Abstract
Purpose: Decompressive craniectomy (DC) has been proposed as lifesaving treatment in aneurysmal subarachnoid haemorrhage (aSAH) patients with elevated intracranial pressure (ICP). However, data is sparse and controversy exists whether the underlying cause of elevated ICP influences neurological outcome. The purpose of this study is to clarify the role of the underlying cause of elevated ICP on outcome after DC.
Materials and methods: We retrospectively studied the one-year neurological outcome in a single-centre cohort to identify predictors of favourable (Glasgow Outcome Scale (GOS) 4–5) and unfavourable (GOS 1–3) outcome. Additionally, available individual patient data in the literature was reviewed with a special emphasis on the underlying reason for DC.
Results: From 2006–2015, 53 consecutive aSAH patients underwent DC. Nine (17%) achieved favourable, 44 (83%) unfavourable outcome (31 patients died). One fourth of the patients undergoing DC for hematoma or (hematoma-related) oedema survived favourably (increasing to 46% for patients aged <51 years), versus none of the patients undergoing DC for secondary infarction. Analysis of individual data of 105 literature patients showed a similar trend, although overall outcome was much better: half of the patients undergoing DC for hematoma/oedema regained independence, versus less than one-fourth of patients undergoing DC for secondary infarction.
Conclusions: DC in aSAH patients is associated with high rates of unfavourable outcome and mortality, but hematoma or oedema as underlying reason for DC is associated with better outcome profiles compared to secondary infarction. Future observational cohort studies are needed to further explore the different outcome profiles among subpopulations of aSAH patients requiring DC.
Introduction
Decompressive craniectomy (DC) lowers intracranial pressure (ICP) in traumatic brain injury (TBI) patients, and increases survival in patients with space-occupying middle cerebral artery (MCA) infarction.Citation1–3 Patients with poor-grade aneurysmal subarachnoid haemorrhage (aSAH) frequently suffer from uncontrollably elevated ICP caused by intracerebral hematoma, oedema and/or secondary infarction.Citation4 Data on survival and neurological outcome in aSAH patients undergoing DC is sparse, and the role of DC in aSAH patients is still in a process of being defined.Citation5 Studies reporting on the underlying cause of elevated ICP in aSAH patients and outcome after DC contradict each other: Buschmann et al stated that aSAH patients with progressive brain oedema without radiological signs of infarction and those with hematoma may benefit from DC but that DC should be set restrictively if secondary infarcts are manifest, whereas Güresir et al, however, did not find differences in outcome when patients were assorted by the underlying cause of elevated ICP.Citation6,Citation7
To further clarify this issue, we first analysed the long term neurological outcome in a cohort of consecutive aSAH patients undergoing DC in our academic centre. Second, patient characteristics were analysed in order to identify predictors of favourable and unfavourable outcome. Third, we performed a review of available individual patient data in the literature with a special emphasis on the underlying cause of elevated ICP.
Material and methods
Patients
This retrospective study included all aSAH patients who underwent DC between January 2006 and October 2015 in our academic centre. Patients were selected from a retrospectively created operative database that included all patients undergoing DC in the same time frame. Formal approval of the current retrospective patient chart study was waived by the institutional review board of our hospital. Patient consent was therefore not sought.
Clinical management and decompressive craniectomy
Treatment in the fields was provided by emergency physicians and paramedics, according to Advances Trauma Life Support, standards. Upon admission, patients were examined by a neurologist. Patients then underwent computed tomography (CT) imaging of the brain, where SAH was confirmed. All patients were treated according to our standardized protocol, which closely follows international guidelines.Citation8,Citation9 In short, CT-angiography was used to establish the aneurysmal cause of the SAH. In addition, by using digital subtraction angiography, the choice for clipping or coiling of the aneurysm was determined in consensus by a vascular neurosurgeon and an interventional neuro-radiologist. All ruptured aneurysms were treated as early as feasible (preferably within 24 hours). Following aneurysm treatment, coiled World Federation of Neurological Surgeons Grading System (WFNS) grade I patients were admitted to the brain care unit whereas all other patients were admitted to the intensive care unit (ICU). Nimodipine was administered in a dosage of 60 mg six times daily (or intravenously by continuous infusion if enteral administration was impossible). Whenever clinical signs of delayed cerebral ischemia occurred after occlusion of the aneurysm, hypervolemic and hypertensive therapy with norepinephrine was initiated in the ICU in an attempt to raise the cerebral perfusion pressure. Implantation of an ICP-monitor or external ventricular drain was based on the presence of either brain oedema or hydrocephalus, or both.
The decision to perform DC was based on clinical signs of impending brain herniation (and confirmed with CT-imaging), findings of brain swelling during the clipping procedure, or medically-refractory ICP values >25 mm Hg for longer than one hour despite deep sedation, hyperventilation, and administration of intravenous mannitol.
DC consisted of the excision of a large bone flap and duraplasty. In de novo patients undergoing DC, a large skin incision in the shape of a question mark based at the ear was made. A bone flap with a diameter of at least twelve cm including frontal, temporal and parietal bone was created, with special effort to extend the craniectomy down toward the temporal skull base. The dura was opened widely, to ensure maximal decompression. Large hematomas were evacuated if possible. The cortical surface was covered with the unapproximated dural flaps and absorbable hemostatic cellulose, after which only the skin was closed. In patients who had previously undergone craniotomy for aneurysm clipping, or ICH evacuation, the existing bone flap was removed and extended if deemed necessary by the neurosurgeon. After surgery, patients were admitted to the ICU for supportive therapy.
Cranioplasty
The first follow-up visit to the neurosurgical outpatient clinic was usually scheduled after 12–16 weeks of rehabilitation in a rehabilitation centre/nursing home. When there were no signs of persisting brain swelling by that time, cranioplasty was scheduled in the following weeks/months.
Data collection
Data sources included patients’ rescue and evacuation records (when available), hospital records from our own institution, and the referring hospital when applicable, rehabilitation summaries, and correspondence of neurologists, nursing home physicians and general practitioners caring for the patients before and after discharge from our institution. These records were analysed for demographic characteristics, and presence of comorbidities. Computer tomography studies were evaluated to determine the nature of the underlying pathology, the extent of midline shift, and any associated intracranial injuries. The Glasgow Coma Scale (GCS) score and pupillary light reflexes at the moment of injury/ictus could not be determined in all patients. We therefore recorded GCS scores and pupillary light reflexes at the moment of diagnosis and, to document any deterioration, immediately prior to surgery. Clinician’s notes at one year postoperatively were used to assess outcome according to the Glasgow Outcome Scale (GOS). The timing of DC was classified as primary when decompression was performed within 24 hours after onset, or secondary when decompression was performed ≥24 hours after onset, or not at the initial surgery. The reason for DC was classified as hematoma/oedema, or as secondary infarction. The STROBE guidelines were used in order to report this observational study accurately and completely.Citation10
Literature review
A literature search of the PubMed database up to June 2017 was conducted in order to find available individual patient data. The following keywords were used: decompressive craniectomy, hemicraniectomy or decompression and craniectomy together with subarachnoid haemorrhage. No language, publication date, or publication status restrictions were imposed. The studies had to report neurological outcome of patients of any age with an aSAH who underwent DC. Neurological outcome description could be through GOS or modified Ranking Scale (mRS). Studies were excluded when major pathology was present besides aSAH which caused raised ICP (such as acute subdural hematoma), when no aneurysm treatment was performed. In order to determine prognostic factors that influence long-term neurological outcome, we extracted available individual patient data on the following characteristics: age, gender, neurological condition on admission, treatment modality of aneurysm (clipping or coiling), reason of DC (hematoma/oedema or infarction), timing of DC (primary or secondary), outcome (favourable or unfavourable GOS score).
Data analysis
The neurological condition upon admission was classified as good grade (WFNS I-III or Hunt&Hess I-III) and poor grade (WFNS IV-V or Hunt&Hess IV-V). Favourable outcome was defined as GOS scores 4–5 or mRS scores 0–3 (moderate or low disability, i.e. independence in activities of daily living), unfavourable outcome as GOS scores 1–3 or mRS scores 4–6 (death, persistent vegetative state, or severe disability). Continuous variables were tested for normal distribution using the Shapiro-Wilk test. A variable was considered normally distributed if the Shapiro-Wilk test was >0.9, otherwise the variable was considered as not normally distributed. Means (±standard deviation, SD) are given for continuous variables with a normal distribution whereas median (interquartile range, IQR 25–75%) are given for not normally distributed continuous variables. To compare demographic and baseline characteristics between favourable and unfavourable outcome groups, univariate statistical analysis was performed. The 2-tailed t-test (for comparisons of normally distributed continuous variables), Mann-Whitney U test (for comparisons of continuous variables without a normal distribution), Fisher exact test (for analysis of 2 × 2 tables), and chi-square test (for analysis of N × 2 contingency tables) were done as appropriate to identify differences between groups. Results with a p < .05 were considered statistically significant. IBM SPSS Statistics 23.0 was used for calculations.
Results
Cohort
From January 1, 2006 until December 1, 2015 a total of 1009 aSAH patients was admitted in our academic centre, 56 of them (6%) underwent DC. All of them were in good health before the SAH occurred. Two patients were repatriated to their home country in the weeks following aneurysm treatment and were lost to follow-up. One patient was excluded due to the presence of a large acute subdural hematoma on initial CT, caused by traumatic brain injury following a motor vehicle accident. Therefore, 53 patients were included in the current study. In 30 patients (57%), the aSAH was caused by a ruptured MCA aneurysm. Patient characteristics sorted by neurological outcome are presented in . Overall, nine patients (17%) achieved a favourable neurological outcome after 12 months follow-up, 13 (25%) survived with an unfavourable outcome and 31 patients (58%) died. Twenty-eight patients died following withdrawal of respiratory support because of presumed poor prognosis, one died following restriction of treatment (‘do not resuscitate’) because of presumed poor prognosis, and the remaining two patients died despite maximal treatment (). Secondary infarction as reason for DC was a significant predictor of unfavourable outcome, with none out of 17 surviving favourably (). Patients surviving favourably were younger than patients surviving unfavourable (), but age > mean age (of 50.9 years) only tended to be a significant predictor of poor outcome (Odds ratio (OR) 3.87 [95% confidence interval (CI) 0.85–17.67]; p = .08). In non-intubated/non-sedated patients upon admission, patients surviving favourably had better GCS scores than patients surviving unfavourably (), but GCS <9 only tended to be a significant predictor of poor outcome (OR 7.50 [95% CI 0.82–68.83]; p = .054). illustrates the outcome among different subpopulations when stratified for reason of DC and age group (assorted by mean age). The percentage of patients surviving with favourable outcome varied considerably among different subpopulations. Patients <51 years undergoing DC for hematoma or (hematoma-related) oedema did relatively well, with approximately half of them regaining functional independence at follow-up. In contrast, none of the patients who underwent DC for infarction regained independence.
Figure 1. Outcome of 53 aneurysmal subarachnoid haemorrhage patients undergoing decompressive craniectomy (DC), stratified for age, treatment of aneurysm and reason of DC; GOS: Glasgow Outcome Scale; n: number of patients.
Table 1. Baseline characteristics of 53 aneurysmal subarachnoid haemorrhage patients undergoing decompressive craniectomy categorized by one-year clinical outcome.
Table 2. Causes of death of patients undergoing decompressive craniectomy after aSAH.
Cranioplasty
In 25 patients, cranioplasty was performed after an average of 110 ± 81 (22–245) days. In 9 (36%) patients complications occurred: three suffered from an epidural hematoma (requiring surgical evacuation in two), one suffered from space-occupying subdural hygroma (requiring implantation of a subdural-peritoneal shunt), one suffered from autologous bone graft infection (requiring bone graft removal), and one suffered from raised ICP and neurological drop (requiring a second DC). Three patients needed implantation of a ventricular-peritoneal shunt to treat hydrocephalus. Three patients died after cranioplasty: one died two days after cranioplasty due to epidural bleeding, another 23 days after cranioplasty due to respiratory failure following restriction of treatment because of presumed unfavourable outcome (68-year-old aSAH patient with status epilepticus and E1M4Vtube), and the third 140 days after cranioplasty due to re-bleed of a previously coiled superior wall internal carotid artery aneurysm.
Literature review
The PubMed search yielded a total of 164 citations. Of these, 136 studies were excluded because titles and abstracts did not meet the inclusion criteria. The remaining 28 studies were assessed for eligibility by reading full-text. Of these, five studies were excluded because they met one of the exclusion criteria. By checking the reference lists of the 23 included studies, two additional studies that met the inclusion criteria were identified. In total, 25 studies reporting on 861 patients were included.Citation6,Citation7,Citation11–33 All included studies were retrospective. The favourable outcome rate varied considerably, ranging from zero to 63% for consecutive case series with n ≥ 5 (). On average, favourable neurological outcome was achieved in 32% of patients, after a median follow-up of 12 months. Thirty-eight per cent survived with an unfavourable outcome, overall mortality was 30%. Few studies examined the relationship between the reason of DC and the outcome. Two groups reported significantly lower favourable outcome rates in patients undergoing DC for infarction compared to patients undergoing DC for hematoma/oedema: Buschmann et al. reported favourable outcome in 1/6 patients (17%) undergoing DC for secondary infarction versus 19/32 patients (59%) undergoing DC for hematoma/oedema, and Dorfer et al. reported favourable outcome in 2/20 patients (10%) undergoing DC for secondary infarction versus 16/46 patients (35%) undergoing DC for hematoma/oedema.Citation6,Citation13 One group, Güresir et al, reported similar outcome rates for both indications: 5/23 patients (22%) undergoing DC for secondary infarction survived favourably versus 16/56 patients (29%) undergoing DC for hematoma/oedema.Citation7
Table 3. Baseline characteristics of 25 studies included after systematic review of the literature.
For 105 individual literature cases, the predetermined characteristics could be extracted from 11 studies.Citation6,Citation11,Citation12,Citation18,Citation20,Citation24,Citation26–29,Citation33 Mean follow up was 12 months, ranging from ≥3 months to two years. The percentage of patients surviving with favourable outcome was 45%, 30% survived with unfavourable outcome, and mortality was 25%. presents the baseline characteristics of these 105 cases categorised by long-term clinical outcome. Secondary infarction as reason for DC was a significant predictor of unfavourable outcome (OR 3.42 [95% CI 1.04–11.22]; p = .03). illustrates the outcome when stratified for reason of DC and age group (assorted by mean age). Comparing the 105 individual cases to the total group of 861 patients revealed similar rates of clipping (90% versus 81%), of primary timing of DC (65% versus 59%; cases with unknown timing were excluded from the comparison) and of secondary infarction as reason of DC (17% versus 13%; cases with unknown reason were excluded from the comparison).
Figure 2. Outcome of 105 aneurysmal subarachnoid haemorrhage cases of the literature review undergoing decompressive craniectomy (DC), stratified for age, and reason of DC; GOS: Glasgow Outcome Scale; mRS: modified Ranking Scale; n: number of patients.
Table 4. Baseline characteristics of 105 aneurysmal subarachnoid haemorrhage patients undergoing decompressive craniectomy extracted from the systematic literature review, categorised by long-term clinical outcome.
Discussion
We reviewed the long-term clinical outcome of aSAH patients undergoing decompressive craniectomy by analysing a 10-year consecutive, single-centre patient cohort. Seventeen percent survived favourably, almost 60% died. Patients undergoing DC for hematoma or (hematoma-related) oedema did relatively well, with one fourth of them regaining functional independence at follow-up (increasing to 46% for patients aged <51 years). In contrast, none of the patients who underwent DC for infarction regained independence. The review of available individual patient data of 105 literature cases revealed a similar trend, although overall outcome was much better: half of the patients undergoing DC for hematoma or oedema regained functional independence, versus one fourth of the patients who underwent DC for infarction.
The differences in outcome between our cohort and the literature may have several explanations. First, our lower overall favourable outcome rate may have been caused by the relatively large proportion of patients undergoing DC for secondary infarction (32% versus 17% among the 105 literature cases). Second, 70% of our patients underwent secondary DC compared to 28% among the literature cases. A recent systematic review by Alotaibi et al. reported significantly higher pooled event rates of unfavourable outcome for aSAH patients undergoing late DC compared to aSAH patients undergoing early DC.Citation34 Third, 64% of our patients underwent coiling compared to only 10% among the literature cases. The delay between SAH onset and primary DC may have been longer for patients who first underwent endovascular aneurysm treatment before undergoing DC compared to patients who underwent combined clipping/decompression. Furthermore, the threshold to perform secondary DC may have been higher in patients who previously underwent coiling compared to re-opening the surgical wound and removing the already existing bone flap in patients who previously underwent craniotomy and clipping. Such higher threshold may jeopardize the neurological status of coiled patients before undergoing secondary DC. Fourth, most of our patients died following withdrawal of artificial respiration, because of presumed poor prognosis. May be some of them would have survived if active treatment had been continued. But still, the observation that none of our patients who underwent DC for infarction regained independence versus one fourth in the literature, demands a critical evaluation of clinical management on our side.
Neurological outcome in poor-grade aSAH: DC versus no DC
Thus far, no randomised controlled trial (RCT) comparing DC to best medical treatment has been performed in aSAH patients. According to recent large RCTs comparing DC to best medical treatment in TBI, DC is associated with reduced mortality, increased risk of survival with unfavourable neurological outcome, but no increased chances of favourable outcome: favourable outcome was only achieved in approximately one third of patients.Citation1,Citation2 Similar outcome profiles were reported in Honeybul and Ho’s meta-analysis of RCTs comparing DC to best medical treatment in malignant MCA infarction, although DC within 48 hours of symptom onset was shown to increase favourable outcome compared to best medical treatment.Citation5,Citation35 Alotaibi et al. performed a meta-analysis of three matched controls studies of DC in aSAH patients from D’Ambrosio et al., Uozumi et al., and Zhao et al, and reported similar likelihoods of unfavourable outcome and mortality for patients who underwent DC and matched controls.Citation12,Citation30,Citation32,Citation34 Taken together, one could conclude that DC has no beneficial effect on reaching a higher favourable outcome rate compared to best medical treatment. On the other hand, categorizing our cohort of patients and the literature cases according to age and reason of DC allowed us to identify subgroups of patients with remarkably high favourable outcome rates. The abovementioned data, showing non-superiority of DC over best medical treatment, should therefore be interpreted with caution when evaluating the potential benefit of DC in a specific aSAH patient suffering from uncontrollably elevated ICP caused by hematoma or oedema.
Limitations of the study
The present study has several limitations. First, data analysis in both the cohort and reviewed studies was performed retrospectively. Patients were not randomized for treatment or control groups. Although we identified a subpopulation of patients that seem to benefit most from DC (aSAH patients undergoing DC for hematoma or oedema), we cannot exclude the possibility that similarly favourable outcome would have been obtained in some of these patients when treated with best medical treatment only. Second, there was large heterogeneity in patient characteristics among patients. On the other hand, heterogeneous series like our current cohort and the recently published study by Kapapa et al. reflect the existing large heterogeneity of patients encountered in daily clinical practice.Citation36 Data of such heterogeneous cohorts may serve to better guide clinicians during their pre- and post-surgical counselling, especially when outcome data is categorized according to specific patient characteristics. Third, for only 105 cases of the systematic literature review individual data could be extracted for analysis. Although these cases resembled the total of patients with respect to neurological condition upon admission, aneurysm treatment, timing of DC and reason of DC, the results should be interpreted with caution. Fourth, a major limitation in our analysis of predictors of unfavourable outcome may have been the so-called self-fulfilling prophecy: the tendency to restrict treatment selectively in patients with certain characteristics presumed to predict unfavourable outcome.Citation37,Citation38 Most of the patients in our cohort died of respiratory failure following withdrawal of artificial respiration, because of presumed poor prognosis. Thus, post-surgical symptoms and signs ‘known’ to be related to unfavourable outcome lead to treatment restriction, and the treatment restriction in itself leads to the unfavourable outcome. Probably some of these patients would still have been alive at 12 months’ follow-up if active treatment had been continued. But whether any of them would have survived favourably is highly speculative. Finally, we classified patients who did not regain physical independency as having an unfavourable outcome, but we recently reported normal mental quality of life (QoL) despite worse physical QoL in a cohort of 25 patients undergoing DC for space-occupying MCA infarction.Citation39 Mental QoL was not determined in the studies included in the current study and literature review, but it seems reasonable to assume that several unfavourably surviving patients might have reported similarly good mental QoL.
Future perspectives
In the era of evidence-based medicine, conducting RCTs is considered critical to test common therapies. Based on the results of RCTs for DC in MCA infarction and TBI, which are inconsistent regarding the chances of survival with favourable outcome in the DC group compared to best medical treatment, the decision to perform DC in such patients should be carefully weighed in each individual case.Citation1,Citation2,Citation5,Citation35 In the current cohort study and analysis of available literature cases, favourable outcome rates among aSAH patients undergoing DC differed remarkably when assorted for the reason of DC. Future RCTs designed to identify a potential increase in the proportion of favourable outcome among aSAH patients undergoing DC compared to best medical treatment may therefore not be served by including patients who showed no or little chances of favourable outcome in previous retrospective case series, such as aSAH patients requiring DC because of secondary infarction. On the other hand, a similar trial setup may be considered unethical for aSAH patients requiring DC because of large life-threatening hematoma since, as mentioned earlier, (up to) half of them survive favourably. Before setting up a RCT for DC in aSAH patients, it may be worthwhile to further explore the different outcome profiles among subpopulations in larger prospective case series. With more prognostic factors available, clinicians will be able to more accurately judge whether, and to what extent, an aSAH patient will recover after DC. Such information will allow for a more comprehensive pre-surgical counselling of family members, which, in turn, will strengthen the shared decision-making process.
Conclusions
DC in aSAH patients is associated with high rates of unfavourable outcome and mortality. However, patients with hematoma or oedema as underlying reason for DC have much better outcome profiles than patients with secondary infarction, with (up to) half of them surviving favourably. Larger prospective case series are needed to further identify subpopulations of aSAH patients that benefit most from DC.
Ethical approval
For this type of study formal consent is not required.
Disclosure statement
The authors report no conflicts of interest.
Additional information
Funding
References
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