{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T05:30:21Z","timestamp":1790314221109,"version":"4.1.0"},"reference-count":37,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,4,25]],"date-time":"2025-04-25T00:00:00Z","timestamp":1745539200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science, Technological Development and Innovation of the Republic of Serbia","award":["451-03-137\/2025-03\/200113"],"award-info":[{"award-number":["451-03-137\/2025-03\/200113"]}]},{"name":"Ministry of Science, Technological Development and Innovation of the Republic of Serbia","award":["7754282"],"award-info":[{"award-number":["7754282"]}]},{"name":"Science Fund of the Republic of Serbia","award":["451-03-137\/2025-03\/200113"],"award-info":[{"award-number":["451-03-137\/2025-03\/200113"]}]},{"name":"Science Fund of the Republic of Serbia","award":["7754282"],"award-info":[{"award-number":["7754282"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JoF"],"abstract":"<jats:p>Background: Superficial candidiasis (SC) is widespread in humans worldwide. This study aimed to evaluate species distribution patterns and antifungal susceptibility through cluster analysis. Methods: A total of 180 Candida strains isolated from skin and nail samples of 1593 examined patients with suspected superficial fungal infection were identified by Matrix-assisted laser desorption in ionization-time of flight mass spectrometry (MALDI-TOF MS; Zybio EXS2600, China). Antifungal susceptibility was assessed using the commercial Integral System YEASTS Plus test (ISYPT; Liofilchem\u00ae, Italy). Agglomerative hierarchical cluster analysis was used to analyze species distribution and susceptibility. Results: Candida parapsilosis (44.4%) and C. albicans (40%) were the most prevalent causative agents of SC. Cluster analysis established two defined clusters. Cluster 1 (121 isolates) showed a statistically significant difference compared to Cluster 2 (54 isolates) in species distribution (C. albicans was dominant in the first and C. parapsilosis in the second cluster) as well as in susceptibility to ECN (p \u2264 0.001), KCA (p = 0.030), CLO (p \u2264 0.001), MCZ (p \u2264 0.001), ITZ (p \u2264 0.001), and FLU (p \u2264 0.006). Conclusion: The fact that one-third of isolates exhibited low sensitivity to antifungals highlights the need for a new approach in SC treatment, emphasizing the importance of mycological analyses, including in vitro testing of antifungal effectiveness.<\/jats:p>","DOI":"10.3390\/jof11050338","type":"journal-article","created":{"date-parts":[[2025,4,25]],"date-time":"2025-04-25T08:02:57Z","timestamp":1745568177000},"page":"338","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Superficial Candidiasis: Cluster Analysis of Species Distribution and Their Antifungal Susceptibility In Vitro"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9945-0332","authenticated-orcid":false,"given":"Marina","family":"Ran\u0111elovi\u0107","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, Medical Faculty, University of Ni\u0161, 18000 Ni\u0161, Serbia"},{"name":"Centre of Microbiology, Public Health Institute Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2689-8088","authenticated-orcid":false,"given":"Aleksandra","family":"Ignjatovi\u0107","sequence":"additional","affiliation":[{"name":"Department of Medical Statistics and Informatics, Medical Faculty, University of Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Milica","family":"\u0110or\u0111evi\u0107","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Medical Faculty, University of Ni\u0161, 18000 Ni\u0161, Serbia"},{"name":"Centre of Microbiology, Public Health Institute Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ma\u0161a","family":"Golubovi\u0107","sequence":"additional","affiliation":[{"name":"Department of Dermatology, Clinical Center, University of Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5733-5499","authenticated-orcid":false,"given":"Marko","family":"Stalevi\u0107","sequence":"additional","affiliation":[{"name":"Department of Physiology, Medical Faculty, University of Pri\u0161tina\u2014Kosovska Mitrovica, 38000 Kosovska Mitrovica, Serbia"},{"name":"Doctoral Studies, Faculty of Medicine, University of Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8472-9282","authenticated-orcid":false,"given":"Nata\u0161a","family":"Ran\u010di\u0107","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, Medical Faculty, University of Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3377-9247","authenticated-orcid":false,"given":"Suzana","family":"Ota\u0161evi\u0107","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Medical Faculty, University of Ni\u0161, 18000 Ni\u0161, Serbia"},{"name":"Centre of Microbiology, Public Health Institute Ni\u0161, 18000 Ni\u0161, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1111\/j.1439-0507.2008.01606.x","article-title":"Epidemiological trends in skin mycoses worldwide","volume":"51","author":"Havlickova","year":"2008","journal-title":"Mycoses"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1111\/myc.12900","article-title":"Species distribution and epidemiological characteristics of superficial fungal infections in Southeastern Serbia","volume":"62","author":"Hay","year":"2019","journal-title":"Mycoses"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"ofac559","DOI":"10.1093\/ofid\/ofac559","article-title":"Fungal nomenclature: Managing change is the name of the game","volume":"10","author":"Kidd","year":"2023","journal-title":"Open Forum Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e375","DOI":"10.1016\/S1473-3099(21)00203-6","article-title":"Global guideline for the diagnosis and management of rare yeast infections: An initiative of the ECMM in cooperation with ISHAM and ASM","volume":"21","author":"Chen","year":"2021","journal-title":"Lancet Infect. Dis."},{"key":"ref_5","first-page":"414","article-title":"Superficial Fungal Infection","volume":"Volume 3","author":"Rezaei","year":"2022","journal-title":"Encyclopedia of Infection and Immunity"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1007\/s11046-017-0228-3","article-title":"Isolated cutaneous granuloma caused by Candida glabrata: A rare case report and literature review","volume":"183","author":"Fan","year":"2018","journal-title":"Mycopathologia"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1007\/BF02815627","article-title":"Cutaneous candidosis in immunosuppressed patients","volume":"46","author":"Dorko","year":"2001","journal-title":"Folia Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1016\/j.jaad.2010.09.730","article-title":"Onychomycosis: A proposed revision of the clinical classification","volume":"65","author":"Hay","year":"2011","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/s11046-009-9212-x","article-title":"Candidal onychomycosis: A mini-review","volume":"168","author":"Jayatilake","year":"2009","journal-title":"Mycopathologia"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/s40257-018-0403-4","article-title":"A practical guide to curing onychomycosis: How to maximize cure at the patient, organism, treatment, and environmental level","volume":"20","author":"Gupta","year":"2019","journal-title":"Am. J. Clin. Dermatol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/j.mycmed.2018.03.001","article-title":"Non-culture based assays for the detection of fungal pathogens","volume":"28","year":"2018","journal-title":"J. Mycol. Medicale"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Tian, P.-P., Su, S.-S., Zhu, L.-S., Wang, T., Yang, H., Du, M.-Y., Ding, C.-Z., Wang, L., Fan, W., and Yi, H.-W. (2024). Short-term culture for rapid identification by mass spectrometry and automated antimicrobial susceptibility testing from positive bottles. BMC Infect. Dis., 24.","DOI":"10.1186\/s12879-024-09475-x"},{"key":"ref_13","unstructured":"PA, W. (2008). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts, Clinical and Laboratory Standards Institute. [3rd ed.]. CLSI document M27."},{"key":"ref_14","unstructured":"R Development Core Team (2025, April 22). R: A Language and Environment for Statistical Computing. Available online: http:\/\/www.R-project.org."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e23850","DOI":"10.1002\/jcla.23850","article-title":"Prevalence of superficial-cutaneous fungal infections in Shiraz, Iran: A five-year retrospective study (2015\u20132019)","volume":"35","author":"Khodadadi","year":"2021","journal-title":"J. Clin. Lab. Anal."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Bilal, H., Hou, B., Shafiq, M., Chen, X., Shahid, M.A., and Zeng, Y. (2022). Antifungal susceptibility pattern of Candida isolated from cutaneous candidiasis patients in eastern Guangdong region: A retrospective study of the past 10 years. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.981181"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1007\/s42770-019-00096-0","article-title":"Mycoses in northeastern Brazil: Epidemiology and prevalence of fungal species in 8 years of retrospective analysis in Alagoas","volume":"50","author":"Silva","year":"2019","journal-title":"Braz. J. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ran\u0111elovi\u0107, M., Dimitrijevi\u0107, M., Ota\u0161evi\u0107, S., Stanojevi\u0107, L., I\u0161ljamovi\u0107, M., Ignjatovi\u0107, A., Arsi\u0107-Arsenijevi\u0107, V., and Stojanovi\u0107-Radi\u0107, Z. (2023). Antifungal activity and type of interaction of Melissa officinalis essential oil with antimycotics against biofilms of multidrug-resistant candida isolates from vulvovaginal mucosa. J. Fungi, 9.","DOI":"10.3390\/jof9111080"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Talapko, J., Juzba\u0161i\u0107, M., Matijevi\u0107, T., Pustijanac, E., Beki\u0107, S., Kotris, I., and \u0160krlec, I. (2021). Candida albicans\u2014The virulence factors and clinical manifestations of infection. J. Fungi, 7.","DOI":"10.3390\/jof7020079"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.mycmed.2017.12.008","article-title":"Emergence of non-Candida albicans species: Epidemiology, phylogeny and fluconazole susceptibility profile","volume":"28","author":"Sadeghi","year":"2018","journal-title":"J. Mycol. Medicale"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1590\/S0365-05962004000600005","article-title":"Identification of Candida species and antifungal susceptibility in vitro: A study on 100 patients with superficial candidiasis","volume":"79","author":"Crocco","year":"2004","journal-title":"An. Bras. Dermatol."},{"key":"ref_22","first-page":"290","article-title":"Distribution and antifungal susceptibility profiles of candida species isolated from dermatomycosis patients","volume":"7","author":"Kaya","year":"2024","journal-title":"J. Health Sci. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1111\/jdv.12151","article-title":"Identification and antifungal susceptibility of fungi isolated from dermatomycoses","volume":"28","author":"Silva","year":"2014","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_24","first-page":"678","article-title":"S1 Guideline onychomycosis","volume":"21","author":"Nenoff","year":"2023","journal-title":"JDDG J. Dtsch. Dermatol. Ges."},{"key":"ref_25","first-page":"s165","article-title":"Optimizing topical antifungal therapy for superficial cutaneous fungal infections: Focus on topical naftifine for cutaneous dermatophytosis","volume":"12","author":"Kircik","year":"2013","journal-title":"J. Drugs Dermatol. JDD"},{"key":"ref_26","first-page":"s49","article-title":"Mycological Considerations in the Topical Treatment of Superficial Fungal Infections","volume":"15","author":"Rosen","year":"2016","journal-title":"J. Drugs Dermatol. JDD"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1863","DOI":"10.1111\/jdv.15782","article-title":"Cutaneous candidiasis\u2013an evidence-based review of topical and systemic treatments to inform clinical practice","volume":"33","author":"Taudorf","year":"2019","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_28","unstructured":"Tumietto, F., and Giacomelli, L. (2017). Fenticonazole: An effective topical treatment for superficial mycoses as the first-step of antifungal stewardship program. Eur. Rev. Med. Pharmacol. Sci., 21."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Bojanovi\u0107, M., Ignjatovi\u0107, A., Stalevi\u0107, M., Arsi\u0107-Arsenijevi\u0107, V., Ran\u0111elovi\u0107, M., Gergini\u0107, V., Stojanovi\u0107-Radi\u0107, Z., Stojkovi\u0107, O., \u017divkovi\u0107-Marinkov, E., and Ota\u0161evi\u0107, S. (2022). Clinical presentations, cluster analysis and laboratory-based investigation of Aspergillus otomycosis\u2014A single center experience. J. Fungi, 8.","DOI":"10.3390\/jof8030315"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Stalevi\u0107, M., Ignjatovi\u0107, A., Ran\u0111elovi\u0107, M., Dimitrijevi\u0107, J., and Ota\u0161evi\u0107, S. (2023). Risk factors and cluster analysis of onychomycosis. Acta Medica Median., 62.","DOI":"10.5633\/amm.2023.0404"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Ignjatovi\u0107, A., Arsi\u0107-Arsenijevi\u0107, V., Golubovi\u0107, M., \u0110eni\u0107, S., Mom\u010dilovi\u0107, S., Trajkovi\u0107, A., Ran\u0111elovi\u0107, M., \u0106iri\u0107, V., and Ota\u0161evi\u0107, S. (2020). Recurrent vulvovaginal candidosis and cluster analysis of clinical signs and symptoms: A laboratory-based investigation. J. Fungi, 6.","DOI":"10.3390\/jof6030113"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e20190214","DOI":"10.1590\/0037-8682-0214-2019","article-title":"Relationship between antifungal susceptibility profile and virulence factors in Candida albicans isolated from nail specimens","volume":"53","author":"Mohammadi","year":"2020","journal-title":"Rev. Soc. Bras. Med. Trop."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/s11046-020-00509-x","article-title":"Virulence factors and antifungal susceptibility in Candida species isolated from dermatomycosis patients","volume":"186","author":"Mello","year":"2021","journal-title":"Mycopathologia"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"7","DOI":"10.18869\/acadpub.cmm.1.4.7","article-title":"In vitro activity of econazole in comparison with three common antifungal agents against clinical Candida strains isolated from superficial infections","volume":"1","author":"Abastabar","year":"2015","journal-title":"Curr. Med. Mycol."},{"key":"ref_35","first-page":"32","article-title":"Onychomycosis-causing yeasts in four Mexican dermatology centers and their antifungal susceptibility to azolic compounds","volume":"28","author":"Arenas","year":"2010","journal-title":"Rev. Iberoam. Micol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.riam.2017.05.001","article-title":"Current status of the etiology of candidiasis in Mexico","volume":"34","year":"2017","journal-title":"Rev. Iberoam. Micol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"K\u00fchbacher, A., Burger-Kentischer, A., and Rupp, S. (2017). Interaction of Candida species with the skin. Microorganisms, 5.","DOI":"10.3390\/microorganisms5020032"}],"container-title":["Journal of Fungi"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2309-608X\/11\/5\/338\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:21:34Z","timestamp":1760030494000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2309-608X\/11\/5\/338"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4,25]]},"references-count":37,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["jof11050338"],"URL":"https:\/\/doi.org\/10.3390\/jof11050338","relation":{},"ISSN":["2309-608X"],"issn-type":[{"value":"2309-608X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,4,25]]}}}