Evaluation of virulence factors and azole resistance mechanisms of Candida tropicalis isolates from head and neck cancer patients with OPC
,
Abstract
Background and Objectives: Candida tropicalis is one of the major non-albicans species causing nosocomial infection. There is limited data about mechanisms of azole-resistance and virulence factors of Candida tropicalis. This study was designed to investigate molecular mechanism of azole -resistance and major virulence factors of C. tropicalis isolated from oropharyngeal candidiasis in head and neck cancer patients.
Materials and Methods: After collecting 38 C. tropicalis clinical isolates, antifungal susceptibility pattern and the expression levels of ERG11, CDR1, CDR2 and MDR1 were evaluated. Moreover, proteinase and phospholipase activity and biofilm formation of the isolates were investigated as virulence factors.
Results: We detected fluconazole resistance in 7 C. tropicalis isolates. The expression levels of CDR1, ERG11 and MDR1 were increased respectively. Protease activity and biofilm formation were seen in all isolates. Five isolates did not exhibit phospholipase activity.
Conclusion: Taken together, the overexpressions of ERG11, CDR1 and MDR1 genes were found in fluconazole resistant C. tropicalis, isolated from oropharyngeal candidiasis patients. Also, voriconazole was an effective antifungal against C. tropicalis isolates. The observed high protease enzyme activity and biofilm formation suggested strong pathogenicity of these isolates.
1. Maheronnaghsh M, Fatahinia M, Dehghan P, Zarei Mahmoudabadi A, Kheirkhah M. Comparison of virulence factors of different Candida species isolated from the oral cavity of cancer patients and normal individuals. Jundishapur J Microbiol 2019; 12(5): e91556.
2. da Costa KRC, Ferreira JC, Komesu MC, Candido RC. Candida albicans and Candida tropicalis in oral Candidosis: Quantitative analysis, exoenzyme activity, and antifungal drug sensitivity. Mycopathologia 2009; 167: 73-79.
3. Bensadoun R-J, Patton LL, Lalla RV, Epstein JB. Oropharyngeal candidiasis in head and neck cancer patients treated with radiation: update 2011. Support Care Cancer 2011; 19: 737-744.
4. Silva-Dias A, Miranda IM, Branco J, Monteiro-Soares M, Pina-Vaz C, Rodrigues AG. Adhesion, biofilm formation, cell surface hydrophobicity, and antifungal planktonic susceptibility: relationship among Candida spp. Front Microbiol 2015; 6: 205.
5. Negri M, Silva S, Capoci IRG, Azeredo J, Henriques M. Candida tropicalis biofilms: Biomass, metabolic activity and production. Mycopathologia 2016; 181: 217-224.
6. Zaugg C, Borg-Von Zepelin M, Reichard U, Sanglard D, Monodi M. Secreted aspartic proteinase family of Candida tropicalis. Infect Immun 2001; 69: 405-412.
7. Arastehfar A, Daneshnia F, Hafez A, Khodavaisy S, Najafzadeh MJ, Charsizadeh A, et al. Antifungal susceptibility, genotyping, resistance mechanism, and clinical profile of Candida tropicalis blood isolates. Med Mycol 2020; 58: 766-773.
8. Teo J Q-M, Lee S J-Y, Tan A-L, Lim R S-M, Cai Y, Lim TP, et al. Molecular mechanisms of azole resistance in Candida bloodstream isolates. BMC Infect Dis 2019; 19: 63.
9. Chen P-Y, Chuang Y-C, Wu U-I, Sun H-Y, Wang J-T, Sheng W-H, et al. Clonality of fluconazole-nonsusceptible Candida tropicalis in bloodstream infections, Taiwan, 2011–2017. Emerg Infect Dis 2019; 25: 1660-1667.
10. Negri M, Martins M, Henriques M, Svidzinski TIE, Azeredo J, Oliveira R. Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycopathologia 2010; 169:175-182.
11. Abu-Elteen KH, Elkarmi AZ, Hamad M. Characterization of phenotype-based pathogenic determinants of various Candida albicans strains in Jordan. Jpn J Infect Dis 2001; 54: 229-236.
12. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003; 67: 400-428.
13. Jahanshiri Z, Manifar S, Hatami F, Arastehnazar F, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Genotyping of Candida albicans isolates from oropharyngeal candidiasis in head and neck cancer patients in Iran: Molecular epidemiology and SAP2 gene expression. J Mycol Med 2019; 29: 310-316.
14. Schaller M, Borelli C, Korting HC, Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 2005; 48: 365-377.
15. Ramos Lde S, Barbedo LS, Braga-Silva LA, dos Santos AL, Pinto MR, Sgarbi DB. Protease and phospholipase activities of Candida spp. isolated from cutaneous candidiasis. Rev Iberoam Micol 2015; 32: 122-125.
16. Coronado-Castellote L, Jiménez-Soriano Y. Clinical and microbiological diagnosis of oral candidiasis. J Clin Exp Dent 2013; 5(5): e279-86.
17. Yamada Y, Makimura K, Merhendi H, Ueda K, Nishiyama Y, Yamaguchi H, et al. Comparison of different methods for extraction of mitochondrial DNA from human pathogenic yeasts. Jpn J Infect Dis 2002; 55: 122-125.
18. Arastehfar A, Fang W, Pan W, LacknerM, Liao W, Badiee P, et al. YEAST PANEL multiplex PCR for identification of clinically important yeast species: stepwise diagnostic strategy, useful for developing countries. Diagn Microbiol Infect Dis 2019: 93; 112-119.
19. Clinical and laboratory standards Institute (CLSI), reference method for broth dilution antifungal susceptibility testing of yeasts, in: Document, Approved Standard-Third Edition, 2008. M27- A3. Wayne, P.A.
20. Atiencia-Carrera MB, Cabezas-Mera FS, Vizuete K, Debut A, Tejera E, Machado A. Evaluation of the biofilm life cycle between Candida albicans and Candida tropicalis. Front Cell Infect Microbiol 2022; 12: 953168.
21. Jin Y, Yip HK, Samaranayake YH, Yau JY, Samaranayake LP. Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage incases of human immunodeficiency virus infection. J Clin Microbiol 2003; 41: 2961-2967.
22. Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M, Porta R, et al. Biofilm production by Candida species and inadequate antifungal therapy as predic-tors of mortality for patients with candidemia. J Clin Microbiol 2007; 45: 1843-1850.
23. Ilkhanizadeh-Qomi M, Nejatbakhsh S, Jahanshiri Z, Razzaghi-Abyaneh M. Aspartyl proteinase and phospholipase activities of Candida albicans isolated from oropharyngeal candidiasis in head and neck cancer patients. Jundishapur J Microbiol 2020; 13(9): e105200.
24. Pereira CA, da Costa AC, Machado AK, Beltrame Júnior M, Zöllner MS, Junqueira JC, et al. Enzymatic activity, sensitivity to antifungal drugs and Baccharis dracunculifolia essential oil by Candida strains isolated from the oral cavities of breastfeeding infants and in their mothers’ mouths and nipples. Mycopathologia 2011; 171: 103-139.
25. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003; 67: 400-428.
26. Rezaie S, Ban J, Mildner M, Poitschek C, Brna C, Tschachler E. Characterization of a cDNA clone, encoding a 70 kDa heat shock protein from the dermatophyte pathogen Trichophyton rubrum. Gene 2000; 241: 27-33.
27. Fricke S, Fricke C, Schimmelpfennig C, Oelkrug C, Schönfelder U, Blatz R, et al. A real-time PCR assay for the differentiation of Candida species. J Appl Microbiol 2010; 109: 1150-1158.
28. Shao J, Shi GX, Wang T, Wu D, Wang C. Antiproliferation of Berberine in ombination with fluconazole from the perspectives of reactive oxygen species, ergosterol and drug efflux in a fluconazole-resistant Candida tropicalis isolate. Front Microbiol 2016; 7: 1516.
29. Pfaller MA, Diekema DJ. Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol 2012; 50: 2846-2856.
30. Flowers SA, Barker KS, Berkow EL, Toner G, Chadwick SG, Gygax SE, et al. Gain-of-Function mutations in UPC2 are a frequent cause of ERG11 upregulation in azole-resistant clinical isolates of Candida albicans. Eukaryot Cell 2012; 11: 1289-1299.
31. Chakrabarti A, Chatterjee SS, Rao KL, Zameer MM, Shivaprakash MR, Singhi S, et al. Recent experience with fungaemia: change in species distribution and azole resistance. Scand J Infect Dis 2009; 41: 275-284.
32. Kothavade RJ, Kura MM, Valand AG, Panthaki MH. Candida tropicalis: its prevalence, pathogenicity and increasing resistance to fluconazole. J Med Microbiol 2010; 59: 873-880.
33. Adhikary R, Joshi S. Species distribution and anti-fungal susceptibility of Candidaemia at a multi super-specialty center in Southern India. Indian J Med Microbiol 2011; 29: 309-311.
34. Jiang C, Dong D, Yu B, Cai G, Wang X, Ji Y, et al. Mechanisms of azole resistance in 52 clinical isolates of Candida tropicalis in China. J Antimicrob Chemother 2013; 68: 778-785.
35. Sasani E, Khodavaisy S, Rezaie S, Salehi M, Yadegari MH. The relationship between biofilm formation and mortality in patients with Candida tropicalis candidemia. Microb Pathog 2021; 155: 104889.
36. Jiang C, Ni Q, Dong D, Zhang L, Li Z, Tian Y, et al. The role of UPC2 gene in azole-resistant Candida tropicalis. Mycopathologia 2016; 181: 833-838.
37. Dovo EE, Zohoncon TM, Tovo SF, Soubeiga ST, Kiendrebeogo IT , Yonli AT, et al. First detection of mutated ERG11 gene in vulvovaginal Candida albicans isolates at Ouagadougou/Burkina Faso. BMC Infect Dis 2022; 22: 678.
38. Du W, Coaker M, Sobel JD, Akins RA. Shuttle vectors for Candida albicans: control of plasmid copy number and elevated expression of cloned genes. Curr Genet 2004; 45: 390-398.
39. Liu TL, Znaidi S, Barker KS, Xu L, Homayouni R, Saidane S, et al. Genome-wide expression and location analyses of the Candida albicans Tac1p regulon. Eukaryot Cell 2007; 6: 2122-2138.
40. Jin L, Cao Z, Wang Q, Wang Y, Wang X, Chen H, et al. MDR1 overexpression combined with ERG11 mutations induce high-level fluconazole resistance in Candida tropicalis clinical isolates. BMC Infect Dis 2018; 18: 162.
41. Barchiesi F, Calabrese D, Sanglard D, Falconi Di Francesco L, Caselli F, Giannini D, et al. Experimental induction of fluconazole resistance in Candida tropicalis ATCC 750. Antimicrob Agents Chemother 2000; 44: 1578-1584.
42. Vandeputte P, Larcher G, Berge`s T, Renier G, Chabasse D, Bouchara J-P. Mechanisms of azole resistance in a clinical isolate of Candida tropicalis. Antimicrob Agents Chemother 2005; 49: 4608-4615.
43. Sasani E, Yadegari MH, Khodavaisy S, Rezaie S, Salehi M, Getso MI. Virulence factors and azole-resistant mechanism of Candida tropicalis Isolated from Candidemia. Mycopathologia 2021; 186: 847-856.
44. Choi MJ, Won EJ, Shin JH, Kim SH, Lee W-G, Kim M-N, et al. Resistance mechanisms and clinical features of fluconazole-nonsusceptible Candida tropicalis isolates compared with fluconazole-less-susceptible isolates. Antimicrob Agents Chemother 2016; 60: 3653-3661.
45. Kantarcioglu AS, Yu¨cel A. Phospholipase and protease activities in clinical Candida isolates with reference to the source of strains. Mycoses 2002; 45: 160-165.
46. Deorukhkar SC, Saini S, Mathew S. Virulence factors contributing to pathogenicity of Candida tropicalis and its antifungal susceptibility profile. Int J Microbiol 2014; 2014: 456878.
47. Fule SR, Das D, Fule RP. Detection of phospholipase activity of Candida albicans and non albicans isolated from women of reproductive age with vulvovaginal candidiasis in rural area. Indian J Med Microbiol 2015; 33: 92-95.
48. Ghannoum MA. Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev 2000; 13: 122-143.
49. Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M, Porta R, et al. Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. J Clin Microbiol 2007; 45: 1843-1850.
50. Mohammadi F, Ghasemi Z, Familsatarian B, Salehi E, Sharifynia S, Barikani A, et al. Relationship between antifungal susceptibility profile and virulence factors in Candida albicans isolated from nail specimens. Rev Soc Bras Med Trop 2020; 53: e20190214.
2. da Costa KRC, Ferreira JC, Komesu MC, Candido RC. Candida albicans and Candida tropicalis in oral Candidosis: Quantitative analysis, exoenzyme activity, and antifungal drug sensitivity. Mycopathologia 2009; 167: 73-79.
3. Bensadoun R-J, Patton LL, Lalla RV, Epstein JB. Oropharyngeal candidiasis in head and neck cancer patients treated with radiation: update 2011. Support Care Cancer 2011; 19: 737-744.
4. Silva-Dias A, Miranda IM, Branco J, Monteiro-Soares M, Pina-Vaz C, Rodrigues AG. Adhesion, biofilm formation, cell surface hydrophobicity, and antifungal planktonic susceptibility: relationship among Candida spp. Front Microbiol 2015; 6: 205.
5. Negri M, Silva S, Capoci IRG, Azeredo J, Henriques M. Candida tropicalis biofilms: Biomass, metabolic activity and production. Mycopathologia 2016; 181: 217-224.
6. Zaugg C, Borg-Von Zepelin M, Reichard U, Sanglard D, Monodi M. Secreted aspartic proteinase family of Candida tropicalis. Infect Immun 2001; 69: 405-412.
7. Arastehfar A, Daneshnia F, Hafez A, Khodavaisy S, Najafzadeh MJ, Charsizadeh A, et al. Antifungal susceptibility, genotyping, resistance mechanism, and clinical profile of Candida tropicalis blood isolates. Med Mycol 2020; 58: 766-773.
8. Teo J Q-M, Lee S J-Y, Tan A-L, Lim R S-M, Cai Y, Lim TP, et al. Molecular mechanisms of azole resistance in Candida bloodstream isolates. BMC Infect Dis 2019; 19: 63.
9. Chen P-Y, Chuang Y-C, Wu U-I, Sun H-Y, Wang J-T, Sheng W-H, et al. Clonality of fluconazole-nonsusceptible Candida tropicalis in bloodstream infections, Taiwan, 2011–2017. Emerg Infect Dis 2019; 25: 1660-1667.
10. Negri M, Martins M, Henriques M, Svidzinski TIE, Azeredo J, Oliveira R. Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycopathologia 2010; 169:175-182.
11. Abu-Elteen KH, Elkarmi AZ, Hamad M. Characterization of phenotype-based pathogenic determinants of various Candida albicans strains in Jordan. Jpn J Infect Dis 2001; 54: 229-236.
12. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003; 67: 400-428.
13. Jahanshiri Z, Manifar S, Hatami F, Arastehnazar F, Shams-Ghahfarokhi M, Razzaghi-Abyaneh M. Genotyping of Candida albicans isolates from oropharyngeal candidiasis in head and neck cancer patients in Iran: Molecular epidemiology and SAP2 gene expression. J Mycol Med 2019; 29: 310-316.
14. Schaller M, Borelli C, Korting HC, Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 2005; 48: 365-377.
15. Ramos Lde S, Barbedo LS, Braga-Silva LA, dos Santos AL, Pinto MR, Sgarbi DB. Protease and phospholipase activities of Candida spp. isolated from cutaneous candidiasis. Rev Iberoam Micol 2015; 32: 122-125.
16. Coronado-Castellote L, Jiménez-Soriano Y. Clinical and microbiological diagnosis of oral candidiasis. J Clin Exp Dent 2013; 5(5): e279-86.
17. Yamada Y, Makimura K, Merhendi H, Ueda K, Nishiyama Y, Yamaguchi H, et al. Comparison of different methods for extraction of mitochondrial DNA from human pathogenic yeasts. Jpn J Infect Dis 2002; 55: 122-125.
18. Arastehfar A, Fang W, Pan W, LacknerM, Liao W, Badiee P, et al. YEAST PANEL multiplex PCR for identification of clinically important yeast species: stepwise diagnostic strategy, useful for developing countries. Diagn Microbiol Infect Dis 2019: 93; 112-119.
19. Clinical and laboratory standards Institute (CLSI), reference method for broth dilution antifungal susceptibility testing of yeasts, in: Document, Approved Standard-Third Edition, 2008. M27- A3. Wayne, P.A.
20. Atiencia-Carrera MB, Cabezas-Mera FS, Vizuete K, Debut A, Tejera E, Machado A. Evaluation of the biofilm life cycle between Candida albicans and Candida tropicalis. Front Cell Infect Microbiol 2022; 12: 953168.
21. Jin Y, Yip HK, Samaranayake YH, Yau JY, Samaranayake LP. Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage incases of human immunodeficiency virus infection. J Clin Microbiol 2003; 41: 2961-2967.
22. Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M, Porta R, et al. Biofilm production by Candida species and inadequate antifungal therapy as predic-tors of mortality for patients with candidemia. J Clin Microbiol 2007; 45: 1843-1850.
23. Ilkhanizadeh-Qomi M, Nejatbakhsh S, Jahanshiri Z, Razzaghi-Abyaneh M. Aspartyl proteinase and phospholipase activities of Candida albicans isolated from oropharyngeal candidiasis in head and neck cancer patients. Jundishapur J Microbiol 2020; 13(9): e105200.
24. Pereira CA, da Costa AC, Machado AK, Beltrame Júnior M, Zöllner MS, Junqueira JC, et al. Enzymatic activity, sensitivity to antifungal drugs and Baccharis dracunculifolia essential oil by Candida strains isolated from the oral cavities of breastfeeding infants and in their mothers’ mouths and nipples. Mycopathologia 2011; 171: 103-139.
25. Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003; 67: 400-428.
26. Rezaie S, Ban J, Mildner M, Poitschek C, Brna C, Tschachler E. Characterization of a cDNA clone, encoding a 70 kDa heat shock protein from the dermatophyte pathogen Trichophyton rubrum. Gene 2000; 241: 27-33.
27. Fricke S, Fricke C, Schimmelpfennig C, Oelkrug C, Schönfelder U, Blatz R, et al. A real-time PCR assay for the differentiation of Candida species. J Appl Microbiol 2010; 109: 1150-1158.
28. Shao J, Shi GX, Wang T, Wu D, Wang C. Antiproliferation of Berberine in ombination with fluconazole from the perspectives of reactive oxygen species, ergosterol and drug efflux in a fluconazole-resistant Candida tropicalis isolate. Front Microbiol 2016; 7: 1516.
29. Pfaller MA, Diekema DJ. Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol 2012; 50: 2846-2856.
30. Flowers SA, Barker KS, Berkow EL, Toner G, Chadwick SG, Gygax SE, et al. Gain-of-Function mutations in UPC2 are a frequent cause of ERG11 upregulation in azole-resistant clinical isolates of Candida albicans. Eukaryot Cell 2012; 11: 1289-1299.
31. Chakrabarti A, Chatterjee SS, Rao KL, Zameer MM, Shivaprakash MR, Singhi S, et al. Recent experience with fungaemia: change in species distribution and azole resistance. Scand J Infect Dis 2009; 41: 275-284.
32. Kothavade RJ, Kura MM, Valand AG, Panthaki MH. Candida tropicalis: its prevalence, pathogenicity and increasing resistance to fluconazole. J Med Microbiol 2010; 59: 873-880.
33. Adhikary R, Joshi S. Species distribution and anti-fungal susceptibility of Candidaemia at a multi super-specialty center in Southern India. Indian J Med Microbiol 2011; 29: 309-311.
34. Jiang C, Dong D, Yu B, Cai G, Wang X, Ji Y, et al. Mechanisms of azole resistance in 52 clinical isolates of Candida tropicalis in China. J Antimicrob Chemother 2013; 68: 778-785.
35. Sasani E, Khodavaisy S, Rezaie S, Salehi M, Yadegari MH. The relationship between biofilm formation and mortality in patients with Candida tropicalis candidemia. Microb Pathog 2021; 155: 104889.
36. Jiang C, Ni Q, Dong D, Zhang L, Li Z, Tian Y, et al. The role of UPC2 gene in azole-resistant Candida tropicalis. Mycopathologia 2016; 181: 833-838.
37. Dovo EE, Zohoncon TM, Tovo SF, Soubeiga ST, Kiendrebeogo IT , Yonli AT, et al. First detection of mutated ERG11 gene in vulvovaginal Candida albicans isolates at Ouagadougou/Burkina Faso. BMC Infect Dis 2022; 22: 678.
38. Du W, Coaker M, Sobel JD, Akins RA. Shuttle vectors for Candida albicans: control of plasmid copy number and elevated expression of cloned genes. Curr Genet 2004; 45: 390-398.
39. Liu TL, Znaidi S, Barker KS, Xu L, Homayouni R, Saidane S, et al. Genome-wide expression and location analyses of the Candida albicans Tac1p regulon. Eukaryot Cell 2007; 6: 2122-2138.
40. Jin L, Cao Z, Wang Q, Wang Y, Wang X, Chen H, et al. MDR1 overexpression combined with ERG11 mutations induce high-level fluconazole resistance in Candida tropicalis clinical isolates. BMC Infect Dis 2018; 18: 162.
41. Barchiesi F, Calabrese D, Sanglard D, Falconi Di Francesco L, Caselli F, Giannini D, et al. Experimental induction of fluconazole resistance in Candida tropicalis ATCC 750. Antimicrob Agents Chemother 2000; 44: 1578-1584.
42. Vandeputte P, Larcher G, Berge`s T, Renier G, Chabasse D, Bouchara J-P. Mechanisms of azole resistance in a clinical isolate of Candida tropicalis. Antimicrob Agents Chemother 2005; 49: 4608-4615.
43. Sasani E, Yadegari MH, Khodavaisy S, Rezaie S, Salehi M, Getso MI. Virulence factors and azole-resistant mechanism of Candida tropicalis Isolated from Candidemia. Mycopathologia 2021; 186: 847-856.
44. Choi MJ, Won EJ, Shin JH, Kim SH, Lee W-G, Kim M-N, et al. Resistance mechanisms and clinical features of fluconazole-nonsusceptible Candida tropicalis isolates compared with fluconazole-less-susceptible isolates. Antimicrob Agents Chemother 2016; 60: 3653-3661.
45. Kantarcioglu AS, Yu¨cel A. Phospholipase and protease activities in clinical Candida isolates with reference to the source of strains. Mycoses 2002; 45: 160-165.
46. Deorukhkar SC, Saini S, Mathew S. Virulence factors contributing to pathogenicity of Candida tropicalis and its antifungal susceptibility profile. Int J Microbiol 2014; 2014: 456878.
47. Fule SR, Das D, Fule RP. Detection of phospholipase activity of Candida albicans and non albicans isolated from women of reproductive age with vulvovaginal candidiasis in rural area. Indian J Med Microbiol 2015; 33: 92-95.
48. Ghannoum MA. Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev 2000; 13: 122-143.
49. Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M, Porta R, et al. Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. J Clin Microbiol 2007; 45: 1843-1850.
50. Mohammadi F, Ghasemi Z, Familsatarian B, Salehi E, Sharifynia S, Barikani A, et al. Relationship between antifungal susceptibility profile and virulence factors in Candida albicans isolated from nail specimens. Rev Soc Bras Med Trop 2020; 53: e20190214.
| Files | ||
| Issue | Vol 15 No 1 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i1.11933 | |
| Keywords | ||
| Candida tropicalis; Azole-resistance; Proteinase; Phospholipase; Biofilm | ||
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How to Cite
1.
Jahanshiri Z, Manifar S, Hatami F. Evaluation of virulence factors and azole resistance mechanisms of Candida tropicalis isolates from head and neck cancer patients with OPC. Iran J Microbiol. 2023;15(1):163-173.
