Endovascular treatment of acute arteriosclerotic vertebrobasilar occlusion: A single center experience

Abstract

Objectives

Few experiences on vertebrobasilar occlusion over underlying intracranial atherosclerotic disease have been reported in literature and the optimal strategy on how to perform a mechanical thrombectomy is unclear. The aim of this paper is to bring our experience based on patients admitted with acute vertebrobasilar occlusion with underlying atheromatous lesions.

Materials and Methods

Several data were collected from August 2009 to October 2022 including clinical history, pre- and post-treatment neurological objectivity, diagnostic images and angiographic procedural images, and clinical outcome at 6 months. We selected 13 patients from August 2009 to October 2022, 12 men and 1 woman, aged 40 to 82 years (mean age, 62.6 years).

Results

Mechanical thrombectomy with a thromboaspiration was performed in all patients as beginning of the procedure. In three patients, the procedures resulted in excellent angiographic result and clinical outcome, while in three patients, we observed a failure of the procedural and clinical outcome. For residual intracranial stenosis in three patients, an angioplasty was performed obtaining an ischemic area related to the posterior circulation. In four patients, a stent was placed, in three patients, we obtained a good clinical outcome with a mRS between 0 and 2, while one treatment resulted in death, probably due to a late endovascular treatment.

Conclusions

Endovascular treatment with stent deployment appears to result in an excellent outcome in patients with occlusion of the vertebrobasilar circulation in cases of occlusion on atheromatic plaque. The degree of residual stenosis after thrombospiration can significantly affect subsequent type of treatment.

Highlights

• • Basilar artery occlusion determines several clinical ischemic events associated with high rates of disability and mortality.

• • The most common therapies include stent-retriever thrombectomy (SRT) and rescue treatment. The most commonly used rescue treatment is angioplasty (with or without stent placement).

• • Endovascular treatment with stent deployment appears to result in an excellent outcome in patients with occlusion of the vertebrobasilar circulation in cases of occlusion on atheromatic plaque.

Introduction

Basilar artery occlusion determines several clinical ischemic events associated with high rates of disability and mortality. The most frequent eziopathogenic cause is related to embolization from distal sources, especially from cardiogenic origin. However, in situ thrombosis over underlying intracranial atherosclerotic disease represents 23–41% of the vertebrobasilar ischemia.^1–3 Few experiences on vertebrobasilar cerebro-vascular diseases have been reported in literature and the optimal strategy on how to perform a mechanical thrombectomy is unclear.^1–4 Accordingly, this study aimed to report our experience on different endovascular treatment to investigate prognostic factors for a good outcome.

Materials and method

Between August 2009 and October 2022, 83 patients were admitted to our hospital for acute vertebra-basilar occlusion. Among them, 13 patients were retrospectively selected for underlying atheromatous lesions localized at the predominant vertebral artery or basilar artery. This retrospective study was approved by Hospital Institutional Committee. The study population is composed of individuals who were found to have basilar artery occlusion during mechanical thrombectomy in the vertebrobasilar system and when patients met the following criteria in the pre-procedure evaluation or during endovascular procedure: (1) segmental occlusion of the vessel with distal recanalization of the distal third of the basilar artery by collateral; (2) difficulty to cross the lesion with the mechanical thrombectomy devices; (3) angiographically proven focal significant vessel artery stenosis after mechanical thrombectomy; (4) and recurrent occlusion of the treated vessel. A complete neurological history was taken from the family to establish the correct onset of the neurological symptoms and a clinical examination was performed on all patients by an independent neurologist not involved in the interventional procedure. Such a neurological evaluation was performed before the procedure and again at 24-h, 4-weeks, and 6-months follow-ups. Pre-procedural evaluation was performed with CT scan and perfusion CT scan in the wake-up strokes. All clinical, angiographic, and stenting data were recorded on case report forms by a physician. The clinical end points were as follows: (1) improvement or complete regression of clinical symptoms; (2) any stroke (disabling or not), myocardial infarction, or death within the first 30 days of the procedure;2 repeated medical or endovascular therapy within the 6 months that followed the procedure; (3) and clinical status at the 3-month follow-up visit. Angiographic end points were as follows: (1) vessel lumen patency at the end of the procedure (2) and on any follow-up CT or MRI scan performed during follow-up. Restenosis was defined as a stenosis of 50%.

The pre-procedure and post-procedure protocols were analogous to those previously described.^1–4 All patients were pre-medicated with alteplase following international protocol when the clinical evaluation were in the first 8 h from the onset. 500 mg aspirin and either 500 mg ticlopidine (Ticlid, Roche, Inc.) or 300 mg clopidogrel (Plavix, Sanofi, Inc.) were added when a metallic stent was deployed. Percutaneous access was obtained via one of the femoral arteries; in 1 patient, due to tortuous anatomy of the right vertebral artery, an introducer sheath was positioned in the omolateral radial artery. A NeuronMax 088 or an Infinity introducer sheath was placed at the origin of the vertebral artery. If patient didn’t receive the treatment with alteplase, low dose endovenous heparin was administered at the beginning of the procedure.

Pre-procedural angiographic images were then obtained in orthogonal planes. The lesions were crossed with a hydrophilic-tipped 0.014-inch wire (Trascend or Synchro) within a flexible microcatheter (Offset, stryker; Velocity, Penumbra). A first thromboaspiration passage was usually performed to initially restore the vessel caliber and to understand the nature of the occlusion. Once the vessel patency was restored, an angiography was performed after about 10 min to evaluate the long-term patency of the vessel. If needed, the lesions were then pre-dilated with a 2.0 × 20-mm coronary balloon (Ryurei, Terumo, Tokyo, Japan) at 4 to 6 atm for 30 to 45 s with the use of a standard insufflator, even to evaluate the vessel caliber. The maximal pressure of inflation was achieved by very slowly and gently inflating the balloon until no waist was visible. In some patients, a 3.0 to 4-mm flexible coronary stent (Ultimaster, Terumo, Tokyo, Japan) was then deployed across the point of stenosis, while in another group, a higher caliber coronary balloon was used to restore vessel patency. Deployment of the stents was performed by inflating the balloon at 9 to 10 atm as the requested nominal balloon pressure. Both antiplatelet agents were continued for almost 3 months, after which the patients were only treated with aspirin 100 mg/d.

Statistical analysis

Continuous variables are presented as medians and interquartile ranges (IRQs). The Mann–Whitney U-test was used to compare continuous variables. We analyzed the baseline characteristic and clinical outcome of the patients.

Second, the relationship between each clinical and procedural characteristic and the 3-month and 6-month functional outcome was determined.

All statistical analyses were performed with SPSS software (version 23.0, IBM SPSS).

Results

There were 12 men and 1 woman, aged 40 to 82 years (mean age, 62.6 years). Mechanical thrombectomy with a thromboaspiration catheter was performed in all patients as the beginning of the procedure.

Balloon angioplasty or stent placement was successful in all patients.

In six patients, only mechanical thrombectomy was performed. In three patients, the thromboaspiration was sufficient to restore vessel caliber and a stenosis inferior to 30% remained after the treatment. Two of these were treated with simple thromboaspiration with a thromboaspiration catheter (Catalyst 6, Stryker, Kalamazoo, US; 5MAX, Penumbra, Alameda, US). In three patients, the procedures resulted in failure due to absent vessel caliber restore after thromboaspiration with catheter and stentriever.

In three patients, an angioplasty, with a 3 mm in two patients and a 3.5 mm balloon catheter (Ryurei, Terumo, Tokyo, Japan), was performed. In one patient, we performed an angioplasty at the level of the right predominant vertebral occlusion, while in the other two patients, the angioplasty was performed in the basilar artery. However, in all patients, at 24 h CT, a hypodense area, variable in extension, was evident in the bulbar trunk associated a hyperdense sign on the vertebral or basilar artery associated with a worst clinical outcome.

After mechanical thromboaspiration, in four patients, a stent was placed. In one patient, the stent was placed after 3 days due to residual significant stenosis at the middle third of the basilar artery and to fluctuant clinical symptoms nevertheless the dual anti-aggregant therapy. In other three patients, the stent was placed in acute situation due to early reocclusion of the vessel in the angiography at about 10 min. One patient with a basilar artery occlusion arrived in our hospital after 8 h from the clinical onset and after 4 h from the CT scan. This delay was due to the access of the patient in a hospital not included in the stroke area management. The patient died 6 h after the treatment; however, already during the treatment, he presented abnormal heart rhythm. In the third patient (77 yo), there was the occlusion of the predominant left vertebral artery and of the basilar artery, except at the top. The patient presented NIHSS 15 with a sudden clinical improvement after the recanalization and immediate clinical deterioration after the angiographic worsening. In this patient, a 3.5 mm × 8 mm coronary stent (Ultimaster, Terumo, Tokyo, Japan) was placed. Patient was discharged with NIHSS 2. Even in fourth patient, a direct coronary stenting (3.5 mm × 12 mm, Ultimaster, Terumo, Tokyo, Japan) of the basilar artery was placed with a good clinical outcome (NIHSS onset 13; NIHSS discharge 1).

There were no direct procedure-related myocardial infarctions or deaths. Clinical follow-up was available in 13 patients, with the follow-up period varying from 0 to 6 months.

The most common risk factor found was hypertension (53%) (Table 1). The admission NIHSS score was recorded for all patients. The majority (38%) of the patients presented with moderate stroke (NIHSS score 5–15). Four patients (30%) presented with very severe stroke (NIHSS scale ≥21). The mean NIHSS score was 17 ± 9.7. The average pre-operative pcASPECT score was 9.2 (range 8–10). Six patients received intravenous (IV) alteplase (tissue plasminogen activator [tPA]) prior to mechanical thrombectomy. Six patients were transported from other hospitals (SPOKE) to undergo endovascular treatment at our hospital (HUB).

Table 1.

Clinical/radiological features and outcomes.

Age	62.6 ± 13.8
Male	12 (92%)
Associated condition
Atrial fibrillation	1 (7%)
Diabetes	1 (7%)
Hypertension	7 (53%)
Hypercholesterolemia	1 (7%)
Smoker	3 (23%)
NIHSS score on admission
0	0
1–4	1 (7%)
5–15	5 (38%)
16–20	3 (23%)
21–42	4 (30%)
NIHSS score at discharge	12 ± 14
pcASPECT score	9.25 ± 0.6
Affected vessel
Right vertebral artery	1 (7%)
Left vertebral artery	8 (61%)
Basilar artery	4 (30%)
Time from stroke onset to recanalization	369 ± 158 min
Procedure time	36 ± 21 min
Patients from SPOKE (other hospital)	6 (46%)
Intubation after 24 h from onset	6 (46%)
Ischemic zone after 24–36 h
Midbrain-pons	9 (69%)
Cerebellar ipsilateral	5 (38%)
Cerebellar contralateral	6 (46%)
Supra-tentorial	3 (23%)
TICI ≥2b	11 (84%)
6-months mRS score
0	3 (23%)
1	4 (30%)
2	0 (0%)
3	2 (15%)
4	1 (7%)
5	0 (0%)
6	3 (23%)

The mean time to recanalization with confirmed time of onset was 369 ± 158 min. The average time of the endovascular treatment was 36 ± 21 min. A TICI ≥2b result was achieved in 84% of the patients. After 24 h from onset of symptoms, six patients with low GCS were intubated

All patients had follow-up imaging, several patients (69%) reported ischemic lesions in the midbrain-pons area. No signs of hemorrhage found on follow-up imaging. NIHSS at discharge was 12 ± 14. At 90-day follow-up, 53% of the patients showed a good clinical outcome (mRS score ≤2), and 68% showed a moderate clinical outcome. In total, three deaths occurred in our cohort at 3 months after the onset of the symptoms (23%).

Discussion

Few experiences on the treatment of vertebrobasilar cerebro-vascular atheromatous occlusion have been reported, and the best EVT strategy remains controversial. Clots formed by in situ thrombosis are made of platelets and fibrin. ¹ The most common therapies include stent-retriever thrombectomy (SRT) and rescue treatment. The most commonly used rescue treatment is angioplasty (with or without stent placement); other rescue treatments include switching to another modality (e.g., from using a stent-retriever to performing contact aspiration), intra-arterial thrombolysis (with alteplase or urokinase), and intravenous or administration of intra-arterial glycoprotein IIb/IIIa inhibitor (GPI).^1–10 If one of the aforementioned treatments failed to achieve effective reperfusion, another can be used as a rescue approach.

Nevertheless, many studies have reported high rates of rescue treatment (68.4–100%) in the setting of basilar artery occlusion related to atheromatous plaque.^2,10

Endovascular treatment for patients with this kind of occlusion typically involves two steps: first, performing mechanical thrombectomy with stent-retriever enables the operator to identify and evaluate the culprit vessel and, subsequently, administering rescue treatment to both remove the underlying stenosis and prevent reocclusion.^11,12

Rescue treatments (angioplasty with or without stenting) were reported to be essential for achieving successful recanalization in such patients in the setting of failed stent-retriever.^2–12 This is likely because the use of a stent-retriever predisposes to increased platelet activation and vessel dissection inducing plaque rupture.

In addition, angiographic stenosis after mechanical thrombectomy might occur due to new further adherent clot, dissection, or vasospasm; these would be difficult to differentiate from an elastic recoil due to residual atherosclerotic plaque.

However, fragmented residual clots would migrate to distal branches and do not adhere to the vessel wall when antegrade blood flow is restored after mechanical thrombectomy. Arterial dissection could be easily differentiated by its characteristic angiographic appearance, such as an intimal flap or double lumen. ¹

However, if a focal fixed stenosis is sustained, interventionalists should consider whether intra-arterial disease may be hidden in the occlusion. The third step is to confirm whether the stenosis is hemodinamically significative. If severe stenosis is still observed after a repeated primary thrombectomy, a rescue treatment should be considered. Usually, a stenotic degree major of 70% is considered a significant risk factor for the recurrence of ischemic stroke. A stenotic degree of >70% but with a stenotic lesion that has been repeatedly occluded or a flow that is not fluent is also considered a significant stenosis. The fundamental step is to wait 10–20 min after recanalization. ¹³

Once the significant stenosis was highlighted, angioplasty or stenting was usually performed. In the study of Fan et al., 86.7% of patients (13/15) with underlying atheromatous plaque were treated with intracranial angioplasty with or without stent placement after first-line mechanical thrombectomy with an achieved high rate of successful revascularization (100%) and a favorable outcome (60%), no symptomatic hemorrhage, all with a low mortality rate (13.3%). ¹² Yoon et al. reported the results of emergent angioplasty and stent placement in 40 patients with acute ischemic stroke due to underlying Internal Carotid Artery Stenosis (ICAS). ¹¹ They reported high rates of successful revascularization (95%) and favorable outcome (62.5%) and low rates of symptomatic hemorrhage (7.5%) and mortality (15%). They suggested that intracranial angioplasty with or without stent placement is safe and feasible in hyperacute stroke secondary to underlying ICAS. Gao et al. also reported a 100% successful revascularization rate and a favorable 3-month outcome rate of 46% in a series of 13 patients with acute BAO and underlying ICAS who were treated with stent-retriever thrombectomy and intracranial stent placement. ⁹

The evidence shown demonstrates that angioplasty with balloon or/and stent should be performed as soon as possible in patients with BAO. As a notable result, the rate of mTICI 3 in the atheromatous-related basilar occlusion group was higher than what was observed in the embolic group (Yang et al.) ¹³ probably due to a light thrombus burden over the atheromatous plaque, leading to a lower risk of distal embolization.^13,14

In our experience, the mortality rate is high, even considering mechanical thrombectomy alone performed in the years 2009–2012, using both thromboaspiration and stent-retriever. In subsequent cases, albeit with a poorly representative sample, a poor outcome was shown in patients undergoing angioplasty compared with those treated with coronary stenting. This, in our hypotheses, is due to the type of plaque that caused the occlusion and possible dual antiplatelet therapy, which is still not standardized. Patients treated with stent were subjected to pre-dilatation in order to obtain an appropriate caliber and see the rate of vessel reocclusion. Patients with a residual stenosis of 30–40%, even after catheter thromboaspiration, had no need for further treatment, synonymous with good blood flow that did not promote overlapping thrombosis/platelets aggregates.

Angioplasty alone seemed to have given a good result in terms of angiographic imaging at 10 min however with poor outcome. In our opinion, the type of plaque may influence outcome, not only a subsequent thrombosis. Moreover, a particularly organized plaque may promote further flow turbulence due to recoil with subsequent reocclusion. Therefore, in our opinion, it is essential to treat patients with coronary stents in order to restore direct flow, minimize flow turbulence from stenosis, and reduce plaque recoil.

This study was intended for patients who were undergoing endovascular treatment; since the enrolled patients were not randomized and were limited to achieving recanalization, some selection bias may exist, especially due to the sample size (Figures 1–3).

Figure 2.

Soporous patient with NIHSS 16. (A and B) CT angiography shows segmental occlusions of the left vertebral artery and the basilar artery. (C) Diagnostic angiography shows a significant stenosis with floating thrombus visualized by diagnostic angiography. (D) Thrombospiration. (E) Diagnostic angiography after thrombospiration with 50% residual stenosis. (F) MRI after procedure documented ischemic cerebellar lesion. Clinically asymptomatic patient.

Figure 1.

A patient with hypertensive crises and right motor deficit (NIHSS 12). (A and B) CT angiography shows segmental occlusions of the left vertebral artery and the basilar artery. (C) Diagnostic angiography. (D) Thrombospiration. (E) Unsuccessful attempts after thrombospiration and stentriever. (F) Prolonged and high pressure angioplasty. (G and H) Final angiography documenting important stenosis (greater than 50%). (I and J) CT and MRI after 6 h documenting reocclusion of the vessel with pons stroke.

Figure 3.

Soporous patient with NIHSS 11. (A) CT angiography shows occlusion on left vertebral artery and stenosis on basilar artery. (B and C) Diagnostic angiography confirms the pathological finding. (D) Post-thrombospiration angiography. (E) Angiography 10 min from thrombospiration (worsening stenosis). (F) Coronary stent placement (4 mm × 12 mm). (G) Post stent placement angiography. (H) Post-procedural MRI (not suffering areas). (I) CT angiography at 12 months: excellent result with correct visualization of the circle. Clinically asymptomatic patient.

Conclusion

Endovascular treatment with stent deployment appears to result in an excellent outcome in patients with occlusion of the vertebrobasilar circulation in cases of occlusion on atheromatic plaque. Limited clinical results have been obtained with only angioplasty, excellent with balloon expandable coronary stent. The degree of residual stenosis after thrombospiration can significantly affect the subsequent type of treatment.

ORCID iDs

Valerio Da Ros https://orcid.org/0000-0001-7167-7594

Gianluca Cecchi https://orcid.org/0000-0001-6033-0579