{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,13]],"date-time":"2026-05-13T18:03:12Z","timestamp":1778695392443,"version":"3.51.4"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2021,6,5]],"date-time":"2021-06-05T00:00:00Z","timestamp":1622851200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2021,6,5]],"date-time":"2021-06-05T00:00:00Z","timestamp":1622851200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/n\/a","name":"Ministry of Higher Education Fundamental Research Grant Scheme (FRGS)<\/","doi-asserted-by":"publisher","award":["FP016-2014B"],"award-info":[{"award-number":["FP016-2014B"]}],"id":[{"id":"10.13039\/n\/a","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/n\/a","name":"International Research Funding","doi-asserted-by":"publisher","award":["IF004-2020"],"award-info":[{"award-number":["IF004-2020"]}],"id":[{"id":"10.13039\/n\/a","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Folia Microbiol"],"published-print":{"date-parts":[[2021,10]]},"DOI":"10.1007\/s12223-021-00877-x","type":"journal-article","created":{"date-parts":[[2021,6,5]],"date-time":"2021-06-05T09:02:52Z","timestamp":1622883772000},"page":"741-749","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Investigation of biofilm formation in methicillin-resistant Staphylococcus aureus associated with bacteraemia in a tertiary hospital"],"prefix":"10.1007","volume":"66","author":[{"given":"Wen Kiong","family":"Niek","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cindy Shuan Ju","family":"Teh","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nuryana","family":"Idris","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kwai Lin","family":"Thong","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Soo Tein","family":"Ngoi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4506-1304","authenticated-orcid":false,"given":"Sasheela Sri La Sri","family":"Ponnampalavanar","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,6,5]]},"reference":[{"key":"877_CR1","first-page":"445","volume":"2","author":"NK Archer","year":"2011","unstructured":"Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME (2011) Staphylococcus Aureus Biofilms Virulence 2:445\u2013459","journal-title":"Staphylococcus Aureus Biofilms Virulence"},{"key":"877_CR2","doi-asserted-by":"publisher","first-page":"2151","DOI":"10.1128\/JCM.39.6.2151-2156.2001","volume":"39","author":"CR Arciola","year":"2001","unstructured":"Arciola CR, Baldassarri L, Montanaro L (2001) Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J Clin Microbiol 39:2151\u20132156","journal-title":"J Clin Microbiol"},{"key":"877_CR3","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1078\/1438-4221-00112","volume":"291","author":"S Arvidson","year":"2001","unstructured":"Arvidson S, Tegmark K (2001) Regulation of virulence determinants in Staphylococcus aureus. Int J Med Microbiol 291:159\u2013170","journal-title":"Int J Med Microbiol"},{"key":"877_CR4","doi-asserted-by":"publisher","first-page":"e1000052","DOI":"10.1371\/journal.ppat.1000052","volume":"4","author":"BR Boles","year":"2008","unstructured":"Boles BR, Horswill AR (2008) agr-Mediated dispersal of Staphylococcus aureus biofilms. PLOS Pathog 4:e1000052","journal-title":"PLOS Pathog"},{"key":"877_CR5","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1002\/cmdc.202000677","volume":"16","author":"S Cascioferro","year":"2020","unstructured":"Cascioferro S, Carbone D, Parrino B, Pecoraro C, Giovannetti E, Cirrincione G, Diana P (2020a) Therapeutic strategies to counteract antibiotic resistance in MRSA biofilm-associated infections. ChemMedChem 16:65\u201380","journal-title":"ChemMedChem"},{"key":"877_CR6","doi-asserted-by":"publisher","first-page":"7923","DOI":"10.1021\/acs.jmedchem.9b01245","volume":"63","author":"S Cascioferro","year":"2020","unstructured":"Cascioferro S, Parrino B, Carbone D, Schillaci D, Giovannetti E, Cirrincione G, Diana P (2020b) Thiazoles, their benzofused systems, and thiazolidinone derivatives: Versatile and promising tools to combat antibiotic resistance. J Med Chem 63:7923\u20137956","journal-title":"J Med Chem"},{"key":"877_CR7","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1016\/j.phrp.2013.09.001","volume":"4","author":"J-O Cha","year":"2013","unstructured":"Cha J-O, Yoo JI, Yoo JS, Chung H-S, Park S-H, Kim HS et al (2013) Investigation of biofilm formation and its association with the molecular and clinical characteristics of methicillin-resistant Staphylococcus aureus. Osong Public Health Res Perspect 4:225\u2013232","journal-title":"Osong Public Health Res Perspect"},{"key":"877_CR8","doi-asserted-by":"publisher","first-page":"2215","DOI":"10.1038\/s41598-018-20661-1","volume":"8","author":"D Choe","year":"2018","unstructured":"Choe D, Szubin R, Dahesh S, Cho S, Nizet V, Palsson B et al (2018) Genome-scale analysis of methicillin-resistant Staphylococcus aureus USA300 reveals a tradeoff between pathogenesis and drug resistance. UK-Sci Rep 8:2215","journal-title":"UK-Sci Rep"},{"key":"877_CR9","doi-asserted-by":"publisher","first-page":"1062","DOI":"10.1177\/039139880502801103","volume":"28","author":"JW Costerton","year":"2005","unstructured":"Costerton JW, Montanaro L, Arciola CR (2005) Biofilm in implant infections: its production and regulation. Int J Artif Organs 28:1062\u20131068","journal-title":"Int J Artif Organs"},{"key":"877_CR10","doi-asserted-by":"publisher","first-page":"1318","DOI":"10.1126\/science.284.5418.1318","volume":"284","author":"JW Costerton","year":"1999","unstructured":"Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science (new York, NY) 284:1318\u20131322","journal-title":"Science (new York, NY)"},{"key":"877_CR11","doi-asserted-by":"crossref","unstructured":"Croes S, Deurenberg RH, Boumans M-LL, Beisser PS, Neef C, Stobberingh EE (2009) Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol 9:229.","DOI":"10.1186\/1471-2180-9-229"},{"key":"877_CR12","doi-asserted-by":"publisher","first-page":"38","DOI":"10.3389\/fcimb.2012.00038","volume":"2","author":"D Cue","year":"2012","unstructured":"Cue D, Lei M, Lee C (2012) Genetic regulation of the intercellular adhesion locus in staphylococci. Front Cell Infect Microbiol 2:38","journal-title":"Front Cell Infect Microbiol"},{"key":"877_CR13","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1186\/1749-799X-6-25","volume":"6","author":"KC Eseonu","year":"2011","unstructured":"Eseonu KC, Middleton SD, Eseonu CC (2011) A retrospective study of risk factors for poor outcomes in methicillin-resistant Staphylococcus aureus (MRSA) infection in surgical patients. J Orthop Surg Res 6:25","journal-title":"J Orthop Surg Res"},{"key":"877_CR14","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1111\/j.1469-0691.2012.03846.x","volume":"18","author":"AC Fluit","year":"2012","unstructured":"Fluit AC (2012) Livestock-associated Staphylococcus aureus. Clin Microbiol Infect 18:735\u2013744","journal-title":"Clin Microbiol Infect"},{"key":"877_CR15","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1038\/nrmicro3161","volume":"12","author":"TJ Foster","year":"2014","unstructured":"Foster TJ, Geoghegan JA, Ganesh VK, H\u00f6\u00f6k M (2014) Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12:49\u201362","journal-title":"Nat Rev Microbiol"},{"key":"877_CR16","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1016\/S0022-2143(00)70018-7","volume":"135","author":"P Francois","year":"2000","unstructured":"Francois P, Schrenzel J, Stoerman-Chopard C, Favre H, Herrmann M, Foster TJ et al (2000) Identification of plasma proteins adsorbed on hemodialysis tubing that promote Staphylococcus aureus adhesion. J Lab Clin Med 135:32\u201342","journal-title":"J Lab Clin Med"},{"key":"877_CR17","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1016\/S0140-6736(00)03572-8","volume":"357","author":"SM Jones","year":"2001","unstructured":"Jones SM, Morgan M, Humphrey TJ, Lappin-Scott H (2001) Effect of vancomycin and rifampicin on methicillin-resistant Staphylococcus aureus biofilms. Lancet 357:40\u201341","journal-title":"Lancet"},{"key":"877_CR18","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1111\/j.1574-695X.2011.00821.x","volume":"63","author":"H Kawamura","year":"2011","unstructured":"Kawamura H, Nishi J, Imuta N, Tokuda K, Miyanohara H, Hashiguchi T et al (2011) Quantitative analysis of biofilm formation of methicillin-resistant Staphylococcus aureus (MRSA) strains from patients with orthopaedic device-related infections. FEMS Immunol Med Microbiol 63:10\u201315","journal-title":"FEMS Immunol Med Microbiol"},{"key":"877_CR19","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1111\/j.1749-6632.2011.06281.x","volume":"1241","author":"MR Kiedrowski","year":"2011","unstructured":"Kiedrowski MR, Horswill AR (2011) New approaches for treating staphylococcal biofilm infections. Ann NY Acad Sci 1241:104\u2013121","journal-title":"Ann NY Acad Sci"},{"key":"877_CR20","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1080\/23744235.2019.1593499","volume":"51","author":"JM Kwiecinski","year":"2019","unstructured":"Kwiecinski JM, Jacobsson G, Horswill AR, Josefsson E, Jin T (2019) Biofilm formation by Staphylococcus aureus clinical isolates correlates with the infection type. Infect Dis 51:446\u2013451","journal-title":"Infect Dis"},{"key":"877_CR21","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.ijantimicag.2008.02.009","volume":"32","author":"AS Kwon","year":"2008","unstructured":"Kwon AS, Park GC, Ryu SY, Lim DH, Lim DY, Choi CH et al (2008) Higher biofilm formation in multidrug-resistant clinical isolates of Staphylococcus aureus. Int J Antimicrob Ag 32:68\u201372","journal-title":"Int J Antimicrob Ag"},{"key":"877_CR22","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1128\/MMBR.00013-14","volume":"78","author":"D Lebeaux","year":"2014","unstructured":"Lebeaux D, Ghigo J-M, Beloin C (2014) Biofilm-related infections: Bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol Mol Biol Rev 78:510\u2013543","journal-title":"Microbiol Mol Biol Rev"},{"key":"877_CR23","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1146\/annurev.micro.112408.134306","volume":"64","author":"K Lewis","year":"2010","unstructured":"Lewis K (2010) Persister Cells Ann Rev Microbiol 64:357\u2013372","journal-title":"Persister Cells Ann Rev Microbiol"},{"key":"877_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fcimb.2015.00001","volume":"5","author":"H McCarthy","year":"2015","unstructured":"McCarthy H, Rudkin JK, Black NS, Gallagher L, O\u2019Neill E, O\u2019Gara JP (2015) Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front Cell Infect Microbiol 5:1","journal-title":"Front Cell Infect Microbiol"},{"key":"877_CR25","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1111\/1574-6968.12424","volume":"353","author":"J McCourt","year":"2014","unstructured":"McCourt J, O\u2019Halloran DP, McCarthy H, O\u2019Gara JP, Geoghegan JA (2014) Fibronectin-binding proteins are required for biofilm formation by community-associated methicillin-resistant Staphylococcus aureus strain LAC. FEMS Microbiol Lett 353:157\u2013164","journal-title":"FEMS Microbiol Lett"},{"key":"877_CR26","doi-asserted-by":"publisher","first-page":"824","DOI":"10.5301\/ijao.5000051","volume":"34","author":"L Montanaro","year":"2011","unstructured":"Montanaro L, Poggi A, Visai L, Ravaioli S, Campoccia D, Speziale P et al (2011) Extracellular DNA in biofilms. Int J Artif Organs 34:824\u2013831","journal-title":"Int J Artif Organs"},{"key":"877_CR27","doi-asserted-by":"publisher","first-page":"228","DOI":"10.7883\/yoken.JJID.2018.289","volume":"72","author":"WK Niek","year":"2019","unstructured":"Niek WK, Teh CSJ, Idris N, Thong KL, Ponnampalavanar S (2019) Predominance of ST22-MRSA-IV clone and emergence of clones for methicillin-resistant Staphylococcus aureus clinical isolates collected from a tertiary teaching hospital over a two-year period. Jpn J Infect Dis 72:228\u2013236","journal-title":"Jpn J Infect Dis"},{"key":"877_CR28","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1111\/j.1574-6968.2007.00688.x","volume":"270","author":"JP O'Gara","year":"2007","unstructured":"O\u2019Gara JP (2007) ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 270:179\u2013188","journal-title":"FEMS Microbiol Lett"},{"key":"877_CR29","doi-asserted-by":"publisher","first-page":"678","DOI":"10.3904\/kjim.2013.28.6.678","volume":"28","author":"HS Ok","year":"2013","unstructured":"Ok HS, Lee HS, Park MJ, Kim KH, Kim BK, Wi YM et al (2013) Predictors and clinical outcomes of persistent methicillin-resistant Staphylococcus aureus bacteremia: a prospective observational study. Korean J Intern Med 28:678\u2013686","journal-title":"Korean J Intern Med"},{"key":"877_CR30","doi-asserted-by":"publisher","first-page":"3835","DOI":"10.1128\/JB.00167-08","volume":"190","author":"E O'Neill","year":"2008","unstructured":"O\u2019Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, Loughman A et al (2008) A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol 190:3835\u20133850","journal-title":"J Bacteriol"},{"key":"877_CR31","first-page":"2437","volume":"2011","author":"GA O'Toole","year":"2011","unstructured":"O\u2019Toole GA (2011) Microtiter dish biofilm formation assay. J vis Exp 2011:2437","journal-title":"J vis Exp"},{"key":"877_CR32","doi-asserted-by":"publisher","first-page":"357","DOI":"10.4155\/fmc-2019-0326","volume":"12","author":"B Parrino","year":"2020","unstructured":"Parrino B, Carbone D, Cirrincione G, Diana P, Cascioferro S (2020) Inhibitors of antibiotic resistance mechanisms: clinical applications and future perspectives. Future Med Chem 12:357\u2013359","journal-title":"Future Med Chem"},{"key":"877_CR33","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1016\/j.ejmech.2018.10.036","volume":"161","author":"B Parrino","year":"2019","unstructured":"Parrino B, Schillaci D, Carnevale I, Giovannetti E, Diana P, Cirrincione G, Cascioferro S (2019) Synthetic small molecules as anti-biofilm agents in the struggle against antibiotic resistance. Eur J Med Chem 161:154\u2013178","journal-title":"Eur J Med Chem"},{"key":"877_CR34","doi-asserted-by":"publisher","first-page":"891","DOI":"10.1111\/j.1600-0463.2007.apm_630.x","volume":"115","author":"S Stepanovi\u0107","year":"2007","unstructured":"Stepanovi\u0107 S, Vukovi\u0107 D, Hola V, Bonaventura GD, Djuki\u0107 S, \u0106irkovi\u0107 I et al (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891\u2013899","journal-title":"APMIS"},{"key":"877_CR35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1586\/14787210.7.1.1","volume":"7","author":"J Szab\u00f3","year":"2009","unstructured":"Szab\u00f3 J (2009) hVISA\/VISA: Diagnostic and therapeutic problems. Expert Rev Anti-Infe 7:1\u20133","journal-title":"Expert Rev Anti-Infe"},{"key":"877_CR36","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1007\/s12223-012-0175-9","volume":"58","author":"E Szczuka","year":"2013","unstructured":"Szczuka E, Urba\u0144ska K, Pietryka M, Kaznowski A (2013) Biofilm density and detection of biofilm-producing genes in methicillin-resistant Staphylococcus aureus strains. Folia Microbiol 58:47\u201352","journal-title":"Folia Microbiol"},{"key":"877_CR37","doi-asserted-by":"publisher","first-page":"4465","DOI":"10.1128\/JCM.41.9.4465-4467.2003","volume":"41","author":"A Tristan","year":"2003","unstructured":"Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G (2003) Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol 41:4465\u20134467","journal-title":"J Clin Microbiol"},{"key":"877_CR38","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/S0378-1135(02)00360-7","volume":"92","author":"P Vasudevan","year":"2003","unstructured":"Vasudevan P, Nair MKM, Annamalai T, Venkitanarayanan KS (2003) Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet Microbiol 92:179\u2013185","journal-title":"Vet Microbiol"},{"key":"877_CR39","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1007\/s10096-016-2598-8","volume":"35","author":"D Yahav","year":"2016","unstructured":"Yahav D, Yassin S, Shaked H, Goldberg E, Bishara J, Paul M et al (2016) Risk factors for long-term mortality of Staphylococcus aureus bacteremia. Eur J Clin Microbiol 35:785\u2013790","journal-title":"Eur J Clin Microbiol"}],"container-title":["Folia Microbiologica"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12223-021-00877-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s12223-021-00877-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12223-021-00877-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,18]],"date-time":"2021-09-18T08:20:15Z","timestamp":1631953215000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s12223-021-00877-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,5]]},"references-count":39,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2021,10]]}},"alternative-id":["877"],"URL":"https:\/\/doi.org\/10.1007\/s12223-021-00877-x","relation":{},"ISSN":["0015-5632","1874-9356"],"issn-type":[{"value":"0015-5632","type":"print"},{"value":"1874-9356","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,5]]},"assertion":[{"value":"28 December 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 June 2021","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 Medical Ethics Committee of University Malaya Medical Centre (UMMC) on 7th June 2014 (MEC-ID: 20,145\u2013168) and had conformed to the principles embodied in the Declaration of Helsinki.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}