Stroke is the second leading cause of death globally, accounts for 11% of all UK deaths and is also a leading cause of permanent disability in survivors. Early recognition of symptoms, strong medical infrastructure and pathways, and inhospital medical treatment remain the backbone of stroke management, but increasingly acute stroke patients benefit from surgical interventions. Evidence and guidelines on surgical interventions in acute stroke are reviewed here, specifically focussing on decompressive hemicraniectomy, posterior fossa decompression, and surgical clipping and coil embolization of ruptured intracranial aneurysms. Literature search was conducted using MEDLINE and Web of Science search indexes.
Key randomised controlled trials (RCTs) in decompressive hemicraniectomy include DECIMAL, HAMLET, DESTINY and DESTINY II trials, leading to current UK recommendation of timely surgery in malignant large MCA infarction, with no age exclusion but consideration based on individual wellbeing. In ruptured aneurysm surgery, the landmark ISAT study led to global changes in practice to favour coiling over clipping generally, however its inclusion criteria limits the recommendations to specific patient subsets. Other important RCTs include the BRAT and CARAT studies, and the ISAT II is currently in progress. Early intervention within 72 hours is also recommended based on current evidence. The quality of evidence regarding posterior fossa decompression in cerebellar stroke is low, with no large RCTs. However, based on small positive studies the clinical consensus is generally that decompression has benefit in deteriorating patients. Large RCTs are required to establish definitive guidelines with regards to operation timing and surgical indications.
The World Health Organization defines stroke is a vascular clinical syndrome, characterised by quickly progressing focal or diffuse signs of cerebral function disruption, which either lasts for over 24 hours or causes death (3). Globally, stroke is the second leading cause of death after coronary heart disease (4). 230 out of every 100000 people in the UK will suffer a stroke for the first time (5), accounting for 11% of all UK deaths and also being one of the top causes of permanent disability (6).
Stroke can occur almost anywhere within the central nervous system; most commonly known to affect the vasculature of the brain, however strokes of the spinal cord can also occur, as well as of the arteries of the eye. There are two main types of stroke with multiple different subtypes (7). Ischaemic stroke is the most common, comprising around 85% of all strokes – these are generally caused by arterial occlusion by a thrombus or embolus but can also occur due to systemic hypoperfusion (shock) or cerebral venous thrombosis. Haemorrhagic stroke makes up the remainder, with 10% of all strokes being due to intracerebral or primary cerebral haemorrhage, and 5% caused by subarachnoid haemorrhage. These generally occur due to an underlying vessel pathology – often an intracranial aneurysm or arteriovenous malformation.
When death doesn’t occur in a stroke, patient function is often impeded by long-term neurological symptoms which is usually graded by the modified Rankin Scale (mRS) from 0-6, with scores <2 corresponding to functional independence and <1 being classified as excellent function (8). Both the location and volume of the stroke determines the extent of neurological symptoms and subsequent functional outcome in both haemorrhagic and ischaemic types (9).
Naturally, the main strategy of intervention is to aim to restore blood flow during the acute phase of stroke in order to limit lesion size, which grows irreversibly within hours. Modern management requires top medical infrastructure in terms of prehospital care and streamlined inhospital pathways, in order to diagnose and treat stroke early. Medical management remains the backbone in stroke treatment, with intravenous thrombolysis being the only generally accepted and recommended pharmacological treatment for acute ischaemic stroke (10).
However, increasingly stroke victims are benefiting from surgical interventions, recently with mechanical thrombectomy being shown to substantially improve functional outcome and potentially reduce mortality in ischaemic strokes as compared to those treated by thrombolysis alone (11, 12). Other important areas of surgical management include prophylactic carotid endarterectomy used in carotid artery stenosis, decompression surgeries in massive infarctions and some haemorrhagic strokes, and the repair of ruptured intracranial aneurysms in subarachnoid haemorrhagic stroke. This review focuses specifically on the use of decompressive hemicraniectomy in malignant MCA infarction; posterior fossa decompression in cerebellar stroke; and coil embolization and neurosurgical clipping in ruptured intracranial aneurysmal haemorrhage.
2. DECOMPRESSIVE HEMICRANIECTOMY
Neurosurgical intervention is often thought reserved for haemorrhagic stroke, however in cases of massive cerebral ischaemia due to ischaemic stroke, subsequent oedema and raised intracranial pressure (ICP) can lead to an often fatal deterioration.
Large infarction, referring to a cerebral infarction which involves >50% of the middle cerebral artery’s territory unilaterally, is the prime cause of mortality in the acute stage of stroke – despite comprising less than 10-15% of all ischaemic strokes (13). Malignant large infarction (MLI) occurs when complete occlusion of the proximal middle cerebral artery (MCA) or distal internal carotid artery (ICA) causes a massive infarction in one hemisphere (14), characterised as a malignant space-occupying supratentorial infarct. This condition presents in up to 10% of ischaemic stroke patients and has a mortality of 70-80% in spite of intensive medical care, with death usually occurring within the first 4-5 days; medical management targets the cerebral oedema, however, surgical decompressive hemicraniectomy (DC) is often required (15-17). This is due to the fact that severe cytotoxic oedema and raised intracranial pressure (ICP) can cause subsequent herniation of structure through the tentorium
|Figure 1 – CT images of a 46-year-old patient with a space-occupying ‘malignant’ MCA infarction of the right hemisphere.(1)|
or falx cerebri, in addition to coning of brainstem through the foramen magnum.
As prognosis of malignant stroke patients is poor, clinical or imaging characteristics implying its rapid and progressive deterioration must be recognised. Deterioration begins within 2-3 days after stroke, with presenting symptoms including sudden hemiplegia, homonymous hemianopia, lesional side eye/head deviation and dysphasia. After these initial symptoms, precipitous coma and papillary dilation occur simultaneously, followed by death (18). In the UK, previous NICE guidelines advised that DC be considered in patients under 60 years, with clinical deficits suggesting MCA territory infarction and NIHSS score above 15 including a decrease in consciousness level, as well as CT-imaging showing an infarct of at least 50% MCA territory without ACA/PCA involvement, or an infarct volume >145cm3 on diffusion-weighted MRI (19). The most recent NICE-accredited guidelines were recently published by the Royal College of Physicians, containing the key difference that patients >60 years should also be considered for DC dependant on their individual wellbeing; additional advice on patient’s independence being that their pre-stroke mRS score should be <2 (20).
Before the 21st century, DC was seldom performed for stroke due to the belief that survival may be increased but only accompanied by vast neurological deficiency. Interest in the procedure was stimulated from the early 2000s by various studies showing potential improvement of neurological outcome on top of the decrease in mortality (21, 22). 3 European randomised, controlled trials – the DECIMAL, DESTINY and HAMLET trials – showed significant reduction in mortality and an increase of good functional outcomes in DC over nonsurgical treatment (23), but an important point of whether poor functional outcome was increased by surgery was not well-addressed.
A 2016 study of 213 MLI patients compared the outcomes of those undergoing standard medical treatment with those having DC (13). Importantly, when analysing poor outcomes this study separated patients who suffered death from patients who survived but with poor function, allowing the incidence of poor functional outcomes to be compared between the surgical and nonsurgical group. Surgery was found to be significantly superior with regards to decreasing mortality, increasing good functional outcomes, and importantly, decreasing poor functional outcomes in survivors.
|Figure 2 – CT scanning of a patient following decompression hemicraniectomy. (1)|
When selecting patients suitable for DC, certain factors are thought to be related to better outcomes. First, as in many diseases, age is an important predictor of outcome. Multiple studies have shown that younger patients are linked with better outcomes after craniectomy to treat stroke (24, 25). However, whether age is a general indicator for disease recovery as opposed to specifically being prognostic for DC may be debatable (13). Recently, the DESTINY II trial (26) explicitly studied surgery in older patients and found DC to provide a substantial survival benefit in patients over 60 similar to that seen in younger patients, thereby leading to the change in the 2016 NICE-accredited guidelines which states that patients should not be excluded from treatment based on age (20).
In various neurological diseases, the most important element clinical indicator on the Glasgow Coma Scale (GCS) for a good outcome has been shown to be the patient’s motor response in the acute stage (27, 28). In MLI, patients who could localise to pain or better (≥M5 on GCS) at the clinical deterioration or operation stage have been shown to have a statistically significantly better outcome compared with patients exhibiting <M5, who generally had a poor outcome whether surgery was performed or not (13). The same study did not find a patient’s motor performance at initial presentation to have a significant impact on their outcome. Therefore when predicting outcome, it is the patient’s performance at clinical deterioration that is important as opposed to during the initial manifestation.
Many studies have inferred that early surgical treatment within 24-28 hrs of malignant stroke diagnosis is more likely to produce a better outcome, however, this guidance may have been skewed by the improper differentiation of MLI from large infarction (21, 29, 30). Often in these studies, diagnoses have been made purely by imaging showing infarction of more than two-thirds accompanied by signs of mass effect, in spite of whether clinical deterioration had occurred or not. This leads to potentially unnecessary early DC on patients who may have recovered without surgery. Therefore, calling early surgery a prognostic indicator for better outcomes in MLI may not yet be justified, and the question of whether DC is indicated by early radiographic signs or by clinical deterioration of the patient is controversial.
Lin et al. (13) found no significant difference in terms of dates of deterioration and surgery between cases of good surgical outcomes and poor ones. Taking note of this result, they suggest that if there is no clear predictor of a radiographically large infarction becoming a malignant one, a timely surgery at the earliest signs of deterioration as opposed to the earliest possible surgery without deterioration is more likely to obtain a better prognosis. A few studies have shown strong indicators for early malignant stroke prediction, including diffusion-weighted MRI showing lesional volume of larger than 145cm3 (31) and complete perfusion deficit of the MCA region on MR-angiography (32).
3. POSTERIOR FOSSA DECOMPRESSION
Cerebellar strokes (CS) are fairly uncommon, accounting for under 1 in 10 of all strokes (33). Ischaemic and haemorrhagic stroke of the cerebellum are major causes of significant morbidity requiring long-term care and particularly in an ageing population, with less than 40% of haemorrhagic patients being independent at 1 year (34). Cerebellar infarction is roughly two thirds as common as cerebellar haemorrhage (35). Cerebellar haemorrhage occurs most commonly between the ages of 60 and 80, in agreement with the age incidence of all intracerebral haemorrhages (36), and shows wide-ranging mortality rates from 20% up to 75% in differing reports (37-39). In Europe and the US, the overall incidence has been reported to be between 9-15% (40, 41). Malignant space-occupying oedema occurs commonly in up to 54% of ischaemic CS patients which can lead to the fatal deterioration (42), whilst in haemorrhagic CS the space-occupying bleed itself leads to the deterioration.
The cerebellum lies in the posterior fossa of the cranium – the deepest and most confined space in the skull and therefore has a very low threshold for expansion of its contents due to a space-occupying lesion. In CS, the fatal deterioration occurs by a combination of: acute obstructive hydrocephalus and subsequent increased supratentorial pressure due to blocking of 4th ventricle; direct compression on pons and midbrain; herniation of the superior vermis cerebelli superiorly through the tentorial notch; and herniation of cerebellar tonsils inferiorly through the foramen magnum (43). The management choices for deteriorating cerebellar strokes are controversial regarding the amount of surgical intervention particularly due to the lack of randomised controlled trials, but since the last 2-3 decades most agree surgical decompression of the posterior fossa, via suboccipital craniectomy and dural expansion, is usually required as a life-saving measure in deteriorating patients (44).
Deterioration in CS has been defined as clinical signs of compression of the brainstem with neurological deterioration (45), obstructive hydrocephalus (46), depression in consciousness levels, GCS<12 on admission, rapid coma (47), and GCS depression of 2 points or more. A 2011 study defined radiographic signs for deterioration to be evidence of compression of the 4th ventricle and hydrocephalus (48). Brainstem compression signs are thought to be a key point where CS begins to worsen, therefore the American Stroke Association (ASA) recommend frequent monitoring for arousal levels and new brainstem signs in patients at
|Figure 3 – Pre and postsurgical CT imaging showing deterioration and treatment. (A and B) Large left cerebellar infarct with brainstem compression and early hydrocephalus. (C and D) Right frontal external ventricular drain placed, and emergent posterior fossa decompression performed. (E and F) A left-sided subdural hematoma developing, likely due to overdrainage. (2)|
high risk of deterioration (17).
Most literature available on the outcomes of posterior fossa decompression (PFDC) are small case-control studies or retrospective analyses, unlike the comparatively well-studied DC for MLI. This may be because the benefits of surgical intervention in these cases have generally appeared clear. Since the earliest publications in the 1950s (49), multiple reports have shown unilateral and bilateral suboccipital craniectomy beneficial in deteriorating CS. One of the larger series in 1999, showed that 40% out of 84 massive cerebellar infarction patients required surgical decompression, and 74% were seen to have good outcomes, with mRS scores of 1 or less (46).
With regards to timing of PFDC in cerebellar infarction, most studies have shown that the time interval does not particularly affect outcome (17). Additionally, whether surgery should be performed on clinically well patients with radiographic signs of deteriorations, and whether to include ventriculostomy and necrotic tissue removal within the procedure, are yet unknown (50, 51). Therefore, ASA guidelines state that “suboccipital craniectomy with dural expansion should be performed in patients with cerebellar infarctions who deteriorate neurologically despite maximal medical therapy”, but do not yet give any further guidance with regards to timings, patient status and operative technique (17).
A 2013 retrospective study on patients with malignant ischaemic CS found that postsurgical GCS scores were higher in surgically treated comatose patients, compared with non-surgically treated comatose patients whose scores dropped. Other studies have also shown this, leading many to recommend that surgery be performed prior to deterioration – it is thought that these patients may have fared even better had they been treated earlier (45, 52). Additionally, noncomatose patients who were operated also benefitted GCS improvement, while no significant difference was found between the pre and post-treatment periods in noncomatose patients who were not operated (53). The study suggested that low GCS did not necessarily mean a poor outcome and that early surgery may be important to prevent deterioration. In general, evidence has consistently shown that postsurgical outcomes correlate with presurgical status (37, 39). In one series, mortality of patients conscious presurgically was 17% versus 75% in those who were unconscious (38).
In 2016 (2), a retrospective study of emergency PFDC in both haemorrhagic and ischaemic CS patients found a significant association between increasing age and mortality, as to be expected. It also found that PFDC on patients >70 years, on average, had a poorer outcome than those between 60 and 70. Another interesting association observed was that smaller craniectomy sizes were correlated with higher mortality at 1 and 3-month stages, but not after 1 year. This is likely attributable to the idea that size of the craniectomy is important during the peak stages of swelling, but after 1 year death is probably caused by subsequent medical complications as opposed to the surgery itself. Significant associations were not seen in other factors such as size or location of lesion, however the sample size was small at 34.
Another 2016 study found a reduction in mortality when PFDC was performed in haemorrhagic strokes as opposed to medical management and external ventricular drainage (54). A third 2016 study exhibited favourably clinical outcomes and improved mortality in preventative PFDC performed on patients who show an infarct volume ratio between 0.25 and 0.33 with no brainstem infarction, and recommends PFDC in these specific patients (55).
4. CLIPPING AND COILING
Only 5% of all strokes are accounted for by subarachnoid haemorrhage (SAH), but the rates of mortality and permanent disability are high with large cohort studies showing 1-month mortality rates ranging from 32% to 42% (56, 57), and rates of dependency in survivors around 50% (58). In surviving patients the most important prognostic indicator is thought to be the clinical severity at presentation, particularly level of consciousness. This is generally measured using validated scales such as the old, but still commonly used, Hunt and Hess scale which incorporates headache, neck stiffness and focal neurological deficits with levels of consciousness (59). However a large discrepancy is seen in different observer measurements with this scale (60), therefore scales which specifically incorporate the GCS are preferred, having less variability. The World Federation of Neurological Surgeons (WFNS) scale is a 5-grade system based on the GCS plus focal neurological deficits, and has better interobserver agreement than Hess and Hunt’s (61).
The distinctive hallmark of SAH is the sudden onset thunderclap headache. A sentinel headache – a minor haemorrhage 2-8 weeks before the major subarachnoid haemorrhage – has been reported in between 10-43% of sufferers (62, 63), and interestingly, one study found that this may increase the odds of early rebleeding by up to 10 times (64). The most common symptoms presented with are headache, nausea and vomiting, loss of consciousness, and nuchal rigidity in roughly 4 in 10 patients (65). Seizures also occur in 1 in 5 patients, usually in the first 24 hours after haemorrhage and particularly in those associated with MCA and ACOM aneurysms, or additional intracerebral haemorrhage (66).
Variability in presentation does occur, and can lead to common mis- or delayed diagnosis. In the late 1900s over half SAH patients were missed, and today, although improved, around 12% of cases still aren’t correctly diagnosed (67). The main error leading to misdiagnosis is thought to be failure to order a noncontrast CT-scan – with close to 100% sensitivity in the first 3 days posthaemorrhage – in patients with little neurological deficit at presentation, which is subsequently linked with almost quadruple times increased 1-year mortality or disability (68). 5-7 days posthaemorrhage the sensitivity of CT scanning reduces significantly, and lumbar puncture (LP) for xanthachromia confirms diagnosis. MR-imaging developments can sometimes allow diagnosis without LP (69).
Figure 4 – Surgical clipping of a ruptured MCA aneurysm. (70)
With regards to surgical treatment of aneurysmal SAH, the main aim is to occlude the bleeding ruptured aneurysm, or to prevent aneurysmal rebleeding. Patients who live past the first day of haemorrhage have a 35-40% risk of aneurysmal rebleeding, however after a month without rebleeding this reduces to a yearly risk of 3% (71). There are two main surgical options: neurosurgical clipping, or endovascular coiling. With regards to timing of surgery, a meta-analysis of 1814 patients (72) found that early intervention within 72 hours of SAH, on patients with good clinical condition pre-surgery (WFNS 1-3), causes a significantly better outcome. A 1500 patient observational study showed no difference improvement of outcome in good neurological grade patients treated early, but poor grade patients had better outcomes (73). Ultraearly surgery <12 hours after onset did not increase the frequency of dependant survivors in poor WFNS score patients (74). The consensus is that patients with ruptured aneurysms, who exhibit good to moderate clinical grades presurgery (WFNS 1-4/Hunt and Hess I-IV), should be operated on with 72 hours of the initial bleeding. In those with multiple aneurysms, the primary surgery should only target the ruptured aneurysm (75).
The largest randomised controlled trial (RCT) directly comparing the efficacy of clipping with coiling was the International Subarachnoid Aneurysm Trial (ISAT) which involved 42 centres in the UK and Europe and screened 9559 patients in total (76). The main inclusion criterion was that the patient suffered a ruptured intracranial aneurysm which was deemed equally accessible and treatable by either surgical clipping or endovascular coiling. Other criteria included good neurological grading (WFNS 1-3), and age under 70. 2143 patients fitting the study criteria were recruited and randomly assigned to the clipping or coiling group. At the end of the study, the primary outcome of death and dependency rate was favourable in the coiling group, showing 23.5% compared with 30.9% in the clipping group. 1-year rebleeding rates however were higher in coiling, at 2.6% versus 1% in clipping.
Figure 5 – Angiography showing an initially coiled aneurysm (A) which suffered a recanalisation complication (B), and was subsequently re-coiled (D). (70)
A 5 year follow-up report of the ISAT stated a higher death rate in clipping of 14% over 11%, and a still increased rebleeding rate, however the rates of independent survival outcomes did not favour one group over the other (77). Therefore the initial report of a 7.4% reduction in death and dependency using coiling reduced down to only 3% in longer-term follow up. An important secondary outcome seen was that age under 40, larger aneurysmal lumen size and incomplete occlusion were risk factors for rebleeding in coiling (78). A further study analysing mortality only in the ISAT found no advantage of coiling over clipping in patients under 40 years, and suggest that clipping may be favourable for these patients with regards to life expectancy (79).
More recently the Barrow Ruptured Aneurysm Trial (BRAT) (80), a smaller RCT, found a significantly better 1-year outcome in coiling over clipping in posterior circulation aneurysms. However, the study’s allowance of crossing over between treatment groups makes the reported benefit of coiling controversial. An older, non-randomised trial – the Cerebral Aneurysm Rerupture after Treatment (CARAT) trial – found the risk of rerupture postsurgery was higher in coiling, however this difference was not present after adjustment (81). It also found intraoperative risk of aneurysmal rupture was 14% lower in coiling, but that the risk of death or disability in cases of this was doubled at 63% compared with 31% in clipping (82).
Whilst the landmark nature of the ISAT study changed practice worldwide to generally favour coil embolization (83), the numerous design limitations must be considered. Only 22% of patients screened were recruited due to the tight inclusion criteria, and 97% of patients had anterior circulation aneurysms. At the time of the trial, MCA aneurysms were generally considered unsuitable for coiling due to their anatomical difficulty for coiling, therefore they were represented in less than 15% of recruits (84). 92% of recruits had aneurysms less than 1 cm in diameter, which generally have a better prognosis regardless of treatment (85). Also, only 12% recruits presented with WFNS grade 3, therefore were underrepresented in the study as compared to patients presenting with good neurological grading. Anyone above 70 years old was excluded from the trial, therefore the ISAT cannot be used to help decide treatment in this subset of patients. Additionally, coiling was performed, on average, 1.1 days after haemorrhage whilst clipping was performed 1.5 days after, and this key difference may well have influenced results. Based on these limitations, among others, the ISAT results can be applied well to anterior circulation aneurysms under 1 cm diameter, with good presenting neurological grades, but posterior circulation aneurysms, larger aneurysms, higher WFNS grades and complicated aneurysmal morphologies are not well addressed. The ISAT II study, scheduled to complete in 2024 aims to address the limitations of the original study by including larger aneursyms, posterior circulation aneurysms, older patients, higher WFNS grades, and also incorporates angiographic surveillance in both clipping and coiling groups (86).
5. CONCLUDING REMARKS
The increasing use and benefit of surgical intervention as a part of the management of acute stroke has become clear over the past few decades, with multiple different surgical procedures being developed and evidenced to supplement the already well-versed medical treatment protocols. Whilst many interventions are now well-evidenced, some are less so and require significant further research in the future.
Overall, decompressive hemicraniectomy shows good evidence for improving outcomes in malignant MCA infarction when performed in a timely manner. 4 key RCTs since the 21st century have led to clear and evolving guidelines, with the recent 2016 UK guidelines exhibiting evidence-based changes to recommendations. Posterior fossa decompression is far less evidenced, with small studies showing improved outcomes in cerebellar stroke. The lack of RCTs have led to recommendations being based on clinical consensus as opposed to clear evidence, therefore large future RCTs are required to establish definitive guidelelines. Studies show strong evidence for early intervention in aneurysmal repair, and the landmark ISAT study changed global practice to favour coil embolization over clipping. However, the ISAT’s evidence is limited to a specific subset of patients, therefore a wider study cohort is being incorporated into the follow-up ISAT II study, due to complete over the next decade.
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