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Review

Intracranial Stent-assisted Revascularization for Acute Ischemic Stroke

Hopkins, Levy, Siddiqui, Karmon, Natarajan

November 2009
2152-4343

Abstract

In this article, we provide a snapshot of the strengths and limitations of current FDA-approved stroke therapies and discuss the rationale, technique, outcomes, limitations, and future of stent-assisted recanalization.

Current FDA-approved Stroke Therapies

Acute ischemic stroke intervention has been galvanized by the correlation of clinical outcome with radiographic revascularization.1–6 Data from several well-designed trials demonstrate that recanalization is associated with improved outcome.1–10 A critical corollary to the importance of recanalization is the importance of time-to-recanalization.6–8 These realizations are directing government policy, reimbursement patterns, and overall physician interest toward increased commitment to developing rapid recanalization tools and creating an infrastructure to ensure patients receive such therapies. The recanalization rates achieved with intravenous (IV) recombinant tissue plasminogen activator (rt-PA) for proximal, large-vessel arterial occlusion are poor and range from only 10% for internal carotid artery (ICA) occlusion to 30% for middle cerebral artery (MCA) occlusion.11 Intravenous thrombolysis (IVT) is not as effective for thromboembolic obstruction of these large proximal vessels as compared with more distal, smaller vessels.12 A National Institutes of Health Stroke Scale (NIHSS) score of > 12 suggests an occlusion of a proximal large vessel and therefore, a high thrombus burden.13 The main concerns with intra-arterial (IA) and IV pharmacological thrombolysis have been the rate of hemorrhage, the inability to effectively dissolve platelet-rich clots, lengthy times to recanalization, and the inability to prevent abrupt reocclusion at the initial site of obstruction.14 Reocclusion has been reported to occur after IVT (in 34% of patients) and IA pharmacologic thrombolysis (in 17%) and is associated with poor outcomes.15,16 Endovascular mechanical therapies yield higher recanalization rates and allow a slightly broader treatment window, and hence, lead to better outcomes in this group of patients. The Merci® mechanical clot retriever (Concentric Medical, Mountain View, California) and the Penumbra device (Penumbra, Inc., Alameda, California) are mechanical thrombectomy devices that have been approved by the FDA for patients with stroke symptoms in whom IV rt-PA therapy is a failure or a contraindication.9,17 Although recanalization with the newer-generation Merci® mechanical clot retriever, in conjunction with pharmacological therapy, is successful in 70% of patients,9 this rate is only marginally superior to the 66% recanalization rate in the Prolyse in Acute Cerebral Thromboembolism II trial.18 The recanalization rate with the device alone was only 50%, multiple passes (average 5–6) were required before establishment of flow in the occluded vessel and concomitant use of IA fibrinolytics increased the rate of hemorrhagic transformation. With the Penumbra device, despite an 81.6% recanalization rate, only 25% of patients recovered to a modified Rankin Scale (mRS) score of ≤ 2, with mortality at 3 months in 32.8% and symptomatic intracranial hemorrhage (ICH) in 11.2%; furthermore, it took an average of 40 minutes to achieve flow restoration after delivery of the device to the target vessel.19

Rationale for Stent-assisted Recanalization

The cardiac roadmap has shown evolution from pharmacological thrombolysis to angioplasty and finally stenting as primary therapy for acute occlusion of coronary arteries. Although a similar roadmap could be traced for intervention in acute ischemic stroke, there are major differences in the pathology of an acute intracranial artery occlusion when compared to an acute coronary artery occlusion, and differences between intracranial and coronary vasculature. In the coronary vasculature, the arterial wall contains equal thicknesses of intima, media, and adventitia and is supported by the cardiac muscles. By contrast, in cerebral arteries, the media occupies three-fifths of the thickness, with intima and adventitia occupying one-fifth each. These vessels are surrounded by cerebrospinal fluid, and the lack of a supporting structure places them at higher risk of dissection or rupture. Most acute coronary artery occlusions are the result of destabilization of an in situ plaque, causing plaque rupture and thrombosis, whereas most acute cerebral artery occlusions are due to an embolus in a normal vessel. The major benefit of stent-assisted revascularization over other mechanical revascularization strategies is the resulting high rates of immediate, sustained flow restoration in occluded vessels.20–22 Stents are obviously of value in the setting of an acute occlusion in an intracranial vessel narrowed by atherosclerotic plaque.

Early Experience with Balloon-Mounted Stents

Initial clinical experience with stent-assisted intracranial revascularization involved the use of coronary balloon-mounted stents to reestablish flow through acutely occluded vessels after conventional pharmacologic and mechanical approaches had failed. A report of 19 patients treated at two centers with coronary balloon-mounted stents reported overall recanalization rate of 79%.23 Eight lesions were located at the internal carotid artery terminus, 7 in the M1, M2 segment of the MCA, and 4 in the basilar artery. Sauvageau et al24 reported 10 patients who underwent MCA stenting after failed Merci retrieval for acute MCA occlusion with a balloon-mounted (coronary) Vision stent (Guidant Corporation, Indianapolis, Indiana) deployed in each of 4 patients. In another report, 168 patients with acute stroke in which 20 patients received coronary stents were studied.25 In this study, stent-assisted revascularization (odds ratio = 4.8, confidence interval = 1.8–10.0, p Self-Expanding Stents Self-expanding stents (SES) designed specifically for the cerebrovasculature are now available and can be delivered to target areas of intracranial stenosis with a success rate of > 95%; these devices have an increased safety profile because they are deployed at significantly lower pressures than balloon-mounted coronary stents.26 Higher rates of recanalization and lower rates of vasospasm and side-branch occlusion were noticed with SES compared with balloon-mounted stents in a canine model of vessels acutely occluded with thromboemboli.27 As most cases of acute intracranial vascular occlusions are related to an embolus in the absence of any in situ vascular pathology, balloon angioplasty with high-pressure balloons and balloon-expandable stents is typically not necessary to recanalize the vessel and may only increase the chance of serious complications, such as vessel rupture or dissection. Finally, SES may cause less endothelial damage and, therefore, may result in lower rates of early reocclusion or late stent restenosis. SES with higher radial force (e.g., Wingspan, Boston Scientific Corp., Natick, Massachusetts) will likely play a key role in the management of patients with acute stroke related to intracranial atherosclerotic disease.26 Five intracranial SES are currently available: 1) the Neuroform stent (Boston Scientific), 2) the Enterprise stent (Codman Neurovascular, Raynham, Massachusetts), 3) the Leo stent (Balt Extrusion, Montmorency, France), 4) the Solitaire/Solo stent (ev3, Inc., Irvine, California), and 5) the Wingspan stent. The first four devices are currently marketed for stent-assisted coil embolization of wide-necked aneurysms, whereas the Wingspan stent is approved for the treatment of symptomatic intracranial atherosclerotic disease. Both the Neuroform and the Wingspan stents have an open-cell design, whereas the Enterprise, Leo, and Solitaire/Solo stents have a closed-cell design. The closed-cell design allows resheathing of the stent after partial deployment (70% deployment for the Enterprise; 90% for the Leo) or even full deployment (Solitaire/Solo).

Patient and Device Selection

Currently, Wingspan SES placement for acute stroke therapy is performed at select centers as a bailout maneuver after failure of current FDA-approved revascularization methods under a provision for humanitarian device exemption as part of an FDA-approved Phase II study. At our center, such patients are those who present for treatment outside the time window for IVT or those in whom IVT is a failure or a contraindication and presentation is within 8 hours of stroke symptom onset with a large vessel occlusion. As the longest length of the Wingspan stent is 20 mm, and the use of overlapping stents is not approved only patients with clot length Technique of SES-assisted Revascularization The stenting procedure may be performed under either general anesthesia or local anesthesia with conscious sedation and via the femoral or radial artery approach, according to the interventionist’s preferences. A 6-French (Fr) guide catheter (or larger) is placed in the target vessel proximal to the occlusion. A sufficient quantity of heparin is administered to maintain an activated coagulation time in the target range of 250–300 seconds. To minimize the release of distal emboli, the occlusion is crossed in a fashion similar to that used for the Merci clot retriever. First, a 0.014-inch steerable wire is softly advanced through the clot. A low-profile microcatheter is then advanced over the wire distal to the occlusion. Following microangiographic confirmation that the microcatheter is distal to the occlusion, an exchange wire is brought through the microcatheter and anchored distal to the occlusion. The microcatheter is removed and the stent delivery catheter is delivered over the exchange wire. To minimize the release of debris, the stent is deployed first distal to the occlusion (thus trapping any debris that may be later released between the stent and the vessel wall), then through the occlusion, and finally just proximal to the occlusion. All efforts should be made to assure that the stent is completely opposed to the vessel wall. If a portion of the stent is not expanded to at least 50% of the parent-vessel diameter, post-stent angioplasty (dilation) with an angioplasty balloon may be performed with an undersized balloon (up to, but not exceeding, the parent-vessel diameter) using a slow-inflation technique (approximately 1 atmosphere/30 seconds).

SES antiplatelet protocol. Patients who are not taking aspirin or clopidogrel/ticlopidine are treated with aspirin (650 mg; enteric-coated, if necessary) and a loading dose of either clopidogrel (600 mg) or ticlopidine (1 g) on admission. Aspirin (325 mg daily; enteric-coated, if necessary) and clopidogrel (75 mg daily) or ticlopidine (250 mg twice daily) are continued after the procedure (aspirin for lifetime; clopidogrel or ticlopidine for 3 months). Glycoprotein (GP) IIb-IIIa inhibitors (such as abciximab) are used if intraluminal thrombus develops during the procedure. If a GP IIb-IIIa inhibitor is used, the activated clotting time will be maintained at

Results of SES for Acute Stroke Revascularization

Two cases were reported in 2006 of the successful use of SES in stroke due to MCA occlusion as a bail-out after failed revascularization with other modalities.28,29 Levy et al21 described the use of SES (Neuroform or Wingspan) to treat 18 patients with stroke (19 lesions) presenting with acute focal occlusions involving the MCA M1 and/or M2 segment (9 lesions), ICA-T (7 lesions), or vertebrobasilar system (3 lesions). Stent placement was the initial mechanical maneuver in 6 cases, whereas other cases involved a combination of pharmacologic and/or mechanical maneuvers prestenting, including 10 balloon angioplasties and 9 clot-retrieval attempts. GP IIb-IIIa inhibitors were administered in 10 patients intraprocedurally or immediately postprocedurally to avoid acute in-stent thrombosis. Thrombolysis in myocardial infarction (TIMI) grade 2 or 3 revascularization30 was achieved in 15 of 19 lesions (79%). No intraprocedural complications occurred, but 7 patients had ICH (either intraparenchymal or subarachnoid) on postprocedural CT imaging, 2 of which were fatal. One patient developed early stent rethrombosis. The in-hospital mortality rate was 38.9% (7 of 18 patients). Four patients had mRS scores of ≤ 3 at the 3-month follow-up evaluation. Zaidat et al22 evaluated the use of Neuroform (4 patients) or Wingspan stents (5 patients) in 9 patients with acute stroke with occlusions involving the MCA (6 lesions), ICA (2 lesions), or the vertebrobasilar junction (1 lesion). Successful stent deployment across the clot occurred in 8 of 9 (89%) patients. In 1 patient, a Wingspan stent could not be tracked beyond the MCA–ICA junction and was deployed in the proximal clot. Complete (TIMI 3) and partial or complete (TIMI 2 or 3) recanalization occurred in 67% and 89% of the patients, respectively. There was 1 case of ICH (11%) and 1 of acute in-stent thrombosis (successfully treated with abciximab and balloon angioplasty). The mortality rate was 33% (3 of 9 patients). All survivors achieved an mRS score of ≤ 2. Follow-up angiography was performed in 4 of the 9 patients at a mean of 8 months (range, 2–14 months) and showed no stent restenosis. Brekenfeld et al20 reported use of the Wingspan stent as rescue therapy in combination with different thrombolytic agents, percutaneous balloon angioplasty, and mechanical thromboembolectomy in 12 patients with acute ischemic stroke (6 with anterior circulation; 6 with posterior circulation; median presentation NIHSS score was 14). TIMI 2 or 3 recanalization was achieved in 92% of patients; no complications or hemorrhage occurred. A multicenter retrospective review of prospectively collected data by Mocco and colleagues50 of 20 acute ischemic stroke patients (mean presentation NIHSS score, 17) treated with Enterprise stent placement as a bail-out procedure after current embolectomy options had been exploited showed TIMI 2 or 3 recanalization in all patients (100%) and improvement in NIHSS of ≥ 4 points at discharge in 75% of patients. Adjunctive therapy included Merci retrieval (12 patients), angioplasty (7 patients), GP IIb-IIIa inhibition (12 patients), IA nitroglycerin administration (1 patient), Wingspan stent deployment (3 patients), and Xpert stent (Abbott Laboratories) deployment (1 patient). The authors found that the Enterprise stent could be more easily navigated to and deployed at the occlusion site than the Wingspan stent, attested by its use in 3 cases of failed Wingspan stenting. On the basis of these preliminary data, we received FDA approval for a pilot study, Stent-Assisted Recanalization in acute Ischemic Stroke (SARIS),31 to evaluate the Wingspan stent for revascularization in patients who did not improve after IVT or had a contraindication for IVT. The mean time from stroke onset to intervention was 5 hours and 13 minutes. Total time from procedure onset to vessel recanalization was 45 minutes. The average presenting NIHSS score was 14. Seventeen patients presented with a TIMI score of 0, and 3 patients with a TIMI score of 1. Occluded vessels included the right MCA (11 patients), left MCA (5 patients), basilar artery (3 patients), and right carotid-T (1 patient). Intracranial SES were placed in 19 of 20 enrolled patients. One patient experienced recanalization of the occluded vessel with positioning of the Wingspan stent delivery system prior to stent deployment. In 2 patients, the tortuous vessel did not allow tracking of the Wingspan stent. The more navigable Enterprise stent was used in both these cases. Twelve patients had other adjunctive therapies: IA eptifibatide (10 patients), IA rt-PA (2 patients), angioplasty (8 patients), and IV rt-PA (2 patients). TIMI 2 or 3 recanalization was achieved in 100% of patients; 65% of patients improved > 4 points in NIHSS score after treatment. One patient (5%) had symptomatic ICH and 2 had asymptomatic ICH. At the time of the 1-month follow-up evaluation, 12 of 20 (60%) patients had an mRS score of ≤ 2 and 9 (45%) had an mRS score of ≤ 1. Mortality at 1 month was 25% (5 patients). None of the patients enrolled in this study died due to any cause related to stent placement; all deaths were due to the severity of the initial stroke and associated comorbidities. In our experience with endovascular acute ischemic stroke revascularization in 193 patients treated between 2006 and 2008 (Natarajan SK et al, unpublished data, 2009), there were 52 (26.9%) patients who underwent stent-assisted recanalization as a bail-out after failed attempts with FDA-approved modalities. TIMI 2 or 3 recanalization was achieved in 71.2% of patients with a symptomatic ICH rate of 11.5%. The outcomes at 3 months were mRS ≤ 2 in 42.3% of patients and death in 21.2% of patients. One patient (1.9%) who had an acute ischemic stroke with a chronic MCA-M1 occlusion with Moyamoya collaterals had immediate occlusion of a Neuroform stent, which was salvaged by balloon angioplasty. There was no further restenosis in any of the patients, including this patient at 3 months.

Limitations of Current Stent-assisted Revascularization Technology

Currently, available SES are mainly useful for occlusions in large vessels like the ICA, proximal MCA-M1, basilar artery, intracranial vertebral artery, anterior cerebral artery-A1, and posterior cerebral artery-P1. They cannot be used in smaller vessels or for clots that are longer in length than the stent or located at bifurcations. The need for aggressive antiplatelet therapy for 3–6 months after SES placement21,22,32–34 is a major disadvantage. Patients treated for the prevention of recurrent stroke with chronic aspirin therapy face a hemorrhagic complication rate of 2.22 per 100 patient-years.35 With dual-antiplatelet therapy, the risk is increased.36–39 Zaidat et al22 reported an 11% hemorrhage rate associated with stent placement for acute stroke. Moreover, Levy et al21 reported lethal hemorrhages as a complication in 11% of patients treated with stent placement for acute stroke. The current experience with stent-assisted recanalization is very limited, and the longer-term results have not been reported. Using an SES for revascularization involves leaving a permanent implant in the vessel, and this may not be justifiable, as most occlusions in acute ischemic stroke are embolic occlusion of normal cranial arteries. Embolectomy would be the right option in such cases in preference to a permanent implant. Thus, long-term surveillance of patients treated with stent-assisted revascularization for acute ischemic stroke is critical, especially in view of the mid-term results of Wingspan stent implantation for atherosclerotic intracranial stenosis showing a 25–29% in-stent restenosis rate.34,40–42 Although most patients with in-stent stenosis are asymptomatic, some may require target lesion revascularization.41,43 Zaidat et al22 reported 1 case (11%) of immediate in-stent restenosis after acute stroke treatment. The Enterprise stent has a lesser radial expansive force than the Wingspan stent and may perhaps incur lower rates of in-stent stenosis.44 The possibility of a bioresorbable intracranial stent in the near future may also be a solution for this issue.45 Another limitation of stent-assisted revascularization is that, despite the higher recanalization rates, the rates of symptomatic ICH are high and the outcomes are only marginally better than those reported with other modalities. One should also understand that all outcome data about stent-assisted revascularization come from small case series that attempt to establish the safety and effectiveness of stent-assisted revascularization and did not primarily try to prove better outcomes. Better patient selection supported by physiology-based imaging may decrease hemorrhage rates and improve outcomes in the future.

Stent Platform-based Revascularization Strategies

Temporary endovascular bypass. The advent of closed-cell stents that can be used as a temporary endovascular bypass to achieve immediate, high rates of flow restoration and then resheathed or removed after recanalization is achieved has obviated the need for dual antiplatelet therapy and eliminated the long-term risk involved in leaving a permanent implant. Kelly et al46 and Hauck et al47 reported the use of the Enterprise stent as a temporary endovascular bypass in acute stroke. In both cases, the stent was partially deployed for some time and retrieved, with successful recanalization of the occluded vessel. Stent-platform-based thrombectomy device. The Solitaire™ FR Revascularization Device is a recoverable, self-expanding thrombectomy device that was developed based on the Solitaire/Solo stent. The advantage of Solitaire FR is that it is a fully recoverable SES-platform-based device that can be used as both a temporary endovascular bypass and a thrombectomy device. Moreover, it can be electrolytically detached like a coil in the event that permanent stent placement is necessary, such as in the setting of an atherothrombotic lesion. We evaluated the safety and efficacy of this device in a canine stroke model with soft and firm clots (Natarajan SK et al, unpublished data, 2009). The device could be easily deployed and recovered and restored TIMI 2 or 3 flow immediately in all cases. Minimal residual clot in 2 of 4 instances required a second pass for complete clot retrieval. Minimal vasospasm was observed in 2 of 4 cases.

The Future

Although limitations of current stent technology may not allow the rationalization of stent-assisted revascularization as a primary therapy in all ischemic stroke patients, it is obviously a good bail-out modality that achieves immediate sustained flow restoration in a high percentage of patients in certain vessel locations. It is envisioned that improvements in stent technology in the future will allow stent-assisted revascularization in more distal locations. Improvements in systemic drugs, drug-eluting stents (DES), and stents coated with stem cells may accelerate stent endothelialization, thus obviating the need for or decreasing the duration of antiplatelet therapy after stent implantation. DES and biodegradable stents specially designed for the intracranial circulation may decrease neointimal hyperplasia and in-stent stenosis in the future. Stent platform-based thrombectomy devices that can be deployed if necessary and afford flexibility (depending on the type of occlusive lesion) may become the primary therapy for acute ischemic stroke.

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From *University at Buffalo, State University of New York, Buffalo, New York and §Millard Fillmore Gates Hospital, Kaleida Health; Departments of Neurosurgery & Radiology and Toshiba Stroke Research Center, Buffalo, New York.

Manuscript submitted July 29, 2009, provisional acceptance given August 17, 2009, accepted September 9, 2009.

Correspondence: L. Nelson Hopkins, MD, University at Buffalo, State University of New York, Neurosurgery, 3 Gates Circle, Buffalo, NY 14209. E-mail: lnhbuffns@aol.com

Disclosures: Dr. Hopkins receives research support from Toshiba; serves as a consultant to Abbott, Boston Scientific, Cordis, Micrus, and W. L. Gore; has a financial interest in AccessClosure, Boston Scientific, and Micrus; serves as a board member, trustee, or holds an officer position in AccessClosure and Micrus; and receives honoraria from Bard, Boston Scientific, and Cordis. Dr. Levy receives research grant support (principal investigator: Stent-Assisted Recanalization in acute Ischemic Stroke, SARIS), other research support (devices), and honoraria from Boston Scientific and research support from Micrus Endovascular and ev3; has ownership interests in Intratech Medical Ltd. and Mynx/Access Closure; serves as a consultant on the board of Scientific Advisors to Codman Neurovascular/Cordis Corporation; serves as a consultant per project and/or per hour for Micrus Endovascular, ev3, and TheraSyn Sensors, Inc.; and receives fees for carotid stent training from Abbott Vascular and ev3. Dr. Levy receives no consulting salary arrangements. All consulting is per project and/or per hour. Dr. Siddiqui has received research grants from the University at Buffalo and from the National Institutes of Health (NINDS 1R01NS064592-01A1, Hemodynamic induction of pathologic remodeling leading to intracranial aneurysms); is a consultant to Codman Neurovascular/Cordis Corporation, Concentric Medical, ev3, and Micrus Endovascular; serves on speakers’ bureaus for Codman Neurovascular/Cordis Corporation and Genentech; and has received honoraria from Genentech, Neocure Group LLC, an American Association of Neurological Surgeons’ course, and an Emergency Medicine Conference and from Codman Neurovascular/Cordis Corporation for training other neurointerventionists. Dr. Siddiqui receives no consulting salary arrangements. All consulting is per project and/or per hour. Dr. Karmon and Dr. Natarajan have no disclosure information to report.


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