
==== Front
Brain Spine
Brain Spine
Brain & Spine
2772-5294
Elsevier

S2772-5294(24)00586-1
10.1016/j.bas.2024.103330
103330
Brain
An overview of decision-making in cerebrovascular treatment strategies: Part II - Ruptured aneurysms
Versyck Georges georges.versyck@uzleuven.be
a⁎
van Loon Johannes ad
Lemmens Robin bd
Demeestere Jelle bd
Bonne Lawrence cd
Peluso Jo P. cd
De Vleeschouwer Steven ad
a Department of Neurosurgery, University Hospitals Leuven, Leuven, Belgium
b Department of Neurology, University Hospitals Leuven, Leuven, Belgium
c Department of Interventional Radiology, University Hospitals Leuven, Leuven, Belgium
d Neuro-vascular Unit, University Hospitals Leuven, Leuven Brain Institute (LBI), Belgium
⁎ Corresponding author. Herestraat 49, 3000, Leuven, Belgium. georges.versyck@uzleuven.be
06 9 2024
2024
06 9 2024
4 10333024 6 2024
28 8 2024
4 9 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction

Decision-making for the treatment of ruptured aneurysms is an intricate process, which involves several factors. There has been a rapid advancement in endovascular, but also in the surgical treating field of ruptured intracranial aneurysms, with a growing body of evidence for either treatment technique.

Research question

As there is a wide variety of treatment possibilities, it can be hard to understand the intricacies which lie behind the decision-making process for a given aneurysm.

Materials and methods

An overview of the most relevant literature in decision-making on ruptured intracranial aneurysms is given.

Results

Different decision-altering factors were identified, which can be divided into information from the general evidence, to influential factors such as the patient's age, initial presenting status, and aneurysmal factors such as size, morphology and aneurysmal location.

Discussion and conclusion

This review provides an evidence-based overview of the most pertinent literature on these different aspects of decision-making in ruptured aneurysm cases and provides some recommendations after each of these segments. As always, all different aspects of the patient and aneurysmal factors should be taken into consideration before coming to a conclusion, as to obtain the best possible result for an individual patient.

Highlights

• Coiling is preferred for ruptured aneurysms when an equipoise exists.

• Ruptured WNA have similar outcomes after clipping and endovascular treatment.

• Ruptured posterior circulation aneurysms are best treated endovascularly.

• Controversy exists among the best treatment modality for ruptured MCA aneurysms.

Keywords

Ruptured intracranial aneurysm
Subarachnoid hemorrhage
Decision-making
Endovascular therapy
Microsurgical clipping
==== Body
pmcAbbreviations

ICA internal carotid artery

mRS modified Rankin Scale

GOS Glasgow Outcome Scale

RROC Raymond-Roy occlusion classification

RCT Randomized controlled trial

ISAT international subarachnoid aneurysm trial

BRAT Barrow ruptured aneurysm trial

SAH subarachnoid hemorrhage

ET endovascular therapy

PComm posterior communicating artery

MCA middle cerebral artery

WFNS world federation of neurological surgeons

HH Hunt and Hess

AComm anterior communicating artery

WNA Wide-neck aneurysm

BAC balloon-assisted coiling

SAC stent-assisted coiling

FD flow diverter

WEB Woven EndoBridge

DAPT Dual antiplatelet therapy

DACA distal anterior cerebral artery

PICA posterior inferior cerebellar artery

OphA carotid-ophthalmic artery

SR systematic review

RS retrospective study

PS prospective study

1 Introduction

Intracranial aneurysm treatment dates back from 1885, when Horsley performed a bilateral cervical carotid artery occlusion for an internal carotid artery (ICA) aneurysm. Over the years, management of intracranial aneurysms changed substantially with the introduction of clipping and the widespread use of the operating microscope in the 1960's (Lai and O'Neill, 2017; Dandy, 1938). Similarly, in the early 1990's, endovascular treatment with Guglielmi detachable coils was introduced in the treatment of aneurysms (Guglielmi et al., 1991). Over time, adjunctive measures such as balloon- and stent-assisted coiling were implemented, and more recently intravascular- and intrasaccular flow divertors, as well as neck-bridging devices were introduced to aid in treating more complex aneurysms and achieving better aneurysm occlusions (Lee et al., 2022).

This abundance of choice, variability in treatment experience and the large variety of aneurysm presentations, shapes, locations, and sizes, results in therapeutic heterogeneity and large variability in decision making. This was found in a study on ruptured intracranial aneurysms, where there was only a 17.5% agreement between the different specialties regarding their preferred treatment modality (Darsaut et al., 2019a).

Generally, the decision-making process for a suitable treatment modality for a particular aneurysm, comes down deciding on different patient- and aneurysm-related factors:- Patient related factors mainly include information coming from general evidence, the patient's age, as well as the initial clinical presentation status which might affect the decision.

- Aneurysm-related factors consist of aneurysm size, morphology (wide-neck aneurysms) and aneurysm location.

In this paper, an overview of the most relevant literature will be provided concerning the different factors which guide decision-making in ruptured saccular aneurysm treatment.

2 Aims and methods

This paper aims to provide an overview of the literature that shapes clinical decision-making in the treatment of saccular aneurysms. By critically evaluating and synthesizing the most relevant research, this review intends to create a framework to guide treatment decisions in clinical practice. The review is structured into two main sections: Part I covers unruptured aneurysms, while Part II focuses on ruptured aneurysms.

To build this framework, studies were selected that have made significant contributions to the understanding of intracranial aneurysm management in a real-world setting. These sources include landmark studies, clinical guidelines, expert consensus reports, and influential trials. The selection was driven by the need to highlight the key evidence that clinicians rely on for decision-making.

It is important to approach recent cohort studies with caution, as many centers currently favor an endovascular-first strategy for treating aneurysms. This shift often results in more complex cases being designated to surgical clipping, inherently increasing the risk of complications in these cases. The goal of this overview is not to provide treatment indications, but rather provide evidence when the decision to treat a given ruptured aneurysm is already taken.

In Part II, we concentrate on the unique challenges presented by ruptured intracranial aneurysms. This section emphasizes the critical factors that must be considered when determining treatment strategies. Through this review, we aim to provide clinicians with clear, evidence-based guidance tailored to the complexities of managing ruptured aneurysms.

3 Outcome parameters

The desired goal of aneurysm treatment comes down to having a safe and effective treatment.

The safety of a treatment is often summarized in the clinical outcome of the patient. This is measured by the modified Rankin Scale (mRS) or the Glasgow Outcome Scale (GOS). The mRS is often dichotomized into scores 0–2 and 3–6, where the latter delineates death or dependency. Similar divisions exist for the GOS, where a score of 1–3 indicates death or dependency, and 4–5 indicates a good clinical outcome (Gaastra et al., 2022). New neurological deficits or complications are often missed in the classic mRS- and GOS-grading systems but can lead to debilitating daily complaints. When specific data on this topic is unavailable, it is frequently summarized in a “morbidity” parameter.

Treatment efficacy is mostly assessed by preventing rebleeding. This is often correlated with the degree of aneurysm occlusion achieved by the index treatment. In endovascular cohorts, this is scored on the (modified) Raymond-Roy occlusion classification (RROC), delineating between a complete occlusion (grade 1), residual neck filling (without filling of the aneurysmal sack) as a grade 2, and any filling inside the aneurysm sack as a grade 3 occlusion. Grades 1 and 2 are often combined as an adequate occlusion (Pierot et al., 2020; Darsaut et al., 2023). The occlusion-status after microsurgical clipping is often scored in a similar manner. Even after successful initial treatment, a recanalization or regrowth of the aneurysm is possible, with a new risk of a recurrent bleeding. After significant recanalization (RROC 3) during follow-up, the decision for retreatment is taken, but a retreatment comes with new risks for procedural complications (Metayer et al., 2021).

4 Patient-related factors influencing decision-making

4.1 Best available general evidence

The first randomized controlled trial (RCT) comparing coiling and microsurgical clipping for ruptured aneurysms was performed in Helsinki, where at 1 year follow-up, no major differences in outcome were noted (Koivisto et al., 2000). The International Subarachnoid Aneurysm Trial (ISAT), the largest RCT comparing coiling and clipping to date, included 2143 patients (9559 patients screened) with ruptured aneurysms where both treatment modalities were deemed suitable. The study reported a better clinical outcome after coiling, as shown by an mRS of 0–2 in 76.3% of coiled patients compared to 69.4% for clipping after 1 year (Molyneux et al., 2002). Later iterations of ISAT did show that clipping was associated with better angiographic outcomes (82% vs 66% complete occlusion at one year) and fewer retreatments (3.8% vs 17.4% after 20 months) (Molyneux et al., 2005; Campi et al., 2007). The Barrow Ruptured Aneurysm Trial (BRAT), which included 500 patients with a subarachnoid hemorrhage (SAH), showed similar results concerning mRS and retreatment rates (McDougall et al., 2012). After longer follow-up intervals however, the mRS-advantage of coil-embolization was lost in both BRAT and ISAT (Spetzler et al., 2020; Molyneux et al., 2015).

A Cochrane systematic review comparing clipping and coiling for ruptured aneurysms from 2018 included 2458 aneurysms across 4 RCT's (ISAT being the largest study) and showed similar results with functional outcomes in favor of coiling and angiographic outcomes in favor of clipping (Lindgren et al., 2018). A more recent systematic review from 2022 with 7391 patients from 28 studies, (including prospective studies), revealed similar outcomes, with lower rebleeding rates for clipped patients (Zhu et al., 2022), an overview is presented in Table 1.Table 1 Overview of patient- and aneurysm related factors influencing treatment decisions in ruptured aneurysms. Abbreviations: RCT: randomized controlled trial, SR: systematic review, RS: retrospective study, PS: prospective study.

Table 1Ruptured aneurysms	Favors endovascular	No significant difference	Favors microsurgical	Most relevant evidence	Type of study	
General evidence	mRS	Long term mRS	Occlusion	Molyneux et al., 2002	RCT	
Retreatment	McDougall et al., 2012	RCT	
Rebleeding	Lindgren et al., 2018	SR	
Elderly population	mRS for ICA/PComm aneurysms	mRS Barthel index
Mortality Rebleeding/retreatment	mRS for ACM aneurysms	Molyneux et al., 2002	RCT	
McDougall et al., 2012	RCT	
Proust et al., 2018	RCT	
Bekelis et al., 2016	RS	
Dawod et al., 2020	Meta-analysis	
Young population	mRS/GOS		mRS	Dawod et al., 2020	SR	
Mitchell et al., 2008	RCT-based	
Poor clinical presentation		mRS Complications	Lower mortality	Xia et al., 2017	SR	
Small aneurysms		mRS Complications		Li et al., 2017	RS	
Zhao et al., 2019	RS	
Large/giant aneurysms	Complications	mRS Mortality	Recanalization	Dengler et al., 2016	SR	
Santoro et al., 2022	RS	
WNA		mRS Complications Occlusion	Retreatment	Mascitelli et al., 2019	RCT	
Fiorella et al., 2017	SR	
Mascitelli et al., 2021	PS	

Ever since the publication of ISAT, endovascular therapy (ET) has become the preferred treatment modality for ruptured intracranial aneurysms that are deemed treatable by surgical and endovascular therapy. The reasons for this advantage of coiling are pondered to be due to the “angry brain” encountered during microsurgery, with brain edema and need for increased retraction, causing additional damage to an already fragile brain (Golnari et al., 2020).

Many aneurysms however, do not fit the ISAT-cohort (small anterior circulation aneurysms), and therefore uncertainty regarding treatment of these “non-ISAT” aneurysms remains. Since the publication of ISAT, new endovascular techniques have been introduced, but to this date no randomized evidence exists to compare them to clipping. To study this, ISAT-2 was initiated in 2012, including both non-ISAT aneurysms and novel endovascular methods. An interim-analysis in 2019 however did not show any differences (Darsaut et al., 2019b). A score was devised for the selection of treatment modality for ruptured aneurysms in 2021, based on the Japanese stroke database with 3547 patients. This score has 6 prognostic factors to predict poor mRS-outcome at discharge and in-hospital mortality for both treatment modalities. The model was validated on an external Japanese dataset, but care should be taken not to generalize this model, as it is based on an exclusively Japanese population and advanced anatomical factors are lacking (Yoshiyama et al., 2021).In conclusion, general clinical evidence shows that, compared to clipping, coiling for ruptured aneurysms results in better clinical outcomes at one year, but worse angiographical results, with a higher rebleeding and retreatment-rate compared to clipping when a clinical equipoise exists. At longer follow-up intervals, the difference in clinical outcome for both treatment modalities disappears.

4.2 Age

As individuals age, vascular changes and the presence of multiple comorbidities as well as general frailty can complicate both endovascular therapy (ET) and surgical clipping of aneurysms. Tortuous blood vessels and atherosclerotic plaques can make endovascular access more challenging and elevate the risk of thromboembolic complications. Similarly, surgical clipping becomes more difficult and riskier when dealing with atherosclerotic aneurysms due to the increased complexity in securing the clip effectively (Willinsky et al., 2003; Hamouda et al., 2024; Yue et al., 2016). The 2012 European Stroke Organization guidelines recommend the use of ET in patients with advanced age, as long-term durability of the treatment is of less importance (Steiner et al., 2013). The newer American Heart Association guidelines from 2023 however, give no preference for either treatment modality in older patients (Hoh et al., 2023).

Evidence for older patients remains scarce, with only a few publications available. A French RCT compared ET and clipping in 41 patients >70 years old, but showed no difference in mRS- outcome, as can be expected in this underpowered study (Proust et al., 2018). Subgroup analysis of patients aged ≥65 years old in ISAT failed to show any benefit of ET compared to clipping. The only exception was seen when ET was used for older patients with ICA and posterior communicating artery (PComm) aneurysms and in clipping for middle cerebral artery (MCA) aneurysms. The complication risk and presence of delayed neurological deficits were similar in both groups (Catapano et al., 2021). A subgroup-analysis of the elderly population in the BRAT-cohort also failed to show any difference in functional independence one year after treatment (Catapano et al., 2021). Similarly, a retrospective analysis of 3210 Medicare patients, aged ≥65 years, showed no difference in mortality and readmission rates between both treatment modalities (Bekelis et al., 2016). A systematic review of 13 cohort studies including 7137 patients that compared ET and clipping in an older patient cohort (>54 years old) showed no difference between ET and clipping with regards to functional outcome (63% vs 64%) and treatment efficacy (rebleeding and re-treatment) (Dawod et al., 2020).

Younger patients could potentially benefit more from a surgical approach, considering the lower retreatment-rates and smaller risk of rebleeding after microsurgery (Mitchell et al., 2008), but data from the aforementioned systematic review showed better functional outcomes for the ET-group in younger patients (77% vs 69% good neurological outcome) (Dawod et al., 2020). A post-hoc study on the ISAT-data found that there was no difference in mortality for patients aged <40 years who had ET or clipping, and that for these patients a theoretical advantage for clipping exists due to the better long-term protection from SAH (Mitchell et al., 2008).Decision-making for both elderly and young patients remains difficult, as there are no pre- specified age-groups or clear cut-off values for age-related outcomes. Most evidence on this matter comes either from small studies, or from subgroup analyses, rendering any conclusions difficult.

4.3 Clinical presentation

The clinical severity of a SAH is classified with the World Federation of Neurological Surgeons (WFNS) or Hunt and Hess (HH) grades at presentation, where a higher grade is indicative of a worse prognosis. A WFNS- or HH-grade of 4–5 is regarded as a poor-grade SAH, and this accounts for 20–30% of patients. Half of the patients with a poor-grade SAH will have a poor mRS-outcome (Zhao et al., 2016). A systematic review with 3 RCT's and 16 cohort studies included 1416 patients with a poor-grade SAH. This review did not show any difference in good outcome (34.3% vs 43.5%) or rebleeding (13.6% vs 10.2%) between coiling and clipping, but the coiled group did have a higher mortality rate (34.2% vs 21.5%) (Xia et al., 2017). In these poor-grade SAH patients, factors such as clinical herniation signs and presence of a space-occupying hematoma, as well as age, will also affect clinical outcome, apart from the initial presentation (Schuss et al., 2016; Liu et al., 2020).There is currently insufficient evidence to decide on the preferred treatment modality based on the initial clinical status alone, and other factors should be included in the decision-making process for poor-grade SAH patients.

5 Aneurysm-related factors

5.1 Size

Small aneurysms (≤3 mm) are challenging for both ET and clipping (endovascular navigation, coil prolapse, insufficient tissue for clip placement, …). There are only two studies which compared ET and clipping for small aneurysms. One study entails a variety of aneurysms, and the other is a cohort of small anterior communicating artery aneurysms (AComm). They both reported no differences in functional outcome (84.9% vs 80% good mRS-outcome) or complication rates (Li et al., 2017; Zhao et al., 2019).Given the paucity of data on this subject, no conclusions can be made on the best treatment of ruptured small aneurysms.

Large and giant aneurysms (>10 mm and >25 mm respectively) pose different challenges compared to the smaller aneurysms. They often require adjunct endovascular therapies such as stenting or flow diversion to provide a stable scaffold for subsequent coiling and require more complex clip reconstructions and/or bypass surgery.

CLARITY was a prospective study on complications of ET (mainly coiling) in ruptured aneurysms with 782 patients, which showed significantly more thrombo-embolic events when the aneurysm dome was >10 mm (Pierot et al., 2010). A different study by Zhang et al., found that aneurysms >10 mm also had an increased risk of recanalization after ET (Zhang et al., 2018). The giant intracranial aneurysm study group published results from prospective and retrospective cohorts with 581 giant aneurysms, where no differences in mortality between clipping and ET were seen (Dengler et al., 2016). An Italian retrospective study with 162 patients also found no differences in mortality or functional outcomes between clipping and ET, but did show more complications and less recanalization in the surgical group (Santoro et al., 2022).Large and giant aneurysms are a separate entity and remain difficult to treat for both ET and clipping, other factor such as aneurysm morphology and location, as well as calcification-status will play an important role in the selection of the preferred treatment modality.

5.2 Wide-neck aneurysms

Aneurysms with a neck-width of ≥4 mm or a dome-neck ratio <2 are classified as wide-neck aneurysms (WNA). Wide-neck aneurysms often require more complex clip reconstructions and endovascular adjuncts such as stents or flow-diverters to prevent coil protrusion in the parent vessel (Hendricks et al., 2020).

In BRAT, functional outcomes were similar after ET versus clipping in WNA, with poor outcomes in 35% of patients. Microsurgical clipping did display better angiographic outcomes (84% vs 51% complete occlusion) and lower retreatment rates (0% vs 26%) compared to ET. However, these results should be interpreted with caution, as advanced endovascular methods were not widely used yet during BRAT (Mascitelli et al., 2019; Fiorella et al., 2017).

A systematic review on WNA revealed occlusion-rates of 52.5% and 39.8% for clipping and ET respectively, and safety events at one year follow-up were noted in 24.3% and 21.1% (Hendricks et al., 2020). Following these findings, the prospective EVERRUN-registry was set up with a propensity-score analysis to compare clipping and ET. Functional outcomes, complication rates and final angiographic outcomes were all similar between both modalities, but there were more retreatments in the endovascular group (0% vs 12.7%) (Mascitelli et al., 2021).

Given the lower occlusion-rates of coiling and balloon-assisted coiling (BAC), stent-assisted coiling (SAC) was developed to provide an intravascular scaffold and achieve more durable endovascular results. A meta-analysis comparing SAC and non-SAC found that the use of a stent gave a higher complete occlusion rate (73.4% vs 61%) and fewer recurrences (4.8% vs 16.6%) (Zhang et al., 2019). The general complication-rate of SAC is estimated to be around 20.8%, with 9% experiencing thrombo-embolic complications (Bsat et al., 2020). Given the lack of prospective studies on this topic, the SAVE-registry was set up to evaluate SAC outcomes, but to date, a direct comparison between SAC and clipping is lacking (Li et al., 2022).

Flow diverters (FD) provide an alternative to SAC, as they provide additional flow modulation away from the aneurysm neck. Concerning ruptured saccular aneurysms, adequate occlusion was achieved in 79%, although this came at the cost of a 23% complication-rate, as thrombo-embolic and hemorrhagic complications occurred in 9.9% and 12% of patients. The complication rate for posterior circulation aneurysms was even higher at 27%. With these high complication-rates, many authors propose this technique only being used when no other endovascular and surgical options are available (Cagnazzo et al., 2018; Madaelil et al., 2017).

Both SAC and FD are examples of permanent intravascular devices, where (temporary) dual anti-platelet therapy (DAPT) is necessary to prevent thrombo-embolic complications and stent-occlusion. Ruptured aneurysms often require a ventriculostomy in case of hydrocephalus, and DAPT increases ventricular drain-related bleedings from 9% to 20.9% (Cagnazzo et al., 2020). Coronary-intervention studies also show that prolonged use of DAPT is associated with more major bleeding and non-cardiac deaths (Yin et al., 2019). Given these concerns, both SAC and FD remain second-choice options in daily practice when treating ruptured aneurysms.

To better deal with wide-neck aneurysms and obviate the need of DAPT, intrasaccular flow disruptors were developed. As these devices don't protrude into the parent vessel, anti-platelet therapy isn't always necessary. The Woven EndoBridge (WEB) has an adequate occlusion-rate of 84.8% in ruptured aneurysms. The complication-rate is lower than SAC and FD at 9.4%, and only 4.8% of cases needing retreatment. Most studies on WEB in ruptured aneurysms are based on retrospective data and showed no rebleeding (Monteiro et al., 2022). The only prospective data on rebleeding comes from the CLARYS-study, where no rebleeding was seen at one month in 60 patients (Spelle et al., 2021).Wide-neck aneurysms seem to be the topic of discussion amongst ruptured aneurysms where both ET and clipping have their merits. Currently the best data comes from prospective studies comparing clipping and coiling/BAC. This data shows similar functional outcomes, complication rates, but again fewer retreatments in the clipped patients.

5.3 Location

Ruptured aneurysms in the anterior circulation are widely represented in ISAT (97.3% of aneurysms), apart from a relative under-representation of MCA aneurysms (comprising 14.1% of the population, compared to 20–30% in epidemiological studies) and distal anterior cerebral artery aneurysms (DACA). An overview is given on the management-decisions for the different locations of ruptured aneurysms in Table 2 (Etminan and Macdonald, 2021).Table 2 Overview of aneurysmal locations influencing treatment outcomes for different modalities in ruptured IA. Abbreviations: RCT: randomized controlled trial, SR: systematic review, RS: retrospective study.

Table 2Ruptured aneurysms	Favors endovascular	No significant difference	Favors microsurgical	Most relevant study	Type of study	
Posterior circulation	mRS			Molyneux et al., 2002	RCT	
Lindgren et al., 2018	SR	
PICA	Fewer cranial nerve palsies	mRS	Occlusion	Ali et al., 2022	SR	
OphA		mRS
Mortality Occlusion		Falk Delgado et al., 2017	Meta-analysis	
PComm	mRS			Taweesomboonyat et al., 2019	RCT	
Molyneux et al., 2005	RS	
AComm		mRS Mortality Rebleeding	Occlusion Retreatment	Molyneux et al., 2005	RCT	
Moon et al., 2015	RCT	
Sattari et al., 2023	SR	
DACA		mRS Morbidity	Occlusion Recurrence Rebleeding	Petr. et al., 2017	SR	
MCA		mRS Occlusion		Zijlstra et al., 2016	SR	

Posterior circulation aneurysms are generally being treated with ET, as surgery poses more difficulties with the deeper location of these aneurysms, important perforators and surrounding cranial nerves. Posterior circulation aneurysms were part of a subgroup-analysis in BRAT, which found better functional outcomes in the coiled group, with a good functional outcome at 1-year follow-up of 82% vs 36%, persisting at 3-years follow-up (75% vs 38%) (Spetzler et al., 2013). This point was further confirmed in a subgroup analysis of the Cochrane review of Lindgren et al., in 2018 (Lindgren et al., 2018).

Basilar apex aneurysms comprise the most frequently encountered posterior circulation aneurysms and follow every principle of a posterior circulation aneurysm.

Some debate remains among the posterior inferior cerebellar artery (PICA) aneurysms. These aneurysms are more superficially located, and the parent artery may have a tortuous course, sometimes necessitating more advanced ET. A systematic review with 17 studies on 455 saccular PICA aneurysms showed similar functional outcomes for clipping and ET, with better complete occlusion rates after clipping (95% vs 69%). When combining data from both ruptured and unruptured PICA aneurysms, a higher rate of cranial nerve palsies was observed after clipping (23% vs 2.4%). In-depth data concerning these cranial nerve palsies is lacking, as it isn't specified whether these are transient in nature or persistent (Ali et al., 2022).In general, ruptured posterior circulation aneurysms are better treated through endovascular measures, some PICA aneurysms might be an exception where a surgical approach might be better suited when adjunctive endovascular measures other than simple coiling are necessary.

Ophthalmic artery (OphA) aneurysms are quite rare, comprising around 5% of all intracranial aneurysms. The proximity of the optic nerve makes for a large morbidity risk after treatment. A meta-analysis on ruptured OphA aneurysms with 152 patients reported no differences in functional outcomes (76% and 71% after coiling and clipping respectively) and similar occlusion- and survival rates (Falk Delgado et al., 2017). To our knowledge, there are no comparative studies published on visual outcomes after treatment for a ruptured OphA.

PComm aneurysms were widely represented in ISAT (accounting for 25% of treated aneurysms), where a better functional outcome for endovascular therapy was seen one year after treatment (Molyneux et al., 2002). A single-center series with 189 PComm aneurysms with coiling and clipping showed similar functional outcomes for both groups, as well as similar complication rates (Taweesomboonyat et al., 2019).

Carotid artery aneurysms remain a poorly studied subject, where only a handful of studies exist on ruptured ICA aneurysms. The most convincing data comes from PComm aneurysms, where an endovascular approach was deemed favorable. Further studies on both PComm and OphA aneurysms fail to show any difference between both treatment modalities concerning functional outcomes.

AComm aneurysms represent the most frequent type of ruptured aneurysms (30–40%) and are often more complex aneurysms because of their double inflow and the presence of 2 or 3 outflow-branches (Fig. 2) (Perlmutter and Rhoton, 1976).

Subgroup analysis of AComm aneurysms in ISAT showed similar functional outcomes for both clipping and ET (Molyneux et al., 2005). A subgroup analysis of BRAT also found no differences in functional outcomes and retreatments (2.3%) at 1 and 3 years of follow-up between clipping and coiling (Moon et al., 2015). Further analysis of the BRAT-cohort and AComm aneurysms treated with ET in the post-BRAT era, was done to evaluate the influence of technological advancements such as BAC and SAC on patient outcomes. The updated cohort had significantly more WNA and showed similar functional outcomes and retreatment rates as before (Moon et al., 2017). A large systematic review with 18 studies and 2368 patients performed a subgroup analysis on ruptured AComm aneurysms, revealing similar functional outcomes (good mRS in 74.8% vs 60.3%), mortality rate (8.1% vs 11.9%) and rebleeding rates (1.7% vs 4.0%) between clipping and ET. Aneurysm obliteration was significantly higher in 89.1% in clipping (89.1%) versus ET (78.6%), with subsequent lower retreatment rates (4.4% vs 10.6%) and recurrences (3.1% vs 10.8%) (Sattari et al., 2023).

Some case series found anatomical factors, such as an aspect ratio of <1.6 and lower dome-neck ratios (Fig. 1), predictive of a surgical-approach as the preferred treatment option (Lee and Park, 2022; Darkwah Oppong et al., 2019). The orientation of AComm aneurysms is important in choosing a treatment approach, as anteriorly orientated aneurysms are more readily accessible with clipping, opposed to the posteriorly oriented aneurysms (Debono et al., 2004). With a posterior projection, more vessel occlusions and subsequent ischemia were seen after clipping, and it was pondered that these lesions should preferably be treated endovascularly, whereas the anterior-facing fundi were favored for surgery (Proust et al., 2003; Choi et al., 2011).Current evidence on AComm aneurysms suggests similar outcomes for both patient groups concerning functional outcome, mortality and rebleeding rates. Aneurysm obliteration, retreatments and recurrences are all better for surgically treated patients. Specific anatomical factors such as aneurysm orientation should be considered, which can lead to a worse surgical outcome in posteriorly angulated aneurysms.

Fig. 1 Drawing representing 3 types of basilar apex bifurcation aneurysms. The top aneurysm represents a small-neck aneurysm, the black arrow measures the aneurysm neck, the white arrow measures the dome, and the yellow arrow measures aneurysm height. The dome-neck ratio (DNR) is calculated by dividing the dome- and neck diameters. The aspect ratio is the maximum height divided by the neck diameter. The two bottom aneurysms represent different types of wide-neck aneurysms. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 1

Fig. 2 Frontal view of a 3D-rendered wide-neck AComm aneurysm, originating from a solitary left anterior cerebral artery (*). The neck-width is measured at 4.6 mm, indicating a wide-neck aneurysm. Notice the trifurcational anatomy of the A2 branches, which surround the aneurysm dome.

Fig. 2

Distal anterior cerebral artery aneurysms or pericallosal artery aneurysms have a small parent artery diameter, a wide neck or branching vessels originating from the aneurysm neck and are often associated with hematomas. Surgical caveats include the need for a parasagittal craniotomy with possible sacrifice of bridging veins (and associated venous infarction), as well as adherent cingulate gyri and a deep/narrow surgical corridor to reach these aneurysms. The endovascular treatment of these aneurysms is more challenging due to their distal location and the anatomical variations (Monroy-Sosa et al., 2017). As DACA aneurysms were only present in 4% of patients in ISAT, controversy concerning optimal treatment strategy still exists (Molyneux et al., 2002).

Anatomical factors to guide treatment-decisions often rely on the relative position of the aneurysm compared to the genu of the corpus callosum. So-called supra-genu aneurysms are preferably treated surgically, and infra-genu aneurysms treated with ET for their ease of accessibility (Take et al., 2021; Carvi y Nievas, 2013). A systematic review with 30 studies and 1050 ruptured DACA aneurysms, found higher complete occlusion rates (94% vs 62%), less recurrences (3% vs 18%), rebleeding (2% vs 4%), and more technical completions (98% vs 90%) in the surgical group. There were no significant differences in functional outcomes, nor morbidity (16–19%) when comparing clipping and ET (Petr et al., 2017).Based on these data, DACA aneurysms should preferably be treated by surgical means when the anatomy is favorable (supra-genu location). The infra-genu DACA aneurysms are more suitable for an endovascular treatment, given the similar functional outcomes.

Middle cerebral artery aneurysms are often treated surgically, due to their superficial location, wide necks and variable bi- or tri-furcational anatomy, as well as vessels branching from the aneurysm dome. To date, there are no randomized trials which compare ET and clipping in patients with MCA aneurysms, but the MCAAT was initiated in 2021, a randomized study comparing both modalities in ruptured and unruptured MCA aneurysms (Darsaut et al., 2022).

Subgroup analysis of MCA aneurysms in the interim-analysis of the ISAT-2 trial did not find any differences in functional outcome but did reveal more adequate occlusions (91% vs 78%) at 1 year in favor of clipping (Darsaut et al., 2021). A subgroup analysis of clipped MCA aneurysms in the BRAT-cohort found a good functional outcome for HnH I-III patients in 70% and 36% in grade IV-V patients, and a complete obliteration in 88% of patients (Mooney et al., 2019). A systematic review with 51 studies and 4065 patients showed similar favorable clinical and angiographic outcomes when comparing coiling and clipping (Zijlstra et al., 2016).It seems that in selected surgical series, microsurgical clipping has an advantage over coiling, but that disappears in a larger systematic review of observational studies. The results of the MCAAT, which will also randomize for ET and clipping in ruptured aneurysms, will provide a better insight in the preferred modality.

6 Conclusion

In this review, an overview is provided of the most relevant literature on decision-making for ruptured saccular intracranial aneurysms. As evident, only a handful of high-quality studies have been performed, and those who are still going on or recently finished, suffered from slow recruiting (ISAT-2). New randomized trials such as the MCAAT, are still being initiated, and should be encouraged, as to shed a better light on the current practice. Case series (prospective and retrospective) will always have inherent selection-biases which will influence the subsequent results and must be interpreted with caution. We aimed to select different systematic reviews when good RCT's were lacking, to give some idea where the current best available evidence lies. Very few guidelines exist to help in making a correct assessment for which treatment modality best suits a single aneurysm. As such, decision-making should always occur in a multi-disciplinary fashion with people directly involved with the patient. Not only neurosurgeons and neuro-interventionalists should be present, but also neurologists, as to provide a neutral party in these discussions and outcome assessments.

The neurovascular community might feel the need to evolve towards more comprehensive, multimodal score systems that accurately capture the large diversity both of patients’ and aneurysmal factors in decision-making steps for aneurysm repair in patients with aneurysmal subarachnoid hemorrhage.

Declaration

This research was made possible by the 10.13039/501100003130 FWO strategic basic research grant 1SH1424N.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
==== Refs
References

Ali A.M.S. Hannan C.J. Islim A.I. Mascitelli J.R. Javadpour M. Surgical and endovascular treatment of saccular posterior inferior cerebellar artery aneurysms: systematic review and meta-analysis World Neurosurg 162 2022 168 177
Bekelis K. Gottlieb D. Su Y. Surgical clipping versus endovascular coiling for elderly patients presenting with subarachnoid hemorrhage J. Neurointerventional Surg. 8 9 2016 913 918
Bsat S. Bsat A. Tamim H. Safety of stent-assisted coiling for the treatment of wide-necked ruptured aneurysm: a systematic literature review and meta-analysis of prevalence Intervent Neuroradiol. 26 5 2020 547 556
Cagnazzo F. Di Carlo D.T. Cappucci M. Lefevre P.H. Costalat V. Perrini P. Acutely ruptured intracranial aneurysms treated with flow-diverter stents: a systematic review and meta-analysis Am. J. Neuroradiol. 39 9 2018 1669 1675 30049721
Cagnazzo F. Di Carlo D.T. Petrella G. Perrini P. Ventriculostomy-related hemorrhage in patients on antiplatelet therapy for endovascular treatment of acutely ruptured intracranial aneurysms. A meta-analysis Neurosurg. Rev. 43 2 2020 397 406 29968172
Campi A. Ramzi N. Molyneux A.J. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT) Stroke 38 5 2007 1538 1544 17395870
Carvi y Nievas M.N. The influence of configuration and location of ruptured distal cerebral anterior artery aneurysms on their treatment modality and results: analysis of our casuistry and literature review Neurol. Res. 32 2013 73 81
Catapano J.S. Zeoli T. Frisoli F.A. Burk-hardt J.K. Lawton M.T. Long-term independence in older patients with aneurysmal subarachnoid hemorrhage in the barrow ruptured aneurysm trial World Neurosurg 147 2021 98 104
Choi J.H. Kang M.J. Huh J.T. Influence of clinical and anatomic features on treatment decisions for anterior communicating artery aneurysms J Korean Neurosurg Soc 50 2 2011 81 88 22053224
Dandy W. Intracranial aneurysm of the internal carotid artery cured by operation Ann. Surg. 107 1938 654 659 17857170
Darkwah Oppong M. Deuschl C. Pierscianek D. Treatment allocation of ruptured anterior communicating artery aneurysms: the influence of aneurysm morphology Clin. Neurol. Neurosurg. 186 2019 1 6
Darsaut T.E. Fahed R. Macdonald R.L. Surgical or endovascular management of ruptured intracranial aneurysms: an agreement study J. Neurosurg. 131 1 2019 25 31
Darsaut T.E. Roy D. Weill A. A randomized trial of endovascular versus surgical management of ruptured intracranial aneurysms: interim results from ISAT2 Neurochirurgie 65 6 2019 370 376 31229533
Darsaut T.E. Keough M.B. Sagga A. Surgical or endovascular management of middle cerebral artery aneurysms: a randomized comparison World Neurosurg 149 2021 521 534
Darsaut T.E. Keough M.B. Boisseau W. Middle cerebral artery aneurysm trial (MCAAT): a randomized care trial comparing surgical and endovascular management of MCA aneurysm patients World Neurosurg 160 2022 e49 e54 34971833
Darsaut T.E. Findlay J.M. Bojanowski M.W. A pragmatic randomized trial comparing surgical clipping and endovascular treatment of unruptured intracranial aneurysms AJNR Am J Neuroradiol 44 6 2023 634 640 37169541
Dawod G. Henkel N.D. Salahuddin H. Outcomes of treatment modalities for ruptured intracranial aneurysms based on age. A meta- analysis J. Stroke Cerebrovasc. Dis. 29 9 2020 1 11
Debono B. Proust F. Langlois O. Anévrismes rompus de l'artère communicante anterieure: Choix thérapeutique à propos d’une série consécutive de 119 cas Neurochirurgie 50 2004 21 32 15097917
Dengler J. Maldaner N. Gläsker S. Outc43ome of surgical or endovascular treatment of giant intracranial aneurysms, with emphasis on age, aneurysm location, and unruptured aneuryms-A systematic review and meta-analysis Cerebrovasc. Dis. 41 2016 187 198 26764969
Etminan N. Macdonald R.L. Neurovascular disease, diagnosis, and therapy: subarachnoid hemorrhage and cerebral vasospasm Handb. Clin. Neurol. 176 2021 135 169 33272393
Falk Delgado A. Andersson T. Falk Delgado A. Ruptured carotid- ophthalmic aneurysm treatment: a non-inferiority meta-analysis comparing endovascular coiling and surgical clipping Br. J. Neurosurg. 31 3 2017 345 349 28637115
Fiorella D. Arthur A.S. Chiacchierini R. Emery E. Molyneux A. Pierot L. How safe and effective are existing treatments for wide-necked bifurcation aneurysms? Literature-based objective performance criteria for safety and effectiveness J. Neurointerventional Surg. 9 12 2017 1197 1201
Gaastra B. Ren D. Alexander S. Evidence-based interconversion of the Glasgow Outcome and modified Rankin scales: pitfalls and best practices J. Stroke Cerebrovasc. Dis. 31 12 2022 1 6
Golnari P. Nazari P. Garcia R.M. Volumes, outcomes, and complications after surgical versus endovascular treatment of aneurysms in the United States (1993–2015): continued evolution versus steady-state after more than 2 decades of practice J. Neurosurg. 134 3 2020 848 861 32032946
Guglielmi G. Vinuela F. Dion J. Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: preliminary clinical experience J. Neurosurg. 75 1 1991 8 14 2045924
Hamouda A.M. Cwajna M. Elfil M. Derhab M. Desouki M.T. Kobeissi H. Impact of frailty on post-operative outcomes following subarachnoid hemorrhage: a systematic review and meta-analysis Clin. Neurol. Neurosurg. 224 2024 1 6
Hendricks B.K. Yoon J.S. Yaeger K. Wide-neck aneurysms: systematic review of the neurosurgical literature with a focus on definition and clinical implications J. Neurosurg. 133 1 2020 159 165 31200376
Hoh B.L. Ko N.U. Amin-Hanjani S. Guideline for the management of patients with aneurysmal subarachnoid hemorrhage: a guideline from the American Heart association/American stroke association Stroke 54 7 2023 314 370 2023
Koivisto T. Vanninen R. Hurskainen H. Saari T. Hernesniemi J. Vapalahti M. Outcomes of early endovascular versus surgical treatment of ruptured cerebral aneurysms: a prospective randomized study Stroke 31 10 2000 2369 2377 11022066
Lai L.T. O’Neill A.H. History, evolution, and continuing innovations of intracranial aneurysm surgery World Neurosurg 102 2017 673 681 28189863
Lee S.H. Park J.S. Outcome of ruptured anterior communicating artery aneurysm treatment compared between surgical clipping and endovascular coiling: a single-center analysis Medicine (Baltim.) 101 38 2022 e30754
Lee K.S. Zhang J.J.Y. Nguyen V. The evolution of intracranial aneurysm treatment techniques and future directions Neurosurg. Rev. 45 2022 1 25
Li J. Su L. Ma J. Kang P. Ma L. Ma L. Endovascular coiling versus microsurgical clipping for patients with ruptured very small intracranial aneurysms: management strategies and clinical outcomes of 162 cases World Neurosurg 99 2017 763 769 26732968
Li G. Han Y. Ding S. Pan Y. Zhang X. Zhao B. Stent-assisted coiling of acutely ruptured cerebral aneurysm: a multicenter prospective registry study (SAVE) BMC Neurol. 22 1 2022 1 5 34979972
Lindgren A. Vergouwen M Di van der Schaaf I. Endovascular coiling versus neurosurgical clipping for people with aneurysmal subarachnoid haemorrhage Cochrane Database Syst. Rev. 2018 8 2018
Liu J. Xiong Y. Zhong M. Predicting long-term outcomes after poor- grade aneurysmal subarachnoid hemorrhage using decision tree modeling Neurosurgery 87 3 2020 523 529 32171016
Madaelil T.P. Moran C.J. Cross D.T. Kansagra A.P. Flow diversion in ruptured intracranial aneurysms: a meta-analysis AJNR Am J Neuroradiol 38 3 2017 590 28007770
Mascitelli J.R. Lawton M.T. Hendricks B.K. Nakaji P. Zabramski J.M. Spetzler R.F. Analysis of wide-neck aneurysms in the barrow ruptured aneurysm trial Neurosurgery 85 5 2019 622 631 30346618
Mascitelli J.R. Lawton M.T. Hendricks B.K. Endovascular therapy versus microsurgical clipping of ruptured wide neck aneurysms (EVERRUN registry): a multicenter, prospective propensity score analysis J. Neurosurg. 2021 1 8 Published online November 5
McDougall C.G. Spetzler R.F. Zabramski J.M. The barrow ruptured aneurysm trial: clinical article J. Neurosurg. 116 1 2012 135 144 22054213
Metayer T. Lechanoine F. Bougaci N. Retreatment of previously treated intracranial aneurysm: procedural complications and risk factors for complications Neurochirurgie 68 2021 150 155 34487752
Mitchell P. Kerr R. Mendelow A.D. Molyneux A. Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? J. Neurosurg. 108 3 2008 437 442 18312088
Molyneux A. Kerr R. Stratton I. Sandercock P. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial Lancet 360 2002 1267 1274 12414200
Molyneux A.J. Kerr R.S. Yu L.M. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and Lancet 366 2005 809 817 16139655
Molyneux A.J. Birks J. Clarke A. Sneade M. Kerr R.S.C. The durability of endovascular coiling versus neurosurgical clipping of ruptured cerebral aneurysms: 18 year follow-up of the UK cohort of the International Subarachnoid Aneurysm Trial (ISAT) Lancet 385 2015 691 697 25465111
Monroy-Sosa A. Nathal E. Rhoton A.L. Operative management of distal anterior cerebral artery aneurysms through a mini anterior interhemispheric approach World Neurosurg 108 2017 519 528 28919562
Monteiro A. Lazar A.L. Waqas M. Treatment of ruptured intracranial aneurysms with the Woven EndoBridge device: a systematic review J. Neurointerventional Surg. 14 4 2022 366 370
Moon K. Levitt M.R. Almefty R.O. Treatment of ruptured anterior communicating artery aneurysms: equipoise in the endovascular era? Neurosurgery 77 4 2015 566 571 26308643
Moon K. Park M.S. Albuquerque F.C. Levitt M.R. Mulholland C.B. McDougall C.G. Changing paradigms in the endovascular management of ruptured anterior communicating artery aneurysms Neurosurgery 81 4 2017 581 584 28327983
Mooney M.A. Simon E.D. Brigeman S. Long-term results of middle cerebral artery aneurysm clipping in the Barrow Ruptured Aneurysm Trial J. Neurosurg. 130 3 2019 895 901 29701554
Perlmutter D. Rhoton A.L. Microsurgical anatomy of anterior cerebral anterior communicating recurrent artery complex Surg. Forum 27 1976 464 465 1019940
Petr O. Coufalová L. Bradáč O. Rehwald R. Glodny B. Beneš V. Safety and efficacy of surgical and endovascular treatment for distal anterior cerebral artery aneurysms: a systematic review and meta-analysis World Neurosurg 100 2017 557 566 27923755
Pierot L. Cognard C. Anxionnat R. Ricolfi F. Ruptured intracranial aneurysms: factors affecting the rate and outcome of endovascular treatment complications in a series of 782 patients (CLARITY study) Radiology 256 3 2010 916 923 20720074
Pierot L. Moret J. Barreau X. Aneurysm treatment with woven EndoBridge in the cumulative population of 3 prospective, multicenter series: 2-year follow-up Neurosurgery 87 2 2020 357 367 31960052
Proust F. Debono B. Hannequin D. Treatment of anterior communicating artery aneurysms: complementary aspects of microsurgical and endovascular procedures J. Neurosurg. 99 1 2003 3 14
Proust F. Bracard S. Lejeune J.P. A randomized controlled study assessing outcome, cognition, autonomy and quality of life in over 70-year- old patients after aneurysmal subarachnoid hemorrhage Neurochirurgie 64 6 2018 395 400 30340777
Santoro A. Armocida D. Paglia F. Treatment of giant intracranial aneurysms: long-term outcomes in surgical versus endovascular management Neurosurg. Rev. 2022 3759 3770 Published online 36269463
Sattari S.A. Shahbandi A. Lee R.P. Surgery or endovascular treatment in patients with anterior communicating artery aneurysm: a systematic review and meta-analysis World Neurosurg 175 2023 31 44 37011760
Schuss P. Hadjiathanasiou A. Borger V. Wispel C. Vatter H. Güresir E. Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome—a single-center series World Neurosurg 85 2016 125 129 26341439
Spelle L. Herbreteau D. Caroff J. CLinical Assessment of WEB device in Ruptured aneurYSms (CLARYS): results of 1-month and 1-year assessment of rebleeding protection and clinical safety in a multicenter study Hemorrhagic stroke J NeuroIntervent Surg 2021 1 8 Published online
Spetzler R.F. McDougall C.G. Albuquerque F.C. The barrow ruptured aneurysm trial: 3-year results: clinical article J. Neurosurg. 119 1 2013 146 157 23621600
Spetzler R.F. McDougall C.G. Zabramski J.M. Ten-year analysis of saccular aneurysms in the barrow ruptured aneurysm trial J. Neurosurg. 132 3 2020 771 776 30849758
Steiner T. Juvela S. Unterberg A. European stroke organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage general considerations Cerebrovasc. Dis. 35 2013 93 112 23406828
Take Y. Kamide T. Kikkawa Y. Current treatment options and prognostic factors for ruptured distal anterior cerebral artery aneurysms Surg. Neurol. Int. 12 171 2021 1 5 33500816
Taweesomboonyat C. Tunthanathip T. Kaewborisutsakul A. Outcome of ruptured posterior communicating artery aneurysm treatment comparing between clipping and coiling techniques World Neurosurg 125 2019 183 188 30743033
Willinsky R.A. Taylor S. TerBrugge K. Farb R. Tomlinson G. Montanera W. Neurologic complications of cerebral angiography: prospective analysis of 2899 procedures and review of the literature Neuroradiology 227 2003 522 528
Xia Z.W. Liu X.M. Wang J.Y. Coiling is not superior to clipping in patients with high-grade aneurysmal subarachnoid hemorrhage: systematic review and meta-analysis World Neurosurg 98 2017 411 420 27867126
Yin S.H.L. Xu P. Wang B. Duration of dual antiplatelet therapy after percutaneous coronary intervention with drug-eluting stent: systematic review and network meta-analysis BMJ 365 2019
Yoshiyama M. Ikawa F. Hidaka T. Development and validation of scoring indication of surgical clipping and endovascular coiling for aneurysmal subarachnoid hemorrhage from the post hoc analysis of Japan stroke data bank Neurol. Med.-Chir. 61 2021 107 116
Yue Q. Liu Y. Leng B. Xu B. Gu Y. Chen L. A prognostic model for early post-treatment outcome of elderly patients with aneurysmal subarachnoid hemorrhage World Neurosurg 95 2016 253 261 27544333
Zhang Q. Jing L. Liu J. Predisposing factors for recanalization of cerebral aneurysms after endovascular embolization: a multivariate study J. Neurointerventional Surg. 10 3 2018 252 257
Zhang X. Zuo Q. Tang H. Stent assisted coiling versus non-stent assisted coiling for the management of ruptured intracranial aneurysms: a meta-analysis and systematic review J. Neurointerventional Surg. 11 5 2019 489 496
Zhao B. Yang H. Zheng K. Preoperative and postoperative predictors of long-term outcome after endovascular treatment of poor-grade aneurysmal subarachnoid hemorrhage J. Neurosurg. 126 6 2016 1764 1771 27367238
Zhao B. Xing H. Fan L. Endovascular coiling versus surgical clipping of very small ruptured anterior communicating artery aneurysms World Neurosurg 126 2019 e1246 e1250 30898747
Zhu W. Ling X. Petersen J.D. Liu J. Xiao A. Huang J. Clipping versus coiling for aneurysmal subarachnoid hemorrhage: a systematic review and meta- analysis of prospective studies Neurosurg. Rev. 45 2 2022 1291 1302 34870768
Zijlstra I. Verbaan D. Majoie C.B. Vandertop P. Van Den Berg R. Coiling and clipping of middle cerebral artery aneurysms: a systematic review on clinical and imaging outcome J. Neurointerventional Surg. 8 1 2016 24 29
