Multilaboratory study of epidemiological cutoff values for detection of resistance in eight Candida species to fluconazole, posaconazole, and voriconazole

Espinel-Ingroff, A.; Pfaller, M. A.; Bustamante, B.; Canton, E.; Fothergill, A.; Fuller, J.; Gonzalez, G. M.; Lass-Flörl, C.; Lockhart, S. R.; Martin-Mazuelos, E.; Meis, J. F.; Melhem, M. S. C.; Ostrosky-Zeichner, L.; Pelaez, T.; Szeszs, M. W.; St-Germain, G.; Bonfietti, L. X.; Guarro, J.; Turnidge, J.

doi:10.1128/aac.02615-13

Cited by 105Antifungal resistance and susceptibilityYeasts and Rust Fungi StudiesFungal Plant Pathogen Control

Multilaboratory study of epidemiological cutoff values for detection of resistance in eight Candida species to fluconazole, posaconazole, and voriconazole

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Espinel-Ingroff, A., Pfaller, M. A., Bustamante, B., Canton, E., Fothergill, A., Fuller, J., Gonzalez, G. M., Lass-Flörl, C. +11 more·2014·Antimicrobial Agents and Chemotherapy

DOI 10.1128/aac.02615-13PMC PMC4023759

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Abstract

Although epidemiological cutoff values (ECVs) have been established for Candida spp. and the triazoles, they are based on MIC data from a single laboratory. We have established ECVs for eight Candida species and fluconazole, posaconazole, and voriconazole based on wild-type (WT) MIC distributions for isolates of C. albicans (n=11,241 isolates), C. glabrata (7,538), C. parapsilosis (6,023), C. tropicalis (3,748), C. krusei (1,073), C. lusitaniae (574), C. guilliermondii (373), and C. dubliniensis (162). The 24-h CLSI broth microdilution MICs were collated from multiple laboratories (in Canada, Brazil, Europe, Mexico, Peru, and the United States). The ECVs for distributions originating from ≥6 laboratories, which included ≥95% of the modeled WT population, for fluconazole, posaconazole, and voriconazole were, respectively, 0.5, 0.06 and 0.03 μg/ml for C. albicans, 0.5, 0.25, and 0.03 μg/ml for C. dubliniensis, 8, 1, and 0.25 μg/ml for C. glabrata, 8, 0.5, and 0.12 μg/ml for C. guilliermondii, 32, 0.5, and 0.25 μg/ml for C. krusei, 1, 0.06, and 0.06 μg/ml for C. lusitaniae, 1, 0.25, and 0.03 μg/ml for C. parapsilosis, and 1, 0.12, and 0.06 μg/ml for C. tropicalis. The low number of MICs (<100) for other less prevalent species (C. famata, C. kefyr, C. orthopsilosis, C. rugosa) precluded ECV definition, but their MIC distributions are documented. Evaluation of our ECVs for some species/agent combinations using published individual MICs for 136 isolates (harboring mutations in or upregulation of ERG11, MDR1, CDR1, or CDR2) and 64 WT isolates indicated that our ECVs may be useful in distinguishing WT from non-WT isolates.

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With respect to CLSI clinical breakpoints, fluconazole resistance, defined as MIC values ≥8 mg/L for C. albicans, has been reported overall to be as high as 3.5%.
“With respect to CLSI clinical breakpoints, fluconazole resistance, defined as MIC values ≥8 mg/L for C. albicans, has been reported overall to be as high as 3.5%.43–48”
From Molecular and genetic basis of azole antifungal resistance in the opportunistic pathogenic fungusCandida albicans (2020) · cites this paper as [48]

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Epidemiology and Molecular Basis of Resistance to Fluconazole Among Clinical Candida parapsilosis Isolates in Kuwait
Asadzadeh, M., Ahmad, S., Al‐Sweih, N., & Khan, Z. (2017) · Microbial Drug Resistance · doi:10.1089/mdr.2016.0336 · Cited by 52 · see citing works
Candidemia surveillance in Iowa: emergence of echinocandin resistance
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Fluconazole Resistance in Isolates of Uncommon Pathogenic Yeast Species from the United Kingdom
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Susceptibility Test Methods: Yeasts and Filamentous Fungi
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Minimal inhibitory concentration distributions and epidemiological cutoff values of five antifungal agents against Sporothrix brasiliensis
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Emerging Candida species isolated from renal transplant recipients: Species distribution and susceptibility profiles
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Species distribution and susceptibility profiles of Candida species isolated from vulvovaginal candidiasis, emergence of C. lusitaniae
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Candida/Candida biofilms. First description of dual-species Candida albicans/C. rugosa biofilm
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Detection of neonatal unit clusters of Candida parapsilosis fungaemia by microsatellite genotyping: Results from laboratory‐based sentinel surveillance, South Africa, 2009‐2010
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Linezolid in Combination With Azoles Induced Synergistic Effects Against Candida albicans and Protected Galleria mellonella Against Experimental Candidiasis
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Multicentre study to determine the Etest epidemiological cut-off values of antifungal drugs in Candida spp. and Aspergillus fumigatus species complex
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Proton pump inhibitors act synergistically with fluconazole against resistant Candida albicans
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Head‐to‐head comparison of CLSI, EUCAST, Etest and VITEK®2 results for Candida auris susceptibility testing
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Activity of Potent and Selective Host Defense Peptide Mimetics in Mouse Models of Oral Candidiasis
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Antifungal Resistance among Less Prevalent Candida Non-albicans and Other Yeasts versus Established and under Development Agents: A Literature Review
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Pulsed Electric Field-Assisted Sensitization of Multidrug-Resistant Candida Albicans to Antifungal Drugs
Novickij, V., Švedienė, J., Paškevičius, A., Markovskaja, S., Girkontaitė, I., Zinkevičienė, A., Lastauskienė, E., & Novickij, J. (2017) · Future Microbiology · doi:10.2217/fmb-2017-0245 · Cited by 29 · see citing works
Nanotechnology-Based Approaches for Voriconazole Delivery Applied to Invasive Fungal Infections
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Future Research Priorities in Fungal Resistance
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Azole resistance in Candida from animals calls for the One Health approach to tackle the emergence of antimicrobial resistance
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The ‘cephalosporin era’ of triazole therapy: isavuconazole, a welcomed newcomer for the treatment of invasive fungal infections
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CoERG11 A395T mutation confers azole resistance in Candida orthopsilosis clinical isolates
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First description of Candida nivariensis in Brazil: Antifungal susceptibility profile and potential virulence attributes
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Support for the EUCAST and revised CLSI fluconazole clinical breakpoints by Sensititre(R) YeastOne(R) for Candida albicans: a prospective observational cohort study
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In vitro activity of two amphotericin B formulations against Malassezia furfur strains recovered from patients with bloodstream infections
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Frequency, virulence factors and antifungal susceptibility of Candida parapsilosis species complex isolated from patients with candidemia in the central region of Argentina
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Multicenter Evaluation of the New Vitek 2 Yeast Susceptibility Test Using New CLSI Clinical Breakpoints for Fluconazole
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Positive regulation of the Candida albicans multidrug efflux pump Cdr1p function by phosphorylation of its N-terminal extension
Tsao, S., Weber, S., Cameron, C. A., Nehme, D., Ahmadzadeh, E., & Raymond, M. (2016) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkw252 · Cited by 21 · see citing works
Whole Genome Sequence of the Heterozygous Clinical Isolate Candida krusei 81-B-5
Cuomo, C. A., Shea, T., Yang, B., Rao, R. P., & Forche, A. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.043547 · Cited by 21 · see citing works
Novel high-throughput screening method using quantitative PCR to determine the antimicrobial susceptibility of Orientia tsutsugamushi clinical isolates
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Crossover between the control of fungal pathogens in medicine and the wider environment, and the threat of antifungal resistance
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Photodynamic antimicrobial chemotherapy (PACT) using toluidine blue inhibits both growth and biofilm formation by Candida krusei
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Are In Vitro Susceptibilities to Azole Antifungals Predictive of Clinical Outcome in the Treatment of Candidemia?
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Candida fermentati as a Cause of Persistent Fungemia in a Preterm Neonate Successfully Treated by Combination Therapy with Amphotericin B and Caspofungin
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Susceptibility profile of Candida rugosa (Diutina rugosa) against antifungals and compounds of essential oils
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Azole-Resilient Biofilms and Non-wild Type C. albicans Among Candida Species Isolated from Agricultural Soils Cultivated with Azole Fungicides: an Environmental Issue?
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Voriconazole treatment of Candida tropicalis meningitis
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In vitro virulence determinants, comparative pathogenicity of Diutina (Candida) mesorugosa clinical isolates and literature review of the D. rugosa complex
Montoya, A. M., Luna-Rodríguez, C. E., Gracia-Robles, G., Rojas, O. C., Treviño‐Rangel, R. D. J., & González, G. M. (2019) · Mycologia · doi:10.1080/00275514.2019.1585161 · Cited by 14 · see citing works
Commercial Methods for Antifungal Susceptibility Testing of Saprophytic Molds: Can They Be Used to Detect Resistance?
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Synergistic Antifungal Activity of Phellodendri Cortex and Magnoliae Cortex against Candida albicans
Hyunjeong, N. A., & Kim, T. (2022) · Journal of the Korean Wood Science and Technology · doi:10.5658/wood.2022.50.1.12 · Cited by 13 · see citing works
Antifungal susceptibility testing results of New Zealand yeast isolates, 2001–2015: Impact of recent CLSI breakpoints and epidemiological cut-off values for Candida and other yeast species
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Cross-resistance between voriconazole and fluconazole for non-albicans Candida infection: a case-case-control study
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Candida lusitaniae MICs to the echinocandins are elevated but FKS -mediated resistance is rare
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A proposal for antifungal epidemiological cut-off values against Histoplasma capsulatum var. capsulatum based on the susceptibility of isolates from HIV-infected patients with disseminated histoplasmosis in Northeast Brazil
Brilhante, R. S. N., Guedes, G. M. D. M., da Silva, M. L. Q., Castelo‐Branco, D. D. S. C. M., Cordeiro, R. D. A., Sidrim, J. J. C., & Rocha, M. F. G. (2018) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2018.03.017 · Cited by 11 · see citing works
Situación de la resistencia antifúngica de especies del género Candida en Perú
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The Role of New Posaconazole Formulations in the Treatment of Candida albicans Infections: Data from an In Vitro Pharmacokinetic-Pharmacodynamic Model
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In-vitro pharmacokinetic/pharmacodynamic model data suggest a potential role of new formulations of posaconazole against Candida krusei but not Candida glabrata infections
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Expression of ERG11 and efflux pump genes CDR1, CDR2 and SNQ2 in voriconazole susceptible and resistant Candida glabrata strains
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Toward Harmonization of Voriconazole CLSI and EUCAST Breakpoints for Candida albicans Using a Validated In Vitro Pharmacokinetic/Pharmacodynamic Model
Beredaki, M.-I., Georgiou, P., Siopi, M., Kanioura, L., Andes, D. R., Arendrup, M. C., Mouton, J. W., & Meletiadis, J. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00170-20 · Cited by 9 · see citing works
Voriconazole efficacy against Candida glabrata and Candida krusei: preclinical data using a validated in vitro pharmacokinetic/pharmacodynamic model
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Phytochemical characterization and inhibition of Candida sp. by the essential oil of Baccharis trimera (Less.) DC
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Green Preparation of Antimicrobial 1D-Coordination Polymers: [Zn(4,4′-bipy)Cl2]∞ and [Zn(4,4′-bipy)2(OAc)2]∞ by Ultrasonication of Zn(II) Salts and 4,4′-Bipyridine
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First isolation of Candida metapsilosis in Kuwait, an emerging global opportunistic pathogen
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Diphenyl diselenide suppresses key virulence factors of Candida krusei, a neglected fungal pathogen
da Silva, B. G. M., Pinto, A. P., Passos, J. C. D. S., da Rocha, J. B. T., Alberto-Silva, C., & Costa, M. S. (2022) · Biofouling · doi:10.1080/08927014.2022.2084388 · Cited by 8 · see citing works
Comparative evaluation of E-test and CLSI methods for Itraconazole, Fluconazole and Ketoconazole susceptibilities of Microsporum canis strains
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A gain-of-function mutation in PDR1 of Candida glabrata decreases EPA1 expression and attenuates adherence to epithelial cells through enhancing recruitment of the Mediator subunit Gal11A
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Annual Report on the External Quality Assessment Scheme for Clinical Microbiology in Korea (2015)
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Emerging threat of candida resistance among neonates at a teaching institute of Jharkhand
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Voriconazole and posaconazole therapy for experimental Candida lusitaniae infection
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Voriconazole minimum inhibitory concentrations are predictive of treatment outcome in experimental murine infections by Candida glabrata
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Bilateral Candida endophthalmitis accompanying Candida lusitaniae bloodstream infection: A case report
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Efficacy of echinocandins against murine infections by Diutina (Candida) rugosa
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When Conventional Methods Fail: First Detection of a Candida viswanathii Outbreak in Europe in a Pediatric Hospital Revealed by Whole Genome Sequencing and FT-IR Spectroscopy
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Experimental Therapy with Azoles against Candida guilliermondii
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(MeOPhSe)2, a synthetic organic selenium compound, inhibits virulence factors of Candida krusei: Adherence to cervical epithelial cells and biofilm formation
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Potential Original Drug for Aspergillosis: In Vitro and In Vivo Effects of 1-N,N-Dimethylamino-5-Isocyanonaphthalene (DIMICAN) on Aspergillus fumigatus
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Candida en la cavidad oral de pacientes con VIH en Cali, Colombia: determinación de especies y sensibilidad al fluconazol
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Susceptibility Testing of Candida auris Isolates
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3 / CoERG11 A395T mutation confers azole resistance in Candida orthopsilosis clinical isolates
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Case Commentary: Extending our therapeutic range against multidrug-resistant Candida
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Antifungal and Cytocompatible Properties of Juglans regia Extract for Dental Applications: A Novel Approach Against Oral Candida Infections
Miranda, D. G., Ramos, L. D. P., Morais, F. V., Nascimento, L. S., Ferreira, I. B., Guimarães, B. M., Tomé, F. M., Rodrigues, F. P., & Carrouel, F. (2025) · Applied Sciences · doi:10.3390/app151910531 · Cited by 1 · see citing works
Hot Topics in Antifungal Susceptibility Testing: a New Drug, a Bad Bug, Sweeping Caspofungin Testing under the Rug, and Solving the Epidemiological Cutoff Value Shrug
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Susceptibility Test Methods: Yeasts and Filamentous Fungi
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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
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Triazole and Echinocandin MIC Distributions with Epidemiological Cutoff Values for Differentiation of Wild-Type Strains from Non-Wild-Type Strains of Six Uncommon Species of Candida
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Wild-Type MIC Distributions and Epidemiologic Cutoff Values for Fluconazole and Candida: Time for New Clinical Breakpoints?
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Self-citation

Authors: Espinel-Ingroff, A., Pfaller, M. A., Bustamante, B., Canton, E., Fothergill, A., Fuller, J., Gonzalez, G. M., Lass-Flörl, C., Lockhart, S. R., Martin-Mazuelos, E., Meis, J. F., Melhem, M. S. C., Ostrosky-Zeichner, L., Pelaez, T., Szeszs, M. W., St-Germain, G., Bonfietti, L. X., Guarro, J., & Turnidge, J.
Affiliations: VCU Medical Center, Richmond, Virginia, USA
University of Iowa (US)
Universidad Peruana Cayetano Heredia (PE)
Unidad de Microbiologia Experimental, Centro de Investigacion, Hospital Universitario La Fe, Valencia, Spain
The University of Texas at San Antonio Health Science Center (US)
University of Alberta (CA)
Universidad Autonóma de Nuevo León, Monterrey, Nuevo León, Mexico
The Innsbruck Medical University, Division of Hygiene and Medical Microbiology, Innsbruck, Austria
Centers for Disease Control and Prevention (US)
Hospital Universitario de Valme, Seville, Spain
Radboud University Nijmegen (NL)
Fungal Taxonomy Laboratories, Adolfo Lutz Institute, São Paulo City, Brazil
University of Texas Health Science Center, Houston, Texas, USA
Hospital General Universitario Gregorio Maraňón, Facultad de Medicina, Universidad Complutense, Madrid, Spain
Instituto Adolfo Lutz (BR)
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Quebec, Canada
Institut de Recerca Biomèdica Catalunya Sud (ES)
The University of Adelaide (AU)
ORCID: Pfaller, M. A.
Bustamante, B.
Lockhart, S. R.
Meis, J. F.
Bonfietti, L. X.
Guarro, J.
Turnidge, J.
Venue: Antimicrobial Agents and Chemotherapy
Publisher: American Society for Microbiology
Published: 2014-04
Volume: 58
Issue: 4
Pages: 2006-2012
ISSN: 0066-4804 (ISSN-L)
1098-6596
DOI: 10.1128/aac.02615-13
PMC: PMC4023759
OpenAlex: W2113614834
Cited by: 105
References: 40
Citations by year: 2026: 2 · 2025: 2 · 2024: 2 · 2023: 7 · 2022: 7 · 2021: 6 · 2020: 6 · 2019: 12 · 2018: 11 · 2017: 15 · 2016: 11 · 2015: 18 · 2014: 6
FWCI: 11.68
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Antimicrobial Agents and Chemotherapy (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Rovira & Virgili repository (submittedVersion, cc-by)
Radboud Repository (Radboud University) (submittedVersion, other-oa)
Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Fungal Plant Pathogen Control
Keywords: epidemiological cut-off values, Candida, antifungal resistance, fluconazole, posaconazole, voriconazole, triazole antifungals, Candida albicans, Candida glabrata, Candida parapsilosis, Candida tropicalis, Candida krusei, Candida lusitaniae, Candida guilliermondii, Candida dubliniensis
MeSH terms: Antifungal Agents, Candida, Microbial Sensitivity Tests, Pyrimidines, Triazoles, Fluconazole, Voriconazole

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Multilaboratory study of epidemiological cutoff values for detection of resistance in eight Candida species to fluconazole, posaconazole, and voriconazole

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