Cranial nerve palsy in spontaneous dissection of the extracranial internal carotid artery

Spontaneous dissection of the internal carotid artery (ICA) is now recognized as one of the common causes of ischemic stroke in younger patients. The annual incidence of symptomatic ICA dissection is more than equals 2.6/100,000. ^[1] Because some ICA dissections may either be asymptomatic or cause minor transient symptoms that are not reported by the patient, the actual incidence of the disease is likely even higher.

With progress in neuroimaging techniques and with more widespread availability of these diagnostic methods, more patients with ICA dissection are identified and a wider spectrum of clinical presentations of these dissections is recognized. ^[2] In an overwhelming majority of patients, the dissection involves the extracranial segment of the ICA and only infrequently does it extend to the intracranial segment of the artery or involve only the intracranial segment. ^[3]

The common clinical presentations of ICA dissections are hemicrania and ipsilateral oculosympathetic palsy or hemicrania and delayed focal cerebral ischemic symptoms (stroke or transient ischemic attacks). Sometimes the two syndromes coexist, with one predominating the clinical picture. Additional manifestations such as neck pain, amaurosis fugax, subjective or objective bruits, dysgeusia, or cranial nerve palsies may occur, but they are less frequent. Spontaneous dissections of the ICA may present as stroke, transient ischemic attacks, or amaurosis fugax with or without headache, bruits, or oculosympathetic palsy. Sometimes the only symptom is hemicrania or a bruit.

Earlier work documented that dysgeusia occurred in some patients with ICA dissection. ^[4] This was attributed to involvement of the chorda tympani nerve. Later, involvement of the hypoglossal nerve and other lower cranial nerve palsies associated with ICA dissections were reported. ^[5-7] With increased awareness of the disease and with increasing reports of cases and series, more cases of cranial nerve palsies in ICA dissections have been reported, including trigeminal nerve palsy. ^[8-22] Two fairly distinct syndromes of cranial nerve palsies are recognized in association with ICA dissection. Usually, but not always, other clinical manifestations of ICA dissection also are present. These include a syndrome of lower cranial nerve palsies ^[15] and a syndrome of ocular motor palsies. ^[20] In the syndrome of lower cranial nerve palsies, cranial nerve XII is almost invariably involved. Other lower cranial nerves (IX, X, and XI) also may be involved--all of them or any combination. ^[15]

The objective of this study was to characterize cranial nerve palsies in spontaneous dissections of the extracranial ICA and to determine the frequency of such palsies among patients who present with ICA dissections.

Methods.

Medical records of all adult patients with spontaneous dissections of the cervical ICA who were seen at the Mayo Clinic from 1970 through 1993 were studied. All patients had neurologic evaluation and had been seen by at least one staff neurologist. Most patients had been seen by a staff neurosurgeon. The diagnosis was confirmed with cerebral angiography in all but eight patients, in whom the diagnosis was made with MRI and magnetic resonance angiography only. Patients with simultaneous or concomitant ICA and vertebral artery dissections and those with intracranial dissections or intracranial extension of dissection were excluded from the study. Of the 190 patients identified, 99 were men and 91 were women. Age at onset ranged from 18 to 76 years (mean 45.5 years). ICA dissection was unilateral in 155 patients and bilateral in 35 patients (18%). The dissections involved 225 ICAs.

Results.

Cranial nerve palsies were noted in 20 patients; additionally, 3 patients had dysgeusia without other cranial nerve involvement presumed to be due to involvement of the chorda tympani nerve. Of these 23 patients, 7 were women and 16 were men, their mean age was 51.5 years (range 35 to 76 years). The clinical details on these patients are summarized in the Table 1. Cranial nerve XII was the most frequently involved cranial nerve in ICA dissections--in 10 of the 23 patients (43%) and in more than 5% of all the patients with ICA dissections. Cranial nerve V was the second most frequently involved cranial nerve--in 7 of the 23 patients (30%) and in 3.7% of all patients with ICA dissections. Cranial nerves IX and X were each involved in six patients, and cranial nerve XI was involved in five patients. Cranial nerves III and VI were each involved in two patients, and involvement of cranial nerves IV and VIII was noted in one patient each. One patient with flame-like occlusion of the ICA above the bifurcation had ischemic optic neuropathy without evidence of emboh or retinal ischemia.

In one patient with isolated cranial nerve XII palsy, cranial nerve involvement was the only manifestation of the ICA dissection. Headache was present in all but four patients (83%); it was unilateral in all but two patients. In six patients, a syndrome of hemicrania plus ipsilateral cranial nerve palsy was the sole clinical manifestation of the ICA dissection. Oculosympathetic palsy was noted in 13 patients (56%). In one patient, oculosympathetic palsy and an ipsilateral palsy of cranial nerve XII were the only manifestations of the ICA dissection. Cerebral ischemic symptoms (transient ischemic attacks or stroke) were noted in four patients. One of these patients also had an episode of amaurosis fugax.

A distinct syndrome of lower cranial nerve palsies with invariable involvement of cranial nerve XII with or without additional involvement of cranial nerve IX, X, or XI appeared to be a notable mode of presentation of ICA dissection. This syndrome is frequently associated with an ipsilateral headache (60% of the cases of this series) and oculosympathetic palsy (40% of the cases in this series). Overall, more than 5% of ICA dissections presented with this syndrome of lower cranial nerve palsies, which was often, although not always, associated with an ipsilateral headache.

A syndrome of ocular motor palsies was present in five patients (overall, in 2.6% of the patients with ICA dissections), consisting of involvement of cranial nerve III in two patients, cranial nerve VI in two patients, and cranial nerve IV in one patient. All five patients had headaches (hemicranial in four). In four patients, headache and ocular motor palsies were the major manifestations of the ICA dissection. One of these patients had ipsilateral trigeminal nerve involvement, and two patients had additional oculosympathetic palsy.

Seven patients had involvement of cranial nerve V. A syndrome of hemicrania and trigeminal nerve involvement and oculosympathetic palsy was noted in four patients (more than 2% of all patients with ICA dissections).

Discussion.

A recently identified clinical presentation of ICA dissection is single or multiple cranial nerve palsy. This may occur as an isolated phenomenon but is often noted in conjunction with other manifestations of ICA dissection, such as hemicrania, oculosympathetic palsy, focal cerebral ischemic symptoms and signs, or bruits. It is always ipsilateral to the ICA dissection. If additional cerebral ischemic manifestations develop in the distribution of the ICA involved by dissection, such as contralateral hemiparesis or sensory manifestations, the clinical picture may then resemble a brainstem dysfunction. This false localizing sign ^[22] may draw attention to the vertebrobasilar circulation, whereas the pathologic process is in the ICA circulation. When present, additional manifestations, such as anterior hemicrania, oculosympathetic palsy, or carotid bruits, are helpful in establishing a correct diagnosis clinically.

Of interest is the mechanism of cranial nerve involvement in ICA dissection. Many of the reports on ICA dissection associated with hypoglossal palsy or palsy of lower cranial nerves have attributed the palsy to the mechanical compression or stretching of the lower cranial nerves below the jugular foramen by the expanded or aneurysmal ICA involved by dissection. Below the jugular foramen, in the retrostyloid and posterior retroparotid space, cranial nerves IX to XII are juxtaposed to the ICA, and cranial nerves X and XII have the longest anatomic relationship to this artery. Although this ``mechanical'' theory of compression or stretching may explain some of the lower cranial nerve palsies related to ICA dissection, it does not explain all of them. Many dissections have not been associated with aneurysm formation, and the evidence for any arterial expansion is unclear in many. In 10 of our patients with lower cranial nerve palsies, angiography showed the presence of dissecting aneurysms in only 2. In the early 1980s, when uncertainty still existed about the relationship of ICA dissection and lower cranial nerve palsies, one of our patients with an ICA dissection and involvement of cranial nerves IX to XII underwent a combined exploration through a suboccipital craniotomy and upper cervical incision. The ICA was not expanded externally. The clinically involved nerves were identified and were grossly normal. ^[17] Furthermore, the mechanical theory does not explain other cranial nerve palsies, such as palsies of the trigeminal nerve or ocular motor palsies, that occur with extracranial ICA dissections. In all our patients, ICA dissection involved only the extracranial segment of the vessel. In only one patient with palsies of cranial nerves III and V did the dissection extend into the carotid canal, but there was no extension to the cavernous segment, where the ICA is in proximity with oculomotor nerves. Therefore, even in this case, a mechanical cause could not be speculated.

A more plausible mechanism for cranial nerve palsies in ICA dissection is impairment, transient or permanent, of the blood supply to the cranial nerves. This may be mechanical, embolic, or hemodynamic. Diseases that affect the blood vessels, such as diabetes or connective tissue disorders, may cause cranial nerve palsies. ^[23-27] In the practice of interventional neuroradiology, cranial nerve palsies are recognized complications of intra-arterial embolization. This observation provides evidence that embolic blockage of a nutrient artery of a cranial nerve may cause palsy of that nerve. Havelius et al., ^[6] in a study of autopsy material, identified a very minor artery sometimes leaving the ICA close to the base of the skull. These authors commented that if this minor artery contributes to the vascular supply of the nearby cranial nerves, its compromise may cause segmental ischemic damage to these nerves.

Three vascular systems play a significant role in nutrient supply to most of the cranial nerves: the inferolateral trunk, often arising from the ICA; the middle meningeal system; and the ascending pharyngeal system. The middle meningeal and ascending pharyngeal systems derive from the external carotid artery, but variations may occur. Specific supply of the inferolateral trunk corresponds to cranial nerves III, IV, and VI and the first division of cranial nerve V. The middle meningeal system supplies nutrient arteries to cranial nerve VII and the second and third divisions of the trigeminal nerve. The ascending pharyngeal system supplies cranial nerves IX through XII. ^[28] Several variations may be encountered in the collateral nutrient arterial supply of the cranial nerves, for example, an anomalously arising ascending pharyngeal artery from the cervical ICA supplying the lower cranial nerves. These nutrient arteries are too small (200 to 300 micro meter in diameter) to be readily visualized on routine angiograms. Often, high-quality selective angiograms with subtraction and magnification are required to visualize these small arteries. ^[29] Even then, these arteries are better visualized in younger subjects than older ones. Although these vessels can be demonstrated with high-quality techniques, their occlusion is difficult to demonstrate or document.

We conclude that cranial nerve palsies are noted in more than 10% of patients with extracranial ICA dissections. Although compression or stretching of the cranial nerves by the expanded artery may explain some of these cranial nerve palsies, most of them likely result from compromise of the nutrient arterial supply to the related nerve. This compromise may be caused by distal embolization, pressure gradient changes in collateral supply, or anomalous origin of the nutrient vessel and its compromise by the dissection.