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Utility of Antifungal Susceptibility Testing and Clinical Correlations

  • Daniel J. Diekema
  • Michael A. Pfaller
Chapter

Abstract

In this chapter, we review the available published data addressing the clinical relevance of antifungal susceptibility test results. By far the most data exist to support the clinical relevance of AFST results for Candida against fluconazole, and these data suggest that the clinical utility of this information mirrors that put forward for antibacterial susceptibility testing. Clinical relevance has also been demonstrated for selected other antifungal agents against Candida and Cryptococcus spp. By contrast, little direct support for the clinical utility of AFST for moulds is available.

Keywords

Invasive Aspergillosis Invasive Candidiasis Antifungal Susceptibility Candida Isolate Clinical Breakpoint 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Clinical and Laboratory Standards Institute (formerly National Committee for Clinical Laboratory Standards) (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard, 3rd edn. M27-A3. Clinical and Laboratory Standards Institute, WayneGoogle Scholar
  2. 2.
    Rodriguez-Tudela JL, Barchiesi F, Bille J et al (2003) Method for the determination of minimum inhibitory concentration by broth dilution of fermentative yeasts. Clin Microbiol Infect 9:1–8CrossRefGoogle Scholar
  3. 3.
    Clinical and Laboratory Standards Institute (formerly National Committee for Clinical Laboratory Standards) (2008) Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. Approved Standard 2nd edn. M38-A2. Clinical and Laboratory Standards Institute, WayneGoogle Scholar
  4. 4.
    Rodriguez-Tudela JL, Donnelly JP, Arendrup MC et al (2008) EUCAST (European Committee for Antimicrobial Susceptibility Testing) technical note on the method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for conidia-forming moulds. Clin Microbiol Infect 14:982–984CrossRefGoogle Scholar
  5. 5.
    Clinical and Laboratory Standards Institute (formerly National Committee for Clinical Laboratory Standards) (2004) Methods for antifungal disk diffusion susceptibility testing of yeasts: approved guideline, M44-A. Clinical and Laboratory Standards Institute, WayneGoogle Scholar
  6. 6.
    Clinical and Laboratory Standards Institute (formerly National Committee for Clinical Laboratory Standards) (2008) Method for antifungal disk diffusion susceptibility testing of filamentous fungi: proposed guideline. M51-P. Clinical and Laboratory Standards Institute, WayneGoogle Scholar
  7. 7.
    Barry AL, Pfaller MA, Brown SD et al (2000) Quality control limits for broth microdilution susceptibility tests of ten antifungal agents. J Clin Microbiol 38:3457–3459PubMedGoogle Scholar
  8. 8.
    Barry AL, Bille J, Brown S et al (2003) Quality control limits for fluconazole disk susceptibility tests on Mueller-Hinton agar with glucose and methylene blue. J Clin Microbiol 41:3410–3412PubMedCrossRefGoogle Scholar
  9. 9.
    Krisher K, Brown SD, Traczewski MM (2004) Quality control parameters for broth microdilution tests of anidulafungin. J Clin Microbiol 42:490PubMedCrossRefGoogle Scholar
  10. 10.
    Pfaller MA, Diekema DJ (2002) Role of sentinel surveillance of candidemia: trends in species distribution and antifungal susceptibility. J Clin Microbiol 40:3551–3557PubMedCrossRefGoogle Scholar
  11. 11.
    Pfaller MA, Messer SA, Boyken L et al (2002) In vitro activities of 5-fluorocytosine against 8,803 clinical isolates of Candida spp.: global assessment of primary resistance using National Committee for Clinical Laboratory Standards susceptibility testing methods. Antimicrob Agents Chemother 46:3518–3521PubMedCrossRefGoogle Scholar
  12. 12.
    Pfaller MA, Messer SA, Hollis RJ et al (2002) In vitro activities of ravuconazole and voriconazole compared with those of four approved systemic antifungal agents against 6,970 clinical isolates of Candida spp. Antimicrob Agents Chemother 46:1723–1727PubMedCrossRefGoogle Scholar
  13. 13.
    Pfaller MA, Diekema DJ, Jones RN, The SENTRY Participants Group et al (2002) Trends in antifungal susceptibility of Candida spp. isolated from pediatric and adult patients with bloodstream infections: SENTRY Antimicrobial Surveillance Program, 1997 to 2000. J Clin Microbiol 40:852–856PubMedCrossRefGoogle Scholar
  14. 14.
    Pfaller MA, Messer SA, Boyken L et al (2003) Variation in susceptibility of bloodstream isolates of Candida glabrata to fluconazole according to patient age and geographic location. J Clin Microbiol 41:2176–2179PubMedCrossRefGoogle Scholar
  15. 15.
    Pfaller MA, Diekema DJ (2004) Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J Clin Microbiol 42:4419–4431PubMedCrossRefGoogle Scholar
  16. 16.
    Pfaller MA, Diekema DJ (2004) Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 10(suppl 1):11–23PubMedCrossRefGoogle Scholar
  17. 17.
    Pfaller MA, Messer SA, Boyken L et al (2004) Further standardization of broth microdilution methodology for in vitro susceptibility testing of caspofungin against Candida species by sue of an international collection of more than 3,000 clinical isolates. J Clin Microbiol 42:3117–3119PubMedCrossRefGoogle Scholar
  18. 18.
    Pfaller MA, Hazen KC, Messer SA et al (2004) 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 42:3607–3612PubMedCrossRefGoogle Scholar
  19. 19.
    Pfaller MA, Boyken L, Messer SA et al (2004) Evaluation of the Etest method using Mueller-Hinton agar with glucose and methylene blue for determining amphotericin B MICs for 4,936 clinical isolates of Candida species. J Clin Microbiol 42:4977–4979PubMedCrossRefGoogle Scholar
  20. 20.
    Pfaller MA, Messer SA, Boyken L et al (2004) Geographic variation in the susceptibilities of invasive isolates of Candida glabrata to seven systemically active antifungal agents: a global assessment from the ARTEMIS Antifungal Surveillance Program conducted in 2001 and 2002. J Clin Microbiol 42:3142–3146PubMedCrossRefGoogle Scholar
  21. 21.
    Pfaller MA, Messer SA, Boyken L, Hollis RJ et al (2004) In vitro activities of voriconazole, posaconazole, and fluconazole against 4,169 clinical isolates of Candida spp. and Cryptococcus neoformans collected during 2001 and 2002 in the ARTEMIS global antifungal surveillance program. Diagn Microbiol Infect Dis 48:201–205PubMedCrossRefGoogle Scholar
  22. 22.
    Pfaller MA, Boyken L, Hollis RJ et al (2005) In vitro susceptibilities of clinical isolates of Candida species, Cryptococcus neoformans, and Aspergillus species to itraconazole: global survey of 9,359 isolates tested by Clinical and Laboratory Standards Institute broth microdilution methods. J Clin Microbiol 43:3807–3810PubMedCrossRefGoogle Scholar
  23. 23.
    Pfaller MA, Boyken L, Hollis RJ et al (2005) In vitro activities of anidulafungin against more than 2,500 clinical isolates of Candida spp., including 315 isolates resistant to fluconazole. J Clin Microbiol 43:5425–5427PubMedCrossRefGoogle Scholar
  24. 24.
    Pfaller MA, Diekema DJ, Rinaldi MG, The Global Antifungal Surveillance Group et al (2005) Results from the ARTEMIS DISK Global Antifungal Surveillance Study: a 6.5-year analysis of susceptibilities of Candida and other yeast species to fluconazole and voriconazole by standardized disk diffusion testing. J Clin Microbiol 43:5848–5859PubMedCrossRefGoogle Scholar
  25. 25.
    Pfaller MA, Boyken L, Messer SA et al (2005) 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 43:5208–5213PubMedCrossRefGoogle Scholar
  26. 26.
    Pfaller MA, Boyken L, Hollis RJ et al (2006) In vitro susceptibilities of Candida spp. to caspofungin: four years of global surveillance. J Clin Microbiol 44:760–763PubMedCrossRefGoogle Scholar
  27. 27.
    Pfaller MA, Diekema DJ, Rex JH et al (2006) Correlation of MIC with outcome for Candida species tested against voriconazole: analysis and proposal for interpretive breakpoints. J Clin Microbiol 44:819–826PubMedCrossRefGoogle Scholar
  28. 28.
    Pfaller MA, Diekema DJ, Sheehan DJ (2006) Interpretive breakpoints for fluconazole and Candida revisited: a blueprint for the future of antifungal susceptibility testing. Clin Microbiol Rev 19:435–447PubMedCrossRefGoogle Scholar
  29. 29.
    Pfaller MA, Boyken L, Hollis RJ et al (2006) Global surveillance of the in vitro activity of micafungin against Candida: a comparison with caspofungin using Clinical and Laboratory Standards Institute recommended methods. J Clin Microbiol 44:3533–3538PubMedCrossRefGoogle Scholar
  30. 30.
    Pfaller MA, Messer SA, Hollis RJ, Boyken L, Tendolkar S, Kroeger J, Diekema DJ (2009) Variation in susceptibility of bloodstream isolates of Candida glabrata to fluconazole according to patient age and geographic location in the U.S., 2001–2007. J Clin Microbiol 47:3185–3190PubMedCrossRefGoogle Scholar
  31. 31.
    Pfaller MA, Diekema DJ, Ghannoum A et al (2009) Wild type MIC distribution and epidemiologic cutoff values for Aspergillus fumigatus and three triazoles as determined by the CLSI broth microdilution methods. J Clin Microbiol 47:3142–3146PubMedCrossRefGoogle Scholar
  32. 32.
    Diekema DJ, Messer SA, Boyken LD, Hollis RJ, Kroeger J, Tendolkar S, Pfaller MA (2009) In vitro activity of seven systemically active antifungal agents against a large global collection of rare Candida species as determined by CLSI broth microdilution methods. J Clin Microbiol 47:3170–3177PubMedCrossRefGoogle Scholar
  33. 33.
    Diekema DJ, Messer SA, Hollis RJ, Boyken L, Tendolkar S, Kroeger J, Jones RN, Pfaller MA (2009) A global evaluation of voriconazole activity tested against recent clinical isolates of Candida spp. Diagn Microbiol Infect Dis 63:233–236PubMedCrossRefGoogle Scholar
  34. 34.
    Pfaller MA, Diekema DJ, Ostrosky-Zeichner L et al (2008) Correlation of MIC with outcome for Candida species tested against caspofungin, anidulafungin, and micafungin: analysis and proposal for interpretive MIC breakpoints. J Clin Microbiol 46:2620–2629PubMedCrossRefGoogle Scholar
  35. 35.
    Pfaller MA, Messer SA, Bolmstrom A (1998) Evaluation of Etest for determining in vitro susceptibility of yeast isolates to amphotericin B. Diagn Microbiol Infect Dis 32:223–227PubMedCrossRefGoogle Scholar
  36. 36.
    Espinel Ingroff A, Pfaller MA, Messer SA et al (2004) Multicenter comparison of the Sensititre YeastOne colorimetric antifungal panel with the NCCLS M27-A2 reference method for testing new antifungal agents against clinical isolates of Candida spp. J Clin Microbiol 42:718–721PubMedCrossRefGoogle Scholar
  37. 37.
    Pfaller MA, Diekema DJ, Procop GW, Rinaldi MG (2007) Multicenter comparison of the VITEK 2 yeast susceptibility test with the CLSI broth microdilution reference method for testing fluconazole against Candida spp. J Clin Microbiol 45:796–802PubMedCrossRefGoogle Scholar
  38. 38.
    Pfaller MA, Diekema DJ, Procop GW, Rinaldi MG (2007) Multicenter comparison of the VITEK 2 yeast susceptibility test with the CLSI broth microdilution reference method for testing amphotericin B, flucytosine, and voriconazole against Candida spp. J Clin Microbiol 45:3522–3528PubMedCrossRefGoogle Scholar
  39. 39.
    Torres-Rodriguez JM, Alvarado-Ramirez E (2007) In vitro susceptibilities to yeasts using the ATB FUNGUS 2 method compared to Sensititre YeastOne and standard CLSI M27-A2 methods. J Antimicrob Chemother 60:658PubMedCrossRefGoogle Scholar
  40. 40.
    Rex JH, Pfaller MA (2002) Has antifungal susceptibility testing come of age? Clin Infect Dis 35:982–989PubMedCrossRefGoogle Scholar
  41. 41.
    Rex JH, Pfaller MA, Galgiani JN et al (1997) Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro – in vivo correlation data for fluconazole, itraconazole, and Candida infections. Clin Infect Dis 24:235–247PubMedCrossRefGoogle Scholar
  42. 42.
    Rex JH, Pfaller MA, Walsh TJ et al (2001) Antifungal susceptibility testing: practical aspects and current challenges. Clin Microbiol Rev 14:643–658PubMedCrossRefGoogle Scholar
  43. 43.
    Andes D (2003) Clinical pharmacodynamics of antifungals. Infect Dis Clin N Am 17:635–649CrossRefGoogle Scholar
  44. 44.
    Andes D (2003) In vivo pharmacodynamics of antifungal drugs in treatment of candidiasis. Antimicrob Agents Chemother 47:1179–1186PubMedCrossRefGoogle Scholar
  45. 45.
    Andes D, Marchill K, Lawther J et al (2003) In vivo pharmacodynamics of HMR 3270, a glucan synthase inhibitor, in a murine candidiasis model. Antimicrob Agents Chemother 47:1187–1192PubMedCrossRefGoogle Scholar
  46. 46.
    Voss A, de Pauw BE (1999) High-dose fluconazole therapy in patients with severe fungal infections. Eur J Clin Microbiol Infect Dis 18:165–174PubMedCrossRefGoogle Scholar
  47. 47.
    Morrell M, Fraser VJ, Kollef MJ (2005) Delaying empiric treatment of Candida bloodstream infection until positive blood culture results are obtained: a potential risk factor for mortality. Antimicrob Agents Chemother 49:3640PubMedCrossRefGoogle Scholar
  48. 48.
    Garey KW, Rege M, Pai MP et al (2006) Time to initiation of fluconazole therapy impacts mortality in patients with candidemia: a multi-institutional study. Clin Infect Dis 43:25PubMedCrossRefGoogle Scholar
  49. 49.
    Collins CD, Eschenauer GA, Salo SL, Newton DW (2007) To test or not to test: a cost minimization analysis of susceptibility testing for patients with documented Candida glabrata fungemias. J Clin Microbiol 45:1884PubMedCrossRefGoogle Scholar
  50. 50.
    Perkins MD, Sabuda DM, Elsayed S, Laupland KB (2007) Adequacy of empirical antifungal therapy and effect of outcome among patients with invasive Candida species infections. J Antimicrob Chemother 60:613CrossRefGoogle Scholar
  51. 51.
    Ostrosky-Zeichner L, Rex JH, Pfaller MA et al (2008) Rationale for reading fluconazole MICs at 24h rather than 48h when testing Candida spp. by the CLSI M27-A2 standard method. Antimicrob Agents Chemother 52:4175–4177PubMedCrossRefGoogle Scholar
  52. 52.
    Pfaller MA, Boyken LB, Hollis RJ et al (2008) Validation of 24-hour fluconazole MIC readings versus the CLSI 48-hour broth microdilution reference method: results from a global Candida antifungal surveillance program. J Clin Microbiol 46:3585–3590PubMedCrossRefGoogle Scholar
  53. 53.
    Pappas PG, Kauffman CA, Andes D et al (2009) Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 48:503–535PubMedCrossRefGoogle Scholar
  54. 54.
    Andes D, van Ogtrop M (1999) Characterization and quantitation of the pharmacodynamics of fluconazole in a neutropenic murine disseminated candidiasis infection model. Antimicrob Agents Chemother 43:2116–2120PubMedGoogle Scholar
  55. 55.
    Louie A, Drusano GL, Banerjee P et al (1998) Pharmacodynamics of fluconazole in a murine model of systemic candidiasis. Antimicrob Agents Chemother 42:1105–1109PubMedGoogle Scholar
  56. 56.
    Rodriguez-Tudela JL, Almirante B, Rodriguez-Pardo D et al (2007) Correlation of the MIC and Dose/MIC ratio of fluconazole to the therapeutic response of patients with mucosal candidiasis and candidemia. Antimicrob Agents Chemother 51:3599–3604PubMedCrossRefGoogle Scholar
  57. 57.
    Cuesta I, Bielza C, Larranaga P et al (2009) Data mining validation of fluconazole breakpoints established by the European Committee on Antimicrobial Susceptibility Testing. Antimicrob Agents Chemother 53:2949–2954PubMedCrossRefGoogle Scholar
  58. 58.
    Pfaller MA, Andes D, Diekema DJ, Espinel-Ingroff A, Sheehan D, The CLSI Subcommittee for Antifungal Susceptibility Testing (2010) Wild-type MIC distributions, epidemiological cutoff values and species-specific clinical breakpoints for fluconazole and Candida: time for harmonization of CLSI and EUCAST broth microdilution methods. Drug Resist Updat 13:180–195PubMedCrossRefGoogle Scholar
  59. 59.
    Ostrosky-Zeichner L, Oude Lashof AML, Kullberg BJ (2003) Voriconazole salvage treatment of invasive candidiasis. Eur J Clin Microbiol Infect Dis 22:651–655PubMedCrossRefGoogle Scholar
  60. 60.
    Kartsonis NA, Saah A, Lipka CJ et al (2004) Second-line therapy with caspofungin for mucosal or invasive candidiasis: results from the caspofungin compassionate use study. J Antimicrob Chemother 53:878–881PubMedCrossRefGoogle Scholar
  61. 61.
    Rodriguez-Tudela JL, Donnelly JP, Arendrup MC et al (2008) EUCAST technical note on voriconazole. Clin Microbiol Infect 14:985–987CrossRefGoogle Scholar
  62. 62.
    Pfaller MA, Andes D, Arendrup MC et al (2011) Clinical breakpoints for voriconazole and Candida spp. revisited: review of microbiologic, molecular, pharmacodynamic, and clinical data as they pertain to the development of species-specific interpretive criteria. Diagn Microbiol Infect Dis 70:330–343PubMedCrossRefGoogle Scholar
  63. 63.
    Park BJ, Arthington-Skaggs BA, Hajjeh RA et al (2006) Evaluation of amphotericin B interpretive breakpoints for Candida bloodstream isolates by correlation with therapeutic outcome. Antimicrob Agents Chemother 50:1287–1292PubMedCrossRefGoogle Scholar
  64. 64.
    Clancy CJ, Nguyen MH (1999) Correlation between in vitro susceptibility determined by Etest and response to therapy with amphotericin B: results from a multicenter prospective study of candidemia. Antimicrob Agents Chemother 43:1289–1290PubMedGoogle Scholar
  65. 65.
    Gibbs WJ, Drew RH, Perfect JR (2005) Liposomal amphotericin B: clinical experience and perspectives. Expert Rev Anti Infect Ther 3:167–181PubMedCrossRefGoogle Scholar
  66. 66.
    Krogh-Madsen M, Arendrup MC, Heslet L et al (2006) Amphotericin B and caspofungin resistance in Candida glabrata isolates recovered from a critically ill patient. Clin Infect Dis 42:938–944PubMedCrossRefGoogle Scholar
  67. 67.
    Law D, Moore CB, Denning DW (1997) Amphotericin B resistance testing of Candida spp.: a comparison of methods. J Antimicrob Chemother 40:109–112PubMedCrossRefGoogle Scholar
  68. 68.
    Nguyen MH, Clancy CJ, Yu VL et al (1998) So in vitro susceptibility data predict the microbiologic response to amphotericin B? Results of a prospective study of patients with Candida fungemia. J Infect Dis 177:425–430PubMedCrossRefGoogle Scholar
  69. 69.
    Nolte FS, Parkinson T, Falconer DJ et al (1997) Isolation and characterization of fluconazole- and amphotericin B-resistant Candida albicans from blood of two patients with leukemia. Antimicrob Agents Chemother 44:196–199Google Scholar
  70. 70.
    Sterling TR, Gasser RA, Ziegler A (1996) Emergence of resistance to amphotericin B during therapy for Candida glabrata infection in an immunocompetent host. Clin Infect Dis 23:187–188PubMedCrossRefGoogle Scholar
  71. 71.
    Sterling T, Merz WG (1998) Resistance to amphotericin B: emerging clinical and microbiological patterns. Drug Resist Updat 1:161–165PubMedCrossRefGoogle Scholar
  72. 72.
    Wanger A, Mills K, Nelson PW et al (1995) Comparison of Etest and National Committee for Clinical Laboratory Standards broth macrodilution method for antifungal susceptibility ­testing: enhanced ability to detect amphotericin B-resistant Candida isolates. Antimicrob Agents Chemother 39:2520–2522PubMedGoogle Scholar
  73. 73.
    McClenny NB, Fei H, Baron EJ et al (2002) Change in colony morphology of Candida lusitaniae in association with development of amphotericin B resistance. Antimicrob Agents Chemother 46:1325–1328PubMedCrossRefGoogle Scholar
  74. 74.
    O’Day M, Ray WA, Robinson RD et al (1987) Correlation of in vitro and in vivo susceptibility of Candida albicans to amphotericin B and natamycin. Investig Ophthalmol Vis Sci 29:596–603Google Scholar
  75. 75.
    Canton E, Peman J, Gobernado M et al (2004) Patterns of amphotericin B killing kinetics against seven Candida species. Antimicrob Agents Chemother 48:2477–2482PubMedCrossRefGoogle Scholar
  76. 76.
    Spellberg BJ, Filler SG, Edwards JE Jr (2006) Current treatment strategies for disseminated candidiasis. Clin Infect Dis 42:244–251PubMedCrossRefGoogle Scholar
  77. 77.
    Blignant E, Molepo J, Pujol C et al (2005) Clade-related amphotericin B resistance among South African Candida albicans isolates. Diagn Microbiol Infect Dis 53:29–31CrossRefGoogle Scholar
  78. 78.
    Hajjeh RA, Sofair AN, Harrison IH et al (2004) Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol 42:1519–1527PubMedCrossRefGoogle Scholar
  79. 79.
    Kao AS, Brandt ME, Pruitt WR et al (1999) The epidemiology of candidemia n two United States cities: results of a population-based active surveillance. Clin Infect Dis 29:1164–1170PubMedCrossRefGoogle Scholar
  80. 80.
    Yang YL, Li SY, Chang HH (2005) Susceptibilities to amphotericin B and fluconazole of Candida species in TSARY 2002. Diagn Microbiol Infect Dis 51:179–183PubMedCrossRefGoogle Scholar
  81. 81.
    Favel A, Michel-Nguyen A, Datry A et al (2004) Susceptibility of clinical isolates of C. lusitaniae to five systemic antifungal agents. J Antimicrob Chemother 53:526–529PubMedCrossRefGoogle Scholar
  82. 82.
    Hawkins JL, Baddour LM (2003) Candida lusitaniae infections in the era of fluconazole availability. Clin Infect Dis 36:e14–e18PubMedCrossRefGoogle Scholar
  83. 83.
    Minari A, Hachem R, Raad I (2001) Candida lusitaniae: a cause of breakthrough fungemia in cancer patients. Clin Infect Dis 32:186–190PubMedCrossRefGoogle Scholar
  84. 84.
    Peyron F, Favel A, Michel-Nguyen A et al (2001) Improved detection of amphotericin B-resistant isolates of Candida lusitaniae by Etest. J Clin Microbiol 39:339–342PubMedCrossRefGoogle Scholar
  85. 85.
    Miller NS, Dick JD, Merz WG (2006) Phenotypic switching in Candida lusitaniae on copper sulfate indicator agar: association with amphotericin B resistance and filamentation. J Clin Microbiol 44:1536–1539PubMedCrossRefGoogle Scholar
  86. 86.
    Yoon SA, Vazquez JA, Stefan PE et al (1999) High-frequency, in vitro reversible switching of Candida lusitaniae clinical isolates from amphotericin B susceptibility to resistance. Antimicrob Agents Chemother 43:836–845PubMedGoogle Scholar
  87. 87.
    Bartizal K, Odds FC (2003) Influences of methodological variables on susceptibility testing of caspofungin against Candida species and Aspergillus fumigatus. Antimicrob Agents Chemother 47:2100–2107PubMedCrossRefGoogle Scholar
  88. 88.
    Odds FC, Motyl M, Andrade R et al (2004) Interlaboratory comparison of results of susceptibility testing with caspofungin against Candida and Aspergillus species. J Clin Microbiol 42:3475–3482PubMedCrossRefGoogle Scholar
  89. 89.
    Park S, Kelly R, Kahn JN et al (2005) Specific substitutions in the echinocandins target Fks1p account for reduced susceptibility of rare laboratory and clinical Candida sp. isolates. Antimicrob Agents Chemother 49:3264–3273PubMedCrossRefGoogle Scholar
  90. 90.
    Pfaller MA, Boyken L, Hollis RJ, Kroeger J, Messer S, Tendolkar S, Jones RN, Turnidge J, Diekema DJ (2010) Wild-type MIC distributions and epidemiological cutoff values (ECVs) for the echinocandins and Candida spp. J Clin Microbiol 48(1):52–56PubMedCrossRefGoogle Scholar
  91. 91.
    Chandrasekar PH, Sobel JD (2006) Micafungin: a new echinocandins. Clin Infect Dis 42:1171–1178PubMedCrossRefGoogle Scholar
  92. 92.
    Colombo AL, Melo ASA, Rosas RFC et al (2003) Outbreak of Candida rugosa candidemia: an emerging pathogen that may be refractory to amphotericin B therapy. Diagn Microbiol Infect Dis 46:253–257PubMedCrossRefGoogle Scholar
  93.  93.
    Colombo AL, Perect J, DiNubile M et al (2003) Global distribution and outcomes for Candida species causing invasive candidiasis: results from an international randomized double-blind study of caspofungin versus amphotericin B for the treatment of invasive candidiasis. Eur J Clin Microbiol Infect Dis 22:470–474PubMedCrossRefGoogle Scholar
  94.  94.
    Glasmacher A, Cornely OA, Orlopps K et al (2006) Caspofungin treatment in severely ill, immunocompromised patients: a case-documentation study of 118 patients. J Antimicrob Chemother 57:127–134PubMedCrossRefGoogle Scholar
  95.  95.
    Kartsonis N, Killar J, Mixson L et al (2005) Caspofungin susceptibility testing of isolates from patients with esophageal candidiasis or invasive candidiasis: relationship of MIC to treatment outcome. Antimicrob Agents Chemother 49:3616–3623PubMedCrossRefGoogle Scholar
  96.  96.
    Krause DS, Reinhardt J, Vazquez JA et al (2004) Phase, randomized dose-ranging study evaluating the safety and efficacy of anidulafungin in invasive candidiasis and candidemia. Antimicrob Agents Chemother 48:2021–2024PubMedCrossRefGoogle Scholar
  97.  97.
    Mora-Duarte J, Betts R, Rotstein C et al (2002) Comparison of caspofungin and amphotericin B for invasive candidiasis. N Engl J Med 347:2020–2029PubMedCrossRefGoogle Scholar
  98.  98.
    Ostrosky-Zeichner L, Kontoyiannis D, Raffalii J et al (2005) International, open-label, noncomparative, clinical trial of micafungin alone and in combination for treatment of newly diagnosed and refractory candidemia. Eur J Clin Microbiol Infect Dis 24:654–661PubMedCrossRefGoogle Scholar
  99.  99.
    Reboli AC, Rotstein C, Pappas PG et al (2007) Anidulafungin versus fluconazole for invasive candidiasis. N Engl J Med 356:2472–2482PubMedCrossRefGoogle Scholar
  100. 100.
    Pappas PG, Rotstein CM, Betts RF et al (2007) Micafungin versus caspofungin for treatment of candidemia and other forms of invasive candidiasis. Clin Infect Dis 45:883–893PubMedCrossRefGoogle Scholar
  101. 101.
    Cappelletty D, Eiselstein-McKitrick K (2007) The echinocandins. Pharmacotherapy 27(3):369PubMedCrossRefGoogle Scholar
  102. 102.
    Perlin DS (2007) Resistance to echinocandins-class antifungal drugs. Drug Resist Updat 10:121PubMedCrossRefGoogle Scholar
  103. 103.
    Baixench MT, Aoun N, Desnos-Ollivier M et al (2007) Acquired resistance to echinocandins in Candida albicans: case report and review. J Antimicrob Chemother 59:1076PubMedCrossRefGoogle Scholar
  104. 104.
    Louie A, Deziel M, Liu W et al (2005) Pharmacodynamics of caspofungin in a murine model of systemic candidiasis: importance of persistence of caspofungin in tissues to understanding drug activity. Antimicrob Agents Chemother 49:5058–5068PubMedCrossRefGoogle Scholar
  105. 105.
    Andes D, Diekema DJ, Pfaller MA et al (2008) In vivo pharmacodynamic characterization of anidulafungin in a neutropenic murine candidiasis model. Antimicrob Agents Chemother 52:539–550PubMedCrossRefGoogle Scholar
  106. 106.
    Andes D, Diekema DJ, Pfaller MA et al (2008) In vivo pharmacodynamic target investigation for micafungin against C. albicans and C. glabrata in a neutropenic murine candidiasis model. Antimicrob Agents Chemother 52:3497–3503PubMedCrossRefGoogle Scholar
  107. 107.
    Kuse ER, Chutchotisakd P, da Cunha CA et al (2007) Micafungin versus liposomal amphotericin B for candidemia and invasive candidiasis: a phase III randomized double-blind trial. Lancet 369:1519PubMedCrossRefGoogle Scholar
  108. 108.
    Hernandez S, Lopez-Ribot JL, Najvor LK et al (2004) Caspofungin resistance in Candida albicans: correlating clinical outcome with laboratory susceptibility testing of three isogenic isolates serially obtained from a patient with progressive Candida esophagitis. Antimicrob Agents Chemother 48:1382–1383PubMedCrossRefGoogle Scholar
  109. 109.
    Dodgson KJ, Dodgson AR, Pujol C et al (2005) Caspofungin resistant C. glabrata. Clin Microbiol Infect 11(suppl 2):364Google Scholar
  110. 110.
    Moudgal V, Little T, Boikov D et al (2005) Multiechinocandin- and multiazole-resistant Candida parapsilosis isolates serially obtained during therapy for prosthetic valve endocarditis. Antimicrob Agents Chemother 49:767–769PubMedCrossRefGoogle Scholar
  111. 111.
    Laverdiere M, Lalonde RG, Baril JG et al (2006) Progressive loss of echinocandins activity following prolonged use for treatment of Candida albicans oesophagitis. J Antimicrob Chemother 57:705–708PubMedCrossRefGoogle Scholar
  112. 112.
    Thompson GR, Wiederhold NP, Vallor AC et al (2008) Development of caspofungin resistance following prolonged therapy for invasive candidiasis secondary to Candida glabrata infection. Antimicrob Agents Chemother 52:3783–3785PubMedCrossRefGoogle Scholar
  113. 113.
    Garcia-Effron G, Kontoyiannis DP, Lewis RE, Perlin DS (2008) Caspofungin-resistant Candida tropicalis strains causing breakthrough fungemia in patients at high risk for hematologic malignancies. Antimicrob Agents Chemother 52:4181–4183PubMedCrossRefGoogle Scholar
  114. 114.
    Garcia-Effron G, Park S, Perlin DS (2009) Correlating echinocandin MIC and kinetic inhibition of FKS1 mutant glucan synthases for Candida albicans: implications for interpretive breakpoints. Antimicrob Agents Chemother 53:112–122PubMedCrossRefGoogle Scholar
  115. 115.
    Garcia-Effron G, Lee S, Park S et al (2009) Effect of Candida glabrata FKS1 and FKS2 mutations on echinocandin sensitivity and kinetics of 1, 3-beta-D glucan synthase: implication for the existing susceptibility breakpoint. Antimicrob Agents Chemother 53:3690–3699PubMedCrossRefGoogle Scholar
  116. 116.
    Pfaller MA, Diekema DJ, Andes D, Arendrup MC, Brown SD, Lockhart SR, Motyl M, Perlin D, The CLSI Subcommittee for Antifungal Testing (2011) Clinical breakpoints for the echinocandins and Candida revisited: integration of molecular, clinical, and microbiological data to arrive at species-specific interpretive criteria. Drug Resist Updat 14:164–176PubMedCrossRefGoogle Scholar
  117. 117.
    Denning DW, Radford SA, Oakley KL et al (1997) Correlation between in-vitro susceptibility testing to itraconazole and in-vivo outcome of Aspergillus fumigatus infection. J Antimicrob Chemother 40:401–414PubMedCrossRefGoogle Scholar
  118. 118.
    Mosquera J, Warn PA, Morrissey J et al (2001) Susceptibility testing of Aspergillus flavus: inoculum dependence with itraconazole and lack of correlation between susceptibility to amphotericin B in vitro and outcome in vivo. Antimicrob Agents Chemother 45:1456–1462PubMedCrossRefGoogle Scholar
  119. 119.
    Johnson EM, Oakley KL, Radford SA et al (2000) Lack of correlation of in vitro amphotericin B susceptibility testing with outcome in a murine model of Aspergillus infection. J Antimicrob Chemother 45:85–93PubMedCrossRefGoogle Scholar
  120. 120.
    Lass-Florl C, Kofler G, Kropshofer G et al (1998) In-vitro testing of susceptibility to amphotericin B is a reliable predictor of clinical outcome in invasive aspergillosis. J Antimicrob Chemother 42:497–502PubMedCrossRefGoogle Scholar
  121. 121.
    Steinbach WJ, Benjamin DK, Kontoyiannis DP et al (2004) Infections due to Aspergillus terreus: a multicenter retrospective analysis of 83 cases. Clin Infect Dis 39:192–198PubMedCrossRefGoogle Scholar
  122. 122.
    Steinbach WJ, Perfect JR, Schell WA et al (2004) In vitro analyses, animal models, and 60 clinical cases of invasive Aspergillus terreus infection. Antimicrob Agents Chemother 48:3217–3225PubMedCrossRefGoogle Scholar
  123. 123.
    Lionakis MS, Lewis RE, Chamilos G et al (2005) Aspergillus susceptibility testing in patients with cancer and invasive aspergillosis: difficulties in establishing correlation between in vitro susceptibility data and the outcome of initial amphotericin B therapy. Pharmacotherapy 25:1174–1180PubMedCrossRefGoogle Scholar
  124. 124.
    Howard SJ, Cerar D, Anderson MJ et al (2009) Frequency and evolution of azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis 15:1068–1076PubMedCrossRefGoogle Scholar
  125. 125.
    Denning DW, Vankateswarlu K, Oakley KL et al (1997) Itraconazole resistance in Aspergillus fumigatus. Antimicrob Agents Chemother 41:1364–1368PubMedGoogle Scholar
  126. 126.
    Verweij PE, Mellado E, Melchers WJG (2007) Multiple-triazole-resistant aspergillosis. N Engl J Med 356:1481PubMedCrossRefGoogle Scholar
  127. 127.
    Rodriguez-Tudela JL, Alcazar-Fuoli L, Mellado E et al (2008) Epidemiological cutoffs and cross-resistance to azole drugs in Aspergillus fumigatus. Antimicrob Agents Chemother 52:2468PubMedCrossRefGoogle Scholar
  128. 128.
    Diekema DJ, Messer SA, Hollis RJ et al (2003) Activities of caspofungin, itraconazole, posaconazole, ravuconazole, voriconazole, and amphotericin B against 448 recent clinical isolates of filamentous fungi. J Clin Microbiol 41:3623–3626PubMedCrossRefGoogle Scholar
  129. 129.
    Greenberg RN, Mullane K, van Burik JA et al (2006) Posaconazole as salvage therapy for zygomycosis. Antimicrob Agents Chemother 50:126–133PubMedCrossRefGoogle Scholar
  130. 130.
    van Burik JAH, Hare RS, Solomon HF et al (2006) Posaconazole is effective as salvage therapy in zygomycosis: a retrospective summary of 91 cases. Clin Infect Dis 42:e61–e65PubMedCrossRefGoogle Scholar
  131. 131.
    Jessup CJ, Pfaller MA, Messer SA et al (1998) Fluconazole susceptibility testing of Cryptococcus neoformans: comparison of two broth microdilution methods and clinical correlates among isolates from Ugandan AIDS patients. J Clin Microbiol 36:2874–2876PubMedGoogle Scholar
  132. 132.
    Witt MD, Lewis RJ, Larsen RA et al (1996) Identification of patients with acute AIDS-associated cryptococcal meningitis who can be effectively treated with fluconazole: the role of antifungal susceptibility testing. Clin Infect Dis 22:322–328PubMedCrossRefGoogle Scholar
  133. 133.
    Aller AL, Martin-Mazuelos E, Lozano F et al (2000) Correlation of fluconazole MICs with clinical outcome in cryptococcal infection. Antimicrob Agents Chemother 44:1544–1548PubMedCrossRefGoogle Scholar
  134. 134.
    Dannaoui E, Abdul M, Michel-Nguyen A et al (2006) Results obtained with various antifungal susceptibility testing methods do not predict early clinical outcome in patients with cryptococcosis. Antimicrob Agents Chemother 50:2464–2470PubMedCrossRefGoogle Scholar
  135. 135.
    Wheat LJ, Connolly P, Smedema M et al (2001) Emergence of resistance to fluconazole as a cause of failure during treatment of histoplasmosis in patients with acquired immunodeficiency syndrome. Clin Infect Dis 33:1910–1913PubMedCrossRefGoogle Scholar
  136. 136.
    Walsh T, Annaissie EJ, Denning DW et al (2008) Treatment of Aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 46:327–360PubMedCrossRefGoogle Scholar
  137. 137.
    Chapman SW, Dismukes WE, Proia LA et al (2008) Clinical practice guidelines for the management of Blastomycosis: 2008 update by the Infectious Diseases Society of America. Clin Infect Dis 46:1801–1812PubMedCrossRefGoogle Scholar
  138. 138.
    Galgiani JN, Ampel NM, Blair JE et al (2005) Coccidioidomycosis. Clin Infect Dis 41:1217–1223PubMedCrossRefGoogle Scholar
  139. 139.
    Saag MS, Graybill RJ, Larsen RA et al (2000) Practice guidelines for the management of cryptococcal disease. Clin Infect Dis 30:710–718PubMedCrossRefGoogle Scholar
  140. 140.
    Wheat LJ, Friefeld AG, Kleiman MB et al (2007) Clinical practice guidelines for the management of patients with histoplasmosis: 2007 update by the Infectious Diseases Society of America. Clin Infect Dis 45:807–825PubMedCrossRefGoogle Scholar
  141. 141.
    Kauffman C, Bustamante B, Chapman SW, Pappas PG (2007) Clinical practice guidelines for the management of patients with sporotrichosis: 2007 update by the Infectious Diseases Society of America. Clin Infect Dis 45:1255–1265PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Division of Infectious Diseases, Department of Internal MedicineUniversity of Iowa Carver College of MedicineIowa CityUSA
  2. 2.University of Iowa College of Public HealthIowa CityUSA
  3. 3.Division of Clinical Microbiology, Department of PathologyUniversity of Iowa Carver College of MedicineIowa CityUSA

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