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(Stroke. 1997;28:2507-2512.)
© 1997 American Heart Association, Inc.

Articles

Subtypes of Ischemic Stroke

A Hospital-Based Stroke Registry in Taiwan (SCAN-IV)

Ping-Keung Yip, MD; Jiann-Shing Jeng, MD; Ti-Kai Lee, MD; Yang-Chyuan Chang, MD; Zei-Shung Huang, MD, PhD; Sien-Kiat Ng, MD; Rong-Chi Chen, MD

From the Departments of Neurology (P-K.Y., J-S.J., Y-C.C, R-C.C.) and Internal Medicine (T-K.L., Z-S.H., S-K.N.), National Taiwan University Hospital, and En Chu Kong Hospital (T-K.L., R-C.C.), Taipei, Taiwan, Republic of China.

Correspondence to Ping-Keung Yip, MD, Division of Cerebrovascular Disease, Department of Neurology, National Taiwan University Hospital, No. 7 Chung-Shan S Rd, Taipei 100, Taiwan, Republic of China. E-mail liu4138{at}ms2.mmh.org.tw

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose To better understand the clinical pattern and further elucidate the risk factors and outcome in different subtypes of cerebral infarction (CI) of the Chinese in Taiwan, we analyzed the National Taiwan University Hospital Stroke Registry in 1995 and performed an ethnic comparison with similar data banks.

Methods From the National Taiwan University Hospital Stroke Registry in 1995, 676 patients (383 men and 293 women; mean age, 64.9 years; SD, 13.8 years; range, 1 to 98 years) with CI were recruited for this analysis. CI was classified into five subtypes based on clinical manifestations, ultrasonographic studies, and neuroimaging findings: large-artery atherosclerosis, lacunae, cardioembolism, other less common determined causes, and undetermined cause. Vascular risk factors, extracranial carotid artery atherosclerosis, and 30-day case-fatality rates were investigated in each subtype of CI.

Results Of all CI patients, 17%, 29%, 20%, 6%, and 29% were classified as large-artery atherosclerosis, lacunae, cardioembolism, other determined causes, and undetermined cause subtypes, respectively. The present results were compared with those from eight similar Western stroke registries. The relative incidence of lacunar CI in Chinese patients was more common, but large-artery atherosclerotic CI was less common than in whites. Hypertension was frequently seen in CI patients, especially in those with lacunae (85%) and large-artery atherosclerosis (69%). Patients with cardioembolism had a higher percentage of atrial fibrillation (69%), left ventricular hypertrophy, and ischemic heart disease than the other patients. Patients with large-artery atherosclerosis had more vascular risk factors, such as hypertension, diabetes mellitus, smoking, and carotid stenosis. Cardioembolic patients had higher case-fatality rates than other CI patients. Of the cardioembolic patients, 17.3% and 21.8% died within 30 days and during hospitalization, respectively.

Conclusions The proportion of CI subtypes varied in different stroke registries. This may be partly due to applied classification criteria and racial-ethnic differences. Awareness of the risk factors and outcome in each subtype of stroke may afford further insights into the surveillance and treatment of cerebrovascular disease.

Key Words: racial differences • registries • stroke classification • Taiwan

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The causes of acute CI are heterogeneous, including large-artery atherosclerosis, disease of small penetrating arteries (lacunae), cardiogenic or artery-to-artery embolism, coagulopathy, and many nonatherosclerotic vasculopathies.^{1 2 3} Different causes of CI have different clinical presentations, risk factors, courses, and outcomes. Furthermore, these may affect the attitude of investigation and management. Many studies have disclosed that there are significant racial-ethnic differences in the distribution of extracranial or intracranial carotid atherosclerosis and vascular risk factors.^{4 5 6 7 8 9 10 11 12} Chinese,^{4 5 6 7} Japanese,^{8 9} Hispanics, and blacks^{10 11} have a greater preponderance of intracranial atherosclerosis than whites, but different ischemic stroke subtypes have received less attention in the Chinese than in whites. A well-organized SDB can provide much information and insight into these problems.^{13 14 15}

SCAN is a hospital-based investigation. The aims of the SCAN project are to study the epidemiological and pathophysiological characteristics of different types of stroke,¹⁶ to assess the relation of various cardiovascular risk factors to cerebrovascular disease and carotid atherosclerosis,^{16 17} and to probe the extent and severity of atherosclerosis in the carotid arteries.^{18 19}

The present study was the fourth part of the SCAN project; we sought to determine the causes of ischemic stroke in our population, to compare our results with those from similar investigations of different ethnic groups, and to seek explanations for any differences in those results that might exist.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
From the NTUH Stroke Registry in 1995, 676 consecutive patients with CI in 1 year were analyzed prospectively. A detailed medical record regarding medical history, acute stroke presentation, physical and neurological findings, clinical course, outcome, and laboratory results was reviewed in each patient. History of potential vascular risk factors and conditions assumed to be associated with atherosclerosis and stroke were determined in each patient, as previously described.¹⁶ Most patients received at least one brain imaging (CT or MRI) study. These patients were further classified into five categories based on clinical features, brain imaging, cardiac imaging (transthoracic and/or transesophageal echocardiography), ultrasonography of extracranial and/or intracranial large arteries, angiography (MR or conventional angiography), and other remarkable laboratory findings. These diagnostic criteria were basically adopted from the TOAST²⁰ classification system. Diagnosis of acute stroke with other determined causes was supported by the criteria of nonatherosclerotic vasculopathy, hematologic/other, migrainous stroke, and drug-related categories noted in the Baltimore-Washington Cooperative Young Stroke Study criteria.²¹ The diagnostic criteria were as follows.

Large-Artery Atherosclerosis
Clinically, the patient has cerebral cortical impairment (eg, aphasia, neglect, apraxia, anopia, restricted motor involvement) or brain stem or cerebellar dysfunction. A history of intermittent claudication, transient ischemic attacks in the same vascular territory, or carotid bruit supports the clinical diagnosis. Radiologically, ipsilateral extracranial or intracranial atherosclerosis by angiogram or ultrasonogram shows significant (50%) stenosis, occlusion, or ulcerated plaques. Infarct areas are greater than 1.5 cm in diameter on CT or MRI.

Small-Artery Occlusion (Lacunae)
Clinically, the patient has one of the traditional clinical lacunar syndromes and does not have evidence of cerebral cortical dysfunction. A history of hypertension or diabetes mellitus supports the clinical diagnosis. Radiological findings include a normal image or a small (<1.5 cm in diameter) deep lesion on CT/MRI. Evidence of cardiac sources of embolism or atherothrombosis is absent.

Cardioembolic Infarction
Cinically, the patient has sudden-onset cerebral cortical impairment or brain stem or cerebellar dysfunction. The arterial occlusions are presumably due to an embolus arising in the heart (eg, rheumatic mitral valve disease with or without atrial fibrillation, nonvalvular atrial fibrillation, sick sinus syndrome, recent [6 weeks before stroke] myocardial infarction, cardiac thrombus, valvular vegetation, akinetic left ventricular segment, atrial myxoma, dilated cardiomyopathy, prosthetic mitral or aortic valve, paradoxical emboli). Radiologically, brain CT/MRI findings are similar to those described for large-artery atherosclerosis. The angiogram or ultrasonogram does not show significant (50%) stenosis or ulcerated plaques in the proximal large-artery supply.

Acute Stroke of Other Determined Etiology
This category consists of patients with rare causes of stroke, such as nonatherosclerotic vasculopathies (eg, dissection, postirradiation vasculopathy, fibromuscular dysplasia, arteritis, migraine, drug-related vasculopathy), hematological disorders (eg, protein C, protein S, or antithrombin III deficiency, thrombotic or idiopathic thrombocytopenic purpura, antiphospholipid syndrome, nephrotic syndrome), or other specific vasculopathy.²¹

Stroke of Undetermined Etiology
This category includes patients without likely etiology determined despite an extensive evaluation. Patients with two or more potential causes of stroke with equal priority are also included in this category.

All patients were evaluated or reviewed by at least two staff neurologists from the list of authorship, and all completed questionnaires were reviewed and coordinated by one of us (J-S.J.) before analysis. Each ischemic stroke was assigned a specific cause or subtype according to predetermined criteria.

Statistical Analysis
Statistical analyses were performed with the use of SPSS for Windows. The Mantel-Haenszel ² test was applied to examine the difference in categorical risk factors between the subtypes of CI.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Of the 676 patients with CI, there were 383 men and 293 women (mean age, 64.9 years; SD, 13.8 years; range, 1 to 98 years). Sixty-four patients (9.5%; 35 men and 29 women) were younger than 45 years. No significant difference in age at onset among subtypes of CI was noted except that patients with stroke of other determined etiology were younger than those in other subtypes. The distribution of age and sex in different subtypes of CI is shown in Table 1.

View this table: [in this window] [in a new window]   Table 1. Age and Sex Distribution of Different Subtypes of CI

Of the patients with an identified type of CI, lacunar infarction was the most common type (195 patients or 29%). There were 133 patients (20%) with CEI, and 69% of these patients had atrial fibrillation with or without valvular disease. Stroke of other determined etiology was identified in 39 patients (6%). Of these less common etiologies (Table 2), postradiotherapy vasculopathy, coagulopathy (eg, protein C or S deficiency, nephrotic syndrome), giant aneurysm, carotid artery dissection, and mitochondrial disease were more frequently seen. Despite many investigations, 196 patients (29%) were without an identified cause for their stroke.

View this table: [in this window] [in a new window]   Table 2. Less Common Identified Causes of Cerebral Infarction in 1995 NTUH Stroke Registry

The characteristics and prevalence of the stroke risk factors in different subtypes of CI are listed in Table 3. Hypertension was frequently seen in CI patients, particularly in patients with lacunar infarction (85%) and large-artery atherosclerotic infarction (69%). Approximately one fourth of patients had recurrent stroke in each subtype of CI. Atrial fibrillation, ischemic heart disease, and cardiomegaly were frequently found in CEI patients. The habits of smoking and alcohol drinking were found more often in patients with large-artery atherosclerosis than in other patients. Serum levels of cholesterol did not differ significantly among various subtypes of CI.

View this table: [in this window] [in a new window]   Table 3. Clinical Characteristics of 676 Patients With Different Subtypes of Cerebral Infarction

Of all CI patients, 520 had received extracranial duplex ultrasound examinations (77% performance rate). Among these 520 patients, 355 (68%) had extracranial carotid artery atherosclerosis, and 63 (12%) had severe carotid stenosis (luminal stenosis 50%). In different subtypes of CI patients, 50% of patients with large-artery atherosclerosis, 2% with lacunae, 3% with cardioembolism, and 16% with stroke of other determined etiology had carotid stenosis 50%. (Table 3).

The 30-day and in-hospital case-fatality rates of all CI patients were 5.8% and 8.0%, respectively. Patients with CEI had a higher case-fatality rate than other CI patients. Twenty-three CEI patients (17.3%) died within 1 month, and 29 CEI patients (21.8%) died during hospitalization. Compared with the other CI patients, there was a significantly higher in-hospital case-fatality rate in CEI (P<.001; odds ratio, 6.03; 95% confidence interval, 3.25 to 11.21; x² test). Only one patient with lacunar CI died (due to sepsis) in the present stroke registry.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
To identify the pathogenesis of stroke is critical for both clinical practice and academic research. However, it is sometimes difficult to classify the subtype (cause) of CI.²² For example, lacunar infarction can also be caused by large-artery occlusion, emboli, or intracranial branch atheromatous occlusion in addition to small penetrating artery disease.²³ In addition, it is difficult to judge the CI subtype of a case with both atrial fibrillation and high carotid stenosis.²⁴ Therefore, a reliable classification system for acute CI is crucial for clinicians. Several clinical classification systems have been used to categorize the subtypes of CI.^{2 20 21 25 26} The interobserver reliability of these CI classification systems has been judged fair to good.^{21 27 28} In the present study we adopted a classification system basically from the TOAST²⁰ and Baltimore-Washington Cooperative Young Stroke Study criteria²¹ because clinical analyses of subtypes of CI have proved to have good interobserver reliability.^{21 27}

The relative incidences of each subtype of CI in a selective sample of other large-scale stroke registries are listed in Table 4. We did not include studies without further classification of subtype of CI. Nine stroke registries, including the present study, are listed for comparison.^{3 29 30 31 32 33 34 35} The classification of CI differed among these studies. Even the definition of subtype of CI in different studies may not be identical. The terms "cerebral thrombosis," "atherosclerosis," and "large-vessel atherothrombosis" were grouped together as "large-artery atherosclerosis." Both embolic CI and CEI were displayed according to the different study results.

View this table: [in this window] [in a new window]   Table 4. Relative Incidences of Cerebral Infarction Causes Reported From Selected Stroke Registry Studies

Of the identified causes of CI, lacunar infarct was the most common subtype (29%) in the present study. Our proportion of lacunar infarct was higher than that in the Western stroke registries, ranging from 10% to 24% in most studies,^{3 29 30 31 32 33} except NINCDS and UCSD SDBs (27%).^{26 35} Our percentage of lacunar infarct was comparable to other available Chinese hospital-based studies, such as People's Republic of China (27%),³⁶ Hong Kong (27%),³⁷ and one previous study in Taiwan (29%).³⁸ On the other hand, the large-artery atherosclerotic subtype of CI in our study constituted only 17%. Although the relative proportion of the same subtype in other studies varied from 14% to 66%, most of the Western stroke registries reported a higher proportion in this category. The discrepancy in these studies may be influenced by numerous factors, but the following three factors deserve special attention: (1) different study design, ie, the operational criteria for ischemic stroke subtypes have a major impact on the categories of large-vessel atherosclerosis and undetermined causes; (2) composition of different racial-ethnic populations, eg, 58% were black in the NINCDS SDB, which might account for the higher proportion of lacunar stroke but a smaller proportion of the large-vessel atherosclerotic subtype^{26 39} ; (3) patient selection methods, ie, the inclusion of outpatients with minor stroke will also result in more lacunar and less large-vessel ischemic stroke, eg, the UCSD SDB.³⁵ The apparent differences in these two subtypes of CI between Westerners and our population confirm the contention of previous studies in racial differences regarding the distribution of occlusive cerebrovascular disease.^{4 5 6 7 10 12}

In most of these studies, approximately 20% of the cases were classified as the CEI subtype, with no significant difference in this subtype between different races.^{3 29 34 35} In our study and the studies conducted by Sacco et al³⁴ and Yatsu et al,³² 29% to 40% of the cases were classified as undetermined causes. In the studies conducted by Friday et al³³ and Bogousslavsky et al,³ only 1% and 8% of the cases were classified as undetermined causes, respectively. In general, the higher the relative incidence of undetermined subtype, the lower is the relative incidence of large-artery atherosclerotic subtype.

Since NTUH is a referral hospital that serves more problematic patients, the proportion and composition of the category of stroke of determined causes should be viewed cautiously. However, nasopharyngeal carcinoma is one of the leading causes of cancer in the Chinese, especially the inhabitants of southeastern mainland China and Taiwan.^{40 41 42} Most of the patients with nasopharyngeal carcinoma receive radiation therapy on their neck and nasopharyngeal regions. Therefore, it is not surprising that radiation vasculopathy is more frequently seen in Taiwan.⁴³

Hypertension was a more powerful risk factor for patients with large-artery atherosclerosis (69%) and lacunae (85%) than for patients with CEI (55%) and less common identified causes (38%). This result was similar to our previously reported findings¹⁶ and the SDB results.³⁹ Hypertension might contribute similarly to the development of large- and small-artery diseases. Diabetes mellitus also showed findings comparable to hypertension. There was no doubt that atrial fibrillation, left ventricular hypertrophy, and ischemic heart disease were more commonly seen in the CEI subtype. Overall, patients with large-artery atherosclerosis had more vascular risk factors, such as hypertension, diabetes mellitus, smoking, ischemic heart disease, hyperlipidemia, and carotid stenosis, than other CI patients.

The case-fatality rate of all CI patients at 30 days was 5.8%, lower than the previous studies reported in Taiwan, ranging from 7.8% to 10%.^{38 44 45} Our study results showed that there was a significant difference in case-fatality rates among subtypes of CI. Patients with CEI had a higher case-fatality rate than the other CI patients. Of these CEI patients, atrial fibrillation with or without valvular heart disease was frequently seen (69%). The 30-day case-fatality rate for CEI patients was 17.3%. In Rochester, Minn, the 30-day mortality rate in patients with CEI was nearly three times greater than in patients without CEI (23% versus 8%).⁴⁶ In the Framingham Study, CI patients with atrial fibrillation were nearly twice as likely to be fatal as those without atrial fibrillation.⁴⁷ Another study also showed that stroke patients with atrial fibrillation have a higher risk of death during both the acute and chronic phases after the first acute stroke event.⁴⁸ In contrast, patients with lacunar infarction had low mortality. Only one patient (0.5%) died in our stroke registry. Other studies also revealed that there was significant difference in mortality after stroke between lacunar and nonlacunar infarction. In Perth, Australia, only 1.6% of those with lacunar CI died within 28 days of stroke.⁴⁹ In the Rochester⁵⁰ and Northern Manhattan⁵¹ studies, survival was significantly better for patients with lacunar infarction than for patients with nonlacunar infarction.

In conclusion, the proportions of different CI subtypes vary in different stroke registries. This may be explained by different criteria used for classification and methodologies of study and by racial-ethnic differences. Awareness of the risk factors and outcome in each subtype of stroke may afford further insights into the surveillance and treatment of cerebrovascular disease.

	Selected Abbreviations and Acronyms

 

CEI = cardioembolic infarction CI = cerebral infarction NIN(C)DS = National Institute of Neurological (and Communicative) Disorders and Stroke NTUH = National Taiwan University Hospital SCAN = Stroke and Cerebral Atherosclerosis Study of National Taiwan University Hospital SDB = Stroke Data Bank TOAST = Trial of ORG 10172 in Acute Stroke Treatment UCSD = University of California, San Diego

Received June 27, 1997; revision received September 5, 1997; accepted September 16, 1997.

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