{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T12:08:11Z","timestamp":1791288491182,"version":"4.3.0"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,8,5]],"date-time":"2022-08-05T00:00:00Z","timestamp":1659657600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,8,5]],"date-time":"2022-08-05T00:00:00Z","timestamp":1659657600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100003725","name":"National Research Foundation of Korea","doi-asserted-by":"publisher","award":["2020R1F1A1067794"],"award-info":[{"award-number":["2020R1F1A1067794"]}],"id":[{"id":"10.13039\/501100003725","id-type":"DOI","asserted-by":"publisher"}]},{"name":"R&D Fund for the research of infectious diseases in Republic of Korea","award":["HG18C0062"],"award-info":[{"award-number":["HG18C0062"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Antimicrob Resist Infect Control"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>We investigated the trend change in vancomycin-intermediate <jats:italic>Staphylococcus aureus<\/jats:italic> (VISA)\/heterogeneous VISA (hVISA) prevalence among methicillin-resistant <jats:italic>S. aureus<\/jats:italic> (MRSA) bacteremia strains and antistaphylococcal antibiotic use together with mutation studies of vancomycin resistance-related gene loci to evaluate the impact of changes in antibiotic use after new antistaphylococcal antibiotics became available.\n<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>Among 850 healthcare-associated MRSA isolates from 2006 to 2019 at a tertiary hospital in South Korea, hVISA\/VISA was determined by modified PAP\/AUC analysis, and the identified hVISA\/VISA strains were genotyped. Gene mutations at <jats:italic>vraSR, graSR, walKR<\/jats:italic>, and <jats:italic>rpoB<\/jats:italic> were studied by full-length sequencing. Antistaphylococcal antibiotic use in 2005\u20132018 was analyzed.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Two VISA and 23 hVISA strains were identified. The prevalence rate ratio of hVISA\/VISA carrying mutations at the two-component regulatory systems among MRSA was 0.668 (95% CI 0.531\u20130.841; <jats:italic>P<\/jats:italic>\u2009=\u20090.001), and the prevalence rate ratio of hVISA\/VISA carrying <jats:italic>rpoB<\/jats:italic> gene mutations was 1.293 (95% CI 0.981\u20131.702; 174 <jats:italic>P<\/jats:italic>\u2009=\u20090.068). Annual vancomycin use density analyzed by days of therapy (DOT) per 1,000 patient-days did not decrease significantly, however the annual average length of time analyzed by the number of days vancomycin was administered for each case showed a significantly decreasing trend.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>During the 14-year period when the average length of vancomycin therapy decreased every year with the availability of alternative antibiotics, the prevalence of hVISA\/VISA did not decrease significantly. This seems to be because the resistant strains carrying the <jats:italic>rpoB<\/jats:italic> mutations increased despite the decrease in the strains carrying the mutations at the two-component regulatory systems.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s13756-022-01140-9","type":"journal-article","created":{"date-parts":[[2022,8,5]],"date-time":"2022-08-05T10:07:22Z","timestamp":1659694042000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Impact of vancomycin use trend change due to the availability of alternative antibiotics on the prevalence of Staphylococcus aureus with reduced vancomycin susceptibility: a 14-year retrospective study"],"prefix":"10.1186","volume":"11","author":[{"given":"Yu Ri","family":"Kang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Si-Ho","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Doo Ryeon","family":"Chung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jae-Hoon","family":"Ko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kyungmin","family":"Huh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sun Young","family":"Cho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheol-In","family":"Kang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kyong Ran","family":"Peck","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,8,5]]},"reference":[{"key":"1140_CR1","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1093\/jac\/40.1.135","volume":"40","author":"K Hiramatsu","year":"1997","unstructured":"Hiramatsu K, Hanaki H, Ino T, Yabuta K, Oguri T, Tenover FC. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother. 1997;40:135\u20136.","journal-title":"J Antimicrob Chemother"},{"key":"1140_CR2","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1128\/CMR.00042-09","volume":"23","author":"BP Howden","year":"2010","unstructured":"Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev. 2010;23:99\u2013139.","journal-title":"Clin Microbiol Rev"},{"key":"1140_CR3","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1086\/381093","volume":"38","author":"PG Charles","year":"2004","unstructured":"Charles PG, Ward PB, Johnson PD, Howden BP, Grayson ML. Clinical features associated with bacteremia due to heterogeneous vancomycin-intermediate Staphylococcus aureus. Clin Infect Dis. 2004;38:448\u201351.","journal-title":"Clin Infect Dis"},{"key":"1140_CR4","doi-asserted-by":"publisher","first-page":"1355","DOI":"10.1086\/606027","volume":"200","author":"IG Bae","year":"2009","unstructured":"Bae IG, Federspiel JJ, Mir\u00f3 JM, Woods CW, Park L, Rybak MJ, et al. Heterogeneous vancomycin-intermediate susceptibility phenotype in bloodstream methicillin-resistant Staphylococcus aureus isolates from an international cohort of patients with infective endocarditis: prevalence, genotype, and clinical significance. J Infect Dis. 2009;200:1355\u201366.","journal-title":"J Infect Dis"},{"key":"1140_CR5","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1128\/AAC.01133-10","volume":"55","author":"SJ van Hal","year":"2011","unstructured":"van Hal SJ, Paterson DL. Systematic review and meta-analysis of the significance of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. Antimicrob Agents Chemother. 2011;55:405\u201310.","journal-title":"Antimicrob Agents Chemother"},{"key":"1140_CR6","doi-asserted-by":"publisher","first-page":"637656","DOI":"10.3389\/fmicb.2021.637656","volume":"12","author":"AM Turner","year":"2021","unstructured":"Turner AM, Lee JYH, Gorrie CL, Howden BP, Carter GP. Genomic insights into last-line antimicrobial resistance in multidrug-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus. Front Microbiol. 2021;12:637656.","journal-title":"Front Microbiol"},{"key":"1140_CR7","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1093\/infdis\/jit136","volume":"208","author":"S Dereskinski","year":"2013","unstructured":"Dereskinski S. The multiple paths to heteroresistance and intermediate resistance to vancomycin in Staphylococcus aureus. J Infect Dis. 2013;208:7\u20139.","journal-title":"J Infect Dis"},{"key":"1140_CR8","doi-asserted-by":"publisher","first-page":"5222","DOI":"10.1128\/AAC.00437-10","volume":"54","author":"L Cui","year":"2010","unstructured":"Cui L, Isii T, Fukuda M, Ochiai T, Neoh HM, Camargo IL, et al. An RpoB mutation confers dual heteroresistance to daptomycin and vancomycin in Staphylococcus aureus. Antimicrob Agents Chemother. 2010;54:5222\u201333.","journal-title":"Antimicrob Agents Chemother"},{"key":"1140_CR9","doi-asserted-by":"publisher","first-page":"e00550-17","DOI":"10.1128\/mSphere.00550-17","volume":"3","author":"R Gu\u00e9rillot","year":"2018","unstructured":"Gu\u00e9rillot R, Gon\u00e7alves da Silva A, Monk I, Giulieri S, Tomita T, Alison E, et al. Convergent evolution driven by rifampin exacerbates the global burden of drug-resistant Staphylococcus aureus. mSphere. 2018;3:e00550-17.","journal-title":"mSphere"},{"key":"1140_CR10","first-page":"2163","volume":"7","author":"Y Wang","year":"2016","unstructured":"Wang Y, Li X, Jiang L, Han W, Xie X, Jin Y, et al. Novel mutation sites in the development of vancomycin- intermediate resistance in Staphylococcus aureus. Front Microbiol. 2016;7:2163.","journal-title":"Front Microbiol"},{"key":"1140_CR11","doi-asserted-by":"publisher","first-page":"2149","DOI":"10.1093\/jac\/dkq292","volume":"65","author":"WE Rose","year":"2010","unstructured":"Rose WE, Knier RM, Hutson PR. Pharmacodynamic effect of clinical vancomycin exposures on cell wall thickness in heterogeneous vancomycin-intermediate Staphylococcua aureus. J Antimicrob Chemother. 2010;65:2149\u201354.","journal-title":"J Antimicrob Chemother"},{"key":"1140_CR12","doi-asserted-by":"publisher","first-page":"e0136082","DOI":"10.1371\/journal.pone.0136082","volume":"10","author":"S Zhang","year":"2015","unstructured":"Zhang S, Sun X, Chang W, Dai Y, Ma X. Systematic review and meta-analysis of the epidemiology of vancomycin-intermediate and heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. PLoS ONE. 2015;10:e0136082.","journal-title":"PLoS ONE"},{"key":"1140_CR13","doi-asserted-by":"publisher","first-page":"12689","DOI":"10.1038\/s41598-020-69058-z","volume":"10","author":"A Shariati","year":"2020","unstructured":"Shariati A, Dadashi M, Moghadam MT, van Belkum A, Yaslianifard S, Darban-Sarokhalil D. Global prevalence and distribution of vancomycin resistant, vancomycin intermediate and heterogeneously vancomycin intermediate Staphylococcus aureus clinical isolates: a systematic review and meta-analysis. Sci Rep. 2020;10:12689.","journal-title":"Sci Rep"},{"key":"1140_CR14","doi-asserted-by":"publisher","first-page":"1843","DOI":"10.1093\/jac\/dks131","volume":"67","author":"KH Park","year":"2012","unstructured":"Park KH, Kim ES, Kim HS, Park SJ, Bang KM, Park HJ, et al. Comparison of the clinical features, bacterial genotypes and outcomes of patients with bacteraemia due to heteroresistant vancomycin-intermediate Staphylococcus aureus and vancomycin-susceptible S. aureus. J Antimicrob Chemother. 2012;67:1843\u20139.","journal-title":"J Antimicrob Chemother"},{"key":"1140_CR15","doi-asserted-by":"publisher","first-page":"464","DOI":"10.1016\/j.diagmicrobio.2016.09.015","volume":"86","author":"YR Kang","year":"2016","unstructured":"Kang YR, Chung DR, Baek JY, Kim SH, Cho SY, Ha YE, et al. Decreasing prevalence of heterogeneous vancomycin-intermediate Staphylococcus aureus among blood isolates in Korean hospitals. Diagn Microbiol Infect Dis. 2016;86:464\u20136.","journal-title":"Diagn Microbiol Infect Dis"},{"key":"1140_CR16","unstructured":"CLSI. Clinical and Laboratory Standards Institute (CLSI), Performance standards for antimicrobial susceptibility testing; 31st Edition, 2021; (M100-S25) Wayne, PA."},{"key":"1140_CR17","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1128\/JCM.01128-10","volume":"49","author":"SW Satola","year":"2011","unstructured":"Satola SW, Farley MM, Anderson KF, Patel JB. Comparison of detection methods for heteroresistant vancomycin-intermediate Staphylococcus aureus, with the population analysis profile method as the reference method. J Clin Microbiol. 2011;49:177\u201383.","journal-title":"J Clin Microbiol"},{"key":"1140_CR18","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1093\/jac\/47.4.399","volume":"47","author":"M Wootton","year":"2001","unstructured":"Wootton M, Howe RA, Hillman R, Walsh TR, Bennett PM, MacGowan AP. A modified population analysis profile (PAP) method to detect hetero-resistance to vancomycin in Staphylococcus aureus in a UK hospital. J Antimicrob Chemother. 2001;47:399\u2013403.","journal-title":"J Antimicrob Chemother"},{"key":"1140_CR19","doi-asserted-by":"publisher","first-page":"1008","DOI":"10.1128\/JCM.38.3.1008-1015.2000","volume":"38","author":"MC Enright","year":"2000","unstructured":"Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000;38:1008\u201315.","journal-title":"J Clin Microbiol"},{"key":"1140_CR20","doi-asserted-by":"publisher","first-page":"2155","DOI":"10.1128\/AAC.46.7.2155-2161.2002","volume":"46","author":"DC Oliveira","year":"2002","unstructured":"Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2002;46:2155\u201361.","journal-title":"Antimicrob Agents Chemother"},{"key":"1140_CR21","doi-asserted-by":"publisher","first-page":"5442","DOI":"10.1128\/JCM.41.12.5442-5448.2003","volume":"41","author":"D Harmsen","year":"2003","unstructured":"Harmsen D, Claus H, Witte W, Rothg\u00e4nger J, Claus H, Turnwald D, Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41:5442\u20138.","journal-title":"J Clin Microbiol"},{"key":"1140_CR22","doi-asserted-by":"publisher","first-page":"4060","DOI":"10.1128\/JCM.40.11.4060-4067.2002","volume":"40","author":"P Gilot","year":"2002","unstructured":"Gilot P, Lina G, Cochard T, Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol. 2002;40:4060\u20137.","journal-title":"J Clin Microbiol"},{"key":"1140_CR23","doi-asserted-by":"publisher","first-page":"2233","DOI":"10.1128\/jcm.33.9.2233-2239.1995","volume":"33","author":"FC Tenover","year":"1995","unstructured":"Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33:2233\u20139.","journal-title":"J Clin Microbiol"},{"key":"1140_CR24","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1093\/jac\/dkp394","volume":"65","author":"Y Kato","year":"2010","unstructured":"Kato Y, Suzuki T, Ida T, Maebashi K. Genetic changes associated with glycopeptide resistance in Staphylococcus aureus: predominance of amino acid substitutions in YvqF\/VraSR. J Antimicrob Chemother. 2010;65:37\u201345.","journal-title":"J Antimicrob Chemother"},{"key":"1140_CR25","doi-asserted-by":"publisher","first-page":"5845","DOI":"10.1128\/AAC.01139-12","volume":"56","author":"C Hafer","year":"2012","unstructured":"Hafer C, Lin Y, Kornblum J, Lowy FD, Uhlemann AC. Contribution of selected gene mutations to resistance in clinical isolates of vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother. 2012;56:5845\u201351.","journal-title":"Antimicrob Agents Chemother"},{"key":"1140_CR26","doi-asserted-by":"publisher","first-page":"e01082-20","DOI":"10.1128\/AAC.01082-20","volume":"64","author":"H Kim","year":"2020","unstructured":"Kim H, Kim ES, Lee SC, Yang E, Kim HS, Sung H, et al. Decreased incidence of methicillin-resistant Staphylococcus aureus bacteremia in intensive care units: a 10-year clinical, microbiological, and genotypic analysis in a tertiary hospital. Antimicrob Agents Chemother. 2020;64:e01082-20.","journal-title":"Antimicrob Agents Chemother"},{"key":"1140_CR27","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1186\/s13756-018-0422-1","volume":"7","author":"CH Chiang","year":"2018","unstructured":"Chiang CH, Pan SC, Yang TS, Matsuda K, Kim HB, Choi YH, et al. Healthcare-associated infections in intensive care units in Taiwan, South Korea, and Japan: recent trends based on national surveillance reports. Antimicrob Resist Infect Control. 2018;7:129.","journal-title":"Antimicrob Resist Infect Control"},{"key":"1140_CR28","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1128\/AAC.00520-13","volume":"58","author":"YK Yoon","year":"2014","unstructured":"Yoon YK, Park DW, Sohn JW, Kim HY, Kim YS, Lee CS, et al. Multicenter prospective observational study of the comparative efficacy and safety of vancomycin versus teicoplanin in patients with health care-associated methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob Agents Chemother. 2014;58:317\u201324.","journal-title":"Antimicrob Agents Chemother"},{"key":"1140_CR29","doi-asserted-by":"publisher","first-page":"e18","DOI":"10.1093\/cid\/ciq146","volume":"52","author":"C Liu","year":"2011","unstructured":"Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, Gorwitz RJ, et al. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis. 2011;52:e18\u201355.","journal-title":"Clin Infect Dis"},{"key":"1140_CR30","doi-asserted-by":"publisher","first-page":"988","DOI":"10.3389\/fmicb.2019.00988","volume":"10","author":"L Maudsdotter","year":"2019","unstructured":"Maudsdotter L, Ushijima Y, Morikawa K. Fitness of spontaneous rifampicin-resistant Staphylococcus aureus isolates in a biofilm environment. Front Microbiol. 2019;10:988.","journal-title":"Front Microbiol"}],"container-title":["Antimicrobial Resistance &amp; Infection Control"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13756-022-01140-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13756-022-01140-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13756-022-01140-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T10:42:49Z","timestamp":1660560169000},"score":1,"resource":{"primary":{"URL":"https:\/\/aricjournal.biomedcentral.com\/articles\/10.1186\/s13756-022-01140-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,5]]},"references-count":30,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["1140"],"URL":"https:\/\/doi.org\/10.1186\/s13756-022-01140-9","relation":{},"ISSN":["2047-2994"],"issn-type":[{"value":"2047-2994","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,5]]},"assertion":[{"value":"17 March 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"26 July 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 August 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This study was approved by the local institutional ethics board (SMC 2020-01-014). The need for informed consent was waived because this study used anonymized clinical data form novel hospital`s data warehouse. The study was performed in accordance with the guidelines followed as per the Declaration of Helsinki.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"The manuscript is approved by all authors for publication.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"101"}}