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Elevated Plasma Heparin-Binding Protein Is Associated with Early Death After Resuscitation from Cardiac Arrest

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Elevated Plasma Heparin-Binding Protein Is Associated with Early Death After Resuscitation from Cardiac Arrest Ristagno et al. Critical Care (2016) 20:251 DOI 10.1186/s13054-016-1412-4 RESEARCH Open Access Elevated plasma heparin-binding protein is associated with early death after resuscitation from cardiac arrest Giuseppe Ristagno1, Serge Masson1, Marjaana Tiainen2, Stepani Bendel3, Roberto Bernasconi1, Tero Varpula4, Valentina Milani1, Jukka Vaahersalo4, Michela Magnoli1, Eberhard Spanuth5, Simona Barlera1, Roberto Latini1, Sanna Hoppu6, Ville Pettilä4,7, Markus B. Skrifvars4,8* and FINNRESUSCI Study Group Abstract Background: An intense systemic inflammatory response is observed following reperfusion after cardiac arrest. Heparin-binding protein (HBP) is a granule protein released by neutrophils that intervenes in endothelial permeability regulation. In the present study, we investigated plasma levels of HBP in a large population of patients resuscitated from out-of-hospital cardiac arrest. We hypothesized that high circulating levels of HBP are associated with severity of post-cardiac arrest syndrome and poor outcome. Methods: Plasma was obtained from 278 patients enrolled in a prospective multicenter observational study in 21 intensive care units (ICU) in Finland. HBP was assayed at ICU admission and 48 h later. Multiple organ dysfunction syndrome (MODS) was defined as the 24 h Sequential Organ Failure Assessment (SOFA) score ≥ 12. ICU death and 12-month Cerebral Performance Category (CPC) were evaluated. Multiple linear and logistic regression tests and receiver operating characteristic curves with area under the curve (AUC) were performed. Results: Eighty-two percent of patients (229 of 278) survived to ICU discharge and 48 % (133 of 276) to 1 year with a favorable neurological outcome (CPC 1 or 2). At ICU admission, median plasma levels of HBP were markedly elevated, 15.4 [9.6–31.3] ng/mL, and persisted high 48 h later, 14.8 [9.8–31.1] ng/mL. Admission levels of HBP were higher in patients who had higher 24 h SOFA and cardiovascular SOFA score (p < 0.0001) and in those who developed MODS compared to those who did not (29.3 [13.7–60.1] ng/mL vs. 13.6 [9.1–26.2] ng/mL, p < 0.0001; AUC = 0.70 ± 0.04, p = 0.0001). Admission levels of HBP were also higher in patients who died in ICU (31.0 [17.7–78.2] ng/mL) compared to those who survived (13.5 [9.1–25.5] ng/mL, p < 0.0001) and in those with anunfavorable12-monthneurologicaloutcomecomparedtothosewithafavorableone(18.9[11.3–44.3] ng/mL vs. 12.8 [8.6–30.4] ng/mL, p < 0.0001). Admission levels of HBP predicted early ICU death with an AUC of 0.74 ± 0. 04 (p < 0.0001) and were independently associated with ICU death (OR [95 %CI] 1.607 [1.076–2.399], p = 0.020), but not with unfavorable 12-month neurological outcome (OR [95 %CI] 1.154 [0.834–1.596], p =0.387). Conclusions: Elevated plasma levels of HBP at ICU admission were independently associated with early death in ICU. Keywords: Cardiac arrest, Heparin-binding protein, Post resuscitation, Outcome * Correspondence: [email protected] 4Division of Intensive Care Medicine, Department of Anaesthesiology, Intensive Care and Pain Medicine, University of Helsinki and Helsinki University Hospital, Topeliuksenkatu 5, PL 266, 00029 HUS, Helsinki, Finland 8Australian and New Zealand Intensive Care Research Centre, School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ristagno et al. Critical Care (2016) 20:251 Page 2 of 8 Background Uusimaa Hospital district (FINNRESUSCI TUTKIMUS Despite initially successful resuscitation, mortality after §10, 20.1.201) in addition to local ethics approvals in cardiac arrest remains high, with more than half of six of the World Medical Association Declaration of patients not surviving to hospital discharge due to “post- Helsinki. Informed consent from the patient’snextof cardiac arrest syndrome” [1, 2]. Beside myocardial dys- kin was obtained for data collection and blood sam- function and evolving brain injury, a prominent patho- pling. All cardiac arrest patients in whom blood sam- physiological process characterizing such a syndrome is ples were obtained at intensive care unit (ICU) the systemic inflammation subsequent to whole-body admission were included in the study. Information on ischemia/reperfusion [2–6]. Accordingly, the systemic the 12-month neurological outcome was available for inflammatory response observed after cardiopulmonary 276 patients. Thus, these 276 patients were included in resuscitation (CPR) provides evident similarities to sepsis the long-term outcome analysis. and septic shock, with progression toward circulatory failure and multiple organ dysfunction syndrome (MODS) Data collection, processing, and outcomes [4, 5]. Indeed, severe organ dysfunction in two or more The participating hospitals were a part of the Finnish organ systems is very common in post-cardiac arrest Intensive Care Consortium (FICC) and used the same patients and is associated with early mortality [7]. electronic data management system and data validation Heparin-binding protein (HBP), also called azurocidin software (Web Validator, Tieto, Helsinki, Finland). Data or cationic antimicrobial protein of 37 kDa, is a multi- on study patients were prospectively collected using an functional protein contained within the secretory and internet-based case report form. Pre-hospital data were azurophilic granules of polymorphonuclear leukocytes, collected by the paramedics in accordance with the and is rapidly released upon adhesion of leukocytes to Utstein Guidelines and included: whether the arrest was endothelial cells. Once released, HBP acts as chemo- witnessed or not; the administration of bystander-initiated attractant and activator of monocytes and macrophages, life support; the time from call to the dispatch center and and increases vascular permeability with consequent return of spontaneous circulation (ROSC); and the use of edema and hypoperfusion [8, 9]. adrenaline. In-hospital care data were collected electronic- The systemic inflammatory response following resusci- ally and comprised the use of vasopressors and induced tation from cardiac arrest includes leukocyte activation, hypothermia, the Sequential Organ Failure Assessment endothelial injury, and vascular response with vascular (SOFA) score, the Acute Physiology and Chronic Health leakage; thus, elevation in plasma levels of HBP is ex- Evaluation (APACHE) II score, and ICU mortality. The pected and might represent a potential prognostic marker condition of MODS was defined as a SOFA score ≥ 12 [2–4]. Indeed, in a small cohort of cardiac arrest patients, [14, 15]. More specifically, the SOFA score was reported early elevation of HBP after resuscitation predicted organ as worst value during the first 24 hours (h) of ICU care. A failure and poor long-term neurological outcome [10]. In specialist in neurology blinded to the management in the the present observational study, we examined HBP plasma ICU contacted patients discharged from the hospital by levels in a large population of patients resuscitated from phone 1 year after cardiac arrest and determined neuro- out-of-hospital cardiac arrest. Since HBP has been shown logical outcome according to the Pittsburgh Cerebral Per- to predict circulatory failure and increase risk of death in formance Categories (CPC). We defined 12-month good the critically ill patient [9–12], we hypothesized that high outcome as CPC 1–2, and 12-month poor outcome as circulating levels of HBP in patients resuscitated from CPC 3–5. cardiac arrest would be associated with the severity of organ dysfunction and early death. Methods of measurement Plasma levels of HBP at ICU admission and 48 hours Methods later were measured blinded to case identity and clinical Study design, setting, and selection of participants data. Blood samples were collected into ethylenedi- The study was an observational cohort study, in which aminetetraacetic (EDTA) acid tubes and were kept at plasma levels of HBP were assessed in adult patients room temperature for 30–60 min before being centri- resuscitated from out-of-hospital cardiac arrest. Pa- fuged at 2200 g for 10 min. Plasma samples were then tients included in the present study were part of the frozen at -20 °C in each participating hospital, prior to FINNRESUSCI study, a nationwide prospective obser- being transferred in frozen form to Kuopio University vational cohort study conducted in 21 hospitals in Hospital, where they were stored at -70 °C. Upon ana- Finland between March 1, 2010 and February 28, 2011 lysis, samples were thawed and divided into aliquots. and aiming to evaluate post-resuscitation care and out- HBP levels were assayed in a single batch using an enzyme come of out-of-hospital cardiac arrest [13]. The study was immunoassay from Axis-Shield Diagnostics (Dundee, approved by the ethics committee of the Helsinki and Scotland), according to manufacturer’s recommendations. Ristagno et al. Critical Care (2016) 20:251 Page 3 of 8 Limit of detection is reported to be 5.9 ng/mL. Inter- Results assay coefficients of variation were measured in 11 The FINNIRESUSCI study included 548 patients [13], replicates and were 11 % at 21 ng/mL and 7 % at whose clinical characteristics are reported in Additional 81 ng/mL. file 1. Among these, informed consent for blood sam- pling was obtained for 245 patients at the time of ICU admission and for an additional 33 patients prior to Statistical analysis subsequent sampling 48 h later, giving a total study sam- Categorical variables are presented as proportions and ple of 278 patients.
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