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Mycopathologia

, Volume 171, Issue 6, pp 411–416 | Cite as

In Vitro Susceptibility of a Large Collection of Candida Strains Against Fluconazole and Voriconazole by Using the CLSI Disk Diffusion Assay

  • Ana Carolina Azevedo
  • Fernando César Bizerra
  • Daniel Arquimedes da Matta
  • Leila Paula de Almeida
  • Robert Rosas
  • Arnaldo Lopes ColomboEmail author
Article

Abstract

We evaluated all Candida spp. isolates obtained from patients admitted to two tertiary care hospitals between 1999 and 2003 in the city of São Paulo, Brazil. The in vitro activities of fluconazole (FCZ) and voriconazole were determined by the agar disk diffusion test using the Clinical and Laboratory Standards Institute M44-A guidelines. The inhibition zone diameters were read and interpreted automatically by the BIOMIC® image-analysis plate reader system. We tested a total of 4,625 strains, including 2,393 strains of C. albicans (51.7%), 658 of C. tropicalis (14.2%), 503 of C. glabrata (10.9%), 495 of C. parapsilosis (10.7%), 292 of C. rugosa (6.3%), 195 of C. guilliermondii (4.2%) and 89 of other Candida species (2.0%). Only 2.0% of the strains tested were classified as dose-dependent susceptible (DDS), and 5.8% of them were resistant to FCZ. The resistance or DDS to fluconazole was verified mainly among C. glabrata (7.8%), C. krusei (67.9%) and C. rugosa (65.1%). Voriconazole exhibited better activity in vitro than fluconazole, even in isolates fluconazole resistant. The resistance of fluconazole and voriconazole did not increase in the isolates of Candida spp. during the evaluated period.

Keywords

Disk diffusion Candida spp. Fluconazole Voriconazole 

References

  1. 1.
    Colombo AL, Nucci M, Park BJ, Nouer SA, Arthington-Skaggs B, da Matta DA, et al. Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers. J Clin Microbiol. 2006;44(8):2816–23.PubMedCrossRefGoogle Scholar
  2. 2.
    Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Meis JF, Gould IM, et al. Results from the ARTEMIS DISK global antifungal surveillance study, 1997 to 2005: an 8.5-year analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol. 2007;45(6):1735–45.PubMedCrossRefGoogle Scholar
  3. 3.
    da Matta VL, de Souza Carvalho Melhem M, Colombo AL, Moretti ML, Rodero L, Duboc de Almeida GM, et al. Antifungal drug susceptibility profile of Pichia anomala isolates from patients presenting with nosocomial fungemia. Antimicrob Agents Chemother. 2007;51(4):1573–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Colombo AL, Janini M, Salomao R, Medeiros EA, Wey SB, Pignatari AC. Surveillance programs for detection and characterization of emergent pathogens and antimicrobial resistance: results from the division of infectious diseases, UNIFESP. An Acad Bras Cienc. 2009;81(3):571–87.PubMedCrossRefGoogle Scholar
  5. 5.
    Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts. Informational supplement–third edition, M27-S3. Wayne, PA; 2008.Google Scholar
  6. 6.
    Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard–third edition, M27-A3. Wayne, PA; 2008.Google Scholar
  7. 7.
    Barry AL, Pfaller MA, Brown SD, Espinel-Ingroff A, Ghannoum MA, Knapp C, et al. Quality control limits for broth microdilution susceptibility tests of ten antifungal agents. J Clin Microbiol. 2000;38(9):3457–9.PubMedGoogle Scholar
  8. 8.
    Barry AL, Pfaller MA, Rennie RP, Fuchs PC, Brown SD. Precision and accuracy of fluconazole susceptibility testing by broth microdilution, Etest, and disk diffusion methods. Antimicrob Agents Chemother. 2002;46(6):1781–4.PubMedCrossRefGoogle Scholar
  9. 9.
    Hazen KC, Baron EJ, Colombo AL, Girmenia C, Sanchez-Sousa A, del Palacio A, et al. Comparison of the susceptibilities of Candida spp. to fluconazole and voriconazole in a 4-year global evaluation using disk diffusion. J Clin Microbiol. 2003;41(12):5623–32.PubMedCrossRefGoogle Scholar
  10. 10.
    Pfaller MA, Barry A, Bille J, Brown S, Ellis D, Meis JF, et al. Quality control limits for voriconazole disk susceptibility tests on Mueller-Hinton agar with glucose and methylene blue. J Clin Microbiol. 2004;42(4):1716–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Pfaller MA, Boyken L, Hollis RJ, Kroeger J, Messer SA, Tendolkar S, et al. Comparison of results of fluconazole and voriconazole disk diffusion testing for Candida spp. with results from a central reference laboratory in the ARTEMIS DISK global antifungal surveillance program. Diagn Microbiol Infect Dis. 2009;65(1):27–34.PubMedCrossRefGoogle Scholar
  12. 12.
    Pfaller MA, Boyken L, Messer SA, Tendolkar S, Hollis RJ, Diekema DJ. Comparison of results of voriconazole disk diffusion testing for Candida species with results from a central reference laboratory in the ARTEMIS global antifungal surveillance program. J Clin Microbiol. 2005;43(10):5208–13.PubMedCrossRefGoogle Scholar
  13. 13.
    Clinical and Laboratory Standards Institute (CLSI). Method for antifungal disk diffusion susceptibility testing of yeasts. Approved standard, M44-A. Wayne, PA; 2004.Google Scholar
  14. 14.
    Clinical and Laboratory Standards Institute (CLSI). Zone diameter interpretive standards, corresponding minimal inhibitory concentration (MIC) interpretive breakpoints, and quality control limits for antifungal disk diffusion susceptibility testing of yeasts. Informational supplement, M44-S2. Wayne, PA; 2007.Google Scholar
  15. 15.
    Clinical and Laboratory Standards Institute (CLSI). Method for antifungal disk diffusion susceptibility testing of yeasts. Approved guideline-second edition, M44-A2. Wayne, PA; 2009.Google Scholar
  16. 16.
    Clinical and Laboratory Standards Institute (CLSI). Zone diameter interpretive standards, corresponding minimal inhibitory concentration (MIC) interpretive breakpoints, and quality control limits for antifungal disk diffusion susceptibility testing of yeasts. Informational supplement, M44-S3. Wayne, PA; 2009.Google Scholar
  17. 17.
    Matar MJ, Ostrosky-Zeichner L, Paetznick VL, Rodriguez JR, Chen E, Rex JH. Correlation between E-test, disk diffusion, and microdilution methods for antifungal susceptibility testing of fluconazole and voriconazole. Antimicrob Agents Chemother. 2003;47(5):1647–51.PubMedCrossRefGoogle Scholar
  18. 18.
    Godoy P, Tiraboschi IN, Severo LC, Bustamante B, Calvo B, Almeida LP, et al. Species distribution and antifungal susceptibility profile of Candida spp. bloodstream isolates from Latin American hospitals. Mem Inst Oswaldo Cruz. 2003;98(3):401–5.PubMedCrossRefGoogle Scholar
  19. 19.
    Antunes AG, Pasqualotto AC, Diaz MC, d’Azevedo PA, Severo LC. Candidemia in a Brazilian tertiary care hospital: species distribution and antifungal susceptibility patterns. Rev Inst Med Trop Sao Paulo. 2004;46(5):239–41.PubMedCrossRefGoogle Scholar
  20. 20.
    da Matta DA, de Almeida LP, Machado AM, Azevedo AC, Kusano EJ, Travassos NF, et al. Antifungal susceptibility of 1000 Candida bloodstream isolates to 5 antifungal drugs: results of a multicenter study conducted in Sao Paulo, Brazil, 1995–2003. Diagn Microbiol Infect Dis. 2007;57(4):399–404.PubMedCrossRefGoogle Scholar
  21. 21.
    Passos XS, Costa CR, Araujo CR, Nascimento ES, e Souza LK, Fernandes Ode F, et al. Species distribution and antifungal susceptibility patterns of Candida spp. bloodstream isolates from a Brazilian tertiary care hospital. Mycopathologia. 2007;163(3):145–51.PubMedCrossRefGoogle Scholar
  22. 22.
    Ribeiro MA, Dietze R, Paula CR, Da Matta DA, Colombo AL. Susceptibility profile of vaginal yeast isolates from Brazil. Mycopathologia. 2001;151(1):5–10.PubMedCrossRefGoogle Scholar
  23. 23.
    Fricker-Hidalgo H, Vandapel O, Duchesne MA, Mazoyer MA, Monget D, Lardy B, et al. Comparison of the new API Candida system to the ID 32C system for identification of clinically important yeast species. J Clin Microbiol. 1996;34(7):1846–8.PubMedGoogle Scholar
  24. 24.
    Ramani R, Gromadzki S, Pincus DH, Salkin IF, Chaturvedi V. Efficacy of API 20C and ID 32C systems for identification of common and rare clinical yeast isolates. J Clin Microbiol. 1998;36(11):3396–8.PubMedGoogle Scholar
  25. 25.
    Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Bijie H, Dzierzanowska D, et al. Results from the ARTEMIS DISK global antifungal surveillance study, 1997 to 2007: 10.5-year analysis of susceptibilities of noncandidal yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol. 2009;47(1):117–23.PubMedCrossRefGoogle Scholar
  26. 26.
    Colombo AL, Da Matta D, De Almeida LP, Rosas R. Fluconazole susceptibility of Brazilian Candida isolates assessed by a disk diffusion method. Braz J Infect Dis. 2002;6(3):118–23.PubMedCrossRefGoogle Scholar
  27. 27.
    Pfaller MA, Hazen KC, Messer SA, Boyken L, Tendolkar S, Hollis RJ, et al. Comparison of results of fluconazole disk diffusion testing for Candida species with results from a central reference laboratory in the ARTEMIS global antifungal surveillance program. J Clin Microbiol. 2004;42(8):3607–12.PubMedCrossRefGoogle Scholar
  28. 28.
    Pfaller MA, Diekema DJ, Rex JH, Espinel-Ingroff A, Johnson EM, Andes D, et al. Correlation of MIC with outcome for Candida species tested against voriconazole: analysis and proposal for interpretive breakpoints. J Clin Microbiol. 2006;44(3):819–26.PubMedCrossRefGoogle Scholar
  29. 29.
    Pfaller MA, Diekema DJ, Sheehan DJ. Interpretive breakpoints for fluconazole and Candida revisited: a blueprint for the future of antifungal susceptibility testing. Clin Microbiol Rev. 2006;19(2):435–47.PubMedCrossRefGoogle Scholar
  30. 30.
    Aquino VR, Lunardi LW, Goldani LZ, Barth AL. Prevalence, susceptibility profile for fluconazole and risk factors for candidemia in a tertiary care hospital in southern Brazil. Braz J Infect Dis. 2005;9(5):411–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Girao E, Levin AS, Basso M, Gobara S, Gomes LB, Medeiros EA, et al. Trends and outcome of 1121 nosocomial bloodstream infections in intensive care units in a Brazilian hospital, 1999–2003. Int J Infect Dis. 2008;12(6):e145–6.PubMedCrossRefGoogle Scholar
  32. 32.
    Franca JC, Ribeiro CE, Queiroz-Telles F. Candidemia in a Brazilian tertiary care hospital: incidence, frequency of different species, risk factors and antifungal susceptibility. Rev Soc Bras Med Trop. 2008;41(1):23–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Barton R, Bijie H, et al. Geographic variation in the frequency of isolation and fluconazole and voriconazole susceptibilities of Candida glabrata: an assessment from the ARTEMIS DISK global antifungal surveillance program. Diagn Microbiol Infect Dis. 2010;67(2):162–71.PubMedCrossRefGoogle Scholar
  34. 34.
    Pasqualotto AC, Zimerman RA, Alves SH, Aquino VR, Branco D, Wiltgen D, et al. Take control over your fluconazole prescriptions: the growing importance of Candida glabrata as an agent of candidemia in Brazil. Infect Control Hosp Epidemiol. 2008;29(9):898–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Andrews JI, Fleener DK, Messer SA, Hansen WF, Pfaller MA, Diekema DJ. The yeast connection: is Candida linked to breastfeeding associated pain? Am J Obstet Gynecol. 2007;197(4):e421–4.CrossRefGoogle Scholar
  36. 36.
    Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20(1):133–63.PubMedCrossRefGoogle Scholar
  37. 37.
    Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Nagy E, Dobiasova S, et al. Candida krusei, a multidrug-resistant opportunistic fungal pathogen: geographic and temporal trends from the ARTEMIS DISK antifungal surveillance program, 2001 to 2005. J Clin Microbiol. 2008;46(2):515–21.PubMedCrossRefGoogle Scholar
  38. 38.
    Pfaller MA, Diekema DJ, Colombo AL, Kibbler C, Ng KP, Gibbs DL, et al. Candida rugosa, an emerging fungal pathogen with resistance to azoles: geographic and temporal trends from the ARTEMIS DISK antifungal surveillance program. J Clin Microbiol. 2006;44(10):3578–82.PubMedCrossRefGoogle Scholar
  39. 39.
    Colombo AL, Melo AS, Crespo Rosas RF, Salomao R, Briones M, Hollis RJ, et al. Outbreak of Candida rugosa candidemia: an emerging pathogen that may be refractory to amphotericin B therapy. Diagn Microbiol Infect Dis. 2003;46(4):253–7.PubMedCrossRefGoogle Scholar
  40. 40.
    Espinel-Ingroff A, Boyle K, Sheehan DJ. In vitro antifungal activities of voriconazole and reference agents as determined by NCCLS methods: review of the literature. Mycopathologia. 2001;150(3):101–15.PubMedCrossRefGoogle Scholar
  41. 41.
    White TC, Holleman S, Dy F, Mirels LF, Stevens DA. Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob Agents Chemother. 2002;46(6):1704–13.PubMedCrossRefGoogle Scholar
  42. 42.
    Johnson LB, Kauffman CA. Voriconazole: a new triazole antifungal agent. Clin Infect Dis. 2003;36(5):630–7.PubMedCrossRefGoogle Scholar
  43. 43.
    Panackal AA, Gribskov JL, Staab JF, Kirby KA, Rinaldi M, Marr KA. Clinical significance of azole antifungal drug cross-resistance in Candida glabrata. J Clin Microbiol. 2006;44(5):1740–3.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Ana Carolina Azevedo
    • 1
  • Fernando César Bizerra
    • 1
  • Daniel Arquimedes da Matta
    • 1
  • Leila Paula de Almeida
    • 1
  • Robert Rosas
    • 1
  • Arnaldo Lopes Colombo
    • 1
    Email author
  1. 1.Disciplina de Infectologia, Departamento de MedicinaUniversidade Federal de São PauloSão PauloBrazil

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