Reconstructive endovascular treatment of patients with ruptured distal intracranial aneurysms in posterior circulation: a retrospective cohort study

Introduction

The rupture of intracranial aneurysms (IAs) can result in subarachnoid hemorrhage (SAH), potentially causing serious neurological impairments and even death (1). Posterior circulation aneurysms are relatively rare, accounting for only 10% of IAs (2). Posterior circulation aneurysms are risk factors for complications in the endovascular treatment of intracranial aneurysms, and due to their deep location and proximity to important cranial nerves, ruptures often lead to severe neurological deficits, disability, or even life-threatening conditions (3,4). Distal intracranial aneurysms (DIAs) account for only 1–9% of all IAs and are also relatively rare (5). They are defined as aneurysms occurring beyond the circle of Willis (6). In the posterior circulation, distal aneurysms are located in arteries such as the posterior cerebral artery distal to the posterior communicating artery (P2–P4 segments), or in arteries beyond the first segment of the superior cerebellar artery (SCA), anterior inferior cerebellar artery (AICA), and posterior inferior cerebellar artery (PICA). Morphologically, distal aneurysms include both fusiform and saccular types (6,7). Endovascular treatment of posterior circulation DIAs is particularly challenging and involves technical difficulties (8). Surgical clipping for this type of aneurysm presents numerous challenges. For instance, posterior circulation DIAs are often located in deep brain tissues, such as the cerebellum or pons. The small sac or wide neck makes it difficult to maintain patency of the parent artery during clipping (8). Endovascular treatment of ruptured posterior circulation DIAs also poses certain challenges. First, the parent artery has a small diameter and is more tortuous, making it hard to maintain patency after embolization of the aneurysm. Second, the aneurysm’s remote location complicates endovascular procedures, leading to a higher likelihood of procedure-related complications such as arterial perforation, dissection, or intraoperative aneurysm rupture (9). With advances in interventional techniques and materials, methods for operating in distal arteries have become more refined. Clinically, endovascular treatment is being increasingly adopted for such aneurysms. In this study, we retrospectively analyzed the clinical and imaging data of patients with ruptured posterior circulation DIAs treated with endovascular treatment at The First Affiliated Hospital of Harbin Medical University to evaluate the safety and efficacy of endovascular treatment for ruptured DIAs in the posterior circulation. We present this article in accordance with the STROCSS reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1147/rc).

Methods

Patients

We retrieved data from The First Affiliated Hospital of Harbin Medical University for all patients diagnosed with IAs from September 2014 to August 2023. Based on the hospital records, computed tomography (CT) and digital subtraction angiography (DSA) results, we selected the patients with ruptured distal aneurysms of the intracranial posterior circulation who underwent endovascular treatment. This single-center, retrospective cohort study involved the analysis of the clinical and imaging data of these patients. The inclusion criteria were as follows: (I) all aneurysms located in the posterior circulation; (II) confirmation of ruptured aneurysms by CT and DSA; (III) parent arteries of the aneurysms located on the posterior cerebral artery distal to the P1 segement (P2–P4 segments) or on arteries beyond the first segment of the SCA, AICA, and PICA (6,9); (IV) only one aneurysm or multiple aneurysms, with all being DIAs; and (V) underwent reconstructive endovascular treatment with patent parent arteries. The exclusion criteria were as follows: (I) parent artery sacrifice surgery with postoperative occlusion of the distal parent artery, (II) concurrent intracranial vascular malformations, (III) patients with multiple aneurysms in which some were not DIAs, and (IV) a pre-onset modified Rankin scale (mRS) score greater than 2. The study flowchart is shown in Figure 1.

Figure 1 Flowchart of the patient selection process.

The Ethics Committee of First Affiliated Hospital of Harbin Medical University approved this study (No. 202496) and complied with the principles of the Declaration of Helsinki (as revised in 2013). Written informed consent was obtained from all patients before the procedure.

Procedure

All procedures were performed by neurointerventional doctors with >10 years of experience at our center. Patients underwent endovascular treatment under general anesthesia and systemic heparinization. Before the procedure, three-dimensional (3D) rotational angiography and 3D reconstruction were performed. We performed preoperative DSA examinations on all patients. Based on the specific characteristics of each patient’s aneurysm, including the aneurysm size, morphology, neck width, and parent artery diameter, we decided whether to perform simple coil embolization or stent-assisted embolization and devised the most suitable surgical plan for the patient. If stent-assisted embolization was required, the stents used included the Enterprise stent (Codman Neurovascular, Raynham, MA, USA), a low-profile visualized intraluminal support (LVIS) device (MicroVention-Terumo, Aliso Viejo, CA, USA), and the Neuroform system (Stryker Neurovascular, Fremont, CA, USA). During the procedure, we used intraoperative angiography to confirm the immediate success of the surgery. Patients with aneurysmal SAH often present with acute hydrocephalus. For these patients, external ventricular drainage (EVD) was performed before or after aneurysm embolization if necessary based on symptoms, conditions, and CT results.

For all patients undergoing stent-assisted embolization, antiplatelet therapy was required. A loading dose of 300 mg aspirin and 300 mg clopidogrel was administered at least 2 hours before the procedure, either orally or via a nasogastric tube. Additionally, tirofiban was administered during the procedure as an alternative to preprocedural oral antiplatelet therapy. Tirofiban was given as an intravenous bolus (8 µg/kg) over a 3-minute period during stent placement, which was followed by a maintenance dose of 0.1 µg/kg/min for 24–48 hours postoperatively. Before discontinuation of tirofiban, a loading dose of 300 mg of aspirin and 300 mg of clopidogrel was administered orally or via a nasogastric tube, the tirofiban dose was halved, and tirofiban was eventually discontinued. Subsequently, 100 mg of aspirin and 75 mg of clopidogrel were administered daily for 3 months. After this period, patients were continued with 100 mg of aspirin alone for at least an additional 3 months, making the total duration of antiplatelet therapy more than 6 months. In contrast, patients who had simple coiling did not receive any antiplatelet therapy during or after the surgery.

Data collection

The baseline data of the patients included age, gender, clinical data [including Hunt-Hess grades and World Federation of Neurological Surgeons (WFNS) grades], procedure-related data, and aneurysm characteristics. In-hospital complications after surgery included hemorrhagic complications, ischemic complications, shunt-dependent hydrocephalus, and symptomatic vasospasm, among others, which could result in prolonged hospitalization. The assessment of in-hospital complications required consideration of the patient’s postoperative symptoms, signs, CT, magnetic resonance imaging, and DSA results. Symptomatic vasospasm was characterized by neurological deterioration, such as a decreased level of consciousness or the onset of new motor or language impairments, along with increased transcranial Doppler velocities and/or narrowing of major cerebral arteries as observed on CT angiography or magnetic resonance angiography (10). We classified complications by severity based on the following criteria: disabling stroke was defined by any of the following: (I) mRS score ≥3 or an increase in individual baseline mRS score by at least 1 category was defned as disabling stroke and (II) National Institutes of Health Stroke Scale (NIHSS) score ≥7 or a change in NIHSS of more than 4 points (11).

Clinical data were carefully gathered through neurological examinations and telephone interviews at specific intervals: 30 days postsurgery, 6 months, and then annually. We used the mRS to assess patients at discharge and at the final follow-up, with the mRS score at the final follow-up used as the patient’s clinical outcome.

Angiography follow-up assessments with DSA were scheduled at 6 months after the procedure until 1 year after the procedure. The grading scale for Raymond-Roy was as follows: class I, complete occlusion; class II, residual neck; and class III, residual aneurysm (12).

Statistical analysis

The Shapiro-Wilk test was performed to determine whether the data were normally distributed. For continuous variables, results are presented as either the mean ± standard deviation (SD) or as the median with interquartile range (IQR) depending on their distribution. The categorical variables are expressed as counts and percentages for clarity. Kaplan-Meier survival analysis was employed to estimate the cumulative survival rates without complications and the overall cumulative survival rates during the follow-up period. SPSS 27 software (IBM Corp., Armonk, NY, USA) was used to conduct statistical analyses.

Results

Baseline characteristics

This study included 49 patients who received endovascular treatment at our hospital, comprising a total of 53 ruptured distal aneurysms in the posterior circulation. Among these patients, there were 16 males (32.7%), and the mean age of all patients was 59.0±12.7 years. Nearly half (n=24, 49.0%) of the patients had a history of hypertension. One (2.0%) patient had a history of diabetes, 9 (18.4%) patients had coronary artery disease, 11 (22.4%) patients had a history of smoking, and 7 (14.3%) patients had a history of alcohol abuse. The median maximum diameter of all aneurysms was 4.6 mm (IQR, 3.0–7.0 mm). Regarding Hunt-Hess grades, 8.2% (4/49) of patients were grade 1, 55.1% (27/49) were grade 2, 22.4% (11/49) were grade 3, 10.2% (5/49) were grade 4, and 4.1% (2/49) were grade 5. In terms of WFNS grading, 29 (59.2%) patients were grade 1, 10 (20.4%) patients were grade 2, 2 patients (4.1%) patients were grade 3, 3 (6.1%) patients were grade 4, and 5 (10.2%) patients were grade 5. According to the modified Fisher grade, 17 (34.7%) patients were grade 1, 14 (28.6%) patients were grade 2, 3 (6.1%) patients were grade 3, and 15 (30.6%) patients were grade 4.

Regarding the location of the aneurysms, 6 (11.3%) aneurysms were in the P2 segment of the posterior cerebral artery, 1 (1.9%) was in the P3 segment, 14 (26.4%) were in the SCA, 10 (18.9%) were in the AICA, and 22 (41.5%) were in the PICA. Three patients (6.1%) had multiple aneurysms, all of which were distal aneurysms in the posterior circulation. Additionally, 31 (63.3%) patients had intraventricular hemorrhage. The details are shown in Table 1.

Procedure-related data

The procedure was successfully performed on all 49 patients, representing a 100% success rate. A total of 15 patients underwent stent-assisted embolization, totaling 17 stents. In one patient, two Neuroform Atlas stents were implanted simultaneously, and in another patient, one LVIS stent and one Enterprise stent were used. Among the stent-assisted embolization procedures, 13 used a single stent. Of these, 3 involved an Enterprise stent, 7 involved an LVIS stent, 1 involved a Neuroform Atlas stent, and 2 involved a Neuroform EZ stent. There were 34 patients who underwent simple coil embolization, accounting for 69.4% of all patients. The median number of coils used per aneurysm was 5.0 (IQR, 4.0–8.0). The median surgery time for all patients was 87.5 minutes (IQR, 63.8–106.3 minutes). A total of 4 patients (8.2%) underwent EVD. All patients received reconstructive endovascular treatment instead of parent artery sacrifice, and immediate postoperative angiography confirmed that all parent arteries were patent (Figure 2).

Figure 2 Example of reconstructive endovascular treatment in a patient with a ruptured distal left superior cerebellar artery aneurysm. (A) Preoperative DSA. (B) Preoperative head CT revealed subarachnoid hemorrhage. (C) Intraoperative coil embolization of the aneurysm. (D-F) Immediate postoperative angiography showed complete aneurysm embolization and patent parent artery.

In-hospital complications

A total of 16 (32.7%) patients experienced complications during hospitalization, among whom 5 (31.25%) had a disabling stroke. Six (12.2%) patients had hemorrhagic complications. Four patients had aneurysm rebleeding; three of these patients died during hospitalization, resulting in an in-hospital mortality rate of 6.1%. The remaining rebleeding patient underwent craniotomy for aneurysm clipping and had an mRS score of 3 at discharge. One patient experienced worsening headache on the first postoperative day. A following head CT showed a right frontal lobe hemorrhage, resulting in an mRS score of 1 at discharge. Another patient experienced a decline in consciousness on the first postoperative day. A following head CT showed left basal ganglia hemorrhage, resulting in an mRS score of 5 at discharge. A total of seven patients experienced ischemic complications, all occurring within 9 days postoperatively. Following head CT or diffusion-weighted imaging showed infarctions in the occipital lobe, cerebellum, or thalamus, manifesting as symptoms such as decreased consciousness, limb weakness, or numbness. One patient had both ischemic complications and shunt-dependent hydrocephalus and underwent lateral ventricle drainage on the second day after aneurysm embolization. This patient had a Hunt-Hess grade of 3 before procedure and an mRS score of 1 at discharge. Four patients developed shunt-dependent hydrocephalus, primarily presenting with impaired consciousness and limb weakness (Table 2). No patients experienced symptomatic vasospasm. The details of complications during hospitalization for patients after differentiation between simple coiling and stent-assisted cases are listed in Table 3.

Clinical outcomes

For all survivors, the clinical follow-up time ranged from 6 to 113 months, with a median follow-up time of 39 months (IQR, 21.0–70.5 months). During clinical follow-up, two patients developed new symptoms: one patient died 6 months postoperatively due to aneurysm rebleeding, and another patient experienced a cerebral infarction 2 years postoperatively, received conservative treatment, and had an mRS score of 0 at the last follow-up. The overall mortality rate of the patients was 8.2% (4/49). The details of the clinical outcomes are presented in Table 2. The 1-year complication-free survival rate for all patients was 69.4%, and the 1-year cumulative survival rate was 89.3%.

Angiography outcomes

Among the 46 surviving patients, 35 patients (with a total of 35 aneurysms) underwent angiographic follow-up, with a follow-up rate of 76.1% and a median follow-up time of 8.5 months (IQR, 6.0–12.0 months). The complete occlusion (Raymond-Roy grade 1) rate was 82.9% (29/35). During follow-up, four patients had a residual neck (Raymond-Roy grade 2) in their aneurysms, while two patients had a residual aneurysm, graded as Raymond-Roy grade 3 (Table 2).

Discussion

In this study, we retrospectively analyzed patients with ruptured DIAs of the posterior circulation who underwent endovascular treatment at our hospital. Sixteen (32.7%) patients experienced complications during hospitalization, with three patients dying, resulting in an in-hospital mortality rate of 6.1%. All surviving patients underwent clinical follow-up, with two developing new symptoms during the follow-up period. The total mortality rate was 8.2%. Imaging follow-up was conducted for 35 patients, with a follow-up rate of 76.1% and a complete occlusion rate of 82.9%.

For treating DIAs in the intracranial posterior circulation, there are two surgical options: open surgery and endovascular treatment. Due to the unique characteristics of posterior circulation aneurysms, such as their deeper anatomical location and proximity to important cranial nerves, craniotomy and clipping pose higher risks and operational difficulties (13). Regarding distal posterior circulation aneurysms, a meta-analysis by Petr et al. of 796 PICA aneurysms concluded that the long-term favorable neurological prognosis rate for the endovascular treatment group was 93.3%, which was higher than the 91.5% for the craniotomy group (14). Zhou et al. reported that for proximal PICA aneurysms, endovascular treatment could be the preferred option, as surgical exposure of these aneurysms is more challenging. Zhou et al. also analyzed 30 patients with ruptured intracranial distal aneurysms and found that endovascular treatment has significant advantages, such as being less invasive, technically safer, and offering better long-term outcomes (9). Based on the clinical experience of our center, endovascular intervention is preferred for most ruptured posterior circulation DIAs.

Intracranial distal aneurysms have unique anatomical features. Carter et al. found that their vascular walls are thinner, and the aneurysms are smaller and less stable compared to those formed in larger arteries (15). Additionally, the middle layer of the vascular wall in distal aneurysms lacks smooth muscle cells, resulting in weaker vascular elasticity and a higher likelihood of rupture. The p2-p3 segments of the PICA are the most common locations for distal posterior circulation aneurysms and have a higher rupture frequency compared to distal anterior circulation aneurysms (6,16). Cao et al. analyzed 90 ruptured DIAs and found that small aneurysms with a diameter of less than 4 mm accounted for 36.7% (33/90) of the ruptured aneurysms (8). In this study, PICA aneurysms had the highest proportion among all ruptured posterior circulation DIAs, reaching 41.5% (22/53). Additionally, there were 25 distal aneurysms with a diameter of less than 4 mm, accounting for 47.2% (25/53) of all posterior circulation DIAs, which is higher than the proportion of DIAs reported in previous studies (8).

Previous studies have shown that the rupture of DIAs not only causes SAH but also results in intracerebral hemorrhage in more than half of the cases, leading to worse outcomes compared to aneurysms in other locations (17,18). Moreover, in another study, a higher proportion (36.6%) of patients with ruptured DIAs were classified as WFNS grade IV–V (8). In our study, 31 patients with ruptured DIAs had concomitant intraventricular hemorrhage, accounting for 63.3%. Additionally, 8 patients were classified as WFNS grade IV–V, representing 16.3%, which is lower than the proportion reported in previous studies (8).

Endovascular treatment-related complications of posterior circulation DIAs are relatively common. This may be due to the DIAs’ distant location, morphology, anatomical variations, and the higher technical difficulty of the procedure (17). Compared to aneurysms in other common locations, DIAs have a higher rate of procedure-related complications (19). Liang et al. analyzed 99 patients with posterior circulation aneurysms who underwent endovascular treatment, finding a complication rate of 17.2% (20). In our study, 16 (32.7%) patients experienced complications during hospitalization, which is higher than the complication rate for endovascular treatment of ruptured posterior circulation aneurysms (29.4%), consistent with the conclusions of previous studies (21).

Ischemic complications are the most common complications during hospital stays. Zhao et al. examined patients with ruptured aneurysms who received endovascular treatment and found that 12.2% of them experienced ischemic complications (22). In our study, we observed an incidence of ischemic complications at 14.3%, which was higher than that reported in previous findings (8). This might occur because small blood vessels get blocked off during coil embolization or when stents are placed. In cases where patients receive stent-assisted embolization, their resistance to antiplatelet drugs could also contribute to ischemic problems after surgery. Liang et al. investigated 99 patients with large aneurysms in posterior circulation who were treated with endovascular methods and found that 3.4% of them had hemorrhagic events, with 1.9% experiencing SAH during the periprocedural period (20). In our study, we observed hemorrhagic complications in 12.2% of cases, with 8.2% of them having a rebleeding episode, indicating a higher rate of bleeding problems compared to large-vessel aneurysms in posterior circulation. This could be because aneurysms in this area are more distant, making it harder to access the blood vessels and complete the procedure effectively.

Zhong et al. examined 111 patients who had basilar artery trunk aneurysms and received endovascular treatment. Among them, 92 (82.9%) patients showed favorable clinical outcomes, with a score of 0–2 on the mRS at their last follow-up (23). Zhou et al. studied 30 patients with ruptured aneurysms in distant locations, with 89.3% of the patients having an mRS score of 0–2 during clinical follow-up (9). In our study, we found that 85.7% of patients had an mRS score of 0–2 at their last follow-up, which matches findings from previous studies.

In a previous study employing angiography follow-up, a total of 151 cases of DIAs were examined, among whom 136 (90.1%) were rated as Raymond-Roy grade 1–2 (8). For cases involving ruptured aneurysms, the likelihood of recanalization following endovascular treatment tends to be higher. This could be due to the increased activity within the vessel wall following rupture, resulting in more dynamic lesions (24,25). In our study, 35 patients who survived underwent angiographic follow-up, resulting in a follow-up rate of 76.1% (35 out of 46 patients). Among these patients, 94.3% were classified as Raymond-Roy grade 1–2. The main reasons for remnants at the neck of the aneurysm or recurrence of the aneurysm may include the following: (I) difficulty in densely packing small aneurysms, leading to remnants at the neck; (II) numerous DIAs with wide necks, making coil embolization challenging due to the small diameter of the parent artery and thus complicating stent-assisted embolization; and (III) dissecting aneurysms being more prevalent in DIAs, with the parent artery lacking typical vascular wall components, increasing the risk of intraoperative rupture and recurrence after hemodynamic impact (9). Advancements in technology have led to the development of more flexible and adaptable devices in clinical settings, such as softer coils and microcatheters specifically designed for operations in distal vessels. These advancements are expected to enhance the effectiveness of endovascular treatment for DIAs in the future.

This study involved several limitations which should be addressed. First, as we employed a retrospective, single-center design with a relatively small sample size, bias was unavoidable. Additionally, important treatment methods such as glue injection and parent artery sacrifice were not included in this study. Furthermore, the angiographic follow-up rate was only 76.1%, with a significant rate of loss to follow-up, which might have affected the analysis of angiographic outcomes. Therefore, future studies should involve multiple centers with larger sample sizes and higher follow-up rates.

Conclusions

This study observed a relatively high incidence of complications during patients’ hospital stays and follow-up. However, the clinical follow-up results were satisfactory, and the imaging follow-up showed a high and satisfactory rate of aneurysm occlusion. In summary, endovascular treatment of ruptured DIAs in the posterior circulation appears to be feasible, safe, and effective, although attention should still be paid to the occurrence of related complications.

Acknowledgments

Funding: This study was sponsored by the National Natural Science Foundation of China (No. 82071309) and the Postgraduate Research & Practice Innovation Program of Harbin Medical University (No. YJSCX2023-204HYD).

Footnote

Reporting Checklist: The authors have completed the STROCSS reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1147/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1147/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The Ethics Committee of First Affiliated Hospital of Harbin Medical University approved this study (No. 202496). Written informed consent was obtained from all patients. The study also complied with the principles of the Declaration of Helsinki (as revised in 2013).

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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