Surgical Trials in Intracerebral Hemorrhage
2013; Lippincott Williams & Wilkins; Volume: 44; Issue: 6_suppl_1 Linguagem: Inglês
10.1161/strokeaha.113.001494
ISSN1524-4628
AutoresPaul Vespa, Neil A. Martin, Mario Zuccarello, Issam A. Awad, Daniel F. Hanley,
Tópico(s)Acute Ischemic Stroke Management
ResumoHomeStrokeVol. 44, No. 6_suppl_1Surgical Trials in Intracerebral Hemorrhage Free AccessResearch ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessResearch ArticlePDF/EPUBSurgical Trials in Intracerebral Hemorrhage Paul M. Vespa, MD, Neil Martin, MD, Mario Zuccarello, MD, Issam Awad, MD and Daniel F. Hanley, MD Paul M. VespaPaul M. Vespa From the Departments of Neurology and Neurosurgery (P.M.V.) and Department of Neurosurgery (N.M.), David Geffen School of Medicine at UCLA, CA; Department of Neurosurgery, University of Cincinnati, Cincinnati, OH (M.Z.); Department of Neurosurgery, University of Chicago, Chicago, IL (I.A.); and Department of Neurology, John Hopkins University, Baltimore, MD (D.F.H.). , Neil MartinNeil Martin From the Departments of Neurology and Neurosurgery (P.M.V.) and Department of Neurosurgery (N.M.), David Geffen School of Medicine at UCLA, CA; Department of Neurosurgery, University of Cincinnati, Cincinnati, OH (M.Z.); Department of Neurosurgery, University of Chicago, Chicago, IL (I.A.); and Department of Neurology, John Hopkins University, Baltimore, MD (D.F.H.). , Mario ZuccarelloMario Zuccarello From the Departments of Neurology and Neurosurgery (P.M.V.) and Department of Neurosurgery (N.M.), David Geffen School of Medicine at UCLA, CA; Department of Neurosurgery, University of Cincinnati, Cincinnati, OH (M.Z.); Department of Neurosurgery, University of Chicago, Chicago, IL (I.A.); and Department of Neurology, John Hopkins University, Baltimore, MD (D.F.H.). , Issam AwadIssam Awad From the Departments of Neurology and Neurosurgery (P.M.V.) and Department of Neurosurgery (N.M.), David Geffen School of Medicine at UCLA, CA; Department of Neurosurgery, University of Cincinnati, Cincinnati, OH (M.Z.); Department of Neurosurgery, University of Chicago, Chicago, IL (I.A.); and Department of Neurology, John Hopkins University, Baltimore, MD (D.F.H.). and Daniel F. HanleyDaniel F. Hanley From the Departments of Neurology and Neurosurgery (P.M.V.) and Department of Neurosurgery (N.M.), David Geffen School of Medicine at UCLA, CA; Department of Neurosurgery, University of Cincinnati, Cincinnati, OH (M.Z.); Department of Neurosurgery, University of Chicago, Chicago, IL (I.A.); and Department of Neurology, John Hopkins University, Baltimore, MD (D.F.H.). Originally published1 Jun 2013https://doi.org/10.1161/STROKEAHA.113.001494Stroke. 2013;44:S79–S82Pathophysiology of Intracerebral HemorrhageIntracerebral hemorrhage (ICH) is crucially important neurological emergency with high societal impact of >1 million deaths worldwide each year.1–3 The pathophysiology of intracerebral hemorrhage can be considered to occur in ≤2 conceptual phases. In the first phase, there is immediate cellular injury in the hemorrhage core because of the acute bleed and early hemorrhagic expansion. The final hemorrhagic volume after the period of hemorrhagic expansion and the location are of hemorrhage are strong predictors of outcome.4,5 Prevention of hemorrhagic expansion can be achieved,6 but doing so does not improve outcome. The second conceptual phase of brain hemorrhage is the persistent hematoma phase characterized by progressive damage to perihematomal tissue caused by mass effect, excitotoxic edema, and progressive neurotoxicity resulting from iron, thrombin, blood breakdown products, free radical formation, protease activation and inflammation, and hyperglycolysis.7–12 The evolutionary damage to the perihematomal tissue is complex and involves multiple mechanisms that are presumed to be linked to the presence of the mass of collected blood and progressive edema. Animal models demonstrate that persistence of the hematoma in brain tissue results in progressive brain edema, metabolic distress, and potentially other mechanisms, which result in long-term disability. We hypothesize that in humans, early removal of the hemorrhage from the parenchyma will result in avoidance or mitigation of these secondary insults and result in substantially enhanced neurological recovery.Surgery for ICHThe effectiveness of craniotomy in the treatment of ICH remains controversial, despite having been evaluated during the past 4 decades. To date, ≤7 randomized trials of surgical intervention have been completed and published in the English language (Table).13–19 Results of individual trials have generally failed to demonstrate improvement in outcome in surgically treated patients.Table. Randomized Surgical Trials for Intracerebral HemorrhageAuthorInterventionYearN, SurgeryN, MedicalTiming, hEffectMcKissock et al13Craniotomy1961899172NoneJuvela et al14Craniotomy1989262648NoneBatjer et al15Craniotomy19908924NoneMorgenstern et al16Craniotomy1998171712NoneAuer et al17Endoscopic1989505048PositiveZuccarello et al18Crani/Stereo199991124NoneMendelow et al19Craniotomy200550353024NeutralInterestingly, the 1 positive trial used a minimally invasive surgical approach. A variety of factors have been addressed that may explain the lack of greater efficacy for invasive surgical evacuation of ICH in prior trials, including late timing of surgery beyond a therapeutic window, inadequately powered sample size, incomplete evacuation, primary damage of the hemorrhage, recurrent bleeding in the immediate postoperative period, persistent intraventricular hemorrhage. However, the type of surgical technique and the damage induced by the operative procedure itself has not been adequately investigated.The Surgical Trial in Intracererbral Hemorrhage (STICH) trial has offered promise for the effect of limited surgery on the basis of the observation that evacuation of surface hematomas seems to result in improved outcome. However, conventional open evacuation surgery did not improve outcome in the overall STICH cohort. STICH II is a randomized controlled trial of 600 patients that was designed as an open craniotomy trial for lobar hematomas that are based or near the cortex with no intraventricular component. Thus, it tests a form of less invasive craniotomy. STICH II data are expected in the spring of 2013. Many questions were raised by STICH I and II, including whether open surgery creates new traumatic brain injury, if open surgery results in near-complete hematoma evacuation, and whether recurrent bleeding after surgery negates the potential benefits of hematoma volume reduction. Comparison of STICH I and II will provide some of these answers. However, these questions are best answered through the use of minimally invasive surgery performed in a prospective fashion with serial imaging to determine the adequacy of hematoma evacuation, surgical induced injury, and recurrence of bleeding.16Minimally Invasive Neurosurgery for Hemorrhage EvacuationMinimally invasive surgery generally refers to the concept of creating minimal trauma to normal appearing tissue during the process of removing the hematoma. This stands in distinction from the open craniotomy in which a large bone flap is created; the brain is exposed, retracted, and manipulated to inspect the site of bleeding and suction blood from multiple areas. Two main types of minimally invasive surgery have been attempted for hematoma removal. The first is endoscopic evacuation of the hematoma. In endoscopic evacuation, a small burr hole is created, and an endoscope measuring from 5 to 8 mm diameter is inserted through normal brain tissue into the hematoma. Suction and irrigation are applied to remove the hematoma. The brain is then visualized via the endoscope to determine the site of bleeding and to determine the amount of ICH evacuated. Auer et al17 reported the first randomized trial of endoscopic-guided hemorrhage evacuation. This trial of 100 patients demonstrated a trend toward decreased morbidity and mortality in the surgical arm, particularly in younger patients with subcortical hematomas. Patients were randomized to stereotactic-guided endoscopic evacuation or medical therapy within 24 hours of symptom onset. The investigators found that, at 6 months, 40% of surgically treated patients had no or minimal disability compared with 25% of patients in the medically treated group (P 80% hematoma removal.For both the MISTIE and the ICES studies, the inclusion and exclusion criteria are summarized below: inclusion criteria: spontaneous, supratentorial, primary ICH within 48 hours from onset, men or women, aged 18 to 89 years, inclusive, written informed consent ICH volume >20 cc, Glasgow Coma Score >5, National Institutes of Health Stroke Scale score >5. The exclusion criteria are: ICH secondary to: cervico-cephalic aneurysm, intracranial arteriovenous malformation, intracranial tumor, trauma, hemorrhagic transformation of an ischemic infarction, isolated intraventricular hemorrhage, Glasgow Coma Score 72 hours, whereas the ICES procedure is a rapid process of hematoma volume reduction >1 hour. It is unclear if 1 approach is superior. (3) The optimal hematoma location for surgery remains unclear, but may be better after bleeding has stopped in the 24- to 72-hour time window.16,29 There may be brain regions that are better adaptable to 1 minimally invasive technique. (4) Selection of candidates who are likely to respond to minimally invasive surgery remains unclear. The predictors of poor outcome without surgery include hemorrhage location, but it is not clear that these predictors hold true once surgery has been performed (as is suggested by preliminary ICES and MISITE data). Preliminary reports of these studies suggest that 180-day prognosis is associated with residual size of the postsurgical hematoma.16,27ConclusionsICH is a devastating illness for which preliminary data from surgical trials indicate that surgery may be helpful. To date, this premise remains unproven. Ongoing trials, including STICH II, MISTIE, and ICES, are attempting to determine the potential for surgical efficacy for limited craniotomy and image guide minimally invasive surgical removal using thrombolysis or endoscopic evacuation. Preliminary results seem promising.AcknowledgementsWe acknowledge the clinical trial expertise of Karen Lane, Amanda Bistran-Hall, Courtney Real, and the entire Brain Injury Outcomes center.DisclosuresDrs Vespa, Martin, Awad, Zuccarrelo, and Hanley have received funding from the National Institutes of Health Stroke Scale. Dr Vespa is consultant for Edge Pharmaceutical. Dr Martin is a consultant for Zoll. Dr Hanley receives medical legal consultation fees.FootnotesCorrespondence to Paul M. Vespa, MD, FCCM, FAAN, David Geffen School of Medicine at UCLA, 757 Westwood Blvd, Room 6236A, Los Angeles, CA 90095. E-mail [email protected]References1. Sacco S, Marini C, Toni D, Olivieri L, Carolei A. Incidence and 10-year survival of intracerebral hemorrhage in a population-based registry.Stroke. 2009; 40:394–399.LinkGoogle Scholar2. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF. Spontaneous intracerebral hemorrhage.N Engl J Med. 2001; 344:1450–1460.CrossrefMedlineGoogle Scholar3. Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster G. Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality.Stroke. 1993; 24:987–993.LinkGoogle Scholar4. Brott T, Broderick J, Kothari R, Barsan W, Tomsick T, Sauerbeck L, et al. Early hemorrhage growth in patients with intracerebral hemorrhage.Stroke. 1997; 28:1–5.LinkGoogle Scholar5. Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T. Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course.Stroke. 1996; 27:1783–1787.LinkGoogle Scholar6. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al.; FAST Trial Investigators. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage.N Engl J Med. 2008; 358:2127–2137.CrossrefMedlineGoogle Scholar7. Gebel JM, Jauch EC, Brott TG, Khoury J, Sauerbeck L, Salisbury S, et al. Natural history of perihematomal edema in patients with hyperacute spontaneous intracerebral hemorrhage.Stroke. 2002; 33:2631–2635.LinkGoogle Scholar8. Lee KR, Kawai N, Kim S, Sagher O, Hoff JT. Mechanisms of edema formation after intracerebral hemorrhage: effects of thrombin on cerebral blood flow, blood-brain barrier permeability, and cell survival in a rat model.J Neurosurg. 1997; 86:272–278.CrossrefMedlineGoogle Scholar9. Kim-Han JS, Kopp SJ, Dugan LL, Diringer MN. Perihematomal mitochondrial dysfunction after intracerebral hemorrhage.Stroke. 2006; 37:2457–2462.LinkGoogle Scholar10. Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage.Lancet Neurol. 2006; 5:53–63.CrossrefMedlineGoogle Scholar11. Zazulia AR, Videen TO, Powers WJ. Transient focal increase in perihematomal glucose metabolism after acute human intracerebral hemorrhage.Stroke. 2009; 40:1638–1643.LinkGoogle Scholar12. Miller CM, Vespa PM, McArthur DL, Hirt D, Etchepare M. Frameless stereotactic aspiration and thrombolysis of deep intracerebral hemorrhage is associated with reduced levels of extracellular cerebral glutamate and unchanged lactate pyruvate ratios.Neurocrit Care. 2007; 6:22–29.CrossrefMedlineGoogle Scholar13. McKissock W, Richardson A, Taylor J. Primary intracerebral hemorrhage: a controlled trial of surgical and conservative treatment.Lancet1961; 2:221–226.CrossrefGoogle Scholar14. Juvela S, Heiskanen O, Poranen A, Valtonen S, Kuurne T, Kaste M, et al. The treatment of spontaneous intracerebral hemorrhage. A prospective randomized trial of surgical and conservative treatment.J Neurosurg. 1989; 70:755–758.CrossrefMedlineGoogle Scholar15. Batjer HH, Reisch JS, Allen BC, Plaizier LJ, Su CJ. Failure of surgery to improve outcome in hypertensive putaminal hemorrhage. A prospective randomized trial.Arch Neurol. 1990; 47:1103–1106.CrossrefMedlineGoogle Scholar16. Morgenstern LB, Demchuk AM, Kim DH, Frankowski RF, Grotta JC. Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage.Neurology. 2001; 56:1294–1299.CrossrefMedlineGoogle Scholar17. Auer LM, Deinsberger W, Niederkorn K, Gell G, Kleinert R, Schneider G, et al. Endoscopic surgery versus medical treatment for spontaneous intracerebral hematoma: a randomized study.J Neurosurg. 1989; 70:530–535.CrossrefMedlineGoogle Scholar18. Zuccarello M, Brott T, Derex L, Kothari R, Sauerbeck L, Tew J, et al. Early surgical treatment for supratentorial intracerebral hemorrhage: a randomized feasibility study.Stroke. 1999; 30:1833–1839.LinkGoogle Scholar19. Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, 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; 365:387–397.CrossrefMedlineGoogle Scholar20. Niizuma H, Otsuki T, Johkura H, Nakazato N, Suzuki J. CT-guided stereotactic aspiration of intracerebral hematoma—result of a hematoma-lysis method using urokinase.Appl Neurophysiol. 1985; 48:427–430.MedlineGoogle Scholar21. Schaller C, Rodhe V, Meyer B, et al. Stereotactive puncture and lysis of spontaneous intracerebral hemorrhage using recombinant tissue-plasminogen activator.Neurosurgery1995; 36:328–335.CrossrefMedlineGoogle Scholar22. Rohde V, Rohde I, Thiex R, Ince A, Jung A, Dückers G, et al. Fibrinolysis therapy achieved with tissue plasminogen activator and aspiration of the liquefied clot after experimental intracerebral hemorrhage: rapid reduction in hematoma volume but intensification of delayed edema formation.J Neurosurg. 2002; 97:954–962.CrossrefMedlineGoogle Scholar23. Vespa P, McArthur D, Miller C, O'Phelan K, Frazee J, Kidwell C, et al. Frameless stereotactic aspiration and thrombolysis of deep intracerebral hemorrhage is associated with reduction of hemorrhage volume and neurological improvement.Neurocrit Care. 2005; 2:274–281.CrossrefMedlineGoogle Scholar24. Barrett RJ, Hussain R, Coplin WM, Berry S, Keyl PM, Hanley DF, et al. Frameless stereotactic aspiration and thrombolysis of spontaneous intracerebral hemorrhage.Neurocrit Care. 2005; 3:237–245.CrossrefMedlineGoogle Scholar25. Cho DY, Chen CC, Chang CS, Lee WY, Tso M. Endoscopic surgery for spontaneous basal ganglia hemorrhage: comparing endoscopic surgery, stereotactic aspiration, and craniotomy in noncomatose patients.Surg Neurol. 2006; 65:547–55; discussion 555.CrossrefMedlineGoogle Scholar26. Nishihara T, Morita A, Teraoka A, Kirino T. Endoscopy-guided removal of spontaneous intracerebral hemorrhage: comparison with computer tomography-guided stereotactic evacuation.Childs Nerv Syst. 2007; 23:677–683.CrossrefMedlineGoogle Scholar27. Hanley DF, et al. MISTIE Phase II results: Safety, efficacy, and surgical performance. Available at:AHA ISC Stroke Conference2012. http://my.americanheart.org/professional/Sessions/InternationalStrokeConference/ScienceNews/ISC-2012-Late-Breaking-Science-Oral-Abstracts_UCM_435384_Article.jsp. Accessed February 2, 2013.Google Scholar28. Dye JA, Dusick JR, Lee DJ, Gonzalez NR, Martin NA. Frontal bur hole through an eyebrow incision for image-guided endoscopic evacuation of spontaneous intracerebral hemorrhage.J Neurosurg. 2012; 117:767–773.CrossrefMedlineGoogle Scholar29. Steiner T, Vincent C, Morris S, Davis S, Vallejo-Torres L, Christensen MC. Neurosurgical outcomes after intracerebral hemorrhage: results of the Factor Seven for Acute Hemorrhagic Stroke Trial (FAST).J Stroke Cerebrovasc Dis. 2011; 20:287–294.CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Mei L, Fengqun M, Xiaozhuo L, Qing W, Mingming F, Zhengyao Z, Dongpo S, Qian H and Tong C (2022) Effect Western Medicines Combined With Nao-Xue-Shu in Patients With Hypertensive Intracerebral Hemorrhage: A Network Meta-Analysis, Frontiers in Pharmacology, 10.3389/fphar.2022.892904, 13 Aronowski J, Sansing L, Xi G and Zhang J (2022) Mechanisms of Damage After Cerebral Hemorrhage Stroke, 10.1016/B978-0-323-69424-7.00008-9, (92-102.e9), . Boniece I (2021) Stroke Mount Sinai Expert Guides, 10.1002/9781119293255.ch27, (250-264), Online publication date: 19-Jan-2021. Lee J and Rybinnik I (2021) Spontaneous Intracerebral Hemorrhage Cerebrovascular Disorders, 10.1007/978-1-0716-1530-0_20, (333-357), . Parrella E, Gussago C, Porrini V, Benarese M and Pizzi M (2020) From Preclinical Stroke Models to Humans: Polyphenols in the Prevention and Treatment of Stroke, Nutrients, 10.3390/nu13010085, 13:1, (85) Iliev B, Schlegel A, Mielke D, Rohde V and Malinova V (2019) Intrahematomal catheter placement with connection to the ventricular system allows more effective thrombolysis of combined intracerebral and intraventricular hematomas, Neurosurgical Review, 10.1007/s10143-019-01170-9, 43:6, (1531-1537), Online publication date: 1-Dec-2020. Jang J, Cho W, Hong N, Pang C, Lee S, Kang H and Kim J (2020) Surgical strategy for patients with supratentorial spontaneous intracerebral hemorrhage: minimally invasive surgery and conventional surgery, Journal of Cerebrovascular and Endovascular Neurosurgery, 10.7461/jcen.2020.22.3.156, 22:3, (156-164), Online publication date: 30-Sep-2020. Liu H, Wu X, Tan Z, Guo H, Bai H, Wang B, Cui W, Zheng L, Sun F, Zhang X, Fan R, Wang P, Jing W, Gao J, Guo W and Qu Y (2020) Long-Term Effect of Endoscopic Evacuation for Large Basal Ganglia Hemorrhage With GCS Scores ≦ 8, Frontiers in Neurology, 10.3389/fneur.2020.00848, 11 Miki K, Yagi K, Nonaka M, Iwaasa M, Abe H, Morishita T, Arima H and Inoue T Spot sign as a predictor of rebleeding after endoscopic surgery for intracerebral hemorrhage, Journal of Neurosurgery, 10.3171/2017.12.JNS172335, 130:5, (1485-1490) Qiu S, Liu T, Cao G, Wu K and Zhao T (2019) Treatment of intracranial hemorrhage with neuroendoscopy guided by body surface projection, Medicine, 10.1097/MD.0000000000015503, 98:19, (e15503), Online publication date: 1-May-2019. Miki K, Yagi K, Nonaka M, Iwaasa M, Abe H, Morishita T, Arima H and Inoue T (2018) Intraoperative Active Bleeding in Endoscopic Surgery for Spontaneous Intracerebral Hemorrhage is Predicted by the Spot Sign, World Neurosurgery, 10.1016/j.wneu.2018.05.022, 116, (e513-e518), Online publication date: 1-Aug-2018. Chartrain A, Kellner C, Fargen K, Spiotta A, Chesler D, Fiorella D and Mocco J (2017) A review and comparison of three neuronavigation systems for minimally invasive intracerebral hemorrhage evacuation, Journal of NeuroInterventional Surgery, 10.1136/neurintsurg-2017-013091, 10:1, (66-74), Online publication date: 1-Jan-2018. El Husseini N, Hoffman B, Bennett E, Li Y, Williamson Taylor R, Hailey C, Richardson K, Li Y, Laskowitz D and James M (2018) Association of IL6ST (gp130) Polymorphism with Functional Outcome Following Spontaneous Intracerebral Hemorrhage, Journal of Stroke and Cerebrovascular Diseases, 10.1016/j.jstrokecerebrovasdis.2017.08.017, 27:1, (125-131), Online publication date: 1-Jan-2018. Xu X, Zheng Y, Chen X, Li F, Zhang H and Ge X (2017) Comparison of endoscopic evacuation, stereotactic aspiration and craniotomy for the treatment of supratentorial hypertensive intracerebral haemorrhage: study protocol for a randomised controlled trial, Trials, 10.1186/s13063-017-2041-1, 18:1, Online publication date: 1-Dec-2017. Cai Q, Zhang H, Zhao D, Yang Z, Hu K, Wang L, Zhang W, Chen Z and Chen Q (2017) Analysis of three surgical treatments for spontaneous supratentorial intracerebral hemorrhage, Medicine, 10.1097/MD.0000000000008435, 96:43, (e8435), Online publication date: 1-Oct-2017. Wang W, Zhou N and Wang C (2017) Minimally Invasive Surgery for Patients with Hypertensive Intracerebral Hemorrhage with Large Hematoma Volume: A Retrospective Study, World Neurosurgery, 10.1016/j.wneu.2017.05.158, 105, (348-358), Online publication date: 1-Sep-2017. Guptill J, Raja S, Boakye-Agyeman F, Noveck R, Ramey S, Tu T and Laskowitz D (2016) Phase 1 Randomized, Double-Blind, Placebo-Controlled Study to Determine the Safety, Tolerability, and Pharmacokinetics of a Single Escalating Dose and Repeated Doses of CN-105 in Healthy Adult Subjects, The Journal of Clinical Pharmacology, 10.1002/jcph.853, 57:6, (770-776), Online publication date: 1-Jun-2017. Hanley D, Lane K, McBee N, Ziai W, Tuhrim S, Lees K, Dawson J, Gandhi D, Ullman N, Mould W, Mayo S, Mendelow A, Gregson B, Butcher K, Vespa P, Wright D, Kase C, Carhuapoma J, Keyl P, Diener-West M, Muschelli J, Betz J, Thompson C, Sugar E, Yenokyan G, Janis S, John S, Harnof S, Lopez G, Aldrich E, Harrigan M, Ansari S, Jallo J, Caron J, LeDoux D, Adeoye O, Zuccarello M, Adams H, Rosenblum M, Thompson R and Awad I (2017) Thrombolytic removal of intraventricular haemorrhage in treatment of severe stroke: results of the randomised, multicentre, multiregion, placebo-controlled CLEAR III trial, The Lancet, 10.1016/S0140-6736(16)32410-2, 389:10069, (603-611), Online publication date: 1-Feb-2017. Kim Y, Yoon D, Kim J, Park K, Lee J, Song H and Bae J (2017) Citation Classics in Stroke: The Top-100 Cited Articles on Hemorrhagic Stroke, European Neurology, 10.1159/000479626, 78:3-4, (210-216), . Chartrain A and Mocco J (2017) Centralization of Intracerebral Hemorrhage Care, World Neurosurgery, 10.1016/j.wneu.2016.11.113, 97, (716-717), Online publication date: 1-Jan-2017. Boccardi E, Cenzato M, Curto F and Motto C (2017) Diagnosis and Therapy in the Acute Phase of Hemorrhagic Stroke: Latest Developments Hemorrhagic Stroke, 10.1007/978-3-319-32130-1_1, (1-97), . Vespa P, Hanley D, Betz J, Hoffer A, Engh J, Carter R, Nakaji P, Ogilvy C, Jallo J, Selman W, Bistran-Hall A, Lane K, McBee N, Saver J, Thompson R and Martin N (2016) ICES (Intraoperative Stereotactic Computed Tomography-Guided Endoscopic Surgery) for Brain Hemorrhage, Stroke, 47:11, (2749-2755), Online publication date: 1-Nov-2016. Hanley D (2016) Prognostic scales versus clinical judgment in ICH, Nature Reviews Neurology, 10.1038/nrneurol.2016.11, 12:4, (192-193), Online publication date: 1-Apr-2016. Wang W (2016) Minimally Invasive Surgical Treatment of Acute Epidural Hematoma: Case Series, BioMed Research International, 10.1155/2016/6507350, 2016, (1-8), . Aronowski J, Wagner K, Xi G and Zhang J (2016) Mechanisms of Cerebral Hemorrhage Stroke, 10.1016/B978-0-323-29544-4.00008-6, (102-112.e6), . Wang T, Guan Y, Du J, Liu G, Gao F and Zhao X (2015) Factors affecting the evacuation rate of intracerebral hemorrhage in basal ganglia treated by minimally invasive craniopuncture, Clinical Neurology and Neurosurgery, 10.1016/j.clineuro.2015.04.020, 134, (104-109), Online publication date: 1-Jul-2015. Etminan N, Beseoglu K and Hänggi D (2015) Neurosurgery in Hemorrhagic Stroke PanVascular Medicine, 10.1007/978-3-642-37078-6_108, (2799-2821), . Etminan N, Beseoglu K and Hänggi D (2014) Neurosurgery in Hemorrhagic Stroke PanVascular Medicine, 10.1007/978-3-642-37393-0_108-1, (1-24), . Flaherty M and Beck J (2013) Surgery for Intracerebral Hemorrhage, Stroke, 44:10, (2953-2954), Online publication date: 1-Oct-2013. June 2013Vol 44, Issue 6_suppl_1 Advertisement Article InformationMetrics © 2013 American Heart Association, Inc.https://doi.org/10.1161/STROKEAHA.113.001494PMID: 23709739 Manuscript receivedMarch 20, 2013Manuscript acceptedApril 10, 2013Originally publishedJune 1, 2013 Keywordscomaintracerebral hemorrhagesurgerythrombolysiscerebral edemaendoscopyPDF download Advertisement SubjectsCerebrovascular Disease/StrokeIntracranial HemorrhageTreatment
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