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(Stroke. 1996;27:650-653.)
© 1996 American Heart Association, Inc.

Articles

Evaluation of Intracranial and Extracranial Carotid Steno-Occlusive Diseases in Taiwan Chinese Patients With MR Angiography

Preliminary Experience

Hon-Man Liu, MD; Yong-Kwang Tu, MD, PhD; Ping-Keung Yip, MD Cheng-Tau Su, MD

From the Departments of Medical Imaging (H.-M.L., C.-T.S.), Neurosurgery (Y.-K.T.), and Neurology (P.-K.Y.), National Taiwan University Hospital (Taipei), Republic of China.

Correspondence to Hon-Man Liu, MD, Department of Medical Imaging, National Taiwan University Hospital, No 7 Chung Shan South Rd, Taipei, Taiwan 100, Republic of China.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose We attempted to evaluate the location of vascular lesions in cases of cerebrovascular steno-occlusive diseases in Chinese persons living in Taiwan.

Methods With three-dimensional time-of-flight magnetic resonance angiography (MRA) as a screening tool, 108 symptomatic patients with cerebrovascular steno-occlusive diseases were examined. Cardioembolic disease and cerebral hemorrhage cases were excluded. The degrees of stenosis of bilateral cervical carotid arteries and their major intracranial tributaries were recorded. They were categorized as nonsignificant stenosis (0% to 49%), significant stenosis (50% to 99%), and total occlusion.

Results Our data revealed that 32.4% of the cases were normal in either cervical carotid arteries or their intracranial tributaries. In 24.1% of the cases, significant extracranial-carotid stenosis or occlusion was the only finding on MRA. In 25.9% of the cases, only significant intracranial-tributary stenosis was found. In 17.6% of them, significant lesions were found in both extracranial and intracranial carotid artery tributaries.

Conclusions A racial difference between Chinese and white patients in location of lesion in cerebrovascular steno-occlusive diseases was confirmed. About one third of symptomatic Chinese patients living in Taiwan showed small-vessel disease. Approximately 24% of patients had only extracranial carotid disease, and about 26% had only intracranial carotid tributary disease. We need a larger series of patients to confirm these findings. However, MRA might be a good screening tool for steno-occlusive cerebrovascular diseases, especially in persons of a race with more intracranial carotid disease, such as the Chinese.

Key Words: angiography • carotid arteries • magnetic resonance imaging • stenosis • Chinese

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Racial differences in location of lesions in cerebrovascular occlusive disease have been reported between white, black, Japanese, and Chinese persons.^{1 2 3 4 5 6 7 8} However, the studies regarding the Chinese are either incomplete or simply involve small series. In this study, we propose to (1) confirm the prior report that the Chinese have more severe intracranial lesions on MRA, which is one of the latest noninvasive modalities, and (2) evaluate the incidence of ICCA and ECCA lesions in symptomatic patients, with MRA as a tool.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
From October 1994 through February 1995, after routine MR imaging, 108 randomly selected patients were examined prospectively with MRA for the clinical diagnosis of carotid occlusive disease. Eighty-seven patients were admitted to our hospital for acute stroke, and 21 acute-stroke patients were referred from other community hospitals for MR examinations. There were 71 men and 37 women ranging in age from 44 to 85 years. We excluded patients with cardiogenic conditions such as atrial fibrillation or flutter, recent myocardial infarction, valvular heart diseases, endocarditis, and ischemic cardiomyopathy from this study. All patients suspected of having an embolic source underwent electrocardiography, transthoracic echocardiography, and/or transesophageal echocardiography. Patients presented initially as having sudden onset of hemiparesis in 51 cases, hemiplegia in 30, TIA in 12, and alternation of consciousness in 15. In those patients presenting with TIA, 7 complained of weakness or numbness of the face or limbs. Four patients suffered from transient blurring of vision, and 1 had language difficulty. Among the 15 patients presenting with alternation of consciousness, 8 were in a state of coma or stupor (4 found in the bathroom, 2 on the sidewalk, and 2 in bed), 2 were confused, and 5 had seizures. Hemiparesis was found in all of them during neurological examination. Aphasia was also found in 8 of the 10 patients with right hemiparesis in this group.

The history of potential vascular risk factors associated with carotid atherosclerosis was obtained from each patient and from the medical records. A diagnosis of hypertension was made if the patient's blood pressure surpassed 160 (systolic) and/or 95 (diastolic) mm Hg on repeated measurements during hospitalization or if the patient was being treated with antihypertensive drugs. A diagnosis of diabetes mellitus was based on clinical assessment, fasting serum glucose level, or sometimes the oral glucose tolerance test. History of cigarette smoking was positive if the patient had smoked 10 or more cigarettes daily for more than 10 years. Hypercholesterolemia was defined as a total fasting serum cholesterol level of 220 mL/dL. Coronary heart disease referred to the presence of history of angina pectoris, acute myocardial infarction, or electrocardiographic evidence of old myocardial infarction or ischemic changes.

All the MR studies were performed within 1 week after the clinical onset suggestive of carotid steno-occlusive disease. All the MRAs were obtained on a 1.5-T machine (GE, Signa, Advantage) with a standard head coil. Two sets of MRAs were performed separately at the cervical carotid and the circle of Willis. We used the time-of-flight angiography principle for imaging. Images were acquired in the axial planes by means of three-dimensional acquisition, gradient-echo technique with spoiling, and flow compensation. The repetition time, echo time, and flip angle were 31.3 milliseconds, 6.9 milliseconds, and 20° for the cervical carotid study and 56 milliseconds, 6.9 milliseconds, and 20° for the study in the circle of Willis, respectively. The magnetization transfer contrast technique was applied in the study of the circle of Willis for better resolution, contrast-to-noise ratio, and background suppression.^{9 10 11} For magnetization transfer contrast, we delivered another sinc pulse at 1500 Hz from the resonance of free water once per repetition time cycle, and it had a width of 500 Hz. We used a matrix of 192 and field of view of 20 to 24 cm. The slice thicknesses were 2 mm in the cervical portion and 1.2 or 1.5 mm in the region of the circle of Willis. One acquisition was obtained in each study. The scanning times were 2 minutes 49 seconds and 4 minutes 21 seconds, respectively.

All the ICCA and ECCA findings were categorized as symptomatic side or contralateral side, according to the clinical history. Results that were 50% were recorded as significant stenosis.^{12 13 14 15 16 17} The measurements of stenosis were computed directly on the maximum intensity projection views of MRAs. Collapsed views were also taken into measurement in the evaluation of steno-occlusion of the ICCA tributary. The percent stenosis was computed by measuring the residual lumen diameter and the original diameter at the site of maximum stenosis in each segment of the artery and dividing the difference by the original diameter. Vessels in which a signal void on MRA was accompanied by evidence of regained flow distal to the proximal part were considered patent and predefined as 80% to 99% stenosis. Thus they were recorded as (1) normal or nonclinically significant stenosis (ie, <50% stenosis), (2) clinically significant stenosis (ie, 50% stenosis), or (3) total occlusion on the symptomatic side and the contralateral side, respectively.

Carotid siphon stenosis was not included in this study because of the possibility of artifacts arising from the anterior clinoid processes, sphenoid sinuses, and intravoxel dephasing.¹⁸ All the cases with ECCA occlusion were associated with carotid siphon occlusion, but the middle cerebral artery could be just as generalized, smoothly small, or independently focally stenotic in this study.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Among the 108 patients, no significant abnormality in either ECCA or ICCA was noted in 35 cases (32.4%). Significant steno-occlusive lesions were found exclusively in the ECCA in 26 cases (24.1%) and solely in the ICCA in 28 cases (25.9%) on the symptomatic side. In 19 cases (17.6%), significant lesions were found in both the ECCA and ICCA.

The distribution of the groups with either ECCA or ICCA lesions is summarized in Table 1.

View this table: [in this window] [in a new window]   Table 1. Distribution of Lesions Involving Either the ECCA or ICCA on the Symptomatic Side

Nineteen patients were found to have lesions in both the ECCA and ICCA corresponding to clinical symptoms (Table 2). Significant stenosis was noted in both the ECCA and ICCA in 7 cases; lesions exclusively in the ipsilateral ICCA with nonsignificant stenosis in the ECCA were seen in 6 cases and lesions solely in the ipsilateral ECCA with nonsignificant stenosis in the ICCA in 5 cases. Nonsignificant stenoses were noted in both the ECCA and ICCA in 1 case. Significant lesions were found in the ICCA in a total of 41 cases (28+7+6 cases, or 38.0%), whereas they were found in the ECCA in 38 cases (26+7+5 cases, or 35.2%).

View this table: [in this window] [in a new window]   Table 2. Patients With Both Ipsilateral ECCA and ICCA Lesions

In the 12 patients presenting with TIA, 5 had significant steno-occlusive lesions in the ipsilateral ECCA alone, 4 had lesions in the ipsilateral ICCA alone, 2 had lesions in both the ICCA and ECCA, and 1 revealed no significant change in either the ECCA or ICCA.

In the 8 patients presenting with stupor or coma, 2 had bilateral severe stenosis in bilateral ECCAs and ICCAs, 1 had ipsilateral ECCA and ICCA occlusion with contralateral severe stenosis in the ECCA, 1 had ipsilateral ECCA and ICCA severe stenosis with contralateral ECCA occlusion, 2 had ipsilateral ICCA occlusion and also vertebrobasilar stenosis, 1 had bilateral ICCA severe stenosis, and 1 had ipsilateral ICA severe stenosis and also vertebrobasilar stenosis.

The clinical characteristics of the 108 patients are shown in Table 3.

View this table: [in this window] [in a new window]   Table 3. Demographic Characteristics in 108 Chinese Patients With Different Locations of Lesions

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
MRA, especially the three-dimensional time-of-flight technique, is useful as a noninvasive diagnostic tool for the evaluation of suspected extracranial and intracranial steno-occlusive disease.^{18 19 20 21} In the studies of Masaryk et al²⁰ and Heiserman et al,²¹ the correlation of MRA and conventional angiography was about 80% to 98% in the diagnosis of ECCA diseases. Overall sensitivities of 85% and 88% and specificities of 96% and 97% for the ICCA and middle cerebral artery, respectively, have been reported.¹⁸

In the treatment of a patient with cerebral ischemia, location and severity of the occlusive disease within the ECCA and ICCA are the major considerations for applying guidelines for care.²² Racial differences in the distribution of extracranial and cerebral vascular occlusive disease are well documented.^{1 2 3 4 5 6 7 8} However, most of the data were related to white, black, and Japanese patients. Few reports discuss Chinese populations, particularly regarding incidences of intracranial and extracranial lesions.^{3 6 7 23 24}

In Brust's series,³ among the 16 Chinese patients, 5 had significant stenosis in the ECCA, and only 1 had significant stenosis in the ICCA. Huang et al²³ mentioned that the Chinese might either have a decreased occurrence of larger cerebral artery disease or are similar to the Japanese and blacks in having more intracranial vascular diseases, but specific data were not available. This was the same in the review done by Caplan.²²

The work of Feldmann et al⁷ was the first study that specifically compared the differences between the Chinese and white populations in the distribution of occlusive cerebrovascular diseases, but their study had a selection bias. They compared clinical and angiographic features of 24 white and 24 Chinese patients with symptomatic occlusive cerebrovascular diseases. In their study, each Chinese patient was matched with the next white patient in the angiography record of the same age and sex. They found that the Chinese had more severe intracranial lesions and concluded that the preponderance of intracranial vascular lesions in Chinese patients was similar to that seen in blacks and Japanese. Our study might also have a selection bias because we studied only the patients referred for MR examinations. From our study, the incidence of lesions in ECCA and ICCA in our Chinese population was different from that of whites. The Chinese in our study do have more severe intracranial lesions (Table 4). The involvement of the ICCA in cerebrovascular disease among Chinese patients may be as high as 38% in our study. Our figures are higher than the data reported by Leung et al.²⁴ They examined the intracranial and extracranial arteries supplying the brains of 114 consecutive Chinese patients and reported that 31.4% of the subjects had at least one of the intracranial main cerebral arteries affected by severe atherosclerosis. The percentage rose from approximately 30% in the sixth and seventh decades to approximately 50% in the eighth and ninth decades, and in the affected subjects more than one vessel was usually involved. In 18% of the subjects, the ECCA was narrowed by >50% in their study, whereas it was narrowed by about 35.2% in our series. With advanced age, the incidence of severe extracranial disease leveled off, while that of the intracranial vessel disease continued to increase. Many of those severe stenoses were located in the very distal branches in the leptomeningeal surface.

View this table: [in this window] [in a new window]   Table 4. Distribution in Symptomatic Significant Carotid Steno-Occlusive Diseases in Chinese and White Patients

In our study, the petrous ICCA was not in the examination field, so there may be some overestimation in the percentage of negative MRA findings. However, according to our experience, atherosclerosis in the petrous portion is usually found concomitantly in patients with either ECCA or ICCA atherosclerosis. About one third of our patients revealed no significant vascular change in either the ECCA or ICCA, and we suspect that most of them might have lesions in the very distal branches of the carotid arteries, which was out of the resolution of current MRA techniques.

As reviewed by Inzitari et al,⁸ the intracranial vessels might be distinct from extracranial ones, not only in the anatomic location but also in their atherosclerotic process, and the chemical composition of the vascular wall of cerebral arteries might vary between individuals of different races. In Moossy's²⁵ conclusion on the data of the International Atherosclerotic Project, there was no reliable evidence of a qualitative difference in the lesions of cerebral atherosclerosis among diverse autopsy populations. However, quantitative differences exist in lesion severity and in intracranial versus extracranial atherosclerosis among different races. In an autopsy comparison of Japanese men who lived in Japan and Hawaii,²⁶ the Hawaiian subjects had more atherosclerosis of the circle of Willis but less intraparenchymal arterial atherosclerosis. Gorelick²⁷ stated that the increase in cerebral atherosclerosis as age advances is highly influenced by genetic and environmental risk factors, and racial differences in the distribution of cerebral atherosclerosis might also be highly influenced by these factors. Further investigations are needed, since the natural history and the treatment of intracranial occlusive lesions might differ from those of extracranial diseases.

In conclusion, our data suggest that ICCA steno-occlusive disease in our group of Chinese patients is not uncommon. Intracranial small- and medium-vessel disease may be an important cause of ischemic stroke in the Chinese. Since this is preliminary data, larger series of consecutive enrolled patients from comparable populations that could be deemed representative of the Chinese and white populations are required to clarify our findings.

	Selected Abbreviations and Acronyms

 

ECCA = extracranial carotid artery ICCA = intracranial carotid artery MRA = magnetic resonance angiography TIA = transient ischemic attack

Received August 1, 1995; revision received January 3, 1996; accepted January 15, 1996.

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