamp":1760151356594,"version":"build-2065373602"},"reference-count":28,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,3,17]],"date-time":"2022-03-17T00:00:00Z","timestamp":1647475200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Korea Research Foundation","award":["NRF-2021R1A2B5B02002220"],"award-info":[{"award-number":["NRF-2021R1A2B5B02002220"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The emergence of antimicrobial-resistant Staphylococcus aureus has become a grave concern worldwide. In this study, 95 strains of S. aureus isolated from stool samples were collected from Busan, South Korea to characterize their antimicrobial susceptibility, enterotoxin genes, and molecular typing using matrix-assisted laser desorption\/ionization time-of-flight mass spectrometry (MALDI-TOF MS) and random amplification of polymorphic DNA (RAPD) assay. Only two strains showed no drug resistance, whereas resistance to three or more antibiotics was observed in 87.4% of strains. Ampicillin resistance was the most common at 90% and all strains were susceptible to vancomycin. The distribution of enterotoxin genes encoded in isolates was sea (32.6%), sec (11.6%), seg (19%), sea &amp; sec (2.1%), and sec &amp; seg (34.7%). Molecular typing using both MALDI-TOF MS and RAPD indicated that S. aureus exhibited diverse clonal lineages and no correlations were observed among the profiling of enterotoxin, MALDI-TOF MS, and RAPD. This investigation provides useful information on foodborne pathogenic S. aureus that has a significant public health impact in South Korea.<\/jats:p>","DOI":"10.3390\/microorganisms10030642","type":"journal-article","created":{"date-parts":[[2022,3,20]],"date-time":"2022-03-20T21:34:27Z","timestamp":1647812067000},"page":"642","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Molecular Typing, Antibiotic Resistance and Enterotoxin Gene Profiles of Staphylococcus aureus Isolated from Humans in South Korea"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2460-8080","authenticated-orcid":false,"given":"Sunghyun","family":"Yoon","sequence":"first","affiliation":[{"name":"National Center for Toxicological Research, U.S. Food and Drug Administration, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yon Kyoung","family":"Park","sequence":"additional","affiliation":[{"name":"Microbiology Division, Busan Institute of Health and Environment, Busan 616-100, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tae Sung","family":"Jung","sequence":"additional","affiliation":[{"name":"Laboratory of Aquatic Animal Diseases, Research Institute of Life Science, College of Veterinary Medicine, Gyeongsang National University, Jinju 660-701, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Seong Bin","family":"Park","sequence":"additional","affiliation":[{"name":"Coastal Research & Extension Center, Mississippi State University, Pascagoula, MS 39567, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,17]]},"reference":[{"key":"ref_1","first-page":"63","article-title":"Staphylococcus aureus and Food Poisoning","volume":"2","author":"Baron","year":"2003","journal-title":"Genet. Mol. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"4683","DOI":"10.1128\/JCM.41.10.4683-4687.2003","article-title":"Detection of Staphylococcus aureus Enterotoxins A to D by Real-Time Fluorescence PCR Assay","volume":"41","author":"Klotz","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.3390\/toxins2082177","article-title":"Staphylococcal Enterotoxins","volume":"2","author":"Pinchuk","year":"2010","journal-title":"Toxins"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.ijfoodmicro.2010.06.002","article-title":"Detection of Staphylococcus aureus Enterotoxins in Sheep Cheese and Dairy Desserts by Multiplex PCR Technique","volume":"142","author":"Ertas","year":"2010","journal-title":"Int. J. Food Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3057","DOI":"10.1007\/s00018-010-0389-4","article-title":"Mobile Genetic Elements of Staphylococcus aureus","volume":"67","author":"Malachowa","year":"2010","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e00181-19","DOI":"10.1128\/CMR.00181-19","article-title":"Antimicrobial Resistance in ESKAPE Pathogens","volume":"33","author":"Forde","year":"2020","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1097\/MOG.0b013e32831ba094","article-title":"Enteric Infections and Diagnostic Testing","volume":"25","author":"Bennett","year":"2009","journal-title":"Curr. Opin. Gastroenterol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1874","DOI":"10.1053\/j.gastro.2009.02.072","article-title":"Diagnosis and Treatment of Acute or Persistent Diarrhea","volume":"136","author":"Pawlowski","year":"2009","journal-title":"Gastroenterology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2980","DOI":"10.1128\/JCM.00431-11","article-title":"Utility of Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry Following Introduction for Routine Laboratory Bacterial Identification","volume":"49","author":"Neville","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e02231","DOI":"10.1016\/j.heliyon.2019.e02231","article-title":"Molecular Typing of Staphylococcus aureus from Different Sources by RAPD-PCR Analysis","volume":"5","author":"Zare","year":"2019","journal-title":"Heliyon"},{"key":"ref_11","first-page":"269","article-title":"Application of MALDI-TOF MS Fingerprinting as a Quick Tool for Identification and Clustering of Foodborne Pathogens Isolated from Food Products","volume":"40","author":"Elbehiry","year":"2017","journal-title":"New Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"5005","DOI":"10.1007\/s11033-014-3367-3","article-title":"Staphylococcus aureus Mobile Genetic Elements","volume":"41","author":"Alibayov","year":"2014","journal-title":"Mol. Biol. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"43","DOI":"10.4142\/jvs.2009.10.1.43","article-title":"A multiplex real-time PCR for differential detection and quantification of Salmonella spp., Salmonella enterica serovar Typhimurium and Enteritidis in meats","volume":"10","author":"Lee","year":"2009","journal-title":"J. Vet. Sci."},{"key":"ref_14","unstructured":"Weinstein, M.P., Patel, J.B., Bobenchik, A.M., Campeau, S., Cullen, S.K., Galas, M.F., Gold, H., Humphries, R.M., and Kirn, T.J. (2021). M100 ED31, Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1111\/j.1365-2672.1974.tb00446.x","article-title":"The Incidence of Enterotoxin Production in Strains of Staphylococcus aureus Isolated from Foods","volume":"37","author":"Payne","year":"1974","journal-title":"J. Appl. Bacteriol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.ijfoodmicro.2007.02.013","article-title":"Novel Multiplex PCR for the Detection of the Staphylococcus aureus Superantigen and Its Application to Raw Meat Isolates in Korea","volume":"117","author":"Hwang","year":"2007","journal-title":"Int. J. Food Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1590\/S1517-83822009000100025","article-title":"Ocurrence of Staphylococcus aureus and Multiplex Pcr Detection of Classic Enterotoxin Genes in Cheese and Meat Products","volume":"40","author":"Pelisser","year":"2009","journal-title":"Braz. J. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.ijfoodmicro.2004.05.008","article-title":"Coagulase-Positive Staphylococci and Staphylococcus aureus in Food Products Marketed in Italy","volume":"98","author":"Normanno","year":"2005","journal-title":"Int. J. Food Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"627","DOI":"10.2754\/avb200372040627","article-title":"Detection of the Genes for Staphylococcus aureus Enterotoxins by PCR","volume":"72","author":"Tesfaye","year":"2003","journal-title":"Acta Vet. BRNO"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2868","DOI":"10.1128\/JCM.00506-11","article-title":"Comparison of Direct Colony Method versus Extraction Method for Identification of Gram-Positive Cocci by Use of Bruker Biotyper Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry","volume":"49","author":"Alatoom","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.syapm.2010.12.001","article-title":"Phenotypic and Genotypic Analyses of Lactic Acid Bacteria in Local Fermented Food, Breast Milk and Faeces of Mothers and Their Babies","volume":"34","author":"Albesharat","year":"2011","journal-title":"Syst. Appl. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Firacative, C., Trilles, L., and Meyer, W. (2012). MALDI-TOF MS Enables the Rapid Identification of the Major Molecular Types within the Cryptococcus neoformans\/C. gattii Species Complex. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0037566"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1518","DOI":"10.1128\/JCM.02219-10","article-title":"Isolation and Characterization of \u201cPseudomonas andersonii\u201d from Four Cases of Pulmonary Granulomas and Emended Species Description","volume":"49","author":"Simmon","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1016\/j.syapm.2011.05.002","article-title":"Comparison of Genotypic and Phenotypic Cluster Analyses of Virulence Determinants and Possible Role of CRISPR Elements towards Their Incidence in Enterococcus faecalis and Enterococcus faecium","volume":"34","author":"Pavlovic","year":"2011","journal-title":"Syst. Appl. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"7","DOI":"10.3201\/eid1701.P11101","article-title":"Foodborne Illness Acquired in the United States-Major Pathogens","volume":"17","author":"Scallan","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1089\/fpd.2012.1278","article-title":"Differences in Virulence Genes and Genome Patterns of Mastitis-Associated Staphylococcus aureus among Goat, Cow, and Human Isolates in Taiwan","volume":"10","author":"Chu","year":"2013","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1111\/jam.13133","article-title":"Characterization of Staphylococcus aureus faecal isolates associated with food-borne disease in Korea","volume":"121","author":"Shin","year":"2016","journal-title":"J. Appl. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3411","DOI":"10.1128\/JCM.37.10.3411-3414.1999","article-title":"Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in Staphylococcal isolates","volume":"37","author":"Bohach","year":"1999","journal-title":"J. Clin. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/3\/642\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:38:07Z","timestamp":1760135887000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/3\/642"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,17]]},"references-count":28,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["microorganisms10030642"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms10030642","relation":{},"ISSN":["2076-2607"],"issn-type":[{"type":"electronic","value":"2076-2607"}],"subject":[],"published":{"date-parts":[[2022,3,17]]}}}