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

Pfaller, Michael A.; Andes, David; Arendrup, Maiken C.; Diekema, Daniel J.; Espinel-Ingroff, Ana; Alexander, Barbara D.; Brown, Steven D.; Chaturvedi, Vishnu; Fowler, Cynthia L.; Ghannoum, Mahmoud A.; Johnson, Elizabeth M.; Knapp, Cynthia C.; Motyl, Mary R.; Ostrosky-Zeichner, Luis; Walsh, Thomas J.

doi:10.1016/j.diagmicrobio.2011.03.002

Cited by 130Antifungal resistance and susceptibilityBacterial Identification and Susceptibility TestingFungal Plant Pathogen Control

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

Pfaller, Michael A., Andes, David, Arendrup, Maiken C., Diekema, Daniel J., Espinel-Ingroff, Ana, Alexander, Barbara D., Brown, Steven D., Chaturvedi, Vishnu +7 more·2011·Diagnostic Microbiology and Infectious Disease

DOI 10.1016/j.diagmicrobio.2011.03.002

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Abstract

We reassessed the Clinical and Laboratory Standards Institute (CLSI) clinical breakpoints (CBPs) for voriconazole. We examined i) the essential (EA: ±2 dilutions) and categorical agreement between 24-h CLSI and EUCAST methods for voriconazole testing of Candida, ii) wild-type (WT) MICs and epidemiologic cutoff values (ECVs) for voriconazole by both CLSI and EUCAST methods, and iii) correlation of MICs with outcomes from previously published data using CLSI methods. We applied these findings to propose new 24-h species-specific CLSI CBPs. Adjusted 24-h CBPs for voriconazole and C. albicans, C. tropicalis, and C. parapsilosis (susceptible, ≤ 0.125 μg/mL; intermediate, 0.25-0.5 μg/mL; resistant, ≥ 1 μg/mL) should be more sensitive for detecting emerging resistance among common Candida species and provide consistency with EUCAST CBPs. In the absence of CBPs for voriconazole and C. glabrata (and less common species), we recommend that their respective ECVs be used to detect the emergence of non-WT strains.

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Inherently resistant Candida spp. have become more common among clinical isolates during treatment.
“Consequently, inherently resistant Candida spp. have become more common among clinical isolates during treatment (1).”
From Azole Susceptibility and Transcriptome Profiling in Candida albicans Mitochondrial Electron Transport Chain Complex I Mutants (2013) · cites this paper as [1]

Voriconazole versus Amphotericin B for Primary Therapy of Invasive Aspergillosis
Herbrecht, R., Denning, D. W., Patterson, T. F., Bennett, J. E., Greene, R. E., Oestmann, J.-W., Kern, W. V., Marr, K. A., Ribaud, P., Lortholary, O., et al. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa020191 · Cited by 3,304 · see citing works
Clinical Practice Guidelines for the Management Candidiasis: 2009 Update by the Infectious Diseases Society of America
Pappas, P. G., Kauffman, C. A., Andes, D., Benjamin, D. K., Calandra, T. F., Edwards, J. E., Filler, S. G., Fisher, J. F., Kullberg, B.-J., Zeichner, L. O., et al. (2009) · Clinical Infectious Diseases · doi:10.1086/596757 · Cited by 3,191 · see citing works
Self-citation
Delaying the Empiric Treatment of Candida Bloodstream Infection until Positive Blood Culture Results Are Obtained: a Potential Risk Factor for Hospital Mortality
Morrell, M., Fraser, V. J., & Kollef, M. H. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.9.3640-3645.2005 · Cited by 1,286 · see citing works
Time to initiation of fluconazole therapy impacts mortality in patients with candidemia: A multi-institutional study.
Garey, K. W., Rege, M., Pai, M. P., Mingo, D. E., Suda, K. J., Turpin, R. S., & Bearden, D. T. (2006) · Clinical Infectious Diseases · doi:10.1086/504810 · Cited by 1,171 · see citing works
Voriconazole Compared with Liposomal Amphotericin B for Empirical Antifungal Therapy in Patients with Neutropenia and Persistent Fever
Walsh, T. J., Pappas, P., Winston, D. J., Lazarus, H. M., Petersen, F., Raffalli, J., Yanovich, S., Stiff, P., Greenberg, R., Donowitz, G., et al. (2002) · New England Journal of Medicine · doi:10.1056/nejm200201243460403 · Cited by 979 · see citing works
Self-citation
Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters
Sanglard, D., Kuchler, K., Ischer, F., Pagani, J. L., Monod, M., & Bille, J. (1995) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.39.11.2378 · Cited by 815 · see citing works
Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences
Sanglard, D., & Odds, F. C. (2002) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(02)00181-0 · Cited by 784 · see citing works
Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-Year Analysis of Susceptibilities of Candida Species to Fluconazole and Voriconazole as Determined by CLSI Standardized Disk Diffusion
Pfaller, M. A., Diekema, D. J., Gibbs, D. L., Newell, V. A., Ellis, D., Tullio, V., Rodloff, A., Fu, W., & Ling, T. A. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.02117-09 · Cited by 718 · see citing works
Self-citation
Rare and Emerging Opportunistic Fungal Pathogens: Concern for Resistance beyondCandida albicansandAspergillus fumigatus
Pfaller, M. A., & Diekema, D. J. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.10.4419-4431.2004 · Cited by 695 · see citing works
Self-citation
Voriconazole Treatment for Less‐Common, Emerging, or Refractory Fungal Infections
Perfect, J. R., Marr, K. A., Walsh, T. J., Greenberg, R. N., Dupont, B., Torre‐Cisneros, J., Just‐Nübling, G., Schlamm, H. T., Lutsar, I., Espinel‐Ingroff, A., et al. (2003) · Clinical Infectious Diseases · doi:10.1086/374557 · Cited by 672 · see citing works
Self-citation
Clinical Practice Guidelines for the Management of Candidiasis: 2009 Update by the Infectious Diseases Society of America
Parczewska, O. K., Posaconazol, przeciwgrzybicze, L., Anidulafungina, Micafungina, & wrażliwość, O. (2009) · Cited by 656 · see citing works
Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene
Sanglard, D., Ischer, F., Monod, M., & Bille, J. (1997) · Microbiology · doi:10.1099/00221287-143-2-405 · Cited by 587 · see citing works
Setting and Revising Antibacterial Susceptibility Breakpoints
Turnidge, J. D., & Paterson, D. L. (2007) · Clinical Microbiology Reviews · doi:10.1128/cmr.00047-06 · Cited by 580 · see citing works
Voriconazole versus a regimen of amphotericin B followed by fluconazole for candidaemia in non-neutropenic patients: a randomised non-inferiority trial
Kullberg, B., Sobel, J., Ruhnke, M., Pappas, P., Viscoli, C., Rex, J., Cleary, J., Rubinstein, E., Church, L., Brown, J., et al. (2005) · The Lancet · doi:10.1016/s0140-6736(05)67490-9 · Cited by 521 · see citing works
Antifungal Susceptibility Survey of 2,000 Bloodstream Candida Isolates in the United States
Ostrosky‐Zeichner, L., Rex, J. H., Pappas, P. G., Hamill, R. J., Larsen, R. A., Horowitz, H. W., Powderly, W. G., Hyslop, N. E., Kauffman, C. A., Cleary, J. D., et al. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.10.3149-3154.2003 · Cited by 494 · see citing works
Self-citation
In vitro activities of posaconazole, fluconazole, itraconazole, voriconazole, and amphotericin B against a large collection of clinically important molds and yeasts.
Sabatelli, F., Patel, R., Mann, P. A., Mendrick, C. A., Norris, C. C., Hare, R., Loebenberg, D., Black, T. A., & McNicholas, P. M. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00163-06 · Cited by 491 · see citing works
Method for antifungal disk diffusion susceptibility testing of yeasts : Approved guideline
Rex, J. H., & Clinical (2009) · Clinical and Laboratory Standards Institute eBooks · Cited by 425 · see citing works
European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria
Kahlmeter, G. (2003) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkg312 · Cited by 404 · see citing works
Breakthrough Fungal Infections in Stem Cell Transplant Recipients Receiving Voriconazole
Imhof, A., Balajee, S. A., Fredricks, D. N., Englund, J. A., & Marr, K. A. (2004) · Clinical Infectious Diseases · doi:10.1086/423274 · Cited by 402 · see citing works
Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors
Sanglard, D., Ischer, F., Monod, M., & Billé, J. (1996) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.40.10.2300 · Cited by 402 · see citing works
Statistical characterisation of bacterial wild-type MIC value distributions and the determination of epidemiological cut-off values
Turnidge, J. D., Kahlmeter, G., & Kronvall, G. (2006) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2006.01377.x · Cited by 399 · see citing works
Has antifungal susceptibility testing come of age
Rex, J. H., & Pfaller, M. A. (2002) · Clinical Infectious Diseases · doi:10.1086/342384 · Cited by 361 · see citing works
Self-citation
A Randomized, Double‐Blind, Double‐Dummy, Multicenter Trial of Voriconazole and Fluconazole in the Treatment of Esophageal Candidiasis in Immunocompromised Patients
Ally, R., Schürmann, D., Kreisel, W., Carosi, G., Aguirrebengoa, K., Dupont, B., Hodges, M., Troke, P., Romero, A. J., & the Esophageal Candidiasis Study Group (2001) · Clinical Infectious Diseases · doi:10.1086/322653 · Cited by 331 · see citing works
Mechanisms of Azole Resistance in Clinical Isolates of Candida glabrata Collected during a Hospital Survey of Antifungal Resistance
Sanguinetti, M., Posteraro, B., Fiori, B., Ranno, S., Torelli, R., & Fadda, G. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.2.668-679.2005 · Cited by 319 · see citing works
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
Pfaller, M. A., Andes, D., Diekema, D. J., Espinel-Ingroff, A., & Sheehan, D. (2010) · Drug Resistance Updates · doi:10.1016/j.drup.2010.09.002 · Cited by 314 · see citing works
Self-citation
The presence of an R467K amino acid substitution and loss of allelic variation correlate with an azole-resistant lanosterol 14alpha demethylase in Candida albicans
White, T. C. (1997) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.41.7.1488 · Cited by 292 · see citing works
Correlation of MIC with Outcome for Candida Species Tested against Voriconazole: Analysis and Proposal for Interpretive Breakpoints
Pfaller, M. A., Diekema, D. J., Rex, J. H., Espinel-Ingroff, A., Johnson, E. M., Andes, D., Chaturvedi, V., Ghannoum, M. A., Odds, F. C., Rinaldi, M. G., et al. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.44.3.819-826.2006 · Cited by 258 · see citing works
Self-citation
Multiechinocandin- and Multiazole-ResistantCandida parapsilosisIsolates Serially Obtained during Therapy for Prosthetic Valve Endocarditis
Moudgal, V. V., Little, T., Boikov, D. A., & Vázquez, J. A. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.2.767-769.2005 · Cited by 241 · see citing works
In Vitro Activities of Ravuconazole and Voriconazole Compared with Those of Four Approved Systemic Antifungal Agents against 6,970 Clinical Isolates of Candida spp
Pfaller, M. A., Messer, S. A., Hollis, R. J., Jones, R. N., & Diekema, D. J. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.6.1723-1727.2002 · Cited by 232 · see citing works
Self-citation
In vivo pharmacokinetics and pharmacodynamics of a new triazole, voriconazole, in a murine candidiasis model
Andes, D., Marchillo, K., Stamstad, T., & Conklin, R. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.10.3165-3169.2003 · Cited by 231 · see citing works
Self-citation
Adequacy of empirical antifungal therapy and effect on outcome among patients with invasive Candida species infections
Parkins, M. D., Sabuda, D. M., Elsayed, S., & Laupland, K. B. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm212 · Cited by 229 · see citing works
Susceptibility Tests of Anaerobic Bacteria: Statistical and Clinical Considerations
Metzler, C. M., & DeHaan, R. M. (1974) · The Journal of Infectious Diseases · doi:10.1093/infdis/130.6.588 · Cited by 196 · see citing works
Application of Real-Time Quantitative PCR to Molecular Analysis of Candida albicans Strains Exhibiting Reduced Susceptibility to Azoles
Chau, A. S., Mendrick, C. A., Sabatelli, F. J., Loebenberg, D., & McNicholas, P. M. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.6.2124-2131.2004 · Cited by 187 · see citing works
Optimizing the correlation between results of testing in vitro and therapeutic outcome in vivo for fluconazole by testing critical isolates in a murine model of invasive candidiasis
Rex, J. H., Nelson, P. W., Paetznick, V. L., Lozano-Chiu, M., Espinel-Ingroff, A., & Anaissie, E. J. (1998) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.42.1.129 · Cited by 167 · see citing works
Self-citation
Comparison of Visual and Spectrophotometric Methods of Broth Microdilution MIC End Point Determination and Evaluation of a Sterol Quantitation Method for In Vitro Susceptibility Testing of Fluconazole and Itraconazole against Trailing and Nontrailing Candida Isolates
Arthington-Skaggs, B. A., Lee-Yang, W., Ciblak, M. A., Frade, J. P., Brandt, M. E., Hajjeh, R. A., Harrison, L. H., Sofair, A. N., & Warnock, A. D. W. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.8.2477-2481.2002 · Cited by 158 · see citing works
Wild-Type MIC Distributions and Epidemiological Cutoff Values for the Echinocandins and Candida spp
Pfaller, M. A., Boyken, L. B., Hollis, R. J., Kroeger, J. S., Messer, S. A., Tendolkar, S., Jones, R. N., Turnidge, J. D., & Diekema, D. J. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.01590-09 · Cited by 154 · see citing works
Self-citation
Development of Fluconazole Resistance inCandida albicansCausing Disseminated Infection in a Patient Undergoing Marrow Transplantation
Marr, K. A., White, T. C., van Burik, J. H., & Bowden, R. A. (1997) · Clinical Infectious Diseases · doi:10.1086/515553 · Cited by 145 · see citing works
Clinical Significance of Azole Antifungal Drug Cross-Resistance in Candida glabrata
Panackal, A. A., Gribskov, J. L., Staab, J. F., Kirby, K. A., Rinaldi, M. G., & Marr, K. A. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.44.5.1740-1743.2006 · Cited by 144 · see citing works
International and Multicenter Comparison of EUCAST and CLSI M27-A2 Broth Microdilution Methods for Testing Susceptibilities of Candida spp. to Fluconazole, Itraconazole, Posaconazole, and Voriconazole
Espinel‐Ingroff, A., Barchiesi, F., Cuenca‐Estrella, M., Pfaller, M. A., Rinaldi, M. G., Rodríguez-Tudela, J. L., & Verweij, P. E. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.8.3884-3889.2005 · Cited by 140 · see citing works
Self-citation
Triazole Cross-Resistance among Candida spp.: Case Report, Occurrence among Bloodstream Isolates, and Implications for Antifungal Therapy
Magill, S. S., Shields, C. E., Sears, C. L., Choti, M. A., & Merz, W. G. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.44.2.529-535.2006 · Cited by 137 · see citing works
Interpretation of Trailing Endpoints in Antifungal Susceptibility Testing by the National Committee for Clinical Laboratory Standards Method
Revankar, S. G., Kirkpatrick, W. R., McAtee, R. K., Fothergill, A. W., Redding, S. W., Rinaldi, M. G., & Patterson, T. F. (1998) · Journal of Clinical Microbiology · doi:10.1128/jcm.36.1.153-156.1998 · Cited by 133 · see citing works
Comparison of the Antifungal Susceptibility Testing Subcommittee of the European Committee on Antibiotic Susceptibility Testing Proposed Standard and the E-Test with the NCCLS Broth Microdilution Method for Voriconazole and Caspofungin Susceptibility Testing of Yeast Species
Chryssanthou, E., & Cuenca‐Estrella, M. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.10.3841-3844.2002 · Cited by 113 · see citing works
Rapid Acquisition of Stable Azole Resistance by Candida glabrata Isolates Obtained before the Clinical Introduction of Fluconazole
Borst, A., Raimer, M. T., Warnock, D. W., Morrison, C. J., & Arthington, B. A. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.2.783-787.2005 · Cited by 107 · see citing works
Candidaemia associated with decreased in vitro fluconazole susceptibility: is Candida speciation predictive of the susceptibility pattern?
Oxman, D., Chow, J. K. L., Frendl, G., Hadley, S., Hershkovitz, S., Ireland, P., McDermott, L. A., Tsai, K., Marty, F. M., Kontoyiannis, D. P., et al. (2010) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkq136 · Cited by 104 · see citing works
Genetic Dissection of Azole Resistance Mechanisms in Candida albicans and Their Validation in a Mouse Model of Disseminated Infection
MacCallum, D. M., Coste, A., Ischer, F., Jacobsen, M. D., Odds, F. C., & Sanglard, D. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01645-09 · Cited by 98 · see citing works
Multiple Resistant Phenotypes of Candida albicans Coexist during Episodes of Oropharyngeal Candidiasis in Human Immunodeficiency Virus-Infected Patients
Lopez-Ribot, J. L., McAtee, R. K., Perea, S. H., Kirkpatrick, W. R., Rinaldi, M. G., & Patterson, T. F. (1999) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.43.7.1621 · Cited by 94 · see citing works
Voriconazole: A second-generation triazole
Chandrasekar, P. H., & Manavathu, E. K. (2001) · Drugs of today · doi:10.1358/dot.2001.37.2.614849 · Cited by 91 · see citing works
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
Pfaller, M. A., Boyken, L. B., Messer, S. A., Tendolkar, S., Hollis, R. J., & Diekema, D. J. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.10.5208-5213.2005 · Cited by 89 · see citing works
Self-citation
Candida glabrata Fungemia in Transplant Patients Receiving Voriconazole after Fluconazole
Alexander, B. D., Schell, W. A., Miller, J. L., Long, G. D., & Perfect, J. R. (2005) · Transplantation · doi:10.1097/01.tp.0000173771.47698.7b · Cited by 78 · see citing works
Self-citation
Use of Fluconazole as a Surrogate Marker To Predict Susceptibility and Resistance to Voriconazole among 13,338 Clinical Isolates of Candida spp. Tested by Clinical and Laboratory Standards Institute-Recommended Broth Microdilution Methods
Pfaller, M. A., Messer, S. A., Boyken, L., Rice, C., Tendolkar, S., Hollis, R. J., & Diekema, D. J. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.01551-06 · Cited by 77 · see citing works
Self-citation
Comparison of the Broth Microdilution (BMD) Method of the European Committee on Antimicrobial Susceptibility Testing with the 24-Hour CLSI BMD Method for Testing Susceptibility of Candida Species to Fluconazole, Posaconazole, and Voriconazole by Use of Epidemiological Cutoff Values
Pfaller, M. A., Espinel‐Ingroff, A., Boyken, L. B., Hollis, R. J., Kroeger, J. S., Messer, S. A., Tendolkar, S., & Diekema, D. J. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.02441-10 · Cited by 73 · see citing works
Self-citation
Breakpoints for Susceptibility Testing Should Not Divide Wild-Type Distributions of Important Target Species
Arendrup, M. C., Kahlmeter, G., Rodrı́guez-Tudela, J. L., & Donnelly, J. P. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01624-08 · Cited by 62 · see citing works
Self-citation
Wild-Type MIC Distributions and Epidemiological Cutoff Values for Posaconazole and Voriconazole and Candida spp. as Determined by 24-Hour CLSI Broth Microdilution
Pfaller, M. A., Boyken, L. B., Hollis, R. J., Kroeger, J. S., Messer, S. A., Tendolkar, S., & Diekema, D. J. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.02161-10 · Cited by 61 · see citing works
Self-citation
Emerging azole antifungals
Chen, A. L., & Sobel, J. D. (2005) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.10.1.21 · Cited by 60 · see citing works
Potential confusion regarding the term 'resistance' in epidemiological surveys
Simjee, S., Silley, P., Werling, H. O., & Bywater, R. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm423 · Cited by 59 · see citing works
EUCAST Technical Note on voriconazole
* (2008) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2008.02087.x · Cited by 59 · see citing works
Comparison of 24-Hour and 48-Hour Voriconazole MICs as Determined by the Clinical and Laboratory Standards Institute Broth Microdilution Method (M27-A3 Document) in Three Laboratories: Results Obtained with 2,162 Clinical Isolates of Candida spp. and Other Yeasts
Espinel‐Ingroff, A., Cantón, R., Pemán, J., Rinaldi, M. G., & Fothergill, A. W. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.00654-09 · Cited by 49 · see citing works
Self-citation
Validation of 24-Hour Fluconazole MIC Readings versus the CLSI 48-Hour Broth Microdilution Reference Method: Results from a Global Candida Antifungal Surveillance Program
Pfaller, M. A., Boyken, L. B., Hollis, R. J., Kroeger, J. S., Messer, S. A., Tendolkar, S., & Diekema, D. J. (2008) · Journal of Clinical Microbiology · doi:10.1128/jcm.01391-08 · Cited by 47 · see citing works
Self-citation
Harmonization of antimicrobial breakpoints in Europe — Can it be achieved?
Kahlmeter, G., & Brown, D. F. J. (2004) · Clinical Microbiology Newsletter · doi:10.1016/s0196-4399(04)80015-1 · Cited by 46 · see citing works
Comparative in Vitro Activity of Voriconazole and Itraconazole Against Fluconazole-Susceptible and Fluconazole-Resistant Clinical Isolates of Candida Species from Spain
Cuenca‐Estrella, M., Dı́az-Guerra, T. M., Mellado, E., Monz�n, A., & Rodr�guez-Tudela, J. L. (1999) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s100960050313 · Cited by 45 · see citing works
Rationale for Reading Fluconazole MICs at 24 Hours Rather than 48 Hours When Testing Candida spp. by the CLSI M27-A2 Standard Method
Ostrosky‐Zeichner, L., Rex, J. H., Pfaller, M. A., Diekema, D. J., Alexander, B. D., Andes, D. R., Brown, S. D., Chaturvedi, V. P., Ghannoum, M. A., Knapp, C. C., et al. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00420-08 · Cited by 45 · see citing works
Self-citation
Activity of voriconazole, itraconazole, fluconazole and amphotericin B in vitro against 1763 yeasts from 472 patients in the voriconazole phase III clinical studies
Johnson, E. M., Espinel‐Ingroff, A., Székely, A., Hockey, H. P., & Troke, P. F. (2008) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2008.05.023 · Cited by 43 · see citing works
Self-citation
Comparison of Visual 24-Hour and Spectrophotometric 48-Hour MICs to CLSI Reference Microdilution MICs of Fluconazole, Itraconazole, Posaconazole, and Voriconazole for Candida spp.: a Collaborative Study
Espinel‐Ingroff, A., Barchiesi, F., Cuenca‐Estrella, M., Fothergill, A. W., Pfaller, M. A., Rinaldi, M. G., Rodríguez-Tudela, J. L., & Verweij, P. E. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.9.4535-4540.2005 · Cited by 39 · see citing works
Self-citation
Validation of 24-Hour Posaconazole and Voriconazole MIC Readings versus the CLSI 48-Hour Broth Microdilution Reference Method: Application of Epidemiological Cutoff Values to Results from a Global Candida Antifungal Surveillance Program
Pfaller, M. A., Boyken, L. B., Hollis, R. J., Kroeger, J. S., Messer, S. A., Tendolkar, S., & Diekema, D. J. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.02437-10 · Cited by 34 · see citing works
Self-citation
Azole Resistance of Candida glabrata in a Case of Recurrent Fungemia
Posteraro, B., Tumbarello, M., La Sorda, M., Spanu, T., Trecarichi, E. M., De Bernardis, F., Scoppettuolo, G., Sanguinetti, M., & Fadda, G. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.00526-06 · Cited by 30 · see citing works
Myelofibrosis Complicated by Infection Due toCandida albicans: Emergence of Resistance to Antifungal Agents During Therapy
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The global problem of antifungal resistance: prevalence, mechanisms, and management
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The Candida albicans Histone Acetyltransferase Hat1 Regulates Stress Resistance and Virulence via Distinct Chromatin Assembly Pathways
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Tan, J., Zhang, J., Chen, W., Sun, Y., Wan, Z., Li, R., & Liu, W. (2015) · Mycopathologia · doi:10.1007/s11046-014-9831-8 · Cited by 36 · see citing works
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Song, Y. B., Suh, M. K., Ha, G. Y., & Kim, H. (2015) · Annals of Dermatology · doi:10.5021/ad.2015.27.6.715 · Cited by 35 · see citing works
Comparative genomic and transcriptomic analyses unveil novel features of azole resistance and adaptation to the human host in Candida glabrata
Salazar, S. B., Wang, C., Münsterkötter, M., Okamoto, M., Takahashi-Nakaguchi, A., Chibana, H., Lopes, M. M., Güldener, U., Butler, G., & Mira, N. P. (2018) · FEMS Yeast Research · doi:10.1093/femsyr/fox079 · Cited by 31 · see citing works
The impact of new epidemiological cutoff values on Candida glabrata resistance rates and concordance between testing methods
Ben-Ami, R., Hilerowicz, Y., Novikov, A., & Giladi, M. (2014) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2014.02.008 · Cited by 12 · see citing works

Efficacy of Voriconazole in Treatment of Murine Pulmonary Blastomycosis
Sugar, A. M., & Liu, X. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.2.601-604.2001 · Cited by 73 · see citing works
Clinical Isolates of Aspergillus Species Remain Fully Susceptible to Voriconazole in the Post-Voriconazole Era
Guinea, J., Recio, S., Peláez, T., et al. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00629-08 · Cited by 25 · see citing works
Therapeutic drug monitoring in voriconazole-associated hyponatremia
Xu, R.-A., Zheng, S.-L., Xiao, L., et al. (2013) · Medical Mycology Case Reports · doi:10.1016/j.mmcr.2013.06.003 · Cited by 5 · see citing works
Cloning and Characterization of Rat BAT3 cDNA
Ozaki, T., Hanaoka, E., Naka, M., et al. (1999) · DNA and Cell Biology · doi:10.1089/104454999315222 · Cited by 22 · see citing works
Subtherapeutic levels of voriconazole in continuous renal replacement therapy patients
Azócar, M., Barraza, M., Torres, J., et al. (2019) · Journal of Analytical & Pharmaceutical Research · doi:10.15406/japlr.2019.08.00313

Authors: Pfaller, M. A., Andes, D., Arendrup, M. C., Diekema, D. J., Espinel-Ingroff, A., Alexander, B. D., Brown, S. D., Chaturvedi, V., Fowler, C. L., Ghannoum, M. A., Johnson, E. M., Knapp, C. C., Motyl, M. R., Ostrosky-Zeichner, L., & Walsh, T. J.
Affiliations: University of Iowa (US)
University of Wisconsin–Madison (US)
Statens Serum Institut (DK)
Duke University (US)
New York State Department of Health (US)
bioMérieux (United States) (US)
Case Western Reserve University (US)
Merck & Co., Inc., Rahway, NJ, USA (United States) (US)
Cornell University (US)
Corresponding author: Pfaller, Michael A.
ORCID: Pfaller, Michael A.
Andes, David
Arendrup, Maiken C.
Diekema, Daniel J.
Alexander, Barbara D.
Brown, Steven D.
Chaturvedi, Vishnu
Ghannoum, Mahmoud A.
Johnson, Elizabeth M.
Motyl, Mary R.
Walsh, Thomas J.
Venue: Diagnostic Microbiology and Infectious Disease
Publisher: Elsevier BV
Published: 2011-07
Volume: 70
Issue: 3
Pages: 330-343
ISSN: 0732-8893 (ISSN-L)
DOI: 10.1016/j.diagmicrobio.2011.03.002
OpenAlex: W2129135057
Cited by: 130
References: 70
Citations by year: 2025: 2 · 2024: 3 · 2023: 10 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 7 · 2018: 1 · 2017: 7 · 2016: 7 · 2015: 15 · 2014: 15 · 2013: 18 · 2012: 29
FWCI: 15.32
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Diagnostic Microbiology and Infectious Disease (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Bacterial Identification and Susceptibility Testing
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Fungal Plant Pathogen Control
Keywords: voriconazole, clinical breakpoints, Candida, antifungal susceptibility testing, Candida albicans, Candida tropicalis, Candida parapsilosis, Candida glabrata
MeSH terms: Antifungal Agents, Candida, Candidiasis, Humans, Microbial Sensitivity Tests, Pyrimidines, Triazoles, Voriconazole

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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

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