Introduction

Surgical treatment of cerebrovascular disorders with cerebral revascularization procedures has remained a formidable task for neurosurgeons for centuries. Despite remarkable advances in medical management and noninvasive procedures, cerebrovascular revascularization with extracranial-intracranial (EC-IC) bypass procedures has withstood the test of time and continue to represent the mainstay for various neurovascular pathologies. These procedures are generally divided into flow replacement or high-flow and flow supplementation or low-flow EC-IC bypass, and this chapter will use this subdivision. Careful patient selection and adequate preoperative imaging have proven to be the best indicators of bypass graft patency.

History of Cerebral Bypass

Vascular procedures have their origins in the 2nd century AD with Antyllus performing ligature of the popliteal artery for treatment of popliteal aneurysms. John Hunter helped clinicians gain an understanding of collateral flow with his ligatures for treatment of popliteal aneurysms, and this procedure became known as the Hunterian ligature. The history of cerebrovascular bypass techniques dates back to 1964 with the first attempt comprising the use of a plastic tube as a shunt between the superficial temporal artery (STA) and the anterior cerebral artery (ACA) for treatment of an ACA aneurysm by Pool and Potts. Unfortunately, the shunt failed after postoperative thrombosis, but this inspired others to search for feasible bypass methods. Using microsurgical techniques learned in the lab of R.M. Peardon Donaghy and the invention of 9-0 nylon sutures, Yasargil performed the first successful STA–middle cerebral artery (MCA) bypass on a dog in 1966. The following year, he performed this procedure on a patient with chronic carotid artery occlusion. He published his series in 1970, quickly popularizing this surgical technique. The use of other external carotid vessels and in situ bypass options were popularized over the following decade.

Bypass procedures were considered the sine qua non for the treatment of a plethora of neurovascular diseases until 1985, when the results of the Cooperative Study on EC-IC bypass trial were published in the New England Journal of Medicine, raising questions about the efficacy of bypass procedures for treatment of occlusive neurovascular disease. The trial compared bypass surgery plus best medical care to best medical care in patients with internal carotid artery (ICA) or MCA occlusive disease. Nonfatal and fatal strokes occurred both more frequently and earlier in patients who underwent surgery. The use of bypass procedures diminished dramatically, but the trial was criticized for including patients who did not require surgery as determined by cerebral blood flow (CBF) imaging. CBF imaging for determining failed cerebral autoregulation was not widely available at the time of the trial. The Carotid Occlusion Surgery Study (COSS) trial was designed to assess whether EC-IC bypass combined with the best medical management would decrease the rate of ipsilateral stroke in patients with symptomatic ICA occlusion. This trial had improved selection criteria as patients had to have increased oxygen extraction fraction (OEF) as confirmed by positron emission tomography (PET). The COSS trial randomized 98 patients to medical treatment and 97 to the EC-IC bypass, of which 93 had surgery. The 2-year stroke rate in the medical group was 22.7% and in the surgical group was 21%. Although the trial was subjected to significant criticism, especially in regard to the methodology for PET inclusion criteria, the use of EC-IC bypass for carotid occlusions has not gained popularity. Therefore, in light of the controversial results of the EC-IC bypass trial and the COSS trial, the current use of bypass procedures is mainly for treatment of complex unclippable intracranial aneurysms or moyamoya disease and for select patients with occlusive cerebrovascular disease who fail medical management. ,

Indications

Moyamoya Disease

Moyamoya disease is characterized by progressive occlusion of large intracranial vessels, namely, the distal ICA and proximal ACA and MCA. Over time, a collateral network of fragile vessels forms to supply the ischemic areas and appears as a “puff of smoke” on angiography. The pathophysiology of moyamoya disease was first described in Japan in the 1960s. Patients commonly present with ischemic symptoms or intracranial hemorrhage from the fragile collateral vascular network. Hemorrhagic presentations are more common in Asian adults, whereas ischemic presentations are more common in North American adults. Revascularization procedures have been shown to improve long-term outcomes in patients with moyamoya disease. ,

The Japanese Adult Moyamoya Trial was a multicenter, prospective, randomized, controlled trial, which randomized patients with hemorrhagic presentation to surgical management with low-flow bypass or nonsurgical management with blood pressure control. The study found that the surgical group had a significantly decreased rate of rebleeding (3.2%/y vs. 8.2%/y; P = .048). Common revascularization procedures for moyamoya include direct revascularization with STA-MCA bypass and indirect procedures with encephaloduroarteriosynangiosis (EDAS), encephalomyosynangiosis (EMS), and omental flaps. Indirect procedures are preferred in children, whereas direct and combined (direct and indirect) procedures are preferred in adults.

Cerebrovascular Occlusive Disease

Chronic cerebrovascular occlusive disease leads to decreased parenchymal perfusion. With progression of the occlusive disease, there is an increase in the OEF and development of collateral circulation. When the collateral perfusion fails to match the parenchymal oxygen requirements, ischemic manifestations occur. Medical management of intracerebral occlusive disease (ICOD) includes administration of antiplatelets, anticoagulants, and cholesterol medications with management of risk factors such as hypertension, lifestyle, physical activity, and diet. Surgical options for patients refractory to maximal medical therapy are somewhat limited, because original attempts at intracranial endarterectomy were largely unsuccessful and revascularization procedures are used sporadically for ICOD.

The COSS was a multicenter, randomized controlled trial designed to determine whether EC-IC bypass surgery combined with maximal medical therapy reduces the rate of ipsilateral stroke in patients with ICA occlusion and hemodynamic cerebral insufficiency confirmed with PET. The trial was terminated at 2 years despite excellent bypass graft patency (98% at 30 days) and improved cerebral hemodynamics. STA-MCA anastomosis did not provide an overall benefit regarding ipsilateral 2-year stroke recurrence, mainly because of a much better than expected stroke recurrence rate (22.7%) in the medical group but also because of a significant postoperative stroke rate (15%). , The Japanese EC-IC bypass trial (JET) was designed to determine whether STA-MCA bypass with maximal medical therapy is superior to maximal medical therapy alone in patients with recently symptomatic cerebral ischemia from chronic ICA or MCA stenosis with hemodynamic instability using single-photon emission computed tomography (SPECT) scanning combined with acetazolamide combined to measure CBF and cerebrovascular reactivity (CVR), which represent the degree of hemodynamic failure. , The study found that bypass improved the 2-year outcome in these patients but was never published in a peer-reviewed English journal. The JET-2 study was then performed and revealed that patients with CBF greater than 80% or CVR greater than 10% have low rates of recurrent stroke and are unlikely to benefit from EC-IC bypass. In summary, studies published for cerebrovascular occlusive disease showed no benefit of bypass over medical management. The Carotid and Middle Cerebral Artery Occlusion Surgery Study (CMOSS), is underway in China, which may provide further insights into the role of bypass for atherosclerotic disease ( ClinicalTrials.gov ; NCT01758614 ).

Intracranial Aneurysms

Bypass procedures have been used in the surgical management of complex intracranial aneurysms. Despite low evidence (level 3) and lack of randomized trials validating the value of bypass procedures, they are particularly useful when sacrifice of a parent vessel or reconstruction of a major branch is required for repair of complex aneurysms. The advent of endovascular techniques with stent assisted coiling and flow diversion had decreased the number of open surgical procedures for complex aneurysms. However, the role of bypass surgery remains essential for management of certain complex aneurysms with critical branches arising from the dome or the neck. In addition, giant aneurysms are often well suited for treatment with bypass when there is need for decompression to alleviate mass effect.

Skull Base Tumors

Bypass techniques have been used liberally for complex skull base tumors encasing large intracranial vessels to achieve complete resection with flow replacement using saphenous vein or radial artery grafts. For tumors invading the ICA, vascular sacrifice may be necessary as further tumor spread will likely compromise the involved vessel. Interposition grafts have been used from cervical to petrous and supraclinoid ICA for paragangliomas and skull base tumors surrounding the carotid. , The advent of radiosurgery has led to declining use of bypass for complete resection of tumors that encase medium to large intracranial vessels, as tumor remnants can be safely radiated with reasonable outcomes. When planning surgical resection of lesions involving large vessels, BTO is helpful for determining the safety of vascular sacrifice and the need for bypass. Patients with symptoms of hypoperfusion during BTO of the ICA usually require sparing their carotid or blood flow replacement with bypass.

Need for Bypass and Type of Bypass

Bypass can be divided in two main categories, namely, flow replacement and flow augmentation. Another traditional classification has been used based on the flow of the bypass and divides these procedures into high versus low flow. The type of bypass required in tumor or vascular procedures is usually determined by the diameter and flow of the involved vessel and presence of distal collaterals, which can be determined by vascular imaging and quantitative flow measurements. Although patients may tolerate vessel sacrifice when the tumor has occluded the involved vessel, some cases can present with delayed neurologic deficits (5% to 22% morbidity following parent vessel sacrifice after BTO). Origitano et al. reported a cohort of patients with 22% (4/18) delayed (>72 h) ischemic events despite vascular assessment including angiogram with manual carotid compression testing, transcranial doppler evaluation, xenon-133 ( 133 Xe) CBF studies, and SPECT compression studies.

Radiographic BTO can elucidate the individual need for bypass for flow replacement before vessel sacrifice. This can be determined by angiographic visualization and analysis of the distal territory and its collateral vascular supply for the involved vessel. BTO is performed with a balloon catheter positioned within the affected vessel as close as possible to the lesion and the balloon is inflated to achieve flow arrest. Collateral circulation can be evaluated by angiographic visualization of collateral flow with injection of contrast in the contralateral ICA or the dominant vertebral artery (VA). This can be done in patients under general anesthesia with neuromonitoring or with analysis of blood flow and response to the acetazolamide challenge test. Alternatively, it can be done in awake patients using the Matas maneuver (angiography of the nontested ICA during manual carotid compression on the tested side) and the Allcock maneuver (angiography of the VA during manual carotid compression on the tested side) with analysis of angiographic images for visualization of the ACA and the MCA on the tested side by the cross flow. A baseline clinical exam is performed prior to occlusion and the patient undergoes serial neurologic testing when this is done awake to evaluate patients who may require revascularization to protect them from delayed ischemic stroke. We prefer using awake clinical testing, and, in our experience, patients who tolerate BTO over 20 to 30 minutes with hypotensive challenge, where mean arterial pressure is reduced by 20%, tolerate vessel sacrifice fairly well without need for a bypass. Other means of assessment include measurement of stump pressure distal to the occlusion using the balloon catheter before, during, and after the balloon occlusion include electroencephalography (EEG), PET, and SPECT imaging. Patients who fail immediately after balloon occlusion, as determined by changes on neurological exam, and patients with SPECT abnormalities noted after the procedure will likely need a high-flow bypass. Patients who have mild neurological changes noted after hypotensive challenge might be considered for low-flow or small vessel bypass to supplement the flow.

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