Progress in Antifungal Susceptibility Testing of Candida spp. by Use of Clinical and Laboratory Standards Institute Broth Microdilution Methods, 2010 to 2012

Pfaller, M. A.; Diekema, D. J.

doi:10.1128/jcm.00937-12

Cited by 484Antifungal resistance and susceptibilityBacterial Identification and Susceptibility TestingYeasts and Rust Fungi Studies

Progress in Antifungal Susceptibility Testing of Candida spp. by Use of Clinical and Laboratory Standards Institute Broth Microdilution Methods, 2010 to 2012

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Pfaller, M. A., Diekema, D. J.·2012·Journal of Clinical Microbiology

DOI 10.1128/jcm.00937-12PMC PMC3421803

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Abstract

Antifungal susceptibility testing of Candida has been standardized and refined and now may play a useful role in managing Candida infections. Important new developments include validation of 24-h reading times for all antifungal agents and the establishment of species-specific epidemiological cutoff values (ECVs) for the systemically active antifungal agents and both common and uncommon species of Candida . The clinical breakpoints (CBPs) for fluconazole, voriconazole, and the echinocandins have been revised to provide species-specific interpretive criteria for the six most common species. The revised CBPs not only are predictive of clinical outcome but also provide a more sensitive means of identifying those strains with acquired or mutational resistance mechanisms. This brief review serves as an update on the new developments in the antifungal susceptibility testing of Candida spp. using Clinical and Laboratory Standards Institute (CLSI) broth microdilution (BMD) methods.

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Fungal infections generally follow the 90/60 rule for predicting therapeutic outcomes based on in vitro susceptibility testing.
“Fungal infections generally follow the”
From Antifungal tolerance is a subpopulation effect distinct from resistance and is associated with persistent candidemia (2018) · cites this paper as [3]
The section on the clinical impact of antifungal susceptibility testing says results for several organism–drug combinations, most notably Candida species and azoles, have predictive utility consistent with the 90/60 rule. That supports the rule for those combinations, but not the claim that fungal infections generally follow it. (LLM, conf=0.86)
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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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Rationale for Reading Fluconazole MICs at 24 Hours Rather than 48 Hours When Testing Candida spp. by the CLSI M27-A2 Standard Method
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Amphotericin B resistance testing of Candida spp.: a comparison of methods
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Population-Based Surveillance
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Laboratory methods for flucytosine (5-fluorocytosine)
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Does One Voriconazole Breakpoint Suit All Candida Species?
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Azole Antifungal Resistance in Candida albicans and Emerging Non-albicans Candida Species
Whaley, S. G., Berkow, E. L., Rybak, J. M., Nishimoto, A. T., Barker, K. S., & Rogers, P. D. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02173 · Cited by 900 · see citing works
The Surgical Infection Society Revised Guidelines on the Management of Intra-Abdominal Infection
Mazuski, J. E., Tessier, J. M., May, A. K., Sawyer, R. G., Nadler, E. P., Rosengart, M. R., Chang, P. K., O’Neill, P. J., Mollen, K. P., Huston, J. M., et al. (2017) · Surgical Infections · doi:10.1089/sur.2016.261 · Cited by 593 · see citing works
Changes in the epidemiological landscape of invasive candidiasis
Lamoth, F., Lockhart, S. R., Berkow, E. L., & Calandra, T. (2018) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkx444 · Cited by 547 · see citing works
Emerging Threats in Antifungal-Resistant Fungal Pathogens
Sanglard, D. (2016) · Frontiers in Medicine · doi:10.3389/fmed.2016.00011 · Cited by 420 · see citing works
Multidrug-resistant endemic clonal strain of Candida auris in India
Chowdhary, A., Anil Kumar, V., Sharma, C., Prakash, A., Agarwal, K., Babu, R., Dinesh, K. R., Karim, S., Singh, S. K., Hagen, F., et al. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2027-1 · Cited by 373 · see citing works
Malassezia ecology, pathophysiology, and treatment
Theelen, B., Cafarchia, C., Gaitanis, G., Bassukas, I. D., Boekhout, T., & Dawson, T. L. (2017) · Medical Mycology · doi:10.1093/mmy/myx134 · Cited by 343 · see citing works
Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance.
Healey, K. R., Zhao, Y., Perez, W. B., Lockhart, S. R., Sobel, J. D., Farmakiotis, D., Kontoyiannis, D. P., Sanglard, D., Taj-Aldeen, S. J., Alexander, B. D., et al. (2016) · Nature Communications · doi:10.1038/ncomms11128 · Cited by 276 · see citing works
Antifungal tolerance is a subpopulation effect distinct from resistance and is associated with persistent candidemia
Rosenberg, A., Ene, I. V., Bibi, M., Zakin, S., Segal, E. S., Ziv, N., Dahan, A. M., Colombo, A. L., Bennett, R. J., & Berman, J. (2018) · Nature Communications · doi:10.1038/s41467-018-04926-x · Cited by 270 · see citing works
“Studying growth dynamics and quantifying tolerance revealed that it is: (1) a subpopulation effect and the size of the subpopulation is stable; (2) due to slow growth in drug stress; (3) correlates with intracellular drug levels; (4) dependent upon stress response pathways, and (5) mechanistically distinct from resist…”
Background
Candida auris–Associated Candidemia, South Africa
Magobo, R. E., Corcoran, C., Seetharam, S., & Govender, N. P. (2014) · Emerging Infectious Diseases · doi:10.3201/eid2007.131765 · Cited by 259 · see citing works
Non- albicans Candida Infection: An Emerging Threat
Deorukhkar, S. C., Saini, S., & Mathew, S. K. (2014) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2014/615958 · Cited by 251 · see citing works
Genomic epidemiology of the UK outbreak of the emerging human fungal pathogen Candida auris
Rhodes, J., Abdolrasouli, A., Farrer, R. A., Cuomo, C. A., Aanensen, D. M., Armstrong-James, D., Fisher, M. C., & Schelenz, S. (2018) · Emerging Microbes & Infections · doi:10.1038/s41426-018-0045-x · Cited by 246 · see citing works
Echinocandin and Triazole Antifungal Susceptibility Profiles for Clinical Opportunistic Yeast and Mold Isolates Collected from 2010 to 2011: Application of New CLSI Clinical Breakpoints and Epidemiological Cutoff Values for Characterization of Geographic and Temporal Trends of Antifungal Resistance
Pfaller, M. A., Messer, S. A., Woosley, L. N., Jones, R. N., & Castanheira, M. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.00308-13 · Cited by 237 · see citing works
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Epidemiology, species distribution, antifungal susceptibility, and outcome of Candidemia across five sites in Italy and Spain
Bassetti, M., Merelli, M., Righi, E., Diaz-Martin, A., Rosello, E. M., Luzzati, R., Parra, A., Trecarichi, E. M., Sanguinetti, M., Posteraro, B., et al. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.01998-13 · Cited by 228 · see citing works
Age and Gender Affect the Composition of Fungal Population of the Human Gastrointestinal Tract
Strati, F., Paola, M. D., Stefanini, I., Albanese, D., Rizzetto, L., Lionetti, P., Calabrò, A., Jousson, O., Donati, C., Cavalieri, D., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01227 · Cited by 224 · see citing works
Whole genome sequencing of emerging multidrug resistant Candida auris isolates in India demonstrates low genetic variation
Sharma, C., Kumar, N., Pandey, R., Meis, J. F., & Chowdhary, A. (2016) · New Microbes and New Infections · doi:10.1016/j.nmni.2016.07.003 · Cited by 202 · see citing works
Nosocomial Candidiasis: Antifungal Stewardship and the Importance of Rapid Diagnosis
Pfaller, M. A., & Castanheira, M. (2015) · Medical Mycology · doi:10.1093/mmy/myv076 · Cited by 161 · see citing works
Self-citation
Oropharyngeal candidiasis in hospitalised COVID‐19 patients from Iran: Species identification and antifungal susceptibility pattern
Salehi, M., Ahmadikia, K., Mahmoudi, S., Kalantari, S., Jamalimoghadamsiahkali, S., Izadi, A., Kord, M., Manshadi, S. A. D., Seifi, A., Ghiasvand, F., et al. (2020) · Mycoses · doi:10.1111/myc.13137 · Cited by 160 · see citing works
New pathogens, new tricks: emerging, drug‐resistant fungal pathogens and future prospects for antifungal therapeutics
Geddes‐McAlister, J., & Shapiro, R. S. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13739 · Cited by 159 · see citing works
Virulence Factors Contributing to Pathogenicity of Candida tropicalis and Its Antifungal Susceptibility Profile
Deorukhkar, S. C., Saini, S., & Mathew, S. K. (2014) · International Journal of Microbiology · doi:10.1155/2014/456878 · Cited by 152 · see citing works
Drug resistance in eukaryotic microorganisms
Fairlamb, A. H., Gow, N. A. R., Matthews, K. R., & Waters, A. P. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.92 · Cited by 152 · see citing works
Antimicrobial Susceptibility Testing of Antimicrobial Peptides to Better Predict Efficacy
Mercer, D. K., Torres, M. D. T., Duay, S. S., Lovie, E., Simpson, L. W., von Köckritz‐Blickwede, M., de la Fuente‐Núñez, C., O′Neil, D. A., & Angeles-Boza, A. M. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00326 · Cited by 136 · see citing works
Antifungal Pharmacokinetics and Pharmacodynamics
Lepak, A. J., & Andes, D. R. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019653 · Cited by 134 · see citing works
Molecular Identification and Antifungal Susceptibility of Yeast Isolates Causing Fungemia Collected in a Population-Based Study in Spain in 2010 and 2011
Guinea, J., Zaragoza, Ó., Escribano, P., Martín‐Mazuelos, E., Pemán, J., Sánchez, F., & Cuenca‐Estrella, M. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02155-13 · Cited by 129 · see citing works
Isavuconazole, micafungin, and 8 comparator antifungal agents' susceptibility profiles for common and uncommon opportunistic fungi collected in 2013: temporal analysis of antifungal drug resistance using CLSI species-specific clinical breakpoints and proposed epidemiological cutoff values
Pfaller, M. A., Rhomberg, P. R., Messer, S. A., Jones, R. N., & Castanheira, M. (2015) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2015.04.008 · Cited by 127 · see citing works
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Rapid antifungal susceptibility testing by matrix-assisted laser desorption ionization-time of flight mass spectrometry analysis.
Vella, A., De Carolis, E., Vaccaro, L., Posteraro, P., Perlin, D. S., Kostrzewa, M., Posteraro, B., & Sanguinetti, M. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.00903-13 · Cited by 124 · see citing works
Candida parapsilosis Resistance to Fluconazole: Molecular Mechanisms and In Vivo Impact in Infected Galleria mellonella Larvae
Souza, A. C. R., Fuchs, B. B., Pinhati, H. M. S., Siqueira, R. A., Hagen, F., Meis, J. F., Mylonakis, E., & Colombo, A. L. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01177-15 · Cited by 121 · see citing works
Current status of antifungal resistance and its impact on clinical practice
Alcázar‐Fuoli, L., & Mellado, E. (2014) · British Journal of Haematology · doi:10.1111/bjh.12896 · Cited by 118 · see citing works
Is the emergence of fungal resistance to medical triazoles related to their use in the agroecosystems? A mini review
Ribas, A. D. R. E., Spolti, P., Ponte, E. M. D., Donato, K. Z., Schrekker, H. S., & Fuentefría, A. M. (2016) · Brazilian Journal of Microbiology · doi:10.1016/j.bjm.2016.06.006 · Cited by 111 · see citing works
First Report of Candidemia Clonal Outbreak Caused by Emerging Fluconazole-Resistant Candida parapsilosis Isolates Harboring Y132F and/or Y132F+K143R in Turkey
Arastehfar, A. A., Daneshnia, F., Polat, S. H., Fang, W., Yaşar, M., Polat, F., Metin, D. Y., Rigole, P., Coenye, T., İlkit, M., et al. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01001-20 · Cited by 110 · see citing works
Caspofungin MICs correlate with treatment outcomes among patients with Candida glabrata invasive candidiasis and prior echinocandin exposure.
Shields, R. K., Nguyen, M. H., Press, E. G., Updike, C. L., & Clancy, C. J. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00136-13 · Cited by 105 · see citing works
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., et al. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02615-13 · Cited by 105 · see citing works
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Antifungal susceptibility, genotyping, resistance mechanism, and clinical profile of Candida tropicalis blood isolates
Arastehfar, A. A., Daneshnia, F., Hafez, A. I., Khodavaisy, S., Najafzadeh, M. J., Charsizadeh, A., Zarrinfar, H., Salehi, M., Shahrabadi, Z. Z., Sasani, E., et al. (2019) · Medical Mycology · doi:10.1093/mmy/myz124 · Cited by 100 · see citing works
Epidemiology, clinical characteristics, and outcome of candidemia in a tertiary referral center in Italy from 2010 to 2014
The Candidemia Study Group, Barchiesi, F., Orsetti, E., Gesuita, R., Skrami, E., & Manso, E. (2015) · Infection · doi:10.1007/s15010-015-0845-z · Cited by 100 · see citing works
Nationwide Study of Candidemia, Antifungal Use, and Antifungal Drug Resistance in Iceland, 2000 to 2011
Ásmundsdóttir, L. R., Erlendsdóttir, H., & Gottfreðsson, M. (2012) · Journal of Clinical Microbiology · doi:10.1128/jcm.02566-12 · Cited by 99 · see citing works
Emergence of non-Candida albicans species: Epidemiology, phylogeny and fluconazole susceptibility profile
Sadeghi, G., Ebrahimi-Rad, M., Mousavi, S. F., Shams-Ghahfarokhi, M., & Razzaghi-Abyaneh, M. (2018) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2017.12.008 · Cited by 96 · see citing works
UncommonCandidaSpecies Fungemia among Cancer Patients, Houston, Texas, USA
Jung, D. S., Farmakiotis, D., Jiang, Y., Tarrand, J. J., & Kontoyiannis, D. P. (2015) · Emerging infectious diseases · doi:10.3201/eid2111.150404 · Cited by 96 · see citing works
Advances in Identification of Clinical Yeast Isolates by Use of Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry
Buchan, B. W., & Ledeboer, N. A. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.03105-12 · Cited by 95 · see citing works
Regional data analysis of Candida non‐albicans strains collected in United States medical sites over a 6‐year period, 2006–2011
Pfaller, M. A., Jones, R. N., & Castanheira, M. (2014) · Mycoses · doi:10.1111/myc.12206 · Cited by 91 · see citing works
Self-citation
Invasive candidiasis in intensive care units in China: a multicentre prospective observational study
Guo, F., Yang, Y., Kang, Y., Zang, B., Cui, W., Qin, B., Qin, Y., Fang, Q., Qin, T., Jiang, D., et al. (2013) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkt083 · Cited by 91 · see citing works
Synergistic Effect of Fluconazole and Calcium Channel Blockers against Resistant Candida albicans
Liu, S., Yue, L., Gu, W., Li, X., Zhang, L., & Sun, S. (2016) · PLOS ONE · doi:10.1371/journal.pone.0150859 · Cited by 87 · see citing works
Curcumin as a Promising Antibacterial Agent: Effects on Metabolism and Biofilm Formation inS. mutans
Li, B., Li, X., Lin, H., & Zhou, Y. N. (2018) · BioMed Research International · doi:10.1155/2018/4508709 · Cited by 86 · see citing works
Clonal Candidemia Outbreak by Candida parapsilosis Carrying Y132F in Turkey: Evolution of a Persisting Challenge
Arastehfar, A. A., Polat, S. H., Daneshnia, F., Pan, W., Hafez, A. I., Fang, W., Liao, W., Şahbudak-Bal, Z., Metin, D. Y., de Almeida, J. N., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.676177 · Cited by 86 · see citing works
In Vitro Activities of Isavuconazole and Comparator Antifungal Agents Tested against a Global Collection of Opportunistic Yeasts and Molds
Pfaller, M. A., Messer, S. A., Rhomberg, P. R., Jones, R. N., & Castanheira, M. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.00863-13 · Cited by 85 · see citing works
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Self-citation

Authors: Pfaller, M. A., & Diekema, D. J.
Affiliations: University of Iowa (US)
ORCID: Pfaller, M. A.
Diekema, D. J.
Venue: Journal of Clinical Microbiology
Publisher: American Society for Microbiology
Published: 2012-09
Volume: 50
Issue: 9
Pages: 2846-2856
ISSN: 0095-1137 (ISSN-L)
1098-660X
DOI: 10.1128/jcm.00937-12
PMC: PMC3421803
OpenAlex: W2120299440
Cited by: 484
References: 105
Citations by year: 2026: 15 · 2025: 20 · 2024: 24 · 2023: 29 · 2022: 26 · 2021: 41 · 2020: 41 · 2019: 31 · 2018: 43 · 2017: 46 · 2016: 45 · 2015: 41 · 2014: 47 · 2013: 31 · 2012: 4
FWCI: 4.88
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Clinical Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Pfizer
Eisai
Astellas Pharma
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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
Keywords: Candida, antifungal susceptibility testing, broth microdilution, epidemiological cut-off values, clinical breakpoints, fluconazole, voriconazole, echinocandins, antifungal resistance, Candida species, CLSI guidelines
MeSH terms: Antifungal Agents, Candida, Candidiasis, Humans, Microbial Sensitivity Tests

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Progress in Antifungal Susceptibility Testing of Candida spp. by Use of Clinical and Laboratory Standards Institute Broth Microdilution Methods, 2010 to 2012

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