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Abstract
Background Dissecting aneurysms located along the distal segments of the posterior inferior cerebellar artery (PICA) are extremely rare, accounting for only 0.5–0.7% of all intracranial aneurysms. Treatment of these aneurysms is challenging, both surgically and endovascularly. We present our preliminary experience and clinical data utilizing Onyx as an embolization agent in the treatment of these lesions with proximal parent artery preservation.
Methods 7 consecutive ruptured peripheral PICA aneurysms, in 7 patients, were treated with superselective Onyx embolization at our institutions. According to the anatomical classification of Lister et al, these aneurysms were located in the lateral medullary segment (n=1), tonsillomedullary segment (n=1), and the telovelotonsillary segment (n=5) of the PICA. Technical feasibility, procedure related complications, angiographic results, follow-up diagnostic imaging, and clinical outcome were evaluated.
Results In all cases, endovascular treatment was successful, with complete occlusion of the aneurysm with proximal parent artery preservation at the final postprocedural angiogram. Procedure related complications were not observed. One patient with a poor clinical condition at admission died during the initial hospital stay due to extensive subarachnoid and intraventricular hemorrhage. No rebleeding or recanalization was noted during follow-up. Two patients had a residual moderate to severe disability at follow-up. Favorable outcomes, with no or mild disability, were observed in four of the surviving patients.
Conclusions Angiographic, diagnostic imaging, and clinical results of our small series indicate that Onyx embolization of dissecting distal PICA aneurysms with parent artery preservation is an effective option with acceptable morbidity and mortality rate, in those cases in which surgical clipping or endovascular coiling of the aneurysmal sac is not suitable.
- Aneurysm
- Dissection
- Liquid Embolic Material
- Subarachnoid
- Hemorrhage
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Background
Overall, posterior inferior cerebellar artery (PICA) aneurysms are rare, accounting for only 0.5–3% of all intracranial aneurysms.1 They mostly arise near the origin of the PICA from the vertebral artery (VA) or the first anteromedullary segment of the vessel.2 ,3 Early aneurysm treatment is necessary in patients presenting with subarachnoid hemorrhage (SAH) as rebleeding rates may be as high as 78%.4 A much smaller proportion, termed distal PICA aneurysms, arise from peripheral PICA segments. Aneurysms located in distal portions of the PICA are subclassified into saccular and fusiform types. Saccular lesions are at hemodynamically stressful locations that usually arise at bifurcations or vessel bends and can be treated either surgically or endovascularly without sacrifice of the parent vessel. Fusiform aneurysms, defined as aneurysm not centered at a vessel ramification and involving longitudinally a wide circumference of the vessel wall, arise spontaneously anywhere along the course of the PICA as a consequence of dissection. Dissecting aneurysms located in the distal PICA are extremely rare, accounting for only 0.5–0.7% of all intracranial aneurysms.5–7 Distal PICA aneurysms are difficult to treat both surgically and endovascularly. Surgical treatment is considered challenging and is associated with a rather high morbidity/mortality rate.8 ,9 Embolization of the aneurysm sac may be difficult or impossible because of the distal location or the unfavorable configuration of the aneurysm. The pre-existing literature regarding endovascular treatment of these lesions is limited and controversial.10–14
We present our preliminary experience and clinical data utilizing Onyx embolization in the treatment of distal dissecting PICA aneurysms.
Methods
We retrospectively reviewed the records of all patients with PICA aneurysms treated at our referral centers between September 2012 and October 2014. Of the 27 PICA aneurysms embolized endovascularly, the vast majority were saccular aneurysms located at the VA/PICA junction (20 cases). Seven ruptured peripheral PICA aneurysms in seven patients (four men; aged 56–85 years; mean age 68 years) were treated with Onyx embolization at our institutions. Non-enhanced CT of the head was indicative of an SAH in all patients, primarily involving the posterior fossa, with intraventricular extension as the result of rupture of a peripheral aneurysm. The Hunt–Hess grade was 4 in five patients and grade 5 in two patients. According to the anatomical classification described by Lister et al,15 the aneurysms were located in the lateral medullary segment (n=1), tonsillomedullary segment (n=1), and the telovelotonsillary segment (n=5) of the PICA. The aneurysm involved the left PICA in four cases and the right PICA in three cases. Average diameter was 3 mm (range 2.2–3.8 mm) (table 1).
Summary of Patient and Aneurysm Characteristics
Technique
Indication for and type of endovascular treatment was a joint decision between the neurointerventional and neurosurgical teams. The endovascular embolization method was selected on the basis of location, morphology, and presumed etiology of the aneurysm. All procedures were performed under general anesthesia after obtaining informed consent from the patient's family members.
Endovascular treatment of the aneurysms was performed on a biplane angiographic unit (Allura Xper FD20/20; Philips Medical Systems, Best, The Netherlands; Artis zee, Siemens, Erlangen, Germany).
After catheterization, four patients received systemic heparinization to increase the activated clotting time to approximately 300 s during the procedure, and the remaining three patients were treated without therapeutic heparinization. A 6 F guiding catheter was advanced into the VA via the transfemoral route. In four patients, a TransForm balloon (Stryker Neurovascular, Freemont, California, USA) was coaxially navigated within the VA and placed across the PICA ostium, for safety purposes (figure 1). Under roadmapping, the tip of a Marathon microcatheter (Covidien, Irvine, California, USA) was gently introduced into the PICA and navigated into the proximal portion of the peripheral dissecting aneurysm. After confirming the microcatheter tip location by angiogram, the Marathon lumen was flushed with 0.25 mL of dimethyl sulfoxide. Subsequent injection of Onyx 18 or 34 was closely monitored under subtracted fluoroscopy (blank roadmapping). Onyx was injected with the ‘reflux–hold–reinjection’ technique to block a short proximal segment of parent artery and avoid reflux to the proximal trunk and perforators (figure 2). The injection was stopped for 20 s to 2 min to solidify the Onyx and was then restarted to occlude the aneurysm. The injection was completed when the aneurysm and diseased vessel segment were completely occluded (figure 3). Reflux of Onyx into the proximal vessel was strictly controlled. Superselective embolization of the dissecting aneurysm with proximal PICA segment preservation was obtained. After the procedure, the patient was monitored in the neurology/neurosurgery intensive care unit.
Pretreatment lateral images of the seven cases in the series treated endovascularly with parent artery occlusion utilizing Onyx as the liquid embolic material. Case Nos 1–4 required TransForm balloon utilization for posterior inferior cerebellar artery origin protection.
An elderly patient was transported to the hospital in a comatose state (Hunt–Hess grade 5). Ruptured dissecting left posterior inferior cerebellar artery (PICA) aneurysm. (A) Non-enhanced CT axial image, demonstrating an extensive amount of subarachnoid hemorrhage primarily involving the left cerebellomedullary cistern. Digital subtraction angiography (B frontal and C lateral views) shows the dissecting aneurysm involving the tonsillomedullary and telovelotonsillar segments of the PICA (arrows). (D) Three-dimensional view shows the aneurysm. (E) Endovascular trapping with Onyx 34 of the ruptured dissecting left PICA aneurysm. (F) Postoperative control angiogram shows complete occlusion of the diseased segments and the aneurysm with preserved patency of the anterior and lateral medullary segments of the left PICA (arrow).
An elderly patient was transported to the hospital in a stuporous state. Neurological examination disclosed a moderate left side hemiparesis (Hunt–Hess grade 4). Ruptured dissecting right posterior inferior cerebellar artery (PICA) aneurysm. (A) Non-enhanced CT right parasagittal image, demonstrating an extensive amount of subarachnoid hemorrhage, primarily involving the right cerebellomedullary cistern and third ventricle. (B) Digital subtraction angiography (lateral view) shows the dissecting aneurysm involving the telovelotonsillar segment of the PICA (arrow). (C) Three-dimensional view shows the irregular morphology of the aneurysm (arrow). (D) Microcatheter contrast injection within the aneurysm, demonstrating a long segment of distal right PICA involved by disease. (E) Endovascular trapping with Onyx 34 of the ruptured dissecting right PICA aneurysm. (F) Postoperative control angiogram shows complete occlusion of the diseased segments and aneurysm with preserved patency of the anterior and lateral medullary segments of the right PICA.
Results
Post-treatment and follow-up angiographic and CT/CT angiography data
In the acute stage after SAH, endovascular treatment was performed successfully in all seven patients included in the study. The final angiogram showed obliteration of the aneurysm in all patients, with preservation of the proximal segments of the PICA (figure 4).
An elderly patient was transported to the hospital in a stuporous state. Neurological examination disclosed a right side hemiparesis (Hunt–Hess grade 4). Ruptured dissecting left posterior inferior cerebellar artery (PICA) aneurysm. (A) Non-contrast CT demonstrated a subarachnoid hemorrhage in the subtentorial cisterns, more prominent involving the left cerebellomedullary cistern. (B) Digital subtraction angiography (lateral view) shows the dissecting aneurysm involving the telovelotonsillar segment of the PICA (arrow). (C) Three-dimensional view shows the irregular morphology of the aneurysm (arrow). (D) Microcatheter contrast injection within the aneurysm, demonstrating a long segment of distal left PICA involved by disease. (E) Endovascular trapping with Onyx 18 of the ruptured dissecting left PICA aneurysm. (F) Postoperative control angiogram demonstrating complete occlusion of the diseased segments and aneurysm with preserved patency of the anterior and lateral medullary segments of the left PICA.
One patient with a very poor clinical condition (Hunt–Hess grade 5) at admission died during the initial hospital stay on postoperative day (POD) 3 due to sequelae of extensive SAH and intraventricular hemorrhage. Follow-up imaging using CT/CT angiography/angiography was performed in the remaining six patients to assess for infarction in the territory of the treated artery and to determine the status of the embolized aneurysms. All patients had a postprocedural CT (POD 0–1), and five of the surviving patients underwent an additional follow-up CT (average 2.8 months, range 1–8 months). Only in a limited number of cases was a follow-up cerebral angiogram examination feasible. In one patient, a follow-up cerebral angiogram was performed at the time of discharge (8 days), and two patients underwent a 6 month follow-up cerebral angiogram. None of the patients had rebleeding after treatment (CT follow-up range POD 0–8 months; mean follow-up time 2 months). There was no recanalization of the embolized aneurysm on any of the follow-up studies. Although small distal PICA cerebellar infarcts were observed on postprocedural head CT scan (four patients), these findings were not associated with any adverse clinical sequelae.
Follow-up clinical data
Clinical follow-up data were collected between 3 weeks and 10 months (mean 5.8 months) during clinic visit or by telephone interview. Clinical outcome was graded according to the modified Rankin Scale (mRS).
Six of the seven patients demonstrated no clinical adverse events from the procedure during hospital admission or on follow-up. At the most recent follow-up, mRS assessment showed an mRS score of 0–1 in four patients and an mRS score of 4–5 in two patients (primarily related to the initial SAH).
Discussion
Aneurysms of the vertebrobasilar system comprise fewer than 10% of all intracranial aneurysms;16 of these, only approximately 0.8% involve the cerebellar arteries.5 Intracranial aneurysms located in the distal posterior circulation vessels are even rarer, accounting for only 5% of all posterior circulation aneurysms.17 Overall, aneurysms located in the distal cerebellar arteries are extremely rare, ranging from 0.7% to 0.9%.18 The pathophysiology leading to the formation of a distal cerebellar artery aneurysm is not well known; suggested mechanisms include trauma or infection (mycotic).19 ,20 The role of hemodynamic stress in the formation of these lesions is unknown.
The prognosis is poor regarding the natural history of these aneurysms after rupture. If left untreated, ruptured aneurysms of the posterior circulation are associated with a high rebleeding rate, with the 30 day survival rate reported to be as low as 11%.21
Due to the rarity of these lesions, there are a paucity of data pertaining to treatment and specifically to feasibility, safety, and efficacy of endovascular therapy in this subset of aneurysm population. The long term treatment durability in terms of recurrence, retreatment, and rehemorrhage rates also remains unknown.
In general, surgical treatment of cerebellar artery aneurysms is considered challenging due to the close relationship of the these arteries with cranial nerves III–X. Furthermore, because most distal cerebellar artery aneurysms are secondary to arterial dissection encompassing the entire circumference of the vessel, surgical options such as clipping with salvage of the parent artery are frequently not possible20–22 and the only vessel preservation surgical treatment in most cases is trapping of the aneurysm in conjunction with a PICA–PICA bypass distal to the lesion.
On the other hand, endovascular coiling with parent artery preservation of fusiform or very wide neck, distal cerebellar artery aneurysms is extremely complicated or may even be impossible due to the lack of a distinct aneurysm neck. Additionally, the small caliber of the parent artery in most cases does not allow the use of remodeling techniques, such as balloon assistance or stent assistance.
Among different surgical and endovascular therapeutic strategies, distal superselective parent artery occlusion has been reported for the treatment of distal intracranial aneurysms,13 ,23 ,24 including some distal PICA aneurysms (table 2).
Series of ruptured peripheral posterior inferior cerebellar artery dissecting aneurysms endovascularly treated
Contralateral PICA, ipsilateral anterior inferior cerebellar artery, and superior cerebellar artery often have anastomotic connections with the affected PICA.19 ,31 In these cases, the PICA would be filled retrogradely from the pial collateral circulation if peripheral segments are iatrogenically occluded,13 ,23 ,24 minimizing the risk of infarct. Cases of cerebellar ischemia after distal occlusion of the PICA are described in the literature; however, the infarct volume was limited and thus well tolerated.22 ,23 Brainstem perforators arise from first three segments of the PICA, and all attempts should be made to preserve these segments during aneurysm embolization.32
In our series, utilizing Onyx 18 or 34 in the treatment of distal dissecting PICA aneurysms, a more controlled injection of the cohesive embolization material was attained when compared with glue. Furthermore, this decreases the risk of entrapment of the catheter, which is possible with an adhesive embolization liquid. Compared with other techniques, Onyx embolization has the advantage of increasing the rate of parent artery preservation, which minimizes the risk of symptomatic ischemic complications. This technique also has a lower risk of aneurysm rupture over endovascular coiling because there is no interaction between the coils with the weakened aneurysm wall. The high quality fluoroscopy and intermittent control angiographies during Onyx embolization reduces the risk of distal migration or proximal reflux of the embolizing agent.
We experienced no intraprocedural complications with Onyx embolization, which is consistent with the low complication rates reported in the literature.14 However, the procedure must be performed very carefully to avoid acute increases in intra-aneurysmal pressure. Additionally, for added safety or control, a balloon catheter may be placed in the VA across the ostium of the PICA. Liquid embolic reflux must be accurately controlled, especially proximal to the caudal loop, to avoid non-target embolization and perforator occlusion.
The are several limitations in our series, including the retrospective nature. There was an absence of standardization in the follow-up time points and a limited number of follow-up cerebral angiograms, lack of randomization with other therapeutic approaches, including surgical procedures and coil embolization, and a small number of patients. This makes estimation of the adverse event rate imprecise. Our preliminary case series illustrates a promising technique with clinical results in the treatment of a very challenging subtype of intracranial aneurysm.
Conclusions
Preliminary angiographic, diagnostic imaging, and clinical results of our series indicate that Onyx embolization of dissecting distal PICA aneurysms with parent artery preservation is an effective option with low procedure related morbidity and mortality rates, in cases in which surgical clipping or endovascular coiling of the aneurysmal sac is not suitable. Nevertheless, larger studies with standardized time points for follow-up are necessary to compare the different treatment options and definitively determine the complication rate of this technique.
References
Footnotes
Contributors ASP and FM: study design, data acquisition, data analysis, data interpretation, and manuscript preparation. AKW: study design, data interpretation, and manuscript revision. PK: data acquisition, data analysis, data interpretation, and manuscript revision. MJG: data analysis, data interpretation, and manuscript revision. SYH, JDL, MH, MP, and CB: data acquisition.
Competing interests AKW: consultant for Stryker Neurovascular; research grant from Philips Healthcare and Wyss Institute; and speaker for Harvard Postgraduate Course and Miami Cardiovascular Institute. MJG: consultant for Codman Neurovascular and Stryker Neurovascular; and research grants from NIH, eV3/Covidien Neurovascular, Codman Neurovascular, Fraunhofer Institute, Wyss Institute, Philips Healthcare, Stryker Neurovascular, Silk Road, and Lazarus-Effect. PK: consultant for Stryker Neurovascular, Covidien, and MicroVention.
Ethics approval The study was approved by the local institutional review board.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement Unpublished data may be available to academic researchers on a per request basis to the corresponding author.