Microsurgery of Basilar Apex Aneurysms

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CHAPTER 373 Microsurgery of Basilar Apex Aneurysms

Bernard R. Bendok, Daniel L. Surdell, Arun K. Sherma, H. Hunt Batjer

Basilar Apex Project

The surgical management of basilar apex aneurysms remains one of the most challenging areas of neurosurgery. The technical demands of treating these aneurysms has inspired several generations of surgeons to push the limits of technical achievement. Advances in neuroanesthesia, cerebral protection paradigms, and critical care management have enhanced overall outcomes. Although endovascular techniques present an alternative to open surgery for select aneurysms of the basilar apex, open surgical approaches remain necessary in many cases.

Basilar Apex Aneurysm Surgery: Clinical Experience

Dr. Charles Drake shared his insight into basilar apex aneurysm surgery throughout his career in multiple publications and lectures.1–14 In an update on his experience in 1990, he described 545 patients who had been treated, with good outcomes achieved in 475 patients (87%).13 During the past 40 years, other experienced surgeons have also contributed to this challenging area of neurosurgery.14–25 This list includes well-trained young individuals with intense dedication to neurovascular surgery and sufficient experience who also can achieve successful results when treating basilar apex aneurysms.15

In a review of their experience with 303 basilar apex aneurysms, Samson and colleagues16 demonstrated a statistical correlation between poor outcome and various factors: poor admission grade (Hunt-Hess grades IV and V), patient age older than 65 years, computed topography (CT) demonstration of thick basal cistern clot, aneurysm diameter larger than 20 mm, and symptoms attributable to brainstem compression. In a review of all series published between 1980 and 1989, Wascher and Spetzler17 found, for a total of 957 patients, that the rate of good outcome was 82.4% and that the mortality rate was 5.1%. These series included results for a heterogeneous group of aneurysm sizes, patient ages, and clinical presentations. In a report focusing on the management outcomes of 179 unruptured posterior circulation aneurysms, of which 99 were bifurcation aneurysms, Rice and colleagues18 found a 4.2% combined morbidity and mortality rate. This variability in morbidity and mortality based on clinical factors and aneurysmal morphology must be considered when comparing clip ligation with endovascular options for specific patients. Lozier and associates reported their retrospective review of the perioperative and long-term clinical outcomes in a cohort of prospectively enrolled patients.19 They identified 98 consecutively treated basilar apex aneurysms. Eighty-four of the 98 aneurysms were directly clipped. Fifty patients presented with subarachnoid hemorrhage (SAH), and 19 aneurysms were giant. The surgical morbidity rates were 19% for the entire group and 8.8% for the unruptured and nongiant subgroup. The most common complication was perforator injury. Sixty-seven percent of patients were independent at discharge and 79% at the 3-month follow-up. Ninety-three percent of the subgroup of patients with nongiant and unruptured aneurysms were independent at discharge and 100% at the 3-month follow-up. In a multivariate analysis, unruptured giant aneurysm status was found to confer a tremendous risk for poor outcome in this series.19 An important issue to consider when assessing the efficacy of a treatment modality for aneurysms is the rate of complete aneurysm occlusion that can be achieved. In a series reported by Samson and colleagues,16 postoperative angiography was performed in 246 patients. Residual aneurysm was identified in 6% (i.e., complete aneurysm occlusion in 94%). This rate of complete aneurysm occlusion is superior to the current results achieved with endovascular treatment.26–30

Microsurgical Anatomy of the Interpeduncular Cistern

The technical challenges of clipping basilar apex aneurysms are related to the complex anatomy in and around the interpeduncular cistern and the depth of dissection through narrow corridors that is required to safely secure these lesions. The subarachnoid space within the interpeduncular cistern is enclosed by the clivus and posterior clinoid process anteriorly, the medial aspects of the temporal lobes and tentorial edges laterally, the cerebral peduncles posteriorly, and the mamillary bodies and posterior perforated substance superiorly. The terminal basilar artery has a normal diameter of 2.7 to 4.3 mm and lies 15 to 17 mm posterior to the posterior aspect of the internal carotid arteries (ICAs).25,31,32 This proximity to the ICA provided a basis for seeking a transsylvian approach to basilar apex aneurysms. A point proximal to the bifurcation of the basilar artery gives rise to bilateral superior cerebellar arteries (SCAs), which may be duplicated. The dentate nuclei are irrigated by these vessels.20

The posterior cerebr alarteries (PCAs) originate at the basilar bifurcation. They are usually 2 to 3 mm in diameter. The size of the segment of the PCA from the basilar bifurcation to the junction with the posterior communicating artery (i.e., P1 segment) depends on the extent to which the posterior communicating artery contributes to blood flow in the distal PCA. A fetal PCA implies that the P1 is a vestigial band, with all PCA blood flow originating from the carotid artery.

Visualization and preservation of the thalamoperforating arteries is an essential technical nuance of basilar apex aneurysm surgery. These critical perforators arise from the posterior aspect of the basilar trunk, the proximal P1 segments, and the posterior communicating arteries. The cranial nerve most intimately associated with this region is the oculomotor nerve that traverses the space between the PCA and the SCA within the interpeduncular cistern. The membrane of Liliequist21 forms an anterior “curtain” for the interpeduncular cistern. This membrane is a thick layer of arachnoid that anchors from the mamillary bodies superiorly and extends anteriorly and inferiorly before folding posteriorly to form the roof of the prepontine cistern. The basilar apex can be located above, below, or at the level of the dorsum sellae.

Surgical Strategies

Basilar apex aneurysms account for about half of posterior circulation aneurysms. Posteriorly located perforators must be protected, or disabling neurological deficits will result. Optimal surgical results and outcomes require excellent technical skill, superb knowledge of operative anatomy, and familiarity with operative nuances accumulated by Drake, Yasargil, and a generation of surgeons who followed.

The two pure approaches for basilar apex aneurysms are the subtemporal approach and the transsylvian approach. In our practice, we employ both approaches but are increasingly relying on a new modification or hybrid approach.22 We emphasize the importance of tailoring the operation to the patient’s particular anatomy. Considering the key assets and liabilities of each approach allows a more rational design of operative strategies for each patient. The pure transsylvian approach has several assets:

• Neurosurgeons are familiar with this approach because it is used for more common aneurysms and tumors.
• Proximal control is straightforward.
• Exposure of both P1 segments for temporary trapping is uncomplicated.
• Wide exposure is possible.

The transsylvian exposure also has liabilities:

• Exposure of posteriorly located perforators is difficult.
• Inspection of distal aspect of clip blade is difficult.
• Technical features make treatment of directly anteriorly or directly posteriorly projecting aneurysms very difficult.

The subtemporal approach offers the surgeon many assets:

• Proximal control is easy
• The lateral view facilitates dissection of the perforators.
• Tentorial division allows exposure of the upper one third of the clivus for low-lying bifurcations.
• Fenestrated clips can be placed with excellent visualization of the thalamoperforators.
• Exposure and clipping of anteriorly or posteriorly directed aneurysms is more feasible than with the transsylvian approach.

The subtemporal exposure also has liabilities:

• The field is narrow.
• Access to the proximal contralateral P1 for temporary trapping is poor.
• The temporal lobe can be injured in fresh SAH in poor-grade or obese patients.
• Cranial nerve III palsy often occurs postoperatively (usually transient).
• Intraoperative bleeding can be difficult to control.

Pure Transsylvian Approach

The transsylvian exposure provides excellent visualization for aneurysms with necks at the level between the middle depth of the sella turcica and a line 1 cm superior to the posterior clinoid process (Fig. 373-1). Aneurysms with necks lying inferior to the midsellar level are better approached through the subtemporal corridor or a “half-and-half” conversion with tentorial division.23,25 Extremely high aneurysms are difficult to approach but are probably best tackled through a transsylvian approach above the carotid bifurcation. The orbitozygomatic osteotomy is helpful when tackling high aneurysms because the surgeon’s line of sight can angle more superiorly. Several maneuvers, including drilling the posterior clinoid for low-lying lesions, have been described to tackle anatomic problems encountered during transsylvian exposure.3,33 A transcavernous approach has also been described.34

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FIGURE 373-1 The pterional exposure provides excellent visualization of the neck of basilar bifurcation aneurysms that originate between the midsellar depth and a line 1 cm superior to the posterior clinoid process.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

Operative Technique

Yasargil20 pioneered the transsylvian approach for basilar apex aneurysms. The advantages of this approach include its familiarity to neurosurgeons, the proximity of the basilar artery to the carotid artery, and the wide exposure of the interpeduncular cistern that can be achieved by opening the membrane of Liliequist. We typically approach midline basilar apex aneurysms from the right side. A left-sided approach is valid when the patient has a right hemiparesis or left third nerve palsy. Some anatomic variants also warrant a left-sided approach. For example, an aneurysm that tilts to the left side makes it difficult to dissect the left PCA off the aneurysm from the right. Occasionally, the entire basilar artery is displaced to the left, making a right-sided transsylvian approach difficult.

Positioning

Precise positioning is critical to optimize exposure of the basilar apex. Excellent positioning can be achieved with four steps after the Mayfield-Kees skull fixation device is placed with two pins on the contralateral side of the frontal bone and with a single pin placed superior to the mastoid process (Fig. 373-2). First, the head is elevated above the long access of the body to maximize venous drainage. Second, the head is rotated away from the operative side by 20 degrees. Third, flexion of the neck brings the chin toward the contralateral shoulder and ensures the plane of the floor of the anterior cranial fossa is perpendicular to the long axis of the body. Fourth, the head is extended until the maxillary eminence is well above the orbital rim.

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FIGURE 373-2 Positioning for a pterional approach. A, The Mayfield-Kees skull fixation device is placed with two pins anteriorly across the midline and the single pin posteriorly to facilitate a flat, nonobstructive surgical field. The head is elevated slightly from the long axis of the body. B, Rotation of the head to the contralateral side by 20 degrees minimizes subsequent temporal lobe encroachment on the operative field. C, Flexion of the neck brings the chin toward the contralateral shoulder and ensures that the plane of the floor of the anterior cranial fossa is perpendicular to the long axis of the body. This maneuver allows maximal surgical comfort and flexibility and prevents encroachment of the surgeon’s arms and microscope into the ipsilateral shoulder. D, Extension of the head is then achieved in a somewhat exaggerated degree compared with anterior circulation surgery to minimize subsequent diencephalic retraction. The maxillary eminence is elevated well above the superior orbital ridge.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

Scalp Incision

The incision is begun at the zygoma and carried superiorly in a straight line for about 10 cm above the superior temporal line and then curved gently forward toward the midline (Fig. 373-3). Care is taken to ensure that the incision is within 1 cm of the tragus to avoid damage to the frontalis branch of the facial nerve. We preserve at least one branch of the superficial temporal artery. In addition to maximizing scalp healing potential, preservation of the vessel may prove useful if a revascularization procedure is needed. We retract the scalp flap with fishhooks and perform an interfascial dissection of the temporalis muscle. Using a knife, we incise the temporalis fascia from the area of the zygoma to just 1 cm below the muscle attachment to the temporal bone and then to the area of the keyhole. The knife is used to prevent shrinkage of the temporalis fascia and to facilitate complete closure. We use cautery to cut the muscle through the opening made with the knife and then peel the muscle off the temporal squama and retract it over the scalp flap with fishhooks (Fig. 373-4).

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FIGURE 373-3 Scalp incision for a pterional approach.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

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FIGURE 373-4 The temporalis fascia and muscle are incised with the cutting cautery, taking care to avoid injury to the deep neurovascular bundle in the muscle. The resultant single-layer flap is dissected from the underlying bone and retained with fishhook retractors.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

Craniotomy

We perform a three- or four-hole craniotomy (Fig. 373-5). The fourth hole is reserved for older patients with presumed adherent dura. The first bur hole is placed just above the zygomatic arch. The second bur hole is superior to the first bur hole and just inferior to the superior temporal line. The third bur hole is placed at the anatomic key hole. The optional fourth bur hole is placed medial and anterior to the second bur hole. A power-driven craniotome is used to incise the bone. After elevating the bone flap, we drill enough bone to expose the temporal tip and the floor of the middle fossa all the way back to the zygomatic root. This degree of temporal exposure can be critical if conversion to a half-and-half or subtemporal approach is needed. We then perform an aggressive resection of the sphenoid ridge with rongeurs and a cutting bur on an air-driven drill (Fig. 373-6). Preferably, the bony exposure is carried to the lateral aspect of the superior orbital fissure. We remove the inner table of the frontal bone for a distance of 2 cm from the bur hole at the anatomic key hole. After adequate bony exposure, we obtain hemostasis with bone wax, oxidized cellulose, and tack-up sutures. This avoids run-down later in the case.

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FIGURE 373-5 Pterional craniotomy. A critical aspect of the craniotomy is a generous anterior temporal craniectomy.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

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FIGURE 373-6 Aggressive resection of the sphenoid ridge.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

We then incise the dura in a semilunar fashion, with the medial limb extending to the frontal bone 1 cm below the medial edge of the craniotomy. The lateral limb crosses the sylvian fissure and extends anteriorly to a point 1 cm below the sylvian fissure at the edge of the craniectomy. At this point, for ruptured aneurysms, we place a ventriculostomy catheter using anatomic points defined by Paine and coworkers35 if the brain appears to be tight. The point of entry is the vertex of an isosceles right triangle whose hypotenuse overlies the sylvian fissure and whose sides are 2.5 cm long (Fig. 373-7). A ventricular catheter is used to puncture the frontal lobe at this point. We suture the catheter posterior to the dura and allow continuous drainage during the microsurgical dissection.

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FIGURE 373-7 Reliable access to the frontal horn of the lateral ventricle may be obtained during a pterional craniotomy employing Paine’s point. The landmarks for this point involve the creation of a 2.5-cm isosceles right triangle whose anterior limb abuts on the dura overlying the sphenoid ridge and whose posterior limb touches the sylvian fissure. The hypotenuse overlies the sylvian fissure. A Silastic brain catheter is used to enter the frontal cortex perpendicularly at the vertex of the triangle.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

Subarachnoid Exposure

Subarachnoid dissection is done under the microscope. During the initial subarachnoid dissection, two goals are kept in mind: (1) maximizing brain relaxation by generous arachnoidal opening, allowing for egress of cerebrospinal fluid (CSF), and (2) extensive dissection of the sphenoidal portion of the sylvian fissure. CSF released from the subarachnoid space results in further brain relaxation, even after spinal or ventricular drainage and particularly when SAH has produced loculated pockets of CSF. The principle of wide and complete sylvian fissure dissection is critical because, during the procedure, it is necessary to displace the frontal and temporal lobes independently. To avoid kinking a middle cerebral artery (MCA) branch during the approach, a lateral to medial dissection is performed to expose the M2 branches, MCA bifurcation, M1 trunk, carotid bifurcation and the contents of the carotid cistern.

The dissection is begun into the opercular insular fissure about 2 cm posterior to the sphenoid ridge. We carry this dissection medially to incorporate the carotid cistern. A T-shaped incision is made in a posterolateral direction toward the insertion of cranial nerve III into the cavernous sinus. We then return to the lateral sylvian fissure and dissect the arachnoid down to the carotid bifurcation, effectively liberating the entire segment of the MCA (i.e., M1 segment). When necessary, bridging veins are coagulated and cut to facilitate the separation of the frontal and temporal lobes. In effect, this exposure allows for generous displacement of the frontal lobe without placing undue traction on the carotid artery, the anterior cerebral artery, or the MCA.

We then turn our attention to the arachnoid, which tethers the gyrus rectus to the optic nerve. Dissecting the arachnoid further frees the frontal lobe and opens the prechiasmatic cistern. At this point, the temporal lobe is usually found to be displaced posteriorly, which can result in uncal tissue herniating medially over the incisura and obstructing the view of the interpeduncular cistern. Although retraction of this tissue is an option, we have occasionally performed a subpial uncal resection with good results. Post and colleagues36 reported their initial experience using uncal resection (10 × 10 × 15 mm volume) to optimize transsylvian access to the basilar apex without sacrifice of the pretemporal veins. Their initial clinical experience included eight patients—four of whom were treated for basilar apex aneurysms. They found that no patient developed venous infarction or new postoperative seizure. Cadaver analysis revealed that there was similar exposure to the upper basilar complex; however, the additional exposure from uncal resection did increase visualization of the ipsilateral PCAs and SCAs compared with the pretemporal approach. These investigators did report that the angle of view is limited to a more superior-lateral perspective when compared with the pretemporal approach. Therefore, the transuncal approach may be less suited for very large or giant basilar apex aneurysms when proximal control of the basilar trunk is obscured by the dome of the aneurysm.36 For this approach, we routinely use frontal and temporal lobe retractors. When a significant amount of posterior temporal lobe retraction is needed with or without conversion to a half-and-half or extended lateral approach, it is wise to coagulate and cut the veins that drain the temporal lobe into the sphenoparietal sinus. Rupture of one of these veins later could obstruct the view during a critical part of the procedure.

After temporal and frontal lobe retraction is optimum, we turn our attention to the three corridors that allow access to the interpeduncular cistern from this vantage point: the space between the carotid and the optic nerve, the retrocarotid space, and the area superior to the carotid bifurcation. Ideally, we dissect through each of these corridors to maximize the routes of access to the interpeduncular cistern. Individual anatomic variations may make one of these spaces more or less accessible. A medially displaced carotid, for example, makes the retrocarotid space more relevant for access. With these three windows in mind, we then identify the posterior communicating artery and dissect along its inferior surface toward its junction with the PCA. This is the safest approach to the basilar apex because it avoids injury to the anterior thalamoperforating vessels and ensures that the dissection can lead to the inferior aspect of the P1-P2 junction (the P2 segment represents the PCA from the junction with the posterior communicating artery to where the artery passes the posterior midbrain). This prevents dissection superior to the P1 segment, which could result in perforator injury and an inadvertent and premature encounter with the aneurysm. After the P1-P2 junction is defined, we turn our attention to sharply opening the membrane of Liliequist inferiorly and medially. This dissection facilitates access to the basilar trunk and proximal carotid and allows removal of subarachnoid clot.

Our dissection then turns medially along the inferior edge of P1, across the front of the basilar apex toward the contralateral SCA and the inferior aspect of the contralateral P1. The inferior aspect is favored because perforators are spared and inadvertent aneurysmal rupture is avoided. At this point, we define an area on the basilar artery that can safely and comfortably accommodate a temporary clip. Occasionally, this area is below the SCA if the space between the PCAs and the SCAs is too narrow for a clip. After this is done, attention is turned to the superior aspect of the contralateral P1, where we dissect arachnoid adhesions and free perforators that may be adherent to the neck or dome. We then do the same for the ipsilateral P1.

After both P1 segments have been adequately dissected, we address the critical perforators that stream up the posterior aspect of the basilar artery and frequently adhere to the back wall of the aneurysm. Clipping should not be attempted until all these perforators are seen and freed. Using the suction tip, the aneurysm dome can be gently moved forward to create a plane for the clip blade behind the basilar artery. This maneuver can be done more easily for the aneurysm if a temporary clip is on the basilar artery. We typically employ 10 to 15 minutes for temporary occlusion with the patient in burst suppression with mild hypothermia. When there is a need to access the aneurysm from above the carotid bifurcation, a space can be created by dissecting through the arachnoid that adheres to the perforators emanating from the M1 and A1 segments and gently elevating the optic tract.

Clip Application

The narrow confines of the interpeduncular cistern make adequate visualization during clip placement challenging. The clip applier can easily obstruct visualization. During clip application, it is useful to insert the ipsilateral blade gently along the neck while leaving the contralateral blade wide open after the ipsilateral blade is in position; the mouthpiece can be used to shift the scope to see the contralateral neck. We have found several maneuvers to be extremely helpful in maximizing visualization during clipping. The first maneuver takes advantage of the wide dissection medial and lateral to the carotid, which is described earlier. A right-handed surgeon operating from the right-hand side can insert the clip and clip applier lateral to the carotid and insert the suction medial to the carotid. This prevents the loss of vision that can be caused by the clip applier. A left-handed surgeon can similarly insert the clip applier and clip medial to the carotid. Another maneuver involves using an inverted bayoneted clip, which minimizes encroachment on the surgeon’s visual field. It is critical to avoid the tendency to use excessively long clips because perforators can be closed behind the bifurcation. After the clip is applied, vigilant inspection of the clip blades must be performed to ensure complete neck clipping and to make sure that no perforators were enclosed in the clips.

Orbitozygomatic Approach

A helpful supplement to the transsylvian approach is the orbitozygomatic osteotomy.37,38 The initial incision is similar to the standard pterional craniotomy.26 The inferior limb of the incision is completed after the scalp is dissected from the temporalis fascia, preserving the superficial temporal artery. The scalp is mobilized anteriorly, and the temporalis fascia is exposed. The fascia is incised and elevated to avoid injury to the frontalis branch of the facial nerve. The dissection continues anteriorly to expose the orbital rim, malar eminence, and zygomatic arch. The temporalis muscle is raised separately, which exposes the pterion and the zygomatic root. The scalp flap and temporalis muscles are reflected anteriorly and inferiorly, respectively. Bur holes are placed in the temporal bone over the zygoma and pterion. A pterional craniotomy is performed. The periorbita is dissected with a No. 1 Penfield dissector. A reciprocating saw is used to perform the orbital and zygomatic osteotomies.27 The first osteotomy is an oblique cut across the zygomatic root. The second and third cuts divide the zygoma just superior to the level of the malar eminence. The third cut extends from the inferior orbital fissure. Care is taken with thin retractors to protect the periorbita. The dura is elevated from the anterior wall of the temporal fossa and the orbital roof. The fourth cut divides the superior orbital rim and roof and is begun 1 to 2 mm lateral to the supraorbital canal. The last two cuts connect the superior and inferior orbital fissures. This is performed after the inferior orbital fissure is identified by direct vision or palpation of the infratemporal fossa with a No. 4 Penfield dissector. Reciprocating saw blade is engaged in the upper end of the fissure, and a short cut is made to the edge of the previously made notch in the temporal fossa. The final cut extends from the lateral margin of the superior orbital fissure to join the fifth cut. Removal of additional bone at the skull base decreases retraction and increases the angle of view superiorly toward the basilar apex.26 After the bony removal is accomplished, the dura is opened, the sylvian fissure is widely split, and the microsurgical dissection proceeds similarly to the traditional transsylvian approach.

The relationship between the aneurysm origin and the posterior clinoid process can help guide decisions regarding the surgical approach.28 High- or low-lying aneurysm necks are defined as occurring higher or lower than 5 mm, respectively.29 Some neurosurgeons prefer an orbitozygomatic craniotomy to approach normal or high-lying aneurysms.28 In those that are low lying, resection of three bony obstacles (the anterior clinoid process, the posterior clinoid process, and the dorsum sellae) can be advantageous.30

Youssef and colleagues31 reported on a cadaver study to quantify the effects of anterior and posterior clinoidectomy as they relate to the carotid-oculomotor window when exposing the basilar apex. This was after a frontotemporal-orbitozygomatic craniotomy. They found that the anterior clinoidectomy and ICA mobilization increased the carotid-oculomotor space 44% anteriorly and 28% posteriorly. The posterior clinoidectomy increased the exposed length of the basilar artery 69%. They concluded that superficial wide-field exposure, expansion of the carotid-oculomotor window, and increased exposure of the basilar apex improve visualization, facilitate clip application, and allow for proximal control.31 Chanda and Nanda’s32 cadaver study involved a stepwise dissection starting with a frontal temporal craniotomy, then an orbitozygomatic craniotomy, followed by drilling the posterior clinoid process. These investigators found that, on average, a 13.4-mm segment of the basilar artery was gained.

Pretemporal Transzygomatic Transcavernous Approach

Krisht and Kadri39 described the use of the pretemporal transzygomatic transcavernous approach to treat higher complexity basilar apex aneurysms surgically. They defined basilar apex aneurysms as highly complex if they were larger than 2 cm, very dysmorphic, or wide based; had a low bifurcation; were posterior or posteroinferior projecting; possessed dolichoectatic changes of the basilar apex compromising the surgical view; or were associated with additional aneurysms affecting the surgical view.39 The technique begins with an extended pterional craniotomy with temporal extension. This allows for an inferior reflection of the temporalis muscle. After the craniotomy, the temporal squama is drilled flush with the middle fossa floor. The sphenoid wing is drilled from its lateral to its medial extent until the anterior clinoid process is reached. The meningo-orbital artery is exposed, coagulated, and cut. During this step, the posterior third of the lateral and superior orbital wall is removed while preserving the periorbita. The anterior clinoid process is exposed and removed.

The meningo-orbital artery is the site where the dissection plane between the dura propria of the temporal lobe and the lateral wall of the cavernous sinus can begin.39 The third cranial nerve is identified lateral to the anterior clinoid process and followed to the level of its exit through the dura at the level of the oculomotor trigone. The fourth nerve is also identified in its epidural course as it crosses over the oculomotor nerve. Adequate exposure of the course of the oculomotor nerve is better achieved if this plane is dissected along its posterolateral extension over the V1 and V2 segments of cranial nerve V, to the level of the ganglion. The space between V1 and V2 is a common area of bleeding controlled with Surgicel (Ethicon, Inc., Somerville, NJ) or Tisseel VH fibrin sealant (Baxter AG, Vienna, Austria).

The anterior clinoid process removal involves detaching its three bony connections39: the sphenoid bone over the superior orbital fissure, the roof of the optic canal, and the optic strut, usually performed with a 2- to 3-mm diamond drill bit.

The dura is cut in a curved T-shaped fashion, with the vertical arm of the T following the sphenoid wing indentation.39 The incision extends all the way to the entrance of the third nerve and into the oculomotor trigone. This allows for visualization of the third nerve both intradurally and extradurally and allows for increased mobilization of the nerve for exposure of the interpeduncular fossa and region of the posterior clinoid process. Also, releasing the nerve from the dural attachment makes it more tolerant of the mobilization.39 The subarachnoid dissection is similar to that presented for the transsylvian approach.

Krisht and associates34 reported their results using this technique for the treatment of 50 basilar apex aneurysms, which by their definition were complex. Half of the patients presented with SAH. Thirty-six patients were female and 14 were male, with a mean age of 52.2 years (32 to 76 years old). Ninety-eight percent (49 of 50) were successfully clipped without procedure-related mortality. Two deaths occurred—one from delayed bowel ischemia and a second from the effects of vasospasm. The investigators reported three ischemia-related events, of which two were procedural related. All patients experienced partial or complete cranial nerve III palsy, with full recovery in all but 1 patient. At discharge, the Glasgow Outcome Scale scores were 4 and 5 in 88% of patients; at the 6-month follow-up, the Rankin Outcome Scale scores were 0 to 2 in 92% of patients.34

Subtemporal Approach

Most basilar apex aneurysms that were treated by Drake were treated with a subtemporal approach.8 As outlined previously, several situations make this approach preferable to the transsylvian route. A right-sided approach usually is preferable to prevent damaging the dominant temporal lobe. Several circumstances make a left-sided approach more reasonable. A left cranial nerve III palsy or right hemiparesis favors a left-sided approach to avoid injury to the right cranial nerve III and cerebral peduncle. Occasionally, a tilt of the basilar apex can elevate one P1 segment significantly above the other. If the left PCA is significantly higher than the right PCA, a right-sided approach could risk trapping the left PCA in the blades.

CSF drainage is paramount to the success of this approach. When the subtemporal approach is used, we place a lumbar drain routinely in the operating room before positioning the patient. CSF drainage is particularly important after SAH. When positioning the Mayfield fixation device, the surgeon should always consider the possibility of needing to convert to a transsylvian approach; the ability to do this without redraping is obviously advantageous. After the Mayfield head frame has been positioned with one pin over the forehead and two pins over the occiput, we place the patient on the side and allow the dependent arm to rest in a sling. We use gel pads to protect the axilla. The chest area, hips, and legs are appropriately padded and taped to the operating table (Fig. 373-8). After the patient is well positioned, we elevate the head slightly and then tilt the vertex 10 to 20 degrees below horizontal to allow the temporal lobe to fall away from the middle fossa floor, minimizing retraction and maximizing the working space.

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FIGURE 373-8 Positioning for a subtemporal approach.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

For unruptured aneurysms, we use a straight incision, which extends 10 cm up from a point 1 cm anterior to the tragus (Fig. 373-9). The craniotomy is then based over the zygomatic root and has a diameter of about 3.5 cm. For patients with recent SAH, we favor a larger craniotomy. We use an upside-down horseshoe incision and then perform a craniotomy in addition to an anterior craniectomy (Fig. 373-10). The wider exposure allows inferior temporal gyrus resection if it is needed for further exposure. Resection of bone down to the floor of the middle fossa minimizes the need for brain retraction. After the craniotomy, the dura is opened in a cruciate fashion such that the inferior limb can be secured inferiorly to minimize extradural bleeding and maximize exposure (Fig. 373-11). Hyperventilation, diuresis, and lumbar drainage often result in sufficient brain relaxation to maneuver subtemporally. In patients with a recent hemorrhage, these maneuvers may not be sufficient. In this situation, we have frequently resected the inferior temporal gyrus with the fusiform and parahippocampal gyri. We have not noticed any increased morbidity associated with this method, and the resulting exposure is usually excellent. When resorting to this resection, we have found it helpful to leave the medial pia-arachnoid tissue to serve as an anchor for the retractor. When the uncus is elevated, cranial nerve III elevates with the uncus. To further enhance exposure, we place a tentorial stitch as advocated by Drake.8 This stitch is placed posterior to the dural insertion of cranial nerve IV. For an extremely low-lying aneurysm, splitting the tentorium may be necessary. Bleeding can be minimized by aggressively coagulating the tentorium over the incision site and by placing small pieces of cotton in the dural leaflets with a nerve hook.

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FIGURE 373-9 Skin incision and craniotomy for a subtemporal approach for an unruptured aneurysm.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

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FIGURE 373-10 Skin incision and craniotomy for a subtemporal approach for a ruptured aneurysm.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

image

FIGURE 373-11 Dura tacked up for a subtemporal exposure.

(From Apuzzo MLF, ed. Brain Surgery: Complications, Avoidance and Management. New York: Churchill Livingstone; 1993.)

After adequate exposure is achieved, the arachnoid between cranial nerve III and the incisura should be dissected. The next structure to be identified is the SCA as it curves back around the cerebral peduncle into the ambient cistern. The surgeon then follows the SCA medially toward the basilar artery. This route ensures that proximal control will be achieved before encountering the sac. The basilar artery can be cleared anteriorly and posteriorly for a temporary clip. The inferior margin of the ipsilateral P1 is then identified, and dissection is carried across the anterior aspect of the basilar artery to the contralateral P1. Mistaking the contralateral SCA for the P1 can lead to occlusion of the contralateral P1 and its perforators with a clip. The SCA is differentiated from the PCA by remembering that the PCA is usually larger and invested with thicker tissue, whereas the SCA is usually red. This can be confirmed by continuing the dissection across to the contralateral P1-P2 junction and identifying the posterior communicating artery and cranial nerve III passing between the SCA and the P1.

After the anterior aspect of the basilar artery and both P1 origins have been identified and dissected free of arachnoid adhesions and blood, attention is turned to the posterior aspect of the aneurysm complex. Perforators emanating from the posterior wall of the basilar artery are often adherent to the neck and must be dissected free. This dissection is best started at the ipsilateral P1 and carried to the contralateral P1. The goal of this dissection is to create room for safe application of an aneurysm clip. Clip length should match the neck length as closely as possible because excessively long clips risk occluding medial perforators emanating from the contralateral P1. Short-bladed fenestrated clips are almost always used, with the P1 included in the fenestration. Conventional clips are appropriate for apex aneurysms projecting straight anteriorly or posteriorly. Although anteriorly projecting aneurysms may obscure the contralateral P1, the contralateral P1 occasionally can be visualized during the final phase of clip closure. Control of the microscope with the mouthpiece allows subtle maneuvering that can enhance visualization on both sides of the aneurysm during clip closure. The advantages of the subtemporal approach include the ease of visualization of posterior perforators and the ease of proximal control.22 The disadvantages of the approach include difficult access to the contralateral P1, which may be important for trapping or for inspection of the P1 perforators; the narrow field of view; and difficulty using the technique when the brain is swollen after SAH.22

Pterional Approach through the Extended Lateral Corridor

The main limitation of the subtemporal approach is the limited ability to see the contralateral P1 and its medial perforators. In contrast, the transsylvian approach is limited by poor visualization of the posterior perforators of the basilar artery. In an effort to combine the advantages of the subtemporal and transsylvian approaches while minimizing the limitations of each, we have developed a modified approach, the pterional approach through the extended lateral corridor (PAVEL).22,40 This extended lateral exposure has eliminated most of the risks and liabilities of the pure transsylvian and subtemporal approaches, and we employ it for the treatment of most upper basilar aneurysms that are treated surgically. The essential elements of PAVEL include the following:

• It is performed from the surgeon’s dominant side, which facilitates a due lateral dissection plane and clipping.
• Wide opening of the sylvian fissure is possible.
• The surgical field is centered on cranial nerve III.
• Mesial temporal lobe structures are elevated out of the incisura to the level of the cerebral peduncle.
• Posterior dissection is performed behind and below ipsilateral P1, not through the neck.
• The initial clip is fenestrated with a very small blade to close the contralateral neck.
• The final clip is a short, conventional clip to eliminate residual neck filling through the fenestration.

For this approach, the patient is positioned as for a pterional craniotomy. The head is rotated no more than 30 degrees away from the operative side to minimize the temporal lobe encroaching on the incisura. A frontotemporal scalp incision is extended down to the zygoma. The scalp is incised to the subgaleal plane but not through the temporalis fascia. As the scalp is reflected anteriorly in the subgaleal plane, we use an interfacial technique to identify the fat pad containing the frontalis branch of the facial nerve. This tissue is dissected away from the temporalis fascia to minimize retraction on the nerve. The temporalis muscle is divided along the zygoma, the anterior temporal squama, and the superior temporal line and reflected posteriorly, as described by Heros and Lee.41 These maneuvers minimize obstruction of the view along the skull base and usually obviate the need for a skull base approach such as the orbitozygomatic resection.

The craniotomy is performed with bur holes in the keyhole, at the posterior exposure of the superior temporal line, and at the root of the zygoma. A power craniotome is used to connect the bur holes and to extend the flap anteriorly to the mid-supraorbital ridge, yielding a rectangular free bone flap. An extensive subtemporal craniectomy is then performed to provide generous exposure of the anterior temporal tip. A drill and rongeurs are used to remove the inner table and thin the diploë of the frontal bone from the sphenoid ridge to the anterior extent of the flap. This provides additional exposure along the skull base and limits frontal lobe retraction. The sphenoid ridge is then drilled down to a degree that creates a continuous, unobstructed view along the skull base from the middle fossa floor to the floor of the frontal fossa. This extensive bony resection is essential to providing an unobstructed view of the basal cisterns while minimizing the need for brain retraction.

Dural Opening

After the bony resection is complete, the dura is opened with a semilunar incision extending from the anterior extent of the exposed frontal floor superiorly across the sylvian fissure to the posterior-inferior extent of the exposed middle fossa floor. The dural flap can then be reflected anterior-inferiorly with its base flush against the skull base.

Cerebrospinal Fluid Drainage, Hyperventilation, and Diuresis

As with the traditional approaches, CSF drainage, hyperventilation, and diuresis are critical for maximizing the view of the basilar apex without excessive brain retraction. CSF drainage can be accomplished by lumbar drainage or intraoperative ventricular puncture. We use the previously described Paine’s point to accurately tap the ventricle.35

Microdissection

As noted in the description of the transsylvian approach, the first critical phase of the microdissection in the extended lateral approach is to widely and completely dissect the sylvian fissure from the insular component medially through the sphenoidal fissure, including the carotid cistern. This maneuver is only complete when the surgeon can gently displace the frontal and temporal lobes independently, creating no traction whatsoever on the carotid, M1 segment, or M2 segment. At the completion of that sylvian dissection, the prechiasmatic cistern is opened to allow further CSF evacuation.

The next phase of the operation is to facilitate gravitational displacement of the temporal lobe directly posteriorly. The veins draining from the temporal lobe to the sphenoparietal sinus are divided, allowing gravitational displacement of the temporal lobe. Unlike during the subtemporal approach, the arachnoid binding cranial nerve III to the uncus is then sharply divided. Unlike the subtemporal maneuver, for this approach, the uncus must be displaced away from the third cranial nerve. A convenient way to organize this approach is to center the microsurgical field on the third cranial nerve all the way back to the interpeduncular cistern. By gently and sharply dissecting the mesial uncus from the third nerve, one arrives at the membrane of Liliequist uneventfully. With wide dissection of Liliequist, proximal control is achieved, and any subarachnoid clot can be removed. It is important to keep the anterior choroidal artery in view because it does come into the microsurgical field and could be compromised inadvertently as it swings up into the choroidal fissure. The initial phase of the dissection is facilitated by a frontal lobe retractor, and at this point, we normally insert a temporal lobe retractor, the tip of which is placed on the uncus, facilitating exposure of the tentorial incisura all the way back to the cerebral peduncle. With stealthy, subtle maneuvering of the microscope, the surgeon maneuvers the field of view to facilitate a directly lateral exposure of the basilar artery and the posterior reaches behind it. For left-handed surgeons, a left-sided approach is ideal. Dissection and clipping can occur from a lateral trajectory.

At this point, a temporary clip site is identified across the basilar trunk, and attention is turned to the posteriorly located thalamoperforate arteries. An important feel in the dissection of these vessels evolves over numerous years of experience with this exposure. Unlike cranial base tumor surgery, with vascular disease, the vascular structures can be displaced by the surgeon’s dominant or nondominant hand. In this circumstance, as the posterior aspect of the basilar artery is manipulated, gentle anterior displacement is performed, widening access to the perforating vessels. It is important to remember that most basilar apex aneurysms begin ballooning out just inferior to the P1 origins. Because of that circumstance and the fact that the perforators are easier to dissect proximal to where they become stretched around the posterior aspect of the fundus, dissection of these perforators is performed just inferior to the ipsilateral P1 segment. It is much more difficult to dissect these perforators above the P1 when trying to displace the actual fundus of the aneurysm anteriorly and to the contralateral side. This space is very tight and not conducive to safe dissection. As the P1 is mobilized anteriorly with the suction, the surgeon’s dominant hand can enter laterally to sharply dissect first the ipsilateral and then the contralateral thalamoperforators from posterior to the sac. This portion of the procedure is identical to what would be done using a subtemporal approach. With experience, it is possible to recognize the difference in course between the ipsilateral and contralateral perforators, which is critical because the contralateral P1 is exceptionally difficult to see from behind the complex. The initial course of P1 is almost always anterior as well as superior. After the contralateral thalamoperforators are identified, the posterior neck dissection is complete. At that point, using the advantages of the transsylvian component of this procedure, the contralateral neck can be dissected through this wide exposure.

Clipping is performed in two stages. The first step has the goal of closing the contralateral neck and gathering the neck into a much narrower structure. We use a short-bladed fenestrated clip, include the P1 in the fenestration, and work across to precisely close the contralateral neck. This maneuver always leaves filling of the sac through the fenestration just medial to the ipsilateral P1. During clip passage, the posterior blade is passed first while exposure is maintained with the suction tube; after the posterior blade is in precise precision, the mouthpiece is used to shift the scope anteriorly to benefit from the anterior transsylvian exposure. The contralateral P1 is identified, and the anterior blade is closed precisely to seal the contralateral neck. The residual aneurysm neck is then clipped superior to the P1 with a short conventional blade that misses the end of the fenestration of the primary clip.

Timing of Treatment

The peak incidence of repeat hemorrhage after SAH occurs in the first 48 hours.42 The peak incidence of vasospasm occurs 7 to 10 days after SAH.43 Early surgery after SAH avoids the morbidity and mortality associated with repeat hemorrhage and allows aggressive medical and interventional management of vasospasm.43 However, certain patients with basilar apex aneurysms may be harmed by early surgery. It has been our practice to delay surgery in the high-grade patient (i.e., Hunt-Hess grades IV and V) for a few days unless acceptable occlusion with endovascular therapy is feasible. We have frequently considered endovascular treatment for patients with high clinical grades. Of the various approaches, we have found that the subtemporal approach is particularly not well tolerated soon after hemorrhage in the high-grade patient. We have occasionally used aminocaproic acid in patients for whom we delay surgery, particularly if the subarachnoid portion of the bleeding is modest.

Temporary Occlusion

Proximal occlusion and trapping have important roles in basilar apex aneurysm surgery. The application of cerebral protectants such as barbiturates or propofol to achieve burst suppression, coupled with mild hypothermia (32° to 34°C) has increased the safety of temporary occlusion.44,45 Temporary occlusion allows the surgeon to soften the sac sufficiently to visualize the posterior perforators and safely place a clip and to mobilize the sac out of the interpeduncular cistern for posteriorly projecting aneurysms. Proximal occlusion is often sufficient, and complete trapping is needed, as in the case of thrombotic giants. In this situation, an anterior approach is advantageous because the contralateral P1 can be well visualized. The amount of time available for temporary occlusion is not entirely clear and may vary and depend on complex parameters, which are not yet easily decipherable. In a study considering 121 patients, patient age older than 61 years and poor neurological grade (i.e., Hunt-Hess grades III and IV) were associated with decreased tolerance for temporary occlusion compared with younger patients and those with lower-grade disease. In this study, patients occluded for less than 14 minutes did not develop infarcts, whereas those occluded for more than 31 minutes routinely developed infarcts. Although not statistically significant, there was a trend toward more infarction for occlusions proximal to perforator segments of the M1 and basilar artery and for increasing episodes of temporary occlusion.

Complication Avoidance

As for any other surgery, approaching the operation with a clear understanding of all complications and strategies for avoidance is paramount to achieving good results. Even technical perfection, however, does not preclude complications. One of the earliest technical challenges of surgery in the interpeduncular cistern was described by Drake: preservation of the perforators. Even transient occlusion of a perforator with a temporary clip can injure the vessel permanently. Temporary occlusion should be used when it can result in better visualization of the posterior perforators. This is particularly true of large aneurysms. Sharp dissection, maximal illumination, and the microscope mouthpiece are essential to safe and effective perforator visualization and dissection.

Leaving neck remnants can result in delayed aneurysm growth and hemorrhage.46–49 Whenever feasible, a second, small “baby clip” should be used to occlude neck remnants or “dog ears.” When these remnants cannot be tackled safely, the patient should be followed with serial angiography. If the remnant can be occluded by endovascular approaches, this should be considered.37 Clear distinction should be made between neck remnants and dome remnants, which represent a more dangerous and unstable situation. Such situations should be managed promptly with reoperation,38,46,50 if deemed feasible, or with endovascular coiling.

One of the major advantages of the endovascular era is that when a microsurgeon approaches a basilar apex aneurysm, the goal does not necessarily have to be focused on a perfect anatomic clip closure. In a number of circumstances when we encountered surprising findings such as perforator origins that were problematic related to the aneurysm fundus, we have gathered the neck with the previously described clip strategies only where it can be done safely and then stopped. This often leaves a tiny remaining portion of the neck patent, which can easily be accessible endovascularly. Usually a single coil deployed through that segment gives a perfect anatomic closure.

Intraoperative rupture is perhaps the most notorious intraoperative complication in aneurysm surgery.51 This complication is particularly dangerous for basilar apex aneurysms. When rupture occurs, the patient should be placed in burst suppression if this has not already been done. Gentle tamponade with a small piece of cotton is often effective. If tamponade fails within several minutes, temporary occlusion should be seriously considered. Prophylactic temporary occlusion in our opinion also reduces the incidence of intraoperative rupture.45 The use of adenosine has been reported52 for inducing temporary asystole when treating an intracranial aneurysm, and we have employed this occasionally with good results.

Each of the described approaches has its own unique complications. The subtemporal approach can be associated with temporal lobe swelling and herniation postoperatively. Serious consideration should be given to partial anterior temporal lobectomy when the temporal lobe appears “boggy.” We think the subtemporal approach should be avoided in the acute setting in a patient with a high-grade aneurysm. The vein of Labbé should be respected with this approach. We have found that placing moist Gelfoam and cottonoids on the vein and its connection with the transverse or sigmoid sinus before retraction helps avoid injury. The transsylvian approach can be associated with kinking of the Ml and its branches, with resulting postoperative infarction.27 In treating giant aneurysms, we avoid overly aggressive evacuation of the sac because collapse of the large sac may injure perforators owing to an “accordion” phenomenon.

Endovascular Management of Basilar Apex Aneurysms

Aneurysm coiling for some aneurysms has improved the natural history of SAH during short-term follow-up.53,54 The data regarding the use of detachable coils in the management of basilar apex aneurysms has significantly increased. Lessons have been learned regarding the safety, efficacy, limitations, and durability of coiling in this area. Although safety data are encouraging, concern remains regarding recurrence and higher rates of rehemorrhage after coiling when compared with clipping. Endovascular treatment is mainly a function of the morphology of the basilar apex aneurysm. The three most important factors are aneurysm neck size, aneurysm size, and relationship to the PCA.29 In a study by Raymond and colleagues of 31 patients treated with detachable coils, 29% of wide-necked aneurysms had a significant rate of recurrence.55 Of patients with aneurysm necks less than 4 mm, 77% had complete aneurysm occlusion.55 In a nonselected study population with basilar apex aneurysms, Klein and colleagues56 produced PCA occlusion in five patients (24%). This study highlights the fact that PCA anatomy can prevent complete aneurysm occlusion in a significant number of patients.

The multicenter Cerebral Aneurysm Rerupture After Treatment (CARAT)57 study reported the outcomes of patients with ruptured intracranial aneurysms treated with coil embolization or surgical clipping for basilar apex aneurysms. The degree of aneurysm occlusion after treatment was evaluated as a predictor of nonprocedural rehemorrhage. Of 1001 patients, there were 19 postprocedural rehemorrhages, with 58% of these leading to death. Degree of aneurysm occlusion after treatment was strongly associated with risk for rehemorrhage. The rehemorrhage rate after complete occlusion was 1.1%; it was 2.9% for 91% to 99% occlusion, 5% for 70% to 90% occlusion, and 17.6% for less than 70% occlusion. The authors reported that the risk for rehemorrhage tended to be greater after coil embolization than after surgical clipping, 3.4% and 1.3%, respectively. Overall, the degree of occlusion after initial treatment is a strong predictor of the risk for rehemorrhage in patients presenting with SAH, justifying attempts to completely occlude aneurysms. To achieve complete aneurysm occlusion safely in a high percentage of patients, coiling should be limited to small aneurysms with neck sizes less than 4 mm and PCAs that do not originate from the dome.55,56,58

Conclusion

Achieving successful outcomes for patients with simple and complex aneurysms of the basilar apex requires thoughtful diagnostic work-up, careful preparation and development of a strategic plan, and a detailed microsurgical understanding of normal neuroanatomy and the patient’s specific anatomic variables. It is critical that multidisciplinary teams evaluate these patients.59 These aneurysms should not be treated at centers that are not identified as cerebrovascular centers, with all that entails. The time has passed when the focus was on the rhetoric of determining whether clipping or coiling was the superior option. Our understanding of these lesions and complications of therapy has taken us to a point at which cases can be analyzed critically and decisions highly individualized. Critical variables include patient age and therefore years of exposure to recurrence, clinical grade, neck width, size of the aneurysm, associated thrombosis, and anatomic variance.

If a surgical strategy is determined to be optimum for the individual patient, enormous concentration must be focused on every detail of the operation because the margin for error is nonexistent. The surgeon should be experienced, relaxed, and psychologically prepared for unexpected problems of anatomy or intraoperative rupture. During times of temporary arterial occlusion, the surgeon must move quickly and thoughtfully to minimize the ischemic risk. In the current era, surgical teams must be able to slip in and out of these narrow confines, leaving only a clip or two as evidence that the spaces have been violated.

Suggested Readings

Batjer H, Samson D. Intraoperative aneurysmal rupture: incidence, outcome, and suggestions for surgical management. Neurosurgery. 1986;18:701-707.

Batjer HH, Frankfurt AI, Purdy PD, et al. Use of etomidate, temporary arterial occlusion, and intraoperative angiography in surgical treatment of large and giant cerebral aneurysms. J Neurosurg. 1988;68:234-240.

Batjer HH, Samson DS. Causes of morbidity and mortality from surgery of aneurysms of the distal basilar artery. Neurosurgery. 1989;25:904-915.

Bendok BR, Ali MJ, Malisch TW, et al. Coiling of cerebral aneurysm remnants after clipping. Neurosurgery. 2002;51:693-697.

Bendok BR, Getch CC, Malisch TW, Batjer HH. Treatment of aneurysmal subarachnoid hemorrhage. Semin Neurol. 1998;18:521-531.

Bendok BR, Getch CC, Parkinson R, et al. Extended lateral transsylvian approach for basilar bifurcation aneurysms. Neurosurgery. 2004;55:174-178.

Ciacci J, Bendok B, Getch C, Batjer HH. Pterional approach to distal basilar aneurysms via the extended lateral corridor: PAVEL. Tech Neurosurg. 2000;6:221-227.

Drake CG. Bleeding aneurysms of the basilar artery: direct surgical management in four cases. J Neurosurg. 1961;18:230-238.

Drake CG. Ligation of the vertebral (unilateral or bilateral) or basilar artery in the treatment of large intracranial aneurysms. J Neurosurg. 1975;43:255-274.

Drake CG. The treatment of aneurysms of the posterior circulation. Clin Neurosurg. 1979;26:96-144.

Drake CG, Barr HW, Coles JC, Gergely NF. The use of extracorporeal circulation and profound hypothermia in the treatment of ruptured intracranial aneurysm. J Neurosurg. 1964;21:575-581.

Drake CG, Peerless SJ. Giant fusiform intracranial aneurysms: review of 120 patients treated surgically from 1965 to 1992. J Neurosurg. 1997;87:141-162.

Gross BA, Hage ZA, Daou M, et al. Surgical and endovascular treatments for intracranial aneurysms. Curr Treat Options Cardiovasc Med. 2008;10:241-252.

Heros RC, Lee SH. The combined pterional/anterior temporal approach for aneurysms of the upper basilar complex: technical report. Neurosurgery. 1993;33:244-250.

Hsu FP, Clatterbuck RE, Spetzler RF. Orbitozygomatic approach to basilar apex aneurysms. Neurosurgery. 2005;56:172-177.

Johnston SC, Dowd CF, Higashida RT, et al. Predictors of rehemorrhage after treatment of ruptured intracranial aneurysms: the cerebral aneurysm rerupture after treatment (carat) study. Stroke. 2008;39:120-125.

Krisht AF, Kadri PA. Surgical clipping of complex basilar apex aneurysms: a strategy for successful outcome using the pretemporal transzygomatic transcavernous approach. Neurosurgery. 2005;56:261-273.

Krisht AF, Krayenbuhl N, Sercl D, et al. Results of microsurgical clipping of 50 high complexity basilar apex aneurysms. Neurosurgery. 2007;60:242-250.

Lawton MT. Basilar apex aneurysms: surgical results and perspectives from an initial experience. Neurosurgery. 2002;50:1-8.

Paine JT, Batjer HH, Samson D. Intraoperative ventricular puncture. Neurosurgery. 1988;22:1107-1109.

Raymond J, Roy D, Bojanowski M, et al. Endovascular treatment of acutely ruptured and unruptured aneurysms of the basilar bifurcation. J Neurosurg. 1997;86:211-219.

Rice BJ, Peerless SJ, Drake CG. Surgical treatment of unruptured aneurysms of the posterior circulation. J Neurosurg. 1990;73:165-173.

Samson D, Batjer HH, Bowman G, et al. A clinical study of the parameters and effects of temporary arterial occlusion in the management of intracranial aneurysms. Neurosurgery. 1994;34:22-28.

Samson D, Batjer HH, Kopitnik TAJr. Current results of the surgical management of aneurysms of the basilar apex. Neurosurgery. 1999;44:697-702.

Vinuela F, Duckwiler G, Mawad M. Guglielmi detachable coil embolization of acute intracranial aneurysm: perioperative anatomical and clinical outcome in 403 patients. J Neurosurg. 1997;86:475-482.

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