(Stroke. 1995;26:761-766.)
© 1995 American Heart Association, Inc.
Articles |
Study of Aneurysmal Subarachnoid Hemorrhage in Izumo City, Japan
From the Department of Neurosurgery, Shimane Prefectural Central Hospital (T.I., Y.T., N.O.), and Shimane Medical University Hospital (M.T., K.M.), Izumo City, Japan.
Correspondence to Tetsuji Inagawa, MD, Department of Neurosurgery, Shimane Prefectural Central Hospital, 116 Imaichi-cho, Izumo, Shimane 693, Japan.
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Abstract |
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Background and Purpose Estimation of the actual incidence rate of subarachnoid hemorrhage and evaluation of the treatment require the inclusion of all patients in a defined geographic area.
Methods During 1987 through 1992 in Izumo City, Japan, we estimated the incidence rate of subarachnoid hemorrhage by including dead-on-arrival patients and by further adding the results obtained after reviewing all death certificates registered in this city in the corresponding period. In addition, we compared the management and surgical outcomes in hospitalized patients from 1987 through 1992 with outcomes from 1980 through 1986.
Results During 1987 through 1992, we diagnosed 123 patients as having subarachnoid hemorrhage. The crude and the age- and sex-adjusted incidence rates using the 1990 population statistics for Japan were 25 (95% confidence interval, 21 to 30) per 100 000/y and 23 (95% confidence interval, 19 to 28) per 100 000/y for all ages, respectively; these occurrences are the highest among those reported to date. Of these patients, 8% died before receiving medical attention, 27% in the first week, and 39% at 1 month. The survival curve for 2 years improved significantly from 1980-1986 to 1987-1992 in patients with admission grades 4 and 5 (P=.035) and in operated patients with preoperative grades 1 through 3 (P=.036). However, there was little improvement in the overall management results (P=.168), possibly because patients with high risk and/or old age were admitted and/or diagnosed more often in the latter period.
Conclusions The incidence rate of subarachnoid hemorrhage is much higher than that reported so far in the literature, and despite improvement of management and surgical therapy, the actual case-fatality rate is still high, mainly because of the high mortality rate directly associated with the primary bleeding.
Key Words: cerebral aneurysm • epidemiology • Japan • subarachnoid hemorrhage
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Introduction |
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In 1988, Inagawa et al1 2 reported the incidence and outcome of aneurysmal subarachnoid hemorrhage (SAH) in Izumo City, Japan, during the period 1980 through 1984. The reported incidence, 21/100 000 per year for all age groups in the city, was the highest among all studies published up to that time. However, there is still a possibility that patients who were dead on arrival and who died before being hospitalized or receiving medical attention were not included in the study because the studies were based on hospitalized patients. On the other hand, during the last decade, there have been major changes in the management of aneurysmal SAH. Currently, patients with aneurysmal SAH are admitted more often, regardless of their clinical condition or age, and whenever possible they are examined by computed tomography (CT) even if they are moribund or dead on arrival. In addition, we reviewed all death certificates registered in Izumo City from 1987 through 1992 to analyze the causes of death in patients who died before reaching the hospital. The primary purpose of this study was to ascertain the community incidence or mortality rate of first aneurysmal SAH in Izumo City during 1987 through 1992. Second, by comparing the survival rate of hospitalized patients during 1987 through 1992 with that during 1980 through 1986, we evaluated whether the overall management outcome for patients with aneurysmal SAH has improved.
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Subjects and Methods |
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Izumo City is located in the western part of Japan and covers a rural area of about 175 km.2 There are no large industries, and social and demographic composition is relatively stable. Izumo City has two hospitals with neurosurgical departments: Shimane Prefectural Central Hospital with 665 beds and Shimane Medical University Hospital with 616 beds. Because these hospitals are designated emergency centers, all patients with verified or suspected SAH, even if moribund, are immediately referred to the neurosurgical department of either hospital, irrespective of age or condition. In this study, determination of SAH required confirmation by at least one of three diagnostic procedures: brain CT, autopsy, or surgery. Demonstration of blood in the cerebrospinal fluid after a spinal tap was not used as a diagnostic criterion of SAH because this may occur in other diseases, such as cerebral hemorrhage. We divided the 13 years from 1980 through 1992 into two periods: the 7 years from January 1, 1980, through December 31, 1986, and the 6 years from January 1, 1987, through December 31, 1992. During 1980-1986, we analyzed only hospitalized patients with first SAH who were admitted to the neurosurgical department of either hospital. However, during 1987-1992, we analyzed not only hospitalized patients with first SAH but also those who were dead on arrival or who had not yet received medical attention. In the latter period, even for patients who had died by the time of referral or were moribund at admission, we intended to perform CT scans as much as possible to confirm SAH, and clinical information was collected from relatives. In addition, we reviewed the death certificates of all 3562 residents who died during 1987-1992, and we analyzed those suspected to have died of SAH.
According to the national census of Japan, the population of Izumo City was 80 749 as of October 1, 1985, and 82 679 as of October 1, 1990. The estimates of disease incidence rates during the two study periods were based on the census populations of 1985 and 1990, respectively. The age- and sex-adjusted annual incidence and mortality rates were estimated using the 1990 Japan census population data. Clinical condition was graded according to the scale of Hunt and Hess.3 The degree of SAH on the admission CT scan was graded from 0 to 4.4 The outcome at 2 years after SAH was classified according to the Glasgow Outcome Scale.5 The patients underwent follow-up review by a variety of methods after discharge, including personal consultation, telephone interview, and written correspondence. No patients were lost to follow-up review up to 2 years after the initial SAH.
The confidence intervals (CIs) of the incidence rates were calculated
according to the method of Schoenberg.6 For statistical
analyses, 
2 test, Fisher's exact test, or
Mann-Whitney U test was used. The possibility of survival
was estimated by the Kaplan-Meier product-limit method,7
and the curves of different groups were compared by the log-rank test.
Cox proportional hazards analysis8 was used to
identify variables that predicted 2-year survival for patients during
1980-1992. The variables assessed were age, sex, time from SAH to
admission, clinical grade on admission, SAH grade on initial CT scan,
concomitant hematoma on CT scan, site of ruptured aneurysms, and
rebleeding. Each variable was assessed individually, and those found to
be significant (P<.05) were used for multivariate
analysis.
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Results |
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During the 13-year period from 1980 through 1992, 234 patients were diagnosed as having SAH. All of the 234 patients, including those who were dead on arrival, underwent CT scanning. Of these patients, SAH was verified in 233: by CT scan only in 67 (29%), by CT scan and surgery in 135 (58%), by CT scan and autopsy in 25 (11%), and by CT scan, surgery, and autopsy in 6 (3%). In one patient, although SAH was not detected by CT scan, a ruptured aneurysm was confirmed at surgery. The exact location of the ruptured aneurysm was confirmed by angiography and/or autopsy in 211 patients (90%); 61 of them (29%) had multiple aneurysms. In the remaining 23 patients, aneurysm was not confirmed; however, CT findings of these patients were identical to those suggesting SAH due to ruptured aneurysms. Of these patients, 6 were dead on admission, 10 were not examined or were incompletely examined by angiography because of poor clinical condition and/or very old age, and in 7 aneurysm was not identified by four-vessel cerebral angiography.
During 1980-1986, 105 patients with first SAH were admitted to Shimane Prefectural Central Hospital and 6 to Shimane Medical University Hospital; all of them were hospitalized at neurosurgical departments. On the other hand, during 1987-1992, 114 patients with first SAH were admitted to Shimane Prefectural Central Hospital and 9 to Shimane Medical University Hospital; 113 were hospitalized, and 10 were dead on arrival. Among the patients dead on arrival, 7 were admitted at departments other than neurosurgical departments and were discovered only after their death certificates were reviewed. We reviewed the charts of these 7 patients for clinical details and autopsy findings, and if available, we checked their CT scans again. As a result, we were able to make a final diagnosis of SAH.
The percentage of elderly patients aged over 70 years was significantly
higher during 1987-1992 (33%) than during 1980-1986 (19%)
(P=.009) (Table 1
). During 1987-1992, the
age-specific average annual incidence rate of first SAH increased with
increasing age, and the highest incidence rate was found in the decade
of oldest age (Table 2). The average annual incidence
rates of first SAH per 100 000 population during 1987-1992 are shown
in Table 3. When the incidence rates based on
hospitalized patients during 1980-1986 were calculated, both the crude
and the age- and sex-adjusted annual incidence rates were 20 (95% CI,
17 to 24) per 100 000 population for all ages.
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In the first analysis of single variables for 234 SAH patients during 1980 through 1992, eight variables appeared to influence survival rates independently: patient age (70 years or older), timing of admission (within 6 hours or dead on arrival), clinical grade on admission (grades 4 and 5 or dead on arrival), concomitant hematoma on CT scans (intracerebral hematoma, ventricular hemorrhage, or subdural hematoma), SAH grade on CT scan (grades 3 and 4), rebleeding, anterior cerebral artery aneurysms, and middle cerebral artery aneurysms. When these variables were used to develop a Cox multivariate regression analysis, the most important predictors of survival in order of decreasing reliability were clinical grade on admission (risk ratio [RR], 3.64; 95% CI, 2.08 to 6.44; P<.0001), rebleeding (RR, 3.41; 95% CI, 2.02 to 5.74; P<.0001), SAH grade (RR, 2.96; 95% CI, 1.62 to 5.73; P=.0003), and middle cerebral artery aneurysms (RR, 0.48; 95% CI, 0.25 to 0.90; P=.0210). However, the other variables dropped below the level of significance.
When comparing the two study periods, 78 (70%) of 111 patients during 1980-1986 were admitted within 6 hours after initial SAH, whereas during 1987-1992, 10 (8%) of 123 patients were dead on admission, and 85 (69%) were admitted within 6 hours (P=.480). Of the 111 patients admitted during 1980-1986, 48 (43%) were clinical grade 1 or 2, 29 (26%) were grade 3, 13 (12%) were grade 4, and 21 (19%) were grade 5; of the 113 patients admitted during 1987-1992, 50 (44%) were clinical grade 1 or 2, 21 (19%) were grade 3, 14 (12%) were grade 4, and 28 (25%) were grade 5 (P=.169). During 1980-1986, 33 of 111 patients had rebleeding (9 before and 24 after admission), whereas during 1987-1992, 29 of 113 hospitalized patients had rebleeding (7 before and 22 after admission) (P=.297). There were no significant differences between the two study periods in the SAH grades or the rate of concomitant hematoma on CT scans and the sites of ruptured aneurysms.
When comparing the survival curves in hospitalized patients, excluding 10 dead-on-arrival cases, the survival rates at 2 years during 1980-1986 were 53% for overall management patients, 70% for those with admission grades 1 through 3, 15% for those with admission grades 4 and 5, 58% for those aged 69 years or younger, and 29% for those aged 70 to 79 years, whereas these rates during 1987-1992 were 62% (P=.168), 83% (P=.082), 26% (P=.035), 72% (P=.063), and 60% (P=.053), respectively.
Fig 1 illustrates the survival curves of the management
patients with first SAH during 1987-1992, including not only
hospitalized patients but also those who were dead on arrival. Of the
123 patients, 11% (13) were dead on day 0 (defined as the day of
hemorrhage), 23% (28) by day 3, 27% (33) by day 7, 39% (48) within 1
month, and 39% (48) within 6 months. The causes of death within 1 or 6
months were poor condition or death before arrival (33 cases),
rebleeding (8 cases), vasospasm (6 cases), and medical complication (1
case). In this period, both the age- and sex-adjusted 30-day and
6-month mortality rates were 10 (95% CI, 7 to 13) per 100 000
population for all ages, 13 (95% CI, 9 to 17) per 100 000 population
for the 20-to-89-year age group, and 15 (95% CI, 11 to 20) per
100 000 population for the 30-to-89-year age group. The percentages of
favorable outcome including good recovery or moderate disability at 2
years after SAH were 61% (45 cases) for patients aged 69 years or
younger and 39% (11 cases) for those aged 70 to 79 years
(P=.042); however, there was no significant difference in
the survival curves between these groups (P=.519).
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69 years
vs 70 to 79 years (P=.5191);
Fig 2 shows the operation rate for hospitalized patients
with SAH, excluding dead-on-arrival cases. During 1980-1986, the age
distribution resembled a bell curve, and the operation rate decreased
after 70 years of age. However, during 1987-1992, the pattern shifted
so that the numbers of patients in their fifties, sixties, and
seventies were almost equal, and there was no significant difference in
the operation rate among the three age groups under 80 years.
Ultimately, 64% (71 patients) during 1980-1986 and 63% (71) during
1987-1992 underwent surgery (P=.485); of these, 72% (51)
during 1980-1986 and 77% (55) during 1987-1992 did so by day 3
(P=.281). When comparing the survival curves in patients who
were surgically treated, the survival rates at 2 years during 1980-1986
were 79% for all patients, 85% for those with preoperative grades 1
through 3, 40% for those with preoperative grades 4 and 5, 81% for
those aged 69 years or younger, and 57% for those aged 70 to 79 years,
whereas these rates during 1987-1992 were 90% (P=.069),
97% (P=.036), 58% (P=.310), 92%
(P=.091), and 83% (P=.137), respectively (Fig 3). In hospitalized patients, the most important reason
for nonoperation was poor patient condition, and the ultimate outcome
of these patients was very poor regardless of the study period. During
1980-1986, 93% (37 of 40) of patients who did not undergo surgery died
within 6 months after SAH, whereas during 1987-1992, 81% (34 of 42) of
patients died within 6 months (P=.112).
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Discussion |
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To study the incidence or mortality rate of SAH, we should take into account the following points. If we study a large geographic region, a number of SAH patients, especially those in the outlying areas, may never reach the hospital and die before receiving medical attention.1 2 9 10 In hospital-based studies, we may miss patients who die before being hospitalized or receiving medical attention.11 12 13 14 In contrast, in community-based studies, if populations are too small to allow accurate incidence rates, it is difficult to assess the current management or surgical outcome.2 Accurate diagnosis of SAH is another very important factor for this kind of study. At present, CT and/or autopsy are essential for definite diagnosis of SAH because clinical symptoms and/or spinal tap alone are not sufficient.1 2 15 Finally, the denominators for calculating annual incidence rate vary, with some studies covering the population of all ages, while other studies are confined to certain age groups.1
In this community-based study during 1987-1992, the crude and the
age- and sex-adjusted annual incidence rates of SAH due to aneurysm or
presumed aneurysm are highest among those reported to date. Izumo City
has one of the highest proportions of elderly residents in Japan. This
may be why the age- and sex-adjusted incidence rates for this study
were lower than the crude annual incidence rates: the incidence rate of
SAH increased with age. In published studies, the annual incidence
rates of SAH due solely to aneurysmal rupture were reported to be 6 to
21 per 100 000 for all ages,1 11 12 15 16 17 28 per 100 000
for the 30-to-88-year age group,18 and 96 per 100 000 for
the 
40-year age group13 ; 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.12 16 17 19 20 21 22 23 24 25 26 27 28 Table 4 shows the
published annual incidence rates of SAH in the contemporary CT era. On
the other hand, when calculating the incidence rates based on hospital
data during 1980-1986, both the crude and the age- and sex-adjusted
annual incidence rates of SAH decreased to 20 (95% CI, 17 to 24) per
100 000 population. In the study during 1987-1992, we diagnosed 10
patients who were dead on arrival as having had SAH, and after
reviewing death certificates, we found 7 other patients with SAH.
Therefore, if we had missed these 17 patients, the crude annual
incidence rate of SAH for all ages would have been estimated as 21
(95% CI, 18 to 26) per 100 000 population. This rate is similar to
that for 1980-1986 in this study and the same as the rate of 21 per
100 000 population for 1980-1984,1 both of which were
based on hospital data. The difference between the two study periods
seems to have resulted from a more thorough and accurate diagnosis
policy during 1987-1992 than was used during 1980-1986.
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With regard to sex difference by age, in patients older than 60 years, SAH occurred predominantly in women, whereas in those younger than 60 years, there was a preponderance of men. In published studies, it has been reported that the incidence rate of SAH is higher in women older than 70 years.17 18 19 22 The reason for this inversion at age 60 or 70 years in the incidence rate of SAH is unclear, and further study is necessary.
The most important predictor of survival was clinical grade on admission, followed by incidence of rebleeding and SAH grade. It has been well established that management outcome depends on patient grading,2 12 34 incidence of rebleeding,35 patient age,2 34 36 and timing of admission,34 37 associated with survival of patients with ruptured aneurysms. Age and timing of admission were not significant predictors of outcome probably because there is a close correlation between these variables and clinical grade.34 36
In this study, although the actual overall outcome during 1987-1992 is still disappointing, the results may be more favorable than those in published epidemiological studies, especially those in elderly patients. This is probably due to the more aggressive surgical and management policy adopted in this city. According to epidemiological studies, 8% to 15% of patients with SAH died before receiving medical attention,11 12 14 and the overall case-fatality rate was 35% within 8 hours after onset of SAH,13 20% to 37% within 48 hours,14 19 38 39% to 43% in the first week,13 14 38 and 46% to 61% at 1 month.13 15 18 20 29 38 These results seem to represent largely the natural course after SAH because surgery was seldom performed.
Although the overall survival probability did not improve significantly from 1980-1986 to 1987-1992, the analysis of hospitalized patients with SAH (excluding dead-on-arrival cases) shows a tendency toward better outcome among high-risk patients, elderly patients aged 70 to 79 years, and low-risk patients who were surgically treated. Improvement of outcome in high-risk patients may be due to improvement in management rather than in surgical practice, since the number of high-risk patients who were surgically treated was still small, and the improvement of surgical results did not reach statistical significance. In hospitalized patients, whether patients are eligible for surgery is one of the most important factors for outcome. In elderly patients, the increase in the operation rate might contribute to the improvement of management outcome. In this study, there was no significant difference in the timing of operation between the two study periods. Therefore, improvement of surgical results in low-risk patients may be due to other factors, such as management techniques before, during, and/or after surgery. So far, there have been few epidemiological studies that have investigated whether management outcome for patients with aneurysmal SAH has improved.11 12 23 Ingall et al11 in their study in Rochester, Minnesota, from 1975 through 1984 showed a decreasing trend in the case-fatality rate for SAH patients, which was probably related to changes in management. Fogelholm et al23 in their study in central Finland reported that survival after SAH in the 1980s improved only marginally compared with that in the 1970s, while the quality of life for the survivors was better in the later period. In any event, despite the improvement in both contemporary medical and surgical therapy and in a more active treatment policy for elderly patients, there has been little improvement in the overall management results. This is probably because improvements were counterbalanced by increasing numbers of hospitalized patients with high risk and/or old age, resulting from a more aggressive policy for SAH treatment.
Received October 4, 1994; revision received January 27, 1995; accepted January 27, 1995.
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T. Mannami, H. Iso, S. Baba, S. Sasaki, K. Okada, M. Konishi, S. Tsugane, and for the Japan Public Health Center-Based Prospecti Cigarette Smoking and Risk of Stroke and its Subtypes Among Middle-Aged Japanese Men and Women: The JPHC Study Cohort I Stroke, June 1, 2004; 35(6): 1248 - 1253. [Abstract] [Full Text] [PDF]
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T. Yoneyama, H. Kasuya, H. Onda, H. Akagawa, K. Hashiguchi, T. Nakajima, T. Hori, and I. Inoue Collagen Type I {alpha}2 (COL1A2) Is the Susceptible Gene for Intracranial Aneurysms Stroke, February 1, 2004; 35(2): 443 - 448. [Abstract] [Full Text] [PDF]
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H. Onda, H. Kasuya, T. Yoneyama, T. Hori, T. Nakajima, and I. Inoue Endoglin Is Not a Major Susceptibility Gene for Intracranial Aneurysm Among Japanese Stroke, July 1, 2003; 34(7): 1640 - 1644. [Abstract] [Full Text] [PDF]
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 T. Vogel, R. Verreault, J.-F. Turcotte, M. Kiesmann, and M. Berthel Review Article. Intracerebral Aneurysms: A Review With Special Attention to Geriatric Aspects J. Gerontol. A Biol. Sci. Med. Sci., June 1, 2003; 58(6): M520 - 524. [Abstract] [Full Text] [PDF]
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H. Ohkuma, H. Tabata, S. Suzuki, and M. S. Islam Risk Factors for Aneurysmal Subarachnoid Hemorrhage in Aomori, Japan Stroke, January 1, 2003; 34(1): 96 - 100. [Abstract] [Full Text] [PDF]
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H. Ohkuma, S. Fujita, and S. Suzuki Incidence of Aneurysmal Subarachnoid Hemorrhage in Shimokita, Japan, From 1989 to 1998 Stroke, January 1, 2002; 33(1): 195 - 199. [Abstract] [Full Text] [PDF]
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D. Krex, A. Ziegler, H. K. Schackert, and G. Schackert Lack of Association Between Endoglin Intron 7 Insertion Polymorphism and Intracranial Aneurysms in a White Population: Evidence of Racial/Ethnic Differences Stroke, November 1, 2001; 32(11): 2689 - 2694. [Abstract] [Full Text] [PDF]
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T. Inagawa Trends in Incidence and Case Fatality Rates of Aneurysmal Subarachnoid Hemorrhage in Izumo City, Japan, Between 1980-1989 and 1990-1998 Stroke, July 1, 2001; 32(7): 1499 - 1507. [Abstract] [Full Text] [PDF]
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 R. P. Kivisaari, O. Salonen, A. Servo, T. Autti, J. Hernesniemi, and J. Ohman MR Imaging After Aneurysmal Subarachnoid Hemorrhage and Surgery: A Long-term Follow-up Study AJNR Am. J. Neuroradiol., June 1, 2001; 22(6): 1143 - 1148. [Abstract] [Full Text] [PDF]
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T. Niskakangas, J. Ohman, M. Niemela, E. Ilveskoski, T. A. Kunnas, and P. J. Karhunen Association of Apolipoprotein E Polymorphism With Outcome After Aneurysmal Subarachnoid Hemorrhage : A Preliminary Study Stroke, May 1, 2001; 32(5): 1181 - 1184. [Abstract] [Full Text] [PDF]
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 M. L. Hackett and C. S. Anderson Health outcomes 1 year after subarachnoid hemorrhage: An international population-based study Neurology, September 12, 2000; 55(5): 658 - 662. [Abstract] [Full Text] [PDF]
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 L. Mariani, M. G. Bianchetti, G. Schroth, and R. W. Seiler Cerebral aneurysms in patients with autosomal dominant polycystic kidney disease—to screen, to clip, to coil? Nephrol. Dial. Transplant., October 1, 1999; 14(10): 2319 - 2322. [Full Text] [PDF]
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A. Ronkainen, M. Niskanen, R. Piironen, and J. Hernesniemi Familial Subarachnoid Hemorrhage : Outcome Study Stroke, May 1, 1999; 30(5): 1099 - 1102. [Abstract] [Full Text] [PDF]
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K. Yamashita, S. Kashiwagi, S. Kato, T. Takasago, and H. Ito Cerebral Aneurysms in the Elderly in Yamaguchi, Japan : Analysis of the Yamaguchi Data Bank of Cerebral Aneurysm From 1985 to 1995 Stroke, October 1, 1997; 28(10): 1926 - 1931. [Abstract] [Full Text]
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J. W. Hop, G. J.E. Rinkel, A. Algra, and J. van Gijn Case-Fatality Rates and Functional Outcome After Subarachnoid Hemorrhage : A Systematic Review Stroke, March 1, 1997; 28(3): 660 - 664. [Abstract] [Full Text]
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 W. I. Schievink Intracranial Aneurysms N. Engl. J. Med., January 2, 1997; 336(1): 28 - 40. [Full Text] [PDF]
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G. J.E. Rinkel, N. E.M. Prins, and A. Algra Outcome of Aneurysmal Subarachnoid Hemorrhage in Patients on Anticoagulant Treatment Stroke, January 1, 1997; 28(1): 6 - 9. [Abstract] [Full Text]
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L. L. Teunissen, G. J.E. Rinkel, A. Algra, and J. van Gijn Risk Factors for Subarachnoid Hemorrhage : A Systematic Review Stroke, March 1, 1996; 27(3): 544 - 549. [Abstract] [Full Text]
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