Clinical Neurology and Neurosurgery 119 (2014) 110–115
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Emergent intracranial stenting for acute M2 occlusion of middle cerebral artery Sang Min Sung a,b,d,∗ , Tae Hong Lee a,c , Sang Won Lee e , Han Jin Cho a,b , Kyu Hyun Park a,b , Dae Soo Jung a,b a
Stroke Center, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea Department of Neurology, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea c Department of Diagnostic Radiology, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea d Biomedical Research Institute, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea e Department of Neurosurgery, Pusan National University Yangsan Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea b
a r t i c l e
i n f o
Article history: Received 18 April 2013 Received in revised form 19 November 2013 Accepted 28 January 2014 Available online 6 February 2014 Keywords: Acute ischemic stroke Second segment of middle cerebral artery Self-expandable stent Intracranial stenting Recanalization
a b s t r a c t Objective: Intracranial stenting is a possible option as a rescue strategy for acute secondary division (M2) occlusion of middle cerebral artery (MCA) when intravenous thrombolysis is ineffective or contraindicated. Methods: We reviewed 10 patients of acute M2 occlusion treated by intracranial stenting who were ineligible for intravenous thrombolysis or resistant to intravenous thrombolysis. All patients underwent intracranial stenting with the Wingspan stent system. We analyzed clinical and angiographic outcomes. Results: The mean NIHSS score on admission was 13.8 points (range 6–23). The occlusion sites were located in the superior division (n = 4, left: 3, right: 1), the middle division (n = 1, right) and the inferior division (n = 5, all: right) of MCA. The mean time interval from stroke symptom onset to stenting was 348.9 ± 90.4 min. Successful recanalization was achieved in all patients. No intracranial hemorrhage, vessel perforations or dissections occurred in any patient. One patient developed acute thrombosis in distal ICA of the stented side at 4 days after a stent placement and was managed with mechanical thrombectomy. All patients improved on the NIHSS (mean amount: 8.8) and to the NIHSS score of 5 ± 4.6 (median 4.5, range 0–15) at 7 days. At discharge, an mRS of ≤3 was achieved in 8 patients (80%) and an mRS of ≤2 was achieved in 6 patients (60%). Conclusions: Endovascular recanalization with a Wingspan stent can be a safe and feasible procedure for acute M2 occlusion when intravenous thrombolysis is ineffective or not available. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Successful recanalization is an important factor in determining good outcome in acute ischemic stroke [1]. However, the efficacy of intravenous tPA for complete recanalization is relatively low, and the recanalization rate for acute M2 occlusions after intravenous tPA is approximately 30% [2]. Intra-arterial thrombolysis alone, or in combination with intravenous thrombolysis may be more effective. However, the rate of recanalization of chemical intra-arterial and intravenous thrombolysis is still unsatisfactory. The rates of symptomatic intracranial hemorrhage were 6.4% in NINDS [3] and 10% in PROACT II studies [4]. There are several exclusion criteria
∗ Corresponding author at: Stroke Center, Pusan National University Hospital, School of Medicine, Pusan National University, 10, Ami-Dong 1-Ga, Seo-Gu, Busan 602-739, Republic of Korea. Tel.: +82 51 240 7317; fax: +82 51 245 2783. E-mail addresses: [email protected], [email protected] (S.M. Sung). 0303-8467/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2014.01.027
of intravenous and intra-arterial thrombolysis. Main exclusion criteria are (1) significant head trauma or prior stroke in previous 3 months. (2) Symptoms suggesting subarachnoid hemorrhage. (3) History of previous intracranial hemorrhage. (4) Elevated blood pressure (systolic > 185 mm Hg or diastolic >110 mm Hg). (5) Platelet count 1.7 or PT > 15 s. (7) Current use of direct thrombin inhibitors or direct factor Xa inhibitors with elevated sensitive laboratory tests (such as aPTT, INR, platelet count, and ecarin clotting time; TT; or appropriate factor Xa activity assays). (8) Blood glucose concentration 1/3 cerebral hemisphere) [5]. Recent case series reported acceptable safety, good outcomes and good recanalization rates with intracranial stenting in patients with acute MCA occlusion if other recanalization modalities have failed or in patients who have been ineligible for intravenous tPA [6–12]. However, there has not been much reported regarding the use of intracranial stents for recanalization of acute M2 occlusions.
S.M. Sung et al. / Clinical Neurology and Neurosurgery 119 (2014) 110–115
We report recanalization rates, complications, and outcomes of patients treated with intracranial stenting as a rescue procedure for acute M2 occlusion.
2. Materials and methods Ten patients with acute M2 occlusion were treated by intracranial stenting in our stroke center between May 1, 2010 and September 31, 2011. Our Institutional Review Board approved collection of interventional and clinical data for this study. Informed consent was obtained from the patient or the next of kin in this off-label stenting for recanalization. We treated patients in whom recanalization was not achieved with intravenous thrombolysis, patients who were ineligible for intravenous thrombolysis or who presented after 3 h of symptom onset. Stenting was completed within 8 h from stroke symptom onset. Diffusion-weighted image (DWI), computed tomography (CT), CT perfusion (CTP), and CT angiography were performed to assess for arterial occlusion and diffusion/perfusion mismatch. DWI was done in all patients and CTP was done in 8 patients. We analyzed demographic features, clinical characteristics, location of occlusion, symptom onset to arrival time, symptom onset to stenting time, use of adjunctive chemical therapies (urokinase or glycoprotein IIb/IIIa inhibitors), and procedural complications. National Institute of Health Stroke Scale (NIHSS) was checked before and at 7 days after stenting. The modified Rankin Score (mRS) was also checked at discharge. Outcome was stratified to “good” (mRS 0–2), “moderate” (mRS 3), and “poor” (mRS 4–6). Recanalization result was evaluated by the Thrombolysis in Cerebral Infarction (TICI) score (graded as 0 for absent perfusion, 1 for minimal distal perfusion, 2 for partial perfusion, and 3 for complete perfusion). Interventional procedures were performed in the neuroangiography room equipped with a digital subtraction angiography system (Axiom Artis, Siemens, Germany). All stents were deployed under local anesthesia. Percutaneous access using 6-French sheath was gained via the common femoral artery. Diagnostic angiography including all cerebral arteries was performed to evaluate the site of vessel occlusion and collateral circulation. After angiographic confirmation of acute M2 occlusion, a 6F guiding catheter (Envoy, Cordis Endovascular Corporation, USA) was positioned in the distal cervical or petrous internal carotid artery (ICA). A microcatheter (Echelon 10, Micro Therapeutics, USA) was used to cross the occlusion segment over a 0.014-in. microwire (Transend, Boston Scientific Corporation, USA). The lesion length was estimated from the proximal vessel occlusion to the beginning of the normal vessel distal to the clot on microcatheter angiography. A slightly oversized (0.5–1.0 mm) stent was used to allow complete apposition to the vessel wall. A Wingspan stent catheter was advanced across the lesion using the road map, and the stent was slowly deployed. If an in-stent stenosis was found on post-stenting angiography, balloon angioplasty using a Gateway balloon (Boston Scientific Corporation, USA) was performed within stent with slow balloon inflation to prevent vascular dissection or rupture. If a residual thrombosis was seen on post-stenting angiography, a microcatheter was navigated into the thrombotic segment, and then immediate thrombolysis with urokinase was given to dissolve the thrombosis. If recurrent thrombosis or reocclusion was identified on post-stenting angiography, intra-arterial injection of 6 mg abciximab (Reopro; Centocor, Leiden, Netherlands) through a guiding catheter was administered, and repeated 2 mg abciximab bolus was administered until a complete thrombolysis was achieved. Angiographic recanalization result was assessed according to the Thrombolysis in Cerebral Infarction (TICI) score [13]. After the procedure, a complete neurological examination was performed on all patients by a vascular neurologist, and all patients
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underwent non-enhanced brain CT for detection of possible hemorrhagic complications. MR diffusion imaging was performed on the first post-procedural day. After the procedure, daily aspirin 100 mg and clopidogrel 75 mg were administered; 2850 IU of low-molecular-weight nadroparin calcium (Fraxiparine; GlaxoSmithKline, Notre Dame De Ville, France) was also administered subcutaneously 2 or 3 times a day for at least three days. All patients were reevaluated in follow up 90 days after stenting (Figs. 1 and 2). 3. Results Ten patients (4 men and 6 women, mean age 68.4 ± 14.4) were included in this study from May 2010 until September 2011. The patients’ mean NIHSS score on admission was 13.8 points with standard deviation of 5.2 points. (range 6–23) The occlusion sites were located in the superior division (n = 4, left: 3, right: 1), the middle division (n = 1, right) and the inferior division (n = 5, all: right) of MCA. The mean time interval from stroke symptom onset to arrival at emergency department was 141 ± 116 min (Table 1). Two patients were taking 100 mg of aspirin daily prior to the ischemic stroke (patient 8 and 9). Four patients received a standard intravenous tPA (0.9 mg/kg body weight). Two patients (patient 3 and 6) arrived in our center beyond the 3-h time window. Another 4 patients were not able to receive an intravenous rtPA because patient 5 had the gastric polypectomy 12 days ago before he admitted to the emergency department, patient 7 had the Ventriculo-Peritoneal shunt after intracerebral hemorrhage, patient 8 was taking warfarin for atrial fibrillation and patient 10 had another acute ischemic stroke 2 days ago before referral to our center. Successful stent deployment and recanalization were achieved in all patients (TICI 2a: 1, TICI 2b: 6, TICI 3: 3) (Table 2). The mean time interval from stroke symptom onset to stenting was 348.9 ± 90.4 min. In 5 patients (50%), an in-stent stenosis was found on post-stenting angiography and was dilated with balloon angioplasty using a Gateway balloon. Additional post-stenting intra-arterial chemical thrombolysis was used in 9 patients. These included glycoprotein IIb/IIIa inhibitor (n = 3, mean dose; 11 mg) and urokinase (n = 7, mean dose; 292,857 U). We had no perforations or dissections at the target artery in any of the patients. One (patient 9) developed acute thrombosis in distal ICA of the stented side at 4 days after a stent placement and was managed with mechanical thrombectomy. None of the patients had intracranial hemorrhage on control CT. Table 2 shows the lesion location, the stent used, the angiographic results and the complications of stenting. Neurologic improvement on the NIHSS (mean improvement: 8.8 points) at 7 days after stenting occurred in all patients. At 7 days, patients’ NIHSS score was 5 ± 4.6 (median 4.5, range 0–15). Table 3 shows interval improvement in main neurological functions at 7 days after stenting. An mRS of ≤3 was achieved in 8 patients (80%) and an mRS of ≤2 was achieved in 6 patients (60%) at discharge. No ischemic events developed within 90 days follow up after stenting. 4. Discussion The European Cooperative Acute Stroke Study (ECASS) III trial allows the window for thrombolysis to extend to 4.5 h from the time of stroke symptom onset [14]. This extended time window may slightly increase the number of patients who receive intravenous tPA, but is unlikely to increase the rate of recanalization. There will still remain a portion of acute ischemic stroke patients who have contraindications to intravenous tPA, and only a small number of patients are still admitted in this time window. Also, the efficacy of intravenous tPA for recanalization is not sufficient. The recanalization rate with intravenous tPA is only 30% for M2
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S.M. Sung et al. / Clinical Neurology and Neurosurgery 119 (2014) 110–115
Fig. 1. Patient 2 presented with acute right MCA infarction. (A) DWI shows acute infarction in the right insula and frontal lobe (NIHSS score: 13). (B) CT perfusion images show perfusion defect with large area of diffusion/perfusion mismatching area in the right MCA territory. (C) Right ICA angiogram shows complete occlusion of proximal inferior M2 segment (arrow). Anteroposterior (D) and lateral (E) radiographies show full dilatation without a remnant stenosis of the Wingspan stent at proximal inferior M2 segment. (F) Post-procedural angiogram reveals near-complete recanalization of the inferior M2 segment (TICI grade 2b with sufficient collateral flow).
S.M. Sung et al. / Clinical Neurology and Neurosurgery 119 (2014) 110–115
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Fig. 2. Patient 8 presented with acute right MCA infarction. (A) DWI shows acute infarction in right insula and frontal and parietal lobes (NIHSS score: 6). Anteroposterior oblique (B) and lateral (C) views of the right ICA angiogram show complete occlusion of proximal inferior M2 segment (arrow). Post-stenting radiography (D) and angiogram (E) after two Wingspan stents deployment reveal complete recanalization of the inferior M2 segment. (F) Post-procedural angiogram reveals complete recanalization without remnant or distal migrated thrombosis (TICI grade 3) of the MCA.
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Table 1 Clinical characteristics and outcomes of 10 patients undergoing stenting for acute M2 occlusion. Patients no.
1 2 3 4 5 6 7 8 9 10
Sex/age
F/41 M/53 M/61 M/62 M/66 F/76 F/77 F/79 F/82 F/87
Vascular risk factors
None AF HT, AF, smoking HT None None None HT, AF HT HT
Time (minutes)
Occlusion segment/side
Sx onset to arrival
Sx onset to stenting
204 370 229 153 43 218 28 19 26 120
314 472 476 256 263 399 249 441 331 288
Inferior/right Inferior/right Inferior/right Middle/right Superior/left Superior/left Inferior/right Inferior/right Superior/right Superior/left
NIHSS score
Discharge
Initial
7 Days (change)
mRS
18 13 12 15 23 13 19 6 12 7
5 (13↓) 6 (7↓) 3 (9↓) 2 (13↓) 15 (8↓) 0 (13↓) 4 (15↓) 0 (6↓) 10 (2↓) 5 (2↓)
3 2 2 1 4 0 1 0 4 3
Abbreviations: NIHSS, National Institutes of Health Stroke Scale; mRS, modified Rankin scale; Sx, Symptom; AF, atrial fibrillation; HT, hypertension.
Table 2 Interventional details for 10 patients undergoing stenting for acute M2 occlusion. Patients no.
IV tPA
Stent used (mm)
PTA for stenosis
IA UK (unit)
IA Reopro
Procedural complications
Symptomatic ICH
TICI grade
1 2 3 4 5 6 7 8 9 10
Done Done No No Done No No No Done No
2.5/20 2.5/20 2.5/20 3.0/20 2.5/20 3.5/20 2.5/20 3.5/20 & 3.5/20 2.5/20 3.0/20
Done No Done No Done No No Done No Done
200,000 – 400,000 300,000 500,000 230,000 300,000 – 120,000 –
– – – – – – 10 mg 10 mg – 14 mg
None None None None None None None None Nonea None
None None None None None None None None None None
2b 2b 2b 2b 2a 3 2b 3 2b 3
Abbreviations: M2, second segment of MCA; IV, intravenous; PTA, percutaneous balloon angioplasty; IA, intra-arterial; UK, urokinase; ICH, intracranial hemorrhage; TICI; Thrombolysis in Cerebral Infarction. a Thrombotic occlusion of ipsilateral distal internal carotid artery at the 4th post-stenting days.
occlusion [2]. Intra-arterial thrombolysis extends the time window for patients with MCA occlusion to 6 h from symptom onset. Direct intra-arterial thrombolysis appears to improve the likelihood of successful recanalization. The recanalization rate for M1 occlusions was 66% for IA pro-urokinase in the Prolyse in Acute Cerebral Thromboembolism (PROACT) II trial [4]. The Interventional Management of Stroke Trial (IMS) II demonstrated better recanalization rates (53%) in the group treated with combined intravenous plus intra-arterial tPA [15]. Mechanical thromboembolectomy is proposed for treatment in case of failed recanalization after thrombolysis or in patients with contraindications for thrombolytic therapy. But, overall recanalization rate of the FDA approved Merci Retriever System was only 55% (47–63%) [16]. Recently published IMS III showed better reperfusion rate for M2 occlusion (70% for single and 77% for multiple occlusions, based on a TICI score of 2–3). But, reperfusion rates, as measured by a TICI score of 2b–3, were 44% for a single M2 occlusion and 23% for multiple M2 occlusions. [17]. Mechanical recanalization may have lower
rates of intracranial hemorrhage and higher rates of recanalization compared with intra-arterial thrombolytics [18] but a recent clinical registry of 1000 patients treated with mechanical clot retrieval suggested the opposite [19]. The failure of thrombolysis to achieve sufficient recanalization led to the advent of mechanical recanalization using intracranial stenting [20]. The main advantage of intracranial stents over other mechanical thrombolysis is rapid flow restoration. A self-expandable Wingspan stent has several advantages over a balloon-mounted stent. The Wingspan stent can be delivered to the target vessel with reduced barotrauma, theoretically decreasing the risk of parent vessel dissection or rupture. The stents adapt to the shape and diameter of the affected artery much better than balloon-mounted stents. Modifications to delivery microcatheter have made Wingspan stent much easier to navigate to target vessels, particularly in patients with tortuous arterial anatomy [21]. Several case series showed that intracranial stents could be used for acute ischemic stroke treatment with high recanalization and low complication rates [6–12]. Zaidat et al.
Table 3 Changes of main neurological deficits before and after stenting at 7 days. Patients no.
Speech Before
1 2 3 4 5 6 7 8 9 10
Global Global Glocal
After
Normal Global Normal
Gaze preference
Hemianopia
Motor power (U, L)
Sensory dysfunction
Extinction
Before
After
Before
After
Before
After
Before
Before
After
+ + +
– – –
Complete Complete
– –
Complete Complete Complete Complete Complete
+ + +
– – –
– – –
– – – –
4/5, 4/5 4/5, 5/5 5/5, 5/5 5/5, 5/5 3/5, 4/5
+ + +
+ + + +
1/5, 1/5 2/5. 3/5 3/5, 3/5 2/5, 3/5 2/5, 2/5 1/5, 2/5
4/5, 5/5
+
+
+
–
3/5, 3/5 3/5, 3/5
3/5, 3/5 4/5, 4/5
+
–
+
–
Abbreviations: U, upper extremity; L, lower extremity.
– – – – Partial
After
S.M. Sung et al. / Clinical Neurology and Neurosurgery 119 (2014) 110–115
reported nine patients with acute ischemic stroke who underwent acute self-expanding intracranial stent placement. This report did not include the isolated MCA M2 occlusion. They had partial and complete recanalization (TICI 2 and 3) in 89% who were treated at a mean time of 5.1 h from the time of stroke onset and six of the patients had a good clinical outcome (mRS ≤ 2) at 90-day follow-up. Brekenfeld et al. [10] retrospectively reported the feasibility and the safety of a self-expanding Wingspan stent for acute cerebral artery occlusion. Although the number of patients (n = 12) was small, they had partial and complete recanalization (TIMI 2 and 3) in 92%. However, they did not include a case of the isolated MCA M2 occlusion either. The Stent-Assisted Recanalization in Acute Ischemic Stroke (SARIS) trial is the first FDA-approved prospective trial investigating stenting using Neuroform or Wingspan for the treatment of acute stroke. Twenty adult patients with poor NIHSS scores (mean, 14 ± 3.8) were treated within 5.5 h of symptom onset on average. They did not specify the occluded division of MCA. They had partial or complete recanalization in all treated patients (TIMI 2 = 40%, TIMI 3 = 60%). Moderate to good clinical outcomes (mRS ≤ 3) were achieved in 60% of patients at 30-day follow-up. Compared to SARIS trial, we only used a Wingspan stent for recanalization. Our patients improved on the NIHSS (mean improvement of 8.8 points) to a NIHSS score of 5 ± 4.6 (median 4.5; range 0–15) at 7 days after stenting. At discharge, an mRS of ≤3 was achieved in our eight patients and an mRS of ≤2 was achieved in 6 out of 10 patients (60%). In the MERCI and Penumbra trials, the functional outcome of an mRS ≤ 2 was achieved in 36% and 25% of the patients, respectively [16,22]. Brekenfeld et al. [10] achieved the functional outcome of a mRS ≤ 2 in only 25% of the patients. The most important step to improved clinical outcome for acute ischemic stroke patients is the time to recanalization [23]. Our mean time interval from stroke symptom onset to stenting (348.9 vs 393 min) was shorter than the study of Brekenfeld et al. This might explain the better functional outcomes of our cases. Even though the number of patients in our study was small, our neurological and functional outcomes showed that recanalization with an intracranial stent was a good rescue modality for an acute M2 occlusion if the patient was properly selected. There are some limitations in our case series. The small number of patients limits the good clinical outcome and recanalization rate in our case series. When intravenous thrombolysis with tPA was ineffective or not available for an acute M2 occlusion, we attempted stenting as a salvageable method regardless of whether the occlusion was caused by an embolic or atherosclerotic origin. It is difficult to distinguish completely which is an embolic or atherosclerotic origin by clinical symptoms and images. A concern is the rate of restenosis after placement of stent in distal small intracranial arteries. Mechanical devices may cause vascular injury, leading to exposed endothelium allowing platelet aggregation or thrombus formation, which in turn may lead to acute or subacute reocclusion [24]. Restenosis rates are reported to range between 10% and 30% with bare metal stents placed in the intracranial circulation [25]. These rates could be lower in the future with aggressive medical therapy including an antiplatelet and a statin. We need to follow-up a long-term stent patency and a recurrence of in-stent thrombosis of our patients. 5. Conclusions This case series, although limited by small number of patient, suggest that the recanalization with an intracranial stent is safe and feasible in selected patients of acute M2 occlusion and can provide good recanalization rate and functional outcome. If there exists a diffusion/perfusion mismatch or a clinical/diffusion mismatch, recanalization with an intracranial stent can be a rescue therapy for acute M2 occlusions when intravenous thrombolysis
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has failed or is contraindicated. Its long term effect on angiographic and clinical outcomes remains to be evaluated. References [1] Molina CA, Alvarez-Sabín J. Recanalization and reperfusion therapies for acute ischemic stroke. Cerebrovasc Dis 2009;27(Suppl. 1):162–7. [2] Wolpert SM, Bruckmann H, Greenlee R. Neuroradiologic evaluation of patients with acute stroke treated with recombinant tissue-plasminogen activator. AJNR Am J Neuroradiol 1993;14:3–13. [3] The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 1995;333(24):1581–7. [4] Furlan A, Higashida R, Wechsler L, Gent M, Rowley H, Kase C, et al. Intraarterial prourokinase for acute ischemic stroke. The PROACT II study: a randomized controlled trial. Prolyse in acute cerebral thromboembolism. JAMA 1999;282:2003–11. [5] Jauch EC, Saver JL, Adams Jr HP, Bruno A, Connors JJ, Demaerschalk BM, et al. 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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Emergent intracranial stenting for acute M2 occlusion of middle cerebral artery Sang Min Sung a,b,d,∗ , Tae Hong Lee a,c , Sang Won Lee e , Han Jin Cho a,b , Kyu Hyun Park a,b , Dae Soo Jung a,b a
Stroke Center, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea Department of Neurology, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea c Department of Diagnostic Radiology, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea d Biomedical Research Institute, Pusan National University Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea e Department of Neurosurgery, Pusan National University Yangsan Hospital, School of Medicine, Pusan National University, Busan, Republic of Korea b
a r t i c l e
i n f o
Article history: Received 18 April 2013 Received in revised form 19 November 2013 Accepted 28 January 2014 Available online 6 February 2014 Keywords: Acute ischemic stroke Second segment of middle cerebral artery Self-expandable stent Intracranial stenting Recanalization
a b s t r a c t Objective: Intracranial stenting is a possible option as a rescue strategy for acute secondary division (M2) occlusion of middle cerebral artery (MCA) when intravenous thrombolysis is ineffective or contraindicated. Methods: We reviewed 10 patients of acute M2 occlusion treated by intracranial stenting who were ineligible for intravenous thrombolysis or resistant to intravenous thrombolysis. All patients underwent intracranial stenting with the Wingspan stent system. We analyzed clinical and angiographic outcomes. Results: The mean NIHSS score on admission was 13.8 points (range 6–23). The occlusion sites were located in the superior division (n = 4, left: 3, right: 1), the middle division (n = 1, right) and the inferior division (n = 5, all: right) of MCA. The mean time interval from stroke symptom onset to stenting was 348.9 ± 90.4 min. Successful recanalization was achieved in all patients. No intracranial hemorrhage, vessel perforations or dissections occurred in any patient. One patient developed acute thrombosis in distal ICA of the stented side at 4 days after a stent placement and was managed with mechanical thrombectomy. All patients improved on the NIHSS (mean amount: 8.8) and to the NIHSS score of 5 ± 4.6 (median 4.5, range 0–15) at 7 days. At discharge, an mRS of ≤3 was achieved in 8 patients (80%) and an mRS of ≤2 was achieved in 6 patients (60%). Conclusions: Endovascular recanalization with a Wingspan stent can be a safe and feasible procedure for acute M2 occlusion when intravenous thrombolysis is ineffective or not available. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Successful recanalization is an important factor in determining good outcome in acute ischemic stroke [1]. However, the efficacy of intravenous tPA for complete recanalization is relatively low, and the recanalization rate for acute M2 occlusions after intravenous tPA is approximately 30% [2]. Intra-arterial thrombolysis alone, or in combination with intravenous thrombolysis may be more effective. However, the rate of recanalization of chemical intra-arterial and intravenous thrombolysis is still unsatisfactory. The rates of symptomatic intracranial hemorrhage were 6.4% in NINDS [3] and 10% in PROACT II studies [4]. There are several exclusion criteria
∗ Corresponding author at: Stroke Center, Pusan National University Hospital, School of Medicine, Pusan National University, 10, Ami-Dong 1-Ga, Seo-Gu, Busan 602-739, Republic of Korea. Tel.: +82 51 240 7317; fax: +82 51 245 2783. E-mail addresses: [email protected], [email protected] (S.M. Sung). 0303-8467/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2014.01.027
of intravenous and intra-arterial thrombolysis. Main exclusion criteria are (1) significant head trauma or prior stroke in previous 3 months. (2) Symptoms suggesting subarachnoid hemorrhage. (3) History of previous intracranial hemorrhage. (4) Elevated blood pressure (systolic > 185 mm Hg or diastolic >110 mm Hg). (5) Platelet count 1.7 or PT > 15 s. (7) Current use of direct thrombin inhibitors or direct factor Xa inhibitors with elevated sensitive laboratory tests (such as aPTT, INR, platelet count, and ecarin clotting time; TT; or appropriate factor Xa activity assays). (8) Blood glucose concentration 1/3 cerebral hemisphere) [5]. Recent case series reported acceptable safety, good outcomes and good recanalization rates with intracranial stenting in patients with acute MCA occlusion if other recanalization modalities have failed or in patients who have been ineligible for intravenous tPA [6–12]. However, there has not been much reported regarding the use of intracranial stents for recanalization of acute M2 occlusions.
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We report recanalization rates, complications, and outcomes of patients treated with intracranial stenting as a rescue procedure for acute M2 occlusion.
2. Materials and methods Ten patients with acute M2 occlusion were treated by intracranial stenting in our stroke center between May 1, 2010 and September 31, 2011. Our Institutional Review Board approved collection of interventional and clinical data for this study. Informed consent was obtained from the patient or the next of kin in this off-label stenting for recanalization. We treated patients in whom recanalization was not achieved with intravenous thrombolysis, patients who were ineligible for intravenous thrombolysis or who presented after 3 h of symptom onset. Stenting was completed within 8 h from stroke symptom onset. Diffusion-weighted image (DWI), computed tomography (CT), CT perfusion (CTP), and CT angiography were performed to assess for arterial occlusion and diffusion/perfusion mismatch. DWI was done in all patients and CTP was done in 8 patients. We analyzed demographic features, clinical characteristics, location of occlusion, symptom onset to arrival time, symptom onset to stenting time, use of adjunctive chemical therapies (urokinase or glycoprotein IIb/IIIa inhibitors), and procedural complications. National Institute of Health Stroke Scale (NIHSS) was checked before and at 7 days after stenting. The modified Rankin Score (mRS) was also checked at discharge. Outcome was stratified to “good” (mRS 0–2), “moderate” (mRS 3), and “poor” (mRS 4–6). Recanalization result was evaluated by the Thrombolysis in Cerebral Infarction (TICI) score (graded as 0 for absent perfusion, 1 for minimal distal perfusion, 2 for partial perfusion, and 3 for complete perfusion). Interventional procedures were performed in the neuroangiography room equipped with a digital subtraction angiography system (Axiom Artis, Siemens, Germany). All stents were deployed under local anesthesia. Percutaneous access using 6-French sheath was gained via the common femoral artery. Diagnostic angiography including all cerebral arteries was performed to evaluate the site of vessel occlusion and collateral circulation. After angiographic confirmation of acute M2 occlusion, a 6F guiding catheter (Envoy, Cordis Endovascular Corporation, USA) was positioned in the distal cervical or petrous internal carotid artery (ICA). A microcatheter (Echelon 10, Micro Therapeutics, USA) was used to cross the occlusion segment over a 0.014-in. microwire (Transend, Boston Scientific Corporation, USA). The lesion length was estimated from the proximal vessel occlusion to the beginning of the normal vessel distal to the clot on microcatheter angiography. A slightly oversized (0.5–1.0 mm) stent was used to allow complete apposition to the vessel wall. A Wingspan stent catheter was advanced across the lesion using the road map, and the stent was slowly deployed. If an in-stent stenosis was found on post-stenting angiography, balloon angioplasty using a Gateway balloon (Boston Scientific Corporation, USA) was performed within stent with slow balloon inflation to prevent vascular dissection or rupture. If a residual thrombosis was seen on post-stenting angiography, a microcatheter was navigated into the thrombotic segment, and then immediate thrombolysis with urokinase was given to dissolve the thrombosis. If recurrent thrombosis or reocclusion was identified on post-stenting angiography, intra-arterial injection of 6 mg abciximab (Reopro; Centocor, Leiden, Netherlands) through a guiding catheter was administered, and repeated 2 mg abciximab bolus was administered until a complete thrombolysis was achieved. Angiographic recanalization result was assessed according to the Thrombolysis in Cerebral Infarction (TICI) score [13]. After the procedure, a complete neurological examination was performed on all patients by a vascular neurologist, and all patients
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underwent non-enhanced brain CT for detection of possible hemorrhagic complications. MR diffusion imaging was performed on the first post-procedural day. After the procedure, daily aspirin 100 mg and clopidogrel 75 mg were administered; 2850 IU of low-molecular-weight nadroparin calcium (Fraxiparine; GlaxoSmithKline, Notre Dame De Ville, France) was also administered subcutaneously 2 or 3 times a day for at least three days. All patients were reevaluated in follow up 90 days after stenting (Figs. 1 and 2). 3. Results Ten patients (4 men and 6 women, mean age 68.4 ± 14.4) were included in this study from May 2010 until September 2011. The patients’ mean NIHSS score on admission was 13.8 points with standard deviation of 5.2 points. (range 6–23) The occlusion sites were located in the superior division (n = 4, left: 3, right: 1), the middle division (n = 1, right) and the inferior division (n = 5, all: right) of MCA. The mean time interval from stroke symptom onset to arrival at emergency department was 141 ± 116 min (Table 1). Two patients were taking 100 mg of aspirin daily prior to the ischemic stroke (patient 8 and 9). Four patients received a standard intravenous tPA (0.9 mg/kg body weight). Two patients (patient 3 and 6) arrived in our center beyond the 3-h time window. Another 4 patients were not able to receive an intravenous rtPA because patient 5 had the gastric polypectomy 12 days ago before he admitted to the emergency department, patient 7 had the Ventriculo-Peritoneal shunt after intracerebral hemorrhage, patient 8 was taking warfarin for atrial fibrillation and patient 10 had another acute ischemic stroke 2 days ago before referral to our center. Successful stent deployment and recanalization were achieved in all patients (TICI 2a: 1, TICI 2b: 6, TICI 3: 3) (Table 2). The mean time interval from stroke symptom onset to stenting was 348.9 ± 90.4 min. In 5 patients (50%), an in-stent stenosis was found on post-stenting angiography and was dilated with balloon angioplasty using a Gateway balloon. Additional post-stenting intra-arterial chemical thrombolysis was used in 9 patients. These included glycoprotein IIb/IIIa inhibitor (n = 3, mean dose; 11 mg) and urokinase (n = 7, mean dose; 292,857 U). We had no perforations or dissections at the target artery in any of the patients. One (patient 9) developed acute thrombosis in distal ICA of the stented side at 4 days after a stent placement and was managed with mechanical thrombectomy. None of the patients had intracranial hemorrhage on control CT. Table 2 shows the lesion location, the stent used, the angiographic results and the complications of stenting. Neurologic improvement on the NIHSS (mean improvement: 8.8 points) at 7 days after stenting occurred in all patients. At 7 days, patients’ NIHSS score was 5 ± 4.6 (median 4.5, range 0–15). Table 3 shows interval improvement in main neurological functions at 7 days after stenting. An mRS of ≤3 was achieved in 8 patients (80%) and an mRS of ≤2 was achieved in 6 patients (60%) at discharge. No ischemic events developed within 90 days follow up after stenting. 4. Discussion The European Cooperative Acute Stroke Study (ECASS) III trial allows the window for thrombolysis to extend to 4.5 h from the time of stroke symptom onset [14]. This extended time window may slightly increase the number of patients who receive intravenous tPA, but is unlikely to increase the rate of recanalization. There will still remain a portion of acute ischemic stroke patients who have contraindications to intravenous tPA, and only a small number of patients are still admitted in this time window. Also, the efficacy of intravenous tPA for recanalization is not sufficient. The recanalization rate with intravenous tPA is only 30% for M2
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Fig. 1. Patient 2 presented with acute right MCA infarction. (A) DWI shows acute infarction in the right insula and frontal lobe (NIHSS score: 13). (B) CT perfusion images show perfusion defect with large area of diffusion/perfusion mismatching area in the right MCA territory. (C) Right ICA angiogram shows complete occlusion of proximal inferior M2 segment (arrow). Anteroposterior (D) and lateral (E) radiographies show full dilatation without a remnant stenosis of the Wingspan stent at proximal inferior M2 segment. (F) Post-procedural angiogram reveals near-complete recanalization of the inferior M2 segment (TICI grade 2b with sufficient collateral flow).
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Fig. 2. Patient 8 presented with acute right MCA infarction. (A) DWI shows acute infarction in right insula and frontal and parietal lobes (NIHSS score: 6). Anteroposterior oblique (B) and lateral (C) views of the right ICA angiogram show complete occlusion of proximal inferior M2 segment (arrow). Post-stenting radiography (D) and angiogram (E) after two Wingspan stents deployment reveal complete recanalization of the inferior M2 segment. (F) Post-procedural angiogram reveals complete recanalization without remnant or distal migrated thrombosis (TICI grade 3) of the MCA.
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Table 1 Clinical characteristics and outcomes of 10 patients undergoing stenting for acute M2 occlusion. Patients no.
1 2 3 4 5 6 7 8 9 10
Sex/age
F/41 M/53 M/61 M/62 M/66 F/76 F/77 F/79 F/82 F/87
Vascular risk factors
None AF HT, AF, smoking HT None None None HT, AF HT HT
Time (minutes)
Occlusion segment/side
Sx onset to arrival
Sx onset to stenting
204 370 229 153 43 218 28 19 26 120
314 472 476 256 263 399 249 441 331 288
Inferior/right Inferior/right Inferior/right Middle/right Superior/left Superior/left Inferior/right Inferior/right Superior/right Superior/left
NIHSS score
Discharge
Initial
7 Days (change)
mRS
18 13 12 15 23 13 19 6 12 7
5 (13↓) 6 (7↓) 3 (9↓) 2 (13↓) 15 (8↓) 0 (13↓) 4 (15↓) 0 (6↓) 10 (2↓) 5 (2↓)
3 2 2 1 4 0 1 0 4 3
Abbreviations: NIHSS, National Institutes of Health Stroke Scale; mRS, modified Rankin scale; Sx, Symptom; AF, atrial fibrillation; HT, hypertension.
Table 2 Interventional details for 10 patients undergoing stenting for acute M2 occlusion. Patients no.
IV tPA
Stent used (mm)
PTA for stenosis
IA UK (unit)
IA Reopro
Procedural complications
Symptomatic ICH
TICI grade
1 2 3 4 5 6 7 8 9 10
Done Done No No Done No No No Done No
2.5/20 2.5/20 2.5/20 3.0/20 2.5/20 3.5/20 2.5/20 3.5/20 & 3.5/20 2.5/20 3.0/20
Done No Done No Done No No Done No Done
200,000 – 400,000 300,000 500,000 230,000 300,000 – 120,000 –
– – – – – – 10 mg 10 mg – 14 mg
None None None None None None None None Nonea None
None None None None None None None None None None
2b 2b 2b 2b 2a 3 2b 3 2b 3
Abbreviations: M2, second segment of MCA; IV, intravenous; PTA, percutaneous balloon angioplasty; IA, intra-arterial; UK, urokinase; ICH, intracranial hemorrhage; TICI; Thrombolysis in Cerebral Infarction. a Thrombotic occlusion of ipsilateral distal internal carotid artery at the 4th post-stenting days.
occlusion [2]. Intra-arterial thrombolysis extends the time window for patients with MCA occlusion to 6 h from symptom onset. Direct intra-arterial thrombolysis appears to improve the likelihood of successful recanalization. The recanalization rate for M1 occlusions was 66% for IA pro-urokinase in the Prolyse in Acute Cerebral Thromboembolism (PROACT) II trial [4]. The Interventional Management of Stroke Trial (IMS) II demonstrated better recanalization rates (53%) in the group treated with combined intravenous plus intra-arterial tPA [15]. Mechanical thromboembolectomy is proposed for treatment in case of failed recanalization after thrombolysis or in patients with contraindications for thrombolytic therapy. But, overall recanalization rate of the FDA approved Merci Retriever System was only 55% (47–63%) [16]. Recently published IMS III showed better reperfusion rate for M2 occlusion (70% for single and 77% for multiple occlusions, based on a TICI score of 2–3). But, reperfusion rates, as measured by a TICI score of 2b–3, were 44% for a single M2 occlusion and 23% for multiple M2 occlusions. [17]. Mechanical recanalization may have lower
rates of intracranial hemorrhage and higher rates of recanalization compared with intra-arterial thrombolytics [18] but a recent clinical registry of 1000 patients treated with mechanical clot retrieval suggested the opposite [19]. The failure of thrombolysis to achieve sufficient recanalization led to the advent of mechanical recanalization using intracranial stenting [20]. The main advantage of intracranial stents over other mechanical thrombolysis is rapid flow restoration. A self-expandable Wingspan stent has several advantages over a balloon-mounted stent. The Wingspan stent can be delivered to the target vessel with reduced barotrauma, theoretically decreasing the risk of parent vessel dissection or rupture. The stents adapt to the shape and diameter of the affected artery much better than balloon-mounted stents. Modifications to delivery microcatheter have made Wingspan stent much easier to navigate to target vessels, particularly in patients with tortuous arterial anatomy [21]. Several case series showed that intracranial stents could be used for acute ischemic stroke treatment with high recanalization and low complication rates [6–12]. Zaidat et al.
Table 3 Changes of main neurological deficits before and after stenting at 7 days. Patients no.
Speech Before
1 2 3 4 5 6 7 8 9 10
Global Global Glocal
After
Normal Global Normal
Gaze preference
Hemianopia
Motor power (U, L)
Sensory dysfunction
Extinction
Before
After
Before
After
Before
After
Before
Before
After
+ + +
– – –
Complete Complete
– –
Complete Complete Complete Complete Complete
+ + +
– – –
– – –
– – – –
4/5, 4/5 4/5, 5/5 5/5, 5/5 5/5, 5/5 3/5, 4/5
+ + +
+ + + +
1/5, 1/5 2/5. 3/5 3/5, 3/5 2/5, 3/5 2/5, 2/5 1/5, 2/5
4/5, 5/5
+
+
+
–
3/5, 3/5 3/5, 3/5
3/5, 3/5 4/5, 4/5
+
–
+
–
Abbreviations: U, upper extremity; L, lower extremity.
– – – – Partial
After
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reported nine patients with acute ischemic stroke who underwent acute self-expanding intracranial stent placement. This report did not include the isolated MCA M2 occlusion. They had partial and complete recanalization (TICI 2 and 3) in 89% who were treated at a mean time of 5.1 h from the time of stroke onset and six of the patients had a good clinical outcome (mRS ≤ 2) at 90-day follow-up. Brekenfeld et al. [10] retrospectively reported the feasibility and the safety of a self-expanding Wingspan stent for acute cerebral artery occlusion. Although the number of patients (n = 12) was small, they had partial and complete recanalization (TIMI 2 and 3) in 92%. However, they did not include a case of the isolated MCA M2 occlusion either. The Stent-Assisted Recanalization in Acute Ischemic Stroke (SARIS) trial is the first FDA-approved prospective trial investigating stenting using Neuroform or Wingspan for the treatment of acute stroke. Twenty adult patients with poor NIHSS scores (mean, 14 ± 3.8) were treated within 5.5 h of symptom onset on average. They did not specify the occluded division of MCA. They had partial or complete recanalization in all treated patients (TIMI 2 = 40%, TIMI 3 = 60%). Moderate to good clinical outcomes (mRS ≤ 3) were achieved in 60% of patients at 30-day follow-up. Compared to SARIS trial, we only used a Wingspan stent for recanalization. Our patients improved on the NIHSS (mean improvement of 8.8 points) to a NIHSS score of 5 ± 4.6 (median 4.5; range 0–15) at 7 days after stenting. At discharge, an mRS of ≤3 was achieved in our eight patients and an mRS of ≤2 was achieved in 6 out of 10 patients (60%). In the MERCI and Penumbra trials, the functional outcome of an mRS ≤ 2 was achieved in 36% and 25% of the patients, respectively [16,22]. Brekenfeld et al. [10] achieved the functional outcome of a mRS ≤ 2 in only 25% of the patients. The most important step to improved clinical outcome for acute ischemic stroke patients is the time to recanalization [23]. Our mean time interval from stroke symptom onset to stenting (348.9 vs 393 min) was shorter than the study of Brekenfeld et al. This might explain the better functional outcomes of our cases. Even though the number of patients in our study was small, our neurological and functional outcomes showed that recanalization with an intracranial stent was a good rescue modality for an acute M2 occlusion if the patient was properly selected. There are some limitations in our case series. The small number of patients limits the good clinical outcome and recanalization rate in our case series. When intravenous thrombolysis with tPA was ineffective or not available for an acute M2 occlusion, we attempted stenting as a salvageable method regardless of whether the occlusion was caused by an embolic or atherosclerotic origin. It is difficult to distinguish completely which is an embolic or atherosclerotic origin by clinical symptoms and images. A concern is the rate of restenosis after placement of stent in distal small intracranial arteries. Mechanical devices may cause vascular injury, leading to exposed endothelium allowing platelet aggregation or thrombus formation, which in turn may lead to acute or subacute reocclusion [24]. Restenosis rates are reported to range between 10% and 30% with bare metal stents placed in the intracranial circulation [25]. These rates could be lower in the future with aggressive medical therapy including an antiplatelet and a statin. We need to follow-up a long-term stent patency and a recurrence of in-stent thrombosis of our patients. 5. Conclusions This case series, although limited by small number of patient, suggest that the recanalization with an intracranial stent is safe and feasible in selected patients of acute M2 occlusion and can provide good recanalization rate and functional outcome. If there exists a diffusion/perfusion mismatch or a clinical/diffusion mismatch, recanalization with an intracranial stent can be a rescue therapy for acute M2 occlusions when intravenous thrombolysis
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