Article Text
PDF
Abstract
Background and purpose Acute ischemic stroke (AIS) caused by basilar artery occlusion (BAO) is a very severe neurological disease with a high mortality rate and poor clinical outcomes. In this study, we compared our experience of mechanical thrombectomy using the Solitaire stent (Solitaire thrombectomy) and manual aspiration thrombectomy using the Penumbra reperfusion catheter (Penumbra suction thrombectomy) in patients with AIS caused by BAO.
Materials and methods Between March 2011 and December 2011, 13 patients received Solitaire thrombectomy. In January 2012, the Korean Food and Drug Administration banned the use of the Solitaire stent as a thrombectomy device, and a further 18 patients received Penumbra suction thrombectomy until December 2013. We compared parameters between patients treated with each device.
Results Successful recanalization rates (Thrombolysis in Cerebral Infarction (TICI) score ≥2b: 84.6% vs 100%, p=0.168) and clinical outcomes (judged by the modified Rankin Scale scores recorded at 3 months: 3.6±2.6 vs 3.2±2.6, p=0.726) were not significantly different between the two groups. However, complete recanalization rates (TICI score of 3: 23.1% vs 72.2%, p=0.015) and total procedure times (101.9±41.4 vs 62.3±34.8 min, p=0.044) were significantly higher, and shorter, respectively, in patients treated by Penumbra suction thrombectomy.
Conclusions The two thrombectomy devices were associated with similar recanalization rates and clinical outcomes in patients with AIS caused by BAO. However, Penumbra suction thrombectomy seemed to allow more rapid and complete recanalization than Solitaire thrombectomy.
- Stroke
Statistics from Altmetric.com
Introduction
Early recanalization of an occluded artery is very important to improve functional outcomes and reduce mortality in patients with acute ischemic stroke (AIS).1 Among AIS patients, those with acute infarctions caused by basilar artery occlusion (BAO) have very poor outcomes and the highest mortality rate.2 Recently, various thrombectomy devices allowing intra-arterial (IA) approaches to AIS have been introduced; these allow high rates of recanalization and improve the clinical outcomes for patients with AIS.3 The two prevalent modes of mechanical thrombectomy devices used today are the stent-type clot retrieval devices, such as the Solitaire stent (ev3, Solitaire AB/FR Inc, Irvine, California, USA) and the Trevo system (Trevo Retriever; Concentric Medical Inc, Mountain View, California, USA), more recently, and the suction thrombectomy devices, such as the Penumbra system (Penumbra, Alameda, California, USA).
The Solitaire stent was originally designed for stent assisted coil embolization of wide necked aneurysms, but the fact that the stent is retrievable and self-expandable allowed it to be used as a mechanical thrombectomy device in patients with AIS.4 The Solitaire stent was shown to be effective as a thrombectomy device in the SWIFT (Solitaire FR With the Intention for Thrombectomy) trial.5 In contrast, the Penumbra system has three main components: a reperfusion catheter, a separator, and a thrombus removal ring. The system was shown to be effective in the Penumbra Pivotal Stroke Trial.6 Several studies on manual aspiration thrombectomy (MAT), using reperfusion catheters only, found that a simple modification of the Penumbra system rendered it safe and effective when used for revascularization of acute large vessel occlusions.7 ,8 However, direct comparisons seeking to determine which device is better in terms of thrombectomy have not been performed.
In the present study, we retrospectively analyzed data from 31 patients with AIS caused by BAO who were treated via mechanical thrombectomy, using the Solitaire stent (Solitaire thrombectomy), or by MAT, using the Penumbra reperfusion catheter (Penumbra suction thrombectomy). We compared the effectiveness of the two devices in terms of technical results and clinical outcomes.
Methods
Patients
We retrospectively collected data from 31 patients with AIS caused by BAO who received IA thrombectomy within 8 h of stroke symptom onset or who had unclear onset stroke within 12 h from the ‘last normal time’, from March 2011 to December 2013. In Korea, the Solitaire AB stent was originally introduced for stent assisted coil embolization but off-label use as a thrombectomy device commenced in 2010. In our stroke center, we commenced Solitaire thrombectomy in December 2010. Thus 13 consecutive patients with AIS caused by BAO underwent Solitaire thrombectomy from March 2011 to December 2011. However, in January 2012, the Korean Food and Drug Association banned the use of the Solitaire AB stent as a thrombectomy device. At that time, the Solitaire FR stent used for thrombectomy had not been introduced in Korea. Thus we had access to only the Penumbra system. Since that time, an additional 18 consecutive patients with AIS caused by BAO underwent Penumbra suction thrombectomy, to December 2013. We reviewed all of the clinical and angiographic data.
Acute stroke management protocol
Neurological evaluation was performed on presentation to the emergency room. The National Institutes of Health Stroke Scale (NIHSS) was administered by at least two stroke neurologists. If a patient was in a complete coma, we recorded an NIHSS score of 36. Non-contrast brain CT scans were performed immediately after presentation to rule out intracerebral hemorrhage (ICH). If no ICH was evident on CT scans obtained within 3 h of symptom onset, we commenced treatment with recombinant tissue plasminogen activator (Actylase; Boehringer Ingelheim, Basel, Switzerland) to achieve intravenous (IV) thrombolysis. The indications/contraindications for IV thrombolysis were those of the guidelines for early management of adults with ischemic stroke.9 After commencing treatment with recombinant tissue plasminogen activator, we performed stroke setting MRI using a 1.5 T magnet (Magnetom Avanto; Siemens Medical Solutions, Erlangen, Germany). The MRI procedure consisted of b0 and b1000 DWIs, GREs, FLAIRs, gadolinium (Gadovist, Gadobutrol; Schering, Berlin, Germany) enhanced T1WI, gadolinium enhanced extracranial and intracranial MR angiography, and perfusion MRI. If the patient had a condition that did not allow MRI, we performed a dynamic CT perfusion series (CT angiography/8 level perfusion CT/delayed enhanced CT). If a basilar artery (BA) occlusion was evident on MR angiography or CT angiography, we prepared the patient for IA thrombectomy after obtaining informed consent. IV thrombolysis was not performed in patients with suspected AIS who presented more than 3 h after symptom onset. Informed consent for the conduct of IA thrombectomy was obtained before each procedure in the presence of at least two legal representatives. The study was approved by our institutional review board.
Interventional procedures
All procedures were performed by an experienced neurointerventionist and a neurologist (who was also a trained neurointerventionist), using a biplane angiography system (Artis Zee Biplane; Siemens). First, the femoral artery was punctured under local anesthesia, and a 6 F femoral sheath was placed. Next, the sheath was changed to a 6 F Shuttle catheter (Shuttle-SL guide sheath; Cook, Bloomington, Indiana, USA) and the dominant vertebral artery (VA) was selected using an angiocatheter with a guidewire. The tip of the Shuttle catheter was placed on the distal portion of the V2 segment. If atherosclerotic stenosis was present in the dominant VA, we gained access via the non-dominant VA to avoid further embolization. However, if the other side of the VA was hypoplastic or occluded, we performed balloon angioplasty in the stenotic segment to approach the occlusion segment.
For Solitaire thrombectomy, a microcatheter (Rebar 18; ev3 Inc, Irvine, California, USA or Prowler Selector Plus; Cordis Neurovascular, Miami Lakes, Florida, USA) with a 0.014 inch microguidewire (Traxcess; MicroVention, Tustin, California, USA) was passed through the occlusion site and placed distally. Subsequent angiography was performed to estimate the length of the occluded segment. A Solitaire AB stent was introduced through the microcatheter. The size of the stent was dictated by the artery affected and the length of the occluded segment. The stent was fully deployed and held in position for 2–5 min using angiography to confirm flow restoration. If flow restoration was achieved, the microcatheter and stent were pulled back, with application of negative suction pressure through the Shuttle catheter, using a 50 mL syringe to reduce distal embolization. In cases of persistent occlusion or incomplete recanalization, the Solitaire stent was reintroduced up to five or six times to achieve maximal recanalization.
For Penumbra suction thrombectomy, we advanced the 054 Penumbra reperfusion catheter with a microcatheter and a microwire coaxially to the proximal end of the thrombus, to wedge the catheter to the clot. After withdrawal of the microcatheter and microwire, we connected a 50 mL syringe to the proximal end of the reperfusion catheter. The catheter was held in place for 1–2 min and then withdrawn slowly, maintaining a vacuum between the tip and the clot with application of negative suction pressure through the Shuttle catheter, also using the 50 mL syringe. If the vacuum became released during catheter withdrawal, we placed a Penumbra reperfusion catheter on the proximal BA or distal VA and performed angiography via that catheter to explore whether recanalization had been successful. In cases of persistent occlusion or incomplete recanalization, the microcatheter and microwire were reintroduced and the procedure repeated until maximal recanalization was achieved. This method differed from conventional Penumbra thrombectomy performed in the Penumbra Pivotal Trial, which used a Penumbra reperfusion catheter, the Penumbra separator and aspiration pump, as well as direct thrombus extraction using a thrombus removal ring if residual thrombus remained.6 Our method is the same as a direct aspiration first pass technique (ADAPT), except that we used a conventional Penumbra catheter instead of the newer Penumbra Max catheter.10 ,11
Heparinized saline was continuously infused through the catheter/microcatheter to prevent in-catheter thrombosis. Thrombolysis in Cerebral Infarction (TICI) scores were estimated via final angiography after thrombectomy.12 Successful recanalization was defined as TICI scores of 2b and 3, and complete recanalization as a score of 3.
A control CT scan was repeated immediately and 24 h after the thrombectomy to detect hemorrhagic complications. Symptomatic hemorrhage was defined according to the National Institute of Neurological Disorders and Stroke (NINDS) trial13 as any hemorrhage related temporally to deterioration in a patient's clinical condition.
Data collection and statistical analysis
We collected data on baseline characteristics, stroke risk factors, initial neurological status, procedural results, and clinical outcomes at discharge and at 3 months after discharge, using the modified Rankin Scale (mRS) scoring. A good outcome was defined as an mRS score of 0, 1, or 2, and a poor outcome as a score of 5 or 6. Time to treatment was defined as the time interval from presentation at the emergency room to entering the angiosuite, and the total procedure time was defined as the time interval from entering to leaving the angiosuite. We analyzed differences between the Solitaire thrombectomy group and the Penumbra thrombectomy group using SPSS V.19.0 (SPSS, Chicago, Illinois, USA). We used the unpaired t test, the χ2 test, and Fisher's exact test, as appropriate. A p value ≤0.05 was considered to indicate statistical significance.
Results
Baseline characteristics, stroke risk factors, and procedural and clinical results are summarized in table 1.
Comparisons between the Solitaire thrombectomy and Penumbra suction thrombectomy groups
Patient data
In the Solitaire thrombectomy group, mean age of the 13 patients was 68.9±10.4 years (range 47–83; median 72 years), and the male:female ratio was 7:6. Mean time from stroke onset to hospital presentation was 231.2±191.5 min (range 0–569; median 160 min), and the initial NIHSS score was 27.3±11.0 (range 9–36; median 34). Twelve of 13 patients underwent MRI before treatment; the remaining patient could not undergo MRI due to an implanted cardiac pacemaker and instead underwent CT perfusion. Cardiovascular risk factors were hypertension in 53.8%, diabetes in 15.4%, smoking in 23.1%, alcohol use in 23.1%, atrial fibrillation in 46.2%, a prior stroke in 23.1%, and a history of dyslipidemia in 7.7% (mean total cholesterol level 191.5±55.5 mg/dL). Stroke etiology was cardiogenic embolism in 9 patients (69.2%) and large artery atherosclerosis in 4 (30.8%). Five of the 13 patients underwent IV thrombolysis (38.5%).
In the Penumbra suction thrombectomy group, mean age of the 18 patients was 66.4±11.4 years (range 47–85; median 69 years), and the male:female ratio was 14:4. Mean time from stroke onset to hospital presentation was 127.2±94.2 min (range 30–390; median 97 min) and the initial NIHSS score was 21.3±9.7 (range 8–34; median 23). All patients underwent MRI before treatment. Cardiovascular risk factors were hypertension in 44.48%, diabetes in 55.6%, smoking in 66.7%, alcohol use in 66.7%, atrial fibrillation in 4.4%, a prior stroke in 83.3%, and a history of dyslipidemia in 100% (mean total cholesterol level 155.1±26.8 mg/dL). Stroke etiology was a cardiogenic embolism in 10 patients (55.6%), large artery atherosclerosis in 7 (38.9%), and undetermined in 1 (5.6%). Nine of the 18 patients underwent IV thrombolysis (50%).
The Penumbra suction thrombectomy group contained a high proportion of patients who had experienced prior strokes, and who exhibited multiple risk factors, including diabetes, smoking, alcohol use, and a history of dyslipidemia.
Angiographic data
In the Solitaire thrombectomy group, time to treatment was 117.4±57.0 (range 40–240; median 104) min, and total procedure time was 101.9±41.4 (range 30–145, median 101) min. One of 13 patients received balloon angioplasty of the VA to access the intracranial occlusion site prior to thrombectomy. All 13 patients had TICI scores of 0 on initial angiography, and a mean of 3.08 runs of Solitaire stent was needed to achieve maximum recanalization (range 1–6, median 3). All patients achieved a TICI grade >2a. Successful recanalization was achieved in 11 patients (84.6%) and complete recanalization in 3 (23.1%). Procedure related complications developed in two patients undergoing several runs of Solitaire stent. One experienced a massive subarachnoid hemorrhage (SAH) because of rupture of the BA during the procedure and one developed an intraventricular hemorrhage, with SAH also evident on post-procedural CT. An additional patient showed small amounts of ICH on CT, but this did not cause deterioration of the patient's clinical condition (asymptomatic ICH).
In the Penumbra suction thrombectomy group, time to treatment was 109.2±65.4 (range 57–318; median 89) min and total procedure time was 62.3±34.8 (range 28–140, median 53) min. Two of 18 patients received balloon angioplasty of the VA to access the intracranial occlusion site prior to thrombectomy. All 18 patients had TICI scores of 0 on initial angiography. Successful recanalization was achieved in all patients (100%), and complete recanalization in 13 (72.2%). No procedure related complication developed in any patient. Twelve patients showed contrast extravasation on the infarcted area on CT scans obtained immediately after the procedure but this disappeared on follow-up CTs.
Comparisons of the two groups showed a shorter total procedure time and a higher rate of complete recanalization in the Penumbra suction thrombectomy group.
Clinical outcomes
In the Solitaire thrombectomy group, mean NIHSS score on discharge was 17.6±15.4 (range 0–36; median 12) and the mRS score was 3.5±2.2 (range 0–6; median 4). Three patients died during their hospital stay. The causes of death were massive SAH due to BA rupture in one patient and infarction progression in two patients. At 3 months, the mRS score was 3.6±2.6 (range 0–6; median, 5). Three further patients died after discharge. Good outcomes were apparent in five patients (38.5%), and poor outcomes in seven (53.8%).
In the Penumbra suction thrombectomy group, mean NIHSS score on discharge was 16.4±14.0 (range 0–36; median 11) and the mRS score was 3.7±1.8 (range 0–6; median 3.5). Four patients died during their hospital stay. The causes of death were infarction progression in three patients and cardiac death in one patient. At 3 months, the mRS score was 3.3±2.6 (range 0–6; median 3.5). Three more patients died after discharge. Good outcomes were achieved by eight patients (44.4%), whereas eight experienced poor outcomes (44.4%).
Discussion
AIS caused by BAO is associated with very poor outcomes and has the highest mortality rate of any form of AIS.2 One study evaluating patients with BAO induced AIS who were treated conservatively found that 96.3% of patients (26 of 27) died, and the remaining patient had an mRS score of 5 (very poor) 1 month after admission.14 However, recent trials of various mechanical thrombectomy devices used to treat BAO reported high recanalization rates (74–100%), with a relatively high rate of good outcomes at 3 months (29–50%), and low mortality rates (12–50%) (table 2).15–22 In our study, the overall recanalization rate (94%), good outcome rate (42%), and mortality rate (42%) were similar to those of prior studies. However, we confirmed that successful recanalization did not always lead to a good outcome (‘futile recanalization’)23 in patients with AIS caused by BAO.
Comparison of the results of the present study with those of other recent studies
We found that the recanalization rates and clinical outcomes did not differ significantly when different thrombectomy devices were used. However, total procedure times and complete recanalization rates were significantly shorter and higher, (respectively, in patients treated with Penumbra suction thrombectomy. We believe the main reason for the shorter procedure time and higher complete recanalization rate in the Penumbra suction thrombectomy group was our technical improvements. It is possible that we went through a learning curve when seeking to efficiently perform thrombectomies.24 This is also the principal limitation of our study. We did not treat all patients during the same interval. As mentioned in the Methods section, we initially used mechanical thrombectomy featuring Solitaire stents. In the Solitaire thrombectomy period, our interventional skills, including intracranial access and proper device use, were deficient. Thus procedure related complications were experienced only during the Solitaire thrombectomy period, although the core procedure, selection of the occluded artery, was similar when either method was used. Over time, we found that this became easier.
To our knowledge, only one previous study has compared neurological and radiological outcomes of patients treated with Solitaire stents and the Merci/Penumbra system.25 In this study, the authors concluded that the Solitaire stent afforded faster, safer, and more efficient thrombectomy than did the Merci or Penumbra systems.25 However, only 2 of the 51 patients with occlusions in the posterior circulation were included in the study.25 We suggest anatomical differences between the anterior and posterior circulations as possible reasons for the differences between the this study and ours.
Theoretically, in Solitaire thrombectomy, microcatheter selection of the occluded artery allows thrombectomy to proceed. In Penumbra thrombectomy, however, a reperfusion catheter with a much larger bore than that of a microcatheter must be delivered to the occlusion site before performing thrombectomy. Generally, the larger bore Penumbra reperfusion catheter allows easier and complete recanalization.10 However, delivery of larger bore catheters to the anterior circulation is difficult because of the tortuous curvature of the carotid siphon. In the posterior circulation, however, the course of the vessel is relatively straight, and delivery of larger bore catheters is easier. We use a 054 Penumbra reperfusion catheter for firstline treatment and, in most cases, we could deliver the catheter to the occlusion site without any difficulty because the outer diameter of the distal end of a 054 catheter is 1.65 mm but the diameter of the BA is generally more than 3 mm.26 Recently, Penumbra MAX/MAX ACE catheters for MAT have been developed.10 ,11 These catheters have long distal flexible segments allowing easier delivery than traditional Penumbra catheters. As we described in the Method section, our technique was different from the conventional Penumbra thrombectomy used in the Penumbra Pivotal Trial, but very similar to the ADAPT technique. A recent trial on the ADAPT technique using Penumbra MAX/MAX ACE catheters demonstrated that recanalization rates and clinical outcomes were similar to those achieved using stent retrieval.11 The successful recanalization rate of the device was 78% in the Penumbra MAX/MAX ACE catheter trial and 75.9% and 68% in the Solitaire and Trevo trials, respectively. Good outcomes were achieved by 40% of patients in the Penumbra MAX/MAX ACE catheters trial and 36% and 40% of patients in the Solitaire and Trevo trials, respectively.11
IA intervention in patients with AIS is a complex and time sensitive procedure. Thus we could not record exact recanalization times (from femoral puncture to the achievement of maximal recanalization). The only data available were total procedure times. We found that the total procedure time was almost halved using Penumbra suction thrombectomy. We believe that this cannot be explained by technical improvements alone. In fact, in technical terms, Penumbra suction thrombectomy is more rapid than Solitaire thrombectomy which, in most cases, requires repeat attempts at successful recanalization. If recanalization fails on the first attempt during Solitaire thrombectomy, stent re-sheathing and reselection of the occluded artery are necessary. During Penumbra suction thrombectomy, however, if the vacuum was released during catheter withdrawal, we placed a Penumbra reperfusion catheter on the distal VA or proximal BA and performed angiography via that catheter, because clots could be sucked into the catheter (this is a ‘disrupted clot type’ procedure).7 If persistent occlusion was shown by angiography, we simply reinserted the microcatheter/microwire into the Penumbra reperfusion catheter and reselected the occluded artery. This saved a great deal of time.
Distal embolization is of concern during mechanical thrombectomy. Thus the manufacturers of the stent-type clot retrieval devices recommend the use of a balloon guide catheter to arrest the flow causing distal embolization. But, the use of a balloon guiding catheter for posterior circulation infarction is not as well described as for anterior circulation infarction. In the present study, we used a 6 F Shuttle catheter to achieve maximal support, and negative suction through the catheter was applied during stent retrieval or catheter withdrawal. Although we did not use a balloon catheter, we found no distal embolization in our study. We believe that the partial flow arrest achieved via a Shuttle catheter with an outer diameter greater than that of the more usual guiding catheter helped prevent distal embolization.
Conclusions
This study has several limitations, including retrospective data collection, single center experience, and small number of patients. In addition, as we mentioned previously, this study was not performed during the same interval, and the results were mainly self-adjudicated (eg, TICI scores). Furthermore, we used Solitaire AB stents instead of Solitaire FR stents in the Solitaire thrombectomy group, although the basic characteristics of the two devices are not different. Regardless, to our knowledge, this is the first study to compare the neurological and radiological outcomes of patients with AIS caused by BAO who were treated using Solitaire thrombectomy and Penumbra suction thrombectomy. In addition, although not all of the patients were treated during the same time interval, all work was performed by the same investigators in the same environment. We found that the thrombectomy device used did not affect recanalization rate or clinical outcome. Notably, however, a discrepancy between the recanalization rate and clinical outcome remained evident in patients with AIS caused by BAO.
References
Footnotes
Contributors Study conception and design: DSC and BHL. Data collection: all authors. Data analysis and interpretation: SS, DSC, and N-CC. Literature research: SS and O-YK. Drafting the manuscript: SS. Revision of the manuscript for important intellectual content: SS, DSC, MKO, and K-JP. Approval of the final version of the manuscript: all authors.
Competing interests None.
Ethics approval The study was approved by the institution review board of Gyeongsang National University Hospital.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement Unpublished anonymised/de-identified data may be available. This would be on a per request basis. Please email the corresponding author or first author (sonsn@hanmail.net) for the data.