Race and Sex Differences in the Distribution of Cerebral Atherosclerosis
Background and Purpose The purpose of this study was to assess the influence of race, sex, and other risk factors on the location of atherosclerotic occlusive lesions in cerebral vessels. Previous angiographic studies of patients with stroke or transient ischemic attack (TIA) suggest that extracranial atherosclerosis is more common in whites and intracranial disease is more common in blacks. Noninvasive techniques such as duplex ultrasound, transcranial Doppler (TCD), and magnetic resonance angiography (MRA) allow vascular assessment of a more representative proportion of patients than does conventional angiography alone.
Methods Consecutive patients evaluated at a community hospital for stroke or TIA over a 2-year period were reviewed. Lesions were defined as a 50% or greater atherosclerotic stenosis by angiography, duplex ultrasound, or TCD, or a moderate stenosis by MRA.
Results Whites were more likely than blacks to have extracranial carotid artery lesions (33% versus 15%, P=.001), but the proportion of patients with intracranial lesions was similar (24% versus 22%). Men were more likely to have intracranial lesions than women (29% versus 14%, P=.03). When multivariate logistic regression analysis was used, white race was the only predictor for extracranial carotid artery lesions, and male sex was the only predictor for intracranial lesions. The cause of stroke/TIA was extracranial carotid artery disease in 8% and intracranial disease in 8% of all patients in the study.
Conclusions The distribution of cerebral atherosclerosis is influenced by race and sex but not by other vascular risk factors. In our patient population, intracranial disease is as common a cause of cerebral ischemia as extracranial carotid disease.
Previous studies suggest that there are racial differences in stroke risk, the type of stroke, and the distribution of atherosclerosis in cerebral vessels.1 2 3 4 5 6 7 8 9 10 11 12 13 In the United States, for example, blacks have a higher risk of stroke than do whites, even after adjustment for differences in risk factors.9 12 Blacks also have fewer TIAs5 and are more likely than whites to have lacunar stroke than other stroke subtypes.14 In a review of stroke and race, Caplan et al8 noted that blacks were more likely to have atherosclerosis involving the intracranial cerebral vessels, whereas whites more commonly had disease of the extracranial vessels, particularly the cervical carotid artery. Differences in risk factors could not entirely explain the racial differences in the distribution of vascular lesions. A similar although less impressive difference was noted between sexes, with women more likely to have intracranial lesions and men more likely to have extracranial disease.
Many previous studies of racial differences in the distribution of cerebral atherosclerosis relied on data derived from autopsy or cerebral angiography and therefore may be subject to selection bias. Patients suspected of having surgically accessible carotid artery disease, for example, are probably more likely to have cerebral angiography than are patients with lacunar stroke. The current availability of noninvasive vascular imaging techniques, such as carotid duplex ultrasonography, TCD, and MRA, allows evaluation of the cerebrovascular tree in a larger percentage of patients than was previously possible. We sought to confirm previous observations about racial differences in the distribution of cerebral atherosclerosis using both invasive and noninvasive vascular imaging studies in a series of patients admitted with ischemic stroke or TIA. This approach provides an assessment of the cerebral vasculature in a more representative sample of patients than by conventional angiography alone.
In addition, little is known about the prevalence of symptomatic intracranial atherosclerosis. The extracranial carotid artery is routinely assessed by duplex ultrasound in patients admitted with stroke or TIA, but assessment of intracranial vessels may not be performed if the condition is thought to be rare. We determined the percentage of patients in our series who had either intracranial atherosclerotic lesions or extracranial carotid lesions as the sole cause of their stroke or TIA.
Subjects and Methods
Consecutive patients seen by the Neurology Service and admitted with acute ischemic stroke or TIA over a 2-year period (April 1993 to March 1995) were reviewed. The study was performed in accordance with institutional guidelines. Information collected included demographics, risk factors, tests performed, and results of the neurological evaluation. Hypertension was defined as a history of elevated blood pressure before admission that required treatment with antihypertensive medications or persistently elevated blood pressure (systolic blood pressure >140 mm Hg or diastolic blood pressure >90 mm Hg) during follow-up. Diabetes mellitus was defined as a history of diabetes treated with medication before admission or persistently elevated glucose (fasting level >7.8 mmol/L) during follow-up. Patients with coronary artery disease had a history of either angina, myocardial infarction, or coronary artery disease demonstrated by cardiac catheterization or stress testing. The presence of high- or moderate-risk cardiac sources for embolism (as defined by Hart15 ) was determined after review of the electrocardiogram, telemetry, echocardiography, and Holter monitor studies. Lipid disorder was defined as a history of an abnormal lipid profile that required either dietary or pharmacological intervention. Smoking, alcohol, and illicit drug use were documented by quantity-frequency assessment at time of admission and toxicology screen in some patients.
Carotid duplex studies were performed on a Siemens Quantum 2000 ultrasound unit. The degree of stenosis was estimated with B-mode imaging and Doppler flow studies using standard criteria.16 17 TCD studies of intracranial vessels were performed on a Biosound Genesis CFM unit. A stenosis ≥50% was defined as an elevation in PSV by use of standard criteria (PSV >150 cm/s for proximal MCA, PSV >120 cm/s for basilar or vertebral artery, or PSV >90 cm/s for intracranial carotid artery).18 The degree of stenosis by conventional angiography was measured as the percent stenosis at the point of greatest narrowing divided by the luminal dimension in a normal segment of the vessel. For the extracranial carotid artery, the NASCET method for estimating percent stenosis was used.19
MRA was performed on a 1.5-T superconducting magnet (GE Signa) with the use of a protocol of two-dimensional phase-contrast sequences and both two- and three-dimensional time-of-flight sequences. Conventional angiograms and MRAs were reviewed by a single neuroradiologist (H.A.) who was blinded to the clinical data. A moderately severe stenosis was defined as a focal vascular narrowing sufficient to result in >50% observed luminal narrowing, possibly with loss of signal at the region of stenosis. Using similar definitions, other authors have found good correlation between findings on MRA and conventional angiography.20 21 22
Patients were categorized as having an extracranial carotid lesion if a ≥50% stenosis due to atherosclerosis was found by angiography or carotid ultrasound or if MRA suggested a moderately severe stenosis. The origin of the vertebral artery could not be accurately evaluated by either ultrasound or MRA, and because the number of patients with vertebral artery angiography was small, we did not systematically assess atherosclerosis at this site. Patients were considered to have an intracranial lesion if a ≥50% stenosis due to atherosclerosis was found in an intracranial vessel by angiography or TCD or if a moderately severe stenosis was found by MRA. Analyses were also performed with different criteria, including >70% extracranial carotid stenosis, symptomatic extracranial carotid stenosis, symptomatic intracranial stenosis, and number of stenotic lesions.
At the time of discharge, the neurological evaluation of each stroke patient was reviewed by a neurologist (R.J.W.) and classified as to stroke subtype with the TOAST classification.23
The risk factor profile, distribution of stroke subtypes, and location of atherosclerotic lesions were compared between black and white patients. To assess the extent to which different findings between blacks and whites could be due to different levels of diagnostic testing, we compared the percentage of patients who had each diagnostic test by racial groups. Continuous variables were compared with the use of independent t tests. Categorical variables were compared with the use of χ2 or two-tailed Fisher's exact tests when the expected cell counts were <5.
Risk factors that were significantly different between races or that were considered possible determinants for the presence of intracranial or extracranial lesions were chosen as variables in a multivariate analysis. Variables were entered in a stepwise fashion into a multivariate logistic regression model to determine independent predictors of either an extracranial carotid or an intracranial lesion. Statistical significance was defined as an α level of .05 by use of two-tailed tests.
During a 2-year period, 274 patients with ischemic stroke or TIA were evaluated. The mean age was 66.7 years, and 10% of the subjects were younger than 45. The distribution of race and sex was as follows: 32% black women, 28% black men, 22% white men, 17% white women. The majority (71%) of patients studied resided within one of five zip codes surrounding the hospital. During the time period of this study, the racial composition of this area was 59% black, 40% white, and 1% other races.
Risk factors included hypertension (70%), coronary artery disease (33%), diabetes mellitus (30%), smoking (27%), lipid disorder (12%), and recent history of drug abuse (4%). All patients underwent brain imaging, by computed tomography (91%) and/or magnetic resonance imaging (58%). Cardiac evaluation included transthoracic echocardiography (77%), Holter monitor studies (45%), cardiac telemetry (8%), and transesophageal echocardiography (5%).
Neurovascular studies included carotid duplex studies (60%), MRA (49%), conventional angiography (14%), and TCD (14%). The extracranial carotid artery was evaluated in 83% of patients, and the intracranial vessels were evaluated in 57% of patients by at least one modality. Patients who did not have carotid studies performed were more likely to have coronary artery disease (51% versus 28%, P=.003) and were more likely to be classified as having either cardioembolic stroke (31% versus 17%, P<.05) or indeterminate stroke due to incomplete work-up (26% versus 5%, P<.001). Patients who did not have intracranial studies were older (aged 70.0 versus 63.9 years, P=.001), more likely to have coronary artery disease (45% versus 22%, P<.001), and more likely to be classified as having cardioembolic stroke (31% versus 10%, P<.0001) or indeterminate stroke due to incomplete evaluation (15% versus 4%, P<.01). Patients who were moribund on admission had fewer intracranial (12% versus 62%, P<.001) and extracranial carotid studies (42% versus 88%, P<.001) performed than did other patients.
Risk Factors by Race and Sex
There were significant differences in risk factors between races and sexes (Table 1⇓). Blacks tended to be younger and were more likely to smoke cigarettes and have a history of alcohol or drug abuse. White patients were more likely to have coronary artery disease, a high-risk cardiac source for embolism, and TIAs in the absence of stroke. Men were more likely to have alcoholism as a risk factor, and women were more likely to have TIA in the absence of stroke.
Diagnostic Testing by Race and Sex
Black patients were more likely than whites to have echocardiography, magnetic resonance imaging, and MRA studies (Table 2⇓). When all vascular tests were combined, however, blacks and whites had a similar degree of evaluation of either intracranial or extracranial vessels. Men were more likely than women to have MRA and TCD studies, but the use of other tests was similar. When all vascular tests were combined, there was no statistically significant difference between sexes in the evaluation of intracranial or extracranial vessels.
White patients were more than twice as likely as blacks to be classified with cardioembolic stroke when compared by use of the TOAST criteria (Table 3⇓). Other stroke subtypes were similar between races. Men were more likely than women to be classified as having a large artery atherosclerosis or cardioembolic stroke, but this difference did not reach statistical significance.
Extracranial Carotid Artery Lesions
Among patients who underwent evaluation of the extracranial carotid artery, 22% were found to have lesions (6% with occlusion and 16% with stenosis). Seven percent of patients had bilateral lesions. Two thirds of extracranial carotid lesions were symptomatic at the time of admission. Compared with patients without lesions, patients with extracranial carotid lesions tended to be older (69.8 versus 65.0 years, P=.05) and were more likely to present with only TIA (28% versus 15%, P=.05). Patients with extracranial carotid lesions were also less likely to abuse alcohol (2% versus 12%, P=.05). Extracranial carotid disease was determined to be the sole cause for stroke or TIA in 8% of all patients in the study.
Whites were more than twice as likely as blacks to have extracranial carotid lesions (33% of whites versus 15% of blacks, P=.001). These findings were true whether the criteria for extracranial carotid lesion was ≥50% stenosis, ≥70% stenosis (23% of whites versus 9% of blacks, P=.01), or symptomatic stenosis (24% of whites versus 9% of blacks, P=.003). There was no difference between sexes in the presence of extracranial carotid lesions (22% of men versus 21% of women).
Among patients who had intracranial vascular studies performed, 22% were found to have intracranial lesions. There were 34 patients with a total of 46 intracranial lesions (MCA, 14; basilar artery, 8; intracranial carotid artery, 8; posterior cerebral artery, 7; anterior cerebral artery, 5; intracranial vertebral artery, 4). Twenty-seven lesions (59%) were symptomatic (79% of patients with intracranial lesions). Six patients had intracranial occlusions, most of which were in the vertebrobasilar circulation. In all patients with intracranial occlusion, the clinical picture was consistent with large-artery thrombosis, and none had a cardiac source for embolism. Seven patients with intracranial lesions also had extracranial carotid lesions, two of which were symptomatic.
Patients with symptomatic intracranial lesions made up 9% of all patients in the study, and intracranial stenosis was the sole cause of stroke/TIA in 8% of patients. Lesions involving the MCA, basilar artery, or intracranial vertebral artery were more likely to be symptomatic, whereas lesions in the posterior or anterior cerebral arteries were frequently asymptomatic.
The percentage of patients with intracranial lesions was similar between races (24% of whites versus 22% of blacks). There was no significant racial difference when either symptomatic intracranial lesions or multiple lesions were analyzed. Intracranial lesions were more common in men than in women (29% of men versus 14% of women, P=.03), but this difference was not statistically significant when only symptomatic lesions were considered. No association was found between the presence of intracranial lesions and any other risk factor. There was also no correlation found between the intracranial vessel involved and race, sex, or any risk factor, except that patients with carotid siphon stenosis tended to have fewer TIAs than did other patients (10% versus 48%, P=.013).
Relative Distribution of Atherosclerotic Lesions
We examined the relative distribution of disease in the group of patients found to have atherosclerotic occlusive lesions (Figure⇓). Whites had more extracranial carotid lesions than intracranial lesions, and whites were more likely than blacks to have tandem lesions (17% versus 2%, P=.04). Although the prevalence of intracranial lesions was similar between races, the relative distribution of atherosclerotic lesions between extracranial, intracranial, and tandem locations differed significantly (P=.01).
Logistic Regression Analysis
Age, race, sex, hypertension, diabetes, coronary artery disease, smoking, drug abuse, and alcohol abuse were entered as covariates into a stepwise, multivariate logistic regression model to predict the presence of extracranial carotid lesions. White race emerged as the only independent predictor in this study population (OR, 2.85; 95% CI, 2.05 to 3.97). The OR remained significant when all covariates were entered into the model simultaneously. When the same covariates were used in an analysis of intracranial lesions, male sex was found to be an independent predictor of the presence of intracranial lesions (OR, 2.42; 95% CI, 1.60 to 3.66). When the data set was restricted to the 149 patients who had both extracranial and intracranial vascular studies performed, white race continued to be an independent predictor of extracranial lesions, but no factor remained as a predictor for intracranial lesions.
Bauer et al1 first suggested racial differences in the distribution of cerebral atherosclerosis in an angiographic study of patients admitted to a single hospital. Whites were more likely to have occlusive lesions (particularly involving the extracranial carotid artery), whereas blacks tended to have tortuous or dilated vessels with diffuse, nonocclusive atherosclerosis. In the Joint Study of Extracranial Arterial Occlusion,3 whites were twice as likely as blacks to have extracranial carotid disease. In the small number of patients with MCA lesions, blacks were disproportionately represented. The authors were careful to note, however, that patients in the study were not necessarily representative of the general population with stroke.
Gorelick et al6 7 studied the determinants of extracranial versus intracranial atherosclerosis in a series of patients with angiograms of the anterior and posterior circulation. Whites were more likely to have extracranial carotid lesions, TIAs, and lesions at the vertebral artery origin. Blacks were more likely to have lesions involving the intracranial carotid artery, MCA stem, and distal basilar artery. In the largest study to date, Inzitari et al10 used discriminant function analysis of data from the Extracranial/Intracranial Bypass Study to study the influence of race and risk factors on the location of cerebral atherosclerosis in 1367 patients with cerebral angiography. Race was the only factor that remained an independent determinant of location of atherosclerosis. The effect was much greater in Asians than in blacks, with both groups having more intracranial lesions and fewer extracranial lesions than did whites. The authors noted the potential problem of selection bias in their study population but concluded that “angiographic studies cannot be carried out ethically on population samples.”
Autopsy studies only partially support the findings of angiographic studies. Williams et al24 found little difference between blacks and whites in the presence of atherosclerosis of the circle of Willis in autopsy samples from Alabama and Minnesota. Using autopsy material from New Orleans, Solberg and McGarry4 reported that blacks not only had more intracranial atherosclerosis than whites but also more extracranial carotid atherosclerosis (although this latter finding was not statistically significant in all age groups). Lesions were defined as raised atherosclerotic plaques in the vessel wall and did not necessarily imply vascular stenosis or symptomatic lesions. Screening studies in the general population that used ultrasound have found similar degrees of carotid artery plaque and intimal wall thickening in both races but with significant differences in the distribution of lesions within the extracranial carotid artery itself (eg, common carotid artery versus origin of the internal carotid artery).25
In our study, the use of noninvasive vascular tests in addition to cerebral angiography allowed us to assess both the intracranial and extracranial cerebral vasculature in a large proportion of our patients. Unlike other studies performed in tertiary referral centers, our subjects consisted of consecutive admissions to a community hospital of patients with symptoms of cerebral ischemia. The hospital serves a primarily biracial population, so that 60% of our patients were black and 40% were white. The extracranial carotid artery was assessed in 83% of patients, and the intracranial vessels were assessed in 57%. Not surprisingly, patients with probable cardioembolic stroke or patients who were moribund on admission were less likely to have extensive vascular testing performed, but the overall use of vascular testing was not different between races and sexes.
Our findings agree with previous studies that suggested that atherosclerotic occlusive lesions of the extracranial carotid artery are more common in whites than in blacks.1 2 3 7 26 Our finding of a twofold higher prevalence of extracranial carotid lesions in whites is similar to other studies using either angiography or carotid ultrasound.3 11 26 27 This finding was robust and did not change when different criteria for extracranial carotid lesions were used. We could not confirm, however, the suggestion of previous studies that intracranial disease is more common in blacks than in whites. Instead, we found that the percentage of patients with intracranial lesions was similar between races, regardless of whether symptomatic or asymptomatic lesions were considered.
Our results differ in some respects from the results of the Northern Manhattan Stroke Study, in which the distribution of atherosclerosis was studied in a series of white, black, and Hispanic patients.13 In that study, intracranial stenosis was assessed primarily by use of TCD and conventional angiography, and only symptomatic lesions were studied. Unlike our results, Sacco et al13 found no difference between races in the proportion of patients with extracranial atherosclerotic stroke. Intracranial atherosclerotic stroke was associated with younger age, hypercholesterolemia, and insulin-dependent diabetes and was more common in blacks and Hispanics than in whites (unadjusted OR, 7.9; 95% CI, 1.1 to 59). After adjusting for risk factors, however, the association of intracranial atherosclerosis with nonwhite patients was not statistically significant (OR, 4.4; 95% CI, 0.6 to 35), similar to our findings.
Among our patients who had atherosclerotic lesions, the relative distribution of lesions between intracranial and extracranial vessels differed between races (Figure⇑) because of the increased proportion of whites with extracranial or tandem lesions. As a result, whites with atherosclerotic occlusive disease are more likely to have extracranial carotid lesions than intracranial ones, whereas a similar proportion of blacks have intracranial and extracranial lesions. How race influences the distribution of cerebral atherosclerosis is uncertain, because no correlation was found with other risk factors (except sex, as discussed below). Although we found no association of location of lesion with history of known lipid disorder, lipids and lipoprotein concentrations were not systematically measured in our study. Blacks have a different lipid profile than do whites,28 and the presence of carotid artery disease correlates with different apolipoprotein polymorphisms in blacks than in whites.29 Lipoprotein(a) is a lipid component influenced by genetic factors, and lipoprotein(a) concentrations are higher on average in blacks than in whites.30 31 Elevated lipoprotein(a) concentrations are associated with stroke and cerebrovascular atherosclerosis in white32 33 and Asian34 populations, but its importance as a risk factor for stroke in blacks and its influence on the distribution of cerebrovascular lesions are unknown.
We also found that men were more likely than women to have intracranial lesions, despite previous suggestions that the opposite is true.8 This difference remained significant after adjustment for other risk factors but was not statistically significant when only symptomatic intracranial lesions were considered. In the EC/IC Bypass Study,35 there were four times as many men as women with MCA occlusive disease, but few other studies have examined this relationship.
There are few data about the prevalence of intracranial disease among patients admitted to the hospital with stroke or TIA. Among all patients in our study (including those without vascular assessment), 8% had an intracranial lesion as the sole cause of stroke/TIA. An equal percentage of patients (8%) had an extracranial carotid artery lesion as the sole cause of cerebral ischemia. These percentages are likely underestimates, because not all patients had complete vascular assessment and some patients with atherosclerotic lesions had another possible cause of symptoms. Despite some differences in methodology, our results are remarkably similar to those reported in the Northern Manhattan Stroke Study,13 in which stroke was due to extracranial atherosclerosis in 9% of patients and intracranial atherosclerosis in 8% of patients.
There are several limitations to our study. Our subjects consisted of hospital admissions to a single institution with a particular racial mix, and our findings may not be applicable to other populations. Not all patients underwent vascular assessment, particularly of intracranial vessels, which raises the possibility of selection bias. It is likely, however, that there is less selection bias in our study than in previous studies limited to patients undergoing conventional angiography. In addition, we found no significant difference between blacks and whites in terms of the percentage of patients having either extracranial carotid or intracranial vascular studies. Patients who did not have vascular studies were more often either moribund or had a high-risk cardiac source for embolism. From a pragmatic standpoint, assessment of intracranial vessels in these patients would have been unlikely to alter therapy, but had they been assessed, the percentage of patients with symptomatic intracranial lesions might have been greater.
The use of noninvasive technology to assess the vascular anatomy also has limitations. MRA, for example, tends to overestimate the degree of stenosis, and the image can be degraded by movement or flow artifact. More blacks than whites in our study had MRA. If MRA consistently overestimated lesions, this imbalance would tend to increase the percentage of blacks found to have intracranial lesions; despite this potential bias, however, we still did not find more intracranial lesions in blacks, as anticipated. To minimize sources of error when comparing several techniques for vascular assessment, we used standardized criteria to define lesions and accepted as lesions only markedly abnormal findings in patients with good-quality images. Using similar criteria, other studies report a good correlation between MRA and conventional angiography.20 21 22
Our results suggest that in a community hospital with a population similar to ours, intracranial disease may be as common a cause of stroke/TIA as extracranial carotid disease. In contrast to the wealth of information from recent studies concerning the treatment of extracranial carotid artery stenosis, there are limited data concerning effective therapy for intracranial disease. The retrospective Warfarin-Aspirin Symptomatic Intracranial Disease Study36 suggested that patients with intracranial occlusive disease had fewer strokes and vascular events when treated with warfarin than with aspirin, although this benefit was tempered by an increased risk of hemorrhagic complications. With the current availability of noninvasive testing for intracranial vessels, symptomatic intracranial lesions will be detected increasingly, underscoring the need for prospective studies of effective treatment for intracranial occlusive disease.
Selected Abbreviations and Acronyms
|MCA||=||middle cerebral artery|
|MRA||=||magnetic resonance angiography|
|PSV||=||peak systolic velocity|
|TIA||=||transient ischemic attack|
We thank Dorah Brager for assistance with database management and preparation of this manuscript.
- Received June 14, 1996.
- Revision received July 26, 1996.
- Accepted July 26, 1996.
- Copyright © 1996 by American Heart Association
Bauer RB, Sheehan S, Wechsler N, Meyer J. Arteriographic study of sites, incidence, and treatment of arteriosclerotic cerebrovascular lesions. Neurology. 1962;12:698-711.
Heyden S, Heymand A, Goree JA. Nonembolic occlusion of the middle cerebral and carotid arteries: a comparison of predisposing factors. Stroke. 1970;1:363-369.
Gorelick PB, Caplan LR, Hier DB, Parker SL, Patel D. Racial differences in the distribution of anterior circulation occlusive disease. Neurology. 1984;34:54-59.
Gorelick PB, Caplan LR, Hier DB, Patel D, Langenberg P, Pessin MS, Biller J, Kornack D. Racial differences in the distribution of posterior circulation occlusive disease. Stroke. 1985;16:785-790.
Caplan LR, Gorelick PB, Hier DB. Race, sex and occlusive cerebrovascular disease: a review. Stroke. 1986;17:648-655.
Gillum RF. Stroke in blacks. Stroke. 1988;19:1-9.
Gil-Peralta A, Alter M, Lai SM, Fiday G, Otero A, Katz M, Comerota AJ. Duplex Doppler and spectral flow analysis of racial differences in cerebrovascular atherosclerosis. Stroke. 1990;21:740-744.
Kittner SJ, McCarter RJ, Sherwin RW, Sloan MA, Stern BJ, Johnson CJ, Buchholz D, Seipp MJ, Price TR. Black-white differences in stroke risk among young adults. Stroke. 1993;24(suppl I):I-13-I-15.
Sacco RL, Kargman DE, Giu Q, Zamanillo MC. Race-ethnicity and determinants of intracranial atherosclerotic cerebral infarction: the Northern Manhattan Stroke Study. Stroke. 1995;26:14-20.
Friday G, Lai SM, Alter M, Sobel E, LaRue L, Gil-Peralta A, McCoy RL, Levitt LP, Isack T. Stroke in the Lehigh Valley: racial/ethnic differences. Neurology. 1989;39:1165-1168.
Hennerici M, Mohr JP, Rautenberg W, Steinke W. Ultrasound imaging and Doppler sonography in the diagnosis of cerebrovascular diseases. In: Barnett HJM, Mohr JP, Stein BM, Yatsu FM, eds. Stroke: Pathophysiology, Diagnosis, and Management. 2nd ed. New York, NY: Churchill Livingstone; 1992:241-268.
Babikian VL. Transcranial Doppler evaluation of patients with ischemic cerebrovascular disease. In: Babikian VL, Wechsler LR, eds. Transcranial Doppler Ultrasonography. Baltimore, Md: Mosby-Year Book, Inc; 1993:87-104.
Rother J, Wentz KU, Rautenberg W, Schwartz A, Hennerici M. Magnetic resonance angiography in vertebrobasilar ischemia. Stroke. 1993;24:1310-1315.
Mittl RL, Broderick M, Carpenter JP, Goldberg HI, Listerud J, Mishkin MM, Berkowitz HD, Atlas SW. Blinded-reader comparison for magnetic resonance angiography and duplex ultrasonography for carotid artery bifurcation stenosis. Stroke. 1994;25:4-10.
Adams HJ, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE, and the TOAST Investigators. Classification of subtype of acute ischemic stroke: definitions for use in a multicenter clinical trial—TOAST Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993;24:35-41.
Williams O, Resch JA, Loewenaon RB. Cerebral atherosclerosis: a comparative autopsy study between Nigerian Negroes and American Negroes and Caucasians. Neurology. 1969;19:205-210.
Russo LR. Carotid system transient ischemic attacks: clinical, racial, and angiographic correlations. Stroke. 1981;12:470-473.
Ryu JE, Murros K, Espeland MA, Rubens J, McKinney WM, Toole JF, Crouse JR. Extracranial carotid atherosclerosis in black and white patients with transient ischemic attacks. Stroke. 1989;20:1133-1137.
Kasturi R, Yatsu FM, Alam R, Rogers S. Restriction fragment length polymorphism of the apoprotein A-I-C-III gene cluster in control and stroke-prone white and black subjects: racial differences. Stroke. 1992;23:1257-1264.
Parra H-J, Luyeye I, Bouramoue C, Demarquilly C, Fruchart J-C. Black-white differences in serum Lp(a) lipoprotein levels. Clin Chim Acta. 1987;167:27-31.
Schreiner PJ, Morrisett JD, Sharrett AR, Patsch W, Tyroler HA, Wu K, Heiss G. Lipoprotein[a] as a risk factor for preclinical atherosclerosis. Arterioscler Thromb. 1993;13:826-833.
Pedro-Botet J, Senti M, Nogues X, Rubies-Prat J, Roquer J, D'Olhaberriague L, Olive J. Lipoprotein and apolipoprotein profile in men with ischemic stroke: role of lipoprotein(a), triglyceride-rich lipoproteins, and apolipoprotein E polymorphism. Stroke. 1992;23:1556-1562.
Woo J, Lau E, Lam CW, Kay R, Teoh R, Wong HY, Prall WY, Kreel L, Nicholls MG. Hypertension, lipoprotein(a), and apolipoprotein A-I as risk factors for stroke in the Chinese. Stroke. 1991;22:203-208.
Bogousslavsky J, Barnett HJM, Fox AJ, Hachinski VC, Taylor W, for the EC/IC Bypass Study Group. Atherosclerotic disease of the middle cerebral artery. Stroke. 1986;17:1112-1120.
Chimowitz MI, Kokkinos J, Strong J, Brown MB, Levine SR, Silliman S, Pessin MS, Weichel E, Sila CA, Furlan AJ, Kargmen DE, Sacco RL, Wityk RJ, Ford G, Fayad PB, for the Warfarin-Aspirin Symptomatic Intracranial Disease Study Group. The Warfarin-Aspirin Symptomatic Intracranial Disease Study. Neurology. 1995;45:1488-1493.