16 Perforator Injury During Open Skull Base Surgery

The basal perforating vessels (perforators) of the brain represent small direct arterial branches of the vertebrobasilar, internal carotid, and main cerebral arteries that supply the paramedian regions of the brainstem, diencephalon, and deep regions of the cerebral hemispheres (notably, the basal ganglia and internal capsules) (Fig. 16.1). These often-delicate perforator vessels serve the critical role of perfusing key areas of the cerebrum and brainstem and therefore must be preserved during open skull base surgery to prevent significant postoperative neurological sequelae. Despite significant advancements in neurosurgical techniques and intraoperative technologies, these small and tenuous vessels, which often measure less than 1 mm in diameter, remain at significant risk of damage during neurosurgical procedures, particularly during manipulation of and dissection around the delicate neurovascular structures of the skull base. An in-depth knowledge of perforator anatomy serves an indispensable role in skull base neurosurgery—because great care must be taken by the surgeon to navigate around and avoid damage of these critical structures. A comprehensive understanding of the microvascular anatomy of the cerebral circulation, including the origins of perforator arteries, their takeoff trajectories, subarachnoid course, anastomoses, and subsequent branching patterns and parenchymal distributions, is essential for selection of appropriate microsurgical or endovascular treatment modalities, particularly when the anatomy of the skull base is distorted by complex vascular or neoplastic disease. This chapter will discuss basal perforator anatomy, relevant skull base pathology, and complication avoidance when planning and performing an open surgical approach to complex pathology of the skull base.

16.3 Vascular Challenges

The vascular challenges related to perforator injury during open skull base surgery stem from the delicate nature of the basal perforator vessels, their complex and highly variable anatomy, the abundance of numerous ramifying extracerebral branches, and the often close association with skull base pathology. These vascular challenges of skull base surgery can be further complicated by multiple reoperations, radiation therapy, and chemotherapy—distorting normal anatomical planes and obscuring skull base anatomy. Table 16.1 outlines the basal perforator vessels derived from each of the major cerebral arteries and summarizes the literature regarding their parent segments, numbers (mean and range), vessel diameters (mean and range), takeoff trajectories, and structures supplied.

Table 16.1 Overview of basal perforator vessels derived from each of the major cerebral arteries, their parent segments, numbers, vessel diameters, takeoff trajectories, and structures supplied

16.4 Perforator Injury Avoidance

Micromirrors and endoscopes prove particularly useful for direct visualization of critical neurovascular structures, such as perforator vessels that remain out of view when using the operating microscope (e.g., perforators located behind the dome of an aneurysm or on the deep aspect of a tumor).13 These modalities prove particularly useful after placement of a microsurgical clip, as they allow the surgeon to visualize the backside of the aneurysm, evaluate the aneurysm’s hidden anatomical features, and ensure optimal clip placement that does not incorporate any perforators or other critical neurovascular structures into the clip construct. In addition, angled endoscopes can be useful when attempting to visualize vasculature displaced or hidden by tumors near the skull base, which can parasitize branches from the main cerebral arteries and perforators that surround them.

Microvascular Doppler ultrasonography is a valuable tool for real-time assessment of blood flow through vessels in a noninvasive manner based upon their flow velocity.¹⁴ Although the probe can measure as small as 1 mm, it can prove to be difficult to accurately assess perforator vessel flow dynamics when placing the probe on target perforator vessels in a deep surgical field without also detecting the flow of nearby vessels, thereby confounding intraoperative assessment of vessel patency.^{15 ,​ 16} Further, microvascular Doppler ultrasonography cannot always reliably discern whether blood flow within a perforator vessel is sufficient to avoid infarction and cannot reliably assess flow within vessels smaller than 0.5 mm in diameter.¹⁷ In contrast to the conventional microvascular Doppler ultrasonography probe, a microvascular ultrasonic flow probe (Microvascular Flowprobe, Transonics Systems Inc., Ithaca, NY) has been shown in both in vitro and in vivo studies to provide the operator with both a quantitative and a qualitative assessment of vessel flow dynamics that is not confounded by factors such as hematocrit or vessel wall thickness.^{18 ,​ 19}

Electrophysiological monitoring with motor evoked potentials can detect decreased blood flow through the anterior choroidal artery (AChA), medial striate artery (MSA), or lenticulostriate artery (LSA) perforator branches within 60 seconds,^{20 ,​ 21 ,​ 22} but detection of flow disturbance within perforators of the posterior communicating artery (PComA) or posterior thalamic arteries cannot be monitored in this fashion, as they may not supply the pyramidal tract. Furthermore, variant anatomy, collateralization, and certain highly variable perforating vessels (e.g., recurrent artery of Huebner [RAH]) can defy consistent localization, and therefore, disturbance of their flow cannot always be reliably detected via electrophysiological monitoring. The use of motor and somatosensory evoked potentials allows the operator to intraoperatively assess for compromised cerebral blood flow and infarction by observing either a decrease or a loss of evoked potentials. It should be noted, however, that electrophysiological monitoring can be influenced by anesthetic technique and in some instances can have either false-negative or false-positive evoked potential changes in the setting of ischemic and no ischemic injury, respectively.^{23 ,​ 24}

Traditionally, intraoperative DSA has been used in combination with direct visualization to assess for patency of nearby parent or branching vessels and remains widely used in vascular and skull base neurosurgery.^{25 ,​ 26} Its advantages include evaluation of the entire cerebral circulation, and it can reveal adequacy of aneurysmal clip placement or residual arteriovenous malformations and fistulas. However, this method can be logistically difficult, invasive, time-consuming, and costly and can have limited resolution—making confirmation of perforator vessel patency difficult or impossible.

Fluorescein or ICG angiography has proven to be a particularly useful tool in many tumor and vascular neurosurgical cases. Fluorescein and ICG video angiography are rapid and repeatable modalities (after 20- to 30-minute washout delay) that are readily incorporated into the operating microscope and use intravascular fluorescence that enables visualization of small perforator vessels that can be difficult to discern with conventional intraoperative DSA. However, appreciable fluorescence of perforators can be restricted to the operative field and can be obscured by blood, pathology, or normal brain parenchyma. Moreover, fluorescein or ICG video angiography does not provide a quantitative assessment of perforator flow. Despite this, Raabe et al²⁷ demonstrated that ICG video angiography was comparable with intra- and postoperative DSA in 90% of cases and provided neurosurgeons with clinically significant intraoperative information leading to aneurysmal clip correction in 9% of cases.

Intraoperative assessment of perforator flow dynamics with the abovementioned modalities can provide critical information to the skull base neurosurgeon and can help with complication avoidance. However, it is our experience that these technologies must be combined with clinical judgment, adequate perforator dissection, and careful intraoperative inspection of the perforator branches to minimize the risk of postoperative perforator artery distribution infarctions.

The anterior communicating artery (AComA) complex constitutes the most common site of intracranial aneurysms and is associated with approximately 30% of ruptured aneurysms.28 ^{,​ 29} Given the frequent heterogeneity of the vascular anatomy in this area (with anomalies present in up to 60% of cases), the high degree of variability in angioarchitecture of aneurysms of this region (i.e., aneurysm neck, dome size, sac morphology, and projection orientation), and the proximity of these aneurysms to neighboring perforator vessels and other critical neurovascular structures of the skull base, they prove to be some of the most challenging cases to treat surgically.²⁹

Aneurysms of the AComA can be approached from interhemispheric, supraorbital, orbitozygomatic, subfrontal, pterional, or extended skull base approaches. The laterality of the approach to this region often depends on symmetry of the A1 segments. If the A1 segments are symmetric, a right-sided approach is often favored to avoid involvement of the speech-dominant hemisphere. However, if one of the A1 segments is hypoplastic (i.e., <1.5 mm), then an approach on the dominant A1 side is preferred to ensure early proximal control and optimal viewing of the aneurysmal neck and dome. Regardless of surgical approach, careful dissection of the surrounding structures, particularly the optic nerve, internal carotid artery (ICA), ipsi- and contralateral A1 segments, ipsi- and contralateral frontopolar and orbitofrontal arteries, and neighboring perforator vessels must be methodically carried out. The aneurysmal neck must be carefully defined, and cleavage planes should be dissected around the neck of the aneurysm after proximal and distal control has been attained. Neighboring perforator arteries, namely, the MSA and RAH, should be dissected proximally and distally and then carefully displaced to allow clip application without occlusion of these vessels. If clip application cannot be accomplished without occlusion of adherent or intimately associated perforator vessels, a fenestrated aneurysmal clip should be employed to incorporate these delicate vessels into the construct without disturbing their flow.

Tumors of the anterior skull base and suprasellar compartment are a diverse group that encompass pathologies such as meningioma, hemangiopericytoma, pituitary adenoma, craniopharyngioma, chordoma, esthesioneuroblastoma, sarcoma, and lymphoma, among many others. These tumors may involve the anterior skull base’s contents and can displace or even encase critical neurovascular structures of this region. Accordingly, maximal safe or gross total resection can be difficult without sacrificing or disturbing flow of associated perforators. Some tumor types, such as pituitary adenomas, tend to encase nearby cerebral vasculature (e.g., ICAs) but in most cases can be separated relatively easily, whereas other tumors, like aggressive fibrous meningiomas, have a proclivity for invasion of nearby vessel adventitia—making the surgical separation of tumor from involved vessels difficult or impossible without sacrifice or leaving residual tumor behind. Preservation of involved perforators should be attempted at all costs and mandates the skull base neurosurgeon to understand the involved parent and branching perforator vessels by studying each patient’s preoperative magnetic resonance imaging (MRI) and vascular imaging.

In the case of large clinoidal meningiomas, which tend to encase neighboring vessels and perforator branches, surgical treatment of these typically benign tumors can prove particularly difficult.30 ^{,​ 31} In our experience, a pterional transylvian approach is favored, with careful dissection of the middle cerebral artery in distal-to-proximal fashion toward the ICA bifurcation. Encased perforators (e.g., LSA, MSA, and AChA) must be meticulously dissected and freed from the tumor using a combination of microdissection, bipolar electrocautery, and microscissors to facilitate their separation. The surgeon should carefully explore the entrance points of the perforator vessels into the tumor along with their exit points (when applicable) and dissect along the anatomical layer that separates the vessels from the tumor. Knowledge of the parent vessel course relative to the tumor and perforator entrance points is essential when dissecting these small, often friable perforators free, as intratumoral vasculature can further complicate their identification and dissection. When identification of these branches is difficult, dividing the tumor into several segments or carefully debulking can improve visualization and ease of identification of involved perforator vessels—aiding in their safe dissection and separation from the tumor. Carefully debulking a tumor that encases the perforators can help minimize the risk of progressive compression and disruption of normal perforator flow dynamics, leading to vessel thrombosis and stroke.

Understanding of the preoperative anatomy is essential for intraoperative decision-making, because inadvertent sacrifice of a perforator branch will likely lead to a significant postoperative neurological deficit. Leaving behind a small amount of tumor that can be treated postoperatively with adjuvant radiotherapy or chemotherapy is almost always preferable to an aggressive gross total resection with significant postoperative neurological deficit.

16.5.2 Open Skull Base Surgery for Pathology Near the Posterior Circulation

Posterior circulation aneurysms broadly encompass PComA aneurysms, basilar apex aneurysms, and those of major branches of the vertebral and basilar arteries (anterior inferior cerebellar artery and posterior inferior cerebellar artery). PComA aneurysms represent roughly 30% of all intracranial aneurysms.³² These aneurysms have unique variability in their projection orientation. In large PComA aneurysms, the microvascular anatomy can be significantly distorted on preoperative DSA. Large PComA aneurysms can appear to arise from an absent or hypoplastic PComA, which results from direct aneurysmal compression. The neighboring AChA can also be displaced posteromedially and mistaken for an MSA, and the thalamoperforate artery (TPA) branches can be similarly pushed posteromedially by the aneurysm. PComA aneurysms can be approached via pterional, orbitozygomatic, or lateral supraorbital approaches and may require anterior clinoidectomy for expansion of the paraclinoid space (i.e., optic-carotid and carotid-oculomotor windows) to ensure adequate visualization and proximal control. Regardless of the approach, the same principles for safe, effective surgical clipping apply. The PComA aneurysm dome may be adherent to the oculomotor nerve and is often not dissected free because of the risk of injury to the third nerve. A temporary clip can be placed across a perforator-free zone of the supraclinoid ICA to facilitate aneurysmal neck dissection. Opening of the cistern of the lamina terminalis enables better visualization of collateralization of the PComA with the AComA and anterior cerebral artery, nearby perforator vessels, and eventual placement of a permanent clip without perforator flow disturbance. A medial trajectory is then used to check the distal clip interface to ensure no perforators are caught in the clip. This is facilitated by mild lateral displacement of the ICA.

Basilar apex aneurysms comprise approximately 5 to 8% of all intracranial aneurysms and are associated with a high risk of rupture.³² Although most basilar apex aneurysms are now treated endovascularly, these aneurysms are particularly prone to recanalization and regrowth after coiling, necessitating subsequent definitive open neurosurgical treatment.³³ These aneurysms are technically difficult to access because of their deep-seated location, extremely narrow surgical corridors, difficulty attaining sufficient proximal and distal exposure of the basilar artery, and close association with basilar apex perforator arteries. Interestingly, the basilar bifurcation complex has significantly less anatomic variability and complexity than the AComA complex.³⁴ Nevertheless, inadvertent occlusion of the basilar apex perforators carries significant risk of severe neurological impairment and death. Basilar apex aneurysms can be approached via subtemporal, pterional, transcavernous, and other extended skull base approaches. The region of the interpeduncular fossa is crowded by several different groups of perforators, namely, the TPA of the P1 segment, thalamogeniculate artery of the P2 segment, AChA, medial posterior choroidal artery, lateral posterior choroidal artery, and perforators deriving from the superior cerebellar artery. Like with all aneurysm surgery, direct visualization of the nearby perforators is essential during the clipping process. In the case of the transcavernous approach for basilar apex aneurysms, the posterior clinoid process may need to be removed to improve visualization of the contralateral P1 segment and its perforators, which can be inadvertently included in the clip construct—as they are often hidden behind the aneurysm. In the case of perforators adherent to the aneurysmal dome, placement of temporary clips alone or in combination with adenosine-induced cardiac pause (0.3—0.4 mg/kg body weight) to soften the aneurysmal dome prior to their dissection can be particularly helpful. The senior author often prefers a lateral subtemporal approach to basilar apex aneurysms, as described by Drake,³⁵ to better visualize the posterior P1 perforators during clip placement.

Preoperative understanding of the aneurysmal neck and fundus, its projection orientation, its relationship to the dorsum sellae, the angle of bifurcation and height of the basilar apex, and the angle between the P1 segments can help dictate the most appropriate neurosurgical approach for a patient with this type of aneurysm. An approach that maximizes visualization of the aneurysm neck and fundus, nearby neurovascular structures, and perforators is likely to decrease inadvertent perforator injury and thereby minimize postoperative morbidity and mortality.

Tumors involving the posterior circulation encompass a wide variety of neoplastic pathologies and include meningioma, schwannoma, glioma, giant cell tumor, chordoma, chondrosarcoma, epidermoid tumors, and metastases, among many others. Like tumors near the anterior circulation, these tumors can vary in their involvement of surrounding vasculature. Petroclival meningiomas are often large and can encase the nearby surrounding posterior circulation vasculature and perforator vessels and can also displace and adhere to the brainstem and its associated cranial nerves. They may also parasitize the brainstem perforating vasculature. These collective features make petroclival meningiomas technically challenging tumors to resect despite their typically benign pathology. Approaches to petroclival meningiomas are patient-specific; depend on tumor size, location, and extension; and span frontotemporal, orbitozygomatic, subtemporal-transzygomatic, presigmoid, retrosigmoid, anterior, posterior, and combined petrosal, retrolabyrinthine, translabyrinthine, transcochlear, far lateral, and extreme lateral approaches.³⁶ Because of the close anatomic relationships these lesions have to critical neurovascular structures, a systematic, multidisciplinary approach must be employed to improve long-term patient outcomes.³⁷ Nevertheless, the same surgical principles apply in the successful resection of these tumors. Preoperative understanding of the tumor’s relationship to the posterior circulation, perforator branches, draining veins and dural venous sinuses, and cranial nerves is essential when planning a skull base approach for these tumors. The senior author favors developing a plane between the tumor capsule and adjacent vessels, when possible. Again, in the case of tumor encasement of the posterior circulation and perforators, identification of their entry and exit points aids in the careful microsurgical dissection and separation of these vessels from the tumor. In cases where the main cerebral vessels and perforators cannot be safely separated from the tumor, a near-total or subtotal resection of the tumor is favored to avoid major ischemic complications. This is especially true when the tumor shares blood supply with brainstem perforators. The skull base surgeon must incorporate a patient’s preoperative functional status and quality of life, likelihood of progression-free survival, and possibility of durable disease control with adjuvant therapies into the surgical decision-making process. Leaving behind a small amount of tumor that can be treated with adjuvant radiotherapy is almost always preferable to attempting a curative, aggressive gross total resection with significant postoperative neurological deficit and subsequent poor quality of life.

16.6 Case Examples

A 76-year-old man with a history of hypertension, type 2 diabetes, and prostate cancer (status post radical prostatectomy) presented initially to ophthalmology with 1 year of worsening vision and was found to have a right homonymous superior quadrantanopia. MRI of brain with and without contrast revealed a contrast-enhancing lesion of the left optic tract and posterior clinoid region (Fig. 16.2a–c). He underwent a left frontotemporal approach for biopsy and gross total resection (Video 16. 1). Pathology was consistent with pilocytic astrocytoma of the optic tract. Upon completion of tumor resection, the patient was noted to have diminished motor-evoked potentials involving the right hand. At this point, a dilute solution of papaverine (3 mg/mL) was applied to the ICA, A1, M1, P1, superior cerebellar artery, PComA, and all visualized perforator vessels. Microvascular Doppler ultrasonography and ICG video angiography were then performed, which both demonstrated delayed flow of the left PComA, consistent with dissection. The patient’s blood pressure was liberalized with a mean arterial pressure (MAP) goal of greater than 85 mm Hg, and an additional aliquot of papaverine solution (3 mg/mL) was irrigated onto the left PComA and nearby perforators. Repeat ICG video angiography was performed, which demonstrated left PComA vessel patency with similar slightly diminished filling. The patient’s motor evoked potentials improved but did not return to baseline. Of note, the left AChA demonstrated normal flow on intraoperative microvascular Doppler ultrasonography and ICG video angiography. Despite additional intraoperative papaverine, documented perforator vessel patency on microvascular Doppler ultrasonography and ICG video angiography, and postoperative care with permissive hypertension, high-rate intravenous fluids (125 mL/hour), and aspirin (325 mg) on postoperative day 1, the patient sustained an infarction in a left AChA distribution with right upper and right lower extremity weakness postoperatively (Fig. 16.2e). Postoperative MRI of brain with and without contrast demonstrated gross total resection (Fig. 16.2d).

Related posts:

Endovascular Options to Treat Iatrogenic Vascular Injury and Tumor Involvement of the Skull Base Dealing with Vascular Injury During Middle Fossa Surgery Simulation and Training—Preparing for Vascular Injury Dealing with Major Intraoperative Vascular Injury Extracranial Anterior Cranial Base Surgery for Vascular Tumors Extracranial Lateral Cranial Base Vascular Tumor Surgery

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