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Original Paper

Free Access

Early Vasospasm after Aneurysmal Subarachnoid Hemorrhage Predicts the Occurrence and Severity of Symptomatic Vasospasm and Delayed Cerebral Ischemia

Jabbarli R.a, e · Reinhard M.b · Shah M.a · Roelz R.a · Niesen W.-D.b · Kaier K.c · Taschner C.d · Weyerbrock A.a · Van Velthoven V.a, f

Author affiliations

aDepartment of Neurosurgery, bDepartment of Neurology, cInstitute for Medical Biometry and Medical Informatics, and dDepartment of Neuroradiology, University Medical Center Freiburg, Freiburg im Breisgau, and eDepartment of Neurosurgery, University Hospital Essen, Essen, Germany; fDepartment of Neurosurgery, Universitair Ziekenhuis Brussel, Brussels, Belgium

Corresponding Author

Ramazan Jabbarli, MD

Department of Neurosurgery

University Medical Center Freiburg

DE-79106 Freiburg im Breisgau (Germany)

E-Mail ramazan.jabbarli@uniklinik-freiburg.de

Related Articles for ""

Cerebrovasc Dis 2016;41:265-272

Abstract

Background: Cerebral vasospasm usually develops several days after subarachnoid hemorrhage (SAH) and is generally acknowledged as a strong outcome predictor. In contrast, much less is known about the nature and eventual consequences of early angiographic vasospasm (EAVS) seen on admission digital subtraction angiography (DSA). Therefore, we aimed at identifying the risk factors and clinical impact of EAVS after SAH. Methods: Five hundred and thirty-one SAH patients with admission DSA performed within 72 h after the bleeding event were selected from a comprehensive database containing all consecutive SAH patients treated at our institution between January 2005 and December 2012. Predictors of EAVS, as well as associations between EAVS and delayed vasospasm-related complications, and unfavorable outcome (defined as modified Rankin scale >3) were evaluated in univariate and multivariate analyses. Results: EAVS was seen on 60 DSAs (11.3%) and was independently correlated with delayed symptomatic vasospasm requiring intra-arterial spasmolysis (OR 5.24, p < 0.0001), angioplasty (OR 2.56, p = 0.015) and repetitive endovascular treatment (OR 4.71, p < 0.0001). EAVS also increased the risk for multiple versus single territorial infarction on the follow-up CT scan(s) (OR 2.04, p = 0.047) and independently predicted unfavorable outcome (OR 2.93, p = 0.008). The presence of radiographic signs suspicious for fibromuscular dysplasia were independently associated with the occurrence of EAVS (OR 2.98, p = 0.026) and the need for repetitive endovascular vasospasm treatment (OR 3.95, p = 0.019). Conclusions: In view of the strong correlation with delayed symptomatic vasospasm and its ischemic complications, EAVS can be considered an alerting signal for severe symptomatic vasospasm. Therefore, more attention should be paid to the presence of EAVS on admission DSA.

© 2016 S. Karger AG, Basel


Introduction

Although angiographic vasospasm following aneurysmal subarachnoid hemorrhage (SAH) has been described over 60 years ago [1], its true significance for the clinical course and outcome of SAH is still under debate [2].

Cerebral vasospasm usually develops between 4 and 12 days after the bleeding event [3]. It correlates with delayed cerebral infarction [4] and is a major source of morbidity and mortality of SAH patients [5]. Besides this ‘typical' form of cerebral vasospasm, there is also a so-called early angiographic vasospasm (EAVS) that can be visualized on admission angiography in about 1 out of 10 SAH patients [6,7].

Although the EAVS phenomenon after SAH is not so unusual, it has been poorly investigated to date. There is an opinion that EAVS might reflect a residual level of vasoconstriction related to the bleeding event [6,7,8]. As to EAVS predictors, only admission Glasgow coma scores <14 and admission sodium >138 mmol/l have shown independent correlations with the occurrence of EAVS [7]. However, these parameters do not allow any causative conclusions.

EAVS has been reported to correlate with the functional outcome of SAH [6,7,9], but the correlation between EAVS and delayed symptomatic vasospasm could not be proven [6]. Therefore, the possible mechanism underlying the clinical impact of EAVS is still controversial.

In the present study, we aimed at identifying the associations between EAVS and the occurrence and severity of symptomatic vasospasm and delayed cerebral ischemia (DCI). We also focused on independent risk factors for EAVS.

Materials and Methods

Patient Population

Patients were selected from our clinical database containing all consecutive patients with SAH treated at our institution between January 2005 and December 2012. Inclusion criteria were the following: (1) SAH from untreated and ruptured aneurysm and (2) admission digital subtraction angiography (DSA) performed within 72 h after the bleeding event.

The study was approved by the Institutional Ethics Committee (Ethik-Kommission, Albert-Ludwigs-Universität Freiburg, registration number: 446/13). All persons or their relatives gave their informed consent within the treatment contract after admission to hospital. The study was performed within the clinical trial registered in the German clinical trial register (DRKS, unique identifier DRKS00005486, http://www.drks.de/).

SAH Management

All patients were admitted and initially treated in our neurointensive care unit. After interdisciplinary assessment, the ruptured aneurysm was treated either by coiling or by clipping. Acute hydrocephalus was treated with external ventricular drainage (EVD). All patients underwent at least 1 post-treatment CT scan; additional CT scans were performed upon clinical indications.

Vasospasm Management

Transcranial Doppler (TCD) ultrasound was performed once a day for the period of 3 weeks. The cutoff for absolute mean flow velocities indicative for clinically relevant vasospasm was set at 160 cm/s. Oral nimodipine (360 mg/day) and maintenance of euvolemia was obligatory in all patients. In cases of vasospasm on TCD, the conservative management was enhanced by induced hypertension (providing the mean arterial pressure over 90 mm Hg). In the following cases, patients underwent DSA for verification of vasospasm and, if necessary, therapy: (a) clinical deterioration not explained by other complications and (b) consecutive increase of TCD velocities over the abovementioned cutoff despite conservative management, especially in unconscious patients. Accordingly, the cases with angiographically documented vasospasm that were consistent with clinical deterioration not explained by other causes (re-bleeding, hydrocephalus, etc.) were defined as ‘symptomatic vasospasm'. Endovascular treatment of symptomatic vasospasm consisted primarily of intra-arterial application of vasodilators (papaverine and/or nimodipine). In case of inefficacy of these vasodilators, patients additionally underwent angioplasty. In case of persisting vasospasm (judged upon clinical symptoms and/or TCD observations), repetitive endovascular treatments were performed. Therefore, the severity of symptomatic vasospasm was judged upon the need for angioplasty and/or repetitive endovascular treatments. The detailed description of clinical management of SAH patients at our institution has already been reported previously [9,10,11].

Data Management

Various demographic and clinical parameters of the patients were collected from electronic medical records: age, sex, preexisting morbidity, laboratory measurements at admission (white blood cell count, blood sugar and hemoglobin), initial clinical grade according to Hunt and Hess [12], treatment modality, certain clinical events of the postoperative course (need for decompressive craniectomy, vasospasm on TCD and symptomatic vasospasm requiring endovascular treatment), as well as the functional outcome at discharge and at 6 months after SAH according to modified Rankin scale (mRS) [13]. Hunt and Hess grade was dichotomized into good (1-3) and poor (4 and 5) grade, mRS score into favorable (1-3) and unfavorable (4-6) outcome.

The following radiographic data of patients were also collected for the present study:

- The severity of SAH was evaluated according to the original Fisher score [14] with dichotomization into low (1 or 2) and high (3 or 4) grades; the presence of intracerebral hematoma (ICH) was recorded as a separate variable; moreover, intraventricular hemorrhage (IVH) was assessed in a dichotomized (present/absent) and quantitative manner using the original Graeb score [15];

- The radiographic evidence of DCI was evaluated upon the new cerebral infarctions in follow-up CT scans up to 6 weeks post-SAH, which were reviewed by the first author (R.J.) blinded at that time for any clinical information. Hypodensities resulting from ICH, EVD or surgical approach were excluded. The development of multiple territorial infarctions was additionally addressed;

- The admission DSA reports were reviewed with regard to the location and size of ruptured aneurysm. In addition, the presence of an unequivocal narrowing of the arterial vessel lumen on the admission DSA not attributable to an intrinsic disease (such as arteriosclerosis) was defined as EAVS, whereas the cases with isolated catheter-induced vasospasm (associated with the catheter placement into the proximal internal carotid or vertebral arteries and restricted to these vessels) were not accounted. Finally, abnormal angiographic findings indicative for the presence of a systemic vascular pathology were also recorded in the database according to the original assessment and interpretation of the reporting neuroradiologists.

Statistical Analysis

Data analysis was performed with use of PRISM (version 5.0, GraphPad Software Inc., San Diego, Calif., USA) and SPSS (version 21, SPSS Inc., IBM, Chicago, Ill., USA) statistical software. Differences with p values <0.05 were considered statistically significant. For univariate correlations, differences between continuous variables were analyzed using the Student t test for normally distributed data and the Mann-Whitney U test for non-normally distributed data; associations between categorical variables were analyzed using the chi-square or Fisher exact tests, as appropriate.

In order to detect EAVS predictors, all parameters present at the time of admission DSA were first tested in the univariate analysis. Then, variables with p value <0.1 were included into the multivariate logistic regression analysis.

The associations between EAVS and delayed vasospasm-related complications and functional outcome were also evaluated stepwise in univariate and multivariate manner. The significant correlations from univariate analyses with p values <0.05 were then evaluated in a multivariate analysis.

Results

Patient Population

Between January 2005 and December 2012, 531 individuals with acute SAH and admission DSA performed within 72 h after the bleeding event were treated at our institution and therefore included to the final analysis. The mean age of the cohort was 55.4 years (range 21-94 years), 332 patients (62.5%) were females. Unfavorable outcome at discharge was observed in 296 cases (55.7%), including 85 patients with in-hospital mortality (16%). At 6-months' follow-up, the number of patients with unfavorable outcome decreased by 86 cases (n = 210, 39.5%).

EAVS: Incidence and Risk Factor(s)

In 60 admission DSAs (11.3%), angiographic vasospasm was identified (fig. 1). Different admission variables were correlated with the occurrence of EAVS (table 1). Univariate analysis showed significant correlations between EAVS and typical angiographic characteristics of fibromuscular dysplasia (FMD) in extracranial carotid and/or vertebral arteries (p = 0.0095, observed in 4.3% of patients (n = 23/531), predominantly females (n = 20/23, 87%); fig. 2), as well as a trend toward higher rates of EAVS among patients with higher Hunt and Hess (p = 0.0726) and Fisher grades (p = 0.0786). These 3 parameters were included in the multivariate analysis of EAVS predictors (table 2). However, FMD remained the only significant risk factor for EAVS in the multivariate correlation (OR 2.98, p = 0.026). In addition, SAH patients with angiographic signs of FMD also showed an independent correlation with the need for repetitive endovascular treatments for delayed symptomatic vasospasm (OR 3.95, p = 0.019; online suppl. table e1; for all online suppl. material, see www.karger.com/doi/10.1159/000443744).

Table 1

Univariate correlations of predictors for EAVS

http://www.karger.com/WebMaterial/ShowPic/492777

Table 2

Multivariate analysis for predictors of EAVS

http://www.karger.com/WebMaterial/ShowPic/492776

Fig. 1

Admission DSA of 2 patients with EAVS.

http://www.karger.com/WebMaterial/ShowPic/492773

Fig. 2

Admission DSA (2 different cases) with angiographic signs of FMD in extracranial carotid arteries.

http://www.karger.com/WebMaterial/ShowPic/492772

EAVS as a Predictor of Delayed Ischemic Complications and Functional Outcome

During the course of the disease, symptomatic vasospasm requiring endovascular intervention occurred in 86 patients (16%). The first intra-arterial spasmolysis was performed on the median post-SAH day 9 (±3.7 days). Cerebral infarction was documented in 250 patients (47%).

Univariate analyses (table 3) showed significant associations between EAVS and the occurrence of delayed symptomatic vasospasm requiring endovascular treatment, vasospasm-related ischemic complications and outcome. The occurrence of vasospasm on TCD was not more common in individuals developing EAVS.

Table 3

Univariate correlations between the presence of EAVS and the clinical course of SAH

http://www.karger.com/WebMaterial/ShowPic/492775

In summary, both univariate and multivariate analyses showed significant correlations between EAVS and:

- The risk for multiple territorial versus single territorial infarctions (OR 2.04, p = 0.047);

- The need for endovascular vasospasm treatment with vasodilators (OR 5.24, p < 0.0001);

- The need for endovascular vasospasm treatment with angioplasty (OR 2.56, p = 0.015);

- The need for repetitive endovascular treatments of vasospasm (OR 4.71, p < 0.0001; online suppl. tables e2, e3, e4 and e5, respectively).

Of note, EAVS was superior to vasospasm on TCD with regard to the prediction of delayed symptomatic angiographic vasospasm.

In the multivariate analysis, EAVS showed an independent predictive value for functional outcome (OR 2.93, p = 0.008; table 4). Finally, SAH patients with EAVS had significantly lower rates of clinical improvement (i.e., any decrease in mRS-score) at 6 months' clinical follow-up (OR 0.38, p = 0.0018; table 3).

Table 4

Multivariate analysis for predictors of unfavorable outcome

http://www.karger.com/WebMaterial/ShowPic/492774

Discussion

In this large monocentric series of SAH patients, we identified the strong correlation between the following angiographic findings: the presence of FMD and EAVS on admission DSA and development of late intractable angiographic vasospasm. EAVS independently predicted the functional outcome of SAH through the unambiguous associations with delayed symptomatic vasospasm and ischemic complications.

Etiology of EAVS

The definite etiology and risk factors for the development of EAVS are still unknown. It has been assumed that the magnitude of initial brain injury may contribute to the development of very early angiographic changes [7]. Elevated intracranial pressure and release of vasoactive products after severe brain injury could also have an impact on the occurrence of EAVS [7]. Finally, there is the possibility that EAVS actually represents delayed vasospasm from a prior undiagnosed SAH or an even more remote SAH after which the arteries did not return to normal diameter [6].

The question of possible clinical predictors of EAVS has already been addressed previously; poor initial clinical condition [6,7], serum sodium >138 mmol/l [6,7], different variables describing the severity of SAH on the initial CT scan (ICH, IVH and thick basal subarachnoid clot) [6,7], larger aneurysms [6,7], the history of SAH [6,7] and arterial hypertension [6,7] were reported to be associated with the occurrence of EAVS. However, many of these parameters do not allow any causative conclusions. In addition, the independent predictive value of most of these variables remains unclear.

In our monocentric series, morphologic signs indicative of FMD on admission DSA were the only predictor of EAVS (independently from the initial clinical condition and the severity of SAH). Moreover, the presence of FMD was also associated with sustained delayed vasospasm requiring repetitive endovascular treatment. Hence, our data, although of retrospective nature, explicitly show the strong correlation between the presence of an angiopathy risk factor (FMD) and the predisposition to severe symptomatic vasospasms. To date, age-related changes of the intracranial vasculature have been intensively discussed as important factors influencing the probability and severity of vasospasm [10]. Our data on correlation between FMD and severe vasospasm underlines the crucial role of anatomic and functional condition of vessels for the development and severity of symptomatic vasospasm after SAH.

FMD is an idiopathic, segmental, non-atherosclerotic arteriopathy that generally affects small- to medium-sized arteries [16,17]. Patients with FMD are known to be predisposed to spontaneous dissections, intracranial aneurysms and carotid cavernous fistulae [16]. The possible predisposition of FMD patients to the development of sustained vascular spasms has been discussed previously [16,18,19,20]. Castellano et al. [18] described a clinical case of severe coronary vasospasm attributable to FMD. The susceptibility of intracranial vasculature to symptomatic vasospasms in FMD patients suffering aneurysmal bleeding has also been reported [16,21,22,23]. Overall, the data regarding possible associations between FMD and post-SAH vasospasm are very limited to date and only based on case reports.

Based on our present results, the macrovascular status on admission, particularly the presence of FMD, may represent an essential biomarker in the early stratification of SAH patients for the risk of symptomatic vasospasm.

Early Vasospasm Strongly Predicts Delayed Symptomatic Vasospasm and DCI

All previous publications uniquely point to the high risk of poor functional outcome in patients developing EAVS after aneurysm rupture [6,7,9]. Furthermore, strong associations between EAVS with early [9] and delayed [6,11] cerebral infarctions could also be shown. In particular, EAVS was included to a risk score (BEHAVIOR score) for prediction of cerebral infarction after SAH in our recent publication [11]. Our present extended analysis shows the dramatic impact of EAVS on the occurrence of DCI in SAH patients. EAVS not only predicted the occurrence of DCI as such. EAVS also significantly increased the likelihood of multiple territorial infarctions (vs. mono-territorial infarctions). This strong correlation between EAVS and DCI is likely to be responsible for the significant impact of EAVS on the functional outcome of SAH.

The currently available data [6,7] on the association between EAVS and delayed symptomatic vasospasm delivers conflicting results. In particular, Qureshi et al. [7] found that EAVS was associated with increased risk of symptomatic vasospasm. However, Baldwin et al. [6] could not confirm this association in their report.

Our data can clarify the question of the correlation between early and delayed vasospasm, which is discrepant to date. We could not only confirm the strong correlation between early and late vasospasm. We also identified the correlation between the early vasospasm with the severity and duration of delayed symptomatic vasospasm (need for additional angioplasty and repetitive spasmolysis). Interestingly, EAVS was even superior to vasospasm on TCD with regard to the prediction of delayed symptomatic vasospasm requiring endovascular treatment.

This strong correlation between early and late angiographic vasospasm suggests a common nature in these 2 vasospastic events. EAVS can likely introduce the initial (albeit ‘harmless', but alerting) phase of ultimately symptomatic vasospasm. Therefore, SAH patients with vasospasm on admission DSA, particularly those with a decreased level of consciousness, regardless the presence of vasospasm on TCD, could benefit from preventive (even repeated) angiographic visualization(s) of the intracranial vasculature during the critical phase of disease, that is, between the end of the first and the second weeks of SAH.

To sum up the novel findings, our data point to the probably essential role of the macrovascular status for the predisposition to EAVS and severe delayed symptomatic vasospasm. Moreover, we could not only confirm the strong correlation between EAVS and delayed vasospasm. We also identified EAVS as an independent predictor of the severity of delayed vasospasm and the severity of DCI after SAH.

Study Limitations

The retrospective nature of this study limits the accuracy of the assessed risk factors. In addition, the question of the radiographic reliability and clinical generalizability of the diagnosis of FMD in the investigated cohort must also be acknowledged. So, other clinical findings indicative for FMD could not be found in the medical records for any of the patients with the signs of FMD on DSA. However, FMD is known for its distinct radiographic pattern that usually makes biopsy unnecessary [23]. In healthy individuals, FMD has usually an asymptomatic clinical course [24] that explains the absence of previous clinical correlates to radiographic evidence of FMD in our cohort. In addition, the reported incidence (4.3%) and female prevalence of FMD are in line with other large angiographic studies [24].

Then, besides the first routine post-treatment imaging, later follow-up CT scans were performed only upon clinical indications. This might have led to a detection bias in favor of patients with worse clinical condition, as well as underestimation of delayed asymptomatic infarctions [11].

Moreover, there is increasing evidence in the literature on the diagnostic value of perfusion CT imaging in the management of DCI [25,26]. However, this diagnostic modality has not been used in our clinic in the described observational period. Therefore, we could not assess the value of perfusion CT imaging in SAH upon our cohort.

Finally, in order to preserve the representative number of SAH patients, we did not limit the time frame for EAVS to 48 h and included all individuals with admission DSA performed within 72 h after the aneurysmal bleeding. However, this 72-hour cutoff still allows the differentiation between early and ‘classical' (delayed) cerebral vasospasm since the latter occurs between days 4 and 12 after SAH [3].

Conclusions

EAVS after aneurysm rupture is a reliable and early predictor for delayed symptomatic vasospasm requiring endovascular treatment, frequently in a repetitive manner. EAVS strongly increases the risk for DCI, especially multiple territorial infarctions. Therefore, EAVS is uniquely associated with poor functional outcome and limited clinical improvement. SAH individuals with macrovascular changes on DSA compatible with FMD show a significant predisposition to the development of early and severe delayed symptomatic vasospasm.

Sources of Funding/Disclosures

None.


References

  1. Ecker A, Riemenschneider PA: Arteriographic evidence of spasm in cerebral vascular disorders. Neurology 1953;3:495-502.
  2. Loch Macdonald R: Vasospasm: my first 25 years-what worked? What didn't? What next? Acta Neurochir Suppl 2015;120:1-10.
    External Resources
  3. Heros RC, Zervas NT, Varsos V: Cerebral vasospasm after subarachnoid hemorrhage: an update. Ann Neurol 1983;14:599-608.
  4. Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, Ruefenacht D, Schmiedek P, Weidauer S, Pasqualin A, Macdonald RL: Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke 2011;42:919-923.
  5. Adamczyk P, He S, Amar AP, Mack WJ: Medical management of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a review of current and emerging therapeutic interventions. Neurol Res Int 2013;2013:462491.
  6. Baldwin ME, Macdonald RL, Huo D, Novakovic RL, Goldenberg FD, Frank JI, Rosengart AJ: Early vasospasm on admission angiography in patients with aneurysmal subarachnoid hemorrhage is a predictor for in-hospital complications and poor outcome. Stroke 2004;35:2506-2511.
  7. Qureshi AI, Sung GY, Suri MA, Straw RN, Guterman LR, Hopkins LN: Prognostic value and determinants of ultraearly angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 1999;44:967-973; discussion 973-974.
  8. Schmidt JM, Rincon F, Fernandez A, Resor C, Kowalski RG, Claassen J, Connolly ES, Fitzsimmons BF, Mayer SA: Cerebral infarction associated with acute subarachnoid hemorrhage. Neurocrit Care 2007;7:10-17.
  9. Jabbarli R, Reinhard M, Niesen WD, Roelz R, Shah M, Kaier K, Hippchen B, Taschner C, Van Velthoven V: Predictors and impact of early cerebral infarction after aneurysmal subarachnoid hemorrhage. Eur J Neurol 2015;22:941-947.
  10. Jabbarli R, Glasker S, Weber J, Taschner C, Olschewski M, Van Velthoven V: Predictors of severity of cerebral vasospasm caused by aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 2013;22:1332-1339.
  11. Jabbarli R, Reinhard M, Roelz R, Shah M, Niesen WD, Kaier K, Taschner C, Weyerbrock A, Van Velthoven V: Early identification of individuals at high risk for cerebral infarction after aneurysmal subarachnoid hemorrhage: the BEHAVIOR score. J Cereb Blood Flow Metab 2015;35:1587-1592.
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  23. O'Shaughnessy BA, Eddleman C, Bendok BR, Parkinson RJ, Awad IA, Batjer HH: Ruptured superior cerebellar artery aneurysm in a child with bilateral fibromuscular hyperplasia of the renal arteries: case report and review of the literature. J Neurosurg 2005;102(3 suppl):338-341.
  24. Olin JW, Sealove BA: Diagnosis, management, and future developments of fibromuscular dysplasia. J Vasc Surg 2011;53:826-836.e1.
  25. Etminan N, Beseoglu K, Heiroth HJ, Turowski B, Steiger HJ, Hanggi D: Early perfusion computerized tomography imaging as a radiographic surrogate for delayed cerebral ischemia and functional outcome after subarachnoid hemorrhage. Stroke 2013;44:1260-1266.
  26. Tsuang FY, Chen JY, Lee CW, Li CH, Lee JE, Lai DM, Hu FC, Tu YK, Hsieh ST, Wang KC: Risk profile of patients with poor-grade aneurysmal subarachnoid hemorrhage using early perfusion computed tomography. World Neurosurg 2012;78:455-461.

Author Contacts

Ramazan Jabbarli, MD

Department of Neurosurgery

University Medical Center Freiburg

DE-79106 Freiburg im Breisgau (Germany)

E-Mail ramazan.jabbarli@uniklinik-freiburg.de


Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: August 10, 2015
Accepted: December 30, 2015
Published online: February 03, 2016
Issue release date: April 2016

Number of Print Pages: 8
Number of Figures: 2
Number of Tables: 4

ISSN: 1015-9770 (Print)
eISSN: 1421-9786 (Online)

For additional information: https://www.karger.com/CED


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References

  1. Ecker A, Riemenschneider PA: Arteriographic evidence of spasm in cerebral vascular disorders. Neurology 1953;3:495-502.
  2. Loch Macdonald R: Vasospasm: my first 25 years-what worked? What didn't? What next? Acta Neurochir Suppl 2015;120:1-10.
    External Resources
  3. Heros RC, Zervas NT, Varsos V: Cerebral vasospasm after subarachnoid hemorrhage: an update. Ann Neurol 1983;14:599-608.
  4. Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, Ruefenacht D, Schmiedek P, Weidauer S, Pasqualin A, Macdonald RL: Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke 2011;42:919-923.
  5. Adamczyk P, He S, Amar AP, Mack WJ: Medical management of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a review of current and emerging therapeutic interventions. Neurol Res Int 2013;2013:462491.
  6. Baldwin ME, Macdonald RL, Huo D, Novakovic RL, Goldenberg FD, Frank JI, Rosengart AJ: Early vasospasm on admission angiography in patients with aneurysmal subarachnoid hemorrhage is a predictor for in-hospital complications and poor outcome. Stroke 2004;35:2506-2511.
  7. Qureshi AI, Sung GY, Suri MA, Straw RN, Guterman LR, Hopkins LN: Prognostic value and determinants of ultraearly angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 1999;44:967-973; discussion 973-974.
  8. Schmidt JM, Rincon F, Fernandez A, Resor C, Kowalski RG, Claassen J, Connolly ES, Fitzsimmons BF, Mayer SA: Cerebral infarction associated with acute subarachnoid hemorrhage. Neurocrit Care 2007;7:10-17.
  9. Jabbarli R, Reinhard M, Niesen WD, Roelz R, Shah M, Kaier K, Hippchen B, Taschner C, Van Velthoven V: Predictors and impact of early cerebral infarction after aneurysmal subarachnoid hemorrhage. Eur J Neurol 2015;22:941-947.
  10. Jabbarli R, Glasker S, Weber J, Taschner C, Olschewski M, Van Velthoven V: Predictors of severity of cerebral vasospasm caused by aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 2013;22:1332-1339.
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