Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition
Abstract
Most cases of candidiasis have been attributed to C. albicans, but recently, non- Candida albicans Candida (NCAC) species have been identified as common pathogens. The ability of Candida species to form biofilms has important clinical repercussions due to their increased resistance to antifungal therapy and the ability of yeast cells within the biofilms to withstand host immune defenses. Given this clinical importance of the biofilm growth form, the aim of this study was to characterize biofilms produced by three NCAC species, namely C. parapsilosis, C. tropicalis and C. glabrata. The biofilm forming ability of clinical isolates of C. parapsilosis, C. tropicalis and C. glabrata recovered from different sources, was evaluated by crystal violet staining. The structure and morphological characteristics of the biofilms were also assessed by scanning electron microscopy and the biofilm matrix composition analyzed for protein and carbohydrate content. All NCAC species were able to form biofilms although these were less extensive for C. glabrata compared with C. parapsilosis and C. tropicalis. It was evident that C. parapsilosis biofilm production was highly strain dependent, a feature not evident with C. glabrata and C. tropicalis. Scanning electron microscopy revealed structural differences for biofilms with respect to cell morphology and spatial arrangement. Candida parapsilosis biofilm matrices had large amounts of carbohydrate with less protein. Conversely, matrices extracted from C. tropicalis biofilms had low amounts of carbohydrate and protein. Interestingly, C. glabrata biofilm matrix was high in both protein and carbohydrate content. The present work demonstrates that biofilm forming ability, structure and matrix composition are highly species dependent with additional strain variability occurring with C. parapsilosis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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. glabrata colonizes host tissues as well as abiotic surfaces as biofilms.
“Moreover, C. glabrata colonizes host tissues as well as abiotic surfaces as biofilms (Silva et al., 2009).”
From Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate (2015) · cites this paper as Silva et al., 2009
C. glabrata biofilms display antifungal resistance and are characterized by a compact dense structure of yeast cells nested in an extracellular matrix composed of high levels of proteins and carbohydrates including β-1,3 glucan.
“C. glabrata biofilms display antifungal resistance, and are characterized by a compact dense structure of yeast cells nested in an extracellular matrix which is composed of high levels of proteins and carbohydrates including β-1,3 glucan [50,51,52].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [51]
Biofilm formation ability is a virulence factor of Candida glabrata.
“particularly biofilm formation ability”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [40]
Candida glabrata biofilm matrix contains proteins, carbohydrates (e.g., β-1,3 glucans), and ergosterol.
“with proteins, carbohydrates (e.g., β-1,3 glucans), and ergosterol in their matrixes [40,41,44].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [40]
Candida glabrata clinical isolates have the ability to form a compact biofilm structure in different multilayers.
“Candida glabrata clinical isolates have the ability to form a compact biofilm structure in different multilayers [40,41]”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [40]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Colorimetric Method for Determination of Sugars and Related Substances
DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956) · Analytical Chemistry · doi:10.1021/ac60111a017 · Cited by 52,269 · see citing works
Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms
Donlan, R. M., & Costerton, J. W. (2002) · Clinical Microbiology Reviews · doi:10.1128/cmr.15.2.167-193.2002 · Cited by 6,644 · see citing works
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995) · Annual Review of Microbiology · doi:10.1146/annurev.mi.49.100195.003431 · Cited by 4,718 · see citing works
Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., McCormick, T., & Ghannoum, M. A. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.18.5385-5394.2001 · Cited by 1,578 · see citing works
<i>Candida</i> Infections of Medical Devices
Kojic, E. M., & Darouiche, R. O. (2004) · Clinical Microbiology Reviews · doi:10.1128/cmr.17.2.255-267.2004 · Cited by 1,055 · see citing works
Epidemiology of nosocomial fungal infections
Fridkin, S. K., & Jarvis, W. R. (1996) · Clinical Microbiology Reviews · doi:10.1128/cmr.9.4.499 · Cited by 782 · see citing works
Hajjeh, R. A., Sofair, A. N., Harrison, L. H., Lyon, G. M., Arthington-Skaggs, B. A., Mirza, S. A., Phelan, M., Morgan, J., Lee-Yang, W., Ciblak, M. A., et al. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.4.1519-1527.2004 · Cited by 649 · see citing works
Biofilm formation by Candida species on the surface of catheter materials in vitro
Hawser, S. P., & Douglas, L. J. (1994) · Infection and Immunity · doi:10.1128/iai.62.3.915-921.1994 · Cited by 599 · see citing works
<i>Candida</i> biofilms on implanted biomaterials: a clinically significant problem
Ramage, G., MartÃnez, J. P., & López-Ribot, J. L. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00117.x · Cited by 575 · see citing works
Al-Fattani, M. A., & Douglas, L. J. (2006) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46569-0 · Cited by 548 · see citing works
Heterogeneity in biofilms: Table 1
WIMPENNY, J. W. T., Manz, W., & Szewzyk, U. (2000) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2000.tb00565.x · Cited by 530 · see citing works
Comparison of Biofilms Formed byCandidaalbicansandCandidaparapsilosison Bioprosthetic Surfaces
Kuhn, D. M., Chandra, J., Mukherjee, P. K., & Ghannoum, M. A. (2002) · Infection and Immunity · doi:10.1128/iai.70.2.878-888.2002 · Cited by 485 · see citing works
Resistance of Candida albicans biofilms to antifungal agents in vitro
Hawser, S., & Douglas, L. (1995) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.39.9.2128 · Cited by 407 · see citing works
Baillie, G. S. (2000) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/46.3.397 · Cited by 389 · see citing works
Application of DNA typing methods to epidemiology and taxonomy of Candida species
Scherer, S. W., & Stevens, D. A. (1987) · Journal of Clinical Microbiology · doi:10.1128/jcm.25.4.675-679.1987 · Cited by 380 · see citing works
Shin, J. H., Kee, S., Shin, M., Kim, S. H., Shin, D. H., Lee, S. K., Suh, S., & Ryang, D. W. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.4.1244-1248.2002 · Cited by 335 · see citing works
Epidemiological trends in nosocomial candidemia in intensive care
Bassetti, M., Righi, E., Costa, A., Fasce, R., Molinari, M. P., Rosso, R., Pallavicini, F. B., & Viscoli, C. (2006) · BMC Infectious Diseases · doi:10.1186/1471-2334-6-21 · Cited by 332 · see citing works
Role of dimorphism in the development of Candida albicans biofilms
BAILLIE, G. S., & DOUGLAS, L. J. (1999) · Journal of Medical Microbiology · doi:10.1099/00222615-48-7-671 · Cited by 304 · see citing works
Jin, Y., Yip, H. K., Samaranayake, Y. H., Yau, J. Y. Y., & Samaranayake, L. P. (2003) · Journal of Clinical Microbiology · doi:10.1128/jcm.41.7.2961-2967.2003 · Cited by 254 · see citing works
Ramage, G., VandeWalle, K., Bachmann, S. P., Wickes, B. L., & Lopez-Ribot, J. L. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.11.3634-3636.2002 · Cited by 238 · see citing works
Penetration of <i>Candida</i> Biofilms by Antifungal Agents
Al-Fattani, M. A., & Douglas, L. J. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.9.3291-3297.2004 · Cited by 235 · see citing works
MUKHERJEE, P., & Chandra, J. (2004) · Drug Resistance Updates · doi:10.1016/j.drup.2004.09.002 · Cited by 222 · see citing works
Kumamoto, C. A. (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00371-5 · Cited by 217 · see citing works
Characteristics of biofilm formation by Candida tropicalis and antifungal resistance
Bizerra, F. C., Nakamura, C. V., Poersch, C. D. O., Svidzinski, T. I. E., Quesada, R. M. B., Goldenberg, S., Krieger, M. A., & Yamada‐Ogatta, S. F. (2008) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2007.00347.x · Cited by 170 · see citing works
High frequency of Candida parapsilosis on the hands of healthy hosts
Bonassoli, L. A., Bertoli, M., & Svidzinski, T. I. E. (2004) · Journal of Hospital Infection · doi:10.1016/j.jhin.2004.06.033 · Cited by 149 · see citing works
Nucci, M., & Colombo, A. L. (2007) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2006.11.009 · Cited by 139 · see citing works
Thein, Z. M., Samaranayake, Y. H., & Samaranayake, L. P. (2007) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2007.01.009 · Cited by 133 · see citing works
Biofilm Formation by and Antifungal Susceptibility of Candida Isolates from Urine
Jain, N., Kohli, R., Cook, E., Gialanella, P., Chang, T., & Fries, B. C. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02439-06 · Cited by 129 · see citing works
The Prevalence of Yeasts in Clinical Specimens from Cancer Patients
Kiehn, T. E., Edwards, F. F., & Armstrong, D. (1980) · American Journal of Clinical Pathology · doi:10.1093/ajcp/73.4.518 · Cited by 118 · see citing works
Fungal infections associated with HIV infection
Samaranayake, L. P., Fidel, P., Naglik, Sweet, S., Teanpaisan, R., Coogan, M. M., Blignaut, E., & Wanzala, P. (2002) · Oral Diseases · doi:10.1034/j.1601-0825.8.s2.6.x · Cited by 107 · see citing works
Weinberger, M., Leibovici, L., Perez, S., Samra, Z., Ostfeld, I., Levi, I., Bash, E., Turner, D., Goldschmied‐Reouven, A., Regev‐Yochay, G., et al. (2005) · Journal of Hospital Infection · doi:10.1016/j.jhin.2005.02.009 · Cited by 95 · see citing works
In Vitro Method To Study Antifungal Perfusion in Candida Biofilms
Samaranayake, Y. H., Ye, J., Yau, J. Y. Y., Cheung, B. P. K., & Samaranayake, L. P. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.2.818-825.2005 · Cited by 83 · see citing works
Interspecies variation in Candida biofilm formation studied using the Calgary biofilm device
Parahitiyawa, N., Samaranayake, Y. H., Samaranayake, L. P., Ye, J., Tsang, P. W., Cheung, B. P. K., Yau, J. Y. Y., & Yeung, S. K. W. (2006) · Apmis · doi:10.1111/j.1600-0463.2006.apm_394.x · Cited by 77 · see citing works
Tsai, H., & Bobek, L. A. (1997) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.41.10.2224 · Cited by 72 · see citing works
Fungal Infections in Solid Organ Transplant Patients
Hagerty, J. A., Ortiz, J., Reich, D. J., & Manzarbeitia, C. (2003) · Surgical Infections · doi:10.1089/109629603322419607 · Cited by 68 · see citing works
Fanello, S., Bouchara, J., Jousset, N., Delbos, V., & Leflohic, A.-M. (2001) · Journal of Hospital Infection · doi:10.1053/jhin.2000.0849 · Cited by 64 · see citing works
Extraction of exopolymers from biofilms: the protective effect of glutaraldehyde
Azeredo, J., Henriques, M., Sillankorva, S., & de Oliveira, R. P. S. (2003) · Water Science & Technology · doi:10.2166/wst.2003.0312 · Cited by 45 · see citing works
Self-citationBiofilm production by clinical isolates ofCandidaspecies
Kumar, C. P. G., & Menon, T. (2006) · Medical Mycology · doi:10.1080/13693780500338084 · Cited by 44 · see citing works
Rho, J., Shin, J. H., Song, J. W., Park, M., Kee, S. J., Jang, S. J., Park, Y. K., Suh, S., & Ryang, D. W. (2004) · PubMed · Cited by 34 · see citing works
Torulopsis glabrata an emerging yeast pathogen in cancer patients
Krcmery, V. (1999) · International Journal of Antimicrobial Agents · doi:10.1016/s0924-8579(98)00066-1 · Cited by 16 · see citing works
Flagged first, then by citations
Research works printed but not linked: 9
- Kumamoto CA. 7 Candida biofi lms. Curr Opin Microbiol 2002; 5: 608-611 .
- Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, 16 Lappin-Scott HM. Microbial biofi lms. Annu Rev Microbial 1995; 49: 711-745 .
- Mukherjee PK, Chandra J. 19 Candida biofi lm resistance. Drug Resist Update 2004; 7: 301-309 .
- Jin Y, Yip KH, Samaranayake YH, Yau JY, Samaranayake LP. 23 Biofi lm-forming ability of Candida albicans is unlikely to con- tribute to high levels of oral yeast carriage in cases of human immunodefi ciency virus infection. J Clin Microbiol 2003; 41: 2961-2967 .
- Ramage G, Martinez JP, Lopez-Ribot JL. 24 Candida biofi lms on im- planted biomaterials: a clinically signifi cant problem. FEMS Yeast Res 2006; 6: 979-986 .
- Kuhn DM, Chandra J, Mukherjee PK, Ghannoum MA. Comparison 35 of biofi lms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun 2002; 70: 878-888 .
- Wimpenny J, Manz W, Szewzyk U. Heterogeneity in biofi lms. 38 FEMS Microbiol Rev 2000; 24: 661-671 .
- Al-Fattani MA, Douglas LJ. Penetration of 39 Candida biofi lms by anti- fungal agents. Antimicrob Agents Chemother. 2004; 48: 3291-3297 .
- Kumar CPG, Menon T. Biofi lm production by clinical isolates of 41 Candida species. Med Mycol 2006; 44: 99-101 .
Cited by
Sorted by citations
Sardi, J. C. O., Scorzoni, L., Bernardi, T., Fusco-Almeida, A. M., & Mendes Giannini, M. J. S. (2013) · Journal of Medical Microbiology · doi:10.1099/jmm.0.045054-0 · Cited by 1,184 · see citing works
Silva, S., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2012) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2011.00278.x · Cited by 969 · see citing works
Self-citationEssential Oils and Antifungal Activity
Nazzaro, F., Fratianni, F., Coppola, R., & Feo, V. D. (2017) · Pharmaceuticals · doi:10.3390/ph10040086 · Cited by 854 · see citing works
Emerging opportunistic yeast infections
Miceli, M. H., Díaz, J. A., & Lee, S. A. (2011) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(10)70218-8 · Cited by 811 · see citing works
Candida Biofilms: Threats, Challenges, and Promising Strategies
Cavalheiro, M., & Teixeira, M. C. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00028 · Cited by 690 · see citing works
Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors
Gonçalves, B., Ferreira, C., Alves, C. T., Henriques, M., Azeredo, J., & Silva, S. (2016) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2015.1091805 · Cited by 669 · see citing works
Self-citationMechanisms of Antifungal Drug Resistance
Cowen, L. E., Sanglard, D., Howard, S. J., Rogers, P. D., & Perlin, D. S. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019752 · Cited by 647 · see citing works
Ramage, G., Rajendran, R., Sherry, L., & Williams, C. (2012) · International Journal of Microbiology · doi:10.1155/2012/528521 · Cited by 583 · see citing works
Mechanisms of <i>Candida</i> Biofilm Drug Resistance
Taff, H. T., Mitchell, K. F., Edward, J. A., & Andes, D. R. (2013) · Future Microbiology · doi:10.2217/fmb.13.101 · Cited by 422 · see citing works
Candida parapsilosis: from genes to the bedside
Tóth, R., Nosek, J., Mora-Montes, H. M., Gabaldon, T., Bliss, J. M., Nosanchuk, J. D., Turner, S. A., Butler, G., Vágvölgyi, C., & Gácser, A. (2019) · Clinical Microbiology Reviews · doi:10.1128/cmr.00111-18 · Cited by 327 · see citing works
Adherence and biofilm formation of non-Candida albicans Candida species
Silva, S., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.02.003 · Cited by 304 · see citing works
Self-citationCandida Species Biofilms’ Antifungal Resistance
Silva, S. M., Rodrigues, C. F., Araújo, D., Rodrigues, M. E., & Henriques, M. (2017) · Journal of Fungi · doi:10.3390/jof3010008 · Cited by 308 · see citing works
Self-citationCandida glabrata: A review of its features and resistance
Rodrigues, C. F., Silva, S., & Henriques, M. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2009-3 · Cited by 268 · see citing works
Self-citationFungal Biofilms, Drug Resistance, and Recurrent Infection
Desai, J. V., Mitchell, A. P., & Andes, D. R. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019729 · Cited by 252 · see citing works
Fungal Biofilms and Polymicrobial Diseases
Costa-Orlandi, C. B., Sardi, J. D. C. O., Pitangui, N. D. S., de Oliveira, H. C., Scorzoni, L., Galeane, M. C., Medina‐Alarcón, K. P., Melo, W., Marcelino, M., Braz, J. D., et al. (2017) · Journal of Fungi · doi:10.3390/jof3020022 · Cited by 237 · see citing works
Kean, R., Delaney, C., Sherry, L., Borman, A., Johnson, E. M., Richardson, M. D., Rautemaa-Richardson, R., Williams, C., & Ramage, G. (2018) · mSphere · doi:10.1128/msphere.00334-18 · Cited by 220 · see citing works
The vaginal mycobiome: A contemporary perspective on fungi in women's health and diseases
Bradford, L. L., & Ravel, J. (2016) · Virulence · doi:10.1080/21505594.2016.1237332 · Cited by 188 · see citing works
Update on Antifungal Drug Resistance
Perlin, D. S., Shor, E., & Zhao, Y. (2015) · Current Clinical Microbiology Reports · doi:10.1007/s40588-015-0015-1 · Cited by 174 · see citing works
Biofilm formation in medically important Candida species
Malinovská, Z., Čonková, E., & Váczi, P. (2023) · Journal of Fungi · doi:10.3390/jof9100955 · Cited by 167 · see citing works
Candida Biofilms: Development, Architecture, and Resistance
Chandra, J., & Mukherjee, P. K. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mb-0020-2015 · Cited by 169 · see citing works
Candidaemia in adult cancer patients: risks for fluconazole-resistant isolates and death
Slavin, M. A., Sorrell, T. C., Marriott, D., Thursky, K., Nguyen, Q. A., Ellis, D. H., Morrissey, C. O., Chen, S. C.-A., & on behalf of the Australian Candidemia Study, A. S. F. I. D. (2010) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkq053 · Cited by 163 · see citing works
Marcos-Zambrano, L. J., Escribano, P., Bouza, E., & Guinea, J. (2014) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2014.08.012 · Cited by 161 · see citing works
Contributions of the Biofilm Matrix to Candida Pathogenesis
Nett, J. E., & Andes, D. R. (2020) · Journal of Fungi · doi:10.3390/jof6010021 · Cited by 158 · see citing works
Zago, C. E., Silva, S. M., Sanitá, P. V., Barbugli, P. A., Dias, C. M. I., Lordello, V. B., & Vergani, C. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123206 · Cited by 156 · see citing works
Self-citationCurrent perspective on emergence, diagnosis and drug resistance in Candida auris
Sarma, S., & Upadhyay, S. (2017) · Infection and Drug Resistance · doi:10.2147/idr.s116229 · Cited by 147 · see citing works
The Interface between Fungal Biofilms and Innate Immunity
Kernien, J. F., Snarr, B. D., Sheppard, D. C., & Nett, J. E. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01968 · Cited by 151 · see citing works
Portrait of Candida Species Biofilm Regulatory Network Genes
Araújo, D., Henriques, M., & Silva, S. M. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.09.004 · Cited by 135 · see citing works
Self-citationInsights into Candida tropicalis nosocomial infections and virulence factors
Negri, M., Silva, S., Henriques, M., & Oliveira, R. (2012) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-011-1455-z · Cited by 132 · see citing works
Recent trends in molecular diagnostics of yeast infections: from PCR to NGS
Arastehfar, A. A., Boekhout, T., Butler, G., Cesare, G. B. D., Dolk, E., Gabaldón, T., Hafez, A. I., Hube, B., Hagen, F., Hovhannisyan, H., et al. (2019) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuz015 · Cited by 136 · see citing works
Holland, L., Schröder, M., Turner, S. A., Taff, H. T., Andes, D. R., Grózer, Z., Gácser, A., Ames, L., Haynes, K., Higgins, D. G., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004365 · Cited by 132 · see citing works
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
Self-citationCandida glabrata: A Lot More Than Meets the Eye
Kumar, K., Askari, F., Sahu, M. S., & Kaur, R. (2019) · Microorganisms · doi:10.3390/microorganisms7020039 · Cited by 128 · see citing works
Branco, J., Miranda, I. M., & Rodrigues, A. G. (2023) · Journal of Fungi · doi:10.3390/jof9010080 · Cited by 133 · see citing works
Alfouzan, A. F., Almejrad, L., & Albarrag, A. (2017) · The Journal of Advanced Prosthodontics · doi:10.4047/jap.2017.9.5.402 · Cited by 123 · see citing works
Muadcheingka, T., & Tantivitayakul, P. (2015) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2015.03.002 · Cited by 120 · see citing works
Ouyang, K., Mortimer, M., Holden, P. A., Cai, P., Wu, Y., Gao, C., & Huang, Q. (2020) · Environment International · doi:10.1016/j.envint.2020.105485 · Cited by 113 · see citing works
Gamaletsou, M. N., Walsh, T. J., Zaoutis, T., Pagoni, M., Kotsopoulou, M., Voulgarelis, M., Panayiotidis, P., Vassilakopoulos, T., Angelopoulou, M. K., Marangos, M., et al. (2014) · Clinical Microbiology and Infection · doi:10.1111/1469-0691.12312 · Cited by 112 · see citing works
Biofilm formation by five species of Candida on three clinical materials
Estivill, D., Arias, Á., Lana, Á. T., Carrillo‐Muñoz, A. J., & Arévalo, M. P. (2011) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2011.05.019 · Cited by 112 · see citing works
Sublethal Concentrations of Silver Nanoparticles Stimulate Biofilm Development
Yang, Y., & Alvarez, P. J. J. (2015) · Environmental Science & Technology Letters · doi:10.1021/acs.estlett.5b00159 · Cited by 112 · see citing works
Şahal, G., Woerdenbag, H. J., Hinrichs, W. L. J., Visser, A., Tepper, P. G., Quax, W. J., van der Mei, H. C., & Bilkay, I. S. (2019) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2019.112188 · Cited by 112 · see citing works
Ramage, G., Milligan, S. G., Lappin, D. F., Sherry, L., Sweeney, P. M., Williams, C., Bagg, J., & Culshaw, S. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00220 · Cited by 106 · 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
Negri, M., Martins, M. I. B. C., Henriques, M., Svidzinski, T. I. E., Azeredo, J., & Oliveira, R. (2009) · Mycopathologia · doi:10.1007/s11046-009-9246-0 · Cited by 103 · see citing works
Self-citationAlves, C. T., Ferreira, I. C., Barros, L., Silva, S., Azeredo, J., & Henriques, M. (2014) · Future Microbiology · doi:10.2217/fmb.13.147 · Cited by 102 · see citing works
Self-citationSilva, 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
Self-citationLopes, S. P., Ceri, H., Azevedo, N. F., & Pereira, M. O. (2012) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2012.04.020 · Cited by 100 · see citing works
Is the oral fungal pathogen Candida albicans a cariogen?
Pereira, D., Seneviratne, C. J., Koga‐Ito, C. Y., & Samaranayake, L. P. (2017) · Oral Diseases · doi:10.1111/odi.12691 · Cited by 103 · see citing works
Biofilm formation by zygomycetes: quantification, structure and matrix composition
Singh, R., Rudramurthy, S. M., & Chakrabarti, A. (2011) · Microbiology · doi:10.1099/mic.0.048504-0 · Cited by 98 · see citing works
Czechowicz, P., Nowicka, J., & Gościniak, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23115895 · Cited by 114 · see citing works
Conserved and Divergent Roles of Bcr1 and CFEM Proteins in Candida parapsilosis and Candida albicans
Ding, C., Vidanes, G. M., Maguire, S. L., Guida, A., Synnott, J. M., Andes, D. R., & Butler, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028151 · Cited by 93 · see citing works
CandidaBiofilms and the Host: Models and New Concepts for Eradication
Tournu, H., & Dijck, P. V. (2011) · International Journal of Microbiology · doi:10.1155/2012/845352 · Cited by 91 · see citing works
Effect of Jujube Honey on Candida albicans Growth and Biofilm Formation
Ansari, M. J., Al-Ghamdi, A., Usmani, S., Al-Waili, N., Sharma, D., Adgaba, N., & Alattal, Y. (2013) · Archives of Medical Research · doi:10.1016/j.arcmed.2013.06.003 · Cited by 88 · see citing works
Pathak, A., Sharma, S., & Shrivastva, P. (2012) · Journal of Applied Oral Science · doi:10.1590/s1678-77572012000100013 · Cited by 87 · see citing works
The Extracellular Matrix of Fungal Biofilms
Mitchell, K. F., Żarnowski, R., & Andes, D. R. (2016) · Advances in experimental medicine and biology · doi:10.1007/5584_2016_6 · Cited by 88 · see citing works
Pannanusorn, S., Fernandez, V., & Römling, U. (2012) · Mycoses · doi:10.1111/myc.12014 · Cited by 88 · see citing works
Alnuaimi, A. D., O’brien-simpson, N. M., Reynolds, E. C., & McCullough, M. J. (2013) · FEMS Yeast Research · doi:10.1111/1567-1364.12068 · Cited by 86 · see citing works
The effect of biomaterials and antifungals on biofilm formation by Candida species: a review
Cuéllar‐Cruz, M., Vega‐González, A., Mendoza‐Novelo, B., López-Romero, E., Ruiz‐Baca, E., Escorza, M. A. Q., & Villagómez-Castro, J. C. (2012) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-012-1634-6 · Cited by 82 · see citing works
Zhang, F., Yao, T., Ren, Y., Yao, K., He, Q., Wan, Y., & Chi, Y. (2018) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2018.04.002 · Cited by 81 · see citing works
Comparative analysis of Candida biofilm quantitation assays
Taff, H. T., Nett, J. E., & Andes, D. R. (2011) · Medical Mycology · doi:10.3109/13693786.2011.580016 · Cited by 81 · see citing works
Silicone colonization by non-Candida albicans Candida species in the presence of urine
Silva, S. M., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2010) · Journal of Medical Microbiology · doi:10.1099/jmm.0.017517-0 · Cited by 79 · see citing works
Self-citation<i>Candida</i> 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
Biofilm Specific Activity: A Measure to Quantify Microbial Biofilm
Corte, L., Pierantoni, D. C., Tascini, C., Roscini, L., & Cardinali, G. (2019) · Microorganisms · doi:10.3390/microorganisms7030073 · Cited by 80 · see citing works
Participation of Candida albicans Transcription Factor RLM1 in Cell Wall Biogenesis and Virulence
Delgado-Silva, Y., Vaz, C., Carvalho-Pereira, J., Carneiro, C., Nogueira, E., Correia, A., Carreto, L. C., Silva, S. M., Faustino, A., Pais, C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086270 · Cited by 78 · see citing works
Self-citationDominguez, E., Zarnowski, R., Sanchez, H., Covelli, A. S., Westler, W. M., Azadi, P., Nett, J., Mitchell, A. P., & Andes, D. R. (2018) · mBio · doi:10.1128/mbio.00451-18 · Cited by 77 · see citing works
Exopolysaccharide analysis of biofilm‐forming <i>Candida albicans</i>
Lal, P., Sharma, D., Pruthi, P., & Pruthi, V. (2010) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2009.04634.x · Cited by 76 · see citing works
Ismaila, A. A., Ahmad, K., Siddique, Y., Wahab, M. A. A., Kutawa, A. B., Adamu, A., Zobir, S. A. M., Abdu, A., & Abdullah, S. N. A. (2022) · Horticultural Plant Journal · doi:10.1016/j.hpj.2022.02.004 · Cited by 82 · see citing works
Neji, S., Hadrich, I., Trabelsi, H., Abbes, S., Cheikhrouhou, F., Sellami, H., Makni, F., & Ayadi, A. (2017) · Journal of Biomedical Science · doi:10.1186/s12929-017-0376-2 · Cited by 74 · see citing works
Biology and genetics of the pathogenic yeast Candida parapsilosis
Nosek, J., Holesova, Z., Kosa, P. F., Gácser, A., & Tomáška, Ľ. (2009) · Current Genetics · doi:10.1007/s00294-009-0268-4 · Cited by 70 · see citing works
Photodynamic inactivation of a multispecies biofilm using curcumin and LED light
Quishida, C. C. C., Mima, E. G. D. O., Jorge, J. H., Vergani, C. E., Bagnato, V. S., & Pavarina, A. C. (2016) · Lasers in Medical Science · doi:10.1007/s10103-016-1942-7 · Cited by 70 · see citing works
Junqueira, J. C., Jorge, A. O. C., Barbosa, J. O., Rossoni, R. D., Vilela, S. F. G., Costa, A. C. B. P., Primo, F. L., Gonçalves, J. M., Tedesco, A. C., & Suleiman, J. M. A. H. (2012) · Lasers in Medical Science · doi:10.1007/s10103-012-1050-2 · Cited by 69 · see citing works
Novel strategies to fightCandidaspecies infection
Rodrigues, M. E., Silva, S. M., Azeredo, J., & Henriques, M. (2014) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2014.974500 · Cited by 68 · see citing works
Self-citationNatural Compounds: A Hopeful Promise as an Antibiofilm Agent Against Candida Species
Shariati, A., Didehdar, M., Razavi, S., Heidary, M., Soroush, F., & Chegini, Z. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.917787 · Cited by 72 · see citing works
Monteiro, D. R., Silva, S. M., Negri, M., Gorup, L. F., Camargo, E. R., Oliveira, R., Barbosa, D. B., & Henriques, M. (2012) · Journal of Applied Microbiology · doi:10.1111/jam.12102 · Cited by 66 · see citing works
Self-citationSimitsopoulou, M., Pešková, P., Tasina, E., Katragkou, A., Kyrpitzi, D., Velegraki, A., Walsh, T. J., & Roilides, E. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02541-12 · Cited by 66 · see citing works
Fungal Biofilms: Update on Resistance
Borghi, E., Borgo, F., & Morace, G. (2016) · Advances in experimental medicine and biology · doi:10.1007/5584_2016_7 · Cited by 67 · see citing works
Resistance of Candida albicans Biofilms to Drugs and the Host Immune System
Sandai, D. A., Tabana, Y., Ouweini, A. E., & Ishola, O. A. (2016) · Jundishapur Journal of Microbiology · doi:10.5812/jjm.37385 · Cited by 67 · see citing works
Assessment and Optimizations of Candida albicans In Vitro Biofilm Assays
Lohse, M. B., Gulati, M., Arevalo, A. V., Fishburn, A. T., Johnson, A. D., & Nobile, C. J. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02749-16 · Cited by 65 · see citing works
Understanding the mechanisms of resistance to azole antifungals in Candida species
Li, Y., Hind, C. K., Furner-Pardoe, J., Sutton, J. M., & Rahman, K. M. (2025) · JAC-Antimicrobial Resistance · doi:10.1093/jacamr/dlaf106 · Cited by 66 · see citing works
Luiz, R. L. F., Vila, T. V. M., de Mello, J. C. P., Nakamura, C. V., Rozental, S., & Ishida, K. (2015) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-015-0597-4 · Cited by 67 · see citing works
Linking Cellular Morphogenesis with Antifungal Treatment and Susceptibility in Candida Pathogens
Sharma, J., Rosiana, S., Razzaq, I., & Shapiro, R. S. (2019) · Journal of Fungi · doi:10.3390/jof5010017 · Cited by 64 · see citing works
Rao, H., Choo, S., Mahalingam, S. R. R., Adisuri, D. S., Madhavan, P., Akim, A. M., & Chong, P. P. (2021) · Molecules · doi:10.3390/molecules26071870 · Cited by 64 · see citing works
The Impact of Biofilm Formation on the Persistence of Candidemia
Li, W., Chen, Y., Kuo, S., Chen, F., & Lee, C. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01196 · Cited by 63 · see citing works
The role of antifungals against Candida biofilm in catheter-related candidemia
Bouza, E., Guinea, J., & Guembe, M. (2014) · Antibiotics · doi:10.3390/antibiotics4010001 · Cited by 62 · see citing works
Role of Vaginal Mucosa, Host Immunity and Microbiota in Vulvovaginal Candidiasis
Balakrishnan, S., Yamang, H., Lorenz, M., Chew, S.-Y., & Than, L. (2022) · Pathogens · doi:10.3390/pathogens11060618 · Cited by 64 · see citing works
Virulence of Clinical Candida Isolates
Mroczyńska, M., & Brillowska‐Dąbrowska, A. (2021) · Pathogens · doi:10.3390/pathogens10040466 · Cited by 59 · see citing works
Candida Prosthetic Joint Infection. A Review of Treatment Methods
Cobo, F., Rodríguez‐Granger, J., Sampedro, A., Aliaga–Martínez, L., & Navarro‐Marí, J. M. (2017) · Journal of Bone and Joint Infection · doi:10.7150/jbji.17699 · Cited by 58 · see citing works
Arias, L. S., Pessan, J. P., Neto, F. N. D. S., de Lima, B. H. R., Camargo, E. R., Ramage, G., Delbem, A. C. B., & Monteiro, D. R. (2020) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2020.111080 · Cited by 59 · see citing works
Johnson, C. J., Kernien, J. F., Hoyer, A. R., & Nett, J. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-13588-6 · Cited by 58 · see citing works
Evaluation of the biofilm life cycle between Candida albicans and Candida tropicalis
Atiencia-Carrera, M. B., Cabezas-Mera, F. S., Vizuete, K. S., Debut, A., Tejera, E., & Machado, A. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.953168 · Cited by 61 · see citing works
Connolly, L. A., Riccombeni, A., Grózer, Z., Holland, L., Lynch, D. B., Andes, D. R., Gácser, A., & Butler, G. (2013) · Molecular Microbiology · doi:10.1111/mmi.12345 · Cited by 58 · see citing works
Fonseca, E., Silva, S., Rodrigues, C. F., Alves, C. T., Azeredo, J., & Henriques, M. (2014) · Biofouling · doi:10.1080/08927014.2014.886108 · Cited by 56 · see citing works
Self-citationThree-species biofilm model onto plasma-treated titanium implant surface
Matos, A. O., Ricomini-Filho, A. P., Beline, T., Ogawa, E. S., Oliveira, B. E. C., de Almeida, A. B., Nociti, F. H., Rangel, E. C., da Cruz, N. C., Sukotjo, C., et al. (2017) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2017.01.035 · Cited by 56 · see citing works
The Clinical Importance of Fungal Biofilms
Ramage, G., & Williams, C. (2013) · Advances in applied microbiology · doi:10.1016/b978-0-12-407673-0.00002-3 · Cited by 54 · see citing works
Susceptibility of multispecies biofilm to photodynamic therapy using Photodithazine®
Quishida, C. C. C., Carmello, J. C., Mima, E. G. D. O., Bagnato, V. S., Machado, A. L., & Pavarina, A. C. (2013) · Lasers in Medical Science · doi:10.1007/s10103-013-1397-z · Cited by 55 · see citing works
Gaining Insights from Candida Biofilm Heterogeneity: One Size Does Not Fit All
Kean, R., Delaney, C., Rajendran, R., Sherry, L., Metcalfe, R., Thomas, R., McLean, W., Williams, C., & Ramage, G. (2018) · Journal of Fungi · doi:10.3390/jof4010012 · Cited by 53 · see citing works
Ramı́rez-Zavala, B., Weyler, M., Gildor, T., Schmauch, C., Kornitzer, D., Arkowitz, R. A., & Morschhäuser, J. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003696 · Cited by 53 · see citing works
In vivo Candida glabrata biofilm development on foreign bodies in a rat subcutaneous model
Kucharíková, S., Neirinck, B., Sharma, N., Vleugels, J., Lagrou, K., & Dijck, P. V. (2014) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dku447 · Cited by 53 · see citing works
Biofilm formation inCandida glabrata: What have we learnt from functional genomics approaches?
d’Enfert, C., & Janbon, G. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov111 · Cited by 54 · see citing works
Antifungal Carvacrol Loaded Chitosan Nanoparticles
Vitali, A., Stringaro, A., Colone, M., Muntiu, A., & Angiolella, L. (2021) · Antibiotics · doi:10.3390/antibiotics11010011 · Cited by 52 · see citing works
Emerging Nanomedicine Therapies to Counter the Rise of Methicillin-Resistant Staphylococcus aureus
Hibbitts, A., & O’Leary, C. (2018) · Materials · doi:10.3390/ma11020321 · Cited by 52 · see citing works
- Authors
- Silva, S., Henriques, M., Martins, A., Oliveira, R., Williams, D., & Azeredo, J.
- Affiliations
- Institute for Biotechnology and Bioengineering (PT)
- Cardiff University (GB)
- Venue
- Medical Mycology
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-11-03
- Volume
- 47
- Issue
- 7
- Pages
- 681-689
- ISSN
- 0268-1218 (ISSN-L)
- 1369-3786
- 1460-2709
- OpenAlex
- W2040661614
- Cited by
- 390
- References
- 40
- Citations by year
- 2026: 14 · 2025: 25 · 2024: 25 · 2023: 25 · 2022: 28 · 2021: 24 · 2020: 31 · 2019: 23 · 2018: 25 · 2017: 29 · 2016: 31 · 2015: 29 · 2014: 19 · 2013: 20 · 2012: 16
- FWCI
- 9.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Medical Mycology (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- 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 parapsilosis, Candida tropicalis, Candida glabrata, biofilm formation, biofilm matrix composition, biofilm structure, strain differences, antifungal resistance, candidiasis, clinical isolates
- MeSH terms
- Candida, Candidiasis, Carbohydrates, Female, Fungal Proteins, Humans, Mouth, Urinary Tract, Vagina, Biofilms
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review