Lymphopenic hospital acquired sepsis (L-HAS): An immunological phenotype conferring higher risk of mortality

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Escudero-Acha, A. González-Castro, Y. Peñasco, M. Feo-Gonzalez" "autores" => array:4 [ 0 => array:2 [ "nombre" => "P." "apellidos" => "Escudero-Acha" ] 1 => array:2 [ "nombre" => "A." "apellidos" => "González-Castro" ] 2 => array:2 [ "nombre" => "Y." "apellidos" => "Peñasco" ] 3 => array:2 [ "nombre" => "M." 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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" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "D." "apellidos" => "Andaluz-Ojeda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "J.R." "apellidos" => "Gómez-López" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] 3 => array:3 [ "nombre" => "J.F." "apellidos" => "Bermejo-Martín" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "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" => "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, ≤775lymphocytes/mm3 and greater. Time was censored at 90 days following HAS diagnosis. Cum: cumulative." ] ] ] "textoCompleto" => "The clinical profile of Hospital Acquired Sepsis (HAS) is poorly known. In a recent work,<a class="elsevierStyleCrossRef" href="#bib0055">1</a> we found that patients suffering from HAS show many of the risk factors associated with cardiovascular disease and cancer.Lymphopenia is a frequent finding in sepsis patients.<a class="elsevierStyleCrossRefs" href="#bib0060">2–4</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">5</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">6</a>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.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.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% (n=134) of them being male. Some serious comorbidities were: cardiac disease 63.8% (n=125), cancer 34.2% (n=67), chronic kidney disease 19.4% (n=38), immunosuppression 17.9% (n=35) and chronic hepatic disease 6.1% (n=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.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%).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]×103/mm3) vs (10.9 [6.5–17.0]×103/mm3) p<0.001. On the contrary, median values of eosinophil and lymphocyte counts decreased from admission to diagnosis: (0.11 [0.04–0.22]×103/mm3) vs (0.02 [0.00–0.11]×103/mm3) for eosinophils and (1.6 [1.0–2.3]×03/mm3) vs (0.8 [0.4–1.3]×103/mm3]) for lymphocytes (with differences yielding a p<0.001 in both cases). Median values of monocytes and basophil counts did not change in a significant manner between both moments.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).Lymphocytes and eosinophil counts at HAS diagnosis showed significant AUCs for identifying survivors at hospital discharge (Supplementary Fig. 1), with an (AUC [CI95%], p) 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 p<0.05 as previously described<a class="elsevierStyleCrossRef" href="#bib0085">7</a> for distinguishing between both kinds of patients in the AUC analysis was 775cells/mm3 for lymphocytes and 13cells/mm3 for eosinophils.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 ≤775cells/mm3 at diagnosis of HAS was an independent predictor of mortality in the multivariate analysis: (1.98 [1.00–3.92], p=0.049) (OR 1.98 [CI 95% 1.00–3.92], p = 0.049) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). In turn, showing a eosinophil count ≤13cells/mm3 at diagnosis of HAS conferred a non-significant higher risk of mortality (1.87 [0.95–3.70], p=0.072). Finally, the Kaplan–Meier curves at 90 days following diagnosis of HAS showed that patients with ≤775lymphocytes/mm3 died earlier (media 48.6 days [40.3–56.8]) than patients with >775lymphocytes/mm3 (media 60.5 [53.1–67.9]), p=0.030 (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).<elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia>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.Early identification of patients at risk of death is a crucial step in the clinical management of sepsis.<a class="elsevierStyleCrossRefs" href="#bib0090">8–10</a> In this regard, this study provides a cut-off value for lymphocyte counts (≤775cells/mm3) 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/mm3 continue presenting higher risk to mortality.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.In conclusion, lymphopenic HAS (L-HAS) (≤775lymphocytes/mm3) 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.Conflict of interestNone.FundingThis 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”." "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" => "Institution where the work was done: Hospital Clínico Universitario de Valladolid, Av. Ramón y Cajal, 3, 47003, Valladolid, Spain." ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "The following are the supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia>" "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" => "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, ≤775lymphocytes/mm3 and greater. Time was censored at 90 days following HAS diagnosis. Cum: cumulative." ] ] 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" => "OR: odds ratio; CI: confidence interval." "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">p \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">≤775lymphocytes/mm3 \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 => "xTab2151937.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Multivariate regression analysis to predict hospital mortality risk in patients with ≤775lymphocytes/mm3 at diagnosis of HAS." ] ] 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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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,

Corresponding author

xtina.lopez.mestanza@hotmail.com

Corresponding author.

, D. Andaluz-Ojedab, J.R. Gómez-Lópezc, J.F. Bermejo-Martína

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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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">The clinical profile of Hospital Acquired Sepsis &#40;HAS&#41; is poorly known&#46; In a recent work&#44;<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&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Lymphopenia is a frequent finding in sepsis patients&#46;<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2&#8211;4</span></a> Sepsis affects the immune system by directly altering the lifespan&#44; production and function of the effector cells responsible for homeostasis&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> Lymphopenia is also found in other severe infections like pneumonia needing of hospitalization&#44; and it is associated to an increased risk of mortality&#46;<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&#46; The objective of the present study was to evaluate the association between lymphocyte counts and mortality risk of the patients suffering from HAS&#46; The predictive ability of the other leukocyte subpopulations was also assessed&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The study was approved by the Clinical Research and Ethics Committee of our hospital&#46; Informed consent was waived due to the observational nature of the study&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">A total of 196 patients were included in the study&#46; Hospital and 90 days mortality was 45&#46;4&#37;&#46; The median age of HAS patients was of 73 years &#40;IQR&#58; 68&#46;1&#8211;71&#46;4&#41;&#44; with 68&#46;4&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>134&#41; of them being male&#46; Some serious comorbidities were&#58; cardiac disease 63&#46;8&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>125&#41;&#44; cancer 34&#46;2&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>67&#41;&#44; chronic kidney disease 19&#46;4&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>38&#41;&#44; immunosuppression 17&#46;9&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>35&#41; and chronic hepatic disease 6&#46;1&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>12&#41; &#40;Supplementary Table 1&#41;&#46; Sepsis with organ failure &#40;severe sepsis&#47;septic shock&#41; was present in 146 patients &#40;74&#46;5&#37;&#41; with 75 of these patients dying during the first 90 days&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">HAS emerged 10 days following hospital admission in median &#40;IQR&#44; 11&#46;4&#8211;14&#46;5&#41;&#46; The most frequent source of infection was the respiratory tract &#40;29&#46;1&#37;&#41;&#44; followed by bacteraemia &#40;25&#37;&#41; &#40;Supplementary Table 1&#41;&#46; Microorganisms were isolated in one hundred and fifty patients &#40;76&#46;5&#37;&#41;&#46; Gram negative bacteria were the most common microorganisms &#40;58&#46;6&#37;&#41;&#44; followed by Gram positive cocci &#40;46&#46;0&#37;&#41;&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">We collected leukocyte subpopulations counts at hospital admission and also at HAS diagnosis&#46; Patients with HAS showed a significant increase in the median values of neutrophil counts from admission to diagnosis&#58; &#40;5&#46;3 &#91;4&#46;00&#8211;7&#46;4&#93;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>&#47;mm<span class="elsevierStyleSup">3</span>&#41; <span class="elsevierStyleItalic">vs</span> &#40;10&#46;9 &#91;6&#46;5&#8211;17&#46;0&#93;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>&#47;mm<span class="elsevierStyleSup">3</span>&#41; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#46; On the contrary&#44; median values of eosinophil and lymphocyte counts decreased from admission to diagnosis&#58; &#40;0&#46;11 &#91;0&#46;04&#8211;0&#46;22&#93;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>&#47;mm<span class="elsevierStyleSup">3</span>&#41; <span class="elsevierStyleItalic">vs</span> &#40;0&#46;02 &#91;0&#46;00&#8211;0&#46;11&#93;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>&#47;mm<span class="elsevierStyleSup">3</span>&#41; for eosinophils and &#40;1&#46;6 &#91;1&#46;0&#8211;2&#46;3&#93;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>0<span class="elsevierStyleSup">3</span>&#47;mm<span class="elsevierStyleSup">3</span>&#41; <span class="elsevierStyleItalic">vs</span> &#40;0&#46;8 &#91;0&#46;4&#8211;1&#46;3&#93;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">3</span>&#47;mm<span class="elsevierStyleSup">3</span>&#93;&#41; for lymphocytes &#40;with differences yielding a <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001 in both cases&#41;&#46; Median values of monocytes and basophil counts did not change in a significant manner between both moments&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Median values of lymphocytes at HAS diagnosis were higher in survivors than in non survivors&#46; Survivors showed also higher median values of eosinophils at HAS diagnosis than non survivors&#46; On the contrary&#44; monocyte&#44; basophil and neutrophil counts did not show differences between both groups &#40;Supplementary Table 1&#41;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Lymphocytes and eosinophil counts at HAS diagnosis showed significant AUCs for identifying survivors at hospital discharge &#40;Supplementary Fig&#46; 1&#41;&#44; with an &#40;AUC &#91;CI95&#37;&#93;&#44; <span class="elsevierStyleItalic">p</span>&#41; of &#40;0&#46;59 &#91;0&#46;59&#8211;0&#46;67&#93;&#44; 0&#46;042&#41; and &#40;0&#46;60 &#91;0&#46;52&#8211;0&#46;68&#93;&#44; 0&#46;023&#41; respectively&#46; Other leukocyte subtypes failed to discriminate survivors from non survivors&#46; 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&#91;Age&#40;years&#41;&#93;&#44; &#91;Sex&#40;male&#41;&#93;&#44; &#91;&#8220;Sepsis code&#8221; implemented&#93;&#44; &#91;antecedent of vascular disease&#93;&#44; &#91;antecedent of cancer&#93;&#44; &#91;antecedent of chronic kidney disease&#93;&#44; &#91;sepsis with organ failure&#93;&#44; &#91;more than one episode of sepsis during hospital admission&#93;&#44; &#91;surgical intervention&#93; and &#91;time &#40;days&#41; from admission to sepsis diagnosis&#93;&#46; The presence of a lymphocyte count &#8804;775<span class="elsevierStyleHsp" style=""></span>cells&#47;mm<span class="elsevierStyleSup">3</span> at diagnosis of HAS was an independent predictor of mortality in the multivariate analysis&#58; &#40;1&#46;98 &#91;1&#46;00&#8211;3&#46;92&#93;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;049&#41; &#40;OR 1&#46;98 &#91;CI 95&#37; 1&#46;00&#8211;3&#46;92&#93;&#44; <span class="elsevierStyleItalic">p</span> &#61; 0&#46;049&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; In turn&#44; showing a eosinophil count &#8804;13<span class="elsevierStyleHsp" style=""></span>cells&#47;mm<span class="elsevierStyleSup">3</span> at diagnosis of HAS conferred a non-significant higher risk of mortality &#40;1&#46;87 &#91;0&#46;95&#8211;3&#46;70&#93;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;072&#41;&#46; Finally&#44; the Kaplan&#8211;Meier curves at 90 days following diagnosis of HAS showed that patients with &#8804;775<span class="elsevierStyleHsp" style=""></span>lymphocytes&#47;mm<span class="elsevierStyleSup">3</span> died earlier &#40;media 48&#46;6 days &#91;40&#46;3&#8211;56&#46;8&#93;&#41; than patients with &#62;775<span class="elsevierStyleHsp" style=""></span>lymphocytes&#47;mm<span class="elsevierStyleSup">3</span> &#40;media 60&#46;5 &#91;53&#46;1&#8211;67&#46;9&#93;&#41;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;030 &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</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&#44; the neutrophil&#44; accompanied by a decrease in the prototypic cell of the adaptive immunity&#44; the lymphocyte&#46; Neutrophil count expansion could represent a kind of compensatory mechanism responding to the decrease in the lymphocyte counts&#44; which precedes the emergence of HAS&#46; The significant decrease in lymphocyte counts found from admission to diagnosis of HAS cannot be explained by hemodilution due to fluid administration&#44; since counts of the other leukocyte subsets were not affected&#46; In consequence&#44; this is the first report providing evidence that sepsis does induce diminution of lymphocyte counts in blood&#46;</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&#46;<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">8&#8211;10</span></a> In this regard&#44; this study provides a cut-off value for lymphocyte counts &#40;&#8804;775<span class="elsevierStyleHsp" style=""></span>cells&#47;mm<span class="elsevierStyleSup">3</span>&#41; which is useful for the early identification of those patients at higher risk of mortality&#44; independently of their accompanying co-morbidities &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Also we repeat analysis excluding immunosuppressed patients and we found that those patients with &#8804;775 lymphocytes&#47;mm<span class="elsevierStyleSup">3</span> continue presenting higher risk to mortality&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Lymphocyte counting is a simple and inexpensive test&#44; widely available in most hospital settings&#46; In our study&#44; the eosinophil count at diagnosis of HAS conferred a nonsignificant higher risk of mortality&#46; Some limitations of our work were its retrospective nature&#44; the absence of some variables like the albumin levels or severity scores like SOFA or APACHE&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">In conclusion&#44; lymphopenic HAS &#40;L-HAS&#41; &#40;&#8804;775<span class="elsevierStyleHsp" style=""></span>lymphocytes&#47;mm<span class="elsevierStyleSup">3</span>&#41; constitutes a particular immunological phenotype of the disease conferring a two-fold increase in the risk of hospital mortality&#46; Patients with L-HAS deserve special care and close monitoring of vital signs&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Conflict of interest</span><p id="par0075" class="elsevierStylePara elsevierViewall">None&#46;</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&#44; commercial or not-for-profit sectors&#46; Salaries from the authors are paid by the &#8220;Consejer&#237;a de Sanidad de Castilla y Le&#243;n&#44; Spain&#8221;&#46;</p></span></span>"
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            "apendice" => "<p id="par0090" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article&#58;<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Kaplan&#8211;Meier survival curve&#46; Groups were compared by the log rank test &#40;Mantel&#8211;Henzel&#41;&#46; Circulating Lymphocyte Count &#40;CLC&#41; at HAS diagnosis were divided in two groups&#44; &#8804;775<span class="elsevierStyleHsp" style=""></span>lymphocytes&#47;mm<span class="elsevierStyleSup">3</span> and greater&#46; Time was censored at 90 days following HAS diagnosis&#46; Cum&#58; cumulative&#46;</p>"
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                  \t\t\t\t\tvoid\n
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                  \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&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="3" align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#40;95&#37; CI&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Age &#40;years&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&#46;034&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">&#91;1&#46;002&#8211;1&#46;067&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;040&nbsp;\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
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                  \t\t\t\t">Sex &#40;male&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">2&#46;067&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">&#91;0&#46;978&#8211;4&#46;369&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;057&nbsp;\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">&#8220;Sepsis Code&#8221; implemented&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
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                  \t\t\t\t">0&#46;583&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="left" valign="\n
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                  \t\t\t\t">&#91;0&#46;294&#8211;1&#46;157&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;123&nbsp;\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
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                  \t\t\t\t">Vascular disease&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&#46;419&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">&#91;0&#46;650&#8211;3&#46;096&#93;&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
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                  \t\t\t\t">0&#46;380&nbsp;\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
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                  \t\t\t\t">Cancer&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&#46;385&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="left" valign="\n
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                  \t\t\t\t">&#91;0&#46;680&#8211;2&#46;818&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;369&nbsp;\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
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                  \t\t\t\t">Chronic kidney disease&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
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                  \t\t\t\t">1&#46;693&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#91;0&#46;713&#8211;4&#46;021&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \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&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">4&#46;687&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="left" valign="\n
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                  \t\t\t\t">&#91;1&#46;889&#8211;11&#46;629&#93;&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&#46;001&nbsp;\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&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&#46;346&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#91;1&#46;529&#8211;7&#46;324&#93;&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&#46;003&nbsp;\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 &#40;days&#41; from admission to sepsis diagnosis&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&#46;036&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#91;1&#46;000&#8211;1&#46;074&#93;&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&#46;050&nbsp;\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&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&#46;316&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#91;0&#46;144&#8211;0&#46;696&#93;&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&#46;004&nbsp;\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">&#8804;775<span class="elsevierStyleHsp" style=""></span>lymphocytes&#47;mm<span class="elsevierStyleSup">3</span>&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
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Article information

ISSN: 21735727
Original language: English

DOI:10.1016/j.medine.2018.09.015

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Year/Month	Html	Pdf	Total

2024 November	9	9	18
2024 October	32	36	68
2024 September	32	23	55
2024 August	36	37	73
2024 July	27	21	48
2024 June	34	39	73
2024 May	22	24	46
2024 April	35	32	67
2024 March	31	15	46
2024 February	27	32	59
2024 January	23	26	49
2023 December	26	35	61
2023 November	28	27	55
2023 October	26	28	54
2023 September	22	32	54
2023 August	18	21	39
2023 July	23	24	47
2023 June	30	14	44
2023 May	30	26	56
2023 April	19	14	33
2023 March	36	22	58
2023 February	43	25	68
2023 January	20	17	37
2022 December	44	28	72
2022 November	34	23	57
2022 October	44	27	71
2022 September	23	23	46
2022 August	26	31	57
2022 July	27	23	50
2022 June	19	14	33
2022 May	40	29	69
2022 April	35	31	66
2022 March	40	46	86
2022 February	35	19	54
2022 January	33	39	72
2021 December	32	38	70
2021 November	32	30	62
2021 October	91	55	146
2021 September	34	22	56
2021 August	33	34	67
2021 July	14	22	36
2021 June	22	10	32
2021 May	25	43	68
2021 April	64	97	161
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