{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T02:08:58Z","timestamp":1790647738819,"version":"4.1.0"},"reference-count":42,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,6,9]],"date-time":"2022-06-09T00:00:00Z","timestamp":1654732800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"MML Centre, Warsaw"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Staphylococcus\u00a0lugdunensis is an opportunistic pathogen found in the healthy human skin microbiome bacterial community that is able to cause infections of diverse localization, manifestation, and course, including laryngological infections, such as necrotizing sinusitis. Chronic maxillary sinusitis is a disease present in up to one third of European and American populations, and its etiology is not fully described. Within this study, we aimed to characterize 18 S. lugdunensis strains recovered from maxillary sinuses and evaluate them as etiological agents of chronic disease. We performed MLST analysis, the complex analysis of both phenotypic and genetic virulence factors, antibiotic susceptibility profiles, and biofilm formation assay for the detection of biofilm-associated genes. Altogether, S. lugdunensis strains were clustered into eight different STs, and we demonstrated several virulence factors associated with the chronic disease. All tested strains were able to produce biofilm in vitro with numerous strains with a very strong ability, and overall, they were mostly susceptible to antibiotics, although we found resistance to fosfomycin, erythromycin, and clindamycin in several strains. We believe that further in-depth analysis of S. lugdunensis strains from different niches, including the nasal one, should be performed in the future in order to reduce infection rate and broaden the knowledge about this opportunistic pathogen that is gaining attention.<\/jats:p>","DOI":"10.3390\/ijms23126450","type":"journal-article","created":{"date-parts":[[2022,6,10]],"date-time":"2022-06-10T02:25:33Z","timestamp":1654827933000},"page":"6450","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["May Staphylococcus\u00a0lugdunensis Be an Etiological Factor of Chronic Maxillary Sinuses Infection?"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8337-6975","authenticated-orcid":false,"given":"Maja","family":"Kosecka-Strojek","sequence":"first","affiliation":[{"name":"Department of Microbiology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University in Krakow, Gronostajowa 7, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3509-8111","authenticated-orcid":false,"given":"Mariola","family":"Wolska-G\u0119barzewska","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University in Krakow, Gronostajowa 7, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrianna","family":"Podbielska-Kubera","sequence":"additional","affiliation":[{"name":"MML Centre, Bagno 2, 00-112 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alfred","family":"Samet","sequence":"additional","affiliation":[{"name":"MML Centre, Bagno 2, 00-112 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5528-8898","authenticated-orcid":false,"given":"Beata","family":"Krawczyk","sequence":"additional","affiliation":[{"name":"Department of Molecular Biotechnology and Microbiology, Faculty of Chemistry, Gdansk University of Technology, Gabriela Narutowicza 11\/12, 80-233 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacek","family":"Mi\u0119dzobrodzki","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University in Krakow, Gronostajowa 7, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Micha\u0142","family":"Michalik","sequence":"additional","affiliation":[{"name":"MML Centre, Bagno 2, 00-112 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1007\/s10096-019-03571-6","article-title":"Staphylococcus lugdunensis: Antimicrobial susceptibility and optimal treatment options","volume":"38","author":"Taha","year":"2019","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1111\/j.1469-0691.2009.02813.x","article-title":"Staphylococcus lugdunensis in several niches of the normal skin flora","volume":"16","author":"Bieber","year":"2010","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e1400216","DOI":"10.1126\/sciadv.1400216","article-title":"Staphylococcus aureus and the ecology of the nasal microbiome","volume":"1","author":"Liu","year":"2015","journal-title":"Sci. Adv."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e00205-20","DOI":"10.1128\/CMR.00205-20","article-title":"Staphylococcus lugdunensis: A skin commensal with invasive pathogenic potential","volume":"34","author":"Heilbronner","year":"2021","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2393","DOI":"10.1128\/JCM.00740-08","article-title":"Microbiological characteristics, presumptive identification, and antibiotic susceptibilities of Staphylococcus lugdunensis","volume":"46","author":"Thean","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2030","DOI":"10.1128\/JCM.00177-15","article-title":"Implementation of matrix-assisted laser desorption ionization-time of flight mass spectrometry in routine clinical laboratories improves identification of coagulase-negative staphylococci and reveals the pathogenic role of Staphylococcus lugdunensis","volume":"53","author":"Argemi","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1128\/CMR.00072-12","article-title":"Matrix-assisted laser desorption ionization-time of flight mass spectrometry: A fundamental shift in the routine practice of clinical microbiology","volume":"26","author":"Clark","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1186\/s12941-020-00367-x","article-title":"Coagulase-negative staphylococci (CoNS) as a significant etiological factor of laryngological infections: A review","volume":"19","author":"Michalik","year":"2020","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/1939-4551-7-25","article-title":"ICON: Chronic rhinosinusitis","volume":"7","author":"Bachert","year":"2014","journal-title":"World Allergy Organ. J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1989","DOI":"10.1007\/s00405-015-3650-5","article-title":"The pathophysiological role of bacterial biofilms in chronic sinusitis","volume":"273","author":"Dlugaszewska","year":"2016","journal-title":"Eur. Arch. Otorhinolaryngol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1177\/194589240602000113","article-title":"Endoscopically guided aerobic cultures in postsurgical patients with chronic rhinosinusitis","volume":"20","author":"Coffey","year":"2006","journal-title":"Am. J. Rhinol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"549","DOI":"10.2500\/ajra.2009.23.3366","article-title":"Impaired mucosal healing and infection associated with Staphylococcus aureus after endoscopic sinus surgery","volume":"23","author":"Foreman","year":"2009","journal-title":"Am. J. Rhinol. Allergy"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Michalik, M., Samet, A., Marsza\u0142ek, A., Krawczyk, B., Kot\u0142owski, R., Nowicki, A., Anyszek, T., Nowicki, S., Kur, J., and Nowicki, B. (2018). Intra-operative biopsy in chronic sinusitis detects pathogenic Escherichia coli that carry fimG\/H, fyuA and agn43 genes coding biofilm formation. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0192899"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Krawczyk, B., Michalik, M., Fordon, M., Wysocka, M., Samet, A., and Nowicki, B. (2020). Escherichia coli strains with virulent factors typical for uropathogens were isolated from sinuses from patients with chronic rhinosinusitis-case report. Pathogens, 9.","DOI":"10.3390\/pathogens9050318"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Both, A., Huang, J., Qi, M., Lausmann, C., Wei\u00dfelberg, S., B\u00fcttner, H., Lezius, S., Failla, A.V., Christner, M., and Stegger, M. (2021). Distinct clonal lineages and within-host diversification shape invasive Staphylococcus epidermidis populations. PLoS Pathog., 17.","DOI":"10.1371\/journal.ppat.1009304"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nature18634","article-title":"Human commensals producing a novel antibiotic impair pathogen colonization","volume":"535","author":"Zipperer","year":"2016","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"eaah4680","DOI":"10.1126\/scitranslmed.aah4680","article-title":"Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis","volume":"9","author":"Nakatsuji","year":"2017","journal-title":"Sci. Transl. Med."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2419","DOI":"10.3389\/fmicb.2018.02419","article-title":"Staphylococcus aureus nasal colonization: An update on mechanisms, epidemiology, risk factors, and subsequent infections","volume":"9","author":"Sakr","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2730","DOI":"10.1038\/s41467-019-10646-7","article-title":"Lugdunin amplifies innate immune responses in the skin in synergy with host- and microbiota-derived factors","volume":"10","author":"Bitschar","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1016\/j.tim.2021.07.008","article-title":"Staphylococcus\u00a0lugdunensis","volume":"29","author":"Heilbronner","year":"2021","journal-title":"Trends Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/S1684-1182(10)60074-6","article-title":"Staphylococcus lugdunensis infective endocarditis: A literature review and analysis of risk factors","volume":"43","author":"Liu","year":"2010","journal-title":"J. Microbiol. Immunol. Infect."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.jinf.2016.10.003","article-title":"The occurrence of infective endocarditis with Staphylococcus lugdunensis bacteremia: A retrospective cohort study and systematic review","volume":"74","author":"Non","year":"2017","journal-title":"J. Infect."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Preda, M., Mihai, M.M., Popa, L.I., Di\u021bu, L.-M., Holban, A.M., Manolescu, L.S.C., Popa, G.-L., Muntean, A.-A., Gheorghe, I., and Chifiriuc, C.M. (2021). Phenotypic and genotypic virulence features of staphylococcal strains isolated from difficult-to-treat skin and soft tissue infections. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0246478"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3003","DOI":"10.1128\/JCM.00988-12","article-title":"Multilocus sequence typing analysis of Staphylococcus lugdunensis implies a clonal population structure","volume":"50","author":"Chassain","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Argemi, X., Hansmann, Y., Prola, K., and Pr\u00e9vost, G. (2019). Coagulase-negative staphylococci pathogenomics. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20051215"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3258","DOI":"10.1093\/jac\/dkx291","article-title":"Characterization of two novel variants of staphylococcal cassette chromosome mec elements in oxacillin-resistant Staphylococcus lugdunensis","volume":"72","author":"Chang","year":"2017","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"6453","DOI":"10.1128\/JB.01195-12","article-title":"Iron-regulated surface determinant (Isd) proteins of Staphylococcus lugdunensis","volume":"194","author":"Zapotoczna","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1128\/MMBR.00013-14","article-title":"Biofilm-related infections: Bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics","volume":"78","author":"Lebeaux","year":"2014","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Aubourg, M., Dhalluin, A., Gravey, F., Pottier, M., Thomy, N., Bernay, B., Goux, D., Martineau, M., and Giard, J.-C. (2020). Phenotypic and proteomic approaches of the response to iron-limited condition in Staphylococcus lugdunensis. BMC Microbiol., 20.","DOI":"10.1186\/s12866-020-02016-x"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e0159821","DOI":"10.1128\/spectrum.01598-21","article-title":"Inactivation of the response regulator AgrA has a pleiotropic effect on biofilm formation, pathogenesis and stress response in Staphylococcus lugdunensis","volume":"10","author":"Aubourg","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"39","DOI":"10.3389\/fmicb.2020.00039","article-title":"Role of the LytSR two-component regulatory system in Staphylococcus lugdunensis biofilm formation and pathogenesis","volume":"11","author":"Dahyot","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"278","DOI":"10.3389\/fcimb.2019.00278","article-title":"Development and Validation of a Reference Data Set for Assigning Staphylococcus Species Based on Next-Generation Sequencing of the 16S-23S rRNA Region","volume":"9","author":"Sabat","year":"2019","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1136\/mp.54.4.244","article-title":"Identification of slide coagulase positive, tube coagulase negative Staphylococcus aureus by 16S ribosomal RNA gene sequencing","volume":"54","author":"Woo","year":"2001","journal-title":"Mol. Pathol. MP"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"333","DOI":"10.3201\/eid1202.050962","article-title":"Sequencing and staphylococci identification","volume":"12","author":"Mellmann","year":"2006","journal-title":"Emerg. Infect. Dis."},{"key":"ref_36","first-page":"891","article-title":"Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci","volume":"115","author":"Hola","year":"2007","journal-title":"J. Pathol. Microbiol. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Yeh, C.F., Liu, T.P., Cheng, C.W., Chang, S.C., Lee, M.H., and Lu, J.J. (2015). Molecular characteristics of disease-causing and commensal Staphylococcus lugdunensis isolates from 2003 to 2013 at a tertiary hospital in Taiwan. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0134859"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1128\/JCM.38.2.877-880.2000","article-title":"PCR-Based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains","volume":"38","author":"Frebourg","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1007\/s10096-014-2291-8","article-title":"Virulence factors among Staphylococcus lugdunensis are associated with infection sites and clonal spread","volume":"34","author":"Giormezis","year":"2015","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Szabados, F., Nowotny, Y., Marlinghaus, L., Korte, M., Neumann, S., Kaase, M., and Gatermann, S.G. (2011). Occurrence of genes of putative fibrinogen binding proteins and hemolysins, as well as of their phenotypic correlates in isolates of S. lugdunensis of different origins. BMC Res. Notes, 4.","DOI":"10.1186\/1756-0500-4-113"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1002\/jcla.20352","article-title":"fbl gene as a species-specific target for Staphylococcus lugdunensis identification","volume":"24","author":"Chatzigeorgiou","year":"2010","journal-title":"J. Clin. Lab. Anal."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"334.e1","DOI":"10.1016\/j.cmi.2016.12.018","article-title":"VISLISI trial, a prospective clinical study allowing identification of a new metalloprotease and putative virulence factor from Staphylococcus lugdunensis","volume":"23","author":"Argemi","year":"2017","journal-title":"Clin. Microbiol. Infect."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/12\/6450\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:27:08Z","timestamp":1760138828000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/12\/6450"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,9]]},"references-count":42,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,6]]}},"alternative-id":["ijms23126450"],"URL":"https:\/\/doi.org\/10.3390\/ijms23126450","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,9]]}}}