Korean Journal of Cerebrovascular Surgery 2004;6(2):122-129.
Published online September 1, 2004.
Clinical Features of Posterior Inferior Cerebella Artery Aneurysms.
Kim, Byong Cheol , Cho, Byung Moon , Ryu, Kyung Sik , Moon, Eng Myung , Ahn, Sung Ki , Lee, Ho Kook , Hong, Seung Koan , Park, Se Hyuck , Choi, Sun Kil , Oh, Sae Moon
Department of Neurosurgery, College of Medicine Hallym University, Seoul, Korea. nschbm@hanmail.net
Abstract
OBJECTIVE
The purpose of this study is to characterize the distribution of posterior inferior cerebellar artery (PICA) aneurysm, the computed tomography (CT) patterns of hemorrhage, and the clinical presentation thereof. METHODS: We reviewed the records 1050 patients with intracranial aneurysms treated at our institution between January 1999 and November 2003. Upon clinical review of radiological data and postoperative reports, we found 20 patients with PICA aneurysms. RESULTS: The incidence of PICA aneurysms was 1.9% of all intracranial aneurysms. The location of PICA aneurysms varied. Of the 20 PICA aneurysm cases, ruptured aneurysms accounted for 18 cases. Review of only these ruptured cases resulted in the following observations : Subarachnoid hemorrhage (SAH) was presented in 94.4% of cases. Isolated infratentorial and supratentorial SAH was present in 7 cases (38.9%) and 2 cases (11.1%), respectively. SAH involving the infratentorial and supratentorial region was present in 8 cases (44.5%). Intraventricular hemorrhage (IVH) with or without associated SAH was seen in 77.8% of cases, whereas isolated IVH was seen in only one case. Perimedullary large hematoma was present in 50% of cases, while the hematoma was consistently thicker on the aneurysm side. Hydrochephalus was present in 16 cases (88.9%). Although patients' postoperative outcomes were excellent or good in 70% of the above cases, initial angiograms failed to reveal ruptured PICA aneurysms in 3 cases. CONCLUSION: PICA aneurysm is rare in most aneurysm cases. However, awareness of a possibility of PICA aneurysm and its features are still nonetheless important. IVH and hydrocephalus are commonly presented with a ruptured PICA aneurysm and complete vertebral angiography is a required to recognize this condition.
Key Words: Posterior inferior cerebellar artery, Subarachnoid hemorrhage, Aneurysm

Introduction


  
Aneurysms of the Posterior Inferior Cerebellar Artery (PICA) are rare, accounting for 0.5-3% of intracranial aneurysms.12)19) PICA aneurysms occur in the most complex and variable course of the cerebellar arteries. Most lesions reside on the intracranial vertebral artery, adjacent to the origin of the PICA, but are sometimes difficult to visualize or are angiographically occult, especially when perforating vessels are concerned.
   PICA aneurysms can be easily missed on initial radiographic examination in patients with SAH. Both distal vertebral arteries need to be imaged in the setting of acute SAH to screen for the possibility of PICA aneurysm. Determining which of several aneurysms has ruptured is critical because the surgical approach to a ruptured PICA aneurysm is different from that for supratentorial aneurysms. Knowledge of computed tomography(CT) patterns of hemorrhage and site of ruptured PICA aneurysms would be useful for planning both the diagnostic evaluation and the surgical approach to patients with aneurismal SAH.
   Previously, clinical and radiological characteristics of PICA aneurysms were not sufficiently evaluated because of the limited number of cases. In this study, we have analyzed the clinical features, radiological findings, and postoperative results of 20 patients with PICA aneurysms. 

Clinical Materials and Methods

   We reviewed a total of 1050 patients who underwent surgical treatment for aneurysms at Hallym University Medical Center between January 1999 and November 2003 and found 20 patients with PICA aneurysm. We analyzed the clinical profiles, and reviewed imaging and radiological data and post-operative reports to form the basis of this report.
   In some cases, over the foramen magnum and permedullary region were absent or were degraded by beam hardening of motion artifact. In the former cases, we excluded those regions from the series. In the latter cases, we considered the findings as being negative for SAH.
   Of the 20 PICA aneurysms observed, there were 18 ruptured and 2 unruptured PICA aneurysms. We reviewed CT scans from patients who had ruptured PICA aneurysms confirmed via angiography. Presence or absence of hemorrhage along the convexity or in the following subarachnoid spaces were noted:cisterna magna, foramen magnum, perimedullary region, cerebellopontine cistern, prepontine cistern, perimesencephalic cistern, suprasellar cistern, sylvian fissure, and interhemispheric fissure. Specific sites of intraventricular hemorrhage(IVH) and ventriculomegaly consistent with hydrocephalus were also noted.
   The locations of the PICA aneurysms were divided into six segments:vertebral artery(VA)-PICA junction, the anterior and lateral medullary segments, the tonsillomedullary segment, the telovelotonsillar segment, and the cortical segment. The clinical outcomes were categorized according to the Glasgow Outcome Scale(GOS) as favorable(good recovery and moderate disability) or unfavorable(severe disability, vegetative state or dead). Case details are illustrated in Table 1


Illustrative Cases

1. Case 5:This case was treated by endovascular surgery
  
A 38-year-old female was admitted due to deteriorating mental state. At admission, her state was rated at Hunt-Hess (H-H) grade V state. The initial CT scan revealed SAH, cerebellar ICH and IVH. The patient had undergone external ventricular drainage. She underwent coil embolization but right PICA was occluded, and not visualized on the angiogram. The final outcome was death(Fig. 1).

2. Case 11:This is a case which an angiogram failed to detect PICA aneurysm
  
A 48-year-old man visited the hospital due to headache and mentality deterioation. There was no aneurysm detected in the initial angiogram but the aneurysm in the tonsilomedullary segment and vasospasm of the vertebral artery was identified on the follow-up angiogram, two weeks later. He had undergone the operation. The aneurysm was missed in the initial angiogram because of the oblique view of vertebral artery was not checked(Fig. 2).

3. Case 19:This is a case of unruptuered PICA aneurysm associated with ruptured anterior communicating artery(ACoA) aneurysm
  
A 61-year-old male was admitted to the hospital after experiencing sudden onset of severe headaches. The initial brain CT showed SAH. The ACoA aneurysm and left PICA aneurysm were detected in the angiogram and multi ditector (MD) CT angiogram. The left PICA aneurysm was on the VA-PICA junction. The patient had undergone pterional approach and ACoA aneurysm neck clipping. About 2 weeks later, he experienced another far lateral suboccipital craniotomy and PICA aneurysm neck clipping. His outcome was good recovery state with alert mentality(Fig. 3).

Results

   In our series, the incidence of PICA aneurysms was 1.9% of all intracranial aneurysms, including both ruptured and unruptured aneurysms. The mean age at presentation was 51.3 years(range of 24-75 years) and there were 5 male and 15 female patients. In ruptured aneurysms, the Hunt and Hess grade of the patients were as follows:two patients were grade 1, eight were grade 2, one was grade 3, five were grade 4, and two were grade 5(refer to case details in Table 1).

1. Initial CT findings of ruptured PICA aneurysms 
   Among 18 confirmed cases of ruptured PICA aneurysm, SAH was present in 17 cases(94.4%). SAH was observed in the isolated infratentorial region in 7 cases(38.9%) and in the isolated supratentorial SAH in 2 cases(11.1%). SAH involving the infratentorial and supratentorial region was present in 8(44.5%) cases. SAH along the convexity was present in 2 cases(11.1%). IVH with or without associated SAH was present in 14 cases(77.8%), whereas isolated IVH was observed in 1 case(5.6%). Hemorrhage was present in the fourth, third, and lateral ventricles in 77.8%, 55.5%, and 50.0% of the cases, respectively. Intraparenchymal hemorrhage was noted in 1 case. Perimedullary large hematoma was present in 50% of the cases(Table 2). 
   Examination of hematomas in cisterns revealed that the hematoma were consistently thicker on the aneurysm side, indicating a correlation between the side of the aneurysm and the direction of hematoma spread. In initial CT scan hydrochephalus was seen in 16 cases (88.9%). Images over foramen magnum and the perimedullary region were degraded by beam hardening of motion artifact for two patients, and hence deemed negative for SAH.

2. Angiographic findings of PICA aneurysms
  
Of the total of 20 PICA aneurysm cases, 8 cases(40.0%) were located in the VA-PICA, 4 cases(20%) in the lateral medullary segment, 3 cases(15.5%) in the tonsillomedullary segment, 3 cases(15.5%) in the telovelotonsillary segment, and 2 cases(10.0%) in the cortical segment. Ninety percent of the aneurysms were saccular, arising at branching points or sharp hemodynamic angles; 10% were fusiform lesions(one in the VA-PICA junction and the other in the tonsillomedullary segment). The size of the aneurysms ranged from 3 mm to 25 mm(mean 8.45 mm). More aneurysms were located on the left PICA than on the right(L:R=12:8). Associated unruptured aneurysms of anterior circulation were noted in three cases and associated vascular anomalies were identified in five cases(three were contralateral hypoplastic AICA, PICA, or VA, one was contralateral PICA was absent and its territory was supplied by the ipsilateral PICA, and one was ipsilateral VA aplasia). In one case associated with ipsilateral cerebellar arterivenous malformation(AVM) was found to be supplied by the superior cerebellar artery(SCA) and PICA harboring the aneurysm. The initial angiogram failed to reveal a ruptured PICA aneurysm in 3 cases.

3. Treatment and outcomes of PICA aneurysms
  
All patients diagnosed with acute hemorrhage were placed on routine procedures including bed rest, blood pressure control and pain control if required. Nearly fifty-six percent of the patients with acute SAH required emergency ventriculostomy for hydrocephalus. In 7 cases(38.9%), patients required a permanent shunt. Nineteen of the total 20 patients were treated by surgery. Combinations of midline, lateral, and far-lateral suboccipital skull-base exposures were used, depending on the site of origin of the aneurysm from PICA. Of the 19 cases treated by surgery, 16 cases(84.2%) were clipped, 2 cases(10.5%) were wrapped, and one case was treated by endovascular surgery. Two patients were noted to have severe angiographic vasospasm.
   Sixty-five percent of the patients(13 of 20) experienced some consequences of their disease and/or complications during the course of their treatment, including;pneumonia (two cases), sepsis(three case), meningitis(three cases), cerebrospinal fluid collection of operation site(three cases), transient he-miparesis(one case), and double vision(two cases). Two patients died. One patient was diagnosed with VA-PICA aneurysm and H-H grade V. Surgery was not performed on this patient due to a pre-existing cardiac problem and old age creating a high risk of complications. The other deceased patient was treated by endovascular surgery. Treatment was complicated by infarction in the PICA territory due to coil occlusion. However, overall, the outcome was favorable(good recovery and moderate disability) in 70.0% of cases(Table 1). 

Discussion

   Aneurysms arising from PICA are uncommon. In our series, the incidence of PICA aneurysms was 1.9% of all intracranial aneurysms, including both ruptured and unruptured aneurysms. The first case of an aneurysm arising from the origin of the PICA has been credited to Cruveilhier12) in 1829 and first reported a distal segment of the PICA aneurysm in 1864.7)
   The PICA is the largest and most distal branch of the VA with a highly variable normal anatomy. It is not unusual for the PICA to be absent. When the PICA is absent, the anterior inferior cerebellar artery(AICA), or less commonly, the superior cerebellar artery, supplies the territory normally nourished by the PICA.20) The frequent aberrancy of PICA may be a result of the plexiform fetal development of the posterior fossa circulation(either absent, misplaced, communicating,9) extracranial origin,16) double origin,24) or multiple). In our cases, various vascular anomalies are noted, such as contralateral hypoplastic AICA, PICA, VA, or contralateral PICA being absent and its territory supplied by the ipsilateral PICA and associated with AVM and unruptured aneurysms of the anterior circulation.
  
The PICA has been divided into five segments12)18) and two loops, based on its relationship to the medulla oblongata and the cerebellum. The anterior medullary, lateral medullary, and tonsillomedullary segments(including the caudal loop) may give rise to brainstem perforators. The telovelotonsillar (including the cranial loop) and cortical segments do not have the same effect. It has, therefore, been suggested that occlusion of the PICA proximal to the choroidal points can be life threatening.12)
   Aneurysms were also classified according to their potential evolution into saccular and fusiform types. Viewed through an angiograph, dissections may appear as a saccular or fusiform widening of the vessel, usually in association with a proximal stenosis. The majority arise at the VA-PICA junction or on the first medullary segments.6)12) Although saccular intracranial aneurysms usually arise from the bifurcation of arteries, PICA aneurysms occasionally have no associated branching artery around the aneurysmal neck.17)18) Horiuchi et al.10) reported that 75% of patients with the distal PICA aneurysms have no branching artery. Such branchless aneurysms can arise from a straight portion of the artery in addition to a turning point.12)23) Hemodynamic stress or congenital factors could be involved in the branchless aneurysm formation. The PICA develops from plexiform formations around the brainstem, which may lead to many anatomical variations of the PICA. Such developmental characteristics would act as an important congenital factor for aneurysm formation at the straight portion of the arteries.15) In this series, 18 aneurysms were saccular, and 2 aneurysms fusiform(one in the VA-PICA junction and the other in the tonsillomedullary segment). A left dominance was reported in patients with dissecting distal PICA aneurysm.5) The left dominance of the dissecting aneurysm may have been caused by more hemodynamic stress than on the right side because the left vertebral artery was well developed. The location of PICA aneurysms varied from the VA-PICA to cortical segment. Distal PICA aneurysms are rare, their incidence has been reported to range between 0.28 and 1% of all intracranial aneurysms.10)17)19)27)33) According to Lewis et al.,17) 35% of distal PICA aneurysms affected the telovelotonsillar segment. In this series, the locations of PICA aneurysms were 8(40.0%) in the vertebral-PICA junction, 4(20.0%) in the lateral medullary segment, 3(15.5%) in the tonsillomedullary segment, 3(15.5%) in the telovelotonsillary segment, and 2(10.0%) in the cortical segment. In other words, 12(60.0%) of 20 cases were peripheral PICA aneurysms.
  
Determining which of the multiple aneurysms has ruptured might be guided by the knowledge of typical patterns of hemorrhage seen in ruptured PICA aneurysms. The largest series in the literature detailing CT patterns of hemorrhage in ruptured PICA aneurysms describes 44 cases.14) Kallmes et al.14) found that ruptured PICA aneurysms almost always coexist with hydrocephalus and IVH, as seen in 93% of cases, and almost never coexist with SAH along the convexity. In those cases, posterior fossa SAH was present in 42(95%) of 44 cases. In addition, 13(30%) of 44 cases, SAH was limited to the posterior fossa alone, without evidence of supratentorial SAH. 
   Early CT literature suggested that extensive supratentorial SAH was unusual with ruptured posterior fossa aneurysms. It was present in 9% of cases.25) More recent literature has noted extensive supratentorial SAH in as many as 50% of ruptured posterior fossa aneurysms. Kalles et al.14) found that extensive supratentorial SAH was present in 70% of cases. In our series, SAH was present in 17 out of 18 cases(isolated IVH was seen in only one case), and observed in isolated infratentorial region in 7 cases(38.9%). Nearly 56% of the reviewed cases showed evidence of supratentorial SAH. Our results are similar to previous reporting on this topic.
   The above results should discourage practitioners from discounting ruptured PICA aneurysms in the setting of extensive supratentorial SAH. Convexity SAH may result from the flow of CSF containing hemorrhage within the subarachnoid space. In our series, convexity SAH was present in 2 cases(11.1%). A CT scan taken relatively early after an aneurysm rupture may have contributed to the low frequency of convexity SAH in our series. SAH extending to the level of the cerebral convexity was rare in ruptured PICA aneurysms.
  
Bleeding from proximal PICA segment aneurysms, including the VA-PICA junction, usually produces clots within the ipsilateral basal cisterns, with or without extension into the fourth ventricle.14) Kayama et al.14) reported that in the case of VA-PICA aneurysms, hematomas in the ambient cistern were thicker on the aneurysm side. Lesions arising distal to the medullary PICA segments, particularly those originating from the caudal loop or at a low origin of the PICA are more commonly associated with hemorrhage extending into the fourth ventricle.14)25) Isolated IVH without SAH is uncommonly associated with aneurysms of the VA-PICA junction(less than 5% of ruptured PICA aneurysms).2)12)14)28)31) Previous reports have noted high frequencies of IVH associated with ruptured PICA aneurysms. Sadato et al. found IVH 100% of cases.25) Kallmes et al.14) found that ruptured PICA aneurysms almost always coexist with hydrocephalus and IVH, as seen in 93% of cases. Previous reports have noted the frequency of hydrocephalus among ruptured aneurysms of all locations to be approximately 30% and more commonly(29-55%) with ruptured posterior fossa aneurysms than other types.21) It is likely that the higher frequency of hydrocephalus associated with PICA aneurysms compared with other is related to the high frequency of IVH in ruptured PICA aneurysms. In the cases under study, IVH with or without associated SAH was present in 77.8% of cases, whereas isolated IVH was seen in only one case. Hydrocephalus was seen in 88.9% of cases. The high frequency of IVH and hydrocephalus may result from the close association between the PICA and the foramen of Luschka and Magendie, with retrograde flow of extravasated blood into the fourth ventricle.25)29) Because this series was limited to 20 cases, we cannot comment on specificity of a given CT and angiographic finding for ruptured PICA aneurysms. However, IVH and hydrocephalus are more common in ruptured PICA aneurysms than in ruptured supratentorial aneurysms.29)
  
Complete four-vessel angiography is important in all cases of an aneurysmal SAH, but bilateral vertebral arteriography is particularly essential with aneurysms of PICA aneurysms. The bilateral vertebral angiogram will also provide valuable information detailing the vascular anatomy of the posterior fossa, such as the presence of the contralateral PICA or collateral circulatory patterns. Even with adequate initial angiography, PICA aneurysms may not be seen initially, as this occurred with patients in this study. Perhaps due to the localized vasospasm or a clot in the aneurysm neck,26) PICA aneurysms may have been difficult to detect. The initial angiogram failed to reveal a ruptured PICA aneurysm in 3 cases of this series. Special attention to the PICA should be required in patients with unknown origin of SAH. Recently, multi-detector CT(MD CT) angiography has been proposed as a substitute for conventional angiography for patients with SAH.3)
  
The first surgical treatment of a peripheral PICA aneurysm is accredited to Olivecrona in 1932.1) DeSaussure et al.4) in 1958 reported two PICA aneurysms that had been defined by preoperative angiography and then trapped surgically. An understanding of the PICA anatomy is essential to formulating a therapeutic plan. The best treatment option for a PICA aneurysm depends on a number of factors, including aneurysm location, morphological structure, and clinical presentation. The ideal treatment of a truly saccular lesion is clipping or endovascular obliteration of the aneurysm neck. A different strategy must be considered, however, whenever the dissection or when a seemingly saccular lesion cannot be clipped without parent vessel occlusion. The PICA segments proximal to the choroidal point give off important perforator branches to the brainstem and the choroidal plexus of the fourth ventricle. Occlusion of the PICA proximal to



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