Cerebral revascularization for skull base tumors represents a complex subset of the intracranial bypass procedures with unique challenges compared to revascularization for intracranial aneurysms. Skull base tumors requiring cerebral revascularization may include meningioma, schwannoma, chordoma, chondrosarcoma, and aggressive malignancies (squamous cell carcinoma, adenoid cystic carcinoma, etc.) The decision to perform a bypass could be either pre-operative such as flow augmentation for partial vessel occlusion from tumor invasion and flow replacement for total vessel occlusion by the tumor, or intra-operative to salvage vascular injury during tumor excision. Vascular injury during skull base tumor excision typically occurs due to encasement or invasion of blood vessels, presence of scar tissue, loss of normal arachnoid planes, and unexpected vascular anatomy. This chapter reviews the key management strategies and technical considerations gleaned from the senior author’s (LNS) vast experience performing bypass surgery for skull base tumors over three decades. We also use case examples to highlight the decision-making process involved in the optimal management of these lesions.
Key wordsCerebral revascularization – skull base tumors – EC-IC bypass – high-flow bypass
5 Bypass in the Treatment of Skull Base Tumors
5.1 Key Learning Points
Common risk factors for intraoperative vascular injury during skull base tumor surgery are reoperation for previously resected or irradiated tumors, tumor dissection from vessel wall, unexpected vascular anatomy, surgeon disorientation, and use of drills, ultrasonic aspirators, or laser in proximity to vasculature.
Skull base pathologies that may necessitate flow replacement include meningioma, schwannoma, chordoma, chondrosarcoma, and malignant lesions such as squamous cell carcinoma, adenoid cystic carcinoma, and osteogenic sarcoma.
Various techniques such as direct suturing, local intracranial-intracranial bypasses, and high-flow bypass exist for vessel reconstruction and replacement. The ability of a patient to tolerate occlusion of a major artery depends on the artery, collateral flow, and patient’s age.
Extracranial (EC) to intracranial (IC) bypass for cerebral vascularization was introduced by Yasargil in 1967 in the form of superficial temporal artery (STA) to middle cerebral artery (MCA) bypass for cerebral ischemia in a patient with carotid occlusion. 1 The first high-flow EC-IC bypass was performed a few years later by Lougheed and colleagues utilizing a saphenous vein graft (SVG) between the common carotid artery (CCA) and intracranial internal carotid artery (ICA). 2 Over subsequent decades, new techniques and refinement of existing techniques were introduced by various surgeons in North America, Asia, and Europe. Following the results of the EC-IC bypass trial 3 and Carotid Occlusion Surgery Study (COSS), 4 EC-IC bypass is now seldom performed for flow augmentation in patients with cerebral ischemia due to atherosclerotic steno-occlusive disease. However, an EC-IC bypass continues to be indicated for flow augmentation in select patients with steno-occlusive pathology due to moyamoya disease, and for flow replacement in some patients with complex intracranial aneurysms and skull base tumors. 5 , 6 , 7 , 8 , 9
5.3 Vascular Challenge
Skull base tumors can affect various components of the cerebral vasculature including arteries, capillaries, and veins. In this chapter, we will discuss arterial problems that occur during the resection of skull base tumors and the use of bypasses for flow replacement in the event of injury. 7 , 8 , 10
Arterial involvement by tumors may be encasement (partial or complete) or actual wall invasion of vessels varying in size from perforators to major vessels such as ICA, basilar artery (BA), or vertebral artery (VA). In addition to tumor involvement of arteries, iatrogenic injuries during surgical dissection may occur, leading to significant bleeding and brain infarction. When arterial occlusion occurs, an ischemic stroke may result from failure of collateral circulation to maintain adequate blood flow or from thromboembolic complications.
Involvement of small arteries and capillaries may manifest as invasion of pial vasculature by the tumor and cause vasogenic edema of the brain or brainstem. This type of involvement often precludes complete resection of the tumor. Severe neurological deficits could occur when resection of such tumors is attempted in the brainstem or other eloquent brain regions.
Venous involvement can occur from tumor invasion of large dural venous sinuses, 11 or displacement, encasement, or invasion of large cortical veins such as vein of Labbe. 12 Similar to iatrogenic arterial injuries, venous injury may occur during tumor dissection, and could lead to postoperative venous infarction and hemorrhage.
5.4 Injury Avoidance
Injury to arterial structures during skull base tumor resection commonly occurs in the following situations:
Cases involving reoperation for disease progression, disease recurrence, or inadequate resection during primary surgery. These cases are technically more challenging due to the presence of scar tissue and loss of normal arachnoid planes. A history of prior radiation often adds to the complexity. Awareness of the increased risk of vascular injury during these cases is critical. Extensive preoperative vascular imaging and provocation tests, and preparation for a bypass procedure may be necessary. A T2-weighted magnetic resonance imaging (MRI) can be helpful to assess arachnoid planes and to detect vessel narrowing. Contrast enhancement may not be a reliable indicator of vessel wall invasion.
Tumor dissection from the vessel wall. Vascular injuries are more common when the artery is encased or invaded by the tumor. When vessels are invaded by a malignant skull base tumor, resection of the tumor and bypass may be needed for oncological reasons. During resection of benign skull base tumors, if arterial narrowing is not seen on preoperative imaging, it is reasonable to attempt tumor dissection off the vessel wall. If possible, proximal and distal control of the vessel should be established first. If arterial narrowing is visible on preoperative imaging such as T2-weighted MRI, options include subtotal tumor resection or gross total resection and bypass. Smaller arteries are more prone to injury than larger arteries. To dissect small arteries away from the tumor, microdissection should be attempted after finding an arachnoid plane.
Unexpected vascular anatomy. The skull base surgeon should thoroughly review preoperative imaging and have a low threshold to obtain additional vascular imaging such as cerebral angiogram.
Use of drills in proximity to major arteries during bony exposure. We avoid using a cotton patty in the vicinity of the drill to reduce the risk of inadvertent injury to adjacent vascular or neural structures.
Tumor resection with ultrasonic aspirators or laser. Use of less aggressive tips and low power settings in the vicinity of vascular structures can mitigate this risk.
Surgeon disorientation, especially in minimally invasive approaches. Use of image guidance can help orient the surgeon to the anatomy when needed.
5.5 Related Pathologies
A variety of skull base tumors can affect adjacent vascular structures. These include:
Meningioma: This is the most common skull base tumor with vascular involvement. Skull base meningiomas may encase large arteries including the ICA, MCA, ACA (anterior cerebral artery), VA, or BA and their branches. Intradural meningiomas which are virgin lesions usually maintain an arachnoid plane around the tumor which facilitates removal. However, perforators may still be difficult to dissect. Recurrent or progressive tumors after prior surgery and/or radiotherapy and higher grade virgin tumors (WHO grade 2 or 3 meningiomas) may show dense adhesion or invasion of adjacent vasculature making it difficult to dissect without injury to the artery. Extradural meningiomas can often be dissected away from encased arteries; however, when the artery is encased and narrowed this becomes difficult or impossible.
Schwannoma: Schwannomas very rarely encase arteries. However, dense adhesion to arteries may be seen, especially in previously operated or irradiated tumors, and could result in injury during dissection.
Chordoma and chondrosarcoma: Encasement of the ICA in the cavernous sinus is common. These tumors can usually be dissected free from adjacent arteries during the first surgery. Recurrent tumors are often densely adherent or invade the wall of the arteries and there is a high risk of vascular injury during operations for recurrent tumors.
Aggressive malignancies (e.g., squamous cell carcinoma, osteogenic sarcoma, adenoid cystic carcinoma): When tumor involves the ICA or the VA, arterial resection may be required for oncological reasons to achieve a clean margin.
5.6 Management Strategy
Arterial bypass may be necessary prophylactically or as a salvage strategy in various skull base tumors to reduce the risk of perioperative stroke. Preoperative assessment of vascular flow dynamics is imperative for skull base tumors adjacent to or involving major vascular structures. The ability of patient to tolerate occlusion of a major artery depends on the artery, collateral flow, and patient’s age.
5.6.1 Internal Carotid Artery
In our practice, even if the patient has good collaterals and tolerates balloon occlusion test (BOT), we usually reconstruct the parent artery to reduce the risk of recurrent long-term thromboembolic complications from the permanently occluded artery. This is based on our prior reported experience with ICA occlusion following balloon occlusion testing and cerebral blood flow studies. 13 We found that despite the presence of excellent collateral circulation during testing, ICA occlusion caused a major stroke in approximately 13% of the patients. 13 For this reason, we prefer to reconstruct all injured arteries when possible, regardless of the collateral circulation. However, exceptions may be made when the patient is younger than 50 years of age, the preoperative angiogram shows excellent sources of collateral flow, and there are no changes in somatosensory evoked potential (SSEP) and motor evoked potential (MEP) intraoperatively.
5.6.2 Vertebral Artery (VA)
Our preference is to not occlude the VA if possible. However, one VA can be occluded in the extradural portion (V2 or V3 segment) when it is the nondominant VA, the posterior inferior cerebellar artery (PICA) does not arise from the V2 or V3 segment, and the VA has good connection to the BA (i.e., it does not terminate as PICA).
5.6.3 Basilar Artery
An injured BA must always be reconstructed or replaced. The ability to tolerate temporary occlusion depends on flow through posterior communicating artery (PComA) collaterals, and on the presence of important perforating arteries in the temporarily occluded segment.
5.6.4 Middle Cerebral Artery
A significant stroke may occur after MCA occlusion either due to the failure of hemispheric collateral circulation or due to the occlusion of lenticulostriate perforating vessels leading to a capsular infarct. If the M1 segment of the MCA is damaged, direct suturing or an extracranial to intracranial bypass should be performed to revascularize the brain in an expeditious manner. When M2 or M3 segments of MCA are damaged, they can be reconstructed by direct suturing or by EC-IC bypass. If arterial injury is probable such as in recurrent or progressive tumors after prior surgery or radiation, then a bypass using the radial artery (RA) (first preference) or anterior tibial artery (ATA) may be performed as a first-stage surgery prior to tumor resection. Although the ATA has a larger diameter than the RA and therefore less incidence of spasm, RA is preferred over ATA because of ease of graft harvest. ATA is preferred over SV because the vein dilates upon exposure to arterial flow, thereby creating turbulence.
5.6.5 Anterior Cerebral Artery
If necessary, a nondominant ACA can be occluded in the A1 segment without risk of postoperative stroke, provided there is good flow through the anterior communicating artery (AComA) and major perforating arteries such as Heubner’s artery are not occluded.
5.6.6 Other Arteries
The PCA and smaller posterior circulation vessels such as anterior inferior cerebellar artery (AICA) and PICA may be reconstructed by direct suturing whenever feasible. If primary repair is not feasible, flow replacement in the basilar and PCA can be provided through a VA or ECA to P2 bypass preferably using a radial artery graft (RAG). For PICA injuries, given the tortuous nature of the vessel, an end-to-end anastomosis is usually attempted first. Alternative options depending on site of injury include side-to-side anastomosis (PICA–PICA, PICA–AICA), PICA reimplantation, occipital artery to PICA bypass, and vessel repair with short interposition graft utilizing occipital artery or RA.
In the case of tumor adherent to or invading small arteries supplying the brainstem or small perforators in the anterior circulation, it is safer to leave a small amount of residual tumor to reduce the risk of infarction.
In cases where the resection site has previously been operated upon or irradiated, or if there is encasement or narrowing of the vessel by tumor, the risk of an intraoperative arterial injury is high and preparation for a bypass may be necessary prior to initiation of tumor resection if preoperative imaging demonstrates lack of adequate collateral circulation. In the case of an unexpected arterial injury, the artery should always be reconstructed or replaced since the surgeon may not know the status of the collateral circulation. In these situations, obtaining adequate proximal and distal vascular control may be challenging.
5.7 Technical Considerations
Three different types of vessel reconstruction and replacement may be considered:
Direct suturing: This is usually performed using an 8–0 or 9–0 nylon suture. Direct suture repair is suitable for small arteries and small tears in larger arteries.
Local intracranial to intracranial bypasses: These can be of different types: (1) reimplantation of an artery via end-to-side anastomosis, (2) direct reconnection via end-to-end anastomosis or utilizing a short interposition graft, (3) side-to-side anastomosis (e.g., distal ACA–ACA, PICA–PICA, AICA–PICA). 14 Local bypasses may be suitable for reconstruction of small- or medium-sized arteries.
EC-IC bypass: The flow rate through an EC-IC bypass depends on baseline flow through the recipient and donor vessels and diameter of the bypass graft. EC-IC bypasses can be categorized as:
Low-flow bypass (<50 mL/min): These can be used for flow replacement of small- or medium-sized arteries where the demand is low, or for flow augmentation. Examples include STA–MCA and occipital artery (OA)–PICA bypasses.
Moderate-flow bypass (50–99 mL/min): These are typically used for flow replacement in the posterior circulation. An RAG is used as the bypass graft in moderate-flow bypasses. 15
High-flow bypass (>100 mL/min): These are typically used for flow replacement in the anterior circulation in situations of high demand (e.g., ICA replacement in a patient with poor collaterals). RAG is usually the preferred bypass graft followed by anterior tibial artery graft (ATAG) 16 or saphenous vein graft (SVG). 17
Very high flow bypass (>200 mL/min): Use of SVG, ATAG, or large diameter RAG may lead to a very high flow bypass. These bypasses are optimal for flow replacement of the ICA in patients who have absent collateral circulation through the ACom and PCom. A consideration with very high flow bypasses is that turbulent flow at the anastomotic site due to abrupt vessel diameter change, typically at the recipient vessel site, may promote graft thrombosis. Therefore, care should be taken to connect the graft to a large recipient vessel or an arterial bifurcation. Very high flow bypasses must be used with caution in patients with chronic ischemia due to the danger of postoperative hyperemia that could lead to hemorrhage or brain edema.
5.7.1 Technique of High-Flow Bypass
The surgeon, assistant, anesthesiologist, scrub nurse, circulating nurse, and neurophysiologist should all be familiar with their role in the operation and function smoothly as a team.
The patient is administered 325 mg Aspirin before the surgery in order to prevent graft thrombosis. If the patient is allergic to Aspirin, 75 mg clopidogrel may be used. Patient positioning depends on the location and type of pathology, and planned donor and recipient vessels. An arterial sheath should be placed if an intraoperative angiogram is being considered. Type of craniotomy and skull base approach is dictated by lesion location, size, expected pathology, and patient’s preoperative symptoms. A subcutaneous tunnel or an open graft channel is created to pass the graft from the intracranial to the extracranial space. With RAG or ATAG, a preauricular or postauricular channel that is superficial to the mandible may be used. With SVG, a postauricular channel is preferred if recipient vessel is the MCA so that the graft is oriented parallel to the sylvian fissure and the MCA prior to its entry into the cranium in order to reduce flow turbulence in the graft. If the recipient vessel is the supraclinoid ICA, then a preauricular channel is preferred for the SVG. A preauricular channel may be created by open dissection after connecting the neck and cranial incisions or via tunneling using a large-bore chest tube. For postauricular channels, we prefer to connect the cranial incision to the neck incision in a curvilinear fashion behind the ear and dissect the subcutaneous space down to the cranium. We also create a groove in the bone along the tunnel with the ultrasonic bone curette to allow more space for the graft to expand and to prevent compression by the skin.
The graft is extracted just prior to the anastomosis and prepared by flushing with heparinized saline followed by pressure distension. The pressure distension technique is very important to prevent postoperative vasospasm (usually occurring by day 3–5 postoperatively), and is utilized for arterial grafts. 15 The distal end of the graft is cut obliquely to create an oval opening and fish-mouthed by spatulation if needed. For bypasses using arterial or venous grafts, 3,000 to 4,000 units of heparin is administered intravenously. We perform the distal anastomosis first because it is technically easier to perform a deeper anastomosis with a mobile graft. Recipient arteries typically used in high-flow bypasses include M2 segment of the MCA, P2 segment of the PCA, supraclinoid ICA, or VA. For venous grafts, it is better to use an M1 or M2 bifurcation. A segment of the recipient vessel devoid of major perforators is identified and temporary clips are placed. The patient is placed in electroencephalographic burst suppression using Propofol, and systolic blood pressure is increased by 20% above baseline by the anesthesiologist prior to temporary clipping. The neurophysiologist should alert the surgeon and anesthesiologist about any changes in SSEP or MEP during clamping. If changes are seen, BP augmentation and expansion of the circulating blood volume via fluid or blood transfusion is performed as necessary. The temporary clip may also be released if possible. A marking pen is used to mark the side wall of the recipient vessel and distal end of the graft. A small arteriotomy is created in the recipient vessel and enlarged into an ovoid opening which is approximately one and a half to two times the recipient vessel diameter. The graft is preferably oriented at a 45-degree angle (donor to recipient) for an end-to-side anastomosis. Suture size depends on size of the vessels and typically 8–0 or 9–0 nylon sutures are used for intracranial vessels. Anchor sutures are placed at opposing ends of the arteriotomy. We prefer to use a running suture for the more difficult side and running or interrupted figure-of-eight sutures for the easier side. Special attention is needed to ensure that suture bites include the intima and media of the artery and are limited to one wall of the vessel. The graft is flushed with heparinized saline before tying the last suture. A temporary clip is placed on the graft and the temporary clips on the recipient artery are removed. The graft is then brought to the donor site via the previously created pre- or postauricular channel.
The donor artery may be the ECA, cervical ICA, V2 or V3 segment of VA, OA near the digastric groove, or, occasionally, STA just inferior to the zygomatic process, or the internal maxillary artery. The size of the donor vessel limits the volume of flow into the graft. An end-to-end or end (graft)-to-side (donor artery) anastomosis is performed. An end-to-side anastomosis is preferred when there is a significant disparity between diameters of graft and donor vessels. When an end-to-side anastomosis is performed, a vascular punch is utilized to create an oval opening in the donor artery, usually 3.5 to 4.5 mm diameter. The anastomosis is usually performed with 8–0 nylon or 7–0 Prolene sutures. Running sutures are used on one side and interrupted figure-of-eight sutures are used on the other side during anastomosis. The graft is placed on slight tension during anastomosis since both arterial and venous grafts expand on resumption of flow. This is especially important with venous grafts. RAGs are back bled to remove air prior to tying the last suture. With SVGs, air is removed through needle puncture or through a side branch since back bleeding is not possible. Temporary clips are opened proximally followed by the distal ones and the graft is inspected for leaks or kinking. Flow in the graft and the recipient vessel is then confirmed using a micro-Doppler probe and an indocyanine green (ICG) angiogram. Generally, the anastomosis time should be less than 45 minutes, and preferably less than 30 minutes. However, for PCA and SCA it can be as long as 50 minutes.
During closure, the dura mater is cut in a circular or cruciate fashion to allow free passage of the graft. The bone flap is subsequently replaced after an opening is created in it to accommodate the graft freely without a kink. The subcutaneous tissues and skin are then approximated. In the case of donor vessels originating in the neck, the neck is closed last. Flow through the graft is checked using micro-Doppler after each step during closure.
In addition to intraoperative Doppler sonography and ICG angiography, an immediate postoperative digital subtraction angiography (DSA) is usually performed to evaluate the entire graft to exclude any areas of significant stenosis or kinking, assess the flow rate, and visualize the distal circulation. If any problems are detected with Doppler sonography or ICG angiography intraoperatively, an intraoperative DSA or computed tomography angiography (CTA) using a portable scanner may be performed.
Postoperatively, Doppler sonography of the graft is performed every hour for the first 24 hours to monitor graft patency. Thereafter, we usually perform Duplex evaluation of the graft and assess flow daily for about 7 days. 18 Good diastolic flow is taken as an indicator of graft patency. Systolic flow is not a reliable indicator as it may be present with a nearly occluded graft. A sharp reduction in flow by 30% or more is a cause for concern and should be investigated with an urgent CTA. 19 Patients are administered Acetylsalicylic Acid = Aspirin 325 mg daily for at least 6 weeks with arterial grafts and lifelong with SVG. Long-term follow-up is performed with annual CTA or magnetic resonance (MR) angiography.
Although rare, problems may be encountered with grafts immediately during or after the procedure. These include thrombosis or other obstruction at either the donor or recipient anastomotic site, focal stenosis of the graft, and obstruction caused by the bone flap or subcutaneous tunnel. If an issue with the graft is detected in the immediate postoperative period, it is usually revised. If complete graft occlusion occurs in a more delayed manner and the patient is asymptomatic, no intervention is performed. If partial graft occlusion occurs, tissue plasminogen activator is administered into the graft after obtaining endovascular access. Despite pressure distention, graft vasospasm may still occur rarely and can be treated by endovascular angioplasty with a high-pressure balloon such as the Gateway® balloon. 20 , 21 The patient is administered dual antiplatelet therapy and heparinized during the endovascular procedure. Stenosis of the graft near the proximal or distal end has been noted occasionally during follow-up. Short segment (<1 cm) stenosis can be repaired with segmental resection and re-anastomosis. Longer segment stenosis can be treated with segmental resection and replacement with new donor interposition graft or by creating a Y-shaped construct with a new donor graft connecting an area of the existing bypass graft that is proximal to the stenosis to a new distal site on the intracranial vessel. 20