{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:51:10Z","timestamp":1787028670289,"version":"build-2736575974"},"reference-count":42,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2019,6,7]],"date-time":"2019-06-07T00:00:00Z","timestamp":1559865600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Technology","award":["NMRPG6G6011-2"],"award-info":[{"award-number":["NMRPG6G6011-2"]}]},{"name":"Ministry of Science and Technology","award":["NMRPG3H0171"],"award-info":[{"award-number":["NMRPG3H0171"]}]},{"name":"Chang Gung Medical Research Program Foundation","award":["CMRPG6F0341-3"],"award-info":[{"award-number":["CMRPG6F0341-3"]}]},{"name":"Chang Gung Medical Research Program Foundation","award":["CMRPG6G0231"],"award-info":[{"award-number":["CMRPG6G0231"]}]},{"name":"Chang Gung Medical Research Program Foundation","award":["CMRPG6H0401"],"award-info":[{"award-number":["CMRPG6H0401"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Methicillin-resistant Staphylococcus aureus (MRSA) causes superficial infections such as cellulitis or invasive infections such as osteomyelitis; however, differences in MRSA isolates from cellulitis (CL-MRSA) and from osteomyelitis (OM-MRSA) at the same local area remain largely unknown. A total of 221 MRSA isolates including 106 CL-MRSA strains and 115 OM-MRSA strains were collected at Chang-Gung Memorial Hospital in Taiwan between 2016 and 2018, and their genotypic and phenotypic characteristics were compared. We found that OM-MRSA isolates significantly exhibited higher rates of resistance to multiple antibiotics than CL-MRSA isolates. Genotypically, OM-MRSA isolates had higher proportions of the SCCmec type III, the sequence type ST239, and the spa type t037 than CL-MRSA isolates. Besides the multidrug-resistant lineage ST239-t037-SCCmecIII more prevalent in OM-MRSA, higher antibiotic resistance rates were also observed in several other prevalent lineages in OM-MRSA as compared to the same lineages in CL-MRSA. Furthermore, when prosthetic joint infection (PJI) associated and non-PJI-associated MRSA strains in osteomyelitis were compared, no significant differences were observed in antibiotic resistance rates between the two groups, albeit more diverse genotypes were found in non-PJI-associated MRSA. Our findings therefore suggest that deep infections may allow MRSA to evade antibiotic attack and facilitate the convergent evolution and selection of multidrug-resistant lineages.<\/jats:p>","DOI":"10.3390\/jcm8060816","type":"journal-article","created":{"date-parts":[[2019,6,7]],"date-time":"2019-06-07T05:25:56Z","timestamp":1559885156000},"page":"816","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Comparison of Methicillin-Resistant Staphylococcus aureus Isolates from Cellulitis and from Osteomyelitis in a Taiwan Hospital, 2016\u20132018"],"prefix":"10.3390","volume":"8","author":[{"given":"Kuo-Ti","family":"Peng","sequence":"first","affiliation":[{"name":"Department of Orthopaedic Surgery, Chang Gung Memorial Hospital, Chiayi 61363, Taiwan"},{"name":"College of Medicine, Chang Gung University, Taoyuan 33303, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tsung-Yu","family":"Huang","sequence":"additional","affiliation":[{"name":"Division of Infectious Diseases, Department of Internal Medicine, Chang Gung Memorial Hospital, Chiayi 61363, Taiwan"},{"name":"Graduate Institute of Clinical Medical Sciences, College of Medicine, Chang Gung University, Taoyuan 33303, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7619-1902","authenticated-orcid":false,"given":"Yao-Chang","family":"Chiang","sequence":"additional","affiliation":[{"name":"Department of Nursing, Chang Gung University of Science and Technology, Chiayi 61363, Taiwan"},{"name":"Division of Basic Medical Sciences, and Chronic Diseases and Health Promotion Research Center, Chang Gung University of Science and Technology, Chiayi 61363, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Yi","family":"Hsu","sequence":"additional","affiliation":[{"name":"Department of Orthopaedic Surgery, Chang Gung Memorial Hospital, Chiayi 61363, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fang-Yi","family":"Chuang","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Chang Gung Memorial Hospital, Chiayi 61363, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiang-Wen","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Nursing, Chang Gung University of Science and Technology, Chiayi 61363, Taiwan"},{"name":"Division of Basic Medical Sciences, and Chronic Diseases and Health Promotion Research Center, Chang Gung University of Science and Technology, Chiayi 61363, Taiwan"},{"name":"Research Center for Industry of Human Ecology and Research Center for Chinese Herbal Medicine, Chang Gung University of Science and Technology, Taoyuan 33303, Taiwan"},{"name":"Department of Rehabilitation, Chang Gung Memorial Hospital, Chiayi 61363, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6492-0346","authenticated-orcid":false,"given":"Pey-Jium","family":"Chang","sequence":"additional","affiliation":[{"name":"Graduate Institute of Clinical Medical Sciences, College of Medicine, Chang Gung University, Taoyuan 33303, Taiwan"},{"name":"Department of Nephrology, Chang Gung Memorial Hospital, Chiayi 61363, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,6,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1086\/379321","article-title":"Is methicillin-resistant Staphylococcus aureus more virulent than methicillin-susceptible S. aureus? A comparative cohort study of British patients with nosocomial infection and bacteremia","volume":"37","author":"Melzer","year":"2003","journal-title":"Clin. Infec. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1056\/NEJM199808203390806","article-title":"Staphylococcus aureus infections","volume":"339","author":"Lowy","year":"1998","journal-title":"N. Engl. J. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3222","DOI":"10.1128\/JCM.01423-08","article-title":"Predominance of methicillin-resistant Staphylococcus aureus among pathogens causing skin and soft tissue infections in a large urban jail: Risk factors and recurrence rates","volume":"46","author":"David","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1056\/NEJMoa025025","article-title":"Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene","volume":"348","author":"Chang","year":"2003","journal-title":"N. Engl. J. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1603","DOI":"10.1086\/345368","article-title":"Linezolid resistance in Staphylococcus aureus: Characterization and stability of resistant phenotype","volume":"186","author":"Pillai","year":"2002","journal-title":"J. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1093\/jac\/dkg104","article-title":"Linezolid resistance in clinical isolates of Staphylococcus aureus","volume":"51","author":"Wilson","year":"2003","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2423","DOI":"10.1128\/JCM.00254-06","article-title":"Comparisons of community-associated methicillin-resistant Staphylococcus aureus (MRSA) and hospital-associated MSRA infections in Sacramento, California","volume":"44","author":"Huang","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1086\/533502","article-title":"What is community-associated methicillin-resistant Staphylococcus aureus?","volume":"197","author":"David","year":"2008","journal-title":"J. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1128\/AAC.46.4.1147-1152.2002","article-title":"Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains","volume":"46","author":"Ma","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2637","DOI":"10.1128\/AAC.48.7.2637-2651.2004","article-title":"Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC","volume":"48","author":"Ito","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"178","DOI":"10.3201\/eid0702.010204","article-title":"The changing epidemiology of Staphylococcus aureus?","volume":"7","author":"Chambers","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/S1473-3099(05)70112-2","article-title":"Community-acquired meticillin-resistant Staphylococcus aureus: An emerging threat","volume":"5","author":"Zetola","year":"2005","journal-title":"Lancet Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5113","DOI":"10.1128\/JCM.41.11.5113-5120.2003","article-title":"Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: Establishing a national database","volume":"41","author":"McDougal","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/j.jiac.2018.03.004","article-title":"Change in genotype of methicillin-resistant Staphylococcus aureus (MRSA) affects the antibiogram of hospital-acquired MRSA","volume":"24","author":"Harada","year":"2018","journal-title":"J. Infect. Chemother."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1186\/s13059-016-1022-0","article-title":"Identification of source and sink populations for the emergence and global spread of the East-Asia clone of community-associated MRSA","volume":"17","author":"Ward","year":"2016","journal-title":"Genome Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.ijantimicag.2011.01.011","article-title":"Community-associated meticillin-resistant Staphylococcus aureus in children in Taiwan, 2000s","volume":"38","author":"Huang","year":"2011","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1111\/1469-0691.12705","article-title":"New epidemiology of Staphylococcus aureus infection in Asia","volume":"20","author":"Chen","year":"2014","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1016\/S1473-3099(13)70136-1","article-title":"Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Asia","volume":"13","author":"Chuang","year":"2013","journal-title":"Lancet Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1008","DOI":"10.1128\/JCM.38.3.1008-1015.2000","article-title":"Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus","volume":"38","author":"Enright","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"5442","DOI":"10.1128\/JCM.41.12.5442-5448.2003","article-title":"Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management","volume":"41","author":"Harmsen","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2155","DOI":"10.1128\/AAC.46.7.2155-2161.2002","article-title":"Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus","volume":"46","author":"Oliveira","year":"2002","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1016\/S0966-842X(01)02175-8","article-title":"The emergence and evolution of methicillin-resistant Staphylococcus aureus","volume":"9","author":"Hiramatsu","year":"2001","journal-title":"Trends Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2976","DOI":"10.1001\/jama.290.22.2976","article-title":"Comparison of community-and health care\u2013associated methicillin-resistant Staphylococcus aureus infection","volume":"290","author":"Naimi","year":"2003","journal-title":"JAMA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.jhin.2005.01.027","article-title":"Three-year survey of community-acquired methicillin-resistant Staphylococcus aureus producing Panton-Valentine leukocidin in a French university hospital","volume":"61","author":"Naas","year":"2005","journal-title":"J. Hosp. Infect."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.tim.2008.05.002","article-title":"The role of virulence determinants in community-associated MRSA pathogenesis","volume":"16","author":"Diep","year":"2008","journal-title":"Trends Microbiol."},{"key":"ref_26","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_27","unstructured":"Hsiao, C.H., Ong, S.J., Chuang, C.C., Ma, D.H., and Huang, Y.C. (2015). A comparison of clinical features between community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus keratitis. J. Ophthalmol., 2015."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"117","DOI":"10.4103\/1319-1683.74320","article-title":"A review of community-acquired methicillin-resistant Staphylococcus aureus for primary care physicians","volume":"17","author":"Bukharie","year":"2010","journal-title":"J. Family Community Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.ajic.2010.01.006","article-title":"Health care-associated and community-associated methicillin-resistant Staphylococcus aureus infections: A comparison of definitions","volume":"38","author":"McCarthy","year":"2010","journal-title":"Am. J. Infect. Control"},{"key":"ref_30","unstructured":"CLSI (2016). CLSI Supplement M100S. Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [26th ed.]."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1587","DOI":"10.1345\/aph.1R211","article-title":"Treatment of methicillin-resistant Staphylococcus aureus infections with a minimal inhibitory concentration of 2 ug\/mL to vancomycin: Old (trimethoprim\/sulfamethoxazole) versus new (daptomycin or linezolid) agents","volume":"46","author":"Campbell","year":"2012","journal-title":"Ann. Pharmacother."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1111\/j.1469-0691.2007.01720.x","article-title":"A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I\u2013V","volume":"13","author":"Boye","year":"2007","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5026","DOI":"10.1128\/JCM.43.10.5026-5033.2005","article-title":"Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus","volume":"43","author":"Zhang","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1128\/JCM.44.3.1141-1144.2006","article-title":"Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from-resistant staphylococci","volume":"44","author":"McClure","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1136\/bmj.1.5219.124-a","article-title":"\u201cCelbenin\u201d-resistant staphylococci","volume":"1","author":"Jevons","year":"1961","journal-title":"Br. Med. J."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"874","DOI":"10.1016\/S0140-6736(06)68853-3","article-title":"Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat","volume":"368","author":"Grundmann","year":"2006","journal-title":"Lancet"},{"key":"ref_37","unstructured":"Nathwani, D., Davey, P.G., and Marwick, C.A. (2010). MRSA: Treating people with infection. BMJ Clin. Evid., 2010."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1093\/cid\/cir842","article-title":"Systemic antibiotic therapy for chronic osteomyelitis in adults","volume":"54","author":"Spellberg","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.12659\/AJCR.911393","article-title":"Idiosyncratic Drug-Induced Liver Injury Due to Ciprofloxacin: A Report of Two Cases and Review of the Literature","volume":"19","author":"Radovanovic","year":"2018","journal-title":"Am. J. Case Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"656","DOI":"10.2106\/JBJS.16.01002","article-title":"Oral-Only Linezolid-Rifampin Is Highly Effective Compared with Other Antibiotics for Periprosthetic Joint Infection: Study of a Mouse Model","volume":"99","author":"Thompson","year":"2017","journal-title":"J. Bone. Joint Surg. Am."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1745","DOI":"10.1073\/pnas.1814265116","article-title":"Sequential evolution of virulence and resistance during clonal spread of community-acquired methicillin-resistant Staphylococcus aureus","volume":"116","author":"Copin","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1002\/jor.23656","article-title":"Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections","volume":"36","author":"Li","year":"2018","journal-title":"J. Orthop. Res."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/8\/6\/816\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:56:52Z","timestamp":1760187412000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/8\/6\/816"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,6,7]]},"references-count":42,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2019,6]]}},"alternative-id":["jcm8060816"],"URL":"https:\/\/doi.org\/10.3390\/jcm8060816","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,6,7]]}}}