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Interventional Neuroradiology logoLink to Interventional Neuroradiology
. 2020 Aug 25;26(5):566–574. doi: 10.1177/1591019920954082

Endovascular treatment for the flow-related aneurysm originating from an anterior inferior cerebellar artery supplying the cerebellar arteriovenous malformation

Kun Hou 1, Kan Xu 1, Xuan Chen 1, Yiheng Wang 1, Kailing Li 1, Jinlu Yu 1,
PMCID: PMC7645184  PMID: 32842831

Abstract

Background

When a flow-related aneurysm originates from an anterior inferior cerebellar artery (AICA) supplying the cerebellar arteriovenous malformation (AVM), the management becomes very complicated. Endovascular treatment (EVT) was an option, but no consensus has been achieved.

Methods and materials: A retrospective investigation was performed for patients with flow-related aneurysm originating from an AICA supplying the cerebellar AVM.

Results

Ten patients, harboring 13 aneurysms, were identified. Of the 5 a1 aneurysms, 2 underwent stent assisted coiling, 2 underwent parent artery occlusion (PAO), and 1 was intact. Of the 8 a2 aneurysms, 3 underwent coiling with preservation of the AICA, 3 underwent PAO with Onyx, 1 underwent PAO with coils, and 1 was intact. Seven patients underwent partial embolization of the cerebellar AVM, 3 were intact. One patient died 6 hours postoperatively for cerebellar AVM rebleeding. During a follow-up from 6 months to 6 years, 9 patients had favorable recovery.

Conclusion

For the flow-related aneurysm originating from an AICA supplying the cerebellar AVM, the EVT depends on the specific circumstances. When the aneurysm is located at the a1 segment, coiling of the aneurysm with preservation of the parent AICA should be performed. PAO is the last resort. When the a2 aneurysm is proximal to the internal auditory artery, coiling of the aneurysm with preservation of the AICA is preferred. When the aneurysm is distal to the internal auditory artery, PAO can be safely performed.

Keywords: Anterior inferior cerebellar artery, flow-related aneurysm, cerebellar arteriovenous malformation, endovascular treatment

Introduction

The cerebellum has 3 pairs of main feeding arteries: the superior cerebellar artery (SCA), the anterior inferior cerebellar artery (AICA), and the posterior inferior cerebellar artery (PICA). Generally speaking, the cerebellar arteries give rise to the brainstem branches at their proximal segments, with their distal segments supplying the cerebellum.1

Among the cerebellar arteries, the AICA is the most variable one and provides blood supply to some vital structures. The AICA always gives rise to the brainstem perforating arteries, internal auditory artery (IAA), recurrent perforating arteries, and subarcuate artery at its a1-a2 segments. Inadvertent occlusion of the AICA proximal to the a2 segment can lead to a set of symptoms as vertigo, tinnitus, hearing loss, facial paresis, Horner’s syndrome, and cerebellar ataxia.2,3

For flow-related aneurysms originating from an AICA supplying the cerebellar AVM, the management becomes very complicated. Because we have to take into account the IAA, the perforating branches to the brainstem, and the AVM at the same time. Currently, for the flow-related aneurysm originating from an AICA supplying the cerebellar AVM, endovascular treatment (EVT) and open surgery are available options.47

However, literature on the EVT for the flow-related aneurysm originating from an AICA supplying the cerebellar AVM is limited. In this article, we would conduct a retrospective single center study.

Materials and methods

A retrospective investigation was performed for patients admitted for cerebellar AVM between Jan 2015 and Oct 2019 in our institution. This study was approved by the Ethics Committee of our institution (Approval No. 2020-328). The inclusion criteria were: a) The AICA is the main feeding artery b) flow-related aneurysm was identified on the AICA, c) undergoing EVT for the flow-related aneurysm.

Determination of the bleeding source

For patients with cerebellar AVM and flow-related aneurysm, we define the bleeding source from the following aspects. a) For patients presented with only SAH, flow-related AICA aneurysm would be primarily considered the bleeding source. b) For patients presented with cerebellar hematoma with no or tiny SAH, AVM would be considered the bleeding source. c) For patients presented with cerebellar hematoma and evident or extensive SAH, the most neighboring lesion (aneurysm or AVM nidus) would be considered the bleeding source. d) For patients with multiple flow-related aneurysms, the size and morphology of the aneurysms and the spatial relationship of the aneurysms with the most concentrated site of hemorrhage would be comprehensively analyzed to identify the bleeding source. If the bleeding source could not be identified, more aggressive management targeting both the AVM and flow-related aneurysm would be adopted.

EVT for aneurysm

For ruptured aneurysms, when the aneurysm is on the a1 segment of AICA near the basilar artery-AICA junction, stent assisted coiling with preservation of the AICA is performed. In this case, the Solitaire stent (4 mm × 15 mm, Medtronic, Irvine, California, USA) would be deployed from the basilar artery to the AICA trunk. If the AICA can’t be preserved, parent artery occlusion (PAO) with coils is the last resort. For a2 segment aneurysms before the IAA, coiling of the aneurysm with preservation of the parent artery is preferred, or the parent artery is occluded with coils. For aneurysms distal to the IAA, PAO with coils or Onyx is performed. Of note, when performing PAO with Onyx, retrograde occlusion of the IAA should be avoided.

For unruptured AICA aneurysms, if the risk of EVT is high, a wait-and-see regimen would be adopted. For aneurysms other than AICA aneurysms, if the risk of EVT is low, one-stage treatment is performed, or a wait-and-see regimen would be adopted.

For patients who would undergo emergent stent assisted coiling of rupture intracranial aneurysms, loading dosage of dual antiplatelet agents (aspirin 300 mg, clopidogrel 300 mg) would be administered preoperatively. From the first postoperative day, dual antiplatelet (aspirin 100 mg/day, clopidogrel 75 mg/day) would be initiated and sustained for 3 months. And then, single antiplatelet regimen (aspirin 100 mg/day) would be sustained permanently.

EVT for AVM

For ruptured AVMs, obliteration with Onyx is performed. Occlusion of the aneurysm in the AVM nidus is in priority. If no aneurysm is identified in the AVM nidus, volume reduction or complete occlusion of the AVM can be performed. If the aneurysm is at the distal segment of AICA and close to the AVM nidus, obliteration of the aneurysm and AVM can be performed simultaneously. Retrograde occlusion of the IAA by embolization material should be avoided.

For unruptured AVMs, a wait-and-see regimen can be adopted. If the bleeding source could not be identified, more aggressive management targeting both the AVM and flow-related aneurysm would be adopted.

Results

General information

Ten patients aged between 30 and 65 (47.7 ± 7.8) years were identified (Table 1). The male to female ratio was 1:9. Eight patients were admitted for intracranial hemorrhage, of which 7 were subarachnoid hemorrhage, 1 was cerebellar hemorrhage. One patient presented with hemifacial spasm and another presented with trigeminal neuralgia. The Hunt-Hess grades were 0, 1, 2, and 3 in 2, 2, 3, and 3 patients, respectively.

Table 1.

Clinical data of the patients.

No. Age/sex Presentation Hunt-Hess grade AVM location Size AICA anatomy Segment and branch supplying the AVM Other AVM feeder Venous drainage Aneurysm Spetzler-Martin grade Bleeding source Treatment AICA preservation Complication Follow-up imaging Follow-up period mRS score
1 51/F SAH III Cerebellar hemisphere 1 cm×2 cm Bifurcate a4 segment of the caudal branch PICA Superficial vein: single cortical vein to venous sinus a1 segment near the AICA origin 1 Aneurysm Stent assisted coiling of aneurysm, partial Onyx embolization of the AVM through the AICA Preservation of the main trunk and the rostral branch, sacrificing the caudal branch distal to a4 segment No No recurrence of the aneurysm, no enlargement of the AVM 6 years 0
2 32/F SAH I Cerebellar hemisphere 2 cm×3 cm Single trunk a3 segment No Superficial and deep veins: cortical and brainstem veins to Galen vein 1 at a1 segment, 2 at a2 segment (1 premeatal, 1 postmeatal) 3 Aneurysm a1 intact, coiling of a2 aneurysms, preservation of AICA, partial Onyx embolization of the AVM through the AICA Sacrificing AICA distal to a3 segment No Died for cerebellar hemorrhage 6 hours postoperatively Not applicable Death
3 56/M Cerebellar hematoma III Cerebellar hemisphere and vermis 5 cm×6 cm Single trunk a2 segment PICA, SCA Superficial vein: multiple cortical veins to venous sinus a2 segment (postmeatal) 4 AVM Embolization of the aneurysm and partial occlusion of the AVM through the AICA and PICA with Onyx Sacrificing AICA distal to a2 segment No No recurrence of the aneurysm, no enlargement of the AVM 5 years 2
4 42/F Hemifacial spasm 0 Cerebellar hemisphere and cerebellopontine angle 4 cm×4 cm Bifurcate a2 segment of both the rostral and caudal branches No Superficial and deep veins: cortical and brainstem veins to Galen vein a1 segment near the AICA origin 4 Not applicable Stent assisted coiling of the aneurysm, partial embolization of the AVM through the AICA Preservation of the main trunk and the caudal branch, sacrificing the rostral branch distal to a2 segment No Disappearance of the deep venous drainage 5.5 years 0
5 50/F SAH II Cerebellar hemisphere 2 cm×3 cm Single trunk a3 segment SCA Superficial vein: single cortical vein to venous sinus 1 a2 segment (meatal), 1 distal SCA 2 Aneurysm Coiling of the aneurysm with preservation of the parent artery, AVM and SCA aneurysm intact Preservation of the main trunk No Recurrence of the aneurysm (refused to further treatment) 1.5 years 0
6 65/F SAH I Cerebellar hemisphere 0.5 cm×1 cm Single trunk a2 segment SCA Superficial vein: single cortical vein to venous sinus a2 segment (postmeatal) 1 Aneurysm Embolization of the aneurysm and partial occlusion of the AVM with Onyx Sacrificing AICA distal to a2 segment No No recurrence of the aneurysm, no enlargement of the AVM 5 years 0
7 50/F SAH III Cerebellar hemisphere and vermis 3 cm×4 cm Single trunk a2 segment PICA Superficial and deep veins: cortical and brainstem veins to Galen vein a1 segment 4 Aneurysm PAO of the aneurysm with coils, AVM intact PAO of a1 segment No No recurrence of the aneurysm, no enlargement of the AVM 5 years 0
8 51/F SAH II Cerebellar hemisphere 0.5 cm×1 cm Duplicate AICAs a2 segment of both AICAs No Superficial vein: single cortical vein to suboccipital venous plexus a2 segment of rostral branch (meatal) 1 Aneurysm Embolization of the aneurysm and partial occlusion of the AVM with Onyx Sacrificing superior AICA distal to a2 segment No No recurrence of the aneurysm, no enlargement of the AVM 5.5 years 0
9 50/F SAH 2 Cerebellar hemisphere 1 cm×1.5 cm Bifurcate a3 segment of the rostral branch No Superficial vein: single cortical vein to venous sinus a2 segment (premeatal) 1 Aneurysm PAO of the aneurysm with coils, AVM intact Preservation of the main trunk and the caudal branch, sacrificing the rostral branch distal to a2 segment No No recurrence of the aneurysm, no enlargement of the AVM 10 months 0
10 30/F Trigeminal neuralgia 0 Cerebellar hemisphere and cerebellopontine angle 3 cm×3 cm Single trunk a2 segment PICA, SCA Multiple superficial and deep veins 1 a1 segment, 1 a2 segment (meatal), 1 distal SCA 3 Not applicable Obliterating the a1 segment, reducing flow of SCA aneurysm and AVM PAO of a1 segment No No recurrence of the aneurysm, no enlargement of the AVM 6 months 0

AICA: anterior inferior cerebellar artery; AVM: arteriovenous malformation; F: female; M: male; mRS: modified Rankin Scale; PAO: parent artery occlusion; PICA: posterior inferior cerebellar artery; SAH: subarachnoid hemorrhage; SCA: superior cerebellar artery.

Angioarchitecture of the AVM

Six AVMs were located at the cerebellar hemisphere, 2 involved the cerebellar hemisphere and vermis, and 2 involved the cerebellar hemisphere and cerebellopontine angle. The AVM was fed solely by the AICA in 4 patients, conjointly by the PICA and/or SCA in 6 patients. The Spetzler-Martin grades were I, II, III, and IV in 4, 1, 2, and 3 patients. Five AVMs were drained by single superficial vein, 1 was drained by multiple superficial veins, 4 were drained by superficial and deep veins.

Angioarchitecture of the AICA and aneurysm location

The AICA was single trunk without bifurcation in 6 patients, single trunk with bifurcation in 3 patients. One patient had duplicate AICAs. The AICA fed the AVM from the a2, a3, and a4 segment in 6, 3, and 1 patient, respectively. Thirteen aneurysms were identified on the AICAs. Single AICA aneurysm was identified in 8 patients, multiple AICA aneurysms were identified in 2 patients (1 with 2 and another with 3). Two patients were concurrent with distal SCA aneurysm.

EVT for the aneurysm and AVM

Aneurysm

Of the 5 a1 aneurysms, 2 underwent stent assisted coiling, 2 underwent PAO, and 1 was intact. Of the 8 a2 aneurysms, 3 underwent coiling with preservation of the AICA, 3 underwent PAO with Onyx, 1 underwent PAO with coils, and 1 was intact (PAO at a1 segment). Of the 2 SCA aneurysms, 1 was occluded with Onyx and 1 was intact.

AVM

Seven patients underwent partial embolization, 3 were intact.

Outcome

One patient died 6 hours postoperatively for AVM rebleeding. During a follow-up from 6 months to 6 years, 9 patients had favorable recovery, of which 8 patients with a modified Rankin Scale score of 0 and 1 patient with a score of 2. Recurrence was identified in 1 a2 aneurysm. As the patient refused further management, conservative treatment was adopted.

Several illustrative cases were presented in Figures 1 to 4.

Figure 1.

Figure 1.

Perioperative imaging of case 2. (a–b) Angiogram of the right vertebral artery in anteroposterior view and 3-D reconstruction shows an AVM supplied by the AICA. Three flow-related aneurysms (arrow) (1 on a1, 2 on a2) are noted. (c) Angiogram in venous phase shows the AVM is drained both by the cortical and deep veins. (d–e) Both of the a2 segment aneurysms are coiled (asterisk). The AVM and draining vein (arrow) are embolized with Onyx. (f) Head computed tomography 6 hours postoperatively reveals cerebellar hemorrhage.

AICA: anterior inferior cerebellar artery; AVM: arteriovenous malformation.

Figure 2.

Figure 2.

Perioperative angiogram of case 7. (a) Angiogram of the left vertebral artery in AP view reveals an AVM mainly supplied by the left AICA. The a1 segment conforms to arterial dissecting. (b) Angiogram in venous phase shows the AVM is drained by cortical and deep Galen (asterisk) veins. (c) Postoperative angiogram shows the a1 segment is coiled. (d–f), Follow-up angiogram shows no recurrence of the a1 dissecting aneurysm. The AVM is also supplied by the posterior inferior cerebellar artery and drained by deep veins.

AICA: anterior inferior cerebellar artery; AP: anteroposterior; AVM: arteriovenous malformation.

Figure 3.

Figure 3.

Perioperative angiogram of case 8. (a–b) Angiogram of the left vertebral artery in AP view and 3-D reconstruction reveals right duplicate AICAs (asterisk). A dissecting aneurysm (arrow) is located at the a2 segment of the superior AICA. (c) Angiogram in late arterial phase reveals an AVM (ellipse) supplied by the duplicate AICAs and drained by suboccipital venous plexus (arrow). (d) The a2 aneurysm is completely obliterated. The AVM is also partially obliterated with Onyx via the superior AICA. (e) Follow-up angiogram shows the Onyx cast in vessel lumen. (f) Follow-up angiogram shows no recurrence of the aneurysm. The residual AVM is supplied by the inferior AICA.

AICA: anterior inferior cerebellar artery; AP: anteroposterior; AVM: arteriovenous malformation.

Figure 4.

Figure 4.

Endovascular treatment of case 1, 4, 5, and 9. (a) Case 1, Angiogram of the left VA in AP and lateral views shows an AVM supplied by the AICA. An a1 aneurysm located at the AICA’s origination from the basilar artery, which is coiled with stent assistance (arrow). The AVM is also partially embolized. (b) Case 4, Preoperative angiogram (left) of the left VA in AP view shows an AVM supplied by an enlarged AICA. An a1 aneurysm is also noted. Postoperative angiogram (right) of the left VA in AP view shows stent (arrow) assisted coiling of the aneurysm and partial embolization of the AVM with Onyx. (c) Case 5, Angiogram of the left VA in AP view (left) and 3-D reconstruction (right) reveals and AVM supplied by an enlarged AICA. An a2 aneurysm (arrow) is identified, which recurs after coiling (left). An unruptured distal SCA aneurysm (arrow) is also noted (right). (d) Case 9, Postoperative angiogram of the right VA in AP view shows an AICA aneurysm (arrow) at the rostral trunk is obliterated with coils (left). Follow-up angiogram shows no recurrence of the a2 aneurysm (right). The AVM is left intact.

AICA: anterior inferior cerebellar artery; AP: anteroposterior; AVM: arteriovenous malformation; VA: vertebral artery.

Discussion

Intracranial aneurysm can be identified in as high as 20% of the patients with brain AVM, the rate of which might be higher in patients with cerebellar AVM.8,9 Intracranial aneurysms concurrent with brain AVM could be classified into the intranidal, flow-related, and unrelated to the AVM aneurysms. The intranidal and flow-related aneurysms have higher incidence of rupture than those unrelated to the AVM nidus.9,10 Hence, the management of AVM concurrent with flow-related aneurysms is more complicated and should be more aggressive.

The cerebellum was supplied by three pairs of arteries: the SCA, AICA, and PICA. Among the 3 arteries, the AICA is most variable. It can be divided into four segments: a1 to a4. It gives rise to perforating arteries to the brainstem, choroidal branches to the tela and choroid plexus, and nerve-related arteries including the labyrinthine, recurrent perforating, and subarcuate arteries at the a1-a2 segments.11 During the EVT for vascular lesions involving the AICA, the a1-a2 segment should be preserved as far as possible.2 Hence, the EVT is very complicated for cerebellar AVM mainly supplied by the AICA and the concurrent flow-related AICA aneurysm.12

For AICA supplied cerebellar AVM and the concurrent flow-related AICA aneurysm, the principle of EVT is targeted management of the bleeding source. If the AVM has ruptured, embolization of the AVM, especially the focal weak structures of the AVM, is of utmost importance.13,14 If the AICA aneurysm is unruptured and distal to the IAA and near the AVM nidus, the aneurysm could be obliterated by the retrograde Onyx during embolizing the AVM.

If the unruptured AICA aneurysm is far from the AVM nidus, a wait-and see regimen can be adopted, as some unruptured aneurysms could experience spontaneous thrombosis after obliteration of the AVM.10,15 But, the remodeling and regression process of aneurysm goes slowly after AVM elimination. Catastrophic rupture should be considered for irregular and big feeding artery aneurysm, due to the increase in feeding artery pressure following endovascular embolization of the AVM.16 As presented in our illustrative case 2, the a1 aneurysm was left intact (Figure 1). When the flow-related aneurysm has ruptured, stent assisted coiling or PAO should be performed. The AVM can be partially embolized or left intact during management of the ruptured aneurysm.

In our case 1 and 4 (Figure 4(a) and (b)), as the a1 aneurysms are round-shaped dissection, stent assisted coiling of the aneurysms with preservation of the AICA was planned. In these two cases, as the caliber of the a1 segment was enlarged, the stent was successfully advanced from the basilar artery to the a1 segment. During follow-up catheter angiogram, the stent was still patent. In case 7 (Figure 2), as the a1 segment of AICA conformed to arterial dissection and lost normal morphology, no perforating artery might originate from the aneurysm, PAO of the AICA is a relative safe option. Besides, this AVM was also supplied by the PICA. Retrograde blood flow from the PICA supplied AVM could also perfuse the territory of AICA after obliteration of the a1 segment of AICA.

For a2 segment aneurysm, as illustrated in case 2 (Figure 1), satisfactory radiological embolization of the aneurysm with preservation of the AICA can be achieved. However, the long-term efficacy is uncertain. As illustrated in case 5 (Figure 4(c)), recurrence was noted during follow-up. Hence, for a2 segment aneurysm distal to the IAA, PAO is recommended. For a2 segment aneurysm proximal to the IAA, PAO is the last resort. In case 9, as the a2 segment was dissected, preservation of the AICA was difficult. Fortunately, the artery distal to the aneurysm could receive retrograde blood from the AVM even after proximal occlusion (Figure 4(d)).

The anatomical variation of AICA can also affect the strategy of EVT.2 As illustrated in case 8 (Figure 3), obliteration of the superior AICA with Onyx was performed because the superior AICA was high and might not give rise to the IAA. Hence, besides the location of aneurysm, the anatomical variation of AICA also affects the management.

For the treatment of cerebellar AVM, we adopted the following principle. If the AVM was unruptured, a wait-and-see regimen can be adopted. If the AVM had ruptured, targeted management of the weak point of the AVM should be performed. In case 2 (Figure 1), as she presented with SAH, distal AICA aneurysms were considered the source of bleeding. EVT of the distal AICA aneurysms was the main target. To promote spontaneous resolution of the proximal AICA aneurysm, the AVM was also simultaneously embolized with Onyx. However, the patient experienced fatal postoperative hemorrhage. Rupture of the AVM was considered the cause of delayed bleeding, which might be due to normal perfusion pressure breakthrough after occlusion of the draining vein.17 So, although EVT is a reasonable choice, open surgery remains an important option for the management of cerebellar AVM. Complete cerebellar AVM removal can avoid this fatal postoperative hemorrhage.

In conclusion, for the flow-related aneurysm originating from an AICA supplying the cerebellar AVM, the EVT depends on the specific circumstances. If the aneurysm has ruptured, treatment should be focused on the aneurysm. When the aneurysm is located at the a1 segment, stent assisted coiling with preservation of the parent AICA should be tried as far as possible. PAO is the last resort. For a2 segment aneurysm, when it is proximal to the IAA, coiling of the aneurysm with preservation of the AICA is preferred. When the aneurysm is distal to the IAA, PAO can be safely performed. During PAO for a1 segment aneurysm or a2 segment aneurysm proximal to the IAA, coils should be used. During PAO for a2 segment aneurysm distal to the IAA, both coils and Onyx can also be used. Retrograde obliteration of the IAA should be avoided when using Onyx.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Informed consent

Informed consent was obtained from all individual participants included in the study.

ORCID iDs

Kun Hou https://orcid.org/0000-0001-7112-7883

Jinlu Yu https://orcid.org/0000-0003-2329-7946

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