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(Stroke. 1996;27:625-629.)
© 1996 American Heart Association, Inc.
Articles |
Incidence of Subarachnoid Hemorrhage
Role of Region, Year, and Rate of Computed Tomography: A Meta-Analysis
From the University Departments of Neurology (F.H.H.L., G.J.E.R., J. van G.) and Epidemiology (A.A.), Utrecht, Netherlands.
Correspondence to F.H.H. Linn, MD, Department of Neurology, Heidelberglaan 100, 3584 CX Utrecht, Netherlands. E-mail a.algra@neuro.azu.nl.
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Abstract |
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Background and Purpose The incidence of subarachnoid hemorrhage (SAH) has been estimated for many years at 10 to 15 per 100 000 person-years, but the most recent studies yield lower figures, of 6 to 8 per 100 000 person-years. To investigate the cause of this apparent decline, we studied the influence of year of study, rate of CT, and region.
Methods We performed a meta-analysis of SAH incidence studies from 1960 onward and assessed the influence of the three factors by means of univariate and multivariate Poisson regression analyses.
Results Eighteen studies fulfilled predefined inclusion criteria. In three Finnish studies, the pooled incidence was 21.4 per 100 000 person-years (95% confidence interval [CI], 19.5 to 23.4); in 15 non-Finnish studies, it was 7.8 per 100 000 person-years (95% CI, 7.2 to 8.4). With univariate analysis, in non-Finnish studies the incidence decreased 0.96% for each percentage point increase of patients investigated with CT (rate ratio, 0.9904; 95% CI, 0.9878 to 0.9930). With 100% CT scanning, the incidence of SAH outside Finland is estimated at 6 per 100 000 person-years. The rate ratio for year of study was 0.952 (95% CI, 0.935 to 0.969) for each later year in the period 1960 to 1994. In multivariate analysis, only the use of CT was independently related to SAH incidence. For the Finnish studies, the rate ratios for use of CT and year of study were not statistically significant. We also found in six studies that incidence for women was 1.6 (95% CI, 1.1 to 2.3) times higher than that for men (7.1 [95% CI, 5.4 to 8.7] and 4.5 [95% CI, 3.1 to 5.8], respectively).
Conclusions The actual incidence of SAH has remained stable over the last three decades; the apparent decline in incidence is entirely explained by the greater proportion of patients investigated with CT. The incidence of SAH in Finland is almost three times as high as in other parts of the world.
Key Words: computed tomography • epidemiology • Finland • meta-analysis • subarachnoid hemorrhage
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Introduction |
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In epidemiological studies before 1970, the incidence of subarachnoid hemorrhage (SAH) was estimated between 10 and 15 per 100 000 per year,1 2 and in a long-term study the incidence remained stable for a period of 40 years.3 In a number of recent studies, however, the incidence was between 5 and 10 per 100 000 per year.4 5 6 7 The apparent decline in the incidence of SAH might be explained by a genuine decline in the incidence of SAH, by incomplete case finding in recent studies, or by too loose diagnostic criteria in the older studies. In studies that did not use CT scanning to confirm the diagnosis, SAH may have been overdiagnosed since lumbar puncture alone is often inaccurate.8
To assess the relationship between the reported incidence of SAH and the rate of CT scanning, year of study, and geographic differences, we conducted a systematic review of all epidemiological studies on SAH performed after 1960.
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Methods |
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To identify studies on the incidence of SAH between 1960 and 1994, we performed a Medline search from 1960 onward and a Science Citation Index search beginning with the publications of Pakarinen,1 Phillips et al,9 Bonita and Thomson,10 and Sacco et al11 from 1980 onward (the introduction of a computerized system). In addition, we searched the reference lists of all relevant publications for other incidence studies about SAH or stroke. In case of multiple publications on the same population, we used the most recent publication. If a single population was studied in two or more periods, we separately used the incidence rates that were found for each study period.
Two authors (F.H.H.L. and G.J.E.R.) independently reviewed all eligible studies and completed a data form to compare items regarding population at risk, case finding, and diagnosis of SAH. In case of disagreement, the data were reviewed by the two other authors. Basic inclusion criteria for our review were the following: (1) results include or at least allow calculation of the overall incidence of SAH; (2) prospective, population-based design; (3) study population representative of the population in general; and (4) upper limit of age for the study population not below 75 years and lower limit of age not above 25 years. With regard to case finding, studies with door-to-door interviewing were not included. We further had decided beforehand that studies would be analyzed only if all hospitals serving the study population had been involved in the study and if the study investigator(s) had reviewed more than two thirds of the patients or their medical records. Two studies were excluded on the basis of this last criterion.12 13
For all included studies, we recorded the case-finding methods and diagnostic criteria that were used. For each study we tabulated the percentage of patients in whom SAH was proven by CT, angiography, or autopsy. If in studies on incidence of stroke in general the proportion of patients with SAH who were investigated with CT was not given separately, we used that given for all stroke patients. In three studies only a single, all-inclusive percentage was given for the proportion of patients investigated with CT, lumbar puncture, angiography, or any combination of these procedures. For two of these we successfully retrieved the rate of CT scanning alone in patients with SAH by contacting the authors of these studies,14 15 but data were not available for the third study.16
We used incidence rates relating to the entire populations of each study, without adjustments for age or sex. In three studies the denominator was only a restricted study population: with a lower age limit (16 years,17 20 years,16 and 25 years18 ) or with an upper age limit (75 years).18 Since such methods overestimate the incidence,19 in these instances we recalculated the incidence rates for the entire populations by means of unpublished data supplied by the original authors. We did not assign an arbitrary number of SAH cases for the population below 25 years of age in the three studies in question, because this number is negligible.4 10 20 In the study with an upper age limit of 75 years,18 we estimated the number of SAH cases in the group older than 75 years by using the age-specific, population-based mortality data on SAH for the population involved in that study and by assuming that the case-fatality rate of SAH in patients older than 75 years is 1.5 that of patients below that age.21 22
We separately analyzed data from different countries if there seemed to be marked differences in incidence. When possible, we also used incidence rates relating to men and women separately in studies without age limits. Subdivisions in age-specific incidence rates were precluded by the variety of age stratifications used in the different studies.
Data Analysis
For each of the selected studies, the overall incidence was
verified or computed if necessary. Ninety-five percent confidence
intervals (CIs) were calculated with Poisson methods.23 We
determined the relationship between the percentage of CT scans on the
one hand and year of the study on the other with the incidence of SAH
by means of univariate Poisson regression. These were
expressed as rate ratios with corresponding 95% CIs.
Multivariate Poisson regression was used to assess the
independent contribution of these variables to the SAH
incidence.24
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Results |
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We found 18 prospective, population-based studies that fulfilled the selection criteria; one of these described two periods.17 The methods for case finding and diagnosis are summarized in the Table
. The proportion of patients
investigated with CT ranged from 0% to 100%. Angiography was
performed in 76% of patients in one study,5 in 61% of
patients in another study,10 and in less than 40% in all
other studies. Autopsy rates among deceased patients were 50% or
higher in four studies10 17 25 26 and less than 40% in
all other studies.
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For all studies combined, the incidence of SAH was 10.5 (95% CI, 9.9
to 11.2) per 100 000 person-years, based on 10.6 million
person-years at risk. In only 6 of 18 studies (without age limits),
incidences were given for women and men
separately.4 6 7 14 20 28 For women the incidence was 7.1
(95% CI, 5.4 to 8.7) and for men 4.5 (95% CI, 3.1 to 5.8) per
100 000 person-years. Thus, the incidence in women was 1.6 times
higher (95% CI, 1.1 to 2.3) than in men. There was a marked difference
between incidences reported from Finland and those from non-Finnish
countries. The incidence for the three Finnish studies combined was
21.4 (95% CI, 19.5 to 23.4) per 100 000
person-years,18 25 26 as opposed to an overall
incidence from the 15 other studies of 7.8 (95% CI, 7.2 to 8.4) per
100 000 person-years (Fig 1). For every non-Finnish
region studied, the incidence was within the range of the pooled
incidence of the remaining non-Finnish studies. Because the incidence
in the Finnish studies was 2.7 times (95% CI, 2.4 to 3.1) as high as
in the other studies and was still 2.1 times as high after adjustments
for percentage of CT and year of study, we analyzed the data of
both groups separately.
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In the non-Finnish studies (8.4 million person-years at risk), the
use of CT to confirm the diagnosis significantly influenced the
resulting incidence rates; the more patients were investigated by CT,
the lower the incidence (Fig 2). The rate ratio for the
use of CT scan was 0.9904 (95% CI, 0.9878 to 0.9930), which means that
for each percentage point of patients investigated with CT scanning,
the incidence decreases by almost 1% (0.96%). If all patients had
been investigated with CT, the expected incidence, according to this
univariate Poisson model, would be 5.7 per 100 000
person-years. If the analysis on rate of CT was restricted
to the studies with known CT scan proportions, the rate ratio was
0.9929 (95% CI, 0.9897 to 0.9962). The incidence is also influenced by
the year in which the study was performed (Fig 1
); for each later year
the study was performed, the incidence decreased by 4.8% (rate ratio,
0.9521; 95% CI, 0.9354 to 0.9691). On the basis of the time trend
alone, the expected incidence in 1995 would be 4.6 per 100 000
person-years. In a multivariate analysis
including both factors, the year of study was no longer a contributor
to the incidence of SAH (P=.67), whereas the rate ratio for
use of CT scanning was essentially the same as in the
univariate model (0.9898; 95% CI, 0.9862 to 0.9935).
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In the three Finnish studies, together constituting 2.2 million person-years at risk, neither the year of study nor the percentage of CT scanning was related to SAH incidence.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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We found that the actual incidence of SAH has remained stable over the last three decades. The apparent decline in recent years is entirely explained by the increasing proportion of patients investigated with CT. If all patients in the non-Finnish studies had been investigated with CT, the incidence of SAH would, according to our model, approximate 6 per 100 000 per year. This is in accordance with the low incidence of SAH at 6 to 8 per 100 000 per year found in recent studies in Western Europe and North America, in which high proportions of patients were investigated with CT. In one study that provided data on the incidence of SAH in a single population in two separate time periods (1975 to 1978 and 1985 to 1988) in which use of CT was low (1% and 37%, respectively),17 the rates were similar in both periods. This supports the notion that there is no actual decline in incidence of SAH.
The stable incidence of SAH contrasts with the decline in mortality from stroke in general, which may be related to a reduction in cardiovascular risk factors, including hypertension and smoking.32 Since hypertension and probably smoking are risk factors for SAH as well, a decline in incidence can be expected after reduction of these risk factors.33 34 However, the effect of risk factor reduction on incidence of SAH is difficult to measure because of the small number of patients with SAH in incidence studies. In our study we could not assess the effect of risk factor reduction since these factors were not studied in a uniform fashion.
In Finnish studies, the incidence was strikingly higher than in all other studies. Since this discrepancy could not be attributed to differences in case finding, diagnostic criteria, or age limits in the population, the incidence of SAH seems truly higher in Finland than in other regions. The higher frequency of surveillance of sudden deaths in two of the three Finnish studies compared with one of 15 non-Finnish studies is not sufficient as an explanation for the higher incidence of SAH in Finland. First, the difference in incidence between Finnish and non-Finnish studies does not disappear when only the studies with surveillance of sudden death are compared; second, in population-based studies the proportion of patients who die before reaching medical attention approximates 10% to 15%,35 which is far too low to explain the discrepancy. In Finland, all cardiovascular diseases including stroke are relatively frequent,36 37 which can perhaps be attributed to the high prevalence of hypertension in Finland.38 39 Since hypertension is a well-established risk factor also for SAH, the high prevalence of hypertension may at least partly account for the high incidence rate of SAH in Finland. Dietary factors have also tentatively been linked to the high incidence of cardiovascular and cerebrovascular diseases in Finland,40 but none of these factors, not even cholesterol, have been substantiated as risk factors for SAH.34 Since the risk for SAH is in part genetically determined,41 a higher prevalence in Finland of genes linked to aneurysm formation may also play a role in the higher incidence of SAH. The marked difference in incidence of SAH between Finland and other countries suggests that Finnish data on risk factors, changes in incidence of SAH over time, and prevalence of aneurysms cannot be extrapolated to other western countries.
We found a significant effect of sex in six (all non-Finnish) studies that analyzed men and women separately. The higher risk for women is in accordance with the higher frequency of women in most large series of SAH and might be influenced by hormonal factors.42 However, the higher risk of women is based on only one fifth of all patients in this review; because of the scarcity of data it was not possible to confirm these findings for all studies.
The methods of the studies we reviewed differed widely, but because we selected only prospective, population-based studies that fulfilled previously defined criteria and because methods of case finding and diagnosis for SAH were comparable, we were able to analyze the influence of year of the study and CT scanning. A possible flaw of our study is that we extrapolated the proportion of patients with CT for stroke in general to the subset of patients with SAH in five non-Finnish studies that did not separately report this proportion. For two other studies the authors provided unpublished data on the proportion of patients with SAH that were investigated with CT, and in both cases this was similar to that of patients with stroke in general. Moreover, if the analysis of the influence of CT is restricted to the studies with known CT scan proportions, the rate ratio was similar to all studies, including those with estimated CT rates. It is therefore not probable that our extrapolation in the other studies has introduced important bias.
Neither angiography nor lumbar puncture can replace CT in epidemiological studies on SAH. Angiography can demonstrate an aneurysm but is rarely performed in patients in poor clinical condition or in those who are elderly; this criterion will therefore underestimate the true incidence. Lumbar puncture can falsely suggest a diagnosis of SAH in patients with an intracerebral hematoma or in patients with a traumatic tap.43 Even if patients with focal signs are excluded, the clinical diagnosis of SAH, based only on a history of sudden headache or unconsciousness combined with a stiff neck or xanthochromic spinal fluid, is erroneous in 20% of patients.8 43 CT scanning allows not only an accurate diagnosis but also the recognition of a nonaneurysmal pattern of hemorrhage, the so-called perimesencephalic hemorrhage, in which blood is confined to the cisterns around the midbrain.44 Because this type of hemorrhage occurs in approximately 10% of all patients with a SAH,44 45 some overestimation of the incidence of aneurysmal SAH still occurs if this type of hemorrhage is included. Unfortunately, in none of the studies were patients with perimesencephalic, nonaneurysmal hemorrhage distinguished from patients with aneurysmal hemorrhage, not even in the study in which all patients were investigated with CT.46 We conclude that CT is an important tool in the diagnosis of SAH and that only studies with a high rate of CT scanning can reliably estimate the true incidence of SAH.
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Acknowledgments |
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We thank Drs Ricci (Italy), Leyten (Netherlands), Sarti (Finland), and Térent (Sweden) for giving us further details about their studies.
Received October 12, 1995; revision received December 28, 1995; accepted January 5, 1996.
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 S. Gallas, J. Drouineau, J. Gabrillargues, A. Pasco, C. Cognard, L. Pierot, and D. Herbreteau Feasibility, Procedural Morbidity and Mortality, and Long-Term Follow-Up of Endovascular Treatment of 321 Unruptured Aneurysms AJNR Am. J. Neuroradiol., January 1, 2008; 29(1): 63 - 68. [Abstract] [Full Text] [PDF]
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J. Wolstenholme, O. Rivero-Arias, A. Gray, A. J. Molyneux, R. S.C. Kerr, J. A. Yarnold, M. Sneade, and on behalf of the International Subarachnoid Aneury Treatment Pathways, Resource Use, and Costs of Endovascular Coiling Versus Surgical Clipping After aSAH Stroke, January 1, 2008; 39(1): 111 - 119. [Abstract] [Full Text] [PDF]
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N K de Rooij, F H H Linn, J A van der Plas, A Algra, and G J E Rinkel Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends J. Neurol. Neurosurg. Psychiatry, December 1, 2007; 78(12): 1365 - 1372. [Abstract] [Full Text] [PDF]
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B. Lubicz, M. Levivier, O. Francois, P. Thoma, N. Sadeghi, L. Collignon, and D. Baleriaux Sixty-Four-Row Multisection CT Angiography for Detection and Evaluation of Ruptured Intracranial Aneurysms: Interobserver and Intertechnique Reproducibility AJNR Am. J. Neuroradiol., November 1, 2007; 28(10): 1949 - 1955. [Abstract] [Full Text] [PDF]
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 H.-J. Priebe Aneurysmal subarachnoid haemorrhage and the anaesthetist Br. J. Anaesth., July 1, 2007; 99(1): 102 - 118. [Abstract] [Full Text] [PDF]
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M. J.H. Wermer, I. C. van der Schaaf, A. Algra, and G. J.E. Rinkel Risk of Rupture of Unruptured Intracranial Aneurysms in Relation to Patient and Aneurysm Characteristics: An Updated Meta-Analysis Stroke, April 1, 2007; 38(4): 1404 - 1410. [Abstract] [Full Text] [PDF]
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 Y. M. Ruigrok, G. J.E. Rinkel, R. van't Slot, M. Wolfs, S. Tang, and C. Wijmenga Evidence in favor of the contribution of genes involved in the maintenance of the extracellular matrix of the arterial wall to the development of intracranial aneurysms Hum. Mol. Genet., November 15, 2006; 15(22): 3361 - 3368. [Abstract] [Full Text] [PDF]
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D J Nieuwkamp, G J E Rinkel, R Silva, P Greebe, D A Schokking, and J M Ferro Subarachnoid haemorrhage in patients >=75 years: clinical course, treatment and outcome J. Neurol. Neurosurg. Psychiatry, August 1, 2006; 77(8): 933 - 937. [Abstract] [Full Text] [PDF]
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 R. Al-Shahi, P. M White, R. J Davenport, and K. W Lindsay Subarachnoid haemorrhage BMJ, July 29, 2006; 333(7561): 235 - 240. [Full Text] [PDF]
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 D J Verlaan, M-P Dube, J St-Onge, A Noreau, J Roussel, N Satge, M C Wallace, and G A Rouleau A new locus for autosomal dominant intracranial aneurysm, ANIB4, maps to chromosome 5p15.2-14.3. J. Med. Genet., June 1, 2006; 43(6): e31 - e31. [Abstract] [Full Text] [PDF]
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V. L. Feigin and M. Findlay Advances in Subarachnoid Hemorrhage Stroke, February 1, 2006; 37(2): 305 - 308. [Full Text] [PDF]
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 J. I. Suarez, R. W. Tarr, and W. R. Selman Aneurysmal Subarachnoid Hemorrhage N. Engl. J. Med., January 26, 2006; 354(4): 387 - 396. [Full Text] [PDF]
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V. L. Feigin, G. J.E. Rinkel, C. M.M. Lawes, A. Algra, D. A. Bennett, J. van Gijn, and C. S. Anderson Risk Factors for Subarachnoid Hemorrhage: An Updated Systematic Review of Epidemiological Studies Stroke, December 1, 2005; 36(12): 2773 - 2780. [Abstract] [Full Text] [PDF]
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J. R. Cebral, M. A. Castro, J. E. Burgess, R. S. Pergolizzi, M. J. Sheridan, and C. M. Putman Characterization of Cerebral Aneurysms for Assessing Risk of Rupture By Using Patient-Specific Computational Hemodynamics Models AJNR Am. J. Neuroradiol., November 1, 2005; 26(10): 2550 - 2559. [Abstract] [Full Text] [PDF]
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M. J.H. Wermer, P. Greebe, A. Algra, and G. J.E. Rinkel Incidence of Recurrent Subarachnoid Hemorrhage After Clipping for Ruptured Intracranial Aneurysms Stroke, November 1, 2005; 36(11): 2394 - 2399. [Abstract] [Full Text] [PDF]
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 G. M. Teasdale, J. M. Wardlaw, P. M. White, G. Murray, E. M. Teasdale, V. Easton, and on behalf of the Davie Cooper Scottish Aneurysm St The familial risk of subarachnoid haemorrhage Brain, July 1, 2005; 128(7): 1677 - 1685. [Abstract] [Full Text] [PDF]
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V. Feigin, V. Parag, C. M. M. Lawes, A. Rodgers, I. Suh, M. Woodward, K. Jamrozik, H. Ueshima, and on behalf of the Asia Pacific Cohort Studies Colla Smoking and Elevated Blood Pressure Are the Most Important Risk Factors for Subarachnoid Hemorrhage in the Asia-Pacific Region: An Overview of 26 Cohorts Involving 306 620 Participants Stroke, July 1, 2005; 36(7): 1360 - 1365. [Abstract] [Full Text] [PDF]
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S. Akpek, A. Arat, H. Morsi, R. P. Klucznick, C. M. Strother, and M. E. Mawad Self-Expandable Stent-Assisted Coiling of Wide-Necked Intracranial Aneurysms: A Single-Center Experience AJNR Am. J. Neuroradiol., May 1, 2005; 26(5): 1223 - 1231. [Abstract] [Full Text] [PDF]
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J. B. Springborg, H.-J. Frederiksen, V. Eskesen, and N. V. Olsen Trends in monitoring patients with aneurysmal subarachnoid haemorrhage Br. J. Anaesth., March 1, 2005; 94(3): 259 - 270. [Abstract] [Full Text] [PDF]
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L. M. Flett, C. S. Chandler, D. Giddings, and A. Gholkar Aneurysmal Subarachnoid Hemorrhage: Management Strategies and Clinical Outcomes in a Regional Neuroscience Center AJNR Am. J. Neuroradiol., February 1, 2005; 26(2): 367 - 372. [Abstract] [Full Text] [PDF]
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Y.B.W.E.M. Roos, G. Pals, P.M. Struycken, G.J.E. Rinkel, M. Limburg, J.C. Pronk, J.S.P. van den Berg, J.A.F.M. Luijten, P.L. Pearson, M. Vermeulen, et al. Genome-Wide Linkage in a Large Dutch Consanguineous Family Maps a Locus for Intracranial Aneurysms to Chromosome 2p13 Stroke, October 1, 2004; 35(10): 2276 - 2281. [Abstract] [Full Text] [PDF]
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 H. Nikaido, H. Tsunoda, Y. Nishimura, T. Kirino, and T. Tanaka Potential Role for Heat Shock Protein 72 in Antagonizing Cerebral Vasospasm After Rat Subarachnoid Hemorrhage Circulation, September 28, 2004; 110(13): 1839 - 1846. [Abstract] [Full Text] [PDF]
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B. Stegmayr, M. Eriksson, and K. Asplund Declining Mortality From Subarachnoid Hemorrhage: Changes in Incidence and Case Fatality From 1985 Through 2000 Stroke, September 1, 2004; 35(9): 2059 - 2063. [Abstract] [Full Text] [PDF]
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Y.M. Ruigrok, U. Seitz, S. Wolterink, G.J.E. Rinkel, C. Wijmenga, and Z. Urban Association of Polymorphisms and Haplotypes in the Elastin Gene in Dutch Patients With Sporadic Aneurysmal Subarachnoid Hemorrhage Stroke, September 1, 2004; 35(9): 2064 - 2068. [Abstract] [Full Text] [PDF]
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 Y.M. Ruigrok, G.J.E. Rinkel, A. Algra, T.W.M. Raaymakers, and J. van Gijn Characteristics of intracranial aneurysms in patients with familial subarachnoid hemorrhage Neurology, March 23, 2004; 62(6): 891 - 894. [Abstract] [Full Text] [PDF]
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D. Gaist, L. Pedersen, S. Cnattingius, and H. T. Sorensen Parity and Risk of Subarachnoid Hemorrhage in Women: A Nested Case-Control Study Based on National Swedish Registries Stroke, January 1, 2004; 35(1): 28 - 32. [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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S. Yamada, M. Utsunomiya, K. Inoue, K. Nozaki, S. Miyamoto, N. Hashimoto, K. Takenaka, T. Yoshinaga, and A. Koizumi Absence of Linkage of Familial Intracranial Aneurysms to 7q11 in Highly Aggregated Japanese Families Stroke, April 1, 2003; 34(4): 892 - 900. [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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J Isaksen, A Egge, K Waterloo, B Romner, and T Ingebrigtsen Risk factors for aneurysmal subarachnoid haemorrhage: the Tromso study J. Neurol. Neurosurg. Psychiatry, August 1, 2002; 73(2): 185 - 187. [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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M. Johansson, K. G. Cesarini, C. F. Contant, L. Persson, and P. Enblad Changes in Intervention and Outcome in Elderly Patients With Subarachnoid Hemorrhage Stroke, December 1, 2001; 32(12): 2845 - 2949. [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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M U Schuhmann, E Rickels, S K Rosahl, C G Schneekloth, and M Samii Acute care in neurosurgery: quantity, quality, and challenges J. Neurol. Neurosurg. Psychiatry, August 1, 2001; 71(2): 182 - 187. [Abstract] [Full Text] [PDF]
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Y. M. Ruigrok, E. Buskens, and G. J. E. Rinkel Attributable Risk of Common and Rare Determinants of Subarachnoid Hemorrhage Stroke, May 1, 2001; 32(5): 1173 - 1175. [Abstract] [Full Text] [PDF]
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L H Pobereskin Incidence and outcome of subarachnoid haemorrhage: a retrospective population based study J. Neurol. Neurosurg. Psychiatry, March 1, 2001; 70(3): 340 - 343. [Abstract] [Full Text] [PDF]
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C. N. Mhurchu, C. Anderson, K. Jamrozik, G. Hankey, D. Dunbabin, W.T. Longstreth Jr, and L. M. Nelson Hormonal Factors and Risk of Aneurysmal Subarachnoid Hemorrhage : An International Population-Based, Case-Control Study Editorial Comment : The Gender Gap in Aneurysmal Subarachnoid Hemorrhage Stroke, March 1, 2001; 32(3): 606 - 612. [Abstract] [Full Text] [PDF]
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J. van Gijn and G. J. E. Rinkel Subarachnoid haemorrhage: diagnosis, causes and management Brain, February 1, 2001; 124(2): 249 - 278. [Abstract] [Full Text] [PDF]
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P Mitchell and J Jakubowski Estimate of the maximum time interval between formation of cerebral aneurysm and rupture J. Neurol. Neurosurg. Psychiatry, December 1, 2000; 69(6): 760 - 767. [Abstract] [Full Text] [PDF]
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O G Nilsson, A Lindgren, N Stahl, L Brandt, and H Saveland Incidence of intracerebral and subarachnoid haemorrhage in southern Sweden J. Neurol. Neurosurg. Psychiatry, November 1, 2000; 69(5): 601 - 607. [Abstract] [Full Text] [PDF]
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Anonymous Epidemiology of Aneurysmal Subarachnoid Hemorrhage in Australia and New Zealand : Incidence and Case Fatality From the Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS) Stroke, August 1, 2000; 31(8): 1843 - 1850. [Abstract] [Full Text] [PDF]
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T. Ingall, K. Asplund, M. Mahonen, and R. Bonita A Multinational Comparison of Subarachnoid Hemorrhage Epidemiology in the WHO MONICA Stroke Study Stroke, May 1, 2000; 31(5): 1054 - 1061. [Abstract] [Full Text] [PDF]
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J. M. Wardlaw and P. M. White The detection and management of unruptured intracranial aneurysms Brain, February 1, 2000; 123(2): 205 - 221. [Abstract] [Full Text] [PDF]
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D. Gaist, M. Væth, I. Tsiropoulos, K. Christensen, E. Corder, J. Olsen, and H. T. Sørensen Risk of subarachnoid haemorrhage in first degree relatives of patients with subarachnoid haemorrhage: follow up study based on national registries in Denmark BMJ, January 15, 2000; 320(7228): 141 - 145. [Abstract] [Full Text]
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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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T. W. M. Raaymakers Aneurysms in relatives of patients with subarachnoid hemorrhage: Frequency and risk factors Neurology, September 1, 1999; 53(5): 982 - 982. [Abstract] [Full Text]
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T. Truelsen, R. Bonita, J. Duncan, N. E. Anderson, and E. Mee Changes in Subarachnoid Hemorrhage Mortality, Incidence, and Case Fatality in New Zealand Between 1981–1983 and 1991–1993 Stroke, November 1, 1998; 29(11): 2298 - 2303. [Abstract] [Full Text] [PDF]
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A. Ronkainen, H. Miettinen, K. Karkola, S. Papinaho, R. Vanninen, M. Puranen, and J. Hernesniemi Risk of Harboring an Unruptured Intracranial Aneurysm Stroke, February 1, 1998; 29(2): 359 - 362. [Abstract] [Full Text] [PDF]
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G. J. E. Rinkel, M. Djibuti, A. Algra, and J. van Gijn Prevalence and Risk of Rupture of Intracranial Aneurysms : A Systematic Review Stroke, January 1, 1998; 29(1): 251 - 256. [Abstract] [Full Text] [PDF]
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E. H Brilstra, J. W Hop, and G. J E Rinkel Quality of life after perimesencephalic haemorrhage J. Neurol. Neurosurg. Psychiatry, September 1, 1997; 63(3): 382 - 384. [Abstract] [Full Text] [PDF]
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T. Ostbye, A. R. Levy, and N. E. Mayo Hospitalization and Case-Fatality Rates for Subarachnoid Hemorrhage in Canada From 1982 Through 1991 : The Canadian Collaborative Study Group of Stroke Hospitalizations Stroke, April 1, 1997; 28(4): 793 - 798. [Abstract] [Full Text]
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S. E. Vermeer, G. J. E. Rinkel, and A. Algra Circadian Fluctuations in Onset of Subarachnoid Hemorrhage : New Data on Aneurysmal and Perimesencephalic Hemorrhage and a Systematic Review Stroke, April 1, 1997; 28(4): 805 - 808. [Abstract] [Full Text]
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