Abstract
Object
Cerebral catheter angiography is the gold standard for diagnosing cerebral artery vasospasm (vasospasm) in aneurysmal subarachnoid hemorrhage (SAH). We have previously published a meta-analysis of prediction of delayed cerebral ischemia (DCI) from transcranial Doppler (TCD) evidence of vasospasm. Analogous data relating to prediction of DCI have not been previously collated for cerebral angiography nor reconciled against TCD.
Methods
We searched PUBMED, the Cochrane database, and clinicaltrials.gov for studies that used cerebral angiography for diagnosis of vasospasm and evaluated DCI in patients with SAH. We performed a random-effects meta-analysis of prediction of DCI with cerebral angiography, reconciling its accuracy against that of TCD. We also report quality of evidence for the value of cerebral angiography and TCD in SAH based on pooled data from our meta-analyses.
Results
A total of 15 studies (n = 5463) were included in the meta-analysis. Sensitivity (SN), specificity (SP), positive predictive value (PPV), and negative predictive value (NPV) of cerebral angiography for prediction of DCI are 57, 68, 32, and 90%. These metrics for TCD, based on our previous meta-analysis, are 90, 71, 57, and 92%. We report that test accuracy estimates are “moderate” for TCD and “low” for angiography based on pooled data from our meta-analyses.
Conclusion
TCD evidence of vasospasm is a better predictor of DCI than angiographic vasospasm. Future comparative effectiveness studies can better define the value of these diagnostic tools in patients with SAH.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12028-018-0572-2/MediaObjects/12028_2018_572_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12028-018-0572-2/MediaObjects/12028_2018_572_Fig2_HTML.png)
Similar content being viewed by others
References
Dorsch NW. Cerebral arterial spasm–a clinical review. Br J Neurosurg. 1995;9(3):403–12.
Adams HP Jr, Kassell NF, Torner JC, Haley EC Jr. Predicting cerebral ischemia after aneurysmal subarachnoid hemorrhage: influences of clinical condition, CT results, and antifibrinolytic therapy. A report of the Cooperative Aneurysm Study. Neurology. 1987;37(10):1586–91.
Fergusen S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurdsosurgery. 2007;60(4):658–67.
Rabinstein AA, Friedman JA, Weigand SD, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2004;35(8):1862–6.
Vergouwen MD. Participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage. Vasospasm versus delayed cerebral ischemia as an outcome event in clinical trials and observational studies. Neurocrit Care. 2011;15(2):308–11.
Taki W, Sakai N, Suzuki H, Group, P. Determinants of poor outcome after aneurysmal subarachnoid hemorrhage when both clip** and coiling are available: prospective Registry of Subarachnoid Aneurysms Treatment (PRESAT) in Japan. World Neurosurg. 2011;76(5):437–45.
Etminan N, Vergouwen MD, Ilodigwe D, Macdonald RL. Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2011;31(6):1443–51.
Moppett IK, Mahajan RP. Transcranial Doppler ultrasonography in anaesthesia and intensive care. Br J Anaesth. 2004;93(5):710–24.
Kumar G, Alexandrov AV. Vasospasm surveillance with transcranial Doppler sonography in subarachnoid hemorrhage. J Ultrasound Med. 2015;34(8):1345–50.
Lindegaard KF, Bakke SJ, Grolimund P, et al. Assessment of intracranial hemodynamics in carotid artery disease by transcranial Doppler ultrasound. J Neurosurg. 1985;63(6):890–8.
Sloan MA, Haley EC Jr, Kassell NF, et al. Sensitivity and specificity of transcranial Doppler ultrasonography in the diagnosis of vasospasm following subarachnoid hemorrhage. Neurology. 1989;39(11):1514–8.
Sloan MA, Burch CM, Wozniak MA, et al. Transcranial Doppler detection of vertebrobasilar vasospasm following subarachnoid hemorrhage. Stroke. 1994;25(11):2187–97.
Burch CM, Wozniak MA, Sloan MA, et al. Detection of intracranial internal carotid artery and middle cerebral artery vasospasm following subarachnoid hemorrhage. J Neuroimaging. 1996;6(1):8–15.
Wozniak MA, Sloan MA, Rothman MI, et al. Detection of vasospasm by transcranial Doppler sonography. The challenges of the anterior and posterior cerebral arteries. J Neuroimaging. 1996;6(2):87–93.
Kumar G, Shahripour RB, Harrigan MR. Vasospasm on transcranial Doppler is predictive of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Neurosurg. 2016;124(5):1257–64.
Moher D, Liberati A, Tetzlaff J, Altman DG, Group, P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
Cochrane Study Quality Guide. https://cccrg.cochrane.org/sites/cccrg.cochrane.org/files/public/uploads/StudyQualityGuide_May%202013.pdf. Accessed Oct 2017.
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.
Huedo-Medina TB, Sanchez-Meca J, Marin-Martinez F, Botella J. Assessing heterogeneity in meta-analysis: Q statistic or I 2 index? Psychol Methods. 2006;11(2):193–206.
Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.
Bax L, Yu LM, Ikeda N, Tsuruta H, Moons KG. Development and validation of MIX: comprehensive free software for meta-analysis of causal research data. BMC Med Res Methodol. 2006;6:50.
Arias EJ, Vajapey S, Reynolds MR, et al. Utility of screening for cerebral vasospasm using digital subtraction angiography. Stroke. 2015;46(11):3137–41.
Ferguson S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658–67.
Killeen RP, Mushlin AI, Johnson CE, et al. Comparison of CT perfusion and digital subtraction angiography in the evaluation of delayed cerebral ischemia. Acad Radiol. 2011;18(9):1094–100.
Matsuda N, Naraoka M, Ohkuma H, et al. Effect of cilostazol on cerebral vasospasm and outcome in patients with aneurysmal subarachnoid hemorrhage: a randomized, double-blind, placebo-controlled trial. Cerebrovasc Dis. 2016;42(1–2):97–105.
Ohman J, Servo A, Heiskanen O. Risks factors for cerebral infarction in good-grade patients after aneurysmal subarachnoid hemorrhage and surgery: a prospective study. J Neurosurg. 1991;74(1):14–20.
Otite F, Mink S, Tan CO, et al. Impaired cerebral autoregulation is associated with vasospasm and delayed cerebral ischemia in subarachnoid hemorrhage. Stroke. 2014;45(3):677–82.
Proust F, Debono B, Gerardin E, et al. Angiographic cerebral vasospasm and delayed ischemic deficit on anterior part of the circle of Willis. Usefulness of transcranial Doppler. Neurochirurgie. 2002;48(6):489–99.
Santos GA, Petersen N, Zamani AA, et al. Pathophysiologic differences in cerebral autoregulation after subarachnoid hemorrhage. Neurology. 2016;86(21):1950–6.
Schmidt JM, Wartenberg KE, Fernandez A, et al. Frequency and clinical impact of asymptomatic cerebral infarction due to vasospasm after subarachnoid hemorrhage. J Neurosurg. 2008;109(6):1052–9.
Shimoda M, Takeuchi M, Tominaga J, et al. Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: serial magnetic resonance imaging. Neurosurgery. 2001;49(6):1341–8.
Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and-independent effects. Stroke. 2011;42(4):924–9.
Weidauer S, Lanfermann H, Raabe A, et al. Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke. 2007;38(6):1831–6.
Brown RJ, Kumar A, Dhar R, Sampson TR, Diringer MN. The relationship between delayed infarcts and angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2013;72(5):702–7.
Dehdashti AR, Mermillod B, Rufenacht DA, Reverdin A, de Tribolet N. Does treatment modality of intracranial ruptured aneurysms influence the incidence of cerebral vasospasm and clinical outcome? Cerebrovasc Dis. 2004;17(1):53–60.
Li ZQ, Wang QH, Chen G, Quan Z. Outcomes of endovascular coiling versus surgical clip** in the treatment of ruptured intracranial aneurysms. J Int Med Res. 2012;40(6):2145–51.
Schünemann H, Brozek J, Guyatt G, Oxman A, GRADE handbook for grading quality of evidence and strength of recommendations, ed. T.G.W. Group 2013, guidelinedevelopment.org/handbook.
Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58.
Wardlaw JM, Offin R, Teasdale GM, Teasdale EM. Is routine transcranial Doppler ultrasound monitoring useful in the management of subarachnoid hemorrhage? J Neurosurg. 1998;88(2):272–6.
Venkatraman A, Khawaja AM, Gupta S, et al. Intra-arterial vasodilators for vasospasm following aneurysmal subarachnoid hemorrhage: a meta-analysis. J Neurointerv Surg. 2018;10(4):380–7.
Funding
None.
Author information
Authors and Affiliations
Contributions
GK contributed to study conception, design, acquisition of data, analysis, statistical analysis, writing of manuscript, critical revision, study supervision, and final approval. OMD helped in acquisition of data, analysis, writing of manuscript, critical revision, and final approval. CCC contributed to acquisition of data, analysis, writing of manuscript, critical revision, and final approval. COC involved in analysis, supervision, writing and critical revision, and final approval. AVA helped in analysis, supervision, writing and critical revision, and final approval.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kumar, G., Dumitrascu, O.M., Chiang, CC. et al. Prediction of Delayed Cerebral Ischemia with Cerebral Angiography: A Meta-Analysis. Neurocrit Care 30, 62–71 (2019). https://doi.org/10.1007/s12028-018-0572-2
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12028-018-0572-2