Journal of Clinical Neuroscience 20 (2013) 6–12 Contents lists available at SciVerse ScienceDirect Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn Review Hemicraniectomy in the management of space-occupying ischemic stroke Julia Flechsenhar a, Johannes Woitzik b, Klaus Zweckberger c, Hemasse Amiri d, Werner Hacke d, Eric Jüttler a,d,⇑ a Center for Stroke Research Berlin (CSB), Charité-University Medicine Berlin, Berlin, Germany Department of Neurosurgery, Charité-University Medicine Berlin, Berlin, Germany c Department of Neurosurgery, University of Heidelberg, Heidelberg, Germany d Department of Neurology, University of Heidelberg, Heidelberg, Germany b a r t i c l e i n f o Article history: Received 31 December 2011 Accepted 13 February 2012 Keywords: Decompressive hemicraniectomy Ischemic stroke Malignant infarction a b s t r a c t A space-occupying mass effect is a common ﬁnding in several stroke subtypes. A large, intracranial mass is a potentially life-threatening complication, irrespective of its underlying origin, with transtentorial or transforaminal herniation being the common endpoint and often the cause of death. Prompt and adequate intervention is therefore required. Although sufﬁcient data on the management of large haematomas are lacking, there is good evidence from randomized trials that in younger patients with life-threatening, space-occupying, so-called ‘‘malignant’’ middle cerebral artery (MCA) infarctions, early hemicraniectomy decreases mortality without increasing the number of severely disabled survivors. Yet many questions concerning hemicraniectomy in malignant MCA infarction remain open: the deﬁnition of a malignant MCA infarct within the ﬁrst hours, optimal timing of surgery, quality of life and acceptance of remaining disability, the role of aphasia in patients with dominant hemispheric infarcts, the effect of age, and the inﬂuence of the pre-morbid status on decision making. The joint efforts of neurologists, neurosurgeons, intensive care physicians, and rehabilitation physicians are needed to design and conduct studies that might answer these questions. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction and deﬁnition Regardless of the underlying pathology, all types of stroke are associated with accompanying brain edema, which is classiﬁed traditionally into three subtypes: vasogenic, cytotoxic and interstitial. In severe ischemic stroke, a combination is always found, with cytotoxic brain edema having the leading role.1–4 In most patients, accompanying brain edema does not lead to a relevant mass effect, but between 1% and 10% of supratentorial ischemic infarctions are associated with serious brain swelling, which usually manifests between 2 days and 5 days after stroke. Clinically, the formation of serious brain edema after MCA infarction follows a uniform course beginning with compression of the ventricular system, subsequent brain tissue shift, usually to the contralateral side, compression of formerly healthy brain structures, and later a critical increase of intracranial pressure (ICP) with subsequent complications such as compromised cerebral blood ﬂow, and ﬁnally transtentorial or transforaminal herniation and death. Under standard care up to 80% of patients meet this fate within the ﬁrst week after symptom ⇑ Corresponding author. Present address: Department of Neurology, Rehabilitation and University Hospitals Ulm, Oberer Eselsberg 45, D-89081 Ulm, Germany. Tel.: +49 731 177 5263; fax: +49 731 177 1202. E-mail address: [email protected] (E. Jüttler). 0967-5868/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jocn.2012.02.019 onset.5–12 The term ‘‘malignant MCA infarction’’ was coined5 for these catastrophic infarctions (Fig. 1). 2. Diagnosis Early diagnosis and prediction of a malignant course are important for the timely identiﬁcation of patients who may require closer monitoring and may proﬁt from more aggressive intervention.13 Although the term ‘‘malignant MCA infarction’’ was introduced in 1996, there is still no generally accepted deﬁnition of this condition, especially early after symptom onset.5 This lack of a clear deﬁnition has been superseded by the uniform inclusion criteria of several trials, deﬁning a population in whom particular interventions were deployed.14–18 Based on the inclusion and exclusion criteria of these trials, the diagnosis of a ‘‘malignant MCA infarction’’ can be made by assessing clinical presentation at stroke onset, the clinical course, and neuroimaging ﬁndings. At presentation patients suffering from a malignant MCA infarction show dense hemiplegia, head and eye deviation, unilateral severe hypaesthesia or anaesthesia, often hemianopsia and always a multimodal neglect syndrome and global aphasia (when the dominant hemisphere is affected). The National Institutes of Health Stroke Scale (NIHSS) score is typically > 15.13–16 The NIHSS 7 J. Flechsenhar et al. / Journal of Clinical Neuroscience 20 (2013) 6–12 Fig. 1. Axial CT scans (left to right: 24, 36, 72 and 96 hours after symptom onset) showing the natural course of malignant middle cerebral artery infarction. Massive spaceoccupying edema with brain tissue shift resulted in transtentorial herniation. (Reproduced from Future Neurology, May 2008, Vol. 3, No. 3, Pages 251–6438 with the permission of Future Medicine Ltd.). score, however, underestimates the severity of a non-dominant infarction.13 The typical clinical course of patients with a malignant MCA infarction starts with a very early impaired level of consciousness (score of P1 in item 1a of the NIHSS or <14 on the Glasgow Coma Scale [GCS]), often even at ﬁrst presentation or within the ﬁrst few hours, followed by a progressive deterioration over the next 24 hours to 48 hours, regularly associated with a reduced ventilatory drive, usually requiring mechanical ventilation.5,13,14,17 On neuroimaging, the relative and absolute infarction size, as viewed on CT scans or MRI, seems to be major determinant for the development of life-threatening edema after MCA infarction. If at least 2/3 of the MCA territory or > 82 mL on diffusionweighted imaging (DWI) is involved, the infarct size has a positive and negative predictive value of about 90%, especially when combined with MCA plus internal carotid artery occlusion.14,15,18–21 between patients, so body and head positioning should be tested individually and adapted continuously by monitoring ICP and CPP in different positions and taking into account ventilation and blood ﬂow in the jugular veins. As an example of a speciﬁc conservative intervention, the antiedematous effect of osmotic substances is, at least from a physiological point of view, based on the integrity of the blood–brain barrier, which, however, is largely disrupted in the infarcted territory. Therefore, osmotic therapy seems of little pathophysiological value. Most other intensive care measures aim to lower ICP, but signiﬁcant increases in ICP usually occur late, when local mass effect has already led to severe destruction of vital brain structures. Sometimes herniation may even occur before signiﬁcant increases in ICP.29 3. Treatment options In contrast to the rather complex and poorly understood pathophysiological theories underlying conservative treatments, the beneﬁts of decompressive surgery are based on purely mechanical effects. In malignant MCA infarction, ipsilateral hemicraniectomy (‘‘external decompressive surgery’’) is the procedure most widely recommended and frequently followed. Additional removal of necrotic tissue, usually temporal lobectomy (‘‘internal decompression’’) is more controversial.30–32 Serious complications from hemicraniectomy seem uncommon, although no reliable data are available so far. Wound and bone infections, epidural or subdural hematomas, hygroma, hydrocephalus or the sinking skin ﬂap syndrome and paradoxical herniation have been reported.30,33–36 A far more common and widely underestimated complication arises when hemicraniectomy is insufﬁcient and leads to local shear stress and venous insufﬁciency at the bone margins, and at worst, to herniation through the craniectomy defect.37 A sufﬁcient diameter is critical, not only to prevent these complications but also for the craniectomy to be effective: The volume of brain tissue shifting out of the skull is directly correlated to the diameter of the bone ﬂap removed. The following formula is based on the assumption of a globus and a circular bone ﬂap, but may be used to estimate the volume gain (for deﬁnitions of the variables see Fig. 2): The therapeutic goal of any treatment in malignant MCA infarction is to interrupt the vicious cycle of brain swelling, mass effect, increased intracranial pressure (ICP), reduced cerebral perfusion and energy supply, further brain tissue damage, subsequent edema formation, and ﬁnally, herniation. 3.1. Conservative therapy Basic conservative therapy is not different from that applied for stroke in general and aims to optimize cerebral perfusion and energy supply and to minimize cerebral metabolic demands by general measures such as adequate oxygen supply, maintenance of adequate blood pressure, normothermia, and optimal body and head positioning. Speciﬁc conservative interventions in malignant MCA infarction may include deep sedation, barbiturates, buffers, hypothermia, osmotic therapy, steroids, and controlled hyperventilation.22,23 To our knowledge, there is no adequate evidence to support any of these therapies in malignant MCA infarction.22–24 The results from randomized trials indicate that these measures may not be much better than palliative care, and several reports suggest that some are not only largely ineffective but may be even harmful.6,14,15,17,18,22–28 There are various possible explanations why these therapies often fail. For example, upright body positioning for basic management is often recommended and is said to lower ICP through improved venous drainage. However, the effect of body positioning on ICP and cerebral perfusion pressure (CPP) differs greatly 3.2. Surgical intervention Additional volume ¼ p h22 3 ð3 r2 h2 Þ p h21 3 ð3 r1 h1 Þ Malignant MCA infarctions usually require an additional volume of P 80 mL to 100 mL, so the diameter of the craniectomy should be at least 12 cm to be effective (Fig. 2).38 8 J. Flechsenhar et al. / Journal of Clinical Neuroscience 20 (2013) 6–12 Fig. 2. (a) Diagram of a hemicraniectomy in a malignant middle cerebral artery infarction showing the parameters used to calculate the relationship between the diameter of the craniotomy and volume gain. (Reproduced from Future Neurology, May 2008, Vol. 3, No. 3, Pages 251–6438 with the permission of Future Medicine Ltd.) (b) Graph showing the relationship between the diameter of the hemicraneictomy and the volume gain. r = radius, h = the distance from the thin white line joining the edges of the craniectomy defect to the dura. 3.3. Clinical experience Dating back to at least 1935,39 hemicraniectomy in space-occupying stroke is by no means new. A continuously growing body of evidence from observational and comparative studies and parallel ﬁndings in animal studies provides evidence for the beneﬁts of hemicraniectomy in lowering mortality and improving functional outcome in survivors of malignant MCA infarction, yet the procedure remains an intensely debated issue in neurointensive care.14,40–45 Between 2000 and 2009 seven randomized and controlled trials were initiated: (i) The American Hemicraniectomy And Durotomy Upon Deterioration From Infarction Related Swelling Trial (HeADDFIRST); (ii) the German DEcompressive Surgery for the Treatment of malignant INfarction of the middle cerebral arterY (DESTINY) trial; (iii) the French DEcompressive Craniectomy In MALignant middle cerebral artery infarcts (DECIMAL) trial; (iv) the Dutch Hemicraniectomy After Middle cerebral artery infarction with Life-threatening Edema Trial (HAMLET); (v) the Philippine HEmicraniectomy for Malignant Middle cerebral artery Infarcts (HeMMI) trial; (vi) the Turkish DEcompressive surgery for the treatment of Malignant Infarction of the middle cerebral artery in a TURkish population (DEMITUR) trial; and (vii) the Decompressive Hemicraniectomy in Malignant Middle Cerebral Artery Infarction: a Randomized Controlled Trial Enrolling a Group of Patients Older than 60 Years of Age.14,17,18,46–49 Results are available from DESTINY, DECIMAL, HAMLET, and a pooled analysis of these three trials.16 All three trials had similar inclusion and exclusion criteria including clinical signs of infarction in the territory of the MCA, a decrease in the level of consciousness, a pre-existing modiﬁed Rankin Scale (mRS) score of 0 or 1, and life expectancy of at least 3 years in each trial. DECIMAL included patients 18 years to 55 years of age, whereas HAMLET and DESTINY included patients aged 18 years to 60 years of age. In DECIMAL a score on the National Institutes of Health Stroke Scale (NIHSS) of >15 was an inclusion criterion for patients with infarctions of the dominant or non-dominant hemispheres. HAMLET and DESTINY used different criteria for the NIHSS scores depending on the affected hemisphere: >15 in HAMLET and >18 in DESTINY for infarctions of the non-dominant hemisphere, and >20 for infarctions of the dominant hemisphere. Inclusion criteria on neuroimaging also differed between the three trials: In HAMLET and DESTINY, at least two-thirds of the MCA territory, and in DESTINY, at least part of the basal ganglia needed to be involved, whereas in DECIMAL more than 50% with a volume of at least 145 mL in DWI needed to be involved. In HAMLET patients with infarctions of the complete hemisphere were excluded, whereas in DECIMAL and DESTINY, patients with additional anterior and/or posterior cerebral artery infarctions could enter the study. For differences in time to treatment, see Table 1. The primary outcome measure in DECIMAL and DESTINY was the mRS score dichotomized into 0–3 compared to 4–6 after 6 months, whereas in HAMLET this same primary endpoint was assessed after 1 year. DESTINY and DECIMAL assessed mRS scores after 1 year as a secondary endpoint. All three trials used a 1:1 randomization to either hemicraniectomy or conservative treatment. Treatment protocols were broadly similar. All three trials were stopped prematurely: DECIMAL was designed to include a maximum of 60 patients based on interim analyses. Recruitment was stopped in March 2006, however, after only 38 patients had been enrolled between December 2001 and November 2005, because of the slow enrolment, because there 9 J. Flechsenhar et al. / Journal of Clinical Neuroscience 20 (2013) 6–12 Table 1 DECIMAL, DESTINY and HAMLET trials on the effect of decompressive hemicraniectomy (DHC) in the management of space-occupying ischemic stroke Trial and treatment type DESTINY DHC Conservative DECIMAL DHC Conservative HAMLET DHC Conservative HAMLET DHC Conservative Time to treatment (hours) Mortality after 1 year (%) Absolute risk reduction (%) <36 18 53 35 <43 25 78 53 <51 19 78 59 51–99 27 36 8 DECIMAL = the French DEcompressive Craniectomy In MALignant middle cerebral artery infarcts trial, DESTINY = the German DEcompressive Surgery for the Treatment of malignant INfarction of the middle cerebral artery, HAMLET = the Dutch Hemicraniectomy After Middle cerebral artery infarction with Life-threatening Edema Trial. was a signiﬁcant difference in mortality favoring decompressive surgery, and because the opportunity arose for a pooled analysis of the three trials. A total of 112 patients were to have been enrolled in HAMLET but recruitment was stopped in February 2008 on the advice of the data monitoring committee after an interim analysis of the primary endpoint of 50 patients made it highly unlikely that a statistically signiﬁcant difference would be seen at the end of the trial. At that time, 64 patients had been enrolled between November 2002 and October 2007. A maximum of 68 patients were to have been enrolled DESTINY using a sequential trial design based on mortality after 30 days. Recruitment was temporarily stopped in November 2005 after a planned interim analysis showed a signiﬁcant beneﬁt of surgery based on 30-day mortality. At this time 32 patients had been enrolled between February 2004 and October 2005. The trial was then stopped after a recalculation of the sample size projection based on the primary endpoint indicated that 188 patients would be needed to show a signiﬁcant difference14,15,18 Fig. 3 and Table 1 show the results of DESTINY, DECIMAL and HAMLET and pooled data of these trials. Surgical treatment is subdivided in patients operated within and beyond 48 hours after symptom onset. None of the three trials showed a statistically signiﬁcant difference between the two treatment groups for the mRS score dichotomized into 0–1 compared to 4–6, thereby missing their primary endpoints. Detailed comparative results of the three trials are provided in Table 2. Most deaths occurred early (DECIMAL: 100% within 4 weeks, DESTINY: 90% within 8 days, HAMLET: 91% within 14 days) and were due to transtentorial herniation, thereby contradicting the results of larger case series indicating that a considerable number of deaths occur after discharge.35 Interestingly, in patients treated early, mortality rates under conservative treatment in HAMLET and DECIMAL were much higher than in DESTINY: 78% compared to 53%. Comparatively low mortality rates in conservatively treated patients have also been reported in HeADDFIRST (46%). One explanation may be that most patients in DESTINY and HeADDFIRST were treated in an experienced neurocritical care unit including maximum invasive neuromonitoring and treatment, whereas in HAMLET and DECIMAL these patients were usually referred to a stroke unit14,15,18,47 Fig. 3. The pooled data showing functional outcome after 1 year of the French DEcompressive Craniectomy In MALignant middle cerebral artery infarcts trial (DECIMAL), the German DEcompressive Surgery for the Treatment of malignant INfarction of the middle cerebral arterY trial (DESTINY), and the Dutch Hemicraniectomy After Middle cerebral artery infarction with Life-threatening Edema Trial (HAMLET). Cons = conservative treatment, DHC = decompressive hemicraniectomy, mRS = modiﬁed Rankin Scale score. 10 J. Flechsenhar et al. / Journal of Clinical Neuroscience 20 (2013) 6–12 Table 2 Comparative results of primary and secondary endpoints of DESTINY, DECIMAL and HAMLET trials on the effect of decompressive hemicraniectomy in the management of spaceoccupying ischemic stroke Outcome at 30 days Mortality Outcome at 6 months mRS 63 mRS 64 DESTINY DECIMAL HAMLET * N.A. N.A. N.S. (PE) N.S. (PE) * ** N.A. N.A. N.A. mRS (non-dichotomized) Barthel Index NIHSS Mortality Outcome at 12 months mRS 63 mRS 64 mRS (non-dichotomized) Barthel Index NIHSS Mortality SIS SF-36 MADRS Retrospective ‘‘agreement to treatment’’ ‘‘Life worth living on follow-up’’ ’’Satisﬁed with treatment’’ * * N.S. N.A. N.A. * * ** N.S. N.S. * ** * ** N.A. N.A. N.A. N.A. N.S. (PE) N.S. N.D. N.S. N.A. N.S. N.S. N.S. N.S. * ** ** N.A. N.A. N.D. N.A. N.A. Patients: Surgical: 100% Medical: 100% N.A. Patients: Surgical: 100% Medical: 100% N.A. Physical domain: # Mental domain: N.S. N.S. Patients: Surgical: 100% Medical: 92% Caregivers: Surgical: 90% Medical: 92% MADRS = Montgomery and Asperg Depression Rating Scale, mRS = modiﬁed Rankin scale, N.A. = not assessed, N.D. = not determined (no statistical analysis), NIHSS = National Institutes of Health Stroke Scale, N.S. = no statistically signiﬁcant difference, PE = primary endpoint, SF-36 = Short Form-36 Questionnaire; SIS = Stroke Impact Scale. * p < 0.05 – a statistically signiﬁcant difference between surgically and medically treated patients in favor of surgery. ** p<0.01 – a highly signiﬁcant statistical difference between surgically and medically treated patients in favor of surgery; # p < 0.05 – a statistically signiﬁcant difference between surgically and medically treated patients in favor of medical treatment. Before these trials were completed, a prospectively planned pooled analysis including all patients from DECIMAL and DESTINY and 23 patients from HAMLET was performed, based on a protocol with uniform inclusion and exclusion criteria. This pooled analysis forms the basis of most current guidelines and recommendations for acute stroke treatment concerning surgical treatment of malignant MCA infarction:50–53 93 patients treated within 48 hours after symptom onset were included (51 treated by hemicraniectomy and 42 treated conservatively). Mortality at 1 year was signiﬁcantly decreased from 71.4% in the conservative group to 21.6% in the surgery group (absolute risk reduction 49.8%). More patients in the group treated surgically had an mRS score 64 (74.5% compared to 23.8%) and an mRS score 63 (43.1% compared to 21.4%). The numbers needed to treat (NNT) were: two patients for survival with an mRS score 64; four for survival with an mRS score 63; and two for survival irrespective of functional outcome. Very severe disability (mRS score 5) was not increased (4% after surgery compared to 5% after conservative treatment). The number of moderately to severely disabled patients (mRS score 4) increased from 2.4% after conservative treatment to 31.4% after hemicraniectomy.16 4. Open questions and future perspectives Although hemicraniectomy is a standard procedure in neurosurgery worldwide, there is no one standardized operative procedure.54 Opinions differ deeply regarding the diameter of craniectomy and the mode of duraplasty. Facts about the impact of these aspects on outcome are not available38 and they are still being researched.55 Another important aspect is the timing of hemicraniectomy. The randomized trials indicate that it beneﬁts patients only when performed early, at least within 48 hours of symptom onset. However, the number of patients in these trials who were treated within 48 hours is still very small, and a valid comparison with patients who have been treated later is not possible.14,16 As described in Section 3.3, the results from HAMLET are not helpful in this regard. Some studies suggest an improved outcome when hemicraniectomy is performed very early compared to delayed treatment.31,56 However, in other case series and non-randomized studies, the time to treatment had no inﬂuence on outcome.57,58 More data are needed from larger prospective registries to estimate the effect of early treatment as a possible basis for future trials. As long as these data are unavailable, hemicraniectomy should be performed as soon as possible. As in other diseases, but particularly in stroke, older patients with malignant MCA infarctions have a poorer outcome than do younger patients. There are several studies on hemicraniectomy in these patients that suggest age limits of 50 years, 55 years, or 60 years.35,58–69 Interpretation of these ﬁndings is limited by older patients undergoing surgery signiﬁcantly later in most of studies and being treated less aggressively than younger patients. The subgroup analyses of the randomized trials did not indicate poorer outcome in patients P50 years of age compared to younger patients, but were not powered to detect such differences.14,16 Furthermore, the age limit for inclusion in these trials was 60 years, and so far there are no data from randomized trials on patients older than 60 years. To further assess the question of how to treat older patients, DESTINY II is ongoing and has already enrolled more than 100 patients.70 Until the results are available, the choice of treatment in older patients with malignant MCA infarction is a difﬁcult decision that should be made on an individual basis.70–73 Treatment of patients with malignant MCA infarction of the dominant hemisphere is another controversial issue. In the past, in many centres, decompressive surgery was not considered. From the randomized trials and larger prospective case series there is no indication that patients with dominant malignant infarctions J. Flechsenhar et al. / Journal of Clinical Neuroscience 20 (2013) 6–12 do not proﬁt from surgical treatment.14,16 Neither mortality nor functional outcome seems dependent on the side of the lesion in any of the larger prospective studies.61 Indeed, the handicap caused by aphasia may be balanced by the neuropsychological deficits (that is, the severe attention deﬁcit, apraxia and anosognosia in patients with infarction of the non-dominant hemisphere).74,75 In addition, in the long term, aphasia in dominant malignant MCA infarction is rarely complete and shows remarkable improvement.30,33,62,74,76 Only a few studies suggest a more severe impairment in dominant malignant MCA infarction.77 Much criticism has been directed to the assessment strategies of functional outcome in studies and trials on malignant MCA infarction. It is often criticised that standard outcome measures such as the Barthel Index, Glasgow Outcome Scale and mRS, with their emphasis on motor abilities, may not account for all relevant remaining deﬁcits. Especially controversial is the dichotomization between favorable and unfavorable outcomes in a condition with a high mortality rate under conservative treatment and such severe primary disablement. It may be questioned as to whether the terms ‘‘favorable’’ and ‘‘unfavorable’’ apply here or whether they should be replaced by ‘‘acceptable’’ and ‘‘unacceptable’’ for the patients. To answer this question more data on the quality of life of patients after malignant MCA infarction are needed. 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