Intracranial arterial stenoses: current viewpoints, novel approaches, and surgical perspectives

Abstract

Ten percent of all strokes occurring in the USA are caused by intracranial arterial stenosis (IAS). Symptomatic IAS carries one of the highest rates of recurrent stroke despite intensive medical therapy (25 % in high-risk groups). Clinical results for endovascular angioplasty and stenting have been disappointing. The objectives of this study were to review the contemporary understanding of symptomatic IAS and present potential alternative treatments to resolve factors not addressed by current therapies. We performed a literature review on IAS pathophysiology, natural history, and current treatment. We present an evaluation of the currently deficient aspects in its treatment and explore the role of alternative surgical approaches. There is a well-documented interrelation between hemodynamic and embolic factors in cerebral ischemia caused by IAS. Despite the effectiveness of medical therapy, hemodynamic factors are not addressed satisfactorily by medications alone. Collateral circulation and severity of stenosis are the strongest predictors of risk for stroke and death. Indirect revascularization techniques, such as encephaloduroarteriosynangiosis, offer an alternative treatment to enhance collateral circulation while minimizing risk of hemorrhage associated with hyperemia and endovascular manipulation, with promising results in preliminary studies on chronic cerebrovascular occlusive disease. Despite improvements in medical management for IAS, relevant aspects of its pathophysiology are not resolved by medical treatment alone, such as poor collateral circulation. Surgical indirect revascularization can improve collateral circulation and play a role in the treatment of this condition. Further formal evaluation of indirect revascularization for IAS is a logical and worthy step in the development of intracranial atherosclerosis treatment strategies.

Conflict of interest statement

Conflict of interest None

Figures

Fig. 1

Pathophysiology of intracranial atherosclerosis. A The endothelial injury and increased permeability induced by factors such as hypertension and smoking generates adhesion of monocytes and lymphocytes to the disrupted vessel lining, followed by migration beneath the endothelial surface and cellular aggregation in the subendothelial tissue. Macrophages take up lipid, forming foam cells, and these and other macrophages are activated and cytokines and growth factors are released, leading to smooth muscle cell migration and proliferation. B There is formation of a fibrous cap that covers a mixture of leukocytes, lipid, and necrotic tissue. Eventually the fibrous cap ruptures and ulcerates generating platelet aggregation and embolus formation. C The early endothelial injury generates disturbances of the laminar flow, which creates flow separation and oscillatory shear stress. This precipitates a cycle of further endothelial and arterial wall damage. Stenosis of the vessel lumen, in concert with embolus generation, produces strokes in a complementary occurrence of hypoperfusion and embolism (D)

Fig. 2

Collaterals in moyamoya disease. Lateral angiogram after common carotid injection in a 46-year-old female with advanced moyamoya disease, Suzuki stage 6. The internal carotid artery (ICA) is completely occluded above the origin of the ophthalmic artery (empty black arrow). Moyamoya lenticulo-striate vessels are regressing (arrowhead) and the cerebral circulation depends exclusively on collaterals. There are spontaneous transosseous anastomoses from the anterior branch of the superficial temporal artery (STA) to frontal cortical vessels (white arrow), anterior meningeal branches (black arrow) from the ophthalmic artery, and the middle meningeal artery (MMA) to the pericallosal and callosomarginal arteries in the parietal region (empty white arrow)

Fig. 3

Flow changes associated with EC-IC bypass. A qualitative depiction of flow patterns in intracranial stenosis with reduction of flow velocities associated with arterial narrowing before the stenosis and acceleration of flow in the stenotic segment. Distal flow can reach critical low velocities (blue and black arrows). After bypass placement, a theoretical competitive flow introduced by the bypass on the post-stenotic arterial segment can precipitate increased turbulence, stasis of flow and thrombosis of adjacent perforators, and the stenotic segment itself

Fig. 4

Post-EDAS development of collaterals. a, b Anteroposterior and lateral preoperative angiograms on a 62-year-old female post-angioplasty and stenting of atherosclerotic stenosis of the cavernous left internal carotid artery, who developed re-stenosis of the treated segment and additional tandem stenosis of the petrous ICA and left MCA (black arrows). c Capillary phase angiogram demonstrates a significantly reduced area of the MCA territory being perfused by the left ICA injection. d Six months post-EDAS, lateral angiogram of the external carotid artery (ECA) demonstrates multiple new collaterals developed from the superficial temporal artery (black arrows) and the middle meningeal artery (white arrows) with direct anastomosis to the MCA and cortical blush in the MCA territory. e Capillary phase of left ECA angiography demonstrates a significant contribution to the irrigation of the left MCA territory by the new collaterals from the ECA branches. f Composite image of the postoperative ECA capillary phase (black outline) supraimposed on the preoperative ICA injection (white outline) demonstrates complementary development of collaterals in the preoperatively hypoperfused cortical MCA territory