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Korean Circulation Journal logoLink to Korean Circulation Journal
. 2016 Jul 21;46(4):507–514. doi: 10.4070/kcj.2016.46.4.507

Thirty-Year Trends in Mortality from Cerebrovascular Diseases in Korea

Seung Won Lee 1,2, Hyeon Chang Kim 2,3,, Hye Sun Lee 4, Il Suh 3
PMCID: PMC4965429  PMID: 27482259

Abstract

Background and Objectives

Cerebrovascular disease is a leading cause of mortality and morbidity in Korea. Understanding of cerebrovascular disease mortality trends is important to reduce the health burden from cerebrovascular diseases. We examined the changing pattern of mortality related to cerebrovascular disease in Korea over 30 years from 1983 to 2012.

Subjects and Methods

Numbers of deaths from cerebrovascular disease, hemorrhagic stroke, and cerebral infarction were obtained from the national Cause of Death Statistics. Crude and age-adjusted mortality rates were calculated for men and women for each year. Penalized B-spline methods, which reduce bias and variability in curve fitting, were used to identify the trends of 30-year mortality and identify the year of highest mortality.

Results

During the 30 years, cerebrovascular disease mortality has markedly declined. The age-adjusted cerebrovascular disease mortality rate has decreased by 78% in men and by 68% in women. In the case of hemorrhagic stroke, crude mortality peaked in 2001 but age-adjusted mortality peaked in 1994. Between 1994 and 2012, age-adjusted mortality from hemorrhagic stroke has decreased by 68% in men and 59% in women. In the case of cerebral infarction, crude and age-adjusted mortality rates steeply increased until 2004 and 2003, respectively, and both rates decreased rapidly thereafter.

Conclusion

Cerebrovascular disease mortality rate has significantly decreased over the last 30 years in Korea, but remains a health burden. The prevalence of major cardiovascular risk factors are still highly prevalent in Korea.

Keywords: Cerebrovascular disorders, Stroke, Mortality, Trends, Korea

Introduction

Cerebrovascular disease mortality ranks as the second most common cause of death around the world,1) but, in Korea, cerebrovascular disease is the leading cause of death among single -organ diseases.2),3) Every year approximately 105000 people experience a new or recurrent stroke and more than 26000 people die.2) Fortunately, there have been great improvements in the management of stroke over the last decades. Among the Organization for Economic Cooperation and Development (OECD) member countries, Korea recorded the lowest in-hospital, 30-day case-fatality rate for ischemic stroke and the third lowest rate for hemorrhagic stroke in 2009.2),4) Understanding cerebrovascular disease mortality trends is important to reduce the health burden. Mortality trends of cerebrovascular diseases have been reported in many countries including Korea.5),6),7) However, there are only a few studies reporting long-term trends in mortality from cerebrovascular diseases in the Korean population. Thus, we examined the 30-year changing pattern of cerebrovascular disease mortality in Korea to further understand and quantify recent trends in mortality by analyzing the Cause of Death statistics from Statistics Korea.

Subjects and Methods

Annual mortality data were obtained from the Korean Statistical Information Service managed by Statistics Korea (former the Korea National Statistical Office). Mortality statistics with cause of death information have been available since 1983. Causes of death were coded according to the International Classification of Disease, 10th Revision. For the purpose of this study, deaths from cerebrovascular disease (I60-69) were further classified into hemorrhagic stroke (I60-62), cerebral infarction (I63), unspecified stroke (I64), and other cerebrovascular diseases (I65-69). Hemorrhagic stroke included subarachnoid hemorrhage (I60), intracerebral hemorrhage (I61), and other nontraumatic intracranial hemorrhage (I62). Mortality rates from total heart diseases (I00-13 and I20-51) and ischemic heart disease (I20-25) were previously reported.8)

Crude and age-adjusted mortalities were calculated only for cerebrovascular disease, hemorrhagic stroke, and cerebrovascular disease, because reported numbers of deaths from unspecified stroke and other cerebrovascular diseases showed great fluctuation in the 1990s and early 2000s, probably due to changes in classifying causes of death. We calculated age-adjusted mortality through a direct standardization method using the age distribution of the Korean population in 2000 as the standard population. We analyzed data using 10-year age intervals and the same population structure for standardization in men and women to compare mortality by sex. We also presented penalized B-Splines to explore the non-linear pattern of the crude death rate and age-adjusted death rate per 100000 over time in years. Penalized regression methods are used to quantify the notion of roughness of a curve through a suitable penalty function and the necessary compromise between bias and variability in curve fitting can be explicit in estimation of the problem.9)

Results

Numbers of deaths from cerebrovascular disease

Table 1 and Fig. 1 show the number of deaths from cerebrovascular diseases for each year. The absolute number of deaths from cerebrovascular disease did not change much between 1983 and 1990, but it increased rapidly in the early 1990s then stayed high until 2002. However, after 2002, the number of deaths from cerebrovascular disease has consistently declined. The number of deaths from cerebrovascular disease was 26922 in 1983, peaked at 37131 in 1994, and decreased to 25447 by 2013. Number of deaths from hemorrhagic stroke peaked in 2002, while deaths from cerebral infarction reached its peak in 2004. In 1983, deaths from hemorrhagic stroke (n=5549) were almost 8 times more common than deaths from cerebral infarction (n=703). However, since 2003, cerebral infarction has been the most common cause of death among cerebrovascular diseases. The number of deaths from unspecified stroke increased steeply between 1996 and 1998, but it rapidly decreased until recently since 1998.

Table 1. Numbers of deaths from cerebrovascular diseases.

Year Cerebrovascular disease (I60-69) Hemorrhagic stroke (I60-62) Cerebral infarction (I63) Unspecified stroke (I64) Other cerebrovascular disease (I65-69)
Total Men Women Total Men Women Total Men Women Total Men Women Total Men Women
1983 26922 14749 12173 5549 3190 2359 703 381 322 10254 5713 4541 10416 5465 4951
1984 26919 14551 12368 5623 3160 2463 758 416 342 9736 5298 4438 10802 5677 5125
1985 27883 15047 12836 6235 3484 2751 1070 579 491 10117 5479 4638 10461 5505 4956
1986 26966 14513 12453 6371 3557 2814 1172 626 546 9941 5347 4594 9482 4983 4499
1987 25984 13693 12291 6230 3371 2859 1181 612 569 9570 5087 4483 9003 4623 4380
1988 26234 13722 12512 6679 3606 3073 1238 614 624 9680 5064 4616 8637 4438 4199
1989 26505 13848 12657 7230 3788 3442 1533 820 713 9574 4947 4627 8168 4293 3875
1990 27039 13902 13137 6909 3590 3319 1681 898 783 9808 5081 4727 8641 4333 4308
1991 27152 13680 13472 7535 3908 3627 1897 1035 862 8739 4298 4441 8981 4439 4542
1992 32236 15642 16594 8969 4486 4483 2495 1297 1198 9125 4458 4667 11647 5401 6246
1993 35216 16943 18273 9802 4817 4985 2803 1433 1370 9450 4607 4843 13161 6086 7075
1994 37131 17793 19338 10022 5001 5021 3149 1644 1505 10502 4995 5507 13458 6153 7305
1995 36416 17300 19116 9868 4822 5046 3767 1915 1852 10337 4988 5349 12444 5575 6869
1996 34590 16508 18082 10052 4906 5146 4111 2090 2021 9788 4661 5127 10639 4851 5788
1997 33966 16467 17499 9946 4917 5029 4449 2299 2150 11565 5553 6012 8006 3698 4308
1998 34464 16555 17909 10197 5045 5152 4451 2275 2176 17201 8037 9164 2615 1198 1417
1999 34374 16390 17984 10653 5200 5453 4944 2498 2446 16151 7426 8725 2626 1266 1360
2000 34754 16537 18217 10695 5240 5455 7357 3496 3861 13324 6224 7100 3378 1577 1801
2001 35295 17035 18260 10766 5270 5496 7987 3839 4148 11219 5409 5810 5323 2517 2806
2002 37067 17511 19556 10839 5318 5521 10027 4686 5341 9126 4212 4914 7075 3295 3780
2003 36396 17176 19220 10751 5265 5486 11479 5257 6222 7202 3311 3891 6964 3343 3621
2004 34003 16166 17837 9874 4837 5037 11793 5430 6363 5768 2669 3099 6568 3230 3338
2005 31195 14886 16309 9098 4405 4693 10664 4988 5676 4226 1990 2236 7207 3503 3704
2006 29951 14460 15491 8526 4150 4376 10177 4767 5410 4005 1960 2045 7243 3583 3660
2007 29277 13941 15336 8030 3965 4065 10693 4904 5789 2944 1391 1553 7610 3681 3929
2008 27932 13553 14379 7733 3877 3856 9582 4444 5138 2568 1283 1285 8049 3949 4100
2009 25836 12648 13188 7207 3586 3621 8475 4010 4465 2113 1047 1066 8041 4005 4036
2010 26514 12865 13649 7503 3717 3786 8164 3791 4373 1908 943 965 8939 4414 4525
2011 25404 12185 13219 7112 3518 3594 7860 3520 4340 1653 828 825 8779 4319 4460
2012 25744 12380 13364 6767 3337 3430 7490 3469 4021 1554 706 848 9933 4868 5065
2013 25447 12096 13351 6710 3318 3392 7558 3468 4090 1387 629 758 9792 4681 5111

Fig. 1. Number of deaths from cerebrovascular disease.

Fig. 1

Crude and age-adjusted mortality from cerebrovascular disease

The crude mortality rate from cerebrovascular disease showed fluctuating patterns until 2002, but thereafter it decreased. In the 1980s, the crude mortality rate for men was higher than for women, but the gender difference gradually decreased and has reversed since 1991. The crude mortality rate from cerebrovascular disease in 1983 was 73.3 per 100000 in men and 61.5 per 100000 women. In 2012, the crude mortality rate per 100000 was 49.2 for men and 53.1 for women. After the highest crude mortality rate in 1994, there were 33% and 14% mortality decreases in men and women, respectively, until 2012.

Age-adjusted mortality rates from cerebrovascular disease has decreased too, until recently, but the rate has been always higher in men than in women. In 1983, the age-adjusted mortality rate for men was about 2 times higher than for women (124.3 vs. 68.1 per 100000). But the sex difference has gradually reduced to 28.7 per 100000 men and 17.2 per 100000 women in 2012 (Fig. 2).

Fig. 2. Crude and age-adjusted mortality from cerebrovascular diseases fitted by Penalized B-Splines method. (A) Crude mortality from cerebrovascular diseases in men. (B) Crude mortality from cerebrovascular diseases in women. (C) Age-adjusted mortality from cerebrovascular diseases in men. (D) Age-adjusted mortality from cerebrovascular diseases in women.

Fig. 2

Crude and age-adjusted mortality from hemorrhagic stroke

Crude mortality rate from hemorrhagic stroke showed upward trends between 1983 and 2001. But, after 2001, the rate has rapidly decreased. The crude mortality rate for men was higher than for women until 1991, but thereafter the rate for women was higher than men. In 1983, the crude mortality rate from hemorrhagic stroke per 100000 was 15.8 for men and 11.9 for women, but the corresponding rate was 13.3 for men and 13.7 for women in 2012. After the highest mortality rate in 2001, there was about a 39.8% decrease in men and 41.5% decrease in women until 2012.

Age-adjusted hemorrhagic stroke mortality rate peaked in 1994, then the rate decreased in both men and women. Unlike crude mortality, the age-adjusted mortality rate has been consistently higher in men than in women. The age-adjusted hemorrhagic stroke mortality rate per 100000 was 24.4 for men and 14.2 for women in 1983. However, the corresponding rate decreased to 8.6 for men and 5.8 for women by 2012. After the highest age-adjusted mortality rate in 1994, there was a 68.1% decrease in men and a 41.5% decrease in women until 2012 (Fig. 3). It is also notable that crude hemorrhagic stroke mortality peaked in 2001, but the age-adjusted mortality peaked much earlier in 1994.

Fig. 3. Crude and age-adjusted mortality from hemorrhagic stroke fitted by Penalized B-Splines method. (A) Crude mortality from hemorrhagic stroke in men. (B) Crude mortality from hemorrhagic stroke in women. (C) Age-adjusted mortality from hemorrhagic stroke in men. (D) Age-adjusted mortality from hemorrhagic stroke in women.

Fig. 3

Crude and age-adjusted mortality rates from cerebral infarction

Crude mortality rate from cerebral infarction increased until 2004. But, thereafter, the rate has rapidly decreased. Crude mortality rate per 100000 was 1.9 for men and 1.6 for women in 1983, which increased to 22.3 in men and 26.3 for women in 2004, then decreased to 13.8 for men and 16 for women by 2012. After the highest age-adjusted mortality rate in 2004, there was a 30.7% decrease in men and 32.2% decrease in women.

Age-adjusted cerebral infarction mortality rates peaked in 2003. Unlike crude mortality, the age-adjusted cerebral infarction mortality rate has been consistently higher in men than in women. After the highest age-adjusted mortality in 2003, there was about 61.8% decrease in men and 65.6% decrease in women (Fig. 4). Figures without penalized regression splines for cerebrovascular diseases are provided as supplemental data (Supplementary Figs. 1 to 3 in the online-only Data Supplement).

Fig. 4. Crude and age-adjusted mortality from cerebral infarction fitted by Penalized B-Splines method. (A) Crude mortality from cerebral infarction in men. (B) Crude mortality from cerebral infarction in women. (C) Age-adjusted mortality from cerebral infarction in men. (D) Age-adjusted mortality from cerebral infarction in women.

Fig. 4

Discussion

Our study reports the death rate of major cerebrovascular diseases in the Korean population and their trends over the last 30 years. The age-standardized mortality rate from cerebrovascular diseases has significantly decreased since 1983 in Korea and the decline in mortality from cerebrovascular diseases was more prominent in men than women. Over the last three decades, the age-adjusted mortality rate from cerebrovascular diseases decreased, but temporarily increased between 1991 and 1993. This fluctuation might be due to changes of classification of the Cause of Death Statistics in Korea. During the same time period, deaths from hypertensive disease (I10-I15) significantly decreased.8)

In most developed countries, cerebrovascular disease had been among the leading causes of death in the past, but it has decreased in recent decades.10),11) In particular, Australia, New Zealand, and the UK showed a continuous decline in cerebrovascular disease mortality since 1950. The United States showed a steep declining trend since the 1970s and the trend was more prominent in men than women.10),11),12) Among Asian countries, Japan had the highest cerebrovascular disease mortality in the 1950s (433 per 100000 in men in 1957), but the rate significantly decreased to less than 100 per 100000 by 2004.6),10) Recent studies reported that the stroke mortality rate of Korea was double that of Japan in the beginning of the 2000s,10) although both Japan and Korea showed decreasing mortality trends for stroke at that time.13)

A number of studies reported the accelerated decline in stroke mortality during the late 1970s and the early 1980s. Among them, some earlier studies reported declining trends in the stroke incidence rate as well as stroke fatalities during the 1970s,14),15) suggesting that the effect of stroke incidence rate on stroke mortality.14) However, there was no significant association between stroke mortality and stroke incidence in Sweden.15) This study reported that a decline of mortality from stroke may be due to a decline of smoking and blood pressure (BP) together with an increase in the use of anti-hypertensive treatments rather than changes of stroke incidence.15) Accordingly, it may be because acute stroke events have become less severe and the survival rate of stroke patients is increasing.

The successful control of risk factors may have contributed to declining incidence and fatality of stroke, which may lead to the decreasing trends of stroke mortality.16),17) In most populations, hypertension is the most attributable factor for cerebrovascular disease.18),19),20) In a previous study analyzing data from 1998-2011 available in the Korea National Health Nutrition Examination Survey (KNHANES),21) the age-adjusted prevalence of hypertension decreased by 0.2 to 0.3 percent annually. The study reported that mean systolic BP level decreased by 8 mmHg in men and by 10 mmHg in women during this period which suggested that decreasing BP was largely due to lowered BP levels among patients with diagnosed hypertension.21) The improved BP control might contribute to the remarkable decrease in stroke mortality in Korea. In another systematic review of data from Korean or other populations, the attributable risk of hypertension for ischemic stroke was 19.9 to 30.5% in men and 17.1 to 26.6% in women.22) At ages 40 to 69, usual BP is directly related to stoke mortality in a meta-analysis of clinical trials.23) On the other hand, a few studies were unconvincing that improvement in control of hypertension resulted in a decline of mortality from stroke.24) However, according to a meta-analysis of clinical trials in 1992, anti-hypertensive treatment reduced fatal strokes by 33% and cardiovascular mortality by 22%.25),26) The use of cholesterol-lowering medications also decreased stroke risk and mortality in observational studies and clinical trials.27),28) Improved acute stroke management might also contribute to the mortality decline.7) Between 1998 and 2002, the prevalence of hypertension decreased, whereas the prevalence of hypercholesterolemia significantly increased in both sexes.4) Smoking rate decreased only in men, whereas the prevalence of diabetes did not change over time. Another study reported epidemiologic trends of ischemic stroke between 2002 and 2010, by analyzing data from the Korean Stroke Registry.29) Patient's age steadily increased, while prevalence of risk factors such as hypertension, diabetes, and smoking declined. Although cerebrovascular disease mortality rate has decreased over the last 30 years, cerebrovascular disease still remains a great burden to society and is a major cardiovascular risk factor prevalent among Koreans. To further reduce the burden of cerebrovascular disease, we need to monitor the trends of mortality from cerebrovascular disease and its subcategories, because management and prevention strategies for different stroke types vary.

The major strength of the present study is that it analyzed nationwide mortality data covering 30 years in the Korean population. But, there are also several limitations to be discussed. First, validity of cause of death can be debated. The Statistics Korea report annually the Cause of Death Statistics, and the database are primarily based on the death certificates. A previous study retrospectively compared the Cause of Death Statistics with hospital medical records, and reported the overall accuracy of causes of death as 91.9%.30) Second, there are still a significant number of deaths recorded without underlying causes in the Death Statistics. In 2012, 9.4% of deaths were classified as unknown, although the deaths by unknown causes are decreasing. Thus there is a possibility of underestimation of mortality from cerebrovascular disease. Third, the reported number of cerebrovascular deaths can be influenced by the health care system. Over the last decades, Korea experienced marked improvement in medical service accessibility and health care technologies. These changes might affect the reported number of cerebrovascular diseases. Lastly, there is no available nationwide data on the incidence of cerebrovascular disease, so we cannot explore the underlying causes of changing mortality trends.

In conclusion, cerebrovascular disease mortality has significantly decreased over the last 30 years, but remains a great health burden and the prevalence of major for cardiovascular risk factors are still highly prevalent in Korea. We need to continuously monitor the trends of mortality from cerebrovascular disease and its subcategories to further reduce cerebrovascular disease burdens.

Acknowledgments

This work was supported by the Korean Health Technology R&D Project, Ministry of Health & Welfare, Korea (HI13C0715).

Footnotes

The authors have no financial conflicts of interest.

Supplementary Materials

The online-only Data Supplement is available with this article at http://dx.doi.org/10.4070/kcj.2016.46.4.507.

Supplementary Fig. 1

Crude and age-adjusted mortality from cerebrovascular disease (I60-I69).

kcj-46-507-s001.pdf (42.7KB, pdf)
Supplementary Fig. 2

Crude and age-adjusted mortality from hemorrhagic stroke (I60-62).

kcj-46-507-s002.pdf (42.1KB, pdf)
Supplementary Fig. 3

Crude and age-adjusted mortality rates from cerebral infarction (I63).

kcj-46-507-s003.pdf (41.9KB, pdf)

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Fig. 1

Crude and age-adjusted mortality from cerebrovascular disease (I60-I69).

kcj-46-507-s001.pdf (42.7KB, pdf)
Supplementary Fig. 2

Crude and age-adjusted mortality from hemorrhagic stroke (I60-62).

kcj-46-507-s002.pdf (42.1KB, pdf)
Supplementary Fig. 3

Crude and age-adjusted mortality rates from cerebral infarction (I63).

kcj-46-507-s003.pdf (41.9KB, pdf)

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