Emergent carotid artery stenting in patients with acute ischemic stroke due to cervical internal carotid artery steno-occlusive lesion: Comparison of tandem intracranial occlusion and isolated cervical internal carotid artery occlusion

Abstract

Purpose

Acute ischemic strokes caused by steno-occlusive lesion of the cervical internal carotid artery are associated with poor clinical outcome. We evaluated the clinical efficacy of emergent carotid artery stenting for the management of these lesions. We compared the clinical outcomes regarding the intracranial lesion, namely tandem occlusions versus isolated cervical internal carotid artery occlusion.

Materials and methods

We retrospectively reviewed patients with acute ischemic stroke who underwent carotid artery stenting for cervical internal carotid artery steno-occlusive lesion between 2011 and 2018. After dividing the patients into two groups according to the presence or absence of intracranial lesions (tandem group and isolated cervical group), we analyzed demographic data, angiographic findings, and clinical outcomes. A modified Rankin Scale score ≤2 was defined as a favorable clinical outcome.

Results

Of 75 patients, 46 patients (61.3%) had tandem lesions, and the remaining 29 had only cervical internal carotid artery steno-occlusive lesion. Successful stenting was performed in all patients with favorable clinical outcomes (64.0%). Successful reperfusion score (thrombolysis in cerebral infarction ≥2 b) was 84.0%; tandem group (76.1%) versus isolated cervical group (96.6%) of cases. Mean modified Rankin Scale score at 90-days was 2.09. The rate of favorable clinical outcome showed no statistically significant difference between the two groups (p = 0.454).

Conclusions

Endovascular treatment in patients with acute ischemic stroke due to cervical internal carotid artery steno-occlusive lesion is a technically feasible and clinically effective intervention regardless of intracranial occlusion. Therefore, we recommend endovascular treatment regardless of the presence of concomitant intracranial artery occlusion for patients with acute ischemic stroke caused by cervical internal carotid artery steno-occlusive lesion.

Introduction

Early recanalization of occluded artery in patients with acute ischemic stroke (AIS) plays an important role in patients’ clinical outcomes and reduction of mortality.¹ Endovascular thrombectomy has been proven effective for intracranial vascular occlusions.^2,3 In presence of AIS due to intracranial arterial occlusion, 10–20% of the patients are known to also present with a lesion in the ipsilateral extracranial carotid artery.⁴ Most patients with isolated stenosis of the carotid artery are asymptomatic or only have mild symptoms.⁵ However, some patients develop severe ischemic stroke, most of which result in poor prognosis. Furthermore, recent studies reported that 50–65% of patients with acute cervical ICA occlusion also have a tandem lesion (proximal intracranial occlusion and cervical carotid artery occlusion or stenosis >90%), primarily in the distal ICA or middle cerebral artery segments.^6,7

Data on the outcome of endovascular therapy for tandem lesion were inadequate.⁸ In clinical practice, endovascular intervention for AIS caused by steno-occlusive lesion of the cervical ICA is a complicated procedure involving consideration of several factors. Cerebral hyperperfusion syndrome, distal embolism, and arterial dissection during carotid artery stenting (CAS) are a possibility, and because the state of the distal cervical ICA is unknown, blind navigation is inevitable. Furthermore, these risks are elevated in cases of tandem occlusion that involve intracranial arterial occlusion. Due to these risks and the relatively long procedure time, endovascular procedures for tandem occlusions are rarely performed compared to solitary cervical ICA occlusion in clinical settings such as our stroke center. However, a recent meta-analysis showed the benefit of endovascular treatment for tandem lesions with AIS, though heterogeneity of the treatment methods precludes the chance of defining a standardized treatment method.⁹

In this work, we analyzed the clinical outcomes of emergent CAS for AIS with severe stenosis or occlusion of the cervical ICA and the efficacy of endovascular intervention in relation to the presence of an accompanying intracranial arterial occlusion. Individual clinical outcomes for endovascular treatment for tandem lesion and isolated cervical ICA occlusion with AIS have been published in several studies, and there is no direct comparison between the two groups.

Materials and method

Patient group

We retrospectively reviewed the medical records of 267 patients who underwent CAS between January 2011 and November 2018 at our stroke center (Figure 1). Of those 185 patients who underwent scheduled stenting, who arrived more than 8 h after the onset of AIS (or arrived at an unknown time), or who arrived more than 12 h after the last normal time were excluded. A total of 82 patients arrived at the emergency department within 12 h of stroke onset, underwent magnetic resonance imaging (MRI), and received emergent CAS. After retrospectively reviewing patients’ medical records, intervention images, procedure results, and preoperative and postoperative MRI and computed tomography (CT) scans, we additionally excluded seven patients, because the cause of AIS seemed to be due to carotid artery dissection (n = 6) or cardiogenic embolism (n = 1). This decision was made based on the hypothesis that it would be difficult to ensure homogeneity of patients because the brain shows some degree of adaptation to ischemic lesions in patients with ICA stenosis with atherosclerosis but patients with aortic dissection or embolism exhibit a rapid decline of the brain blood flow without such adaptation.

Figure 1.

Flow diagram showing screening and selection of patients. pts: patients; hrs: hours; ICA: internal carotid artery; pICA: proximal internal carotid artery.

Hence, 75 patients were included in this study. The patients were divided into tandem occlusion (n = 46) and isolated cervical occlusion (n = 29) groups. The sites of intracranial arterial occlusions in the tandem group included the anterior cerebral artery (ACA), middle cerebral artery (MCA, M1 or M2 segment), and distal ICA. The Institutional Review Board waived the requirement to obtain informed consents owing to the study’s retrospective nature.

Diagnostic tools

All patients underwent MRI under the protocol for AIS, and the 3-T (Ingenia; Philips, Eindhoven, Netherlands) or 1.5-T (Avanto; Siemens, Erlangen, Germany) MR scanners were used. The MRI protocol consisted of the diffusion-weighted images (DWI) with b-values of 0 and 2000, gradient echo images (GRE), fluid-attenuated inversion recovery (FLAIR) images, gadolinium-enhanced T1 weighted images, gadolinium-enhanced MR angiography of the major cervical and intracranial arteries, and perfusion-weighted MR images (PWI). The patient’s eligibility for endovascular therapy was based on the following criteria: modified Rankin Scale (mRS) 0–2 before AIS, initial National Institutes of Health Stroke Scale (NIHSS) score of ≥4, DWI-Alberta Stroke Program Early Computed Tomography Scores (ASPECTS) ≥4 and/or PWI/DWI mismatch that was greater than one-third on visual assessment. Further, the following were the imaging criteria for exclusion from endovascular treatment: visible infarctions in more than one-third of the middle cerebral artery territory on DWI, no relevant mismatch on PWI, and evidence of hemorrhage on CT or MRI.

Endovascular treatment

In total, 52 patients out of 75 (69.3%) underwent intravenous thrombolysis using recombinant tissue plasminogen activator (rt-PA, Alteplase; Boehringer Ingelheim, Basel, Switzerland) prior to the interventional procedure. Patients presenting within 4.5 h of symptom onset and without contraindications were immediately given 0.9 mg/kg of rt-PA intravenously. If immediate neurologic improvement was not observed, patients were then transferred to the intervention suite. On the other hand, patients presenting after 4.5 h of symptom onset were immediately transferred to the intervention suite without systemic thrombolytic therapy.

Biplane angiography (Artis Zee Biplane; Siemens, Erlangen, Germany or Allura Xper; Philips Healthcare, Best, The Netherlands) was used for the intervention and after establishing local anesthesia in the inguinal region, a femoral sheath was inserted into the common femoral artery. Angiography was performed for bilateral carotid arteries and vertebral artery to confirm collateral flow from anterior and posterior communicating arteries prior to CAS. A 6 Fr Shuttle was placed in the ipsilateral common carotid artery and a 0.014-inch microwire was passed through the cervical ICA stenosis or occlusion. Then, a microwire and microcatheter were used to navigate to the distal ICA and selective angiography was performed to confirm intracranial tandem occlusion. A self-expandable stent was inserted into the lesion site after dilatation of the stenosed or occluded cervical ICA using a 4 - or 5-mm balloon (Aviator plus PTA balloon; Cordis, Miami Lakes, Florida, USA or Ultra-soft SV balloon; Boston Scientific, Maple Grove, Minnesota, USA). The type of stent was selected based on the ICA course. A closed-cell stent (Carotid WallStent; Boston Scientific, Marlborough, Massachusetts, USA) was used for relatively straight cervical ICA course, and an open-cell stent (RX Acculink carotid stent; Abbott Vascular, Santa Clara, California, USA) was used for curved courses. When the stent did not fully expand, additional dilatation was performed using a 5 - or 6-mm balloon.

For patients with intracranial tandem occlusion, thrombectomy was performed by placing a stent in the proximal carotid artery and a microcatheter into the distal area of the thrombus in the occluded site. Mechanical thrombectomy was performed using a stent-retriever device (Solitaire; Covidien, Irvine California, USA or Eric; MicroVention, Tustin, California, USA) or penumbra system (PS; Penumbra; Alameda, California, USA) (Figure 2). Thrombectomy was performed by pulling back the device and microcatheter concurrently under continuous aspiration through the intermediate catheter (6 Fr Neuron catheter; Penumbra; Alameda, California, USA; or 5 Fr Sofia catheter; MicroVention, Tustin, California, USA). Thrombectomy was repeated in case of incomplete recanalization.

Figure 2.

Case example of 72-year-old man with acute onset of left hemispheric syndrome (NIHSS score 19). (a) Pre-procedural extracranial lateral projection angiography. Note the severe stenosis of the right cervical ICA (arrow). (b) Pre-procedural intracranial anterior to posterior projection of right internal carotid angiography. Note the tandem occlusion of the proximal portion on the right MCA M1 segment (arrow). (c) Subtracted image acquired immediately after stent deployment shows recanalization of right cervical ICA. (d) After intracranial thrombectomy, the vessel is fully recanalized to a TICI 2b state. NIHSS: National Institutes of Health Stroke Scale; ICA: internal carotid artery; MCA: middle cerebral artery; TICI: thrombolysis in cerebral infarction.

Clopidogrel and aspirin dosage was determined based on whether rt-PA was used prior to the emergent CAS. If a patient received IV rt-PA prior to the procedure, atorvastatin (80 mg) was administered, and a maintenance dose of clopidogrel (75 mg), aspirin (100 mg), and atorvastatin (80 mg/day) was started 24 h later. However, for patients who did not receive rt-PA, a loading dose of clopidogrel (300 or 600 mg), aspirin (300 mg), and atorvastatin (80 mg) was administered, followed by a maintenance dose of clopidogrel (75 mg) with aspirin (100 mg) and atorvastatin (80 mg/day). The initial loading dose of clopidogrel was set to 300 or 600 mg by the clinician.

Patients who underwent emergent CAS were transferred to the ICU and placed on blood pressure, oxygen saturation, and ECG monitoring for 48 h. They also underwent neurologic testing every hour. Patients’ systolic BP was strictly maintained at 110–120 mmHg to prevent potential cerebral hyperperfusion syndrome within 24 h of the endovascular procedure.

Clinical and radiologic assessment and follow-up

The technical success of emergent CAS was assessed based on the postprocedural thrombolysis in cerebral infarction (TICI) score after recanalization of the ICA was established. A TICI score of 2 b or higher was defined as successful recanalization.¹⁰ To detect potential intracranial hemorrhage or cerebral edema, CT was performed on all patients within 24 h of the procedure. MRI was performed three to five days after the procedure to identify the extent of cerebral infarction. Secondary bleeding complications were recorded using the European Cooperative Acute Stroke Study (ECASS) III classification (HI-1/HI-2/PH-1/PH-2).¹¹ All CT, MRI, and angiography images were evaluated in consensus by two interventional radiologists.

NIHSS scores 48 h after the procedure and at discharge and mRS scores 90 days later were assessed by neurologists at the stroke center. Cases where the NIHSS score decreased from the baseline by 4 points or higher or where post-procedural NIHSS score was between 0 and 2 were defined as early neurological improvement.¹² Furthermore, mRS score of between 0 and 2 90 days after was defined as favorable clinical outcome.¹³

Patients who underwent endovascular treatment were prescribed aspirin (100 mg/day), clopidogrel (75 mg/day), and atorvastatin (40–80 mg/day) upon discharge and were instructed to maintain the regimen until at least 90 days after the procedure. Patients underwent neurologic testing on the day of discharge and at every follow-up. Follow-up MRI and neurologic examination were recommended at 6 and 12 months after procedure and once every year thereafter.

Statistical analysis

Study data were tested for normal distribution using Kolmogorov–Smirnov test. Normally distributed variables were compared using independent t-test and were presented as mean ± standard deviation. Categorical variables were compared using the Chi-squared test or Fisher’s exact test for small cell values. Then, multivariate logistic regression was performed for statistically significant (p < 0.05) variables. All statistical analyses were performed using SPSS (IBM SPSS Statistics for Windows, Version 24.0. Armonk, NY: IBM Corp).

Results

Tables 1 and 2 show the characteristics of the patient group and results of endovascular treatment.

Table 1.

Clinicoradiological characteristics of patient population.

Age, years	73.6 ± 9.1 (46–89)
Female	16/75 (21.3)
Initial NIHSS	12.7 ± 5.8 (4–24)
Symptom to arrival, min	195.9 ± 158.9 (30–600)
Arrival to groin puncture, min	94.1 ± 50.1 (19–320)
Cervical ICA stenosis, %	97.2 ± 5.7 (80–100)
Intracranial occlusion, %	46/75 (61.3)
ICA-T	8/46 (17.4)
MCA-M1	24/46 (52.2)
MCA-M2	13/46 (28.3)
ACA	1/46 (2.2)

Note: Values are shown as mean ± SD (range), n/N (%).

NIHSS: National Institutes of Health Stroke Scale; ICA: internal carotid artery; MCA: middle cerebral artery; ACA: anterior cerebral artery.

Table 2.

Clinicoradiological outcomes after endovascular treatment according to lesion type of the intracranial arterial occlusion.

	Isolated cervical occlusion (n = 29)	Tandem occlusion (n = 46)	p value
TICI 2 b-3 (n (%))	28 (96.6)	35 (76.1)	0.019*
TICI 3 (n (%))	26 (89.7)	19 (41.3)	0.001*
Procedure time (min)	52.5 ± 15.12	84.4 ± 24.34	0.001*
Mean mRS at 90-days	1.78 ± 1.91	2.37 ± 2.13	0.234
mRS ≤2 (n (%))	20 (68.9)	29 (63.0)	0.476
Mortality at 90-days (n (%))	1 (3.4)	5 (10.9)	0.373
Initial NIHSS	11.8 ± 5.67	13.3 ± 6.36	0.201
Mean NIHSS after 24 to 48 h	3.8 ± 3.73	7.1 ± 7.31	0.018*
Early neurological improvement (n (%))	24 (82.8)	32 (69.6)	0.193
Symptomatic ICH (n (%))	2 (6.9)	7 (15.2)	0.244

Note: Values are shown as mean ± SD (range).

^*p < 0.05.

TICI: thrombolysis in cerebral infarction; mRS: modified Rankin Scale; NIHSS: National Institutes of Health Stroke Scale; ICH: intracerebral hemorrhage.

Patient group and results of interventional treatment

The mean NIHSS score in the early neurologic testing was 12.7 ± 5.8 (range 4–24), and all patients had a NIHSS score of 4 or higher upon admission. The mean preoperative DWI-ASPECTS score was 6.2 ± 1.4 in the tandem occlusion group and 5.7 ± 1.5 in the isolated cervical occlusion group. There were no significant differences in the mean DWI-ASPECTS between the two groups (p = 0.276). In the initial diagnostic cerebral angiography, 41 out of 75 patients (54.7%) showed complete occlusion of the cervical ICA, and 34 (45.3%) showed severe stenosis (80–99%). CAS for the cervical ICA was successful for all 75 patients regardless of the type of stent used: Carotid WallStent (49/75 = 65.3%), RX Acculink carotid stent (26/75 = 34.7%). Mechanical thrombectomy was performed for additional intracranial arterial occlusion in 40 out of 46 patients with tandem occlusion (86.9%); penumbra system was used on 23 patients and stent-retriever device (Solitaire: 12, Eric: 5) was used on 17 patients. Six patients in the tandem occlusion group (13.0%) did not receive thrombectomy, one patient due to the position of the thrombus in the distal M2 segment and five due to spontaneous intracranial recanalization (Figure 3). Distal protection device (Emboshield; Abbott Vascular, Redwood City, California, USA or Spider FX; EV3, Plymouth, Minnesota, USA) was used for all patients in the isolated cervical ICA occlusion group and for 16 patients (16/46, 34.8%) in the tandem occlusion group who had a high risk for distal embolism due to large thrombus in the cervical ICA. Successful recanalization (TICI ≥2 b) was achieved in 63 patients (84.0%), and 45 patients (60.0%) had a TICI score of 3. Successful recanalization rate was higher in the isolated cervical ICA occlusion group (28/29, 96.6%) than in the tandem occlusion group (35/46, 76.1%) (p = 0.019).

Figure 3.

Case example of 69-year-old man with tandem occlusion (NIHSS score 19). (a and b): Initial MR images demonstrate wide spread mismatch between extent of lesion of diffusion-weighted image and perfusion-weighted image with mean transit time in the left MCA territory. (c) Diagnostic angiography shows total occlusion of left cervical ICA (arrow). (d) After passing the cervical ICA occlusion using a 0.014-inch microwire, anterior to posterior projection of left internal carotid angiography shows tandem occlusion of the left MCA M1 segment (arrow). (e) After stent placement and balloon angioplasty, anterior to posterior projection angiography shows complete restoration of left cervical ICA. (f) Post-procedural intracranial anterior to posterior projection angiography. The spontaneous recanalization of the left MCA is observed (arrow). NIHSS: National Institutes of Health Stroke Scale; MCA: middle cerebral artery; ICA: internal carotid artery.

Twenty-one patients showed temporary hemodynamic changes, such as hypotension and bradycardia, during or immediately after balloon dilatation of the cervical ICA, but the symptoms were reversed after termination of balloon dilatation. Six patients developed procedure-related complications. One patient developed right hemiplegia and dysarthria during balloon dilatation, both of which were reversed without sequelae once angioplasty was terminated. Two patients had arterial dissection during angioplasty of the cervical ICA; stenting was performed, and recanalization was achieved without residual dissection. Three patients (4%) developed cerebral hyperperfusion syndrome, one of whom did not show neurologic recovery until 24 h after the procedure. A follow-up MRI was performed on the patient and blood pressure and brain pressure were intensively managed. The patient fully recovered, apart from experiencing proximal limb weakness and was discharged 26 days after admission.

Clinical outcomes

Six of these patients (8%) expired; one died from pneumonia, and five died from acute cerebral hemorrhage even after decompressive craniectomy. The mean mRS score after three months was 2.09 ± 1.91 (range, 0–6), and 48 (64%) patients showed favorable clinical outcome (mRS ≤2). The mean mRS score after three months did not significantly differ between the isolated cervical ICA occlusion group (1.78 ± 1.91) and tandem occlusion group (2.37 ± 2.13) (p = 0.522). During the follow-up after discharge, 50 patients (66.7%) underwent at least one follow-up imaging test. Only one of these patients showed a moderate in-stent restenosis at the six-month follow-up. None of the surviving patients showed neurologic aggravation or ischemic symptoms during the follow-up period.

Fifty-two (69.3%) patients received IV rt-PA as thrombolytic therapy prior to the endovascular treatment. The remaining 23 patients arrived after 4.5 h of symptom onset and were prescribed the initial loading dose of clopidogrel as per the protocol. Eleven of these 23 patients were prescribed 600 mg of clopidogrel, while 12 patients were prescribed 300 mg. Thirty-five (35/52, 67.3%) patients who received IV rt-PA prior to procedure showed favorable clinical outcomes. Fifteen out of 23 patients (65.2%) who did not receive IV rt-PA showed favorable clinical outcomes. There were no significant differences in the favorable clinical outcome rate between the two groups (p = 0.598). Table 3 shows a summary of the predictors of favorable clinical outcome.

Table 3.

Multivariate predictors of favorable clinical outcome.

Variable	OR (95% CI)	p value
Age	0.93 (0.83–1.19)	NS
Gender, Male	1.07 (0.14–7.39)	NS
Initial NIHSS	0.79 (0.64–1.81)	NS
TICI 3 (n (%))	8.43 (1.04–78.9)	0.044
Early neurological improvement	10.67 (1.46–65.4)	0.024

NS: not significant; NIHSS: National Institutes of Health Stroke Scale; TICI: thrombolysis in cerebral infarction.

Discussion

In our study, intracranial tandem occlusion was discovered following cerebral angiography performed immediately after establishing recanalization of the cervical ICA in 61.3% of patients. The duration of procedure was significantly shorter for the isolated cervical ICA occlusion group than for the tandem occlusion group, presumably because the former group did not require endovascular treatment of additional intracranial arterial occlusion. Previous studies reported that the favorable clinical outcome rate is lower among the tandem occlusion group than that in the isolated cervical ICA occlusion group because the golden time for cerebral reperfusion is likely to be missed in the former group due to the longer duration of procedure.^6,14 However, those studies involved a small sample size (≤20) and the findings were not statistically significant. In contrast, we found that both groups showed high technical success rate and favorable clinical outcome rates regardless of the presence of a tandem intracranial occlusion. This could be related to a previous finding that tandem intracranial occlusion is a good indicator of thrombectomy because such cases involve normal intracranial vessels and are mostly caused by distal embolism.¹⁵ In addition, the presence of a tandem intracranial occlusion may not have a grave impact on clinical outcomes, as the time it takes to remove the thrombus in the intracranial artery is minimal compared to the time for taking an MRI, inserting a sheath in the femoral artery, and placing a catheter in the ICA. Successful recanalization rate was significantly higher in the isolated cervical ICA occlusion group. However, there were no significant differences in the favorable clinical outcome rate, symptomatic intracerebral bleeding, and mortality rate between the two groups. Comparisons of clinical outcomes between the tandem occlusion group and the isolated cervical ICA occlusion group in our study showed that cervical ICA occlusion played a major role in the development of AIS in these patients and that the occurrence of tandem intracranial occlusions was incidental. Previous studies have shown that successful recanalization rate may not be a predictor of favorable clinical outcome in acute cervical ICA occlusion, though this finding remains controversial.^16,17 The lack of marked differences in clinical outcomes between the two groups may be understood from the findings of Kim et al.¹⁸ that development of intracranial collateral flow, as opposed to the presence of intracranial arterial occlusion, affects the severity of stroke and favorable clinical outcome after 90 days. Hauck et al.¹⁹ also found that patients with collateral flow show a higher rate of favorable clinical outcome than those without collateral flow even in the presence of complete ICA occlusion. Hence, although direct comparison with previous findings is limited, the present study considered endovascular treatment to be an effective treatment for acute cervical ICA occlusion with AIS regardless of a tandem intracranial occlusion.

Some patients with tandem lesions achieve spontaneous intracranial recanalization after recanalization of the cervical ICA.^7,20 In our study, five patients (5/46, 10.9%) with tandem lesions achieved spontaneous intracranial recanalization after balloon dilatation that was performed prior to stenting of the cervical ICA, so additional intracranial thrombectomy was not required (Figure 3).

Cerebral hyperperfusion syndrome is a rare but fatal complication of CAS. Its known risk factors include prolonged hypertension, diabetes, old age, severe carotid artery stenosis without well-developed collateral flow, reduced vascular elasticity, and symptomatic carotid artery stenosis.²¹ Patients with AIS caused by a cervical ICA steno-occlusive lesion often have a number of these risk factors, so the actual incidence is higher than the reported number. Many studies on AIS caused by carotid artery occlusion did not mention the incidence of hyperperfusion syndrome after emergent CAS. However, considering that the incidence of hyperperfusion syndrome after general CAS is about 3–7%, the incidence of hyperperfusion syndrome after emergent CAS is predicted to be similar or slightly higher. Therefore, intensive observation measures, such as close monitoring, frequent neurologic assessment, and strict blood pressure management are crucial for lowering the above-mentioned complications and achieving favorable clinical outcomes. Moreover, PWI/DWI mismatch, which represents ischemic penumbra, is useful for deciding whether an interventional procedure for recanalization would be beneficial for the patient involved.

The use of dual antiplatelet agents is generally recommended before and after CAS in order to prevent acute or chronic in-stent thrombosis.²² A recently published study showed that emergent CAS with antithrombotic agents in conjunction to thrombectomy appears to be the best treatment strategy for AIS with tandem occlusion.²³ In our study, patients who received rt-PA therapy prior to the intervention were not prescribed antiplatelet agents. On the contrary, patients who did not receive rt-PA therapy prior to intervention were prescribed double antiplatelet regimen with 300 or 600 mg initial loading dose of clopidogrel and 300 mg of aspirin. However, there were no significant differences in the favorable clinical outcome rate between patients who received rt-PA and those who did not. This is presumably because our sample size was relatively small, and our patient groups were slightly heterogeneous.

This study has a few limitations. First, there was an unavoidable selection bias due to the retrospective nature of the study. Second, MRI scans were taken for all patients prior to the procedure to confirm their lesions. This means that patients without MRI scanning to confirm the lesions were excluded, which may also have contributed to the selection bias. Third, our sample size for each of the two groups was relatively small for an accurate statistical comparison. Fourth, there was a limitation in standardizing the treatment modality used in this study due to the advances of techniques and devices for the interventional procedure over several years. Finally, the antiplatelet dosage differed according to the prescribing clinician. This may have influenced the clinical outcomes, including the onset of symptomatic intracerebral hemorrhage.

Conclusion

Interventional treatment for AIS caused by cervical ICA steno-occlusive lesion has reasonable efficacy, stability, and technical validity, and produced favorable clinical outcomes regardless of the presence of a tandem occlusion in the intracranial artery. Therefore, we recommend endovascular treatment for patients with AIS caused by cervical ICA steno-occlusive lesions regardless of the occurrence of concomitant tandem intracranial occlusions.

Authors’ contributions

Conceptualization: Sung Eun Park, Dae Seob Choi, Hye Jin Baek. Data curation: Sung Eun Park, Kyeong Hwa Ryu, Seunguk Jung. Formal analysis: Ji Young Ha, Ho Cheol Choi, Sangmin Lee, Jungho Won. Investigation: Sung Eun Park, Ho Cheol Choi, Jungho Won Writing – original draft: Sung Eun Park, Dae Seob Choi Writing – review and editing: Sung Eun Park, Hye Jin Baek.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Ethical approval

The institutional review board approved this study (IRB file No. 2018-03-008-003).

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Sung E Park https://orcid.org/0000-0002-2832-8900

Hye J Baek https://orcid.org/0000-0001-7349-2841

Seunguk Jung https://orcid.org/0000-0003-2331-024X