Approaches for identifying and measuring heteroresistance in azole-susceptible Candida isolates
Open accessAbstract
Heteroresistance to antifungal agents poses a significant challenge in the treatment of fungal infections. Currently, the absence of established methods for detecting and measuring heteroresistance impedes progress in understanding this phenomenon in fungal pathogens. In response to this gap, we present a comprehensive set of new and optimized methods designed to detect and quantify azole heteroresistance in Candida albicans . Here, we define two primary assays for measuring heteroresistance: population analysis profiling, based on growth on solid medium, and single-cell assays, based on growth in liquid culture. We observe good correlations between the measurements obtained with liquid and solid assays, validating their utility for studying azole heteroresistance. We also highlight that disk diffusion assays could serve as an additional tool for the rapid detection of heteroresistance. These methods collectively provide a versatile toolkit for researchers seeking to assess heteroresistance in C. albicans . They also serve as a critical step forward in the characterization of antifungal heteroresistance, providing a framework for investigating this phenomenon in diverse fungal species and in the context of other antifungal agents. Ultimately, these advancements will enhance our ability to effectively measure antifungal drug responses and combat fungal infections. IMPORTANCE: Heteroresistance involves varying antimicrobial susceptibility within a clonal population. This phenomenon allows the survival of rare resistant subpopulations during drug treatment, significantly complicating the effective management of infections. However, the absence of established detection methods hampers progress in understanding this phenomenon in human fungal pathogens. We propose a comprehensive toolkit to address this gap in the yeast Candida albicans , encompassing population analysis profiling, single-cell assays, and disk diffusion assays. By providing robust and correlated measurements through both solid and liquid assays, this work will provide a framework for broader applications across clinically relevant Candida species. These methods will enhance our ability to understand this phenomenon and the failure of antifungal therapy.
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For diagnosed fungal infections, antifungal heteroresistance may lead to persistent infections that require longer or more aggressive treatment regimens.
“For diagnosed fungal infections, it may lead to persistent infections that require longer or more aggressive treatment regimens [27,28,29,30].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [30]
The Introduction (page not available in our copy) links fungal heteroresistance to relapse during azole treatment and failure to clear infection, supporting the possibility of persistent infection. It does not say that patients require longer or more aggressive treatment regimens. (LLM, conf=0.86)
Experimental — accuracy not yet measuredPAP assay has been proved to efficiently test heteroresistance to azoles and echinocandins in C. albicans, C. haemulonii, C. tropicalis, N. glabrata, C. parapsilosis, C. neoformans and S. cerevisiae.
“PAP has been proved to efficiently test the heteroresistance to azoles and echinocandins in C. albicans, C. haemulonii, C. tropicalis, N. glabrata, C. parapsilosis, C. neoformans and S. cerevisiae, etc. [30].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [30]
The Results sections report that PAP assays measured fluconazole heteroresistance in C. albicans and detected it in some isolates of other listed yeasts. But the study did not test echinocandins, and it recovered no heteroresistant colonies from its C. parapsilosis or S. cerevisiae isolates. The Results mention earlier PAP adaptations for C. neoformans and echinocandin treatment; they do not establish efficient testing for both drug classes across every species named. (LLM, conf=0.90)
Experimental — accuracy not yet measuredSingle-cell assays may reveal a wide spectrum of adaptation mechanisms.
“Though the protocols are lengthier, they may reveal a wide spectrum of adaptation mechanisms [30].”
From Insight into the Mechanisms and Clinical Relevance of Antifungal Heteroresistance (2025) · cites this paper as [30]
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- Authors
- Gautier, C., Maciel, E. I., & Ene, I. V.
- Affiliations
- Institut Pasteur (FR)
- Corresponding author
- Ene, Iuliana V.
- Venue
- Microbiology Spectrum
- Publisher
- American Society for Microbiology
- Published
- 2024-04-02
- Volume
- 12
- Issue
- 4
- Pages
- e0404123-e0404123
- ISSN
- 2165-0497 (ISSN-L)
- PMC
- PMC10986555
- OpenAlex
- W4393411060
- Cited by
- 23
- References
- 58
- Citations by year
- 2026: 12 · 2025: 9 · 2024: 2
- FWCI
- 7.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Microbiology Spectrum (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Agence Nationale de la Recherche (GENOMEHET)
- Fondation pour la Recherche Médicale (Espoirs de la Recherche Postdoctoral Fellowship)
- Institut Pasteur (Pasteur Carnot PTR)
- CIFAR
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Fungal Plant Pathogen Control
- Keywords
- heteroresistance, azole resistance, Candida albicans, antifungal susceptibility, population analysis profiling, single cell testing, disk diffusion, fungal drug resistance, antifungal treatment failure
- MeSH terms
- Antifungal Agents, Azoles, Candida, Candida albicans, Humans, Microbial Sensitivity Tests, Mycoses, Drug Resistance, Fungal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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