(Stroke. 2001;32:1499.)
© 2001 American Heart Association, Inc.
Original Contributions |
From the Department of Neurosurgery, Shimane Prefectural Central Hospital, Izumo, Japan.
Correspondence to Tetsuji Inagawa, MD, Department of Neurosurgery, Shimane Prefectural Central Hospital, Himebara-cho, Izumo, Shimane 693-8555, Japan. E-mail inagawa{at}spch.izumo.shimane.jp
| Abstract |
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MethodsWe compared the incidence and case fatality rates of aneurysmal SAH during the 9-year period 19901998 with those during the 10-year period 19801989 in Izumo City, Japan.
ResultsDuring
19801989 and 19901998, we diagnosed 170 and 188 patients as having
aneurysmal SAH, respectively. The percentage of very elderly
patients aged
80 years increased from 5% (8 patients) during
19801989 to 18% (33 patients) during 19901998
(P<0.001). The age-specific
incidence rate of SAH has a tendency to increase with increasing age.
The crude and the age- and sex-adjusted incidence rates using the 1995
population statistics for Japan were 21 and 23 per 100 000/y for all
ages during 19801989 and 25 and 23 per 100 000/y during 19901998,
respectively. The 3-month case fatality rate of patients aged
79
years decreased from 38% during 19801989 to 26% during 19901998
(P=0.021), whereas the case
fatality rates in patients aged
80 years were very high (63% and
79%, respectively) regardless of study periods. Consequently, the
overall case fatality rates for patients with SAH were similar for the
2 study periods (39% and 36%).
ConclusionsThe age-
and sex-adjusted incidence rates of aneurysmal SAH were stable
over the 19-year period since 1980 and, despite improvement of outcome
in patients aged
79 years, the overall case fatality rate was not
lower because the improvements were counterbalanced by increasing
numbers of very elderly patients
Key Words: cerebral aneurysm epidemiology incidence Japan subarachnoid hemorrhage
| Introduction |
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| Subjects and Methods |
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We collected data on the following risk factors: hypertension, cigarette smoking, alcohol consumption, diabetes mellitus, serum total cholesterol level, and body mass index (BMI). Hypertension was defined as a history of hypertension, regardless of treatment with antihypertension medication. For smoking, patients were divided into 3 groups: (1) current smokers; (2) former smokers; and (3) never smokers. Alcohol intake was also divided into 3 categories: (1) daily drinking; (2) occasional drinking; and (3) no alcohol consumption. Information on diabetes was based on medical history. Serum total cholesterol levels were obtained on admission to hospital, and BMI was calculated as weight divided by height squared. Serum total cholesterol levels and BMI were expressed as the mean±SD.
According to the national census of Japan, the population of
Izumo City was 80 749 at October 1, 1985, 82 679 at October 1, 1990,
and 84 854 at October 1, 1995. The estimates of disease incidence
rates during the 2 study periods were based on the census populations
of 1985 and 1995, respectively, and the rates of the whole period
during 19801998 were based on 1990 census population. The age- and
sex-adjusted annual incidence and mortality rates were estimated with
the 1995 Japan census population data. The CIs of the incidence rates
were calculated according to the method of
Schoenberg.20 For statistical analyses, unpaired
t test,
2 test, or Fishers exact test was
used.
| Results |
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Number of Patients With Aneurysmal
SAH
The age and sex distributions of the patients with SAH
are shown in
Table 2
. When the 2 study periods are compared, the population of Izumo City was 38 578 for men and 42 171 for women in
1985, and it was 40 779 and 44 075 in 1995, respectively. The ratio
of women to men of the population was almost the same: 1.1 for both
years. However, the number of male SAH patients in the 2 study periods
was the same (75), but the number of women increased from 95 during
19801989 to 113 during 19901998. Therefore, the ratio of women to
men was 1.3 during 19801989 and 1.5 during 19901998.
|
During 19801998, the number of SAH patients, including
both sexes, was highest in the group aged 50 to 59 years. However, when
the 2 study periods were compared, the peak number of SAH patients
shifted to the older age group at the later period. Among women,
although the number of SAH patients was highest in those aged 50 to 59
years during 19801989, it was highest in those aged 70 to 79 years
during 19901998. The proportions of elderly patients aged
70 years
were 17% (13 of 75 patients) during 19801989 and 20% (15 of 75
patients) during 19901998 in men
(P=0.417), 27% (26 of 95
patients) and 54% (61 of 113 patients) in women
(P<0.001), and 23% (39 of 170
patients) and 40% (76 of 188 patients) in those including both sexes
(P<0.001). In addition, the
proportion of very elderly patients aged
80 years and including both
sexes increased from 5% (8 of 170 patients) during 19801989 to 18%
(33 of 188 patients) during 19901998
(P<0.001).
During 19801998, the mean age for patients with SAH, including both men and women, was 62.5 years (range, 17 to 97 years). The mean age for SAH patients, including both men and women, increased from 59.6 years during 19801989 to 65.1 years during 19901998 (P<0.001). The mean age for women was significantly higher during 19901998 (68.6 years) than during 19801989 (62.5 years) (P=0.001). However, for men, while it increased from 55.8 years during 19801989 to 59.9 years during 19901998, the difference was not statistically significant (P=0.051).
Incidence Rates
During 19801998, the age-specific average annual
incidence rate of aneurysmal SAH increased with increasing age,
and after 50 years of age, the increase in the rate became steeper
(Table 2
). During 19801989, the peak incidence rate of
aneurysmal SAH was observed in the eighth decade for both men
and women. However, during 19901998, the age-specific average annual
incidence rate of SAH increased with increasing age, and the highest
incidence rate was found in the oldest age group. During 19901998,
the highest incidence rate of aneurysmal SAH was 99 (95% CI,
43 to 195) per 100 000 population of the ninth decade for men, 175
(95% CI, 64 to 382) per 100 000 population of the 10th decade for
women, and 133 (95% CI, 49 to 291) per 100 000 population of the 10th
decade for men and women combined. In both study periods, the
age-specific average annual incidence rates were higher in men than in
women in the younger age groups, but they were higher in women than in
men in the older age groups. The reversals of the incidence rates were
observed in the sixth to the eighth decades.
The average annual crude and adjusted incidence rates for
aneurysmal SAH per 100 000 population were calculated in the
different age groups to allow comparison with data from other published
studies (Tables 2
and 3
). During 19801998, both the crude
and the age- and sex-adjusted annual incidence rates were 23 (95% CIs,
21 to 25 and 21 to 26, respectively) per 100 000 population for all
ages. Both the crude and the age-adjusted annual incidence rates for
SAH were higher in women than in men. The crude annual incidence rates
were 20 (95% CI, 17 to 23) per 100 000 population for men and 25
(95% CI, 22 to 29) per 100 000 population for women, and the
age-adjusted annual incidence rates were 21 (95% CI, 17 to 24) and 26
(95% CI, 22 to 30), respectively. Over the 2 study periods, the crude
annual incidence rates for men were almost equal: 19 (95% CI, 15 to
24) per 100 000 population during 19801989 and 20 (95% CI, 16 to
26) per 100 000 population during 19901998, whereas those for women
increased from 23 (95% CI, 18 to 27) per 100 000 population during
19801989 to 28 (95% CI, 24 to 34) per 100 000 population during
19901998. However, the age-adjusted annual incidence rates were
relatively stable in both sexes. During 19801989, the age-adjusted
annual incidence rates were 21 (95% CI, 17 to 26) per 100 000
population for men and 25 (95% CI, 20 to 30) per 100 000 population
for women, whereas during 19901998 they were 20 (95% CI, 16 to 25)
and 26 (95% CI, 21 to 31), respectively. As a result, the age- and
sex-adjusted annual incidence rates, including both sexes, became the
same for the 2 study periods: 23 (95% CIs, 20 to 27 during 19801989
and 20 to 26 during 19901998) per 100000
population.
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3-Month Case Fatality Rates
Table 4
shows a comparison of the 3-month case
fatality rates of aneurysmal SAH in the different age groups
between the 2 study periods. In this study, to analyze the
relationship between age and sex and outcome, we stratified SAH
patients into those aged
59 years, 60 to 69 years, 70 to 79 years,
and
80 years for men and women separately. In both study periods, no
significant differences were found in the case fatality rates among the
patients aged
59 years, 60 to 69 years, and 70 to 79 years. However,
in the latter period and in the total during 19801998, the case
fatality rates were significantly higher in patients aged
80 years
than in those aged
79 years (both
P<0.001). In both study
periods, there were no significant differences between men and women in
the case fatality rates in each age group. Over the 2 study periods,
there was a trend toward better outcomes in the later period in
patients aged
79 years in both men and women. The case fatality rate
of the patients aged
79 years (both sexes) decreased from 38% (61 of
162 patients) during 19801989 to 26% (41 of 155 patients) during
19901998 (P=0.021). However,
the case fatality rates in patients aged
80 years were very high,
regardless of study periods: 63% (5 of 8 patients) during 19801989
and 79% (26 of 33 patients) during 19901998
(P=0.981). During the total
study period during 19801998, 37% (133) of 358 patients with
aneurysmal SAH died within 3 months. The average annual age-
and sex-adjusted mortality rates were 9 (95% CI, 7 to 11) per 100 000
population for all ages during 19801989 and 8 (95% CI, 6 to 10)
during 19901998
(Table 5
).
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Risk Factors
Table 6
shows risk factors of patients with
aneurysmal SAH. In both study periods, approximately half of
the patients had a history of hypertension. The rates of cigarette
smoking and daily alcohol intake were significantly higher in men than
in women in both study periods. When the 2 study periods were compared,
cigarette smoking in men was much less during 19901998 than during
19801989 because of a decreasing trend in the proportion of men
smoking. However, there were no significant differences between the 2
study periods in the other risk factors, regardless of sex. The average
serum total cholesterol levels were 183±41 mg/dL (132
patients) during 19801989, 192±41 mg/dL (136 patients) during
19901998 (P=0.963), and
188±41 mg/dL (268 patients) for both study periods. The mean BMIs were
22±3 (38 patients) during 19801989, 22±4 (68 patients) during
19901998 (P=0.521), and 22±3
(106 patients) for the total series.
|
In relation to age, there was a tendency for the percentages
of patients with a history of hypertension to be higher in elderly
patients than in younger patients in both men and women. In total,
during 19801998, including both men and women, the rates of patients
with hypertension were 46% (104 of 227 patients) for those aged
69
years and 58% for those aged
70 years (57 of 98 patients)
(P=0.041). In contrast, the
rates of cigarette smoking and drinking were lower in elderly patients
than in younger patients, regardless of sex. In total, during
19801998, the percentages of current smokers were 44% for those aged
69 years (94 of 212 patients) and 12% for those aged
70 years (12
of 98 patients) (P<0.001),
whereas the rates of those drinking daily were 39% (82 of 211
patients) and 15% (15 of 100 patients), respectively
(P<0.001).
| Discussion |
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In this study the results during 19801989 indicate that the incidence rate of aneurysmal SAH increased almost linearly with increasing age and reached the maximum level at the age of 70 to 79 years but declined after the age of 80 years. However, during 19901998, the incidence rate of SAH increased with increasing age, and the highest incidence rate was found in the oldest age group. Furthermore, the highest incidence rates were found in the ninth decade for men and the 10th decade for women; those rates were definitely higher than those reported in other studies. In most published series for geographic regions other than Izumo, the maximum incidence rate was observed during the eighth decade.1 4 7 9 10 11 In such studies there may be no very old residents, and/or some very old patients with SAH might be missed. In Izumo City, the higher annual incidence rate in the elderly seems primarily to be due to not only aging of the residents but also a more thorough and accurate diagnosis policy, even for very old patients. In the past Izumo study during 19871992, the tendency for an increase in the incidence rate of SAH with increasing age was more apparent when the analysis included patients with both proven and possible SAH than when the analysis included only those with proven SAH.3 For patients with possible SAH, most of them were very old, and the death certificates were written by general practitioners in private clinics.3 Therefore, it may be concluded that the age-specific incidence rate of aneurysmal SAH increases with increasing age, and with aging of the population, the maximum age-specific incidence rate of SAH shifts to the very old age group.
In published series for geographic regions other than Izumo,
the annual incidence rates of SAH per 100 000 population solely due to
aneurysmal rupture were reported to be 9 to 16 for all
ages,4 7 9 28 30
28 for the group aged 30 to 88
years,10 and 96 for the
group aged
40 years.8 On
the other hand, the annual incidence rates of so-called primary or
spontaneous SAH, which includes bleeding due to not only
aneurysmal rupture but also arteriovenous malformation and
other diseases, were 2 to 24 per 100 000 for all
ages,* 11 to 19 per l00 000 for the group aged
15
years,18 26 and
16 to 20 per l00000 for the group aged
20
years.35 36 In
our past Izumo studies, the crude annual incidence rates of
aneurysmal SAH per 100 000 population were 21 to 25 for all
ages, 30 to 34 for the group aged 20 to 89 years, and 35 to 39 for the
group aged 30 to 89 years; the age- and sex-adjusted annual incidence
rates per 100000 population were 18 to 23, 27 to 31, and 32 to 37,
respectively.5 6 19
Furthermore, in Izumo City, when patients with possible SAH were
included in the incidence rate calculations, the crude and the age- and
sex-adjusted annual incidence rates per 100000 population rose to 32
and 29, 43 and 39, and 50 and 47,
respectively.3
In this study the crude annual incidence rates of
aneurysmal SAH in Izumo City were higher during 19901998 than
during 19801989. In addition, the crude annual incidence rates of
aneurysmal SAH were lower than the age- and sex-adjusted annual
incidence rates during 19801989, whereas during 19901998 the crude
annual incidences of aneurysmal SAH were higher than the age-
and sex-adjusted annual incidence rates. Izumo City has one of the
highest proportions of elderly residents in Japan, with 11.4% of the
population aged
70 years compared with 9.4% for Japan as a whole in
1995. In addition, whereas the average annual number of SAH patients
aged
69 years was relatively constant (13.1 during 19801989 and
12.4 during 19901998), the average number of SAH patients aged
70
years doubled from 3.9 during 19801989 to 8.4 during 19901998. In
our hospitals, since 1987, even if patients had died by the time of
referral or were moribund at admission, we attempted as much as
possible to perform CT scans to confirm SAH, and we reviewed the death
certificates of all residents who died during 19871998. Thus, aging
of the residents in Izumo City and a recent more thorough and accurate
diagnosis policy, even for elderly patients, may explain why the crude
annual incidence rates of aneurysmal SAH were higher during
19901998 than during 19801989 and why the age-adjusted incidence
rates were lower than the crude annual incidence rates during the
latter period. At any rate, our findings suggest a clearly higher
incidence than those reported in other series, and the annual incidence
rate of aneurysmal SAH observed in Izumo City appears to be the
highest among those reported to date.
Regarding the annual incidence rate of SAH by sex,
some published studies have reported a higher annual incidence rate in
men,17 19 34 36
whereas others have indicated a higher incidence rate in
women.
Among previous studies that calculated the incidence rate of SAH in
relation to both age and sex, some reported a higher incidence rate in
women than in men for patients older than 60 to 70
years,1 3 5 6 10 21 25 28
whereas in other series no consistent trend toward any sex
difference was observed after stratification by
age.11 19 In our
previous Izumo studies, there was no relationship between the
age-specific incidence rate of SAH and sex during
19801984.19 However,
during 19871992, SAH in patients aged <60 years occurred more often
in men than in women, whereas women aged
60 years were affected more
often.3 5 6
In both periods of this study, the age-specific average annual
incidence rates were higher in men than in women in younger age groups,
whereas they were higher in women than in men in older age groups. The
explanation for this sex-related difference is still unknown but is
probably related to hormonal factors. Further inquiries into the
reversal of the incidence rates that was observed in the sixth to the
eighth decades are indicated.
According to published epidemiological studies other than
Izumo, 8% to 15% of patients with SAH died before receiving medical
attention,7 9 18 23 28
and overall case fatality rates were 20% to 37% within 48
hours,1 11 22 23
31% to 43% in the first
week,8 22 23 28 34
33% to 61% at 1
month,
and 33% to 77% at 1
year.8 13 23 25 31 34
These results generally seem to represent the natural course of
the condition because surgery was seldom performed. In patients with
SAH, aging is a well-known factor associated with poor
outcome.3 4 5 10 12 38 39 40 41 42
Regarding the effect of sex on prognosis after SAH, while some
community- and hospital-based series suggested that prognosis was
different between men and women, most community-based studies have
demonstrated no relationship between sex and
outcome.
Thus far, several epidemiological studies have investigated whether
management outcome for patients with aneurysmal SAH has
improved.4 7 9 13 14 16 18
In some studies, a decreasing trend in the case fatality rate for
patients with SAH was demonstrated, whereas in most series, outcome for
SAH patients was improved only marginally or essentially
unchanged.4 7 9 13 14 16 18
In our previous Izumo studies, 7% to 8% of patients with
aneurysmal SAH died before receiving medical attention or
suffered cardiorespiratory arrest on
arrival,5 12 and
overall case fatality rates were 27% to 33% in the first
week,5 12 40
34% to 40% at 1
month,5 12 40
41% to 46% at 1
year,5 40 46
38% at 2 years,12 and 46%
to 50% at 5
years.5 40 In
addition, in Izumo City, when patients with both proven and possible
SAH were included, overall case fatality rates rose to 43% in the
first week, 53% at 1 month, 55% at 1 year, and 58% at 5
years.3 In this city, while
there was a tendency toward a better surgical outcome in SAH patients
between 19801986 and 19871992, the probability of overall survival
did not improve
significantly.5
It is considered natural that the case fatality rate should
be elevated among elderly patients with SAH. In this study there were
no big differences among patients aged
59 years, 60 to 69 years, and
70 to 79 years in the 3-month case fatality rates after SAH. However,
there was a definite difference between patients aged
79 years and
those aged
80 years, especially in the later period. The 3-month case
fatality rate in men and women was similar in both study periods. In
the comparison of the 2 study periods by age, there was a trend toward
better outcomes in the later period in patients aged
79 years. In our
previous Izumo studies, clinical grades on admission were rather higher
in recent years than those in earlier periods, and the number of
patients who died before admission or suffered cardiorespiratory arrest
on arrival was
higher.5 12 40
However, during 19911996 in this city, the survival rate for patients
with SAH who underwent aneurysm clipping improved to 100% at 1
month and 97% at 2 years.12
Thus, one of the possible reasons for a substantial decrease in the
3-month case fatality in patients aged
79 years was the improvement
in surgical results. In fact,
Inagawa38 39
reported that the recent surgical outcome for patients aged 70 to 79
years is not necessarily poor, even with early surgery. On the other
hand, despite the improvement in the outcome for patients aged
79
years, the case fatality rates in those aged
80 years were very high,
regardless of the study period. Furthermore, during 19801989, the
proportion of patients aged
80 years was only 5%, whereas during
19901998 the rate increased to 18%. Consequently, in the
analysis of the case fatality rates for patients with SAH,
including those aged
80 years, the results in the 2 study periods
became almost similar: the average annual age- and sex-adjusted
mortality rates were 9 per 100 000 population for all ages during
19801989 and 8 during 19901998. Therefore, it may be concluded that
there was little improvement in the 3-month case fatality rate for all
patients between 19801989 and 19901998, mainly because improvements
were counterbalanced by increasing numbers of very elderly patients. In
total, during 19801998, 37% of patients with aneurysmal SAH
died within 3 months.
Hypertension,6 47 48 49 50 51 cigarette smoking,6 47 48 50 52 53 54 55 56 57 58 59 60 and alcohol consumption6 50 55 57 61 have been studied as independent risk factors for SAH. The risk of SAH was especially high among lean hypertensive subjects and lean smoking subjects, that is, BMI was inversely associated with the risk of SAH.48 The relation between serum total cholesterol and stroke risk is still not clear. In several studies, serum total cholesterol level has been positively related to nonhemorrhagic stroke and inversely associated with hemorrhagic stroke, including both SAH and intracerebral hemorrhage.56 62 63 64 However, a consistent relationship between serum total cholesterol and SAH has not been found.48 50 63 64 Diabetes is a well-known risk factor for ischemic cerebral infarction through hypertension and atherosclerosis, and recent studies have shown that diabetes may carry a real risk of intracerebral hemorrhage.6 65 However, it is uncertain whether the prevalence of diabetes in patients with SAH is higher than in the general population.6 48 66 In this study the percentages of male patients with SAH who had a smoking or drinking habit were a little higher than in those of the general Japanese population, and the rate of smoking in male patients seems to be markedly higher than those in other developed countries. However, the rates of smoking and drinking in female patients seem to be less than those in not only the Japanese general population but also other developed countries. With respect to other risk factors, the percentages of patients with SAH who had a history of hypertension or diabetes mellitus were comparable to those of the Japanese general population, and the values of serum total cholesterol and BMI were not different from those in the Japanese general population. In addition, the prevalence of risk factors was not higher during 19901998 compared with that during 19801989. Therefore, in this study we were not able to confirm the consistent relationship between these risk factors and aneurysmal SAH, and the high incidence rate of SAH in this city, especially in female subjects, and recent improvement of outcome could not be elucidated by risk factors adequately.
It seems likely that in the near future we will encounter an
increasing number of very elderly patients with aneurysmal SAH,
some of whom may be aged
100 years. The question of what should be
done for such very elderly patients will be a matter of
concern.
| Footnotes |
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2 References 1 3 5 6 8 10 21 23 27 28 37 . ![]()
3 References 7 8 10 13 18 21 22 23 24 26 31 34 . ![]()
4 References 4 11 13 15 16 22 29 43 44 45 . ![]()
Received October 4, 2000; revision received January 15, 2001; accepted February 19, 2001.
| References |
|---|
|
|
|---|
2. Harmsen P, Berglund G, Larsson O, Tibblin G, Wilhelmsen L. Stroke registration in Göteborg, Sweden, 197075: incidence and fatality rates. Acta Med Scand. 1979;206:337344.[Medline] [Order article via Infotrieve]
3. Inagawa T. What are the actual incidence and mortality rates of subarachnoid hemorrhage? Surg Neurol. 1997;47:4753.[Medline] [Order article via Infotrieve]
4. Inagawa T. Incidence, fatality and mortality rates of subarachnoid hemorrhage [in Japanese]. Neurol Med (Tokyo). 1997;46:545555.
5.
Inagawa T, Tokuda
Y, Ohbayashi N, Takaya M, Moritake K. Study of aneurysmal
subarachnoid hemorrhage in Izumo City, Japan.
Stroke. 1995;26:761766.
6. Inagawa T, Takechi A, Yahara K, Saito J, Moritake K, Kobayashi S, Fujii Y, Sugimura C. Primary intracerebral and aneurysmal subarachnoid hemorrhage in Izumo City, Japan, part I: incidence and seasonal and diurnal variations. J Neurosurg. 2000;93:958966.[Medline] [Order article via Infotrieve]
7.
Ingall TJ, Whisnant
JP, Wiebers DO, OFallon W. Has there been a decline in
subarachnoid hemorrhage mortality?
Stroke. 1989;20:718724.
8.
Kiyohara Y, Ueda K,
Hasuo Y, Wada J, Kawano H, Kato I, Sinkawa A, Ohmura T, Iwamoto H, Omae
T, Fujishima M. Incidence and prognosis of subarachnoid
hemorrhage in a Japanese rural community.
Stroke. 1989;20:11501155.
9.
Phillips LH II,
Whisnant JP, OFallon WM, Sundt TM Jr. The unchanging pattern of
subarachnoid hemorrhage in a community.
Neurology. 1980;30:10341040.
10.
Sacco RL, Wolf
PA, Bharucha NE, Meeks SL, Kannel WB, Charette LJ, McNamara PM, Palmer
EP, DAgostino R. Subarachnoid and
intracerebral hemorrhage: natural history,
prognosis, and precursive factors in the Framingham Study.
Neurology. 1984;34:847854.
11.
Sarti C,
Tuomilehto J, Salomaa V, Sivenius J, Kaarsalo E, Narva EV, Salmi K,
Torppa J. Epidemiology of subarachnoid
hemorrhage in Finland from 1983 to 1985.
Stroke. 1991;22:848853.
12. Inagawa T, Shibukawa M, Inokuchi F, Tokuda Y, Okada Y, Okada K. Primary intracerebral and aneurysmal subarachnoid hemorrhage in Izumo City, Japan, part II: management and surgical outcome. J Neurosurg. 2000;93:967975.[Medline] [Order article via Infotrieve]
13. Brown RD Jr, Whisnant JP, Sicks JD, OFallon WM, Wiebers DO. Stroke incidence, prevalence, and survival secular trends in Rochester, Minnesota, through 1989. Stroke. 1996;27:373380.
14.
Fogelholm R,
Hernesniemi J, Vapalahti M. Impact of early surgery on outcome after
aneurysmal subarachnoid hemorrhage: a
population-based study. Stroke. 1993;24:16491654.
15.
Harmsen P,
Tsipogianni A, Wilhelmsen L. Stroke incidence rates were unchanged,
while fatality rates declined, during 19711987 in Göteborg, Sweden.
Stroke. 1992;23:14101415.
16.
Immonen-Räihä
P, Mähönen M, Tuomilehto J, Salomaa V, Kaarsalo E, Narva EV, Salmi
K, Sarti C, Sivenius J, Alhainen K, Torppa J. Trends in case-fatality
of stroke in Finland during 1983 to 1992.
Stroke. 1997;28:24932499.
17.
Terént A.
Increasing incidence of stroke among Swedish women.
Stroke. 1988;19:598603.
18.
Truelsen T,
Bonita R, Duncan J, Anderson NE, Mee E. Changes in subarachnoid
hemorrhage mortality, incidence, and case fatality in New
Zealand between 19811983 and 19911993.
Stroke. 1998;29:22982303.
19.
Inagawa T,
Ishikawa S, Aoki H, Takahashi M, Yoshimoto H. Aneurysmal
subarachnoid hemorrhage in Izumo City and Shimane
prefecture of Japan: incidence.
Stroke. 1988;19:170175.
20. Schoenberg BS. Calculating confidence intervals for rates and ratios: simplified method utilizing tabular values based on the Poisson distribution. Neuroepidemiology. 1983;2:257265.
21. Anderson CS, Jamrozik KD, Burvill PW, Chakera TMH, Johnson GA, Stewart-Wynne EG. Determining the incidence of different subtypes of stroke: results from the Perth Community Stroke Study, 19891990. Med J Aust. 1993;158:8589.[Medline] [Order article via Infotrieve]
22.
Bonita R,
Beaglehole R, North JDK. Subarachnoid hemorrhage in New
Zealand: an epidemiological study.
Stroke. 1983;14:342347.
23.
Bonita R, Thomson
S. Subarachnoid hemorrhage:
epidemiology, diagnosis, management, and
outcome. Stroke. 1985;16:591594.
24. Broderick JP, Brott T, Tomsick T, Miller R, Huster G. Intracerebral hemorrhage more than twice as common as subarachnoid hemorrhage. J Neurosurg. 1993;78:188191.[Medline] [Order article via Infotrieve]
25.
Carolei A, Marini
C, Di Napoli M, Di Gianfilippo G, Santalucia P, Baldassarre M, De
Matteis G, Di Orio F. High stroke incidence in the prospective
community-based LAquila registry (19941998): first years results.
Stroke. 1997;28:25002506.
26.
Ellekjær H,
Holmen J, Indredavik B, Terent A. Epidemiology
of stroke in Innherred, Norway, 1994 to 1996: incidence and 30-day
case-fatality rate. Stroke. 1997;28:21802184.
27.
Jerntorp P,
Berglund G. Stroke registry in Malmö, Sweden.
Stroke. 1992;23:357361.
28. Pakarinen S. Incidence, aetiology, and prognosis of primary subarachnoid haemorrhage: a study based on 589 cases diagnosed in a defined urban population during a defined period. Acta Neurol Scand. 1967;43(suppl 29):1128.
29.
Fogelholm R.
Subarachnoid hemorrhage in middle Finland: incidence,
early prognosis and indications for neurosurgical treatment.
Stroke. 1981;12:296301.
30. Kristensen MØ. Increased incidence of bleeding intracranial aneurysms in Greenlandic Eskimos. Acta Neurochir (Wien). 1983;67:3743.[Medline] [Order article via Infotrieve]
31.
Bamford J,
Sandercock P, Dennis M, Burn J, Warlow C. A prospective study of acute
cerebrovascular disease in the community: the Oxfordshire Community
Stroke Project, 198186, II: incidence, case fatality rates and
overall outcome at one year of cerebral infarction, primary
intracerebral and subarachnoid
haemorrhage. J Neurol
Neurosurg Psychiatry. 1990;53:1622.
32.
Giroud M, Milan
C, Beuriat P, Gras P, Essayagh E, Arveux P, Dumas R. Incidence and
survival rates during a two-year period of
intracerebral and subarachnoid
haemorrhages, cortical infarcts, lacunes and transient
ischaemic attacks: the stroke registry of Dijon: 19851989.
Int J Epidemiol. 1991;20:892899.
33.
Herman B, Leyten
ACM, van Luijk JH, Frenken CWGM, op de Coul AAW, Schulte BPM.
Epidemiology of stroke in Tilburg, the
Netherlands: the population-based stroke incidence register, 2:
incidence, initial clinical picture and medical care, and three week
case fatality. Stroke. 1982;13:629634.
34.
Sivenius J,
Heinonen OP, Pyörälä K, Salonen J, Riekkinen P. The incidence of
stroke in the Kuopio area of east Finland.
Stroke. 1985;16:188192.
35.
Gross CR, Kase
CS, Mohr JP, Cunningham SC, Baker WE. Stroke in south Alabama:
incidence and diagnostic features-a population based study.
Stroke. 1984;15:249255.
36.
Tanaka H, Ueda Y,
Date C, Baba T, Yamashita H, Hayashi M, Shoji H, Owada K, Baba KI,
Shibuya M, Kon T, Detels R. Incidence of stroke in Shibata, Japan:
19761978. Stroke. 1981;12:460466.
37.
Jamrozik K,
Broadhurst RJ, Lai N, Hankey GJ, Burvill PW, Anderson CS. Trends in the
incidence, severity, and short-term outcome of stroke in Perth, Western
Australia. Stroke. 1999;30:21052111.
38. Inagawa T. Management outcome in the elderly patient following subarachnoid hemorrhage. J Neurosurg. 1993;78:554561.[Medline] [Order article via Infotrieve]
39. Inagawa T. Dissection from fundus to neck for ruptured anterior and middle cerebral artery aneurysms at the acute stage. Acta Neurochir (Wien). 1999;141:563570.[Medline] [Order article via Infotrieve]
40.
Inagawa T,
Takahashi M, Aoki H, Ishikawa S, Yoshimoto H. Aneurysmal
subarachnoid hemorrhage in Izumo City and Shimane
prefecture of Japan: outcome.
Stroke. 1988;19:176180.
41. Inagawa T, Yamamoto M, Kamiya K, Ogasawara H. Management of elderly patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 1988;69:332339.[Medline] [Order article via Infotrieve]
42.
Yamashita K,
Kashiwagi S, Kato S, Takasago T, Ito H. Cerebral aneurysms in
the elderly in Yamaguchi, Japan: analysis of the Yamaguchi data
bank of cerebral aneurysm from 1985 to 1995.
Stroke. 1997;28:19261931.
43.
Ingall TJ,
Asplund K, Mähönen M, Bonita R. A multiple comparison of
subarachnoid hemorrhage:
epidemiology in the WHO MONICA stroke study.
Stroke. 2000;31:10541061.
44. Kongable GL, Lanzino G, Germanson TP, Truskowski LL, Alves WM, Torner JC, Kassell NF. Gender-related differences in aneurysmal subarachnoid hemorrhage. J Neurosurg. 1996;84:4348.[Medline] [Order article via Infotrieve]
45. Rosenørn J, Eskesen V, Schmidt K. Clinical features and outcome in females and males with ruptured intracranial saccular aneurysms. Br J Neurosurg. 1993;7:287290.[Medline] [Order article via Infotrieve]
46. Inagawa T, Yoshimoto H, Aoki H, Ishikawa S, Takahashi M. The incidence and outcome of aneurysmal subarachnoid hemorrhage in relation to the size of the geographic area [in Japanese]. Jpn J Stroke. 1988;10:334339.
47.
Bonita R.
Cigarette smoking, hypertension and the risk of subarachnoid
hemorrhage: a population-based case-control study.
Stroke. 1986;17:831835.
48. Knekt P, Reunanen A, Aho K, Heliövaara M, Rissanen A, Aromaa A, Impivaara O. Risk factors for subarachnoid hemorrhage in a longitudinal population study. J Clin Epidemiol. 1991;44:933939.[Medline] [Order article via Infotrieve]
49. Taylor CL, Yuan Z, Selman WR, Ratcheson RA, Rimm AA. Cerebral arterial aneurysm formation and rupture in 20,767 elderly patients: hypertension and other risk factors. J Neurosurg. 1995;83:812819.[Medline] [Order article via Infotrieve]
50.
Teunissen LL,
Rinkel GJE, Algra A, van Gijn J. Risk factors for subarachnoid
hemorrhage: a systematic review.
Stroke. 1996;27:544549.
51. Toftdahl DB, Torp-Pedersen C, Engel UH, Strandgaard S, Jespersen B. Hypertension and left ventricular hypertrophy in patients with spontaneous subarachnoid hemorrhage. Neurosurgery. 1995;37:235240.[Medline] [Order article via Infotrieve]
52. Adamson J, Humphries SE, Ostergaard JR, Voldby B, Richards P, Powell JT. Are cerebral aneurysms atherosclerotic? Stroke. 1994;25:963966.[Abstract]
53. Bell BA, Symon L. Smoking and subarachnoid hemorrhage. BMJ. 1979;1:577578.
54. Colditz GA, Bonita R, Stampfer MJ, Willett WC, Rosner B, Speizer FE, Hennekens CH. Cigarette smoking and risk of stroke in middle-aged women. N Engl J Med. 1988;318:937941.[Abstract]
55.
Juvela S, Hillbom
M, Numminen H, Koskinen P. Cigarette smoking and alcohol consumption as
risk factors for aneurysmal subarachnoid
hemorrhage. Stroke. 1993;24:639646.
56.
Leppala JM,
Virtamo J, Fogelholm R, Albanes D, Heinonen OP. Different risk factors
for different stroke subtypes: association of blood pressure,
cholesterol, and antioxidants.
Stroke. 1999;30:25352540.
57.
Longstreth WT Jr,
Nelson LM, Koepsell TD, van Belle G. Cigarette smoking, alcohol use,
and subarachnoid hemorrhage.
Stroke. 1992;23:12421249.
58. Qureshi AI, Sung GY, Suri MFK, Straw RN, Guterman LR, Hopkins LN. Factors associated with aneurysm size in patients with subarachnoid hemorrhage: effect of smoking and aneurysm location. Neurosurgery. 2000;46:4450.[Medline] [Order article via Infotrieve]
59. Shinton R, Beevers G. Meta-analysis of relation between cigarette smoking and stroke. BMJ. 1989;298:789794.
60. Weir BKA, Kongable GL, Kassell NF, Schultz JR, Truskowski LL, Sigrest A. Cigarette smoking as a cause of aneurysmal subarachnoid hemorrhage and risk for vasospasm: a report of the Cooperative Aneurysm Study. J Neurosurg. 1998;89:405411.[Medline] [Order article via Infotrieve]
61.
Leppala JM,
Paunio M, Virtamo J, Fogelholm R, Albanes D, Taylor PR, Heinonen OP.
Alcohol consumption and stroke incidence in male smokers.
Circulation. 1999;100:12091214.
62. Gatchev O, Rastam L, Lindberg G, Gullberg B, Eklund GA, Isacsson SO. Subarachnoid hemorrhage, cerebral hemorrhage, and serum cholesterol concentration in men and women. Ann Epidemiol. 1993;3:403409.[Medline] [Order article via Infotrieve]
63. Neaton JD, Wentworth DN, Cutler J, Stamler J, Kuller L. Risk factors for death from different types of stroke. Ann Epidemiol. 1993;3:493499.[Medline] [Order article via Infotrieve]
64.
Yano K, Reed DM,
MacLean CJ. Serum cholesterol and hemorrhagic stroke in the
Honolulu Heart Program. Stroke. 1989;20:14601465.
65.
Juvela S.
Prevalence of risk factors in spontaneous intracerebral
hemorrhage and aneurysmal subarachnoid
hemorrhage. Arch
Neurol. 1996;53:734740.
66.
Adams HP Jr,
Putman SF, Kassell NF, Torner JC. Prevalence of diabetes mellitus among
patients with subarachnoid hemorrhage.
Arch Neurol. 1984;41:10331035.
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