Prediction of Delayed Cerebral Ischemia with Cerebral Angiography: A Meta-Analysis
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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.
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.
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.
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.
KeywordsMeta-analysis Brain ischemia Cerebral vasospasm Cerebral angiography Transcranial Doppler sonography
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.
Source of support
Compliance with Ethical Standards
Conflict of interest
The authors declare that they have no conflict of interest.
- 1.Dorsch NW. Cerebral arterial spasm–a clinical review. Br J Neurosurg. 1995;9(3):403–12.Google Scholar
- 2.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.Google Scholar
- 3.Fergusen S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurdsosurgery. 2007;60(4):658–67.Google Scholar
- 4.Rabinstein AA, Friedman JA, Weigand SD, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2004;35(8):1862–6.Google Scholar
- 5.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.Google Scholar
- 6.Taki W, Sakai N, Suzuki H, Group, P. Determinants of poor outcome after aneurysmal subarachnoid hemorrhage when both clipping and coiling are available: prospective Registry of Subarachnoid Aneurysms Treatment (PRESAT) in Japan. World Neurosurg. 2011;76(5):437–45.Google Scholar
- 7.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.Google Scholar
- 8.Moppett IK, Mahajan RP. Transcranial Doppler ultrasonography in anaesthesia and intensive care. Br J Anaesth. 2004;93(5):710–24.Google Scholar
- 9.Kumar G, Alexandrov AV. Vasospasm surveillance with transcranial Doppler sonography in subarachnoid hemorrhage. J Ultrasound Med. 2015;34(8):1345–50.Google Scholar
- 10.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.Google Scholar
- 11.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.Google Scholar
- 12.Sloan MA, Burch CM, Wozniak MA, et al. Transcranial Doppler detection of vertebrobasilar vasospasm following subarachnoid hemorrhage. Stroke. 1994;25(11):2187–97.Google Scholar
- 13.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.Google Scholar
- 14.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.Google Scholar
- 15.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.Google Scholar
- 16.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.Google Scholar
- 17.Cochrane Study Quality Guide. https://cccrg.cochrane.org/sites/cccrg.cochrane.org/files/public/uploads/StudyQualityGuide_May%202013.pdf. Accessed Oct 2017.
- 18.DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.Google Scholar
- 19.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.Google Scholar
- 20.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.Google Scholar
- 21.Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.Google Scholar
- 22.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.Google Scholar
- 23.Arias EJ, Vajapey S, Reynolds MR, et al. Utility of screening for cerebral vasospasm using digital subtraction angiography. Stroke. 2015;46(11):3137–41.Google Scholar
- 24.Ferguson S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658–67.Google Scholar
- 25.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.Google Scholar
- 26.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.Google Scholar
- 27.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.Google Scholar
- 28.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.Google Scholar
- 29.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.Google Scholar
- 30.Santos GA, Petersen N, Zamani AA, et al. Pathophysiologic differences in cerebral autoregulation after subarachnoid hemorrhage. Neurology. 2016;86(21):1950–6.Google Scholar
- 31.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.Google Scholar
- 32.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.Google Scholar
- 33.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.Google Scholar
- 34.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.Google Scholar
- 35.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.Google Scholar
- 36.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.Google Scholar
- 37.Li ZQ, Wang QH, Chen G, Quan Z. Outcomes of endovascular coiling versus surgical clipping in the treatment of ruptured intracranial aneurysms. J Int Med Res. 2012;40(6):2145–51.Google Scholar
- 38.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.Google Scholar
- 39.Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58.Google Scholar
- 40.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.Google Scholar
- 41.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.Google Scholar