Tortuosity of the internal carotid artery (or loop) is generally defined as an S- or C-shaped elongation or curving in the course of the artery (Fig. 6.7a). Coiling is a term used to describe an exaggerated, redundant S-shaped curve, or a complete circle, in the longitudinal axis of the artery (Fig. 6.7b). Tortuosity and coiling are thought to be congenital developmental abnormalities that may become exaggerated with aging. They usually do not produce clinical symptoms.

Kinking is a sharp angulation with stenosis of segments of the internal carotid artery (Fig. 6.7c) and appears to be somewhat different than tortuosity and coiling. Kinking is less frequently bilateral and usually affects a few centimeters or more above the carotid bifurcation.

Poststenotic dilatation may be present. Frequently, an atherosclerotic plaque on the concave side of the kink further narrows the lumen.

Unlike tortuosity and coiling, kinking is thought to be an acquired abnormality, occurring mostly in older people in whom arteriosclerotic disease and hypertension are important factors. Changes in head and neck positions may produce cerebral ischemia in patients with carotid kinking, whereas tortuosity and coiling are usually asymptomatic.

Single stenotic lesions may or may not produce carotid ­territory symptoms (hemispheric) or vertebrobasilar territory symptoms (nonhemispheric). The collateral system comes into play when resistance in the stenotic major artery is greater than the resistance in the smaller circulative collateral channel. As stenosis becomes more severe and the collateral channel arteries dilate in response to increased flow, the collateral channels will increase flow up to the point of capacity. It can then be seen that the more proximal the obstruction, the greater the potential for collateral pathways to exist. Proximal occlusion of the arteries arising from the aortic arch is, therefore, rarely associated with the stroke syndrome because of this collateral flow. Branches of each subclavian artery may anastomose with collaterals of the opposite subclavian artery and the branches of the external carotid system.

The subclavian steal syndrome [23] occurs with proximal subclavian occlusion and retrograde flow down the vertebral artery (Figs. 6.8 and 6.9a). In innominate artery obstruction, the retrograde flow may be down to the carotid artery (Fig. 6.9b). Therefore, vascular surgeons may use the mechanism of collateral flow in a constructive manner; a patient who has both a carotid stenosis and subclavian steal syndrome may be completely relieved of steal ­symptoms by CEA.

An interesting collateral pathway is the retrograde flow that may occur in the external carotid system by proximal occlusion of the common carotid artery (Fig. 6.9c). Collateral flow to the internal carotid artery occurs by way of the ophthalmic artery or the circle of Willis. Patients with a proximal internal carotid occlusion might have blood flow up the external carotid artery and retrograde through the supraorbital and frontal arteries into the ophthalmic artery and, finally, antegrade in the distal internal carotid artery and the circle of Willis. This important pathway is the basis of the supraorbital Doppler cerebrovascular examination. Patients with proximal internal carotid occlusion and external carotid stenosis may be relieved of symptoms with correction of the external carotid occlusion, which alleviates symptoms of hypoperfusion [24]. Finally, emboli may course via the external carotid artery to the eye, producing amaurosis fugax in patients with a functional collateral pathway [25].

The major collateral pathway, of course, is the circle of Willis (Figs. 6.10 and 6.11). This unique circle provides the major pathway between the internal carotid, the external carotid, and the vertebrobasilar systems. The circle of Willis is anatomically complete in only one-third of patients, but it is physiologically adequate in around two-thirds of patients (Fig. 6.12). Collateral arteries between the occipital branches of the external carotid arteries may bypass stenosis of the origin of both vertebral arteries and the muscular branches of the vertebral arteries (Figs. 6.13, 6.14, and 6.15), or between the cervical branches of the thyrocervical trunk and vertebral arteries. Figures 6.16, 6.17, and 6.18 summarize the important collateral pathways in patients with an occluded internal carotid artery.

Numerous theories exist as to the mechanism by which atherosclerosis develops in the carotid arteries, but whether you prescribe to the mechanical, sheer stress, chemical injury, or infectious theory [26], the basic lesion is essentially the same. Atherosclerosis accounts for approximately 90% of extracranial cerebrovascular disease, with the remaining 10% being attributed to such disease processes as fibromuscular dysplasia, traumatic or spontaneous ­dissection, aneurysms, and arteritis, including Takayasu’s arteritis.

The pathology of carotid and vertebral artery atherosclerosis is similar to the process of atherosclerosis affecting coronaries and other arteries. The early stage of the lesion is initiated by intimal accumulation of lipoprotein particles which will undergo oxidative modification and elaborate cytokines that cause expression of adhesion molecules and chemoattractants; this will facilitate the uptake and migration of monocytes into the arterial wall. These monocytes become lipid-laden macrophages (foam cells) as a consequence of accumulation of modified lipoproteins and subsequently release additional cytokines, matrix metalloproteinases, and oxidants. This is followed by smooth muscle cell migration from the media to the intima. These will proliferate and elaborate extracellular matrix as extracellular lipid accumulates in a central core surrounded by a layer of connective tissue, which is called the fibrous cap, which in many advanced plaques becomes calcified. The atherosclerotic lesion initially grows in an outward direction; however, once advanced, it will grow inward and encroach on the lumen, causing stenosis.

These plaques occur preferentially at areas of vessel bifurcations, and the process is similar to that seen with coronary artery disease. It can begin in the bulbous portion of the internal carotid artery on its posterior lateral wall. The atherosclerosis appears as a fatty strip subintimally with a collection of fat cells that progresses to a fibrous plaque in the subendothelial layer, causing gradually decreasing flow. These plaques can enlarge in several ways. They may just continue to slowly enlarge from an accumulation of cholesterol and fibroblasts, leading to a central necrosis and rupture of the intimal lining of the vessel. This will lead to discharge of atheromatous debris into the lumen of the vessel, which can embolize. The exposed necrotic core of the lesion can then become a nidus for platelet deposition and further embolization to the brain. Progressive accumulation of the arteriosclerotic process, often with thrombotic debris, may result in stenosis or total occlusion in the carotid artery, with subsequent thrombosis of the internal carotid artery distal to the lesion (Fig. 6.19). Another mechanism by which there may be sudden plaque enlargement is intraplaque hemorrhage [27], which may produce acute narrowing of the lumen. If the intima overlying the site of the plaque hemorrhage ulcerates, the necrotic contents of the atheromas escape into the lumen and cause cerebral embolization with transient ischemic attacks (TIA) or cerebral infarcts. Nonulcerated lesions may alter flow and produce mural thrombi, which may fragment, causing embolization (Fig. 6.20). The friability of these lesions is often not appreciated until seen by the vascular surgeon (Fig. 6.21).

Blaisdell et al. [28] and Hass et al. [29] studied the distribution of the atherosclerotic lesions involved in cerebrovascular disease and found that approximately one-third of responsible lesions that were surgically inaccessible occurred in the intracranial distribution. The remaining two-thirds of the lesions were in extracranial locations.

The common carotid bifurcation and the proximal internal carotid artery account for 50% of the lesions. Vertebral artery lesions account for 20%, left subclavian arterial lesions account for 10–15%, and lesions of the innominate and right subclavian arteries account for 15%; and more than one lesion may be present (Fig. 6.22).

Generally, the most common cause of cerebral ischemic events is embolic phenomena, primarily arterial in origin (carotid) and secondary to cardiac sources. The irregular plaque surface produces turbulence, which will act as a stimulus for platelet aggregation. If the platelet aggregates become large enough and embolize to an important vessel in the brain, symptoms will occur. If the platelet aggregates break up quickly from mechanical forces or from the effect of arterial prostacyclin, the symptoms will be transient, i.e., TIAs. If the embolic fragment persists, however, it can lead to focal infarction (Fig. 6.23). As noted in Fig. 6.24, the end result of the atherosclerotic plaque might be an internal carotid artery thrombosis. When an arteriosclerotic plaque expands to produce a critical reduction in blood flow, the vessel will ultimately undergo thrombosis. In the case of the internal carotid artery, this column of thrombus stops at the ophthalmic artery and remains stable, and if there is sufficient collateral circulation via the circle of Willis, the thrombotic event may be entirely asymptomatic (Fig. 6.24). However, if small thrombi rather than a thrombotic column form and are subsequently carried to the intracranial vessels by continuous blood flow, then the patient will experience cerebral symptoms that can vary from transient amaurosis fugax or hemispheric events to a profound hemiplegia, depending upon the extent of the propagated thrombus or embolus (Fig. 6.25). In addition, if the collateral circulation to the circle of Willis is inadequate, the sudden loss of blood flow through a diseased internal carotid artery may induce a sudden drop in flow to the cerebral hemisphere, resulting in ischemic infarction as a consequence of inadequate proximal blood flow.

A less common cause of cerebrovascular ischemia is fibromuscular dysplasia (FMD), which is usually more distally located in the internal carotid artery. The most common form of this disease is characterized by hyperplasia of the media producing alternating bands of thinned areas, leading to a beady appearance on angiography. Often, the internal carotid artery is involved at long lengths. Always look for evidence of fibromuscular dysplasia elsewhere. It will involve both internal carotid arteries in 65% of patients [30].

It has been stated that a 70–80% reduction of the cross-sectional area of the arterial lumen must be present to produce a hemodynamically significant drop in the usual flow rate in the cerebrovascular system [31]. However, this may not always be the case. Important mechanisms of collateral flow and hemodynamic events that decrease cardiac output or systemic blood pressure, such as postural hypotension and cardiac arrhythmia, may produce transient episodes of ischemia. Embolization has been a documented cause of TIAs by proven ophthalmologic examination. Intraluminal particles of platelet fibrin aggregates, cholesterol fragments, and small clots have been noted. Most TIAs are probably caused by this mechanism. There is a permanent neurologic deficit as a result of permanently disrupted flow. A pale infarct occurs with focal cell necrosis and cerebral softening. The blood vessels lose integrity at the periphery of the infarct at a relatively ischemic spot. However, where neural death has not occurred, neurologic function may be altered and blood flow, while slow, may still be present.

The following well-defined syndromes of cerebrovascular ischemia have emerged: