(Stroke. 1997;28:660-664.)
© 1997 American Heart Association, Inc.
Articles |
Case-Fatality Rates and Functional Outcome After Subarachnoid Hemorrhage
A Systematic Review
From the University Department of Neurology, Utrecht, Netherlands.
Correspondence to Jeannette W. Hop, MD, University Department of Neurology, Hpn G.03.228, PO Box 85500, 3508 GA Utrecht, Netherlands. E-mail j.w.hop{at}neuro.azu.nl.
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Abstract |
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Background During the last three decades, new management strategies have been developed for patients with aneurysmal subarachnoid hemorrhage. To assess whether the case-fatality rate has improved after the introduction of new management strategies, we studied outcome in all population-based studies from 1960 onward.
Summary of Review To identify population-based studies that reported on case-fatality rate in subarachnoid hemorrhage, we performed a MEDLINE search and checked all reference lists of the studies found. Two authors (J.W.H. and G.J.E.R.) independently assessed all studies for eligibility, using predefined criteria for case finding and diagnosis, and extracted data on case-fatality rates. We used weighted linear regression analysis to quantify change in case-fatality rate over time. We found 21 studies, describing 25 study periods between 1960 and 1992. Case-fatality rates varied between 32% and 67%, with the exception of one recent study. The case-fatality rate decreased by 0.5% per year (95% confidence interval, -0.1 to 1.2); the decline was steeper after adjustment for age and sex (0.9% per year; 95% confidence interval, -0.7 to 2.6; data from 12 studies).
Conclusions The case-fatality rate after subarachnoid hemorrhage has decreased during the last three decades. A plausible explanation for this decrease is the improved management of patients with subarachnoid hemorrhage.
Key Words: morbidity • outcome • subarachnoid hemorrhage
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Introduction |
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During the last three decades, new diagnostic techniques and therapeutic strategies have emerged for patients with subarachnoid hemorrhage (SAH). The introduction of CT and catheter angiography improved accuracy of diagnosis and provided a tool in the evaluation of the clinical course.1 The application of the operating microscope refined microsurgical techniques.2 More recently, the calcium antagonist nimodipine, which results in a 40% reduction of poor outcome, has become widely used.3 Since fluid restriction and use of antihypertensive drugs were found to be harmful, hypervolemia, hemodilution, and in some instances even induced hypertension are now used instead.4 5 Moreover, the timing of surgery has shifted for certain categories of patients from late (>10 days) to early (0 to 3 days) after the SAH.6 7
To investigate whether the case-fatality rate and morbidity in patients with SAH have improved after the introduction of new management strategies, we studied outcome in all population-based studies from 1960 onward that fulfilled predefined criteria.
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Methods |
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To find population-based studies on SAH, a MEDLINE search was performed (key words: subarachnoid hemorrhage and stroke, outcome, mortality, case fatality, population, or epidemiology in different combinations). For studies thus found, reference lists were checked to find additional studies. This method of cross-checking was continued until no further studies were found. For population-based studies that reported on incidence but not on outcome, a new search with all authors of the incidence study was performed to detect any further outcome studies.
Inclusion criteria for this review were as follows: (1) publication between 1965 and 1995 and period of survey after 1960; (2) study period not longer than 10 years, unless separate results per decade are given; (3) population-based design, defined by the following criteria: the study population is representative of the population in general, all hospitals serving the study population have been involved, all death certificates have been examined or data on deaths of nonhospitalized patients have been obtained from the coroner; (4) upper limit of age for the study not below 75 years and lower limit not above 25 years; (5) for population-based studies about stroke in general, SAH should be considered as a separate entity with defined clinical criteria and a defined number of cases that include or at least allow calculation of case-fatality rates; and (6) review of at least two thirds of the records by the study investigators.
All eligible studies were independently reviewed by two authors (J.W.H. and G.J.E.R.) to extract data on case-finding methods, diagnostic criteria for SAH, number of patients, proportion of patients who underwent CT scanning, time of follow-up, number of deaths among patients with SAH, and, if available, functional outcome among patients who had survived the bleed. In case of disagreement, the article was reread and discussed until agreement was achieved. Studies that described two or more periods were considered separate studies.7 8 9 In one study describing two periods, the first period concerned only hospital-based data9 ; since the hospitals in question are designated emergency centers and since all patients, even if moribund, are immediately referred, both periods were included.
Data on functional outcome after SAH were extracted if available, and if necessary they were adjusted to fit into the modified Rankin Scale, a handicap scale that grades patients on their overall level of independence with reference to their previous lifestyle.10 11 If functional outcome was assessed by the Glasgow Outcome Scale (GOS),12 this adjustment was as follows: GOS 5=Rankin 0+1; GOS 4=Rankin 2+3; GOS 3=Rankin 4; and GOS 2=Rankin 5. If no scale was used, patients considered to have "returned to their previous lifestyle" were graded Rankin 0 to 2.
Data Analysis
In the data analysis the relationship between the case-fatality
rate and the mid–calendar year of the study was quantified by means of
weighted linear regression, in which the inverse of the standard error
of the case-fatality rate for each study was taken as weight. The
results are expressed as the percent decrease of the case-fatality rate
per calendar year increase.
Nine of the 24 studies did not assess outcome at 1 month but at 2 weeks,13 3 weeks,7 14 or 3 months.15 16 17 18 19 An initial analysis was performed on all studies, including those studies with outcome assessed at any time between 2 weeks and 3 months. Because the Kaplan-Meier survival curve for SAH shows a steep decline in the first 2 weeks but a more or less horizontal course after the initial 2 or 3 weeks,7 15 20 21 22 23 24 we performed a second analysis that included only the studies that assessed the case-fatality rate at precisely 1 month.
To take age and sex differences between studies into account, we entered variables for mean age and percentage of women into the weighted linear regression model and calculated age- and sex-adjusted values for the change in case-fatality rate per calendar year.
To assess the influence of differences in case-finding methods, another analysis was performed with exclusion of five studies that did not examine all death certificates.9 13 17 25 26
Moreover, proportions of patients who died before hospitalization, arrived dead on admission, or died on the day of admission were retrieved from each study; for studies in which this percentage was below 15%, case-fatality rates were recalculated as if 15% had died before or on the day of admission.
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Results |
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We selected 21 studies, describing 25 study periods between 1960 and 1992. Table 1
summarizes the characteristics of
these studies.
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A total number of 2155 patients with SAH were included in these studies: 1068 women and 998 men (for 89 patients sex was not reported). Mean age at the time of the hemorrhage was 55 years (data derived from 15 studies). Mean age for women was 58 years; this increased from 57 years in the period 1977 to 1984 to 59 years between 1985 and 1992. Mean age for men was 53 years, with no increase over time (mean of 53 years for 1977 to 1984 and 52 years for 1985 to 1992).
Weighted linear regression analysis of all studies showed that the
case-fatality rate decreased 0.8% per year (95% confidence interval
[CI], 0.1 to 1.5; Table 2, Figure). The
most recent study had an exceptionally low case-fatality rate (8%;
range in other studies, 32% to 67%).32 Exclusion of this
study altered the result to a decrease of 0.5% per year (95% CI,
-0.1% to 1.2%). Because of this substantial difference, this study
was excluded in all other analyses.
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Exclusion of studies with outcome assessment at an interval other than 1 month did not essentially alter the results. After adjustment for age and sex in the 12 studies in which these data were available, the crude decline in case-fatality rate (0.6% per year) increased to 0.9% per year (95% CI, -0.7% to 2.6%). The decline in case-fatality rate was not influenced by adjustment for proportion of patients that underwent a CT scan or by the examination of only coroners' data and not all death certificates. After recalculation of the percentage of patients who died before admission to 15%, the results were essentially the same.
Table 3 shows data from eight studies that provided
information on functional outcome. Ten percent to 20% of all patients
became disabled, with loss of independence. Although only eight of 21
studies provided data on functional outcome and the time of outcome
assessment varied from 1 to 48 months, weighted linear regression of
these data showed an increase in the proportion of patients who
remained independent after their SAH of 1.5% per year (95% CI, 0.1%
to 2.8%).
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Discussion |
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The results of our review show a 15% decrease in case-fatality rate of SAH during the last three decades. Although the confidence intervals include zero, indicating that the results might also be consistent with no trend in case-fatality rate, this decrease is consistent through all analyses we performed and becomes stronger if data are adjusted for age and sex.
The mean age of patients included in the studies with SAH has increased over time, which negatively affects the unadjusted case-fatality rates in the later studies because outcome is less favorable in older patients.38 39
Our results should be interpreted with some caution since a number of other factors may have influenced our results. First, although we used predefined criteria for methods of case finding, considerable differences in completeness of case finding remain between studies. Because patients who die at home or in a nursing home are most difficult to detect, studies with more complete case finding in this subset of patients may report higher case-fatality rates, but analysis in which we used recalculated data with a minimum of 15% dead on admission did not alter the results. Also, whether data on out-of-hospital deaths were obtained from the coroners' office or by the examination of all death certificates had no influence. Second, unpublished data may not have been included. Since the studies in this review do not concern clinical trials or treatment evaluations with possible "negative" results, the potential issue of publication bias is not likely in this review. Third, not all studies used the same clinical criteria for the diagnosis of SAH. We assume that the majority of cases studied have been true SAH cases because the definitions show a great overlap and because most patients have been investigated by lumbar puncture or CT. However, before CT scanners became widely available, some patients with intracerebral hemorrhage were probably misdiagnosed as having SAH.1
Since case-fatality rates for SAH and intracerebral hemorrhage are similar,40 inclusion of some patients with intracerebral hemorrhage will not have biased the results. Fourth, we compared studies from different countries, with possible differences in management strategies and hence different case-fatality rates. In this review, however, there is a random distribution of countries studied over time. It is very unlikely that the most recent studies were all undertaken in places with "better" management strategies and therefore lower case-fatality rates. Two studies that were undertaken in the same place but at different time intervals8 9 both showed a decrease in case-fatality rate over time and thus supported our findings in all other analyses. Moreover, we excluded the most recent study, which had a very low case-fatality rate. Exclusion of this study resulted in an underestimation of the actual decrease in case-fatality rate, and its findings support the presence of a true decline.
A plausible explanation for the decrease in case-fatality rate over time is the improved management of patients with SAH. Management strategies that may have contributed to the improved outcome include (1) better case-finding methods that identify less severe cases; (2) more accurate diagnostic tools, such as CT and MR techniques; and (3) improved medical and surgical treatment regimens.
The substantial effects on outcome by treatments such as nimodipine in randomized trials41 are much stronger than the modest effects on the case-fatality rate in population-based samples. This discrepancy might be explained by two factors. First, new treatment strategies have predominantly been introduced in the past 5 to 10 years. The effect on case-fatality rate might become more substantial in the future. Second, the effect is diluted by extremes of the clinical spectrum: patients who will recover in any case or those who die early after the initial bleed. A considerable and stable number of patients (10% to 20%) die at home or arrive dead on admission,8 20 42 43 and another 12% to 30%7 23 never recover from the initial bleed. Thus, only a small proportion of all patients with SAH will profit from new medical or surgical treatment regimens.
Our analysis showed that the proportion of patients who remain independent has increased. This is consistent with the decrease in case-fatality rate and indicates that the smaller proportion of deaths is associated with a larger proportion of independent patients. However, many patients who survived their bleed are left severely disabled, and even patients who remain independent may experience great difficulties in resuming their previous lifestyle.44 Evaluation of new modes of treatment should therefore focus not only on case-fatality rate but also on improvement of functional outcome and quality of life.
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Footnotes |
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The opinions expressed in this article are not necessarily those of the editors or of the American Heart Association.
Received July 10, 1996; revision received November 5, 1996; accepted December 3, 1996.
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A. T. Fraticelli, B. P. Cholley, M.-R. Losser, J.-P. Saint Maurice, and D. Payen Milrinone for the Treatment of Cerebral Vasospasm After Aneurysmal Subarachnoid Hemorrhage Stroke, March 1, 2008; 39(3): 893 - 898. [Abstract] [Full Text] [PDF]
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Y. M. Ruigrok and G. J.E. Rinkel Genetics of Intracranial Aneurysms Stroke, March 1, 2008; 39(3): 1049 - 1055. [Abstract] [Full Text] [PDF]
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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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 H. Takao and T. Nojo Treatment of Unruptured Intracranial Aneurysms: Decision and Cost-effectiveness Analysis Radiology, September 1, 2007; 244(3): 755 - 766. [Abstract] [Full Text] [PDF]
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A. M. Bakker, S. M. Dorhout Mees, A. Algra, and G. J.E. Rinkel Extent of Acute Hydrocephalus After Aneurysmal Subarachnoid Hemorrhage as a Risk Factor for Delayed Cerebral Infarction Stroke, September 1, 2007; 38(9): 2496 - 2499. [Abstract] [Full Text] [PDF]
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L. A. Lanterna, Y. Ruigrok, S. Alexander, J. Tang, F. Biroli, L. T. Dunn, and W. S. Poon Meta-analysis of APOE genotype and subarachnoid hemorrhage: Clinical outcome and delayed ischemia Neurology, August 21, 2007; 69(8): 766 - 775. [Abstract] [Full Text] [PDF]
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S. M Dorhout Mees, W. M van den Bergh, A. Algra, and G. J E Rinkel Achieved serum magnesium concentrations and occurrence of delayed cerebral ischaemia and poor outcome in aneurysmal subarachnoid haemorrhage J. Neurol. Neurosurg. Psychiatry, July 1, 2007; 78(7): 729 - 731. [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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J. I. Suarez Timing of Neuropsychological Outcome Measures in Patients With Subarachnoid Hemorrhage Stroke, June 1, 2007; 38(6): 1724 - 1725. [Full Text] [PDF]
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I. Linfante and A. K. Wakhloo Brain Aneurysms and Arteriovenous Malformations: Advancements and Emerging Treatments in Endovascular Embolization Stroke, April 1, 2007; 38(4): 1411 - 1417. [Abstract] [Full Text] [PDF]
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R.T. Higashida, B.J. Lahue, M.T. Torbey, L.N. Hopkins, E. Leip, and D.F. Hanley Treatment of Unruptured Intracranial Aneurysms: A Nationwide Assessment of Effectiveness AJNR Am. J. Neuroradiol., January 1, 2007; 28(1): 146 - 151. [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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W. M. van den Bergh and on behalf of the MASH Study Group Randomized Controlled Trial of Acetylsalicylic Acid in Aneurysmal Subarachnoid Hemorrhage: The MASH Study Stroke, September 1, 2006; 37(9): 2326 - 2330. [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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A Petzold, G Keir, A Kay, M Kerr, and E J Thompson Axonal damage and outcome in subarachnoid haemorrhage. J. Neurol. Neurosurg. Psychiatry, June 1, 2006; 77(6): 753 - 759. [Abstract] [Full Text] [PDF]
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L. Hacein-Bey, D.R. Harder, H.T. Meier, P.N. Varelas, N. Miyata, K.K. Lauer, J.F. Cusick, and R.J. Roman Reversal of Delayed Vasospasm by TS-011 in the Dual Hemorrhage Dog Model of Subarachnoid Hemorrhage AJNR Am. J. Neuroradiol., June 1, 2006; 27(6): 1350 - 1354. [Abstract] [Full Text] [PDF]
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The CARAT Investigators* Rates of Delayed Rebleeding From Intracranial Aneurysms Are Low After Surgical and Endovascular Treatment Stroke, June 1, 2006; 37(6): 1437 - 1442. [Abstract] [Full Text] [PDF]
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S. Juvela and J. Siironen D-Dimer as an Independent Predictor for Poor Outcome After Aneurysmal Subarachnoid Hemorrhage Stroke, June 1, 2006; 37(6): 1451 - 1456. [Abstract] [Full Text] [PDF]
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M. J.H. Wermer, I. C. van der Schaaf, B. K. Velthuis, C. B. Majoie, K. W. Albrecht, and G. J.E. Rinkel Yield of Short-Term Follow-up CT/MR Angiography for Small Aneurysms Detected at Screening Stroke, February 1, 2006; 37(2): 414 - 418. [Abstract] [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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M. Wintermark, N.U. Ko, W.S. Smith, S. Liu, R.T. Higashida, and W.P. Dillon Vasospasm after Subarachnoid Hemorrhage: Utility of Perfusion CT and CT Angiography on Diagnosis and Management AJNR Am. J. Neuroradiol., January 1, 2006; 27(1): 26 - 34. [Abstract] [Full Text] [PDF]
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C J M Frijns, R Fijnheer, A Algra, J A van Mourik, J van Gijn, and G J E Rinkel Early circulating levels of endothelial cell activation markers in aneurysmal subarachnoid haemorrhage: associations with cerebral ischaemic events and outcome J. Neurol. Neurosurg. Psychiatry, January 1, 2006; 77(1): 77 - 83. [Abstract] [Full Text] [PDF]
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W J Schuiling, P J W Dennesen, J T. J Tans, L M Kingma, A Algra, and G J E Rinkel Troponin I in predicting cardiac or pulmonary complications and outcome in subarachnoid haemorrhage J. Neurol. Neurosurg. Psychiatry, November 1, 2005; 76(11): 1565 - 1569. [Abstract] [Full Text] [PDF]
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 K. Takeuchi, M. Renic, Q. C. Bohman, D. R. Harder, N. Miyata, and R. J. Roman Reversal of delayed vasospasm by an inhibitor of the synthesis of 20-HETE Am J Physiol Heart Circ Physiol, November 1, 2005; 289(5): H2203 - H2211. [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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 W A Liebenberg, R Worth, G B Firth, J Olney, and J S Norris Aneurysmal subarachnoid haemorrhage: guidance in making the correct diagnosis Postgrad. Med. J., July 1, 2005; 81(957): 470 - 473. [Abstract] [Full Text] [PDF]
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W. M. van den Bergh and on behalf of the MASH Study Group Magnesium Sulfate in Aneurysmal Subarachnoid Hemorrhage: A Randomized Controlled Trial Stroke, May 1, 2005; 36(5): 1011 - 1015. [Abstract] [Full Text] [PDF]
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 M. Ishiguro, T. L. Wellman, A. Honda, S. R. Russell, B. I. Tranmer, and G. C. Wellman Emergence of a R-Type Ca2+ Channel (CaV 2.3) Contributes to Cerebral Artery Constriction After Subarachnoid Hemorrhage Circ. Res., March 4, 2005; 96(4): 419 - 426. [Abstract] [Full Text] [PDF]
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 A. M. Naidech, N. Janjua, K. T. Kreiter, N. D. Ostapkovich, B.-F. Fitzsimmons, A. Parra, C. Commichau, E. S. Connolly, and S. A. Mayer Predictors and Impact of Aneurysm Rebleeding After Subarachnoid Hemorrhage Arch Neurol, March 1, 2005; 62(3): 410 - 416. [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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K Doi Current status and future potential of computer-aided diagnosis in medical imaging Br. J. Radiol., January 1, 2005; 78(suppl_1): S3 - s19. [Abstract] [Full Text] [PDF]
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M. Shojima, M. Oshima, K. Takagi, R. Torii, M. Hayakawa, K. Katada, A. Morita, and T. Kirino Magnitude and Role of Wall Shear Stress on Cerebral Aneurysm: Computational Fluid Dynamic Study of 20 Middle Cerebral Artery Aneurysms Stroke, November 1, 2004; 35(11): 2500 - 2505. [Abstract] [Full Text] [PDF]
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J. A. Iniesta, R. Gonzalez-Conejero, C. Piqueras, V. Vicente, and J. Corral Platelet GP IIIa Polymorphism HPA-1 (PlA) Protects Against Subarachnoid Hemorrhage Stroke, October 1, 2004; 35(10): 2282 - 2286. [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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W.-D. Niesen, M. Rosenkranz, W. Schummer, C. Weiller, and U. Sliwka Cerebral Venous Flow Velocity Predicts Poor Outcome in Subarachnoid Hemorrhage Stroke, August 1, 2004; 35(8): 1873 - 1878. [Abstract] [Full Text] [PDF]
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A. Slowik, A. Borratynska, J. Pera, M. Betlej, T. Dziedzic, T. Krzyszkowski, R. Czepko, D. A. Figlewicz, and A. Szczudlik II Genotype of the Angiotensin-Converting Enzyme Gene Increases the Risk for Subarachnoid Hemorrhage From Ruptured Aneurysm Stroke, July 1, 2004; 35(7): 1594 - 1597. [Abstract] [Full Text] [PDF]
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Y.M. Ruigrok, G.J.E. Rinkel, C. Wijmenga, G. Tromp, and S. Wills Familial Intracranial Aneurysms * Response Stroke, March 1, 2004; 35 (3): e59 - e60. [Full Text] [PDF]
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M. J.H. Wermer, E. Buskens, I. C. van der Schaaf, P. M.M. Bossuyt, and G. J.E. Rinkel Yield of screening for new aneurysms after treatment for subarachnoid hemorrhage Neurology, February 10, 2004; 62(3): 369 - 375. [Abstract] [Full Text] [PDF]
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S. Juvela Treatment Options of Unruptured Intracranial Aneurysms Stroke, February 1, 2004; 35(2): 372 - 374. [Full Text] [PDF]
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S. Juvela Prehemorrhage Risk Factors for Fatal Intracranial Aneurysm Rupture Stroke, August 1, 2003; 34(8): 1852 - 1857. [Abstract] [Full Text] [PDF]
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J. Ballard, K. T. Kreiter, J. Claassen, R. G. Kowalski, E. S. Connolly, and S. A. Mayer Risk Factors for Continued Cigarette Use After Subarachnoid Hemorrhage Stroke, August 1, 2003; 34(8): 1859 - 1863. [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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J. P. Broderick, C. M. Viscoli, T. Brott, W. N. Kernan, L. M. Brass, E. Feldmann, L. B. Morgenstern, J. L. Wilterdink, and R. I. Horwitz Major Risk Factors for Aneurysmal Subarachnoid Hemorrhage in the Young Are Modifiable Stroke, June 1, 2003; 34(6): 1375 - 1381. [Abstract] [Full Text] [PDF]
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L. Cambj-Sapunar, M. Yu, D. R. Harder, and R. J. Roman Contribution of 5-Hydroxytryptamine1B Receptors and 20-Hydroxyeiscosatetraenoic Acid to Fall in Cerebral Blood Flow After Subarachnoid Hemorrhage Stroke, May 1, 2003; 34(5): 1269 - 1275. [Abstract] [Full Text] [PDF]
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S. C. Johnston, R. T. Higashida, D. L. Barrow, L. R. Caplan, J. E. Dion, G. Hademenos, L. N. Hopkins, A. Molyneux, R. H. Rosenwasser, F. Vinuela, et al. Recommendations for the Endovascular Treatment of Intracranial Aneurysms: A Statement for Healthcare Professionals from the Committee on Cerebrovascular Imaging of the American Heart Association Council on Cardiovascular Radiology Stroke, October 1, 2002; 33(10): 2536 - 2544. [Full Text] [PDF]
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C. H.S. Leung, W.S. Poon, L.M. Yu, G. K.C. Wong, and H.K. Ng Apolipoprotein E Genotype and Outcome in Aneurysmal Subarachnoid Hemorrhage Stroke, February 1, 2002; 33(2): 548 - 552. [Abstract] [Full Text] [PDF]
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H. Kimura, K. Sasaki, T. Meguro, and J. H. Zhang Phosphatidylinositol 3-Kinase Inhibitor Failed to Reduce Cerebral Vasospasm in Dog Model of Experimental Subarachnoid Hemorrhage Stroke, February 1, 2002; 33(2): 593 - 599. [Abstract] [Full Text] [PDF]
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A. Ronkainen, M. Niskanen, J. Rinne, T. Koivisto, J. Hernesniemi, and M. Vapalahti Evidence for Excess Long-Term Mortality After Treated Subarachnoid Hemorrhage Stroke, December 1, 2001; 32(12): 2850 - 2853. [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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A. G. Hamedani, C. K. Wells, L. M. Brass, W. N. Kernan, C. M. Viscoli, J. N. Maraire, I. A. Awad, and R. I. Horwitz A Quality-of-Life Instrument for Young Hemorrhagic Stroke Patients Stroke, March 1, 2001; 32(3): 687 - 695. [Abstract] [Full Text] [PDF]
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W.T. Longstreth Jr., C. Bernick, A. Fitzpatrick, M. Cushman, L. Knepper, J. Lima, and C.D. Furberg Frequency and predictors of stroke death in 5,888 participants in the Cardiovascular Health Study Neurology, February 13, 2001; 56(3): 368 - 375. [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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Y. M. Ruigrok, G. J. E. Rinkel, E. Buskens, B. K. Velthuis, and J. van Gijn Perimesencephalic Hemorrhage and CT Angiography : A Decision Analysis Stroke, December 1, 2000; 31(12): 2976 - 2983. [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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E. J. Roos, G. J. E. Rinkel, B. K. Velthuis, and A. Algra The relation between aneurysm size and outcome in patients with subarachnoid hemorrhage Neurology, June 27, 2000; 54(12): 2334 - 2336. [Abstract] [Full Text] [PDF]
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T. W M Raaymakers Functional outcome and quality of life after angiography and operation for unruptured intracranial aneurysms J. Neurol. Neurosurg. Psychiatry, May 1, 2000; 68(5): 571 - 576. [Abstract] [Full Text]
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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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L. Lennihan, S. A. Mayer, M. E. Fink, A. Beckford, M. C. Paik, H. Zhang, Y.-C. Wu, L. M. Klebanoff, E. C. Raps, and R. A. Solomon Effect of Hypervolemic Therapy on Cerebral Blood Flow After Subarachnoid Hemorrhage : A Randomized Controlled Trial Stroke, February 1, 2000; 31(2): 383 - 391. [Abstract] [Full Text] [PDF]
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The Magnetic Resonance Angiography in Relatives of Risks and Benefits of Screening for Intracranial Aneurysms in First-Degree Relatives of Patients with Sporadic Subarachnoid Hemorrhage N. Engl. J. Med., October 28, 1999; 341(18): 1344 - 1350. [Abstract] [Full Text] [PDF]
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S. C. Johnston, D. R. Gress, and J. G. Kahn Which unruptured cerebral aneurysms should be treated?: A cost-utility analysis Neurology, June 1, 1999; 52(9): 1806 - 1806. [Abstract] [Full Text] [PDF]
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 D. J Hellawell, R. Taylor, and B. Pentland Persisting symptoms and carers' views of outcome after subarachnoid haemorrhage Clinical Rehabilitation, April 1, 1999; 13(4): 333 - 340. [Abstract] [PDF]
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F H H Linn, G J E Rinkel, A Algra, and J van Gijn Headache characteristics in subarachnoid haemorrhage and benign thunderclap headache J. Neurol. Neurosurg. Psychiatry, November 1, 1998; 65(5): 791 - 793. [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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T. W. M. Raaymakers, G. J. E. Rinkel, M. Limburg, and A. Algra Mortality and Morbidity of Surgery for Unruptured Intracranial Aneurysms : A Meta-Analysis Stroke, August 1, 1998; 29(8): 1531 - 1538. [Abstract] [Full Text] [PDF]
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J. W. Hop, G. J. E. Rinkel, A. Algra, and J. van Gijn Quality of Life in Patients and Partners After Aneurysmal Subarachnoid Hemorrhage Stroke, April 1, 1998; 29(4): 798 - 804. [Abstract] [Full Text] [PDF]
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