Cited by 222Antifungal resistance and susceptibilityAntibiotic Resistance in BacteriaFungal Plant Pathogen Control

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Mechanism of Increased Fluconazole Resistance in Candida glabrata during Prophylaxis

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Bennett, John E., Izumikawa, Koichi, Marr, Kieren A.·2004·Antimicrobial Agents and Chemotherapy

DOI 10.1128/aac.48.5.1773-1777.2004PMC PMC400565

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Abstract

Candida glabrata can become resistant to fluconazole, causing persistent colonization and invasive infection during prolonged exposure to the drug. To determine the mechanism of resistance in this setting, weekly oropharyngeal cultures for C. glabrata were obtained over a 2-year period from hematopoietic stem cell transplant recipients who were receiving fluconazole prophylaxis. In 20 patients from whom at least two isolates of the same karyotype were obtained more than two weeks apart, fluconazole MICs doubled every 31 days on average. The mechanism of fluconazole resistance in isolates from the 14 of the 20 patients studied in whom MICs changed at least fourfold was studied. Cellular resistance was accompanied by increased drug efflux as measured by decreased accumulation of fluconazole and rhodamine 6G and increased abundance of transcripts from two drug transporters, CgCDR1 and PDH1. The rapidity and regularity of the rising resistance indicated that C. glabrata is able to upregulate drug efflux without losing the ability to maintain colonization.

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Candiduria; a review article with specific data from Iran
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“tropicalis is currently observed [54,70] as a consequence of the massive preventive application of fluconazole [71,72] and common use of agricultural fungicides, structurally similar to azoles [73].”
Background
In vitro activity of essential oils extracted from condiments against fluconazole-resistant and -sensitive Candida glabrata
Soares, I., Loreto, É. S., Rossato, L. L., Mário, D. N., Venturini, T. P., Baldissera, F. G., Santúrio, J. M., & Alves, S. H. (2015) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2015.06.003 · Cited by 33
“glabrata stands out due to its lower susceptibility to antifungal agents, particularly to azoles [2,16].”
Background
Luliconazole, a new antifungal against Candida species isolated from different sources
Taghipour, S., Kiasat, N., Shafiei, S., Halvaeezadeh, M., Rezaei‐Matehkolaei, A., & Mahmoudabadi, A. Z. (2017) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2017.11.004 · Cited by 33
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The Epidemiology of Invasive Candidiasis
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Background
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Song, J. W., Shin, J. H., Kee, S., Kim, S. H., Shin, M., Suh, S., & Ryang, D. W. (2008) · Medical Mycology · doi:10.1080/13693780802210726 · Cited by 33
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“Overexpression of CgCDR1, CgCDR2, and CgSNQ2-encoded efflux pumps has been shown to be a major mechanism contributing to the drug resistance [ 25- 27 ].”
Background
Do all candidemic patients need an ophthalmic examination?
Vinikoor, M. J., Zoghby, J., Cohen, K. L., & Tucker, J. D. (2013) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2012.12.014 · Cited by 31
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Background
Candida glabrata Transcription Factor Rpn4 Mediates Fluconazole Resistance through Regulation of Ergosterol Biosynthesis and Plasma Membrane Permeability
Pais, P., Califórnia, R., Galocha, M., Viana, R., Ola, M., Cavalheiro, M., Takahashi‐Nakaguchi, A., Chibana, H., Butler, G., & Teixeira, M. C. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00554-20 · Cited by 36
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“and PDH1 (Bennett et al., 2004; Sanguinetti et al., 2005; Ferrari et al., 2009). Borst et al. (2005) reported a rapid and stable acquisition of azole resistance by C.”
BackgroundInfluential
Laboratory Isolation and Identification of Candida Species
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Background
Antifungal effect of Atorvastatin against Candida species in comparison to Fluconazole and Nystatin
Nasr Esfahani, A., Golestannejad, Z., Khozeimeh, F., Dehghan, P., Maheronnaghsh, M., & Zarei, Z. (2019) · Medicine and Pharmacy Reports · doi:10.15386/mpr-1209 · Cited by 28
“Widespread prophylactic use of routine antifungal drugs in such patients has led to acquired resistance of isolated strains [7].”
Background
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“Previous studies investigated the importance of these molecular mechanisms but were generally limited to a set of related isolates sequentially obtained from the same patient (13, 29, 44).”
Background
Relationship between respiration deficiency and azole resistance in clinical Candida glabrata
Peng, Y., Dong, D., Jiang, C., Yu, B., Wang, X., & Ji, Y. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00821.x · Cited by 27
“glabrata has been increasing rapidly (Bennett et al., 2004) and is now a prominent problem in the clinic.”
Background
The EPA2 adhesin encoding gene is responsive to oxidative stress in the opportunistic fungal pathogen Candida glabrata
Juárez-Cepeda, J., Orta-Zavalza, E., Cañas-Villamar, I., Arreola-Gómez, J., Pérez-Cornejo, G. P., Hernández-Carballo, C. Y., Gutiérrez-Escobedo, G., Castaño, I., & Peñas, A. D. L. (2015) · Current Genetics · doi:10.1007/s00294-015-0473-2 · Cited by 24
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Background
Potent antimicrobial agents against azole-resistant fungi based on pyridinohydrazide and hydrazomethylpyridine structural motifs
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Background
Prevalence of Antifungal Resistance, Genetic Basis of Acquired Azole and Echinocandin Resistance, and Genotyping of Candida krusei Recovered from an International Collection
Khalifa, H. O., Hubka, V., Watanabe, A., Nagi, M., Miyazaki, Y., Yaguchi, T., & Kamei, K. (2021) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01856-21 · Cited by 22
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Background
The activity of echinocandins, amphotericin B and voriconazole against fluconazole-susceptible and fluconazole-resistant Brazilian Candida glabrata isolates
Mario, D. A. N., Denardi, L. B., Bandeira, L. A., Antunes, M. S., Santúrio, J. M., Severo, L. C., & Alves, S. H. (2012) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762012000300022 · Cited by 21
“However, when comparing MICs, the correlation between voriconazole and fluconazole cross-resistance is evident (Table II) (Bennett et al. 2004).”
BackgroundInfluential
Saponins of Trifolium spp. Aerial Parts as Modulators of Candida Albicans Virulence Attributes
Budzyńska, A., Sadowska, B., Więckowska-Szakiel, M., Micota, B., Stochmal, A., Jędrejek, D., Pecio, Ł., & Różalska, B. (2014) · Molecules · doi:10.3390/molecules190710601 · Cited by 21
“The molecular basis of fluconazole resistance includes modifications in the ERG11 gene encoding the main enzymes of ergosterol biosynthesis, overexpression of genes encoding efflux pumps, and others which have not been well defined yet [23,24].”
Background
Antifungal Activities of Diphenyl Diselenide alone and in Combination with Fluconazole or Amphotericin B against Candida glabrata
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“glabrata isolates easily develop resistance after exposure to treatment with this azole [11, 32].”
Background
Antifungal resistance: the clinical front.
Perfect, J. R. (2004) · PubMed · Cited by 21
Carbonic anhydrase activators: Activation of the β-carbonic anhydrase from the pathogenic yeast Candida glabrata with amines and amino acids
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Roles of Cellular Respiration, Cg CDR1 , and Cg CDR2 in Candida glabrata Resistance to Histatin 5
Helmerhorst, E. J., Venuleo, C., Sanglard, D., & Oppenheim, F. G. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.50.3.1100-1103.2006 · Cited by 20
“Resistance to azoles has been associated with the upregulation of the genes CgCDR1 and CgCDR2 (also designated PDH1) which encode proteins belonging to the ATP binding cassette family of multidrug resistance membrane-associated efflux pumps (1, 2, 12, 19, 20, 23).”
Background
Crystal Structures of Candida albicans Dihydrofolate Reductase Bound to Propargyl‐Linked Antifolates Reveal the Flexibility of Active Site Loop Residues Critical for Ligand Potency and Selectivity
Paulsen, J. L., Bendel, S. D., & Anderson, A. C. (2011) · Chemical Biology & Drug Design · doi:10.1111/j.1747-0285.2011.01169.x · Cited by 20
“glabrata has been shown to express efflux pumps, inducing resistance to the clinically used azole antifungal agents (8,9).”
Background
Evaluation of Polymorphic Locus Sequence Typing for Candida glabrata Epidemiology
Katiyar, S. K., Shiffrin, E., Shelton, C. A., Healey, K. R., Vermitsky, J., & Edlind, T. (2016) · Journal of Clinical Microbiology · doi:10.1128/jcm.03106-15 · Cited by 20
“enzyme digestion (14, 23, 31), (iii) multilocus variable-number”
BackgroundResult
Biguanides enhance antifungal activity against Candida glabrata
Xu, S., Feliu, M., Lord, A. K., Lukason, D. P., Negoro, P. E., Khan, N. S., Dagher, Z., Feldman, M. B., Reedy, J. L., Steiger, S. N., et al. (2018) · Virulence · doi:10.1080/21505594.2018.1475798 · Cited by 21
“Additionally, the use of broad spectrum antibiotics and suboptimal dosing practices are significant contributors to the rise of drug resistance [16].”
Background
Environmental pH modulates biofilm formation and matrix composition in Candida albicans and Candida glabrata
Gonçalves, B., Fernandes, L., Henriques, M., & Silva, S. M. (2020) · Biofouling · doi:10.1080/08927014.2020.1793963 · Cited by 22
Effects of Antifungal Agents Alone and in Combination Against Candida glabrata Strains Susceptible or Resistant to Fluconazole
Alves, I. A., Bandeira, L. A., Mario, D. A. N., Denardi, L. B., Neves, L. V., Santúrio, J. M., & Alves, S. H. (2012) · Mycopathologia · doi:10.1007/s11046-012-9538-7 · Cited by 19
“glabrata have shown primary resistance to fluconazole, and others easily develop fluconazole resistance after exposure during treatment [6].”
Background
Structural analysis of the active sites of dihydrofolate reductase from two species of Candida uncovers ligand-induced conformational changes shared among species
Paulsen, J. L., Viswanathan, K., Wright, D. L., & Anderson, A. C. (2013) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2013.01.008 · Cited by 18
Antimycotic Drugs and their Mechanisms of Resistance to Candida Species
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Reconstitution of high-level micafungin resistance detected in a clinical isolate of Candida glabrata identifies functional homozygosity in glucan synthase gene expression
Niimi, K., Woods, M. A., Maki, K., Nakayama, H., Hatakenaka, K., Chibana, H., Ikeda, F., Ueno, K., Niimi, M., Cannon, R. D., et al. (2012) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dks112 · Cited by 18
Fluconazole resistance in Candida glabrata is associated with increased bud formation and metallothionein production
Samaranayake, Y. H., Cheung, B. P. K., Wang, Y., Yau, J. Y. Y., Yeung, K. W. S., & Samaranayake, L. P. (2012) · Journal of Medical Microbiology · doi:10.1099/jmm.0.044123-0 · Cited by 18
“These include increased expression of the ABC transporter genes CDR1 and CDR2 (PDH1), which results in decreased accumulation of intracellular FL (Bennett et al., 2004; Miyazaki et al., 1998; Sanglard et al., 1999), and the increased expression of ERG11 (also known as CYP51) encoding the FL target lanosterol 14a-demet…”
BackgroundInfluential
Candida albicans growth and germ tube formation can be inhibited by simple diphenyl diselenides [(PhSe)2, (MeOPhSe)2, (p-Cl-PhSe)2, (F3CPhSe)2] and diphenyl ditelluride
Rosseti, I. B., Wagner, C., Fachinetto, R., Taube, P. S., & Costa, M. S. (2010) · Mycoses · doi:10.1111/j.1439-0507.2010.01888.x · Cited by 18
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Oral candidosis: characterization of a sample of recurrent infections and study of resistance determinants.
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Unexpected effects of azole transporter inhibitors on antifungal susceptibility in Candida glabrata and other pathogenic Candida species
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Self-citation
In vitrosynergy with fluconazole plus doxycycline or tigecycline against clinicalCandida glabrataisolates
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Sodium houttuyfonate enhances the mono-therapy of fluconazole on oropharyngeal candidiasis (OPC) through HIF-1α/IL-17 axis by inhibiting cAMP mediated filamentation in Candida albicans-Candida glabrata dual biofilms
Chen, M., Cheng, T., Xu, C., Pan, M., Wu, J., Wang, T., Wu, D., Yan, G., Wang, C., & Shao, J. (2022) · Virulence · doi:10.1080/21505594.2022.2035066 · Cited by 14
“glabrata is intrinsically resistant to azole and can readily acquire drug resistance during prolonged azole administration, either in vitro or in vivo [59].”
Background
Secretion of the acid trehalase encoded by the CgATH1 gene allows trehalose fermentation by Candida glabrata
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“…susceptibility to commonly used antifungal agents, or even because of increasing occurrence of drug-resistant strains, contributing to the high mortality rates observed for C. glabrata bloodstream infections (Bouchara et al. 2000; Bennett et al. 2004; Posteraro et al. 2006; Panackal et al. 2006).”
Background
Poly(methyl methacrylate) with Oleic Acid as an Efficient Candida albicans Biofilm Repellent
Petrović, M., Ranđelović, M., Igić, M., Randjelović, M., Arsić-Arsenijević, V. S., Ebersold, M. M., Otašević, S., & Milošević, I. (2022) · Materials · doi:10.3390/ma15113750 · Cited by 13
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“glabrata infection, especially in older patients, is significant given the inherently reduced susceptibility of this species to azoles and the relatively high frequency with which isolates acquire azole resistance during treatment (Bennett et al., 2004; Sanglard et al., 2001).”
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Candidemia in the critically ill: initial therapy and outcome in mechanically ventilated patients
Ferrada, M. A., Quartin, A. A., Kett, D. H., & Morris, M. I. (2013) · BMC Anesthesiology · doi:10.1186/1471-2253-13-37 · Cited by 12
“Some forms of resistance may not be relevant during early therapy; for example, fluconazole resistance in Candida glabrata is mediated by inducible enzymes that may not be expressed early in the course of treatment [30].”
Background
Antifungal Targets, Mechanisms of Action, and Resistance in Candida albicans
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What ‘Omics can tell us about antifungal adaptation
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Resistance to Antifungal Agents
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Differential expression of the Candida glabrata CgRTA1 and CgRSB1 genes in response to various stress conditions
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“Candida glabrata is much more ready to display variation in phenotypes contributing to drug resistance partially due to its haploid nature [32].”
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Antifungal Targets, Mechanisms of Action, and Resistance in Candida albicans
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Proteomic analysis of cytosolic proteins associated with petite mutations in Candida glabrata
y Penha, C. V. L., Kubitschek-Barreira, P. H., Larcher, G., Perales, J., León, I. R., Lopes-Bezerra, L. M., & Bouchara, J. P. (2010) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2010007500125 · Cited by 8
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“The effect of milbemycin A4 oxime upon the uptake of fluconazole was measured in the azole resistant strain, Cg40a, and the azole susceptible mutant, 84870, using our previously published method (Bennett et al., 2004).”
BackgroundMethodInfluentialSelf-citation
Empirical treatment of candidemia in intensive care units: Fluconazole or broad-spectrum antifungal agents?
Guinea, J., Peláez, T., Rodríguez‐Créixems, M., Torres-Narbona, M., Muñóz, P., Alcalá, L., & Bouza, E. (2008) · Medical Mycology · doi:10.1080/13693780802415556 · Cited by 8
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“albicans [3–6] and in a number of non-albicans species as well [7].”
Background
Antifungal susceptibility against yeasts isolated from pediatric oncology patients
Kersun, L. S., Reilly, A. F., Ingram, M. E., Nicholaou, M., & McGowan, K. L. (2008) · Medical Mycology · doi:10.1080/13693780701874523 · Cited by 6
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Yoo, J. I., Kim, H. S., Choi, C. W., Yoo, J. S., Yu, J. Y., & Lee, Y. S. (2013) · Osong Public Health and Research Perspectives · doi:10.1016/j.phrp.2013.10.001 · Cited by 4
Pulsed-Field Gel Electrophoresis
Wu, F., & Della‐Latta, P. (2007) · Springer eBooks · doi:10.1007/0-387-32892-0_9 · Cited by 4
Evaluation of Susceptibility to Fluconazole and Voriconazole in Oral Candida glabrata Isolates from Drug Addicts
Golirad, N., Fozouni, L., & Pordeli, H. (2019) · international journal high risk behaviors & addiction · doi:10.5812/ijhrba.92807 · Cited by 4
“lation of methylated sterols, which disrupt the cell membrane structure and function (9).”
Background
Genotypic, phenotypic, and proteomic characterization of Candida glabrata during sequential fluconazole exposure
Samaranayake, Y. H., Cheung, B. P. K., Yau, J. Y. Y., Yeung, K. W., & Samaranayake, L. P. (2011) · Journal of Investigative and Clinical Dentistry · doi:10.1111/j.2041-1626.2011.00044.x · Cited by 4
Evaluation of Antifungal Selective Toxicity Using Candida glabrata ERG25 and Human SC4MOL Knock-In Strains
Nakano, K., Okamoto, M., Takahashi‐Nakaguchi, A., Sasamoto, K., Yamaguchi, M., & Chibana, H. (2023) · Journal of Fungi · doi:10.3390/jof9101035 · Cited by 3
Hospitalized COVID-19 Patients with Urinary Tract Infection in Iran: Candida Species Distribution and Antifungal Susceptibility Patterns
Shiyadeh, Z. S., Farahyar, S., Larijani, L. V., Beardsley, J., Nouri, N., Mahmoudi, S., Mohammadi, S. R., Rodrigues, C. F., & Roudbary, M. (2024) · Antibiotics · doi:10.3390/antibiotics13070633 · Cited by 3
“Still, antifungal susceptibility testing is highly recommended for clinical isolates of Candida spp. because C. krusei has intrinsic resistance to FLZ [53], and C. glabrata species have been reported as having high MICs values or being FLZ resistant [47].”
BackgroundResult
Emerging Fungal Infections
Garnica, M. M., & Nucci, M. (2010) · Springer eBooks · doi:10.1007/978-3-642-15742-4_27 · Cited by 3
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“glabrata is maintained, or tolerated, at high levels in the kidneys of immunocompetent mice, the mice did not die and there was little inflammation associated with the fungal cells [113, 114].”
Background
Molecular Characterization and In Vitro Antifungal Susceptibility of Candida Glabrata Clinical Isolates with Reduced Echinocandin Susceptibility and High Level Multi-Azole Resistance
Baxa, J. A. V. D. (2014) · Clinical Microbiology Open Access · doi:10.4172/2327-5073.1000154 · Cited by 2
“glabrata is not uncommon (~25%) and is generally due to the upregulation of synthesis of one or more members of two classes of efflux proteins, the ATP binding cassette (ABC) transporters and the major facilitator superfamily (recently known as MDR1) of efflux pumps [4,7-13].”
Background
Using Yeast to Discover Inhibitors of Multidrug Efflux in Candida albicans
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Characterizing Candida glabrata Pdr1, a Hyperactive Transcription Factor Involved in Azole Resistance
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Zap1 is required for Candida glabrata response to fluconazole
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Risk factors associated with fluconazole resistance in Candida parapsilosis candidemia: A case–case study
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“22 This was found to be associated with the development of specific mutations in genes responsible for ergosterol synthesis and decreased affinity for fluconazole.”
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Fungal Infections After Hematopoietic Cell Transplantation
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“Similar effects have been observed in a prophylactic use of fluconazole with Candida glabrata and Candida krusei colonization [31,32].”
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Authors: Bennett, J. E., Izumikawa, K., & Marr, K. A.
Affiliations: National Institutes of Health (US)
University of Washington (US)
ORCID: Bennett, John E.
Izumikawa, Koichi
Marr, Kieren A.
Venue: Antimicrobial Agents and Chemotherapy
Publisher: American Society for Microbiology
Published: 2004-05
Volume: 48
Issue: 5
Pages: 1773-1777
ISSN: 0066-4804 (ISSN-L)
1098-6596
DOI: 10.1128/aac.48.5.1773-1777.2004
PMC: PMC400565
OpenAlex: W2108027055
Cited by: 217
References: 20
Citations by year: 2025: 4 · 2024: 5 · 2023: 2 · 2022: 6 · 2021: 7 · 2020: 6 · 2019: 10 · 2018: 11 · 2017: 10 · 2016: 7 · 2015: 10 · 2014: 15 · 2013: 17 · 2012: 11
FWCI: 8.64
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Antimicrobial Agents and Chemotherapy (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5k08ai001571-02)
National Institute of Allergy and Infectious Diseases (AI01571)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
Life Sciences › Agricultural and Biological Sciences › Plant Science › Fungal Plant Pathogen Control
Keywords: Candida glabrata, fluconazole resistance, antifungal prophylaxis, hematopoietic stem cell transplant recipients, drug efflux, oropharyngeal colonization, invasive candidiasis
MeSH terms: Antifungal Agents, Candidiasis, Fluorescent Dyes, Karyotyping, Rhodamines, Blotting, Northern, Fluconazole, Electrophoresis, Gel, Pulsed-Field, Reverse Transcriptase Polymerase Chain Reaction, Drug Resistance, Fungal, Drug Resistance, Multiple, Fungal, Candida glabrata

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Mechanism of Increased Fluconazole Resistance in Candida glabrata during Prophylaxis

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