INTRODUCTION
Despite advances in endovascular and microsurgical techniques, blood blister-like aneurysms (BBAs) frequently present a tremendous therapeutic challenge due to their unfavorable morphology and histology [
9,
15]. Although the efficacy of microsurgical treatment of BBA has been demonstrated, the endovascular intervention has gradually become the preferred alternative for BBA treatment, owing to its lower complication rate and better prognosis [
10,
13,
14,
17]. Numerous interventional techniques in the treatment of BBA, including stenting with or without coiling, endovascular trapping, and a combination of other procedures, have been suggested to treat BBAs, but a standard protocol has not yet been established [
12,
17]. Recently, more reports have focused on the invention of the flow diverter (FD) for BBA treatment [
14,
21]. However, the flow diverters also have critical issues of a low initial occlusion rate and early rebleeding [
21]. In our country, FD is currently allowed for limited indications. FD is not allowed for treating ruptured aneurysms.
In the present series, to achieve complete aneurysm exclusion and parent artery preservation, we attempted to treat ruptured BBAs with double stent-assisted coiling (SAC) using Neuroform Atlas stents (NASs) (Stryker Neurovascular, Kalamazoo, MI, USA). Our aim was to evaluate the efficacy of double SAC using NASs for the endovascular reconstructive treatment of ruptured BBAs by reviewing patients’ clinical and radiological data.
DISCUSSION
The present study demonstrates that Double SAC with NASs is a feasible and effective approach for treating ruptured BBAs of the supraclinoid ICA. Despite the small sample size, our findings indicate that this endovascular technique offers favorable angiographic and clinical outcomes with a relatively low rate of symptomatic complications.
BBAs are fragile, thin-walled aneurysms that pose significant treatment challenges due to their rapid morphological changes and high risk of rebleeding [
9,
15]. While microsurgical clipping has traditionally been used, endovascular treatment has gained popularity due to its less invasive nature. Several endovascular techniques have been proposed for BBA treatment, including simple coiling, SAC, flow diversion, and vessel occlusion [
10,
12,
13,
17]. However, each technique has its limitations. Simple coiling is often inadequate due to the wide-necked or nonexistent neck of BBAs. SAC provides a scaffold for coil embolization while preserving the parent artery. In this study, double SAC with NASs was employed to enhance the stability of the coil mass and promote aneurysm occlusion. The overlapping stents provide additional support to the fragile aneurysm wall and promote endothelialization. To treat ruptured BBAs in the acute stage, it is critical to block blood flow from the affected wall to prevent rebleeding and regrowth. Stent porosity is strongly correlated with hemodynamic changes, and an animal study confirmed that a higher metal coverage rate is positively associated with improved angiographic and clinical outcomes [
13]. Overlapping stents may divert more blood flow from the affected segment than a single stent by decreasing stent porosity, further straightening the parent vessel, and increasing stent thickness. Greater strut density and thickness facilitate neointima formation [
8]. Therefore, multiple stents not only provide immediate protection against hemorrhage by redirecting flow, disrupting intra-aneurysmal circulation, and dispersing the inflow jet, but also enhance angiographic outcomes and improve the long-term durability of coils by promoting further stent endothelialization and intravascular remodeling [
5]. A proportion meta-analysis compared angiographic outcomes between single and multiple SACs in BBA treatment [
12]. The study found that the complete occlusion rate was higher in the group with two or more stents (80.39%) compared to the single stent group (48.10%). Additionally, the recurrence rate was lower in the multiple stents group (14.29%) than in the single stent group (25.32%). These findings suggest that using multiple stents in SAC may lead to better angiographic outcomes. Several studies have investigated the use of multiple (three or more) overlapping stents combined with coiling for treating ruptured BBAs [
10,
18]. These studies suggest that multiple overlapping stents with coiling can be a feasible alternative for treating ruptured BBAs. Although overlapping stents may modify intra-aneurysmal flow by reducing overall porosity, we acknowledge that NASs are not designed as flow diverters and do not replicate the flow-diverting characteristics of dedicated FD devices. In this study, the suggestion of hemodynamic benefit remains hypothetical and is not supported by computational fluid dynamics or direct hemodynamic measurements. Therefore, any potential flow-disrupting effect should be interpreted with caution.
FD devices have emerged as a significant advancement in the endovascular treatment of intracranial aneurysms, including BBAs. Their unique mechanism focuses on reconstructing the parent artery and promoting aneurysm thrombosis by diverting blood flow away from the aneurysm sac. FDs have demonstrated substantial efficacy in achieving complete aneurysm occlusion. In a study involving 30 patients with ruptured BBAs treated with the Flow-Redirection Endoluminal Device (FRED), complete obliteration was achieved in 80% of patients at six months and 92% at a median follow-up of 22 months [
2,
14]. The structural design of FDs contributes to the long-term stability of aneurysm occlusion, reducing the likelihood of recanalization. A meta-analysis reported a complete occlusion rate of 72% for BBAs treated with FDs, indicating durable outcomes [
21]. However, the use of FDs is associated with certain risks. In the aforementioned study with the FRED device, major stroke or death occurred in 17% of patients [
14,
21]. Immediate complete occlusion is not always achieved with FDs. In the same study, only 33% of patients had immediate complete aneurysm obliteration post-procedure, with others requiring extended periods to reach full occlusion [
14]. Patients undergoing FD treatment need prolonged dual antiplatelet therapy to prevent thromboembolic events, which can complicate management, especially in cases of ruptured aneurysms where there is a risk of hemorrhagic complications. Therefore, further studies are needed to evaluate the safety and effectiveness of FD treatment for BBAs. A proportion meta-analysis compared SAC with FD in managing BBAs. The long-term complete occlusion rate was higher in the FD group (89.26%) than in the SAC group (70.26%). Additionally, the aneurysm recanalization rate was lower in the FD group (4.54%) versus the SAC group (25.38%). However, rates of mortality, favorable functional outcomes, procedural complications, and rebleeding showed no significant differences between the two procedures. These results indicate that while FD may offer more favorable angiographic outcomes, SAC remains a viable option, especially when considering individual patient factors [
12]. In our country, the use of FD is not currently permitted for ruptured aneurysms, including BBAs, but is allowed for BBAs that recur after the acute phase. Therefore, in accordance with current insurance policies, we prioritize double SAC for ruptured BBAs and apply FD treatment for BBAs that recur during follow-up after the acute phase. In this study, using double SAC with easy-to-handle NASs, coils could be safely placed using the jailing technique and/or semi-jailing technique or through a stent strut within the fragile aneurysm wall. As a result, no reruptures of BBAs occurred during or after the procedure. Additionally, the deployment of NASs was technically easier than that of FDs, allowing for more accurate stent placement at the intended location.
In this study, we exclusively used NASs due to their superior deliverability and procedural flexibility, especially in the tortuous anatomy of ruptured BBAs. Compared to LVIS (Low-profile Visualized Intraluminal Support) stents, which require a larger microcatheter and limit coiling techniques, NASs allow for easier navigation and enable coiling through the stent struts or via semi-jailing. Although LVIS is available for use in ruptured aneurysms in our country, our institutional preference for NASs reflects their practical advantages in achieving safe and effective double SAC, despite the limitation of being non-retrievable once partially deployed.
Based on our experience, double SAC using NASs is particularly suitable in the following indications: (1) ruptured BBAs at the non-branching site of the supraclinoid ICA, (2) wide-neck morphology with shallow sac depth, (3) poor response to conventional SAC or coil instability after initial embolization, and (4) contraindications to FD due to local regulations or bleeding risks.
Periprocedural complication rates in our study were comparable to or lower than those reported for other endovascular techniques. Asymptomatic in-stent thrombosis occurred in 40% of cases, but all were successfully managed with intra-arterial thrombolysis without clinical deterioration. Only one patient (10%) experienced symptomatic thromboembolic events, which occurred seven days after the procedure and improved significantly over time. Prior SAC series have indicated that thromboembolism rates are approximately 4-8% [
4,
6]. In a series of 19 cases of Y-SAC reported by Spiotta and colleagues, intraprocedural thromboembolism occurred in 3 cases (16%), while delayed thromboembolism was observed in 2 cases (11%) [
19]. They reported that the Y-stent design, which involved two overlapping stents in the distal basilar artery—one telescoped over the other—along with additional intraluminal “hardware” (stent overlap), was less amenable to endothelialization without the scaffolding provided by adjacent intima. However, overlapping stenting in a telescoping fashion, as used in this study, does not interfere with the main blood flow, unlike Y- or X-stenting in a crossing fashion. Thus, the risk of thromboembolism is expected to be lower. The author of the present study previously proposed endovascular reconstruction using a filland-tunnel technique, a type of multiple overlapping stenting, for fusiform vertebral artery dissecting aneurysms with ipsilateral dominance, reporting excellent outcomes [
11]. Additionally, he documented 23 cases of rescue stenting with NASs during stent-assisted coiling of saccular aneurysms, demonstrating favorable clinical and angiographic outcomes [
3]. No intraoperative ruptures or periprocedural rebleeding events were observed, highlighting the technical safety of the procedure when performed under careful anticoagulation management. All but two patients with poor-grade SAH achieved favorable clinical outcomes (mRS 0-1) at a mean follow-up of 41.0 months, indicating that double SAC with NASs can lead to good long-term functional results. Our study showed a high rate of technical success with double SAC using NASs. Immediate angiographic results demonstrated complete occlusion in 60% of aneurysms, with progressive occlusion observed during follow-up. The use of double SAC with NASs allowed for both immediate aneurysm protection and vessel reconstruction. Additionally, stent overlap reinforced the aneurysm neck, promoting long-term occlusion and parent artery preservation. Our results showed a high rate of complete aneurysm occlusion at follow-up, with only one patient requiring retreatment with FD due to recurrence. These findings align with previous reports suggesting that NASs, with their open-cell design and improved conformability, contribute to enhanced vessel wall reconstruction and aneurysm stability [
7]. Although various types of stents have been used in previous studies on BBA treatment, the present study is notable for achieving favorable treatment outcomes using only two NASs within a consistent treatment strategy, despite its retrospective design.
Thromboembolic complications are a significant concern in SAC for the treatment of SAH. Managing these complications and determining the optimal antiplatelet therapy to prevent them are key considerations in treating patients with ruptured intracranial aneurysms. The use of antiplatelet therapy in SAH patients undergoing SAC must balance the risk of thromboembolic events with the potential for bleeding complications. A DELPHI consensus among neurointerventional experts suggests a periprocedural dual-antiplatelet regimen, typically involving intravenous aspirin and a glycoprotein IIb/IIIa inhibitor, followed by a transition to oral antiplatelet agents within 24 hours post-procedure [
16]. This approach aims to mitigate the risks associated with antiplatelet therapy in the acute setting of SAH. Multiple SAC carries a higher risk of thromboembolic complications compared to single SAC; however, this difference may be mitigated when adjusting for aneurysm characteristics. Despite the higher complication rates, the overall morbidity and mortality associated with SAC for ruptured aneurysms may be lower than expected [
1,
20]. While multiple SAC for ruptured aneurysms presents inherent risks, appropriate antiplatelet management can help reduce thromboembolic complications. The optimal antiplatelet regimen remains an active area of research, with recent evidence suggesting that shorter dual antiplatelet treatment durations may be sufficient in some cases.
We fully acknowledge the limitations of our small sample size. With only ten cases included, this study lacks sufficient statistical power to draw definitive conclusions regarding complication rates or treatment efficacy. As such, we present our findings as preliminary and observational, emphasizing the need for larger, multicenter prospective studies to validate our treatment strategy.