Original Paper

Neuroepidemiology 2010;34:9096
DOI: 10.1159/000264826

Received: July 12, 2009

Accepted: September 16, 2009
Published online: December 11, 2009

Mortality and Predictors of Death 1 Month and

3 Years after First-Ever Ischemic Stroke:
Data from the First National Acute Stroke Israeli
Survey (NASIS 2004)
Silvia Koton a David Tanne b Manfred S. Green c Natan M. Bornstein d
a

Stanley Steyer School of Health Professions, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv,
Stroke Center, Department of Neurology and Sagol Neuroscience Center, Chaim Sheba Medical Center,
Tel Hashomer, c School of Public Health, University of Haifa, Haifa, and d Neurology Department and Stroke Unit,
Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
b

Key Words
Ischemic stroke Mortality rate, ischemic stroke Diabetes
Chronic heart failure Dementia Peripheral artery disease
Predictor

Abstract
Background: Despite declining age-adjusted stroke mortality rates, the disease remains the third most common cause
of death in Israel. Based on a national survey, we examined
mortality rates during the first 3 years after a first-ever acute
ischemic stroke (IS) and the major predictors of short-term
(1 month) and long-term (3 years) mortality. Methods: In the
National Acute Stroke Israeli Survey (NASIS 2004), data were
collected on all hospitalized stroke patients in Israel during
a 2-month period. Mortality rates for first-ever IS were assessed at 1 month and 3 years and predictors of death were
evaluated using the Cox proportional hazard model. Results: A total of 1,079 first-ever IS patients were included.
Survival data were complete for over 99% of patients. Cumulative mortality rates were 9.9% at 1 month and 31.1% at 3
years. Of the survivors at 1 month, 23.5% did not survive for
3 years. At 1 month, the hazard ratio (HR) for death significantly increased with stroke severity. One-month mortality

2009 S. Karger AG, Basel

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was also associated with a decreased level of consciousness

(HR 2.9, 95% CI 1.75.1), total anterior circulation infarction
(TACI); HR 4.9, 95% CI 1.615.2), temperature on admission
(HR 1.5, 95% CI 1.12.1 per 1 C), age (HR 1.04, 95% CI 1.021.07
per year) and glucose levels on admission (HR 1.003, 95% CI
1.0011.006 per 1 mg/dl). Age-adjusted proportions of diabetes and chronic heart failure were considerably higher in
the deceased compared with survivors at 3 years (48 vs. 38
and 21 vs. 9%, respectively). In the multivariate survival analyses, predictors of death at 1 month also predicted death at
3 years; however, history of dementia (HR 1.5, 95% CI 1.02.4),
diabetes (HR 1.6, 95% CI 1.02.4), peripheral artery disease
(HR 1.7, 95% CI 1.12.8), chronic heart failure (HR 1.6, 95% CI
1.12.4) and malignancy (HR 1.7, 95% CI 1.12.7) were additional predictors of long-term mortality for patients surviving the first month after stroke. Conclusions: Approximately
one third of patients did not survive 3 years after the firstever IS. While age and markers of severe stroke were the major predictors of death at 1 month, comorbidities and variables associated with atherosclerotic vascular disease predicted long-term mortality. Improved control of these factors
can potentially reduce long-term mortality in stroke victims.
Copyright 2009 S. Karger AG, Basel

Silvia Koton, PhD

Stanley Steyer School of Health Professions
Sackler Faculty of Medicine, Tel Aviv University
Tel Aviv 69978 (Israel)
Tel. +972 3 6407 157, Fax +972 3 6409 496, E-Mail koton @ post.tau.ac.il

Introduction

Stroke is the third most common cause of death in European countries, accounting for high mortality in both
the short- and long-term. Reports from the European
Registries of Stroke Collaboration show that 1-month
mortality after stroke ranges from 13 to 27% [1]. The impact of stroke on mortality is evident several years after
the event: the risk of mortality for 1-year survivors is approximately 10% for each of the following 4 years, twice
as high as expected for the general population of the same
age and sex [2]. Age [3] and severity of stroke [3, 4] have
been reported to be the two major predictors of mortality
at 30 days. Age [35], previous cardiac disease [6], cardioembolic stroke [3], and diabetes [7] have been identified
as predictors of long-term mortality. Age-adjusted mortality rates after stroke have declined considerably during
the last decades in Israel. However, mortality trends show
a greater decline for Jews than for Arabs, a finding probably related to differences in risk factor distribution [8].
Identifying predictors of death after acute stroke is important for the development of secondary prevention
strategies and setting targets in the management of acute
stroke. Based on data from the first National Acute Stroke
Israeli Survey (NASIS 2004) [9], we present the rates of
mortality after first-ever acute ischemic stroke (IS) during the first 3 years after stroke and examine the major
potential predictors of short-term (1 month) versus longterm (3 years) mortality after IS.

clinical outcome was completed for all patients during hospitalization. Information on the etiology of IS was collected according
to the TOAST criteria. However, 42% of the ISs were classified as
undetermined mainly due to lack of in-hospital investigations.
The clinical OCSP criteria, which reflect the extent of the stroke,
were preferred for the classification of events in the present
study.
Mortality rates were prospectively assessed at 1 month and 3
years following stroke by means of matching patients files with
national mortality data. The study was approved by the ethical
committees of the participating hospitals.
Statistical Analysis
Cumulative mortality rates at the 1-month and 3-year followups were calculated for all hospitalized patients with first-ever IS.
Differences in baseline variables between survivors and non-survivors at 1 month and 3 years after the stroke were assessed with
the 2 test for proportions and the Students t test for continuous
variables. Determinants of death were evaluated using the Cox
proportional hazard model at 1 month and 3 years. The KaplanMeier survival curve at 1 month and 3 years and adjusted HR for
mortality at both periods are presented. At 3-year follow-up, data
analysis was conducted only for 1-month survivors. Analyses
were performed with the SAS 9.1 software.

Results

The NASIS 2004 was the first national prospective survey on

cerebrovascular diseases in Israel. The survey methods were reported elsewhere [9]. Briefly, the study included all patients with
acute stroke aged 618 year, hospitalized during FebruaryMarch
2004 in all 28 medical centers that admit stroke patients in Israel
(n = 2,175). Data were collected prospectively. In each hospital, a
coordinating physician was responsible for data collection
throughout hospital wards. Whenever the coordinating physician
raised doubt regarding diagnosis, a central adjudication committee made the final decision. IS (n = 1,558, 71.6%) and intracerebral
hemorrhage (ICH; n = 159, 7.3%) were differentiated using head
computerized tomography (CT), performed on 96.4% of the patients. If brain CT or MRI were not performed, patients were regarded as undetermined stroke (n = 78, 3.6%). Transient ischemic
attack was diagnosed in 380 patients (17.5%). In the present study,
only first-ever IS (not transient ischemic attack) patients were included (n = 1,079, 69.3% of all IS).
A structured data form including demographics, characteristics, stroke severity on admission (by NIHSS), clinical classification of the IS (by Oxfordshire Community Stroke Project, OCSP
classification [10]), diagnostic tests performed, management and

A total of 1,079 first-ever IS patients were included; the

mean age was 71 8 13 years and there were slightly more
men (53%) than women. Survival data during the study
period were complete for over 99% of patients. Cumulative rates of mortality were 9.9% at 1-month and 31.1% at
3-year follow-up. The annual risk of death was highest in
the first year (21.0%). For 1-year survivors, the annual
mortality rate during the 2nd and 3rd year after the stroke
was approximately 6.5%. Two hundred and twenty-six of
the 960 survivors at 1 month (23.5%) did not survive 3
years after the stroke. Survival curves at 1 month and 3
years are shown in the figure 1. Ninety-two percent of the
patients were treated with antithrombotics (aspirin, clopidogrel/ticlopidine, dipyridamole or coumadin), and
11% received coumadin.
Survivors at 1 month (n = 960, 90.1%) were significantly younger at stroke onset than the deceased (mean
age 70 8 13 years. for survivors vs. 78 8 12 for deceased,
p ! 0.0001). Table 1 presents the characteristics of the
study population according to survival status at 1 month.
The proportion of males was higher among survivors,
compared with the deceased (p = 0.03). Comorbidity and
decreased level of consciousness on admission were significantly more frequent among deceased patients, while
dyslipidemia and current smoking were more common
among survivors.

Predictors of Death after IS

Neuroepidemiology 2010;34:9096

Methods

91

100
98

Survivors (%)

96
94
92
90
88

Survivors (%)

0 0.5 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 18 19 20 22 23 24 25 27 28 29 30
Time from onset of IS (days)

100
98
96
94
92
90
88
86
84
82
80
78
76
0

8 10 12 14 16 18 20 22 24 26
Time from onset of IS (months)

28

30

32

34

36

Fig. 1. Kaplan-Meier survival curve for

IS patients at 1-month and 3-year (for 1month survivors only) follow-up.

Patients alive 3 years after the stroke (n = 734, 68.9%)

were significantly younger at baseline than non-survivors (mean age 67.6 8 12.4 years for survivors vs. 78.4 8
10.5 for non-survivors, p ! 0.0001). Table 2 presents the
characteristics of the patients by survival status at 3 years.
Similarly to the findings for 1 month, 3-year survivors
differed from non-survivors in most baseline characteristics. As expected, short- and long-term mortality was
positively associated with stroke severity. In the analysis
of mortality by arterial territory of the stroke, the highest
mortality rates were found for patients with total anterior
circulation (TACI) stroke (table 3). Age-adjusted proportions of diabetes, chronic heart failure (CHF) and periph92

Neuroepidemiology 2010;34:9096

eral artery disease were higher in the deceased compared

with survivors at 3 years (48 vs. 38, 21 vs. 9 and 7 vs. 6%,
respectively).
Variables identified in the multivariate survival analysis as independent predictors of death at 1 month and 3
years are presented in table 4. Age, decreased level of consciousness, severity of stroke (by NIHSS), and TACI were
positively associated with death at both periods. However, comorbidity including history of dementia, diabetes, CHF, peripheral artery disease and malignancy were
positively associated only with death at 3 years after the
stroke.

Koton /Tanne /Green /Bornstein

Table 1. Characteristics of first-ever

IS patients by survival status at 1-month
follow-up

Survivors
(n = 960, 90.1%)
Male gender
Hypertension
Dyslipidemia
Diabetes
Atrial fibrillation
Current smoking
Prior heart disease1
Peripheral artery disease
Malignancy
Family history of stroke (55 years)
Dementia
Decreased level of consciousness
Glucose on admission, mg/dl
Temperature on admission, C
WBC on admission, /mm3
SBP on admission, mm Hg
DBP on admission, mm Hg

517 (53.9)
648 (73.2)
431 (44.9)
375 (39.1)
152 (16.0)
193 (20.2)
306 (31.9)
64 (6.7)
64 (6.7)
29 (3.1)
63 (6.7)
91 (9.5)
151.5877.1
36.680.5
8,81883,134
161.7828.2
85.8814.7

Deceased
(n = 106, 9.9%)
45 (42.5)
73 (68.9)
37 (34.9)
44 (41.5)
40 (38.1)
9 (8.5)
42 (40.0)
8 (7.7)
15 (14.4)
1 (1.0)
13 (12.8)
61 (57.6)
178.6889.6
36.880.7
10,23684,162
157.4830.2
81.9818.3

p
0.03
0.35
0.05
0.63
<0.0001
0.004
0.11
0.71
0.005
0.23
0.03
<0.0001
0.004
0.002
0.0009
0.15
0.04

Unless otherwise indicated the values are the number of patients with percentages in
parentheses.
1
Prior acute myocardial infarction or angina pectoris or congestive heart failure or
valvular heart disease.

Table 2. Characteristics of first-ever

Survivors
(n = 734, 68.9%)

IS patients by survival status at 3-year

follow-up
Male gender
Hypertension
Dyslipidemia
Diabetes
Atrial fibrillation
Current smoking
Prior heart disease2
Peripheral artery disease
Malignancy
Family history of stroke (55 years)
Dementia
Decreased level of consciousness
Glucose on admission, mg/dl
Temperature on admission, C
WBC on admission, /mm3
SBP on admission, mm Hg
DBP on admission, mm Hg

412 (56.1)
530 (72.6)
354 (48.2)
286 (39.0)
87 (12.0)
167 (22.9)
206 (28.1)
43 (5.9)
39 (5.4)
23 (3.2)
27 (3.7)
41 (5.6)
150.6876.7
36.680.5
8,63482,880
161.5827.0
85.9814.0

Deceased1
(n = 226, 23.5%)
105 (46.5)
168 (75.0)
77 (34.2)
89 (39.4)
65 (29.2)
26 (11.6)
100 (44.3)
21 (9.4)
25 (11.2)
6 (2.7)
36 (16.4)
50 (22.1)
154.5878.7
36.680.6
9,41583,789
162.2831.4
85.4816.7

p
0.01
0.5
0.0002
0.9
<0.0001
0.0002
<0.0001
0.07
0.003
0.7
<0.0001
<0.0001
0.5
0.4
0.005
0.7
0.7

Unless otherwise indicated the values are the number of patients with percentages in
parentheses.
1
Among 1-month survivors only.
2 Prior acute myocardial infarction or angina pectoris or congestive heart failure or
valvular heart disease.

Predictors of Death after IS

Neuroepidemiology 2010;34:9096

93

Table 3. One-month and 3-year mortality by stroke severity and

Discussion

vascular territory
1-month mortality
(n = 106, 9.9%)

3-year mortality1
(n = 226, 23.5%)

12 (2.2)
24 (9.0)
15 (11.0)
23 (34.9)
31 (58.5)

66 (12.5)
70 (28.8)
50 (41.3)
26 (60.5)
13 (59.1)

Arterial territory (by OCSP classification)

Total anterior circulation
43 (37.7)
Partial anterior circulation
36 (8.5)
Posterior circulation
16 (6.7)
Lacunar
4 (1.8)
Unknown
7 (13.0)

36 (50.7)
107 (27.7)
33 (14.7)
39 (17.3)
8 (17.0)

Stroke severity on admission

NIHSS 5
NIHSS 610
NIHSS 1115
NIHSS 1620
NIHSS >20

The values are the number of patients with percentages in parentheses.

1
Among 1-month survivors only.

Cumulative rates of mortality for first-ever IS patients

in this national stroke survey increased from approximately 10% at 1 month to almost one third of patients 3
years after the event. Almost one quarter of survivors at
1 month did not survive 3 years. Survivors at 1 month and
3 years differed from non-survivors in most baseline
characteristics. Decreased level of consciousness, severity
of stroke (by NIHSS), arterial territory and age were positively associated with death both at 1 month and 3 years
after IS. Comorbidities and variables associated with atherosclerotic vascular disease were additional independent determinants of long-term mortality. Our findings
are not surprising: population-based studies have reported that up to 70% of deaths during the first month after
a stroke are attributable to the stroke, acute cardiovascu-

Table 4. Cox survival model1 for determinants of 1-month and 3-year mortality in first-ever IS patients

Age (per year)

Decreased level of consciousness
Severity on admission
NIHSS 5
NIHSS 610
NIHSS 1115
NIHSS 1620
NIHSS >20
Temperature on admission
Glucose level on admission
Arterial territory (OCSP classification)
Lacunar infarction
TACI
PACI
POCI
Unknown
Dementia (prior to stroke)
Diabetes
CHF
Peripheral artery disease
Malignancy

1-month mortality
HR (95% CI)

3-year mortality2
HR (95% CI)

1.04 (1.021.07)
2.9 (1.75.1)

0.0002
0.0001

1.07 (1.061.09)
1.6 (1.02.4)

<0.0001
0.04

0.03
0.4
<0.0001
0.0002
0.008
0.03

1 (Ref.)
1.7 (1.22.5)
2.4 (1.63.6)
4.9 (2.88.8)
3.5 (1.58.1)

0.006
<0.0001
<0.0001
0.003

0.006
0.3
0.2
0.004

1 (Ref.)
1.9 (1.13.3)
1.2 (0.81.8)
0.7 (0.41.2)
1.7 (0.83.6)
1.5 (1.02.4)
1.6 (1.02.4)
1.6 (1.12.4)
1.7 (1.12.8)
1.7 (1.12.7)

0.04
0.4
0.2
0.2
0.05
0.04
0.01
0.03
0.02

1 (Ref.)
2.4 (1.15.0)
1.5 (0.63.7)
6.0 (2.514.5)
6.1 (2.315.8)
1.5 (1.12.1)
1.003 (1.0011.006)
1 (Ref.)
4.9 (1.615.2)
1.8 (0.65.4)
2.3 (0.77.3)
6.4 (1.822.2)

Age (year), gender, hypertension, dyslipidemia, diabetes, atrial fibrillation, current smoking, prior acute
myocardial infarction, angina pectoris, congestive heart failure, valvular heart disease, peripheral artery disease, malignancy, family history of stroke (55 years), dementia prior to stroke, decreased level of consciousness,
glucose on admission (mg/dl), temperature on admission ( C), WBC on admission (per mm3), SBP on admission (mm Hg), DBP on admission (mm Hg), severity of stroke on admission (NIHSS) and arterial territory
(OCSP classification) were included in the model, only significant variables are presented.
2 Among 1-month survivors only.

94

Neuroepidemiology 2010;34:9096

Koton /Tanne /Green /Bornstein

lar events and complications of the index stroke [11, 12].

Neurologic complications of the stroke (e.g. brain edema,
brain herniation and hemorrhagic transformation), acute
cardiac events, pneumonia and pulmonary embolism
have been reported as main causes of death during the
first month after the event [12]. Cardiovascular and respiratory comorbidities, as well as additional non-vascular causes indicating a decreased general health status,
account for most long-term mortality [11, 12].
Prior studies have reported 30-day mortality rates after hospitalized IS of 8 [4] and 13% [13], which are consistent with our findings. Cumulative mortality rates at 1
year in our study were similar to those previously reported in the Northern Manhattan Stroke Study [11], and lower than those reported in other population- and community-based studies [1416]. A recent study reported a 1year case fatality rate of 23.6% for patients hospitalized
with IS [13], a slightly higher rate than ours.
Current smoking was significantly more frequent
among short- and long-term survivors compared with
the deceased. Several studies have reported lower mortality after acute myocardial infarction in smokers [1719].
Smoking is a well-known risk factor for vascular diseases
and mortality; therefore our paradoxical findings might
be explained by differences in the distribution of other
risk factors for stroke mortality, and by differences in comorbidity between smokers and non-smokers. For example, a pattern of higher blood pressure among nonsmokers and ex-smokers than among smokers has been reported in a large epidemiologic study [20]. In addition,
multivessel disease in acute myocardial infarction patients has been shown to be less common among smokers
compared to non-smokers [21], probably due to the fact
that among smokers the acute ischemic event occurs earlier than among non-smokers.
Increased short- and long-term mortality rates for patients with TACI stroke have been reported [22, 23], and
our findings support these reports. Age [3] and severity
of stroke [3, 4] have been reported to be the two major
predictors of mortality at 30 days in population-based
studies. Coma, TACI, posterior circulation infarction,
blood glucose level and WBC count on admission have
also been reported as predictors of short-term mortality
after IS [6]. Our findings support these previous reports.
Age has been reported to be a predictor of mortality 1
[5, 13, 24, 25], 3 [5] and 5 years [3, 4] after stroke. In the
present study, age predicted long-term mortality. A decreased level of consciousness on admission was a strong
determinant of death in our study, similar to previous

reports [26, 27]. The severity of stroke, a well-known predictor of short- and long-term mortality [24, 13], was an
important determinant of death in our study. A history
of previous cardiac disease has also been reported to increase the risk of mortality after stroke [24, 27], similar
to our present findings. Several studies have shown that
pre-stroke dementia is a risk factor for death during the
first year after the stroke [24, 28, 29]. We found that dementia was an independent risk factor for 3-year mortality among IS patients.
In our study, survivors at 3 years were, on average,
more than 10 years younger than the deceased. This considerable difference in age accounts most likely for most
of the long-term mortality. Additionally, risk factors like
malignancy and dementia are difficult to control. However, the age-adjusted proportions of diabetes and CHF
were considerably higher in the deceased compared with
survivors at 3 years; therefore improved control of these
factors can potentially prevent part of the long-term
deaths. Current international guidelines for management
of IS recommend optimal management of vascular risk
factors as part of the secondary prevention treatment
[30]. Unfortunately it is not clear to which extent these
guidelines are implemented.

Predictors of Death after IS

Neuroepidemiology 2010;34:9096

Strengths and Limitations of the Study

The most important strength of our study is the fact
that we analyzed national data collected with strict methodology. Additionally, we have followed up the patients
for a long period and survival data were available for over
99% of patients. However, the study has some limitations.
First, our study included only hospitalized patients. In
Israel, the great majority of stroke patients are hospitalized, yet, our findings might not be generalizable to patients not hospitalized. Second, we did not include patients who died before admission to a hospital. Third, the
NASIS 2004 was conducted only during a 2-month period in all hospitals in Israel. Although our database is not
based on a continuous registry of patients hospitalized
for stroke , we have no reason to believe that determinants
of death after stroke might differ in the complete patient
population hospitalized for stroke compared with the national sample.

Conclusions and Clinical Implications

Long-term mortality among IS patients is associated

not only with age, stroke severity and clinical variables
on admission, but also with characteristics related to co95

morbidities. Our findings support the need for optimal

control of vascular risk factors and rigorous treatment of
atherosclerotic vascular disease as well as other physical
and cognitive comorbidities in order to improve the longterm survival of patients after an IS.

Acknowledgment
We thank Ms. Rita Dichtiar, BSc, for her help with the statistical analyses.

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