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      Low thrombin generation predicts poor prognosis in ischemic stroke patients after thrombolysis

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          Abstract

          Thrombolysis by intravenous recombinant tissue plasminogen activator (rt-PA) is an effective therapy in acute ischemic stroke (AIS). Thrombin generation test (TGT) is a global hemostasis test providing information about the speed and amount of generated thrombin in plasma. Here we aimed to find out whether results of this test before the initiation of thrombolysis might predict outcomes. Study population included 120 consecutive AIS patients, all within 4.5 hours of their symptom onset, who underwent thrombolysis by rt-PA. Blood samples were collected from all patients upon admission and TGT was performed using platelet poor plasma. Clinical data of patients including the NIHSS were registered at admission, day 1 and 7 after therapy. The ASPECT score was assessed using CT images taken before and 24 hours after thrombolysis. Long-term functional outcome was defined 3 months after the event by the modified Rankin Scale. Endogenous Thrombin Potential (ETP) and Peak Thrombin were significantly lower in patients with cardioembolic IS. Symptomatic intracranial hemorrhage (SICH) was found in 6 patients and was significantly associated with low ETP and Peak Thrombin levels. A multiple logistic regression model revealed that an ETP result in the lower quartile is an independent predictor of mortality within the first two weeks (OR: 6.03; 95%CI: 1.2–30.16, p<0.05) and three months after the event (OR: 5.28; 95%CI: 1.27–21.86, p<0.05). Low levels of ETP and Peak Thrombin parameters increase the risk of therapy associated SICH. A low ETP result is an independent predictor of short- and long-term mortality following thrombolysis.

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          Most cited references21

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          Guidelines for Management of Ischaemic Stroke and Transient Ischaemic Attack 2008

          The European Stroke Organisation (ESO) Executive Committee and the ESO Writing Committee (2008)
          This article represents the update of the European Stroke Initiative Recommendations for Stroke Management. These guidelines cover both ischaemic stroke and transient ischaemic attacks, which are now considered to be a single entity. The article covers referral and emergency management, Stroke Unit service, diagnostics, primary and secondary prevention, general stroke treatment, specific treatment including acute management, management of complications, and rehabilitation.
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            Thrombin generation, a function test of the haemostatic-thrombotic system.

            Raed Al-Yamori, S Béguin, Erik De Clercq … (2006)
            By the use of a fluorogenic thrombin substrate and continuous calibration of each individual sample, it is now possible to obtain a thrombin generation (TG) curve (or thrombogram) in plasma, with or without platelets, in an easy routine procedure at high throughput and with an acceptable experimental error (<5%). Evidence is growing that the parameters of the thrombogram, and notably the area under the curve (endogenous thrombin potential, ETP), are useful in assessing bleeding- or thrombotic risk and its modification by antithrombotic- or haemostatic treatment. Available data strongly suggest that conditions (congenital, acquired, drug-induced) that increase TG all cause a thrombotic tendency and that conditions that decrease TG prevent thrombosis but, beyond a limit, cause bleeding. Diminution of TG is a common denominator of all antithrombotic treatment, including anti-platelet drugs. The thrombogram can also be used as a tool in the search for new antithrombotics and reflects the haemorrhagic or thrombotic side effects of other drugs (e.g. oral contraceptives). The thrombogram thus is a promising new approach to clinical management of bleeding and thrombotic disease as well as a tool in drug research and epidemiology. Our experience at this moment is insufficient, however, to already clearly define its limits.
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              Risk factors for severe hemorrhagic transformation in ischemic stroke patients treated with recombinant tissue plasminogen activator: a secondary analysis of the European-Australasian Acute Stroke Study (ECASS II).

              Benjamin R Kummer, Paul Muller, Erich Bluhmki … (2001)
              Intravenous thrombolysis with recombinant tissue plasminogen activator (rtPA) improves the outcome for ischemic stroke patients who can be treated within 3 hours of symptom onset. The efficacy of thrombolysis has been demonstrated despite an increased risk of severe hemorrhagic transformation (HT) in patients treated with rtPA. We performed an analysis of risk factors for severe HT in the second European-Australasian Acute Stroke Study (ECASS II). HTs were classified by using clinical and radiological criteria as follows: hemorrhagic infarction (HI), parenchymal hemorrhage (PH), and symptomatic intracranial hemorrhage (SICH). Potential risk factors for HT were tested by stepwise logistic regression analysis, including rtPA-by-variable interactions. In addition, the distribution of bad outcome (modified Rankin score 5 to 6) at day 90 was stratified according to each category of HT. PH and SICH but not HI were associated with rtPA. Also, PH and SICH but not HI were more severe in rtPA-treated patients than in those receiving placebo. Risk factors for PH were rtPA, extent of parenchymal hypoattenuation on baseline CT, congestive heart failure, increasing age, and baseline systolic blood pressure. The risk of PH on rtPA was increased in older patients and in those who were treated with aspirin before thrombolysis. Risk factors for SICH were rtPA, congestive heart failure, extent of parenchymal hypoattenuation, and increasing age. The risk of SICH on rtPA was increased in patients who were treated with aspirin before thrombolysis. This secondary analysis of ECASS II has confirmed the importance of the extent of hypoattenuation as a risk factor for severe HT. The findings also suggest that older patients and those who have used aspirin before stroke are at higher risk of a severe HT on rtPA.
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                Author and article information

                Contributors
                Renáta Hudák: Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Edina G. Székely: Role: Data curationRole: Formal analysis
                Katalin R. Kovács: Role: Data curationRole: Formal analysisRole: Investigation
                Attila Nagy: Role: Data curationRole: Formal analysisRole: Validation
                Gergely Hofgárt: Role: Formal analysisRole: Investigation
                Ervin Berényi: Role: Data curationRole: Formal analysisRole: Validation
                László Csiba: Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: Validation
                János Kappelmayer: Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: SupervisionRole: Validation
                Zsuzsa Bagoly:
                ORCID: http://orcid.org/0000-0001-5314-5607
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Giuseppe Biagini: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 10 July 2017
                Publication date Collection: 2017
                Volume: 12
                Issue: 7
                Electronic Location Identifier: e0180477
                Affiliations
                [1 ] Department of Laboratory Medicine, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
                [2 ] Department of Laboratory Medicine, Division of Clinical Laboratory Sciences, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
                [3 ] Department of Neurology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
                [4 ] Department of Preventive Medicine, Faculty of Public Health, University of Debrecen, Debrecen, Hungary
                [5 ] Department of Radiology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
                University of Modena and Reggio Emilia, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-5314-5607
                Article
                Publisher ID: PONE-D-17-12617
                DOI: 10.1371/journal.pone.0180477
                PMC ID: 5503253
                PubMed ID: 28692682
                SO-VID: 1a0d4a12-2efd-4ec3-910f-6d9990a341dc
                Copyright © © 2017 Hudák et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 31 March 2017
                Date accepted : 15 June 2017
                Page count
                Figures: 2, Tables: 4, Pages: 13
                Funding
                Funded by: European Union and the European Regonal Development Fund
                Award ID: GINOP-2.3.2-15-2016-00043
                Award Recipient :
                Funded by: National Research, Development and Innovation Fund
                Award ID: K109712
                Award Recipient :
                Funded by: National Research, Development and Innovation Fund
                Award ID: PD111929
                Award Recipient :
                ORCID: http://orcid.org/0000-0001-5314-5607
                Funded by: National Development Agency
                Award ID: TÁMOP 4.2.2.A-11/1/KONV-2012-0045
                Award Recipient :
                ORCID: http://orcid.org/0000-0001-5314-5607
                Funded by: Hungarian Academy of Sciences
                Award ID: Janos Bolyai Fellowship
                Award Recipient :
                ORCID: http://orcid.org/0000-0001-5314-5607
                Funded by: University of Debrecen
                Award ID: Lajos Szodoray Prize
                Award Recipient :
                ORCID: http://orcid.org/0000-0001-5314-5607
                Funded by: European Social Fund and the State of Hungary
                Award ID: TÁMOP-4.2.4.A/2-11/1-2012-0001
                Award Recipient :
                This work was supported by grants from the National Research, Development and Innovation Fund (OTKA K109712, PD111929), the National Development Agency (TÁMOP 4.2.2.A-11/1/KONV-2012-0045) and by the European Union and the European Regional Development Fund, GINOP-2.3.2-15-2016-00043. ZB is the recipient of János Bólyai fellowship and Lajos Szodoray Prize. RH was supported by the European Social Fund in the frame of TÁMOP -4.2.4.A/2-11/1-2012-0001. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Proteins
                Subject: Thrombin
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Cerebrovascular Diseases
                Subject: Stroke
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Stroke
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Cerebrovascular Diseases
                Subject: Stroke
                Subject: Hemorrhagic Stroke
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Stroke
                Subject: Hemorrhagic Stroke
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Hemorrhage
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Hemorrhage
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Hemorrhage
                Subject: Medicine and Health Sciences
                Subject: Pharmaceutics
                Subject: Drug Therapy
                Subject: Antiplatelet Therapy
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Cerebrovascular Diseases
                Subject: Stroke
                Subject: Ischemic Stroke
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Stroke
                Subject: Ischemic Stroke
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Neuroimaging
                Subject: Computed Axial Tomography
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Neuroimaging
                Subject: Computed Axial Tomography
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Tomography
                Subject: Computed Axial Tomography
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Tomography
                Subject: Computed Axial Tomography
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Tomography
                Subject: Computed Axial Tomography
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