(Stroke. 2000;31:1062.)
© 2000 American Heart Association, Inc.
Original Contributions |
Ischemic Stroke Subtypes
A Population-Based Study of Functional Outcome, Survival, and Recurrence
From the Division of Cerebrovascular Diseases (G.W.P., R.D.B., J.P.W., D.O.W.) and Department of Health Sciences Research (J.P.W., J.D.S., W.M.O., D.O.W.), Mayo Clinic and Mayo Foundation, Rochester, Minn.
Correspondence to George W. Petty, MD, Division of Cerebrovascular Diseases, Mayo Clinic, 200 First St SW, Rochester, MN 55905. E-mail petty.george{at}mayo.edu
 |
Abstract |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Background and Purpose—There is scant population-based information on functional outcome, survival, and recurrence for ischemic stroke subtypes.
Methods—We identified all residents of Rochester, Minnesota, with a first ischemic stroke from 1985 through 1989 using the resources of the Rochester Epidemiology Project medical records linkage system. After reviewing medical records and imaging studies, we assigned patients to 4 major ischemic stroke categories based on National Institute of Neurological Diseases and Stroke Data Bank criteria: large-vessel cervical or intracranial atherosclerosis with stenosis (ATH, n=74), cardioembolic (CE, n=132), lacunar (LAC, n=72), and infarct of uncertain cause (IUC, n=164). We used the Rankin disability score to assess functional outcome and the Kaplan-Meier product-limit method and Cox proportional hazards regression analysis with bootstrap validation to estimate rates and identify predictors of survival and recurrent stroke among these patients.
Results—Rankin disabilities were different across stroke subtypes at the time of stroke and 3 months and 1 year later (P=0.001). LAC was associated with milder deficits compared with other subtypes. Mean follow-up among the 442 patients in the cohort was 3.2 years. Estimated rates of recurrent stroke at 30 days were significantly different (P<0.001): ATH, 18.5% (95% CI 9.4% to 27.5%); CE, 5.3% (95% CI 1.2% to 9.6%); LAC, 1.4% (95% CI 0.0% to 4.1%); and IUC, 3.3% (95% CI 0.4% to 6.2%). After adjusting for age, sex, and stroke severity, infarct subtype was an independent determinant of recurrent stroke within 30 days (P=0.0006; eg, risk ratio for ATH compared with CE=3.3, 95% CI 1.2 to 9.3) but not long term (P=0.07). Four of 25 recurrent strokes within 30 days were procedure-related, each in patients with ATH. Five-year death rates were significantly different (P<0.001): ATH, 32.2% (95% CI 21.1% to 43.2%); CE, 80.4% (95% CI 73.1% to 87.6%); LAC, 35.1% (95% CI 23.6% to 46.0%); and IUC, 48.6% (95% CI 40.5% to 56.7%). With adjustment for age, sex, cardiac comorbidity, and stroke severity, the subtype of ischemic stroke was an independent determinant of long-term (P=0.018; eg, risk ratio for ATH compared with cardioembolic=0.47, 95% CI 0.29 to 0.77) but not 30-day survival (P=0.2).
Conclusions—Early recurrence rates for ischemic stroke caused by ATH are higher than those for other subtypes and higher than previous non–population-based studies have reported. Some of the increased risk of early recurrence among patients with ATH may be iatrogenic. Patients with LAC have better poststroke functional status than those with other subtypes. Survival is poorest among those with ischemic stroke with a cardiac source of embolism.
Key Words: cardioembolic stroke • carotid artery diseases • cerebral embolism • epidemiology • lacunar infarction • survival • thrombosis
|
Introduction |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Studies of survival and recurrence after stroke have been reported from numerous sites worldwide,1 2 3 4 5 but there is scant population-based information on outcomes for individual subtypes of ischemic stroke. Comparison of functional outcome and survival and recurrence rates for specific ischemic stroke mechanisms could allow clinicians to identify patients who are at higher risk for stroke recurrence and death, assist investigators in designing future clinical trials of tertiary stroke prevention, and permit health care policy investigators to quantify the societal burden attributable to individual pathophysiological mechanisms of ischemic stroke. We undertook a population-based outcomes study of all residents of Rochester, Minnesota, who had a first ischemic stroke from 1985 through 1989 to assess functional outcome and to estimate and compare rates and identify determinants of recurrence and death for patients with common ischemic stroke subtypes.
|
Subjects and Methods |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Study Population
The Rochester Epidemiology Project medical records linkage system provides resources to identify nearly all new cases of stroke in a community.6 Virtually all medical care in the community is supplied by the Mayo Clinic and its affiliated hospitals or by the Olmsted Medical Group, a smaller group practice, and its hospital. In these institutions, all medical diagnoses made for a resident of the local region are entered into the patient’s medical record, which is then entered into a central computer index. The index includes diagnoses made on region residents at other medical practices in surrounding communities, the University of Minnesota, and the Veterans Administration Hospital in Minneapolis. This index provides access to all inpatient and outpatient data, emergency department visits, nursing home care, and autopsy or death certificate information.
The population of Rochester is 96% white and 51% female. Median age is 31.5 years, compared with 32.9 years in the US population. Education includes 88% high school graduates (75.2%, United States) and 29.5% college graduates (20.3%, United States). The proportion of families with income less than poverty level was 6.9%, compared with 10% for the United States7 Population-based studies of stroke in Rochester are approved by the Mayo Foundation Institutional Review Board.
The medical records of all residents of Rochester who had a diagnosis of stroke or transient ischemic attack or a diagnosis that could be mistaken for stroke or transient ischemic attack during the 5-year period from January 1, 1985, through December 31, 1989, were screened by a neurologist and a trained nurse abstractor to determine whether the case met the criteria for stroke. All identified cases then had verification of residence based on information from city and county directories and earlier medical records. To exclude persons who might have moved to the region to facilitate treatment or diagnosis of an existing disorder, cases were eligible only if the person had been a resident of Rochester for at least 1 year before the stroke. Death certificates and autopsy protocols were also reviewed to identify those with a diagnosis of stroke. The clinical record was then reviewed to determine whether there were any clinical symptoms consistent with stroke. Patients with a clinical diagnosis of stroke or those who had stroke listed as a cause of death on the death certificate who died within 24 hours of symptom onset were excluded if there was no clinical evidence of a focal neurological deficit, no CT or MRI performed, or no autopsy performed. The type of stroke was also determined by using imaging studies and autopsy when available. Definitions of first stroke (hemorrhage or infarction) appear elsewhere1 and are identical to the definitions used in previous studies of stroke incidence, survival, and recurrence in the study region.
A neurologist and a nurse abstractor abstracted the medical record
of each patient in this cohort and recorded on standardized forms
information regarding stroke risk factors and functional status before
or at the time of first cerebral infarction and diagnostic
studies, treatment, and dates of last follow-up and death after the
stroke but before January 1, 1993. A list and definitions of the stroke
risk factors that were recorded have been published
elsewhere.8 9 One study neurologist (G.W.P.) reviewed the
clinical history, neurological examination, diagnostic
studies, and brain imaging studies or
neuroradiology reports of all patients and
assigned infarct subtype classifications by the use of clinical and
radiographic diagnostic rubrics similar to
those of the National Institute of Neurological Diseases and Stroke:
cardioembolic, large-vessel cervical or intracranial
atherosclerosis with occlusion or stenosis of
50%, lacunar, other unusual causes (such as dissection, vasculitis,
and so on), and uncertain cause.9 10 11 Patients with a
cardiac source of embolism had 1 of the following
conditions9 : (1) congestive heart failure at stroke onset,
(2) myocardial infarction within 2 months before stroke onset, (3)
hemodynamically significant mitral valve disease, (4)
prosthetic mitral or aortic valve, (5) atrial fibrillation or
flutter, (6) cardiomyopathy, (7) congenital heart
disease, (8) recent systemic arterial emboli, (9) stroke
within 48 hours after coronary artery bypass surgery, (10)
stroke within 48 hours after left ventricular
aneurysm surgery, (11) stroke related to cardiac
catheterization or pacemaker installation, (12) left
ventricular aneurysm, (13) intracardiac thrombus,
(14) valvular vegetations, (15) sick sinus syndrome, (16)
autopsy evidence of recent myocardial infarction that could be dated at
the time of or before the stroke, (17) autopsy evidence of rheumatic
heart disease, (18) autopsy evidence of recent systemic
arterial emboli that could be dated at the time of or
before the stroke, and (19) autopsy evidence of embolic occlusion of an
intracerebral vessel with little or no evidence of
cervical or intracranial atherosclerotic arterial disease.
Patients with large-vessel cervical or intracranial
atherosclerosis with occlusion or stenosis had
either occlusion or 50% stenosis of a cervicocephalic artery
(carotid, vertebral, basilar, middle cerebral, anterior cerebral, or
posterior cerebral) supplying the vascular territory of the stroke
documented by ultrasound, transcranial Doppler,
oculopneumoplethysmography, cerebral angiography, magnetic resonance
angiography, or autopsy. Patients with lacunar stroke had clinical
syndromes consistent with pure motor stroke, pure sensorimotor
stroke, pure sensory stroke, ataxic hemiparesis, or clumsy hand
dysarthria. Brain CT or MRI among patients with lacunar stroke
demonstrated either no lesion to explain the syndrome or a deep
ischemic stroke in a location consistent with the
clinical syndrome 
15 mm in size. Brain CT, MRI, or autopsy was
performed in 92% of residents of the study region with first stroke
during the time period of this study,7 and all brain
autopsy reports and >98% of brain images were available for review by
the study neurologist at the time of infarct subtype
classification.8 12
Recurrent stroke was defined as a new neurological deficit fitting the
definitions for ischemic or hemorrhagic stroke, occurring after
a period of unequivocal neurological stability or improvement lasting
24 hours and not attributable to edema, mass effect, brain shift
syndrome, or hemorrhagic transformation of the incident cerebral
infarction. All recurrences within 30 days were adjudicated by
2 study neurologists. Autopsy documentation of recent infarction in a
vascular territory different from that of the incident infarction was
counted as a recurrence if the date of the recurrent stroke
could be estimated.1
The Rankin Disability Scale was used to measure functional status before the stroke, the maximal severity of neurological deficits within the first 7 days after the stroke, and functional outcome after first cerebral infarction 3 months and 1 year after the stroke: grade 1, no significant disability, able to perform all usual duties of daily living; grade 2, slight disability, unable to perform some previous activities but able to look after own affairs without assistance; grade 3, moderate disability, requiring some help but able to walk without assistance; grade 4, moderately severe disability, unable to walk and to attend to own bodily needs without assistance; and grade 5, severe disability, bedridden, incontinent, and requiring constant nursing care and attention.13
Statistical Analysis
Patients with uncommon causes of stroke such as vasculitis,
hypercoagulable state as the result of underlying malignancy, and
dissection were excluded from the analysis because of the small
number of subjects. The 
2 test was used to
compare Rankin scores and treatments among the subtypes. The
Kaplan-Meier product-limit method14 was used to
estimate rates of survival and recurrent stroke after first cerebral
infarction for the 4 common ischemic stroke subtypes (cervical
or intracranial large-vessel atherosclerosis with
stenosis, cardioembolic, lacunar, and ischemic stroke
of uncertain cause). Patients were censored at the time of migration
from our locale or at the time of last follow-up or at January 1, 1993.
The log-rank test was used to compare rate estimates and the Cox
proportional hazards model15 was used to estimate the
impact in terms of risk ratios of possible determinants of survival and
recurrent stroke after first cerebral infarction. Previously
published1 multivariable proportional hazards models
of survival and recurrence after first ischemic stroke
in our community were used as the foundation on which the impact of
stroke subtype and Rankin score were assessed. Thus, stroke subtype (4
groups) and maximal deficit Rankin score (3 groups) were "added" to
the existing models.
|
Results |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
First ischemic stroke occurred in 454 residents of Rochester during the time period of the study. Three hundred sixty-two (80%) patients were hospitalized and 342 (75%) were evaluated by a neurologist. Transthoracic or transesophageal echocardiography was performed in 227 (50%) patients. Carotid ultrasound, oculopneumoplethysmography, transcranial Doppler ultrasonography, or cerebral angiography was performed in 54.4% of patients.
Each of the ischemic strokes was assigned a subtype: large-vessel cervical or intracranial atherosclerosis with stenosis, 74 (16%); cardioembolic, 132 (29%); lacunar, 72 (16%); uncertain cause, 164 (36%); and other or unusual causes, 12 (3%). Patients with unusual cause of stroke were excluded from the subsequent analysis, leaving 442 patients in the study group. The mean age and frequencies of cardiac and noncardiac risk factors for each subtype in this cohort have been published previously in a study of subtype incidence.8 The proportions of patients in the subgroups who received aspirin after incident ischemic stroke were different (P=0.001): atherosclerosis with stenosis, 37 (50.0%); cardioembolic, 31 (23.5%); lacunar, 51 (70.8%); and unknown cause 79 (48.2%). The proportions of patients in the subgroups who received intravenous heparin after incident ischemic stroke were different (P=0.004): atherosclerosis with stenosis, 36 (48.6%); cardioembolic, 46 (34.8%); lacunar, 29 (40.3%); and unknown cause, 42 (25.6%). The proportions of patients in the subgroups who received warfarin after incident ischemic stroke were different (P=0.006): atherosclerosis with stenosis, 16 (21.6%); cardioembolic, 43 (32.6%); lacunar, 12 (16.7%); and unknown cause, 25 (15.2%).
Functional Outcome
Table 1
presents the
Rankin scores among the 442 patients with common ischemic
stroke subtypes before the stroke, at maximal neurological deficit at
the time of stroke, and after the stroke. Patients with lacunar
ischemic stroke had milder maximal neurological deficits and
better poststroke Rankin scores compared with patients with other
subtypes. Patients with cardioembolic stroke had poorer prestroke
functional status, more severe neurological deficits at the time of
stroke, and poorer functional outcome compared with other subtypes.
|
Recurrence
During 1425 person-years of follow-up, 110 patients among the 4
common subtypes had recurrent stroke. Seventy-five (68.2%) of these
recurrent strokes were of the same subtype as the incident stroke.
Table 2 and Figure 1 present the Kaplan-Meier estimates
of recurrent stroke for the different subtypes. Twenty-five patients
had recurrent stroke within 30 days, 13 of whom had large-vessel
atherosclerosis with stenosis as the first
stroke subtype. All 30-day recurrent strokes were ischemic.
Four 30-day recurrent strokes were procedure related (cerebral
angiography in 2, carotid endarterectomy in 1,
axillary-axillary bypass in 1 patient with bilateral carotid, and left
vertebral artery occlusions in 1), all among patients with large-vessel
atherosclerosis with stenosis. Ischemic
stroke subtype was a significant predictor of 30-day recurrence
both before (log-rank P=0.0001) and after
(P=0.0006) adjusting for age, sex, and stroke severity
(maximal Rankin score) with use of the proportional hazards model
(Table 3). Ischemic stroke
subtype was not a significant predictor of long-term recurrence
before (log-rank P=0.12) or after (P=0.07)
adjusting for age, stroke severity, and diabetes mellitus with the
proportional hazards model (Table 3).
|
|
|
Survival
Two hundred forty-five patients died during follow-up. Table 4 and Figure 2 present the Kaplan-Meier estimates
of rates of death for the different stroke subtypes. Ischemic
stroke subtype was a significant predictor of 30-day survival before
(log-rank P=0.0001) but not after (P=0.2)
adjusting for age, congestive heart failure, and stroke severity with
the proportional hazards model (Table 5).
Ischemic stroke subtype was a significant predictor of
long-term survival both before (log-rank P=0.0001) and after
(P=0.018) adjusting for age, atrial fibrillation, congestive
heart failure, ischemic heart disease, and stroke severity with
the proportional hazards model (Table 5).
|
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The importance of our study is that it reports outcomes for the 4 common subtypes of ischemic stroke among all residents in a community. The population-based nature of our study limits bias inherent to studies derived from patients who were evaluated at tertiary care centers after referral from inside or outside the community or community-based studies of patients who were referred for hospitalization or evaluation by stroke neurologists. No patients were excluded on the basis of race, age, sex, risk factors, prognosis, or whether or not they were hospitalized, enrolled in a prospective study, or evaluated by a neurologist or cerebrovascular specialist. By including only patients with first stroke, our study eliminates a potential bias common to studies that may have included patients who were selected for referral to study centers because they had single or multiple recurrent cerebral ischemic events.
The unique population-based, subtype-specific, 30-day death rates
(case-fatality rates) appearing in Table 4
and the previously
reported subtype-specific incidence rates derived from this cohort
permit estimation of the annual mortality rates in this country
attributable to each incident stroke subtype.8 16
Approximately 32 724 Americans die each year of a first stroke with a
cardiac source of embolism, 5494 of large-vessel
atherosclerosis with stenosis, 1078 of lacunar
stroke, and 21 560 of ischemic stroke of unknown cause. These
figures underscore the societal importance of research into stroke
cause and primary stroke prevention.
Another important result of our study is the quantification of the magnitude of the risk of early recurrence associated with ischemic stroke due to large-vessel atherosclerosis with stenosis. More than 18% of patients with this subtype had a recurrent stroke within 30 days of the first stroke, higher than the range of 8% to 14% reported in previous hospital-based studies.2 17 18 Our 1-month recurrence rate among patients with this subtype is actually higher than the 3-month recurrence rate of 13% reported recently by Moroney et al.17 Although these variations in recurrence rates may be due to differences in age, sex, race,19 and risk factors among study subjects, we believe methodological differences between studies are a more likely explanation. In addition to the advantages that a population-based study of incident stroke cases has over hospital-based or referral-based studies that include cases of nonincident stroke, differences in definitions (that is, the degree of stenosis sufficient for classification as ischemic stroke due to large-vessel atherosclerosis) and analysis may account for our higher early recurrence rates for patients with large-vessel atherosclerosis with stenosis. In a Stroke Data Bank study of early recurrence, for example, patients were censored at the time of a recurrence related to a procedure, and recurrent stroke was defined as a new deficit that occurred only in a different anatomic or vascular territory from that of the index stroke.18 If a stenotic or occluded artery that has recently given rise to distal embolization or hemodynamic compromise is likely to do so again, as is the assumption behind the rationale for carotid endarterectomy, then excluding recurrences in the same vascular territory as that of the index stroke would guarantee relatively lower recurrence rates for patients with stroke due to large-vessel atherosclerosis with stenosis. Also, if procedure-related recurrences are overrepresented among patients with large-vessel atherosclerosis, as was the case in our cohort, censoring patients at the time of a procedure-related recurrence could also guarantee that recurrence rates for this subtype will be underestimated relative to other subtypes in which procedures such as cerebral angiography and vascular surgery are not likely to be performed. We chose to include procedure-related events as an end point in the recurrence analysis because these procedures are part of a process that clinicians use to select and effect treatment for patients with symptomatic large-vessel atherosclerosis with stenosis. Complications of these procedures, although not a measure of efficacy, are a determinant of effectiveness and thus a potentially important determinant of outcome. Our findings raise the possibility that iatrogenic stroke may not be an insignificant factor contributing to recurrent stroke among patients with large-vessel atherosclerosis with stenosis in the general population, despite the results of the North American Symptomatic Endarterectomy Trial, which demonstrated the efficacy of endarterectomy for stroke prevention among patients with symptomatic carotid bifurcation stenosis.20
Our multivariate model of long-term recurrence
did not identify ischemic stroke subtype as a determinant of
recurrent stroke (Table 3), in contrast to the referral-based
Stroke Data Bank study of Hier et al,21 which identified
ischemic stroke of unknown cause as a predictor of survival
free of recurrent stroke. We believe that the differences between our
findings and those of the Stroke Data Bank in this regard again most
likely relate to differences in methodology and definitions of
recurrent stroke (see above).
Our study also demonstrates significant differences among subtypes not
only for maximal neurological deficits at the time of stroke and
functional outcome at 3 months and 1 year but also for prestroke
functional status (Table 1). Prestroke functional status was
best among those destined to have lacunar stroke or ischemic
stroke due to large-vessel atherosclerosis with
stenosis and worst among those who subsequently had
cardioembolic stroke. These differences probably reflect a higher
prevalence of heart disease and cardiac-related prestroke disability
among those with cardioembolic stroke. Patients with lacunar infarction
and stroke due to large-vessel atherosclerosis with
stenosis had remarkably similar prestroke Rankin score
distributions, but maximal neurological deficits at the time of the
stroke were far worse among patients with large-vessel stenosis
compared with those with lacunar infarction. Patients with lacunar
infarcts had the best functional outcomes, with >80% having minimal
or no impairment 1 year after the stroke.
Consistent with previous studies of our
population9 from earlier time periods, we found that
patients with cardioembolic stroke had worse 30-day and long-term
survival than patients with noncardioembolic stroke (Table 4,
Figure 2). For example, patients with cardioembolic stroke in
our population are nearly 4 times more likely to be dead 30 days after
the stroke than patients with stroke due to large-vessel
atherosclerosis with stenosis and 2.5 times
more likely to be dead 5 years later. Our results in this regard stand
in contrast to the results of the Northern Manhattan Stroke
Study,2 which found similar 30-day and 5-year survival
rates for patients with cardioembolic stroke and ischemic
stroke due to large-vessel atherosclerosis with
stenosis. These differences could reflect differences in age,
sex, race, and risk factor distributions between the populations of our
study region and Northern Manhattan, or they may be due to
methodological differences between the 2 studies. Our study included
all patients with ischemic stroke in the community, whether or
not they were hospitalized, whereas the Northern Manhattan study
included only hospitalized patients. Exclusion of nonhospitalized
patients in a study of survival after stroke may introduce significant
bias.22
A striking finding of our survival model is that ischemic
stroke due to atherosclerosis with stenosis is
associated with better long-term survival than cardioembolic stroke,
even after adjustment for age, sex, atrial fibrillation,
ischemic heart disease, congestive heart failure, and stroke
severity (Table 5). This finding is difficult to explain on the
basis of generally held concepts about the influence of
atherosclerosis and survival and is especially puzzling
given the higher 30-day recurrence rates among patients with
large-vessel atherosclerosis coupled with our previous
finding that recurrence is an important independent determinant
of death.1 It suggests that additional unrecognized risk
factors, unaccounted for in our model, which may be relatively
underrepresented or overrepresented among
patients with cardioembolic stroke or patients with large-vessel
atherosclerosis with stenosis, could influence
survival among these patients.
In summary, early recurrence rates for ischemic stroke due to large-vessel atherosclerosis with stenosis are higher than those for other subtypes and higher than previous non–population-based studies have reported. Some of the increased risk of early recurrence among patients with large-vessel stenosis may be iatrogenic. Patients with cardioembolic stroke have worse prestroke and poststroke functional status than do those with other subtypes. Survival is poorest among those with ischemic stroke with a cardiac source of embolism and best among those with large-vessel atherosclerosis with stenosis, even after adjustment for stroke severity and cardiac comorbidity.
|
Acknowledgments |
|---|
This study was supported by the National Institute of Neurological Disorders and Stroke (NS06663), the Agency for Health Care Policy Research (282-91-0028), and the National Institutes of Health and United States Public Health Service (AR30582). The authors thank Dr D.G. Piepgras for reviewing the manuscript.
Received November 30, 1999; revision received February 4, 2000; accepted February 4, 2000.
|
References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. Petty GW, Brown RD Jr, Whisnant JP, Sicks JD, O’Fallon WM, Wiebers DO. Survival and recurrence after first cerebral infarction: a population-based study in Rochester, Minnesota, 1975 through 1989. Neurology. 1998;50:208–216.
2.
Sacco RL, Shi T, Zamanillo MC, Kargman DE. Predictors
of mortality and recurrence after hospitalized cerebral
infarction in an urban community: the Northern Manhattan Stroke Study.
Neurology. 1994;44:626–634.
3.
Sacco RL, Wolf PA, Kannel WB, McNamara PM. Survival
and recurrence following stroke: the Framingham study.
Stroke. 1982;13:290–295.
4. Burn J, Dennis M, Bamford J, Sandercock P, Wade D, Warlow C. Long-term risk of recurrent stroke after a first-ever stroke: the Oxfordshire Community Stroke Project. Stroke.. 1994;25:333–337.[Abstract]
5.
Hankey GJ, Jamrozik K, Broadhurst RJ, Forbes S,
Burvill PW, Anderson CS, Stewart-Wynne EG. Long-term risk of first
recurrent stroke in the Perth Community Stroke Study.
Stroke. 1998;29:2491–2500.
6. Melton LJ III. History of the Rochester Epidemiology Project. Mayo Clin Proc. 1996;71:266–274.[Abstract]
7. Brown RD, Whisnant JP, Sicks JD, O’Fallon WM, Wiebers DO. Stroke incidence, prevalence, and survival: secular trends in Rochester, Minnesota, through 1989. Stroke. 1996;27:373–380.
8.
Petty GW, Brown RD Jr, Whisnant JP, Sicks JD,
O’Fallon WM, Wiebers DO. Ischemic stroke subtypes: a
population-based study of incidence and risk factors.
Stroke. 1999;30:2513–2516.
9.
Broderick JP, Phillips SJ, O’Fallon WM, Frye RL,
Whisnant JP. Relationship of cardiac disease to stroke occurrence,
recurrence, and mortality. Stroke. 1992;23:1250–1256.
10.
Kunitz SC, Gross CR, Heyman A, Kase CS, Mohr JP, Price
TR, Wolf PA. The pilot Stroke Data Bank: definition, design, and data.
Stroke. 1984;15:740–746.
11.
Broderick J, Brott T, Kothari R, Miller R, Khoury J,
Panicioli A, Gebel J, Mills D, Minneci L, Shukla R. The Greater
Cincinnati/Northern Kentucky Stroke Study: preliminary first-ever and
total incidence rates of stroke among blacks. Stroke. 1998;29:415–421.
12.
Ince B, Petty GW, Brown RD Jr, Chu CP, Sicks JD,
Whisnant JP. Dolichoectasia of the intracranial arteries in patients
with first ischemic stroke: a population-based study.
Neurology. 1998;50:1694–1698.
13. Rankin J. Cerebral vascular accidents in patients over the age of 60, I: general considerations. Scott Med J. 1957;2:127–136.[Medline] [Order article via Infotrieve]
14. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53:457–481.
15. Cox DR. Regression models and life-tables. J R Stat Soc [B]. 1972;34:187–202.
16.
Woo D, Gebel J, Miller R, Kothari R, Brott T, Khoury J,
Salisbury S, Shukla R, Pancioli A, Jauch E, Broderick J. Incidence
rates of first-ever ischemic stroke subtypes among blacks: a
population-based study. Stroke. 1999;30:2517–2522.
17.
Moroney JT, Bageila E, Paik MC, Sacco RL, Desmond DW.
Risk factors for early recurrence after ischemic
stroke: the role of stroke syndrome and subtype. Stroke. 1998;29:2118–2124.
18.
Sacco RL, Foulkes MA, Mohr JP, Wolf PA, Hier DB, Price
TR. Determinants of early recurrence of cerebral infarction:
the Stroke Data Bank. Stroke.. 1989;20:983–989.
19.
Sacco RL, Hauser WA, Mohr JP, Foulkes MA. One-year
outcome after cerebral infarction in whites, blacks, and Hispanics.
Stroke. 1991;22:305–311.
20. North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med. 1991;325:445–453.[Abstract]
21.
Hier DB, Foulkes MA, Swiontoniowski M, Sacco RL,
Gorelick PB, Mohr JP, Price TR, Wolf PA. Stroke recurrence
within 2 years after ischemic infarction. Stroke. 1991;22:155–161.
22. Bonita R, Beaglehole R. Explaining stroke mortality trends. Lancet. 1993;341:1510–1511.[Medline] [Order article via Infotrieve]
This article has been cited by other articles:
 |
|
 |
|
  C. Ellis Does Race/Ethnicity Really Matter in Adult Neurogenics? Am J Speech Lang Pathol, November 1, 2009; 18(4): 310 - 314. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Putaala, S. Curtze, S. Hiltunen, H. Tolppanen, M. Kaste, and T. Tatlisumak Causes of Death and Predictors of 5-Year Mortality in Young Adults After First-Ever Ischemic Stroke: The Helsinki Young Stroke Registry Stroke, August 1, 2009; 40(8): 2698 - 2703. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. M. Famakin, M. I. Chimowitz, M. J. Lynn, B. J. Stern, M. G. George, and for the WASID Trial Investigators Causes and Severity of Ischemic Stroke in Patients With Symptomatic Intracranial Arterial Stenosis Stroke, June 1, 2009; 40(6): 1999 - 2003. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Amarenco, O. Benavente, L. B. Goldstein, A. Callahan III, H. Sillesen, M. G. Hennerici, S. Gilbert, A. E. Rudolph, L. Simunovic, J. A. Zivin, et al. Results of the Stroke Prevention by Aggressive Reduction in Cholesterol Levels (SPARCL) Trial by Stroke Subtypes Stroke, April 1, 2009; 40(4): 1405 - 1409. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Bejot, D. B. Salem, G. V. Osseby, G. Couvreur, J. Durier, C. Marie, Y. Cottin, T. Moreau, and M. Giroud Epidemiology of ischemic stroke from atrial fibrillation in Dijon, France, from 1985 to 2006 Neurology, January 27, 2009; 72(4): 346 - 353. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y Bejot, M Caillier, D Ben Salem, G Couvreur, O Rouaud, G-V Osseby, J Durier, C Marie, T Moreau, and M Giroud Ischaemic stroke subtypes and associated risk factors: a French population based study J. Neurol. Neurosurg. Psychiatry, December 1, 2008; 79(12): 1344 - 1348. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Talelli and R. J. Greenwood Review: Recurrent stroke: where do we stand with the secondary prevention of noncardioembolic ischaemic strokes? Therapeutic Advances in Cardiovascular Disease, October 1, 2008; 2(5): 387 - 405. [Abstract] [PDF]
|
|
|
|
 |
|
 K. Fatema, K. R. Bailey, G. W. Petty, I. Meissner, M. Osranek, A. A. Alsaileek, B. K. Khandheria, T. S. Tsang, and J. B. Seward Increased Left Atrial Volume Index: Potent Biomarker for First-Ever Ischemic Stroke Mayo Clin. Proc., October 1, 2008; 83(10): 1107 - 1114. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. E. Wysokinski, R. D. McBane, P. R. Daniels, S. C. Litin, D. O. Hodge, N. F. Dowling, and J. A. Heit Periprocedural Anticoagulation Management of Patients With Nonvalvular Atrial Fibrillation Mayo Clin. Proc., June 1, 2008; 83(6): 639 - 645. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A Arboix, A Font, C Garro, L Garcia-Eroles, E Comes, and J Massons Recurrent lacunar infarction following a previous lacunar stroke: a clinical study of 122 patients J. Neurol. Neurosurg. Psychiatry, December 1, 2007; 78(12): 1392 - 1394. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. A. Wolf and W. B. Kannel Preventing Stroke: Does Race/Ethnicity Matter? Circulation, November 6, 2007; 116(19): 2099 - 2100. [Full Text] [PDF]
|
|
|
|
|
|
H. Kunte, S. Schmidt, M. Eliasziw, G. J. del Zoppo, J. M. Simard, F. Masuhr, M. Weih, and U. Dirnagl Sulfonylureas Improve Outcome in Patients With Type 2 Diabetes and Acute Ischemic Stroke Stroke, September 1, 2007; 38(9): 2526 - 2530. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Prabhakaran, J. Y. Chong, and R. L. Sacco Impact of Abnormal Diffusion-Weighted Imaging Results on Short-term Outcome Following Transient Ischemic Attack Arch Neurol, August 1, 2007; 64(8): 1105 - 1109. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Benbassat and R. Baumal The time horizons of formal decision analyses QJM, June 1, 2007; 100(6): 383 - 388. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Gongora-Rivera, J. Labreuche, A. Jaramillo, P. G. Steg, J.-J. Hauw, and P. Amarenco Autopsy Prevalence of Coronary Atherosclerosis in Patients With Fatal Stroke Stroke, April 1, 2007; 38(4): 1203 - 1210. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Banks and C. A. Marotta Outcomes Validity and Reliability of the Modified Rankin Scale: Implications for Stroke Clinical Trials: A Literature Review and Synthesis Stroke, March 1, 2007; 38(3): 1091 - 1096. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D.-W. Kang, S. U. Kwon, S.-H. Yoo, K.-Y. Kwon, C. G. Choi, S. J. Kim, J.-Y. Koh, and J. S. Kim Early Recurrent Ischemic Lesions on Diffusion-Weighted Imaging in Symptomatic Intracranial Atherosclerosis Arch Neurol, January 1, 2007; 64(1): 50 - 54. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Nedeltchev, U. Fischer, M. Arnold, P. Ballinari, T. Haefeli, L. Kappeler, C. Brekenfeld, L. Remonda, G. Schroth, and H. P. Mattle Long-Term Effect of Intra-Arterial Thrombolysis in Stroke Stroke, December 1, 2006; 37(12): 3002 - 3007. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Prabhakaran, T. Rundek, R. Ramas, M. S.V. Elkind, M. C. Paik, B. Boden-Albala, and R. L. Sacco Carotid Plaque Surface Irregularity Predicts Ischemic Stroke: The Northern Manhattan Study Stroke, November 1, 2006; 37(11): 2696 - 2701. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Kubo, Y. Kiyohara, T. Ninomiya, Y. Tanizaki, K. Yonemoto, Y. Doi, J. Hata, Y. Oishi, K. Shikata, and M. Iida Decreasing incidence of lacunar vs other types of cerebral infarction in a Japanese population Neurology, May 23, 2006; 66(10): 1539 - 1544. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. R. Kizer, D. O. Wiebers, J. P. Whisnant, J. M. Galloway, T. K. Welty, E. T. Lee, L. G. Best, H. E. Resnick, M. J. Roman, and R. B. Devereux Mitral Annular Calcification, Aortic Valve Sclerosis, and Incident Stroke in Adults Free of Clinical Cardiovascular Disease: The Strong Heart Study Stroke, December 1, 2005; 36(12): 2533 - 2537. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Jackson and C. Sudlow Comparing risks of death and recurrent vascular events between lacunar and non-lacunar infarction Brain, November 1, 2005; 128(11): 2507 - 2517. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. L. Paul, J. W. Sturm, H. M. Dewey, G. A. Donnan, R. A.L. Macdonell, and A. G. Thrift Long-Term Outcome in the North East Melbourne Stroke Incidence Study: Predictors of Quality of Life at 5 Years After Stroke Stroke, October 1, 2005; 36(10): 2082 - 2086. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. C. Kaplan, D. L. Tirschwell, W. T. Longstreth Jr, T. A. Manolio, S. R. Heckbert, D. Lefkowitz, A. El-Saed, and B. M. Psaty Vascular events, mortality, and preventive therapy following ischemic stroke in the elderly Neurology, September 27, 2005; 65(6): 835 - 842. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O Y Bang, P H Lee, K G Heo, U S Joo, S R Yoon, and S Y Kim Specific DWI lesion patterns predict prognosis after acute ischaemic stroke within the MCA territory J. Neurol. Neurosurg. Psychiatry, September 1, 2005; 76(9): 1222 - 1228. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. B. Coutts, M. D. Hill, J. E. Simon, C. -H. Sohn, J. N. Scott, A. M. Demchuk, and for the VISION Study Group Silent ischemia in minor stroke and TIA patients identified on MR imaging Neurology, August 23, 2005; 65(4): 513 - 517. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. W. Petty, B. K. Khandheria, J. P. Whisnant, J. D. Sicks, W. M. O'Fallon, and D. O. Wiebers Outcomes Among Valvular Heart Disease Patients Experiencing Ischemic Stroke or Transient Ischemic Attack in Olmsted County, Minnesota Mayo Clin. Proc., August 1, 2005; 80(8): 1001 - 1008. [Abstract] [PDF]
|
|
|
|
|
|
J Hata, Y Tanizaki, Y Kiyohara, I Kato, M Kubo, K Tanaka, K Okubo, H Nakamura, Y Oishi, S Ibayashi, et al. Ten year recurrence after first ever stroke in a Japanese community: the Hisayama study J. Neurol. Neurosurg. Psychiatry, March 1, 2005; 76(3): 368 - 372. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Christensen and P. M. Rothwell Early Recurrent Stroke or Neurological Deterioration? * Response Stroke, February 1, 2005; 36(2): 231 - 232. [Full Text] [PDF]
|
|
|
|
|
|
D.-W. Kang, L. L. Latour, J. A. Chalela, J. A. Dambrosia, and S. Warach Early and late recurrence of ischemic lesion on MRI: Evidence for a prolonged stroke-prone state? Neurology, December 28, 2004; 63(12): 2261 - 2265. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. U. Heuschmann, P. L. Kolominsky-Rabas, B. Misselwitz, P. Hermanek, C. Leffmann, R. W. C. Janzen, J. Rother, H.-J. Buecker-Nott, K. Berger, and for The German Stroke Registers Study Group Predictors of In-Hospital Mortality and Attributable Risks of Death After Ischemic Stroke: The German Stroke Registers Study Group Arch Intern Med, September 13, 2004; 164(16): 1761 - 1768. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Coull and P. M. Rothwell Underestimation of the Early Risk of Recurrent Stroke: Evidence of the Need for a Standard Definition Stroke, August 1, 2004; 35(8): 1925 - 1929. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. L. Flaherty, K. D. Flemming, R. McClelland, N. W. Jorgensen, and R. D. Brown Jr Population-Based Study of Symptomatic Internal Carotid Artery Occlusion: Incidence and Long-Term Follow-Up Stroke, August 1, 2004; 35(8): e349 - e352. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. O'Rourke, N. Dean, N. Akhtar, and A. Shuaib Current and future concepts in stroke prevention Can. Med. Assoc. J., March 30, 2004; 170(7): 1123 - 1133. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. K. Lovett, A. J. Coull, and P. M. Rothwell Early risk of recurrence by subtype of ischemic stroke in population-based incidence studies Neurology, February 24, 2004; 62(4): 569 - 573. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. J. Adams, M. I. Chimowitz, J. S. Alpert, I. A. Awad, M. D. Cerqueria, P. Fayad, and K. A. Taubert Coronary Risk Evaluation in Patients With Transient Ischemic Attack and Ischemic Stroke: A Scientific Statement for Healthcare Professionals From the Stroke Council and the Council on Clinical Cardiology of the American Heart Association/American Stroke Association Circulation, September 9, 2003; 108(10): 1278 - 1290. [Full Text] [PDF]
|
|
|
|
|
|
R. J. Adams, M. I. Chimowitz, J. S. Alpert, I. A. Awad, M. D. Cerqueria, P. Fayad, and K. A. Taubert Coronary Risk Evaluation in Patients With Transient Ischemic Attack and Ischemic Stroke: A Scientific Statement for Healthcare Professionals From the Stroke Council and the Council on Clinical Cardiology of the American Heart Association/American Stroke Association Stroke, September 1, 2003; 34(9): 2310 - 2322. [Full Text] [PDF]
|
|
|
|
|
|
A. Terent Trends in Stroke Incidence and 10-Year Survival in Soderhamn, Sweden, 1975-2001 Stroke, June 1, 2003; 34(6): 1353 - 1358. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Hillen, C. Coshall, K. Tilling, A. G. Rudd, R. McGovern, and C. D.A. Wolfe Cause of Stroke Recurrence Is Multifactorial: Patterns, Risk Factors, and Outcomes of Stroke Recurrence in the South London Stroke Register Stroke, June 1, 2003; 34(6): 1457 - 1463. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. S. Dunn and A. G. G. Turpie Perioperative Management of Patients Receiving Oral Anticoagulants: A Systematic Review Arch Intern Med, April 28, 2003; 163(8): 901 - 908. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. S. Knopman, W. A. Rocca, R. H. Cha, S. D. Edland, and E. Kokmen Survival Study of Vascular Dementia in Rochester, Minnesota Arch Neurol, January 1, 2003; 60(1): 85 - 90. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. P. Broderick and W. Hacke Treatment of Acute Ischemic Stroke: Part I: Recanalization Strategies Circulation, September 17, 2002; 106(12): 1563 - 1569. [Full Text] [PDF]
|
|
|
|
|
|
S. Bak, S. H. Sindrup, T. Alslev, O. Kristensen, K. Christensen, and D. Gaist Cessation of Smoking After First-Ever Stroke: A Follow-Up Study Stroke, September 1, 2002; 33(9): 2263 - 2269. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Ezzeddine, M. H. Lev, C. T. McDonald, G. Rordorf, J. Oliveira-Filho, F. G. Aksoy, J. Farkas, A. Z. Segal, L. H. Schwamm, R. G. Gonzalez, et al. CT Angiography With Whole Brain Perfused Blood Volume Imaging: Added Clinical Value in the Assessment of Acute Stroke Stroke, April 1, 2002; 33(4): 959 - 966. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Castellanos, J. Castillo, M. M. Garcia, R. Leira, J. Serena, A. Chamorro, and A. Davalos Inflammation-Mediated Damage in Progressing Lacunar Infarctions: A Potential Therapeutic Target Stroke, April 1, 2002; 33(4): 982 - 987. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. P. Whisnant, D. O. Wiebers, W. M. O'Fallon, J. D. Sicks, and R. L. Frye Effect of time since onset of risk factors on the occurrence of ischemic stroke Neurology, March 12, 2002; 58(5): 787 - 794. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. W. Sturm, H. M. Dewey, G. A. Donnan, R. A.L. Macdonell, J. J. McNeil, and A. G. Thrift Handicap After Stroke: How Does It Relate to Disability, Perception of Recovery, and Stroke Subtype?: The North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, March 1, 2002; 33(3): 762 - 768. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Evans, F. Harraf, N. Donaldson, and L. Kalra Randomized Controlled Study of Stroke Unit Care Versus Stroke Team Care in Different Stroke Subtypes Stroke, February 1, 2002; 33(2): 449 - 455. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. Kolominsky-Rabas, M. Weber, O. Gefeller, B. Neundoerfer, and P. U. Heuschmann Epidemiology of Ischemic Stroke Subtypes According to TOAST Criteria: Incidence, Recurrence, and Long-Term Survival in Ischemic Stroke Subtypes: A Population-Based Study Stroke, December 1, 2001; 32(12): 2735 - 2740. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J.P. Mohr, J.L.P. Thompson, R.M. Lazar, B. Levin, R.L. Sacco, K.L. Furie, J.P. Kistler, G.W. Albers, L.C. Pettigrew, H.P. Adams Jr., et al. A Comparison of Warfarin and Aspirin for the Prevention of Recurrent Ischemic Stroke N. Engl. J. Med., November 15, 2001; 345(20): 1444 - 1451. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Staaf, A. Lindgren, and B. Norrving Pure Motor Stroke From Presumed Lacunar Infarct: Long-Term Prognosis for Survival and Risk of Recurrent Stroke Stroke, November 1, 2001; 32(11): 2592 - 2596. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Bronnum-Hansen, M. Davidsen, and P. Thorvaldsen Long-Term Survival and Causes of Death After Stroke Stroke, September 1, 2001; 32(9): 2131 - 2136. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Serena, R. Leira, J. Castillo, J. M. Pumar, M. Castellanos, and A. Davalos Neurological Deterioration in Acute Lacunar Infarctions : The Role of Excitatory and Inhibitory Neurotransmitters Stroke, May 1, 2001; 32(5): 1154 - 1161. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Uchino, D. Billheimer, and S. C. Cramer Entry Criteria and Baseline Characteristics Predict Outcome in Acute Stroke Trials Stroke, April 1, 2001; 32(4): 909 - 916. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. A Hinchey and R. G Holloway Ischaemic stroke subtypes had different short term and long term functional outcomes, mortality, and recurrence rates Evid. Based Med., January 1, 2001; 6(1): 26 - 26. [Full Text]
|
|
|
|
|
|
K. S. Wong, H. Li, Y. L. Chan, A. Ahuja, W. W.M. Lam, A. Wong, and R. Kay Use of Transcranial Doppler Ultrasound to Predict Outcome in Patients With Intracranial Large-Artery Occlusive Disease Stroke, November 1, 2000; 31(11): 2641 - 2647. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A Community-Based Outcome Study of Common Ischemic Stroke Subtypes Journal Watch Neurology, August 23, 2000; 2000(823): 2 - 2. [Full Text]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||