CC BY-NC-ND 4.0 · J Neuroanaesth Crit Care 2019; 06(02): 119-130
DOI: 10.1055/s-0039-1689740
Review Article
Indian Society of Neuroanaesthesiology and Critical Care

Intracerebral Hemorrhage: A Brief Evidence-Based Review of Common Etiologies, Mechanisms of Secondary Injury, and Medical and Surgical Management

Anand K. Sarma
1   Division of Neurocritical Care, Department of Neurology, Wake Forest Baptist Health, Medical Center Boulevard, Winston-Salem, North Carolina, United States
,
Shivani Ghoshal
1   Division of Neurocritical Care, Department of Neurology, Wake Forest Baptist Health, Medical Center Boulevard, Winston-Salem, North Carolina, United States
,
Spencer J. Craven
2   Department of Neurology, Wake Forest Baptist Health, Medical Center Boulevard, Winston-Salem, North Carolina, United States
,
Aarti Sarwal
1   Division of Neurocritical Care, Department of Neurology, Wake Forest Baptist Health, Medical Center Boulevard, Winston-Salem, North Carolina, United States
› Author Affiliations
Further Information

Publication History

Received: 31 January 2019

Accepted after revision: 15 April 2019

Publication Date:
19 June 2019 (online)

Abstract

Intracerebral hemorrhage (ICH) accounts for only 10 to 15% of all strokes but remains a significant cause of morbidity and mortality. Despite lengthy stays in critical care units, only one-half of those experiencing an ICH survive after 30 days, and those who do are often left with considerable disability. Treatment has traditionally focused on minimizing the hemorrhage expansion and reducing clot volume through both medical and surgical means. Management of ICH is a complex and multidisciplinary process. This review will discuss a few common etiologies, explore the pathophysiology of secondary neuronal injury after ICH, review the basics of ICH imaging with computed tomography and magnetic resonance imaging, and highlight latest practices in medical and surgical management. Secondary injury mechanisms such as perihematomal edema and disordered cerebral autoregulation are discussed as potential targets for new treatment modalities. Emergent treatment in the “golden hour” after ictus provides a template of measures to adopt from initial contact with emergency medical services, to the emergency department, and thereafter, triage to the intensive care unit. Medical management including blood pressure control, hemostasis, and coagulopathy reversal are discussed and evidence from trials such as INTERACT 2, ATACH 2, and ANNEXA-4 are given a clinical context. Surgical management including intracranial pressure monitoring, surgical evacuation with open craniotomy, and minimally invasive approaches such as stereotactic-guided aspiration and thrombolysis, ultrasound-induced thrombolysis, image-guided stereotactic endoscopic aspiration, and stereotactic ICH underwater blood aspiration are enumerated. The outcomes and relevance of STICH, MISTIE, and CLEAR trials to present surgical care are elaborated. The review summarizes the current guidelines for the treatment of ICH and the latest literature in the field they are based upon. It aims to provide a concise article beneficial to the emergency physicians and neurointensivists/neuroanesthesiologists.

 
  • References

  • 1 Claude III Hemphill J, Lam A. Emergency neurological life support: intracerebral hemorrhage. Neurocrit Care 2017; 27 (Suppl. 01) 89-101
  • 2 Abegunde DO, Mathers CD, Adam T, Ortegon M, Strong K. The burden and costs of chronic diseases in low-income and middle-income countries. Lancet 2007; 370 (9603) 1929-1938
  • 3 Ikram MA, Wieberdink RG, Koudstaal PJ. International epidemiology of intracerebral hemorrhage. Curr Atheroscler Rep 2012; 14 (04) 300-306
  • 4 Strong K, Mathers C, Bonita R. Preventing stroke: saving lives around the world. Lancet Neurol 2007; 6 (02) 182-187
  • 5 Krishnamurthi RV, Moran AE, Forouzanfar MH. et al; Global Burden of Diseases, Injuries, and Risk Factors 2010 Study Stroke Expert Group. The global burden of hemorrhagic stroke: a summary of findings from the GBD 2010 study. Glob Heart 2014; 9 (01) 101-106
  • 6 Hanley DF, Awad IA, Vespa PM, Martin NA, Zuccarello M. Hemorrhagic stroke: introduction. Stroke 2013; 44 (06) (Suppl. 01) S65-S66
  • 7 van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol 2010; 9 (02) 167-176
  • 8 Ziai WC, Carhuapoma JR. Intracerebral hemorrhage. Continuum (Minneap, Minn) 2018; 24 (06) 1603-1622
  • 9 Falcone GJ, Biffi A, Devan WJ. et al; International Stroke Genetics Consortium. Burden of risk alleles for hypertension increases risk of intracerebral hemorrhage. Stroke 2012; 43 (11) 2877-2883
  • 10 O'Donnell MJ, Xavier D, Liu L. et al; INTERSTROKE investigators. Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet 2010; 376 (9735) 112-123
  • 11 Dye JA, Rees G, Yang I, Vespa PM, Martin NA, Vinters HV. Neuropathologic analysis of hematomas evacuated from patients with spontaneous intracerebral hemorrhage. Neuropathology 2014; 34 (03) 253-260
  • 12 Zhu XL, Chan MS, Poon WS. Spontaneous intracranial hemorrhage: which patients need diagnostic cerebral angiography?. A prospective study of 206 cases and review of the literature. Stroke 1997; 28 (07) 1406-1409
  • 13 Biffi A, Greenberg SM. Cerebral amyloid angiopathy: a systematic review. J Clin Neurol 2011; 7 (01) 1-9
  • 14 McCarron MO, Nicoll JA. Cerebral amyloid angiopathy and thrombolysis-related intracerebral haemorrhage. Lancet Neurol 2004; 3 (08) 484-492
  • 15 Ellis RJ, Olichney JM, Thal LJ. et al. Cerebral amyloid angiopathy in the brains of patients with Alzheimer's disease: the CERAD experience, Part XV. Neurology 1996; 46 (06) 1592-1596
  • 16 Pezzini A, Grassi M, Paciaroni M. et al; Multicenter Study on Cerebral Hemorrhage in Italy (MUCH-Italy) Investigators. Antithrombotic medications and the etiology of intracerebral hemorrhage: MUCH-Italy. Neurology 2014; 82 (06) 529-535
  • 17 National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 1995; 333 (24) 1581-1587
  • 18 Falcone GJ, Radmanesh F, Brouwers HB. et al; International Stroke Genetics Consortium. APOE ∊ variants increase risk of warfarin-related intracerebral hemorrhage. Neurology 2014; 83 (13) 1139-1146
  • 19 Appelboom G, Bruce SS, Hickman ZL. et al. Volume-dependent effect of perihaematomal oedema on outcome for spontaneous intracerebral haemorrhages. J Neurol Neurosurg Psychiatry 2013; 84 (05) 488-493
  • 20 Naidech AM, Bernstein RA, Levasseur K. et al. Platelet activity and outcome after intracerebral hemorrhage. Ann Neurol 2009; 65 (03) 352-356
  • 21 Murthy SB, Moradiya Y, Dawson J, Lees KR, Hanley DF, Ziai WC. VISTA-ICH Collaborators. Perihematomal edema and functional outcomes in intracerebral hemorrhage: influence of hematoma volume and location. Stroke 2015; 46 (11) 3088-3092
  • 22 Venkatasubramanian C, Mlynash M, Finley-Caulfield A. et al. Natural history of perihematomal edema after intracerebral hemorrhage measured by serial magnetic resonance imaging. Stroke 2011; 42 (01) 73-80
  • 23 Arima H, Wang JG, Huang Y. et al; INTERACT Investigators. Significance of perihematomal edema in acute intracerebral hemorrhage: the INTERACT trial. Neurology 2009; 73 (23) 1963-1968
  • 24 Sansing LH, Kaznatcheeva EA, Perkins CJ, Komaroff E, Gutman FB, Newman GC. Edema after intracerebral hemorrhage: correlations with coagulation parameters and treatment. J Neurosurg 2003; 98 (05) 985-992
  • 25 Urday S, Beslow LA, Dai F. et al. Rate of perihematomal edema expansion predicts outcome after intracerebral hemorrhage. Crit Care Med 2016; 44 (04) 790-797
  • 26 Wu TY, Sharma G, Strbian D. et al. Natural history of perihematomal edema and impact on outcome after intracerebral hemorrhage. Stroke 2017; 48 (04) 873-879
  • 27 Lim-Hing K, Rincon F. Secondary hematoma expansion and perihemorrhagic edema after intracerebral hemorrhage: from bench work to practical aspects. Front Neurol 2017; 8: 74
  • 28 Selim M, Norton C. Perihematomal edema: Implications for intracerebral hemorrhage research and therapeutic advances. J Neurosci Res. 2018 10.1002/jnr.24372
  • 29 Qureshi AI, Hanel RA, Kirmani JF, Yahia AM, Hopkins LN. Cerebral blood flow changes associated with intracerebral hemorrhage. Neurosurg Clin N Am 2002; 13 (03) 355-370
  • 30 Gregoire SM, Charidimou A, Gadapa N. et al. Acute ischaemic brain lesions in intracerebral haemorrhage: multicentre cross-sectional magnetic resonance imaging study. Brain 2011; 134 (Pt 8) 2376-2386
  • 31 Nakagawa K, Serrador JM, LaRose SL, Sorond FA. Dynamic cerebral autoregulation after intracerebral hemorrhage: a case-control study. BMC Neurol 2011; 11: 108
  • 32 Minhas JS, Panerai RB, Robinson TG. Feasibility of Improving Cerebral Autoregulation in Acute Intracerebral Haemorrhage (BREATHE-ICH) study: a protocol for an experimental interventional study. BMJ Open 2018; 8 (03) e020758
  • 33 Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke 2012; 43 (08) 2258-2263
  • 34 Diringer MN, Edwards DF. Admission to a neurologic/neurosurgical intensive care unit is associated with reduced mortality rate after intracerebral hemorrhage. Crit Care Med 2001; 29 (03) 635-640
  • 35 Terént A, Asplund K, Farahmand B. et al; Riks-Stroke Collaboration. Stroke unit care revisited: who benefits the most?. A cohort study of 105,043 patients in Riks-Stroke, the Swedish Stroke Register. J Neurol Neurosurg Psychiatry 2009; 80 (08) 881-887
  • 36 Wardlaw JM, Seymour J, Cairns J, Keir S, Lewis S, Sandercock P. Immediate computed tomography scanning of acute stroke is cost-effective and improves quality of life. Stroke 2004; 35 (11) 2477-2483
  • 37 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
  • 38 Cucchiara B, Messe S, Sansing L, Kasner S, Lyden P. CHANT Investigators. Hematoma growth in oral anticoagulant related intracerebral hemorrhage. Stroke 2008; 39 (11) 2993-2996
  • 39 Brott T, Broderick J, Kothari R. et al. Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke 1997; 28 (01) 1-5
  • 40 Hemphill III JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke 2001; 32 (04) 891-897
  • 41 Rost NS, Smith EE, Chang Y. et al. Prediction of functional outcome in patients with primary intracerebral hemorrhage: the FUNC score. Stroke 2008; 39 (08) 2304-2309
  • 42 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
  • 43 Delgado Almandoz JE, Schaefer PW, Goldstein JN. et al. Practical scoring system for the identification of patients with intracerebral hemorrhage at highest risk of harboring an underlying vascular etiology: the Secondary Intracerebral Hemorrhage Score. Am J Neuroradiol 2010; 31 (09) 1653-1660
  • 44 Halpin SF, Britton JA, Byrne JV, Clifton A, Hart G, Moore A. Prospective evaluation of cerebral angiography and computed tomography in cerebral haematoma. J Neurol Neurosurg Psychiatry 1994; 57 (10) 1180-1186
  • 45 Thompson AL, Kosior JC, Gladstone DJ. et al; PREDICTS/Sunnybrook ICH CTA Study Group. Defining the CT angiography ‘spot sign’ in primary intracerebral hemorrhage. Can J Neurol Sci 2009; 36 (04) 456-461
  • 46 Wada R, Aviv RI, Fox AJ. et al. CT angiography “spot sign” predicts hematoma expansion in acute intracerebral hemorrhage. Stroke 2007; 38 (04) 1257-1262
  • 47 Wang W, Zhou N, Wang C. Early-stage estimated value of blend sign on the prognosis of patients with intracerebral hemorrhage. BioMed Res Int 2018; 2018: 4509873
  • 48 Pfleger MJ, Hardee EP, Contant Jr CF, Hayman LA. Sensitivity and specificity of fluid-blood levels for coagulopathy in acute intracerebral hematomas. Am J Neuroradiol 1994; 15 (02) 217-223
  • 49 Rodriguez-Luna D, Piñeiro S, Rubiera M. et al. Impact of blood pressure changes and course on hematoma growth in acute intracerebral hemorrhage. Eur J Neurol 2013; 20 (09) 1277-1283
  • 50 Sakamoto Y, Koga M, Yamagami H. et al; SAMURAI Study Investigators. Systolic blood pressure after intravenous antihypertensive treatment and clinical outcomes in hyperacute intracerebral hemorrhage: the stroke acute management with urgent risk-factor assessment and improvement-intracerebral hemorrhage study. Stroke 2013; 44 (07) 1846-1851
  • 51 Anderson CS, Heeley E, Huang Y. et al; INTERACT2 Investigators. Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med 2013; 368 (25) 2355-2365
  • 52 Qureshi AI, Palesch YY, Barsan WG. et al; ATACH-2 Trial Investigators and the Neurological Emergency Treatment Trials Network. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med 2016; 375 (11) 1033-1043
  • 53 Steiner T, Al-Shahi Salman R, Beer R. et al; European Stroke Organisation. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke 2014; 9 (07) 840-855
  • 54 Mayer SA, Brun NC, Begtrup K. et al; FAST Trial Investigators. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 2008; 358 (20) 2127-2137
  • 55 Shakur H, Roberts I, Bautista R. et al; CRASH-2 trial collaborators. Effects of tranexamic acid on death, vascular occlusive events, and blood transfusion in trauma patients with significant haemorrhage (CRASH-2): a randomised, placebo-controlled trial. Lancet 2010; 376 (9734) 23-32
  • 56 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
  • 57 Gómez-Outes A, Lagunar-Ruíz J, Terleira-Fernández AI, Calvo-Rojas G, Suárez-Gea ML, Vargas-Castrillón E. Causes of death in anticoagulated patients with atrial fibrillation. J Am Coll Cardiol 2016; 68 (23) 2508-2521
  • 58 Hanger HC, Fletcher VJ, Wilkinson TJ, Brown AJ, Frampton CM, Sainsbury R. Effect of aspirin and warfarin on early survival after intracerebral haemorrhage. J Neurol 2008; 255 (03) 347-352
  • 59 Steiner T, Poli S, Griebe M. et al. Fresh frozen plasma versus prothrombin complex concentrate in patients with intracranial haemorrhage related to vitamin K antagonists (INCH): a randomised trial. Lancet Neurol 2016; 15 (06) 566-573
  • 60 Pollack Jr CV, Reilly PA, Eikelboom J. et al. Idarucizumab for dabigatran reversal. N Engl J Med 2015; 373 (06) 511-520
  • 61 Soon CW, Kirsch IR, Connolly AJ, Kwong BY, Kim J. Eosinophil-rich acute febrile neutrophilic dermatosis in a patient with enteropathy-associated T-cell lymphoma, type 1. Am J Dermatopathol 2016; 38 (09) 704-708
  • 62 Ansell JE, Bakhru SH, Laulicht BE. et al. Use of PER977 to reverse the anticoagulant effect of edoxaban. N Engl J Med 2014; 371 (22) 2141-2142
  • 63 Saloheimo P, Ahonen M, Juvela S, Pyhtinen J, Savolainen ER, Hillbom M. Regular aspirin-use preceding the onset of primary intracerebral hemorrhage is an independent predictor for death. Stroke 2006; 37 (01) 129-133
  • 64 Toyoda K, Okada Y, Minematsu K. et al. Antiplatelet therapy contributes to acute deterioration of intracerebral hemorrhage. Neurology 2005; 65 (07) 1000-1004
  • 65 Sansing LH, Messe SR, Cucchiara BL, Cohen SN, Lyden PD, Kasner SE. CHANT Investigators. Prior antiplatelet use does not affect hemorrhage growth or outcome after ICH. Neurology 2009; 72 (16) 1397-1402
  • 66 Moussouttas M, Malhotra R, Fernandez L. et al. Role of antiplatelet agents in hematoma expansion during the acute period of intracerebral hemorrhage. Neurocrit Care 2010; 12 (01) 24-29
  • 67 Baharoglu MI, Cordonnier C, Al-Shahi Salman R. et al; PATCH Investigators. Platelet transfusion versus standard care after acute stroke due to spontaneous cerebral haemorrhage associated with antiplatelet therapy (PATCH): a randomised, open-label, phase 3 trial. Lancet 2016; 387 (10038) 2605-2613
  • 68 Frontera JA, Lewin III JJ, Rabinstein A. et al. Guideline for reversal of antithrombotics in intracranial hemorrhage: a statement for healthcare professionals from the Neurocritical Care Society and Society of Critical Care Medicine. Neurocrit Care 2016; 24 (01) 6-46
  • 69 Li X, Sun Z, Zhao W. et al. Effect of acetylsalicylic acid usage and platelet transfusion on postoperative hemorrhage and activities of daily living in patients with acute intracerebral hemorrhage. J Neurosurg 2013; 118 (01) 94-103
  • 70 Mannucci PM, Remuzzi G, Pusineri F. et al. Deamino-8-D-arginine vasopressin shortens the bleeding time in uremia. N Engl J Med 1983; 308 (01) 8-12
  • 71 Kim JH, Baek CH, Min JY, Kim JS, Kim SB, Kim H. Desmopressin improves platelet function in uremic patients taking antiplatelet agents who require emergent invasive procedures. Ann Hematol 2015; 94 (09) 1457-1461
  • 72 Naidech AM, Maas MB, Levasseur-Franklin KE. et al. Desmopressin improves platelet activity in acute intracerebral hemorrhage. Stroke 2014; 45 (08) 2451-2453
  • 73 Dennis M, Sandercock P, Reid J, Graham C, Forbes J, Murray G. CLOTS (Clots in Legs Or sTockings after Stroke) Trials Collaboration. Effectiveness of intermittent pneumatic compression in reduction of risk of deep vein thrombosis in patients who have had a stroke (CLOTS 3): a multicentre randomised controlled trial. Lancet 2013; 382 (9891) 516-524
  • 74 Morgenstern LB, Hemphill III JC, Anderson C. et al; American Heart Association Stroke Council and Council on Cardiovascular Nursing. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2010; 41 (09) 2108-2129
  • 75 Brain Trauma Foundation; American Association of Neurological Surgeons, Congress of Neurological Surgeons. et al. Guidelines for the management of severe traumatic brain injury. VI. Indications for intracranial pressure monitoring. J Neurotrauma 2007; 24 (Suppl. 01) S37-S44
  • 76 Ziai WC, Melnychuk E, Thompson CB, Awad I, Lane K, Hanley DF. Occurrence and impact of intracranial pressure elevation during treatment of severe intraventricular hemorrhage. Crit Care Med 2012; 40 (05) 1601-1608
  • 77 Da Pian R, Bazzan A, Pasqualin A. Surgical versus medical treatment of spontaneous posterior fossa haematomas: a cooperative study on 205 cases. Neurol Res 1984; 6 (03) 145-151
  • 78 Firsching R, Huber M, Frowein RA. Cerebellar haemorrhage: management and prognosis. Neurosurg Rev 1991; 14 (03) 191-194
  • 79 Hidalgo E, Asthana S, Nishio H. et al. Surgery for hilar cholangiocarcinoma: the Leeds experience. Eur J Surg Oncol 2008; 34 (07) 787-794
  • 80 Mendelow AD, Gregson BA, Fernandes HM. et al; STICH investigators. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial. Lancet 2005; 365 (9457) 387-397
  • 81 Mendelow AD, Gregson BA, Rowan EN, Murray GD, Gholkar A, Mitchell PM. STICH II Investigators. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): a randomised trial. Lancet 2013; 382 (9890) 397-408
  • 82 Gregson BA, Broderick JP, Auer LM. et al. Individual patient data subgroup meta-analysis of surgery for spontaneous supratentorial intracerebral hemorrhage. Stroke 2012; 43 (06) 1496-1504
  • 83 Wang WZ, Jiang B, Liu HM. et al. Minimally invasive craniopuncture therapy vs. conservative treatment for spontaneous intracerebral hemorrhage: results from a randomized clinical trial in China. Int J Stroke 2009; 4 (01) 11-16
  • 84 Hanley DF, Thompson RE, Muschelli J. et al; MISTIE Investigators. Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, phase 2 trial. Lancet Neurol 2016; 15 (12) 1228-1237
  • 85 Hanley DF, Thompson RE, Rosenblum M. et al; MISTIE III Investigators. Efficacy and safety of minimally invasive surgery with thrombolysis in intracerebral haemorrhage evacuation (MISTIE III): a randomised, controlled, open-label, blinded endpoint phase 3 trial. Lancet 2019; 393 10175 1021-1032
  • 86 Wang JW, Li JP, Song YL. et al. Stereotactic aspiration versus craniotomy for primary intracerebral hemorrhage: a meta-analysis of randomized controlled trials. PLoS One 2014; 9 (09) e107614
  • 87 Bhattathiri PS, Gregson B, Prasad KS, Mendelow AD. STICH Investigators. Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: results from the STICH trial. Acta Neurochir Suppl (Wien) 2006; 96: 65-68
  • 88 Hallevi H, Albright KC, Aronowski J. et al. Intraventricular hemorrhage: anatomic relationships and clinical implications. Neurology 2008; 70 (11) 848-852
  • 89 Gaberel T, Magheru C, Emery E. Management of non-traumatic intraventricular hemorrhage. Neurosurg Rev 2012; 35 (04) 485-494 discussion 494–495
  • 90 Morgan T, Awad I, Keyl P, Lane K, Hanley D. Preliminary report of the clot lysis evaluating accelerated resolution of intraventricular hemorrhage (CLEAR-IVH) clinical trial. Acta Neurochir Suppl (Wien) 2008; 105: 217-220
  • 91 Hanley DF, Lane K, McBee N. et al; CLEAR III Investigators. Thrombolytic removal of intraventricular haemorrhage in treatment of severe stroke: results of the randomised, multicentre, multiregion, placebo-controlled CLEAR III trial. Lancet 2017; 389 (10069) 603-611
  • 92 Vespa P, Hanley D, Betz J. et al; ICES Investigators. ICES (Intraoperative Stereotactic Computed Tomography-Guided Endoscopic Surgery) for brain hemorrhage: a multicenter randomized controlled trial. Stroke 2016; 47 (11) 2749-2755
  • 93 Fiorella D, Gutman F, Woo H, Arthur A, Aranguren R, Davis R. Minimally invasive evacuation of parenchymal and ventricular hemorrhage using the Apollo system with simultaneous neuronavigation, neuroendoscopy and active monitoring with cone beam CT. J Neurointerv Surg 2015; 7 (10) 752-757
  • 94 Kellner CP, Chartrain AG, Nistal DA. et al. The stereotactic intracerebral hemorrhage underwater blood aspiration (SCUBA) technique for minimally invasive endoscopic intracerebral hemorrhage evacuation. J Neurointerv Surg 2018; 10 (08) 771-776
  • 95 Day JD. Transsulcal parafascicular surgery using BrainPath® for subcortical lesions. Neurosurgery 2017; 64 (CN_suppl_1) 151-156
  • 96 Labib MA, Shah M, Kassam AB. et al. The safety and feasibility of image-guided BrainPath-mediated transsulcul hematoma evacuation: a multicenter study. Neurosurgery 2017; 80 (04) 515-524
  • 97 Newell DW, Shah MM, Wilcox R. et al. Minimally invasive evacuation of spontaneous intracerebral hemorrhage using sonothrombolysis. J Neurosurg 2011; 115 (03) 592-601
  • 98 Broderick J, Connolly S, Feldmann E. et al; American Heart Association/American Stroke Association Stroke Council; American Heart Association/American Stroke Association High Blood Pressure Research Council; Quality of Care and Outcomes in Research Interdisciplinary Working Group. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Circulation 2007; 116 (16) e391-e413