Advertisement

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

  • Gyanendra Kumar
  • Oana M. Dumitrascu
  • Chia-Chun Chiang
  • Cumara B. O’Carroll
  • Andrei V. Alexandrov
Original Article
  • 130 Downloads

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.

Keywords

Meta-analysis Brain ischemia Cerebral vasospasm Cerebral angiography Transcranial Doppler sonography 

Notes

Author 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.

Source of support

None.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

12028_2018_572_MOESM1_ESM.pdf (297 kb)
Supplementary material 1 (PDF 297 kb)

References

  1. 1.
    Dorsch NW. Cerebral arterial spasm–a clinical review. Br J Neurosurg. 1995;9(3):403–12.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 3.
    Fergusen S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurdsosurgery. 2007;60(4):658–67.CrossRefGoogle Scholar
  4. 4.
    Rabinstein AA, Friedman JA, Weigand SD, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2004;35(8):1862–6.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Moppett IK, Mahajan RP. Transcranial Doppler ultrasonography in anaesthesia and intensive care. Br J Anaesth. 2004;93(5):710–24.CrossRefPubMedGoogle Scholar
  9. 9.
    Kumar G, Alexandrov AV. Vasospasm surveillance with transcranial Doppler sonography in subarachnoid hemorrhage. J Ultrasound Med. 2015;34(8):1345–50.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 12.
    Sloan MA, Burch CM, Wozniak MA, et al. Transcranial Doppler detection of vertebrobasilar vasospasm following subarachnoid hemorrhage. Stroke. 1994;25(11):2187–97.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
  18. 18.
    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.CrossRefPubMedGoogle Scholar
  22. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ferguson S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658–67.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. 30.
    Santos GA, Petersen N, Zamani AA, et al. Pathophysiologic differences in cerebral autoregulation after subarachnoid hemorrhage. Neurology. 2016;86(21):1950–6.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. 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. 39.
    Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society 2018

Authors and Affiliations

  1. 1.Division of Cerebrovascular Diseases, Department of NeurologyMayo ClinicPhoenixUSA
  2. 2.Department of NeurologyCedars-Sinai Medical CenterLos AngelesUSA
  3. 3.Department of NeurologyUniversity of Tennessee Health Science CenterMemphisUSA

Personalised recommendations