Introduction

The maintenance of adequate cerebral blood flow and perfusion may require cerebral revascularization in the face of occlusive disease or as a result of treatment for complex intracranial vascular lesions. With refined criteria and improvements in patient selection, cerebral revascularization has seen resurgence over the last decade. While the most commonly used bypass graft has been the superficial temporal artery (STA), some patients require a higher demand for blood flow, and therefore need a graft that can capacitate these increased needs. Flow requirements can be determined by balloon test occlusion (BTO). Sacrifice of a large parent artery, such as the internal carotid or vertebral artery, may necessitate a high-flow bypass graft, especially if there is minimal collateral reserve demonstrated by BTO. Ultimately, careful patient selection is the most important predictor of successful revascularization strategies. The most commonly utilized high-flow bypass grafts are the radial artery (RA) and the saphenous vein (SV). In this chapter, we discuss the indications and uses of the SV for high-flow augmentation in cerebral revascularization.

Indications for high-flow revascularization

Intracranial and extracranial occlusive vascular disease, can lead to progressive compromise of cerebral blood flow that may necessitate augmentation of cerebral blood flow. Trauma may result in loss or compromise of a major arterial supply to the brain and hence a need for revascularization. Further, as a greater number of complex aneurysm recurrences are seen after endovascular treatment, revascularization strategies have increased in importance. Treating these complex vascular lesions may require complex clip reconstruction techniques requiring extended temporary artery occlusion times or parent artery sacrifice. Lesions located on the M1 and P1 segments may require prophylactic bypass due to the frequent presence of perforating vessels and low tolerance of temporary occlusion in these territories. Further, many vascular lesions involve extensive atherosclerotic changes in the neck, very broad based, or giant in size, thus potentially necessitating branch or parent artery sacrifice. Finally, previously endovascularly treated vascular lesions may require complex vascular reconstructions at retreatment, that is, removal of coil mass, potentially demanding, long parent artery occlusion times. The choice of the anastomosis site is selected based on the location of the lesion, intended territory of revascularization, and properties of the donor and recipient vessels. BTO can facilitate decision making in most cases (Table 12–1). After temporary occlusion of a parent artery, the global cerebral hemodynamics are examined, with particular attention to the vascular reserve provided by the leptomeningial and circle of Willis vessels and subsequently the flow dynamics including venous washout are carefully studied.

Table 12–1 Balloon Test Occlusion Determination of Amount of Required Cerebral Blood Flow.

EEG, electroencephalogram; SPECT, single-photon emission computed tomography.

While angiographic study of the collateral circulation around a particular lesion is helpful, it does not provide a clinical assessment of the patient’s potential cerebral blood flow requirements. In order to determine clinically significant changes regarding the need for reserve flow, the BTO includes clinical examinations, electroencephalogram (EEG), hypotensive challenges with clinical examinations, and single-photon emission computed tomography (SPECT) imaging after performance of the BTO and removal of the balloon. Clinical exams are performed at baseline and every 5 minutes after balloon inflation. If the patient fails the BTO and develops deficits at normotension (120 to 140 systolic), then we feel the patient should undergo a high-flow bypass.

Saphenous vein considerations

The saphenous vein graft has been used for decades for bypass procedures with relatively great success. Lougheed is credited for performing the first intracranial bypass using a saphenous vein graft in 1971.¹ Despite an overall decrease in the use of intracranial SV bypasses due to an increased use of endovascular techniques for complex intracranial vascular disease and an increased experience and usage of radial artery grafts, the SV graft still provides a highly flexible and adaptable bypass graft for a variety of uses, including a primary conduit from the carotid artery or superficial temporal artery or as an interposition graft. The saphenous vein has a measured flow rate between 70 and 200 ml/min and an average diameter of ∼5 mm.^2,3 The advantages of the SV graft are the ease of harvest, autologous source, length of graft able to be obtained, absence of atherosclerotic changes throughout the length of the vessel, absence of vasospasm, and large caliber of graft able to be harvested. Several disadvantages of SV grafts exist and are most commonly frequent caliber mismatch between donor and recipient vessels, which can often lead to intraluminal turbulent flow and eventual thrombosis, the presence of valves that can be sites of thrombus formation, greater possibility of reperfusion hemorrhage, and the potential for kinking at the site of the recipient due to the thick surrounding tissue and vessel wall. Saphenous vein bypass grafts require two separate anastomosis sites and separate incisions for graft harvest, which increases the potential for complications. Although long-term patency rates have not been directly compared between RA and SV grafts, the average patency rate at 5 years postimplantation has been reported to be ∼90% for RA grafts and ∼80% for SV grafts. In the coronary literature, RAs have been consistently reported to have higher patency rates compared to SVs.^2–4

Patients undergoing revascularization procedures are usually placed on aspirin therapy before or immediately after the revascularization procedure. In cases of hypercholesterolemia, a statin can be administered pre- and post-operatively, which has been suggested to positively affect long-term graft patency.^2,3,5 All patients receive preoperative antibiotics within 1 hour prior to incision. The utilization of a neuroanesthesia team has several advantages during all phases of the procedure. Throughout the procedure—adequate cerebral perfusion is maintained adequate pharmacological brain protection, as well as optimal brain relaxation—which reduces the necessity of brain retraction. Postoperatively, controlled emergence, that is, avoidance of hypo- and hyper-tension, and rapid emergence from anesthesia are important so that an adequate neurological exam can be completed without compromising the bypass graft. Intraoperative neurophysiological monitoring is also performed, which includes EEG and somatosensory evoked potentials (SSEPs). Other neuromonitoring, such as brainstem-evoked potentials or cranial nerve monitoring, may be employed depending on the site of surgery and necessity of cranial nerve manipulation. Intraoperative graft patency monitoring can be assessed with ICG video-angiography, micro-Doppler ultrasound, or invasive intraoperative angiography via the femoral arterial rout or via direct cervical arterial puncture.

The patient is positioned with regard to the side of the lesion and the anastomosis site. For anterior circulation lesions, the patient is placed supine with the head turned to the opposite side of the lesion. The vascular grafts are often harvested from the opposite side of the lesion. For posterior circulation lesions, the patient is often placed in the lateral position.

Harvest and bypass procedure

The most common path of the greater SV is just anteromedial to the tibia at the ankle, and, toward the knee, it gradually travels more posterior. Vein mapping can be done with a macro-Doppler or ultrasound machine. In the lower thigh, the SV runs just posterior to the adductor tubercle where it then courses proximally along the lateral surface of the femoral artery. The caliber and shape of the SV is more uniform in the lower thigh and upper leg. At our institution, the dissection of the SV is often started near the ankle, due to its easy identity with ultrasound at this location. Some institutions prefer to harvest the vein from the upper leg using endoscopic techniques. The SV is normally harvested from the side opposite to the site of revascularization. Branches of the SV are ligated and divided as the dissection proceeds more proximally. Once the adductor tubercle is reached, the dissection normally ceases as the more proximal the dissection proceeds; the drainage of the thigh becomes more dependent on the femoral vein. The orientation of the SV graft is extremely important, as the presence of valves puts the graft at risk of thrombosis if placed in the incorrect orientation. As such, the distal end of the SV graft is marked with a suture to ensure the correct orientation. The graft is then removed and placed in a basin filled with heparinized saline. The adventitia, which can be thick, should be carefully removed with tedious and meticulous care. It is particularly important for adventitia to be removed at the anastomotic end, as the suture can become embedded and leave gaps where leakage sites can occur. The orientation of the graft should be reconfirmed by flushing saline through the graft and assessing ease of flow and directionality of valves. To assess the twisting of the graft, a blue ink line is place along the long axis of the SV. The SV graft is then maintained in a basin with heparinized saline until use.

It is important for the bypass procedure to flow efficiently. As such, the intracranial and cervical dissections are performed first. After the exposure of the bypass sites is completed, a subcutaneous tunnel for the bypass graft is made. A large clamp or Betcher is used to dissect a subcutaneous tunnel that runs just superior to the zygoma toward the intracranial or lateral incision, depending on the site for the anastomoses. The subcutaneous tunnel can be made in front or behind the ear, depending on the surgeon’s preference. The subcutaneous tunnel should be large enough to accommodate the graft during passage and without future risk of compression, and is often large enough if it can accommodate the fifth digit. A Penrose drain can be placed in the tunnel space until the graft is ready to be passed. To better accommodate the SV graft, a groove can be made in the zygoma so that bony compression is reduced and the cosmetic footprint on the face is improved. The graft can be passed through the tunnel with a suture attached to one end. The graft is then assessed for twisting by examining the blue ink line drawn along the graft.

The extracranial carotid anastomotic site should be able to accommodate an arteriotomy of at least 4 to 5 mm for the SV graft. Temporary clips are placed on either side of the target anastomotic site. The most common extracranial proximal anastomosis sites are the ICA, ECA, CCA, or VA. When the bypass is to the carotid circulation, the site of anastomosis is usually just distal to the superior thyroid artery on the ECA. The type of anastomosis is an end-to-side to the ECA using beveled ends sutured with a running Proline suture. Using 8- or 9-0 Proline, anchoring sutures are normally initially placed at each of the anastomotic ends, followed by a running 8- or 9-0 Proline. Running suture lines are acceptable as there is no need to compensate for bypass growth. Proline is a more suitable suture type since it is a monofilament and its strength is adequate for the thickness of the graft adventitial tissue. Braided suture is not recommended due to the likelihood of passing adventitial tissue into the suture line. Monofilament Proline suture passes through the graft tissue with less effort and with minimal damage to the graft. The contralateral side is usually sutured first. Since the SV graft is normally much larger than the recipient vessel, the amount of graft tissue will of course be greater than that of the recipient. As a result, the sutures in the graft should be placed with larger gaps than that of the recipient, which will result in an undulated graft. This ensures a more appropriate size-matched anastomotic site. Otherwise, tissue gaps may persist, which will lead to leakage along the suture line. After the contralateral wall has been completed, the suture line is examined for completeness and to ensure that no inclusion of the opposing arterial wall has taken place. The temporary clips are removed from the proximal parent vessel and a temporary clip is placed flush with the proximal anastomosis site. The graft is flushed with heparinized saline to clear the graft of residual blood or clots. The distal end of the SV graft is then positioned near the sight of the estimated distal anastomosis site and trimmed so that mild tension exists in the graft. The graft will often expand, sometimes significantly, after restoration of blood flow, and the intentional mild tension often prevents kinking at the distal anastomotic site. The patient is then systemically anticoagulated to prevent graft thrombosis and clotting during the proximal anastomosis. The arteriotomy in the proximal vessel should be slightly larger than the distal anastomosis site; approximately 6 to 8 mm. Temporary clips are placed on the target vessel around the anastomotic site. The same suture technique is used on the ipsilateral wall of the distal target vessel. Before the anastomosis is completed, the graft is again flushed with heparinized saline and redistended. A clip is then placed onto the SV graft at a site that is flush with the distal anastomosis site to prevent leakage and blood products from pooling in the graft. Subsequently, the proximal temporary clip is removed. After a final inspection of the graft and the anastomosis sites, including evaluation for suture line and kinking, the distal clip can be removed.

Assessment of bypass patency

Intraoperative assessment of bypass patency and functionality is paramount and can avoid complications due to premature graft stenosis or occlusion. While intraoperative catheter angiograms remain the gold standard, this technique requires additional costs and risks to the patient. Micro-Doppler assessment can provide qualitative assessments of flow and patency. Flow through the bypass graft can be nicely evaluated with indocyanine green (ICG) video angiography, which provides visual assessment of patency with little to no risk to the patient.² With this technique, direction of flow can be assessed, and, if the graft needs to be opened or revised, this technique can be performed multiple times to evaluate the graft.

The most common causes for acute graft failure are proximal stenosis or thrombosis at either anastomotic site. Stenosis is likely related to technical errors with the anastomoses. Thrombosis is likely a result of extended graft occlusion time while the distal anastomosis is being completed. If graft patency is not present, the bypass graft is then reopened at the proximal anastomotic site, flushed, and distended with heparinized saline. Once the bypass graft is patent, the graft is again distally clipped, filled with heparinized saline, and the proximal anastomosis is repeated. If clot or stenosis is still present, a 2F Fogerty balloon may be inserted into the graft, inflated, and then carefully pulled out of the graft, thus removing any residual clot within the graft. If adequate back-flow of blood occurs, then the proximal anastomosis is once again completed. If the graft continues to be clotted, the distal anastomosis must be examined using the same steps.

Complications

Cerebral revascularization with SV bypass grafts is more prone to complications than their low-flow counterparts. The most serious complication to avoid is reperfusion injury. The incidence of intracranial hemorrhage after autologous, including SV grafts, is approximately 10%.⁶ These patients have likely had long-standing cerebral perfusion deficits and as such, are likely dysautoregulated and at a higher risk for reperfusion hemorrhage. In addition, patients may be at risk for reperfusion injury from poorly controlled blood pressure or blood flow mismatch changes, especially after high-flow revascularization.^4,6–8 For these reasons, patients are monitored closely in the ICU setting and blood pressure is strictly controlled. Also, most patients requiring high-flow cerebral revascularization do not have vascular reserve, as demonstrated by BTO, so prolonged temporary occlusion times can often lead to territorial infarcts with and without changes in intraoperative neurophysiological monitoring. As such, temporary occlusion times should be minimized. That is, having an efficient and well thought out operative strategy as well as a well-executed plan is paramount. Thromboembolic complications can be encountered after bypass procedures from several different sources, namely the anastomotic sites, turbulent flow and thrombosis within the graft, alterations in intracranial hemodynamics, as well as residual parent artery vascular stumps. Preoperative antiplatelet medications as well as intraoperative anticoagulation can reduce these thromboembolic events. In a delayed fashion, SV grafts can undergo proatherogenic changes after implantation, which can also eventually lead to occlusion. Furthermore, other complications may involve the site of graft harvest, such as infection, lymphadema, or hematoma, or within the graft tunnel itself, such as hematoma. While these complications are very low, close attention should be rendered to the graft harvest site, as these complications can often be overlooked due to the focus on the cerebral manifestations of the revascularization procedure.

Postoperative considerations

It is of paramount importance to proactively minimize the potential for postoperative complications. Patients are normally maintained on antiplatelet, usually aspirin, therapy indefinitely and, depending on the patient’s mobility, on prophylactic doses of heparin beginning 24 to 48 hours postoperatively for deep venous thrombosis/pulmonary embolism prevention. Patients are usually monitored in the intensive care unit for at least 24 to 48 hours after revascularization. Blood pressure monitoring is strict and maintained at normopressure. Graft patency can be assessed after the procedure with Doppler, computed tomography angiography, or magnetic resonance angiography (MRA). Perfusion imaging can be used to assess the status of brain hemodynamics. Cerebral angiography can also be performed when there is concern for graft patency or for routine assessment. The advantage of invasive angiography is the ability to intervene if a problem with the graft is encountered. Follow-up imaging can be performed with MRA/MR perfusion or Doppler ultrasonography.

conclusion

Cerebral revascularization is necessary in some cases of complex vascular disease. High-flow cerebral revascularization can be successfully completed using harvested saphenous vein vascular grafts. Success is dictated by careful patient selection, meticulous surgical technique, thoughtful planning, vigilant peri-operative care, and mindful knowledge of the potential pitfalls and complications that can accompany cerebral revascularization procedures.