Candida albicans Biofilms and Human Disease
Open accessAbstract
In humans, microbial cells (including bacteria, archaea, and fungi) greatly outnumber host cells. Candida albicans is the most prevalent fungal species of the human microbiota; this species asymptomatically colonizes many areas of the body, particularly the gastrointestinal and genitourinary tracts of healthy individuals. Alterations in host immunity, stress, resident microbiota, and other factors can lead to C. albicans overgrowth, causing a wide range of infections, from superficial mucosal to hematogenously disseminated candidiasis. To date, most studies of C. albicans have been carried out in suspension cultures; however, the medical impact of C. albicans (like that of many other microorganisms) depends on its ability to thrive as a biofilm, a closely packed community of cells. Biofilms are notorious for forming on implanted medical devices, including catheters, pacemakers, dentures, and prosthetic joints, which provide a surface and sanctuary for biofilm growth. C. albicans biofilms are intrinsically resistant to conventional antifungal therapeutics, the host immune system, and other environmental perturbations, making biofilm-based infections a significant clinical challenge. Here, we review our current knowledge of biofilms formed by C. albicans and closely related fungal species.
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TL;DR
This review summarizes how *Candida albicans* forms biofilms on medical devices and mucosal surfaces, and how these communities resist antifungal drugs and host defenses. It highlights a six-regulator transcriptional network, matrix- and persister-mediated drug resistance, and the clinical burden of biofilm infections.
Key findings
- *C. albicans* biofilm development proceeds through four stages: adherence of yeast cells, proliferation into a basal layer, growth of pseudohyphae/hyphae with extracellular matrix production, and dispersal of yeast-form cells. Mature biofilms typically form within 24 hours in vitro.
- Six master transcriptional regulators (Efg1, Tec1, Bcr1, Ndt80, Brg1, Rob1) are each required for biofilm development in vitro and in rat catheter/denture models; together they directly bind and likely regulate approximately 1,000 target genes. The review counts 50 transcriptional regulators and 101 nonregulatory genes with functionally validated biofilm roles.
- Biofilm resistance involves early and sustained efflux pump upregulation, extracellular matrix components including β-1,3-glucan and extracellular DNA, and metabolically dormant persister cells. Matrix composition is reported as ~55% proteins/glycoproteins, 25% carbohydrates, 15% lipids, and 5% nucleic acids, with over 500 proteins identified.
- Clinical impact: NIH estimates biofilms account for over 80% of microbial infections in the United States; CTG clade species account for 15% of hospital-acquired sepsis and are the fourth most frequent cause of bloodstream infections; over 5 million central venous catheters are placed annually in the United States (1992–2001 data), with biofilm infection in over 50%; estimated 100,000 deaths and $6.5 billion in excess expenditure annually in the United States; disseminated candidiasis mortality approaches 40% in some cases.
Methods
- Narrative review of published literature on *C. albicans* and related fungal biofilms; no new experimental data are reported.
- Synthesizes in vitro biofilm models (e.g., silicone squares, flow cells), in vivo/ex vivo animal models (rat/rabbit catheter, denture stomatitis, vaginal mucosal, bioluminescence), and genetic/genomic/proteomic studies (knockout screens, transcriptional profiling, proteomics).
- Main analysis is qualitative synthesis, including tables of 50 transcriptional regulators and 101 nonregulatory genes with validated biofilm roles.
Limitations
- Stated: little is known about persister cell formation and regulation; virtually nothing is known about interactions among *Candida* species in polymicrobial biofilms; the majority of newly identified biofilm-network target genes remain unstudied; the biofilm network outline is “undoubtedly incomplete”; and biofilm formation is often loosely defined in non-*Candida* fungi.
- Evident: as a review, it does not present primary experimental data, and its conclusions depend on the designs and conditions of cited studies; many mechanistic findings come from in vitro models or non-*C. albicans* species.
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Integrity signals
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Claims the paper makes
0 of 170 cited sources checked · 0 supported · 0 flagged
- Findingcitation
Each master regulator controls the expression of the other master regulators, resulting in a complex, intertwined regulatory network.
“Each master regulator also controls the expression of the other master regulators, resulting in a complex, intertwined regulatory network.”
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- Findingcitation
Many hundreds of mRNAs and proteins are differentially expressed between biofilms and planktonic cells.
“These studies have revealed that many hundreds of mRNAs and proteins are differentially expressed between biofilms and planktonic cells.”
Quote in the paperNot a substantial claim0 of 3 sources checked - Findingcitation
The network consists of six master transcriptional regulators (Efg1, Tec1, Bcr1, Ndt80, Brg1, and Rob1), each required for biofilm development in both in vitro and in vivo rat catheter and rat denture models.
“This network consists of six master transcriptional regulators (Efg1, Tec1, Bcr1, Ndt80, Brg1, and Rob1), each of which is required for biofilm development in both in vitro and in vivo rat catheter and rat denture models (140).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [140] source
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- Findingcitation
Biofilm architectures in rat and rabbit central venous and indwelling urinary catheter models and in rat denture stomatitis models include numerous yeast cells in the basal region, and hyphae and extracellular matrix extending throughout the biofilm.
“Biofilm architectures in rat and rabbit central venous and indwelling urinary catheter models and in rat denture stomatitis models also include numerous yeast cells in the basal region, and hyphae and extracellular matrix extending throughout the biofilm (5, 84, 131, 134, 166, 173, 199).”
Quote in the paperNot a substantial claim0 of 3 sources checked - Findingown data
Based on the current literature, there are 50 transcriptional regulators and 101 nonregulatory genes with functionally validated roles in biofilm formation.
“Based on the current literature, we count 50 transcriptional regulators (Table 1) and 101 nonregulatory genes (Table 2) that have functionally validated roles in biofilm formation.”
Quote in the paperNot a substantial claim
- Findingcitation
Vaginal mucosal mouse models show similar biofilm architectures, with clear yeast, hyphae, and extracellular matrix throughout biofilms formed on top of mucosal layers.
“Vaginal mucosal mouse models, both in vivo (live mice inoculated with C. albicans on the vaginal mucosa) and ex vivo (vaginas excised from euthanized mice and then inoculated with C. albicans in tissue culture plates), show similar biofilm architectures, with clear yeast, hyphae, and extracellular matrix evident throughout the biofilms formed on top of the mucosal layers (72).”
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- Findingcitation
Candida biofilms obtained from patients with denture stomatitis and from patients with infected intravascular catheters confirm the presence of yeast, hyphae, and extracellular matrix.
“For example, Candida biofilms obtained from patients with denture stomatitis and from patients with infected intravascular catheters confirm the presence of yeast, hyphae and extracellular matrix (114, 162).”
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Deletion of RLM1 causes a reduction in matrix levels.
“Deletion of RLM1 causes a reduction in matrix levels (136), whereas deletion of ZAP1 leads to an increase in the accumulation of extracellular matrix material, probably by upregulating the glucoamylases Gca1 and Gca2 (144).”
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- Findingcitation
Of these 30 transcriptional regulators, 4 (Bcr1, Ace2, Snf5, and Arg81) were also required for biofilm formation under common conditions (shaking in microtiter plates) for in vitro biofilm formation.
“Of these 30, 4 (Bcr1, Ace2, Snf5, and Arg81) were also required for biofilm formation under common conditions (shaking in microtiter plates) for in vitro biofilm formation.”
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- Findingcitation
Two known transcriptional regulators of biofilm matrix production in C. albicans are Rlm1 and Zap1.
“Two known transcriptional regulators of biofilm matrix production in C. albicans are Rlm1 and Zap1.”
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The biofilm master regulator Bcr1 and some of its downstream targets, including Als1, Als3, and Hwp1, are all required for adherence during biofilm formation.
“For example, the biofilm master regulator Bcr1 and some of its downstream targets, including the cell wall proteins Als1, Als3, and Hwp1, are all required for adherence during biofilm formation (23, 138, 141, 143, 145, 212).”
Quote in the paperNot a substantial claim0 of 3 sources checked - Findingcitation
30 transcriptional regulators were identified as important for adherence to a silicone substrate under in vitro flow cell conditions.
“Here, 30 transcriptional regulators were identified as important for adherence to a silicone substrate under these conditions.”
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- Findingcitation
The majority of the 44 additional transcriptional regulators are directly bound by at least one of the 6 master biofilm network regulators.
“The majority of these regulators are directly bound by at least one of the 6 master biofilm network regulators, indicating that they have direct regulatory connections to the core biofilm circuit (Table 1).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Table 1
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- Findingcitation
The drug resistance of persister cells is independent of cell membrane composition and efflux pump expression; rather, it is the result of the metabolically dormant state of the cells.
“Although we know little about the formation and roles of persister cells in C. albicans biofilms, we do know that the drug resistance of persister cells is independent of cell membrane composition and efflux pump expression; rather, it is the result of the metabolically dormant state of the cells (88, 100).”
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Over 500 proteins were identified in the C. albicans biofilm matrix.
“Over 500 proteins were identified in the matrix.”
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- Findingcitation
Polysaccharides make up the second major fraction of the matrix, consisting largely of mannan-glucan complexes made predominantly of α-1,6-linked mannan and α-1,2-linked side chains complexed to β-1,6-glucan.
“Polysaccharides make up the second major fraction of the matrix, consisting largely of mannan-glucan complexes made predominantly of α-1,6-linked mannan and α-1,2-linked side chains complexed to β-1,6-glucan (209).”
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- Findingcitation
The polysaccharide β-1,3-glucan is a known constituent of the biofilm matrix that contributes to its drug-resistance properties.
“One known constituent of the biofilm matrix that contributes to its drug-resistance properties is the polysaccharide β-1,3-glucan (130).”
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- Findingcitation
Treatment of biofilms with DNAse enhanced the activity of caspofungin and amphotericin B in disrupting mature C. albicans biofilms.
“For example, one study reported that treatment of biofilms with DNAse enhanced the activity of caspofungin and amphotericin B in disrupting mature C. albicans biofilms (116).”
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- Findingcitation
The C. albicans biofilm matrix is predominantly composed of proteins and glycoproteins (55%), carbohydrates (25%), lipids (15%), and nucleic acids (5%).
“The C. albicans biofilm matrix is predominantly composed of proteins and glycoproteins (55%), carbohydrates (25%), lipids (15%), and nucleic acids (5%).”
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- Findingcitation
The transcriptional regulator Rlm1 contributes to antifungal drug resistance by regulating the expression of FKS1.
“The transcriptional regulator Rlm1 (discussed above) contributes to antifungal drug resistance by regulating the expression of FKS1 (136).”
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- Findingcitation
Depletion of Hsp90 markedly reduces the number of dispersed cells from a biofilm.
“The molecular chaperone Hsp90 has also been implicated in C. albicans biofilm dispersal, as depletion of Hsp90 markedly reduces the number of dispersed cells from a biofilm (167).”
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- Premisecitation
A near-universal characteristic of biofilms, compared with their free-floating counterparts, is the greater resistance of their cells to chemical and physical insults.
“A near-universal characteristic of biofilms, compared with their free-floating counterparts, is the greater resistance of their cells to chemical and physical insults (31, 32).”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisereasoning
Alterations in the host microbiota, host immune response, or local environment can enable C. albicans to overgrow and cause infection.
“However, alterations in the host microbiota (e.g., due to antibiotics), changes in the host immune response (e.g., during stress, infection by another microbe, or immunosuppressant therapy), or variations in the local environment (e.g., shifts in pH or nutritional content) can enable C. albicans to overgrow and cause infection.”
Quote in the paperNot a substantial claim - Interpretationnone given
The medical impact of C. albicans depends on its ability to thrive as a biofilm.
“the medical impact of C. albicans (like that of many other microorganisms) depends on its ability to thrive as a biofilm, a closely packed community of cells.”
Quote in the paperSubstantial claim - Premisecitation
C. albicans is a member of the healthy microbiota, asymptomatically colonizing the gastrointestinal tract, reproductive tract, oral cavity, and skin of most humans.
“It is a member of the healthy microbiota, asymptomatically colonizing the gastrointestinal (GI) tract, reproductive tract, oral cavity, and skin of most humans (1, 64, 87, 97, 99).”
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C. albicans produces highly structured biofilms composed of multiple cell types encased in an extracellular matrix.
“C. albicans produces highly structured biofilms composed of multiple cell types (i.e., round, budding yeast-form cells; oval pseudohyphal cells; and elongated, cylindrical hyphal cells) encased in an extracellular matrix (23, 61, 158, 161).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationcitation
Together, the six master regulators directly bind to the promoters of and very likely regulate approximately 1,000 target genes.
“Together, these six master regulators directly bind to the promoters of and very likely regulate the expression of approximately 1,000 target genes, some of which are additional transcriptional regulators.”
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- Interpretationcitation
In vitro biofilm formation has, for the most part, correlated well with in vivo and ex vivo biofilm models.
“In vitro biofilm formation has, for the most part, correlated well with in vivo and ex vivo biofilm models.”
Quote in the paperNot a substantial claim - Premisereasoning
C. albicans is not genetically tractable in the conventional sense.
“Although C. albicans is not genetically tractable in the conventional sense (its parasexual cycle is cumbersome to use in the lab), its genome is relatively simple to alter using recombinant DNA technologies.”
Quote in the paperNot a substantial claim - Premisecitation
C. albicans biofilm formation comprises four temporal stages: adherence to a surface, proliferation to form a basal layer, growth of pseudohyphae and hyphae with extracellular matrix production, and slow dispersal of yeast-form cells.
“C. albicans biofilm formation comprises four temporal stages (10, 23, 47, 75, 142, 194) (Figure 1): (a) adherence to a surface (spherical yeast cells), (b) proliferation to form a basal layer of anchoring cells, (c) growth of pseudohyphae (ellipsoid cells joined end to end) and hyphae (chains of cylindrical cells) concomitant with production of extracellular matrix material, and (d) slow dispersal”
Quote in the paperNot a substantial claim0 of 3 sources checked - Interpretationcitation
Because fungal biofilms are largely resistant to current antifungal drugs, high antifungal doses together with removal of the colonized medical device are generally required to treat infections.
“Because fungal biofilms are largely resistant to current antifungal drugs, high antifungal doses together with removal of the colonized medical device are generally required to treat infections (6, 29, 104, 112, 121).”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
A large transcriptional network that controls the development of C. albicans biofilms was described in 2012.
“In 2012, a large transcriptional network that controls the development of C. albicans biofilms was described (140).”
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- Interpretationreasoning
The recent evolution of C. albicans biofilm ability provides an explanation as to why C. albicans and closely related species are only a few of the many fungal species able to form biofilms within a mammalian host.
“This inference provides an explanation as to why C. albicans and closely related species are only a few of the many fungal species able to form biofilms within a mammalian host.”
Quote in the paperSubstantial claim - Interpretationcitation
Nrg1 probably acts through a Set3 chromatin-modifying complex.
“Nrg1 probably acts through a Set3 chromatin-modifying complex (77, 139).”
Quote in the paperNot a substantial claim0 of 2 sources checked - Interpretationreasoning
The ability to form hyphae and the ability of these hyphae to adhere to one another and to yeast cells are critical for normal biofilm development and maintenance.
“Thus, the ability to form hyphae and the ability of these hyphae to adhere to one another and to yeast cells are critical for normal biofilm development and maintenance.”
Quote in the paperSubstantial claim - Premisenone given
The ability of cells in a biofilm to adhere to each other and to surfaces is important for all stages of C. albicans biofilm development.
“The ability of cells in a biofilm to adhere to each other and to surfaces, which can be hard (a medical device) or soft (a mucosal layer), is important for all stages of C. albicans biofilm development.”
Quote in the paperSubstantial claim - Premisenone given
Mature C. albicans biofilms are encased in a complex material known as the extracellular matrix.
“Mature C. albicans biofilms are encased in a complex material known as the extracellular matrix.”
Quote in the paperNot a substantial claim - Premisecitation
Various target genes play roles in hyphal formation, adhesion, drug resistance, and matrix production.
“Work carried out in both planktonic and biofilm conditions has indicated that various target genes play roles in hyphal formation, adhesion, drug resistance, and matrix production (see 61 for a summary), all of which are important characteristics of biofilms.”
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- Interpretationreasoning
The hyphae in biofilms contribute to the overall architectural stability of the biofilm, acting as a support scaffold for yeast cells and other hyphae.
“The hyphae in biofilms contribute to the overall architectural stability of the biofilm, acting as a support scaffold for yeast cells and other hyphae.”
Quote in the paperSubstantial claim - Premisereasoning
The inherent resistance of C. albicans biofilms to antimicrobial agents is a key feature of the biofilm mode of growth.
“The inherent resistance of C. albicans biofilms to antimicrobial agents is a key feature of the biofilm mode of growth.”
Quote in the paperSubstantial claim - Interpretationcitation
Depletion of Hsp90 induces filamentation by relieving Hsp90-mediated repression of the cAMP-PKA signaling pathway.
“Depletion of Hsp90 also induces filamentation by relieving Hsp90-mediated repression of the cAMP-PKA signaling pathway (181).”
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- Interpretationreasoning
The automatic upregulation of efflux pumps contributes to the recalcitrance of biofilms to treatment with antifungal agents.
“This seemingly automatic upregulation of efflux pumps clearly contributes to the recalcitrance of biofilms to treatment with antifungal agents; it may be a manifestation of small-molecule warfare between C. albicans and other microbial species that occupy the same environmental niches.”
Quote in the paperSubstantial claim - Premisecitation
Genes involved in production and delivery of β-1,3-glucans include the synthase-encoding gene FKS1 and the genes BGL2, XOG1, and PHR1.
“Genes involved in production and delivery of β-1,3-glucans include the synthase-encoding gene FKS1 and the genes BGL2, XOG1, and PHR1, which encode proteins involved in the modification and transport of β-glucans (132, 189).”
Quote in the paperNot a substantial claim0 of 2 sources checked - Premisecitation
In C. albicans, two major classes of efflux pumps modulate drug exportation: the ATP-binding cassette transporter superfamily (including CDR1 and CDR2) and the major facilitator class (including MDR1).
“In C. albicans, two major classes of efflux pumps modulate drug exportation: the ATP-binding cassette transporter superfamily (including CDR1 and CDR2) and the major facilitator class (including MDR1) (4, 33, 156).”
Quote in the paperNot a substantial claim0 of 3 sources checked - Interpretationreasoning
Both yeast-form and filamentous cells are required for fully functioning biofilms.
“Thus, both types of cells are required for fully functioning biofilms.”
Quote in the paperSubstantial claim - Premisecitation
C. albicans is not the only fungal species that can form biofilms in a mammalian host.
“As mentioned, C. albicans is not the only fungal species that can form biofilms in a mammalian host.”
Quote in the paperNot a substantial claim - Premisecitation
Candida glabrata forms thin biofilms in vitro without hyphal cells on biotic and abiotic surfaces associated with the human host.
“Candida glabrata (which, despite the name, lies well outside the CTG clade phylogenetically) forms thin biofilms in vitro (without hyphal cells) on biotic and abiotic surfaces associated with the human host (157).”
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- Interpretationreasoning
Among the CTG clade, C. albicans is probably the best biofilm former in the sense that it can form relatively thick biofilms under many different environmental conditions.
“Thus, among the CTG clade, C. albicans is probably the best biofilm former in the sense that it can form relatively thick biofilms under many different environmental conditions.”
Quote in the paperNot a substantial claim - Premisecitation
Morphological examination of lung tissue infected by Pneumocystis jirovecii reveals a biofilm-like growth structure consisting of round yeast-form clusters that can be recapitulated in vitro under certain laboratory conditions.
“Morphological examination of lung tissue infected by P. jirovecii reveals a biofilm-like growth structure consisting of round yeast-form clusters that can be recapitulated in vitro under certain laboratory conditions (35, 36).”
Quote in the paperNot a substantial claim0 of 2 sources checked - Interpretationreasoning
Given that the C. albicans biofilm circuit is a recent evolutionary innovation, it is likely that biofilms from more distantly related fungal species were also relatively recent innovations that independently evolved along those clades.
“The type of biofilm formed by C. albicans is probably unique to the CTG clade; given that the C. albicans biofilm circuit is a recent evolutionary innovation, it is likely that biofilms from more distantly related fungal species were also relatively recent innovations that independently evolved along those clades.”
Quote in the paperNot a substantial claim - Interpretationreasoning
It is unlikely that biofilms from fungal species hundreds of millions of years distant from C. albicans are similar in detail.
“Thus, it is unlikely that biofilms from fungal species hundreds of millions of years distant from C. albicans are similar in detail.”
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Blastoschizomyces capitatus can cause catheter-associated bloodstream infections.
“B. capitatus can cause catheter-associated bloodstream infections”
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The type of biofilm formed by C. albicans is probably unique to the CTG clade.
“The type of biofilm formed by C. albicans is probably unique to the CTG clade; given that the C. albicans biofilm circuit is a recent evolutionary innovation, it is likely that biofilms from more distantly related fungal species were also relatively recent innovations that independently evolved along those clades.”
Quote in the paperNot a substantial claim - Premisecitation
Cells in biofilms have been found to be more resistant to drugs compared with cells grown in suspension culture.
“For example, a number of these biofilm formers (Table 3) have been tested for drug susceptibility in vitro, and cells in biofilms have been found to be more resistant to drugs compared with cells grown in suspension culture.”
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- Premisecitation
Members from Acremonium, Aspergillus, Cladosporium, Fusarium, and Pneumocystis, in addition to Candida, are among the biofilm formers tested for drug susceptibility in vitro.
“These include (in addition to Candida) members from Acremonium, Aspergillus, Cladosporium, Fusarium, and Pneumocystis (9, 20, 35, 42, 79, 160, 176).”
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- Interpretationcitation
Scedosporium prolificans may form biofilms, given that fungus balls resembling biofilm structures have been observed in some clinical cases.
“Scedosporium prolificans, a recently emerging human fungal pathogen of the respiratory system, may also form biofilms, given that fungus balls, resembling biofilm structures, have been observed in some clinical cases (30).”
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- Premisecitation
Blastoschizomyces capitatus has the capacity to form a biofilm both in vitro and in vivo.
“and has the capacity to form a biofilm both in vitro and in vivo (16, 38).”
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A Candida albicans biofilm can act as a safe haven for anaerobic pathogens in oxygen-rich environments.
“Thus, a C. albicans biofilm can act as a safe haven for anaerobic pathogens in oxygen-rich environments.”
Quote in the paperSubstantial claim - Premisecitation
In a study of dual-species biofilms Candida albicans forms with gut microbiota members, biofilms formed by Candida albicans provided a hypoxic microenvironment that could support the growth of Bacteroides fragilis and Clostridium perfringens even though the biofilms were grown under oxygen-rich conditions.
“In this study, biofilms formed by C. albicans provided a hypoxic microenvironment that could support the growth of the two strictly anaerobic bacteria, B. fragilis and C. perfringens—even though the biofilms were grown under oxygen-rich conditions.”
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- Premisecitation
Several studies have investigated dual-species biofilms comprising Candida albicans and a bacterium commonly isolated from denture stomatitis, periodontitis, or dental caries, such as Streptococcus mutans, Streptococcus gordonii, Actinomyces viscosus, or Fusobacterium species.
“Several studies have investigated such dual-species biofilms comprising C. albicans and a bacterium commonly isolated from denture stomatitis, periodontitis, or dental caries, such as Streptococcus mutans, Streptococcus gordonii, Actinomyces viscosus, or Fusobacterium species (12, 81, 82).”
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The Candida species found with Candida albicans in polymicrobial biofilms include Candida dubliniensis, Candida tropicalis, Candida parapsilosis, Candida guillermondii, Candida krusei, and Candida glabrata.
“These species include C. dubliniensis, C. tropicalis, C. parapsilosis, C. guillermondii, C. krusei, and C. glabrata (80, 90, 118, 151).”
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Current antifungal drugs have only two specific targets: ergosterol biosynthesis and 1,3-β-D-glucan synthesis.
“Current antifungal drugs have only two specific targets (ergosterol biosynthesis and 1,3-β-D-glucan synthesis)”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
Pseudomonas aeruginosa secretes a 12-carbon acyl homoserine lactone that modulates hyphal growth by Candida albicans.
“For example, P. aeruginosa secretes a 12-carbon acyl homoserine lactone that modulates hyphal growth by C. albicans (78).”
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- Premisecitation
Screens of chemical libraries have identified compounds that disrupt formation and/or maintenance of biofilms.
“Screens of chemical libraries have identified compounds that disrupt formation and/or maintenance of biofilms (25, 101, 185, 210).”
Quote in the paperSubstantial claim0 of 4 sources checked - Premisecitation
A Fusarium keratitis outbreak occurred in the United States as a result of a contact lens multipurpose solution lacking sufficient antifungal efficacy against Fusarium solani.
“In fact, a Fusarium keratitis outbreak occurred in the United States as a result of a contact lens multipurpose solution lacking sufficient antifungal efficacy against F. solani (24, 105).”
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Other Candida species have been found together with Candida albicans in polymicrobial biofilms from patients.
“other Candida species have been found together with C. albicans in polymicrobial biofilms from patients (27).”
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- Interpretationreasoning
Biofilm formation by an evolutionarily broad range of fungal species has enormous impact on human health.
“Though biofilm formation has been most extensively studied for C. albicans, it is clear—even from this brief discussion—that biofilm formation by an evolutionarily broad range of fungal species has enormous impact on human health.”
Quote in the paperNot a substantial claim
- May combine two claims. 38
- Classified as probably not a substantial claim. 20
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FindingcitationDeletion of ZAP1 leads to an increase in the accumulation of extracellular matrix material, probably by upregulating the glucoamylases Gca1 and Gca2.
“Deletion of RLM1 causes a reduction in matrix levels (136), whereas deletion of ZAP1 leads to an increase in the accumulation of extracellular matrix material, probably by upregulating the glucoamylases Gca1 and Gca2 (144).”
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FindingcitationCells are dispersed continuously throughout C. albicans biofilm formation, and they are thought to be primarily (if not exclusively) in the round yeast form.
“Cells are dispersed continuously throughout biofilm formation, and they are thought to be primarily (if not exclusively) in the round yeast form (194).”
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FindingcitationIn addition to the 6 master transcriptional regulators, another 44 transcriptional regulators have been identified; if any is deleted, some aspect of C. albicans biofilm formation is affected under at least one condition.
“In addition to the 6 master transcriptional regulators discussed above, another 44 transcriptional regulators have been identified; if any of these is deleted, some aspect of C. albicans biofilm formation is affected under at least one condition (Table 1; revised from 61 and 18).”
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FindingcitationDispersed cells have increased adherence properties, the ability to form biofilms more efficiently, and enhanced virulence in mouse models of infection relative to planktonic cells.
“These include (relative to planktonic cells) increased adherence properties, the ability to form biofilms more efficiently, and enhanced virulence in mouse models of infection (194).”
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FindingcitationTwo transcriptional regulators of C. albicans biofilm dispersal have been identified, Nrg1 and Ume6; transcriptional overexpression of either regulator increased the number of dispersed cells actively released from the biofilm.
“Two transcriptional regulators of C. albicans biofilm dispersal have been identified, Nrg1 and Ume6; transcriptional overexpression of either regulator increased the number of dispersed cells actively released from the biofilm (194, 195).”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
FindingcitationThe master regulator Bcr1 is not needed for hyphal formation per se, but it is needed for the hyphae to adhere to one another in biofilms.
“Indeed, the master regulator Bcr1 is not needed for hyphal formation per se, but it is needed for the hyphae to adhere to one another in biofilms (141).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [141] source
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FindingcitationDeletion of YWP1 leads to decreased biofilm dispersal and increased biofilm adhesiveness.
“The cell wall protein Ywp1 is also important for biofilm dispersal, as deletion of YWP1 leads to decreased biofilm dispersal and increased biofilm adhesiveness (69, 70).”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
FindingcitationIn planktonic cells, efflux pumps are typically upregulated in response to antifungal drugs; in biofilms, they become upregulated within the first few hours of surface contact and remain upregulated throughout biofilm development, whether or not an antifungal drug is present.
“In planktonic cells, these efflux pumps are typically upregulated in response to antifungal drugs; in biofilms, however, they become upregulated within the first few hours of surface contact and remain upregulated throughout biofilm development, whether or not an antifungal drug is present (119, 126, 133, 140, 156, 205).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
FindingcitationExtracellular DNA is a component of the matrix in C. albicans and contributes, probably indirectly, to drug resistance.
“Finally, extracellular DNA is also a component of the matrix in C. albicans and contributes, probably indirectly, to drug resistance (117).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [117] source
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FindingcitationMutant strains of individual Set3 complex members formed extra strong biofilms that were incapable of normal biofilm dispersal and especially recalcitrant to mechanical perturbation.
“Indeed, mutant strains of individual Set3 complex members formed extra strong biofilms that were incapable of normal biofilm dispersal and especially recalcitrant to mechanical perturbation (139).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [139] source
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FindingcitationTreatment of biofilms with β-1,3-glucanase increases the susceptibility of biofilms to fluconazole, and addition of exogenous β-1,3-glucans increases the tolerance of planktonic cells to fluconazole.
“Thus, treatment of biofilms with β-1,3-glucanase increases the susceptibility of biofilms to fluconazole (130), and addition of exogenous β-1,3-glucans increases the tolerance of planktonic cells to fluconazole (122).”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
FindingcitationNrg1 and Set3 complex mutants are hyperfilamentous, consistent with their inability to generate yeast-form cells.
“Nrg1 and Set3 complex mutants are hyperfilamentous, consistent with their inability to generate yeast-form cells (77, 195).”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
Findingnone givenEach of these Candida species can form a biofilm in vitro, but the thickness, strength, and robustness in different environmental conditions decrease as species diverge phylogenetically away from C. albicans.
“Each of these species can form a biofilm in vitro, but the thickness, strength, and robustness in different environmental conditions decrease as species diverge phylogenetically away from C. albicans.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisereasoningIn individuals with healthy immune systems, C. albicans is often harmless, kept in balance with other members of the local microbiota.
“In individuals with healthy immune systems, C. albicans is often harmless, kept in balance with other members of the local microbiota.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based). May combine two claims.
Premisenone givenC. albicans biofilms are intrinsically resistant to conventional antifungal therapeutics, the host immune system, and other environmental perturbations.
“C. albicans biofilms are intrinsically resistant to conventional antifungal therapeutics, the host immune system, and other environmental perturbations, making biofilm-based infections a significant clinical challenge.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationCandida infections are especially serious in immunocompromised individuals and in healthy people with implanted medical devices.
“Candida infections are especially serious in immunocompromised individuals (such as those with AIDS or those undergoing anticancer or immunosuppression therapies) and healthy people with implanted medical devices (96, 201).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [96] Kullberg BJ, 2002, Eur. J. Med. Res.
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- cites [201] source
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PremisecitationC. albicans biofilms colonize implanted medical devices and mucosal surfaces, from which they can seed systemic infections in humans.
“In this review, we focus on C. albicans biofilms, which colonize implanted medical devices and mucosal surfaces, from which they can seed systemic infections in humans (46, 47, 64, 89, 97, 161, 172).”
Quote in the paperSubstantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S4 (based).
Premisenone givenBiofilms form on implanted medical devices, including catheters, pacemakers, dentures, and prosthetic joints, which provide a surface and sanctuary for biofilm growth.
“Biofilms are notorious for forming on implanted medical devices, including catheters, pacemakers, dentures, and prosthetic joints, which provide a surface and sanctuary for biofilm growth.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCandida infections range from superficial mucosal and dermal infections to hematogenously disseminated infection with mortality approaching 40% in some cases.
“These infections range from superficial mucosal and dermal infections, such as thrush, vaginal yeast infections, and diaper rash, to hematogenously disseminated infection with sizable mortality rates (approaching 40% in some cases) (21, 148, 202).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
Interpretationnone givenFor many microorganisms, the biofilm state is probably more relevant to their natural settings than to suspension cultures.
“It is now recognized that, for many microorganisms, the biofilm state is probably more relevant to their “natural” settings than to suspension cultures.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.
Interpretationnone givenIn the laboratory, C. albicans biofilms can develop on several substrates and in many types of media, indicating an inherent robustness of biofilm development to changes in external conditions.
“In the laboratory, C. albicans biofilms can develop on several substrates and in many types of media, indicating an inherent robustness of biofilm development to changes in external conditions.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationnone givenOnce it forms on an implanted medical device, a Candida biofilm has the potential to seed disseminated bloodstream infections and lead to invasive systemic infections of tissues and organs.
“Once it forms on an implanted medical device, a Candida biofilm has the potential to seed disseminated bloodstream infections and to lead to invasive systemic infections of tissues and organs.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationUrinary and central venous catheters, pacemakers, mechanical heart valves, joint prostheses, contact lenses, and dentures are all susceptible to C. albicans biofilms.
“Urinary and central venous catheters, pacemakers, mechanical heart valves, joint prostheses, contact lenses, and dentures are all susceptible to C. albicans biofilms (22, 45, 90, 175).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationSpecies within the CTG clade are the fourth most frequent cause of bloodstream infections in clinical settings and are the predominant fungal species isolated from medical device infections.
“Accounting for 15% of all hospital-acquired sepsis cases, species within the CTG clade (predominantly C. albicans, but including several closely related species as well) are the fourth most frequent cause of bloodstream infections in clinical settings and are the predominant fungal species isolated from medical device infections (43, 152, 202, 204).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
Premisenone givenC. albicans is distinguished from many other fungal species by its ability to form both yeast cells and hyphae under many different environmental conditions.
“C. albicans is distinguished from many other fungal species by its ability to form both yeast cells and hyphae under many different environmental conditions.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningBiofilm formation by C. albicans can occur over a broad range of conditions and the genetic requirements likely vary from one condition to the next.
“It is clear that biofilm formation by C. albicans can occur over a broad range of conditions and that the genetic requirements likely vary from one condition to the next.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningHyphae are an important structural component of C. albicans biofilms; genes required for hyphal growth in suspension cultures are also necessary for proper biofilm formation.
“Although they readily form in planktonic cultures, hyphae are an important structural component of C. albicans biofilms; thus, it is not surprising that genes required for hyphal growth in suspension cultures are also necessary for proper biofilm formation.”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
InterpretationreasoningOrthology mapping indicates that the entire set of target genes is significantly enriched for young genes, suggesting that the ability of C. albicans to form biofilms evolved relatively recently.
“Orthology mapping indicates that the entire set of target genes is significantly enriched for “young” genes, suggesting that the ability of C. albicans to form biofilms evolved relatively recently with respect to evolutionary timescales.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationPersister cells are a minor subset of metabolically dormant yeast cells that stochastically arise as phenotypical variants within biofilms and are extremely resistant to antifungal drugs.
“A minor subset of metabolically dormant yeast cells that stochastically arise as phenotypical variants within biofilms, persister cells are extremely resistant to antifungal drugs (100).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [100] source
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InterpretationcitationMost matrix proteins were predicted to be enzymes, including hydrolyzing enzymes, suggesting that the matrix may play an active role in breaking down biopolymers.
“Most of these were predicted to be enzymes, including hydrolyzing enzymes, suggesting that the matrix may play an active role in breaking down biopolymers.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [209] source
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InterpretationreasoningAlthough β-1,3-glucans contribute to drug resistance and are the major cell wall polysaccharide, they constitute only a small fraction of the total polysaccharides present, implying that the matrix is not constructed simply of released cell wall constituents.
“Thus, although β-1,3-glucans contribute to drug resistance and are the major cell wall polysaccharide (130), we now know that they constitute only a small fraction of the total polysaccharides present, implying that the matrix is not constructed simply of released cell wall constituents.”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
InterpretationcitationSecreted extracellular matrix contributes to biofilm drug resistance, both acting as a physical barrier to drug penetration and directly contributing to the overall structural integrity of the biofilm.
“Secreted extracellular matrix also contributes to biofilm drug resistance, both acting as a physical barrier to drug penetration and directly contributing to the overall structural integrity of the biofilm (2, 11, 130, 135).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
InterpretationreasoningThe resistance of C. albicans biofilms is due to the upregulation of efflux pumps, the presence of the extracellular matrix, and the presence of recalcitrant persister cells.
“This resistance is due to the upregulation of efflux pumps, the presence of the extracellular matrix, and the presence of recalcitrant persister cells.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationBlastoschizomyces capitatus is a rare cause of infection in humans, although more cases have been emerging in highly immunocompromised patients in intensive care units.
“Blastoschizomyces capitatus is another rare cause of infection in humans, although more cases have been emerging in highly immunocompromised patients in ICUs.”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationCoccidioides immitis, Paracoccidioides brasiliensis, and Blastomyces dermatitidis are all sources of mycoses in immunocompromised individuals and have also caused endemic outbreaks in specific geographical regions.
“Along with H. capsulatum, Coccidioides immitis, Paracoccidioides brasiliensis, and Blastomyces dermatitidis are all sources of mycoses in immunocompromised individuals and have also caused endemic outbreaks in specific geographical regions (62, 113).”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationcitationHistoplasma capsulatum may exist in biofilms in vivo.
“suggesting that H. capsulatum may exist in biofilms in vivo (154).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [154] source
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PremisecitationHistoplasma capsulatum has been reported to form biofilms consisting of dense clusters of yeast-form cells in vitro.
“There is at least one report of H. capsulatum forming biofilms consisting of dense clusters of yeast-form cells in vitro”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [154] source
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PremisecitationSaccharomyces cerevisiae is able to form a thin biofilm consisting of round, budding yeast-form cells and pseudohyphal cells in vitro.
“and it is able to form a thin biofilm consisting of round, budding yeast-form cells and pseudohyphal cells in vitro (26, 50, 128, 164).”
Quote in the paperNot a substantial claim0 of 4 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAspergillus fumigatus is a common invasive colonizer of the respiratory tract in individuals with cystic fibrosis or other conditions that compromise the immune system.
“Aspergillus fumigatus is a common invasive colonizer of the respiratory tract in individuals with cystic fibrosis or other conditions that compromise the immune system (176).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [176] source
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PremisecitationAspergillomas may form as Aspergillus fumigatus continues to proliferate in the respiratory tract, and these structures share many architectural characteristics with biofilms formed by other fungal species.
“Aspergillomas, or dense hyphal balls, may also form as A. fumigatus continues to proliferate in the respiratory tract; these structures share many architectural characteristics with biofilms formed by other fungal species (159).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [159] source
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Premisenone givenOutside the CTG clade, numerous fungal species have been reported to form biofilms in vitro and in vivo.
“Outside the CTG clade, numerous fungal species have been reported to form biofilms in vitro and in vivo.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationAspergillus is a fungal pathogen of great medical importance that can form biofilms both in vitro and in vivo.
“Aspergillus is a fungal pathogen of great medical importance that can form biofilms both in vitro and in vivo (125, 159).”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationHistoplasma capsulatum is an opportunistic pathogen that infects the respiratory system of mammals, causing histoplasmosis.
“Histoplasma capsulatum is another opportunistic pathogen that infects the respiratory system of mammals, causing histoplasmosis (85).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [85] source
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PremisecitationCandida dubliniensis, Candida parapsilosis, Candida tropicalis, and Candida krusei have all been implicated in biofilm-associated infections.
“The closely related species Candida dubliniensis, Candida parapsilosis, Candida tropicalis, and Candida krusei have all been implicated in biofilm-associated infections (73, 157, 187).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSaccharomyces cerevisiae has been implicated in catheter-associated infections with mixed-species biofilms in patients in intensive care units.
“In a few case studies, however, S. cerevisiae has been implicated in catheter-associated infections with mixed-species biofilms in patients in intensive care units (ICUs)”
Quote in the paperNot a substantial claim0 of 4 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCoccidioides immitis has been reported to form biofilms on medical devices.
“Although rare, C. immitis has been reported to form biofilms on medical devices (40).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [40] source
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InterpretationreasoningCandida albicans and bacteria can interact with each other by secretion of signaling molecules that influence the behavior of one species toward the other, by direct cell-cell physical contact, and by alterations of the local environment that influence the other species.
“From these studies, we have learned that C. albicans and bacteria can interact with each other by secretion of signaling molecules that influence the behavior of one species toward the other, by direct cell-cell physical contact, and by alterations of the local environment that influence the other species (e.g., alterations in pH and oxygen concentrations).”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationFusarium solani, Acremonium implicatum, and Cladosporium sphaerospermum can all form biofilms under laboratory conditions.
“Recent work in vitro has shown that F. solani, A. implicatum, and C. sphaerospermum can all form biofilms under laboratory conditions (211).”
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PremisecitationIt is widely believed that antifungal drugs with new mechanisms of action are needed.
“and it is widely believed that antifungal drugs with new mechanisms of action are needed (4, 18, 79).”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
PremisecitationCandida albicans interacts with several bacterial species found in the gut, such as Enterococcus and Escherichia species; those found in the vagina, such as Lactobacillus species; and those found in the lungs of patients with cystic fibrosis, such as Pseudomonas aeruginosa.
“C. albicans also interacts with several bacterial species found in the gut, such as Enterococcus and Escherichia species; those found in the vagina, such as Lactobacillus species; and those found in the lungs of patients with cystic fibrosis, such as Pseudomonas aeruginosa (13, 34, 54, 78).”
Quote in the paperNot a substantial claim0 of 4 sources checkedMay combine two claims.
PremisecitationWhen cultured together with Candida albicans in ambient oxygen, Bacteroides fragilis and Clostridium perfringens could induce Candida albicans to form mini-biofilms, which could protect the bacteria and allow them to proliferate under otherwise toxic conditions.
“Moreover, when cultured together with C. albicans in ambient oxygen, these anaerobes could induce the latter to form mini-biofilms, which, in turn, could protect the bacteria and allow them to proliferate under otherwise toxic conditions.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [60] source
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The paper relies on this without support.
Virtually nothing is known about the interactions among Candida species in polymicrobial biofilms.
“We know virtually nothing about the interactions among these Candida species in polymicrobial biofilms.”
The paper relies on this without support.
No biofilm-specific drugs exist today for Candida albicans or any microbe.
“No biofilm-specific drugs exist today for C. albicans (or any microbe), making treatment of biofilm-based infections particularly problematic.”
The paper relies on this without support.
Candida albicans is the fungal pathogen most frequently isolated from human infections.
“Although C. albicans is the fungal pathogen most frequently isolated from human infections”
The paper relies on this without support.
Microbial infections are often thought of, and treated, as if a single microbial species were acting alone.
“Microbial infections are often thought of, and treated, as if a single microbial species were acting alone.”
The paper relies on this without support.
Keratitis is generally thought of as a biofilm infection and has been associated with the use of contact lenses.
“Keratitis is generally thought of as a biofilm infection and has been associated with the use of contact lenses.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
C. albicans biofilms exhibit high tolerance to antifungal drugs, posing a substantial challenge in clinical treatment.
“Once established, these biofilms exhibit a high tolerance to antifungal drugs, posing a substantial challenge in clinical treatment [54,55,56,57].”
From Disruption of the UPC2 Gene Enhances Fluconazole Antifungal Activity by Inhibiting HAC1 mRNA Splicing in Candida albicans (2026) · cites this paper as [56]
A well-documented virulence factor of Candida species is the notable ability to form adherent structures, known as biofilms, on surfaces of medical devices.
“A well-documented virulence factor of Candida species is the notable ability to form adherent structures, known as biofilms, on surfaces of medical devices [49–51].”
From Aprepitant, an antiemetic agent, interferes with metal ion homeostasis of<i>Candida auris</i>and displays potent synergistic interactions with azole drugs (2020) · cites this paper as [50]
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- Authors
- Nobile, C. J., & Johnson, A. D.
- Affiliations
- University of California, Merced (US)
- University of California, San Francisco (US)
- Venue
- Annual Review of Microbiology
- Publisher
- Annual Reviews
- Published
- 2015-10-15
- Volume
- 69
- Issue
- 1
- Pages
- 71-92
- ISSN
- 0066-4227 (ISSN-L)
- 1545-3251
- PMC
- PMC4930275
- OpenAlex
- W2170764510
- Semantic Scholar
- 5e945268f6f8fd4d66044feb13a7f07654261596
- Cited by
- 1,057
- References
- 215
- Citations by year
- 2026: 77 · 2025: 106 · 2024: 130 · 2023: 88 · 2022: 138 · 2021: 135 · 2020: 117 · 2019: 91 · 2018: 76 · 2017: 68 · 2016: 28 · 2015: 2
- FWCI
- 8.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annual Review of Microbiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R00AI100896, R01AI083311, T32AI060537)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- Candida albicans, biofilm, candidiasis, fungal infection, human microbiota, antifungal resistance, host immune response, biomedical implants, biofilm-associated infections, mucosal candidiasis, systemic candidiasis, fungal communities
- MeSH terms
- Animals, Candida albicans, Candidiasis, Cell Adhesion, Fungi, Humans, Mycoses, Biofilms
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