Variation in biofilm formation among blood and oral isolates of Candida albicans and Candida dubliniensis | Enfermedades Infecciosas y Microbiología Clínica

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Although other species, such as Candida parapsilosis, Candida glabrata or Candida tropicalis, are being isolated with increasing frequency; Candida albicans is the most frequent aetiological agent of candidiasis.<a class="elsevierStyleCrossRefs" href="#bib0005">1,2</a> Many candidiasis are associated with prostheses, catheters and other indwelling medical devices, where these microorganisms develop biofilms. The presence of extracellular polymers and a different cellular phenotype, called sessile is an important feature in the structure of these microbial comunities. Biofilms impede the actions of the immune system and other defence mechanisms and become recalcitrant to current antifungal treatment.<a class="elsevierStyleCrossRefs" href="#bib0015">3–5</a>C. albicans is also an important pathogen of the oral cavity and other mucosae. This yeast has the ability to grow under diverse oral environmental conditions (e.g. unhygienic dentures, xerostomia) and/or systemic factors, such as diabetes and immunodeficiency. The presence of dentures that are overlaid with proteins and other oral components encourages the development of Candida biofilms and denture stomatitis.<a class="elsevierStyleCrossRef" href="#bib0020">4</a>Candida dubliniensis is an emerging species associated to oral candidiasis, mainly in HIV-infected patients.<a class="elsevierStyleCrossRefs" href="#bib0030">6–8</a> The frequence of deep-seated infections caused by C. dubliniensis is low but probably understimated because C. dubliniensis is closely related to C. albicans and many laboratories are not capable of differentiating between both species.<a class="elsevierStyleCrossRefs" href="#bib0005">1,9–13</a>C. dubliniensis shares many properties with C. albicans and, in addition, shows an important capacity to develop resistance to fluconazole and other antifungal agents under repeated exposure.<a class="elsevierStyleCrossRefs" href="#bib0035">7,14–16</a>The aim of the current study has been to compare the capacity of biofilm production by blood and oral isolates of C. albicans and C. dubliniensis from infected patients.MethodsMicroorganismsA total of 28 C. albicans (16 oral isolates and 12 blood isolates) and 19 C. dubliniensis (11 oral isolates and 8 blood isolates) from the Laboratorio de Micología Médica at the University of the Basque Country were studied. The clinical origin of the isolates and the infections caused have been described previously.<a class="elsevierStyleCrossRefs" href="#bib0040">8–10,17</a> Two strains from the National Collection of Pathogenic Fungi (NCPF), C. albicans NCPF 3153 and C. dubliniensis NCPF 3949, as well as C. albicans NCPF 3153 hypha-defective mutant CA-2 (kindly donated by Professor Antonio Cassone, Istituto Superiore di Sanità, Rome, Italy) were included as reference strains. The identity of all isolates was confirmed by conventional mycology methods, such as the germ tube test in serum, microscopic morphology, chlamydoconidia production in corn meal agar with Tween 80, and carbon source assimilation with the commercial kit ID 32 C (bioMérieux, France).<a class="elsevierStyleCrossRef" href="#bib0090">18</a> All isolates were screened for their ability to grow on Sabouraud dextrose agar at 45°C for 48h, and in the chromogenic media CHROM-Pal's medium<a class="elsevierStyleCrossRef" href="#bib0095">19</a> and ChromID Candida.<a class="elsevierStyleCrossRef" href="#bib0100">20</a> The reactivity with a specific polyclonal anti-C. dubliniensis antibody by an immunofluorescence assay<a class="elsevierStyleCrossRef" href="#bib0105">21</a> and by the Bichro-Dubli latex agglutination test (Fumouze Diagnostics, France)<a class="elsevierStyleCrossRef" href="#bib0110">22</a> were also tested. The identities of those isolates classified as C. dubliniensis were confirmed by means of a polymerase chain reaction (PCR) using the specific primers CDBF28-f (5′-AAATGGGTTTGGTGCCAAATTA-3′), and CDBR110-r (5′-GTTGGCATTGGCAATAGCTCTA-3′) described by Kanbe et al.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> which amplify topoisomerase II gene, giving a DNA product size of 816bp.Preparation of Candida suspensionsPrior to each experiment, yeast isolates were aerobically cultured at 37°C for 24h on Sabouraud dextrose agar (Difco Laboratories, USA) and a loopful of growth was inoculated in YPD broth (yeast extract 10g, peptone 20g, glucose 20g, distilled water 1l). After 24h, the yeasts were harvested, washed twice with phosphate buffered saline (PBS, pH 7.2) and suspended to a concentration of 107 cells/ml. This cell concentration was selected because previous workers have demonstrated an optimal degree of biofilm formation of C. albicans and C. dubliniensis at this particular concentration.<a class="elsevierStyleCrossRef" href="#bib0120">24</a>Production and quantification of Candida biofilmsBiofilm formation was measured using a colorimetric method based on the XTT reduction according to Ramage et al.<a class="elsevierStyleCrossRefs" href="#bib0125">25,26</a> Briefly, C. albicans and C. dubliniensis isolates were suspended in RPMI 1640 broth supplemented with L-glutamine and buffered with MOPS, and 100μl of standard cell suspensions of yeasts (107 cells/ml), prepared as above, were transferred into each well of a flat-bottomed 100-well microtitre plate (BioScreen, Finland). XTT (2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide) (Sigma, USA) was prepared as a saturated solution in 0.5g/l in Ringer's lactate and the solution was filter sterilised using a 0.22-μm-pore-size filter (Sarstedt, Germany), aliquoted and then stored at −70°C until required. Before each assay, an aliquot of stock XTT was thawed and the electron-coupling agent menadione, 10mM prepared in acetone (Sigma) was added to a final concentration of 1μM. The biofilms were washed 3 times with 100μl of PBS to remove loosely adherent cells. Afterwards, 100μl of the XTT–menadione solution was added to each biofilm and control wells to measure background XTT reduction levels, and the plates were incubated in the dark for 1h at 37°C. The colour changes in the XTT reduction assay (which directly correlate with the metabolic activity of the cells within the biofilm) were then measured using a BioScreen C plate incubator (BioScreen) at 492nm. Measurements were repeated at least six times each on different days. The optical densities (OD) corresponding to the biofilm metabolic activities of both Candida species were compared calculating the Student's t-test using the program SPSS (IBM, USA). Biofilm production was scored and divided into 6 categories, according to absorbance at 492nm (A)/transmittance (T), as 6+ (A>1.30/T≤5%), 5+ (A=1–1.29/T=6–10%), 4+ (A=0.70–0.99/T=11–20%), 3+ (A=0.40–0.69/T=21–40%), 2+ (A=0.20–0.39/T=41–60%), and 1+ (A<0.20/T>60%).<a class="elsevierStyleCrossRefs" href="#bib0010">2,27</a> Categories 6+ and 5+ included those high producers of biofilm isolates and categories 2+ and 1+ included poor or non-producers of biofilm. Categories were compared using the Chi-squared test with Yates’ correction when necessary. Differences between the species were considered to be statistically significant at P<0.05.ResultsAll tested isolates of C. albicans and C. dubliniensis produced biofilm on polystyrene (<a class="elsevierStyleCrossRefs" href="#tbl0005">Tables 1 and 2</a> and <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). However, a great variability in biofilm production was observed in both species. The biofilm metabolic activities (A492nm) of C. albicans isolates at 24h ranged between 0.291 and 1.506 (mean 0.869±0.352) and those of C. dubliniensis isolates ranged between 0.438 and 1.145 (mean 0.688±0.199) (P=0.03) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A). C. albicans blood isolates showed a higher metabolic activity in 24h biofilms than in oral isolates (0.955±0.379 vs. 0.805±0.328, respectively, P=0.28). A similar pattern was observed for C. dubliniensis (0.763±0.195 vs. 0.634±0.192, respectively, P=0.17).<elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia>Biofilm metabolic activities of C. albicans isolates at 48h were higher than at 24h (0.945±0.378 vs. 0.869±0.352, respectively, P=0.44) with independence of the origin of these isolates (blood vs. oral isolates: 1.007±0.401 vs. 0.900±0.366, respectively, P=0.48). However, at 48h the biofilms of oral isolates of C. dubliniensis showed more metabolic activity (0.640±0.163) than the biofilms of blood isolates (0.522±0.198) (P=0.19) (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> and <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B). Most C. dubliniensis isolates belonged to genotype I, except isolates 00-133 and 00-135, which were from the genotype II (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). There were no statistically significant differences in biofilm production between both genotypes.C. albicans included a non-statistically significant higher number of isolates classified as high producers of biofilm than C. dubliniensis (P=0.86) at 48h. Ten out of 28 C. albicans isolates (35.7%) were classified as high producers of biofilm at 24h. Of these, 5 were from blood (41.7% of the blood isolates) and 5 from the oral cavity (31.3% of the oral isolates) (P=0.86). This category of high producers of biofilm only grouped 2 out of 19 C. dubliniensis isolates (10.5%) at 24h, but this difference between isolates of both species was not statistically significant (P=0.109). However, at 48h, 10 out of 28 C. albicans isolates (35.7%) and 0 out of 19 C. dubliniensis isolates were classified as high producers of biofilm (P=0.01). At this incubation time, 5 out of 12 (41.7%) blood isolates of C. albicans were high producers of biofilm in comparison to 5 out of 16 oral isolates (31.3%) (P=0.86).DiscussionThe phenomenon of biofilm formation by microbes on inert surfaces has been extensively studied in bacteria and to a lesser extent in fungi, and there appears to be a direct relationship between the capability of the organisms to form a biofilm and their pathogenicity. However, few studies have compared biofilm production among C. albicans bloodstream and oral isolates<a class="elsevierStyleCrossRef" href="#bib0140">28</a> and much less, between oral and blood isolates of C. dubliniensis. The current results confirm that most C. albicans and C. dubliniensis oral and blood isolates develop biofilms on polystyrene plates. We used the colorimetric method based on the XTT reduction in the current study because it correlates well with other quantitative methods, such as ATP or CFU assays used in cross-comparison of species variation in biofilm production.<a class="elsevierStyleCrossRef" href="#bib0145">29</a> The XTT method is more versatile and less-time consuming, and is also particularly suited for assays using microtitre plates that allow the screening a large number of isolates.Shin et al.<a class="elsevierStyleCrossRef" href="#bib0140">28</a> observed that a very low percentage of isolates of C. albicans produced biofilm, regardless of the invasive (bloodstream) or non-invasive origin of the isolates (8% vs. 7%). Conversely, the biofilm production was high when isolates from other species were tested, and those from blood and deep tissues were statistically significant higher producers than those isolates from other clinical specimens. Kumar and Menon,<a class="elsevierStyleCrossRef" href="#bib0150">30</a> using the same medium and method for biofilm production, reported that 11 out of 18 C. albicans isolates (61%) were biofilm producers. Three out of 7 bloodstream isolates (43%) produced biofilm. Non-C. albicans isolates were higher producers of biofilm than those of C. albicans. These authors included 5 reference strains of C. dubliniensis, observing that all of them produced biofilm. In contrast, other authors have reported that isolates of C. albicans produced statistically significantly more biofilm than other Candida species.<a class="elsevierStyleCrossRefs" href="#bib0135">27,29,31–34</a> All isolates in our study showed a variable capability to produce biofilm, being distributed into 3 categories (from high to low producers of biofilm) considering their metabolic activities, and those isolated from the bloodstream were non-statistically significantly higher producers of biofilm than oral ones.These discrepancies could be associated with differences in the methodology used, to the potential variability associated to the geographic origin of the isolates, or to other isolate-associated factors. Shin et al.<a class="elsevierStyleCrossRef" href="#bib0140">28</a> and Kumar and Menon<a class="elsevierStyleCrossRef" href="#bib0150">30</a> used a Sabouraud dextrose broth, and a RPMI-based broth was used in our comparison. Sabouraud dextrose broth with a high content of glucose (8%) has been claimed to simulate the hyperglycaemic milieu found in those patients receiving total parenteral nutrition.<a class="elsevierStyleCrossRefs" href="#bib0140">28,30</a> However, RPMI-based broth is a better promoter of filamentation than Sabouraud dextrose broth,<a class="elsevierStyleCrossRef" href="#bib0175">35</a> a fact that is essential for the first step (adhesion) of biofilm production and can be influenced by different cultural and host factors.<a class="elsevierStyleCrossRefs" href="#bib0180">36–38</a> This influence of the RPMI in germ tube and hypha development could explain the production of biofilm by all the C. albicans and C. dubliniensis isolates tested in the current study.The geographical origin of isolates in the different studies can influence the biofilm production capability, as has been observed for other phenotypic traits of Candida isolates, such as virulence factors or in vitro antifungal susceptibilities.<a class="elsevierStyleCrossRefs" href="#bib0145">29,39</a> This can be another potential explanation of the differences encountered, as Shin et al.<a class="elsevierStyleCrossRef" href="#bib0140">28</a> studied isolates from Korea, and Kumar and Menon<a class="elsevierStyleCrossRef" href="#bib0150">30</a> from India, while in the current study all C. albicans isolates were from Spain. Li et al.,<a class="elsevierStyleCrossRef" href="#bib0200">40</a> studying Canadian isolates of C. albicans, reported that natural clones and clonal lineages of C. albicans exhibited extensive quantitative variations in biofilm formation. Something similar was described by Borecka-Melkusova and Bujdakova<a class="elsevierStyleCrossRef" href="#bib0205">41</a> in C. albicans and C. dubliniensis isolates from Slovakia. Thein et al.<a class="elsevierStyleCrossRef" href="#bib0145">29</a> also reported that growth and virulence of the different species of Candida were highly dependent on the isolates chosen for each study, hence it is important to use multiple clinical isolates and strains for the same species to draw firm conclusions in this regard.There was a high variability in the biofilm production among C. albicans isolates when the interspecies variation of C. albicans and C. dubliniensis isolates was studied. This variability was lower among C. dubliniensis isolates. Kuhn et al.<a class="elsevierStyleCrossRef" href="#bib0210">42</a> observed that XTT results can vary in accordance with the different sensitivity of C. albicans and Candida parapsilosis to tetrazolium salts. C. dubliniensis is more closely related to C. albicans than Candida parapsilosis and probably has a similar sensitivity to XTT than C. albicans. Nevertheless, we found that both Candida species, C. albicans and C. dubliniensis, exhibited good biofilm forming capability on polystyrene surfaces under aerobic conditions. These findings are in agreement with those of Ramage et al.<a class="elsevierStyleCrossRef" href="#bib0120">24</a> who also reported that C. dubliniensis exhibited good biofilm growth on the surface of polystyrene plates.One of the key morphogenesis factors for the phase transition in these dimorphic fungi is the nature of the environment, as the hypha growth is promoted by low oxygen and, nutrient starvation, as occurs in this aerobic and static conditions assay.<a class="elsevierStyleCrossRef" href="#bib0145">29</a> Such a phase transition is dependent upon strain as well as species characteristics, as shown here by the CA-2 hypha-deficient strain of C. albicans, which always exists in the yeast phase, irrespective of its environmental milieu. Both species formed heterogeneous biofilms with strain variations in their morphology and XTT metabolic activity, as has been described previously by Henriques et al.<a class="elsevierStyleCrossRef" href="#bib0160">32</a>In conclusion, there are important differences in biofilm production by C. albicans and C. dubliniensis isolates. These differences should be taken into account when the anti-biofilm activity of antifungal agents or other virulence factors are tested in vitro. This capability for biofilm development may enable C. albicans and C. dubliniensis to maintain their oral ecological niches as commensal microorganisms and can be a major virulence factor during invasive candidiasis with important clinical repercussions.Conflict of interestsThe authors have no conflict of interest to declare." "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:2 [ "identificador" => "xres150697" "titulo" => array:5 [ 0 => "Abstract" 1 => "Introduction" 2 => "Methods" 3 => "Results" 4 => "Conclusions" ] ] 1 => array:2 [ "identificador" => "xpalclavsec138640" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "xres150696" "titulo" => array:5 [ 0 => "Resumen" 1 => "Introducción" 2 => "Métodos" 3 => "Resultados" 4 => "Conclusiones" ] ] 3 => array:2 [ "identificador" => "xpalclavsec138639" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Microorganisms" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Preparation of Candida suspensions" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Production and quantification of Candida biofilms" ] ] ] 6 => array:2 [ "identificador" => "sec0030" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0035" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0040" "titulo" => "Conflict of interests" ] 9 => array:2 [ "identificador" => "xack42223" "titulo" => "Acknowledgements" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2011-03-04" "fechaAceptado" => "2011-06-28" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec138640" "palabras" => array:5 [ 0 => "Biofilm" 1 => "Blood" 2 => "Oral" 3 => "Candida albicans" 4 => "Candida dubliniensis" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec138639" "palabras" => array:5 [ 0 => "Biopelícula" 1 => "Sangre" 2 => "Boca" 3 => "Candida albicans" 4 => "Candida dubliniensis" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "IntroductionBiofilm production is considered a potential virulence factor of some Candida species. For this reason, an understanding of biofilm behavior of Candida albicans and its closely related species Candida dubliniensis is key to the development of effective preventive measures for invasive and oral candidiasis. The aim of this study was to compare the capacity of biofilm production by blood and oral isolates of C. albicans and C. dubliniensis using polystyrene, flat-bottomed 100-well microtiter plates. MethodsA total of 47 isolates, consisting of 28 C. albicans (16 oral and 12 blood isolates) and 19 C. dubliniensis (11 oral and 8 blood isolates) were compared for their biofilm forming ability under aerobic and static conditions. XTT reduction assay was used to quantify the sessile growth. ResultsAll tested isolates produced biofilm, measured as XTT metabolic activity. Biofilm formation by C. albicans isolates was statistically significantly higher than biofilm formation by C. dubliniensis isolates at 24h (P=0.03) and 48h (P=0.0001). There was a higher percentage (41.7%) of high producers of biofilms among C. albicans blood isolates than among oral isolates (31.3%), without statistically significant differences. ConclusionsThis capability may allow C. albicans and C. dubliniensis to maintain their oral ecological niches as commensal or pathogenic microorganisms and can be a major virulence factor during invasive candidiasis. However, the differences in biofilm production among isolates should be taken into account when the anti-biofilm activity of antifungal agents or other virulence factors are tested in vitro." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "IntroducciónEl desarrollo de biopelículas o biocapas se considera un factor de virulencia potencial de algunas especies de Candida. Una comprensión mejor del comportamiento de las biopelículas de Candida albicans y de la especie cercana Candida dubliniensis es clave para desarrollar medida preventyivas eficaces de las candidiasis superficiales (orales) e invasoras. El objetivo de este trabajo ha sido comparar la capacidad de producir biopelícula por parte de los aislamientos orales y de sangre de C. albicans y C. dubliniensis en placas de microtitulación de poliestireno de 100 pocillos con fondo plano. MétodosSe estudiaron 47 aislamientos: 28 C. albicans (16 orales y 12 hemáticos) y 19 C. dubliniensis (11 orales y 8 hemáticos). Se empleó una prueba de cuantificación de la actividad metabólica de las biopelículas (reducción de la sal de tetrazolio denominada XTT). ResultadosTodos los aislamientos mostraron actividad metabólica pero la formación de biopelícula por los aislamientos de C. albicans era significativamente mayor que por los de C. dubliniensis a 24h (P=0,03) y 48h (P=0,0001). Eran más numerosos, los aislamientos de C. albicans muy productores de biopelícula procedentes de sangre (41.7%) que de boca (31.3%) pero las diferencias no eran significativas. ConclusionesLa capacidad de desarrollar biopelículas, podría permitir a C. albicans y C. dubliniensis mantenerse en el nicho oral como comensales o patógenos y ser un importante factor de virulencia en las candidiasis invasoras. Sin embargo, las diferencias encontradas entre los aislamientos productores de biopelícula deben tenerse en cuenta, sobre todo en los estudios in vitro de virulencia o de la acción anti-biopelícula de los fármacos antifúngicos." ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 3757 "Ancho" => 3118 "Tamanyo" => 869987 ] ] "descripcion" => array:1 [ "en" => "Distribution of Candida albicans and Candida dubliniensis isolates on the basis of their capability for producing biofilms at 37°C for 24h (A) and 48h (B)." ] ] 1 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Species \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Biofilm production (XTT metabolic production)</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Blood \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Oral \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. albicans \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1.007±0.401 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.900±0.366 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. dubliniensis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.522±0.198 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.640±0.163 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="3" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"></td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="3" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Reference strains</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. albicans NCPF 3153 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.550±0.024</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. dubliniensis NCPF 3940 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.634±0.069</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. albicans CA-2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.112±0.008</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab244836.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Metabolic activity (XTT) of biofilms produced by Candida albicans and Candida dubliniensis clinical isolates at 48h according to their clinical origin." ] ] 2 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Category \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Biofilm \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="5" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Species (no. of isolates included and percentage)</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">C. albicans</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">C. dubliniensis</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Total \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Blood \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Oral \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Blood \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Oral \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">48h \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">48h \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">48h \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">48h \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">48h \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">High producers of biofilm</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 (16.7%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 (6.3%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3 (6.4%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3 (25%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4 (25%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7 (14.9%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Producers of biofilm</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4 (33.3%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6 (37.5%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 (12.5%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 (18.2%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13 (27.7%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3 (25%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5 (31.3%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5 (62.5%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9 (81.8%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">22 (46.8%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " rowspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Low producers and non-producers of biofilm</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 (25%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 (4.3%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 (0%) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " colspan="2" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Total</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">12 (100%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16 (100%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8 (100%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11 (100%) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">47 (100%) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab244837.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Distribution of clinical isolates of C. albicans and C. dubliniensis on the basis of their capability for producing biofilm at 48h." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:42 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => 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Mukherjee" 4 => "M.A. Ghannoum" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "J Clin Microbiol" "fecha" => "2003" "volumen" => "41" "paginaInicial" => "506" "paginaFinal" => "508" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12517908" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:3 [ "identificador" => "xack42223" "titulo" => "Acknowledgements" "texto" => "María Villar-Vidal and Cristina Marcos-Arias had scholarships from the Universidad del País Vasco-Euskal Herriko Unibertsitatea. We thank José Manuel Aguirre-Urizar, Antonio Cassone, Carmen Rubio, Ricardo Salesa, and Derek Sullivan for kindly providing some of the C. albicans and C. dubliniensis isolates and strains used in this study. This work has been funded in part by projects GIC07 123-IT-222–07 (Departamento de Educación, Universidades e Investigación, Gobierno Vasco), S-PE08UN35 and S-PR09UN01 (Saiotek 2008 and 2009, Departamento de Industria, Comercio y Turismo, Gobierno Vasco) and PI061895/2006 (Fondo de Investigación Sanitaria del Ministerio de Sanidad y Consumo de España)." ] ] ] "idiomaDefecto" => "en" "url" => "/0213005X/0000002900000009/v1_201305090306/S0213005X11002242/v1_201305090306/en/main.assets" "Apartado" => array:4 [ "identificador" => "8591" "tipo" => "SECCION" "es" => array:2 [ "titulo" => "Originales" "idiomaDefecto" => true ] "idiomaDefecto" => "es" ] "PDF" => "https://static.elsevier.es/multimedia/0213005X/0000002900000009/v1_201305090306/S0213005X11002242/v1_201305090306/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0213005X11002242?idApp=UINPBA00004N"]

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Variation in biofilm formation among blood and oral isolates of Candida albicans and Candida dubliniensis

Evaluación de la capacidad de formación de biopelícula de aislamientos clínicos de Candida albicans y Candida dubliniensis

María Villar-Vidal, Cristina Marcos-Arias, Elena Eraso, Guillermo Quindós

Corresponding author

guillermo.quindos@ehu.es

Corresponding author.

Laboratorio de Micología Médica, Departamento de Inmunología, Microbiología y Parasitología, Facultad de Medicina y Odontología, Universidad del País Vasco-Euskal Herriko Unibertsitatea, Bilbao, Spain

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Invasive candidiasis represents about 10&#37; of nosocomial invasive infections&#46; Although other species&#44; such as <span class="elsevierStyleItalic">Candida parapsilosis</span>&#44; <span class="elsevierStyleItalic">Candida glabrata</span> or <span class="elsevierStyleItalic">Candida tropicalis</span>&#44; are being isolated with increasing frequency&#59; <span class="elsevierStyleItalic">Candida albicans</span> is the most frequent aetiological agent of candidiasis&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;2</span></a> Many candidiasis are associated with prostheses&#44; catheters and other indwelling medical devices&#44; where these microorganisms develop biofilms&#46; The presence of extracellular polymers and a different cellular phenotype&#44; called sessile is an important feature in the structure of these microbial comunities&#46; Biofilms impede the actions of the immune system and other defence mechanisms and become recalcitrant to current antifungal treatment&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#8211;5</span></a><span class="elsevierStyleItalic">C&#46; albicans</span> is also an important pathogen of the oral cavity and other mucosae&#46; This yeast has the ability to grow under diverse oral environmental conditions &#40;e&#46;g&#46; unhygienic dentures&#44; xerostomia&#41; and&#47;or systemic factors&#44; such as diabetes and immunodeficiency&#46; The presence of dentures that are overlaid with proteins and other oral components encourages the development of <span class="elsevierStyleItalic">Candida</span> biofilms and denture stomatitis&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Candida dubliniensis</span> is an emerging species associated to oral candidiasis&#44; mainly in HIV-infected patients&#46;<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6&#8211;8</span></a> The frequence of deep-seated infections caused by <span class="elsevierStyleItalic">C&#46; dubliniensis</span> is low but probably understimated because <span class="elsevierStyleItalic">C&#46; dubliniensis</span> is closely related to <span class="elsevierStyleItalic">C&#46; albicans</span> and many laboratories are not capable of differentiating between both species&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;9&#8211;13</span></a><span class="elsevierStyleItalic">C&#46; dubliniensis</span> shares many properties with <span class="elsevierStyleItalic">C&#46; albicans</span> and&#44; in addition&#44; shows an important capacity to develop resistance to fluconazole and other antifungal agents under repeated exposure&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;14&#8211;16</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The aim of the current study has been to compare the capacity of biofilm production by blood and oral isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> from infected patients&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Microorganisms</span><p id="par0020" class="elsevierStylePara elsevierViewall">A total of 28 <span class="elsevierStyleItalic">C&#46; albicans</span> &#40;16 oral isolates and 12 blood isolates&#41; and 19 <span class="elsevierStyleItalic">C&#46; dubliniensis</span> &#40;11 oral isolates and 8 blood isolates&#41; from the Laboratorio de Micolog&#237;a M&#233;dica at the University of the Basque Country were studied&#46; The clinical origin of the isolates and the infections caused have been described previously&#46;<a class="elsevierStyleCrossRefs" href="#bib0040"><span class="elsevierStyleSup">8&#8211;10&#44;17</span></a> Two strains from the National Collection of Pathogenic Fungi &#40;NCPF&#41;&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> NCPF 3153 and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> NCPF 3949&#44; as well as <span class="elsevierStyleItalic">C&#46; albicans</span> NCPF 3153 hypha-defective mutant CA-2 &#40;kindly donated by Professor Antonio Cassone&#44; Istituto Superiore di Sanit&#224;&#44; Rome&#44; Italy&#41; were included as reference strains&#46; The identity of all isolates was confirmed by conventional mycology methods&#44; such as the germ tube test in serum&#44; microscopic morphology&#44; chlamydoconidia production in corn meal agar with Tween 80&#44; and carbon source assimilation with the commercial kit ID 32 C &#40;bioM&#233;rieux&#44; France&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> All isolates were screened for their ability to grow on Sabouraud dextrose agar at 45<span class="elsevierStyleHsp" style=""></span>&#176;C for 48<span class="elsevierStyleHsp" style=""></span>h&#44; and in the chromogenic media CHROM-Pal&#39;s medium<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> and ChromID Candida&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> The reactivity with a specific polyclonal anti-<span class="elsevierStyleItalic">C&#46; dubliniensis</span> antibody by an immunofluorescence assay<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> and by the Bichro-Dubli latex agglutination test &#40;Fumouze Diagnostics&#44; France&#41;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> were also tested&#46; The identities of those isolates classified as <span class="elsevierStyleItalic">C&#46; dubliniensis</span> were confirmed by means of a polymerase chain reaction &#40;PCR&#41; using the specific primers CDBF28-f &#40;5&#8242;-AAATGGGTTTGGTGCCAAATTA-3&#8242;&#41;&#44; and CDBR110-r &#40;5&#8242;-GTTGGCATTGGCAATAGCTCTA-3&#8242;&#41; described by Kanbe et al&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> which amplify topoisomerase II gene&#44; giving a DNA product size of 816<span class="elsevierStyleHsp" style=""></span>bp&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Preparation of <span class="elsevierStyleItalic">Candida</span> suspensions</span><p id="par0025" class="elsevierStylePara elsevierViewall">Prior to each experiment&#44; yeast isolates were aerobically cultured at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h on Sabouraud dextrose agar &#40;Difco Laboratories&#44; USA&#41; and a loopful of growth was inoculated in YPD broth &#40;yeast extract 10<span class="elsevierStyleHsp" style=""></span>g&#44; peptone 20<span class="elsevierStyleHsp" style=""></span>g&#44; glucose 20<span class="elsevierStyleHsp" style=""></span>g&#44; distilled water 1<span class="elsevierStyleHsp" style=""></span>l&#41;&#46; After 24<span class="elsevierStyleHsp" style=""></span>h&#44; the yeasts were harvested&#44; washed twice with phosphate buffered saline &#40;PBS&#44; pH 7&#46;2&#41; and suspended to a concentration of 10<span class="elsevierStyleSup">7</span> cells&#47;ml&#46; This cell concentration was selected because previous workers have demonstrated an optimal degree of biofilm formation of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> at this particular concentration&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Production and quantification of <span class="elsevierStyleItalic">Candida</span> biofilms</span><p id="par0030" class="elsevierStylePara elsevierViewall">Biofilm formation was measured using a colorimetric method based on the XTT reduction according to Ramage et al&#46;<a class="elsevierStyleCrossRefs" href="#bib0125"><span class="elsevierStyleSup">25&#44;26</span></a> Briefly&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates were suspended in RPMI 1640 broth supplemented with L-glutamine and buffered with MOPS&#44; and 100<span class="elsevierStyleHsp" style=""></span>&#956;l of standard cell suspensions of yeasts &#40;10<span class="elsevierStyleSup">7</span> cells&#47;ml&#41;&#44; prepared as above&#44; were transferred into each well of a flat-bottomed 100-well microtitre plate &#40;BioScreen&#44; Finland&#41;&#46; XTT &#40;2&#44;3-bis&#40;2-methoxy-4-nitro-5-sulfophenyl&#41;-2H-tetrazolium-5-carboxanilide&#41; &#40;Sigma&#44; USA&#41; was prepared as a saturated solution in 0&#46;5<span class="elsevierStyleHsp" style=""></span>g&#47;l in Ringer&#39;s lactate and the solution was filter sterilised using a 0&#46;22-&#956;m-pore-size filter &#40;Sarstedt&#44; Germany&#41;&#44; aliquoted and then stored at &#8722;70<span class="elsevierStyleHsp" style=""></span>&#176;C until required&#46; Before each assay&#44; an aliquot of stock XTT was thawed and the electron-coupling agent menadione&#44; 10<span class="elsevierStyleHsp" style=""></span>mM prepared in acetone &#40;Sigma&#41; was added to a final concentration of 1<span class="elsevierStyleHsp" style=""></span>&#956;M&#46; The biofilms were washed 3 times with 100<span class="elsevierStyleHsp" style=""></span>&#956;l of PBS to remove loosely adherent cells&#46; Afterwards&#44; 100<span class="elsevierStyleHsp" style=""></span>&#956;l of the XTT&#8211;menadione solution was added to each biofilm and control wells to measure background XTT reduction levels&#44; and the plates were incubated in the dark for 1<span class="elsevierStyleHsp" style=""></span>h at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; The colour changes in the XTT reduction assay &#40;which directly correlate with the metabolic activity of the cells within the biofilm&#41; were then measured using a BioScreen C plate incubator &#40;BioScreen&#41; at 492<span class="elsevierStyleHsp" style=""></span>nm&#46; Measurements were repeated at least six times each on different days&#46; The optical densities &#40;OD&#41; corresponding to the biofilm metabolic activities of both <span class="elsevierStyleItalic">Candida</span> species were compared calculating the Student&#39;s <span class="elsevierStyleItalic">t</span>-test using the program SPSS &#40;IBM&#44; USA&#41;&#46; Biofilm production was scored and divided into 6 categories&#44; according to absorbance at 492<span class="elsevierStyleHsp" style=""></span>nm &#40;<span class="elsevierStyleItalic">A</span>&#41;&#47;transmittance &#40;<span class="elsevierStyleItalic">T</span>&#41;&#44; as 6&#43; &#40;<span class="elsevierStyleItalic">A</span><span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>1&#46;30&#47;<span class="elsevierStyleItalic">T</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>5&#37;&#41;&#44; 5&#43; &#40;<span class="elsevierStyleItalic">A</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#8211;1&#46;29&#47;<span class="elsevierStyleItalic">T</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#8211;10&#37;&#41;&#44; 4&#43; &#40;<span class="elsevierStyleItalic">A</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;70&#8211;0&#46;99&#47;<span class="elsevierStyleItalic">T</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>11&#8211;20&#37;&#41;&#44; 3&#43; &#40;<span class="elsevierStyleItalic">A</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;40&#8211;0&#46;69&#47;<span class="elsevierStyleItalic">T</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>21&#8211;40&#37;&#41;&#44; 2&#43; &#40;<span class="elsevierStyleItalic">A</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;20&#8211;0&#46;39&#47;<span class="elsevierStyleItalic">T</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>41&#8211;60&#37;&#41;&#44; and 1&#43; &#40;<span class="elsevierStyleItalic">A</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;20&#47;<span class="elsevierStyleItalic">T</span><span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>60&#37;&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2&#44;27</span></a> Categories 6&#43; and 5&#43; included those high producers of biofilm isolates and categories 2&#43; and 1&#43; included poor or non-producers of biofilm&#46; Categories were compared using the Chi-squared test with Yates&#8217; correction when necessary&#46; Differences between the species were considered to be statistically significant at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Results</span><p id="par0035" class="elsevierStylePara elsevierViewall">All tested isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> produced biofilm on polystyrene &#40;<a class="elsevierStyleCrossRefs" href="#tbl0005">Tables 1 and 2</a> and <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; However&#44; a great variability in biofilm production was observed in both species&#46; The biofilm metabolic activities &#40;A492<span class="elsevierStyleHsp" style=""></span>nm&#41; of <span class="elsevierStyleItalic">C&#46; albicans</span> isolates at 24<span class="elsevierStyleHsp" style=""></span>h ranged between 0&#46;291 and 1&#46;506 &#40;mean 0&#46;869<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;352&#41; and those of <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates ranged between 0&#46;438 and 1&#46;145 &#40;mean 0&#46;688<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;199&#41; &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#46; <span class="elsevierStyleItalic">C&#46; albicans</span> blood isolates showed a higher metabolic activity in 24<span class="elsevierStyleHsp" style=""></span>h biofilms than in oral isolates &#40;0&#46;955<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;379 vs&#46; 0&#46;805<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;328&#44; respectively&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;28&#41;&#46; A similar pattern was observed for <span class="elsevierStyleItalic">C&#46; dubliniensis</span> &#40;0&#46;763<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;195 vs&#46; 0&#46;634<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;192&#44; respectively&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;17&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">Biofilm metabolic activities of <span class="elsevierStyleItalic">C&#46; albicans</span> isolates at 48<span class="elsevierStyleHsp" style=""></span>h were higher than at 24<span class="elsevierStyleHsp" style=""></span>h &#40;0&#46;945<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;378 vs&#46; 0&#46;869<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;352&#44; respectively&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;44&#41; with independence of the origin of these isolates &#40;blood vs&#46; oral isolates&#58; 1&#46;007<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;401 vs&#46; 0&#46;900<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;366&#44; respectively&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;48&#41;&#46; However&#44; at 48<span class="elsevierStyleHsp" style=""></span>h the biofilms of oral isolates of <span class="elsevierStyleItalic">C&#46; dubliniensis</span> showed more metabolic activity &#40;0&#46;640<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;163&#41; than the biofilms of blood isolates &#40;0&#46;522<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;198&#41; &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;19&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> and <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46; Most <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates belonged to genotype I&#44; except isolates 00-133 and 00-135&#44; which were from the genotype II &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; There were no statistically significant differences in biofilm production between both genotypes&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">C&#46; albicans</span> included a non-statistically significant higher number of isolates classified as high producers of biofilm than <span class="elsevierStyleItalic">C&#46; dubliniensis</span> &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;86&#41; at 48<span class="elsevierStyleHsp" style=""></span>h&#46; Ten out of 28 <span class="elsevierStyleItalic">C&#46; albicans</span> isolates &#40;35&#46;7&#37;&#41; were classified as high producers of biofilm at 24<span class="elsevierStyleHsp" style=""></span>h&#46; Of these&#44; 5 were from blood &#40;41&#46;7&#37; of the blood isolates&#41; and 5 from the oral cavity &#40;31&#46;3&#37; of the oral isolates&#41; &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;86&#41;&#46; This category of high producers of biofilm only grouped 2 out of 19 <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates &#40;10&#46;5&#37;&#41; at 24<span class="elsevierStyleHsp" style=""></span>h&#44; but this difference between isolates of both species was not statistically significant &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;109&#41;&#46; However&#44; at 48<span class="elsevierStyleHsp" style=""></span>h&#44; 10 out of 28 <span class="elsevierStyleItalic">C&#46; albicans</span> isolates &#40;35&#46;7&#37;&#41; and 0 out of 19 <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates were classified as high producers of biofilm &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46; At this incubation time&#44; 5 out of 12 &#40;41&#46;7&#37;&#41; blood isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> were high producers of biofilm in comparison to 5 out of 16 oral isolates &#40;31&#46;3&#37;&#41; &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;86&#41;&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Discussion</span><p id="par0050" class="elsevierStylePara elsevierViewall">The phenomenon of biofilm formation by microbes on inert surfaces has been extensively studied in bacteria and to a lesser extent in fungi&#44; and there appears to be a direct relationship between the capability of the organisms to form a biofilm and their pathogenicity&#46; However&#44; few studies have compared biofilm production among <span class="elsevierStyleItalic">C&#46; albicans</span> bloodstream and oral isolates<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> and much less&#44; between oral and blood isolates of <span class="elsevierStyleItalic">C&#46; dubliniensis</span>&#46; The current results confirm that most <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> oral and blood isolates develop biofilms on polystyrene plates&#46; We used the colorimetric method based on the XTT reduction in the current study because it correlates well with other quantitative methods&#44; such as ATP or CFU assays used in cross-comparison of species variation in biofilm production&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> The XTT method is more versatile and less-time consuming&#44; and is also particularly suited for assays using microtitre plates that allow the screening a large number of isolates&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Shin et al&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> observed that a very low percentage of isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> produced biofilm&#44; regardless of the invasive &#40;bloodstream&#41; or non-invasive origin of the isolates &#40;8&#37; vs&#46; 7&#37;&#41;&#46; Conversely&#44; the biofilm production was high when isolates from other species were tested&#44; and those from blood and deep tissues were statistically significant higher producers than those isolates from other clinical specimens&#46; Kumar and Menon&#44;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> using the same medium and method for biofilm production&#44; reported that 11 out of 18 <span class="elsevierStyleItalic">C&#46; albicans</span> isolates &#40;61&#37;&#41; were biofilm producers&#46; Three out of 7 bloodstream isolates &#40;43&#37;&#41; produced biofilm&#46; Non-<span class="elsevierStyleItalic">C&#46; albicans</span> isolates were higher producers of biofilm than those of <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; These authors included 5 reference strains of <span class="elsevierStyleItalic">C&#46; dubliniensis</span>&#44; observing that all of them produced biofilm&#46; In contrast&#44; other authors have reported that isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> produced statistically significantly more biofilm than other <span class="elsevierStyleItalic">Candida</span> species&#46;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">27&#44;29&#44;31&#8211;34</span></a> All isolates in our study showed a variable capability to produce biofilm&#44; being distributed into 3 categories &#40;from high to low producers of biofilm&#41; considering their metabolic activities&#44; and those isolated from the bloodstream were non-statistically significantly higher producers of biofilm than oral ones&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">These discrepancies could be associated with differences in the methodology used&#44; to the potential variability associated to the geographic origin of the isolates&#44; or to other isolate-associated factors&#46; Shin et al&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> and Kumar and Menon<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> used a Sabouraud dextrose broth&#44; and a RPMI-based broth was used in our comparison&#46; Sabouraud dextrose broth with a high content of glucose &#40;8&#37;&#41; has been claimed to simulate the hyperglycaemic milieu found in those patients receiving total parenteral nutrition&#46;<a class="elsevierStyleCrossRefs" href="#bib0140"><span class="elsevierStyleSup">28&#44;30</span></a> However&#44; RPMI-based broth is a better promoter of filamentation than Sabouraud dextrose broth&#44;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a> a fact that is essential for the first step &#40;adhesion&#41; of biofilm production and can be influenced by different cultural and host factors&#46;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">36&#8211;38</span></a> This influence of the RPMI in germ tube and hypha development could explain the production of biofilm by all the <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates tested in the current study&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">The geographical origin of isolates in the different studies can influence the biofilm production capability&#44; as has been observed for other phenotypic traits of <span class="elsevierStyleItalic">Candida</span> isolates&#44; such as virulence factors or <span class="elsevierStyleItalic">in vitro</span> antifungal susceptibilities&#46;<a class="elsevierStyleCrossRefs" href="#bib0145"><span class="elsevierStyleSup">29&#44;39</span></a> This can be another potential explanation of the differences encountered&#44; as Shin et al&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> studied isolates from Korea&#44; and Kumar and Menon<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> from India&#44; while in the current study all <span class="elsevierStyleItalic">C&#46; albicans</span> isolates were from Spain&#46; Li et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> studying Canadian isolates of <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; reported that natural clones and clonal lineages of <span class="elsevierStyleItalic">C&#46; albicans</span> exhibited extensive quantitative variations in biofilm formation&#46; Something similar was described by Borecka-Melkusova and Bujdakova<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> in <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates from Slovakia&#46; Thein et al&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> also reported that growth and virulence of the different species of <span class="elsevierStyleItalic">Candida</span> were highly dependent on the isolates chosen for each study&#44; hence it is important to use multiple clinical isolates and strains for the same species to draw firm conclusions in this regard&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">There was a high variability in the biofilm production among <span class="elsevierStyleItalic">C&#46; albicans</span> isolates when the interspecies variation of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates was studied&#46; This variability was lower among <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates&#46; Kuhn et al&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a> observed that XTT results can vary in accordance with the different sensitivity of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">Candida parapsilosis</span> to tetrazolium salts&#46; <span class="elsevierStyleItalic">C&#46; dubliniensis</span> is more closely related to <span class="elsevierStyleItalic">C&#46; albicans</span> than <span class="elsevierStyleItalic">Candida parapsilosis</span> and probably has a similar sensitivity to XTT than <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; Nevertheless&#44; we found that both <span class="elsevierStyleItalic">Candida</span> species&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span>&#44; exhibited good biofilm forming capability on polystyrene surfaces under aerobic conditions&#46; These findings are in agreement with those of Ramage et al&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> who also reported that <span class="elsevierStyleItalic">C&#46; dubliniensis</span> exhibited good biofilm growth on the surface of polystyrene plates&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">One of the key morphogenesis factors for the phase transition in these dimorphic fungi is the nature of the environment&#44; as the hypha growth is promoted by low oxygen and&#44; nutrient starvation&#44; as occurs in this aerobic and static conditions assay&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> Such a phase transition is dependent upon strain as well as species characteristics&#44; as shown here by the CA-2 hypha-deficient strain of <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; which always exists in the yeast phase&#44; irrespective of its environmental milieu&#46; Both species formed heterogeneous biofilms with strain variations in their morphology and XTT metabolic activity&#44; as has been described previously by Henriques et al&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">In conclusion&#44; there are important differences in biofilm production by <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates&#46; These differences should be taken into account when the anti-biofilm activity of antifungal agents or other virulence factors are tested <span class="elsevierStyleItalic">in vitro</span>&#46; This capability for biofilm development may enable <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> to maintain their oral ecological niches as commensal microorganisms and can be a major virulence factor during invasive candidiasis with important clinical repercussions&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conflict of interests</span><p id="par0085" class="elsevierStylePara elsevierViewall">The authors have no conflict of interest to declare&#46;</p></span></span>"
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          "titulo" => array:5 [
            0 => "Resumen"
            1 => "Introducci&#243;n"
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          "titulo" => "Palabras clave"
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              "titulo" => "Microorganisms"
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            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Preparation of Candida suspensions"
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            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Production and quantification of Candida biofilms"
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          "titulo" => "Results"
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          "titulo" => "Conflict of interests"
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          "titulo" => "Acknowledgements"
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          "titulo" => "References"
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    "pdfFichero" => "main.pdf"
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    "fechaRecibido" => "2011-03-04"
    "fechaAceptado" => "2011-06-28"
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          "palabras" => array:5 [
            0 => "Biofilm"
            1 => "Blood"
            2 => "Oral"
            3 => "<span class="elsevierStyleItalic">Candida albicans</span>"
            4 => "<span class="elsevierStyleItalic">Candida dubliniensis</span>"
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec138639"
          "palabras" => array:5 [
            0 => "Biopel&#237;cula"
            1 => "Sangre"
            2 => "Boca"
            3 => "<span class="elsevierStyleItalic">Candida albicans</span>"
            4 => "<span class="elsevierStyleItalic">Candida dubliniensis</span>"
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    "resumen" => array:2 [
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        "titulo" => "Abstract"
        "resumen" => "<span class="elsevierStyleSectionTitle">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Biofilm production is considered a potential virulence factor of some <span class="elsevierStyleItalic">Candida</span> species&#46; For this reason&#44; an understanding of biofilm behavior of <span class="elsevierStyleItalic">Candida albicans</span> and its closely related species <span class="elsevierStyleItalic">Candida dubliniensis</span> is key to the development of effective preventive measures for invasive and oral candidiasis&#46; The aim of this study was to compare the capacity of biofilm production by blood and oral isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> using polystyrene&#44; flat-bottomed 100-well microtiter plates&#46;</p> <span class="elsevierStyleSectionTitle">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A total of 47 isolates&#44; consisting of 28 <span class="elsevierStyleItalic">C&#46; albicans</span> &#40;16 oral and 12 blood isolates&#41; and 19 <span class="elsevierStyleItalic">C&#46; dubliniensis</span> &#40;11 oral and 8 blood isolates&#41; were compared for their biofilm forming ability under aerobic and static conditions&#46; XTT reduction assay was used to quantify the sessile growth&#46;</p> <span class="elsevierStyleSectionTitle">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">All tested isolates produced biofilm&#44; measured as XTT metabolic activity&#46; Biofilm formation by <span class="elsevierStyleItalic">C&#46; albicans</span> isolates was statistically significantly higher than biofilm formation by <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates at 24<span class="elsevierStyleHsp" style=""></span>h &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41; and 48<span class="elsevierStyleHsp" style=""></span>h &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#41;&#46; There was a higher percentage &#40;41&#46;7&#37;&#41; of high producers of biofilms among <span class="elsevierStyleItalic">C&#46; albicans</span> blood isolates than among oral isolates &#40;31&#46;3&#37;&#41;&#44; without statistically significant differences&#46;</p> <span class="elsevierStyleSectionTitle">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">This capability may allow <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> to maintain their oral ecological niches as commensal or pathogenic microorganisms and can be a major virulence factor during invasive candidiasis&#46; However&#44; the differences in biofilm production among isolates should be taken into account when the anti-biofilm activity of antifungal agents or other virulence factors are tested <span class="elsevierStyleItalic">in vitro</span>&#46;</p>"
      ]
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        "resumen" => "<span class="elsevierStyleSectionTitle">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El desarrollo de biopel&#237;culas o biocapas se considera un factor de virulencia potencial de algunas especies de <span class="elsevierStyleItalic">Candida</span>&#46; Una comprensi&#243;n mejor del comportamiento de las biopel&#237;culas de <span class="elsevierStyleItalic">Candida albicans</span> y de la especie cercana <span class="elsevierStyleItalic">Candida dubliniensis</span> es clave para desarrollar medida preventyivas eficaces de las candidiasis superficiales &#40;orales&#41; e invasoras&#46; El objetivo de este trabajo ha sido comparar la capacidad de producir biopel&#237;cula por parte de los aislamientos orales y de sangre de <span class="elsevierStyleItalic">C&#46; albicans</span> y <span class="elsevierStyleItalic">C&#46; dubliniensis</span> en placas de microtitulaci&#243;n de poliestireno de 100 pocillos con fondo plano&#46;</p> <span class="elsevierStyleSectionTitle">M&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se estudiaron 47 aislamientos&#58; 28 <span class="elsevierStyleItalic">C&#46; albicans</span> &#40;16 orales y 12 hem&#225;ticos&#41; y 19 <span class="elsevierStyleItalic">C&#46; dubliniensis</span> &#40;11 orales y 8 hem&#225;ticos&#41;&#46; Se emple&#243; una prueba de cuantificaci&#243;n de la actividad metab&#243;lica de las biopel&#237;culas &#40;reducci&#243;n de la sal de tetrazolio denominada XTT&#41;&#46;</p> <span class="elsevierStyleSectionTitle">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Todos los aislamientos mostraron actividad metab&#243;lica pero la formaci&#243;n de biopel&#237;cula por los aislamientos de <span class="elsevierStyleItalic">C&#46; albicans</span> era significativamente mayor que por los de <span class="elsevierStyleItalic">C&#46; dubliniensis</span> a 24<span class="elsevierStyleHsp" style=""></span>h &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;03&#41; y 48<span class="elsevierStyleHsp" style=""></span>h &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;0001&#41;&#46; Eran m&#225;s numerosos&#44; los aislamientos de <span class="elsevierStyleItalic">C&#46; albicans</span> muy productores de biopel&#237;cula procedentes de sangre &#40;41&#46;7&#37;&#41; que de boca &#40;31&#46;3&#37;&#41; pero las diferencias no eran significativas&#46;</p> <span class="elsevierStyleSectionTitle">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La capacidad de desarrollar biopel&#237;culas&#44; podr&#237;a permitir a <span class="elsevierStyleItalic">C&#46; albicans</span> y <span class="elsevierStyleItalic">C&#46; dubliniensis</span> mantenerse en el nicho oral como comensales o pat&#243;genos y ser un importante factor de virulencia en las candidiasis invasoras&#46; Sin embargo&#44; las diferencias encontradas entre los aislamientos productores de biopel&#237;cula deben tenerse en cuenta&#44; sobre todo en los estudios <span class="elsevierStyleItalic">in vitro</span> de virulencia o de la acci&#243;n anti-biopel&#237;cula de los f&#225;rmacos antif&#250;ngicos&#46;</p>"
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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Distribution of <span class="elsevierStyleItalic">Candida albicans</span> and <span class="elsevierStyleItalic">Candida dubliniensis</span> isolates on the basis of their capability for producing biofilms at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h &#40;A&#41; and 48<span class="elsevierStyleHsp" style=""></span>h &#40;B&#41;&#46;</p>"
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                  <table border="0" frame="\n
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                  \t\t\t\t">Species&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Biofilm production &#40;XTT metabolic production&#41;</td></tr><tr title="table-row"><td class="td" title="\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Blood&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; albicans</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">1&#46;007<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;401&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;900<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;366&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; dubliniensis</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;522<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;198&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;640<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;163&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">C&#46; albicans</span> NCPF 3153&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Category&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Biofilm&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="5" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">Species &#40;no&#46; of isolates included and percentage&#41;</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">C&#46; albicans</span></td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">C&#46; dubliniensis</span></td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Blood&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Oral&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Blood&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Oral&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">48<span class="elsevierStyleHsp" style=""></span>h&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">48<span class="elsevierStyleHsp" style=""></span>h&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">48<span class="elsevierStyleHsp" style=""></span>h&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">48<span class="elsevierStyleHsp" style=""></span>h&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" style="border-bottom: 2px solid black">48<span class="elsevierStyleHsp" style=""></span>h&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">High producers of biofilm</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 &#40;16&#46;7&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1 &#40;6&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3 &#40;6&#46;4&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3 &#40;25&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4 &#40;25&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">7 &#40;14&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Producers of biofilm</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4 &#40;33&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6 &#40;37&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1 &#40;12&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 &#40;18&#46;2&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">13 &#40;27&#46;7&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3 &#40;25&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5 &#40;31&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5 &#40;62&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9 &#40;81&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">22 &#40;46&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Low producers and non-producers of biofilm</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 &#40;25&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 &#40;4&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0 &#40;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">16 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">11 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">47 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab244837.png"
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Distribution of clinical isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> on the basis of their capability for producing biofilm at 48<span class="elsevierStyleHsp" style=""></span>h&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0005"
          "bibliografiaReferencia" => array:42 [
            0 => array:3 [
              "identificador" => "bib0005"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Trends in candidemia and antifungal susceptibility in a university hospital in Northern Ireland 2001&#8211;2006"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "L&#46; Metwally"
                            1 => "M&#46;J&#46; Walker"
                            2 => "P&#46;V&#46; Coyle"
                            3 => "R&#46;J&#46; Hay"
                            4 => "S&#46; Hedderwick"
                            5 => "B&#46;V&#46; McCloskey"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.jinf.2007.04.003"
                      "Revista" => array:6 [
                        "tituloSerie" => "J Infect"
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        "texto" => "<p id="par0090" class="elsevierStylePara elsevierViewall">Mar&#237;a Villar-Vidal and Cristina Marcos-Arias had scholarships from the Universidad del Pa&#237;s Vasco-Euskal Herriko Unibertsitatea&#46; We thank Jos&#233; Manuel Aguirre-Urizar&#44; Antonio Cassone&#44; Carmen Rubio&#44; Ricardo Salesa&#44; and Derek Sullivan for kindly providing some of the <span class="elsevierStyleItalic">C&#46; albicans</span> and <span class="elsevierStyleItalic">C&#46; dubliniensis</span> isolates and strains used in this study&#46; This work has been funded in part by projects GIC07 123-IT-222&#8211;07 &#40;Departamento de Educaci&#243;n&#44; Universidades e Investigaci&#243;n&#44; Gobierno Vasco&#41;&#44; S-PE08UN35 and S-PR09UN01 &#40;Saiotek 2008 and 2009&#44; Departamento de Industria&#44; Comercio y Turismo&#44; Gobierno Vasco&#41; and PI061895&#47;2006 &#40;Fondo de Investigaci&#243;n Sanitaria del Ministerio de Sanidad y Consumo de Espa&#241;a&#41;&#46;</p>"
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Article information

ISSN: 0213005X
Original language: English

DOI:10.1016/j.eimc.2011.06.009

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Year/Month	Html	Pdf	Total

2024 October	8	3	11
2024 September	33	15	48
2024 August	20	25	45
2024 July	24	12	36
2024 June	25	12	37
2024 May	18	14	32
2024 April	17	21	38
2024 March	28	13	41
2024 February	28	18	46
2024 January	28	16	44
2023 December	22	34	56
2023 November	25	29	54
2023 October	29	40	69
2023 September	20	31	51
2023 August	22	24	46
2023 July	15	25	40
2023 June	23	4	27
2023 May	41	7	48
2023 April	41	9	50
2023 March	47	14	61
2023 February	25	22	47
2023 January	21	19	40
2022 December	30	9	39
2022 November	23	20	43
2022 October	25	21	46
2022 September	28	16	44
2022 August	39	16	55
2022 July	31	14	45
2022 June	23	23	46
2022 May	35	21	56
2022 April	149	10	159
2022 March	28	15	43
2022 February	15	15	30
2022 January	18	14	32
2021 December	23	29	52
2021 November	30	23	53
2021 October	27	16	43
2021 September	24	13	37
2021 August	18	7	25
2021 July	38	13	51
2021 June	42	13	55
2021 May	38	14	52
2021 April	58	27	85
2021 March	36	16	52
2021 February	24	7	31
2021 January	23	19	42
2020 December	23	20	43
2020 November	16	14	30
2020 October	9	8	17
2020 September	41	19	60
2020 August	21	7	28
2020 July	28	8	36
2020 June	24	13	37
2020 May	29	23	52
2020 April	13	9	22
2020 March	29	13	42
2020 February	16	15	31
2020 January	33	15	48
2019 December	46	19	65
2019 November	34	5	39
2019 October	15	12	27
2019 September	27	2	29
2019 August	21	4	25
2019 July	18	16	34
2019 June	69	33	102
2019 May	184	84	268
2019 April	76	36	112
2019 March	18	3	21
2019 February	18	15	33
2019 January	9	5	14
2018 December	20	16	36
2018 November	19	8	27
2018 October	27	29	56
2018 September	37	9	46
2018 August	19	3	22
2018 July	18	0	18
2018 June	15	5	20
2018 May	17	2	19
2018 April	19	11	30
2018 March	12	1	13
2018 February	10	0	10
2018 January	13	0	13
2017 December	17	1	18
2017 November	10	4	14
2017 October	13	2	15
2017 September	14	1	15
2017 August	22	2	24
2017 July	17	7	24
2017 June	23	15	38
2017 May	26	2	28
2017 April	25	5	30
2017 March	23	6	29
2017 February	30	4	34
2017 January	28	2	30
2016 December	35	2	37
2016 November	44	2	46
2016 October	82	8	90
2016 September	65	3	68
2016 August	58	5	63
2016 July	34	0	34
2016 June	37	6	43
2016 May	26	1	27
2016 April	25	5	30
2016 March	43	5	48
2016 February	24	6	30
2016 January	43	10	53
2015 December	32	9	41
2015 November	43	5	48
2015 October	55	5	60
2015 September	37	7	44
2015 August	56	4	60
2015 July	29	3	32
2015 June	29	5	34
2015 May	32	2	34
2015 April	24	8	32
2015 March	43	6	49
2015 February	47	1	48
2015 January	32	5	37
2014 December	42	7	49
2014 November	38	3	41
2014 October	31	5	36
2014 September	39	1	40
2014 August	32	1	33
2014 July	35	4	39
2014 June	39	1	40
2014 May	35	3	38
2014 April	32	2	34
2014 March	63	11	74
2014 February	52	6	58
2014 January	47	5	52
2013 December	55	10	65
2013 November	50	7	57
2013 October	61	17	78
2013 September	46	16	62
2013 August	61	11	72
2013 July	49	14	63
2013 June	12	3	15
2013 May	21	9	30
2013 April	19	13	32
2013 March	14	7	21
2013 February	2	3	5
2013 January	1	1	2
2012 December	6	4	10
2012 November	5	3	8
2012 October	2	2	4
2011 November	1235	0	1235

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