First experience with endovascular recanalization of chronic internal carotid artery occlusion

• Andrey E. Petrov
• Nikita Yu. Tukanov
• Vasiliy V. Bobinov
• Sergey A. Goroshchenko
• Arkady A. Ivanov
• Egor G. Kolomin
• Konstantin A. Samochernykh
• Larisa V. Rozhchenko

Abstract

Background. According to WHO, the number of people suffering from atherosclerotic lesions of the brachiocephalic arteries in different age groups is 20–50%. The development of ischemic stroke with existing chronic occlusion of the internal carotid artery (ICA) occurs with a frequency of 6–15%, and the annual risk of developing acute ischemic disorders in the ipsilateral basin, despite adequate drug treatment, ranges from 6 to 20%.

The aim is to evaluate the efficacy and safety of endovascular recanalization in chronic ICA occlusion.

Material and methods. The analysis of the first results of intravascular treatment of 12 patients with chronic ICA occlusion on the basis of the vascular neurosurgical department of the Russian Research Neurosurgical Institute named after Professor A.L. Polenov. The age range is from 42 to 75 years (the average age is 57 years). There were 11 men (91.6%) and 1 woman (8.4%).

Depending on the type of chronic occlusion, according to the D. Hasan scale (2018), the distribution of patients was as follows: type A (the presence of a proximal ICA stump of the “candle” type + retrograde filling of the ICA to the stony/cavernous segments) – 4 patients; type B (the presence of a blindly ending proximal ICA stump without the formation of a “candle” + retrograde filling of the ICA to the rocky/cavernous segments) – 3 patients; type C (occlusion of the ICA from the mouth + retrograde filling of the ICA to the rocky/cavernous segments) – 2 patients; type D (occlusion of the ICA from the mouth with the absence of retrograde filling of the stony/cavernous segments of the ICA) – 3 patients.

Results. In 8 (66.6%) of the 12 patients, the ICA lumen was completely restored. According to the D. Hasan scale, type A was noted in 4 patients, type B in 3 patients, and type C in 1 patient. In 4 (33.3%) patients, technical success was not achieved, of which according to the D. Hasan scale: type D was observed in 3 patients, type C in 1 patient. Of the 8 patients with successful ICA recanalization, all underwent remote monitoring by computed tomographic angiography or digital subtraction angiography. No data confirming restenosis were obtained in 6 patients. There were no episodes of recurrent ischemic disorders. In 1 patient, thrombosis of stented ICA was detected against the background of the patient’s self-withdrawal of double disaggregant therapy. Unsuccessful recanalization (4 patients), in our opinion, is associated with convolution of the ICA and severe scarring in the lumen of the occluded artery.

Conclusion. Intravascular recanalization of chronic ICA occlusion is a promising method that can be effectively used to restore the full-fledged lost artery lumen and normalize brain perfusion to reduce the risks of recurrent ischemic cerebral events.

Keywords:  chronic occlusion of the internal carotid artery; recanalization of the internal carotid artery; stenting of the internal carotid artery; cerebral perfusion; ischemic cerebral events; ischemic stroke

Introduction

Chronic internal carotid artery (ICA) occlusion is a high-risk factor for the development of ischemic stroke (IS). According to the literature, chronic ICA occlusion is detected in 6–15% of patients with IS, and the annual risk of ischemic events in the ipsilateral vascular territory, despite adequate medical therapy, ranges from 6% to 20% [1]. Clear temporal criteria for chronic ICA occlusion have not yet been established. The vast majority of authors define chronic ICA occlusion as a process of complete arterial obliteration lasting 4 weeks or more [2]. According to current Russian clinical guidelines, optimal medical therapy is recommended as the primary treatment method for chronic ICA occlusions. Traditionally, the surgical treatment of chronic ICA occlusion involved the creation of an extracranial-intracranial microvascular anastomosis (EC-IC bypass); however, to date, there is no clear evidence base for the effectiveness of this method. The technique of endovascular recanalization for chronic ICA occlusion, proposed in 2005, allows for the restoration of the lost arterial lumen, thereby eliminating the risk of ischemic events associated with ICA occlusion [3].

The aim of the study is to evaluate the efficacy and safety of endovascular recanalization for chronic ICA occlusion.

Material and methods

The results of treatment for 12 patients with chronic ICA occlusion treated in the Vascular Department of the A.L. Polenov Russian Research Institute of Neurosurgery – a branch of the V.A. Almazov National Medical Research Center of the Ministry of Health of Russia, were analyzed. Occlusions were considered chronic if their duration was 4 weeks or more. The cause of occlusion was atherosclerotic lesion in 10 patients, ICA dissection due to trauma in 1 patient, and in 1 patient, ICA occlusion developed following neck irradiation after removal of a laryngeal neoplasm. The mean patient age was 57 years (range 42 to 75 years). There were 11 men (91.6%) and 1 woman (8.4%).

Inclusion criteria: ICA occlusion in the presence of symptoms of chronic cerebral ischemia; a history of a previous episode/episodes of IS or transient ischemic attack; presence of a perfusion deficit according to cerebral computed tomography (CT) perfusion.

Exclusion criteria: Pregnancy, childhood, contraindications to long-term antiplatelet therapy.

Neurological deficit was absent in 5 patients; 5 patients had contralateral hemiparesis of varying severity; 2 patients had transient visual disturbances on the side of the occluded ICA.

All chronic ICA occlusions, based on examination results, were classified according to the D. Hasan scale (2018): Type A – 4 patients, Type B – 3 patients, Type C – 2 patients, Type D – 3 patients (Table 1, 2).

All patients underwent a neurological examination, multispiral computed tomographic angiography of the brachiocephalic arteries and brain, CT perfusion of the brain, and cerebral angiography, as well as magnetic resonance imaging (MRI) of the brain prior to surgery. A reduction in perfusion parameters was one of the main criteria for selecting patients for the operation.

All patients underwent recanalization of the chronic ICA occlusion using a technique involving stepwise bougienage of the occluded ICA segment with a guidewire followed by ICA stenting with balloon angioplasty, aimed at recreating its natural lumen and restoring normal blood flow.

Prior to surgery, all patients were prescribed dual antiplatelet therapy, and their response to it was monitored (aggregometry with assessment of adenosine diphosphate-induced platelet aggregation). All interventions were performed using a Philips Azurion 7 biplane angiograph (Philips, Amsterdam, The Netherlands).

Surgical Technique. Under general anesthesia, the femoral artery was punctured, and a 9F introducer sheath was placed. Cerebral angiography and angiography of the precerebral arteries were performed. The type of ICA occlusion was determined according to D. Hasan [4]. An angiographic exchange wire was advanced into the external carotid artery (ECA) on the side of the ICA occlusion. The catheter was withdrawn, and a Mo.Ma proximal protection system (Medtronic, USA) was deployed. After inflating the balloons in the ECA and common carotid artery, attempts were made to cross the occlusion zone using an angiographic guidewire and/or a rigid coronary microguidewire such as Whisper, BMW, or HighTorque (Abbott, USA); predilation with a balloon was not performed. Upon successful crossing of the occlusion zone, stents were advanced over the microguidewire and implanted, both intracranially (e.g., Synergy by Boston Scientific, USA; Papyrus by Biotronic, Germany) and extracranially (e.g., Casper by Microvention, USA), followed by dilation with a balloon (e.g., Sterling by Boston Scientific, USA or Submarine Rapid by Medtronic, USA) from the more proximal to the distal arterial segment. The achieved result was verified by angiography.

Prior to discharge from the hospital, a follow-up MRI of the brain, CT perfusion of the brain, and an assessment of the patient’s neurological status were conducted. The observation period ranged from 6 months to 2 years. At 6 months, all patients underwent an MRI of the brain with CT perfusion, CT angiography or digital subtraction angiography of the cerebral and precerebral arteries, and a follow-up neurological examination.

Results

Successful restoration of the ICA lumen was achieved in 8 out of 12 patients (66.7%), while it was unsuccessful in 4 patients (33.3%). Among the successful recanalizations, 4 patients had type A occlusion, 3 had type B, and 1 had type C. All 8 patients who underwent successful recanalization received long-term follow-up imaging via CT angiography or digital subtraction angiography. Of these, 7 patients showed no evidence of restenosis and experienced no episodes of recurrent ischemic events. However, 1 patient developed re-thrombosis of the operated ICA due to the patient’s self-discontinuation of dual antiplatelet therapy (this patient subsequently underwent EC-IC bypass surgery, and no ischemic events were reported within the following year). Regarding the unsuccessful recanalizations in 4 patients, we believe these failures were associated with ICA tortuosity and severe cicatricial changes within the artery. Of these, one patient was classified as Hasan type C, while three were type D.

All patients underwent cerebral CT perfusion both before and after the operation. In 7 out of 8 patients following successful ICA recanalization, restoration of perfusion parameters to normal levels was observed. In 3 out of 5 patients who underwent the intervention, regression of hemiparesis was noted. Patients continued to receive dual antiplatelet therapy for 6 months after the surgery. Follow-up examination was conducted 6 months after discharge from the hospital.

In our view, the predictors of technical success are variants of ICA occlusion with a preserved proximal stump and retrograde distal filling of the ICA up to the ophthalmic segment, which corresponds to types A and B according to D. Hasan.

Clinical Case Report

Patient T., 52 years old, 12 months prior to admission to the neurosurgical hospital, underwent removal of a malignant laryngeal neoplasm followed by a course of radiation therapy. Eight months after the surgery for the neoplasm, he began experiencing transient amblyopia in the right eye. The patient was followed by an ophthalmologist and a neurologist on an outpatient basis. As part of the examination, duplex scanning of the brachiocephalic arteries (BCA) was performed, which diagnosed an occlusion of the right internal carotid artery (ICA). Prior to the surgery, the patient underwent cerebral CT perfusion (Fig. 1), which revealed a significant reduction in perfusion parameters in the right hemisphere, consistent with oligemia.

Preoperative angiography showed occlusion of the right ICA with filling of the proximal stump in a “candle” pattern and retrograde filling of the ophthalmic and cavernous segment of the right ICA (Fig. 2).

According to the proposed technique, a step-by-step intravascular recanalization of the right ICA was performed with complete restoration of its lumen (Fig. 3).

In the postoperative period, CT perfusion of the brain was performed; perfusion parameters were restored to normal (Fig. 4).

The follow-up MRI of the brain revealed no data confirming recent ischemic lesions. Clinically, a complete regression of the visual disturbances was observed.

Discussion

Since clear temporal criteria for chronic ICA occlusion have not yet been defined, the time of ICA occlusion formation can only be presumed based on clinical and diagnostic data. However, it is important to consider that an ischemic event may occur even after the occlusion has formed, and imaging findings can only indirectly indicate the course of the chronic process.

There are 4 types of clinical progression in chronic ICA occlusion:

1) Adequate blood flow compensation through collaterals, with few symptoms or an asymptomatic course; the risk of ischemic events ranges from 2% to 8% per year.

2) Impaired cerebrovascular reserve, leading to the development of hypoperfusion ischemic foci; the risk of ischemic events is up to 30% per year.

3) Adequate blood flow compensation through collaterals, but emboli form and migrate from the proximal and distal ICA stump, presenting a high risk of recurrent ischemic events.

4) Spontaneous recanalization of the occluded ICA is observed in 10% of patients, but there is a risk of embolus formation and migration [5–8].

Surgical procedures performed for chronic ICA occlusion include carotid endarterectomy (CEA), extracranial-intracranial microvascular anastomosis (EC-IC bypass), and endovascular recanalization.

Carotid Endarterectomy

Carotid endarterectomy as an independent method for treating chronic ICA occlusion can only be used in one specific situation: when a localized occlusion zone is identified at the level of the cervical segment of the ICA. In cases of extensive ICA occlusions, the use of carotid endarterectomy is not advisable. In recent years, a significant number of publications have emerged concerning hybrid surgery for both acute and chronic ICA occlusions, where the first stage involves endarterectomy of the ICA origin, followed by recanalization of the ICA [9–14].

Extraintracranial anastomosis

The formation of an extraintracranial bypass (EC-ICMA) is most often understood as the creation of a low-flow (blood flow rate no greater than 25 ml/min) microvascular anastomosis between the branches of the superficial temporal artery and the cortical branches of the middle cerebral artery [15]. Following the first description of this method in 1969 [16], a number of studies followed to evaluate the effectiveness of EC-ICMA compared with drug therapy [17–19]. Due to the inconclusive results of large multicenter studies, controversy continues regarding the indications for EC-ICMA. However, the relevance of this technique remains, and research is underway to clarify the role of EC-ICMA in cerebral revascularization. Current Russian clinical guidelines for the treatment of steno-occlusive lesions of the BCA limit the indications for EC-ICMA to a very limited extent.

Endovascular Recanalization

Endovascular recanalization is the most recent method among surgical treatments for chronic ICA occlusion. The first description of endovascular recanalization was published by T. Terrada (2005), who proposed a method for stenting the occluded ICA using the MoMa proximal protection system [3].

In 2018, D. Hasan et al., based on the examination and treatment of 100 patients, described four radiological types of chronic ICA occlusion: Type A – local occlusion of the cervical ICA segment with a preserved proximal stump of the “candle flame” type and retrograde filling of the ICA above the cervical segment; Type B – local occlusion of the cervical ICA segment without a preserved “candle flame” proximal stump (ending in a blunt stump) but with retrograde filling of the ICA above the cervical segment; Type C – occlusion of the cervical ICA segment without a preserved proximal stump (the common carotid artery continues into the ECA) but with retrograde filling of the ICA above the cervical segment; Type D – Type C but without retrograde filling of the petrous and cavernous segments. According to these authors, successful recanalization is most frequently achievable in Types A and B (16/16 patients, 100%). In contrast, occlusion Types C and D were associated with lower technical success rates (50% or 4/8 patients and 25% or 2/8 patients, respectively) [4].

According to a study by F. Cagnazzo et al. (2020), which analyzed treatment outcomes in 528 patients with chronic ICA occlusion, successful recanalization of symptomatic lesions reduced the probability of embolic complications by approximately 80% compared to medical therapy [20].

Y.L. Fan et al. (2018), when comparing two patient groups (endovascular recanalization of chronic ICA occlusion vs medical therapy), identified significant cognitive improvement in the group of patients who underwent recanalization for chronic ICA occlusion [21]. This fact points to another advantage of endovascular recanalization over medical therapy and low-flow anastomoses.

The emergence of hybrid techniques for treating chronic ICA occlusion has led to successful restoration of the arterial lumen, even in occlusion Types C and D. The principle of hybrid surgery involves the primary removal of calcified and dense fibrous masses occluding the artery, after which endovascular crossing of the occlusion zone becomes possible. J. Li et al. (2019) published a comparison of treatment outcomes between two groups of patients with chronic ICA occlusion (the first group underwent hybrid intervention, the second underwent endovascular recanalization only). The rate of complications and the percentage of technically unsuccessful interventions in the hybrid group were significantly lower than in the endovascular-only group.

Antiplatelet Therapy

Rational prescription of antiplatelet therapy is required in preparation for endovascular recanalization of chronic ICA occlusion. The most common combination is clopidogrel + acetylsalicylic acid (due to irreversible blockade of P2Y12 receptors). However, it is known that clopidogrel does not clinically significantly reduce platelet aggregation in 25% of patients, while options involving ticagrelor and prasugrel present a higher risk of hemorrhagic complications. In our series, patients were prescribed clopidogrel 75 mg (1 tablet once daily) + acetylsalicylic acid 100 mg for 5 days, after which adenosine diphosphate-induced platelet aggregation was assessed and compared to the aggregogram results obtained prior to the initiation of antiplatelet therapy. If insensitivity to clopidogrel was detected, a regimen with ticagrelor (180 mg/day) was prescribed. The dual antiplatelet therapy regimen we use has been successfully applied for the implantation of both stents for brachiocephalic arteries and intracranial stents for atherosclerotic lesions and cerebral aneurysms, which is why it was adopted for the recanalization technique of the occluded ICA. After patency of the ICA was confirmed at 6 months (based on cerebral angiography), antiplatelet agents were discontinued.

Conclusion

The increasing number of scientific publications on the recanalization of chronic internal carotid artery (ICA) occlusion indicates the global adoption of this technology. Techniques for recanalizing chronic ICA occlusions are constantly being updated and refined.

The presented initial experience in performing such surgeries in Russia has demonstrated the safety of the procedure and its high efficacy in terms of restoring cerebral perfusion.

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