Research Article
Makyaj Süngerlerinden İzole Edilen Candida parapsilosis İzolatlarının Antifungal Dirençliliği ve Biyofilm Oluşturma Kapasitelerinin Belirlenmesi
Abstract
Candida parapsilosis, insan derisini ve mukoza zarlarını kolonize edebilen, biyofilm oluşturma yeteneği nedeniyle antifungal tedavilere direnç geliştirebilen fırsatçı bir patojendir. Bu çalışmada makyaj süngerlerinden izole edilen Candida parapsilosis izolatlarının antifungal dirençlilikleri ve biyofilm oluşturma kapasiteleri araştırılmıştır. 46 Candida parapsilosis izolatı arasındaki biyofilm oluşturma kapasiteleri kristal viyole kantitatif yöntemi kullanılarak belirlenmiştir. İzolatlardaki amfoterisin B direnci agar disk difüzyon yöntemi kullanılarak değerlendirilmiştir. Biyofilm üreten türlerin antifungal dirençlilikleri ise gradyan test yöntemi ile değerlendirilmiştir. Kristal viyole analizi sonucunda, izolatların çoğunun zayıf biyofilm üreticisi olduğu 17 izolatın ise orta düzeyde biyofilm üreticisi olduğu belirlendi. Agar disk difüzyon yöntemiyle amfoterisin B'ye karşı izolatların 19,73 ± 1,54 mm ile 23,71 ± 0,70 mm arasında inhibisyon zonu verdiği tespit edildi. Orta düzeyde biyofilm üreticisi olan 17 izolatın ise flukonazol, itrakonazol, klotrimazol, amfoterisin B ve nistatin antifungallerine duyarlı olduğu belirlendi. Çalışmada, makyaj süngerlerinin Candida parapsilosis için rezervuar görevi görebileceğini ve biyofilm oluşturan izolatların antifungal duyarlılığının değerlendirilmesinin önemini vurgulamaktadır. Bu bulgular, kişisel bakım ürünlerinin hijyenik kullanımı ve enfeksiyon kontrol önlemlerinin uygulanması açısından önemlidir.
References
- Agi, V. N., Ollor, O. A., Azike, C. A., and Onwuasoanya, C. V. (2023). Isolation and identification of microorganisms from makeup brushes in Rivers State University Nigeria and its environs. J Adv Microbiol, 23(3), 41-50. DOI: 10.9734/JAMB/2023/v23i3715
- Akgül, Ö., and Bakan, K. (2021). The aerobic bacteria isolated from used cosmetic products and evaluation of antibiotic resistance. Journal of Faculty of Pharmacy of Ankara University, 45(2), 156-168. https://doi.org/10.33483/jfpau.850561
- Arastehfar, A., Daneshnia, F., Najafzadeh, M. J., Hagen, F., Mahmoudi, S., Salehi, M., Zarrinfar, H., Namvar, Z., Zareshahrabadi, Z., Khodavaisy, S., Zomorodian, K., Pan, W., Theelen, B., Kostrzewa, M., Boekhout, T., and Lass-Flörl, C. (2020). Evaluation of molecular epidemiology, clinical characteristics, antifungal susceptibility profiles, and molecular mechanisms of antifungal resistance of Iranian Candida parapsilosis species complex blood isolates. Frontiers in Cellular and Infection Microbiology, 10, 206. https://doi.org/10.3389/fcimb.2020.00206
- Bashir, A., and Lambert, P. (2020). Microbiological study of used cosmetic products: highlighting possible impact on consumer health. Journal of Applied Microbiology, 128(2), 598-605. https://doi.org/10.1111/jam.14479
- Branco, J., Miranda, I. M., and Rodrigues, A. G. (2023). Candida parapsilosis virulence and antifungal resistance mechanisms: a comprehensive review of key determinants. Journal of Fungi, 9(1), 80. https://doi.org/10.3390/jof9010080
- CLSI, (2002). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard—Second Edition. NCCLS document M27-A2 [ISBN 1-56238-469-4]. NCCLS, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898 USA.
- CLSI, (2004). Method for Antifungal Disk Diffusion Susceptibility Testing of Yeasts; Approved Guideline. NCCLS document M44-A [ISBN 1-56238-532-1]. NCCLS, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898 USA.
- Colombo, A. L., de Almeida Júnior, J. N., and Guinea, J. (2017). Emerging multidrug-resistant Candida species. Current Opinion in Infectious Diseases, 30(6), 528-538. https://doi.org/10.1097/QCO.0000000000000411
- Daneshnia, F., de Almeida Júnior, J. N., Ilkit, M., Lombardi, L., Perry, A. M., Gao, M., Nobile, C. J., Egger, M., Perlin, D.S., Zhai, B., Hohl, T. M., Gabaldón, T., Colombo, A. L., Hoenigl, M., and Arastehfar, A. (2023). Worldwide emergence of fluconazole-resistant Candida parapsilosis: current framework and future research roadmap. The Lancet Microbe, 4(6), e470-e480. https://doi.org/10.1016/S2666-5247(23)00067-8
- de Paula Menezes, R., de Oliveira Melo, S. G., Bessa, M. A. S., Silva, F. F., Alves, P. G. V., Araújo, L. B., Penatti, M. P. A., Abdallah, O. S., de Brito Röder, D. V. D., and dos Santos Pedroso, R. (2020). Candidemia by Candida parapsilosis in a neonatal intensive care unit: Human and environmental reservoirs, virulence factors, and antifungal susceptibility. Brazilian Journal of Microbiology, 51, 851-860. https://doi.org/10.1007/s42770-020-00232-1
- Govrins, M., and Lass-Flörl, C. (2024). Candida parapsilosis complex in the clinical setting. Nature Reviews Microbiology, 22(1), 46-59. https://doi.org/10.1038/s41579-023-00961-8
- Grossman, N. T., Pham, C. D., Cleveland, A. A., and Lockhart, S. R. (2015). Molecular mechanisms of fluconazole resistance in Candida parapsilosis isolates from a US surveillance system. Antimicrobial agents and chemotherapy, 59(2), 1030-1037. https://doi.org/10.1128/aac.04613-14
- Melo, A. S., Bizerra, F. C., Freymüller, E., Arthington-Skaggs, B. A., and Colombo, A. L. (2011). Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Medical mycology, 49(3), 253-262.
- Miranda-Cadena, K., Marcos-Arias, C., Mateo, E., Aguirre, J. M., Quindós, G., and Eraso, E. (2018). Prevalence and antifungal susceptibility profiles of Candida glabrata, Candida parapsilosis and their close-related species in oral candidiasis. Archives of Oral Biology, 95, 100-107. https://doi.org/10.1016/j.archoralbio.2018.07.017
- Modiri, M., Khodavaisy, S., Barac, A., Dana, M. A., Nazemi, L., Aala, F., Salehi, M., and Rezaie, S. (2019). Comparison of biofilm-producing ability of clinical isolates of Candida parapsilosis species complex. Journal de mycologie medicale, 29(2), 140-146. https://doi.org/10.1016/j.mycmed.2019.02.003
- Ogbonna, S. I., Odu, N. N., Oparaodu, U. A., Robinson, V. K., and Ebenezer, A. (2024). Antibiogram of bacteria and fungi isolated from makeup kits in Port Harcourt metropolis. Microbiol. Res. Int, 12(2), 30-36. DOI: 10.30918/MRI.122.24.015
- Önal, P., Aygün, F. D., Sever, G. A., Eren, B. A., Kes, G., Aygün, F., Zübarioğlu, T., Beşer, Ö. F., Ocak, S., Yazgan, Z., Aktuğlu Zeybek, Ç., Aygün, G., Camcıoğlu, Y., and Çokuğraş, H. (2024). Emerging trends in pediatric candidemia: mapping the rise in Candida parapsilosis incidence and antifungal resistance in Turkey. Journal of Tropical Pediatrics, 70(5), fmae015. https://doi.org/10.1093/tropej/fmae015
- Özcan Ateş, G., and Otkun, M. (2023). In Vitro Evaluation of Biofilm Forming Capacity and Antifungal Resistance of Yeast Isolated from Individuals Aged 18-25 Years. Sinop Üniversitesi Fen Bilimleri Dergisi, 8(1). https://doi.org/10.33484/sinopfbd.1310745
- Pfaller, M. A., Castanheira, M., Messer, S. A., Moet, G. J., and Jones, R. N. (2010). Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY Antimicrobial Surveillance Program (2008–2009). Diagnostic microbiology and infectious disease, 68(3), 278-283. https://doi.org/10.1016/j.diagmicrobio.2010.06.015
- Ramage, G., Bachmann, S., Patterson, T. F., Wickes, B. L., and López-Ribot, J. L. (2002). Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. Journal of Antimicrobial Chemotherapy, 49(6), 973-980. https://doi.org/10.1093/jac/dkf049
- Sabino, R., Sampaio, P., Carneiro, C., Rosado, L., and Pais, C. (2011). Isolates from hospital environments are the most virulent of the Candida parapsilosis complex. BMC microbiology, 11, 1-10. https://doi.org/10.1186/1471-2180-11-180
- Silva, S., Rodrigues, C. F., Araújo, D., Rodrigues, M. E., and Henriques, M. (2017). Candida species biofilms’ antifungal resistance. Journal of Fungi, 3(1), 8. https://doi.org/10.3390/jof3010008
- Stepanović, S., Vuković, D., Hola, V., Bonaventura, G. D., Djukić, S., Ćirković, I., and Ruzicka, F. (2007). Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Apmis, 115(8), 891-899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
- Tóth, R., Nosek, J., Mora-Montes, H. M., Gabaldon, T., Bliss, J. M., Nosanchuk, J. D., Turner, S. A., Butler, G., Vágvölgyi, C. and Gácser, A. (2019). Candida parapsilosis: from genes to the bedside. Clinical microbiology reviews, 32(2), 10-1128. https://doi.org/10.1128/cmr.00111-18
- Tumbarello, M., Posteraro, B., Trecarichi, E. M., Fiori, B., Rossi, M., Porta, R., de Gaetano Donati, K., La Sorda, M., Spanu, T., Fadda, G., Cauda, R., and Sanguinetti, M. (2007). Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. Journal of clinical microbiology, 45(6), 1843-1850. https://doi.org/10.1128/jcm.00131-07
- Treviño-Rangel, R. D. J., Rodríguez-Sánchez, I. P., Rosas-Taraco, A. G., Hernández-Bello, R., González, J. G., and González, G. M. (2015). Biofilm formation and genetic variability of BCR1 gene in the Candida parapsilosis complex. Revista Iberoamericana de Micología, 32(3), 180-184. https://doi.org/10.1016/j.riam.2014.11.001.
Assessing Antifungal Resistance and Biofilm-Forming Capacity of Candida parapsilosis Isolates from Makeup Sponges
Abstract
Candida parapsilosis is an opportunistic pathogen that can colonize human mucous membranes and skin and develop resistance to antifungal treatments due to its ability to form biofilms. This study investigated the biofilm formation capacities and antifungal resistance of Candida parapsilosis isolates obtained from makeup sponges. The biofilm formation capacities among 46 Candida parapsilosis isolates were determined using the crystal violet quantitative method. Amphotericin B resistance in the isolates was evaluated with the agar disk diffusion method. The antifungal resistances of biofilm-producing species were assessed using the gradient test method. The crystal violet analysis revealed that most isolates were weak biofilm producers, with 17 exhibiting moderate biofilm production. It was determined that the isolates gave inhibition zones between 19.73 ± 1.54 mm and 23.71 ± 0.70 mm against amphotericin B by the agar disk diffusion method. It was concluded that 17 isolates with moderate biofilm production were susceptible to the antifungal agents clotrimazole, fluconazole, itraconazole, amphotericin B, and nystatin. The study emphasizes that makeup sponges may serve as reservoirs for Candida parapsilosis and highlights the importance of evaluating the antifungal susceptibility of biofilm-forming isolates. These findings are significant for the hygienic use of personal care products and implementing infection control measures.
Ethical Statement
It is declared that scientific and ethical principles have been followed while carrying out and writing this study and that all the sources used have been properly cited (Gülçin ÖZCAN ATEŞ.)
Thanks
Identification studies of the isolates with MALDI-TOF MS were conducted in the Hatay Mustafa Kemal University Centre for Implementation and Research of Plant Health Clinic. We thank Dr. Aysun UYSAL for her contributions.
References
- Agi, V. N., Ollor, O. A., Azike, C. A., and Onwuasoanya, C. V. (2023). Isolation and identification of microorganisms from makeup brushes in Rivers State University Nigeria and its environs. J Adv Microbiol, 23(3), 41-50. DOI: 10.9734/JAMB/2023/v23i3715
- Akgül, Ö., and Bakan, K. (2021). The aerobic bacteria isolated from used cosmetic products and evaluation of antibiotic resistance. Journal of Faculty of Pharmacy of Ankara University, 45(2), 156-168. https://doi.org/10.33483/jfpau.850561
- Arastehfar, A., Daneshnia, F., Najafzadeh, M. J., Hagen, F., Mahmoudi, S., Salehi, M., Zarrinfar, H., Namvar, Z., Zareshahrabadi, Z., Khodavaisy, S., Zomorodian, K., Pan, W., Theelen, B., Kostrzewa, M., Boekhout, T., and Lass-Flörl, C. (2020). Evaluation of molecular epidemiology, clinical characteristics, antifungal susceptibility profiles, and molecular mechanisms of antifungal resistance of Iranian Candida parapsilosis species complex blood isolates. Frontiers in Cellular and Infection Microbiology, 10, 206. https://doi.org/10.3389/fcimb.2020.00206
- Bashir, A., and Lambert, P. (2020). Microbiological study of used cosmetic products: highlighting possible impact on consumer health. Journal of Applied Microbiology, 128(2), 598-605. https://doi.org/10.1111/jam.14479
- Branco, J., Miranda, I. M., and Rodrigues, A. G. (2023). Candida parapsilosis virulence and antifungal resistance mechanisms: a comprehensive review of key determinants. Journal of Fungi, 9(1), 80. https://doi.org/10.3390/jof9010080
- CLSI, (2002). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard—Second Edition. NCCLS document M27-A2 [ISBN 1-56238-469-4]. NCCLS, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898 USA.
- CLSI, (2004). Method for Antifungal Disk Diffusion Susceptibility Testing of Yeasts; Approved Guideline. NCCLS document M44-A [ISBN 1-56238-532-1]. NCCLS, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898 USA.
- Colombo, A. L., de Almeida Júnior, J. N., and Guinea, J. (2017). Emerging multidrug-resistant Candida species. Current Opinion in Infectious Diseases, 30(6), 528-538. https://doi.org/10.1097/QCO.0000000000000411
- Daneshnia, F., de Almeida Júnior, J. N., Ilkit, M., Lombardi, L., Perry, A. M., Gao, M., Nobile, C. J., Egger, M., Perlin, D.S., Zhai, B., Hohl, T. M., Gabaldón, T., Colombo, A. L., Hoenigl, M., and Arastehfar, A. (2023). Worldwide emergence of fluconazole-resistant Candida parapsilosis: current framework and future research roadmap. The Lancet Microbe, 4(6), e470-e480. https://doi.org/10.1016/S2666-5247(23)00067-8
- de Paula Menezes, R., de Oliveira Melo, S. G., Bessa, M. A. S., Silva, F. F., Alves, P. G. V., Araújo, L. B., Penatti, M. P. A., Abdallah, O. S., de Brito Röder, D. V. D., and dos Santos Pedroso, R. (2020). Candidemia by Candida parapsilosis in a neonatal intensive care unit: Human and environmental reservoirs, virulence factors, and antifungal susceptibility. Brazilian Journal of Microbiology, 51, 851-860. https://doi.org/10.1007/s42770-020-00232-1
- Govrins, M., and Lass-Flörl, C. (2024). Candida parapsilosis complex in the clinical setting. Nature Reviews Microbiology, 22(1), 46-59. https://doi.org/10.1038/s41579-023-00961-8
- Grossman, N. T., Pham, C. D., Cleveland, A. A., and Lockhart, S. R. (2015). Molecular mechanisms of fluconazole resistance in Candida parapsilosis isolates from a US surveillance system. Antimicrobial agents and chemotherapy, 59(2), 1030-1037. https://doi.org/10.1128/aac.04613-14
- Melo, A. S., Bizerra, F. C., Freymüller, E., Arthington-Skaggs, B. A., and Colombo, A. L. (2011). Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Medical mycology, 49(3), 253-262.
- Miranda-Cadena, K., Marcos-Arias, C., Mateo, E., Aguirre, J. M., Quindós, G., and Eraso, E. (2018). Prevalence and antifungal susceptibility profiles of Candida glabrata, Candida parapsilosis and their close-related species in oral candidiasis. Archives of Oral Biology, 95, 100-107. https://doi.org/10.1016/j.archoralbio.2018.07.017
- Modiri, M., Khodavaisy, S., Barac, A., Dana, M. A., Nazemi, L., Aala, F., Salehi, M., and Rezaie, S. (2019). Comparison of biofilm-producing ability of clinical isolates of Candida parapsilosis species complex. Journal de mycologie medicale, 29(2), 140-146. https://doi.org/10.1016/j.mycmed.2019.02.003
- Ogbonna, S. I., Odu, N. N., Oparaodu, U. A., Robinson, V. K., and Ebenezer, A. (2024). Antibiogram of bacteria and fungi isolated from makeup kits in Port Harcourt metropolis. Microbiol. Res. Int, 12(2), 30-36. DOI: 10.30918/MRI.122.24.015
- Önal, P., Aygün, F. D., Sever, G. A., Eren, B. A., Kes, G., Aygün, F., Zübarioğlu, T., Beşer, Ö. F., Ocak, S., Yazgan, Z., Aktuğlu Zeybek, Ç., Aygün, G., Camcıoğlu, Y., and Çokuğraş, H. (2024). Emerging trends in pediatric candidemia: mapping the rise in Candida parapsilosis incidence and antifungal resistance in Turkey. Journal of Tropical Pediatrics, 70(5), fmae015. https://doi.org/10.1093/tropej/fmae015
- Özcan Ateş, G., and Otkun, M. (2023). In Vitro Evaluation of Biofilm Forming Capacity and Antifungal Resistance of Yeast Isolated from Individuals Aged 18-25 Years. Sinop Üniversitesi Fen Bilimleri Dergisi, 8(1). https://doi.org/10.33484/sinopfbd.1310745
- Pfaller, M. A., Castanheira, M., Messer, S. A., Moet, G. J., and Jones, R. N. (2010). Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY Antimicrobial Surveillance Program (2008–2009). Diagnostic microbiology and infectious disease, 68(3), 278-283. https://doi.org/10.1016/j.diagmicrobio.2010.06.015
- Ramage, G., Bachmann, S., Patterson, T. F., Wickes, B. L., and López-Ribot, J. L. (2002). Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. Journal of Antimicrobial Chemotherapy, 49(6), 973-980. https://doi.org/10.1093/jac/dkf049
- Sabino, R., Sampaio, P., Carneiro, C., Rosado, L., and Pais, C. (2011). Isolates from hospital environments are the most virulent of the Candida parapsilosis complex. BMC microbiology, 11, 1-10. https://doi.org/10.1186/1471-2180-11-180
- Silva, S., Rodrigues, C. F., Araújo, D., Rodrigues, M. E., and Henriques, M. (2017). Candida species biofilms’ antifungal resistance. Journal of Fungi, 3(1), 8. https://doi.org/10.3390/jof3010008
- Stepanović, S., Vuković, D., Hola, V., Bonaventura, G. D., Djukić, S., Ćirković, I., and Ruzicka, F. (2007). Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Apmis, 115(8), 891-899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
- Tóth, R., Nosek, J., Mora-Montes, H. M., Gabaldon, T., Bliss, J. M., Nosanchuk, J. D., Turner, S. A., Butler, G., Vágvölgyi, C. and Gácser, A. (2019). Candida parapsilosis: from genes to the bedside. Clinical microbiology reviews, 32(2), 10-1128. https://doi.org/10.1128/cmr.00111-18
- Tumbarello, M., Posteraro, B., Trecarichi, E. M., Fiori, B., Rossi, M., Porta, R., de Gaetano Donati, K., La Sorda, M., Spanu, T., Fadda, G., Cauda, R., and Sanguinetti, M. (2007). Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. Journal of clinical microbiology, 45(6), 1843-1850. https://doi.org/10.1128/jcm.00131-07
- Treviño-Rangel, R. D. J., Rodríguez-Sánchez, I. P., Rosas-Taraco, A. G., Hernández-Bello, R., González, J. G., and González, G. M. (2015). Biofilm formation and genetic variability of BCR1 gene in the Candida parapsilosis complex. Revista Iberoamericana de Micología, 32(3), 180-184. https://doi.org/10.1016/j.riam.2014.11.001.
There are 26 citations in total.
Details
| Primary Language | English |
|---|---|
| Subjects | Mycology, Medical Mycology |
| Journal Section | RESEARCH ARTICLE |
| Authors | |
| Publication Date | April 30, 2025 |
| Submission Date | March 12, 2025 |
| Acceptance Date | April 24, 2025 |
| Published in Issue | Year 2025 Volume: 16 Issue: 1 |
The works submitted to our journals are first judged grammatically. After this phase, articles are sent two reviewers. If necessary, the third reviewer is assessed. In the publication of works, a decision is made by evaluating the level of contribution to science and readers within the criteria specified in the writing rules. Reviewers are requested to submit their assessments within 30 days at the latest. The reviewers' evaluations and the answers to these evaluations are reviewed by the editor and it is decided whether the work will be published or not.
International Peer Reviewed Journal
The journal doesn’t have APC or any submission charges
This work is licensed under a Creative Commons Attribution 4.0 License