{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T19:22:01Z","timestamp":1790709721116,"version":"4.1.0"},"reference-count":46,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,4,27]],"date-time":"2021-04-27T00:00:00Z","timestamp":1619481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Infected chronic venous ulcers (VUs) represent a major health problem. We analysed the aerobic microbiome in the VUs, the virulence, and drug-resistance of Staphylococcus aureus (SA) strains. Swabs from 143 outpatients and inpatients Polish subjects were collected. SA strains were tested for drug sensitivity using a phenotyping method and for methicillin-resistant SA (MRSA) and macrolide-lincosamide-streptogramin B (MLSB) resistance using PCR. We analysed virulence genes, the genetic similarity of strains, and performed Staphylococcal cassette chromosome mec typing and Staphylococcal protein A typing. SA was isolated as a single one in 34.9% of cases, 31.5% paired with another pathogen, and 33.6% S. aureus combined with at least two other strains. The majority of SA isolates (68.5%) possessed the virulence lukE gene. Drug resistance was significantly common in hospitalised than in ambulatory patients (OR 3.8; 95%CI 1.8\u20137.91). MLSB (altogether in 19.6% isolates) were observed mostly in non-hospitalised patients (OR 9.1; 95%CI 1.17\u201371.02), while MRSA was detected in 11.9% of strains equally. Hospitalisation and patient\u2019s age group (aged &gt; 78.0 or &lt; 54.5 years) were significant predictors of the multi-drug resistant SA (MDR-SA). Over 30% of the infected VUs were associated with multi-species biofilms and presence of potentially highly pathogenic microorganisms. Elderly hospitalised patients with chronic venous ulcers are prone to be infected with a MDR-SA.<\/jats:p>","DOI":"10.3390\/ijerph18094662","type":"journal-article","created":{"date-parts":[[2021,4,27]],"date-time":"2021-04-27T21:18:20Z","timestamp":1619558300000},"page":"4662","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Virulence and Drug-Resistance of Staphylococcus aureus Strains Isolated from Venous Ulcers in Polish Patients"],"prefix":"10.3390","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4383-7380","authenticated-orcid":false,"given":"Mateusz","family":"Gajda","sequence":"first","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Jagiellonian University Medical College, Jagiellonian University, 31-121 Krakow, Poland"},{"name":"Doctoral School of Medical Sciences and Health Sciences, Jagiellonian University Medical College, Jagiellonian University, 31-530 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5266-5395","authenticated-orcid":false,"given":"Emilia","family":"Za\u0142ugowicz","sequence":"additional","affiliation":[{"name":"Faculty of Biology, Jagiellonian University, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monika","family":"Pomorska-Weso\u0142owska","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Analytical and Microbiological Laboratory of Ruda \u015al\u0105ska KORLAB NZOZ, 41-703 Ruda \u015al\u0105ska, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomasz","family":"Bochenek","sequence":"additional","affiliation":[{"name":"Department of Nutrition and Drug Research, Faculty of Health Sciences, Jagiellonian University Medical College, Jagiellonian University, 31-066 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara","family":"Gryglewska","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine and Gerontology, Faculty of Medicine, Jagiellonian University Medical College, Jagiellonian University, 31-531 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dorota","family":"Romaniszyn","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Jagiellonian University Medical College, Jagiellonian University, 31-121 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agnieszka","family":"Chmielarczyk","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Jagiellonian University Medical College, Jagiellonian University, 31-121 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0756-1639","authenticated-orcid":false,"given":"Jadwiga","family":"W\u00f3jkowska-Mach","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Jagiellonian University Medical College, Jagiellonian University, 31-121 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"46S","DOI":"10.1016\/j.jvs.2010.05.124","article-title":"The definition of the venous ulcer","volume":"52","author":"Raffetto","year":"2010","journal-title":"J. Vasc. Surg."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1016\/j.jaad.2014.10.048","article-title":"What\u2019 s new: Management of venous leg ulcers Approach to venous leg ulcers","volume":"74","author":"Alavi","year":"2019","journal-title":"J. Am. Dermatol."},{"key":"ref_3","first-page":"1902","article-title":"Venous leg ulcers","volume":"2016","author":"Nelson","year":"2016","journal-title":"BMJ Clin. Evid."},{"key":"ref_4","first-page":"115","article-title":"Frequency and molecular epidemiology of Panton-Valentine leukocidin gene in Staphylococcus aureus colonising HIV-infected patients","volume":"39","author":"Adnan","year":"2017","journal-title":"Malays. J. Pathol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1855","DOI":"10.1136\/bmj.290.6485.1855","article-title":"Chronic ulceration of the leg: Extent of the problem and provision of care","volume":"290","author":"Callam","year":"1987","journal-title":"Br. Med. J."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1177\/000331979704800111","article-title":"Socioeconomic impact of chronic venous insufficiency and leg ulcers","volume":"48","author":"Ruckley","year":"1997","journal-title":"Angiology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s41038-018-0119-y","article-title":"The venous ulcer continues to be a clinical challenge: An update","volume":"6","author":"Xie","year":"2018","journal-title":"Burn. Trauma"},{"key":"ref_8","first-page":"59","article-title":"Wytyczne Grupy Ekspert\u00f3w w sprawie gojenia owrzodze\u0144 \u017cylnych goleni","volume":"8","author":"Szewczyk","year":"2011","journal-title":"Leczenie Ran"},{"key":"ref_9","first-page":"35","article-title":"Venous thromboembolism\u2014recommendations on the prevention, diagnostic approach and management. The 2017 Polish Consensus Statement","volume":"23","author":"Tomkowski","year":"2017","journal-title":"Acta Angiol."},{"key":"ref_10","unstructured":"Bryant, R.A. (2000). Acute and Chronic Wounds, Mosby. [2nd ed.]."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Agale, S.V. (2013). Chronic Leg Ulcers: Epidemiology, Aetiopathogenesis, and Management. Ulcers, 1\u20139.","DOI":"10.1155\/2013\/413604"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1016\/S1473-3099(05)70295-4","article-title":"The role of nasal carriage in Staphylococcus aureus infections","volume":"5","author":"Wertheim","year":"2005","journal-title":"Lancet Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1007\/s00248-016-0867-9","article-title":"Bacterial Contribution in Chronicity of Wounds","volume":"73","author":"Rahim","year":"2016","journal-title":"Microb. Ecol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/j.bjm.2017.09.003","article-title":"Epidemiology of diabetic foot infections in a reference tertiary hospital in India","volume":"49","author":"Saseedharan","year":"2018","journal-title":"Braz. J. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Dunyach-Remy, C., Essebe, C.N., Sotto, A., and Lavigne, J.P. (2016). Staphylococcus aureus toxins and diabetic foot ulcers: Role in pathogenesis and interest in diagnosis. Toxins, 8.","DOI":"10.3390\/toxins8070209"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4061\/2011\/601905","article-title":"Characterization of Virulence Factors of Staphylococcus aureus: Novel Function of Known Virulence Factors That are Implicated in Activation of Airway Epithelial Proinflammatory Response","volume":"2011","author":"Bien","year":"2011","journal-title":"J. Pathog."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Wojkowska-Mach, J., Godman, B., Glassman, A., Kurdi, A., Pilc, A., Rozanska, A., Skoczy\u0144ski, S., Wa\u0142aszek, M., and Bochenek, T. (2018). Antibiotic consumption and antimicrobial resistance in Poland; Findings and implications 11 Medical and Health Sciences 1117 Public Health and Health Services. Antimicrob. Resist. Infect. Control, 7.","DOI":"10.1186\/s13756-018-0428-8"},{"key":"ref_18","unstructured":"ECDC. European Center for Disease Control and Prevention (2017, August 16). Annual Surveillance Reports and Protocols-Antimicrobial Consumption. Available online: https:\/\/ecdc.europa.eu\/en\/antimicrobial-consumption\/surveillance-anddisease-%0Adata\/report-protocol."},{"key":"ref_19","first-page":"1","article-title":"Longevity and gender as the risk factors of methicillin-resistant Staphylococcus aureus infections in southern Poland","volume":"17","author":"Natkaniec","year":"2017","journal-title":"BMC Geriatr."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/j.micres.2009.03.003","article-title":"Staphylococcus aureus, Staphylococcus epidermidis and Staphylococcus haemolyticus: Methicillin-resistant isolates are detected directly in blood cultures by multiplex PCR","volume":"165","author":"Pereira","year":"2010","journal-title":"Microbiol. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2562","DOI":"10.1128\/AAC.40.11.2562","article-title":"Detection of erythromycin-resistant determinants by PCR","volume":"40","author":"Sutcliffe","year":"1996","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1007\/s100960050222","article-title":"Use of the polymerase chain reaction for rapid detection of high-level mupirocin resistance in staphylococci","volume":"18","author":"Anthony","year":"1999","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"5113","DOI":"10.1128\/JCM.41.11.5113-5120.2003","article-title":"Pulsed-Field Gel Electrophoresis Typing of Oxacillin-Resistant Staphylococcus aureus Isolates from the United States: Establishing a National Database","volume":"41","author":"Mcdougal","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.1086\/644732","article-title":"Topical Antimicrobial Therapy for Treating Chronic Wounds","volume":"49","author":"Lipsky","year":"2009","journal-title":"Clin. Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/s40266-016-0343-8","article-title":"Infection in Venous Leg Ulcers: Considerations for Optimal Management in the Elderly","volume":"33","author":"Pugliese","year":"2016","journal-title":"Drugs Aging"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0042897","article-title":"Comparative analysis of single-species and polybacterial wound biofilms using a quantitative, in vivo, rabbit ear model","volume":"7","author":"Seth","year":"2012","journal-title":"PLoS ONE"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1111\/iwj.12230","article-title":"Recent accomplishments in wound healing","volume":"12","author":"Mudge","year":"2015","journal-title":"Int. Wound J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1111\/j.1365-2133.2010.09804.x","article-title":"Oxygen in acute and chronic wound healing","volume":"163","author":"Schreml","year":"2010","journal-title":"Br. J. Dermatol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1111\/j.1524-475X.2007.00321.x","article-title":"Biofilms in chronic wounds","volume":"16","author":"James","year":"2008","journal-title":"Wound Repair Regen."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1089\/mdr.2015.0224","article-title":"Molecular Epidemiology and Drug Resistance of Acinetobacter baumannii Isolated from Hospitals in Southern Poland: ICU as a Risk Factor for XDR Strains","volume":"22","author":"Chmielarczyk","year":"2016","journal-title":"Microb. Drug Resist."},{"key":"ref_31","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_32","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1017\/ice.2018.183","article-title":"The preventable proportion of healthcare-associated infections 2005\u20132016: Systematic review and meta-analysis","volume":"39","author":"Schreiber","year":"2018","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_33","unstructured":"Olczak-Pie\u0144kowska, A. (2020, June 15). Podsumowanie Aktualnych Danych nt. Konsumpcji Antybiotyk\u00f3w w Krajach unii Europejskiej\u2013Dane Europejskiej Sieci Monitorowania Konsumpcji Antybiotyk\u00f3w ESAC-Net (listopad 2017) Zak\u0142ad Epidemiologii i Mikrobiologii Klinicznej, Narodowy Instytut Lek\u00f3w, Warszawa. Available online: http:\/\/antybiotyki.edu.pl\/wp-content\/uploads\/Biuletyn\/biuletyn-npoa-2018_1.pdf."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.ijid.2015.05.002","article-title":"Evaluation of spa-typing of methicillin-resistant Staphylococcus aureus using high-resolution melting analysis","volume":"38","author":"Mazi","year":"2015","journal-title":"Int. J. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"20380","DOI":"10.2807\/ese.18.04.20380-en","article-title":"Overview of molecular typing methods for outbreak detection and epi-demiological surveillance","volume":"18","author":"Sabat","year":"2013","journal-title":"Euro. Surveill."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Go-pal Rao, G., Batura, R., Nicholl, R., Coogan, F., Patel, B., Bassett, P., and Kearns, A.M. (2019). Outbreak re-port of investigation and control of an outbreak of Panton-Valentine Leukocidin-positive methicillin-sensitive Staphylococcus aureus (PVL-MSSA) infection in neo-nates and mothers. BMC Infect. Dis., 19.","DOI":"10.1186\/s12879-019-3802-0"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.jhin.2016.10.024","article-title":"Molecular analysis of meticillin-resistant Staphylococcus aureus strains isolated from different types of infections from patients hospitalized in 12 regional, non-teaching hospitals in southern Poland","volume":"95","author":"Chmielarczyk","year":"2017","journal-title":"J. Hosp. Infect."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1002\/(SICI)1096-9136(199602)13:2<156::AID-DIA59>3.0.CO;2-U","article-title":"Antibiotic treatment for uncomplicated neuropathic forefoot ulcers in diabetes: A controlled trial","volume":"13","author":"Chantelau","year":"1996","journal-title":"Diabet. Med."},{"key":"ref_39","first-page":"1","article-title":"Ulcer healing time and antibiotic treatment before and after the introduction of the Registry of Ulcer Treatment: An improvement project in a national quality registry in Sweden","volume":"3","author":"Forssell","year":"2013","journal-title":"BMJ Open"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1111\/wrr.12590","article-title":"Consensus guidelines for the identification and treatment of biofilms in chronic nonhealing wounds","volume":"25","author":"Schultz","year":"2017","journal-title":"Wound Repair Regen."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1111\/j.1743-6109.2006.00162.x","article-title":"Diagnostic validity of three swab techniques for identifying chronic wound infection","volume":"14","author":"Gardner","year":"2006","journal-title":"Wound Repair Regen."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1046\/j.1464-5491.2001.00584.x","article-title":"Deep tissue biopsy vs. superficial swab culture monitoring in the microbiological assessment of limb-threatening diabetic foot infection","volume":"18","author":"Pellizzer","year":"2001","journal-title":"Diabet. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1111\/j.1742-481X.2010.00747.x","article-title":"Assessing bacterial burden in wounds: Comparing clinical observation and wound swabs","volume":"8","author":"Miller","year":"2011","journal-title":"Int. Wound J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"959","DOI":"10.12968\/bjon.2003.12.16.11437","article-title":"Reliability in Wound Swabbing","volume":"12","author":"Kelly","year":"2003","journal-title":"Br. J. Nurs."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"776","DOI":"10.1111\/iwj.12926","article-title":"Role of anaerobes in polymicrobial communities and biofilms complicating diabetic foot ulcers","volume":"15","author":"Percival","year":"2018","journal-title":"Int. Wound J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1111\/j.1524-475X.2011.00720.x","article-title":"The importance of a multifaceted approach to characterizing the microbial flora of chronic wounds","volume":"19","author":"Han","year":"2011","journal-title":"Wound Repair Regen."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/18\/9\/4662\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:53:32Z","timestamp":1760162012000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/18\/9\/4662"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,27]]},"references-count":46,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["ijerph18094662"],"URL":"https:\/\/doi.org\/10.3390\/ijerph18094662","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,27]]}}}