Clinical Neurology and Neurosurgery 128 (2015) 117–122
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Decompressive hemicraniectomy with or without clot evacuation for large spontaneous supratentorial intracerebral hemorrhages Yoshua Esquenazi a,d , Sean I. Savitz b , Ramy El Khoury c , Megan A. McIntosh b , James C. Grotta e , Nitin Tandon a,d,∗ a
Vivian L Smith Department of Neurosurgery, University of Texas Medical School at Houston„ USA Department of Neurology, University of Texas Medical School at Houston, USA c Department of Neurology, Tulane University, USA d Mischer Neuroscience Institute, Memorial Hermann Hospital, Houston, TX, USA e Clinical Innovation and Research Institute, Memorial Hermann Hostpial - Texas Medical Center, USA b
a r t i c l e
i n f o
Article history: Received 23 September 2014 Received in revised form 18 October 2014 Accepted 20 November 2014 Available online 27 November 2014 Keywords: Craniectomy Intracerebral hematoma Cerebral edema Hypertensive hemorrhage
a b s t r a c t Objective: The management of patients with supra-tentorial intracerebral hemorrhage (ICH) remains controversial. Here we critically evaluate the safety, feasibility, and outcomes following decompressive hemicraniectomy (HC) with or without clot evacuation in the management of patients with large ICHs. Methods: We analyzed data from 73 consecutive patients managed with a HC for a spontaneous ICH. All relevant patient variables at initial presentation and management were compiled. Variables were modeled as independent regressors against the three-month Glasgow Outcome Score using a multivariate logistic regression model. Results: Over 7 years, HC was performed in 73 patients with clot evacuation in 86% and HC alone in 14%. The average ICH volume was 81 cc and the median HC surface area was 105 cm2 . 26 patients were comatose at initial presentation. Three-month functional outcomes were favorable in 29%, unfavorable in 44% and 27% of patients expired. Admission Glasgow Coma Scale (p = 0.003), dominant hemisphere ICH location (p = 0.01) and hematoma volume (p = 0.002) contributed significantly to the outcome, as estimated by a multivariate analysis. Eight surgical complications occurred. Conclusions: Early HC with or without clot evacuation is feasible and safe for managing spontaneous ICH. Our experience in this uncontrolled retrospective series, the largest such series in the modern era, suggests that it may be of particular benefit in patients with large non-dominant hemisphere ICH who are not moribund at presentation. Our findings suggest that a prospective randomized trial of HC vs. craniotomy for ICH be conducted. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Spontaneous intra-cerebral hemorrhage (ICH), accounts for 10–15% of all strokes in western countries, with a higher incidence in Asian and African-American populations. It is associated with a one-month fatality rate of around 40% [1]. The dismal outcome of patients with ICH, results from the structural loss of essential deep nuclei and from white matter tract disruption, caused by direct injury caused by hematoma [2], loss of cerebral auto regulation and delayed brain swelling. The management strategies for patients with spontaneous supra-tentorial ICH are still
∗ Corresponding author at: 6400 Fannin, Suite 2800, Houston 77030, USA. Tel.: +1 713 704 7123; fax: +1 713 704 7150. E-mail address: [email protected] (N. Tandon). http://dx.doi.org/10.1016/j.clineuro.2014.11.015 0303-8467/© 2014 Elsevier B.V. All rights reserved.
controversial and the role of surgical intervention remains uncertain, despite the advent of minimally invasive techniques. The results of the Surgical Trial in Intra-cerebral Hemorrhage (STICH) [3] and other randomized controlled trials suggest that surgery does not appear to offer any great advantage over conservative medical management in these patients [3–5]. Other randomized studies and several meta-analyses [6–12] have not yet been able to clearly elucidate the role of surgical management for this condition. Most recently, the STICH II trial data suggests that early surgery may have a small but clinically relevant survival advantage for patients with superficial hemorrhages without intra-ventricular hemorrhage (IVH) [13]. Minimally invasive surgical therapies for ICH, using recombinant tissue plasminogen activator (rtPA), and locally delivered ultrasound and thrombolytics are being currently evaluated (MISTIE, CLEAR and SLEUTH trials) [14–16], as is the use of the PPAR gamma agonist – pioglitazone [17,18]. The utility of
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Y. Esquenazi et al. / Clinical Neurology and Neurosurgery 128 (2015) 117–122
these minimally invasive approaches is still being characterized, and the optimal management of ICH is still far from clear. Yet, several patients with large ICHs present a management dilemma in that they may have a reasonable neurological examination at presentation that worsens despite maximal medical management, or may be young, or may have hemorrhages in the non-dominant hemisphere. In such young patients, and even in older patients with large hematomas, significant delayed edema is often seen after an ICH, adding to the elevated intracranial pressure (ICP) and compounding the neural insult. In these situations, there is often no equipoise regarding medical vs. surgical management and instead, management decisions center around urgent surgical intervention vs. a determination of futility. These situations raise important, unanswered questions about the role, timing, nature and outcomes following surgical intervention. A variety of experimental studies have suggested several phases of edema formation following ICH [19]. Peri-hematoma edema volume in humans increases by approximately 75% during the first 24 h after ictus, and the edema around the clot can eventually occupy a volume larger than that of the hematoma itself [20,21]. The cascade of events resulting from worsening edema lead to increased mass effect with damage to adjacent structures/white matter tracts; consequences that could be prevented by an early decompression of the brain by a hemicraniectomy (HC). HC for ICH has previously been reported as small retrospective studies, and by anecdotal case reports [22–27]. These studies have suggested improvements in postoperative mortality and morbidity, as well as improved frequency of good functional outcomes. Furthermore, there are instances where clot removal is difficult due to its deep location, or is incomplete after an attempted clot removal. In both of these instances, technical approaches that mitigate against (ICP) elevation are potentially useful. This is the motivation for this analysis of our experience with the use of early HC in the management of spontaneous supratentorial ICH at our center. 2. Materials and methods A prospectively compiled database of stroke patients was used to identify patients with spontaneous ICH who underwent HC at a single institution from April 2004 to September 2011, within 96 h of the ictus, excluding those with vascular or neoplastic etiology. The local institutional Committee for Protection of Human Subjects approved study design and execution. From the electronic medical record, we compiled demographics, data regarding admission Glasgow Coma Scale (GCS) [28], hemorrhage location (lobar, basal ganglia or both), hemorrhage hemisphere (right vs. left), volume (cc), total craniectomy surface area (cm2 ), presence or absence of IVH, whether or not an external ventricular drain (EVD) was placed, whether clot evacuation or only a HC was performed, the number of days between admission and surgery, length of stay (LOS) in the intensive care unit, total hospital LOS and Glasgow Outcome Scale (GOS) 37 at discharge. Patients were also categorized as having a good or a poor prognosis using the median prognostic score computed by the following equation which has previously been used in the STICH trial as a prognostication tool following ICH [3]: Prognostic score = (10 × admission GCS) − age (years) − (0.64 × volume [ml]). Surgical complications were also assessed, and data regarding the need for ventriculo-peritoneal shunt (VPS) placement, as well as complications from the cranioplasty procedure were compiled. ICH volume was calculated using the ABC/2 method [29], and the total HC size was estimated by a neurosurgeon
by measuring the distance between the posterior and anterior margins of the bone defect on serial 5 mm CT slices. The total area of cranial decompression was calculated by multiplying this value by the slice thickness and then summating it across all slices [30]. Decompressive HC was performed in the fronto-temporo-parietal region. Large bone flaps were removed in each case, followed by a wide non-constricting expansive duraplasty using a reconstituted bovine collagen allograft. A trans-cortical approach to the ICH was used in all cases in which the clot was evacuated. Bone flaps were stored in the tissue bank ( 60 cc, only 33% had a favorable outcome. While these results seem to suggest a better outcome in this group, these patients where younger, had a better neurological condition prior to surgery, and 80% had hemorrhages in the right hemisphere.
Y. Esquenazi et al. / Clinical Neurology and Neurosurgery 128 (2015) 117–122
The small size of this group precludes meaningful statistical comparisons with the larger cohort. Additionally, the possible benefits of HC need to be weighted against the risks. A variety of complications can occur following a HC – these include epidural, subdural hematomas, subdural effusions or hygromas, external cerebral herniation, wound healing problems and wound infections, hydrocephalus, syndrome of the trephined, bone flap resorption after cranioplasty and others [45]. Once patients undergo HC, survivors need to undergo a second surgical intervention to repair the cranial defect (cranioplasty). In our series of 73 patients, there were surgical complication of the original surgery in 6 patients and 2 had infections related to ventricular drains. 33 of the survivors (62%) had undergone an autologous cranioplasty at the time of data compilation, and only two complications were found. Additionally 7 (13%) patients had undergone the placement of a VPS for hydrocephalus, without any complications. Taken together, our cohort had larger hemorrhages (mean volume 81 cc, and median 71 cc compared with 40 cc in the STICH trial), than most reported series. In other words, there was rarely equipoise regarding medical vs. surgical management in this group. Instead, management decisions were chiefly between surgical intervention vs. a determination of futility based on the patient’s clinical state and imaging findings. In this cohort with large hemorrhages, we found that the largest (i.e. massive) hemorrhages were associated with a lower GCS at presentation, were more likely in older patients, were more likely to be taken earlier to surgery, but were associated with a worse overall outcome. Prompt evacuation and HC for the smaller (i.e. moderate sized) hemorrhages in the non-dominant hemisphere of younger patients presenting with a better examination may lead to better outcomes than traditional surgical approaches. 5. Conclusions The current study shows that HC in the management of ICH is feasible, and safe. The retrospective and uncontrolled design of this study precludes strong statements about our data, but despite poor prognostic scores, lower GCS and large clot sizes, the outcomes in our series are favorably comparable with other historical cohorts. HC in addition to early clot evacuation, especially in right hemisphere hemorrhages in younger patients who are not moribund may decrease mortality. It may lead to better functional outcomes than would otherwise be anticipated and deserves further study as part of a prospective randomized trial that critically compares craniectomy vs. craniotomy in the management of large ICHs. Acknowledgement The authors would like to thank all of the members of the neurosurgery, neurology and intensive care teams, and the nurses that contributed to the care of these patients at the Mischer Neuroscience Institute in Memorial Hermann Hospital. References [1] 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(2):167–76. [2] Gebel Jr JM, Jauch EC, Brott TG, Khoury J, Sauerbeck L, Salisbury S, et al. Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 2002;33(11):2636–41. [3] Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, et al. 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):387–97. [4] Fernandes HM, Gregson B, Siddique S, Mendelow AD. Surgery in intracerebral hemorrhage: the uncertainty continues. Stroke 2000;31(10):2511–6.
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[5] Mitchell P, Gregson BA, Vindlacheruvu RR, Mendelow AD. Surgical options in ICH including decompressive craniectomy. J Neurol Sci 2007;261(1/2):89–98. [6] 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(10):1103–6. [7] 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(4):530–5. [8] 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(5):755–8. [9] Morgenstern LB, Frankowski RF, Shedden P, Pasteur W, Grotta JC. Surgical treatment for intracerebral hemorrhage (STICH): a single-center, randomized clinical trial. Neurology 1998;51(5):1359–63. 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Int J Stroke 2013;8(5):388–96. [19] Xi G, Keep RF, Hoff JT. Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J Neurosurg 1998;89(6):991–6. [20] Xi G, Fewel ME, Hua Y, Thompson Jr BG, Hoff JT, Keep RF. Intracerebral hemorrhage: pathophysiology and therapy. Neurocrit Care 2004;1(1):5–18. [21] Gebel Jr 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(11):2631–5. [22] Dierssen G, Carda R, Coca JM. The influence of large decompressive craniectomy on the outcome of surgical treatment in spontaneous intracerebral haematomas. Acta Neurochir (Wien) 1983;69(1–2):53–60. [23] Ma L, Liu WG, Sheng HS, Fan J, Hu WW, Chen JS. Decompressive craniectomy in addition to hematoma evacuation improves mortality of patients with spontaneous basal ganglia hemorrhage. J Stroke Cerebrovasc Dis 2010;19(4):294–8. 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Stroke 1996;27(8):1304–5. [30] Curry Jr WT, Sethi MK, Ogilvy CS, Carter BS. Factors associated with outcome after hemicraniectomy for large middle cerebral artery territory infarction. Neurosurgery 2005;56(4):681–92, discussion 681–92. [31] Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975;1(7905):480–4. [32] Vahedi K, Hofmeijer J, Juettler E, Vicaut E, George B, Algra A, et al. Early decompressive surgery in malignant infarction of the middle cerebral artery: a pooled analysis of three randomised controlled trials. Lancet Neurol 2007;6(3):215–22. [33] Doerfler A, Forsting M, Reith W, Staff C, Heiland S, Schabitz WR, et al. Decompressive craniectomy in a rat model of malignant cerebral hemispheric stroke:
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Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Decompressive hemicraniectomy with or without clot evacuation for large spontaneous supratentorial intracerebral hemorrhages Yoshua Esquenazi a,d , Sean I. Savitz b , Ramy El Khoury c , Megan A. McIntosh b , James C. Grotta e , Nitin Tandon a,d,∗ a
Vivian L Smith Department of Neurosurgery, University of Texas Medical School at Houston„ USA Department of Neurology, University of Texas Medical School at Houston, USA c Department of Neurology, Tulane University, USA d Mischer Neuroscience Institute, Memorial Hermann Hospital, Houston, TX, USA e Clinical Innovation and Research Institute, Memorial Hermann Hostpial - Texas Medical Center, USA b
a r t i c l e
i n f o
Article history: Received 23 September 2014 Received in revised form 18 October 2014 Accepted 20 November 2014 Available online 27 November 2014 Keywords: Craniectomy Intracerebral hematoma Cerebral edema Hypertensive hemorrhage
a b s t r a c t Objective: The management of patients with supra-tentorial intracerebral hemorrhage (ICH) remains controversial. Here we critically evaluate the safety, feasibility, and outcomes following decompressive hemicraniectomy (HC) with or without clot evacuation in the management of patients with large ICHs. Methods: We analyzed data from 73 consecutive patients managed with a HC for a spontaneous ICH. All relevant patient variables at initial presentation and management were compiled. Variables were modeled as independent regressors against the three-month Glasgow Outcome Score using a multivariate logistic regression model. Results: Over 7 years, HC was performed in 73 patients with clot evacuation in 86% and HC alone in 14%. The average ICH volume was 81 cc and the median HC surface area was 105 cm2 . 26 patients were comatose at initial presentation. Three-month functional outcomes were favorable in 29%, unfavorable in 44% and 27% of patients expired. Admission Glasgow Coma Scale (p = 0.003), dominant hemisphere ICH location (p = 0.01) and hematoma volume (p = 0.002) contributed significantly to the outcome, as estimated by a multivariate analysis. Eight surgical complications occurred. Conclusions: Early HC with or without clot evacuation is feasible and safe for managing spontaneous ICH. Our experience in this uncontrolled retrospective series, the largest such series in the modern era, suggests that it may be of particular benefit in patients with large non-dominant hemisphere ICH who are not moribund at presentation. Our findings suggest that a prospective randomized trial of HC vs. craniotomy for ICH be conducted. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Spontaneous intra-cerebral hemorrhage (ICH), accounts for 10–15% of all strokes in western countries, with a higher incidence in Asian and African-American populations. It is associated with a one-month fatality rate of around 40% [1]. The dismal outcome of patients with ICH, results from the structural loss of essential deep nuclei and from white matter tract disruption, caused by direct injury caused by hematoma [2], loss of cerebral auto regulation and delayed brain swelling. The management strategies for patients with spontaneous supra-tentorial ICH are still
∗ Corresponding author at: 6400 Fannin, Suite 2800, Houston 77030, USA. Tel.: +1 713 704 7123; fax: +1 713 704 7150. E-mail address: [email protected] (N. Tandon). http://dx.doi.org/10.1016/j.clineuro.2014.11.015 0303-8467/© 2014 Elsevier B.V. All rights reserved.
controversial and the role of surgical intervention remains uncertain, despite the advent of minimally invasive techniques. The results of the Surgical Trial in Intra-cerebral Hemorrhage (STICH) [3] and other randomized controlled trials suggest that surgery does not appear to offer any great advantage over conservative medical management in these patients [3–5]. Other randomized studies and several meta-analyses [6–12] have not yet been able to clearly elucidate the role of surgical management for this condition. Most recently, the STICH II trial data suggests that early surgery may have a small but clinically relevant survival advantage for patients with superficial hemorrhages without intra-ventricular hemorrhage (IVH) [13]. Minimally invasive surgical therapies for ICH, using recombinant tissue plasminogen activator (rtPA), and locally delivered ultrasound and thrombolytics are being currently evaluated (MISTIE, CLEAR and SLEUTH trials) [14–16], as is the use of the PPAR gamma agonist – pioglitazone [17,18]. The utility of
118
Y. Esquenazi et al. / Clinical Neurology and Neurosurgery 128 (2015) 117–122
these minimally invasive approaches is still being characterized, and the optimal management of ICH is still far from clear. Yet, several patients with large ICHs present a management dilemma in that they may have a reasonable neurological examination at presentation that worsens despite maximal medical management, or may be young, or may have hemorrhages in the non-dominant hemisphere. In such young patients, and even in older patients with large hematomas, significant delayed edema is often seen after an ICH, adding to the elevated intracranial pressure (ICP) and compounding the neural insult. In these situations, there is often no equipoise regarding medical vs. surgical management and instead, management decisions center around urgent surgical intervention vs. a determination of futility. These situations raise important, unanswered questions about the role, timing, nature and outcomes following surgical intervention. A variety of experimental studies have suggested several phases of edema formation following ICH [19]. Peri-hematoma edema volume in humans increases by approximately 75% during the first 24 h after ictus, and the edema around the clot can eventually occupy a volume larger than that of the hematoma itself [20,21]. The cascade of events resulting from worsening edema lead to increased mass effect with damage to adjacent structures/white matter tracts; consequences that could be prevented by an early decompression of the brain by a hemicraniectomy (HC). HC for ICH has previously been reported as small retrospective studies, and by anecdotal case reports [22–27]. These studies have suggested improvements in postoperative mortality and morbidity, as well as improved frequency of good functional outcomes. Furthermore, there are instances where clot removal is difficult due to its deep location, or is incomplete after an attempted clot removal. In both of these instances, technical approaches that mitigate against (ICP) elevation are potentially useful. This is the motivation for this analysis of our experience with the use of early HC in the management of spontaneous supratentorial ICH at our center. 2. Materials and methods A prospectively compiled database of stroke patients was used to identify patients with spontaneous ICH who underwent HC at a single institution from April 2004 to September 2011, within 96 h of the ictus, excluding those with vascular or neoplastic etiology. The local institutional Committee for Protection of Human Subjects approved study design and execution. From the electronic medical record, we compiled demographics, data regarding admission Glasgow Coma Scale (GCS) [28], hemorrhage location (lobar, basal ganglia or both), hemorrhage hemisphere (right vs. left), volume (cc), total craniectomy surface area (cm2 ), presence or absence of IVH, whether or not an external ventricular drain (EVD) was placed, whether clot evacuation or only a HC was performed, the number of days between admission and surgery, length of stay (LOS) in the intensive care unit, total hospital LOS and Glasgow Outcome Scale (GOS) 37 at discharge. Patients were also categorized as having a good or a poor prognosis using the median prognostic score computed by the following equation which has previously been used in the STICH trial as a prognostication tool following ICH [3]: Prognostic score = (10 × admission GCS) − age (years) − (0.64 × volume [ml]). Surgical complications were also assessed, and data regarding the need for ventriculo-peritoneal shunt (VPS) placement, as well as complications from the cranioplasty procedure were compiled. ICH volume was calculated using the ABC/2 method [29], and the total HC size was estimated by a neurosurgeon
by measuring the distance between the posterior and anterior margins of the bone defect on serial 5 mm CT slices. The total area of cranial decompression was calculated by multiplying this value by the slice thickness and then summating it across all slices [30]. Decompressive HC was performed in the fronto-temporo-parietal region. Large bone flaps were removed in each case, followed by a wide non-constricting expansive duraplasty using a reconstituted bovine collagen allograft. A trans-cortical approach to the ICH was used in all cases in which the clot was evacuated. Bone flaps were stored in the tissue bank ( 60 cc, only 33% had a favorable outcome. While these results seem to suggest a better outcome in this group, these patients where younger, had a better neurological condition prior to surgery, and 80% had hemorrhages in the right hemisphere.
Y. Esquenazi et al. / Clinical Neurology and Neurosurgery 128 (2015) 117–122
The small size of this group precludes meaningful statistical comparisons with the larger cohort. Additionally, the possible benefits of HC need to be weighted against the risks. A variety of complications can occur following a HC – these include epidural, subdural hematomas, subdural effusions or hygromas, external cerebral herniation, wound healing problems and wound infections, hydrocephalus, syndrome of the trephined, bone flap resorption after cranioplasty and others [45]. Once patients undergo HC, survivors need to undergo a second surgical intervention to repair the cranial defect (cranioplasty). In our series of 73 patients, there were surgical complication of the original surgery in 6 patients and 2 had infections related to ventricular drains. 33 of the survivors (62%) had undergone an autologous cranioplasty at the time of data compilation, and only two complications were found. Additionally 7 (13%) patients had undergone the placement of a VPS for hydrocephalus, without any complications. Taken together, our cohort had larger hemorrhages (mean volume 81 cc, and median 71 cc compared with 40 cc in the STICH trial), than most reported series. In other words, there was rarely equipoise regarding medical vs. surgical management in this group. Instead, management decisions were chiefly between surgical intervention vs. a determination of futility based on the patient’s clinical state and imaging findings. In this cohort with large hemorrhages, we found that the largest (i.e. massive) hemorrhages were associated with a lower GCS at presentation, were more likely in older patients, were more likely to be taken earlier to surgery, but were associated with a worse overall outcome. Prompt evacuation and HC for the smaller (i.e. moderate sized) hemorrhages in the non-dominant hemisphere of younger patients presenting with a better examination may lead to better outcomes than traditional surgical approaches. 5. Conclusions The current study shows that HC in the management of ICH is feasible, and safe. The retrospective and uncontrolled design of this study precludes strong statements about our data, but despite poor prognostic scores, lower GCS and large clot sizes, the outcomes in our series are favorably comparable with other historical cohorts. HC in addition to early clot evacuation, especially in right hemisphere hemorrhages in younger patients who are not moribund may decrease mortality. It may lead to better functional outcomes than would otherwise be anticipated and deserves further study as part of a prospective randomized trial that critically compares craniectomy vs. craniotomy in the management of large ICHs. Acknowledgement The authors would like to thank all of the members of the neurosurgery, neurology and intensive care teams, and the nurses that contributed to the care of these patients at the Mischer Neuroscience Institute in Memorial Hermann Hospital. References [1] 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(2):167–76. [2] Gebel Jr JM, Jauch EC, Brott TG, Khoury J, Sauerbeck L, Salisbury S, et al. Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 2002;33(11):2636–41. [3] Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, et al. 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):387–97. [4] Fernandes HM, Gregson B, Siddique S, Mendelow AD. Surgery in intracerebral hemorrhage: the uncertainty continues. Stroke 2000;31(10):2511–6.
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