212

Secular Trend of Mortality From Cerebral

Infarction and Cerebral Hemorrhage
in Taiwan, 1974-1988
Chung-Chung Chang, MS, and Chien-Jen Chen, ScD

Background and Purpose: Pathological patterns of stroke are different in various races, with the
predominant stroke type in the Chinese being intracerebral hemorrhage. A total of 31,078 deaths from
cerebral infarction and 77,773 deaths from cerebral hemorrhage in Taiwan were reported for groups of
subjects aged 40-79 years during the period 1974-1988 to elucidate their secular trends.
Methods: Vital statistics and demographic data were collected for analyzing the truncated age-adjusted
mortality rates. Poisson regression analysis was used to estimate the relative risk and 95% confidence
interval.
Results: The mortality rates for cerebral hemorrhage were greater than those for cerebral infarction. The
mortality rates increased exponentially with age for both subtypes. The decline in age-specific mortality for
the period 1974-1983 was much more striking for cerebral hemorrhage than for cerebral infarction.
Mortality from cerebral infarction and hemorrhage increased with age for all birth cohorts except the
cerebral hemorrhage mortality of the oldest cohort. Male/female ratios for both cerebral infarction and
hemorrhage were greater in the younger age groups. The cerebral hemorrhage/infarction ratio during the
period 1984-1988 was highest for the younger age groups and lowest for the oldest age groups.
Conclusions: The different secular trends of mortality from cerebral infarction and hemorrhage imply that
these two patterns of stroke may be associated with some different risk factors. (Stroke 1993;24:212-218)
KEY WORDs * cerebral infarction * cerebral hemorrhage * epidemiology * mortality * Taiwan

P athological patterns of cerebrovascular disease
(CVD) and distributions of cerebrovascular le-
sions are different in various races. Only 6.3-
11.9% of strokes in whites were reported to be intra-
cerebral hemorrhage,'-4 whereas 21-48% of strokes
were estimated to be hemorrhagic in the Chinese.5-7
This racial discrepancy may be attributable to differ-
ences in admission policy, diagnostic accuracy, and age
distribution as well as related risk factors.8 Blacks and
the Japanese have more intracranial occlusive CVD,
whereas whites have more extracranial CVD.9-12 The
preponderance of intracranial vascular lesions in the
Chinese is similar to that seen in blacks and the
Japanese.13,14 This difference in the distribution of
lesions is not readily explained by the differences in
incidence of transient ischemia, hypertension, diabetes,
hypercholesterolemia, or ischemic heart disease.
CVD has been the most common cause of death in
mainland China and Taiwan. It was the leading cause of
death from 1963 to 1982 and has become the second
From the Institute of Public Health, National Taiwan University
College of Medicine (C.-C.C., C.-J.C.), and the Institute of Bio-
medical Sciences, Academia Sinica (C.-J.C.), Taipei, Taiwan,
Republic of China.
Supported by the Department of Health, Executive Yuan,
Republic of China.
Address for reprints: Chien-Jen Chen, ScD, Institute of Public
Health, National Taiwan University College of Medicine, 1.
Jen-Ai Road Section 1, Taipei 10018, Taiwan, Republic of China.
Received September 18, 1992; final revision received November
9, 1992; accepted November 9, 1992.
most common cause of death in Taiwan.'5 Many epide-
miological studies of CVD reported a downward trend
in stroke mortality and morbidity in developed coun-
tries in the past 30 years.'6-22 Stroke mortality has been
decreasing in Taiwan since 1967,23 but the magnitude of
decline is not as striking as that in the United States and
Japan. During the period 1972-1979, stroke mortality
declined 13.8% for men and 16.6% for women in
Taiwan; these percent changes were approximately half
those in the United States and Japan.24 In other words,
stroke mortality in Taiwan decreased by approximately
2% per year from 1972 to 1983 and approximately
4-5% per year after 1984.25 Because the pattern of
CVD is important for diagnostic, therapeutic, rehabili-
tative, and preventive purposes, the present study re-
ports the secular trend of mortality from cerebral
infarction (CI) and cerebral hemorrhage (CH) in Tai-
wan between 1974 and 1988 by age, calendar year, and
birth year by use of Poisson regression analysis.
Subjects and Methods
In Taiwan, because it is mandatory to register any
event of birth, death, marriage and divorce, migration,
and employment in the household registration offices,
the vital statistics and demographic data are very com-
plete.26 Information on all deaths from CVD in Taiwan
was abstracted from annual vital statistics published by
the Department of Health from 1974 to 1988.'5 More
than 95% of the death certificates are issued by physi-
cians in public or private hospitals. Another 4% of the
death certificates, primarily those in which accidents are

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o

o'
500

400-

Calendar
14~~~~~~2
1~ ~ ~ ~ 0(A) Male

year
-CVA
+
CH

involved, are issued by coroners. Only about 0.7-1% of

°
°

30010
Chang and Chen Cerebral Infarction and Hemorrhage in Taiwan

350)

300

250-

0~~~~~~~~~~~~0
a~~~~~~~~ x
<
(B) Female

Calendar year
FIGURE 1. Graphs showing the secu-
213

lar trend of age-adjusted mortality

from cerebrovascular disease (CVA),
cerebral hemorrhage (CH), and cere-
bral infarction (CI) for men (panel A)
and women (panel B) aged 40-79
years in Taiwan, 1974-1988.

The data of midyear population by age and sex in

the death certificates are completed by other health
personnel and local officers, who may not be familiar
with the form of death certificates and diagnostic crite-
ria for CVD. In other words, the causes of death listed
in the certificates are considered accurate to an accept-
able level. Mortality data were grouped by sex, age in
5-year groups, and detailed cause of death. Mortality
from Cl and CH was identified as 433-434 and 431,
respectively, in both the eighth and ninth editions of the
International Classification of Diseases (ICD-8 and
ICD-9, respectively).7 Only few or no deaths were
observed among groups of subjects aged <40 years, and
therefore mortality rates were calculated for groups
aged 40-79 years. A total of 171,022 deaths from CVD,
31,078 deaths from Cl, and 77,773 deaths from CH were
reported for groups aged 40-79 years during the period
1974-1988.
Taiwan were obtained from Demographic Facts, which is
published annually by the Taiwan Ministry of the Inte-
rior.26 From 1974 to 1988, a total of 64,796,035 person-
years were observed for groups aged 40-79 years. To
examine the secular trend of mortality in the last 15
years, truncated age-adjusted mortality rates were cal-
culated using the direct standardization method and
world population in 1976 as the standard population.28
In the data analysis, mortality as grouped by age (eight
5-year groups: 40-44, 45-49, 50-54, 55-59, 60-64,
65-69, 70-74, and 75-79), calendar year (three 5-year
groups: 1974-1978, 1979-1983, and 1984-1988), and
birth year (six 5-year groups: 1909-1913, 1914-1918,
1919-1923, 1924-1928, 1929-1933, and 1934-1938).
The mortality of CVD is assumed to follow a Poisson
distribution. The Poisson regression analysis29 was used
to estimate the relative risk with a 95% confidence

(A) Male (B) Female

1000- . O °100
o -~~1974-78 . O
o -~~1979-83 .
N 1984-88 /
100 loo-

FIGURE 2. Graphs showing mortality

rates fromcerebral infarction by age and
calendar year for men (panel A) and
women (panel B) aged 40-79 years in
Taiwan, 1974-1988.

1- l l
jo p4:ms 0CM<,
,o ^-h
AX0+,h 01 i-*-^--

Age Age

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214 Stroke Vol 24, No 2 February 1993

(A) Male (B) Female

- 1974-78
a0
- 1979-83
0.
0.

14.
- 1984-88 a

4..

4..
*4i4J00 FIGURE 3. Graphs showing mortality
100- rates fromcerebral hemorrhage by age and
10 to
:1 calendaryearfor men (panelA) and women
(panel B) aged 40-79 years in Taiwan,
1974-1988.

1- 1 g
fit (01,15 l.. 10
(OIW llpr l..
Age Age

interval for each age, calendar period, and birth cohort
group based on a maximum-likelihood method. The
statistical package EGRET30 was used in the computation.
Results
Secular trends of age-adjusted mortality from CVD,
CI, and CH for men and women in Taiwan from 1974 to
1988 are shown in Figure 1. There was a significant
decline of CVD and CH mortality for both men and
women, but no decrease in CI was observed until after
1979 for men and after 1981 for women. The mortality
rates of CH were greater than those of CI, and men had
higher mortality rates than women, particularly for CH.
Figure 2 illustrates secular trends of age-specific mor-
tality rates of CI by calendar year. CI mortality rates of
men and women increased exponentially with age. The
relative risks of CI in the group aged 75-79 years
compared with the group aged 40-44 years were 152.4
and 185.9, respectively, for men and women, with a 95%
confidence interval of 130.1-177.5 and 157.4-219.2,
respectively. The changes in age-specific mortality rates
from the period 1974-1978 to the period 1979-1983
were smaller than those from the period 1979-1983 to
the period 1984-1988. The age-adjusted relative risks
(and 95% confidence interval) of CI in the periods
1974-1978 and 1979-1983 compared with the period
1984-1988 were 1.60 (1.54-1.66) and 1.41 (1.36-1.46)
for men and 1.45 (1.40-1.51) and 1.36 (1.30-1.41) for
women.
As shown in Figure 3, CH mortality rates also in-
creased exponentially with age for both men and
women. The relative risks of CH in the group aged
75-79 years compared with the group aged 40-44 years
were 28.3 and 52.8, respectively, for men and women,
with a 95% confidence interval of 26.8-30.0 and 48.9-
56.9, respectively. The change in age-specific mortality
rates of CH from the period 1974-1978 to the period
1979-1983 was similar to that from the period 1979-
1983 to the period 1984-1988 for both men and women.
The age-adjusted relative risks (95% confidence inter-
val) of CH in the periods 1974-1978 and 1979-1983
compared with the period 1984-1988 were 2.84 (2.77-
2.91) and 1.73 (1.69-1.78) for men and 2.65 (2.58-2.73)
and 1.64 (1.59-1.68) for women.
The changing pattern for CH between these two
calendar periods was similar for all age groups of men
and women, as was the pattern for CI except for the
group of women aged 50-54 years. The decline in
age-specific mortality from the period 1974-1988 was
much more striking for CH than for CI, especially for
groups aged .50 years.

TABLE 1. Male/Female Ratio of Cerebral Infarction and Cerebral Hemorrhage by Age and Calendar Year in
Taiwan, 1974-1988
Age Cerebral infarction Cerebral hemorrhage
(years) 1974-1978 1979-1983 1984-1988 1974-1978 1979-1983 1984-1988
40-44 0.92 1.35 1.25 1.82 1.71 2.17
45-49 0.85 1.02 1.57 1.27 1.44 1.71
50-54 0.82 1.40 1.17 1.23 1.24 1.49
55-59 1.05 0.91 1.15 1.30 1.38 1.25
60-64 1.15 1.10 1.01 1.38 1.32 1.26
65-69 1.24 1.06 0.90 1.30 1.19 1.03
70-74 1.11 1.03 1.04 1.17 1.10 0.94
75-79 0.98 0.94 0.93 1.13 1.06 0.94

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 Chang and Chen Cerebral Infarction and Hemorrhage in Taiwan 215

(A) Male (B) Female

11

a a
a
0.
0 0.
a a
a0 a
14 14J
42
---
4J
-
1914-18 0
4J
JJ
0 FIGURE 4. Graphs showing mortality
0 1o rates from cerebral infarction by age and
:.
birth year for men (panel A) and women
-1929-133
-01 929-133 <
1 (panel B) aged 40-79 years in Taiwan,
1974-1988.

`1934-38

11 1 1 ,
/#<oRfi¢oRfCO .%h

Age Age

Mortality rates for CH were higher than those for CI,
and the male/female (M/F) ratio (as shown in Table 1)
ranged from 0.94 to 2.17 for CH and from 0.82 to 1.57
for CI in various age groups during the periods 1974-
1978, 1979-1983, and 1984-1988. The M/F ratio of CH
was greater in the younger age groups. The ratio
increased with the calendar period in groups aged <55
years but decreased with the calendar period in the
older age groups. The M/F ratio of CI increased with
the calendar period for groups aged <60 years and
decreased with the calendar period for the older age
groups.
Figure 4 illustrates secular trends of age-specific
mortality rates for CI for various cohorts according to
their birth years. The mortality rates increased with age
in all birth cohorts for both men and women. But as
shown in Figure 5, the CH mortality of men increased
with age only in the younger cohorts.
There was a decline in CH mortality with age in
cohorts born before 1929. However, the CH mortality of
women either increased or remained similar for all birth
cohorts except the oldest cohort, born in 1909-1913.
Figure 6 presents the secular trends of CH/CI ratio by
age and calendar year. CH/CI ratios of 1974-1978 were
greater than those of 1979-1983 in all age groups for
men and in groups aged >50 years for women. But the
ratios in 1984-1988 were highest in groups aged <50
years for both sexes and lowest in groups aged >49
years for men and in groups aged >55 years for women.
Discussion
Striking contrasts are evident in mortality from CVD
compared with mortality from arteriosclerotic heart
disease within countries and internationally. Interna-

(A) Male (B) Female

G 1000-
0
o1 000-
o
0 0
54 0

a a
If

0 100 -_ $
100-
54
:
-
1909-13 0~~F
4) .4 FIGURE 5. Graphs showing mortality
a rates from cerebral hemorrhage by age and
10-0
0 birth year for men (panel A) and women
-1914-18 10- (panel B) aged 40-79 years in Taiwan,
-+ 1919-23 1974-1988.
~
1924-28
1929-33
1934-38 -
1 -r i 9 IP 9 -l
^-h 0 fC ^"
;FW°' f ° ff AF j~ 4%p j %,W p.~ ,14

Age Age

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216 Stroke Vol 24, No 2 February 1993

(A) Male (B) Female

14-
1974-78
+ 1979-83
12-
1984-88

0
e
Cw-
FIGURE 6. Graphs showing cerebral
id
hemorrhage/cerebral infarction (CHICI)
ratio of cerebrovascular disease by age and
-)
calendar year for men (panel A) and
women (panel B) aged 40-79 years in
Taiwan, 1974-1988.

hi %i`4' jio f oA'

Age Age

tional comparisons have shown that in areas with high
stroke and low arteriosclerotic heart disease rates such
as Japan, the predominant CVD is hypertensive intra-
cerebral hemorrhage.31'32 A large-scale epidemiological
study held in mainland China reported that CI ac-
counted for the majority of completed strokes, the same
as elsewhere in the world.6 But compared with white
and Japanese populations, the percentage of CH (44%)
among incident cases in China was much higher than
that reported for white populations (6-12%)1-4 and
somewhat higher than that for Japanese populations
(17%).33 We present here the first study on the secular
trend of CI and CH among the Chinese population in
Taiwan.
Data from vital statistics may have problems of valid-
ity. Revisions of codes for the ICD and changes of the
diagnostic pattern should be taken into consideration in
the assessment of long-term variations in mortality. In
Taiwan, the ICD-8 (codes 431 for CH and 433-434 for
CI) was used from 1974 to 1980, and the ICD-9 (codes
431 for CH and 433-434 for CI) was used from 1981 to
1988. According to the Japanese Ministry of Health and
Welfare, the comparability ratio for change of CVD
classification from ICD-8 (= 1) to ICD-9 was estimated
at 0.9822.34 In the present analysis, this ratio was not
used, and data were taken as part of a continuous trend.
To indicate that there was no movement from one
diagnostic category to another, secular trends of heart
disease, hypertension, and diabetes mellitus against
stroke are shown in Figure 7. There has been an
increase in the mortality from diabetes mellitus and
heart disease. However, the slight increase in these two
diagnostic categories cannot explain the striking decline
in CVD mortality. Because both incidence and case
fatality have impacts on mortality, the interpretation of
mortality data should be cautious. In a large-scale
hospital-based registry in Taiwan, the 30-day case-
fatality rate was 30.7% for CH and 8.4% for CI in 1985,
and it was 26.8% for CH and 10.1% for CI in 1990.35
The slight decrease in the fatality rate for CH may be
due to the increased proportion of fewer life-threaten-
ing stroke events resulting from improved diagnosis of
cases of milder stroke that previously went undetected.
Because the fatality rate remained rather constant in

- 500- '350
i
8 (A) MALES (B) FEMALES
0 8 300-
; 400

Ct 250-
a
FIGURE 7. Graphs showing com-
0
P 300 aE
200
parison of secular trends of age-
8 adjusted mortality rates from cere-
150 -
brovascular disease (CVA), heart
200 disease (HD), diabetes mellitus
CVA l100 (DM), and hypertension (HT) for
100
--- HD
men (panel A) and women (panel

h---- =.:. DM

- HT
50; B) aged 40-79 years in Taiwan,
1974-1988.
0- =T
111
A .% .% .%k% k% k% k%k%000
calendar year calendar year

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 Chang and Chen Cerebral Infarction and Hemorrhage in Taiwan
the study period, the decline of CVD mortality is
perceived as a decrease in stroke incidence of both CI
and CH. Because computed tomography was not widely
used to evaluate patients with completed stroke before
1980, small CH might be misdiagnosed as CI. By 1989
there were 153 computed tomograms in 21 counties
throughout Taiwan, with a coverage rate of 90%. The
actual proportion of CH may be slightly larger than that
shown in the figures.36
Only population-based incidence studies may moni-
tor changes over time and determine whether the
decline in mortality is explained by improvements in
incidence; however, the secular trend of stroke inci-
dence is not available in Taiwan, as in many other
countries. Over the past 30 years, stroke mortality
declined in the United States and Japan as well as some
other developed countries. There is little doubt that the
decline is real rather than an artifact of reporting or
death certificate coding. The striking decline in stroke
mortality suggests the presence of modifiable environ-
mental factors in the development of stroke.
The decline in stroke mortality is basically attribut-
able to the identification of hypertension as the major
risk factor for stroke, and particularly for CH. It has
been demonstrated that treatment of hypertension may
reduce stroke incidence and mortality. In the United
States stroke mortality has been decreasing rapidly
since 1973; it decreased by approximately 2% per year
from 1950 to 1972 and approximately 7% per year after
1973.18 Possible factors related to such a decline include
the decrease in coronary heart disease mortality, the
smoking cessation program, a high intake of potassium,
fresh fruits, and vegetables, and control of hyperten-
sion.37-39 The sheer magnitude of decline in stroke
mortality before 1950 almost certainly reflected a true
decrease in stroke incidence, although the mechanism
for this decline is uncertain. Antihypertensive therapy
certainly could not explain the decline during this early
period.18
In Japan the age-adjusted death rate from stroke has
decreased for both men and women since 1965, and this
downward trend accelerated in 1971.34 The factors
attributable to the decline may not be the same as those
in the United States. Possible contributing factors were
the progress and implementation of detection and treat-
ment of hypertension, a decrease in salt intake, and an
appropriate increase in the consumption of animal fat
and protein.334041 However, in some European coun-
tries such as Finland and Denmark, the total mortality
of stroke without specifying subtypes did not show any
clear decline.
In Finland the history of heart disease was found to be
associated with CVD mortality, but hypertension, diabe-
tes, pure myocardial infarction, and previous transient
ischemic attacks were not associated with CVD mortali-
ty.21 In Copenhagen the stroke incidence was relatively
high, and there was a slight decrease in stroke incidence
among younger women but not in older women or men.42
The magnitude of the ratio between the male and the
female mean incidence rates by increasing age corre-
sponded exactly to the age distribution of the use of oral
contraceptives in Denmark from 1977 to 1982.43 Signifi-
cant potential risks were found for cigarette smoking, high
blood pressure, diabetes, plasma cholesterol concentra-
tion, and ischemic heart disease.44 Among Swedish women
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217
stroke incidence increased by 38% between the 1970s and
1980s; however, the incidence in men did not change
significantly from the first period to the second.45 The
cause of increased stroke incidence among women has not
been established.
In New Zealand the treatment of hypertension was
estimated to account for roughly 10% of the observed
reduction in deaths from stroke.46 A greater under-
standing of the reasons for the decline in mortality from
stroke is required. Studies on secular trends of mortality
and/or incidence rates for a particular disease can
provide clues or hypotheses for testing its etiology. All
these inconsistent secular trends of stroke morbidity
and mortality in various countries imply that the pattern
of stroke varies in countries and races, and subtypes of
stroke may not share similar risk factors.
Stroke is a disease of high mortality in Taiwan. The
high percentage of CH is definitely a contributing factor
to the high mortality. Studies on possible risk factors of
stroke in the Chinese are rare; only hypertension and a
salty diet have been reported.6 Improved management
of hypertension has been proposed as the main reason
for the recent decline in mortality from stroke. Effective
antihypertensive drugs have been available since the
early 1960s in Taiwan, but the range of agents and their
acceptability have not increased considerably over the
past 20 years. Although the prevalence of hypertension
in Taiwan47 was slightly lower than that in Chicago,48
the proportion of hypertensive patients with adequately
controlled blood pressure was approximately 5% in the
former in contrast with approximately 70% in the latter.
The poor control of hypertension in Taiwan may ac-
count for the slow decline of stroke mortality.
Since 1949, the lifestyles of residents in Taiwan have
undergone profound and accelerating changes in regard
to dietary patterns, employment activity, urbanization,
and medical care. All these changes potentially contrib-
uted to an evolving spectrum of stroke. In the mid-
1970s, community-based nutrition education campaigns
and nationwide programs to identify and treat hyper-
tension were implemented to reduce the daily intake of
animal fat and salt and to control hypertension.
As shown in the present study, the decline of CI
mortality from the period 1974-1978 to the period
1979-1983 might not be influenced by these activities,
because CI mortality in each birth cohort year was still
increasing. CH mortality in younger cohorts also in-
creased, and only in older cohorts did CH mortality
show decline. According to the CH/CI ratio, CH was
relatively more important in the younger than in the
older age groups. This implies that CH is a predominant
type of fatal stroke in the Chinese, particularly in
Chinese youth.
In view of the secular trend of CH/CI ratios, control
of hypertension seems to have more of an effect on CH
than on CI. Some widespread modifiable environmental
factors significantly associated with stroke but not with
hypertension may exist. Thus, the risk factors for CI and
CH may be different. The inconsistent decline pattern
of CI and CH may be attributable to the different
impacts of risk factors such as cigarette smoking, alcohol
consumption, serum cholesterol and triglyceride levels,
diabetes mellitus, and coronary heart disease. Future
investigations through case-control studies and cohort
studies are urgently needed.
218 Stroke Vol 24, No 2 February 1993
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C C Chang and C J Chen

Stroke. 1993;24:212-218
doi: 10.1161/01.STR.24.2.212
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
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