The use of single low-profile visualized intraluminal support stent-assisted coiling in the treatment of middle cerebral artery bifurcation unruptured wide-necked aneurysm

Abstract

Objective

Endovascular treatment of unruptured wide-necked aneurysms located at the middle cerebral artery bifurcation remains challenging. This study aimed to evaluate the safety and efficacy of endovascular treatment for middle cerebral artery bifurcation unruptured wide-necked aneurysms using a low-profile visualized intraluminal support (LVIS) stent.

Methods

We retrospectively reviewed all patients with middle cerebral artery bifurcation unruptured wide-necked aneurysms treated using an LVIS device at our institution between October 2014 and December 2018. Clinical presentation, aneurysmal characteristics, technical feasibility, perioperative complications, clinical outcome, and angiographic and clinical follow-up results were evaluated.

Results

Fifty-seven patients with 57 wide-necked aneurysms arising from the middle cerebral artery bifurcation were identified. The technical success rate of stent deployment was 100%. Immediate postoperative angiograms showed Raymond 1 in 26 aneurysms (45.6%), Raymond 2 in 10 (17.6%), and Raymond 3 in 21 (36.8%). Perioperative complications developed in two patients (3.5%), including one procedure-related hemorrhagic event and one thromboembolic event. The follow-up angiogram was available for 47 aneurysms obtained at an average of 11.7 months (range, 5 to 49 months) after intervention; the latest follow-up angiograms revealed complete occlusion in 37 (78.7%) aneurysms, improvement in three (6.4%), stabilization in five (10.6%), and recanalization in two (4.3%). During the follow-up, one patient was found to have in-stent stenosis and two patients were found to have slow flow or occlusion of the jailed branch. All three of these patients were asymptomatic. No hemorrhagic or thromboembolic events occurred during clinical follow-up.

Conclusions

Our experience suggests that endovascular treatment of middle cerebral artery bifurcation unruptured wide-necked aneurysms with an LVIS stent is safe and effective, but the effect on branches needs to be further studied.

Introduction

Middle cerebral artery (MCA) bifurcation aneurysms are among the most common intracranial aneurysms, accounting for 80–85% of all MCA aneurysms, which account for 18–25% of all intracranial aneurysms.¹ Traditionally, MCA bifurcation aneurysms have been thought to be primarily surgical lesions with a straightforward surgical approach and complete visualization of the anatomy. Recently, the endovascular treatment of intracranial aneurysms has become widely accepted; however, for MCA bifurcation unruptured aneurysms, the best treatment remained controversial. MCA bifurcation aneurysms were often incorporated with the tortuous and acute-angled efferent branch with a wide-necked and multi-lobed shape.² When the aneurysm involves two branches, in previous treatments, a Y-configured stent technique was typically used.³ Additionally, because of the small diameter of the MCA, these lesions could potentially be more difficult to stent or perform balloon-assisted interventions. The low-profile visualized intraluminal support (LVIS) device (MicroVention, USA), a braided stent with high metal coverage, which offers an alternative to conventional stents and flow diverter (FD) stents, was designed for the stent-assisted coil embolization of wide-neck intracranial aneurysms and has been used to treat aneurysms in small parent vessels.⁴ However, there have been few reports on whether the treatment of MCA bifurcation wide-necked aneurysms using a single LVIS stent can effectively protect branch vessels and improve long-term outcomes. Hence, we conducted this retrospective study to examine the safety, deployment feasibility, and treatment effectiveness of the LVIS device in MCA bifurcation unruptured aneurysms.

Methods

This retrospective study was approved by our hospital institutional review board and the need for informed consent was waived.

Patients

We retrospectively reviewed all patients with MCA bifurcation unruptured wide-necked aneurysms treated with an LVIS device at our institution between October 2014 and December 2018. We identified 57 patients with 57 wide-necked aneurysms arising from the MCA bifurcation. Three neurointerventionists (Q. H. H., Y. Z. Y., and Z. W. Z.) assessed the surgical notes, medical charts, and radiologic images of the patients. Furthermore, the patients' demographics, aneurysm characteristics, vascular risk factors, clinical and technical complications, and follow-up angiography data were evaluated.

Procedure details and perioperative medication

All endovascular procedures were performed under general anesthesia via a transfemoral approach using biplane angiographic equipment. Heparin (45 U/kg) was intravenously infused after the femoral sheath was placed and additional heparin was administered every hour with the goal of maintaining the activated clotting time at two to three times that at baseline during the procedure. A 6-F guiding catheter was introduced into the internal carotid artery. On the basis of the images generated from the reconstruction, the working projections (angiographic projections that best delineated the relationship between the aneurysm neck and the parental vessel) were chosen for the procedure. The appropriate coils were selected according to the size of the aneurysm. The smallest 3.5-mm LVIS stent (which is different from the LVIS Jr stent) was used for all cases because the diameter of all parent arteries was ≤3.5 mm. According to the size of the aneurysm neck and angle between the branch and parent artery, the appropriate length of stent was selected to anchor the distal end of the stent and the stent was released using the “barrel technique” at the aneurysm neck. After deployment of the stent, angiography was used to confirm that the stent was completely open and the branch was well protected. We then continued to fill the coils. At the end of the procedure, postoperative angiograms in frontal, lateral, and working projections were acquired to assess the results and rule out any parent artery or branch occlusion and DynaCT (Siemens), VasoCT (Philips), or multi-projection fluoroscopy were performed to identify wall apposition. All patients underwent immediate postoperative CT scanning to detect any possible subarachnoid or intraparenchymal bleeding.

Dual antiplatelet drugs (100 mg/day aspirin plus 75 mg/day clopidogrel) were administered for at least three days prior to the procedure. Platelet function testing (TEG Hemostasis System, Haemoscope Corporation, Niles, IL, USA) was performed routinely before the procedure to evaluate platelet aggregation inhibition with the dual antiplatelet drugs. Ticagrelor (90 mg, twice a day) was used to replace clopidogrel if the patient was not sensitive to clopidogrel. All patients treated with a stent were administered aspirin (100 mg/day) and clopidogrel (75 mg/day) postoperatively for six weeks followed by aspirin alone (100 mg/day) indefinitely.

Clinical assessment and angiographic and clinical follow-up

Clinical outcome was assessed using the modified Rankin Scale (mRS) at discharge and the latest follow-up. The immediate postoperative angiographic results were assessed using the Raymond scale⁵: Raymond 1 (complete occlusion), 2 (residual neck), and 3 (residual aneurysm). The first angiographic follow-up was generally performed at six months using DSA and then MRA or DSA yearly thereafter. The angiographic follow-up results were classified into four categories when compared with the immediate degree of embolization degree: occlusion (no contrast material filling the aneurysm sac), improvement (decreased contrast material filling the aneurysm sac), stabilization (unchanged contrast material filling the aneurysm sac), and recanalization (increased contrast material filling the aneurysm sac).⁶

Aneurysm classification

According to the relationship between the aneurysm and branches of the MCA bifurcation, we divided the aneurysms into the following categories: Ia, the aneurysm mainly involved one branch, and the angle between the involved branch and the proximal parent artery was < 90°; Ib, the aneurysm mainly involved one branch and the angle between the involved branch and the proximal parent artery was ≥90°; IIa, the aneurysm involved two branches and the angles between these two branches and the proximal parent artery were all <90°; IIb, the aneurysm involved two branches, one with an angle <90° to the proximal parent artery, and the other with an angle ≥90°; IIc, the aneurysm involved two branches, the angles between these two branches and the proximal parent artery were all ≥90° (Figure 1). In this study, there were 19 Ia, three Ib, 11 IIa, 16 IIb, and eight IIc aneurysms.

Figure 1.

Aneurysms were divided into five categories according to the relationship between the aneurysm and the branches of the MCA bifurcation.

Results

Baseline characteristics

A total of 57 patients with MCA bifurcation unruptured wide-necked aneurysms treated with an LVIS stent were identified. The patients comprised 23 men and 34 women with a mean age of 60.3 years (range, 36–87 years). Patient risk factors included hypertension (70.2%), diabetes (12.3%), and smoking (3.5%). Aneurysms were incidentally found in 18 patients, whereas the other 39 patients presented with neurological symptoms such as headache, dizziness, blurred vision, tinnitus, or numbness, and so on. Twenty-eight patients (49.1%) had aneurysms in the left MCA bifurcation. The mean maximum diameter of the aneurysms was 5.7 ± 2.5 mm (range, 3.1–13.3 mm), mean neck diameter was 4.4 ± 1.7 mm (range, 2.0–11.0 mm), mean diameter of the distal parent vessels was 2.3 ± 0.5 (range, 1.5–3.2 mm), and mean diameter of the proximal parent vessels was 2.6 ± 0.4 (range, 1.7–3.5 mm). The data are summarized in Table 1.

Table 1.

Baseline characteristics of patients and aneurysm characteristics.

Variable	Valuesa
Age (yr)	60.3 ± 10.0
Sex
Male	23 (40.4%)
Female	34 (59.6%)
Hypertension	40 (70.2%)
Diabetes mellitus	7 (12.3%)
Smoking	2 (3.5%)
Location
L	28 (49.1%)
R	29 (50.9%)
Maximum size (mm)	5.7 ± 2.5
Neck size (mm)	4.4 ± 1.7
Distal parent vessel size (mm)	2.3 ± 0.5
Proximal parent vessel size (mm)	2.6 ± 0.4

^aValues are mean ± SD or number of patients (percentage).

Immediate results and perioperative complications

The technical success rate of stent deployment was 100% and there were no failures in navigating or deploying the LVIS stent. Immediate postoperative angiograms showed complete occlusion (Raymond 1) in 26 aneurysms (45.6%), residual neck (Raymond 2) in 10 (17.6%), and residual aneurysm (Raymond 3) in 21 (36.8%) following endovascular treatment (Table 2).

Table 2.

Immediate and follow-up outcomes.

Variable	Valuesa
Initial aneurysm occlusion
Raymond 1	26 (45.6%)
Raymond 2	10 (17.6%)
Raymond 3	21 (36.8%)
Discharge mRS
0	55
1	1
2	1
3	—
4	—
5	—
6	—
Angiographic FU (months)	11.7 ± 9.7
Clinical FU (months)	13.6 ± 10.8
Angiographic follow-up outcome
Occlusion	37 (78.7%)
Improvement	3 (6.4%)
Stabilization	5 (10.6%)
Recanalization	2 (4.3%)
Clinical follow-up mRS
0	57
1	—
2	—
3	—
4	—
5	—
6	—

^aValues are mean ± SD or number of patients (percentage).

mRS: modified Rankin scale.

Perioperative complications developed in two patients (3.5%) including one procedure-related hemorrhagic event and one thromboembolic event. One intraoperative aneurysm rupture event was encountered as a result of aneurysmal perforation during the placement of the coil. It was well handled by reversal of the anticoagulation and further coiling and resulted in no clinical sequelae. After awaking from anesthesia, one patient suffered right hemiplegia. The CT images did not show any signs of intracranial hemorrhage and DSA excluded main vessel occlusion. This patient was treated with intravenous tirofiban and made a good recovery. Postoperative MRI indicated a scattered infarction in the left basal ganglia. He had only mild right limb weakness at discharge and a mRS score of 0 at the time of his six-month follow-up visit.

Fifty-five patients had a mRS score of 0 at discharge, while one patient had a mRS score of 1 and another patient had a mRS score of 2 (Table 2).

Angiographic and clinical follow-up

Of all 57 patients, angiographic follow-up was available in 47 patients (82.5%). The mean follow-up time for all 47 patients was 11.7 months (range, 5 to 49 months). The final follow-up angiograms revealed complete occlusion in 37 (78.7%) aneurysms, improvement in three (6.4%), stabilization in five (10.6%), and recanalization in two (4.3%). One recanalized aneurysm was retreated with LVIS stent-assisted coils, while another was retreated with FD. On follow-up DSA, one patient was found to have in-stent stenosis and there was no abnormality on CT perfusion imaging (Figure 3). One patient was found to have mild stenosis of the branch covered by the LVIS stent. In addition, occlusion of the jailed branch occurred in one case (Figure 2). All three patients had no clinical ischemic symptoms. The mean clinical follow-up time was 13.6 months (range, 5 to 49 months). No hemorrhagic or thromboembolic events occurred during clinical follow-up. The mRS score was 0 in all patients at the latest follow-up. Data are summarised in Table 2.

Figure 3.

(a) Right ICA angiogram showing an MCA bifurcation aneurysm. (b) Roadmap image revealing the stent microcatheter and coil microcatheter in place. (c, d) The aneurysm underwent stent-assisted coiling with the immediate postoperative angiogram showing the residual aneurysm and good stent apposition to the parent artery wall. (e, f) Complete aneurysm occlusion was achieved at the nine-month follow-up. In-stent stenosis occurred at the distal stent marker.

Figure 2.

Conventional angiogram (a) and three-dimensional angiogram (b) of the right ICA showing an MCA bifurcation aneurysm. (c, d) This aneurysm was treated with LVIS stent-assisted coiling. The immediate postoperative angiogram shows the residual aneurysm. (e, f) A six-month follow-up angiogram showing complete occlusion of the aneurysm and occlusion of the covered branch. (g) Immediate postoperative angiogram showing no abnormality. (h) Follow-up angiogram showing that the MCA flowed back to the temporal lobe.

Discussion

Conventional coiling for wide-necked MCA bifurcation aneurysms remained a technical challenge and its long-term outcome stability remained controversial, due to the bifurcated anatomy, wide necks, dysmorphic shapes, and branches that could be angiographically undecipherable.⁷ More recent technical advancements, including balloon remodeling, stent-assisted coiling, and, lately, the use of FD have increased the number of physicians who have adopted endovascular embolization for the treatment of MCA bifurcation wide-necked aneurysms with satisfactory results.¹ Hagen et al.⁸ reported 67 unruptured MCA bifurcation aneurysms treated with stent-assisted embolization, including the Neuroform (Stryker, USA) and LVIS Jr stents, with a 7.4% perioperative complication rate and a good outcome rate of 86.6% at discharge. Zhou et al.⁹ reported 72 complex MCA aneurysms (51 MCA bifurcation aneurysms) treated using non-LVIS stent-assisted embolization. During angiographic follow-up, 93.4% of all aneurysms were completely occluded, improved, or stable, and only 4.9% recurred. The endovascular stent not only prevents coils from protruding into the parent vessel, but also changes hemodynamics and promotes endothelialization of the aneurysm neck. In this study, LVIS stent-assisted embolization was used with favorable long-term outcomes; the rate of perioperative complications was 3.5%. During follow-up, 95.7% of all aneurysms were completely occluded, improved, or stable, and only 4.3% recurred.

The LVIS stent is a self-expanding closed-cell stent. For lesions in small vessels with acute-angled branches, whether the LVIS stent could open sufficiently and the branches would be well protected was the biggest technical challenge when treating MCA bifurcation wide-necked aneurysms. The LVIS stent has the characteristics of being visible for its full length and high radial support force. In this study, the LVIS stents were all successfully deployed and opened well. The LVIS device with greater bulging capability at the bifurcation can expand into the aneurysm neck using the “barrel technique,” provide greater neck coverage, and change a wide-necked aneurysm into a narrow-necked one, consequently protecting the parent artery and branch.¹⁰ Furthermore, we can push the stent at the aneurysm neck to produce denser metal coverage and improve the hemodynamic effect, which may promote aneurysm thrombosis and complete occlusion of the aneurysm during long-term follow-up. In the treatment of MCA bifurcation aneurysm with an LVIS stent, we usually filled the first coil and did not get out of it. We then released the stent and confirmed using angiography. If the stent was not opened sufficiently or the coil was squeezed into the branch, we withdrew the coil and adjusted the shape of the coil or used another replacement coil. At the same time, we could reduce the packing density of the coils and leave space to prevent the coil from prolapsing into the branch. Because the LVIS stent has high metal coverage, even if there was residue at the opening of the branch, we could obtain good long-term outcomes and a low recanalization rate. In addition, in the treatment of Ia and Ib aneurysms, the stent can be placed in the main branch and another branch can be well protected using the “barrel technique.” For IIa, IIb, or IIc aneurysms, in previous treatments, we required a Y-configured stent technique with other types of stents.³ Now, we can use a single LVIS stent deployed in the branch that is easy to release and change a wide-necked aneurysm into a narrow-necked one using the “barrel technique.”

The occurrence and development of aneurysms are closely related to hemodynamics; therefore, changing hemodynamics is the most fundamental strategy for treating aneurysms. FD with higher metal coverage and better hemodynamic effects has become an important method for treating aneurysms, especially for lateral wall aneurysms of the internal carotid artery and vertebral artery.¹¹ However, for bifurcation aneurysm with branch involvement, the efficacy of FD was not clear because of the persistence of the branch; the effect of high metal coverage on the branches and lenticulostriate perforating arteries was also a major concern in treatment. Furthermore, it became apparent only recently, that braided devices with high surface coverage very frequently caused delayed vasoconstriction peaking three to five weeks after implantation of stents in the proximal and distal landing zones, which in rare cases resulted in stroke.¹² In this study, one patient was found to have in-stent stenosis at the distal stent without ischemic symptoms during the follow-up, which may be associated with neointimal hyperplasia and delayed vasospasm. Bhogal etal.¹³ reported 13 MCA bifurcation aneurysms treated with PED (Covidien, USA) or p64 (Phenox, Germany). They achieved complete occlusion in 50% of patients and near-complete occlusion in 41.7% and two perioperative thromboembolic complications occurred. During the follow-up, angiography of the covered MCA branches showed a reduction in caliber in five (41.7%) and complete occlusion in one (8.3%), which were all asymptomatic. The results reported by Caroff et al.¹⁴ were not so promising. In their retrospective review of 15 saccular MCA bifurcation aneurysms treated with FD, the authors reported ischemic complications in 43% of the cases detected on MRI. Although, there were no mortalities, procedure-related morbidities reached 21% on follow-up, most of which were related to slow flow or occlusion in the covered branches. Complete occlusion was achieved in only 62% of aneurysms. Cagnazzo et al.¹⁵ conducted a meta-analysis on the treatment of MCA aneurysm with FD, including 244 MCA aneurysms (76.3% in the MCA bifurcation). The rate of perioperative complications was 20.7%. During follow-up, the rate of complete or near complete occlusion was 78.7%. Furthermore, 10% of the branches covered by FD were occluded and 26% has slow flow. Therefore, the use of FD stents in treating MCA bifurcation aneurysms has continued cautiously. Nowadays, the use of low-profile FD, like Silk Vista Baby (BALT, France), not only rendered intrasaccular manipulations unnecessary, but also almost certainly prevented recanalization by the formation of the neointima along the surface of the dense mesh. Schob et al.¹⁶ reported 27 aneurysms beyond the circle of Willis treated with Silk Vista Baby. All parent arteries remained patent; 17/27 aneurysms were completely occluded during the follow-up, 6/27 aneurysms showed decreased influx or delayed washout and 1 remained unchanged. But the result of treatment of the MCA bifurcation aneurysms and the effect on branches need further studies.

However, the LVIS stent, which has a more than 20% metal surface, has certain hemodynamic effects on intracranial aneurysms; a single LVIS stent causes more flow diversion than overlapping Enterprise stents but less than a single FD device.¹⁷ In this study, the branches covered by the LVIS stent were well protected and only two patients were found to have covered branch slow flow or occlusion without symptoms of clinical ischemia. In addition, Woven Endobridge (WEB, Sequent medical, USA), a type of intra-aneurysmal FD, was shown to have no effect on the parent artery and did not need antiplatelet therapy; however, its operation is relatively complex and the larger deployment systems make treatment more difficult. Hagen et al.⁸ reported 38 MCA bifurcation aneurysms treated with WEB. There were three perioperative thromboembolic events (7.9%) and eight aneurysms (21.1%) which had to be retreated during the follow-up. The high retreatment rate might correlate with the learning curve in choosing the right device size. With the application of a new generation of smaller deployment systems, better results may be obtained.

In conclusion, this study shows that endovascular treatment of MCA bifurcation unruptured wide-necked aneurysms with an LVIS stent is safe and effective, has a low recurrence rate, and the branches can be well protected. However, there were several limitations of our study, including its retrospective design, patient selection bias, and the limited number of cases in a single institution. At the same time, for MCA bifurcation aneurysms with a very wide neck, we prefer surgical clipping. In the future, a larger sample size and longer follow-up are needed to determine the effect on branches.

Highlights

Although treatment for unruptured wide-necked aneurysms located at the MCA bifurcation remains challenges, endovascular treatment of MCA bifurcation unruptured wide-necked aneurysms with LVIS stent is safety and effective and the branches can be well protected.

Declaration of conflicting interests

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

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The study was supported by the National Key R&D Program of China (2016YFC1300700) and Natural Science Foundation of China (NO. 81571118 & NO. 81771264).

Guarantor

Qinghai Huang, M.D.

Informed consent and ethical approval

This study is a single center experience and pooled data analysis and no human participant procedure were involved. This retrospective study was approved by our hospital institutional review board and informed consent was waived.

ORCID iD

Qinghai Huang https://orcid.org/0000-0001-9068-5194