Combined microsurgical and endovascular approach in the hybrid operating angiosuite: A case series on blood-blister intracranial aneurysms

doi:10.21203/rs.3.rs-4907614/v1

Purpose: Blood blister-like aneurysms (BBAs) are small, fragile vascular lesions that develop on the walls of the supraclinoid internal carotid artery. This absence of a neck complicates surgical and endovascular treatment options. The hybrid operating angiosuite (HOA), which integrates traditional surgical techniques with endovascular interventions, provides an innovative approach to managing BBAs. This study aims to evaluate a series of clinical cases focused on treating BBAs using a combination of microsurgical extracranial-intracranial bypass and endovascular trapping within the HOA.

Methods:We analyzed a series of patients with BBAs treated from 2014 to 2022. Skilled bimanual neurovascular surgeons implemented treatment plans using both microsurgical and neurointerventional techniques across four distinguished neurosurgery centers: Kangdong Sacred Heart Hospital, Seoul St. Mary’s Hospital, Yongin Severance Hospital, and International St. Mary’s Hospital. Clinical outcomes were measured using the Glasgow Outcome Scale (GOS) at discharge and the modified Rankin Score (mRS) during follow-up, with scores of 0–2 indicating favorable outcomes. Follow-up imaging via computed tomography angiography or magnetic resonance angiography was conducted on average 6–12 months post-procedure to assess BBA recurrence and graft vessel patency.

Results: Seven patients (average age, 45 years) were treated at the HOA. The surgical approach included high-flow bypass in five patients and superficial temporal artery double-barrel bypass in two. Follow-up imaging revealed no BBA recurrences and maintained patency of bypass flow.

Conclusion: Our findings suggest that a hybrid approach offers a safer and more effective strategy for managing BBAs, potentially improving patient outcomes.

aneurysm

anastomosis

trapping

subarachnoid hemorrhage

Blood blister-like aneurysms (BBAs) are small, fragile vascular lesions that develop on the walls of the supraclinoid internal carotid artery (ICA) [1–3]. Unlike saccular aneurysms, which possess a neck and can be treated with clipping or coiling, BBAs lack a definitive neck, posing significant challenges for surgical and endovascular treatment strategies [4]. Despite representing 0.4–1.4% of all ruptured ICA aneurysms, BBAs are clinically significant owing to their comparatively high morbidity and mortality [5, 6].

Traditional microsurgical and endovascular treatments are carefully implemented; however, the risk of rebleeding and recurrence persists [7]. Some studies have shown promising results. Specific interventions, like microsurgical trapping and extracranial-intracranial (EC-IC) bypass, along with endovascular techniques such as multi-stenting assisted coiling and flow diverters, have proven effective in maintaining adequate cerebrovascular circulation and resolving pathological lesions [8, 9].

The hybrid operating angiosuite (HOA), which combines conventional surgical techniques with endovascular interventions, offers a sophisticated and cooperative approach to managing BBAs. This integration marks a significant paradigm shift, leading to improved patient outcomes through the coordinated efforts of proficient neurovascular surgeons across surgical and endovascular procedures.

In this regard, we aimed to evaluate a clinical case series focused on managing BBAs through a combined approach of microsurgical EC-IC bypass and endovascular trapping of the ICA within the HOA.

Patient selection

This retrospective study was approved by the local institutional review board, and informed consent was secured from each patient’s family. All procedures involving human participants adhered to the ethical standards set by the institutional and national research committees, as well as to the 1964 Helsinki Declaration and its subsequent amendments or comparable ethical standards. We examined a series of patient cases with BBAs from 2014 to 2022. Treatment plans were executed by skilled bimanual neurovascular surgeons utilizing both microsurgical and neurointerventional techniques in HOAs at four distinguished neurosurgery centers: Kangdong Sacred Heart Hospital, Seoul St. Mary’s Hospital, Yongin Severance hospital, and International St. Mary’s Hospital.

Patients in the study were identified based on the presence of BBAs, characterized by abnormal focal arterial dilatations accompanied by subarachnoid hemorrhage, specifically located at non-branching sites along the supraclinoid ICA. Diagnosis was confirmed through brain computed tomography (CT), three-dimensional CT cerebral angiography (3D-CTA), and digital subtraction angiography (DSA). Patients with unruptured aneurysms or those located at branching points of the ICA were excluded from the study. Additionally, cases treated exclusively by surgical or endovascular methods were omitted from the analysis. Detailed records of patients’ sex, age, and clinical presentation were maintained. The Hunt–Hess (HH) scoring system and the World Federation of Neurosurgical Societies (WFNS) scale were employed for clinical assessment at admission, while the Glasgow Outcome Scale (GOS) was used for postoperative evaluation at discharge.

Hybrid Operating Angiosuite (HOA)

The configuration of an HOA integrates a ceiling-mounted DSA apparatus (Allura FD 20; Philips, Best, The Netherlands) and a floor-fixed DSA apparatus (Artis zeego, Siemens, Erlangen, Germany) with a fully operational surgical suite. This innovative setup includes specialized equipment such as an imaging view box, tools crafted from radiolucent materials (DORO® Radiolucent Retractor System; Promedics, Düsseldorf, Germany), a headrest that allows X-ray penetration (DORO®), and a surgical platform (MAGNUS; Maquet GmbH, Rastatt, Germany) designed for a seamless transition between endovascular and microsurgical procedures. The arrangement enables concurrent neurointerventional procedures supported by specialized personnel. The surgical table’s height is adjustable for optimal microsurgical visualization; however, it must revert to a standard position for acquiring three-dimensional reconstructed images (Fig. 1).

Microsurgical approach

All patients underwent microsurgical EC-IC bypass and endovascular trapping of the BBA-affected ICA segment in the HOA. The high-flow bypass utilized either a saphenous vein or radial artery graft, while low-flow bypass employed a double-barrel technique involving the superficial temporal artery. Following the surgical field’s preparation with precise draping of the head, neck, and inguinal areas, our procedure commenced with a meticulous neck dissection to reveal the common carotid artery (CCA), ICA, external carotid artery (ECA), and superior thyroid artery. Concurrently, a cardiothoracic surgeon harvested a segment of the saphenous vein or radial artery from the ipsilateral limb, marked it to indicate valve presence or orientation, and infused it with heparinized saline for subsequent use. The operation continued with a standard frontotemporal craniotomy, as exposure of the intracranial ICA trunk was unnecessary, eliminating the need for an anterior clinoidectomy. Upon opening the dura mater, a 24-Fr chest tube was utilized to tunnel towards the submandibular area for graft positioning, ensuring adequate length. Microsurgical dissection extended along the Sylvian fissure to fully expose the M2 or M3 segment of the middle cerebral artery (MCA) for a perpendicular anastomosis using 10 − 0 nylon sutures, avoiding a fish-mouth incision due to a discrepancy in donor-recipient size. After completing the distal anastomosis, graft patency was confirmed through intraoperative indocyanine green videoangiography (ICGV). The proximal anastomosis was achieved with 8 − 0 prolene sutures to the ECA or CCA, deliberately excluding the ICA to facilitate subsequent endovascular procedures, ensuring effective vascular reconstruction to restore cerebral perfusion.

Endovascular approach

The endovascular procedure began with intraoperative angiography to verify adequate bypass flow prior to the endovascular trapping of the BBA lesion. For access, either a 6-Fr Envoy guiding catheter (Codman & Shurtleff, Raynham, MA) or a 6-Fr Benchmark guiding catheter (Penumbra, Alameda, CA) was adeptly positioned in the ICA. The diameter of the BBA-affected ICA was measured using reconstruction images from a 3D rotational angiogram (RA), facilitating customized trap planning. Adjustments to the working projections were made to accurately characterize the posterior communicating (Pcom) artery and ensure the preservation margin of the ophthalmic artery. Internal coil trapping was performed using pre-shaped 45-degree or straight 0.010-inch Excelsior microcatheters (Stryker Neurovascular, Kalamazoo, MI), guided by a 0.014-inch micro guidewire (Traxcess; MicroVention, Tustin, CA), which delivered bare-type coils into the pathological segment of the ICA. Coils were selected based on the maximum diameter of the ICA to construct an initial coil framework that avoids contact with the fragile aneurysm sac. In cases where coil migration into the Pcom artery posed a risk, a Sceptor balloon was utilized from behind to provide support and form a basket, ensuring secure trapping of the coil mass. This approach reduces the risk of procedural rupture, ensuring a safe and successful intervention.

Perioperative medical preparation

Preoperative administration of antiplatelet agents was not performed. After confirming adequate blood flow through the bypass graft and positioning the guide within the proximal ICA, a single intravenous bolus of 3000 IU of heparin was administered without the need for additional booster doses. No further pharmacological maintenance was planned for the postoperative period

Clinical and radiological outcome

Postoperative management included monitoring for symptomatic cerebral vasospasm in the ICU. Clinical outcomes were assessed using the GOS at hospital discharge and the modified Rankin Score (mRS) at the most recent follow-up, with scores of 0–2 indicating favorable outcomes and scores of 3–6 indicating unfavorable outcomes. Follow-up assessments using CTA or MRA were conducted at an average of 6–12 months post-procedure to evaluate BBA recurrence and graft vessel patency. Aneurysm recurrences, perioperative complications, and neurological outcomes were also assessed, with follow-up data being essential for evaluating the long-term efficacy of the treatments.

The study involved seven patients treated at an HOA, with an average age of 45 years, comprising two males and five females. All BBAs were in the supraclinoid segment of the ICA. Among these, five cases were identified as dorsal type, one as ventral, and one as medial. Clinical severity was assessed using the H-H grading system, with two patients classified as grade III and five as grade II. The average size of the aneurysms was 1.4 mm. According to the Fisher scale, one patient was grade IV, two were grade III, and four were grade II.

Surgical treatment consisted of a high-flow bypass in five patients and a superficial temporal artery (STA) double-barrel bypass in two patients. In the high-flow bypass cases, a saphenous graft was used in four patients, with three anastomoses to the CCA and one to the ECA. Intracranial vessels used included the M2 superior trunk in three cases and M3 in one case. One patient underwent a high-flow bypass using a radial graft, with anastomosis from the ECA to the M2 superior trunk. Two patients received a double-barrel bypass using STA branches, with anastomoses to the M2 superior and inferior trunks. Following the bypass procedures, the surgical environment transitioned to an endovascular setting, where complete trapping of the ICA segment containing the BBA was achieved using coils, while preserving the ophthalmic and Pcom arteries. The average duration of the combined surgical and endovascular procedure was 370 min, with no procedure-related complications observed. In postoperative ICU management, three patients developed symptomatic cerebral vasospasm, with one patient experiencing a vasospasm-related localized cerebral infarction. This patient had undergone a procedure using the radial artery.

Follow-up imaging with CT or MRA, conducted an average of 9.6 months post-procedure, showed no recurrence of BBAs and maintained patency of the flow. The preoperative WFNS grade ranged from I–IV, while the GOS at discharge was favorable: one patient scored 3 points, one scored 4 points, and five scored 5 points. During long-term follow-up, exceeding an average of 20 months, the final mRS scores were 2 points in one patient, 3 points in one patient, and 0 points in five patients. The patient with a final mRS of 3 experienced an ischemic injury due to SAH-related vasospasm.

Case 1

A 54-year-old man presented with sudden altered consciousness and was diagnosed with extensive subarachnoid hemorrhage (SAH) via CT (Fig. 2). DSA revealed a BBA measuring < 2 mm, attributed to dissection of the right supraclinoid ICA. During the operation in the HOA, a neurovascular surgeon performed a neck dissection while a cardiothoracic surgeon harvested a graft from the leg, anastomosing it to the M2 trunk, saphenous vein, and CCA. Intraoperative angiography confirmed the graft’s patency. The lesion located between the ophthalmic artery and the Pcom was successfully occluded using multiple coils delivered via a microcatheter. Follow-up assessments showed that the patient recovered without neurological deficits. One year later, CTA confirmed that the bypass was well-maintained with no recurrence.

Case 2

A 52-year-old woman presented with a severe acute headache and was diagnosed with Fisher grade II SAH via CT (Fig. 3). DSA revealed a 1.2-mm ventral-type BBA located on the left supraclinoid ICA. During the operation in the HOA, an anastomosis was created connecting the M2 trunk to the CCA using the saphenous vein. Subsequent intraoperative angiography identified rapid growth of the lesion, which was fully occluded with several coils delivered via a balloon-assisted microcatheter. The patient recovered without any neurological deficits, and no recurrence was observed on MRA one year later.

The management of BBAs presents unique challenges due to their small size, fragile walls, and tendency to emerge from non-branching segments of the ICA [10]. Histopathological examinations reveal that at the junction between the eccentrically sclerotic and normal carotid wall, the internal elastic lamina and media are absent [1–3]. This discontinuity is bridged by normal adventitia and fibrinous tissue, rather than the collagenous tissue typically found in aneurysmal walls. In addition to predisposing BBAs to a heightened risk of rupture, these anatomical and morphological peculiarities complicate conventional endovascular and microsurgical interventions, increasing the likelihood of further injury and jeopardizing essential cerebral blood flow. Additionally, the dynamic nature of BBAs, which can rapidly alter in morphology and size, requires an assertive approach that secures the aneurysm while maintaining cerebral perfusion [11].

Microsurgical and endovascular techniques offer distinct advantages and challenges in treating BBAs [12]. Microsurgical approaches, including trapping the aneurysm through clipping (with or without bypass), direct clipping, wrapping, combination clip placement with wrapping, and direct suturing of the arterial walls, offer definitive methods for securing and repairing the aneurysm [13]. However, the risk of intraoperative rupture during these procedures remains significant, with reported risks as high as 43%, warranting further examination and consideration [14]. Conversely, endovascular treatments, such as multi-stent-assisted coil embolization and the use of flow diverters, offer a less invasive alternative that can effectively isolate the BBA [14, 15]. However, the introduction of coils into anatomically fragile regions of the vessel wall carries a persistent risk of rupture, and post-treatment recurrences are challenging to address. Furthermore, the requirement for anticoagulant and antiplatelet medications increases the risk of hemorrhagic complications, particularly in complex clinical scenarios, such as patients with hydrocephalus requiring ventricular catheterization or those with increased intracranial pressure needing decompressive craniectomy [16].

Systematic reviews indicate that the selection of treatment for BBAs significantly depends on the practitioner’s expertise [17–20]. Asserting the superiority of either microsurgery or endovascular treatment remains challenging. However, intraoperative bleeding is observed to be more prevalent during surgical procedures, whereas endovascular treatment is associated with higher rates of recurrence and the need for secondary interventions [21]. Implementation of HOAs in the management of BBAs presents a novel therapeutic option that combines the advantages of microsurgical and endovascular techniques. This integrated approach enables neurovascular surgeons to implement a comprehensive treatment strategy, ensuring circulation-guaranteed trapping of the ICA segment affected by BBAs. This significantly reduces the incidence of rebleeding and recurrence. In our cases, microsurgical EC-IC bypass was performed using either a high-flow or low-flow (double-barrel) anastomosis, which preserved cerebral perfusion and minimized ischemic risks following effective trapping. By avoiding frontal lobe retraction or removing the anterior clinoid process to identify lesions on the ICA and by not performing additional dissection to expose the BBA, we eliminated the risk of intraoperative bleeding caused by manipulation of the blister aneurysm. Following this, the endovascular approach was rapidly employed to secure the pathological lesion with internal coil trapping, thereby eliminating the possibility of lesion recurrence.

EC-IC bypass techniques have effectively mitigated ischemic complications associated with the surgical obliteration of the ICA. Both high-flow bypass (using the radial artery or saphenous vein) and low-flow double-barrel bypass (involving two STAs connected to the superior and inferior trunks of M2) combined with microsurgical BBA trapping have demonstrated reliable outcomes in treating BBAs in patients at high-risk due to poor initial neurological conditions [22]. Kazumata et al. demonstrated a crucial paradigm shift in treating ruptured BBAs, transitioning from conventional clipping to combining radial-artery graft bypass with microsurgical ICA trapping [23]. The retrospective analysis of 20 patients showed that this approach effectively reduces morbidity and mortality, achieving favorable outcomes in 90% of patients. Similarly, a study by Kikkawa et al. involving 16 patients using a saphenous vein demonstrated successful aneurysm elimination and bypass patency, with no cases of infarction in the Pcom/anterior choroidal artery territories or ischemic optic neuropathy at a mean follow-up of 36 months [24]. Balik et al. introduced a case series of 9 patients utilizing a double-bypass technique for treating BBAs, employing intraoperative measurements of MCA blood pressure to determine the most suitable bypass method [25]. This approach demonstrated the technique’s effectiveness and safety, achieving favorable long-term results through customized surgical strategies informed by real-time intraoperative evaluations.

Various treatment outcomes for BBAs reported intraoperative and postoperative bleeding rates for direct clipping or wrapping ranging from 3.7–58.35% and 6.9–12.9%, respectively. In comparison, endovascular approaches noted bleeding rates of 3.2–2.4% for multi-stent coiling and 10.3–7.7% for flow diverter placement [26–29]. Interestingly, trapping has shown a 0% rate of intraoperative and postoperative bleeding, consistent with our case studies [25]. Although treatment-related complications and ischemic infarction rates for trapping are 15.2% and 12.1% during surgery and 28.6% for endovascular options, all bypasses in our study maintained sufficient patency to supply unilateral cerebral blood flow with no associated complications [9, 22, 24, 25, 30]. Conventional microsurgical treatments exhibit a recurrence rate of 10.3%, and endovascular treatments show a 14.4% recurrence rate [27, 31, 32]. Our follow-up study indicated that bypass patency was maintained and no recurrences were observed at the trapping site.

Our findings demonstrate the efficacy and safety of an integrated approach that combines microsurgical EC-IC bypass with endovascular trapping, showing no procedure-related complications—a significant improvement over Kazumata et al. [23], where postoperative infarctions due to vasospasm or thrombosis were common. Utilizing high-flow bypass and STA double-barrel bypasses, followed by endovascular trapping, we effectively maintained flow patency and prevented BBA recurrence, with follow-up imaging at an average of 9.6 months showing no recurrence and well-maintained patency [33]. Our results align closely with Aihara et al. [30], who reported good mRS outcomes (0–2 in 80% of patients) using a similar high-flow bypass strategy. However, we observed fewer severe ischemic complications, likely due to robust cerebral perfusion from strategically chosen grafts. Unlike Szmuda et al. [34], who reported higher incidences of mortality (11.5%) and morbidity (14%), our study demonstrated more favorable outcomes with no immediate surgical complications and lower severe morbidity. Although our strategy effectively addressed the dual challenges of immediate aneurysm control and blood flow preservation to affected cerebral territories, the occurrence of symptomatic cerebral vasospasm in three patients, leading to localized cerebral infarction in one case, indicates that ischemic vasospasm remains a persistent risk, consistent with the findings of Aihara et al. [30].

Despite the promising outcomes, our study has significant limitations that must be acknowledged. Firstly, the retrospective nature of our case series limits the generalizability of the findings. The challenges associated with this approach are considerable, requiring a well-equipped HOA and a surgeon with the technical proficiency to safely and effectively perform EC-IC bypasses. Additionally, endovascular procedures require a skill level to ensure successful vascular occlusion without complications. On a positive note, the multidisciplinary team approach can be beneficial in terms of time management and maintaining the physical condition of the surgeons. While we recognize the low incidence of this condition and the small number of cases in our study, future research is needed to comprehensively compare various treatment techniques. By doing so, we aim to continue improving our approach to enhance the safety, efficacy, and quality of life for patients suffering from BBA aneurysms.

Although various microsurgical and endovascular techniques are available, treating BBAs inherently involves significant risks. Our experience indicates that a hybrid approach provides a safer and more effective solution. The combined strategy has the potential to improve patient outcomes by addressing the complexities inherent to BBAs.

Data availability statement: The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation

Ethics statement: The studies involving humans were approved by local institutional review board. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent for participation was not required from the participants or the participants’ legal guardians/next of kin in accordance with the national legislation and institutional requirements.

Author contributions: Hong Suk Ahn: writing – review & editing, writing – original draft, visualization, validation, software, project administration, formal analysis, conceptualization; Jai Ho Choi: investigation, data curation, resources; So Yeon Kim: investigation, data curation, resources; Hong Jun Jeon: writing – review & editing, software, funding acquisition, data curation, methodology; Byung Moon Cho: writing – review & editing, supervision, resources

Funding: The authors declare that no financial support was received for the research, authorship, and/or publication of this article

Competing interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Table 1 Clinical and procedural characteristics

No.	Gender /Age	Location	H& H grade	Fisher group	Size	Recipient Vessel I	Graft Vessel	Recipient Vessel II	Endovascular trapping	Procedure time (minutes)	Complication
1	F/34	ICA Dorsal	II	II	1.5	NA	Double STA	M2 (Inf.& Sup.)	Coils	325	NA
2	M/54	ICA Dorsal	III	IV	1.7	CCA	Saphenous vein	M2 (Sup.)	Coils	335	NA
3	F/46	ICA Medial	II	III	1.2	ECA	Radial artery	M2 (Sup.)	Coils	397	NA
4	M/56	ICA Dorsal	II	II	1.3	ECA	Saphenous vein	M2 (Sup.)	Coils	426	NA
5	F/37	ICA Dorsal	III	III	1.3	NA	Double STA	M2 (Inf.& Sup.)	Coils	345	NA
6	F/52	ICA Ventral	II	II	1.2	CCA	Saphenous vein	M2 (Sup.)	Coils	480	NA
7	F/45	ICA Dorsal	II	II	1.6	CCA	Saphenous vein	M3	Coils	494	NA

NIHSS, National Institute of Health Stroke Scale; ASPECTS, alberta stroke program early CT score.

Table 2 Clinical and radiological outcome

No.	Immediate Graft Patency	Endovascular Trapping	Vasospasm on ICU	F/U Angio (Mons)	Recurrence	WFNS grade (Preop)	GOS On discharge	Final mRS	Follow-up (months)
1	Good	Complete	-	6	No	I	5	0	18
2	Good	Complete	+	12	No	III	4	2	24
3	Good	Complete	+	7	No	IV	3	3	12
4	Good	Complete	-	12	No	II	5	0	15
5	Good	Complete	+	9	No	II	5	0	32
6	Good	Complete	-	12	No	I	5	0	22
7	Good	Complete	-	9	No	II	5	0	19

NIHSS, National Institute of Health Stroke Scale; ASPECTS, alberta stroke program early CT score.

No competing interests reported.

Combined microsurgical and endovascular approach in the hybrid operating angiosuite: A case series on blood-blister intracranial aneurysms

Status:

Version 1

Abstract

Figures

INTRODUCTION

MATERIALS AND METHODS

Patient selection

Hybrid Operating Angiosuite (HOA)

Microsurgical approach

Endovascular approach

Perioperative medical preparation

Clinical and radiological outcome

RESULTS

Case 1

Case 2

DISCUSSION

Conclusion

Declarations

References

Tables

Additional Declarations

Status:

Version 1