From the Departments of Neurological Sciences (M.P., M.R., A.A., M.B.,
M.C., F.G., C.F.) and Experimental Medicine (F.C.), University "La
Sapienza," Rome, Italy.
Correspondence to Massimiliano Prencipe, MD, Dipartimento di Scienze Neurologiche, Universita degli Studi "La Sapienza," Viale dell'Università 30, 00185 Roma, Italy.
Methods—A cohort of 322 patients with first-ever minor
ischemic strokes (mean age, 55 years; 89% were treated with
antiplatelet or anticoagulant drugs) with minor (Rankin score=2) or
no disability (Rankin score <2) were followed for 10 years, with only
6% lost to follow-up. Death and major stroke recurrence rates
were evaluated by Kaplan-Meier analysis. Hazard ratios and 95%
confidence intervals (CI) of factors with P<.1 at the
log-rank test were evaluated by multivariate Cox
analysis.
Results—The 10-year mortality rate was 32%, with a relative risk
of 1.7 (95% CI, 1.4 to 2.1) compared with the age- and sex-matched
general population. The 10-year recurrence rate of major
strokes was 14%. The hazard ratio (95% CI) of death was 1.1 (1.05 to
1.09) for age (1-year increments), 3.4 (2.2 to 5.2) for minor
disability, 1.8 (1.1 to 3.1) for myocardial infarction (MI), 2.0 (1.1
to 3.7) for nonvalvular atrial fibrillation, and 1.8 (1.2 to
2.7) for hypercholesterolemia. The hazard ratio
(95% CI) of major stroke recurrence was 2.8 (1.3 to 6.2) for
recurrent minor strokes, 3.1 (1.9 to 4.6) for nonlacunar stroke, 2.9
(1.3 to 6.8) for MI, and 3.0 (1.4 to 6.4) for hypertension.
Conclusions—In minor ischemic strokes, age, minor
disability, MI, nonvalvular atrial fibrillation, and
hypercholesterolemia increase the risk of
death; recurrent minor strokes, nonlacunar stroke, MI, and hypertension
increase the risk of major stroke.
Since few studies have evaluated the long-term prognosis of minor
strokes, the determinants of long-term outcome are not well defined in
this subset of stroke patients.18 19 The aim of the
present study was to evaluate the risks of death and major stroke
recurrence in a cohort of patients with minor ischemic
strokes followed up for 10 years.
Patients were considered as stroke cases only if symptoms or signs
lasted longer than 24 hours. We excluded all patients who suffered from
deficits caused by new strokes, cerebral angiography, or carotid
endarterectomy within 30 days of stroke onset. At
discharge, stroke patients were classified as affected by minor
disability when stroke symptoms led to some lifestyle restrictions
(Rankin=2) or by no disability when stroke symptoms did not interfere
with the patient's lifestyle (Rankin <2).
In addition to the cranial CT scan, all patients underwent routine
blood tests, ECG, and Doppler sonography (DUD 800 equipment,
Delalande AHS) of extracranial vessels. Cerebral angiography was
performed in 97 patients selected on a case-by-case basis. Since other
examinations (echocardiography, nuclear magnetic
resonance, anticardiolipin autoantibodies, and fibrinogen) were
performed in only some of the patients (13% to 27%), we did not use
these data in the present analysis.
CT scans were performed with a Sireton 2000 scanner, providing 8-mm
slices. All the CT scans performed within 72 hours of stroke onset were
repeated before patients were discharged, and the second scan was used
for the analysis. Patients with inappropriate CT
ischemic lesions (located in an area not corresponding to the
symptoms of index stroke) or multiple CT ischemic lesions
(silent brain infarctions) were not considered first-ever strokes and
therefore were excluded. For the purposes of this study, lacunar
infarcts were classified as CT lesions with an infarctlike density that
were small (<1.5 cm in diameter) and subcortical. CT ischemic
lesions not fulfilling these criteria were classified as nonlacunar
infarcts. Lacunar strokes were classified as cases presenting a
lacunar syndrome21 and were associated with a lacunar
infarct or a negative CT scan.22 The patients not
fulfilling these criteria were classified as having nonlacunar strokes.
NVAF, prior MI, and other cardiac diseases were diagnosed on the basis
of history, clinical examination, and ECG findings.
We analyzed the following risk factors: arterial
hypertension (antihypertensive treatment regularly taken before or
after stroke), diabetes mellitus (hypoglycemic treatment taken before
or after stroke), and hypercholesterolemia
(total fasting serum cholesterol levels
Follow-up visits included a standardized interview with the patient, a
review of the interim medical records, and general and neurological
examinations. Patients who did not come to the follow-up visits were
contacted by telephone and interviewed according to a standardized
questionnaire. When patients were unable to answer or were dead, a
family member or a proxy was asked to complete the questionnaire. Both
the standardized interview and the telephone questionnaire were aimed
at identifying the causes of death and at classifying new cerebral
events. Data about the time and cause of death were compared with those
written on both the death certificates and medical records
available. All patients were followed up at least once a year for 10
years or until they had a major stroke (Rankin grade
Mortality rates and stroke recurrence rates were estimated by
the Kaplan-Meier method. In the mortality rate analysis,
patients suffering from nonfatal major strokes were censored at the
time of their new stroke. In the stroke recurrence rate
analysis, patients who died from causes other than stroke were
censored at the time of their death. Average annual rates were
calculated according to the formula suggested by Hankey et
al.23 Relative risk of death was calculated by comparing
our mortality rates with those of the age- and sex-matched general
population taken from Italian life tables.24 The CI of
relative risk was computed by assuming a Poisson distribution. The
univariate analysis was performed with the log-rank
test. The independent association between each variable and either
death or stroke recurrence was estimated by means of the Cox
proportional hazard model. We included in the initial model only
variables with a log-rank test value of P<.1. This set
of variables was reduced by backward elimination until only those
significant at P<.05 remained in the model.
As shown in Table 2
Of the 322 patients, 242 (75%) were treated with antiplatelet
drugs and 27 (8%) with oral anticoagulants, and 19 (6%) were
submitted to carotid endarterectomy and
subsequently treated with antiplatelet drugs; the remaining 34
patients (11%) did not take oral anticoagulants or antiplatelet
drugs because of contraindications or refusal to be treated. Of the 22
NVAF patients, 10 (45%) were chronically treated with oral
anticoagulants. Furthermore, both hypertensive and diabetic patients
were regularly treated for their disease.
We lost 19 patients (6%), 8 before and 11 after the fifth year of
follow-up. The median age was 44 years in lost patients and 56 years in
those who completed the follow-up (Mann-Whitney U test,
P=.36). There was no difference in the proportion of male
participants and male lost patients (76% and 74%, respectively;
By the end of the follow-up period, there were 96 deaths, 39 (41%) due
to cardiovascular events (19 were sudden deaths), 24
(25%) to recurrent strokes, 31 (32%) to other diseases (13 caused by
cancer), and 2 (2%) to unknown causes. As shown in Fig 1
By the end of the follow-up period, 69 patients had new cerebral
events, but only 37 (54%) were major strokes. Of these 37 major
strokes, 24 (65%) were fatal, 22 (59%) occurred in the same territory
as the first stroke, and 8 (22%) were preceded by a minor
recurrence. The major recurrences were ischemic
in 18 and hemorrhagic in 1 of the 19 patients who underwent a CT scan.
The cumulative 10-year recurrence rate of major strokes was
14%, with an average annual recurrence rate of 1.5%. At the
univariate analysis, the risk of stroke
recurrence was significantly associated with nonlacunar stroke
(Fig 3
The average annual stroke recurrence rate observed in our study
was extremely low (1.4%). We did not, however, consider as an end
point minor stroke recurrences, which accounted for 46% of all
stroke recurrences, a figure comparable to the 36% to 52%
observed in other studies.7 17 26 27 However, even if we
had included nondisabling strokes, our annual recurrence rate
would have still been lower than the 4% to 9% reported in the
literature.1 6 7 16 The exclusion of early
recurrences, which occur in 3% to 4% of ischemic
strokes,5 28 would not have affected our rates markedly,
given that the average annual rates were calculated over a 10-year
follow-up period. To reduce the risk of missing part of stroke
recurrences, we interviewed the relatives of all patients who
died to identify possible recurrences in the year before their
death. Finally, we do not have sufficient data to quantify the effect
of preventive therapies, but we may assume that the reduction in the
number of recurrences in our cohort is comparable to those
achieved in controlled studies.
Despite the relatively low rate of events, the Cox analysis
identified some independent predictors of death and major stroke
recurrence. We did not find any significant association between
sex and either stroke recurrence or death, but these findings
have a limited value owing to the small proportion of women (24%)
included in our cohort. As expected, age was a strong predictor of
death. The lack of a significant association between age and stroke
recurrence has been observed in other
studies6 7 8 28 and supports the hypothesis that strokes and
stroke recurrences have different risk factors.
We did not find a significant association between the presence of
carotid lesions and either death or stroke recurrence. This
may, however, be due to the fact that angiography was performed in only
30% of the patients and that different treatments (surgery,
anticoagulants) were administered on a case-by case basis.
Consequently, we were unable to evaluate the effect of different
carotid lesions on the long-term outcome.
Prior MI was associated with both death and stroke recurrence,
confirming the poor prognosis associated with this
disease.1 25 29 30 Some studies have reported that NVAF is
an independent predictor of death,25 30 stroke
recurrence4 31 or both,32 although
these findings have not been confirmed by others.6 7 17 28
In our cohort, NVAF was significantly associated with death but not
with stroke recurrence. However, the high value of the hazard
ratio for stroke recurrence (1.9) suggests that the low number
of NVAF patients might have provided a false-negative result (type 2
error).
In some studies hypertension was significantly associated with
death31 or not significantly associated with stroke
recurrence.7 17 32 33 We instead found, in
agreement with other studies, that hypertension was an independent
predictor of stroke recurrence, but not of death.4 6 25 28
Diabetes mellitus emerged as a significant predictor of death but not
of stroke recurrence in some studies,4 25 34 and of
stroke recurrence in the Rochester study.5 However,
in our study, which is in agreement with others,1 17 we did
not find a significant association between diabetes and either death or
stroke recurrence.
Some studies did not find any significant association between
hypercholesterolemia and either stroke
recurrence or death,17 31 but in one statistical
overview of 10 prospective studies, the risk of stroke was
significantly higher in subjects with
hypercholesterolemia than in those
without.35 Likewise, a long-term follow-up study found an
independent negative association between HDL cholesterol
and ischemic stroke mortality.36 In our study we
found that hypercholesterolemia increased the
risk of death but not of stroke recurrence. This association
may be due to the possible role of dyslipidemia as a risk
factor in cardiovascular deaths, which accounted for
41% of all deaths in our cohort of relatively young and prevalently
male patients.
Our data on disability are in agreement with other studies that found a
higher risk of death not only in stroke patients of all
types37 38 but also in lacunar patients.17 39
Since we excluded severely disabled patients, our data suggest that
disability may increase the risk of death through mechanisms other than
complications caused by immobility. By contrast, the association
between disability and stroke recurrence was not present at
the multivariate analysis.
Several studies have observed that mortality rates are lower in lacunar
than in nonlacunar strokes. This difference could be attributed to the
high rate of early deaths observed in nonlacunar strokes. In our study,
however, lacunar patients had a better survival even after exclusion of
early deaths, although the multivariate
analysis did not show a significant association between lacunar
strokes and risk of death. The better survival observed in our lacunar
strokes could therefore be explained by their strong inverse
association with disability. In the Stroke Data Bank, lacunar strokes
had 2-year recurrence rates that were similar to those of
embolic strokes (14.6 and 14.7, respectively) but lower than those of
atherosclerotic strokes (21.9).28 In the Rochester
population, lacunar and nonlacunar patients had a similar probability
of stroke recurrence.40 We found a significant
inverse association between lacunar strokes and major stroke
recurrences. Therefore, our data are consistent with
the hypothesis that lacunar and nonlacunar strokes have a different
pathogenesis.
In conclusion, these findings cannot be automatically applied to the
whole population of stroke patients, but they can provide useful
information on the outcome of a highly selected and treated cohort of
minor strokes. Despite our selection criteria and the best treatment
available, our patients had a risk of death 1.7 times higher than that
of the age- and sex-matched general population. The unexpected
association between death and both minor disability and
hypercholesterolemia suggests that these
factors should receive more attention in future studies on long-term
outcome. Finally, our data on stroke recurrence emphasize the
importance of a differential diagnosis both between major and minor
recurrences and between lacunar and nonlacunar strokes.
Received July 16, 1997;
revision received October 13, 1997;
accepted October 13, 1997.
© 1998 American Heart Association, Inc.
Original Contributions
Long-term Prognosis After a Minor Stroke
10-Year Mortality and Major Stroke Recurrence Rates in a Hospital-Based Cohort
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—Determinants
of long-term outcome are not well defined in minor stroke patients.
This study aims to evaluate which factors are independent long-term
predictors of death and major stroke recurrence in a cohort of
minor ischemic strokes.
Key Words: disability • lacunar infarction • long-term survival • stroke, minor • stroke recurrence
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Stroke has a huge
impact on public health owing to both the high rate of early mortality
and the residual disability of stroke survivors. Furthermore, in the 5
years after a stroke, the risk of dying is 45% to 61%1 2 3 4 5
and that of stroke recurrence is 25% to
37%.1 5 6 7 8 However, recent data point to a shift in the
natural history of stroke toward a less fatal and less disabling
disease.9 10 11 12 These findings are consistent with
hospital-based studies reporting that nearly half of all
ischemic stroke patients survive with minor or no
deficits.2 13 14 Obviously, these minor stroke patients
have a cumulative mortality rate that is lower than that of stroke
patients taken as a whole owing to the fact that they are not affected
by deaths caused by either the initial stroke or the complications of
immobility.8 15 Furthermore, an overview of published data
has shown that stroke recurrence rates are lower in minor than
in major stroke patients.16 Finally, the functional
prognosis of these patients would be even less severe if we consider
that a consistent part of recurrences consists of minor
strokes.7 17
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The study cohort was recruited from stroke patients
consecutively admitted to the Neurological Department of the University
of Rome between January 1977 and March 1986. The inclusion criteria
were as follows: first-ever stroke; admission within 48 hours of stroke
onset; cranial CT scan excluding hemorrhagic or other nonvascular
lesions; minor or no disability (stroke-related disability resulting in
a score <3 on the modified Rankin scale20 ) within 30 days
of stroke onset; no life-threatening diseases within 2 years of
discharge; residence in Rome or surroundings; and consent to
participate. 
2.4 g/L in men
and 2.2 g/L in women, observed on at least two separate occasions).
We did not analyze data on smoking and alcohol consumption
because data available could not be validated by other means.
Furthermore, we analyzed data on history of migraine and use of
oral contraceptives in the 6 months preceding stroke. 3), died, or
refused the follow-up visit. Recurrent minor strokes were registered
but not considered as an end point. Deaths were classified as follows:
stroke deaths were deaths that occurred within 30 days of a recurrent
stroke, regardless of the final cause of death;
cardiovascular deaths were deaths that occurred within
30 days of a cardiovascular event such as MI, ruptured
aortic aneurysm, or other cardiac diseases; in the absence of
other evident causes, sudden deaths were considered
cardiovascular; nonvascular deaths were those due to
other well-defined causes such as cancer, surgery, accidents, or
pneumonia; unclassified deaths were those in which the information
available was insufficient to classify them.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Of the 322 stroke patients fulfilling the inclusion criteria, 244
(76%) were men. The median age of participants was 55 years (56 years
for men and 53 years for women; Mann-Whitney U test,
P=.62). All patients were admitted within 48 hours of stroke
onset, and 299 (93%) of them were admitted within 24 hours. The CT
scan was negative in 66 (20%) of the 322 patients. Table 1
shows the baseline characteristics of
the cohort. The 3 patients with undetermined vascular territory had a
negative CT scan. All the patients with either >70% stenosis
or occlusion of the symptomatic carotid artery were
submitted to cerebral angiography. Nineteen of the 35 patients with
stenosis 70% underwent surgery. Four of the 8 carotid
occlusion cases were dissections. Of the 115 patients diagnosed as
having a lacunar stroke, 36 (31%) had a negative CT scan. Of the 185
patients with no disability at 30 days, 65 (20% of the cohort) had a
Rankin score of 0, and 120 (37% of the cohort) had a Rankin score of
1. Among the 16 patients with other cardiac diseases, there were 2
patients with valvular diseases, 5 with first-degree
atrioventricular block, and 4 with
ventricular and 5 with atrial premature contractions. Seven
patients (2 men and 5 women) were affected by migraine. In 5 of these
cases other potential causes for ischemic stroke were
present as well, and 1 of the 2 remaining patients was taking oral
contraceptives. In addition to this patient, 4 other women were taking
oral contraceptives when they had the stroke. We did not find any
associated disease in 38 patients (12%), 27 of whom were younger than
55 years.
View this table:
[in a new window]
Table 1. Baseline Characteristics of the 322 Patients With
Minor Stokes , the proportions of
most of the baseline characteristics differ in the four age subgroups.
The proportions of men did not differ significantly in these subgroups.
In addition to age and sex distribution analysis, we found that
the proportion of patients with minor disability was significantly
higher (
2 test, P<.001) in nonlacunar (59%)
than in lacunar (13%) strokes. Differences between lacunar and
nonlacunar strokes in all the other baseline characteristics were not
significant. The proportions of hypertensive subjects were
significantly higher in patients with than without minor disability
(62% and 48%, respectively; 2 test, P=.02),
diabetes (72% and 50%, respectively; 2 test,
P=.005), and hypercholesterolemia
(66% and 45%, respectively; 2 test,
P<.001). Of the 35 patients with prior MI, 23 (66%) were
affected by hypertension, 11 (31%) by diabetes, and 16 (46%) by
carotid stenosis. Of the 22 NVAF patients, 14 (64%) were
affected by hypertension, 6 (27%) by diabetes, 6 (27%) by carotid
stenosis, and 1 (5%) by carotid occlusion.
View this table:
[in a new window]
Table 2. Baseline Characteristics by Age Groups 2 test, P=.9). Twenty-one patients (6.5%)
who refused to be visited were interviewed by telephone. Because six of
them were unable to answer, the questions were answered by proxy. , the 10-year cumulative mortality rate
was 32% for stroke patients and 17% for the age- and sex-matched
general population. The relative risk between observed and expected
deaths was 1.7 (95% CI, 1.4 to 2.1). The average annual mortality
rates were 0.4% for the group aged <45 years, 2.4% for the group
aged 45 to 54 years, 5.1% for the group aged 55 to 64 years, and 8.1%
for the group aged 65 years; the cumulative survival curves
stratified according to the four age groups are shown in Fig 2. At the univariate
analysis, the risk of death was significantly associated not
only with age but also with nonlacunar stroke, minor disability, prior
MI, NVAF, hypertension, and diabetes (Table 3). In addition to the variables
shown in Table 3, patients with a Rankin score of either 0 or 1 had
similar 10-year mortality rates (17% and 19%, respectively; log-rank
test, P=.66). For nonlacunar strokes, the 10-year mortality
rate was 47% in those with minor disability and 19% in those with no
disability (log-rank test, P<.001). For lacunar strokes,
the 10-year mortality rate was 69% in patients with minor disability
and 18% in those with no disability (log-rank test,
P<.001). At the multivariate
analysis, the risk of death was significantly and independently
associated with age, minor disability, prior MI, NVAF, and
hypercholesterolemia (Table 3).
View larger version (18K):
[in a new window]
Figure 1. Kaplan-Meier survival curves for minor
ischemic strokes and age- and sex-matched subjects taken from
the general population.
View larger version (21K):
[in a new window]
Figure 2. Kaplan-Meier survival curves for minor
ischemic strokes stratified according to age. Patients
suffering from major stroke were censored at the time of stroke.
View this table:
[in a new window]
Table 3. 10-Year Mortality Rates in 322 Patients With Minor
Ischemic Strokes ), recurrent minor strokes, minor
disability, prior MI, NVAF, and hypertension (Table 4). The recurrence rate was 11%
in the group aged <45 years, 13% in the group aged 45 to 54 years,
14% in the group aged 55 to 64 years, and 17% in the group aged 65
years, but these age-related differences were not statistically
significant. At the multivariate analysis, the
risk of major stroke recurrence was significantly and
independently associated with recurrent minor strokes, nonlacunar
stroke, prior MI, and hypertension (table 4).
View larger version (25K):
[in a new window]
Figure 3. Kaplan-Meier curves of surviving free from major
stroke recurrence in lacunar and nonlacunar strokes. Patients
who died from causes other than stroke were censored at the time of
death.
View this table:
[in a new window]
Table 4. 10-Year Recurrence Rate of Major Strokes in
322 Patients With Minor Ischemic Strokes
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The present hospital-based cohort consists of first-ever
ischemic stroke survivors with minor or no disability within 30
days of stroke onset. These inclusion criteria might explain the high
proportion of patients with negative CT scans (20%) and lacunar
strokes (36%). The young age of our cohort (median age, 55 years)
depends not only on the inclusion criteria used but also on an
admission bias, since elderly stroke patients are frequently treated at
home or admitted to geriatrics departments. Therefore, the relatively
low 10-year cumulative mortality rate observed in this cohort (32%)
cannot be directly compared with the rates of studies with different
age and inclusion characteristics. Furthermore, 89% of the patients
were treated with antiplatelet or anticoagulant drugs, and many
patients were taking other drugs for concomitant diseases. However, in
our patients aged 65 years, the average annual mortality rate was
8.1%. This figure is comparable to the 4-year cumulative mortality
rate of 28% observed in the 30-day stroke survivors of the Lehigh
Valley study25 and is marginally lower than the 9.1%
observed in the 30-day survivors (mean age, 72 years) in the OCSP
study.3 However, the relative risk of death was 1.7 in our
cohort as opposed to 2.3 in the 30-day survivors in the OCSP
study.3 Since the OCSP study is population-based and our
study is hospital-based, the difference between the two studies may
partially be explained by our exclusion of patients suffering from
severe disability, life-threatening diseases, or multiple vascular
brain lesions. Furthermore, our inclusion-exclusion criteria probably
reduced the proportion and the severity of the concomitant diseases
(exhaustion of susceptibles). Finally, only 7% of the patients in the
OCSP study were treated with anticoagulant or antiplatelet
drugs.7
Selected Abbreviations and Acronyms
CI
=
confidence interval
MI
=
myocardial infarction
NVAF
=
nonvalvular atrial fibrillation
OCSP
=
Oxfordshire Community Stroke Project
Acknowledgments
This study was supported by a grant from the National Research
Council (CNR- 95.01021.PF40). The authors thank Lewis Baker for his
assistance in preparing the manuscript.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
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T. Hillen, R. Dundas, E. Lawrence, J. A. Stewart, A. G. Rudd, and C. D. A. Wolfe Antithrombotic and Antihypertensive Management 3 Months After Ischemic Stroke : A Prospective Study in an Inner City Population Stroke, February 1, 2000; 31(2): 469 - 475. [Abstract] [Full Text] [PDF]
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S. C. Johnston, D. R. Gress, and J. G. Kahn Which unruptured cerebral aneurysms should be treated?: A cost-utility analysis Neurology, June 1, 1999; 52(9): 1806 - 1806. [Abstract] [Full Text] [PDF]
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