Journal of Neuroimaging V ol 15 No 1 January 2005 Tsai et al: Common Carotid Artery Occlusion

Clinical and Ultrasonographic Manifestations in Major Causes of Common Carotid Artery Occlusion

Chung-Fen Tsai, MD Jiann-Shing Jeng, MD Chien-Jung Lu, MD Ping-Keung Yip, MD

ABSTRACT
Background and Purpose. Atherosclerosis is the main cause of common carotid artery occlusion in most reports. This study aimed to identify the major causes of common carotid artery occlusion and compare the clinical features and carotid duplex ultrasonography findings of patients with common carotid artery occlusion attributable to each cause. Methods. Patients with common carotid artery occlusion documented by carotid duplex ultrasonography at the Neurovascular Laboratory (National Taiwan University Hospital) from 1988 to 2003 were included. Medical records and ultrasonographic findings were reviewed in detail to clarify the possible etiology of common carotid artery occlusion. Results. A total of 44 patients (male, 27 [61%]; female, 17 [39%]; mean age, 58 years) had common carotid artery occlusion attributable to a carotid duplex ultrasonographyidentifiable cause. The causes of common carotid artery occlusion included atherosclerosis (17 [39%]), Takayasus arteritis (11 [25%]), postirradiation arteriopathy (7 [16%]), cardiac embolism (6 [14%]), syphilis (1), blunt trauma (1), and homocystinuria (1). Among the patients with common carotid artery occlusion due to the 4 major causes, 27 (66%) had ischemic stroke and 14 (34%) had no symptoms or nonlocalizing symptoms. The frequency of symptomatic common carotid artery occlusion was 83% in those with cardioembolism, 76% in those with atherosclerosis, 71% in those with postirradiation arteriopathy, and 36% in those with Takayasus arteritis. Common carotid artery occlusion usually involved the carotid bulb and distal common carotid artery in atherosclerosis (88%) and postirradiation arteriopathy (100%), but not in Takayasus arteritis (27%). Echogenicity of occluded material was heterogeneous in atherosclerosis and post-

irradiation arteriopathy patients but homogeneous in all Takayasus arteritis patients. The authors postulate that the thrombotic mechanism might differ according to etiology. Conclusions. The causes of common carotid artery occlusion are diverse. Atherosclerosis, Takayasus arteritis, and postirradiation arteriopathy are the most common causes of common carotid artery occlusion in Taiwan. The clinical features, pathophysiology, and carotid duplex ultrasonography findings vary according to the cause of common carotid artery occlusion. Key words: Common carotid artery occlusion, ultrasonography, atherosclerosis, Takayasus arteritis, irradiation. Tsai C-F, Jeng J-S, Lu C-J, Yip P-K. Clinical and ultrasonographic manifestations in major causes of common carotid artery occlusion. J Neuroimaging 2005;15:50-56. DOI: 10.1177/1051228404270242

Received January 26, 2004, and in revised form June 8, 2004. Accepted for publication July 29, 2004. From the Department of Neurology (CFT, JSJ, CJL, PKY), Stroke Center ( JSJ, CJL, PKY), National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan, and the Department of Neurology, Cardinal Tien Hospital, Taipei, Taiwan (CFT). Address correspondence to Dr Jiann-Shing Jeng, Department of Neurology, National Taiwan University Hospital, No. 7, Chung-Shan South Road, Taipei 100, Taiwan. Email: jsjeng@ccms.ntu.edu.tw.

Among symptomatic patients with cerebrovascular diseases, the prevalence of those with common carotid artery occlusion (CCAO) is around 2%.1,2 In contrast to the wealth of information about internal carotid artery (ICA) occlusion,3 little is known about the clinical features, neurological symptoms, etiologies, pathogenesis, and carotid duplex ultrasonography (CDU) findings of CCAO. Limited data suggest that the clinical presentation of CCAO could range from asymptomatic disease to severe stroke.4-7 In patients with CCAO, atherosclerosis is considered as the main cause in most studies.2,4-8 The purpose of this study was to present the various major causes of CCAO and to compare the different clinical features, CDU findings, and possible pathogenesis of CCAO attributable to different major causes. Patients and Methods From 1988 to 2003, patients with CCAO documented by extracranial CDU at the Neurovascular Laboratory, National Taiwan University Hospital, Taipei, Taiwan, were recruited into this study. CCAO was defined by charac-

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Copyright 2005 by the American Society of Neuroimaging

Table 1. Clinical Features of the Major Causes of Common Carotid Artery Occlusion
Atherosclerosis (n = 17) Mean age, y Male gender Risk factor no 2* Symptomatic Ipsilateral Contralateral Vertebrobasilar Asyptomatic or nonlocalizing symptoms 70.1 13 (76%) 14 (82%) 13 (76%) 10 (59%) 2 (12%) 1 (6%) 4 (24%) Takayasus Arteritis (n = 11) 35.8 1 (9%) 4 (46%) 4 (36%) 4 (36%) 0 (0%) 0 (0%) 7 (64%) Postirradiation Arteriopathy (n = 7) 58.0 6 (85%) 2 (29%) 5 (71%) 2 (29%) 2 (29%) 1 (14%) 2 (29%) Cardioembolism (n = 6) 71.6 6 (100%) 6 (100%) 5 (83%) 5 (83%) 0 (0%) 0 (0%) 1 (17%) Overall (n = 41) 59.0 26 (63%) 26 (63%) 27 (66%) 21 (51%) 4 (10%) 2 (5%) 14 (34%)

*Risk factors include smoking, diabetes mellitus, hypertension, hyperlipidemia, and other cardiac diseases (including coronary artery disease, myocardial infarction, atrial fibrillation, and valvular heart disease).

teristic CDU findings: (1) lack of lateral expansion of the common carotid artery (CCA) walls on B-mode image, (2) absent signal within the CCA on Doppler spectral analysis, and (3) absence of color flow in the CCA on color Doppler image. A complete CDU study included transverse and longitudinal views of bilateral CCAs, ICAs, external carotid arteries (ECA), and proximal vertebral arteries from C6 to C3. The morphology of the arterial walls, peak systolic and end diastolic velocities, resistivity index, flow direction, and volume in each artery were recorded. Special attention was paid to flow direction of the ophthalmic arteries from the orbital window by transcranial Doppler and of the subclavian arteries. According to Gerlock et al, there are 2 CCAO types: type I, total occlusion of the CCA and ICA, and type II, isolated CCAO and patent ICA with collateral supply from reverse flow of the ipsilateral ECA.9 The medical records of each CCAO patient were comprehensively reviewed. Recorded data included age at diagnosis, sex, cerebrovascular risk factors (hypertension, diabetes mellitus, hyperlipidemia, smoking, coronary artery disease, atrial fibrillation, and other heart disease), occurrence of TIA or stroke, presenting symptoms, other systemic diseases and related therapeutic modalities (including radiotherapy), trauma history, head computed tomography or magnetic resonance image findings, and angiographic findings. Catheter-based angiography or magnetic resonance angiography was also performed in 20 patients, and CCAO was documented in 19 patients. Therefore, the specificity of CDU in identifying CCAO was estimated to be 95%. In each case, every effort was made to determine the cause of CCAO from the history and clinical presentation, image findings, and supporting laboratory results. The etiology of CCAO was identified as atherosclerosis

on the basis of clinical (associated with vascular risk factors) and neurovascular imaging findings. Takayasus arteritis (TA) was identified as the etiology of CCAO if patients met the diagnostic criteria proposed by Ishikawa.10 Postirradiation arteriopathy (PIA) was diagnosed if CCAO patients had a history of radiation therapy over the head and neck because of malignancy. Cardiac embolism was highly suspected if CCAO patients had cardiac arrhythmia with sudden onset focal ischemic symptoms and a fresh thrombus was noted by CDU. The clinical manifestations and CDU findings attributable to CCAO of different causes were compared. Results During a 16-year period, 49 CCAO patients were identified initially and 5 were excluded because of insufficient clinical information. A total of 44 patients (27 men, 17 women, mean age of 58.2 years) were included in this study. During the same period, 42,000 patients underwent CDU at our neurovascular laboratory and the incidence of CCAO was estimated as 0.1%. The causes of CCAO included atherosclerosis (17 [39%]), TA (11 [25%]), PIA (7 [16%]), cardioembolism (6 [14%]), syphilis arteritis (1), blunt injury (1), and homocystinuria (1). Clinical features associated with the 4 major causes are listed in Table 1. The leading cause of CCAO was atherosclerosis. Patients in the group were relatively old and predominantly male and had more cerebrovascular risk factors. TA was the second leading cause of CCAO in the present series. They were mostly young to middle-aged females with relatively few stroke risk factors. Of the 7 patients (mostly men) with PIA-related CCAO, all had received local radiation therapy around the cervical area because of malignancy (nasopharyngeal cancer, thyroid cancer, or

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tonsillar cancer). The time from irradiation to diagnosis of CCAO varied from 1 to 24 years. CCAO of cardioembolic origin was highly suspected in 6 cases. Most had cardiac arrhythmia and 1 had thrombus documented by cardiac echo. Ultrasonographic evidence of fresh, moving emboli included presence of hypoechogenic material and lack of flow signal in the total carotid system on the lesion side. However, on the contralateral side, the CCA was essentially normal in appearance or only mildly stenotic. Minor etiologies were also identified. A 47-year-old man with CCAO had cardiovascular syphilis and aortic regurgitation. Angiography and CDU demonstrated left CCAO and critical stenosis of other major arteries from the aortic arch. A 78-year-old woman sustained right hemiplegia and aphasia following a severe blunt injury to the neck. The left CCA was filled with homogenous and hypoechogenic material without color flow, Doppler signals, and intimal flap.11 A 14-year-old girl had progressive headache, vomiting, and hemiparesis. Left CCAO and severe stenosis of other carotid and vertebral arteries were found. Coagulation and autoimmune workup were all negative. She had marfanoid features such as a long face, scoliosis, slender digits, and joint hyperextensibility, and homocystinuria was diagnosed from laboratory examination.12 Of the patients with CCAO due to the 4 major causes, 14 (34%) had no symptoms or only nonlocalizing symptoms (such as isolated dizziness, lightheadedness, or fatigue) and 27 (66%) had focal ischemic symptoms (such as transient ischemic attack [TIA] or stroke). In the latter group, 21 had ipsilateral TIA or stroke (such as hemiparesis and aphasia). Four patients had ischemic symptoms on the contralateral side, and 2 had symptoms of insufficiency in the vertebrobasilar artery system (such as vertigo and diplopia). Moderate to severe concomitant stenosis of the contralateral carotid arteries or vertebral arteries was usually found from CDU or angiography examination. Frequency of symptomatic CCAO depended on its specific etiology. In the cardioembolic group, 5 (83%) patients had focal ischemic symptoms associated with acute ipsilateral cerebral infarction. Thirteen (76%) patients in the atherosclerosis group and 5 (71%) in the PIA group had obvious TIA or stroke; however, focal ischemic symptoms were only noted in 4 (36%) in the TA group. Regarding the CCAO classification, type II (61%) was more frequent than type I (39%) (Fig 1). But cerebral ischemic symptoms seemed to be more frequent in type I (13 [81%]) than in type II CCAO (13 [52%]). CDU findings associated with different causes of CCAO are shown

Fig 1. Types of common carotid artery occlusion (CCAO) by ultrasonography. (A) Type I, CCAO with internal carotid artery (ICA) occlusion; (B) type II, CCAO with reversed flow of the external carotid artery (ECA) and patent ICA (arrow indicating flow direction). in Table 2. The left side CCAO was more prevalent than the right side, except in the PIA group. Four patients had bilateral CCAO, and all suffered from TA. Topographic localization revealed involvement of the bulb and distal CCA was common in CCAO patients with atherosclerosis (88%) and PIA (100%) but infrequent in CCAO patients with TA (27%). Instead, CCAO in TA was usually at the proximal CCA and was usually associated with subclavian artery stenosis. For PIA, the changes of vessel walls were often segmental, restricted to the irradiated area (100%), not associated with any other peripheral vascular disorder. Table 3 summarizes the CDU assessment of morphology linked to the major causes of CCAO. The echogenicity of CCAO was often heterogeneous in atherosclerosis and PIA but homogeneous in TA (Fig 2). In

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Table 2. Topographic Distribution of the Major Causes of Common Carotid Artery Occlusion (CCAO)
Atherosclerosis (n = 17) Type of CCAO Type I Type II Side of CCAO Left Right Both Carotid bulb involvement Subclavian artery stenosis Takayasus Arteritis (n = 11) Postirradiation Arteriopathy (n = 7) Cardioembolism (n = 6) Overall (n = 41)

7 (41%) 10 (59%) 12 (71%) 5 (29%) 0 15 (88%) 3 (18%)

2 (18%) 9 (82%) 6 (55%) 1 (9%) 4 (36%) 3 (27%) 11 (100%)

4 (57%) 3 (43%) 3 (43%) 4 (57%) 0 7 (100%) 0

3 (50%) 3 (50%) 3 (50%) 3 (50%) 0 4 (67%) 1 (17%)

16 (39%) 25 (61%) 24 (59%) 13 (32%) 4 (10%) 29 (71%) 15 (37%)

Table 3. Ultrasonographic Findings of the Major Causes of Common Carotid Artery (CCA) Occlusion
Atherosclerosis (n = 17) Echogenicity of occluded material Heterogeneous: 17 (100%) Hyperechoic: 17 (100%) Takayasus Arteritis (n = 11) Homogeneous: 11 (100%) Hyperechoic: 11 (100%) Clear-cut, proximal and segmental: 9 (82%) Concentric: 8 (73%) Postirradiation Arteriopathy (n = 7) Heterogeneous: 7 (100%) Hyperechoic: 7 (100%) Irregular, localized to the irradiation area: 7 (100%) Eccentric: 5 (71%) Cardioembolism (n = 6) Hypoechoic to anechoic: 5 (83%) Moving thrombus: 5 (83%) Clear-cut: 6 (100%) Normal or mild stenosis: 5 (83%) Only mild stenosis or normal: 5 (83%)

Margin and location of Irregular and distal: occluded material 15 (88%) Eccentric: 14 (82%) Mode of distribution in the contralateral CCA Surface in the Smooth or rough contralateral CCA

Often smooth: 11 (100%)

Often rough: 7 (100%)

Fig 2. Longitudinal view of color Doppler flow ultrasonography in a patient of Takayasus arteritis. (A) Total occlusion of the left common carotid artery (CCA) with homogeneous echogenicity; (B) nearly total occlusion of the right CCA with a string patent lumen (arrow).

cardiogenic CCAO, fresh-moving thrombi with relative hypoechogenicity within the CCA lumen were noted in 2 cases. Beside the ipsilateral side, the contralateral side of the CCA can provide information regarding the different causes of CCAO. The surface of the contralateral CCA

was often rough in atherosclerosis and PIA patients but usually smooth in TA patients. From the transverse view, stenosis of the contralateral CCA was eccentric in atherosclerosis and PIA patients but often concentric in TA patients. In the cardiogenic group, a marked discrepancy

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was found between the ipsilateral and contralateral carotid arteries. Most patients had only mild stenosis or completely normal contralateral carotid arteries. Discussion Patients with CCAO may have a complex clinical presentation ranging from no symptoms to severe stroke. Because many CCAO patients do not have symptoms, the true prevalence is difficult to estimate.4,8 CCAO may represent a less common but an important form of extracranial cerebrovascular disease. The mechanism of thrombotic process of CCAO is still controversial. CCAO may occur as a result of retrograde thrombosis from the carotid bifurcation or antegrade propagation from the proximal CCA. Podore et al studied 12 CCAO cases and reported that the occlusion began in the CCA in more than half.5 However, Martin et al thought the occlusive process began distally because all of their patients had occlusive plaque at the carotid bifurcation, and during thrombectomy, patent origin was found in 3 cases.7 In our study, we postulated that the thrombotic mechanism might differ according to specific etiology. Thrombosis in atherosclerosis patients (who usually have marked carotid bulb involvement [88%]) may be retrograde, whereas in TA patients (who often have proximal CCA [82%] and subclavian artery involvement [100%]), thrombosis may be antegrade. In PIA, the restricted segmental occlusive lesion might be related to direct radiation exposure since there is no obvious involvement in other areas. The CCAO can be isolated with the patent ICA (type II), or the occlusion can be in both the CCA and ipsilateral ICA (type I). If the CCAO is isolated and the ICA is patent, flow to the cerebrum could be maintained by the extracranial collaterals via the ECA. It would result in retrograde flow in the ipsilateral ECA and antegrade flow in the ICA distal to the occlusion. Although flow could also be supplied by intracranial collateral via the anterior or posterior communicating artery with retrograde flow of the ICA, this is rarely observed clinically.13 In a study by Chang et al, patients with isolated CCAO may have a better outcome than patients with both an occluded CCA and ICA.8 Our study has also shown a higher percentage of symptomatic type I than type II cases of CCAO (82% vs 56%). In previous reports of CCAO, atherosclerosis was always the major etiology.2,4-8 Beyond atherosclerosis, only 1 case series study showed PIA as the cause of CCAO in 3 patients.8 Other causes of CCAO including arteritis, aortic arch dissection, aortic arch aneurysm, fibromuscular dysplasia, thrombocytosis, cardiac source

embolism, and blunt or open trauma have been reported occasionally.4,8,11,12 The mechanism of occlusion and the character, course, and prognosis of CCAO attributable to different causes are not well described. Of the 7 different etiologies of CCAO included in our study, atherosclerosis, TA, PIA, and cardioembolism were the most important and unique. Atherosclerosis patients with CCAO were older, mostly male with multiple vascular risk factors, and were often associated with higher risk of stroke. On the other hand, TA patients were mostly young women with few vascular risk factors and therefore lower risk of stroke. TA is a chronic, inflammatory arteriopathy resulting in progressive stenosis of the aortic arch and its major branches. It has an unexplained predilection for Asians.10 Our previous TA ultrasonographic study revealed that 100% of patients had subclavian artery involvement and 69% had CCA involvement that was often bilateral.14 Homogeneous segmental circumferential intima-media thickening from the proximal CCA is a specific ultrasonographic finding in TA, and the ICA is usually spared in early stage. Sequential study often shows progressive concentric stenosis rather than longitudinal spreading in the CCA. The TA process is in contrast to the atherosclerosis process, which usually begins eccentrically from the carotid bulb, then spreads longitudinally to the CCA and ICA. The third important group of CCAO patients suffers from PIA. Radiation can produce marked morphological changes in blood vessels. In an animal study, a 5-gray irradiation could induce penetration of fat into the wall, atherosclerotic plaque formation in the intima, and structural changes of the elastic fibers in the arteries.15 Besides the direct effect, large arteries can also be affected owing to injury of the vaso vasorum.16 The ultrasonographic findings differ between PIA and atherosclerosis cases. The vessel wall changes are often segmental and restricted to the irradiation exposure area and are accompanied by perivascular fibrosis. Vessel walls usually have a very rough, hard, and sometimes misery surface. Other major vessels such as subclavian arteries are spared. In 1 study of patients who received high-dose radiation therapy for head and neck malignancy within the past 12 years, 21% were found to have advanced carotid stenosis as compared to 4% in the age-matched control group.17 Radiation may accelerate atherosclerotic changes in carotid arteries in the exposed area, and the degree of vascular obstructive lesion correlates with postirradiation duration.18 Cardioembolism to the CCA might be suspected from clinical manifestations and neuroimaging findings, although this has rarely been reported. In our study, there

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were 6 such patients. Five of them had a history of cardiac arrhythmia and presented with acute cerebral infarction. Intracardiac thrombus was documented through transesophageal cardiac echo in 1 case. Kimura et al documented oscillating thomboemboli within the ICA by CDU.19 The ultrasonography findings, which were obtained within 3 days of stroke onset in our patients, showed a very hypoechoic and homogeneous moving thrombus in the occluded CCA. The mobile structure moved distally during the systolic phase of the cardiac cycle and returned to the original position during the diastolic phase. This description is quite different from the CDU findings of CCAO due to other etiologies. Moreover, there is an obvious discrepancy between the contralateral and ipsilateral carotid arteries. In contrast to CCAO on the lesion side, the contralateral carotid arteries are either essentially normal or only mild stenotic (83%). Because a mobile intraluminal embolus may disappear or stabilize gradually and change to a nonmobile hyperechoic thrombus,20 CDU should be performed as soon as possible after the symptom onset to establish the correct diagnosis and consider anticoagulation treatment for secondary prevention of stroke. From the results of the present study, we postulate that the following factors might contribute to the development of symptomatic cerebrovascular disease: (1) the distribution of CCAO; TIA and stroke occur more frequently in type I CCAO than in type II CCAO; (2) the rate of CCAO formation; an obviously higher frequency of focal ischemic symptoms was associated with CCAO due to acute cardioembolism than CCAO due to other etiologies; and (3) the etiologies of CCAO; a lower frequency of stroke or TIA was associated with TA than other causes of CCAO. Besides chronic thrombosis, TA often involves the aortic arch and the proximal portion of its major branches, with less involvement above the carotid bulb. Intracranial and collateral circulation could be preserved and established. However, CCAO due to atherosclerosis or PIA has a predilection for the carotid bulb, ICA, and intracranial portion. This study is a case-series study conducted in a university medical center in Taiwan. Sampling bias due to recruiting more rare or special cases is possible. The distribution of patients according to their CCAO causes should be interpreted with caution. Nevertheless, this study might provide the chance to understand the clinical significance of the different etiologies. Because of geographic and race-ethnic differences, more CCAO patients with TA or PIA were included in this study. As in the previous discussion, TA is more prevalent in Asians than Caucasians and nasopharyngeal carcinoma is one of the leading causes of cancer in Chinese, particularly the

inhabitants of southeastern China and Taiwan.21-23 Most of the patients with nasopharyngeal carcinoma undergo radiation therapy to the neck and nasopharyngeal areas. Therefore, more PIA-induced CCAO cases can be found in Taiwan. In conclusion, CCAO patients may be categorized on the basis of CCAO cause. Atherosclerosis is not the only one major etiology. In our study, TA and PIA are also important CCAO causes, especially in Chinese. The pathogenesis, clinical manifestations, ultrasonographic findings, treatment policies, and prognosis of CCAO due to different causes may be different.

This study was supported in part by the research grant from the Department of Health, Taiwan (DOH92-HP-1114). The authors wish to thank Bao-Show Hwang and Win-Hwen Lin for their technical assistance in ultrasonography. A preliminary report of this study was presented at the 26th annual meeting of American Society of Neuroimaging, New Orleans, March 2003.

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