9.1 Key Learning Points

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  It is critical to check preoperative labs prior to any surgical procedure to assess for thrombocytopenia or any coagulopathy.

  
  
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  A patient’s past medical history which may include bleeding disorders or use of antiplatelet agents or anticoagulation must be considered. Patients should hold all antiplatelet medications for at least 5 to 7 days prior to the procedure, and all anticoagulation at least 3 days prior to the procedure. The indications for the patient’s antiplatelet/anticoagulant use must be discussed with the patient’s primary provider to limit risk of potential thromboembolic complications while the medication is held.

  
  
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  Preoperative imaging should be extensively studied for any vascular involvement by the pathology being treated. Bilateral internal carotid arteries (ICAs) and all its terminal branches must be evaluated. Specifically, thorough evaluation of anterior cerebral arteries (ACAs), A1, A2, anterior communicating artery (AComA), and its branches must be evaluated for encasement.

  
  
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  If the pathology involves the ICAs extensively, preoperative balloon test occlusion (BTO) is recommended to evaluate collateral flow in case the ICA is injured and needs to be sacrificed intraoperatively or postoperatively. The BTO will also guide the total extent of resection the surgeon may pursue.

  
  
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  Preoperative planning of resection of tumors encasing anterior cerebral vasculature should include evaluation of a potential “cortical cuff.” This layer of protective noneloquent brain matter separating tumor and vasculature is best visualized with magnetic resonance imaging (MRI), and the presence of a cortical cuff makes resection by endoscopic approach more feasible. However, the absence of a cortical cuff, as in the case of almost all tuberculum sellae meningiomas, does not eliminate the feasibility of an endoscopic endonasal approach.

  
  
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  Intraoperative image guidance with merged MRI and computed tomography angiography (CTA) modalities is a useful tool during the treatment of complex skull base pathologies.

  
  
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  Prior to starting the procedure, the availability of all surgical instruments and tools which may be required in case of vascular injury should be confirmed. In addition, cross matching the patient and having blood available is recommended.

  
  
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  An experienced team with a two-surgeon, four-handed approach is recommended for complex pathologies in which vascular injuries may be encountered.

  
  
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  We also recommend that more complex pathologies during which vascular injury may be encountered are performed at an institution where both a multidisciplinary team experienced with handling complex pathologies with neurovascular considerations as well as an endovascular team with neurointerventional capabilities are available.

9.2 Introduction

Over the past two decades, expanded endoscopic endonasal approaches (EEAs) have enabled alternate access to anterior skull base pathologies from a route through the paranasal sinuses. ^{1 ,​ 2} The EEAs via transcribriform or transplanum/transtuberculum corridors have allowed treatment of various lesions such as meningiomas, schwannomas, craniopharyngiomas, esthesioneuroblastomas, and other sinonasal malignancies. ² Despite offering a minimal access approach to anterior skull base pathologies, EEAs have the potential for a variety of complications including postoperative cerebrospinal fluid (CSF) leak, impaired olfaction, infection, and vascular injury. Major vascular injury to neighboring structures such as the internal carotid artery (ICA) and anterior cerebral arteries (ACAs) and their branches can result in major morbidity and even mortality. In general, tumors encasing vessels or in the absence of a protective cortical cuff may be better suited for treatment via open transcranial approach. In addition, in the event of a major vascular injury, such as an arterial vessel tear or transection, the ability to perform safe vascular control with temporary clips and direct suture repair, anastomosis, or bypass is more feasible with an open transcranial approach than it is with a narrow endonasal corridor. However, if the tumor is demonstrated on preoperative imaging to be adequately separate from crucial vasculature, the EEAs can be considered as these approaches allow for improved visualization and reduced brain retraction, and a possible lower risk of vascular injury (as opposed to tumors that have vessel encasement). Despite allowing for improved visualization and minimal retraction, whether the EEAs reduce vascular complication rates when compared to open approaches is disputed. In either approach, the occurrence of major vascular injury is rare and EEAs have been repeatedly demonstrated to achieve vascular complication rates that are comparable to those seen in open surgery. ^{3 ,​ 4} Endonasal approaches for pituitary tumor resection have a reported incidence of ICA injury ranging from 0.5 to 1.1%, while more extended approaches have a higher incidence of 4 to 9%. ^{5 ,​ 6 ,​ 7 ,​ 8 ,​ 9} Injuries do occur in both types of procedures but one could argue that it is easier to deal with complications in the open case because of better visualization and a larger working corridor to quickly apply temporary clips and perform direct vessel repair with microanastomosis techniques. In this chapter, we focus on the vascular challenges encountered during EEAs to pathologies affecting the anterior skull base, techniques and strategies which can be employed to reduce vascular complications, and the management of vascular complications intra- and postoperatively.

9.3 Relevant Anatomy

Knowledge of the relevant vascular anatomy is essential to avoid major vascular complications (Fig. 9.1). One of the risk factors for vascular injury is lack of familiarity of the neurovascular anatomy of the skull base and the variations which can be encountered, especially with existing pathologic conditions. The rate of injury to the ICA in transsphenoidal surgery is inversely related to the surgeon’s experience. ¹⁰ This can be supplemented by careful study of the relationships between major blood vessels and surgical landmarks seen on preoperative imaging in conjunction with the use of image guidance; this is crucial due to anatomical variations. The vasculature at risk depends on the pathology and approach utilized. In particular, the vasculature at risk of injury during an EEA to the anterior fossa includes the ICAs, ACAs, and the ethmoidal arteries.

In this chapter we will refer to the Bouthillier et al classification of the segments of the ICA: C1 cervical, C2 petrous, C3 lacerum, C4 cavernous, C5 clinoid, C6 ophthalmic, and C7 communicating (Fig. 9.2). ^{11 ,​ 12} The C3, C4, and C5 segments of the ICA can be injured during a variety of EEA. The C3 segment runs from the end of the carotid canal, passes above the cartilage-filled foramen lacerum, and extends to the anterior portion of the petrolingual ligament. ^{11 ,​ 13} The C4 segment starts from the superior margin of the petrolingual ligament and ends as it exits the cavernous sinus at the proximal dural ring. The cavernous portion of the ICA is divided into three segments—posterior ascending, horizontal, and anterior vertical segments. ¹¹ The C5 segment, also known as the clinoid segment, starts its course at the proximal dural ring and ends at the distal dural ring where the ICA enters the subarachnoid space. ¹¹ In 71% of patients the ICA bulges into the sphenoid sinus but is covered by bone. ¹⁴ Dehiscence of the ICA is seen when the ICA is exposed to the sphenoid sinus due to the absence of the bony wall. The incidence of this variant is not well studied, but its range is estimated from 5 to 30%. ^{15 ,​ 16} This anatomic variant can be dangerous to encounter during EEAs as the bony layer normally serves as a useful protective barrier from injury to the ICA. Additionally, the ICAs may have a smaller inter-artery distance and compress the pituitary gland. In these cases, the vessels may be injured if the dura is opened more laterally without caution. ⁴ Furthermore, the anatomic protection of the cavernous portion of the ICA is limited, as the bony wall covering the ICA is variable and usually thin and insufficient for protection especially during drilling. ¹⁷

Although it is uncommon, there is increased risk of injury to the ACA, especially the orbitofrontal and frontopolar branches due to the proximity of the frontal lobe during transcribriform approaches. ^{18 ,​ 19 ,​ 20} The orbitofrontal artery, usually the first branch of the A2 segment of the ACA, resides in the olfactory sulcus on the frontobasal surface, and it provides the vascular supply to the gyrus rectus. ²¹ The frontopolar artery, usually the second branch of the A2 segment of the ACA, resides superior and medial to the orbitofrontal artery, and it provides the vascular supply to the medial portions of the frontal lobe. ²¹ Both the A1 and A2 segments can be displaced or encased by tumors affecting the anterior skull base and suprasellar region, such as tuberculum sellae meningiomas and craniopharyngiomas. Careful review of the imaging, including MRI, CT angiogram, and sometimes cerebral angiogram, must be performed prior to attempting an EEA.

In the endonasal transcribriform approach, the anterior and posterior ethmoidal arteries, branches of the ophthalmic artery, are typically ligated and divided to devascularize cribriform tumors. ²² The anterior ethmoidal artery enters the nasal cavity and courses between the second and third lamellae. The posterior ethmoidal artery resides along the roof of the ethmoid, anterior to the sphenoid sinus, approximately 5 mm anterior to the optic canal, and it supplies the posterior ethmoid air cells and the nasal septum. ^{22 ,​ 23} The superior portion of the lamina papyracea is removed to expose the posterior or anterior ethmoidal artery. At this point, the ethmoidal arteries may be ligated. The posterior ethmoidal artery is usually larger than the anterior ethmoidal artery and runs more closely to the skull base. ²⁴ Identification of these ethmoidal vessels allows accurate cauterization and division to devascularize the anterior skull base tumor in preparation for cribriform plate resection. One must be cautious not to allow inadequate cauterization and retraction of the artery into the orbit resulting in retrobulbar hematoma, orbital compartment syndrome, and visual loss.

9.4 Vascular Challenges

One of the most significant challenges of endoscopic endonasal surgery (EES) is using instruments in narrow corridors without causing injury to nearby anatomical structures. The narrow nasal corridor and the distances at which instruments are used can present significant challenges during EES especially when vascular complications occur. This can happen at any point during the surgery: during bony exposure, resection of the lesion, and closure of the skull base defect.

The ICA is the most commonly injured vessel during EEAs. Romero et al performed a literature review of vascular injuries during endoscopic procedures that included 7,336 patients and found the arterial injury rate to be 0.34%, and of the 25 cases with an arterial injury, 19 were ICA injuries. ⁴ From these injuries to the ICA, four patients died and two developed neurological deficits. ⁴ Although the reported rates of vascular injury during endonasal endoscopic surgery may potentially be low due to the wider view offered by the endoscope and improved localization of the ICA, injury to the ICA is the most common vascular complication. These rates may increase as the procedure is more frequently used. Injuries to other arteries are less common but have been reported in various retrospective reviews.

Injury to the ACA and its branches is also possible. In a retrospective review done by Kassam et al on 800 cases of endoscopic endonasal skull base surgeries, they found only seven vascular injuries, one of which was an avulsion of the frontopolar (A2) artery which eventually resulted in permanent right hemiparesis. This patient required endovascular treatment to control the bleeding. ²⁵ Romero et al described a case during which a perforator of A1 was torn during removal of a meningioma. The injured vessel was clipped but no new neurological deficit was identified. ⁴ Although injuries to these branches are relatively rare, they are possible during expanded EEAs. These branches can be injured directly or commonly avulsed during tumor removal. It is imperative to avoid removal of tumor until it has been thoroughly dissected off the surrounding tissue, especially when removing the most dorsal portions. When these small caliber arteries are injured, direct repair is nearly impossible from an EEA. Management will generally involve direct coagulation or clipping of the injured vessel. Postoperative angiogram can be performed if there is concern for a pseudoaneurysm or injury to a larger vessel.

9.5 Injury Avoidance

As with any other surgical complication, injury avoidance begins with knowledge of normal anatomy. A thorough knowledge of the sinonasal and intracranial vasculature is required prior to any surgical intervention. Furthermore, the patient’s own preoperative imaging must be studied to examine any anatomical variance as well as any vascular involvement with the lesion itself.

In addition to the MRI to evaluate the lesion, a CTA should be obtained for all lesions involving the anterior skull base and parasellar regions. CTA can provide critical information regarding the location of the ICAs, the ACAs, and their branches. In addition, CTA provides the ability to view the vessels in relation to the bony anatomy of the skull base and the involved pathology. For example, in a case where a tumor is encasing the paraclival segment of the ICA seen on an MRI, it would be useful to know if the bony canal over the ICA is intact or dehiscent on a CTA. Dissecting the tumor off an intact bony carotid canal is much easier and has lower risk for ICA injury than a “naked” ICA without bony protection. We routinely use the preoperative MRI and merge it with the CTA for intraoperative image guidance. A blended hybrid view can help visualize tumor pathology in conjunction with the course of the vasculature (ICA) and the bony structures of the skull base.

If the pathology significantly involves the ICAs or any of the other major surrounding vessels or appears hypervascular with flow voids on the T2 MRI, a diagnostic cerebral angiogram may be helpful to further delineate the surrounding vasculature and blood supply to the tumor. Only a small portion of these skull base lesions will be amenable to preoperative embolization. If the arterial supply is from the ICA, the lesion is typically not amenable to embolization, as there is a considerable risk of causing a thromboembolic complication. In situations where the lesion encases the ICA or if an ICA appears to be at high risk of injury, a preoperative balloon test occlusion (BTO) with hypotensive challenge of the involved ICA can be performed to determine if there is adequate collateral circulation for carotid in the case of an intraoperative ICA injury. If the patient develops focal symptoms during the test, this is an indication that the patient may have an adverse outcome if carotid injury occurs intraoperatively. This test can guide the aggressiveness of resection or raise consideration of preparing for a bypass. ²⁶ Nevertheless, it may be prudent to perform a more conservative resection leaving residual adherent tumor on the ICA in these cases. For more on BTO and evaluation of tumor vasculature, see Chapter 2.

Intraoperative Doppler ultrasound can also be useful to guide the bony exposure of the ICAs as well as tumor dissection off the ICAs. If visualization of the ICA protuberances and the normal bony landmarks (optical carotid recess, optic canal) is inadequate after the sphenoid sinus has been opened, the Doppler can be used in conjunction with image guidance to confirm location of the ICAs. ²⁷ The Doppler also helps in identifying the location of the cavernous portion of the ICA before dural opening.

It is best to have a two-surgeon team with a four-handed approach during complex cases involving the anterior skull base. ²⁸ Having two surgeons with experience in their respective fields improves decision-making and provides the ability for dynamic movement of the endoscope. Before the operation, it is important to review the angiographic imaging, determine the patient risk factors, extent of the tumor, and its relation to the nearby neurovascular structures. It is also important to be comfortable with the anatomy, specifically, the location of the arteries and their landmarks from the endoscopic viewpoint. There are well-established landmarks that can be used to determine the location of specific segments of the ICA (see Chapter 1). ²⁹

Intraoperatively, since the vessels can be pushed away from their normal course, the tumor should be debulked prior to performing extracapsular dissection. It is important to use sharp dissection to release adherent arachnoid that could be tethering the neighboring vessels to the tumor capsule, as in the case of some olfactory and tuberculum meningiomas. If there is tumor encasement or strict adherence, it may be safer to trim the tumor sharply to release the vessel from the tumor, leaving a small residual amount of tumor adherent to the vessel. This is a better alternative than vessel avulsion injury which can result in potential hemorrhage and ischemic stroke. ³⁰

The proper use of surgical equipment also can minimize the risk of arterial injury. Romero et al made some recommendations based on their experiences with arterial complications. They recommended to always keep surgical equipment in view with the endoscope and to only remove the tumor when it is adequately dissected from adjacent structures. ⁴ Angled endoscopes allow the surgeon greater access and generally a wider view. However, greater angulation may mean that there are additional structures which can be visualized but cannot be safely dissected or controlled. We therefore recommend the use of 30-degree angled endoscopes, and increasing angulation only as necessary, particularly in cases that involve the ACAs. In addition, avoiding the use of some equipment in certain locations can help to minimize risk of arterial injury. Romero et al demonstrated one case in which the use of an ultrasonic aspirator during the resection of a pituitary macroadenoma resulted in brisk arterial bleeding which needed to be controlled quickly. Based on their experience, they recommend avoiding the use of ultrasonic aspirators near the cavernous sinus. ⁴ In the event that there is tumor adherence to the ACAs, we recommend that it is better to leave a small remnant attached to the vessels than to risk avulsion or tear to the ACAs.

In the case of the ACAs (A1, A2, and anterior communicating artery) and their branches, tumors of the skull base can adhere to or encase these arteries rendering endoscopic approaches difficult to perform. In these cases, open transcranial approaches may be preferable as these approaches would allow for better control of vascular complications such as hemorrhage. Open approaches would allow the surgeon to repair any arterial injury via direct suture repair or bypass under temporary occlusion. Preoperative imaging with MRI with and without gadolinium and CTA is crucial for determining the extent of vascular involvement of the tumor. However, these studies are limited in their ability to differentiate between visualizing vessels encased by a tumor and a highly vascular tumor.

Also, in the context of ACA injury, the presence of a “cortical cuff” makes an endoscopic approach more favorable. A “cortical cuff” is defined as a protective layer of noneloquent brain tissue that provides a natural plane of separation between tumor and the anterior cerebral vessels. Koutourousiou et al demonstrated that the absence of a cortical cuff between the tumor and anterior cerebral vasculature limited the extent of resection performed endoscopically. ³¹ Therefore, open approaches should be considered when preoperative MRI demonstrates vascular encasement and a gross total resection is indicated.

9.6 Related Pathologies

The risk of vascular injury may be dependent on the characteristics of the pathology being operated. The size, location, and extension into the surrounding neurovasculature are all dependent on the aggressiveness of the lesion. Prior to the operation, it is important to know how the pathology of the patient might alter the surrounding anatomy and change the course of the vasculature. Tumor consistency also plays an important role on how readily dissection away from vascular structures can be performed. Softer tumors (most adenomas and chordomas) can be aspirated with suctions away from vascular structures, whereas firm tumors require more microdissection. Tumors with a firmer, more fibrous consistency present a challenge for endoscopic endonasal removal. Not only do these tumors require more microdissection, but because of their firmer consistency, they may not descend into the sella as easily and may require additional bony removal of the planum sphenoidale. ^{32 ,​ 33}

For suprasellar tumors, such as tuberculum sellae meningiomas and craniopharyngiomas, the ICAs and posterior communicating arteries laterally, the anterior communicating artery and ACAs superiorly, the basilar apex and P1 vessels posteriorly, are at risk. Tuberculum sellae meningiomas tend to occur inferiorly and anteriorly at the anterior wall of the sella turcica. As a result, they are more likely to involve the ACAs. ³⁴ Although craniopharyngiomas can also extend anteriorly, according to the Kassam classification of craniopharyngiomas, types II and III can extend posteriorly, potentially involving the posterior communicating artery and posterior cerebral artery. ²⁸ Again, these tumors should be debulked prior to performing extracapsular dissection to ensure safe vascular dissection. Internal debulking makes it easier to collapse the tumor capsule away from the neurovascular structures. It is important to keep the plane of dissection between the tumor capsule and the tumor arachnoid so that the arachnoid is mobilized toward the side of the vessel which offers a subtle extra barrier of protection. Sometimes the arachnoid needs to be incised sharply to free the adjacent vessel away from the tumor capsule. For both craniopharyngiomas and meningiomas, it is paramount to identify and preserve the superior hypophyseal vessel and perforators that supply the optic apparatus since inadvertent injury to this vessel could lead to postoperative visual loss. For tuberculum sellae meningiomas that invade the optic canal, it is important to identify and protect the ophthalmic artery coursing inferomedial in the optic canal when opening the optic dural sheath.

Chondroid tumors of the clivus are associated with a greater risk of injury compared to pituitary adenomas due to greater involvement of one or both paraclival ICAs (Fig. 9.3 and Fig. 9.4). Fig. 9.3 and Fig. 9.4 demonstrate an illustrative case in which a skull base chondrosarcoma erodes the bony wall around the right paraclival ICA. When there is tumor adjacent or encasing vascular structures without intervening bony protection, such as in the case of a clival chordoma or invasive pituitary adenoma eroding the paraclival carotid canals, a two-suction technique with strong 12 to 14 French Frazier suctions to initially aspirate the tumor followed by smaller size, controlled suctions is recommended. Ultrasonic and side-cutting aspirators should not be used next to the ICA. In addition, sharp ringed curettes should be avoided as these can cut the vessel wall. Blunt ringed/looped curettes can be used judiciously with extreme caution but has less of a vascular risk than sharp (Hardy) curettes. In pathologies that have eroded bone, such as chondrosarcomas, it is important to outfracture and mobilize the fragmented bone away from the ICA vessel wall in order to avoid the sharp edges from encroaching the artery (Fig. 9.3 and Fig. 9.4).

Functional macroadenomas can also increase the risk of vascular injury as their respective hormonal changes can affect tissues and introduce unique difficulties during surgery. High levels of cortisol results in hypertension and connective tissue changes, which can lead to friable changes of the ICA, increasing risk of injury. ^{4 ,​ 35} Growth hormone-secreting adenomas resulting in acromegaly cause anatomic changes such that intranasal anatomy is altered due to bony overgrowth and soft tissue hypertrophy, as well as arterial ectasia, potentially decreasing the intercarotid distance. Both of these anatomical alterations need to be considered and evaluated for with neuroimaging. ³⁶

Furthermore, pathologies including olfactory groove and tuberculum sellae meningiomas may be susceptible to bilateral ACA injury upon their resection. It is therefore important to assess for vascular encasement and for the presence of a cortical cuff between the tumor and arteries on preoperative MRI (T1 + gadolinium and T2 sequences). In olfactory groove meningiomas, the presence of a cortical cuff provides a protective layer of noneloquent brain tissue for the ACAs. This lessens the risk of a vascular injury and impacts the extent of resection. ³¹ However, in tuberculum sellae meningiomas, there is almost always no cortical cuff present because the superior portion of these tumors abut directly against the A1 or AComA (anterior communicating artery) vessels in the suprasellar cistern. Extension of this relationship can lead to encasement and it is important to assess for any tumor encasement of the ACAs and its branches.