{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T00:32:19Z","timestamp":1789605139428,"version":"build-2803163510"},"reference-count":57,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,10,29]],"date-time":"2024-10-29T00:00:00Z","timestamp":1730160000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,10,29]],"date-time":"2024-10-29T00:00:00Z","timestamp":1730160000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100024743","name":"Suez Canal University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100024743","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Infect Dis"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p><jats:italic>Staphylococcus aureus<\/jats:italic> clinical isolates with vancomycin MICs of 2\u00a0\u00b5g\/ml have been associated with vancomycin therapeutic failure and the heterogenous vancomycin-intermediate <jats:italic>S. aureus<\/jats:italic> (hVISA) phenotype. While carriage of <jats:italic>van<\/jats:italic> genes has usually been associated with higher level of MIC and frank vancomycin resistance, the unrecognized risk of hetero-resistance is frequently underestimated. Methods used for assessing vancomycin susceptibility have also shown different concordance and variable performance and accessibility in routine clinical diagnostics posing a challenge to inform treatment selection in hospital settings.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>A total of 195 clinical samples were obtained among which 100 <jats:italic>S. aureus<\/jats:italic> isolates were identified. Ninety-six MRSA isolates have been identified using cefoxitin disc and <jats:italic>mec<\/jats:italic>A gene detection. The <jats:italic>van<\/jats:italic>A and <jats:italic>van<\/jats:italic>B genes have been screened for in the studied isolates using conventional PCR amplification. Examination of reduced vancomycin susceptibility has been performed using vancomycin screen agar, Broth Micro Dilution method (BMD), and VITEK2. Blood isolates were screened for hVISA using PAP-AUC method.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Vancomycin screening agar applied to 96 MRSA isolates revealed 16 isolates with reduced vancomycin susceptibility. Further MIC testing revealed that 7 isolates were VISA and only 1 isolate was identified as VRSA using both BMD MIC method and VITEK2. Among 24 tested blood isolates, 4 isolates (16.7%) revealed the hVISA phenotype as identified using PAP-AUC method. Using PCR, <jats:italic>van<\/jats:italic>A gene was identified in 5 <jats:italic>S. aureus<\/jats:italic> isolates (5%). Three of them were VSSA while the other two isolates were VISA.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>In this study, we report the very low prevalence of VRSA among the tested <jats:italic>S. aureus<\/jats:italic> clinical isolates (1%) and the existence of hVISA phenotype among studied <jats:italic>S. aureus<\/jats:italic> blood isolates at the rate of 16.7% in our setting. Fifty percent (8\/16) of isolates that demonstrated reduced vancomycin susceptibility using vancomycin agar screen tested susceptible using both broth dilution method and VITEK2. These finding together with the concerning silent carriage of <jats:italic>van<\/jats:italic>A gene among VSSA and VISA (5%) may underly hidden and uninvestigated factors contributing to vancomycin treatment failure that warrant cautious vancomycin prescription.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12879-024-10047-2","type":"journal-article","created":{"date-parts":[[2024,10,29]],"date-time":"2024-10-29T09:12:00Z","timestamp":1730193120000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Reduced vancomycin susceptibility in Staphylococcus aureus clinical isolates: a spectrum of less investigated uncertainties"],"prefix":"10.1186","volume":"24","author":[{"given":"Christine E.","family":"Tawfeek","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sally","family":"Khattab","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nermine","family":"Elmaraghy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anwar A.","family":"Heiba","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wedad M.","family":"Nageeb","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,10,29]]},"reference":[{"key":"10047_CR1","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1016\/S0140-6736(89)90076-7","volume":"333","author":"PAC Maple","year":"1989","unstructured":"Maple PAC, Hamilton-Miller JMT, Brumfitt W. World-wide antibiotic resistance in methicillin-resistant Staphylococcus aureus. Lancet. 1989;333:537\u201340.","journal-title":"Lancet"},{"key":"10047_CR2","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":"10047_CR3","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":"10047_CR4","doi-asserted-by":"publisher","first-page":"5751785","DOI":"10.1155\/2016\/5751785","volume":"2016","author":"M Abdel-Maksoud","year":"2016","unstructured":"Abdel-Maksoud M, El-Shokry M, Ismail G, Hafez S, El-Kholy A, Attia E, et al. Methicillin-Resistant Staphylococcus aureus recovered from Healthcare\u2010and Community\u2010Associated infections in Egypt. Int J Bacteriol. 2016;2016:5751785.","journal-title":"Int J Bacteriol"},{"key":"10047_CR5","doi-asserted-by":"crossref","unstructured":"Amr GE, Al Gammal S. Emergence of Vancomycin resistant Staphylococcus aureus isolated from patients in ICUs of Zagazig University Hospitals. Egyptian Journal of Medical Microbiology. 2017;26.","DOI":"10.12816\/0046229"},{"key":"10047_CR6","doi-asserted-by":"publisher","first-page":"134","DOI":"10.18683\/germs.2018.1140","volume":"8","author":"N ElSayed","year":"2018","unstructured":"ElSayed N, Ashour M, Amine AEK. Vancomycin resistance among Staphylococcus aureus isolates in a rural setting, Egypt. Germs. 2018;8:134.","journal-title":"Germs"},{"key":"10047_CR7","doi-asserted-by":"publisher","first-page":"5","DOI":"10.21608\/ejmm.2022.262673","volume":"31","author":"WAM Ibrahiem","year":"2022","unstructured":"Ibrahiem WAM, Rizk DE, Kenawy H, Hassan RHE. Prevalence of vancomycin resistance among clinical isolates of MRSA from different governorates in Egypt. Egypt J Med Microbiol. 2022;31:5\u201314.","journal-title":"Egypt J Med Microbiol"},{"key":"10047_CR8","first-page":"45","volume":"32","author":"NM Gohar","year":"2023","unstructured":"Gohar NM, Balah MM, Sahloul N. Detection of Vancomycin Resistance among Hospital and Community-acquired Methicillin-resistant Staphylococcus aureus isolates. Egypt J Med Microbiol. 2023;32:45\u201352.","journal-title":"Egypt J Med Microbiol"},{"key":"10047_CR9","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1186\/s12879-023-08202-2","volume":"23","author":"A Azzam","year":"2023","unstructured":"Azzam A, Khaled H, Mosa M, Refaey N, AlSaifi M, Elsisi S, et al. Epidemiology of clinically isolated methicillin-resistant Staphylococcus aureus (MRSA) and its susceptibility to linezolid and Vancomycin in Egypt: a systematic review with meta-analysis. BMC Infect Dis. 2023;23:263.","journal-title":"BMC Infect Dis"},{"key":"10047_CR10","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1186\/s13756-023-01291-3","volume":"12","author":"MA Belete","year":"2023","unstructured":"Belete MA, Gedefie A, Alemayehu E, Debash H, Mohammed O, Gebretsadik D, et al. The prevalence of Vancomycin-resistant Staphylococcus aureus in Ethiopia: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2023;12:86.","journal-title":"Antimicrob Resist Infect Control"},{"key":"10047_CR11","doi-asserted-by":"publisher","first-page":"2354","DOI":"10.1128\/AAC.01702-08","volume":"53","author":"M-L Foucault","year":"2009","unstructured":"Foucault M-L, Courvalin P, Grillot-Courvalin C. Fitness cost of VanA-type Vancomycin resistance in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2009;53:2354\u20139.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR12","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/S1473-3099(01)00091-3","volume":"1","author":"K Hiramatsu","year":"2001","unstructured":"Hiramatsu K. Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect Dis. 2001;1:147\u201355.","journal-title":"Lancet Infect Dis"},{"key":"10047_CR13","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 PDR, 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":"10047_CR14","doi-asserted-by":"publisher","first-page":"505","DOI":"10.3760\/cma.j.issn.0366-6999.20120812","volume":"126","author":"W Yan","year":"2013","unstructured":"Yan W, Hu Y, Ai X, Xu H, Sun T. Prevalence and clinical prognosis of heteroresistant Vancomycin-Intermediatestaphylococcus aureusin a tertiary care center in China. Chin Med J (Engl). 2013;126:505\u20139.","journal-title":"Chin Med J (Engl)"},{"key":"10047_CR15","doi-asserted-by":"publisher","first-page":"3541","DOI":"10.1128\/AAC.04765-14","volume":"59","author":"YP Chong","year":"2015","unstructured":"Chong YP, Park K-H, Kim ES, Kim M-N, Kim S-H, Lee S-O, et al. Clinical and microbiologic analysis of the risk factors for mortality in patients with heterogeneous Vancomycin-intermediate Staphylococcus aureus bacteremia. Antimicrob Agents Chemother. 2015;59:3541\u20137.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR16","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":"10047_CR17","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":"10047_CR18","doi-asserted-by":"publisher","first-page":"2077","DOI":"10.1128\/JCM.00448-13","volume":"51","author":"MJ Rybak","year":"2013","unstructured":"Rybak MJ, Vidaillac C, Sader HS, Rhomberg PR, Salimnia H, Briski LE, et al. Evaluation of Vancomycin susceptibility testing for methicillin-resistant Staphylococcus aureus: comparison of Etest and three automated testing methods. J Clin Microbiol. 2013;51:2077\u201381.","journal-title":"J Clin Microbiol"},{"key":"10047_CR19","doi-asserted-by":"publisher","first-page":"1641","DOI":"10.1093\/jac\/dkab065","volume":"76","author":"C Brusamarello","year":"2021","unstructured":"Brusamarello C, Daley AJ, Zhu X, Landersdorfer C, Gwee A. How important are MIC determination methods when targeting Vancomycin levels in patients with Staphylococcus aureus infections? J Antimicrob Chemother. 2021;76:1641\u20133.","journal-title":"J Antimicrob Chemother"},{"key":"10047_CR20","doi-asserted-by":"publisher","first-page":"845","DOI":"10.3390\/diagnostics12040845","volume":"12","author":"H-S Chung","year":"2022","unstructured":"Chung H-S, Lee M. Different antimicrobial susceptibility testing methods to determine Vancomycin susceptibility and MIC for Staphylococcus aureus with reduced Vancomycin susceptibility. Diagnostics. 2022;12:845.","journal-title":"Diagnostics"},{"key":"10047_CR21","doi-asserted-by":"publisher","first-page":"2013","DOI":"10.1128\/JCM.00221-09","volume":"47","author":"JM Swenson","year":"2009","unstructured":"Swenson JM, Anderson KF, Lonsway DR, Thompson A, McAllister SK, Limbago BM, et al. Accuracy of commercial and reference susceptibility testing methods for detecting Vancomycin-intermediate Staphylococcus aureus. J Clin Microbiol. 2009;47:2013\u20137.","journal-title":"J Clin Microbiol"},{"key":"10047_CR22","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1590\/S0036-46652014000600002","volume":"56","author":"FCP Rossatto","year":"2014","unstructured":"Rossatto FCP, Proen\u00e7a LA, Becker AP, Silveira AC, de O, Caier\u00e3o J, D\u2019azevedo PA. Evaluation of methods in detecting Vancomycin MIC among MRSA isolates and the changes in accuracy related to different MIC values. Rev Inst Med Trop Sao Paulo. 2014;56:469\u201372.","journal-title":"Rev Inst Med Trop Sao Paulo"},{"key":"10047_CR23","first-page":"DC01","volume":"9","author":"C Agrawal","year":"2015","unstructured":"Agrawal C, Madan M, Pandey A, Thakuria B. Methicillin resistant Staphylococcus aureus: inconsistencies in Vancomycin susceptibility testing methods, limitations and advantages of each method. J Clin Diagn Res. 2015;9:DC01.","journal-title":"J Clin Diagn Res"},{"key":"10047_CR24","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/j.jgar.2017.04.007","volume":"10","author":"R Diaz","year":"2017","unstructured":"Diaz R, Ramalheira E, Afreixo V, Gago B. Evaluation of Vancomycin MIC creep in Staphylococcus aureus. J Glob Antimicrob Resist. 2017;10:281\u20134.","journal-title":"J Glob Antimicrob Resist"},{"key":"10047_CR25","doi-asserted-by":"publisher","first-page":"e8963","DOI":"10.7717\/peerj.8963","volume":"8","author":"C-F Kuo","year":"2020","unstructured":"Kuo C-F, Lio CF, Chen H-T, Wang Y-TT, Ma KS-K, Chou YT, et al. Discordance of Vancomycin minimum inhibitory concentration for methicillin-resistant Staphylococcus aureus at 2 \u00b5g\/mL between Vitek II, E-test, and broth microdilution. PeerJ. 2020;8:e8963.","journal-title":"PeerJ"},{"key":"10047_CR26","unstructured":"Clinical and Laboratory Standards Institute. In: Wayne CL, editor. Performance standards for antimicrobial susceptibility testing. 34 ed. PA; 2024."},{"key":"10047_CR27","doi-asserted-by":"publisher","first-page":"3847347","DOI":"10.1155\/2021\/3847347","volume":"2021","author":"M Maharjan","year":"2021","unstructured":"Maharjan M, Sah AK, Pyakurel S, Thapa S, Maharjan S, Adhikari N, et al. Molecular confirmation of vancomycin-resistant Staphylococcus aureus with vanA Gene from a hospital in Kathmandu. Int J Microbiol. 2021;2021:3847347.","journal-title":"Int J Microbiol"},{"key":"10047_CR28","doi-asserted-by":"publisher","first-page":"949","DOI":"10.1128\/JCM.02295-09","volume":"48","author":"JWC D C-AB","year":"2010","unstructured":"D C-AB JWC, Michael DW. Novel screening Agar for detection of Vancomycin-Nonsusceptible Staphylococcus aureus. J Clin Microbiol. 2010;48:949\u201351.","journal-title":"J Clin Microbiol"},{"key":"10047_CR29","first-page":"12","volume":"7","author":"HB Othman","year":"2019","unstructured":"Othman HB, Halim RMA, Gomaa FAM, Amer MZ. Vancomycin MIC distribution among methicillin-resistant Staphylococcus aureus. Is reduced Vancomycin susceptibility related to MIC creep? Open Access Maced. J Med Sci. 2019;7:12.","journal-title":"J Med Sci"},{"key":"10047_CR30","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1186\/1471-2334-11-287","volume":"11","author":"Y Harigaya","year":"2011","unstructured":"Harigaya Y, Ngo D, Lesse AJ, Huang V, Tsuji BT. Characterization of heterogeneous Vancomycin-intermediate resistance, MIC and accessory gene regulator (agr) dysfunction among clinical bloodstream isolates of staphyloccocus aureus. BMC Infect Dis. 2011;11:287.","journal-title":"BMC Infect Dis"},{"key":"10047_CR31","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1515\/med-2018-0071","volume":"13","author":"J Xu","year":"2018","unstructured":"Xu J, Pang L, Ma XX, Hu J, Tian Y, Yang YL, et al. Phenotypic and molecular characterisation of Staphylococcus aureus with reduced Vancomycin susceptibility derivated in vitro. Open Med. 2018;13:475\u201386.","journal-title":"Open Med"},{"key":"10047_CR32","doi-asserted-by":"crossref","unstructured":"Zarghami Moghaddam P, Azimian A, Sepahy A, Iranbakhsh A. Isolation and genetic characterization of vancomycin-resistant and mecC\u2009+\u2009methicillin-resistant Staphylococcus aureus strains in clinical samples of Bojnurd, Northeastern Iran. Jundishapur Journal of Microbiology. 2021;14.","DOI":"10.5812\/jjm.118949"},{"key":"10047_CR33","unstructured":"Medhat ED, Magi M, Mohamed EN, El Sayed K, Mohamed EK. The first two vancomycin resistant Staphylococcus aureus isolates in Mansoura university hospital: epidemiology and antimicrobial study. 2008."},{"key":"10047_CR34","first-page":"36","volume":"5","author":"RI Shebl","year":"2019","unstructured":"Shebl RI, Mosaad YO. Frequency and antimicrobial resistance pattern among bacterial clinical isolates recovered from different specimens in Egypt. Cent Afr J Public Heal. 2019;5:36\u201345.","journal-title":"Cent Afr J Public Heal"},{"key":"10047_CR35","doi-asserted-by":"publisher","first-page":"208","DOI":"10.21608\/ajps.2022.269253","volume":"66","author":"K Al-Ghareeb","year":"2022","unstructured":"Al-Ghareeb K, Abdel Gwad A, Gamal El Din M, Azmy A. PREVALENCE OF VANCOMYCIN RESISTANT STAPHYLOCOCCUS AUREUS (VRSA) IN SOME EGYPTIAN HOSPITALS. Al-Azhar J Pharm Sci. 2022;66:208\u201321.","journal-title":"Al-Azhar J Pharm Sci"},{"key":"10047_CR36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2334-6-156","volume":"6","author":"HK Tiwari","year":"2006","unstructured":"Tiwari HK, Sen MR. Emergence of Vancomycin resistant Staphylococcus aureus (VRSA) from a tertiary care hospital from northern part of India. BMC Infect Dis. 2006;6:1\u20136.","journal-title":"BMC Infect Dis"},{"key":"10047_CR37","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/j.jare.2019.10.005","volume":"21","author":"Y Cong","year":"2020","unstructured":"Cong Y, Yang S, Rao X. Vancomycin resistant Staphylococcus aureus infections: a review of case updating and clinical features. J Adv Res. 2020;21:169\u201376.","journal-title":"J Adv Res"},{"key":"10047_CR38","doi-asserted-by":"publisher","first-page":"97","DOI":"10.51429\/EJMM29313","volume":"29","author":"AH Elkhyat","year":"2020","unstructured":"Elkhyat AH, Makled AF, Albeltagy AM, Keshk TF, Dawoud AM. Prevalence of vanA Gene among Methicillin Resistant S. aureus strains isolated from burn Wound infections in Menoufia University Hospitals. Egypt J Med Microbiol. 2020;29:97\u2013104.","journal-title":"Egypt J Med Microbiol"},{"key":"10047_CR39","first-page":"269","volume":"90","author":"WA McGuinness","year":"2017","unstructured":"McGuinness WA, Malachowa N, DeLeo FR. Vancomycin resistance in Staphylococcus aureus. Yale J Biology Med. 2017;90:269\u201381.","journal-title":"Yale J Biology Med"},{"key":"10047_CR40","doi-asserted-by":"publisher","first-page":"345","DOI":"10.2217\/fmb-2018-0346","volume":"14","author":"M Wilcox","year":"2019","unstructured":"Wilcox M, Al-Obeid S, Gales A, Kozlov R, Mart\u00ednez-Orozco JA, Rossi F, et al. Reporting elevated Vancomycin minimum inhibitory concentration in methicillin-resistant Staphylococcus aureus: consensus by an International Working Group. Future Microbiol. 2019;14:345\u201352.","journal-title":"Future Microbiol"},{"key":"10047_CR41","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1128\/jb.175.1.117-127.1993","volume":"175","author":"M Arthur","year":"1993","unstructured":"Arthur M, Molinas C, Depardieu F, Courvalin P. Characterization of Tn1546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol. 1993;175:117\u201327.","journal-title":"J Bacteriol"},{"key":"10047_CR42","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1128\/AAC.00576-06","volume":"51","author":"LM Weigel","year":"2007","unstructured":"Weigel LM, Donlan RM, Shin DH, Jensen B, Clark NC, McDougal LK, et al. High-level Vancomycin-resistant Staphylococcus aureus isolates associated with a polymicrobial biofilm. Antimicrob Agents Chemother. 2007;51:231\u20138.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR43","doi-asserted-by":"publisher","first-page":"4281","DOI":"10.1128\/AAC.48.11.4281-4285.2004","volume":"48","author":"B P\u00e9richon","year":"2004","unstructured":"P\u00e9richon B, Courvalin P. Heterologous expression of the enterococcal vanA operon in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2004;48:4281\u20135.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR44","doi-asserted-by":"crossref","unstructured":"El-Aziz NKA, El-Hamid MIA, Bendary MM, El-Azazy AA, Ammar AM. Existence of vancomycin resistance among methicillin resistant S. aureus recovered from animal and human sources in Egypt. Slovenian Veterinary Research\/Slovenski Veterinarski Zbornik. 2018;55.","DOI":"10.26873\/SVR-649-2018"},{"key":"10047_CR45","doi-asserted-by":"publisher","first-page":"335","DOI":"10.5001\/omj.2014.90","volume":"29","author":"S Saadat","year":"2014","unstructured":"Saadat S, Solhjoo K, Norooz-Nejad M-J, Kazemi A. VanA and vanB positive Vancomycin-resistant Staphylococcus aureus among clinical isolates in Shiraz, South of Iran. Oman Med J. 2014;29:335.","journal-title":"Oman Med J"},{"key":"10047_CR46","doi-asserted-by":"publisher","first-page":"3622","DOI":"10.1128\/AAC.00410-06","volume":"50","author":"B P\u00e9richon","year":"2006","unstructured":"P\u00e9richon B, Courvalin P. Synergism between \u03b2-lactams and glycopeptides against VanA-type methicillin-resistant Staphylococcus aureus and heterologous expression of the vanA operon. Antimicrob Agents Chemother. 2006;50:3622\u201330.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR47","doi-asserted-by":"publisher","first-page":"4119","DOI":"10.1128\/AAC.00286-16","volume":"60","author":"S Audun","year":"2016","unstructured":"Audun S, Torunn P, Wik LK, K\u00e5re B, Gresdal RT, Andreas R, et al. A silenced vanA Gene Cluster on a transferable plasmid caused an outbreak of Vancomycin-Variable Enterococci. Antimicrob Agents Chemother. 2016;60:4119\u201327.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR48","doi-asserted-by":"publisher","first-page":"e85873","DOI":"10.1371\/journal.pone.0085873","volume":"9","author":"NK Qureshi","year":"2014","unstructured":"Qureshi NK, Yin S, Boyle-Vavra S. The role of the Staphylococcal VraTSR Regulatory System on Vancomycin Resistance and vanA Operon expression in Vancomycin-Resistant Staphylococcus aureus. PLoS ONE. 2014;9:e85873.","journal-title":"PLoS ONE"},{"key":"10047_CR49","doi-asserted-by":"publisher","first-page":"3642","DOI":"10.1128\/AAC.00206-09","volume":"53","author":"W Sun","year":"2009","unstructured":"Sun W, Chen H, Liu Y, Zhao C, Nichols WW, Chen M, et al. Prevalence and characterization of heterogeneous Vancomycin-intermediate Staphylococcus aureus isolates from 14 cities in China. Antimicrob Agents Chemother. 2009;53:3642\u20139.","journal-title":"Antimicrob Agents Chemother"},{"key":"10047_CR50","doi-asserted-by":"publisher","first-page":"2424","DOI":"10.1093\/jac\/dkaa221","volume":"75","author":"BE Castro","year":"2020","unstructured":"Castro BE, Berrio M, Vargas ML, Carvajal LP, Millan LV, Rios R, et al. Detection of heterogeneous Vancomycin intermediate resistance in MRSA isolates from Latin America. J Antimicrob Chemother. 2020;75:2424\u201331.","journal-title":"J Antimicrob Chemother"},{"key":"10047_CR51","doi-asserted-by":"publisher","first-page":"194","DOI":"10.4103\/ijmr.IJMR_1976_17","volume":"150","author":"R Amberpet","year":"2019","unstructured":"Amberpet R, Sistla S, Sugumar M, Nagasundaram N, Manoharan M, Parija SC. Detection of heterogeneous Vancomycin-intermediate Staphylococcus aureus: a preliminary report from south India. Indian J Med Res. 2019;150:194\u20138.","journal-title":"Indian J Med Res"},{"key":"10047_CR52","doi-asserted-by":"publisher","first-page":"1594","DOI":"10.1093\/jac\/dkr169","volume":"66","author":"R Khatib","year":"2011","unstructured":"Khatib R, Jose J, Musta A, Sharma M, Fakih MG, Johnson LB, et al. Relevance of Vancomycin-intermediate susceptibility and heteroresistance in methicillin-resistant Staphylococcus aureus bacteraemia. J Antimicrob Chemother. 2011;66:1594\u20139.","journal-title":"J Antimicrob Chemother"},{"key":"10047_CR53","doi-asserted-by":"publisher","first-page":"1489","DOI":"10.1128\/JCM.02302-10","volume":"49","author":"SJ van Hal","year":"2011","unstructured":"van Hal SJ, Wehrhahn MC, Barbagiannakos T, Mercer J, Chen D, Paterson DL, et al. Performance of various testing methodologies for detection of heteroresistant Vancomycin-intermediate Staphylococcus aureus in bloodstream isolates. J Clin Microbiol. 2011;49:1489\u201394.","journal-title":"J Clin Microbiol"},{"key":"10047_CR54","doi-asserted-by":"publisher","first-page":"3158","DOI":"10.1007\/s00284-020-02123-y","volume":"77","author":"MY Lee","year":"2020","unstructured":"Lee MY, Lee WI, Kim MH, Kang SY, Kim YJ. Etest methods for screening heterogeneous Vancomycin-intermediate Staphylococcus aureus (hVISA) strains. Curr Microbiol. 2020;77:3158\u201367.","journal-title":"Curr Microbiol"},{"key":"10047_CR55","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1089\/mdr.2014.0190","volume":"21","author":"S Di Gregorio","year":"2015","unstructured":"Di Gregorio S, Perazzi B, Ordonez AM, De Gregorio S, Foccoli M, Lasala MB, et al. Clinical, microbiological, and genetic characteristics of heteroresistant Vancomycin-intermediate Staphylococcus aureus bacteremia in a teaching hospital. Microb Drug Resist. 2015;21:25\u201334.","journal-title":"Microb Drug Resist"},{"key":"10047_CR56","unstructured":"Nagwa R, Sherif Z. Heterogeneous Vancomycin intermediate resistance within methicillin-resistant staphylococcus aureus clinical isolates in Alexandria province. Egyptian Journal of Medical Microbiology. 2007."},{"key":"10047_CR57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12941-017-0238-5","volume":"16","author":"GE-S Mashaly","year":"2017","unstructured":"Mashaly GE-S, El-Mahdy RH. Vancomycin heteroresistance in coagulase negative Staphylococcus blood stream infections from patients of intensive care units in Mansoura University Hospitals, Egypt. Ann Clin Microbiol Antimicrob. 2017;16:1\u20135.","journal-title":"Ann Clin Microbiol Antimicrob"}],"container-title":["BMC Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12879-024-10047-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12879-024-10047-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12879-024-10047-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,30]],"date-time":"2024-10-30T06:55:29Z","timestamp":1730271329000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcinfectdis.biomedcentral.com\/articles\/10.1186\/s12879-024-10047-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,29]]},"references-count":57,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["10047"],"URL":"https:\/\/doi.org\/10.1186\/s12879-024-10047-2","relation":{},"ISSN":["1471-2334"],"issn-type":[{"value":"1471-2334","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,29]]},"assertion":[{"value":"9 July 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 October 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 October 2024","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 Research Ethics Committee of the Faculty of Medicine, Suez Canal University (Reference Code 4823). Written informed consent was obtained from all participants before participation.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1218"}}