Spontaneoussubarachnoid hemorrhage (SAH) is a type of hemorrhagic stroke associated with high morbidity and mortality rates. As a result of improved diagnostic techniques and treatment modalities, case fatality rates have decreased significantly over the past 3 decades.15However, the reported mortality rate for aneurysmal SAH remains significant (35%), and one-third of survivors remain functionally dependent, even in the long term.18In clinical practice, early and accurate prediction of patient outcomes is essential for decision making (e.g., for the timing of aneurysm repair and the treatment of concomitant disorders). The initial neurological condition on admission has proven to be the strongest predictor of outcome; therefore, it was used in the development of several grading scales over the last several decades.4The first grading scale that became widely accepted was developed by Botterell et al.1in 1956, and it was followed by the Hunt and Hess scale11in 1968. Although the Hunt and Hess scale is still in use at many institutions, the World Federation of Neurosurgical Societies (WFNS) SAH grading scale21(eTable 1), introduced in 1988, is now regarded as the gold standard for initial clinical assessment. Nevertheless, there is room for improvement; 20% of patients with WFNS Grade V SAH recover without any important physical or cognitive deficits.10Therefore, making more accurate initial predictions of outcome after SAH remains a challenge.
The timing of clinical neurological assessment and subsequent grading of the patient are particularly subject to debate.3,6,16,17Owing to the presence of acute hydrocephalus or a large intracerebral hematoma, initial grading of the patient may be significantly impaired. After emergency neurological resuscitation is achieved by CSF drainage and/or craniotomy to remove a clot, the clinical condition of the patient with SAH may improve dramatically, often with consequences for the subsequent treatment strategy.8,14
In 2007, Ransom et al.17reported that an improved clinical condition after CSF drainage is related to a better long-term outcome. In addition, Giraldo et al.6demonstrated that the WFNS grade after neurological resuscitation (rWFNS) was a better predictor of outcome than the WFNS grade on admission. Nevertheless, the design and small sample size of these studies hampers the drawing of firm conclusions. Therefore, the aim of this study was to identify either the traditional on-admission WFNS grade or the postresuscitation rWFNS grade as the most accurate predictor of outcome after SAH.
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Patients and Inclusion Criteria
1998年1月至2014年12月,1620 consecutive patients with a nontraumatic SAH were admitted to our university neurovascular center. All patients with SAH were considered eligible for this study: 1236 patients with saccular SAH, 101 patients with a fusiform aneurysm or an intracranial artery dissection, and 283 patients with a (perimesencephalic) nonaneurysmal SAH. Clinically relevant data were collected prospectively. The study was registered in our local trial register. Given the observational design of the study and the fact that treatment of the patients was given according to standard clinical care, our institutional review board decided, in accordance with Dutch regulations, that informed consent was not required.
Treatment Protocol
A standardized multidisciplinary protocol was applied to all patients with SAH admitted to our center. Before 2002, patients with SAH were subject to emergency digital subtraction angiography (DSA) within 12 hours after admission. From 2002 onward, all patients underwent immediate CT angiography (CTA), followed by DSA within 48 hours in the case of negative CTA results. All imaging studies were evaluated immediately by an interventional neuroradiologist and a vascular neurosurgeon. If an underlying aneurysm was detected, patients in good neurological condition on admission (WFNS Grade I, II, or III) were treated as soon as technically and logistically feasible by using endovascular coiling or neurosurgical clipping, preferably within 72 hours after the ictus.20In the meantime, patients who required CSF drainage underwent external lumbar or ventricular catheterization.
Patients in poor neurological condition on admission (WFNS Grade IV or V) were not immediately considered for aneurysm repair; instead, neurological resuscitation was instigated first. After placement of an external ventricular drain, patients were closely monitored on the intensive care unit. If their clinical condition improved, aneurysm repair was instigated. Patients with a space-occupying intracranial hematoma (e.g., due to a ruptured middle cerebral artery aneurysm) underwent immediate craniotomy, evacuation of the hematoma, and concomitant clipping of the aneurysm regardless of their clinical condition (unless they were moribund). These neurological resuscitation procedures were performed in the first 24 hours after the initial SAH. After the resuscitation, the best neurological score in the first 12 hours after the intervention was considered the rWFNS grade.
All patients who survived the initial treatment period visited our outpatient clinic 6 weeks (± 1 week) after discharge, if their clinical condition permitted. If their clinical condition did not permit them, information on their condition was obtained from their rehabilitation clinic or nursing home. Because a large majority of the patients had a hospital stay of approximately 3 weeks (end of vasospasm period), first-time follow-up was available 9 weeks (± 1 week) after ictus.
Imaging
All available images of the included patients were reanalyzed by 2 reviewers (C.E.v.D. and N.A.B.) to reach agreement on the amount of blood shown on the initial CT scan according to the modified Fisher (mFisher) grade5(eTable 2) and the maximum diameter of the aneurysm. Imaging of the patients admitted before 2000 was not available for reevaluation. Although the radiological reports of these patients were available, their mFisher grade and maximum aneurysm diameter were considered unknown for this study. When it was not possible to identify the symptomatic aneurysm because the patient died before CTA or DSA could be performed (n = 21, all patients at Grade V), the aneurysm location was designated unknown.
Data Analysis
The following data were collected prospectively: date of ictus; age at time of SAH; sex; history of SAH; presence of hypertension; use of a platelet inhibitor or a vitamin K antagonist; the WFNS grade on initial in-hospital assessment; the rWFNS grade; symptomatic aneurysm size, morphology, and location; amount of blood on the initial CT scan; presence of acute hydrocephalus that required initiation of CSF drainage within 24 hours after ictus; type and time of aneurysm repair; and early rebleeding. If it was not possible to identify the symptomatic aneurysm because of multiple aneurysms (n = 22), the largest aneurysm was selected for analysis. When a patient died before CTA or DSA could be performed (n = 21), the aneurysm was considered in the analysis to be of aneurysmal origin with unknown location and size. Hypertension was defined as systolic blood pressure of > 140 mm Hg or diastolic blood pressure of > 90 mm Hg during recent measurements or controlled using antihypertensive drugs. Age of the patient and the location and size of the symptomatic aneurysm were classified according to the recently published PHASES study.7The amount of blood was classified according to the mFisher Scale. Aneurysm morphology was categorized as 1) saccular, 2) fusiform, 3) intracranial artery dissection, or, in the case of a nonaneurysmal SAH, 5) nonaneurysmal or perimesencephalic. A rebleeding of the ruptured aneurysm was defined as a sudden clinical deterioration with a concomitant increase of subarachnoid, intracerebral, or intraventricular blood shown on the subsequent CT scan or when similar signs and symptoms occurred without CT confirmation.
Outcome Measure
The primary outcome measure was poor functional outcome 2 months after the SAH according to the modified Rankin Scale (mRS) score, as assessed by the treating vascular neurosurgeon at follow-up outpatient clinic contacts.23A poor functional outcome was defined as an mRS score of 4–6 (eTable 3).
Statistical Analysis
The data were complete for all covariates except for aneurysm size (13% missing), mFisher grade (9% missing), and aneurysm location (1% missing). For these missing covariate data, multiple imputation (15 data sets) was performed with the linear regression method (multivariate analyses). Categorical data are presented as numbers and percentages, and continuous variables are presented as means with standard deviations or medians with interquartile ranges (IQRs), depending on normality of the data.
The association between the WFNS and rWFNS grades and poor outcome was evaluated using binary logistic regression analysis. After univariate analyses, all clinically relevant covariates with a p value of ≤ 0.15 were entered in the initial multivariate model. A backward stepwise elimination strategy was applied to estimate the odds ratios (OR) with a cutoff point of < 0.05 for inclusion in the final model. Results are presented as ORs with corresponding 95% confidence intervals (CIs). Sensitivity analysis was performed by multivariate logistic regression analysis excluding patients for whom data were missing (complete case analysis).
The discriminative performance of the final model was calculated by a pooled area under the receiver operating characteristic curve (AUC) with a corresponding 95% CI. An AUC of > 0.8 was regarded to indicate a model with good prognostic value.
A 2-tailed p value of < 0.05 was considered statistically significant. Statistical analyses were performed using SPSS (version 22.0) and GraphPad Prism (version 6.00 for Windows, GraphPad Software).
Results
Baseline Patient Characteristics
Baseline patient characteristics are shown inTable 1. A majority (62%) of the patients were female, and the median age was 55 years (IQR 46–65 years). In 1247 (78%) patients, a symptomatic or multiple aneurysms were detected, whereas SAH was considered perimesencephalic or nonaneurysmal in 283 (17%) patients. In patients with a symptomatic aneurysm, the anterior cerebral artery was involved most frequently (33%), followed by the middle cerebral artery (18%). In 198 (12%) patients, a space-occupying intracranial hematoma was present. Hydrocephalus that required acute CSF drainage (within 24 hours after ictus) was present in 362 (22%) patients. Aneurysm repair was performed in 79% of the patients with aneurysmal SAH. In 38 patients, acute craniotomy for the evacuation of a space-occupying intracranial hematoma was performed.
Baseline patient characteristics
| Characteristic | Value* |
|---|---|
| Total no. | 1620 (100) |
| Time frame | |
| 1998–2003 | 462 (29) |
| 2004–2009 | 635 (39) |
| 2010–2014 | 523 (32) |
| Female | 1001 (62) |
| Age in yrs (median [IQR]) | 55 (46–65) |
| Age | |
| <40 yrs | 159 (10) |
| 40–49 yrs | 398 (25) |
| 50–59 yrs | 458 (27) |
| 60–69 yrs | 370 (23) |
| >70 yrs | 235 (15) |
| History | |
| Previous SAH | 31 (2) |
| Hypertension | 336 (21) |
| Vitamin K antagonist | 29 (2) |
| Platelet inhibitor | 68 (4) |
| Initial WFNS grade | |
| I | 848 (53) |
| II | 313 (19) |
| III | 34 (2) |
| IV | 230 (14) |
| V | 195 (12) |
| rWFNS grade | |
| I | 872 (55) |
| II | 332 (20) |
| III | 38 (2) |
| IV | 218 (13) |
| V | 160 (10) |
| SAH type | |
| Aneurysm | 1247 (78) |
| Saccular | 1215 |
| Fusiform aneurysm | 32 |
| Intracranial artery dissection | 69 (4) |
| Perimesencephalic/nonaneurysmal | 283 (17) |
| Unknown | 21 (1) |
| Aneurysm location | |
| Anterior cerebral artery | 514 (33) |
| Middle cerebral artery | 288 (18) |
| Posterior communicating artery | 202 (12) |
| Internal carotid artery | 69 (4) |
| Posterior circulation | 243 (15) |
| Perimesencephalic/nonaneurysmal | 283 (17) |
| Unknown | 21 (1) |
| Aneurysm size | |
| 0–4.9 mm | 227 (14) |
| 5–6.9 mm | 310 (20) |
| 7–9.9 mm | 249 (15) |
| 10–19.9 mm | 205 (13) |
| ≥20 mm | 30 (2) |
| Fusiform/intracranial artery dissection | 101 (6) |
| Perimesencephalic/nonaneurysmal | 283 (17) |
| Unknown | 215 (13) |
| mFisher grade | |
| 0 | 162 (10) |
| 1 | 373 (23) |
| 2 | 286 (18) |
| 3 | 190 (12) |
| 4 | 465 (28) |
| Unknown | 144 (9) |
| Intracerebral hematoma | 198 (12) |
| Subdural hematoma | 20 (1) |
| Hydrocephalus that required CSF drainage† | 362 (22) |
| Acute craniotomy | 38 (2) |
| Early rebleeding (<72 hr) | 81 (5) |
| Type of treatment | |
| Endovascular | 562 (35) |
| Neurosurgical | 497 (31) |
| No treatment | 277 (17) |
| Perimesencephalic/nonaneurysmal | 283 (17) |
Values are numbers (%) of patients unless otherwise noted; values were rounded up to the nearest whole number.
External CSF drainage ≤ 24 hours after ictus and before treatment.
The distribution of WFNS and rWFNS grades is presented in图1左, which illustrates the shift for patients at WFNS Grade IV or V on initial in-hospital assessment to a lower WFNS grade after resuscitation. In the end, 106 (27%) of the 400 patients were in improved neurological condition after the resuscitation.
Left:Distribution of the admission WFNS and rWFNS grades.Right:Percentages of patients with a poor outcome according to each admisssion WFNS and rWFNS grade. Figure is available in color online only.
Baseline patient characteristics in the 3 consecutive time frames (1998–2003, 2004–2009, and 2010–2014) are shown ineTable 4. In recent years, the age of the patients has increased, as has the number of patients at WFNS Grade V on admission. Also, a change in the type of treatment was observed, with patients increasingly being treated endovascularly.
Despite the observed increasing age and percentage of patients at WFNS Grade V on admission, outcomes remained the same throughout the different time frames (eTable 5).
Outcome
Two months after the initial SAH, 52 (3.2%) of the 1620 patients were lost to follow-up. Of the remaining 1568 patients, 394 (25%) had a poor outcome (mRS Score 4–6), and the mortality rate was 17% (Table 2). The distribution of WFNS grades related to poor outcome is depicted inFig. 1 right. The percentage of patients with a poor outcome was higher in those with an rWFNS grade of V than in those with an admission WFNS grade of V (74% vs 67%, respectively; p < 0.001, chi-square test).
Distribution of functional outcome according to mRS score
| Functional Outcome | mRS Score | No. (%) of Patients Classified to Score After 2 mos (n = 1568) |
|---|---|---|
| Good | 0 | 406 (26) |
| 1 | 451 (29) | |
| 2 | 195 (12) | |
| 3 | 122 (8) | |
| Total | 1174 (75) | |
| Poor | 4 | 110 (7) |
| 5 | 22 (1) | |
| 6 | 262 (17) | |
| Total | 394 (25) |
Table 3显示了逻辑回归分析结果。房颤ter univariate analysis, both the WFNS and rWFNS grades were associated with poor functional outcome after 2 months. After adjustment for other significant variables in the univariate analysis, the rWFNS grade remained an independent predictor (p < 0.001), whereas the admission WFNS grade was no longer significantly associated with poor outcome. When the rWFNS grade was excluded from the multivariate analysis, the WFNS remained significantly associated with poor outcome (p < 0.001; data not shown). Other independent predictors of poor outcome were higher age (p < 0.001), larger aneurysm size (p < 0.001), a higher mFisher grade (p < 0.001), and the presence of an intracerebral hematoma (OR 1.8, 95% CI 1.2–2.8; p = 0.002). No significant differences in outcome were observed between patients treated endovascularly and those treated by neurosurgical clipping (OR 0.9, 95% CI 0.6–1.2; p = 0.36).
Results of univariate and multivariate logistic regression analyses for poor outcome 2 months after SAH*
| Covariate (n = 1620) | Univariate Analysis | Multivariate Analysis† | ||||
|---|---|---|---|---|---|---|
| OR | 95% CI | p Value‡ | aOR | 95% CI | p Value‡ | |
| Age | <0.001 | <0.001 | ||||
| <40 yrs | 1.0 | 1.0 | ||||
| 40–49 yrs | 1.3 | 0.8–2.1 | 0.34 | 1.0 | 0.5–1.9 | 0.99 |
| 50–59 yrs | 1.5 | 0.9–2.5 | 0.09 | 1.3 | 0.7–2.3 | 0.47 |
| 60–69 yrs | 1.9 | 1.2–3.1 | 0.01 | 1.6 | 0.9–3.0 | 0.14 |
| >70 yrs | 4.7 | 2.8–7.7 | <0.001 | 4.1 | 2.1–7.8 | <0.001 |
| Male | 0.9 | 0.7–1.1 | 0.40 | |||
| History | ||||||
| Previous SAH | 1.9 | 0.9–4.0 | 0.08 | |||
| Hypertension | 1.4 | 1.1–1.9 | 0.07 | |||
| Vitamin K antagonist | 1.1 | 0.5–2.6 | 0.76 | |||
| Platelet inhibitor | 1.8 | 1.1–3.0 | 0.03 | |||
| Initial WFNS grade | <0.001 | |||||
| I | 1.0 | |||||
| II | 2.9 | 2.0–4.3 | <0.001 | |||
| III | 6.5 | 3.1–13.9 | <0.001 | |||
| IV | 12.6 | 8.8–18.2 | <0.001 | |||
| V | 21.5 | 14.6–31.7 | <0.001 | |||
| rWFNS grade | <0.001 | <0.001 | ||||
| I | 1.0 | 1.0 | ||||
| II | 3.1 | 2.2–4.5 | <0.001 | 1.6 | 1.1–2.5 | 0.02 |
| III | 6.7 | 3.3–13.6 | <0.001 | 3.2 | 1.4–7.4 | 0.005 |
| IV | 12.6 | 8.8–18.0 | <0.001 | 5.7 | 3.7–8.8 | <0.001 |
| V | 29.3 | 19.1–44.8 | <0.001 | 12.1 | 7.3–19.9 | <0.001 |
| Type of SAH | <0.001 | |||||
| Perimesencephalic/nonaneurysmal | 1.0 | |||||
| Aneurysmal (saccular/fusiform) | 5.8 | 3.5–9.4 | <0.001 | |||
| Intracranial artery dissection | 4.5 | 2.1–9.3 | <0.001 | |||
| Aneurysm location | <0.001 | |||||
| Perimesencephalic/nonaneurysmal | 1.0 | |||||
| Anterior cerebral artery | 3.5 | 2.0–6.3 | <0.001 | |||
| Middle cerebral artery | 3.5 | 1.9–6.5 | <0.001 | |||
| Posterior communicating artery | 4.4 | 2.4–8.2 | <0.001 | |||
| Internal carotid artery | 2.8 | 1.3–6.1 | 0.009 | |||
| Posterior circulation artery | 3.9 | 2.1–7.2 | <0.001 | |||
| Aneurysm size | <0.001 | <0.001 | ||||
| Perimesencephalic/nonaneurysmal | 1.0 | 1.0 | ||||
| 0–4.9 mm | 5.0 | 2.6–8.0 | <0.001 | 2.1 | 1.1–4.2 | 0.03 |
| 5–6.9 mm | 4.0 | 2.3–6.7 | <0.001 | 1.8 | 0.9–3.6 | 0.07 |
| 7–9.9 mm | 4.8 | 2.8–8.4 | <0.001 | 1.9 | 0.9–3.8 | 0.08 |
| 10–19.9 mm | 8.1 | 4.8–14.0 | <0.001 | 3.4 | 1.7–6.7 | 0.001 |
| ≥20 mm | 37.7 | 14.8–95.6 | <0.001 | 18.9 | 6.1–58.3 | <0.001 |
| Nonsaccular | 4.0 | 2.1–7.9 | <0.001 | 2.6 | 1.1–6.0 | 0.03 |
| mFisher grade | <0.001 | <0.001 | ||||
| 0 | 1.0 | 1.0 | ||||
| 1 | 1.2 | 0.6–2.6 | 0.64 | 0.8 | 0.3–1.9 | 0.55 |
| 2 | 2.3 | 1.1–4.9 | 0.03 | 1.1 | 0.4–2.7 | 0.85 |
| 3 | 5.5 | 2.6–11.8 | <0.001 | 1.6 | 0.6–4.3 | 0.30 |
| 4 | 17.4 | 8.7–34.5 | <0.001 | 4.1 | 1.7–9.8 | 0.002 |
| Intracerebral hematoma | 3.7 | 2.7–5.1 | <0.001 | 1.8 | 1.2–2.8 | 0.002 |
| Subdural hematoma | 3.7 | 1.5–9.0 | 0.004 | |||
| Hydrocephalus, required CSF drainage§ | 3.6 | 3.4–3.8 | <0.001 | |||
| Type of treatment (coiling vs clipping) | 0.9 | 0.6–1.2 | 0.36 | |||
aOR = adjusted OR.
Boldface type indicates statistical significance (univariate p < 0.15; multivariate p < 0.5).
从多变量回归效应估计were adjusted for all other variables in the model.
Derived from likelihood tests.
CSF drainage ≤ 24 hours and before treatment.
Sensitivity analysis for outcome after 2 months with the original database including missing covariates (complete case analysis) showed essentially the same results (eTable 6).
Model Performance
Regarding discriminative value, the predictive model derived from the multivariate logistic regression analysis resulted in a pooled AUC of 0.87 (95% CI 0.85–0.89; p < 0.001 [Fig. 2]).
Receiver operating characteristic graph representing the discriminative value of the final pooled prediction model. Figure is available in color online only.
Discussion
In this study, we found that, for the most accurate prediction of outcome after SAH, clinical assessment should be performed after neurological resuscitation. Other predictors in our final model were age, aneurysm size, amount of blood on the initial CT scan, and the presence of an intracranial hematoma.
The rWFNS grade determined in the clinical assessment was identified as the strongest predictor of outcome. The superiority of the rWFNS over the admission WFNS grade on admission is rather easy to understand; after “resuscitation” of the patients by CSF drainage or acute craniotomy, only the patients at a truly poor grade remain in this category (Fig. 1 right). The negative predictive values of a space-occupying intracerebral hematoma, age, aneurysm size, and amount of blood on the initial CT scan have been documented before in rather small series but have not always been adjusted for all covariates.2,9
Because the amount of subarachnoid blood on the initial CT scan as categorized by mFisher grade is an independent predictor, among others, the severity of SAH is not represented by the neurological condition alone. Besides the association between mFisher grade and poor outcome because of the increased incidence of delayed cerebral ischemia,5the higher incidence of rebleeding in patients with a mFisher Grade 3 or 4 also might add to the increased risk.22
In our study population, the percentage of patients with poor outcome may be considered relatively low18because of the inclusion of patients with perimesencephalic SAH. Also, in the 1990s, patients with SAH in very poor clinical condition were not always immediately referred to our hospital, leading to an underestimation of the true mortality rate, especially in Time Frame 1. At first glance, it seemed that outcomes after SAH did not improve during the subsequent time frames (eTable 5). However, when we take a closer look ateTable 4, we find an increasing number of patients in poor neurological condition who were actively being treated, resulting in a significantly larger proportion of patients at WFNS Grade V in the last 2 time frames. In addition, although the patients were older over the past few years, outcomes remained the same, which reflects the advances made at our center in the management of patients with SAH.
Recently, Sano et al.19made a plea for revision of the original WFNS grading scale. Their proposed modified WFNS removed the neurological deficit from the scale and instead discriminated between Glasgow Coma Scale scores 13 and 14. This change was supposed to lead to an overall stronger prediction value for outcome, which would especially result in better discrimination between Grades II and III as they pertain to outcome. It is unfortunate that the differences in outcome between patients at Grade III and those at Grade IV failed to be significant in this study, resulting in less accurate discrimination between patients at a low WFNS grade and those at a higher grade. In addition, as already noted by Wang and Heros,24the presence of serious focal neurological deficits is unquestionably important for clinical outcome, and this was confirmed by our study; patients with WFNS Grade III SAH had a twice-as-high risk of poor outcome as those with WFNS Grade II SAH. In addition, when the rWFNS grade was omitted from the multivariate analysis, the admission WFNS grade emerged as most important predictor in the final model, with gradually ascending odds ratios for each individual grade. In this respect, we agree with Wang and Heros24and argue for the use of the original WFNS scale, but only with the assessment of clinical condition after resuscitation.
An important strength of the present study is the accuracy of the model in predicting outcome, because the discriminative value of our model is substantially higher than that of previous models.12
Furthermore, the model was based on a large and representative group of all types of patients with spontaneous SAH, and only a minimal percentage of patients were lost to follow-up.
Some limitations of our study also need to be addressed. First, our prospectively kept cohort was analyzed retrospectively. Therefore, covariates that have been linked to outcome (e.g., laboratory parameters) could not be analyzed. However, it was our intention to develop a “bedside” grading system. Second, although the use of multiple imputation might be considered a weakness, imputing data is a validated and nowadays frequently used method for accounting for missing data.13Last, in patients who underwent immediate craniotomy for the evacuation of a space-occupying hematoma, the aneurysm was invariably treated concomitantly. In such cases, the prognostic value of the rWFNS grade regarding decision making might be considered of less value, because the rWFNS grade was assessed after aneurysm repair and treatment has already been performed. However, in other neurovascular centers, aneurysm repair is not necessarily performed during surgical evacuation of the hematoma but, rather, endovascularly after improvement of the clinical condition of the patient. In these cases, the rWFNS grade is still of contributing value in the decision-making process.
Conclusions
Clinical assessment should be performed after neurological resuscitation for the most accurate prediction of outcome. The rWFNS grade should be used in further research and clinical practice, which might significantly aid decision making at the early stage and provide more accurate information for patients and their relatives.
References
-
1 ↑
BotterellEH,LougheedWM,ScottJW,VandewaterSL:Hypothermia, and interruption of carotid, or carotid and vertebral circulation, in the surgical management of intracranial aneurysms.J Neurosurg13:1–42,1956
-
2 ↑
BrouwersPJ,DippelDW,VermeulenM,LindsayKW,HasanD,van GijnJ:Amount of blood on computed tomography as an independent predictor after aneurysm rupture.Stroke24:809–814,1993
-
3 ↑
ChiangVL,ClausEB,AwadIA:Toward more rational prediction of outcome in patients with high-grade subarachnoid hemorrhage.开云体育app官方网站下载入口46:28–36,2000
-
4 ↑
ConnollyESJr,RabinsteinAA,CarhuapomaJR,DerdeynCP,DionJ,HigashidaRT,et al.:Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association.Stroke43:1711–1737,2012
-
5 ↑
FronteraJA,ClaassenJ,SchmidtJM,WartenbergKE,TemesR,ConnollyESJr,et al.:Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale.开云体育app官方网站下载入口59:21–27,2006
-
6 ↑
GiraldoEA,MandrekarJN,RubinMN,DupontSA,ZhangY,LanzinoG,et al.:Timing of clinical grade assessment and poor outcome in patients with aneurysmal subarachnoid hemorrhage.J Neurosurg117:15–19,2012
-
7 ↑
GrevingJP,WermerMJH,BrownRDJr,MoritaA,JuvelaS,YonekuraM,et al.:Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies.Lancet Neurol13:59–66,2014
-
8 ↑
HasanD,VermeulenM,WijdicksEF,HijdraA,van GijnJ:Management problems in acute hydrocephalus after subarachnoid hemorrhage.Stroke20:747–753,1989
-
9 ↑
HauerbergJ,EskesenV,RosenørnJ:The prognostic significance of intracerebral haematoma as shown on CT scanning after aneurysmal subarachnoid haemorrhage.Br J Neurosurg8:333–339,1994
-
10 ↑
HaugT,SortebergA,FinsetA,LindegaardKF,LundarT,SortebergW:Cognitive functioning and health-related quality of life 1 year after aneurysmal subarachnoid hemorrhage in preoperative comatose patients (Hunt and Hess Grade V patients).开云体育app官方网站下载入口66:475–485,2010
-
11 ↑
HuntWE,HessRM:Surgical risk as related to time of intervention in the repair of intracranial aneurysms.J Neurosurg28:14–20,1968
-
12 ↑
JajaBN,CusimanoMD,EtminanN,HanggiD,HasanD,IlodigweD,et al.:Clinical prediction models for aneurysmal subarachnoid hemorrhage: a systematic review.Neurocrit Care18:143–153,2013
-
13 ↑
JanssenKJM,DondersART,HarrellFEJr,VergouweY,ChenQ,GrobbeeDE,et al.:Missing covariate data in medical research: to impute is better than to ignore.J Clin Epidemiol63:721–727,2010
-
14 ↑
MilhoratTH:Acute hydrocephalus after aneurysmal subarachnoid hemorrhage.开云体育app官方网站下载入口20:15–20,1987
-
15 ↑
NieuwkampDJ,VaartjesI,AlgraA,BotsML,RinkelGJ:年龄和性别的时间趋势dea的风险th of patients admitted with aneurysmal subarachnoid hemorrhage in the Netherlands.Int J Stroke8:Suppl A10090–94,2013
-
16 ↑
PegoliM,MandrekarJ,RabinsteinAA,LanzinoG:Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage.J Neurosurg122:414–418,2015
-
17 ↑
RansomER,MoccoJ,KomotarRJ,SahniD,ChangJ,HahnDK,et al.:External ventricular drainage response in poor grade aneurysmal subarachnoid hemorrhage: effect on preoperative grading and prognosis.Neurocrit Care6:174–180,2007
-
18 ↑
RinkelGJ,AlgraA:Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage.Lancet Neurol10:349–356,2011
-
19 ↑
SanoH,SatohA,MurayamaY,KatoY,OrigasaH,InamasuJ,et al.:Modified World Federation of Neurosurgical Societies subarachnoid hemorrhage grading system.World Neurosurg83:801–807,2015
-
20 ↑
SteinerT,JuvelaS,UnterbergA,JungC,ForstingM,RinkelG:European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage.Cerebrovasc Dis35:93–112,2013
-
21 ↑
TeasdaleGM,DrakeCG,HuntW,KassellN,SanoK,PertuisetB,et al.:A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies.J Neurol Neurosurg Psychiatry51:1457,1988
-
22 ↑
van DonkelaarCE,BakkerNA,VeegerNJ,UyttenboogaartM,MetzemaekersJD,LuijckxGJ,et al.:Predictive factors for rebleeding after aneurysmal subarachnoid hemorrhage: Rebleeding aneurysmal subarachnoid hemorrhage study.Stroke46:2100–2106,2015
-
23 ↑
van SwietenJC,KoudstaalPJ,VisserMC,SchoutenHJ,van GijnJ:Interobserver agreement for the assessment of handicap in stroke patients.Stroke19:604–607,1988
-
24 ↑
WangA,HerosRC:Perspective on “modified WFNS subarachnoid hemorrhage grading system”.World Neurosurg83:734–736,2015
Disclosures
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Drs. Bakker and Veeger had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Author Contributions
Conception and design: van Dijk. Acquisition of data: van Donkelaar, Bakker, Foumani. Analysis and interpretation of data: van Donkelaar, Bakker, Veeger. Drafting the article: van Donkelaar. Critically revising the article: Bakker, Veeger, Uyttenboogaart, Metzemaekers, Eshghi, Mazuri, Foumani, Luijckx, Groen, van Dijk. Reviewed submitted version of manuscript: Bakker, van Dijk. Approved the final version of the manuscript on behalf of all authors: van Donkelaar. Statistical analysis: van Donkelaar, Bakker, Veeger. Study supervision: Groen, van Dijk. Treatment of patients with SAH: Uyttenboogaart, Metzemaekers, Eshghi, Mazuri, Luijckx, Groen, van Dijk.
Supplemental Information
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eTables and Figure.//www.prize-show.com/doi/suppl/10.3171/2016.1.JNS152136.
