Scientific Letter
Lymphopenic hospital acquired sepsis (L-HAS): An immunological phenotype conferring higher risk of mortality
Sepsis nosocomial linfopénica: un fenotipo inmunológico que confiere un mayor riesgo de mortalidad
C. López-Mestanzaa,
, D. Andaluz-Ojedab, J.R. Gómez-Lópezc, J.F. Bermejo-Martína
Autor para correspondencia
a BIO SEPSIS (Group of Biomedical Research in Sepsis), Hospital Clínico Universitario de Valladolid, SACYL, Valladolid, Spain
b Critical Care Medicine Service, Hospital Clínico Universitario de Valladolid, Valladolid, Spain
c General Surgery Service, Hospital de Medina del Campo, SACYL, Medina del Campo-Valladolid, Spain
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López-Mestanza, D. Andaluz-Ojeda, J.R. Gómez-López, J.F. Bermejo-Martín" "autores" => array:4 [ 0 => array:4 [ "nombre" => "C." "apellidos" => "López-Mestanza" "email" => array:1 [ 0 => "xtina.lopez.mestanza@hotmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "D." "apellidos" => "Andaluz-Ojeda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "J.R." "apellidos" => "Gómez-López" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] 3 => array:3 [ "nombre" => "J.F." "apellidos" => "Bermejo-Martín" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "BIO SEPSIS (Group of Biomedical Research in Sepsis), Hospital Clínico Universitario de Valladolid, SACYL, Valladolid, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Critical Care Medicine Service, Hospital Clínico Universitario de Valladolid, Valladolid, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "General Surgery Service, Hospital de Medina del Campo, SACYL, Medina del Campo-Valladolid, Spain" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Sepsis nosocomial linfopénica: un fenotipo inmunológico que confiere un mayor riesgo de mortalidad" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1386 "Ancho" => 1583 "Tamanyo" => 63336 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Kaplan–Meier survival curve. Groups were compared by the log rank test (Mantel–Henzel). Circulating Lymphocyte Count (CLC) at HAS diagnosis were divided in two groups, ≤775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span> and greater. Time was censored at 90 days following HAS diagnosis. Cum: cumulative.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">The clinical profile of Hospital Acquired Sepsis (HAS) is poorly known. In a recent work,<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> we found that patients suffering from HAS show many of the risk factors associated with cardiovascular disease and cancer.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Lymphopenia is a frequent finding in sepsis patients.<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2–4</span></a> Sepsis affects the immune system by directly altering the lifespan, production and function of the effector cells responsible for homeostasis.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> Lymphopenia is also found in other severe infections like pneumonia needing of hospitalization, and it is associated to an increased risk of mortality.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The impact of lymphocyte counts on the prognosis of patients with HAS is unknown. The objective of the present study was to evaluate the association between lymphocyte counts and mortality risk of the patients suffering from HAS. The predictive ability of the other leukocyte subpopulations was also assessed.</p><p id="par0020" class="elsevierStylePara elsevierViewall">The study was approved by the Clinical Research and Ethics Committee of our hospital. Informed consent was waived due to the observational nature of the study.</p><p id="par0025" class="elsevierStylePara elsevierViewall">A total of 196 patients were included in the study. Hospital and 90 days mortality was 45.4%. The median age of HAS patients was of 73 years (IQR: 68.1–71.4), with 68.4% (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>134) of them being male. Some serious comorbidities were: cardiac disease 63.8% (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>125), cancer 34.2% (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>67), chronic kidney disease 19.4% (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>38), immunosuppression 17.9% (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>35) and chronic hepatic disease 6.1% (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>12) (Supplementary Table 1). Sepsis with organ failure (severe sepsis/septic shock) was present in 146 patients (74.5%) with 75 of these patients dying during the first 90 days.</p><p id="par0030" class="elsevierStylePara elsevierViewall">HAS emerged 10 days following hospital admission in median (IQR, 11.4–14.5). The most frequent source of infection was the respiratory tract (29.1%), followed by bacteraemia (25%) (Supplementary Table 1). Microorganisms were isolated in one hundred and fifty patients (76.5%). Gram negative bacteria were the most common microorganisms (58.6%), followed by Gram positive cocci (46.0%).</p><p id="par0035" class="elsevierStylePara elsevierViewall">We collected leukocyte subpopulations counts at hospital admission and also at HAS diagnosis. Patients with HAS showed a significant increase in the median values of neutrophil counts from admission to diagnosis: (5.3 [4.00–7.4]<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>/mm<span class="elsevierStyleSup">3</span>) <span class="elsevierStyleItalic">vs</span> (10.9 [6.5–17.0]<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>/mm<span class="elsevierStyleSup">3</span>) <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001. On the contrary, median values of eosinophil and lymphocyte counts decreased from admission to diagnosis: (0.11 [0.04–0.22]<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>/mm<span class="elsevierStyleSup">3</span>) <span class="elsevierStyleItalic">vs</span> (0.02 [0.00–0.11]<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>/mm<span class="elsevierStyleSup">3</span>) for eosinophils and (1.6 [1.0–2.3]<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>0<span class="elsevierStyleSup">3</span>/mm<span class="elsevierStyleSup">3</span>) <span class="elsevierStyleItalic">vs</span> (0.8 [0.4–1.3]<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>/mm<span class="elsevierStyleSup">3</span>]) for lymphocytes (with differences yielding a <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001 in both cases). Median values of monocytes and basophil counts did not change in a significant manner between both moments.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Median values of lymphocytes at HAS diagnosis were higher in survivors than in non survivors. Survivors showed also higher median values of eosinophils at HAS diagnosis than non survivors. On the contrary, monocyte, basophil and neutrophil counts did not show differences between both groups (Supplementary Table 1).</p><p id="par0045" class="elsevierStylePara elsevierViewall">Lymphocytes and eosinophil counts at HAS diagnosis showed significant AUCs for identifying survivors at hospital discharge (Supplementary Fig. 1), with an (AUC [CI95%], <span class="elsevierStyleItalic">p</span>) of (0.59 [0.59–0.67], 0.042) and (0.60 [0.52–0.68], 0.023) respectively. Other leukocyte subtypes failed to discriminate survivors from non survivors. The optimal operating point (OOP) was calculated for those leukocyte subpopulations showing an AUC <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.05 as previously described<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">7</span></a> for distinguishing between both kinds of patients in the AUC analysis was 775<span class="elsevierStyleHsp" style=""></span>cells/mm<span class="elsevierStyleSup">3</span> for lymphocytes and 13<span class="elsevierStyleHsp" style=""></span>cells/mm<span class="elsevierStyleSup">3</span> for eosinophils.</p><p id="par0050" class="elsevierStylePara elsevierViewall">Categorical variables were created based on the OOPs and the resulting variables for lymphocyte and eosinophil counts were evaluated for hospital mortality prediction using multivariate analysis adjusting by the potential confounding factors selected in the univariate analysis: [Age(years)], [Sex(male)], [“Sepsis code” implemented], [antecedent of vascular disease], [antecedent of cancer], [antecedent of chronic kidney disease], [sepsis with organ failure], [more than one episode of sepsis during hospital admission], [surgical intervention] and [time (days) from admission to sepsis diagnosis]. The presence of a lymphocyte count ≤775<span class="elsevierStyleHsp" style=""></span>cells/mm<span class="elsevierStyleSup">3</span> at diagnosis of HAS was an independent predictor of mortality in the multivariate analysis: (1.98 [1.00–3.92], <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.049) (OR 1.98 [CI 95% 1.00–3.92], <span class="elsevierStyleItalic">p</span> = 0.049) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). In turn, showing a eosinophil count ≤13<span class="elsevierStyleHsp" style=""></span>cells/mm<span class="elsevierStyleSup">3</span> at diagnosis of HAS conferred a non-significant higher risk of mortality (1.87 [0.95–3.70], <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.072). Finally, the Kaplan–Meier curves at 90 days following diagnosis of HAS showed that patients with ≤775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span> died earlier (media 48.6 days [40.3–56.8]) than patients with >775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span> (media 60.5 [53.1–67.9]), <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.030 (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">HAS was characterized by a significant increase in the blood counts of the paradigmatic cell representing innate immunity, the neutrophil, accompanied by a decrease in the prototypic cell of the adaptive immunity, the lymphocyte. Neutrophil count expansion could represent a kind of compensatory mechanism responding to the decrease in the lymphocyte counts, which precedes the emergence of HAS. The significant decrease in lymphocyte counts found from admission to diagnosis of HAS cannot be explained by hemodilution due to fluid administration, since counts of the other leukocyte subsets were not affected. In consequence, this is the first report providing evidence that sepsis does induce diminution of lymphocyte counts in blood.</p><p id="par0060" class="elsevierStylePara elsevierViewall">Early identification of patients at risk of death is a crucial step in the clinical management of sepsis.<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">8–10</span></a> In this regard, this study provides a cut-off value for lymphocyte counts (≤775<span class="elsevierStyleHsp" style=""></span>cells/mm<span class="elsevierStyleSup">3</span>) which is useful for the early identification of those patients at higher risk of mortality, independently of their accompanying co-morbidities (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Also we repeat analysis excluding immunosuppressed patients and we found that those patients with ≤775 lymphocytes/mm<span class="elsevierStyleSup">3</span> continue presenting higher risk to mortality.</p><p id="par0065" class="elsevierStylePara elsevierViewall">Lymphocyte counting is a simple and inexpensive test, widely available in most hospital settings. In our study, the eosinophil count at diagnosis of HAS conferred a nonsignificant higher risk of mortality. Some limitations of our work were its retrospective nature, the absence of some variables like the albumin levels or severity scores like SOFA or APACHE.</p><p id="par0070" class="elsevierStylePara elsevierViewall">In conclusion, lymphopenic HAS (L-HAS) (≤775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span>) constitutes a particular immunological phenotype of the disease conferring a two-fold increase in the risk of hospital mortality. Patients with L-HAS deserve special care and close monitoring of vital signs.</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Conflict of interest</span><p id="par0075" class="elsevierStylePara elsevierViewall">None.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Funding</span><p id="par0080" class="elsevierStylePara elsevierViewall">This research did not received any specific grant from funding agencies in the public, commercial or not-for-profit sectors. Salaries from the authors are paid by the “Consejería de Sanidad de Castilla y León, Spain”.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflict of interest" ] 1 => array:2 [ "identificador" => "sec0010" "titulo" => "Funding" ] 2 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005"><span class="elsevierStyleItalic">Institution where the work was done</span>: Hospital Clínico Universitario de Valladolid, Av. Ramón y Cajal, 3, 47003, Valladolid, Spain.</p>" ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "<p id="par0090" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0020" ] ] ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1386 "Ancho" => 1583 "Tamanyo" => 63336 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Kaplan–Meier survival curve. Groups were compared by the log rank test (Mantel–Henzel). Circulating Lymphocyte Count (CLC) at HAS diagnosis were divided in two groups, ≤775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span> and greater. Time was censored at 90 days following HAS diagnosis. Cum: cumulative.</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:2 [ "leyenda" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">OR: odds ratio; CI: confidence interval.</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-with-role" title="\n \t\t\t\t\ttable-head\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col">Variables \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="3" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Hospital mortality</th></tr><tr title="table-row"><th 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" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th 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" scope="col" style="border-bottom: 2px solid black">OR \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th 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" scope="col" style="border-bottom: 2px solid black">(95% CI) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th 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" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span> \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Age (years) \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">1.034 \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">[1.002–1.067] \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">0.040 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Sex (male) \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">2.067 \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">[0.978–4.369] \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">0.057 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">“Sepsis Code” implemented \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">0.583 \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">[0.294–1.157] \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">0.123 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Vascular disease \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">1.419 \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">[0.650–3.096] \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">0.380 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Cancer \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">1.385 \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">[0.680–2.818] \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">0.369 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Chronic kidney disease \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">1.693 \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">[0.713–4.021] \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">0.233 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Sepsis with organ failure \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">4.687 \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">[1.889–11.629] \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">0.001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">More than one episode of sepsis during hospital admission \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">3.346 \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">[1.529–7.324] \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">0.003 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Time (days) from admission to sepsis diagnosis \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">1.036 \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">[1.000–1.074] \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">0.050 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Surgical intervention \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">0.316 \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">[0.144–0.696] \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">0.004 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">≤775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span> \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">1.983 \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">[1.004–3.919] \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">0.049 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2149228.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Multivariate regression analysis to predict hospital mortality risk in patients with ≤775<span class="elsevierStyleHsp" style=""></span>lymphocytes/mm<span class="elsevierStyleSup">3</span> at diagnosis of HAS.</p>" ] ] 2 => array:5 [ "identificador" => "upi0005" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "Ecomponente" => array:2 [ "fichero" => "mmc1.pdf" "ficheroTamanyo" => 86921 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:10 [ 0 => array:3 [ "identificador" => "bib0055" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Clinical factors influencing mortality risk in hospital-acquired sepsis" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "C. 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| año/Mes | Html | Total | |
|---|---|---|---|
| 2024 Noviembre | 7 | 11 | 18 |
| 2024 Octubre | 49 | 72 | 121 |
| 2024 Septiembre | 48 | 41 | 89 |
| 2024 Agosto | 40 | 26 | 66 |
| 2024 Julio | 49 | 41 | 90 |
| 2024 Junio | 58 | 57 | 115 |
| 2024 Mayo | 50 | 39 | 89 |
| 2024 Abril | 46 | 49 | 95 |
| 2024 Marzo | 45 | 26 | 71 |
| 2024 Febrero | 36 | 43 | 79 |
| 2024 Enero | 38 | 32 | 70 |
| 2023 Diciembre | 26 | 34 | 60 |
| 2023 Noviembre | 51 | 61 | 112 |
| 2023 Octubre | 39 | 26 | 65 |
| 2023 Septiembre | 42 | 37 | 79 |
| 2023 Agosto | 36 | 16 | 52 |
| 2023 Julio | 41 | 23 | 64 |
| 2023 Junio | 28 | 16 | 44 |
| 2023 Mayo | 46 | 36 | 82 |
| 2023 Abril | 29 | 21 | 50 |
| 2023 Marzo | 45 | 36 | 81 |
| 2023 Febrero | 51 | 29 | 80 |
| 2023 Enero | 32 | 20 | 52 |
| 2022 Diciembre | 80 | 37 | 117 |
| 2022 Noviembre | 50 | 33 | 83 |
| 2022 Octubre | 56 | 35 | 91 |
| 2022 Septiembre | 46 | 36 | 82 |
| 2022 Agosto | 42 | 44 | 86 |
| 2022 Julio | 41 | 49 | 90 |
| 2022 Junio | 34 | 41 | 75 |
| 2022 Mayo | 50 | 48 | 98 |
| 2022 Abril | 42 | 27 | 69 |
| 2022 Marzo | 48 | 40 | 88 |
| 2022 Febrero | 48 | 35 | 83 |
| 2022 Enero | 40 | 42 | 82 |
| 2021 Diciembre | 40 | 52 | 92 |
| 2021 Noviembre | 45 | 38 | 83 |
| 2021 Octubre | 58 | 70 | 128 |
| 2021 Septiembre | 27 | 36 | 63 |
| 2021 Agosto | 30 | 37 | 67 |
| 2021 Julio | 24 | 35 | 59 |
| 2021 Junio | 43 | 30 | 73 |
| 2021 Mayo | 52 | 54 | 106 |
| 2021 Abril | 102 | 118 | 220 |
| 2021 Marzo | 97 | 21 | 118 |
| 2021 Febrero | 82 | 24 | 106 |
| 2021 Enero | 75 | 19 | 94 |
| 2020 Diciembre | 77 | 10 | 87 |
| 2020 Noviembre | 34 | 17 | 51 |
| 2020 Octubre | 19 | 15 | 34 |
| 2020 Septiembre | 0 | 0 | 0 |
| 2020 Julio | 28 | 17 | 45 |
| 2020 Junio | 43 | 19 | 62 |
| 2020 Mayo | 35 | 10 | 45 |
| 2020 Abril | 42 | 7 | 49 |
| 2020 Marzo | 32 | 10 | 42 |
| 2020 Febrero | 41 | 21 | 62 |
| 2020 Enero | 0 | 0 | 0 |
| 2019 Diciembre | 4 | 0 | 4 |
| 2019 Noviembre | 5 | 4 | 9 |
| 2019 Octubre | 3 | 0 | 3 |
| 2019 Septiembre | 2 | 2 | 4 |
| 2019 Julio | 0 | 2 | 2 |
| 2019 Junio | 0 | 0 | 0 |
| 2019 Mayo | 0 | 2 | 2 |
| 2019 Abril | 0 | 5 | 5 |
| 2019 Marzo | 0 | 4 | 4 |
| 2019 Febrero | 0 | 1 | 1 |
| 2019 Enero | 0 | 2 | 2 |
| 2018 Diciembre | 9 | 4 | 13 |
| 2018 Noviembre | 9 | 2 | 11 |
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