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Ischemic stroke
Original Research
Emergency carotid artery stenting in patients with acute ischemic stroke due to occlusion or stenosis of the proximal internal carotid artery: a single-center experience
  1. Seungnam Son1,2,
  2. Dae Seob Choi2,3,4,
  3. Min Kyun Oh2,4,5,
  4. Soo-Kyoung Kim1,2,
  5. Heeyoung Kang1,4,
  6. Ki-Jong Park1,4,
  7. Nack-Cheon Choi1,2,4,
  8. Oh-Young Kwon1,4,
  9. Byeong Hoon Lim1,2,4
  1. 1Department of Neurology, Gyeongsang National University School of Medicine, Jinju, Korea
  2. 2Gyeongnam Regional Cardiocerebrovascular Disease Center, Jinju, Korea
  3. 3Department of Radiology, Gyeongsang National University School of Medicine, Jinju, Korea
  4. 4Gyeongsang Institute of Health Science, Gyeongsang National University School of Medicine, Jinju, Korea
  5. 5Rehabilitation Medicine, Gyeongsang National University School of Medicine, Jinju, Korea
  1. Correspondence to Dr Dae Seob Choi, Department of Radiology, Gyeongsang National University School of Medicine, 79 Gangnam-ro, Jinju 660-702, South Korea; choids{at}gnu.ac.kr

Abstract

Background The feasibility, safety and effectiveness of emergency carotid artery stenting (eCAS) in patients with acute ischemic stroke (AIS) due to proximal internal carotid artery (ICA) stenosis or occlusion are still controversial. In this study we analyzed our experience with eCAS in patients with AIS.

Methods Twenty-two eCAS procedures for proximal ICA stenosis or occlusion were performed in 22 patients at our institution between January 2011 and November 2013. The mean time from stroke symptom onset to presentation was 204 min (range 50–630 min) and the mean initial score on the National Institutes of Health Stroke Scale (NIHSS) was 12.55 (range 5–23). Ten patients had total occlusion of the proximal ICA and the remaining 12 patients had near total occlusion or severe stenosis (mean degree 90.7%, range 80–100%). Eleven patients also had tandem occlusion on the more distal intracranial arteries.

Results Successful stent insertion was achieved in all patients and additional thrombectomy using a Solitaire stent or Penumbra aspiration catheter achieved a Thrombolysis In Cerebral Infarction grade of more than 2a in all patients with distal tandem occlusion. Procedure-related complications occurred in one patient (cerebral hyperperfusion syndrome) who recovered successfully. The mean NIHSS score at discharge was 3.55 (range 0–18). The mean modified Rankin Scale score at 3 months was 1±1.67 (range 0–6).

Conclusions eCAS in patients with AIS due to proximal ICA stenosis or occlusion appears to be a technically feasible and effective method for achieving good clinical outcomes.

  • Atherosclerosis
  • Stroke

https://doi.org/10.1136/neurintsurg-2014-011141

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    Introduction

    Early recanalization of an occluded artery is important for improving functional outcome and reducing mortality in patients with acute ischemic stroke (AIS).1 However, the clinical outcome after medical treatment is usually very poor in cases of AIS induced by occlusion or stenosis of the proximal internal carotid artery (ICA) that results in severe neurological symptoms and is usually not accessible by recombinant tissue plasminogen activator (rtPA) thrombolysis.2 ,3 In recent years the feasibility, safety and effectiveness of emergency carotid artery stenting (eCAS) with/without additional intra-arterial (IA) thrombolysis/thrombectomy have been studied extensively and both technically and clinically promising results have been reported.4–17 In addition, it was reported that early CAS (within 2 days) carries no additional risks compared with CAS after 2 days or any other intervention timing up to 90 days.18 Thus, a recent early treatment guideline considers this technique in patients with AIS resulting from cervical atherosclerosis or dissection.19

    However, in actual clinical practice there are several concerns when considering eCAS in patients with AIS, and clinicians usually hesitate to decide on the procedure.20 The concerns include the procedure's technical feasibility (eg, the success of stent insertion under severe stenosis or occlusion and the distal embolization caused by manipulation of highly vulnerable plaque), safety (eg, the potential risk of developing acute in-stent stenosis due to the lack of antiplatelet premedication), related complications (eg, cerebral hyperperfusion syndrome (CHS)) and effectiveness for improving patients’ neurological deficits and long-term follow-up.

    In this study we retrospectively analyzed 22 patients with AIS caused by proximal ICA occlusion or severe stenosis and treated with eCAS within the past 3 years. The effectiveness, safety and clinical outcomes of eCAS were assessed.

    Materials and methods

    Patients

    One hundred and thirty-six CAS procedures were performed in 129 patients at our institution between January 2011 and November 2013. Of these, 28 were performed as an emergency procedure in 28 patients who arrived within 8 h of stroke symptom onset or with unclear-onset stroke within 12 h from ‘last normal time’ according to a review of MRIs and perfusion MRIs. We reviewed all clinical and angiographic data of the patients. Five eCAS cases were excluded because they were performed for the easy assessment of more distal intracranial occlusion by stroke causes other than proximal ICA occlusion or stenosis. All of the excluded patients had proximal ICA stenosis (mean degree of stenosis 62%, range 50–80%) with combined occlusion of the middle cerebral artery (MCA). However, all of these patients had definite cardiogenic embolic sources, and the margin of the stenotic portion was smooth rather than ulcerative. We decided that the mechanism of infarction in these patients was cardiogenic embolism and performed eCAS merely to facilitate assessment. These patients were therefore excluded. In addition, one patient who received eCAS due to proximal ICA occlusion and was transferred to another institution immediately after the procedure was also excluded because we could not obtain any information regarding follow-up results.

    Ultimately, 22 patients who underwent eCAS as a primary treatment for stroke were included in this study (table 1). Twenty patients arrived within 8 h of stroke symptom onset and the remaining two patients arrived with unclear-onset stroke within 12 h from last normal time. The patient group consisted of 20 men (90.9%) and two women (9.1%) with a mean age of 71.2 years (range 41–85 years). Five patients (23%) had prior stroke or a transient ischemic attack (TIA). Stroke risk factors included hypertension (59.0%), diabetes (45.5%), smoking (27.3%), hyperlipidemia (27.3%) and cardiac disease (27.3%). In addition, two patients were diagnosed with cancer of the head or neck and had received radiotherapy previously (9.1%), but we could not determine if the stenosis was caused by radiation or atherosclerosis due to patency of the contralateral ICA and multiple atherosclerogenic risk factors. The causes of ICA occlusion or stenosis were atherosclerosis and/or radiation-induced carotid stenosis in 20 patients (90.9%) and ICA dissection in two patients (9.1%).

    View this table:
    Table 1

    Baseline characteristics of patients, procedural techniques and clinical outcomes

    The mean time from stroke symptom onset to presentation was 204 min (range 50–630 min) and the mean±SD initial National Institutes of Health Stroke Scale (NIHSS) score was 12.55±5.32 (range 5–23; table 1). All patients underwent MRI examinations according to the acute stroke protocol of our institution using a 1.5 Tesla magnet MRI (Magnetom Avanto; Siemens Medical Solutions, Erlangen, Germany). The acute stroke MRI protocol consisted of b0 and b1000 diffusion-weighted images (DWIs), gradient echo images, fluid-attenuated inversion recovery (FLAIR) images, gadolinium (Gadovist, Gadobutrol; Schering, Berlin, Germany)-enhanced T1-weighted images and gadolinium-enhanced magnetic resonance angiography (MRA) of the entire neck and intracranial arteries and/or perfusion-weighted MR images (PWI). The initial lesions on DWI included territorial lesions on the MCA in seven patients, border zone infarction in nine patients and multiple focal infarctions in six patients. The patients did not show any signal intensity changes on FLAIR images and the volume of DWI-PWI mismatch was more than 50%. If an ICA occlusion was observed on MRA we decided on immediate IA intervention. Twelve of the 22 patients received intravenous (IV) thrombolytic therapy using rtPA (Actylase; Boehringer Ingelheim, Basel, Switzerland). The mean time from presentation to femoral puncture was 105.4 min (range 40–320 min).

    The premedication protocols for eCAS differed according to the use of rtPA. If a patient received rtPA, only loading doses of atorvastatin (80 mg/day) were prescribed. In addition, the maintenance dose of clopidogrel (75 mg) with aspirin (100 mg) and atorvastatin (80 mg/day) was started 24 h after rtPA infusion. However, if the patient did not receive rtPA, a loading dose of clopidogrel (600 mg) with aspirin (300 mg) and atorvastatin (80 mg/day) was prescribed and the maintenance dose of clopidogrel (75 mg) with aspirin (100 mg) and atorvastatin (80 mg/day) was continued the day after eCAS.

    Intervention protocol

    All procedures were performed by an experienced neurointerventionist and a neurologist who was a trained neurointerventionist using a biplane angiography system (Artis Zee Biplane; Siemens). First, the femoral artery was punctured under local anesthesia and a femoral sheath was placed. In subjects with total occlusion, diagnostic angiography was performed to confirm the collateral vessels. When patients scored <2 on the American Society of Interventional and Therapeutic Neuroradiology Collateral Flow Grading System (ACG grade),21 the occluded proximal ICA was recanalized. The 6 F femoral sheath was changed to a 6 F shuttle catheter and placed distal to the common carotid artery. We navigated to the MCA using a 0.014 inch microguidewire and microcatheter and performed selective angiography to detect tandem distal occlusions. In patients with near total occlusion and severe stenosis the selective angiography was omitted. Next, predilation was performed using a 3 mm balloon. If a tandem occlusion was not observed at this step we prepared an embolic protection device (EPD) navigated through the stenotic segment and placed it on the distal cervical ICA. In patients with distal tandem occlusion we used a 0.014 inch microguidewire to deliver the balloons and stent instead of EPD. Predilation using a 4 or 5 mm balloon (Aviator plus PTA balloon, Cordis, Miami Lakes, Florida, USA; Ultra-soft SV balloon, Boston Scientific) was performed. The stent was selected according to the ICA course: a closed-cell stent was used in a straight course and an open-cell stent was used in a curved course. If the stenotic portion did not dilated fully despite predilatation and stent deployment, we performed post-dilation cautiously using a 5 mm or 6 mm balloon in selected patients. In patients with tandem occlusion on the more distal intracranial arteries, additional thrombectomy with a Solitare stent (ev3; Solitaire AB/FR, Irvine, California, USA) or manual aspiration thrombectomy using a Penumbra aspiration catheter (PS; Penumbra, Alameda, California, USA) was performed.

    Heparinized saline was continuously infused through the shuttle catheter to prevent in-catheter thrombosis and a 3000 U bolus of heparin was injected before stent deployment. IV atropine and/or IV dopamine was administered when severe hemodynamic effects (bradycardia, asystole or hypotension) developed after balloon inflation.

    Patients who underwent eCAS were monitored in the stroke unit or intensive care unit for 48 h with continuous blood pressure (BP), oxygen saturation and ECG monitoring and received neurological examinations hourly. We conducted extensive BP control in patients achieving complete recanalization to maintain a systolic BP level of 110–120 mm Hg and prevent the development of CHS for at least 48 h after the procedure.

    Follow-up

    The patients who received eCAS, except those prescribed warfarin due to atrial fibrillation, were discharged with dual antiplatelet agents (75 mg/day clopidogrel, 100 mg/day aspirin) and 40–80 mg/day atorvastatin. In the patients who took warfarin we prescribed only 75 mg/day clopidogrel with 40–80 mg/day atorvastatin. The medications were continued for at least 3 months after eCAS. A neurological examination was performed on the discharge day and on the day patients visited the outpatient department. A follow-up vascular evaluation at 6 and 12 months was recommended for all patients after CAS and annually thereafter.

    Results

    Interventional results

    The mean procedure time, including diagnostic angiography, was 61±26.8 min (range 35–140). Ten patients had total occlusion of the proximal ICA and the remaining 12 patients had near total occlusion or severe stenosis (mean degree of stenosis 90.7%, range 80–100%). Eight of the 10 patients with total occlusion were ACG grade 2 and two were ACG grade 0. Stents were inserted successfully in all patients (figures 1⇓–3). Eleven patients also had tandem occlusion of the more distal intracranial arteries on the initial angiogram. Spontaneous recanalization of the tandem occlusion after predilation to the proximal ICA was observed in three of 11 patients (one MCA proximal M1, two proximal M2; figure 1). The remaining eight patients received an additional thrombectomy after stent insertion using a Solitare stent or Penumbra aspiration catheter (figure 2). The final Thrombolysis In Cerebral Infarction (TICI) score in these patients was 3 in four patients, 2b in one patient and 2a in three patients (table 1).

    Figure 1
    Figure 1

    Emergency carotid artery stenting (eCAS) images of a patient with total occlusion on the right side. The patient presented at our institution approximately 180 min after stroke symptom onset and the initial National Institutes of Health Stroke Scale (NIHSS) score was 5. (A) Initial gadolinium-enhanced magnetic resonance angiogram (MRA) shows total occlusion of the right proximal internal carotid artery (ICA). (B) Pre-procedural extracranial lateral projection angiogram. Note the total occlusion of the right proximal ICA (black arrow). (C) Pre-procedural intracranial anterior to posterior (AP) projection of left internal carotid angiogram. The minimal collateral flow via the left anterior communicating artery is observed in the area of the right middle cerebral artery (MCA). Note the tandem occlusion of the proximal portion on the right MCA inferior division (black border arrow). (D) Extracranial lateral projection angiogram obtained immediately after carotid WallStent insertion to proximal ICA. The procedure was performed using Emboshield (black arrow head). (E) Post-procedural intracranial AP projection angiogram. The spontaneous recanalization of the occluded right MCA is observed. Moderate restenosis in the distal portion of the inserted stent was observed on the 6-month follow-up CT angiogram (not shown).

    Figure 2
    Figure 2

    Emergency carotid artery stenting (eCAS) images of a patient with near total occlusion on the right side. This patient presented at our institution approximately 60 min after stroke symptom onset and the initial National Institutes of Health Stroke Scale (NIHSS) score was 6. (A) Initial gadolinium-enhanced magnetic resonance angiogram (MRA) shows total occlusion of the right proximal internal carotid artery (ICA). (B) Pre-procedural extracranial lateral projection angiogram. Note the near total occlusion of the right proximal ICA (black arrow) and poorly visible distal ICA flow. (C) Extracranial lateral projection angiogram obtained immediately after carotid WallStent insertion to proximal ICA. The tandem occlusion on the distal ICA is observed (black border arrow). (D) Extracranial and intracranial lateral projection angiogram obtained immediately after thrombectomy to distal ICA tandem occlusion using a Penumbra aspiration catheter. A residual clot is observed on the proximal portion of the middle cerebral artery (MCA) (black arrow head). (E) Post-procedural extracranial and intracranial anterior to posterior (AP) projection angiogram. The MCA clot is successfully removed via Penumbra suction thrombectomy and the complete restoration of ICA and MCA flow is visible. The right anterior cerebral artery (ACA) arises from the left ACA (azygotic ACA).

    Figure 3
    Figure 3

    Emergency carotid artery stenting (eCAS) images of a patient with near total occlusion on the left side. The patient presented at our institution approximately 60 min after stroke symptom onset and the initial National Institutes of Health Stroke Scale (NIHSS) score was 9. (A) Initial gadolinium-enhanced magnetic resonance angiogram (MRA) shows near total occlusion of the left proximal internal carotid artery (ICA). (B) Pre-procedural extracranial lateral projection angiogram. Note the near total occlusion of the left proximal ICA (black arrow). (C) Post-procedural extracranial lateral projection angiogram. The carotid WallStent was successfully inserted into a pre-existing stenotic portion of the proximal ICA, and restoration of ICA flow is visible. (D) Magnetic resonance fluid-attenuated inversion recovery (MR-FLAIR) images obtained 24 h after eCAS. Cerebrospinal fluid attenuation is not observed in the left hemisphere with whole gyral swelling indicating cerebral hyperperfusion syndrome (CHS). (E) Follow-up MR-FLAIR images obtained 14 days after eCAS. Pre-existing changes due to CHS had disappeared completely. The patient was discharged 26 days after eCAS with mild proximal limb weakness. The NIHSS score at discharge was 3.

    An EPD (Emboshield; Abbott Vascular, Redwood City, California, USA) was used in eight of the 22 patients (36.7%). A stent was implanted in all patients after angioplasty: a Precise PRO RX stent (Cordis) in two patients (9.1%), a carotid WallStent (Boston Scientific/Target Therapeutics) in 16 patients (72.7%) and an RX Aculink carotid stent (Abbott Vascular) in four patients (18.2%).

    Transient hemodynamic changes such as hypotension and bradycardia were observed in nine patients during and/or after balloon inflation, who recovered after medical treatment. No major vascular access site complications were recorded.

    Perioperative myocardial infarction did not develop in any patient, but CHS occurred in one patient (4.5%) who did not show any neurological improvement within 24 h after eCAS so a follow-up MRI was performed. An intensive BP and intracranial pressure control were performed and the patient recovered except for mild proximal limb weakness and was discharged 26 days after eCAS (figure 3).

    Follow-up clinical results

    The mean duration of admission was 11.9 days (range 4–26 days) and seven of the 22 patients required additional rehabilitation. The mean NIHSS score at discharge was 3.55±4.11 (range 0–18). Thirteen patients showed an improvement of more than 10 points in the NIHSS score or had an NIHSS score of 0 or 1 at discharge (59.1%).

    Twenty patients were followed up regularly for more than 3 months. The mean follow-up period after eCAS was 13±11.2 months (range 3–35 months). The mean modified Rankin Scale (mRS) score at 3 months was 1±1.67 (range 0–6) and 20 patients (90.9%) had an mRS score of 0–2. One patient died from pneumonia approximately 1 month after eCAS and another patient with an mRS score of 5 also suffered recurrent pneumonia for 3 months after eCAS. No stroke related to eCAS developed during the follow-up period. Twelve patients (54.5%) underwent follow-up imaging more than once. Among them, only one showed moderate in-stent restenosis of approximately 50% on 6-month follow-up imaging.

    Discussion

    The majority of patients with occlusion and stenosis of the carotid artery are usually asymptomatic or experience mild symptoms.22 However, a small percentage of patients develop severe stroke and their prognosis is usually very poor. In 1986, Meyer et al2 reported their experience with emergency endarterectomy in patients with ICA occlusion and reviewed the prognostic history of these patients; approximately 40–69% of the patients were permanently disabled, 16–55% died due to stroke and only 2–12% had a good recovery.2 IV thrombolysis or IA thrombolysis using rtPA in these patients is usually ineffective. Pechlaner et al3 reported that approximately one-third of patients had extracranial ICA occlusion recanalized after IV thrombolysis within a median of 3.5 days after stroke, but the clinical outcome was not significantly better than patients who did not receive IV thrombolytic therapy. In addition, Ratanaprasatporn et al23 reported that, in patients with AIS with concomitant cervical carotid and intracranial occlusion, IA thrombolysis using rtPA after revascularization of the cervical ICA with CAS increased the rate of recanalization compared with patients given IA thrombolysis via the collateral circulation. In this situation, the proven technical feasibility and good clinical outcomes of eCAS reported in recent studies are promising.4–17 The total percentage of good clinical outcomes (mRS 0–2 at 1–6 months) was 55.7% (127 of 228 patients) in 14 previous studies, and the mortality rate was only 13.6% (31 patients).4–17 Nevertheless, some physicians still hesitate to perform eCAS.

    Technically, eCAS is not as difficult as expected, although we initially hesitated to perform this procedure. During the first year of this study period we performed only five eCAS procedures for patients with severe stroke due to carotid occlusion or tandem distal occlusion; however, in the last year we performed 13 eCAS procedures and gained further experience. The technical success rate in previous studies has ranged from 77.3% to 100%, although nearly all of the patients in those studies had an ICA occlusion.4–17 An important question for patients with AIS due to proximal ICA occlusion or stenosis is whether to open the occluded or stenotic ICA. The patients with AIS due to proximal ICA occlusion or stenosis in the present study showed diverse neurological deficits. If the patients had tandem occlusion on the distal ICA or MCA, the neurological deficits were severe. Conversely, if the patients had good collateral flows via the circle of Willis, they usually experienced minor symptoms. Kim et al2,4 reported that collateral MCA flow in AIS patients with ICA occlusion reduced initial stroke severity and was associated with favorable outcomes at 3 months. The angiographic collateral grade determines the recanalization rate after endovascular revascularization therapy.25 In addition, Hauck et al17 reported that patients with complete ICA occlusion, but partial distal preservation via the collateral circulation, had a higher recanalization rate and good clinical outcome compared with patients without collateral flow. In this study, however, if the patient showed an ACG grade of >3, we performed medical therapy using a volume expander and administered vasopressor agents to enhance the collateral flow.

    Another concern is distal embolization caused by manipulation of highly vulnerable plaque. In elective CAS the EPD is commonly used to prevent distal embolization. However, the use of EPD has been reported only in three recent studies in selected patients5 ,8 ,9 and only one patient suffered distal embolization.5 In our opinion, the prevalence of distal embolization has been significantly underestimated in these previous studies. During the procedure, distal embolization is difficult to detect. IA intervention in patients with AIS is a complex and time-sensitive procedure and the tandem occlusion of the distal artery could mask an additional embolic occlusion. We did not use an EPD in our first six cases but did in eight of the following 16 eCAS cases. We suggest the use of EPD in eCAS even if distal tandem occlusion coexists because the clot burden can be reduced and easier thrombolysis/thrombectomy to the distal occlusion can be performed.

    The use of dual antiplatelet agents is recommended before and after CAS to prevent acute or chronic in-stent thrombosis.26 However, the ideal medical regimen in eCAS is not established. In this study we did not prescribe any antiplatelet agent for patients who received rtPA therapy before eCAS. The patients who did not receive rtPA therapy were prescribed a loading dose of antiplatelet agents, 600 mg clopidogrel with 300 mg aspirin. A loading dose of 300–600 mg clopidogrel rapidly inhibits platelet aggregation but we preferred 600 mg based on the good clinical results obtained in a coronary stenting study.27 Acute or delayed thrombotic complications as well as hemorrhagic events were not observed in this study.

    CHS is a potentially fatal complication of CAS. The known risk factors of CHS are long-standing hypertension, diabetes mellitus, older age, high-grade stenosis with poor collateral circulation, reduced vasoreactivity and symptomatic lesions.28 The patients with AIS due to stenosis or occlusion of the proximal ICA usually had multiple risk factors, so the occurrence of CHS among patients with AIS who receive eCAS is possibly higher than reported. Many previous studies have not mentioned the prevalence of CHS. However, the development of intracerebral hemorrhage, the most fatal form of CHS, has been reported for 21 patients in 10 studies,5––9 ,11–14 ,16 and symptomatic hemorrhage developed in 10 patients5 ,6 ,12 ,13 ,16 and was mostly fatal. Thus, conducting intensive post-procedural care such as full monitoring, frequent neurological assessment and strict BP control is important for achieving good clinical outcomes.

    Information regarding long-term results such as restenosis of the inserted stent and stroke recurrence in patients receiving eCAS is lacking. The main focus of previous studies has been the procedure itself and short-term clinical results; information regarding follow-up vascular investigations has been reported in only four studies.4 ,5 ,9 ,10 Of the patients included in these studies, only one showed asymptomatic moderate stenosis of approximately 40%.5 In addition, stroke recurrence on the ipsilateral side of eCAS was reported in only two cases in a previous study (1 month and 2 months after eCAS).9

    Conclusion

    This study has several limitations, including retrospective data collection, absence of a control group and small number of patients. However, the results indicate that eCAS in patients with AIS due to proximal ICA stenosis or occlusion is a technically feasible and effective method for obtaining good clinical outcomes after stroke.

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    Footnotes

    • Contributors Study conception and design: DSC, BHL. Data collection: all authors. Data analysis and interpretation: SS, DSC, N-CC. Literature research: SS, O-YK. Drafting the manuscript: SS. Revision of the manuscript for important intellectual content: SS, DSC, MKO, K-JP. Approval of final version of manuscript: all authors.

    • Competing interests None.

    • Patient consent Informed consent was obtained from at least two legal representatives of each patient before the procedure.

    • Ethics approval This study was approved by the Gyeongsang National University Hospital Institutional Review Board.

    • 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 for the data.