Comparison of endovascular and microsurgical management of 208 basilar apex aneurysms

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OBJECTIVE

The deep and difficult-to-reach location of basilar apex aneurysms, along with their location near critical adjacent perforating arteries, has rendered the perception that microsurgical treatment of these aneurysms is risky. As a result, these aneurysms are considered more suitable for treatment by endovascular intervention. The authors attempt to compare the immediate and long-term outcomes of microsurgery versus endovascular therapy for this aneurysm subtype.

METHODS

A prospectively maintained database of 208 consecutive patients treated for basilar apex aneurysms between 2000 and 2012 was reviewed. In this group, 161 patients underwent endovascular treatment and 47 were managed microsurgically. The corresponding records were analyzed for presenting characteristics, postoperative complications, discharge status, and Glasgow Outcome Scale (GOS) scores up to 1 year after treatment and compared using chi-square and Student t-tests.

RESULTS

Among these 208 aneurysms, 116 (56%) were ruptured, including 92 (57%) and 24 (51%) of the endovascularly and microsurgically managed aneurysms, respectively. The average Hunt and Hess grade was 2.4 (2.4 in the endovascular group and 2.2 in the microsurgical group; p = 0.472). Postoperative complications of cranial nerve deficits and hemiparesis were more common in patients treated microsurgically than endovascularly (55.3% vs 16.2%, p < 0.05; and 27.7% vs 10.6%, p < 0.05, respectively). However, aneurysm remnants and need for retreatment were more common in the endovascular than the microsurgical group (41.3% vs 2.3%, p < 0.05; and 10.6% vs 0.0%, p < 0.05, respectively). Stent placement significantly reduced the need for retreatment. Rehemorrhage rates and average GOS score at discharge and 1 year after treatment were not statistically different between the two treatment groups.

CONCLUSIONS

Patients with basilar apex aneurysms were significantly more likely to be treated via endovascular management, but compared with those treated microsurgically, they had higher rates of recurrence and need for retreatment. The current study did not detect an overall difference in outcomes at discharge and 1 year after either treatment modality. Therefore, in a select group of patients, microsurgical treatment continues to play an important role.

ABBREVIATIONS ASA = acetylsalicylic acid; CTA = CT angiography; DSA = DS angiography; GOS = Glasgow Outcome Scale; HH = Hunt & Hess; MRA = MR angiography; PEG = percutaneous endoscopic gastrostomy; SAH = subarachnoid hemorrhage.

OBJECTIVE

The deep and difficult-to-reach location of basilar apex aneurysms, along with their location near critical adjacent perforating arteries, has rendered the perception that microsurgical treatment of these aneurysms is risky. As a result, these aneurysms are considered more suitable for treatment by endovascular intervention. The authors attempt to compare the immediate and long-term outcomes of microsurgery versus endovascular therapy for this aneurysm subtype.

METHODS

A prospectively maintained database of 208 consecutive patients treated for basilar apex aneurysms between 2000 and 2012 was reviewed. In this group, 161 patients underwent endovascular treatment and 47 were managed microsurgically. The corresponding records were analyzed for presenting characteristics, postoperative complications, discharge status, and Glasgow Outcome Scale (GOS) scores up to 1 year after treatment and compared using chi-square and Student t-tests.

RESULTS

Among these 208 aneurysms, 116 (56%) were ruptured, including 92 (57%) and 24 (51%) of the endovascularly and microsurgically managed aneurysms, respectively. The average Hunt and Hess grade was 2.4 (2.4 in the endovascular group and 2.2 in the microsurgical group; p = 0.472). Postoperative complications of cranial nerve deficits and hemiparesis were more common in patients treated microsurgically than endovascularly (55.3% vs 16.2%, p < 0.05; and 27.7% vs 10.6%, p < 0.05, respectively). However, aneurysm remnants and need for retreatment were more common in the endovascular than the microsurgical group (41.3% vs 2.3%, p < 0.05; and 10.6% vs 0.0%, p < 0.05, respectively). Stent placement significantly reduced the need for retreatment. Rehemorrhage rates and average GOS score at discharge and 1 year after treatment were not statistically different between the two treatment groups.

CONCLUSIONS

Patients with basilar apex aneurysms were significantly more likely to be treated via endovascular management, but compared with those treated microsurgically, they had higher rates of recurrence and need for retreatment. The current study did not detect an overall difference in outcomes at discharge and 1 year after either treatment modality. Therefore, in a select group of patients, microsurgical treatment continues to play an important role.

ABBREVIATIONS ASA = acetylsalicylic acid; CTA = CT angiography; DSA = DS angiography; GOS = Glasgow Outcome Scale; HH = Hunt & Hess; MRA = MR angiography; PEG = percutaneous endoscopic gastrostomy; SAH = subarachnoid hemorrhage.

Basilar apex aneurysms account for approximately 5%–8% of all cerebral aneurysms.5,7 They present numerous microsurgical challenges because of their deep and difficult-to-reach location, along with the presence of critical adjacent cerebrovascular structures, including perforating arteries.3,6 Lack of microsurgical expertise has further decreased the use of open techniques for clip ligation of these aneurysms. Morbidity and mortality for treatment of ruptured and unruptured aneurysms of this type are as high as 30.6% and 17.5%, respectively.16 As a result, there has been a rapid transition to endovascular management for aneurysms at this location.10

Unfortunately, recent studies have reported recurrence rates as high as 41%, with 26% needing retreatment during long-term follow-up after endovascular treatment.4 Endovascular stent placement has been used to make endovascular treatment a viable option in wide-necked aneurysms and allow for increased packing densities. In this paper we examine the outcomes of patients treated at our institution and the need for retreatment of basilar apex aneurysms based on their hemorrhage status, other presenting data, and treatment modality. Importantly, the unique feature of this report is that it reflects the results of a balanced, multidisciplinary, and collaborative approach among microsurgeons and endovascular interventionists toward these aneurysms.

Methods

Patient Population

Following approval of the study from the Indiana University IRB, we performed a retrospective review of all patients with intracranial aneurysms whose records have been prospectively maintained in our institution's database. This database includes information on all patients since 1977 presenting with intracranial aneurysms at either of two tertiary care hospitals in Indianapolis, Indiana: IU Health Methodist Hospital, and St. Vincent Hospital. A cohort of 208 consecutive patients was identified who underwent treatment for their basilar apex aneurysms from January 2000 to December 2012. We believe this time period allows a good comparison of relatively uniform and recent endovascular and microsurgical techniques. The diagnosis of a basilar apex aneurysm was made based on CT angiography (CTA), MR angiography (MRA), or digital subtraction angiography (DSA). If treatment was necessary, the patient was followed through hospitalization and follow-up outpatient visits. Patients who harbored an untreated basilar apex aneurysm or an aneurysm associated with an arteriovenous malformation were excluded from this study.

In this group, 23% (n = 47) of the patients underwent microsurgical clip ligation, and 77% (n = 161) received endovascular treatment for their aneurysms. An interventional neuroradiologist and a cerebrovascular neurosurgeon reviewed all cases before definitive treatment was rendered. Endovascular embolization was usually preferred over microsurgical treatment if the morphology of the aneurysm was appropriate for endovascular treatment, especially if the patient was older than 50 years of age. The criteria for application of the microsurgical approach included: an expectation that the treating physician would not be able to access or adequately place stable coils within the aneurysm; young age of the patient; anterior projection of the aneurysm; and unruptured status of the aneurysm. Essentially, we practiced the philosophy of “endovascular-first” in most patients, and especially those older than 50 years of age.

Data were recorded from admission until hospital discharge, death, or loss to follow-up. Presentation characteristics included patient age, sex, race, comorbidities, presenting symptoms, Hunt and Hess score (HH) on admission,14 number of aneurysms, aneurysm size (mm), and Fisher grade.8,18

Complications studied included medical (cardiac event, deep vein thrombosis, pulmonary embolus, pulmonary edema, or respiratory insufficiency), rehemorrhage, seizure, hydrocephalus, cerebral vasospasm, radiographic infarction, clinical stroke, cranial nerve deficits, paresis, and need for tracheostomy, permanent CSF diversion, or percutaneous endoscopic gastrostomy. Outcomes recorded include death before hospital discharge; patient Glasgow Outcome Scale (GOS) score17 at discharge, 6 months, and 1 year after treatment; and the occurrence of remnant or recurrent aneurysm neck, coil compaction, and need for retreatment. The method of embolization (coiling alone or stent-assisted coiling) and surgical approach (pterional or subtemporal) were recorded for all endovascular and microsurgical cases.

Microsurgical Treatment

From 2000 to 2012, we used relatively uniform microsurgical techniques for these cases. To be considered for microsurgical treatment, the aneurysm had to be within 5 mm above or below the posterior clinoid and point superiorly or anteriorly. Patients undergoing microsurgery underwent either a pterional craniotomy and generous exposure of their aneurysm following Sylvian fissure dissection, or a middle fossa craniotomy with subtemporal exposure of the basilar apex. A pterional craniotomy was used in most patients based on the preference of the involved surgeons. The additional orbitozygomatic osteotomy was rarely used, and mainly for “high-riding” aneurysms. Temporary occlusion of the basilar artery was obtained using a temporary clip or, occasionally, endovascular balloon occlusion when needed (Fig. 1). Etomidate (0.4 mg/kg) was administered 2 minutes before temporary clip application or inflation of the balloon, and repeated (0.2 mg/kg) every 20 minutes during the period of temporary occlusion.

FIG. 1.
FIG. 1.

Upper: The pterional approach commonly uses the opticocarotid pathway for aneurysm neck exposure and proximal vascular control. Lower: The subtemporal approach is more favorable for low-lying basilar bifurcation aneurysms; it requires temporal lobe retraction and more direct manipulation of the oculomotor nerve. Copyright Aaron Cohen-Gadol. Published with permission from the Neurosurgical Atlas. Figure is available in color online only.

In rare instances, hypothermic arrest was used (4%, n = 2). In most cases, straight fenestrated and/or simple straight clips were deployed. Careful microsurgical inspection of the origin of the basilar apex and the aneurysm neck was performed to avoid any significant compromise in the origin of the posterior cerebral arteries or perforator occlusion after clip placement (Fig. 2). Most patients underwent intraoperative blood flow micro-Doppler ultrasonography to ensure blood flow within the basilar apex and posterior cerebral artery after clip placement. Since 2007, we have used intraoperative indocyanine green or fluorescein videoangiography for qualitative assessment of blood flow within the parent, branching, and perforating vessels and to evaluate aneurysm obliteration. Select aneurysms underwent intraoperative cerebral DSA.

FIG. 2.
FIG. 2.

Methodologies for clip ligation of basilar bifurcation aneurysms via the pterional (upper) and subtempral (lower) approaches are illustrated. The inset demonstrates the closed microsurgical aneurysm clip with exclusion of the aneurysm from circulation and preservation of the parent vessel. Copyright Aaron Cohen-Gadol. Published with permission from the Neurosurgical Atlas. Figure is available in color online only.

Patients were evaluated at follow-up by the treating physician at 3 months, 6 months, and 1 year following treatment, and then periodically based on the preference of the physician. Physical examinations and clinical outcomes were determined by the treating physician. Typical follow-up imaging studies (DSA, CTA, or MRA) were obtained immediately postoperatively and at 1year after treatment followed by periodic imaging. Interpretation of the imaging studies was performed by board-certified neuroradiologists.

Endovascular Treatment

All endovascular procedures were performed with the patient under general anesthesia. Microcatheter, coil, and stent (when indicated) placements were performed with DSA and roadmap technology. For elective cases, patients were given a 5000-unit bolus of heparin after vascular access was obtained.

Stents were used in the setting of dome-to-neck ratios less than 1.5 and aneurysm neck diameters greater than 4 mm, and most typically in the elective setting. When a stent was anticipated, patients were administered daily doses of 325 mg of acetylsalicylic acid (ASA) and 75 mg of clopidogrel for 5 days prior to the procedure. Alternatively, 325 mg of ASA and 600 mg of clopidogrel were given within 24 hours prior to treatment.

Since 2010, a VerifyNow P2Y12 (Accumetrics) point-of-care test has been used by our practice. If patients were found to have a subtherapeutic level on their current regimen, they were given an extra 150-mg dose of clopidogrel. If they still had a subtherapeutic level the following day, patients were switched to prasugrel 10 mg daily. For patients who presented with aneurysmal subarachnoid hemorrhage (SAH), heparin was withheld until the dome or site of the anticipated rupture was protected with coils. Although balloon reconstruction was infrequently required, it was preferred over the use of antiplatelet agents and stent placement during the acute aneurysmal SAH hemorrhage period. All patients underwent postoperative DSA, CTA, or MRA for confirmation of aneurysm obliteration.

Statistical Analysis

Minitab (version 16, Minitab Inc.) was used for statistical analyses. Pearson's chi-square test of independence (χ2) and Student t-test were used to examine the main effects of aneurysm management (endovascular, microsurgical) on presentation characteristics, postoperative complications, and outcomes. Chi-square and t-tests also were used to compare coiling alone versus stentassisted coiling, as well as pterional versus subtemporal microsurgical approaches. Probability values associated with Fisher's exact test were reported for 2 × 2 χ2 tables. Yates correction for continuity was used if expected frequencies were less than 5 in 2 × 2 χ2 tables.

Results

In the database of 2529 patients, 208 consecutive basilar apex aneurysms were studied. Among these 208 patients, 161 received endovascular intervention and 47 underwent microsurgery (Table 1). The average patient ages were 54.1 and 46.8 years (p < 0.05) for those who underwent endovascular and surgical clip ligation, respectively. Sex, race, hypertension, smoking, hyperlipidemia, diabetes, and family history of aneurysms were not statistically different between the treatment groups (Table 1). Among all patients in both groups, 116 (56%) presented with SAH with an average HH grade of 2.4, average Fisher grade of 3.2, and average aneurysm size of 8.3 mm (Table 1). Importantly, evidence of SAH, Fisher grade, and aneurysm size did not significantly differ between the 2 treatment groups.

TABLE 1.

Presentation characteristics by treatment type

VariableEndovascularMicrosurgicalTotalStatisticp Value
No. of patients (%)161 (77.4)47 (22.6)208 (100.0)
Age (yrs)
  Mean (SD)54.1 (10.3)46.8 (8.0)52.4 (10.3)t = −5.090.000
  Range31–7832–6431–78
% female71.476.672.6χ2 = 0.4880.579
% Caucasian97.5100.098.1χ2 = 0.2230.637
% family aneurysm history11.86.410.6χ2 = 1.1290.420
% hypertension41.640.441.4χ2 = 0.0211.000
% smoking70.266.069.2χ2 = 0.3050.593
% hyperlipidemia13.710.613.0χ2 = 0.2950.805
% diabetes mellitus5.68.56.3χ2 = 0.5300.496
% symptomatic3.12.12.9χ2 = 0.1241.000
% ruptured57.551.156.0χ2 = 0.6110.504
% SAH from another source1.90.01.5χ2 = 0.0630.802
Mean (SD) admission HH grade*2.4 (1.3)2.2 (1.4)2.4 (1.3)t = −0.730.472
Mean (SD) Fisher grade3.2 (0.8)3.2 (0.7)3.2 (0.8)t = −0.410.684
Mean (SD) no. of aneurysms1.4 (0.8)1.4 (0.8)1.4 (0.7)t = 0.600.550
Mean (SD) basilar tip aneurysm size in mm8.2 (4.8)8.6 (5.0)8.3 (4.8)t = 0.380.709
Boldface type indicates statistical significance.

Ruptured cases only.

Ruptured aneurysms are specific to the basilar apex, whereas SAH cases refer to aneurysms from another source.

We analyzed postoperative complications based on the mode of treatment as shown in Table 2. Duration of hospital stay for all patients was 12.9 ± 12.1 days; there was no statistical difference between the 2 treatment groups. Cranial nerve deficits and mono- or hemiparesis were more common in the microsurgical group: 16.2% versus 55.3% (p = 0.000), and 10.6% versus 27.7% (p = 0.008), respectively. The incidence of rehemorrhage (1.4%), seizures (4.3%), hydrocephalus (27.4%), shunt placement (9.1%), vasospasm (16.4%), radiographic infarction (13.5%), clinical stroke (12%), tracheostomy (3.9%), and percutaneous endoscopic gastrostomy (PEG; 6.7%) were not statistically different between the 2 groups.

TABLE 2.

Postoperative complications by treatment type

VariableEndovascularMicrosurgicalTotalStatisticp Value
No. of patients (%)161 (77.4)47 (22.6)208 (100.0)
Mean (SD) length of inpatient stay in days12.3 (11.4)14.9 (14.3)12.9 (12.1)t = 1.160.248
% medical complications*29.234.030.3χ2 = 0.4050.589
% rehemorrhage1.90.01.4χ2 = 0.0610.805
% seizure4.44.34.3χ2 = 0.0011.000
% hydrocephalus29.221.327.4χ2 = 1.1460.354
% shunt placement8.710.69.1χ2 = 0.1650.774
% vasospasm16.217.016.4χ2 = 0.0201.000
% radiographic infarction12.417.013.5χ2 = 0.6600.467
% clinical stroke11.214.912.00χ2 = 0.4740.457
% cranial nerve deficits16.255.325.0χ2 = 29.7690.000
% paresis10.627.714.4χ2 = 8.6190.008
% tracheostomy3.16.43.9χ2 = 1.0570.384
% PEG6.28.56.7χ2 = 0.3060.524
Boldface type indicates statistical significance.

Cardiac event, deep vein thrombosis, pulmonary embolus, pulmonary edema, or respiratory insufficiency.

Although not statistically significant, there were no postoperative rehemorrhages in the microsurgical group, whereas there were 3 in the endovascular group (Table 2). One patient presented with HH Grade III, was treated by endovascular coiling, and subsequently developed a left temporal hemorrhage. A repeat angiogram demonstrated occlusion of the aneurysm. The patient was observed and stabilized with a discharge GOS score of 3. A second patient who presented with HH Grade III suffered from an intraprocedural rehemorrhage following placement of 2 coils. Protamine was immediately administered and a follow-up angiogram demonstrated aneurysm occlusion. This patient was also discharged with a GOS score of 3. The third patient presented with HH Grade I and had a ruptured aneurysm requiring stent coiling using clopidogrel and ASA. The aneurysm harbored calcium in the neck and was deemed not suitable for clip ligation. Thirty-six hours after endovascular treatment, this patient suffered a rehemorrhage. A repeat angiogram demonstrated occlusion of the aneurysm. The patient was later found to have severe vasospasm and died.

As shown in Table 3, there was no statistically significant difference in mean GOS score at discharge or 1 year after either treatment method (4.1 ± 1.1, p = 0.287, and 4.6 ± 0.7, p = 0.173, respectively). The incidence rate of mortality before discharge was 4.8%, unrelated to the mode of treatment. Aneurysmal remnant (41.3% vs 2.3%, respectively; p < 0.05), recurrence (17.5% vs 0.0%, respectively; p = 0.001), and retreatment (10.6 vs 0.0, respectively; p = 0.015) were more common in the endovascular group. The average follow-up duration was 31.6 ± 35.7 months and 52.5 ± 43.5 months for endovascular (143/161 patients) and microsurgical (43/47 patients) cases, respectively.

TABLE 3.

Outcomes by treatment type

VariableEndovascularSurgicalTotalStatisticp Value
Overall outcome
  No. of patients (%)161 (77.4)47 (22.6)208 (100.0)
  Mean (SD) GOS score at discharge4.1 (1.2)3.9 (1.1)4.1 (1.1)t = −1.070.287
  Mean (SD) GOS score at 1 yr4.7 (0.6)4.4 (0.8)4.6 (0.7)t = −1.340.173
  % mortality prior to discharge*5.62.14.8χ2 = 0.9530.462
  % resulting in a remnant41.3 (59/143)2.3 (1/43)32.3 (60/186)χ2 = 22.9320.000
  % resulting in recurrence17.5 (25/143)0.0 (0/43)13.4 (25/186)χ2 = 8.6850.001
  Mean (SD) time from treatment to latest follow-up in days949.3 (1072.4)1574.2 (1304.6)1104.6 (1162.3)t = 2.770.007
Ruptured aneurysms
  No. of patients (%)93 (79.5)24 (20.5)117 (100.0)
  Mean (SD) GOS at discharge3.8 (1.2)3.5 (1.2)3.7 (1.2)t = −0.940.352
  Mean (SD) GOS at 1 yr4.5 (0.7)4.3 (0.9)4.5 (0.7)t = −0.770.456
  % mortality prior to discharge*7.54.26.8χ2 = 0.3381.000
  % resulting in a remnant46.3 (38/82)4.4 (1/23)37.1 (39/105)χ2 = 13.5670.0001
  % resulting in recurrence17.1 (14/82)0.0 (0/23)13.3 (14/105)χ2 = 4.5310.036
  Mean (SD) time from treatment to latest follow-up in days861.0 (983.0)1499.0 (1128.0)1024.0 (1053.0)t = 2.420.021
Unruptured aneurysms
  No. of patients (%)68 (74.7)23 (25.3)91 (100.0)
  Mean (SD) GOS at discharge4.6 (0.8)4.4 (0.7)4.6 (0.8)t = −1.420.162
  Mean (SD) GOS at 1 yr4.9 (0.4)4.5 (0.7)4.8 (0.5)t = −1.500.160
  % mortality prior to discharge*2.90.02.2
  % resulting in a remnant34.4 (21/61)0.0 (0/20)25.9 (21/81)χ2 = 9.2950.001
  % resulting in recurrence18.0 (11/61)0.0 (0/20)13.6 (11/81)χ2 = 4.1730.057
  Mean (SD) time from treatment to latest follow-up in days1052.0 (1169.0)1670.0 (1530.0)1201.0 (1282.0)t = 1.570.129
Boldface type indicates statistical significance.

No additional patients had died at latest follow-up.

Calculated as follows: date of last follow-up office visit − initial (index) treatment admission date.

Chi-square test invalid because expected frequencies were < 1, or < 5 in 20% of cells.

Outcomes were further categorized and analyzed by treatment in the ruptured and unruptured settings (Table 3). There continued to be no statistical difference in GOS score at discharge or 1 year for either set of data. Remnants were significantly more common for aneurysms treated with endovascular therapies in the ruptured (46% vs 4%, p = 0.0001) as well as unruptured circumstances (34% vs 0%, p = 0.001). Recurrence rates were similarly noted to be higher in the endovascular group (ruptured 17% vs 0%, p = 0.036; unruptured 18% vs 0%, p = 0.057).

Endovascular Management and Need for Retreatment

An analysis of the 17 patients (10.6%) who were retreated after their initial endovascular intervention is shown in Table 4. Of these 17 patients, 4 (23.5%) required a second retreatment. Following their first retreatment, 8 (47%) demonstrated a remnant. Following the second retreatment, 2 (50%) harbored a persistent remnant. Five patients had their first retreatment during the same hospitalization as their initial treatment. All 5 of these patients had initially presented with SAH. The average time interval between the first and second treatments was longer than between the second and third treatments (15.6 vs 9.6 months, respectively). The average contrast-filling size at retreatment was 6.8 ± 3.9 mm and 5.3 ± 1.3 mm for the first and second retreatments, respectively.

TABLE 4.

Retreated endovascular cases

VariableRetreatment
FirstSecond
No. of patients/aneurysms (%)174
% ruptured prior to retreatment5.90.0
% recurrent following retreatment29.40.0
% remnant following retreatment47.150.0
Mean (SD) time between treatments in days*479 (602)289 (113)
No. treated during same hospitalization for previous treatment (%)5 (29.4)2 (50.0)
Mean (SD) aneurysm size at retreatment in mm6.8 (3.9)5.3 (1.3)
% stent assisted52.975.0
% coiling alone47.125.0
% vasospasm5.90.0
% radiographic infarction5.90.0
% clinical stroke5.90.0
Mean (SD) GOS score at discharge4.7 (0.7)4.8 (0.5)
Mean (SD) GOS at 1 yr4.9 (0.3)4.8 (0.5)
Mean (SD) time from retreatment to latest follow-up in days914 (895)548 (876)

Calculated as follows: retreatment admission date − previous treatment admission date.

Calculated as follows: date of latest follow-up office visit − previous treatment admission date.

For the first retreatment, 9 patients (53%) underwent intervention via stent-coiling, whereas 3 (75%) of the 4 with a second retreatment required stent-coiling. Retreatments were not without risk, as 6% (n = 1) of the patients developed clinical and radiographic cerebral vascular accidents. The average GOS score from discharge through 1-year follow-up was favorable for both groups, ranging from 4.7 to 4.9.

The methods of endovascular embolization of the aneurysms of patients in our study are shown in Table 5. Three of the initial 161 aneurysms were treated with balloon assistance. Because the number of these patients was low, they were grouped into the coiling-alone category. In total, there were 151 coil embolization–alone and 31 stent-assisted coil embolization procedures. A higher percentage of coil embolization–alone cases was associated with SAH (58.3% vs 19.4%, p = 0.000). There was no statistical difference between the 2 groups except in the incidence of recurrences requiring a subsequent treatment. Followup of initial endovascularly managed aneurysms found a 17.5% recurrence rate. A second recurrence was found in 63% of the initially coil embolized–alone aneurysms versus none of the stent-assisted coil embolized aneurysms (p = 0.009).

TABLE 5.

Endovascular treatments by type of embolization

VariableTreatment*Statisticp Value
Coiling AloneStent-Assisted Coiling
No. of patients/aneurysms (%)151 (83.0)31 (17.0)
% of all aneurysms that ruptured prior to treatment58.3 (88/151)19.4 (6/31)χ2 = 15.6030.000
  % of index treatments that ruptured prior to first treatment62.0 (88/142)26.3 (5/19)χ2 = 8.7330.005
  % of first retreatments that ruptured prior to second treatment0.0 (0/8)11.1 (1/9)χ2 = 0.0170.896
% of all treatments resulting in a remnant42.8 (59/138)38.5 (10/26)χ2 = 0.1650.829
  % of index treatments resulting in a remnant42.6 (55/129)28.6 (4/14)χ2 = 1.0310.398
  % of first retreatments resulting in a remnant37.5 (3/8)55.6 (5/9)χ2 = 0.5540.638
  % of second retreatments resulting in a remnant100.0 (1/1)33.3 (1/3)
% of all treatments that recurred20.3 (28/138)7.7 (2/26)χ2 = 2.3230.170
  % of index treatments that recurred17.8 (23/129)14.3 (2/14)χ2 = 0.1101.000
  % of first retreatments that recurred62.5 (5/8)0.0 (0/9)χ2 = 7.9690.009
  % of second retreatments that recurred0.0 (0/1)0.0 (0/3)
% of all treatments requiring retreatment12.6 (19/151)9.7 (3/31)χ2 = 1.271.000
  % of index treatments requiring retreatment11.3 (16/142)5.3 (1/19)χ2 = 0.6400.696
  % of first retreatments requiring second retreatment37.5 (3/8)11.1 (1/9)χ2 = 1.6390.294
  % of second retreatments requiring third retreatment0.0 (0/1)0.0 (0/3)
Mean (SD) HH score upon admission (ruptured cases only)2.4 (1.3)2.2 (1.8)t = 0.260.809
  Average (SD) length of inpatient stay in days12.9 (11.7)9.1 (11.0)t = 1.1720.092
  % vasospasm15.212.9χ2 = 0.1101.000
% radiographic infarction10.621.9χ2 = 0.1400.753
% clinical stroke9.916.1χ2 = 1.0090.344
  Mean (SD) GOS at discharge4.2 (1.1)4.2 (1.3)t = −0.140.892
  Mean (SD) GOS at 6 mos4.6 (0.6)4.5 (0.7)t = 0.610.547
  Mean (SD) GOS at 1 yr4.7 (0.6)4.7 (0.6)t = 0.140.893
Mean (SD) time from index treatment to latest follow-up in days1042.8 (1136.1)797.4 (963.5)t = 1.140.262
Boldface type indicates statistical significance.

Coiling-alone treatments consisted of 142 index treatments, 8 first retreatments, and 1 second retreatment (N = 151). Stent-assisted coiling treatments consisted of 19 index treatments, 9 first retreatments, and 3 second retreatments (N = 31).

Chi-square test invalid because expected frequencies were < 1, or < 5 in 20% of cells.

Calculated as follows: date of latest follow-up office visit − initial (index) treatment admission date.

When we examined the rates of retreatment between coil embolization cases with or without stent-assistance for the initial treatment, there did not appear to be a significant difference (11.9 vs 9.7%, respectively; p = 1.000). Of note, the radiographic infarct and clinical stroke rates were nearly double when a stent was required; however, this difference did not appear to be statistically significant.

Microsurgical Approach

Of the 47 microsurgically managed basilar apex aneurysms, 24 were performed with a pterional craniotomy and 23 with a subtemporal approach (Table 6). There were very few differences between these 2 groups. Right-side approaches were preferred, with only 4 of the 47 procedures performed from the left.

TABLE 6.

Clipping treatments by surgical approach and side of approach*

VariablePterionalSubtemporalStatisticp Value
No. of patients (%)24 (51.1)23 (48.9)
% ruptured prior to treatment50.052.2χ2 = 0.0221.000
% with remnant0.0 (1/21)4.6 (1/22)χ2 = 0.0010.975
Mean (SD) HH score upon admission (ruptured cases only)1.8 (1.3)2.5 (1.5)t = −1.170.254
Mean (SD) length of inpatient stay in days13.2 (14.6)16.7 (14.2)t = −0.830.410
% right-sided approach87.595.7χ2 = 1.0020.609
% micro-Doppler52.4 (11/21)17.4 (4/23)χ2 = 5.9810.025
% intraop angiography only90.5 (19/21)95.7 (22/23)χ2 = 0.4630.599
% indocyanine green fluorescent imaging only0.00.0
% both intraop angiography & indocyanine green fluorescent imaging9.5 (2/21)0.0 (0/23)χ2 = 0.6250.429
% temporary clip81.0 (17/21)30.4 (7/23)χ2 = 11.2990.001
% temporary balloon occlusion assistance14.3 (3/21)30.4 (7/23)χ2 = 1.6300.287
% hypothermic cardiac arrest4.8 (1/21)4.4 (1/23)χ2 = 0.4340.510
% vasospasm16.717.4χ2 = 0.0041.000
% radiographic infarction12.521.7χ2 = 0.7100.461
% clinical stroke12.517.4χ2 = 0.2220.701
% oculomotor palsy29.278.3χ2 = 11.3690.001
Mean (SD) GOS score at discharge4.3 (1.0)3.6 (1.1)t = 2.120.039
Mean (SD) GOS score at 1 yr4.6 (0.8)4.3 (0.8)t = −1.170.254
Mean (SD) time from treatment to latest follow-up in days§2072.8 (1140.1)1099.4 (1297.7)t = 0.2550.015
SAH from another source, retreatments, recurrences, and regrowths are not presented because there were none. Boldface type indicates statistical significance.

Total clipping treatments consisted of 47 index treatments with no retreatments.

One case in which the initial subtemporal approach was re-attempted with a pterional approach on the same side was counted as a pterional approach for analysis.

Chi-square test invalid because expected frequencies were less than 1 or less than 5 in 20% of cells.

Calculated as follows: date of latest follow-up office visit − initial (index) treatment admission date.

Hypothermic cardiac arrest was used in 2 (4.3%) of the operations. Intraoperative angiography was routinely used in 98%. Temporary clip ligation was more commonly used with the pterional approach (81% vs 30%, respectively; p = 0.001), whereas temporary balloon occlusion was slightly more common when using the subtemporal approach (14.3% vs 30.4%, respectively; p = 0.287). Although 78% (n = 17) had oculomotor nerve palsies following a subtemporal approach, only 29% (n = 7) had similar deficits following a pterional approach (p = 0.001). Radiographic and clinical evidence of stroke were found in 8 (17.0%) and 7 (14.9%) of microsurgically managed patients, respectively, without a significant difference between the 2 approaches. Although GOS score at discharge was better with a pterional approach (4.3 vs 3.6, respectively; p = 0.039), this statistical significance was lost at 1 year.

Distribution of Procedures

The number of endovascular and microsurgical procedures for basilar apex aneurysms over time is shown in Fig. 3, and demonstrates that although a variable number of patients with basilar apex aneurysms presented each year, there was an increasing tendency to treat these aneurysms endovascularly. Figure 4 shows the total number of aneurysms managed during the same period (2000–2012) at our institution. There is a relative decline in the use of microsurgical therapy with a significant increase in the use of endovascular modalities. During this period, the number of ruptured aneurysms that did not receive an intervention remained relatively stable. The transition resulting in a majority of aneurysms being treated by an endovascular approach occurred 10 years earlier for basilar aneurysms compared with other aneurysm locations.

FIG. 3.
FIG. 3.

Graph showing the number of basilar apex aneurysms (y-axis) treated per year by either endovascular or microsurgical approaches. Figure is available in color online only.

FIG. 4.
FIG. 4.

Graph showing the total number of patients with basilar apex aneurysms (y-axis) treated by endovascular and microsurgical management from 2000 to 2012. Figure is available in color online only.

Discussion

Microsurgical Approach

Microsurgical clip ligation of basilar aneurysms is technically challenging, and the expertise needed for its performance has dramatically decreased in recent years. The relationship of the basilar apex to the posterior clinoid, and the orientation of the dome and the posterior cerebral arteries, determines the suitability of microsurgery.3 Preservation of the perforating arteries, especially the artery of Percheron, is essential.3,28 Lack of readily available proximal control in “low-lying” aneurysms has been a strong indication for endovascular treatment.

Currently, the most commonly employed surgical approach to the basilar apex is via a pterional craniotomy with a wide Sylvian fissure dissection and separation of the membrane of Liliequist.25 This approach also requires that the neck of the aneurysm be situated no more than 5 mm below the posterior clinoid.2 This approach reduces the amount of brain retraction needed and decreases manipulation of the oculomotor nerve; however, it requires longer working angles around the optic nerves, chiasm, and internal carotid, posterior communicating, and anterior choroidal arteries. Postoperative complication rates range from 11% to 20% with this method.11,20,30,32 Excluding oculomotor nerve palsies, postoperative deficits were found in as many as 28% of the patients in our study. Temporary third cranial nerve palsy is the most common deficit (20%–100%),1,2,19 but resolves by 6 months in up to 95% of patients.32 In our patients, 29% who underwent a pterional approach were found to have oculomotor nerve palsies, whereas 78% of those treated via the subtemporal approach suffered from this deficit. This difference is likely due to anatomical manipulation of the nerve that is more commonly in line with the basilar apex in the subtemporal approach, whereas with the pterional approach, manipulation is predominately tangential to the nerve. Significant morbidity and mortality have been noted to be approximately 7% with these approaches.30 We found the mortality rate at discharge to be 2.1%, with mean GOS scores at discharge ranging from 3.6 to 4.3 (subtemporal and pterional approaches, respectively; p = 0.039). Although the patient's anatomy and the surgeon's experience will dictate the choice of microsurgical approach to the basilar apex, it appears that more favorable outcomes are associated with the pterional route.

Importantly, these results reflect a balanced approach to treatment of basilar bifurcation aneurysms. A number of recent relevant reports have been skewed toward microsurgical or endovascular techniques.

Endovascular Management

Endovascular therapy has continued to play an everincreasing and important role in the management of basilar apex aneurysms.10,27 The treatment trend at our institution is shown in Fig. 3. The treatment method most commonly used was endovascular coiling without stent assistance (83% of the endovascular cases). This is certainly more ideal with a ruptured aneurysm because antiplatelet agents are not needed preoperatively. The placement of an external ventricular drain and/or ventriculoperitoneal shunting is less risky when these agents have not been administered.

One of the challenges with endovascular therapy is the risk of aneurysm recurrence, which was first noted by Mericle et al. in 1998.23 Recurrence of 5% or more of the initial aneurysm volume has been reported in 11% and 22% of patients, with retreatment rates around 4.9%.22,27 Recently, Chalouhi et al.4 investigated long-term follow-up of completely coiled aneurysms and reported recurrence rates as high as 41% with a need for retreatment in 26%. Complication rates are typically low, but can be as high as 12.5%.22

An alternative strategy is balloonassisted coiling of basilar apex aneurysms.21,29,31 Although this modality can facilitate more dense packing of wider-necked aneurysms, it does not require antiplatelet agents and can be used with patients with SAH. However, it requires either a larger base catheter or two access vessels (contralateral vertebral or one of the posterior communicating arteries). It also requires temporary flow arrest through the basilar apex and one of the posterior cerebral arteries. It is also possible that bilateral posterior cerebral arteries, superior cerebellar arteries, and the perforating vessels may need to be temporarily occluded. Despite these precautions and potential associated risks, balloon assistance has been shown to increase the rates of occlusion of wide-necked aneurysms, during both the initial intervention and at follow-up.31

Stent-assisted coiling is a third alternative for endovascular management of wide-based basilar apex aneurysms. It requires antiplatelet agents varying from a daily ASA to dual antiplatelet agents, and the patient should be taking these agents at a therapeutic level.15 Either closed33,34 or opencell12 stents may be used, and each has its own drawbacks and benefits. Other similar techniques, such as the balloonstenting technique,33 Y-stenting,9 and waffle-cone embolization,26 can be used to help reduce recurrence rates; these techniques were used with the patients in our study when appropriate. Our experience has shown that the use of stents reduces the incidence of recurrence, and stents were often used in the treatment of recurrent aneurysms to facilitate dense coil packing. The significant reduction in hospital length of stay for our patients who underwent stent-assisted coil embolization is related to the fact that the majority of these patients underwent elective procedures (67.7%), in contrast to those who underwent coil embolization alone (36.9%, p = 0.002).

Comparison of Endovascular and Microsurgical Management

Whereas at the beginning of this review there was similarity in the volume of cases treated by means of endovascular and microsurgical modalities, endovascular treatment quickly became the modality of choice. If the neurointerventionalist believed a coil could remain in the sac comfortably with or without balloon remodeling in the ruptured setting, or with the use of a stent in the elective setting, endovascular treatment was pursued. While this was initially the treatment philosophy for patients 50 years of age and older, this practice spread over time to all basilar apex aneurysms. Even by the end of the study, microsurgical consideration was pursued in patients if placement of stable coils could not be achieved, if the patient was young (< 50 years old), if there was anterior projection of the aneurysm, and if the aneurysm was unruptured.

We found a statistical difference only in patients' ages between the endovascular and microsurgical treatment groups; the latter were younger on presentation. In terms of perioperative results, cranial nerve deficits were more frequent in the microsurgical group. Many of the posttreatment deficits were temporary and improved with rehabilitation. Despite the fact that these early postoperative deficits were more common in the microsurgical group, the final GOS results were not statistically different between the groups. When differentiating between treatment groups based on rupture status, the GOS score was found to be similar between the groups. This could in part be due to a lack of sensitivity of the GOS in measuring more subtle neuropsychological outcomes. Future studies need to consider this as an important measure for outcomes.

Remnants and recurrences were statistically more frequent in the endovascular group compared with the microsurgical group, which is consistent with other studies.24 Aneurysms treated in the ruptured setting were much more likely to have a remnant (46%) than when treated in the elective setting (34%). Rehemorrhage was more common in the endovascular group, although not statistically significant due to sample size. Other authors have reported that rehemorrhage occurs in 1.3% of patients with coiled basilar apex aneurysms and in 2.1% with partially coiled ones.13 Interestingly, the mortality rate was not statistically different between our 2 groups. Overall, the risk of rehemorrhage with aneurysm remnants is very small after coiling, and larger and longerterm studies are needed to reliably detect the difference between the benefits of more definitive durable microsurgical ligation compared with the risk of rehemorrhage from aneurysm remnants or retreatment.

Despite these findings, microsurgical treatment of these aneurysms declined over the course of the study. This is in part due to the relative ease of access and treatment of these aneurysms endovascularly in comparison with microsurgery (Fig. 3). Further development of endovascular devices may reduce the concerns of recurrence, retreatment, and most importantly, rehemorrhage. However, this creates a new concern for lesions that cannot be treated endovascularly. The microsurgical lesions become more difficult, due both to their complexity and reduced experience of practitioners and trainees. As a result, it would be wise to concentrate the treatment of these aneurysms at high-volume teaching centers where consideration of microsurgery is an option.

Based on this retrospective experience that is confounded by the biases of treating physicians, we recommend the “endovascular-first” strategy in patients older that 50 years of age. Younger patients should be considered for microsurgical clip ligation of the aneurysms that are accessible (relative to the posterior clinoid) and harbor favorable morphological features for microsurgery. The presence of calcification should lead one to seriously consider endovascular options.

Conclusions

Microsurgical treatment of basilar apex aneurysms is associated with a higher rate of early postoperative deficits than endovascular treatment. Despite this, the clinical outcome at 1 year is no different between patient groups undergoing clip ligation versus coil embolization. However, posttreatment remnants, recurrences, and retreatment of basilar apex aneurysms are significantly more common among endovascularly managed aneurysms. The use of endovascular stents appeared to reduce these remnants and recurrences. The consequences of these residual aneurysms require further long-term follow-up studies. In a select group of patients, microsurgical treatment continues to play an important role.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Bohnstedt. Acquisition of data: Cohen-Gadol, Bohnstedt, Ziemba-Davis, Sethia, Payner. Analysis and interpretation of data: Cohen-Gadol, Bohnstedt, Ziemba-Davis, Sethia, Payner. Drafting the article: Cohen-Gadol, Bohnstedt, Ziemba-Davis, Sethia. Critically revising the article: all authors. Reviewed submitted version of manuscript: Cohen-Gadol, Bohnstedt, Sethia, Payner, DeNardo, Scott. Approved the final version of the manuscript on behalf of all authors: Cohen-Gadol. Statistical analysis: Cohen-Gadol, Bohnstedt, Ziemba-Davis, Sethia. Administrative/technical/material support: Bohnstedt, Ziemba-Davis, Sethia, DeNardo, Scott. Study supervision: Cohen-Gadol, Bohnstedt, Sethia, Payner, DeNardo, Scott.

References

  • 1

    Al-Khayat HAl-Khayat HWhite JManner DSamson D: Upper basilar artery aneurysms: oculomotor outcomes in 163 cases. J Neurosurg 102:4824882005

  • 2

    Behari SDas RKJaiswal AKJain VK: Fronto-temporo-orbitozygomatic craniotomy and “half-and-half” approach for basilar apex aneurysms. Neurol India 57:4384462009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Caruso GVincentelli FGiudicelli GGrisoli FXu TGouaze A: Perforating branches of the basilar bifurcation. J Neurosurg 73:2592651990

  • 4

    Chalouhi NBovenzi CDThakkar VDressler JJabbour PStarke RM: Long-term catheter angiography after aneurysm coil therapy: results of 209 patients and predictors of delayed recurrence and retreatment. J Neurosurg 121:110211062014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chou SNOrtiz-Suarez HJ: Surgical treatment of arterial aneurysms of the vertebrobasilar circulation. J Neurosurg 41:6716801974

  • 6

    Drake CG: Bleeding aneurysms of the basilar artery. Direct surgical management in four cases. J Neurosurg 18:2302381961

  • 7

    Drake CG: Further experience with surgical treatment of aneurysm of the basilar artery. J Neurosurg 29:3723921968

  • 8

    Fisher CMKistler JPDavis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:191980

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gao BBaharoglu MICohen ADMalek AM: Y-stent coiling of basilar bifurcation aneurysms induces a dynamic angular vascular remodeling with alteration of the apical wall shear stress pattern. Neurosurgery 72:6176292013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Gruber DPZimmerman GATomsick TAvan Loveren HRLink MJTew JM Jr: A comparison between endovascular and surgical management of basilar artery apex aneurysms. J Neurosurg 90:8688741999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Hauck EFWhite JASamson D: The small “surgical aneurysm” at the basilar apex. J Neurosurg 112:121612212010

  • 12

    Henkes HBose AFelber SMiloslavski EBerg-Dammer EKühne D: Endovascular coil occlusion of intracranial aneurysms assisted by a novel selfexpandable nitinol microstent (neuroform). Interv Neuroradiol 8:1071192002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Henkes HFischer SMariushi WWeber WLiebig TMiloslavski E: Angiographic and clinical results in 316 coil-treated basilar artery bifurcation aneurysms. J Neurosurg 103:9909992005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hunt WEHess RM: Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14201968

  • 15

    Hwang GKim JGSong KSLee YJVillavicencio JBSuroto NS: Delayed ischemic stroke after stent-assisted coil placement in cerebral aneurysm: characteristics and optimal duration of preventative dual antiplatelet therapy. Radiology 273:1942012014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    International Study of Unruptured Intracranial Aneurysms Investigators: Unruptured intracranial aneurysms—risk of rupture and risks of surgical intervention. N Engl J Med 339:172517331998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Jennett BBond M: Assessment of outcome after severe brain damage. Lancet 1:4804841975

  • 18

    Kistler JPCrowell RMDavis KRHeros ROjemann RGZervas T: The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: a prospective study. Neurology 33:4244361983

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Krisht AFKrayenbühl NSercl DBikmaz KKadri PA: Results of microsurgical clipping of 50 high complexity basilar apex aneurysms. Neurosurgery 60:2422522007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Lawton MT: Basilar apex aneurysms: surgical results and perspectives from an initial experience. Neurosurgery 50:1102002

  • 21

    Lefkowitz MAGobin YPAkiba YDuckwiler GRMurayama YGuglielmi G: Balloon-assisted Guglielmi detachable coiling of wide-necked aneurysms: Part II—clinical results. Neurosurgery 45:5315381999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Lozier APConnolly ES JrLavine SDSolomon RA: Guglielmi detachable coil embolization of posterior circulation aneurysms: a systematic review of the literature. Stroke 33:250925182002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Mericle RAWakhloo AKLopes DKLanzino GGuterman LRHopkins LN: Delayed aneurysm regrowth and recanalization after Guglielmi detachable coil treatment. Case report. J Neurosurg 89:1421451998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Molyneux AJKerr RSBirks JRamzi NYarnold JSneade M: Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol 8:4274332009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Nanda ASonig ABanerjee ADJavalkar VK: Microsurgical management of basilar artery apex aneurysms: a single surgeon's experience from Louisiana State University, Shreveport. World Neurosurg 82:1181292014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Padalino DJSingla AJacobsen WDeshaies EM: Enterprise stent for waffle-cone stent-assisted coil embolization of large wide-necked arterial bifurcation aneurysms. Surg Neurol Int 4:92013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Pandey ASKoebbe CRosenwasser RHVeznedaroglu E: Endovascular coil embolization of ruptured and unruptured posterior circulation aneurysms: review of a 10-year experience. Neurosurgery 60:6266372007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Percheron G: [Arteries of the human thalamus. II. Arteries and paramedian thalamic territory of the communicating basilar artery.]. Rev Neurol (Paris) 132:3093241976. (Fr)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Ramakrishnan VQuadri SSodhi ACortez VTaqi M: Safety and efficacy of balloon-assisted coiling of intracranial aneurysms: a single-center study.. J Neurointerv Surg 6:Suppl 1A68A692014. (Poster E-064)

    • Search Google Scholar
    • Export Citation
  • 30

    Samson DBatjer HHKopitnik TA Jr: Current results of the surgical management of aneurysms of the basilar apex. Neurosurgery 44:6977041999

  • 31

    Shapiro MBabb JBecske TNelson PK: Safety and efficacy of adjunctive balloon remodeling during endovascular treatment of intracranial aneurysms: a literature review. AJNR Am J Neuroradiol 29:177717812008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Solomon RAStein BM: Surgical approaches to aneurysms of the vertebral and basilar arteries. Neurosurgery 23:2032081988

  • 33

    Spiotta AMMiranpuri AChaudry MITurner RD IVTurk AS: Combined balloon stent technique with the Scepter C balloon and low-profile visualized intraluminal stent for the treatment of intracranial aneurysms.. J Neurointerv Surg 5:Suppl 3iii79iii822013

    • Search Google Scholar
    • Export Citation
  • 34

    Weber WBendszus MKis BBoulanger TSolymosi LKühne D: A new self-expanding nitinol stent (Enterprise) for the treatment of wide-necked intracranial aneurysms: initial clinical and angiographic results in 31 aneurysms. Neuroradiology 49:5555612007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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Article Information

Contributor Notes

Correspondence Aaron A. Cohen-Gadol, Goodman Campbell Brain and Spine, Indiana University Department of Neurosurgery, 355 W 16th St., Ste. 5100, Indianapolis, IN 46202. email: acohenmd@gmail.com.INCLUDE WHEN CITING Published online January 13, 2017; DOI: 10.3171/2016.8.JNS16703.Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Headings
Figures
  • View in gallery

    Upper: The pterional approach commonly uses the opticocarotid pathway for aneurysm neck exposure and proximal vascular control. Lower: The subtemporal approach is more favorable for low-lying basilar bifurcation aneurysms; it requires temporal lobe retraction and more direct manipulation of the oculomotor nerve. Copyright Aaron Cohen-Gadol. Published with permission from the Neurosurgical Atlas. Figure is available in color online only.

  • View in gallery

    Methodologies for clip ligation of basilar bifurcation aneurysms via the pterional (upper) and subtempral (lower) approaches are illustrated. The inset demonstrates the closed microsurgical aneurysm clip with exclusion of the aneurysm from circulation and preservation of the parent vessel. Copyright Aaron Cohen-Gadol. Published with permission from the Neurosurgical Atlas. Figure is available in color online only.

  • View in gallery

    Graph showing the number of basilar apex aneurysms (y-axis) treated per year by either endovascular or microsurgical approaches. Figure is available in color online only.

  • View in gallery

    Graph showing the total number of patients with basilar apex aneurysms (y-axis) treated by endovascular and microsurgical management from 2000 to 2012. Figure is available in color online only.

References
  • 1

    Al-Khayat HAl-Khayat HWhite JManner DSamson D: Upper basilar artery aneurysms: oculomotor outcomes in 163 cases. J Neurosurg 102:4824882005

  • 2

    Behari SDas RKJaiswal AKJain VK: Fronto-temporo-orbitozygomatic craniotomy and “half-and-half” approach for basilar apex aneurysms. Neurol India 57:4384462009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Caruso GVincentelli FGiudicelli GGrisoli FXu TGouaze A: Perforating branches of the basilar bifurcation. J Neurosurg 73:2592651990

  • 4

    Chalouhi NBovenzi CDThakkar VDressler JJabbour PStarke RM: Long-term catheter angiography after aneurysm coil therapy: results of 209 patients and predictors of delayed recurrence and retreatment. J Neurosurg 121:110211062014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Chou SNOrtiz-Suarez HJ: Surgical treatment of arterial aneurysms of the vertebrobasilar circulation. J Neurosurg 41:6716801974

  • 6

    Drake CG: Bleeding aneurysms of the basilar artery. Direct surgical management in four cases. J Neurosurg 18:2302381961

  • 7

    Drake CG: Further experience with surgical treatment of aneurysm of the basilar artery. J Neurosurg 29:3723921968

  • 8

    Fisher CMKistler JPDavis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:191980

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gao BBaharoglu MICohen ADMalek AM: Y-stent coiling of basilar bifurcation aneurysms induces a dynamic angular vascular remodeling with alteration of the apical wall shear stress pattern. Neurosurgery 72:6176292013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Gruber DPZimmerman GATomsick TAvan Loveren HRLink MJTew JM Jr: A comparison between endovascular and surgical management of basilar artery apex aneurysms. J Neurosurg 90:8688741999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Hauck EFWhite JASamson D: The small “surgical aneurysm” at the basilar apex. J Neurosurg 112:121612212010

  • 12

    Henkes HBose AFelber SMiloslavski EBerg-Dammer EKühne D: Endovascular coil occlusion of intracranial aneurysms assisted by a novel selfexpandable nitinol microstent (neuroform). Interv Neuroradiol 8:1071192002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Henkes HFischer SMariushi WWeber WLiebig TMiloslavski E: Angiographic and clinical results in 316 coil-treated basilar artery bifurcation aneurysms. J Neurosurg 103:9909992005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hunt WEHess RM: Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14201968

  • 15

    Hwang GKim JGSong KSLee YJVillavicencio JBSuroto NS: Delayed ischemic stroke after stent-assisted coil placement in cerebral aneurysm: characteristics and optimal duration of preventative dual antiplatelet therapy. Radiology 273:1942012014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    International Study of Unruptured Intracranial Aneurysms Investigators: Unruptured intracranial aneurysms—risk of rupture and risks of surgical intervention. N Engl J Med 339:172517331998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Jennett BBond M: Assessment of outcome after severe brain damage. Lancet 1:4804841975

  • 18

    Kistler JPCrowell RMDavis KRHeros ROjemann RGZervas T: The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: a prospective study. Neurology 33:4244361983

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Krisht AFKrayenbühl NSercl DBikmaz KKadri PA: Results of microsurgical clipping of 50 high complexity basilar apex aneurysms. Neurosurgery 60:2422522007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Lawton MT: Basilar apex aneurysms: surgical results and perspectives from an initial experience. Neurosurgery 50:1102002

  • 21

    Lefkowitz MAGobin YPAkiba YDuckwiler GRMurayama YGuglielmi G: Balloon-assisted Guglielmi detachable coiling of wide-necked aneurysms: Part II—clinical results. Neurosurgery 45:5315381999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Lozier APConnolly ES JrLavine SDSolomon RA: Guglielmi detachable coil embolization of posterior circulation aneurysms: a systematic review of the literature. Stroke 33:250925182002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Mericle RAWakhloo AKLopes DKLanzino GGuterman LRHopkins LN: Delayed aneurysm regrowth and recanalization after Guglielmi detachable coil treatment. Case report. J Neurosurg 89:1421451998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Molyneux AJKerr RSBirks JRamzi NYarnold JSneade M: Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol 8:4274332009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Nanda ASonig ABanerjee ADJavalkar VK: Microsurgical management of basilar artery apex aneurysms: a single surgeon's experience from Louisiana State University, Shreveport. World Neurosurg 82:1181292014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Padalino DJSingla AJacobsen WDeshaies EM: Enterprise stent for waffle-cone stent-assisted coil embolization of large wide-necked arterial bifurcation aneurysms. Surg Neurol Int 4:92013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Pandey ASKoebbe CRosenwasser RHVeznedaroglu E: Endovascular coil embolization of ruptured and unruptured posterior circulation aneurysms: review of a 10-year experience. Neurosurgery 60:6266372007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Percheron G: [Arteries of the human thalamus. II. Arteries and paramedian thalamic territory of the communicating basilar artery.]. Rev Neurol (Paris) 132:3093241976. (Fr)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Ramakrishnan VQuadri SSodhi ACortez VTaqi M: Safety and efficacy of balloon-assisted coiling of intracranial aneurysms: a single-center study.. J Neurointerv Surg 6:Suppl 1A68A692014. (Poster E-064)

    • Search Google Scholar
    • Export Citation
  • 30

    Samson DBatjer HHKopitnik TA Jr: Current results of the surgical management of aneurysms of the basilar apex. Neurosurgery 44:6977041999

  • 31

    Shapiro MBabb JBecske TNelson PK: Safety and efficacy of adjunctive balloon remodeling during endovascular treatment of intracranial aneurysms: a literature review. AJNR Am J Neuroradiol 29:177717812008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Solomon RAStein BM: Surgical approaches to aneurysms of the vertebral and basilar arteries. Neurosurgery 23:2032081988

  • 33

    Spiotta AMMiranpuri AChaudry MITurner RD IVTurk AS: Combined balloon stent technique with the Scepter C balloon and low-profile visualized intraluminal stent for the treatment of intracranial aneurysms.. J Neurointerv Surg 5:Suppl 3iii79iii822013

    • Search Google Scholar
    • Export Citation
  • 34

    Weber WBendszus MKis BBoulanger TSolymosi LKühne D: A new self-expanding nitinol stent (Enterprise) for the treatment of wide-necked intracranial aneurysms: initial clinical and angiographic results in 31 aneurysms. Neuroradiology 49:5555612007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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