Brief report
Assessment of biofilm production in Candida isolates according to species and origin of infection
Determinación de la producción de biopelícula en aislados de Candida de acuerdo con las especies de Candida y el origen de la infección
María Guembea,
, Raquel Crucesa, Teresa Peláeza,b, Patricia Muñoza,b,c, Emilio Bouzaa,b,c, on behalf of the GEIDI study group
Corresponding author
a Servicio de Microbiología Clínica y Enfermedades Infecciosas, Hospital General Universitario Gregorio Marañón, Madrid, Spain
b Medicine Department, School of Medicine, Universidad Complutense de Madrid, Madrid, Spain
c CIBER de Enfermedades Respiratorias (CIBERES CD06/06/0058), Palma de Mallorca, Spain
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class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] 5 => array:1 [ "colaborador" => "on behalf of the GEIDI study group" ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Servicio de Microbiología Clínica y Enfermedades Infecciosas, Hospital General Universitario Gregorio Marañón, Madrid, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Medicine Department, School of Medicine, Universidad Complutense de Madrid, Madrid, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "CIBER de Enfermedades Respiratorias (CIBERES CD06/06/0058), Palma de Mallorca, Spain" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Determinación de la producción de biopelícula en aislados de <span class="elsevierStyleItalic">Candida</span> de acuerdo con las especies de <span class="elsevierStyleItalic">Candida</span> y el origen de la infección" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1304 "Ancho" => 1640 "Tamanyo" => 94483 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Comparison of biofilm production between <span class="elsevierStyleItalic">Candida</span> species.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Candida albicans</span> is the most common cause of oropharyngeal and cutaneous candidiasis, and non-<span class="elsevierStyleItalic">albicans</span> species are increasingly associated with invasive candidiasis.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">1</span></a><span class="elsevierStyleItalic">Candida</span> bloodstream infection is one of the main nosocomial infections, with high morbidity and mortality. The ease with which some <span class="elsevierStyleItalic">Candida</span> strains adhere to natural or artificial surfaces to create aggregates (biofilm) increases their virulence and the likelihood of chronic infection.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">2</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Biofilm production (BP) by <span class="elsevierStyleItalic">Candida</span> species has been assessed mainly using the crystal violet binding assay. However, most studies report BP without a standard cut-off and are generally based on <span class="elsevierStyleItalic">Candida</span> species isolated from patients with candidemia.<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">3–6</span></a> Data regarding BP in <span class="elsevierStyleItalic">Candida</span> species isolated from different sites are scarce.</p><p id="par0015" class="elsevierStylePara elsevierViewall">Our objective was to test BP in clinical strains of <span class="elsevierStyleItalic">Candida</span> and compare the results between <span class="elsevierStyleItalic">Candida</span> species and between different sites of infection.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Methods</span><p id="par0020" class="elsevierStylePara elsevierViewall">We performed a prospective in vitro study of BP in 200 clinical strains of <span class="elsevierStyleItalic">Candida</span> species isolated from 155 patients admitted to our institution during 2010–2013. The <span class="elsevierStyleItalic">Candida</span> species were distributed as follows: <span class="elsevierStyleItalic">C. albicans</span>, 41 (20.5%); <span class="elsevierStyleItalic">C. parapsilosis</span>, 40 (20.0%); <span class="elsevierStyleItalic">C. krusei</span>, 40 (20.0%); <span class="elsevierStyleItalic">C. glabrata</span>, 39 (19.5%); <span class="elsevierStyleItalic">C. tropicalis</span>, 22 (11.0%); and <span class="elsevierStyleItalic">C. guilliermondii</span>, 18 (9.0%). The sources of the <span class="elsevierStyleItalic">Candida</span> isolates were as follows: urine, 33 (16.5%); biopsy specimens, 28 (14.0%); respiratory tract, 26 (13.0%); blood, 24 (12.0%); sterile liquids, 18 (9.0%); wound, 13 (6.5%); abscess, 10 (5.0%); catheter, 8 (4.0%); prosthetic material, 3 (1.5%); and other, 37 (18.5%).</p><p id="par0025" class="elsevierStylePara elsevierViewall">The yeasts were identified using the ID 32C system (bioMérieux).</p><p id="par0030" class="elsevierStylePara elsevierViewall">BP was assessed using the crystal violet binding assay.<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">3,7</span></a></p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Laboratory procedure</span><p id="par0035" class="elsevierStylePara elsevierViewall">Isolates were grown on Sabouraud dextrose agar for 24<span class="elsevierStyleHsp" style=""></span>h at 37<span class="elsevierStyleHsp" style=""></span>°C. Two or three colonies from each plate were inoculated into 20<span class="elsevierStyleHsp" style=""></span>mL of yeast peptone dextrose (YPD) medium and incubated for 18<span class="elsevierStyleHsp" style=""></span>h at 30<span class="elsevierStyleHsp" style=""></span>°C on an orbital shaker. They were then centrifuged at 3500<span class="elsevierStyleHsp" style=""></span>rpm for 5<span class="elsevierStyleHsp" style=""></span>min, washed twice with 10<span class="elsevierStyleHsp" style=""></span>mL of phosphate-buffered saline, and re-suspended in RPMI 1640 medium. After being standardized to 1<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">6</span><span class="elsevierStyleHsp" style=""></span>CFU/mL in RPMI, 100<span class="elsevierStyleHsp" style=""></span>μL of the suspension was placed in the wells of a 96-well, flat-bottomed microtiter plate and incubated for 24<span class="elsevierStyleHsp" style=""></span>h at 37<span class="elsevierStyleHsp" style=""></span>°C. The suspensions were discarded, and the wells were washed 3 times with sterile phosphate-buffered saline and filled with crystal violet for 15<span class="elsevierStyleHsp" style=""></span>min. The wells were then washed and the residue solubilized with acetic acid. The suspension was transferred to clean wells, and absorbance was detected in the spectrophotometer at 550<span class="elsevierStyleHsp" style=""></span>nm. Each experiment was performed in triplicate, and the average value was used for the analysis.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Statistical analysis</span><p id="par0040" class="elsevierStylePara elsevierViewall">The qualitative variables appear with their frequency distributions. Values for continuous variables are expressed as the mean (SD) with a 95% confidence interval (95% CI) when applicable. Categorical variables were evaluated using the chi-square or 2-tailed Fisher exact test. Normally distributed continuous variables were compared using the <span class="elsevierStyleItalic">t</span> test. We determined the cut-offs for BP using a ROC curve. The Games–Howell test was used to compare BP between the species and between the types of samples. The comparison between BP and origin of the infection was made irrespective of the <span class="elsevierStyleItalic">Candida</span> species.</p><p id="par0045" class="elsevierStylePara elsevierViewall">Statistical significance was set at <span class="elsevierStyleItalic">p</span> <0.05 (2-tailed). All statistical tests were performed using SPSS version 21.0.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Ethics</span><p id="par0050" class="elsevierStylePara elsevierViewall">The study was approved by the local ethics committee.</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Results</span><p id="par0055" class="elsevierStylePara elsevierViewall">Of the 155 patients, 129 (83.2%) had only 1 <span class="elsevierStyleItalic">Candida</span> species isolated in 1 clinical specimen and 26 (16.8%) had 2 or more isolates at the same or different sites (mean [SD] no. of isolates per patient, 1.26 [0.75]). Only 6 patients (3.9%) had the same <span class="elsevierStyleItalic">Candida</span> species in different clinical specimens.</p><p id="par0060" class="elsevierStylePara elsevierViewall">After the analysis using the crystal violet assay, we determined the following cut-offs for BP in <span class="elsevierStyleItalic">Candida</span> strains: low, <1; moderate, 1–2; and high, >2.</p><p id="par0065" class="elsevierStylePara elsevierViewall">BP was low in 53.0% of isolates, moderate in 24.0%, and high in 23.0%. The mean (SD) BP for the different <span class="elsevierStyleItalic">Candida</span> species was as follows: <span class="elsevierStyleItalic">C. albicans</span>, 1.8 (0.5); <span class="elsevierStyleItalic">C. parapsilosis</span>, 1.3 (0.9); <span class="elsevierStyleItalic">C. krusei</span>, 0.4 (0.3); <span class="elsevierStyleItalic">C. glabrata</span>, 0.3 (0.4); <span class="elsevierStyleItalic">C. tropicalis</span>, 2.4 (0.7); and <span class="elsevierStyleItalic">C. guilliermondii</span>, 0.6 (0.5) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> and <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Analysis of the degree of BP in the different <span class="elsevierStyleItalic">Candida</span> species showed that most <span class="elsevierStyleItalic">C. albicans</span> were high or moderate biofilm producers (92.6%) and that <span class="elsevierStyleItalic">C. parapsilosis</span> were mainly low or moderate biofilm producers (72.5%). In contrast, almost all <span class="elsevierStyleItalic">C. krusei</span>, <span class="elsevierStyleItalic">C. glabrata</span>, and <span class="elsevierStyleItalic">C. guilliermondii</span> were low biofilm producers (92.5%, 92.3%, and 77.8%, respectively). The highest BP values were found for <span class="elsevierStyleItalic">C. tropicalis</span> (72.7%).</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">Comparison of <span class="elsevierStyleItalic">Candida</span> BP between clinical specimens revealed that high-biofilm-producing species were those colonizing normally sterile body fluids, biopsy specimens, and catheter samples, whereas low-biofilm-producing species of <span class="elsevierStyleItalic">Candida</span> strains were those colonizing urine and respiratory tract samples (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Comparison of BP according to the origin of the isolates revealed statistically significant differences only between BP in blood and respiratory tract samples (mean BP, 1.4 vs. 0.4; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.002) and between respiratory tract and sterile fluids (mean BP, 0.4 vs. 1.6; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.010), biopsy specimens (mean BP, 0.4 vs. 1.5; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001), and catheter (mean BP, 0.4 vs. 1.7; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.009).</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Discussion</span><p id="par0075" class="elsevierStylePara elsevierViewall">BP in <span class="elsevierStyleItalic">Candida</span> varies with the species and is highest with <span class="elsevierStyleItalic">C. tropicalis</span>. In addition, higher BP correlates with deep-seated infection.</p><p id="par0080" class="elsevierStylePara elsevierViewall">BP is an important virulence factor of <span class="elsevierStyleItalic">Candida</span> species, and the methodology used to test it has not been well standardized. A recent study by Marcos-Zambrano et al.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">3</span></a> was the first to assess the BP of <span class="elsevierStyleItalic">Candida</span> species isolated from blood by comparing biomass production and metabolic activity to establish tentative cut-offs so that isolates could be classed as low-, moderate-, or high-biofilm-producing. In our study, we used the crystal violet assay to detect BP and obtained similar cut-offs to classify <span class="elsevierStyleItalic">Candida</span> strains according to BP.</p><p id="par0085" class="elsevierStylePara elsevierViewall">Analysis of differences in the degree of BP by <span class="elsevierStyleItalic">Candida</span> species revealed that <span class="elsevierStyleItalic">C. tropicalis</span> was the highest biofilm producer and that <span class="elsevierStyleItalic">C. albicans</span> and <span class="elsevierStyleItalic">C. parapsilosis</span> were moderate or high producers, as previously described.<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">8,9</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">BP is highly dependent on the conditions under which the biofilm is formed (e.g., type of implanted device and its location); therefore, its values can differ between sites of infection.<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">10,11</span></a> Shin et al.<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">12</span></a> compared BP in <span class="elsevierStyleItalic">Candida</span> isolated from blood and from other anatomical sites and demonstrated that <span class="elsevierStyleItalic">Candida</span> species isolated from blood produced higher amounts of biofilm than <span class="elsevierStyleItalic">Candida</span> species isolated from other sites (57% vs. 32%, <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001). However, they did not classify BP as low, moderate, or high. In our study, we only found statistically significant differences in BP between blood and respiratory tract samples (mean BP, 1.4 vs. 0.4; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.002). Moreover, we showed that <span class="elsevierStyleItalic">Candida</span> species isolated from samples from patients with deep-seated infection (normally sterile fluids, biopsy specimens, and catheter samples) produced more biofilm than those isolated from urine and respiratory tract samples (mean BP, 1.5 vs. 0.8; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001).</p><p id="par0095" class="elsevierStylePara elsevierViewall">Therefore, our findings demonstrate that, as BP was higher among <span class="elsevierStyleItalic">C. tropicalis</span> and among clinical specimens from deep tissues, it may play a key role in clinical outcome by acting as a reservoir for re-infection. Early detection of <span class="elsevierStyleItalic">Candida</span> BP can be useful in predicting the severity of the infection and in clinical decision making.</p><p id="par0100" class="elsevierStylePara elsevierViewall">One of the main limitations of the study was that the methodology for testing BP could have influenced the results, as we did not test BP in parallel with the metabolic activity of <span class="elsevierStyleItalic">Candida</span> biofilms. Moreover, as the methodologies differ between studies, the results may not be comparable. Another limitation was that we could not compare the differences between species according to the clinical specimens because of the small numbers of isolates in the subgroups. However, our study is the first in which <span class="elsevierStyleItalic">Candida</span> species isolated from several clinical samples are classified according to the degree of BP and in which BP was evaluated according to species of <span class="elsevierStyleItalic">Candida</span> and type of clinical specimens. Research is currently under way in studies based on the XTT assay and larger samples.</p><p id="par0105" class="elsevierStylePara elsevierViewall">Our data demonstrate that BP varies according to the <span class="elsevierStyleItalic">Candida</span> species and the site of the infection. Consequently, the capacity of <span class="elsevierStyleItalic">Candida</span> species to produce biofilm may be a reflection of the pathogenic potential of the isolates.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Financial support</span><p id="par0110" class="elsevierStylePara elsevierViewall">M. Guembe is supported by the Miguel Servet Program (ISCIII-MICINN) from the Health Research Fund (FIS), of the Carlos III Health Institute (ISCIII), Madrid Spain, partially financed by the by the European Regional Development Fund (FEDER) “A way of making Europe”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflicts of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">The authors declare no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres816336" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec813574" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres816335" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec813573" "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" => "Laboratory procedure" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Statistical analysis" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Ethics" ] ] ] 6 => array:2 [ "identificador" => "sec0030" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0035" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0040" "titulo" => "Financial support" ] 9 => array:2 [ "identificador" => "sec0045" "titulo" => "Conflicts of interest" ] 10 => array:2 [ "identificador" => "xack273980" "titulo" => "Acknowledgement" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-12-29" "fechaAceptado" => "2016-04-02" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec813574" "palabras" => array:5 [ 0 => "<span class="elsevierStyleItalic">Candida</span>" 1 => "Biofilm production" 2 => "Clinical samples" 3 => "Crystal violet binding assay" 4 => "Cut-off" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec813573" "palabras" => array:5 [ 0 => "<span class="elsevierStyleItalic">Candida</span>" 1 => "Producción de biopelícula" 2 => "Muestras clínicas" 3 => "Tinción cristal violeta" 4 => "Punto de corte" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The biofilm production (BP) of 200 clinical strains of <span class="elsevierStyleItalic">Candida</span> isolated during 2010–2013 were assessed using an in vitro model and a comparison of the results was made between species and between origins of the infections. The BP was assessed using the crystal violet assay, and the strains were classified as low, moderate, or high biofilm producers. <span class="elsevierStyleItalic">Candida tropicalis</span> had the highest values for BP, which varied depending on the origin of the infection. Assessment of BP is a key diagnostic tool that enables us to better understand <span class="elsevierStyleItalic">Candida</span> infections.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Desde 2010 a 2013 evaluamos la producción de biopelícula (PB) en 200 cepas clínicas de <span class="elsevierStyleItalic">Candida</span> y comparamos los resultados de las especies de <span class="elsevierStyleItalic">Candida</span> entre los orígenes de la infección mediante un modelo in vitro. La PB se determinó con el ensayo de cristal violeta y las cepas se clasificaron como baja, moderada o altamente productoras de biopelícula. <span class="elsevierStyleItalic">C. tropicalis</span> tuvo los valores más altos de PB, y la PB en <span class="elsevierStyleItalic">Candida</span> varió dependiendo del origen de la infección. La determinación de la PB es una herramienta diagnóstica importante para entender mejor las infecciones por <span class="elsevierStyleItalic">Candida</span>.</p></span>" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1304 "Ancho" => 1640 "Tamanyo" => 94483 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Comparison of biofilm production between <span class="elsevierStyleItalic">Candida</span> species.</p>" ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:3 [ "leyenda" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">BP, biofilm production; SD, standard deviation.</p>" "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"><th class="td" title="table-head " rowspan="2" align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Specie (<span class="elsevierStyleItalic">n</span>, %)</th><th class="td" title="table-head " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">BP</th><th class="td" title="table-head " rowspan="2" align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span></th></tr><tr title="table-row"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Mean (SD) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Low<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a><span class="elsevierStyleItalic">N</span> (%) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Moderate<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a><span class="elsevierStyleItalic">N</span> (%) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">High<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a><span class="elsevierStyleItalic">N</span> (%) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><0.001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C. albicans</span> (41, 20.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.8 (0.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 (7.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">19 (46.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">19 (46.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C. parapsilosis</span> (40, 20.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.3 (0.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15 (37.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 (35.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11 (27.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C. krusei</span> (40, 20.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.4 (0.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">37 (92.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 (7.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 (0.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C. glabrata</span> (39, 19.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.3 (0.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">36 (92.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 (7.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 (0.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C. tropicalis</span> (22, 11.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.4 (0.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (4.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 (22.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">16 (72.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C. guilliermondii</span> (18, 9.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.6 (0.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 (77.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 (22.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 (0.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="6" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="6" align="left" valign="top"><span class="elsevierStyleItalic">Clinical specimens (n, %)</span></td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><0.001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Urine (33, 16.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.8 (0.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21 (63.6) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 (27.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 (9.1) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Biopsy (28, 14.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.5 (0.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 (28.6) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10 (35.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10 (35.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Respiratory tract (26, 13.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.4 (0.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">24 (92.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (3.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (3.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Blood (24, 12.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.4 (0.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 (33.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 (33.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 (33.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Normally sterile fluids (18, 9.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.6 (1.1) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6 (33.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 (22.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 (44.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Wound (13, 6.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.9 (0.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 (69.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 (23.1) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (7.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Abscess (10, 5.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.3 (1.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 (50.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 (20.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 (30.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Catheter (8, 4.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 (0.6) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 (25.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 (25.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 (50.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Prosthetic material (3, 1.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.8 (0.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 (0.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 (66.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (33.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Other (37, 18.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.9 (0.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">23 (62.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7 (18.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7 (18.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="6" align="left" valign="top"><span class="elsevierStyleVsp" style="height:1.0px"></span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Total (200)</span> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">106 (53.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">48 (24.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">46 (23.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1372006.png" ] ] ] "notaPie" => array:3 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Low, <1.</p>" ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Moderate, 1–2.</p>" ] 2 => array:3 [ "identificador" => "tblfn0015" "etiqueta" => "c" "nota" => "<p class="elsevierStyleNotepara" id="npar0015">High, >2.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Description of biofilm production according to <span class="elsevierStyleItalic">Candida</span> spp. and clinical specimens.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:12 [ 0 => array:3 [ "identificador" => "bib0070" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Clinical Practice Guideline for the Management of Candidiasis: 2016 update by the Infectious Diseases Society of America" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "P.G. 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Donlan" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.3201/eid0809.020063" "Revista" => array:6 [ "tituloSerie" => "Emerg Infect Dis" "fecha" => "2002" "volumen" => "8" "paginaInicial" => "881" "paginaFinal" => "890" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12194761" "web" => "Medline" ] ] ] ] ] ] ] ] 10 => array:3 [ "identificador" => "bib0120" "etiqueta" => "11" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Differences in biofilm production by three genotypes of <span class="elsevierStyleItalic">Candida parapsilosis</span> from clinical sources" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "J.W. Song" 1 => "J.H. Shin" 2 => "D.H. Shint" 3 => "S.I. Jung" 4 => "D. Cho" 5 => "S.J. Kee" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Med Mycol" "fecha" => "2005" "volumen" => "43" "paginaInicial" => "657" "paginaFinal" => "661" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/16396252" "web" => "Medline" ] ] ] ] ] ] ] ] 11 => array:3 [ "identificador" => "bib0125" "etiqueta" => "12" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Biofilm production by isolates of <span class="elsevierStyleItalic">Candida</span> species recovered from nonneutropenic patients: comparison of bloodstream isolates with isolates from other sources" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "J.H. Shin" 1 => "S.J. Kee" 2 => "M.G. Shin" 3 => "S.H. Kim" 4 => "D.H. Shin" 5 => "S.K. Lee" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "J Clin Microbiol" "fecha" => "2002" "volumen" => "40" "paginaInicial" => "1244" "paginaFinal" => "1248" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/11923339" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack273980" "titulo" => "Acknowledgement" "texto" => "<p id="par0130" class="elsevierStylePara elsevierViewall">We thank Thomas O’Boyle for his help in the preparation of the manuscript.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/2529993X/0000003500000001/v2_201703180226/S2529993X17300138/v2_201703180226/en/main.assets" "Apartado" => array:4 [ "identificador" => "63561" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Brief report" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/2529993X/0000003500000001/v2_201703180226/S2529993X17300138/v2_201703180226/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S2529993X17300138?idApp=UINPBA00004N" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 1 | 2 | 3 |
| 2024 October | 7 | 2 | 9 |
| 2024 September | 22 | 7 | 29 |
| 2024 August | 22 | 1 | 23 |
| 2024 July | 18 | 2 | 20 |
| 2024 June | 17 | 2 | 19 |
| 2024 May | 15 | 8 | 23 |
| 2024 April | 17 | 8 | 25 |
| 2024 March | 22 | 10 | 32 |
| 2024 February | 20 | 2 | 22 |
| 2024 January | 9 | 3 | 12 |
| 2023 December | 16 | 5 | 21 |
| 2023 November | 25 | 4 | 29 |
| 2023 October | 32 | 3 | 35 |
| 2023 September | 12 | 1 | 13 |
| 2023 August | 21 | 2 | 23 |
| 2023 July | 12 | 5 | 17 |
| 2023 June | 4 | 3 | 7 |
| 2023 May | 18 | 6 | 24 |
| 2023 April | 7 | 8 | 15 |
| 2023 March | 16 | 7 | 23 |
| 2023 February | 17 | 3 | 20 |
| 2023 January | 7 | 44 | 51 |
| 2022 December | 22 | 9 | 31 |
| 2022 November | 18 | 14 | 32 |
| 2022 October | 18 | 12 | 30 |
| 2022 September | 13 | 6 | 19 |
| 2022 August | 15 | 10 | 25 |
| 2022 July | 17 | 12 | 29 |
| 2022 June | 19 | 10 | 29 |
| 2022 May | 32 | 6 | 38 |
| 2022 April | 22 | 16 | 38 |
| 2022 March | 16 | 5 | 21 |
| 2022 February | 11 | 4 | 15 |
| 2022 January | 23 | 7 | 30 |
| 2021 December | 47 | 12 | 59 |
| 2021 November | 17 | 10 | 27 |
| 2021 October | 21 | 18 | 39 |
| 2021 September | 18 | 13 | 31 |
| 2021 August | 19 | 8 | 27 |
| 2021 July | 12 | 11 | 23 |
| 2021 June | 17 | 12 | 29 |
| 2021 May | 33 | 6 | 39 |
| 2021 April | 26 | 14 | 40 |
| 2021 March | 18 | 14 | 32 |
| 2021 February | 23 | 4 | 27 |
| 2021 January | 28 | 12 | 40 |
| 2020 December | 17 | 4 | 21 |
| 2020 November | 14 | 9 | 23 |
| 2020 October | 11 | 5 | 16 |
| 2020 September | 14 | 9 | 23 |
| 2020 August | 12 | 9 | 21 |
| 2020 July | 26 | 5 | 31 |
| 2020 June | 23 | 10 | 33 |
| 2020 May | 13 | 9 | 22 |
| 2020 April | 13 | 6 | 19 |
| 2020 March | 10 | 2 | 12 |
| 2020 February | 26 | 11 | 37 |
| 2020 January | 16 | 6 | 22 |
| 2019 December | 13 | 12 | 25 |
| 2019 November | 8 | 8 | 16 |
| 2019 October | 18 | 12 | 30 |
| 2019 September | 12 | 3 | 15 |
| 2019 August | 7 | 3 | 10 |
| 2019 July | 15 | 9 | 24 |
| 2019 June | 18 | 13 | 31 |
| 2019 May | 40 | 17 | 57 |
| 2019 April | 11 | 9 | 20 |
| 2019 March | 10 | 3 | 13 |
| 2019 February | 25 | 7 | 32 |
| 2019 January | 13 | 5 | 18 |
| 2018 December | 2 | 4 | 6 |
| 2018 November | 3 | 4 | 7 |
| 2018 October | 26 | 8 | 34 |
| 2018 September | 9 | 1 | 10 |
| 2018 August | 4 | 1 | 5 |
| 2018 July | 12 | 2 | 14 |
| 2018 June | 11 | 3 | 14 |
| 2018 May | 10 | 1 | 11 |
| 2018 April | 8 | 1 | 9 |
| 2018 March | 11 | 0 | 11 |
| 2018 February | 8 | 1 | 9 |
| 2018 January | 9 | 0 | 9 |
| 2017 December | 15 | 0 | 15 |
| 2017 November | 16 | 0 | 16 |
| 2017 October | 21 | 1 | 22 |
| 2017 September | 19 | 2 | 21 |
| 2017 August | 6 | 0 | 6 |
| 2017 July | 2 | 2 | 4 |
| 2017 February | 42 | 16 | 58 |
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