This study shows that the efficacy of surgical thrombectomy in achieving good outcomes after acute LVO is not inferior to that of the endovascular mechanical thrombectomy. Our results reveal that a surgical team experienced in the treatment of acute LVO can provide door to treatment and start of treatment to recanalization times similar to those of endovascular mechanical thrombectomy, and with full flow replacement (either through direct thrombectomy or bypass). Most failed endovascular treatments of acute LVO stroke were related to precipitating atherosclerotic intracranial disease or arterial dissection. Surgical rescue of such cases provided restoring flow via an emergent STA-MCA bypass. The main clinical outcome drivers in our study were age, hemisphere side, and DWI-ASPECT score at presentation.
Few authors have reported their experience in the surgical treatment of acute LVO through single center case series or case reports[7–11, 14, 15]. The reported advantages of surgical thrombectomy include a high rate of recanalization[8, 10] rare occurrence of distal migration or segmentation of the thrombus[8, 16], the capacity to perform a simultaneous cervical carotid thrombectomy or CEA[15], and its role as rescue treatment for either failed endovascular mechanical thrombectomy or its contraindications (e.g. severe contrast allergy)[10, 17]. The reported disadvantages of surgical embolectomy include postoperative intracerebral hematoma[10, 14], minor subarachnoid hemorrhage[8], and subdural hematoma[10].
An effective surgical thrombectomy treatment of acute LVO stroke requires an experienced team, intentional hospital logistics and mastery of the microsurgical technique of the pterional-transsylvian approach. Our institute has an emergency stroke protocol that integrates the hospital logistics (stroke fast-track pathway in the emergency department); team communication (e.g. between the emergency department, neurosurgery and OR staff); stroke diagnostic guidelines; and OR setup for surgical embolectomy; all of which ensure the fastest management from patient arrival into the hospital to recanalization. Our institutional protocol is optimized to the geopolitical, cultural, and medical logistics of our territory. In addition to our protocol, the human factor is key to achieve such short patient management times. Our team experience in the management of acute LVO stroke and their adherence to the stroke protocol may be the underlying reason for the similar door to treatment times between treatment groups (i.e. endovascular = 69min; surgical = 73min, p = 0.45) in our institution. Although door to treatment time was not statistically different between groups, the time from door to skin incision (interquartile range(IR) = 67) was more variable than that of door to puncture (IR = 23). Such difference may inform of the time-consuming logistics inherent to the preparation for a surgical procedure for each patient, the nature of which was beyond this study. Inoue et.al. reported an onset to surgical recanalization time of 281 min. and a median surgical recanalization (skin incision to patent anterograde flow) time of 79min[8]. Park et.al. reported an onset to recanalization time of 360 min. with a surgical recanalization time of 90 min[14]. Our onset to surgical recanalization time was 231 min., with only 32.5 min. of surgical recanalization time, which were similar to those of the endovascular treatment group (onset to recanalization time = 187min, p = 0.17; endovascular recanalization time = 42min, p = 0.13). The reason underlying the variability in surgical recanalization times in the literature is in great part attributable to operative technique. We believe that a deliberate and customized pterional-transsylvian approach (video) combined with an intentional training on intracerebral revascularization may be key to achieving an efficient surgical treatment of acute LVO, and are transferrable to the developing countries.
Surgical thrombectomy as a second line treatment
The present study supports that both the surgical and endovascular treatment options for acute LVO stroke provided similar good clinical outcomes. Although our results show favorable outcomes in acute LVO patients treated with surgical thrombectomy, the literature strongly supports endovascular mechanical thrombectomy as the first line of treatment for these patients when reasonably available. Fiedler et al. reported a prospective two-center cohort study for patients with acute middle cerebral artery occlusion who failed mechanical thrombectomy[12]. They compared the microsurgical intervention group with the control group (medical treatment only). They found that microsurgical embolectomy (which included the option of extracranial-intracranial bypass) provided better outcomes (mRS score 0–2) at day 90 after stroke. Although this was a small sample and was not a multicenter randomized control trial, it showed that microsurgical revascularization even after mechanical failure may improve outcomes in patients with acute LVO. In addition, surgical thrombectomy could compensate the limitation of mechanical thrombectomy, which patients with mechanical failure, no access route or severe allergy to contrast material and later mentioned tandem lesion. Our results show that the efficacy of surgical thrombectomy is not inferior to mechanical thrombectomy when performed by a well-trained and organized surgical stroke team.
The main challenge regarding indications of surgical embolectomy as a rescue to failed endovascular mechanical thrombectomy is the uncertainty of the length of the window of opportunity to prevent complete infarction of the tissue at risk. This window of opportunity for surgical rescue of failed endovascular acute LVO treatment depends on the presence of clinical to diffusion mismatch at the time of endovascular failure, rather than an onset to procedure time[2]. The clinical-to-diffusion mismatch may be directly related to the presence of collateral flow, rendering some patients with rich collateral vasculature good candidates for delayed rescue surgical thrombectomy. This patient-specific opportunity window opens the possibility for a true indication of surgical thrombectomy as a rescue option in the developed world, and a window of hope for the developing healthcare system.
Surgical thrombectomy in developing countries: role and opportunities
We believe that all patients should have access to the best treatment options regardless of their geopolitical and socioeconomic status. Endovascular thrombectomy is the gold standard treatment option for acute LVO stroke in the developed countries and can be performed by a variety of providers[1, 3, 4]. However, there is a pressing need for a short-term feasible treatment option for acute LVO stroke in the poor and developing countries, where access to endovascular treatment is both very limited and financially prohibitive[18–24]. Thus, surgeons capable of doing microsurgical thrombectomy can solve this complex geopolitical healthcare inequality. For example, in the Indonesian National Brain Center, the largest high-volume stroke center in the country, more than 4000 stroke patients are treated yearly, but the data shows a surprisingly low number of patients who underwent endovascular thrombectomy (< 0,5%). Many factors other than treatment affordability also contribute to this condition, including the lack of access to stroke-ready hospitals, causing patients to come beyond treatment opportunity (minimal penumbra, fully developed stroke). In the rural area, the cost of building an endovascular suite is considerably higher than providing a surgical operating room with a neurosurgical microscope and optimal equipment for bypass. With the aim not to replace endovascular thrombectomy, providing microsurgical thrombectomy can act as a temporary bridging strategy while the Indonesian government is investing in strategies to optimize access to endovascular treatment for most patients. When endovascular treatment becomes available as first line therapy to all Indonesian patients, the surgeon will already have developed the skill to treat failed endovascular cases (e.g., difficult access) or perform salvage treatment such as extracranial to intracranial bypass.
Performing surgical thrombectomy in the developing countries requires intentional logistics and a well-trained neurosugeons and neurosurgical team. Surgical thrombectomy may be a realistic and logistically feasible first line of treatment for acute LVO stroke in the developing countries if decisive and intentional action is taken. Most major city hospitals in the developing countries have at least 1 functional CT scanner capable of performing CT angiograms[18, 22–25]. There is raising awareness of the importance of universal access to acute neurosurgical care in several developing countries, and several governmental agencies are taking action. The Ministry of Health of Indonesia is developing a strategic plan to build centers of neurosurgical excellence in key islands capable of providing emergent care to all patients in their over 10,000 inhabited islands[25]. Such plan includes diagnostic imaging capabilities (CT, MRI, X-Ray) and operating rooms with basic neurosurgical equipment, including a surgical microscope. In addition, we believe that the training passionate and committed neurosurgeons from developing countries to perform surgical thrombectomy is also realistic. Global neurosurgery efforts and clinical fellowships are key to enable and perfect the skillset of neurosurgeons with intentional goal to bridging the gap of inequality to LVO stroke care.
Surgical thrombectomy as a first line treatment for tandem cervical ICA and MCA lesion
Endovascular treatment of tandem acute LVO (i.e. cervical carotid plus intracranial carotid with or without MCA thrombi) does not have the same level of evidence to single LVO. Many randomized clinical trials supporting the endovascular treatment of acute LVO excluded tandem lesions[1, 26]. HERMES and MR CLEAN trials included tandem lesions but excluded severe cervical carotid stenosis (< 70–80%)[1, 27]. Zhu et.al. reported good outcomes for the endovascular treatment of tandem lesions[28, 29]. However, there is a concern about CAS in the hyperacute stage, it means routine dual antiplatelet before CAS were not possible. Slawski et al reported the comparison of CAS with mechanical thrombectomy and CEA with mechanical thrombectomy[30]. There was no statistical difference between both treatment, however, death, re-occlusion, internal carotid artery dissection and symptomatic bleeding occurred in CAS with mechanical thrombectomy group. In general, CAS in acute phase has a risk because the pre-procedural dual antiplatelet loading is impossible for acute LVO patients. Similarly, Hasegawa et.al. described their experience and surgical technique for the treatment of tandem lesions starting from the cranial site followed by the neck[15]. We described our simultaneous approach to a tandem lesion representative of our series (video) with a skin to final recanalization of 34 minutes (cranial = 26min; cervical = 34min). This procedure is superior in terms of recanalization time and allows CEA to be performed instead of CAS. The risk of intracerebral hemorrhage should be reduced. Because CEA should not need to use dual antiplatelet therapy in the hyperacute phase of cerebral embolism. On the other hand, CAS must continue dual antiplatelet therapy to avoid acute stent occlusion, but there should be increased risk of cerebral hemorrhage because cerebral infarction will occur to a greater or lesser extent after thrombectomy. The preferred treatment modality for tandem acute LVO in the developed world varies by country and stroke center, and the final verdict requires inclusion of challenging cervical cases (e.g. complete cervical ICA occlusion, video) in future prospective randomized multicentric clinical trials.
Study limitations
We included consecutive surgical cases with strict selection criteria to minimize sampling and confounding bias. However, there are methodological limitations inherent to the retrospective nature of this study, which used a highly selected patient population. Our study was based on a refined institutional protocol (Fig. 5) and large cerebrovascular surgical experience, which we believe influenced our results for the surgical thrombectomy group. Therefore, our results may be difficult to replicate by other institutions. However, both a protocol and experience are intangible resources that, when applied intentionally, may improve our reported results or constantly improve the efficacy of surgical thrombectomy over time (learning curve). Future prospective multicentric studies are required to define the role of surgical thrombectomy on failed endovascular mechanical thrombectomies and complex tandem lesions.