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Semin Thromb Hemost 2022; 48(07): 828-841
DOI: 10.1055/s-0042-1756191
Review Article

Viscoelastic Testing in the Clinical Management of Subarachnoid Hemorrhage and Intracerebral Hemorrhage

Christine Lodberg Hvas
1   Department of Anesthesiology and Intensive Care, Aarhus University Hospital, Aarhus, Denmark
2   Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
,
Anne-Mette Hvas
3   Faculty of Health, Aarhus University, Aarhus, Denmark
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Abstract

Subarachnoid hemorrhage (SAH) and intracerebral hemorrhage (ICH) are both debilitating and life-threatening incidents calling for immediate action and treatment. This review focuses on the applicability of viscoelastic testing (rotational thromboelastometry or thromboelastography [TEG]) in the management of SAH and ICH. A systematic literature search was performed in PubMed and EMBASE. Studies including patients with SAH or ICH, in which viscoelastic testing was performed, were identified. In total, 24 studies were included for analysis, and further subdivided into studies on SAH patients investigated prior to stenting or coiling (n = 12), ICH patients (n = 8) and studies testing patients undergoing stenting or coiling, or ischemic stroke patients undergoing thrombolysis or thrombectomy and developing ICH as a complication (n = 5). SAH patients had increased clot firmness, and this was associated with a higher degree of early brain injury and higher Hunt-Hess score. SAH patients with delayed cerebral ischemia had higher clot firmness than patients not developing delayed cerebral ischemia. ICH patients showed accelerated clot formation and increased clot firmness in comparison to healthy controls. Patients with hematoma expansion had longer clot initiation and lower platelet aggregation than patients with no hematoma expansion. During stent procedures for SAH, adjustment of antiplatelet therapy according to TEG platelet mapping did not change prevalence of major bleeding, thromboembolic events, or functional outcome. Viscoelastic testing prior to thrombolysis showed conflicting results in predicting ICH as complication. In conclusion, viscoelastic testing suggests hypercoagulation following SAH and ICH. Further investigation of the predictive value of increased clot firmness in SAH seems relevant. In ICH, the prediction of hematoma expansion and ICH as a complication to thrombolysis might be clinically relevant.

Keywords

thromboelastography - subarachnoid hemorrhage - intracerebral hemorrhage - blood coagulation

Financial Support

None.




Publication History

Article published online:
13 September 2022

© 2022. Thieme. All rights reserved.

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  • References

  • 1 Ingall T, Asplund K, Mähönen M, Bonita R. A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke 2000; 31 (05) 1054-1061
    CrossrefPubMedSearch in Google Scholar
  • 2 Connolly Jr ES, Rabinstein AA, Carhuapoma JR. et al; American Heart Association Stroke Council, Council on Cardiovascular Radiology and Intervention, Council on Cardiovascular Nursing, Council on Cardiovascular Surgery and Anesthesia, Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2012; 43 (06) 1711-1737
    CrossrefPubMedSearch in Google Scholar
  • 3 de Rooij NK, Linn FH, van der Plas JA, Algra A, Rinkel GJ. Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends. J Neurol Neurosurg Psychiatry 2007; 78 (12) 1365-1372
    CrossrefPubMedSearch in Google Scholar
  • 4 Etminan N, Chang HS, Hackenberg K. et al. Worldwide incidence of aneurysmal subarachnoid hemorrhage according to region, time period, blood pressure, and smoking prevalence in the population: a systematic review and meta-analysis. JAMA Neurol 2019; 76 (05) 588-597
    CrossrefPubMedSearch in Google Scholar
  • 5 Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 2009; 8 (07) 635-642
    CrossrefPubMedSearch in Google Scholar
  • 6 La Pira B, Singh TD, Rabinstein AA, Lanzino G. Time trends in outcomes after aneurysmal subarachnoid hemorrhage over the past 30 years. Mayo Clin Proc 2018; 93 (12) 1786-1793
    CrossrefPubMedSearch in Google Scholar
  • 7 van Donkelaar CE, Bakker NA, Veeger NJ. et al. Predictive factors for rebleeding after aneurysmal subarachnoid hemorrhage: rebleeding aneurysmal subarachnoid hemorrhage study. Stroke 2015; 46 (08) 2100-2106
    CrossrefPubMedSearch in Google Scholar
  • 8 Larsen CC, Astrup J. Rebleeding after aneurysmal subarachnoid hemorrhage: a literature review. World Neurosurg 2013; 79 (02) 307-312
    CrossrefPubMedSearch in Google Scholar
  • 9 Mourelo-Fariña M, Pértega S, Galeiras R. A model for prediction of in-hospital mortality in patients with subarachnoid hemorrhage. Neurocrit Care 2021; 34 (02) 508-518
    CrossrefPubMedSearch in Google Scholar
  • 10 Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol 2014; 10 (01) 44-58
    CrossrefPubMedSearch in Google Scholar
  • 11 Rowland MJ, Hadjipavlou G, Kelly M, Westbrook J, Pattinson KT. Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth 2012; 109 (03) 315-329
    CrossrefPubMedSearch in Google Scholar
  • 12 Hvas CL, Hvas AM. Hemostasis and fibrinolysis following aneurysmal subarachnoid hemorrhage: a systematic review on additional knowledge from dynamic assays and potential treatment targets. Semin Thromb Hemost 2022; 48 (03) 356-381
    Thieme ConnectPubMedSearch in Google Scholar
  • 13 Nina P, Schisano G, Chiappetta F. et al. A study of blood coagulation and fibrinolytic system in spontaneous subarachnoid hemorrhage. Correlation with Hunt-Hess grade and outcome. Surg Neurol 2001; 55 (04) 197-203
    CrossrefPubMedSearch in Google Scholar
  • 14 Frontera JA, Aledort L, Gordon E. et al. Early platelet activation, inflammation and acute brain injury after a subarachnoid hemorrhage: a pilot study. J Thromb Haemost 2012; 10 (04) 711-713
    CrossrefPubMedSearch in Google Scholar
  • 15 Hirashima Y, Nakamura S, Endo S, Kuwayama N, Naruse Y, Takaku A. Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage. Neurochem Res 1997; 22 (10) 1249-1255
    CrossrefPubMedSearch in Google Scholar
  • 16 Elijovich L, Patel PV, Hemphill III JC. Intracerebral hemorrhage. Semin Neurol 2008; 28 (05) 657-667
    Thieme ConnectPubMedSearch in Google Scholar
  • 17 Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet 2009; 373 (9675): 1632-1644
    CrossrefPubMedSearch in Google Scholar
  • 18 Ovbiagele B, Nguyen-Huynh MN. Stroke epidemiology: advancing our understanding of disease mechanism and therapy. Neurotherapeutics 2011; 8 (03) 319-329
    CrossrefPubMedSearch in Google Scholar
  • 19 Davis SM, Broderick J, Hennerici M. et al; Recombinant Activated Factor VII Intracerebral Hemorrhage Trial Investigators. Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology 2006; 66 (08) 1175-1181
    CrossrefPubMedSearch in Google Scholar
  • 20 Dowlatshahi D, Demchuk AM, Flaherty ML, Ali M, Lyden PL, Smith EE. VISTA Collaboration. Defining hematoma expansion in intracerebral hemorrhage: relationship with patient outcomes. Neurology 2011; 76 (14) 1238-1244
    CrossrefPubMedSearch in Google Scholar
  • 21 Al-Shahi Salman R, Law ZK, Bath PM, Steiner T, Sprigg N. Haemostatic therapies for acute spontaneous intracerebral haemorrhage. Cochrane Database Syst Rev 2018; 4: CD005951
    PubMedSearch in Google Scholar
  • 22 Sprigg N, Flaherty K, Appleton JP. et al; TICH-2 Investigators. Tranexamic acid for hyperacute primary IntraCerebral Haemorrhage (TICH-2): an international randomised, placebo-controlled, phase 3 superiority trial. Lancet 2018; 391 (10135): 2107-2115
    CrossrefPubMedSearch in Google Scholar
  • 23 Hemphill III JC, Greenberg SM, Anderson CS. et al; American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2015; 46 (07) 2032-2060
    CrossrefPubMedSearch in Google Scholar
  • 24 Brummel-Ziedins KE, Wolberg AS. Global assays of hemostasis. Curr Opin Hematol 2014; 21 (05) 395-403
    CrossrefPubMedSearch in Google Scholar
  • 25 Windeløv NA, Welling KL, Ostrowski SR, Johansson PI. The prognostic value of thrombelastography in identifying neurosurgical patients with worse prognosis. Blood Coagul Fibrinolysis 2011; 22 (05) 416-419
    CrossrefPubMedSearch in Google Scholar
  • 26 Li Y, Zhang X, Guo Z. et al. Standard vs. modified antiplatelet therapy based on thromboelastography with platelet mapping for preventing bleeding events in patients undergoing stent-assisted coil for a ruptured intracranial aneurysm. Front Neurol 2021; 11: 615829
    CrossrefPubMedSearch in Google Scholar
  • 27 Ganter MT, Hofer CK. Coagulation monitoring: current techniques and clinical use of viscoelastic point-of-care coagulation devices. Anesth Analg 2008; 106 (05) 1366-1375
    CrossrefPubMedSearch in Google Scholar
  • 28 El-Khawas K, Lloyd-Donald P, Hart GK. et al. Prospective longitudinal evaluation of coagulation with novel thromboelastography technology in patients after subarachnoid hemorrhage: a pilot study. World Neurosurg 2020; 136: e181-e195
    CrossrefPubMedSearch in Google Scholar
  • 29 Lauridsen SV, Hvas CL, Sandgaard E. et al. Thromboelastometry shows early hypercoagulation in patients with spontaneous subarachnoid hemorrhage. World Neurosurg 2019; 130: e140-e149
    CrossrefPubMedSearch in Google Scholar
  • 30 Hvas CL, Lauridsen SV, Pedersen ES, Gyldenholm T, Hvas AM. Ex vivo effect of hemostatic therapy in subarachnoid and intracerebral hemorrhage. Thromb Res 2020; 189: 42-47
    CrossrefPubMedSearch in Google Scholar
  • 31 Xu Y, Qi M, Wang N. et al. The effect of remote ischemic conditioning on blood coagulation function and cerebral blood flow in patients with aneurysmal subarachnoid hemorrhage. Neurol Sci 2020; 41 (02) 335-340
    CrossrefPubMedSearch in Google Scholar
  • 32 Vahtera AS, Junttila EK, Jalkanen LV. et al. Activation of blood coagulation after aneurysmal subarachnoid hemorrhage: a prospective observational trial of rotational thromboelastometry. World Neurosurg 2019; 122: e334-e341
    CrossrefPubMedSearch in Google Scholar
  • 33 Miao W, Zhao K, Deng W, Teng J. Coagulation factor hyperfunction after subarachnoid hemorrhage induces deep venous thrombosis. World Neurosurg 2018; 110: e46-e52
    CrossrefPubMedSearch in Google Scholar
  • 34 Frontera JA, Provencio JJ, Sehba FA. et al. The role of platelet activation and inflammation in early brain injury following subarachnoid hemorrhage. Neurocrit Care 2017; 26 (01) 48-57
    CrossrefPubMedSearch in Google Scholar
  • 35 Ramchand P, Nyirjesy S, Frangos S. et al. Thromboelastography parameter predicts outcome after subarachnoid hemorrhage: an exploratory analysis. World Neurosurg 2016; 96: 215-221
    CrossrefPubMedSearch in Google Scholar
  • 36 Ettinger MG. Coagulation abnormalities in subarachnoid hemorrhage. Stroke 1970; 1 (03) 139-142
    CrossrefPubMedSearch in Google Scholar
  • 37 He Q, Zhou Y, Liu C. et al. Thromboelastography with platelet mapping detects platelet dysfunction in patients with aneurysmal subarachnoid hemorrhage with rebleeding. Neuropsychiatr Dis Treat 2019; 15: 3443-3451
    CrossrefPubMedSearch in Google Scholar
  • 38 He Q, Zhou Y, Liu C. et al. Prediction of hematoma expansion in patients with intracerebral hemorrhage using thromboelastography with platelet mapping: a prospective observational study. Front Neurol 2021; 12: 746024
    CrossrefPubMedSearch in Google Scholar
  • 39 Roh D, Chang T, Zammit C. et al. Functional coagulation differences between lobar and deep intracerebral hemorrhage detected by rotational thromboelastometry: a pilot study. Neurocrit Care 2019; 31 (01) 81-87
    CrossrefPubMedSearch in Google Scholar
  • 40 Lauridsen SV, Hvas AM, Sandgaard E. et al. Coagulation profile after spontaneous intracerebral hemorrhage: a cohort study. J Stroke Cerebrovasc Dis 2018; 27 (11) 2951-2961
    CrossrefPubMedSearch in Google Scholar
  • 41 Roh D, Torres GL, Cai C. et al. Coagulation differences detectable in deep and lobar primary intracerebral hemorrhage using thromboelastography. Neurosurgery 2020; 87 (05) 918-924
    CrossrefPubMedSearch in Google Scholar
  • 42 Bliden KP, Raviv G, Tantry US. et al. “Blueprinting” thrombogenicity and antithrombotic drug response at the bedside in patients presenting emergently with symptoms of acute stroke. J Thromb Thrombolysis 2019; 47 (02) 192-199
    CrossrefPubMedSearch in Google Scholar
  • 43 Meier K, Saenz DM, Torres GL. et al. Thrombelastography suggests hypercoagulability in patients with renal dysfunction and intracerebral hemorrhage. J Stroke Cerebrovasc Dis 2018; 27 (05) 1350-1356
    CrossrefPubMedSearch in Google Scholar
  • 44 Kawano-Castillo J, Ward E, Elliott A. et al. Thrombelastography detects possible coagulation disturbance in patients with intracerebral hemorrhage with hematoma enlargement. Stroke 2014; 45 (03) 683-688
    CrossrefPubMedSearch in Google Scholar
  • 45 Ge H, Yang H, Ren H. et al. Association of thrombelastographic parameters with complications in patients with intracranial aneurysm after stent placement. World Neurosurg 2019; 127: e30-e38
    CrossrefPubMedSearch in Google Scholar
  • 46 Liang C, Yang Y, He Z. et al. Comparison between thromboelastography and the conventional coagulation test in detecting effects of antiplatelet agents after endovascular treatments in acute ischemic stroke patients: a STROBE-compliant study. Medicine (Baltimore) 2020; 99 (10) e19447
    CrossrefPubMedSearch in Google Scholar
  • 47 Yu G, Kim YJ, Jeon SB, Kim WY. Thromboelastography for prediction of hemorrhagic transformation in patients with acute ischemic stroke. Am J Emerg Med 2020; 38 (09) 1772-1777
    CrossrefPubMedSearch in Google Scholar
  • 48 McDonald MM, Wetzel J, Fraser S. et al. Thrombelastography does not predict clinical response to rtPA for acute ischemic stroke. J Thromb Thrombolysis 2016; 41 (03) 505-510
    CrossrefPubMedSearch in Google Scholar
  • 49 Dorhout Mees SM, Kerr RS, Rinkel GJ, Algra A, Molyneux AJ. Occurrence and impact of delayed cerebral ischemia after coiling and after clipping in the International Subarachnoid Aneurysm Trial (ISAT). J Neurol 2012; 259 (04) 679-683
    CrossrefPubMedSearch in Google Scholar
  • 50 Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet 2017; 389 (10069): 655-666
    CrossrefPubMedSearch in Google Scholar
  • 51 Holck MH, Christensen TD, Hvas AM. Influence of selected antithrombotic treatment on thromboelastometric results. Scand J Clin Lab Invest 2018; 78 (1-2): 11-17
    CrossrefPubMedSearch in Google Scholar
  • 52 James RF, Khattar NK, Aljuboori ZS. et al. Continuous infusion of low-dose unfractionated heparin after aneurysmal subarachnoid hemorrhage: a preliminary study of cognitive outcomes. J Neurosurg 2018;
    CrossrefPubMedSearch in Google Scholar