{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,25]],"date-time":"2026-10-25T23:11:28Z","timestamp":1792969888326,"version":"4.5.0"},"reference-count":49,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2023,5,28]],"date-time":"2023-05-28T00:00:00Z","timestamp":1685232000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>This study aimed to evaluate the frequency of isolation of Staphylococcus aureus from different pathological samples processed in the Microbiology Laboratory of the National Institute of Infectious Diseases \u201cProf. Dr. Matei Bal\u0219\u201d, Romania, between 1 January 2017 and 31 December 2022, aiming to establish the ratio of methicillin-resistant to methicillin-susceptible Staphylococcus aureus strains and the antibiotic resistance pattern of isolated microorganisms. The data of isolates originating from routine diagnostic tasks were analyzed retrospectively using laboratory data from the microbiology department. Up to 39.11% of Staphylococcus aureus strains were resistant to oxacillin (MRSA), with 49.97% resistance to erythromycin and 36.06% inducible resistance to clindamycin. Resistance rates to ciprofloxacin, rifampicin, gentamicin, and trimethoprim-sulfamethoxazole were 9.98%, 5.38%, 5.95%, and 0.96%, respectively. There was no resistance to vancomycin. Between 2017 and 2022, the percentage of MRSA strains decreased from 41.71% to 33.63%, sharply increasing to 42.42% in 2021 (the year of the COVID-19 pandemic, when the percentage of strains isolated from lower respiratory tract infections was higher than that of strains isolated from wounds or blood, as in previous years). This study showed a high percentage of MRSA strains (39.11% overall) with a higher proportion of these strains isolated from the blood (42.49%) compared to other clinical specimens.<\/jats:p>","DOI":"10.3390\/antibiotics12060974","type":"journal-article","created":{"date-parts":[[2023,5,28]],"date-time":"2023-05-28T15:30:47Z","timestamp":1685287847000},"page":"974","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":43,"title":["Antimicrobial Resistance of Staphylococcus aureus Isolated between 2017 and 2022 from Infections at a Tertiary Care Hospital in Romania"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5202-8417","authenticated-orcid":false,"given":"Daniela","family":"T\u0103l\u0103pan","sequence":"first","affiliation":[{"name":"Microbiology Department I, Faculty of Medicine, \u201cCarol Davila\u201d University of Medicine and Pharmacy, 050474 Bucharest, Romania"},{"name":"\u201cProf. Dr. Matei Bal\u0219\u201d National Institute of Infectious Diseases, 021105 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreea-Mihaela","family":"Sandu","sequence":"additional","affiliation":[{"name":"\u201cProf. Dr. Matei Bal\u0219\u201d National Institute of Infectious Diseases, 021105 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexandru","family":"Rafila","sequence":"additional","affiliation":[{"name":"Microbiology Department I, Faculty of Medicine, \u201cCarol Davila\u201d University of Medicine and Pharmacy, 050474 Bucharest, Romania"},{"name":"\u201cProf. Dr. Matei Bal\u0219\u201d National Institute of Infectious Diseases, 021105 Bucharest, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nrmicro2200","article-title":"Waves of resistance: Staphylococcus aureus in the antibiotic era","volume":"7","author":"Chambers","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","first-page":"e8867","article-title":"Understanding the Fight Against Resistance: Hospital-Acquired Methicillin-Resistant Staphylococcus aureus vs. Community-Acquired Methicillin-Resistant Staphylococcus aureus","volume":"12","author":"Tsouklidis","year":"2020","journal-title":"Cureus"},{"key":"ref_3","first-page":"280","article-title":"Antibiotic Resistance Pattern of Staphylococcus aureus Isolated from Nostrils of Healthy Undergraduates of Madonna University Elele Campus, Rivers State, Nigeria","volume":"2","author":"Onyeka","year":"2020","journal-title":"Microbes Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1128\/CMR.10.3.505","article-title":"Nasal carriage of Staphylococcus aureus: Epidemiology, underlying mechanisms, and associated risks","volume":"10","author":"Kluytmans","year":"1997","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/s13756-017-0203-2","article-title":"Prevalence and pattern of antibiotic resistance of Staphylococcus aureus isolated from door handles and other points of contact in public hospitals in Ghana","volume":"6","author":"Saba","year":"2017","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1111\/j.1469-0691.2004.01002.x","article-title":"Antibiotic resistance in Staphylococcus aureus colonising the intestines of Swedish infants","volume":"10","author":"Lindberg","year":"2004","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"FSO464","DOI":"10.2144\/fsoa-2019-0122","article-title":"Antibiotic resistance pattern of Staphylococcus aureus with reference to MRSA isolates from pediatric patients","volume":"6","author":"Gurung","year":"2020","journal-title":"Futur. Sci. OA"},{"key":"ref_8","unstructured":"CDC (2022). COVID-19: U.S. Impact on Antimicrobial Resistance, Special Report 2022."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.2147\/RMHP.S261311","article-title":"Antimicrobial Resistance of Staphylococcus aureus Isolated from Hospital Wastewater in Kermanshah, Iran","volume":"13","author":"Akya","year":"2020","journal-title":"Risk Manag. Health Policy"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e2208378119","DOI":"10.1073\/pnas.2208378119","article-title":"Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus: Combining antimicrobial photodynamic and antibiotic treatments","volume":"119","author":"Willis","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/j.1469-0691.2006.01343.x","article-title":"The importance of the development of antibiotic resistance in Staphylococcus aureus","volume":"12","author":"Schito","year":"2006","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.molcel.2015.10.019","article-title":"Blast from the Past: Reassessing Forgotten Translation Inhibitors, Antibiotic Selectivity, and Resistance Mechanisms to Aid Drug Development","volume":"61","author":"Arenz","year":"2016","journal-title":"Mol. Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40360-017-0141-x","article-title":"Antimicrobial resistance profile of Staphylococcus aureus isolates isolated from ear discharges of patients at University of Hawassa comprehensive specialized hospital","volume":"18","author":"Deyno","year":"2017","journal-title":"BMC Pharmacol. Toxicol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1111\/tmi.12692","article-title":"Characterisation of clinical Staphylococcus aureus isolates harbouring mecA or Panton-Valentine leukocidin genes from four tertiary care hospitals in Indonesia","volume":"21","author":"Santosaningsih","year":"2016","journal-title":"Trop. Med. Int. Health"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.tim.2013.11.003","article-title":"The emergence of mecC methicillin-resistant Staphylococcus aureus","volume":"22","author":"Paterson","year":"2013","journal-title":"Trends Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Mlynarczyk-Bonikowska, B., Kowalewski, C., Krolak-Ulinska, A., and Marusza, W. (2022). Molecular Mechanisms of Drug Resistance in Staphylococcus aureus. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158088"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"a026989","DOI":"10.1101\/cshperspect.a026989","article-title":"Approved Glycopeptide Antibacterial Drugs: Mechanism of Action and Resistance","volume":"6","author":"Zeng","year":"2016","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1128\/AAC.05702-11","article-title":"Resistance to Linezolid Caused by Modifications at Its Binding Site on the Ribosome","volume":"56","author":"Long","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1146\/annurev-biochem-062917-011942","article-title":"Ribosome-Targeting Antibiotics: Modes of Action, Mechanisms of Resistance, and Implications for Drug Design","volume":"87","author":"Zhou","year":"2018","journal-title":"Annu. Rev. Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1097\/QCO.0000000000000813","article-title":"Methicillin-resistant Staphylococcus aureus lung infection in coronavirus disease 2019: How common?","volume":"35","author":"Bassetti","year":"2022","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Alshaikh, F.S., Godman, B., Sindi, O.N., Seaton, R.A., and Kurdi, A. (2022). Prevalence of bacterial coinfection and patterns of antibiotics prescribing in patients with COVID-19: A systematic review and meta-analysis. PLoS ONE, 17.","DOI":"10.1101\/2022.03.02.22271779"},{"key":"ref_22","first-page":"1","article-title":"Decreased quality of care for Staphylococcus aureus bacteremia during the COVID-19 pandemic","volume":"22","author":"Beran","year":"2022","journal-title":"BMC Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1016\/j.cmi.2021.06.001","article-title":"The interface between COVID-19 and bacterial healthcare-associated infections","volume":"27","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12879-021-06616-4","article-title":"Clinical outcomes in patients co-infected with COVID-19 and Staphylococcus aureus: A scoping review","volume":"21","author":"Adalbert","year":"2021","journal-title":"BMC Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"405","DOI":"10.3390\/pathophysiology29030032","article-title":"Pathophysiology of Methicillin-Resistant Staphylococcus aureus Superinfection in COVID-19 Patients","volume":"29","author":"Habib","year":"2022","journal-title":"Pathophysiology"},{"key":"ref_26","unstructured":"CDC (2019). Antibiotic Resistance Threats in the United States."},{"key":"ref_27","unstructured":"European Centre for Disease Prevention and Control (2023, April 04). Surveillance Atlas of Infectious Diseases, Available online: http:\/\/atlas.ecdc.europa.eu\/public\/index.aspx."},{"key":"ref_28","first-page":"66","article-title":"Prevalence and characteristics of Staphylococcus aureus isolated from infections in Northeast Romania","volume":"14","author":"Dorneanu","year":"2006","journal-title":"J. Prev. Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1556\/AMicr.55.2008.1.1","article-title":"Incidence, antibiotic resistance and clonal relations of MRSA strains isolated from a Romanian university hospital","volume":"55","author":"Szekely","year":"2008","journal-title":"Acta Microbiol. et Immunol. Hung."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1089\/mdr.2010.0059","article-title":"Molecular Characterization and Antibiotic Susceptibility of Staphylococcus aureus from a Multidisciplinary Hospital in Romania","volume":"16","author":"Ionescu","year":"2010","journal-title":"Microb. Drug Resist."},{"key":"ref_31","first-page":"161","article-title":"Bacterial strains isolated from systemic infections and reported for evaluation and antibiotic resistance surveillance by the \u201cDr. Victor Babes\u201d Clinical Hospital for Infectious and Tropical Diseases, Bucharest","volume":"55","author":"Nica","year":"2010","journal-title":"Bacteriol. Virusol. Parazitol. Epidemiol."},{"key":"ref_32","first-page":"83","article-title":"Antibiotic resistance of Gram-positive cocci isolated in 2008","volume":"55","author":"Tenea","year":"2011","journal-title":"Bacteriol. Virusol. Parazitol. Epidemiol."},{"key":"ref_33","first-page":"1162","article-title":"MecA and pvl genes detection in Staphylococcus aureus strains isolated from lower respiratory tract infections","volume":"114","author":"Nastase","year":"2010","journal-title":"Rev. Med. Chir. Soc. Med. Nat. Iasi."},{"key":"ref_34","first-page":"139","article-title":"Bacterial infections in critically ill patients with SARS-2-COVID-19 infection: Results of a prospective observational multicenter study","volume":"50","author":"Corona","year":"2021","journal-title":"Infection"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2836","DOI":"10.1172\/JCI68834","article-title":"Mechanisms of vancomycin resistance in Staphylococcus aureus","volume":"124","author":"Gardete","year":"2014","journal-title":"J. Clin. Investig."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1093\/femsre\/fux007","article-title":"Antibiotic resistance in Staphylococcus aureus. Current status and future prospects","volume":"41","author":"Foster","year":"2017","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Bakthavatchalam, Y.D., Babu, P., Munusamy, E., Dwarakanathan, H.T., Rupali, P., Zervos, M., Victor, P.J., and Veeraraghavan, B. (2019). Genomic insights on heterogeneous resistance to vancomycin and teicoplanin in Methicillin-resistant Staphylococcus aureus: A first report from South India. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0227009"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1093\/jac\/dkg369","article-title":"Teicoplanin resistance in methicillin-resistant Staphylococcus aureus in an intensive care unit","volume":"52","author":"Cepeda","year":"2003","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2352","DOI":"10.1128\/AAC.00073-06","article-title":"In Vivo Survival of Teicoplanin-Resistant Staphylococcus aureus and Fitness Cost of Teicoplanin Resistance","volume":"50","author":"McCallum","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1093\/jac\/47.2.163","article-title":"In vivo emergence of subpopulations expressing teicoplanin or vancomycin resistance phenotypes in a glycopeptide-susceptible, methicillin-resistant strain of Staphylococcus aureus","volume":"47","author":"Vaudaux","year":"2001","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1186\/s13756-018-0397-y","article-title":"Characteristics of glycopeptide-resistant Staphylococcus aureus strains isolated from inpatients of three teaching hospitals in Warsaw, Poland","volume":"7","author":"Mlynarczyk","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"536","DOI":"10.3201\/eid0805.010387","article-title":"Emergence of Vancomycin-Intermediate Staphylococcus aureus and S. sciuri, Greece","volume":"8","author":"Tsakris","year":"2002","journal-title":"Emerg. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Cata\u00f1o-Correa, J.C., Cardona-Arias, J.A., Mancilla, J.P.P., and Garc\u00eda, M.T. (2021). Bacterial superinfection in adults with COVID-19 hospitalized in two clinics in Medell\u00edn-Colombia, 2020. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0254671"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"908","DOI":"10.3389\/fmicb.2020.00908","article-title":"Dynamic Changes of Staphylococcus aureus Susceptibility to Vancomycin, Teicoplanin, and Linezolid in a Central Teaching Hospital in Shanghai, China, 2008\u20132018","volume":"11","author":"Jian","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"728634","DOI":"10.3389\/fped.2021.728634","article-title":"Antibiotic Resistance Pattern of Staphylococcus aureus Isolated from Pediatrics with Ocular Infections: A 6-Year Hospital-Based Study in China","volume":"9","author":"Zheng","year":"2021","journal-title":"Front. Pediatr."},{"key":"ref_46","unstructured":"(2022, November 23). The European Committee on Antimicrobial Susceptibility Testing. Available online: https:\/\/www.eucast.org\/ast_of_bacteria."},{"key":"ref_47","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (2023, February 21). Breakpoint tables for interpretation of MICs and zone diameters. EUCAST, versions 7.1\u201312.0, 2017\u20132022. Available online: https:\/\/www.eucast.org\/ast_of_bacteria\/previous_versions_of_documents\/."},{"key":"ref_48","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (2022, May 09). EUCAST guidelines for detection of resistance mechanisms and specific resistance of clinical and\/or epidemiological importance. EUCAST, version 2.0, July 2017. Available online: https:\/\/www.eucast.org\/resistance_mechanisms\/."},{"key":"ref_49","unstructured":"EUCAST (2022, November 25). The European Committee on Antimicrobial Susceptibility Testing. Routine and Extended Internal Quality Control for MIC Determination and Disk Diffusion as Recommended by EUCAST, version 6.0\u201310.0, 2017\u20132022. Available online: http:\/\/www.eucast.org."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/6\/974\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:43:42Z","timestamp":1760125422000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/6\/974"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,28]]},"references-count":49,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["antibiotics12060974"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12060974","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,28]]}}}