Original Paper

Neuroepidemiology 2009;33:254260
DOI: 10.1159/000229780

Received: February 11, 2009

Accepted: May 20, 2009
Published online: July 27, 2009

Long-Term Survival after Stroke:

30 Years of Follow-Up in a Cohort, the
Copenhagen City Heart Study
Gudrun Boysen a Jacob Louis Marott b Morten Grnbk c Houry Hassanpour a
Thomas Truelsen d
a

Department of Neurology and b Copenhagen City Heart Study, Bispebjerg Hospital, University of Copenhagen;
National Institute of Public Health, and d Department of Neurology, Rigshospitalet, National University Hospital,
Copenhagen, Denmark

Key Words
Stroke, long-term survival  Cancer  Cerebrovascular
disease  Cardiovascular disease

Abstract
Background and Purpose: Only few have studied long-term
survival after stroke. Such knowledge is essential for the
evaluation of the current and future burden of stroke. The
present study presents up to 30 years of follow-up of patients after a first-ever stroke. Methods: Participants in the
Copenhagen City Heart Study who experienced a first-ever
stroke from 1978 to the end of 2001 were followed to the end
of 2007. Stroke events were validated using the World Health
Organizations definition of stroke. Linkage to the Danish
Civil Registration System enabled identification of participants who died before the end of 2007. The National Register
of Causes of Death provided cause of death. Survival in
stroke patients was compared with survival in participants
in the Copenhagen City Heart Study who did not suffer a
stroke, and with survival in the general Danish population.
Cox regression analyses adjusting for age and gender were
used to compare survival in six consecutive 4-year periods
starting with 19781982. Results: Of 2,051 patients with firstever stroke 1,801 died during follow-up. Causes of death

2009 S. Karger AG, Basel

02515350/09/03330254$26.00/0
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were cerebrovascular disease in 37%, other cardiovascular

diseases in 28%, cancer in 12%, and other causes in 23%. The
most important determinant for long-term survival was age
at time of stroke. In the 65- to 72-year age group 11% survived 15 years after stroke. In the age group !65 years 28%
survived 15 years. For all age groups survival was poorer in
stroke patients than in non-stroke controls. Long-term survival improved steadily over time. Life expectancy after
stroke increased up to 4 years from 1978 to the end of 2001,
exceeding the increase of life expectancy in the general
population. Slightly longer survival was found in women
than in men when adjusted for age at stroke onset. Conclusion: In this cohort long-term survival after stroke gradually
improved over three decades from 1978. The gain in remaining lifetime after stroke exceeded that of the general population.
Copyright 2009 S. Karger AG, Basel

Introduction

Knowledge about long-term survival in stroke patients

as compared to the general population is important for
patients, stroke specialists, and healthcare providers [1
5]. Some population-based studies have shown that about
Prof. Gudrun Boysen
Department of Neurology, Bispebjerg Hospital
University of Copenhagen, Bispebjerg Bakke 23
DK2400 Copenhagen NV (Denmark)
Tel. +45 3531 3596, Fax +45 3531 2595, E-Mail gb01@bbh.regionh.dk

1 in 5 survive for 10 years [1, 4], while less than 1 in 10

survive for 20 years [2]. Age at the time of the stroke event
is the most important determinant for long-term survival followed by the severity of stroke, functional status,
and cardiovascular risk factors [2]. During the past two
decades care and prevention in the stroke unit have gradually improved, and are expected to affect survival after
stroke [6, 7]. Increased life expectancy in the general population [8] might also influence survival after stroke.
The purpose of the present study is to analyze survival up to 30 years after first time-ever stroke based on data
from the Copenhagen City Heart Study (CCHS) [911],
and in addition, to present data on causes of death after
stroke.

Methods
The cohort was followed for 30 years. Details about the CCHS
have previously been published [911]. In brief, the CCHS was
initiated in 1976. A random sample of 19,698 Caucasian men and
women, selected after age stratification from the general populations of sterbro and Nrrebro in Copenhagen, were invited to
participate in the first study examination in 19761978. All participants were invited by letter to three later health examinations
in 19811983, 19911994, and 20012003. The response rates of
persons to the 4 examinations were 74, 70, 61, and 50%, respectively. At the health examination a questionnaire concerning history of stroke and risk factors for vascular disease was completed.
Data on stroke and death were obtained from public registers for
all members of the cohort, i.e. those who responded and non-responders.
Participants
In this cohort those invited to the first examination in 1976
1978 had a mean age of 56.0 years and those invited to the 4th
examination in 20012003 had a mean age of 61.2 years. The control group consisted of individuals from the CCHS cohort without stroke. Participants who experienced stroke before 1978 were
excluded from analysis. Information about first-ever stroke events
was obtained from 1978 and analyzed until the end of 2001. Information on causes of death was obtained until the end of 2006
and on vital status until the end of 2007.
The study was approved by the Danish Data Protection
Agency.

rized as ischemic stroke, intracerebral hemorrhage, and subarachnoid hemorrhage. Events with no information on stroke
subtypes were recorded as unspecified stroke.
First time-ever events occurring during the period 1978 to the
end of 2001 were included. Participants with transient ischemic
attacks (TIAs) and retinal artery occlusion were excluded.
The Danish National Hospital Discharge Register provided
information on hospital admissions for all participants, responders as well as non-responders. This register used the International Classification of Diseases (ICD) codes of the 8th revision (430
438) from 1976 to 1993 and 10th revision (I60I69 and G45) after
January 1994 to describe the stroke events. The stroke diagnoses
were then validated from patients hospital records. Information
about non-hospitalized stroke patients were first obtained from a
positive self-reported stroke event at the study examination and
additional information was obtained from the patients general
practitioners.
Information on Time and Causes of Death
Information on time of death was obtained from 1978 to the
end of 2007 by record linkage to the Danish Civil Registration
System which contains information on all deaths in Denmark.
The National Register of Causes of Death, established by the National Board of Health in 1943 [13], contains all death certificates
and provided the causes of death until the end of 2006. The following ICD codes were used to define the cause of death: cerebrovascular diseases 430438 (ICD-8) and I60I69 (ICD-10); other
cardiovascular diseases 390429 and 440458 (ICD-8) and I00
I52 and I70I99 (ICD-10), and cancer 140209 (ICD-8) and C00
D09 (ICD-10), while the remainder were classified as other causes
of death. Patients who died without being hospitalized but received a stroke diagnosis were registered as fatal unspecified
strokes.
Bias
By validating the stroke diagnosis we discarded false-positive
cases. Except for those participants who at study examination reported having had a stroke for which they had not been admitted
to hospital, we were not in a position to detect false-negative cases. Among participants who reported having had a stroke for
which they had not been admitted to hospital and therefore were
not reported in the register, a diagnosis of stroke was confirmed
in approximately half of the cases. This amounted to about 10%
of those reporting having had a stroke. For persons who did not
respond to the invitation to the health examinations, approximately 1 of 3, we were unable to detect non-hospitalized stroke
events. We may thus have missed about 10% of stroke events in
this group equal to about 4% of the total number of stroke events.
Thereby we may have underestimated the number of strokes by
approximately 4%.

Validation of Stroke Diagnoses

All events were diagnosed according to the World Health Organization definition of stroke: rapidly developing signs of focal
(or global) disturbance of cerebral function with symptoms lasting over 24 h or leading to death with no apparent cause other
than vascular [12]. Diagnoses were based on symptoms and clinical signs, and results from clinical examinations such as CT/MR
scan, autopsy, spinal fluid examination or surgery for intracerebral hemorrhage or subarachnoid hemorrhage that permitted distinction between different stroke subtypes. Stroke was catego-

Study Size
The size of the cohort of 19,698 individuals was determined in
1976 as being suitable for epidemiological studies in cardiovascular disease [11]. At the second examination in 19811983 the cohort was expanded by a random sample of 500 men and women
aged 2024 years. At the third examination in 19911994, the cohort was expanded by 3,000 men and women aged 2049 years,
and at the fourth examination in 20012003 the expansion was by
1,040 persons aged 2029 years from the same area of the town.

Long-Term Survival after Stroke

Neuroepidemiology 2009;33:254260

255

Stroke

No stroke
Age <65
Age 6571
Age 7279
Age >79

Age <65
Age 6571
Age 7279
Age >79

1.0

Survival

0.8
0.6
0.4
0.2
0
0

10

15

20

25

30

Time after stroke onset, years

Fig. 1. Kaplan-Meier survival curves according to quartiles of age

at stroke onset in solid lines. Kaplan-Meier survival curves for a

sample of the 2nd Copenhagen City Heart Study (19811983) with
the same age and sex distribution but without stroke in dashed
lines.

Table 1. Mean age at stroke onset in the Copenhagen City Heart

Study
Years

19781981
19821985
19861989
19901993
19941997
19982001

Women

Men

age, years

age, years

110
128
159
147
237
214

66.7
68.2
72.7
72.1
75.8
77.7

180
175
182
154
187
178

67.2
68.0
68.0
70.9
71.5
74.3

Table 2. Relative risk of death (95% CI) for time period in a sexstratified Cox model adjusted for age at stroke onset

Period

First week

First month

After the
first week

19781981
19821985
19861989
19901993
19941997
19982001

1 (reference)
2.08 (1.223.55)
1.78 (1.043.04)
0.97 (0.521.79)
0.82 (0.451.50)
1.21 (0.692.11)

1 (reference)
1.24 (0.831.86)
1.39 (0.952.04)
0.79 (0.511.22)
0.76 (0.511.14)
0.81 (0.541.21)

1 (reference)
0.87 (0.731.04)
0.82 (0.690.98)
0.72 (0.600.86)
0.66 (0.550.79)
0.56 (0.460.68)

256

Neuroepidemiology 2009;33:254260

Of 24,260 invited participants 464 (1.9%) were lost to follow-up

due to emigration or in 6 cases to settlement in Greenland.
Quantitative Variables
Time of stroke onset was grouped into six consecutive 4-year
periods: (1) January 1, 1978, to December 31, 1981; (2) January 1,
1982, to December 31, 1985; (3) January 1, 1986, to December 31,
1989; (4) January 1, 1990, to December 31, 1993; (5) January 1,
1994, to December 31, 1997, and (6) January 1, 1998, to December
31, 2001.
Statistical Methods
The association between mortality and age at stroke onset was
examined with Kaplan-Meier survival curves, which were also
used to compare survival for the different subtypes of stroke. Cox
regression analyses were used to estimate relative risks of death
after stroke adjusting for age at stroke onset. Time since stroke
was used as the underlying time scale.
By plotting the observed cumulative residuals against the continuous covariate age at stroke and comparing it to random realizations under the model we were able to reveal information
about misspecification of the functional form of that covariate.
The supremum test was performed for cumulative residuals, and
the functional representation of the covariate was acceptable. The
assumption of proportionality in the Cox regression models was
tested with the score process test of Lin et al. [14].
The assumption of proportional hazards in the Cox model was
not met when modeling both acute and long-term survival in the
same model. Therefore long-term survival was estimated after
exclusion of deaths occurring during the first week. The expected
remaining lifetime after stroke was calculated by integrating the
predicted survival curve estimated in the Cox model.
We considered a level of 5% as statistically significant.
All statistical analyses were performed with R (http://www.
cran.r-project.org), version 2.8.0.

Results

In this cohort the participants age increased over the

observation period from a mean age in 19761978 of 56.0
years to a mean age of 61.2 years in 20012003. Age at
time of first-ever stroke increased successively during the
observation period (table 1). During follow-up a total of
2,051 subjects developed a first-ever stroke of whom 1
participant (0.05%) was lost to follow-up. 1,056 (51%)
strokes occurred in men and 995 (49%) in women. Figure
1 shows Kaplan-Meier survival curves according to quartiles of age at stroke onset. A sample of participants from
the second examination (CCHS, 19811983) without
stroke but with a similar age and sex distribution as the
stroke population was used as a reference population. As
expected, survival is lower for participants with stroke
compared to participants without. Clearly survival after
stroke strongly depends on age at stroke onset. In the 65Boysen /Marott /Grnbk /Hassanpour /
Truelsen

19781981
19821985
19861989
19901993
19941997
19982001

1.0

Survival

0.8

0.6

0.4

0.2

0
0

10

15

20

25

Time after stroke onset, years

Table 3. Expected remaining lifetime (years) for 1-week survivors

after stroke according to age at stroke onset and time period

50 years 60 years 70 years 80 years 90 years

Women
19781981
19821985
19861989
19901993
19941997
19982001

14.2
15.0
15.4
16.2
16.7
17.6

9.5
10.5
10.9
11.8
12.4
13.5

5.4
6.2
6.5
7.3
7.8
8.8

2.6
3.1
3.3
3.8
4.2
4.9

1.1
1.3
1.4
1.7
1.9
2.3

Men
19781981
19821985
19861989
19901993
19941997
19982001

13.2
14.2
14.7
15.6
16.2
17.2

8.5
9.4
9.8
10.7
11.3
12.5

4.8
5.4
5.7
6.4
6.8
7.8

2.4
2.8
2.9
3.4
3.7
4.3

1.0
1.2
1.3
1.6
1.7
2.1

Fig. 2. Predicted survival for men aged 70 at the time of stroke for

successive time periods.

to 72-year age group 11% survived 15 years after stroke.

In the age group !65 years 28% survived 15 years, and in
this group 8% were still alive after 25 years.
Acute and Long-Term Survival
Case fatality within 7 days was 17% (358 of 2,051). The
relative risk of death adjusted for age in the first week after stroke was 0.81 (95% CI 0.601.08) in men compared
with women. Beyond the first week the relative risk of
death was 1.19 (95% CI 1.071.32) in men compared with
women. Table 2 shows the relative risk of death within 1
week, 1 month, and after the first week for each time period in a sex-stratified Cox model adjusted for age at
stroke onset. In time periods 19821985 and 19861989
the risk of death within the first week was significantly
higher than in the reference period 19781981. There was
no tendency of a reduced risk of death with time. Analysis of the relative risk of death within the first month
showed an insignificant trend of reduced risk in later periods. Long-term risk of death decreased steadily over
time.
Figure 2 shows the predicted survival curves for men
aged 70 years at time of stroke in the six successive time
periods. Long-term survival steadily improved from 1978
to the end of 2001. A similar pattern was found in women
(not shown). Here only the 1-week survivors were considered.
Long-Term Survival after Stroke

Expected Remaining Lifetime and Gain in Life

Expectancy
Table 3 shows the expected remaining lifetime after
stroke for 1-week survivors in the six 4-year periods for
women and men according to age at stroke onset. A gradual increase in remaining years from 1978 to the end of
2001 is apparent in both sexes and all ages. Women could
expect to live a few more months after stroke than men.
Figures 3a and c show gain in life expectancy from
1981 to the end of 2001 in the general Danish population
in various age groups of women and men as compared
with life expectancy in 1981. Figures 3b and d show gain
in life expectancy after stroke as compared to life expectancy after stroke in 19781982 in the same age groups.
The gain in remaining lifetime after stroke exceeded that
of the general population.
Subclassification of Stroke
There were 863 (42%) unspecified strokes with a mean
age of 74.1 years, 954 (47%) ischemic strokes with mean
age of 70.2 years, 161 (8%) intracerebral hemorrhages
with mean age of 69.6 years, and 73 (4%) subarachnoid
hemorrhages with mean age of 61.8 years. Kaplan-Meier
survival curves for the 4 diagnostic groups unadjusted for
age is shown in figure 4.
Causes of Death
Causes of death in stroke patients were cerebrovascular diseases in 37%, other cardiovascular diseases in 28%,
cancer in 12%, and other causes in 23%.
Neuroepidemiology 2009;33:254260

257

Increase in remaining lifetime, years

Increase in remaining lifetime, years

Female population of Denmark

Age
50 years
60 years
70 years
80 years
90 years

0
1981

1982
1985

1986
1989

1990
1993

1994
1997

1998
2001

Women with stroke (CCHS)

Stroke age
50 years
60 years
70 years
80 years
90 years

0
1978
1981

Age
50 years
60 years
70 years
80 years
90 years

0
1981

1982
1985

1986
1989

1990
1993

1994
1997

1986
1989

1990
1993

1994
1997

1998
2001

1994
1997

1998
2001

Men with stroke (CCHS)

Increase in remaining lifetime, years

Increase in remaining lifetime, years

Male population of Denmark

1982
1985

1998
2001

Stroke age
50 years
60 years
70 years
80 years
90 years

0
1978
1981

1982
1985

1986
1989

1990
1993

Fig. 3. Increase in remaining lifetime for 1-week survivors after stroke in women (b) and in men (d) from 1978

to the end of 2001. The left-hand side shows the increase in remaining lifetime for the entire Danish population
(a, c) from 1981 to the end of 2001.

Discussion

The present study shows that long-term survival after

stroke has improved from 1978 to the end of 2007. The
increase in life expectancy after stroke was markedly
higher than recorded in the general population, as has
been found by others [15]. In our study neither 1-week nor
1-month case fatality decreased significantly between
1978 and 2001, although there was an insignificant trend
to a decrease in 1-month case fatality. Investigators from
different regions of the world have documented a decrease in 1-month case fatality over the last several decades [16, 17]. The largest study based on the entire population of Scotland showed a significant decrease in 30-day
case fatality between 1985 and 2005 [18]. There is no clear
258

Neuroepidemiology 2009;33:254260

explanation for the lack of improvement in our cohort.

Stroke units were gradually implemented in Danish hospitals in the late 1990s; however, not until after 2000
would the majority of stroke patients be admitted to
stroke units. They could therefore have only limited effect in our study period.
The improved long-term survival is in agreement
with other studies with observation periods of 1015
years [1922]. There may be several contributing factors
such as a higher awareness of stroke in the general population and among physicians which may have improved detection of less severe stroke, and the possibility that strokes have generally become milder [2325].
Improved prevention probably has contributed to better
survival.
Boysen /Marott /Grnbk /Hassanpour /
Truelsen

Ischemic stroke
Unspecied stroke
Intracerebral hemorrhage
Subarachnoid hemorrhage

1.0

0.8

Survival

0.6

0.4

0.2

0
0

10

15

20

25

30

Time after stroke onset, years

Fig. 4. The Kaplan-Meier survival curves according to stroke sub-

type.

That survival after stroke is reduced when compared

with that of persons who have not suffered a stroke is in
agreement with most studies on survival after stroke.
Among the different stroke subtypes, patients with ischemic stroke survived substantially longer than those with
intracerebral hemorrhage and unspecified stroke. Patients in the latter group were older than patients in the
other groups, and it probably contains some hemorrhagic events, which may contribute to the lower survival.
In the Dutch TIA Trial [26] 60% had died after 10
years, while in the present study 74% of participants with
ischemic stroke had died at 10 years, which reflects that
our sample was population-based and also included the
severest stroke patients, while the Dutch population consisted of patients with TIAs and minor stroke.
The most frequent cause of death in our stroke patients was cerebrovascular disease, as has been shown by
others [20, 21, 25]. Other cardiovascular diseases come in
as the second most frequent cause of death. The distribution of causes of death was stable during the study period.

were admitted to a number of different services not reporting stroke severity. Neither could we adjust for other
risk factors such as atrial fibrillation, diabetes, smoking,
socioeconomic status, etc., due to inclusion of patients
who did not respond to our invitation. It is also a limitation that most of the stroke diagnoses were obtained
through registers and not hot pursuit. Some stroke
events may have escaped detection due to the limited access to false-negative cases. Among those who did not
respond, patients who were not admitted for their stroke
were not detected, which may amount to approximately
4% of all stroke events in the cohort. The large number of
unspecified strokes is due to insufficient diagnostic capability in the early years of this study.
The strength of this study is its large, well-defined
population-based design, and its length of follow-up.
Stroke events were validated prospectively with uniformity of standardized diagnostic criteria. First-ever stroke
events in participants who responded as well as those
who did not respond were included in this study through
public databases. Each positive diagnosis was validated
from patient hospital records. In responders, also nonfatal non-hospitalized stroke patients were included by
asking either the participants at the study visits or their
general practitioners.
Interpretation
Our results of improved long-term survival after
stroke are in agreement with other studies [1621]. The
improvement may be related to less severity of the strokes,
to increased awareness of stroke in the population, to implementation of stroke units, to better secondary prevention, and to increased life expectancy in the population
as a whole.
Generalizability
Our cohort represents a city population with documented reduced life expectancy compared to the remaining Danish population [29]. Previous studies from CCHS
[911] have documented a high rate of smoking and a
relatively low socioeconomic status both of which may
contribute to unfavorable long-term survival. Our results
may be generalizable to other city populations.
Acknowledgement

Limitations and Strengths

Stroke survival is dependent on stroke severity and
functional status [27, 28]. It is a limitation that we did not
have access to such data in this cohort because patients

We thank Merete Appleyard for her excellent data management throughout the entire study period.
The Copenhagen City Heart Study is supported mainly by the
Danish Heart Foundation.

Long-Term Survival after Stroke

Neuroepidemiology 2009;33:254260

259

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