Skip to main content

Advertisement

SpringerLink
Log in

Imaging Predictors of Vasospasm and Delayed Cerebral Ischaemia After Subarachnoid Haemorrhage

  • Critical Care Neurology (H Hinson, Section Editor)
  • Published:
Current Treatment Options in Neurology Aims and scope Submit manuscript

A Correction to this article was published on 05 January 2021

This article has been updated

Abstract

Purpose of Review

Acute spontaneous subarachnoid haemorrhage (SAH) is a severe disease, frequently complicated by vasospasm and delayed cerebral ischaemia (DCI), which have a negative impact on prognosis. Imaging studies are essential in the diagnosis of SAH. In this article, we review the available imaging techniques for prediction, monitoring and diagnosis of these complications of SAH.

Recent Findings

Non-contrast computed tomography (CT) and transcranial Doppler (TCD) have been so far the mainly used techniques to evaluate SAH patients during the acute stage of disease and to screen for vasospasm and DCI. However, there have been new developments of brain imaging techniques, with the introduction of automated methods to quantify blood volume and cerebral flow velocities, and the use of perfusion studies that could contribute to predict or diagnose such complications. Magnetic resonance (MR) imaging studies are proving useful to evaluate early brain injury and to diagnose DCI. Newer angiography suites have sophisticated post-processing tools that quantify cerebral haemodynamics in SAH and may provide important clues for the diagnosis of vasospasm.

Summary

Imaging studies are part of the standard management of patients with acute SAH. Blood quantification on CT and the evaluation of cerebral flow velocities on TCD are known to predict and monitor the occurrence of vasospasm. DCI has increasingly been recognized as the most clinically relevant complication of SAH but also the most difficult to predict. MR imaging is the most sensitive tool to diagnose DCI. Future developments in imaging are needed to predict this important complication and help to improve the prognosis of patients with SAH.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Change history

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Barry C, Turner RJ, Corrigan F, Vink R. New therapeutic approaches to subarachnoid hemorrhage. Expert Opin Investig Drugs. 2012;21:845–59.

    Article  CAS  PubMed  Google Scholar 

  2. Linn FHH, Rinkel GJE, Algra A, van Gijn J. Incidence of subarachnoid hemorrhage. Stroke. 1996;27:625–9.

    Article  CAS  PubMed  Google Scholar 

  3. •• Connolly ES, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the american heart association/american stroke association. Stroke. 2012;43:1711–37 Essential reading for those who manage SAH, these are the most recent guidelines.

    Article  PubMed  Google Scholar 

  4. Hop JW, Rinkel GJE, Algra A, et al. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28:660–4.

    Article  CAS  PubMed  Google Scholar 

  5. Rinkel GJE, Algra A. Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2011;10:349–56.

    Article  PubMed  Google Scholar 

  6. Vergouwen MDI, Vermeulen M, Muizelaar JP, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies proposal of a multidisciplinary research group. Stroke. 2010;41:2391–5.

    Article  PubMed  Google Scholar 

  7. Frontera JA, Fernandez A, Schmidt JM, Claassen J, Wartenberg KE, Badjatia N, et al. Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke. 2009;40:1963–8.

    Article  PubMed  Google Scholar 

  8. Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, et al. Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke. 2011;42:919–23.

    Article  PubMed  Google Scholar 

  9. Kassell N, Sasaki T, Colohan A, et al. Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke. 1985;16:562–73.

    Article  CAS  PubMed  Google Scholar 

  10. •• Geraghty JR, Testai FD. Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Curr Atheroscler Rep. 2017;19(12):50. https://doi.org/10.1007/s11883-017-0690-x. Important to understand the complex pathophysiology of SAH and its complications.

  11. Rabinstein AA, Friedman JA, Weigand SD, McClelland RL, Fulgham JR, Manno EM, et al. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2004;35:1862–6.

    Article  PubMed  Google Scholar 

  12. Dubosh NM, Bellolio MF, Rabinstein AA, Edlow JA. Sensitivity of early brain computed tomography to exclude aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Stroke. 2016;47:750–5.

    Article  PubMed  Google Scholar 

  13. McCormack RF, Hutson A. Can computed tomography angiography of the brain replace lumbar puncture in the evaluation of acute-onset headache after a negative noncontrast cranial computed tomography scan? Acad Emerg Med. 2010;17:444–51.

    Article  PubMed  Google Scholar 

  14. Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ES, et al. Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery. 2006;59:21–7.

    Article  PubMed  Google Scholar 

  15. Hijdra A, Van Gijn J, Nagelkerke N, et al. Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke. 1988;19:1250–6.

    Article  CAS  PubMed  Google Scholar 

  16. van der Steen WE, Marquering HA, Boers AMM, Ramos LA, van den Berg R, Vergouwen MDI, et al. Predicting delayed cerebral ischemia with quantified aneurysmal subarachnoid blood volume. World Neurosurg. 2019;130:e613–9.

    Article  PubMed  Google Scholar 

  17. Neidert MC, Maldaner N, Stienen MN, Roethlisberger M, Zumofen DW, D’Alonzo D, et al. The barrow neurological institute grading scale as a predictor for delayed cerebral ischemia and outcome after aneurysmal subarachnoid hemorrhage: data from a nationwide patient registry (Swiss SOS). Clin Neurosurg. 2018;83:1286–93.

    Article  Google Scholar 

  18. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.

    Article  CAS  PubMed  Google Scholar 

  19. Zijlstra IA, Gathier CS, Boers AM, Marquering HA, Slooter AJ, Velthuis BK, et al. Association of automatically quantified total blood volume after aneurysmal subarachnoid hemorrhage with delayed cerebral ischemia. Am J Neuroradiol. 2016;37:1588–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Starnoni D, Maduri R, Hajdu SD, Pierzchala K, Giammattei L, Rocca A, et al. Early perfusion computed tomography scan for prediction of vasospasm and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2019;130:e743–52.

    Article  PubMed  Google Scholar 

  21. Dengler NF, Diesing D, Sarrafzadeh A, Wolf S, Vajkoczy P. The Barrow Neurological Institute scale revisited: predictive capabilities for cerebral infarction and clinical outcome in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2017;81:341–9.

    Article  PubMed  Google Scholar 

  22. Inagawa T. Risk factors for cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a review of the literature. World Neurosurg. 2016;85:56–76.

    Article  PubMed  Google Scholar 

  23. • van der Steen WE, Leemans EL, van den Berg R, et al. Radiological scales predicting delayed cerebral ischemia in subarachnoid hemorrhage: systematic review and meta-analysis. Neuroradiology. 2019;61:247–56 Good review of available imaging scales for prediction of DCI.

    Article  PubMed  Google Scholar 

  24. Rosen DS, Macdonald RL, Huo D, Goldenberg FD, Novakovic RL, Frank JI, et al. Intraventricular hemorrhage from ruptured aneurysm: clinical characteristics, complications, and outcomes in a large, prospective, multicenter study population. J Neurosurg. 2007;107:261–5.

    Article  PubMed  Google Scholar 

  25. Eagles ME, Jaja BNR, Macdonald RL. Incorporating a modified graeb score to the modified fisher scale for improved risk prediction of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Clin Neurosurg. 2018;82:299–305.

    Article  Google Scholar 

  26. Platz J, Güresir E, Wagner M, Seifert V, Konczalla J. Increased risk of delayed cerebral ischemia in subarachnoid hemorrhage patients with additional intracerebral hematoma. J Neurosurg. 2017;126:504–10.

    Article  PubMed  Google Scholar 

  27. Reilly C, Amidei C, Tolentino J, Jahromi BS, Macdonald RL. Clot volume and clearance rate as independent predictors of vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2004;101:255–61.

    Article  PubMed  Google Scholar 

  28. Ishihara H, Oka F, Kawano R, Shinoyama M, Nishimoto T, Kudomi S, et al. Hounsfield unit value of interpeduncular cistern hematomas can predict symptomatic vasospasm. Stroke. 2020;51:143–8.

    Article  PubMed  Google Scholar 

  29. Scherer M, Jung JO, Cordes J, et al. Association of cerebrospinal fluid volume with cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a retrospective volumetric analysis. Neurocrit Care. 2020;33(1):152–64. https://doi.org/10.1007/s12028-019-00878-2.

    Article  CAS  PubMed  Google Scholar 

  30. Black MCLP. Hydrocephalus and vasospasm after subarachnoid hemorrhage from ruptured intracranial aneurysms. Neurosurgery. 1986;18:12–6.

    Article  CAS  PubMed  Google Scholar 

  31. Ahn SH, Savarraj JP, Pervez M, et al. The subarachnoid hemorrhage early brain edema score predicts delayed cerebral ischemia and clinical outcomes. Clin Neurosurg. 2018;83:137–45.

    Article  Google Scholar 

  32. Malinova V, Tsogkas I, Behme D, Rohde V, Psychogios MN, Mielke D. Defining cutoff values for early prediction of delayed cerebral ischemia after subarachnoid hemorrhage by CT perfusion. Neurosurg Rev. 2020;43:581–7.

    Article  PubMed  Google Scholar 

  33. Dong L, Zhou Y, Wang M, Yang C, Yuan Q, Fang X. Whole-brain CT perfusion on admission predicts delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Eur J Radiol. 2019;116:165–73.

    Article  PubMed  Google Scholar 

  34. Etminan N, Beseoglu K, Heiroth HJ, Turowski B, Steiger HJ, Hänggi D. Early perfusion computerized tomography imaging as a radiographic surrogate for delayed cerebral ischemia and functional outcome after subarachnoid hemorrhage. Stroke. 2013;44:1260–6.

    Article  PubMed  Google Scholar 

  35. Sanelli PC, Jou A, Gold R, Reichman M, Greenberg E, John M, et al. Using CT perfusion during the early baseline period in aneurysmal subarachnoid hemorrhage to assess for development of vasospasm. Neuroradiology. 2011;53:425–34.

    Article  PubMed  Google Scholar 

  36. Lagares A, Cicuendez M, Ramos A, et al. Acute perfusion changes after spontaneous SAH: a perfusion CT study. Acta Neurochir. 2012;154:402–5.

    Article  Google Scholar 

  37. Duan Y, Xu H, Li R, Zheng K, Hu Z, Wu N, et al. Computed tomography perfusion deficits during the baseline period in aneurysmal subarachnoid hemorrhage are predictive of delayed cerebral ischemia. J Stroke Cerebrovasc Dis. 2017;26:162–8.

    Article  PubMed  Google Scholar 

  38. •• Burkhardt JK, Chen X, Winkler EA, et al. Early hemodynamic changes based on initial color-coding angiography as a predictor for developing subsequent symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. file///Users/isabelfragata/Downloads/burkhardt2017.pdfWorld. Neurosurg. 2018;109:e363–73 Interesting paper on newer developments in color-coded DSA.

    Google Scholar 

  39. Gölitz P, Hoelter P, Rösch J, Roessler K, Knossalla F, Doerfler A. Ultra-early detection of microcirculatory injury as predictor of developing delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Clin Neuroradiol. 2018;28:501–7.

    Article  PubMed  Google Scholar 

  40. Qureshi AI, Sung GY, Suri MAK, Straw RN, Guterman LR, Hopkins LN. Prognostic value and determinants of ultraearly angiographic vasospasm after aneurysmal subarachnoid hemorrhage [1] (multiple letters). Neurosurgery. 1999;44:967–74.

    Article  CAS  PubMed  Google Scholar 

  41. Baldwin ME, Macdonald RL, Huo D, et al. 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 LP – 2511.

    Article  Google Scholar 

  42. Al-Mufti F, Roh D, Lahiri S, et al. Ultra-early angiographic vasospasm associated with delayed cerebral ischemia and infarction following aneurysmal subarachnoid hemorrhage. J Neurosurg. 2017;126:1545–51.

    Article  PubMed  Google Scholar 

  43. •• Frontera JA, Ahmed W, Zach V, et al. Acute ischaemia after subarachnoid haemorrhage, relationship with early brain injury and impact on outcome: a prospective quantitative MRI study. J Neurol Neurosurg Psychiatry. 2015;86:71–8 Important paper on imaging of early brain injury, and its relevance to outcome.

    Article  PubMed  Google Scholar 

  44. Liu Y, Soppi V, Mustonen T, Könönen M, Koivisto T, Koskela A, et al. Subarachnoid hemorrhage in the subacute stage: elevated apparent diffusion coefficient in normal-appearing brain tissue after treatment. Radiology. 2007;242:518–25.

    Article  PubMed  Google Scholar 

  45. Fragata I, Alves M, Papoila AL, Nunes AP, Ferreira P, Canto-Moreira N, et al. Early prediction of delayed ischemia and functional outcome in acute subarachnoid hemorrhage: role of diffusion tensor imaging. Stroke. 2017;48:2091–7.

    Article  PubMed  Google Scholar 

  46. De Marchis GM, Filippi CG, Guo X, et al. Brain injury visible on early MRI after subarachnoid hemorrhage might predict neurological impairment and functional outcome. Neurocrit Care. 2015;22:74–81.

    Article  PubMed  Google Scholar 

  47. Weimer JM, Jones SE, Frontera JA. Acute cytotoxic and vasogenic edema after subarachnoid hemorrhage: a quantitative MRI study. Am J Neuroradiol. 2017;38:928–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J. Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke. 1990;21:1156–61.

    Article  CAS  PubMed  Google Scholar 

  49. Woo PYM, Tse TPK, Chan RSK, Leung LNY, Liu SKK, Leung AYT, et al. Computed tomography interobserver agreement in the assessment of aneurysmal subarachnoid hemorrhage and predictors for clinical outcome. J Neurointerv Surg. 2017;9:1118–24.

    Article  PubMed  Google Scholar 

  50. Zanaty M, Nakagawa D, Starke RM, Leira EC, Samaniego EA, Guerrero WR, et al. Intraventricular extension of an aneurysmal subarachnoid hemorrhage is an independent predictor of a worse functional outcome. Clin Neurol Neurosurg. 2018;170:67–72.

    Article  PubMed  Google Scholar 

  51. Graeb DA, Robertson WD, Lapointe JS, Nugent RA, Harrison PB. Computed tomographic diagnosis of intraventricular hemorrhage. Etiology and prognosis. Radiology. 1982;143:91–6.

    Article  CAS  PubMed  Google Scholar 

  52. Morgan TC, Dawson J, Spengler D, Lees KR, Aldrich C, Mishra NK, et al. The modified graeb score: an enhanced tool for intraventricular hemorrhage measurement and prediction of functional outcome. Stroke. 2013;44:635–41.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Schuss P, Hadjiathanasiou A, Borger V, Wispel C, Vatter H, Güresir E. Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome—a single-center series. World Neurosurg. 2016;85:125–9.

    Article  PubMed  Google Scholar 

  54. •• Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet. 2016;389(10069):655–66. https://doi.org/10.1016/S0140-6736(16)30668-7. Very well written paper on spontaneous SAH, for a global clinical and imaging perspective.

  55. Nabavi DG, LeBlanc LM, Baxter B, et al. Monitoring cerebral perfusion after subarachnoid hemorrhage using CT. Neuroradiology. 2001;43:7–16.

    Article  CAS  PubMed  Google Scholar 

  56. Tateyama K, Kobayashi S, Murai Y, Teramoto A. Assessment of cerebral circulation in the acute phase of subarachnoid hemorrhage using perfusion computed tomography. J Nippon Med Sch. 2013;80:110–8.

    Article  PubMed  Google Scholar 

  57. Fragata I, Alves M, Papoila AL, Diogo M, Canhão P, Canto-Moreira N. Temporal evolution of cerebral computed tomography perfusion after acute subarachnoid hemorrhage: a prospective cohort study. Acta Radiol. 2020;61:376–85.

    Article  PubMed  Google Scholar 

  58. Van Der Schaaf I, Wermer MJ, Van Der Graaf Y, et al. CT after subarachnoid hemorrhage: relation of cerebral perfusion to delayed cerebral ischemia. Neurology. 2006;66:1533–8.

    Article  PubMed  Google Scholar 

  59. Rodriguez-Régent C, Hafsa M, Turc G, Ben Hassen W, Edjlali M, Sermet A, et al. Early quantitative CT perfusion parameters variation for prediction of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. Eur Radiol. 2016;26:2956–63.

    Article  PubMed  Google Scholar 

  60. Takahashi Y, Sasahara A, Yamazaki K, Inazuka M, Kasuya H. Disturbance of CT perfusion within 24 h after onset is associated with WFNS grade but not development of DCI in patients with aneurysmal SAH. Acta Neurochir. 2017;159:2319–24.

    Article  PubMed  Google Scholar 

  61. Fragata I, Alves M, Papoila AL, Nunes AP, Ferreira P, Diogo M, et al. Computed tomography perfusion as a predictor of delayed cerebral ischemia and functional outcome in spontaneous subarachnoid hemorrhage: a single center experience. Neuroradiol J. 2019;32:179–88.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Cremers CHP, van der Schaaf IC, Wensink E, Greving JP, Rinkel GJE, Velthuis BK, et al. CT perfusion and delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2014;34:200–7.

    Article  PubMed  Google Scholar 

  63. Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004;24:916–25.

    Article  CAS  PubMed  Google Scholar 

  64. Sehba FA, Pluta RM, Zhang JH. Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol. 2011;43:27–40.

    Article  CAS  PubMed  Google Scholar 

  65. Sato K, Shimizu H, Fujimura M, Inoue T, Matsumoto Y, Tominaga T. Acute-stage diffusion-weighted magnetic resonance imaging for predicting outcome of poor-grade aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2010;30:1110–20.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Wartenberg KE, Sheth SJ, Michael Schmidt J, Frontera JA, Rincon F, Ostapkovich N, et al. Acute ischemic injury on diffusion-weighted magnetic resonance imaging after poor grade subarachnoid hemorrhage. Neurocrit Care. 2011;14:407–15.

    Article  PubMed  Google Scholar 

  67. De Oliveira Manoel AL, Jaja BN, Germans MR, et al. The VASOGRADE: a simple grading scale for prediction of delayed cerebral ischemia after subarachnoid hemorrhage. Stroke. 2015;46:1826–31.

    Article  PubMed  Google Scholar 

  68. Lee VH, Ouyang B, John S, Conners JJ, Garg R, Bleck TP, et al. Risk stratification for the in-hospital mortality in subarachnoid hemorrhage: the HAIR score. Neurocrit Care. 2014;21:14–9.

    Article  PubMed  Google Scholar 

  69. Fang YJ, Mei SH, Lu JN, Chen YK, Chai ZH, Dong X, et al. New risk score of the early period after spontaneous subarachnoid hemorrhage: for the prediction of delayed cerebral ischemia. CNS Neurosci Ther. 2019;25:1173–81.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Dengler NF, Sommerfeld J, Diesing D, Vajkoczy P, Wolf S. Prediction of cerebral infarction and patient outcome in aneurysmal subarachnoid hemorrhage: comparison of new and established radiographic, clinical and combined scores. Eur J Neurol. 2018;25:111–9.

    Article  CAS  PubMed  Google Scholar 

  71. Fang Y, Lu J, Zheng J, et al. Comparison of aneurysmal subarachnoid hemorrhage grading scores in patients with aneurysm clipping and coiling. Sci Rep. 2020;10:1–9.

    Article  CAS  Google Scholar 

  72. Arias EJ, Vajapey S, Reynolds MR, Chicoine MR, Rich KM, Dacey RG Jr, et al. Utility of screening for cerebral vasospasm using digital subtraction angiography. Stroke. 2015;46:3137–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lysakowski C, Walder B, Costanza MC, Tramèr MR. Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review. Stroke. 2001;32:2292–8.

    Article  CAS  PubMed  Google Scholar 

  74. Lindegaard KF, Nornes H, Bakke SJ, et al. Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochir. 1989;100:12–24.

    Article  CAS  PubMed  Google Scholar 

  75. Connolly F, Schreiber SJ, Leithner C, Bohner G, Vajkoczy P, Valdueza JM. Assessment of intracranial venous blood flow after subarachnoid hemorrhage: a new approach to diagnose vasospasm with transcranial color-coded duplex sonography. J Neurosurg. 2018;129:1136–42.

    Article  PubMed  Google Scholar 

  76. Sviri GE, Ghodke B, Britz GW, Douville CM, Haynor DR, Mesiwala AH, et al. Transcranial doppler grading criteria for basilar artery vasospasm. Neurosurgery. 2006;59:360–5.

    Article  PubMed  Google Scholar 

  77. Neulen A, Stein M, Pantel T, Berres M, Brockmann C, Giese A, et al. Image-guided transcranial Doppler ultrasound for monitoring posthemorrhagic vasospasms of Infratentorial arteries: a feasibility study. World Neurosurg. 2020;134:284–91.

    Article  PubMed  Google Scholar 

  78. Elzaafarany K, Aly MH, Kumar G, Nakhmani A. Cerebral artery vasospasm detection using transcranial Doppler signal analysis. J Ultrasound Med. 2019;38:2191–202.

    Article  PubMed  Google Scholar 

  79. Greenberg ED, Gold R, Reichman M, John M, Ivanidze J, Edwards AM, et al. Diagnostic accuracy of CT angiography and CT perfusion for cerebral vasospasm: a meta-analysis. Am J Neuroradiol. 2010;31:1853–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Neulen A, Pantel T, Dieter A, Kosterhon M, Berres M, Thal SC, et al. Volumetric analysis of intracranial vessels: a novel tool for evaluation of cerebral vasospasm. Int J Comput Assist Radiol Surg. 2019;14:157–67.

    Article  PubMed  Google Scholar 

  81. Neulen A, Kunzelmann S, Kosterhon M, et al. Automated grading of cerebral vasospasm to standardize computed tomography angiography examinations after subarachnoid hemorrhage. Front Neurol. 2020;11:1–10.

    Article  Google Scholar 

  82. Grandin CB, Cosnard G, Hammer F, Duprez TP, Stroobandt G, Mathurin P. Vasospasm after subarachnoid hemorrhage: diagnosis with MR angiography. Am J Neuroradiol. 2000;21:1611–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Hamaguchi A, Fujima N, Yoshida D, Hamaguchi N, Kodera S. Improvement of the diagnostic accuracy of MRA with subtraction technique in cerebral vasospasm. J Neuroimaging. 2014;24:548–53.

    Article  PubMed  Google Scholar 

  84. Hattingen E, Blasel S, Dumesnil R, et al. MR angiography in patients with subarachnoid hemorrhage: adequate to evaluate vasospasm-induced vascular narrowing? Neurosurg Rev. 2010;33:431–9.

    Article  PubMed  Google Scholar 

  85. Takano K, Hida K, Iwaasa M, Inoue T, Yoshimitsu K. Three-dimensional spin-echo-based black-blood MRA in the detection of vasospasm following subarachnoid hemorrhage. J Magn Reson Imaging. 2019;49:800–7.

    Article  PubMed  Google Scholar 

  86. Mossa-Basha M, Huynh TJ, Hippe DS, et al. Vessel wall MRI characteristics of endovascularly treated aneurysms: association with angiographic vasospasm. J Neurosurg. 2019;131:859–67.

    Article  CAS  Google Scholar 

  87. Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJH, Rinkel GJE. Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology. 2009;51:813–9.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Kanazawa R, Kato M, Ishikawa K, Eguchi T, Teramoto A. Convenience of the computed tomography perfusion method for cerebral vasospasm detection after subarachnoid hemorrhage. Surg Neurol. 2007;67:604–11.

    Article  PubMed  Google Scholar 

  89. Binaghi S, Colleoni ML, Maeder P, et al. CT angiography and perfusion CT in cerebral vasospasm after subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2007;28:750–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Wintermark M, Dillon WP, Smith WS, Lau BC, Chaudhary S, Liu S, et al. Visual grading system for vasospasm based on perfusion CT imaging: comparisons with conventional angiography and quantitative perfusion CT. Cerebrovasc Dis. 2008;26:163–70.

    Article  PubMed  Google Scholar 

  91. Lefournier V, Krainik A, Gory B, Derderian F, Bessou P, Fauvage B, et al. Quantification du vasospasme cérébral après hémorragie sous-arachnoïdienne par scanner de perfusion. J Neuroradiol. 2010;37:284–91.

    Article  PubMed  Google Scholar 

  92. Dolatowski K, Malinova V, Frölich AMJ, et al. Volume perfusion CT (VPCT) for the differential diagnosis of patients with suspected cerebral vasospasm: qualitative and quantitative analysis of 3D parameter maps. Eur J Radiol. 2014;83:1881–9.

    Article  CAS  PubMed  Google Scholar 

  93. Wintermark M, Ko NUU, Smith WSS, Liu S, Higashida RT, Dillon WP. Vasospasm after subarachnoid hemorrhage: utility of perfusion CT and CT angiography on diagnosis and management. AJNR Am J Neuroradiol. 2006;27:26–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Moftakhar R, Rowley HA, Turk A, et al. Utility of computed tomography perfusion in detection of cerebral vasospasm in patients with subarachnoid hemorrhage. Neurosurg Focus. 2006;21:E6.

    Article  PubMed  Google Scholar 

  95. Afat S, Brockmann C, Nikoubashman O, Müller M, Thierfelder KM, Brockmann MA, et al. Diagnostic accuracy of simulated low-dose perfusion CT to detect cerebral perfusion impairment after aneurysmal subarachnoid hemorrhage: a retrospective analysis. Radiology. 2018;287:643–50.

    Article  PubMed  Google Scholar 

  96. Ohtonari T, Kakinuma K, Kito T, et al. Diffusion-perfusion mismatch in symptomatic vasospasm after subarachnoid hemorrhage. Neurol Med Chir (Tokyo). 2008;48:331–6 discussion 336.

    Article  Google Scholar 

  97. Rordorf G, Koroshetz WJ, Copen WA, Gonzalez G, Yamada K, Schaefer PW, et al. Diffusion- and perfusion-weighted imaging in vasospasm after subarachnoid hemorrhage. Stroke. 1999;30:599–605.

    Article  CAS  PubMed  Google Scholar 

  98. Vatter H, Güresir E, Berkefeld J, et al. Perfusion-diffusion mismatch in MRI to indicate endovascular treatment of cerebral vasospasm after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2011;82:876–83.

    Article  PubMed  Google Scholar 

  99. • Sharma S, Lubrica RJ, Song M, et al. The role of transcranial doppler in cerebral vasospasm: a literature review. Acta Neurochir Suppl. 2020;127:201–5 Good review on the role of TCD for diagnosis of vasospasm.

    Article  PubMed  Google Scholar 

  100. Mills JN, Mehta V, Russin J, Amar AP, Rajamohan A, Mack WJ. Advanced imaging modalities in the detection of cerebral vasospasm. Neurol Res Int. 2013;2013:1–15.

    Article  Google Scholar 

  101. Sloan MA, Alexandrov AV, Tegeler CH, et al. Assessment: transcranial doppler ultrasonography. Report of the therapeutics and technology assessment Subcommittee of the American Academy of neurology. Neurology. 2004;62:1468–81.

    Article  CAS  PubMed  Google Scholar 

  102. Letourneau-Guillon L, Farzin B, Darsaut TE, Kotowski M, Guilbert F, Chagnon M, et al. Reliability of CT angiography in cerebral vasospasm: a systematic review of the literature and an inter- and intraobserver study. AJNR Am J Neuroradiol. 2020;41:612–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Sanelli PC, Pandya A, Segal AZ, Gupta A, Hurtado-Rua S, Ivanidze J, et al. Cost-effectiveness of CT angiography and perfusion imaging for delayed cerebral ischemia and vasospasm in aneurysmal subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2014;35:1714–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Stecco A, Fabbiano F, Amatuzzo P, Quagliozzi M, Soligo E, Divenuto I, et al. Computed tomography perfusion and computed tomography angiography in vasospasm after subarachnoid hemorrhage. J Neurosurg Sci. 2018;62:397–405.

    PubMed  Google Scholar 

  105. Rabinstein AA, Weigand S, Atkinson JLD, Wijdicks EFM. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005;36:992–7.

    Article  PubMed  Google Scholar 

  106. 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;124:1257–64.

    Article  PubMed  Google Scholar 

  107. Lam JMK, Smielewski P, Czosnyka M, Pickard JD, Kirkpatrick PJ. Predicting delayed ischemic deficits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation. Neurosurgery. 2000;47:819–26.

    Article  CAS  PubMed  Google Scholar 

  108. Budohoski KP, Czosnyka M, Smielewski P, Varsos GV, Kasprowicz M, Brady KM, et al. Cerebral autoregulation after subarachnoid hemorrhage: comparison of three methods. J Cereb Blood Flow Metab. 2013;33:449–56.

    Article  PubMed  Google Scholar 

  109. Rynkowski CB, de Oliveira Manoel AL, dos Reis MM, Puppo C, Worm PV, Zambonin D, et al. Early transcranial Doppler evaluation of cerebral autoregulation independently predicts functional outcome after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2019;31:253–62.

    Article  PubMed  Google Scholar 

  110. Al-Jehani H, Angle M, Marcoux J, et al. Early abnormal transient hyperemic response test can predict delayed ischemic neurologic deficit in subarachnoid hemorrhage. Crit Ultrasound J. 2018;10:1–6.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Bøthun ML, Haaland ØA, Moen G, Logallo N, Svendsen F, Thomassen L, et al. Impaired cerebrovascular reactivity may predict delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. J Neurol Sci. 2019;407:116539.

    Article  PubMed  CAS  Google Scholar 

  112. Carrera E, Kurtz P, Badjatia N, Fernandez L, Claassen J, Lee K, et al. Cerebrovascular carbon dioxide reactivity and delayed cerebral ischemia after subarachnoid hemorrhage. Arch Neurol. 2010;67:434–9.

    Article  PubMed  Google Scholar 

  113. Frontera JA, Rundek T, Schmidt JM, Claassen J, Parra A, Wartenberg KE, et al. Cerebrovascular reactivity and vasospasm after subarachnoid hemorrhage: a pilot study. Neurology. 2006;66:727–9.

    Article  CAS  PubMed  Google Scholar 

  114. Dankbaar JW, de Rooij NK, Rijsdijk M, Velthuis BK, Frijns CJM, Rinkel GJE, et al. Diagnostic threshold values of cerebral perfusion measured with computed tomography for delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke. 2010;41:1927–32.

    Article  PubMed  Google Scholar 

  115. Sanelli PC, Anumula N, Johnson CE, Comunale JP, Tsiouris AJ, Riina H, et al. Evaluating CT perfusion using outcome measures of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2013;34:292–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Mir DI, Gupta A, Dunning A, et al. CT perfusion for detection of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 2014;35:866–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. da Costa L, Fisher J, Mikulis DJ, et al. Early identification of brain tissue at risk for delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. In: Fandino J, Marbacher S, Fathi A-R, et al., editors. Neurovascular Events After Subarachnoid Hemorrhage, vol. 120. Acta Neurochirurgica Supplement. Cham: Springer International Publishing; 2015. p. 105–9.

    Chapter  Google Scholar 

  118. Russin JJ, Montagne A, D’Amore F, He S, Shiroishi MS, Rennert RC, et al. Permeability imaging as a predictor of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2018;38:973–9.

    Article  PubMed  PubMed Central  Google Scholar 

  119. Malinova V, Iliev B, Tsogkas I, et al. Assessment of tissue permeability by early CT perfusion as a surrogate parameter for early brain injury after subarachnoid hemorrhage. J Neurosurg. 2020;23:1–6. https://doi.org/10.3171/2019.5.jns19765.

    Article  Google Scholar 

  120. Hollingworth M, Jamjoom AAB, Bulters D, Patel HC. How is vasospasm screening using transcranial Doppler associated with delayed cerebral ischemia and outcomes in aneurysmal subarachnoid hemorrhage? Acta Neurochir. 2019;161:385–92.

    Article  CAS  PubMed  Google Scholar 

  121. Dhar R, Scalfani MT, Blackburn S, Zazulia AR, Videen T, Diringer M. Relationship between angiographic vasospasm and regional hypoperfusion in aneurysmal subarachnoid hemorrhage. Stroke. 2012;43:1788–94.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Neuroradiology Department, Hospital São José, Centro Hospitalar Universitário de Lisboa Central, Lisbon, Portugal

    Isabel Fragata MD, PhD & Bruno Cunha MD

  2. NOVA Medical School, Universidade Nova de Lisboa, Lisbon, Portugal

    Isabel Fragata MD, PhD & Bruno Cunha MD

  3. Department of Neurosciences and Mental Health, Department of Neurology, Hospital de Santa Maria, CHLN, Lisbon, Portugal

    Patrícia Canhão MD, PhD

  4. Universidade de Lisboa, Faculdade de Medicina, Instituto de Medicina Molecular, Lisbon, Portugal

    Patrícia Canhão MD, PhD

Authors
  1. Isabel Fragata MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Cunha MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrícia Canhão MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabel Fragata MD, PhD.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised due to the incorrect formating of the name of the last author. It should read from 'PatrU´cia CanhÐo’ to ‘Patrícia Canhão’.

This article is part of the Topical Collection on Critical Care Neurology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fragata, I., Cunha, B. & Canhão, P. Imaging Predictors of Vasospasm and Delayed Cerebral Ischaemia After Subarachnoid Haemorrhage. Curr Treat Options Neurol 22, 47 (2020). https://doi.org/10.1007/s11940-020-00653-1

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11940-020-00653-1

Keywords

Search

Navigation