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Surgical Treatment of Giant Basilar Artery Aneurysms
Surgical Treatment of Giant Basilar Artery Aneurysms Christopher C. Getch, MD,* Brian A. O’Shaughnessy, MD,* Bernard R. Bendok, MD,† and H. Hunt Batjer, MD* Microsurgical clip reconstruction of a giant basilar artery aneurysm is considered one of the most challenging operative endeavors in neurosurgical practice. The operation, when carried out successfully, requires both surgical skill and intraoperative judgment. The authors present the surgical approaches and techniques used for the treatment of giant basilar artery aneurysms. In particular, the authors emphasize the extended lateral transsylvian approach, an exposure developed by the senior author (H.H.B.). In addition, this paper details the methods of preoperative evaluation, skull base approaches, proximal occlusive techniques, and the use of cerebral revascularization strategies as an adjunct in aneurysm obliteration. Oper Tech Neurosurg 8:104-113 © 2005 Elsevier Inc. All rights reserved. KEYWORDS basilar artery, clipping, coiling, giant aneurysm, Hunterian, microsurgery
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iant aneurysms (greater than 2.5 cm) of the basilar apex, trunk, or confluence represent some of the most formidable therapeutic challenges confronting vascular neurosurgeons. The poor natural history of these lesions, especially when symptomatic, is well documented.1-3 Drake’s report of 31 patients with untreated giant intracranial aneurysms illustrates the dismal prognosis of these lesions with a 68% mortality rate at 2 years and about an 80% mortality rate at 5 years.2 Advances in surgical technique, anesthesia, imaging, and more recently endovascular technique have helped increase the success of treating these lesions. Each patient harboring a giant basilar aneurysm brings a unique set of problems. We have found that there is no single right answer to treating these aneurysms. More often a customized strategy must be derived from the results of diagnostic tests and from the menu of available treatment options. Diagnostic studies such as magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), computed tomography angiography (CTA), digital subtraction angiography (DSA), MR and CT perfusion, and the results of trial parent artery occlusion allow the selection of treatment options including direct surgical reconstruction with or without a skull base approach,
*Department of Neurological Surgery, Northwestern University Feinberg School of Medicine, Chicago, IL. †Department of Neurological Surgery and Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL. Address reprint requests to Christopher C. Getch, MD, Associate Professor, Department of Neurological Surgery, Northwestern University Feinberg School of Medicine, 676 N. St. Clair Street, Suite 2210, Chicago, IL 60611; [email protected]
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1092-440X/05/$-see front matter © 2005 Elsevier Inc. All rights reserved. doi:10.1053/j.otns.2005.09.003
use of circulatory arrest, revascularization, or permanent parent artery occlusion (Hunterian strategies). This article discusses the treatment of giant basilar artery aneurysms from a surgical perspective including adjunct endovascular strategies when appropriate.
Patient Selection One of the most important factors in achieving a successful surgical outcome is careful patient selection. Information vital for determining whether a patient is a candidate for direct surgical reconstruction or is better managed by a Hunterian strategy is derived primarily from the results of preoperative imaging interpreted in the context of a patient’s clinical status. Routinely, the evaluation of a patient harboring a giant basilar aneurysm includes MRI, CTA, and DSA with a temporary parent artery occlusion test when appropriate. Each modality provides information valuable to the decision-making process. MRI and MRA provide information on the degree of aneurysmal sac thrombosis, quality of the neck tissue, and the precise relationship of the pathology to critical neurologic structures, particularly the cranial nerves and brainstem. CTA with 3-D reconstructions defines branch anatomy and provides information on the presence of calcification within both the sac and neck. Combining CTA and axial MRI is essential in planning the corridor for surgical access and in determining whether a standard or skull base approach would be more beneficial. Wide surgical exposure is fundamental to successful management. Conventional angiography provides essential anatomic and hemodynamic information and the potential for collateral supply. A tempo-
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Figure 1 Anteroposterior (a) and lateral (b) vertebral angiograms show a complex confluence giant aneurysm. Careful analysis of the angiograms reveals a complex aneurysm with a large saccular component and a lower basilar ectatic component. Adequate exposure of an aneurysm in this location includes a suboccipital craniectomy that extends down through the foramen magnum and a limited petrosectomy for additional exposure. The aneurysm was treated with direct clip reconstruction of the saccular component. The ectatic portion did not require treatment.
rary parent artery occlusion test establishes whether a patient is likely to tolerate a Hunterian strategy or whether revascularization is needed before vessel occlusion. Many variables must be considered to determine the appropriateness of direct surgical clip reconstruction for a patient with a giant basilar aneurysm. Several general questions must first be answered. Is the pathology amenable to direct reconstruction? Is the critical anatomy favorable and accessible? Can the reconstruction be accomplished in an acceptable period of temporary arterial occlusion? In our experience, pathologies that are unamenable to direct reconstruction providing a long-term durable solution are dolichoectatic and dissecting aneurysms.4 Both pathologies typically involve a circumferentially diseased vessel that is more successfully managed with Hunterian strategies or with trapping combined with revascularization. Alternatively, in some patients with complex and unreconstructable dolichoectatic lesions, the saccular component alone can be clipped (Fig. 1). In the setting of a dolichoectatic aneurysm, exploration with partial gathering of the sac to relieve mass effect may be beneficial in rare circumstances.4 It is possible that future endovascular technologies may provide a benefit. Favorable anatomy for clip reconstruction depends on configuration and height of the branches and neck (relative to the posterior clinoid), presence of calcification in the neck and sac, the presence and degree of thrombus, collateral supply, and in certain cases, an eccentric displacement of the anatomy that improves access. In general, the presence of extensive calcification is an impediment to direct clipping. It primarily affects clip-closure, necessitating multiple clips in the setting of limited space. Calcification combined with extensive atherosclerosis in
the sac can make clipping more difficult by stenting the neck open and driving the clip onto the parent vessel. The presence of calcification and atherosclerotic changes in the sac and neck are often present simultaneously in the parent vessels and increase the risk of temporary clipping during reconstruction. Massive thrombosis with a small patent aneurysm lumen also increases the risk of unsuccessful clip reconstruction. A significant degree of thrombosis mandates trapping and opening of the aneurysm, increasing the length of ischemia. Aneurysms with a significant degree of thrombosis in elderly patients who are less likely to tolerate temporary occlusion are perhaps better candidates for Hunterian strategies (Fig. 2). Furthermore, a small residual patent lumen within a large thrombotic sac likely necessitates dissection of the thrombus from the proximal neck tissue, potentially leading to intimal injury in the neck and thrombosis of the reconstructed lumen. A broad neck is uniformly encountered in giant aneurysms and is not a contraindication to direct surgical reconstruction. In the setting of a giant aneurysm with a particularly broad neck, the distance from the parent vessel inflow to the outflow branches must be assessed critically. In this setting, it is of primary importance to determine that the outflow branches can be visualized from the operative approach. Exploration of an aneurysm whose outflow is significantly displaced from the parent vessel often reveals poor quality tissue unfavorable for durable reconstruction. Occasionally, eccentric displacement of the vascular anatomy offers an advantage, shortening the working distance to the critical anatomy. Each of these complicating morphological challenges are as-
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duncular cistern, these same maneuvers carry a high risk of neurological injury. When considering direct reconstruction of a giant basilar aneurysm, the surgeon should always have a backup strategy. The presence of a robust collateral supply can provide an exit strategy, increasing the safety of an attempt at direct surgical clipping. In the setting of a giant basilar apex aneurysm, a particularly useful collateral configuration that provides an exit strategy is the presence of a unilateral or bilateral posterior communicating artery. A robust posterior communicating artery offers the option of placing a clip above one posterior cerebral artery and below the other. With its antegrade flow eliminated, the posterior cerebral artery is subsequently irrigated through the patent communicator with a high likelihood that the aneurysm will thrombose even if the proximal P1 is not clipped. This strategy can significantly shorten the distance needed for clip placement, potentially avoid unfavorable neck calcification, and facilitate safe spacing of perforators. Once a giant basilar aneurysm has been deemed surgically reconstructable, access becomes the primary concern. Numerous options are available for gaining access to the upper, mid- and lower basilar trunk: standard approaches, modified skull base approaches, or traditional skull base approaches. Careful consideration must be given to exactly what components of the vascular anatomy must be visualized and how much of the sac and neck must be available for reconstruction.
Surgical Access Pterional (Transsylvian) Approach
Figure 2 Axial CT (a) and lateral vertebral angiogram (b) demonstrate a giant calcified thrombosed basilar apex aneurysm unamenable to direct conventional clip reconstruction. Treatment options considered included reconstruction under circulatory arrest through an extended lateral transsylvian approach with or without orbitozygomatic extension, proximal parent artery occlusion with or without revascularization, and stent reconstruction without coils to redirect flow. Ultimately, a Hunterian strategy was selected.
sociated with large and giant aneurysms throughout the cerebrovascular tree. It is critical to recognize that aneurysms of the upper basilar artery are different than their cohorts in the anterior circulation or proximal vertebral artery. For such a lesion at the bifurcation of the middle cerebral artery (MCA), for example, an abundance of easily acquired exposure facilitates the surgical creativity required to evacuate thrombus, to crush a calcified neck, and to deal with differential wall thickness. The paucity of critical perforating arteries at this location increases the safety margin. When performed in the interpe-
The pterional approach, particularly with wide sylvian fissure dissection, is extremely versatile and used for many aneurysms of the distal basilar complex. Wide dissection of the parasellar cisterns enables access to the interpeduncular cistern by one or more routes. The dissection plane and the approach can be developed lateral to the internal carotid artery wherein the posterior communicating artery is followed to the junction of the P1 and P2 segments of the posterior cerebral artery. P1 is then followed along its inferior surface proximally to isolate proximal control on the distal basilar artery safely away from aneurysmal tissue. Similarly, a dissection plane can be developed medial to the carotid artery that separates the small perforating arteries to the hypothalamic region and optic tract, opening the membrane of Liliequist. Therefore, the basilar trunk is directly exposed in the interpeduncular cistern. In particularly high basilar bifurcation aneurysms, it may be necessary to gain additional superior exposure by developing the plane immediately above the carotid bifurcation. This maneuver can be performed by carefully dividing the arachnoidal fibers that bind the small lenticulostriate vessels. With patience, this tissue can be separated adequately to allow elevation of the optic tract with workable space within the interpeduncular cistern. In fact, regardless of the procedure, defining each of these planes minimizes obscuration of vital anatomy by instruments placed in the exposure. This transsylvian exposure can be used to treat a wide variety of aneurysms in this location because it allows the
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surgeon a good view of the anatomy. It also enables exquisite access to the proximal basilar trunk and both P1 segments for definitive temporary occlusion with aneurysmal decompression, if necessary, to control intraoperative bleeding or to facilitate the dissection of difficult large and giant lesions.
Half-and-Half Approach Drake has described this modification of the pterional exposure to improve access to the posterior reaches of the interpeduncular cistern through a slightly more lateral viewpoint.2 This idea was generated to facilitate exposure to carotid aneurysms after a basilar aneurysm was exposed subtemporally. This approach involves rotating the head a bit more than in a direct transsylvian exposure and mobilizing the temporal lobe with superior and slightly lateral displacement of the uncus. In addition to the improved posterior exposure, this approach offers an improved view of the entire interpeduncular fossa and carotid cistern. In many circumstances, it is a very desirable approach to plan from the outset of the procedure.
Subtemporal Approach The lateral view of the interpeduncular cistern, which was highly developed by Drake,2 perhaps offers the ideal view of the vital perforators posterior to the aneurysmal fundus. For the typical superior-projecting aneurysm, this viewpoint maximizes the surgeon’s ability to salvage the perforating arteries. The contralateral posterior cerebral artery, however, is more difficult to see and quite difficult, if not impossible, to occlude temporarily. For a standard subtemporal clipping, however, the space anterior to the aneurysmal neck can usually be retracted gently so that the contralateral P1 segment with its initial anterior course can be definitively seen. Drake’s innovation of the aperture or fenestrated clip greatly simplified subtemporal clipping of basilar bifurcation aneurysms so that the P1 segment and any associated perforating arteries can be included in the fenestration. The limited exposure afforded by the isolated subtemporal procedure severely limits its application to giant aneurysms in this area, except in the realm of Hunterian strategies with or without revascularization.
Extended Lateral Approach Over the past several years at our institution, a continued struggle with basilar apex aneurysms has resulted in the evolution of a hybrid operative approach. Conceptually, both the transsylvian and subtemporal approaches have certain advantages and disadvantages. The transsylvian view has the advantage that all five involved vessels can be seen en face. The surgeon has immediate access to full trapping of the circulation at that site. The primary disadvantage of the transsylvian view is the relatively poor access to the posterior reaches of the interpeduncular cistern where the perforating vessels lie. The great advantage of the subtemporal view is that the lateral view facilitates exposure and dissection of the posteriorly located perforators as well as ease of proximal control. The primary disadvantage of this approach is that the exposure is narrow. It is rare to have access to all appropriate vessels for a full trapping, should that be required. The extended lateral exposure is performed from the sur-
Figure 3 An intraoperative image after a left-sided extended lateral transsylvian approach to a giant basilar apex aneurysm shows the extensive exposure gained from this approach. The neck of the aneurysm was accessed and clipped through a corridor above the basilar bifurcation. (Color version of figure is available online.)
geon’s dominant side. A traditional pterional craniotomy is performed, followed by wide resection of the temporal squama and sphenoid ridge. An orbitozygomatic osteotomy can be added if the target lesion is very high. The sylvian fissure is dissected completely, and the sphenoparietal venous drainage is detached from the floor of the middle cranial fossa. With complete sylvian dissection and gravitational assistance, the temporal lobe migrates posteriorly. The surgical dissection does not focus on the opticocarotid triangle or the posterior communicating artery corridor. Rather, this approach focuses on the third cranial nerve. All attachments between the third cranial nerve and the uncus are removed. As the exposure deepens, the uncus and all temporal lobe structures that have migrated into the incisura are elevated by a temporal lobe retractor. This maneuver gives the surgeon access to the tentorial incisura as far back as the cerebral peduncle. At that point, when performed from the surgeon’s dominant side, access to the direct lateral view (just as in a subtemporal approach) is impressive (Fig. 3). Therefore, the assets of each primary approach are capitalized on (perforator exposure and access to the contralateral P1 and superior cerebral arteries) and the liabilities of both approaches are eliminated. The surgeon can dissect perforators from a lateral view, and during clip application, with simple adjustments of the microscope, have access to the full benefits of the wide transsylvian view for precise viewing of the contralateral neck. A final point has greatly simplified clipping of these treacherous lesions. The true surgical neck is avoided on the operated side, and the dissection begins inferior to the P1 origin. The difficulty posed by the broad neck of these aneurysms and the constant finding that the aneurysm sac itself begins to develop well below the superior aspect of the P1 origin are thereby eliminated. When performed below the P1 origin, the dissection allows the surgeon to work across the basilar trunk at a site where the distance to be traveled is considerably foreshortened. This key maneuver facilitates a primary clip application using a strong and short fenestrated clip below the proximal P1.
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Cranial Base Exposures for Intracranial Aneurysms In recent years, modifications to some of the previously described operative exposures have enabled neurosurgeons to treat complex aneurysms arising within the constraints of the cranial base more effectively. The broader exposure yielded by these procedures provides the surgeon with an enhanced view of the vascular anatomy with little or no need for brain retraction, and perhaps most importantly, additional working room. The exposures most beneficial to neurovascular surgeons are detailed below.
Orbitozygomatic Approach The addition of an orbital or orbitozygomatic osteotomy to a standard pterional craniotomy should be considered with giant basilar apex aneurysms. The additional 10 to 15 degrees of exposure this maneuver provides is invaluable when a large thrombotic sac is encountered or when high exposure is needed up into the diencephalon. After a standard pterional craniotomy is performed as described previously, dura overlying the orbital roof is stripped posteriorly toward the orbital apex, medial to the cribriform, and lateral to the dura of the superior orbital fissure. Periorbita is stripped from the superior and lateral walls of the orbit to a depth of approximately 3 cm. If the zygomatic process is to be included into the osteotomy, the full extent of the zygomatic arch is exposed before the temporalis muscle is reflected. The orbitzygomatic segment is best resected with a combination of reciprocating saw and osteotomes. The initial bone cuts are made with a reciprocating saw through the supraorbital ridge and frontal zygomatic process. The former is just lateral to the supraorbital foramen. Narrow osteotomes complete the resection across the orbital roof and greater and lesser wings of the sphenoid bone. Once the masseter has been released from the inferior surface of the zygomatic arch, the piece can be removed en bloc. At least 3 cm of the orbital roof and lateral wall must be preserved to minimize the possibility of postoperative pulsatile enophthalmos. Perhaps the most important element of this exposure is the resection of the proximal lesser and greater wings of the sphenoid bone, inclusive of the anterior clinoid process. The postclipping reconstruction is performed in a standard fashion with a microplating system and hydroxyapatite compound or methylmethacrylate to fill in any bony defects.
Petrosal Approach The combined subtemporal, suboccipital, or petrosal approach provides the most direct access to aneurysms from the basilar apex to the vertebrobasilar junction. Variations of this approach include a retrolabyrinthine exposure, a partial labyrinthectomy, a total labyrinthectomy, and a transcochlear resection with facial nerve mobilization. At our institution, the retrolabyrinthine or partial labyrinthine exposure is most favored because they are the only petrosal approaches that preserve hearing. The patient is positioned supine with a shoulder roll ipsilateral to the side of the approach. The head is turned 90 degrees and gently extended toward the floor. If necessary, the shoulder is taped caudally. A curvilinear incision begins 2 cm superior and anterior to the ear. It curves along a 2-cm
C.C. Getch et al. posterior margin from the ear to a point 2-cm inferior to the mastoid tip. The temporalis and occipital frontalis muscles are divided and reflected laterally with the scalp to expose the external auditory meatus centrally, the temporal zygomatic root rostrally, and the entire mastoid process posteroinferiorly. A mastoidectomy is performed with early identification and skeletonization of the transverse and sigmoid sinuses as far laterally as the jugular bulb. When only a retrolabyrinthine, presigmoid exposure is necessary, care is taken to preserve the bony labyrinth. With a partial labyrinthectomy, as many as five additional millimeters of room can be obtained to provide several degrees of added maneuverability at the level of the petrous apex. Doing so requires cautious drilling of the posterior and superior semicircular canals to expose the underlying membranous labyrinth. Once identified, the exposed orifices are immediately waxed. The horizontal semicircular canal is preserved. A completed mastoidectomy should expose the temporal and posterior fossa dura. This dural exposure facilitates the addition of a subtemporal and suboccipital craniotomy. Typically, the dural opening is presigmoid, originating just superior and anterior to the jugular bulb and directed toward the superior petrosal sinus. The sinus is ligated, and the dural cut proceeds rostrally to the dura of the middle fossa. Then the dura is tented laterally. The tentorium is coagulated with the bipolar cautery and cut toward the incisura. Care is exercised to avoid injury to the fourth cranial nerve as it courses adjacent to the midbrain en route to the tentorial edge. The tentorium can be partially excised or coagulated to enhance visualization. The midbrain, clivus, basilar artery, and cranial nerves III to XII are clearly visible with this exposure. A modification of this approach that includes a retrosigmoid dural exposure with ligation of the nondominant transverse sinus has been described. In our experience, however, this maneuver creates an unacceptable risk of venous infarction. After the aneurysm has been secured appropriately, a watertight dural closure should be attempted. A dural graft is necessary. Mastoid air cells should be waxed thoroughly, and fat should be placed in the mastoid defect. Lumbar spinal fluid drainage should be considered when a watertight dural closure cannot be achieved.
Modified Far-Lateral Transcondylar Approach for Lower Basilar Trunk Aneurysms Aneurysms of the confluence and lower basilar trunk up to the origin of the anterior inferior cerebral arteries are comfortably accessible through a far-lateral exposure. The addition of a partial condylectomy gains access to the ventral brainstem. This approach requires that the patient be positioned in a park bench or three-quarter prone position as previously described. We favor a curvilinear incision that typically projects from the midline at C1 to C2 superiorly to 1-cm superior to the inion. It then curves laterally to 2 cm posterior to the ipsilateral ear and continues caudally. It ends 3-cm posteroinferiorly to the mastoid tip, just over top the midportion of the sternocleidomastoid muscle.
Giant basilar aneurysms The scalp and fascia are reflected medially to expose the underlying intermixed fascia of the first layer of muscles, which includes the occipital frontalis, trapezius, and sternocleidomastoid muscles. These muscle layers are divided at their attachment to the superior nuchal line. Trapezius is reflected inferomedially, and the sternocleidomastoid is detached from the mastoid process and reflected inferolaterally. The spinalis capitis and semispinalis capitis are sequentially detached from the occiput. The occipital artery can be dissected free of the longissimus capitis, and this muscle is caudally reflected from its attachment to the undersurface of the mastoid process. With these muscles reflected, the suboccipital triangle is brought into view. The triangle is composed of the recti and obliquus muscles. The superior oblique and inferior oblique muscles can be followed laterally to their attachment to the C1 lateral mass and then should be detached. At this point, a bur hole is placed just caudal to the mastoid. A suboccipital craniotomy is performed inclusive of the foramen magnum. With the vertebral artery isolated in a vessel loop, the atlo-occipital joint is drilled medially to laterally. At least 50% of the joint must be preserved to avoid creating instability and to obviate a subsequent fusion procedure. The condylar vein are encountered with drilling and can typically be controlled with bipolar cautery and bone wax. The dura can be opened in a series of small triangles based on the transverse and sigmoid sinuses and condyle.
Clip Reconstruction Direct clip reconstruction strategies are the most desirable, but successful clip reconstruction is influenced by many variables. These variables include the quality of the tissue in the neck, the presence of calcified athermatous plaque, intraluminal thrombus, favorable primary and vital perforator artery anatomy in relation to the surgical neck, and a wellplanned and executed surgical strategy with adequate exposure. An essential part of direct clip reconstruction is obtaining adequate exposure. Exposure is not limited just to the neck of the aneurysm. Direct visualization of the primary inflow and outflow from the aneurysm is needed because temporary proximal occlusion or trapping is often part of the reconstruction strategy. There must be adequate room for multiple temporary clips to be positioned so that they do not interfere with the definitive clipping. A thorough exploration through an adequate surgical window is essential to eliminate the presence of a small perforator, which commonly emanates from the sac and precludes its inclusion in the clip construct. The final stages of this exploration can be facilitated by placing a temporary proximal clip to reduce the turgor within the aneurysm sac itself. Unfavorable perforator anatomy is an excellent reason to abandon direct surgical reconstruction and to seek an alternative strategy. Based on his clinical experience, Drake believed that less than half of giant basilar aneurysms could be clip-reconstructed directly.2 Once the vessel anatomy has been explored thoroughly and deemed favorable for clipping, the neck tissue must be examined closely to determine whether calcification is present and how it will likely respond to clip compression. An irregular pattern of wall thickness and calcification often
109 results in persistent aneurysmal filling despite the surgeon believing that clipping has been definitive. In our institutional experience, clip reconstruction of a giant aneurysm is almost never encountered. Strategies using multiple short, fenestrated, or angle clips are almost uniformly necessary to reconstruct the broad, thick aneurysm neck. When wall thickness is variable, a combination of straight and fenestrated clips can be used to solve this problem. The fenestrated clip can be placed around the thickened or calcified portion of the neck. Subsequently, a short, powerful straight clip is placed to close the fenestration. The presence of calcified plaque within the neck also can be dealt with using a fenestrated clip. In necks that appear to harbor only thickened tissue, a series of parallel clips can be used. Typically, the first clip is often driven by the thickened neck down onto the parent vessels. This clip, when left in place temporarily, can serve as a support for additional clips as they are stacked on the neck. The first clip is removed as the other clips gain purchase. In the setting of a thrombosed aneurysm, the amount of patent sac lumen must be determined. It is easy to underestimate the amount of patent sac needed for clip reconstruction. Additional tissue that can be used to facilitate reconstruction can be gained by trapping the aneurysm, opening it, and resecting thrombus. A microtipped ultrasonic aspirator and pancake curettes are particularly useful for removing thrombus from the aneurysm sac. At this point, care must be taken not to damage the intimal layers in the neck and parent vessel. Doing so leads to premature thrombosis of the reconstructed vessel. When reconstruction is planned in the setting of a thrombosed giant sac, the time required to clear the thrombus must be carefully calculated into the total time required for reconstruction. When a particularly broad neck is encountered or created by having to leave a large cuff of tissue in the setting of a thrombosed aneurysm, a clip-cut-clip technique can be used. With the aneurysm trapped and evacuated, the clip reconstruction begins ipsilaterally with placement of a short, straight clip. Short clips provide the necessary closing force on the thickened neck. Furthermore, short clips placed in series can compensate for the variable thickness in the aneurysm wall. The placement of a second short, straight clip in series with the first is facilitated by cutting the aneurysmal tissue just distal and parallel to the first clip to within 1 to 2 mm of the tip of the first clip. Several short clips can be deployed in this fashion. When completed, the appearance of the reconstructed neck is slightly saw-toothed.
Hunterian Strategies When direct surgical reconstruction of a giant basilar aneurysm cannot be accomplished, alternative strategies such as endovascular stent-assisted coiling or Hunterian strategies must be considered (Fig. 4). The long-term efficacy of stentbased treatment is still unknown. However, a significant body of literature supports the successful treatment of giant basilar aneurysms with Hunterian strategies.5 Steinberg et al5 reported the extensive London, Ontario experience with Hunterian strategies for the treatment of giant basilar aneurysms. They described the long-term results of 201 patients who underwent deliberate basilar or vertebral
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Figure 4 T1-weighted sagittal MRI (a) demonstrates a giant vertebral artery aneurysm exerting significant mass effect. Right vertebral artery injection (b) reveals a giant right vertebral artery aneurysm. Because the vertebral artery contralateral to the aneurysm provides adequate filling of the basilar artery (c), the optimal strategy includes trapping of the aneurysm segment coupled with revascularization of PICA. The aneurysm can be approached through a suboccipital craniectomy with a modified far-lateral approach.
artery occlusion to giant basilar aneurysms. The mean follow-up was 9.5 years. Several different Hunterian strategies were used to treat giant aneurysms of the posterior circulation. Overall, long-term results were excellent in 68%, good in 5%, and poor in 3%. Twenty-four percent died. Clinical outcomes varied by location. Good to excellent results were achieved in 64% of basilar apex aneurysms, in 76% of basilar
trunk aneurysms, in 74% of vertebrobasilar junction aneurysms, and in 87% of vertebral aneurysms. Various Hunterian strategies resulted in successful aneurysm thrombosis in 78% of patients, and few of these patients developed late neurological complications (4%). Conversely, in patients who had incompletely thrombosed aneurysms, a significantly higher rate of late neurologic deterioration oc-
Giant basilar aneurysms curred (67%), 86% of which proved fatal. Tolerating basilar or vertebral artery occlusion correlated well with the presence of a large (greater than 1 mm) posterior communicating artery. Within the first week of Hunterian treatment, 26 patients (13%) deteriorated from vertebrobasilar ischemia with thrombosis or embolism, which was more common than hemodynamic insufficiency. In addition to a smaller series, these results serve as the foundation for designing a successful Hunterian strategy. The most essential component in the evaluation of a patient being considered for a Hunterian strategy is their response to a balloon trial occlusion (BTO) of either the basilar or vertebral artery. The technique of parent vessel test occlusion has been refined. Now, a highly selective occlusion can be performed at or just proximal or distal to the pathology. Doing so minimizes the risk of complications during the test. Equally importantly, it accurately recreates the hemodynamic environment likely to be encountered during permanent occlusion. Simultaneous angiography offers an even more precise picture of the altered hemodynamic flow by demonstrating the collateral channels. Our protocol for temporary and permanent occlusion of cerebral arteries has been reported.6 It includes simultaneous clinical, angiographic, and neurophysiological assessment in both normotensive and mildly hypotensive (20-30% reduction in the mean arterial pressure) conditions. The single most important factor to be considered when performing a BTO is where the temporary occlusion should be performed. This locale should be determined before access is obtained and should accurately reflect where the parent artery is likely to be sacrificed. The site of temporary arterial occlusion is influenced by a number of factors, including the location of the aneurysm, the presence and size of the vertebral, posterior inferior cerebellar, internal carotid arteries, and finally the presence and size of the posterior communicating arteries. A stable thrombosed aneurysm is the goal, and careful consideration must be given to altered hemodynamics, whether preservation of antegrade flow or reversal of flow gives the most desirable effect. After a patient successfully passes BTO at the appropriate location, permanent occlusion is usually performed in a separate procedure, either surgical or endovascular. In our experience, surgical exploration with clip placement for either proximal occlusion or trapping offers a more precise point of occlusion and may avoid inadvertent perforator occlusion during an endovascular procedure (Fig. 5). In patients who fail BTO, revascularization options must be considered. The location and type of revascularization depend on whether the patient has failed by both clinical and neurophysiological assessments or by EEG or single photon emission computed tomography, or by hypotensive challenge only.
Revascularization Strategies The adjunctive use of cerebral revascularization plays an important role in the surgical treatment of many giant aneurysms of the basilar artery. Two situations in which revascularization is used in the treatment of giant basilar artery
111 aneurysms are the most common: (1) when a Hunterian approach is implemented and the native collateral flow is insufficient to sustain the basilar artery circulation; and (2) as a prophylactic measure when prolonged periods of temporary arterial occlusion are anticipated for aneurysm exclusion and parent artery reconstruction. Although the technical skills required for the anastomosis are almost the same as those applied in anterior circulation, the deep and restricted confines in which the surgeon must work to perform a posterior circulation bypass leads to a considerably more challenging procedure. Initially, the need for revascularization is determined by critical evaluation of the cerebral angiogram, including the caliber of the posterior communicating arteries, the extent of antegrade flow up the basilar trunk, and the symmetry and timing of venous outflow. Angiographic examination of the external carotid artery circulation is advocated at the time of the initial angiogram because it is necessary for planning the specific revascularization procedure. Most frequently, the donor vessel is a branch of the external carotid artery and the recipient is the P2 or P3 branch of the posterior cerebral artery. Because of a variety of anatomical considerations, we favor using the superficial temporal artery rather than the occipital artery. Alternatively, we have had success using a radial artery interposition graft in several cases in which a high-flow bypass was required and no suitable venous conduits were readily accessible. All patients in whom revascularization is being considered must undergo formal BTO. At our institution, the test involves neuroclinical monitoring for 30 minutes, EEG, perfusion imaging, and hypotensive challenge. Patients who fail the test neuroclinically receive a high-flow graft. Those who pass neuroclinically but demonstrate inadequate collateral flow by another testing modality receive a low-flow arterial construct in which the donor pedicle is commonly the superficial temporal artery. A number of variables can render the results of BTO equivocal. For example, a poor-grade patient may be unable to interact and be evaluated neuroclinically. Or, the tortuous nature of the posterior circulation can make it difficult to maneuver the catheters intracranially. Furthermore, when a balloon is expanded in the basilar artery, neuroclinical signs of ischemia may not necessarily be the result of inadequate perfusion of the apical circulation. Rather, it may be a result of compressive effects on perforators arising from the basilar trunk at the site of the expanded balloon. Of final importance is the timing of the revascularization procedure with respect to definitive aneurysm treatment. Several cases have been documented in which a bypass was performed before the aneurysm had been excluded and rupture occurred soon thereafter. Another potentially problematic situation in the patient with an acutely ruptured aneurysm is that a superficial temporal artery graft usually requires several days to mature. During that time an antiplatelet agent is administered to prevent graft thrombosis. However, hemorrhagic complications can occur and aneurysm rebleeding may be all the more devastating. Consequently, we are reluctant to stage the bypass and clipping procedure, particularly in a patient with acute subarachnoid hemorrhage. Typically, the bypass procedure and definitive clip-reconstruction are performed during a single operation.
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Figure 5 Axial (a) and sagittal (b) T1-weighted MRIs demonstrate a giant, partially thrombosed aneurysm at the basilar apex that significantly distorts the midbrain. Anteroposterior (c) and lateral (d) views after left vertebral artery injection reveal a giant basilar apex aneurysm involved with the upper basilar trunk branches. This lesion was considered unamenable to primary clip reconstruction. Treatment options considered included two Hunterian strategies that varied based on the site of vessel occlusion. One option was to occlude the dominant vertebral artery after a BTO test. Alternatively, a potentially more efficacious but higher risk Hunterian strategy involves direct surgical exploration with clip application above the superior cerebellar arteries and below the origin of the posterior cerebral arteries through a standard pterional or subtemporal approach.
Endovascular Considerations The use of endovascular techniques to treat basilar trunk and basilar apex aneurysms is appealing because of the significant risks associated with open surgical procedures to treat these aneurysms. This interest, however, must be tempered by a clear understanding of the inherent risks for a recurrence
after endovascular treatment. The risks of the procedure also must be contemplated thoughtfully because although they are lower than for surgery, they are still significant. Significant contraindications to endovascular approaches for treating basilar trunk and basilar apex aneurysms include bleeding coagulopathies that would make anticoagulation infeasible, significant access issues that would make delivery of
Giant basilar aneurysms devices difficult or impossible, and neurologic impairment due to mass effect. Relative contraindications to endovascular approaches include wide-necked aneurysms that cannot be coiled primarily. Stents, however, have made some of these aneurysms amenable to endovascular treatment. Severe tortuosity of the parent vessels also can make stent delivery difficult or impossible. Although reconstructive strategies pose the above challenges and limitations, proximal occlusive strategies are a strong suit of endovascular approaches. If occlusion can be tolerated, it often can be delivered safely and relatively precisely with endovascular techniques.
Conclusion Giant basilar artery aneurysms remain the most challenging condition treated by cerebrovascular surgeons. The importance of the surrounding neurovascular tissue, the complex arrangement of perforating vessels distorted by mass lesions, and the constricted corridors of surgical access all contribute to this complexity. Since the pioneering work of Yasargil and Drake, both surgical technique and instrumentation have improved significantly as has the opportunity for extensive cranial base resections. The ability of neuroanesthesia and neurocritical care has also dramatically improved to sustain patients during complex procedures and difficult perioperative courses. As a result of these improvements, cerebrovascular surgeons can now attack increasingly severe conditions that were not approached in past decades. Nonetheless, the rate of morbidity associated with surgical therapy remains high. It is important to remember, however, that the natural history of these conditions is also poor. Over the past 15 years, endovascular developments have offered a significant opportunity to improve our overall management outcomes. As we read the literature, however, it is critical to ask the question “Is he or she reporting overall management outcome or procedural outcome?” We must always analyze published reports to determine if strategies reported as successful are, in fact, durable. It remains to be seen whether large and giant aneurysms treated with endovascular techniques remain stable at 6 months, 1 year, 5 years, 10 years, and 15 years after treatment. As practitioners, when we are confronted with extremely difficult problems, it is tempting to quickly select a “minimally invasive” technique, which may be associated with the least immediate risk. Just putting a few coils in a giant basilar aneurysm in hopes that it will improve the natural history is ill advised and quite different from the same maneuver for an aneurysm involving the carotid or middle cerebral artery. In the latter vessels, the ability to gain easy and wide surgical exposure facilitates open surgical treatment of endovascular failures if an aneurysm regrows. Such maneuvers are not
113 possible in the proximal, middle, and distal basilar arteries. The platinum mass is not compressible and usually must be removed to achieve successful aneurysm obliteration. The space required and the manipulation of involved perforating vessels is associated with a very high risk. The point is that we must be thoughtful and judicious in determining the initial plan of action as we develop strategies for these complex patients. The idea that “we can coil it now and then come back and clip it if it grows” is not true of giant lesions of the basilar artery. A variety of influences, not the least of which is the risk of liability, has influenced the increasing centralization of care for patients with complex diseases requiring high technology. Facilities and surgeons that treat high volumes of certain diseases improve patient outcomes. In our opinion, the primary driver of these improvements in outcome is the extraordinary infrastructure required to support these patients. Teams of cerebrovascular specialists, including neuroanesthesia, neurocritical care, neuroradiology, endovascular neurosurgery, microvascular neurosurgery, and internal medicine and its sections, are required to make effective therapeutic decisions and to support the patient through the perioperative period. In these multidisciplinary environments, patients will continue to receive cutting edge care and the substrate will be present to continue to advance the field. Consequently, in future decades, patients with giant basilar aneurysms should achieve better outcomes and increasingly complex lesions will be treated. Management of these conditions falls outside the scope of the “core” of neurosurgical training. Physicians endeavoring to manage these problems should have made a lifelong commitment to developing the requisite skills and experience and to establishing the necessary institutional relationships. Because the incidence of these conditions is so low, interinstitutional collaboration is critical for performing the necessary clinical research to refine techniques.
References 1. Michael WF: Posterior fossa aneurysms simulating tumours. J Neurol Neurosurg Psychiatry 37:218-223, 1974 2. Drake CG: Giant intracranial aneurysms: Experience with surgical treatment in 174 patients. Clin Neurosurg 26:12-95, 1979 3. Bull J: Massive aneurysms at the base of the brain. Brain 92:535-570, 1969 4. O’Shaughnessy BA, Getch CC, Bendok BR, et al: Progressive growth of a giant dolichoectatic vertebrobasilar artery aneurysm after complete Hunterian occlusion of the posterior circulation: Case report. Neurosurgery 55:1223, 2004 5. Steinberg GK, Drake CG, Peerless SJ: Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms. Immediate results and long-term outcome in 201 patients. J Neurosurg 79:161-173, 1993 6. Parkinson RJ, Bendok BR, O’Shaughnessy BA, et al: Temporary and permanent occlusion of cervical and cerebral arteries. Neurosurg Clin N Am 16:249-256, viii, 2005
G
iant aneurysms (greater than 2.5 cm) of the basilar apex, trunk, or confluence represent some of the most formidable therapeutic challenges confronting vascular neurosurgeons. The poor natural history of these lesions, especially when symptomatic, is well documented.1-3 Drake’s report of 31 patients with untreated giant intracranial aneurysms illustrates the dismal prognosis of these lesions with a 68% mortality rate at 2 years and about an 80% mortality rate at 5 years.2 Advances in surgical technique, anesthesia, imaging, and more recently endovascular technique have helped increase the success of treating these lesions. Each patient harboring a giant basilar aneurysm brings a unique set of problems. We have found that there is no single right answer to treating these aneurysms. More often a customized strategy must be derived from the results of diagnostic tests and from the menu of available treatment options. Diagnostic studies such as magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), computed tomography angiography (CTA), digital subtraction angiography (DSA), MR and CT perfusion, and the results of trial parent artery occlusion allow the selection of treatment options including direct surgical reconstruction with or without a skull base approach,
*Department of Neurological Surgery, Northwestern University Feinberg School of Medicine, Chicago, IL. †Department of Neurological Surgery and Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL. Address reprint requests to Christopher C. Getch, MD, Associate Professor, Department of Neurological Surgery, Northwestern University Feinberg School of Medicine, 676 N. St. Clair Street, Suite 2210, Chicago, IL 60611; [email protected]
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use of circulatory arrest, revascularization, or permanent parent artery occlusion (Hunterian strategies). This article discusses the treatment of giant basilar artery aneurysms from a surgical perspective including adjunct endovascular strategies when appropriate.
Patient Selection One of the most important factors in achieving a successful surgical outcome is careful patient selection. Information vital for determining whether a patient is a candidate for direct surgical reconstruction or is better managed by a Hunterian strategy is derived primarily from the results of preoperative imaging interpreted in the context of a patient’s clinical status. Routinely, the evaluation of a patient harboring a giant basilar aneurysm includes MRI, CTA, and DSA with a temporary parent artery occlusion test when appropriate. Each modality provides information valuable to the decision-making process. MRI and MRA provide information on the degree of aneurysmal sac thrombosis, quality of the neck tissue, and the precise relationship of the pathology to critical neurologic structures, particularly the cranial nerves and brainstem. CTA with 3-D reconstructions defines branch anatomy and provides information on the presence of calcification within both the sac and neck. Combining CTA and axial MRI is essential in planning the corridor for surgical access and in determining whether a standard or skull base approach would be more beneficial. Wide surgical exposure is fundamental to successful management. Conventional angiography provides essential anatomic and hemodynamic information and the potential for collateral supply. A tempo-
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Figure 1 Anteroposterior (a) and lateral (b) vertebral angiograms show a complex confluence giant aneurysm. Careful analysis of the angiograms reveals a complex aneurysm with a large saccular component and a lower basilar ectatic component. Adequate exposure of an aneurysm in this location includes a suboccipital craniectomy that extends down through the foramen magnum and a limited petrosectomy for additional exposure. The aneurysm was treated with direct clip reconstruction of the saccular component. The ectatic portion did not require treatment.
rary parent artery occlusion test establishes whether a patient is likely to tolerate a Hunterian strategy or whether revascularization is needed before vessel occlusion. Many variables must be considered to determine the appropriateness of direct surgical clip reconstruction for a patient with a giant basilar aneurysm. Several general questions must first be answered. Is the pathology amenable to direct reconstruction? Is the critical anatomy favorable and accessible? Can the reconstruction be accomplished in an acceptable period of temporary arterial occlusion? In our experience, pathologies that are unamenable to direct reconstruction providing a long-term durable solution are dolichoectatic and dissecting aneurysms.4 Both pathologies typically involve a circumferentially diseased vessel that is more successfully managed with Hunterian strategies or with trapping combined with revascularization. Alternatively, in some patients with complex and unreconstructable dolichoectatic lesions, the saccular component alone can be clipped (Fig. 1). In the setting of a dolichoectatic aneurysm, exploration with partial gathering of the sac to relieve mass effect may be beneficial in rare circumstances.4 It is possible that future endovascular technologies may provide a benefit. Favorable anatomy for clip reconstruction depends on configuration and height of the branches and neck (relative to the posterior clinoid), presence of calcification in the neck and sac, the presence and degree of thrombus, collateral supply, and in certain cases, an eccentric displacement of the anatomy that improves access. In general, the presence of extensive calcification is an impediment to direct clipping. It primarily affects clip-closure, necessitating multiple clips in the setting of limited space. Calcification combined with extensive atherosclerosis in
the sac can make clipping more difficult by stenting the neck open and driving the clip onto the parent vessel. The presence of calcification and atherosclerotic changes in the sac and neck are often present simultaneously in the parent vessels and increase the risk of temporary clipping during reconstruction. Massive thrombosis with a small patent aneurysm lumen also increases the risk of unsuccessful clip reconstruction. A significant degree of thrombosis mandates trapping and opening of the aneurysm, increasing the length of ischemia. Aneurysms with a significant degree of thrombosis in elderly patients who are less likely to tolerate temporary occlusion are perhaps better candidates for Hunterian strategies (Fig. 2). Furthermore, a small residual patent lumen within a large thrombotic sac likely necessitates dissection of the thrombus from the proximal neck tissue, potentially leading to intimal injury in the neck and thrombosis of the reconstructed lumen. A broad neck is uniformly encountered in giant aneurysms and is not a contraindication to direct surgical reconstruction. In the setting of a giant aneurysm with a particularly broad neck, the distance from the parent vessel inflow to the outflow branches must be assessed critically. In this setting, it is of primary importance to determine that the outflow branches can be visualized from the operative approach. Exploration of an aneurysm whose outflow is significantly displaced from the parent vessel often reveals poor quality tissue unfavorable for durable reconstruction. Occasionally, eccentric displacement of the vascular anatomy offers an advantage, shortening the working distance to the critical anatomy. Each of these complicating morphological challenges are as-
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duncular cistern, these same maneuvers carry a high risk of neurological injury. When considering direct reconstruction of a giant basilar aneurysm, the surgeon should always have a backup strategy. The presence of a robust collateral supply can provide an exit strategy, increasing the safety of an attempt at direct surgical clipping. In the setting of a giant basilar apex aneurysm, a particularly useful collateral configuration that provides an exit strategy is the presence of a unilateral or bilateral posterior communicating artery. A robust posterior communicating artery offers the option of placing a clip above one posterior cerebral artery and below the other. With its antegrade flow eliminated, the posterior cerebral artery is subsequently irrigated through the patent communicator with a high likelihood that the aneurysm will thrombose even if the proximal P1 is not clipped. This strategy can significantly shorten the distance needed for clip placement, potentially avoid unfavorable neck calcification, and facilitate safe spacing of perforators. Once a giant basilar aneurysm has been deemed surgically reconstructable, access becomes the primary concern. Numerous options are available for gaining access to the upper, mid- and lower basilar trunk: standard approaches, modified skull base approaches, or traditional skull base approaches. Careful consideration must be given to exactly what components of the vascular anatomy must be visualized and how much of the sac and neck must be available for reconstruction.
Surgical Access Pterional (Transsylvian) Approach
Figure 2 Axial CT (a) and lateral vertebral angiogram (b) demonstrate a giant calcified thrombosed basilar apex aneurysm unamenable to direct conventional clip reconstruction. Treatment options considered included reconstruction under circulatory arrest through an extended lateral transsylvian approach with or without orbitozygomatic extension, proximal parent artery occlusion with or without revascularization, and stent reconstruction without coils to redirect flow. Ultimately, a Hunterian strategy was selected.
sociated with large and giant aneurysms throughout the cerebrovascular tree. It is critical to recognize that aneurysms of the upper basilar artery are different than their cohorts in the anterior circulation or proximal vertebral artery. For such a lesion at the bifurcation of the middle cerebral artery (MCA), for example, an abundance of easily acquired exposure facilitates the surgical creativity required to evacuate thrombus, to crush a calcified neck, and to deal with differential wall thickness. The paucity of critical perforating arteries at this location increases the safety margin. When performed in the interpe-
The pterional approach, particularly with wide sylvian fissure dissection, is extremely versatile and used for many aneurysms of the distal basilar complex. Wide dissection of the parasellar cisterns enables access to the interpeduncular cistern by one or more routes. The dissection plane and the approach can be developed lateral to the internal carotid artery wherein the posterior communicating artery is followed to the junction of the P1 and P2 segments of the posterior cerebral artery. P1 is then followed along its inferior surface proximally to isolate proximal control on the distal basilar artery safely away from aneurysmal tissue. Similarly, a dissection plane can be developed medial to the carotid artery that separates the small perforating arteries to the hypothalamic region and optic tract, opening the membrane of Liliequist. Therefore, the basilar trunk is directly exposed in the interpeduncular cistern. In particularly high basilar bifurcation aneurysms, it may be necessary to gain additional superior exposure by developing the plane immediately above the carotid bifurcation. This maneuver can be performed by carefully dividing the arachnoidal fibers that bind the small lenticulostriate vessels. With patience, this tissue can be separated adequately to allow elevation of the optic tract with workable space within the interpeduncular cistern. In fact, regardless of the procedure, defining each of these planes minimizes obscuration of vital anatomy by instruments placed in the exposure. This transsylvian exposure can be used to treat a wide variety of aneurysms in this location because it allows the
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surgeon a good view of the anatomy. It also enables exquisite access to the proximal basilar trunk and both P1 segments for definitive temporary occlusion with aneurysmal decompression, if necessary, to control intraoperative bleeding or to facilitate the dissection of difficult large and giant lesions.
Half-and-Half Approach Drake has described this modification of the pterional exposure to improve access to the posterior reaches of the interpeduncular cistern through a slightly more lateral viewpoint.2 This idea was generated to facilitate exposure to carotid aneurysms after a basilar aneurysm was exposed subtemporally. This approach involves rotating the head a bit more than in a direct transsylvian exposure and mobilizing the temporal lobe with superior and slightly lateral displacement of the uncus. In addition to the improved posterior exposure, this approach offers an improved view of the entire interpeduncular fossa and carotid cistern. In many circumstances, it is a very desirable approach to plan from the outset of the procedure.
Subtemporal Approach The lateral view of the interpeduncular cistern, which was highly developed by Drake,2 perhaps offers the ideal view of the vital perforators posterior to the aneurysmal fundus. For the typical superior-projecting aneurysm, this viewpoint maximizes the surgeon’s ability to salvage the perforating arteries. The contralateral posterior cerebral artery, however, is more difficult to see and quite difficult, if not impossible, to occlude temporarily. For a standard subtemporal clipping, however, the space anterior to the aneurysmal neck can usually be retracted gently so that the contralateral P1 segment with its initial anterior course can be definitively seen. Drake’s innovation of the aperture or fenestrated clip greatly simplified subtemporal clipping of basilar bifurcation aneurysms so that the P1 segment and any associated perforating arteries can be included in the fenestration. The limited exposure afforded by the isolated subtemporal procedure severely limits its application to giant aneurysms in this area, except in the realm of Hunterian strategies with or without revascularization.
Extended Lateral Approach Over the past several years at our institution, a continued struggle with basilar apex aneurysms has resulted in the evolution of a hybrid operative approach. Conceptually, both the transsylvian and subtemporal approaches have certain advantages and disadvantages. The transsylvian view has the advantage that all five involved vessels can be seen en face. The surgeon has immediate access to full trapping of the circulation at that site. The primary disadvantage of the transsylvian view is the relatively poor access to the posterior reaches of the interpeduncular cistern where the perforating vessels lie. The great advantage of the subtemporal view is that the lateral view facilitates exposure and dissection of the posteriorly located perforators as well as ease of proximal control. The primary disadvantage of this approach is that the exposure is narrow. It is rare to have access to all appropriate vessels for a full trapping, should that be required. The extended lateral exposure is performed from the sur-
Figure 3 An intraoperative image after a left-sided extended lateral transsylvian approach to a giant basilar apex aneurysm shows the extensive exposure gained from this approach. The neck of the aneurysm was accessed and clipped through a corridor above the basilar bifurcation. (Color version of figure is available online.)
geon’s dominant side. A traditional pterional craniotomy is performed, followed by wide resection of the temporal squama and sphenoid ridge. An orbitozygomatic osteotomy can be added if the target lesion is very high. The sylvian fissure is dissected completely, and the sphenoparietal venous drainage is detached from the floor of the middle cranial fossa. With complete sylvian dissection and gravitational assistance, the temporal lobe migrates posteriorly. The surgical dissection does not focus on the opticocarotid triangle or the posterior communicating artery corridor. Rather, this approach focuses on the third cranial nerve. All attachments between the third cranial nerve and the uncus are removed. As the exposure deepens, the uncus and all temporal lobe structures that have migrated into the incisura are elevated by a temporal lobe retractor. This maneuver gives the surgeon access to the tentorial incisura as far back as the cerebral peduncle. At that point, when performed from the surgeon’s dominant side, access to the direct lateral view (just as in a subtemporal approach) is impressive (Fig. 3). Therefore, the assets of each primary approach are capitalized on (perforator exposure and access to the contralateral P1 and superior cerebral arteries) and the liabilities of both approaches are eliminated. The surgeon can dissect perforators from a lateral view, and during clip application, with simple adjustments of the microscope, have access to the full benefits of the wide transsylvian view for precise viewing of the contralateral neck. A final point has greatly simplified clipping of these treacherous lesions. The true surgical neck is avoided on the operated side, and the dissection begins inferior to the P1 origin. The difficulty posed by the broad neck of these aneurysms and the constant finding that the aneurysm sac itself begins to develop well below the superior aspect of the P1 origin are thereby eliminated. When performed below the P1 origin, the dissection allows the surgeon to work across the basilar trunk at a site where the distance to be traveled is considerably foreshortened. This key maneuver facilitates a primary clip application using a strong and short fenestrated clip below the proximal P1.
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Cranial Base Exposures for Intracranial Aneurysms In recent years, modifications to some of the previously described operative exposures have enabled neurosurgeons to treat complex aneurysms arising within the constraints of the cranial base more effectively. The broader exposure yielded by these procedures provides the surgeon with an enhanced view of the vascular anatomy with little or no need for brain retraction, and perhaps most importantly, additional working room. The exposures most beneficial to neurovascular surgeons are detailed below.
Orbitozygomatic Approach The addition of an orbital or orbitozygomatic osteotomy to a standard pterional craniotomy should be considered with giant basilar apex aneurysms. The additional 10 to 15 degrees of exposure this maneuver provides is invaluable when a large thrombotic sac is encountered or when high exposure is needed up into the diencephalon. After a standard pterional craniotomy is performed as described previously, dura overlying the orbital roof is stripped posteriorly toward the orbital apex, medial to the cribriform, and lateral to the dura of the superior orbital fissure. Periorbita is stripped from the superior and lateral walls of the orbit to a depth of approximately 3 cm. If the zygomatic process is to be included into the osteotomy, the full extent of the zygomatic arch is exposed before the temporalis muscle is reflected. The orbitzygomatic segment is best resected with a combination of reciprocating saw and osteotomes. The initial bone cuts are made with a reciprocating saw through the supraorbital ridge and frontal zygomatic process. The former is just lateral to the supraorbital foramen. Narrow osteotomes complete the resection across the orbital roof and greater and lesser wings of the sphenoid bone. Once the masseter has been released from the inferior surface of the zygomatic arch, the piece can be removed en bloc. At least 3 cm of the orbital roof and lateral wall must be preserved to minimize the possibility of postoperative pulsatile enophthalmos. Perhaps the most important element of this exposure is the resection of the proximal lesser and greater wings of the sphenoid bone, inclusive of the anterior clinoid process. The postclipping reconstruction is performed in a standard fashion with a microplating system and hydroxyapatite compound or methylmethacrylate to fill in any bony defects.
Petrosal Approach The combined subtemporal, suboccipital, or petrosal approach provides the most direct access to aneurysms from the basilar apex to the vertebrobasilar junction. Variations of this approach include a retrolabyrinthine exposure, a partial labyrinthectomy, a total labyrinthectomy, and a transcochlear resection with facial nerve mobilization. At our institution, the retrolabyrinthine or partial labyrinthine exposure is most favored because they are the only petrosal approaches that preserve hearing. The patient is positioned supine with a shoulder roll ipsilateral to the side of the approach. The head is turned 90 degrees and gently extended toward the floor. If necessary, the shoulder is taped caudally. A curvilinear incision begins 2 cm superior and anterior to the ear. It curves along a 2-cm
C.C. Getch et al. posterior margin from the ear to a point 2-cm inferior to the mastoid tip. The temporalis and occipital frontalis muscles are divided and reflected laterally with the scalp to expose the external auditory meatus centrally, the temporal zygomatic root rostrally, and the entire mastoid process posteroinferiorly. A mastoidectomy is performed with early identification and skeletonization of the transverse and sigmoid sinuses as far laterally as the jugular bulb. When only a retrolabyrinthine, presigmoid exposure is necessary, care is taken to preserve the bony labyrinth. With a partial labyrinthectomy, as many as five additional millimeters of room can be obtained to provide several degrees of added maneuverability at the level of the petrous apex. Doing so requires cautious drilling of the posterior and superior semicircular canals to expose the underlying membranous labyrinth. Once identified, the exposed orifices are immediately waxed. The horizontal semicircular canal is preserved. A completed mastoidectomy should expose the temporal and posterior fossa dura. This dural exposure facilitates the addition of a subtemporal and suboccipital craniotomy. Typically, the dural opening is presigmoid, originating just superior and anterior to the jugular bulb and directed toward the superior petrosal sinus. The sinus is ligated, and the dural cut proceeds rostrally to the dura of the middle fossa. Then the dura is tented laterally. The tentorium is coagulated with the bipolar cautery and cut toward the incisura. Care is exercised to avoid injury to the fourth cranial nerve as it courses adjacent to the midbrain en route to the tentorial edge. The tentorium can be partially excised or coagulated to enhance visualization. The midbrain, clivus, basilar artery, and cranial nerves III to XII are clearly visible with this exposure. A modification of this approach that includes a retrosigmoid dural exposure with ligation of the nondominant transverse sinus has been described. In our experience, however, this maneuver creates an unacceptable risk of venous infarction. After the aneurysm has been secured appropriately, a watertight dural closure should be attempted. A dural graft is necessary. Mastoid air cells should be waxed thoroughly, and fat should be placed in the mastoid defect. Lumbar spinal fluid drainage should be considered when a watertight dural closure cannot be achieved.
Modified Far-Lateral Transcondylar Approach for Lower Basilar Trunk Aneurysms Aneurysms of the confluence and lower basilar trunk up to the origin of the anterior inferior cerebral arteries are comfortably accessible through a far-lateral exposure. The addition of a partial condylectomy gains access to the ventral brainstem. This approach requires that the patient be positioned in a park bench or three-quarter prone position as previously described. We favor a curvilinear incision that typically projects from the midline at C1 to C2 superiorly to 1-cm superior to the inion. It then curves laterally to 2 cm posterior to the ipsilateral ear and continues caudally. It ends 3-cm posteroinferiorly to the mastoid tip, just over top the midportion of the sternocleidomastoid muscle.
Giant basilar aneurysms The scalp and fascia are reflected medially to expose the underlying intermixed fascia of the first layer of muscles, which includes the occipital frontalis, trapezius, and sternocleidomastoid muscles. These muscle layers are divided at their attachment to the superior nuchal line. Trapezius is reflected inferomedially, and the sternocleidomastoid is detached from the mastoid process and reflected inferolaterally. The spinalis capitis and semispinalis capitis are sequentially detached from the occiput. The occipital artery can be dissected free of the longissimus capitis, and this muscle is caudally reflected from its attachment to the undersurface of the mastoid process. With these muscles reflected, the suboccipital triangle is brought into view. The triangle is composed of the recti and obliquus muscles. The superior oblique and inferior oblique muscles can be followed laterally to their attachment to the C1 lateral mass and then should be detached. At this point, a bur hole is placed just caudal to the mastoid. A suboccipital craniotomy is performed inclusive of the foramen magnum. With the vertebral artery isolated in a vessel loop, the atlo-occipital joint is drilled medially to laterally. At least 50% of the joint must be preserved to avoid creating instability and to obviate a subsequent fusion procedure. The condylar vein are encountered with drilling and can typically be controlled with bipolar cautery and bone wax. The dura can be opened in a series of small triangles based on the transverse and sigmoid sinuses and condyle.
Clip Reconstruction Direct clip reconstruction strategies are the most desirable, but successful clip reconstruction is influenced by many variables. These variables include the quality of the tissue in the neck, the presence of calcified athermatous plaque, intraluminal thrombus, favorable primary and vital perforator artery anatomy in relation to the surgical neck, and a wellplanned and executed surgical strategy with adequate exposure. An essential part of direct clip reconstruction is obtaining adequate exposure. Exposure is not limited just to the neck of the aneurysm. Direct visualization of the primary inflow and outflow from the aneurysm is needed because temporary proximal occlusion or trapping is often part of the reconstruction strategy. There must be adequate room for multiple temporary clips to be positioned so that they do not interfere with the definitive clipping. A thorough exploration through an adequate surgical window is essential to eliminate the presence of a small perforator, which commonly emanates from the sac and precludes its inclusion in the clip construct. The final stages of this exploration can be facilitated by placing a temporary proximal clip to reduce the turgor within the aneurysm sac itself. Unfavorable perforator anatomy is an excellent reason to abandon direct surgical reconstruction and to seek an alternative strategy. Based on his clinical experience, Drake believed that less than half of giant basilar aneurysms could be clip-reconstructed directly.2 Once the vessel anatomy has been explored thoroughly and deemed favorable for clipping, the neck tissue must be examined closely to determine whether calcification is present and how it will likely respond to clip compression. An irregular pattern of wall thickness and calcification often
109 results in persistent aneurysmal filling despite the surgeon believing that clipping has been definitive. In our institutional experience, clip reconstruction of a giant aneurysm is almost never encountered. Strategies using multiple short, fenestrated, or angle clips are almost uniformly necessary to reconstruct the broad, thick aneurysm neck. When wall thickness is variable, a combination of straight and fenestrated clips can be used to solve this problem. The fenestrated clip can be placed around the thickened or calcified portion of the neck. Subsequently, a short, powerful straight clip is placed to close the fenestration. The presence of calcified plaque within the neck also can be dealt with using a fenestrated clip. In necks that appear to harbor only thickened tissue, a series of parallel clips can be used. Typically, the first clip is often driven by the thickened neck down onto the parent vessels. This clip, when left in place temporarily, can serve as a support for additional clips as they are stacked on the neck. The first clip is removed as the other clips gain purchase. In the setting of a thrombosed aneurysm, the amount of patent sac lumen must be determined. It is easy to underestimate the amount of patent sac needed for clip reconstruction. Additional tissue that can be used to facilitate reconstruction can be gained by trapping the aneurysm, opening it, and resecting thrombus. A microtipped ultrasonic aspirator and pancake curettes are particularly useful for removing thrombus from the aneurysm sac. At this point, care must be taken not to damage the intimal layers in the neck and parent vessel. Doing so leads to premature thrombosis of the reconstructed vessel. When reconstruction is planned in the setting of a thrombosed giant sac, the time required to clear the thrombus must be carefully calculated into the total time required for reconstruction. When a particularly broad neck is encountered or created by having to leave a large cuff of tissue in the setting of a thrombosed aneurysm, a clip-cut-clip technique can be used. With the aneurysm trapped and evacuated, the clip reconstruction begins ipsilaterally with placement of a short, straight clip. Short clips provide the necessary closing force on the thickened neck. Furthermore, short clips placed in series can compensate for the variable thickness in the aneurysm wall. The placement of a second short, straight clip in series with the first is facilitated by cutting the aneurysmal tissue just distal and parallel to the first clip to within 1 to 2 mm of the tip of the first clip. Several short clips can be deployed in this fashion. When completed, the appearance of the reconstructed neck is slightly saw-toothed.
Hunterian Strategies When direct surgical reconstruction of a giant basilar aneurysm cannot be accomplished, alternative strategies such as endovascular stent-assisted coiling or Hunterian strategies must be considered (Fig. 4). The long-term efficacy of stentbased treatment is still unknown. However, a significant body of literature supports the successful treatment of giant basilar aneurysms with Hunterian strategies.5 Steinberg et al5 reported the extensive London, Ontario experience with Hunterian strategies for the treatment of giant basilar aneurysms. They described the long-term results of 201 patients who underwent deliberate basilar or vertebral
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Figure 4 T1-weighted sagittal MRI (a) demonstrates a giant vertebral artery aneurysm exerting significant mass effect. Right vertebral artery injection (b) reveals a giant right vertebral artery aneurysm. Because the vertebral artery contralateral to the aneurysm provides adequate filling of the basilar artery (c), the optimal strategy includes trapping of the aneurysm segment coupled with revascularization of PICA. The aneurysm can be approached through a suboccipital craniectomy with a modified far-lateral approach.
artery occlusion to giant basilar aneurysms. The mean follow-up was 9.5 years. Several different Hunterian strategies were used to treat giant aneurysms of the posterior circulation. Overall, long-term results were excellent in 68%, good in 5%, and poor in 3%. Twenty-four percent died. Clinical outcomes varied by location. Good to excellent results were achieved in 64% of basilar apex aneurysms, in 76% of basilar
trunk aneurysms, in 74% of vertebrobasilar junction aneurysms, and in 87% of vertebral aneurysms. Various Hunterian strategies resulted in successful aneurysm thrombosis in 78% of patients, and few of these patients developed late neurological complications (4%). Conversely, in patients who had incompletely thrombosed aneurysms, a significantly higher rate of late neurologic deterioration oc-
Giant basilar aneurysms curred (67%), 86% of which proved fatal. Tolerating basilar or vertebral artery occlusion correlated well with the presence of a large (greater than 1 mm) posterior communicating artery. Within the first week of Hunterian treatment, 26 patients (13%) deteriorated from vertebrobasilar ischemia with thrombosis or embolism, which was more common than hemodynamic insufficiency. In addition to a smaller series, these results serve as the foundation for designing a successful Hunterian strategy. The most essential component in the evaluation of a patient being considered for a Hunterian strategy is their response to a balloon trial occlusion (BTO) of either the basilar or vertebral artery. The technique of parent vessel test occlusion has been refined. Now, a highly selective occlusion can be performed at or just proximal or distal to the pathology. Doing so minimizes the risk of complications during the test. Equally importantly, it accurately recreates the hemodynamic environment likely to be encountered during permanent occlusion. Simultaneous angiography offers an even more precise picture of the altered hemodynamic flow by demonstrating the collateral channels. Our protocol for temporary and permanent occlusion of cerebral arteries has been reported.6 It includes simultaneous clinical, angiographic, and neurophysiological assessment in both normotensive and mildly hypotensive (20-30% reduction in the mean arterial pressure) conditions. The single most important factor to be considered when performing a BTO is where the temporary occlusion should be performed. This locale should be determined before access is obtained and should accurately reflect where the parent artery is likely to be sacrificed. The site of temporary arterial occlusion is influenced by a number of factors, including the location of the aneurysm, the presence and size of the vertebral, posterior inferior cerebellar, internal carotid arteries, and finally the presence and size of the posterior communicating arteries. A stable thrombosed aneurysm is the goal, and careful consideration must be given to altered hemodynamics, whether preservation of antegrade flow or reversal of flow gives the most desirable effect. After a patient successfully passes BTO at the appropriate location, permanent occlusion is usually performed in a separate procedure, either surgical or endovascular. In our experience, surgical exploration with clip placement for either proximal occlusion or trapping offers a more precise point of occlusion and may avoid inadvertent perforator occlusion during an endovascular procedure (Fig. 5). In patients who fail BTO, revascularization options must be considered. The location and type of revascularization depend on whether the patient has failed by both clinical and neurophysiological assessments or by EEG or single photon emission computed tomography, or by hypotensive challenge only.
Revascularization Strategies The adjunctive use of cerebral revascularization plays an important role in the surgical treatment of many giant aneurysms of the basilar artery. Two situations in which revascularization is used in the treatment of giant basilar artery
111 aneurysms are the most common: (1) when a Hunterian approach is implemented and the native collateral flow is insufficient to sustain the basilar artery circulation; and (2) as a prophylactic measure when prolonged periods of temporary arterial occlusion are anticipated for aneurysm exclusion and parent artery reconstruction. Although the technical skills required for the anastomosis are almost the same as those applied in anterior circulation, the deep and restricted confines in which the surgeon must work to perform a posterior circulation bypass leads to a considerably more challenging procedure. Initially, the need for revascularization is determined by critical evaluation of the cerebral angiogram, including the caliber of the posterior communicating arteries, the extent of antegrade flow up the basilar trunk, and the symmetry and timing of venous outflow. Angiographic examination of the external carotid artery circulation is advocated at the time of the initial angiogram because it is necessary for planning the specific revascularization procedure. Most frequently, the donor vessel is a branch of the external carotid artery and the recipient is the P2 or P3 branch of the posterior cerebral artery. Because of a variety of anatomical considerations, we favor using the superficial temporal artery rather than the occipital artery. Alternatively, we have had success using a radial artery interposition graft in several cases in which a high-flow bypass was required and no suitable venous conduits were readily accessible. All patients in whom revascularization is being considered must undergo formal BTO. At our institution, the test involves neuroclinical monitoring for 30 minutes, EEG, perfusion imaging, and hypotensive challenge. Patients who fail the test neuroclinically receive a high-flow graft. Those who pass neuroclinically but demonstrate inadequate collateral flow by another testing modality receive a low-flow arterial construct in which the donor pedicle is commonly the superficial temporal artery. A number of variables can render the results of BTO equivocal. For example, a poor-grade patient may be unable to interact and be evaluated neuroclinically. Or, the tortuous nature of the posterior circulation can make it difficult to maneuver the catheters intracranially. Furthermore, when a balloon is expanded in the basilar artery, neuroclinical signs of ischemia may not necessarily be the result of inadequate perfusion of the apical circulation. Rather, it may be a result of compressive effects on perforators arising from the basilar trunk at the site of the expanded balloon. Of final importance is the timing of the revascularization procedure with respect to definitive aneurysm treatment. Several cases have been documented in which a bypass was performed before the aneurysm had been excluded and rupture occurred soon thereafter. Another potentially problematic situation in the patient with an acutely ruptured aneurysm is that a superficial temporal artery graft usually requires several days to mature. During that time an antiplatelet agent is administered to prevent graft thrombosis. However, hemorrhagic complications can occur and aneurysm rebleeding may be all the more devastating. Consequently, we are reluctant to stage the bypass and clipping procedure, particularly in a patient with acute subarachnoid hemorrhage. Typically, the bypass procedure and definitive clip-reconstruction are performed during a single operation.
C.C. Getch et al.
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Figure 5 Axial (a) and sagittal (b) T1-weighted MRIs demonstrate a giant, partially thrombosed aneurysm at the basilar apex that significantly distorts the midbrain. Anteroposterior (c) and lateral (d) views after left vertebral artery injection reveal a giant basilar apex aneurysm involved with the upper basilar trunk branches. This lesion was considered unamenable to primary clip reconstruction. Treatment options considered included two Hunterian strategies that varied based on the site of vessel occlusion. One option was to occlude the dominant vertebral artery after a BTO test. Alternatively, a potentially more efficacious but higher risk Hunterian strategy involves direct surgical exploration with clip application above the superior cerebellar arteries and below the origin of the posterior cerebral arteries through a standard pterional or subtemporal approach.
Endovascular Considerations The use of endovascular techniques to treat basilar trunk and basilar apex aneurysms is appealing because of the significant risks associated with open surgical procedures to treat these aneurysms. This interest, however, must be tempered by a clear understanding of the inherent risks for a recurrence
after endovascular treatment. The risks of the procedure also must be contemplated thoughtfully because although they are lower than for surgery, they are still significant. Significant contraindications to endovascular approaches for treating basilar trunk and basilar apex aneurysms include bleeding coagulopathies that would make anticoagulation infeasible, significant access issues that would make delivery of
Giant basilar aneurysms devices difficult or impossible, and neurologic impairment due to mass effect. Relative contraindications to endovascular approaches include wide-necked aneurysms that cannot be coiled primarily. Stents, however, have made some of these aneurysms amenable to endovascular treatment. Severe tortuosity of the parent vessels also can make stent delivery difficult or impossible. Although reconstructive strategies pose the above challenges and limitations, proximal occlusive strategies are a strong suit of endovascular approaches. If occlusion can be tolerated, it often can be delivered safely and relatively precisely with endovascular techniques.
Conclusion Giant basilar artery aneurysms remain the most challenging condition treated by cerebrovascular surgeons. The importance of the surrounding neurovascular tissue, the complex arrangement of perforating vessels distorted by mass lesions, and the constricted corridors of surgical access all contribute to this complexity. Since the pioneering work of Yasargil and Drake, both surgical technique and instrumentation have improved significantly as has the opportunity for extensive cranial base resections. The ability of neuroanesthesia and neurocritical care has also dramatically improved to sustain patients during complex procedures and difficult perioperative courses. As a result of these improvements, cerebrovascular surgeons can now attack increasingly severe conditions that were not approached in past decades. Nonetheless, the rate of morbidity associated with surgical therapy remains high. It is important to remember, however, that the natural history of these conditions is also poor. Over the past 15 years, endovascular developments have offered a significant opportunity to improve our overall management outcomes. As we read the literature, however, it is critical to ask the question “Is he or she reporting overall management outcome or procedural outcome?” We must always analyze published reports to determine if strategies reported as successful are, in fact, durable. It remains to be seen whether large and giant aneurysms treated with endovascular techniques remain stable at 6 months, 1 year, 5 years, 10 years, and 15 years after treatment. As practitioners, when we are confronted with extremely difficult problems, it is tempting to quickly select a “minimally invasive” technique, which may be associated with the least immediate risk. Just putting a few coils in a giant basilar aneurysm in hopes that it will improve the natural history is ill advised and quite different from the same maneuver for an aneurysm involving the carotid or middle cerebral artery. In the latter vessels, the ability to gain easy and wide surgical exposure facilitates open surgical treatment of endovascular failures if an aneurysm regrows. Such maneuvers are not
113 possible in the proximal, middle, and distal basilar arteries. The platinum mass is not compressible and usually must be removed to achieve successful aneurysm obliteration. The space required and the manipulation of involved perforating vessels is associated with a very high risk. The point is that we must be thoughtful and judicious in determining the initial plan of action as we develop strategies for these complex patients. The idea that “we can coil it now and then come back and clip it if it grows” is not true of giant lesions of the basilar artery. A variety of influences, not the least of which is the risk of liability, has influenced the increasing centralization of care for patients with complex diseases requiring high technology. Facilities and surgeons that treat high volumes of certain diseases improve patient outcomes. In our opinion, the primary driver of these improvements in outcome is the extraordinary infrastructure required to support these patients. Teams of cerebrovascular specialists, including neuroanesthesia, neurocritical care, neuroradiology, endovascular neurosurgery, microvascular neurosurgery, and internal medicine and its sections, are required to make effective therapeutic decisions and to support the patient through the perioperative period. In these multidisciplinary environments, patients will continue to receive cutting edge care and the substrate will be present to continue to advance the field. Consequently, in future decades, patients with giant basilar aneurysms should achieve better outcomes and increasingly complex lesions will be treated. Management of these conditions falls outside the scope of the “core” of neurosurgical training. Physicians endeavoring to manage these problems should have made a lifelong commitment to developing the requisite skills and experience and to establishing the necessary institutional relationships. Because the incidence of these conditions is so low, interinstitutional collaboration is critical for performing the necessary clinical research to refine techniques.
References 1. Michael WF: Posterior fossa aneurysms simulating tumours. J Neurol Neurosurg Psychiatry 37:218-223, 1974 2. Drake CG: Giant intracranial aneurysms: Experience with surgical treatment in 174 patients. Clin Neurosurg 26:12-95, 1979 3. Bull J: Massive aneurysms at the base of the brain. Brain 92:535-570, 1969 4. O’Shaughnessy BA, Getch CC, Bendok BR, et al: Progressive growth of a giant dolichoectatic vertebrobasilar artery aneurysm after complete Hunterian occlusion of the posterior circulation: Case report. Neurosurgery 55:1223, 2004 5. Steinberg GK, Drake CG, Peerless SJ: Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms. Immediate results and long-term outcome in 201 patients. J Neurosurg 79:161-173, 1993 6. Parkinson RJ, Bendok BR, O’Shaughnessy BA, et al: Temporary and permanent occlusion of cervical and cerebral arteries. Neurosurg Clin N Am 16:249-256, viii, 2005