Log in

Prediction of Delayed Cerebral Ischemia with Cerebral Angiography: A Meta-Analysis

  • Original Article
  • Published:
Neurocritical Care Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Dorsch NW. Cerebral arterial spasm–a clinical review. Br J Neurosurg. 1995;9(3):403–12.

    Article  CAS  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.

    Article  Google Scholar 

  3. Fergusen S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurdsosurgery. 2007;60(4):658–67.

    Article  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.

    Article  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.

    Article  Google Scholar 

  6. 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.

    Article  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.

    Article  CAS  Google Scholar 

  8. Moppett IK, Mahajan RP. Transcranial Doppler ultrasonography in anaesthesia and intensive care. Br J Anaesth. 2004;93(5):710–24.

    Article  CAS  Google Scholar 

  9. Kumar G, Alexandrov AV. Vasospasm surveillance with transcranial Doppler sonography in subarachnoid hemorrhage. J Ultrasound Med. 2015;34(8):1345–50.

    Article  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.

    Article  CAS  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.

    Article  CAS  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.

    Article  CAS  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.

    Article  CAS  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.

    Article  CAS  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.

    Article  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.

    Article  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.

    Article  CAS  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.

    Article  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.

    Article  CAS  Google Scholar 

  21. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.

    Article  CAS  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.

    Article  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.

    Article  CAS  Google Scholar 

  24. Ferguson S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658–67.

    Article  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.

    Article  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.

    Article  CAS  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.

    Article  CAS  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.

    Article  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.

    CAS  PubMed  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.

    Article  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.

    Article  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.

    Article  CAS  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.

    Article  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.

    Article  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.

    Article  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.

    Article  Google Scholar 

  37. 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.

    Article  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.

  39. Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58.

    Article  CAS  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.

    Article  CAS  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.

    Article  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

Authors

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

Correspondence to Gyanendra Kumar.

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.

Supplementary material 1 (PDF 297 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12028-018-0572-2

Keywords

Navigation