The efficacy of luliconazole and caspofungin on planktonic and biofilm of Candida albicans from different sources
Abstract
Background and Objectives: The ability of Candida albicans to produce biofilm is considered an important pathogenic factor. In addition, the low sensitivity of biofilms to antifungal drugs is a challenge for patients, clinicians, and laboratory workers. We aimed to investigate the effectiveness of luliconazole and caspofungin on the planktonic and biofilm types of C. albicans strains.
Materials and Methods: Fifty C. albicans from vaginitis, candiduria, gastrointestinal candidiasis, and saliva were examined for antifungal susceptibility against caspofungin and luliconazole using the CLSI M27 guideline. Moreover, the susceptibility of biofilms was detected using 96 well microplates and the MTT method.
Results: The capacity of the isolates to produce biofilm within 2, 6, and 24 h was different, however, all tested isolates produced biofilm after 24 h. Vaginal and esophagitis isolates had a high and low ability for biofilm production during 24-hour incubation. In our study, 90% of isolates were sensitive to caspofungin, while 7.5 and 2.5% of them were intermediate and resistant. The MIC range of all isolates against luliconazole was 0.01562-1 µg/mL.
Conclusion: The MICs of biofilms were 15.6, and 171.3 higher than that of planktonic cells for caspofungin and luliconazole, respectively. Moreover, paradoxical and trailing effects occurred at 4 and 32 µg/mL of caspofungin and luliconazole, respectively.
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3. Tobudic S, Kratzer C, Lassnigg A, Presterl E. Antifungal susceptibility of Candida albicans in biofilms. Mycoses 2012; 55: 199-204.
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7. Betts RF, Nucci M, Talwar D, Gareca M, Queiroz-Telles F, Bedimo RJ, et al. A Multicenter, double-blind trial of a high-dose caspofungin treatment regimen versus a standard caspofungin treatment regimen for adult patients with invasive candidiasis. Clin Infect Dis 2009; 48: 1676-1684.
8. Mora-Duarte J, Betts R, Rotstein C, Colombo AL, Thompson-Moya L, Smietana J, et al. Comparison of caspofungin and amphotericin B for invasive candidiasis. N Engl J Med 2002; 347: 2020-2029.
9. Gharaghani M, Hivary S, Taghipour S, Zarei-Mahmoudabadi A. Luliconazole, a highly effective imidazole, against Fusarium species complexes. Med Microbiol Immunol 2020; 209: 603-612.
10. Gharaghani M, Taghipour S, Zarei Mahmoudabadi A. Molecular identification, biofilm formation and antifungal susceptibility of Rhodotorula spp. Mol Biol Rep 2020; 47: 8903-8909.
11. Moslem M, Mahmoudabadi AZ. The high efficacy of luliconazole against environmental and otomycosis Aspergillus flavus strains. Iran J Microbiol 2020; 12: 170-176.
12. Taghipour S, Kiasat N, Shafiei S, Halvaeezadeh M, Rezaei-Matehkolaei A, Zarei Mahmoudabadi A. Luliconazole, a new antifungal against Candida species isolated from different sources. J Mycol Med 2018; 28: 374-378.
13. Watanabe R, Huruta H, Ueno Y, Nukada T, Niwa H, Shinyashiki N, et al. Antifungal susceptibility of dermatophytes from racehorses in Japan. Vet Dermatol 2021; 32: 474-e129.
14. Kiasat N, Rezaei-Matehkolaei A, Mahmoudabadi AZ. Microsatellite typing and antifungal susceptibility of Candida glabrata strains isolated from patients with Candida vaginitis. Front Microbiol 2019; 10: 1678.
15. Gharaghani M, Rezaei-Matehkolaei A, Hardani AK, Zarei Mahmoudabadi A. Pediatric candiduria, epidemiology, genotype distribution and virulence factors of Candida albicans. Microb Pathog 2021; 160: 105173.
16. Jafarian H, Gharaghani M, Seyedian SS, Mahmoudabadi AZ. Genotyping, antifungal susceptibility, enzymatic activity, and phenotypic variation in Candida albicans from esophageal candidiasis. J Clin Lab Anal 2021; 35(7): e23826.
17. Kianifar S, Rezaei-Matehkolaei A, Zarei-Mahmoudabadi A. Genotypes analysis of Candida albicans species complex from healthy individual saliva in Ahvaz, Iran. Lett Appl Microbiol 2022; 75: 831-835.
18. CLSI (2017). Reference method for broth dilution antifungal susceptibility testing of yeasts; CLSI standard M27. 4th ed. Wayne, PA: Clinical and Laboratory Standards Institute. https://clsi.org/shop/standards/m27/
19. Tulasidas S, Rao P, Bhat S, Manipura R. A study on biofilm production and antifungal drug resistance among Candida species from vulvovaginal and bloodstream infections. Infect Drug Resist 2018; 11: 2443-2448.
20. Marcos-Zambrano LJ, Escribano P, Bouza E, Guinea J. Susceptibility of Candida albicans biofilms to caspofungin and anidulafungin is not affected by metabolic activity or biomass production. Med Mycol 2016; 54: 155-161.
21. Pereira R, Dos Santos Fontenelle RO, de Brito EHS, de Morais SM. Biofilm of Candida albicans: formation, regulation and resistance. J Appl Microbiol 2021; 131: 11-22.
22. Guembe M, Cruces R, Pelaez T, Munoz P, Bouza E; GEIDI study group. Assessment of biofilm production in Candida isolates according to species and origin of infection. Enferm Infecc Microbiol Clin 2017; 35: 37-40.
23. CLSI (2012). M27-S4: Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Fourth Informational Supplement. Clinical and Laboratory Standards Institute, Annapolis Junction.
https://www.scirp.org/reference/referencespapers?referenceid=3102472
24. de Aquino Lemos J, Costa CR, de Araujo CR, Souza LK, Silva Mdo R. Susceptibility testing of Candida albicans isolated from oropharyngeal mucosa of HIV(+) patients to fluconazole, amphotericin B and Caspofungin. killing kinetics of caspofungin and amphotericin B against fluconazole resistant and susceptible isolates. Braz J Microbiol 2009; 40: 163-169.
25. Shokohi T, Badali H, Amirrajab N, Ataollahi MR, Kouhpayeh SA, Afsarian MH. In vitro activity of five antifungal agents against Candida albicans isolates, Sari, Iran. Curr Med Mycol 2016; 2: 34-39.
26. Yenisehirli G, Bulut N, Yenisehirli A, Bulut Y. In vitro susceptibilities of Candida albicans isolates to antifungal agents in Tokat, Turkey. Jundishapur J Microbiol 2015; 8(9): e28057.
27. Koga H, Tsuji Y, Inoue K, Kanai K, Majima T, Kasai T, et al. In vitro antifungal activity of luliconazole against clinical isolates from patients with dermatomycoses. J Infect Chemother 2006; 12: 163-165.
28. Shokoohi G, Sefidmazgi RR, Etehadnezhad M, Ahmadi B, Javidnia J, Nouripour-Sisakht S, et al. In vitro antifungal activity of luliconazole, efinaconazole, and nine comparators against Aspergillus and Candida strains isolated from otomycosis. Jundishapur J Microbiol 2021; 14(4): e115902.
29. Gharaghani M, Rezaei‐Matehkolaei A, Hardani A, Zarei Mahmoudabadi A. Genotypic diversity and antifungal susceptibility pattern of Candida albicans species isolated from hospitalized paediatric patients with urinary tract infection in Iran. J Appl Microbiol 2021; 131: 1017-1027.
30. Zomorodian K, Bandegani A, Mirhendi H, Pakshir K, Alinejhad N, Poostforoush Fard A. In vitro susceptibility and trailing growth effect of clinical isolates of Candida species to azole drugs. Jundishapur J Microbiol 2016; 9(2): e28666.
2. Zarei Mahmoudabadi A, Zarrin M, Kiasat N. Biofilm formation and susceptibility to amphotericin B and fluconazole in Candida albicans. Jundishapur J Microbiol 2014; 7(7): e17105.
3. Tobudic S, Kratzer C, Lassnigg A, Presterl E. Antifungal susceptibility of Candida albicans in biofilms. Mycoses 2012; 55: 199-204.
4. Ferreira JA, Carr JH, Starling CE, de Resende MA, Donlan RM. Biofilm formation and effect of caspofungin on biofilm structure of Candida species bloodstream isolates. Antimicrob Agents Chemother 2009; 53: 4377-4384.
5. Silva S, Rodrigues CF, Araujo D, Rodrigues ME, Henriques M. Candida species biofilms' antifungal resistance. J Fungi (Basel) 2017; 3: 8.
6. Prazynska M, Bogiel T, Gospodarek-Komkowska E. In vitro activity of micafungin against biofilms of Candida albicans, Candida glabrata, and Candida parapsilosis at different stages of maturation. Folia Microbiol (Praha) 2018; 63: 209-216.
7. Betts RF, Nucci M, Talwar D, Gareca M, Queiroz-Telles F, Bedimo RJ, et al. A Multicenter, double-blind trial of a high-dose caspofungin treatment regimen versus a standard caspofungin treatment regimen for adult patients with invasive candidiasis. Clin Infect Dis 2009; 48: 1676-1684.
8. Mora-Duarte J, Betts R, Rotstein C, Colombo AL, Thompson-Moya L, Smietana J, et al. Comparison of caspofungin and amphotericin B for invasive candidiasis. N Engl J Med 2002; 347: 2020-2029.
9. Gharaghani M, Hivary S, Taghipour S, Zarei-Mahmoudabadi A. Luliconazole, a highly effective imidazole, against Fusarium species complexes. Med Microbiol Immunol 2020; 209: 603-612.
10. Gharaghani M, Taghipour S, Zarei Mahmoudabadi A. Molecular identification, biofilm formation and antifungal susceptibility of Rhodotorula spp. Mol Biol Rep 2020; 47: 8903-8909.
11. Moslem M, Mahmoudabadi AZ. The high efficacy of luliconazole against environmental and otomycosis Aspergillus flavus strains. Iran J Microbiol 2020; 12: 170-176.
12. Taghipour S, Kiasat N, Shafiei S, Halvaeezadeh M, Rezaei-Matehkolaei A, Zarei Mahmoudabadi A. Luliconazole, a new antifungal against Candida species isolated from different sources. J Mycol Med 2018; 28: 374-378.
13. Watanabe R, Huruta H, Ueno Y, Nukada T, Niwa H, Shinyashiki N, et al. Antifungal susceptibility of dermatophytes from racehorses in Japan. Vet Dermatol 2021; 32: 474-e129.
14. Kiasat N, Rezaei-Matehkolaei A, Mahmoudabadi AZ. Microsatellite typing and antifungal susceptibility of Candida glabrata strains isolated from patients with Candida vaginitis. Front Microbiol 2019; 10: 1678.
15. Gharaghani M, Rezaei-Matehkolaei A, Hardani AK, Zarei Mahmoudabadi A. Pediatric candiduria, epidemiology, genotype distribution and virulence factors of Candida albicans. Microb Pathog 2021; 160: 105173.
16. Jafarian H, Gharaghani M, Seyedian SS, Mahmoudabadi AZ. Genotyping, antifungal susceptibility, enzymatic activity, and phenotypic variation in Candida albicans from esophageal candidiasis. J Clin Lab Anal 2021; 35(7): e23826.
17. Kianifar S, Rezaei-Matehkolaei A, Zarei-Mahmoudabadi A. Genotypes analysis of Candida albicans species complex from healthy individual saliva in Ahvaz, Iran. Lett Appl Microbiol 2022; 75: 831-835.
18. CLSI (2017). Reference method for broth dilution antifungal susceptibility testing of yeasts; CLSI standard M27. 4th ed. Wayne, PA: Clinical and Laboratory Standards Institute. https://clsi.org/shop/standards/m27/
19. Tulasidas S, Rao P, Bhat S, Manipura R. A study on biofilm production and antifungal drug resistance among Candida species from vulvovaginal and bloodstream infections. Infect Drug Resist 2018; 11: 2443-2448.
20. Marcos-Zambrano LJ, Escribano P, Bouza E, Guinea J. Susceptibility of Candida albicans biofilms to caspofungin and anidulafungin is not affected by metabolic activity or biomass production. Med Mycol 2016; 54: 155-161.
21. Pereira R, Dos Santos Fontenelle RO, de Brito EHS, de Morais SM. Biofilm of Candida albicans: formation, regulation and resistance. J Appl Microbiol 2021; 131: 11-22.
22. Guembe M, Cruces R, Pelaez T, Munoz P, Bouza E; GEIDI study group. Assessment of biofilm production in Candida isolates according to species and origin of infection. Enferm Infecc Microbiol Clin 2017; 35: 37-40.
23. CLSI (2012). M27-S4: Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Fourth Informational Supplement. Clinical and Laboratory Standards Institute, Annapolis Junction.
https://www.scirp.org/reference/referencespapers?referenceid=3102472
24. de Aquino Lemos J, Costa CR, de Araujo CR, Souza LK, Silva Mdo R. Susceptibility testing of Candida albicans isolated from oropharyngeal mucosa of HIV(+) patients to fluconazole, amphotericin B and Caspofungin. killing kinetics of caspofungin and amphotericin B against fluconazole resistant and susceptible isolates. Braz J Microbiol 2009; 40: 163-169.
25. Shokohi T, Badali H, Amirrajab N, Ataollahi MR, Kouhpayeh SA, Afsarian MH. In vitro activity of five antifungal agents against Candida albicans isolates, Sari, Iran. Curr Med Mycol 2016; 2: 34-39.
26. Yenisehirli G, Bulut N, Yenisehirli A, Bulut Y. In vitro susceptibilities of Candida albicans isolates to antifungal agents in Tokat, Turkey. Jundishapur J Microbiol 2015; 8(9): e28057.
27. Koga H, Tsuji Y, Inoue K, Kanai K, Majima T, Kasai T, et al. In vitro antifungal activity of luliconazole against clinical isolates from patients with dermatomycoses. J Infect Chemother 2006; 12: 163-165.
28. Shokoohi G, Sefidmazgi RR, Etehadnezhad M, Ahmadi B, Javidnia J, Nouripour-Sisakht S, et al. In vitro antifungal activity of luliconazole, efinaconazole, and nine comparators against Aspergillus and Candida strains isolated from otomycosis. Jundishapur J Microbiol 2021; 14(4): e115902.
29. Gharaghani M, Rezaei‐Matehkolaei A, Hardani A, Zarei Mahmoudabadi A. Genotypic diversity and antifungal susceptibility pattern of Candida albicans species isolated from hospitalized paediatric patients with urinary tract infection in Iran. J Appl Microbiol 2021; 131: 1017-1027.
30. Zomorodian K, Bandegani A, Mirhendi H, Pakshir K, Alinejhad N, Poostforoush Fard A. In vitro susceptibility and trailing growth effect of clinical isolates of Candida species to azole drugs. Jundishapur J Microbiol 2016; 9(2): e28666.
| Files | ||
| Issue | Vol 17 No 4 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i4.19261 | |
| Keywords | ||
| Candida albicans Biofilm Planktonic Luliconazole Caspofungin | ||
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How to Cite
1.
Shabanzadeh M, Rezaei-Matehkolaei A, Zarei Mahmoudabadi A. The efficacy of luliconazole and caspofungin on planktonic and biofilm of Candida albicans from different sources. Iran J Microbiol. 2025;17(4):653-659.
