Relevance of External Carotid Artery Disease in Internal Carotid Artery Occlusion

Internal carotid artery (ICA) occlusion has long been thought to carry a poor prognosis despite what is often an asymptomatic presentation. However, increasing recognition of segmentation based on cerebrovascular imaging and/or perfusion monitoring techniques, clinical status of initial presentations, and associated extracranial and intracranial vascular disease, has indicated a heterogeneous population that must be approached thoughtfully to understand the prognosis and determine the optimal treatment strategy.

Prospective studies of patients with known ICA occlusions suggest a delayed stroke rate approaching 25% within 2 to 3 years. Some recent data suggest annual stroke rates of 2.4%, but aggregate vascular events including retinal symptoms and limb-shaking transient ischemic attacks (TIAs) were observed at an annual rate of 6.4%. In patients with compromised cerebrovascular reactivity (CVR), stroke rates can approach 10% to 14% annually versus 4% to 6% in patients with preserved CVR.

The mechanism of acute stroke after ICA occlusion is typically embolism to the middle cerebral artery (MCA) circulation, thrombus extension past the ophthalmic artery into the circle of Willis, or hemodynamic insufficiency in association with either an isolated hemisphere or diffuse extracranial cerebrovascular disease. Stroke at an interval following ICA occlusion may be caused by similar mechanisms but can also arise from a diseased external carotid artery (ECA) or embolization from a remnant ICA cul-de-sac containing thrombus and/or platelet or fibrin debris. In either case, turbulent flow at the carotid bifurcation can sweep atheroembolic material into the intracranial vasculature through external carotid collaterals.

The ECA can serve as the major cerebral collateral in the setting of ICA occlusion, and a proximal ECA stenosis can have a hemodynamic impact on cerebral perfusion. Studies have demonstrated that the ECA contributes to cerebral blood flow compensation in up to 80% of patients with a symptomatic ICA occlusion. The increasing importance of focal contributions to cerebral ischemia, rather than hemispheric-based patterns, has also been emphasized, noting the ECA contributions can substantially lower risks associated specifically with compromised collateral beds. In addition, preserved MCA collateral flow, regardless of the source of collaterals (which can emanate from the ECA and be identified as such), is associated with a significantly improved prognosis in patients with acute stroke caused by ICA occlusion as is the preservation of leptomeningeal collaterals. In addition, several studies have demonstrated improvement in cerebral perfusion following restoration of ECA hemodynamics to normal.

Anatomy of Cerebral Collateral Circulation

Although cerebral collateral blood flow can depend on contralateral intracranial supply and/or basilar artery blood flow from either or both vertebral arteries, it is important to recognize that the circle of Willis is incomplete in as many as 60% of patients. The ECA can provide significant ipsilateral collateral blood flow, but it can also be a source of significant-sized collaterals through which atherosclerotic debris can reach the intracranial vessels.

Adult cerebral collateral arterial branches have been categorized by Alksne into large interarterial connections, intracranial–extracranial connections, and small interarterial anastomoses. Other rare collateral vessels are based on persistent trigeminal and hypoglossal arteries, which provide carotid basilar connections.

The ECA serves as a major extracranial arterial collateral primarily through periorbital branches. Periophthalmic channels depend on the superficial temporal, angular, middle meningeal, and infraorbital arteries. Vertebral collateral is provided through the occipital branch of the ECA as well as the costocervical trunk and the contralateral vertebral artery, which communicates at the level of the intervertebral foramen. Perimeningeal, stylomastoid, and anterior tympanic branches of the ECA can all provide collateral channels of varying degrees of significance ( Figure 1 ).

Methodology of grading ECA collateral flow through digital subtraction arteriography is well described. Categories include grade 0 (no filling of the ophthalmic artery), grade 1 (filling of carotid siphon), and grade 2 (filling of anterior or middle cerebral artery).