Candida glabrata : Review of Epidemiology, Pathogenesis, and Clinical Disease with Comparison to C. albicans

Fidel, Paul L.; Vazquez, Jose A.; Sobel, Jack D.

doi:10.1128/cmr.12.1.80

Cited by 953Antifungal resistance and susceptibilityFungal Infections and StudiesYeasts and Rust Fungi Studies

Candida glabrata : Review of Epidemiology, Pathogenesis, and Clinical Disease with Comparison to C. albicans

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Fidel, Paul L., Vazquez, Jose A., Sobel, Jack D.·1999·Clinical Microbiology Reviews

DOI 10.1128/cmr.12.1.80PMC PMC88907

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Abstract

Until recently, Candida glabrata was considered a relatively nonpathogenic commensal fungal organism of human mucosal tissues. However, with the increased use of immunosuppressive agents, mucosal and systemic infections caused by C. glabrata have increased significantly, especially in the human immunodeficiency virus-infected population. A major obstacle in C. glabrata infections is their innate resistance to azole antimycotic therapy, which is very effective in treating infections caused by other Candida species. Candida glabrata, formerly known as Torulopsis glabrata, contrasts with other Candida species in its nondimorphic blastoconidial morphology and haploid genome. C. glabrata currently ranks second or third as the causative agent of superficial (oral, esophageal, vaginal, or urinary) or systemic candidal infections, which are often nosocomial. Currently, however, there are few recognized virulence factors of C. glabrata and little is known about the host defense mechanisms that protect against infection. Two established animal models (systemic and vaginal) have been established to study treatment, pathogenesis, and immunity. Treatment of C. glabrata infections can include azoles but often requires amphotericin B or flucytosine. This review summarizes all known clinical and experimental information about C. glabrata infections with comparisons to C. albicans as a means of contrasting the two species commonly observed and emphasizing the many recognized differences.

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C. glabrata is a causative agent of urinary tract and vaginal infections.
“C. glabrata is also a causative agent of urinary tract and vaginal infections [10,11].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [10]
The number of candidiasis due to non-Candida albicans Candida (NCAC) species has meaningfully increased, namely in regard to Candida glabrata strains.
“in the last few decades, the number of candidiasis due to non-Candida albicans Candida (NCAC) species has meaningfully raised, namely in regard to C. glabrata strains [1,10,11].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [1]
After Candida albicans, Candida glabrata is one of the most prevalent pathogenic fungi in humans.
“After Candida albicans, Candida glabrata is one of the most prevalent pathogenic fungi in humans.”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [1]
The NHDS approach is likely to underestimate both incidence and mortality of invasive candidiasis because of miscoding, use of codes not captured by the analysis, or failure to code the infection at all.
“Although this approach provides a much more generalizable sample of U.S. hospitals than many other methods of surveillance, it is likely to underestimate both incidence and mortality because of miscoding of IC, use of codes not captured by the analysis, or failure to code the infection at all (79, 154).”
From Epidemiology of Invasive Candidiasis: a Persistent Public Health Problem (2007) · cites this paper as [79]

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Epidemiology of Invasive Candidiasis: a Persistent Public Health Problem
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Effect of Candida glabrata FKS1 and FKS2 Mutations on Echinocandin Sensitivity and Kinetics of 1,3-β- <scp>d</scp> -Glucan Synthase: Implication for the Existing Susceptibility Breakpoint
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Candida Species Exhibit Differential In Vitro Hemolytic Activities
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The epidemiology and outcomes of invasive Candida infections among organ transplant recipients in the United States: results of the Transplant‐Associated Infection Surveillance Network (TRANSNET)
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The Presence of an FKS Mutation Rather than MIC Is an Independent Risk Factor for Failure of Echinocandin Therapy among Patients with Invasive Candidiasis Due to Candida glabrata
Shields, R. K., Nguyen, M. H., Press, E. G., Kwa, A. L., Cheng, S., Du, C., & Clancy, C. J. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00027-12 · Cited by 171 · see citing works
Mechanisms of Azole Resistance in Petite Mutants of Candida glabrata
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The ATP‐binding cassette transporter–encoding gene CgSNQ2 is contributing to the CgPDR1‐dependent azole resistance of Candida glabrata
Torelli, R., Posteraro, B., Ferrari, S., La Sorda, M., Fadda, G., Sanglard, D., & Sanguinetti, M. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06143.x · Cited by 141 · see citing works
Prevalence and Antifungal Susceptibility of 442 Candida Isolates from Blood and Other Normally Sterile Sites: Results of a 2-Year (1996 to 1998) Multicenter Surveillance Study in Quebec, Canada
St-Germain, G., Laverdière, M., Pelletier, R., Bourgault, A.-M., Libman, M., Lemieux, C., & Noël, G. (2001) · Journal of Clinical Microbiology · doi:10.1128/jcm.39.3.949-953.2001 · Cited by 134 · see citing works
Candida glabrata: A Lot More Than Meets the Eye
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Candida glabrata Biofilms: How Far Have We Come?
Rodrigues, C., Rodrigues, M., Silva, S., & Henriques, M. (2017) · Journal of Fungi · doi:10.3390/jof3010011 · Cited by 129 · see citing works
Overexpression of Aldo-Keto-reductase in Azole-resistant clinical isolates of Candida glabrata determined by cDNA-AFLP
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Candida glabratadisplays pseudohyphal growth
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A Nonsense Mutation in the ERG6 Gene Leads to Reduced Susceptibility to Polyenes in a Clinical Isolate of Candida glabrata
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Haploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae
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Role of dectin-2 for host defense against systemic infection with Candida glabrata
Ifrim, D. C., Bain, J. M., Reid, D. M., Oosting, M., Verschueren, I., Gow, N. A. R., van Krieken, J. H., Brown, G. D., Kullberg, B.-J., Joosten, L. A. B., et al. (2014) · Infection and Immunity · doi:10.1128/iai.01189-13 · Cited by 117 · see citing works
Guideline: Vulvovaginal Candidosis (AWMF 015/072), S2k (Excluding Chronic Mucocutaneous Candidosis)
Mendling, W. (2015) · Mycoses · doi:10.1111/myc.12292 · Cited by 117 · see citing works
Facultative Sterol Uptake in an Ergosterol-Deficient Clinical Isolate of Candida glabrata Harboring a Missense Mutation in ERG11 and Exhibiting Cross-Resistance to Azoles and Amphotericin B
Hull, C. M., Parker, J. E., Bader, O., Weig, M., Gross, U., Warrilow, A. G. S., Kelly, D. E., & Kelly, S. L. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.06253-11 · Cited by 113 · see citing works
Intestinal Resident Yeast Candida glabrata Requires Cyb2p-Mediated Lactate Assimilation to Adapt in Mouse Intestine
Ueno, K., Matsumoto, Y., Uno, J., Sasamoto, K., Sekimizu, K., Kinjo, Y., & Chibana, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024759 · Cited by 109 · see citing works
Divergent Approaches to Virulence in C. albicans and C. glabrata: Two Sides of the Same Coin
Galocha, M., Pais, P., Cavalheiro, M., Pereira, D., Viana, R., & Teixeira, M. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092345 · Cited by 105 · see citing works
Candida glabrata and Candida albicans co‐infection of an in vitro oral epithelium
Silva, S., Henriques, M., Hayes, A., Oliveira, R., Azeredo, J., & Williams, D. W. (2011) · Journal of Oral Pathology & Medicine · doi:10.1111/j.1600-0714.2010.00981.x · Cited by 108 · see citing works
Phenotypic switching and filamentation in Candida glabrata
Lachke, S. A., Joly, S., Daniels, K., & Soll, D. R. (2002) · Microbiology · doi:10.1099/00221287-148-9-2661 · Cited by 103 · see citing works
The effect of silver nanoparticles and nystatin on mixed biofilms ofCandida glabrataandCandida albicanson acrylic
Silva, S., Pires, P., Monteiro, D. R., Negri, M., Gorup, L. F., Camargo, E. R., Barbosa, D. B., Oliveira, R., Williams, D. W., Henriques, M., et al. (2013) · Medical Mycology · doi:10.3109/13693786.2012.700492 · Cited by 101 · see citing works
Host Iron Withholding Demands Siderophore Utilization for Candida glabrata to Survive Macrophage Killing
Nevitt, T., & Thiele, D. J. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1001322 · Cited by 95 · see citing works
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Two Clinical Isolates of Candida glabrata Exhibiting Reduced Sensitivity to Amphotericin B Both Harbor Mutations in ERG2
Hull, C. M., Bader, O., Parker, J. E., Weig, M., Gross, U., Warrilow, A. G. S., Kelly, D. E., & Kelly, S. L. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01145-12 · Cited by 90 · see citing works
Mining the oral mycobiome: Methods, components, and meaning
Diaz, P. I., Hong, B.-Y., Dupuy, A. K., & Strausbaugh, L. D. (2017) · Virulence · doi:10.1080/21505594.2016.1252015 · Cited by 87 · see citing works
Comparison of Sterol Import under Aerobic and Anaerobic Conditions in Three Fungal Species, Candida albicans, Candida glabrata, and Saccharomyces cerevisiae
Zavrel, M., Hoot, S. J., & White, T. C. (2013) · Eukaryotic Cell · doi:10.1128/ec.00345-12 · Cited by 86 · see citing works
Changes in Karyotype and Azole Susceptibility of Sequential Bloodstream Isolates from Patients with Candida glabrata Candidemia
Shin, J. H., Chae, M. J., Song, J. W., Jung, S.-I., Cho, D., Kee, S. J., Kim, S. H., Shin, M. G., Suh, S. P., & Ryang, D. W. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.00381-07 · Cited by 86 · see citing works
Multiple Patterns of Resistance to Fluconazole in Candida glabrata Isolates from a Patient with Oropharyngeal Candidiasis Receiving Head and Neck Radiation
Redding, S. W., Kirkpatrick, W. R., Saville, S., Coco, B. J., White, W., Fothergill, A., Rinaldi, M., Eng, T., Patterson, T. F., & Lopez-Ribot, J. (2003) · Journal of Clinical Microbiology · doi:10.1128/jcm.41.2.619-622.2003 · Cited by 85 · see citing works
Candida Species: New Insights into Biofilm Formation
Cuéllar-Cruz, M., López-Romero, E., Villagómez-Castro, J. C., & Ruiz-Baca, E. (2012) · Future Microbiology · doi:10.2217/fmb.12.48 · Cited by 80 · see citing works
The Rewiring of Ubiquitination Targets in a Pathogenic Yeast Promotes Metabolic Flexibility, Host Colonization and Virulence
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Transcription factors CgUPC2A and CgUPC2B regulate ergosterol biosynthetic genes in Candida glabrata: Gene expression in sterol-depleted Candida
Nagi, M., Nakayama, H., Tanabe, K., Bard, M., Aoyama, T., Okano, M., Higashi, S., Ueno, K., Chibana, H., Niimi, M., et al. (2011) · Genes to Cells · doi:10.1111/j.1365-2443.2010.01470.x · Cited by 68 · see citing works
A systematic analysis reveals an essential role for high-affinity iron uptake system, haemolysin and CFEM domain-containing protein in iron homoeostasis and virulence in Candida glabrata
Srivastava, V. K., Suneetha, K. J., & Kaur, R. (2014) · Biochemical Journal · doi:10.1042/bj20140598 · Cited by 69 · see citing works
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Assessment of Candida glabrata Strain Relatedness by Pulsed-Field Gel Electrophoresis and Multilocus Sequence Typing
Lin, C.-Y., Chen, Y.-C., Lo, H.-J., Chen, K.-W., & Li, S.-Y. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.00699-07 · Cited by 62 · see citing works
Ibrexafungerp, a Novel Oral Triterpenoid Antifungal in Development: Overview of Antifungal Activity Against Candida glabrata
Gamal, A., Chu, S., McCormick, T. S., Borroto-Esoda, K., Angulo, D., & Ghannoum, M. A. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.642358 · Cited by 58 · see citing works
Multilocus sequence type analysis reveals both clonality and recombination in populations of Candida glabrata bloodstream isolates from U.S. surveillance studies
Lott, T. J., Frade, J. P., & Lockhart, S. R. (2010) · Eukaryotic Cell · doi:10.1128/ec.00002-10 · Cited by 58 · see citing works
Genome structure and dynamics of the yeast pathogen Candida glabrata
Ahmad, K. M., Kokošar, J., Guo, X., Gu, Z., Ishchuk, O. P., & Piškur, J. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12145 · Cited by 57 · see citing works
Effects of fluconazole onCandida glabratabiofilms and its relationship with ABC transporter gene expression
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Glutathione biosynthesis in the yeast pathogens Candida glabrata and Candida albicans: Essential in C. glabrata, and essential for virulence in C. albicans
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Current trends in candidemia and species distribution among adults: Candida glabrata surpasses C. albicans in diabetic patients and abdominal sources
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New Mechanisms of Flucytosine Resistance in C. glabrata Unveiled by a Chemogenomics Analysis in S. cerevisiae
Costa, C., Ponte, A., Pais, P., Santos, R., Cavalheiro, M., Yaguchi, T., Chibana, H., & Teixeira, M. C. (2015) · PLOS ONE · doi:10.1371/journal.pone.0135110 · Cited by 46 · see citing works
Oral Ibrexafungerp: An Investigational Agent for the Treatment of Vulvovaginal Candidiasis
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The PathoYeastract database: an information system for the analysis of gene and genomic transcription regulation in pathogenic yeasts
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New regulators of biofilm development in Candida glabrata
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A Transcriptomics Approach To Unveiling the Mechanisms of In Vitro Evolution towards Fluconazole Resistance of a Candida glabrata Clinical Isolate
Cavalheiro, M., Costa, C., Silva-Dias, A., Miranda, I. M., Wang, C., Pais, P., Pinto, S. N., Mil-Homens, D., Sato-Okamoto, M., Takahashi-Nakaguchi, A., et al. (2019) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00995-18 · Cited by 42 · see citing works
Epithelial GM-CSF Induction by Candida glabrata
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Phosphorylation of Candida glabrata ATP-binding Cassette Transporter Cdr1p Regulates Drug Efflux Activity and ATPase Stability
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Influence of antifungal polyenes on the adhesion of Candida albicans and Candida glabrata to human epithelial cells in vitro
Dorocka-Bobkowska, B., Konopka, K., & Düzgüneş, N. (2003) · Archives of Oral Biology · doi:10.1016/s0003-9969(03)00174-2 · Cited by 32 · 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
Candida glabrata : new tools and technologies—expanding the toolkit
Ho, H.-L., & Haynes, K. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov066 · Cited by 29 · see citing works
Oral epithelium–Candida glabrata interactions in vitro
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Small chromosomes among Danish Candida glabrata isolates originated through different mechanisms
Ahmad, K. M., Ishchuk, O. P., Hellborg, L., Jørgensen, G., Skvarc, M., Stenderup, J., Jørck-Ramberg, D., Polakova, S., & Piškur, J. (2013) · Antonie van Leeuwenhoek · doi:10.1007/s10482-013-9931-3 · Cited by 29 · see citing works
The phosphoinositide 3-kinase regulates retrograde trafficking of the iron permease CgFtr1 and iron homeostasis in Candida glabrata
Sharma, V., Purushotham, R., & Kaur, R. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.751529 · Cited by 22 · see citing works
Ploidy Variation and Spontaneous Haploid-Diploid Switching of Candida glabrata Clinical Isolates
Zheng, Q., Liu, J., Qin, J., Wang, B., Bing, J., Du, H., Li, M., Yu, F., & Huang, G. (2022) · mSphere · doi:10.1128/msphere.00260-22 · Cited by 20 · see citing works
Differential cell wall remodeling of two chitin synthase deletants Δchs3A and Δchs3B in the pathogenic yeast Candida glabrata: Cell wall remodeling of Δchs3 mutants
Ueno, K., Namiki, Y., Mitani, H., Yamaguchi, M., & Chibana, H. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00728.x · Cited by 17 · see citing works
Genome‐wide survey of transcriptional initiation in the pathogenic fungus, Candida glabrata
Aoyama, T., Nakayama, H., Ueno, K., Inukai, T., Tanabe, K., Nagi, M., Bard, M., & Chibana, H. (2014) · Genes to Cells · doi:10.1111/gtc.12147 · Cited by 12 · see citing works
Candida glabrata induced infection of rat tracheal epithelial cells is mediated by TLR-2 induced activation of NF-κB
Zhang, X., Bai, J., Wu, C.-L., Wu, Y., Zhao, Y., Song, W.-M., & Luo, X.-P. (2016) · Microbial Pathogenesis · doi:10.1016/j.micpath.2015.10.009 · Cited by 11 · see citing works

Time-to-reporting of blood culture positivity and central venous catheter-associated Candida glabrata fungemia in cancer patients
Stempel, J. M., Farmakiotis, D., Tarrand, J. J., & Kontoyiannis, D. P. (2016) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2016.04.001 · Cited by 7 · see citing works
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Authors: Fidel, P. L., Vazquez, J. A., & Sobel, J. D.
Affiliations: Louisiana State University (US)
Division of Infectious Diseases, Wayne State University School of Medicine, Detroit, Michigan2
Wayne State University (US)
ORCID: Fidel, Paul L.
Sobel, Jack D.
Venue: Clinical Microbiology Reviews
Publisher: American Society for Microbiology
Published: 1999-01
Volume: 12
Issue: 1
Pages: 80-96
ISSN: 0893-8512 (ISSN-L)
1098-6618
DOI: 10.1128/cmr.12.1.80
PMC: PMC88907
OpenAlex: W2143839871
Cited by: 953
References: 183
Citations by year: 2026: 15 · 2025: 17 · 2024: 35 · 2023: 43 · 2022: 33 · 2021: 40 · 2020: 37 · 2019: 42 · 2018: 36 · 2017: 48 · 2016: 48 · 2015: 51 · 2014: 51 · 2013: 42 · 2012: 43
FWCI: 18.03
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Clinical Microbiology Reviews (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
Keywords: Candida glabrata, Candida albicans, candidiasis, azole resistance, immunosuppression, HIV infection, nosocomial infections, virulence factors, host defense, animal models of infection, amphotericin B, 5-fluorocytosine, superficial candidiasis, systemic candidiasis, haploid genome
MeSH terms: Animals, Candida, Candida albicans, Candidiasis, Female, Humans

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Candida glabrata : Review of Epidemiology, Pathogenesis, and Clinical Disease with Comparison to C. albicans

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