Skip to main content

Advertisement

Log in

High-Resolution MRI Vessel Wall Imaging in Acute Aneurysmal Subarachnoid Hemorrhage

Spatiotemporal Pattern and Clinicoradiologic Implications

  • Original Article
  • Published:
Clinical Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

The spatiotemporal pattern of vessel wall changes was investigated on two time point magnetic resonance images (MRI) in patients with aneurysmal subarachnoid hemorrhages (aSAH) and its association with clinicoradiologic severity score and delayed cerebral ischemia (DCI) was analyzed.

Methods

A total of 32 prospectively enrolled patients with aSAH (mean age 56.94 years; 9 male and 23 female) underwent vessel wall imaging (VWI) MRI. Of the patients 20 completed two time point MRIs early and late during the admission, 10 patients only had early MRI and 2 patients only had late MRI. Timing of early MRI had a mean of 2.5 days (range 1–6 days) and late MRI had a mean of 10.5 days (range 7–16 days) from time of admission. Spatiotemporal pattern of vessel wall enhancement (VWE), vasospasm, diffusion-weighted imaging (DWI) lesion burden (grade 0–III) and infarcts were analyzed against the clinicoradiologic severity score (high-risk: vasograde red and yellow, low-risk: vasograde green) and DCI.

Results

On the early MRI, mild VWE alone was significantly more frequent in the high-risk group (36.7% versus 20.0%; P = 0.024). On the late MRI, vasospasm was significantly more frequent in the high-risk group (27.2% versus 4.5%; P = 0.022). Vasospasm infrequently showed mild VWE (6.67% on early MRI and 9.09% on late MRI). Both mild VWE alone on early MRI and on late MRI were significantly associated with development of DCI during the admission (P = 0.034 and P = 0.035, respectively).

Conclusion

Mild VWE on early MRI and vasospasm on late MRI were significantly more prevalent in high-risk and DCI patients suggesting VWI might enable imaging of early neuroinflammatory changes which are part of the pathomechanism of vasospasm and DCI.

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

Access this article

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

Similar content being viewed by others

References

  1. van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369:306–18.

    Article  PubMed  Google Scholar 

  2. Frontera JA, Ahmed W, Zach V, Jovine M, Tanenbaum L, Sehba F, 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.

    Article  PubMed  Google Scholar 

  3. Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke. 1994;25:1342–7.

    Article  CAS  PubMed  Google Scholar 

  4. Dieleman N, Yang W, Abrigo JM, Chu WC, van der Kolk AG, Siero JC, et al. Magnetic resonance imaging of plaque morphology, burden, and distribution in patients with symptomatic middle cerebral artery stenosis. Stroke. 2016;47:1797–802.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Han C, Li ML, Xu YY, Ye T, Xie CF, Gao S, et al. Adult moyamoya-atherosclerosis syndrome: clinical and vessel wall imaging features. J Neurol Sci. 2016;369:181–4.

    Article  PubMed  Google Scholar 

  6. Mandell DM, Mossa-Basha M, Qiao Y, Hess CP, Hui F, Matouk C, et al. principles and expert consensus recommendations of the American Society of Neuroradiology. AJNR Am J Neuroradiol. 2017;38:218–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Mossa-Basha M, Hwang WD, De Havenon A, Hippe D, Balu N, Becker KJ, et al. Multicontrast high-resolution vessel wall magnetic resonance imaging and its value in differentiating intracranial vasculopathic processes. Stroke. 2015;46:1567–73.

    Article  PubMed  Google Scholar 

  8. Obusez EC, Hui F, Hajj-Ali RA, Cerejo R, Calabrese LH, Hammad T, et al. High-resolution MRI vessel wall imaging: spatial and temporal patterns of reversible cerebral vasoconstriction syndrome and central nervous system vasculitis. AJNR Am J Neuroradiol. 2014;35:1527–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ryoo S, Cha J, Kim SJ, Choi JW, Ki CS, Kim KH, et al. High-resolution magnetic resonance wall imaging findings of moyamoya disease. Stroke. 2014;45:2457–60.

    Article  PubMed  Google Scholar 

  10. Yuksel S, Tosun YB, Cahill J, Solaroglu I. Early brain injury following aneurysmal subarachnoid hemorrhage: emphasis on cellular apoptosis. Turk Neurosurg. 2012;22:529–33.

    PubMed  Google Scholar 

  11. Sabri M, Lass E, Macdonald RL. Early brain injury: a common mechanism in subarachnoid hemorrhage and global cerebral ischemia. Stroke Res Treat. 2013;2013:394036.

    PubMed  PubMed Central  Google Scholar 

  12. Ostrowski RP, Colohan AR, Zhang JH. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res. 2006;28:399–414.

    Article  CAS  PubMed  Google Scholar 

  13. Fujii M, Yan J, Rolland WB, Soejima Y, Caner B, Zhang JH. Early brain injury, an evolving frontier in subarachnoid hemorrhage research. Transl Stroke Res. 2013;4:432–46.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006;26:1341–53.

    Article  CAS  PubMed  Google Scholar 

  15. Stienen MN, Smoll NR, Weisshaupt R, Fandino J, Hildebrandt G, Studerus-Germann A, et al. Delayed cerebral ischemia predicts neurocognitive impairment following aneurysmal subarachnoid hemorrhage. World Neurosurg. 2014;82:e599–605.

    Article  PubMed  Google Scholar 

  16. Brathwaite S, Macdonald RL. Current management of delayed cerebral ischemia: update from results of recent clinical trials. Transl Stroke Res. 2014;5:207–26.

    Article  CAS  PubMed  Google Scholar 

  17. Dorsch NW, King MT. A review of cerebral vasospasm in aneurysmal subarachnoid haemorrhage Part I: Incidence and effects. J Clin Neurosci. 1994;1:19–26.

    Article  CAS  PubMed  Google Scholar 

  18. Naidech AM, Drescher J, Tamul P, Shaibani A, Batjer HH, Alberts MJ. Acute physiological derangement is associated with early radiographic cerebral infarction after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2006;77:1340–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Yoon DY, Chang SK, Choi CS, Kim WK, Lee JH. Multidetector row CT angiography in spontaneous lobar intracerebral hemorrhage: a prospective comparison with conventional angiography. AJNR Am J Neuroradiol. 2009;30:962–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Fisher CM, Roberson GH, Ojemann RG. Cerebral vasospasm with ruptured saccular aneurysm—the clinical manifestations. Neurosurgery. 1977;1:245–8.

    Article  CAS  PubMed  Google Scholar 

  22. Graham DI, Macpherson P, Pitts LH. Correlation between angiographic vasospasm, hematoma, and ischemic brain damage following SAH. J Neurosurg. 1983;59:223–30.

    Article  CAS  PubMed  Google Scholar 

  23. Edjlali M, Gentric JC, Régent-Rodriguez C, Trystram D, Hassen WB, Lion S, et al. Does aneurysmal wall enhancement on vessel wall MRI help to distinguish stable from unstable intracranial aneurysms? Stroke. 2014;45:3704–6.

    Article  PubMed  Google Scholar 

  24. Matouk CC, Mandell DM, Günel M, Bulsara KR, Malhotra A, Hebert R, Johnson MH, Mikulis DJ, Minja FJ. Vessel wall magnetic resonance imaging identifies the site of rupture in patients with multiple intracranial aneurysms: proof of principle. Neurosurgery. 2013;72:492–6. discussion 496.

    Article  PubMed  Google Scholar 

  25. Mossa-Basha M, Huynh TJ, Hippe DS, Fata P, Morton RP, Levitt MR. Vessel wall MRI characteristics of endovascularly treated aneurysms: association with angiographic vasospasm. J Neurosurg. 2019;131:859–67.

    Article  CAS  Google Scholar 

  26. de Oliveira Manoel AL, Jaja BN, Germans MR, Yan H, Qian W, Kouzmina E, et al. SAHIT collaborators. The VASOGRADE: a simple grading scale for prediction of delayed cerebral Ischemia after subarachnoid hemorrhage. Stroke. 2015;46:1826–31.

    Article  PubMed  Google Scholar 

  27. Yoon DY, Choi CS, Kim KH, Cho BM. Multidetector-row CT angiography of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: comparison of volume-rendered images and digital subtraction angiography. AJNR Am J Neuroradiol. 2006;27:370–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993;24:35–41.

    Article  PubMed  Google Scholar 

  29. Kang DH, Kim BM, Kim DJ, Suh SH, Kim DI, Kim YS, et al. MR-DWI-positive lesions and symptomatic ischemic complications after coiling of unruptured intracranial aneurysms. Stroke. 2013;44:789–91.

    Article  PubMed  Google Scholar 

  30. Kim B, Kim K, Jeon P, Kim S, Kim H, Byun H, et al. Thromboembolic complications in patients with clopidogrel resistance after coil embolization for unruptured intracranial aneurysms. AJNR Am J Neuroradiol. 2014;35:1786–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, 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 

  32. Kesav P, Krishnavadana B, Kesavadas C, Sreedharan SE, Rajendran A, Sukumaran S, et al. Utility of intracranial high-resolution vessel wall magnetic resonance imaging in differentiating intracranial vasculopathic diseases causing ischemic stroke. Neuroradiology. 2019;61:389–96.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  34. Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20.

    Article  CAS  PubMed  Google Scholar 

  35. Teasdale GM, Drake CG, Hunt W, Kassell N, Sano K, Pertuiset B, et al. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry. 1988;51:1457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14–20.

    Article  CAS  PubMed  Google Scholar 

  37. Hsieh K, Verma RK, Schroth G, Gratz PP, Kellner-Weldon F, Gralla J, et al. Multimodal 3 Tesla MRI confirms intact arterial wall in acute stroke patients after stent-retriever thrombectomy. Stroke. 2014;45:3430–2.

    Article  PubMed  Google Scholar 

  38. Power S, Matouk C, Casaubon LK, Silver FL, Krings T, Mikulis DJ, et al. Vessel wall magnetic resonance imaging in acute ischemic stroke: effects of embolism and mechanical thrombectomy on the arterial wall. Stroke. 2014;45:2330–4.

    Article  PubMed  Google Scholar 

  39. Portanova A, Hakakian N, Mikulis DJ, Virmani R, Abdalla WM, Wasserman BA. Intracranial vasa vasorum: insights and implications for imaging. Radiology. 2013;267:667–79.

    Article  PubMed  Google Scholar 

  40. Mandell DM, Matouk CC, Farb RI, Krings T, Agid R, terBrugge K, et al. Vessel wall MRI to differentiate between reversible cerebral vasoconstriction syndrome and central nervous system vasculitis: preliminary results. Stroke. 2012;43:860–2.

    Article  PubMed  Google Scholar 

  41. Kolias AG, Sen J, Belli A. Pathogenesis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: putative mechanisms and novel approaches. J Neurosci Res. 2009;87:1–11.

    Article  CAS  PubMed  Google Scholar 

  42. van der Kleij LA, De Vis JB, Olivot JM, Calviere L, Cognard C, Zuithoff NP, et al. Magnetic resonance imaging and cerebral ischemia after aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Stroke. 2017;48:239–45.

    Article  PubMed  Google Scholar 

  43. Eiden S, Beck C, Venhoff N, Elsheikh S, Ihorst G, Urbach H, et al. High-resolution contrast-enhanced vessel wall imaging in patients with suspected cerebral vasculitis: prospective comparison of whole-brain 3D T1 SPACE versus 2D T1 black blood MRI at 3 Tesla. PLoS ONE. 2019;14:e213514.

    Article  CAS  Google Scholar 

Download references

Funding

SMH AFP Innovation Fund SMH-16-022 and RSNA Research Fellow Grant #RF1614.

Author information

Authors and Affiliations

Authors

Contributions

Conception and design: A.B., C.C.-T.H., S.S., A.M. Acquisition, analysis, or interpretation of data: C.C.-T.H., S.S., T.H. Drafting of the manuscripts or figures: C.C.-T.H., S.S. Critical revision of the manuscript for important intellectual content: C.C.-T.H., S.S., A.M., T.H., A.B. Statistical analysis: C.C.-T.H., Y.L. Obtained funding: A.B., A.M. Administrative, technical, or material support: C.C.-T.H., Y.L., A.B. Study supervision: A.B.

Corresponding author

Correspondence to Aditya Bharatha.

Ethics declarations

Conflict of interest

C.C.-T. Hsu, S. Suthiphosuwan, T. Huynh, A. Murphy, Y. Li and A. Bharatha declare that they have no competing interests.

Ethical standards

This study was approved by the institutional review board of St Michael’s Hospital. REB number: 15-209. All procedures performed in studies involving human participants or on human tissue were in accordance with the ethical standards of the institutional and/or national research committee and with the 1975 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hsu, CT., Suthiphosuwan, S., Huynh, T. et al. High-Resolution MRI Vessel Wall Imaging in Acute Aneurysmal Subarachnoid Hemorrhage. Clin Neuroradiol 30, 801–810 (2020). https://doi.org/10.1007/s00062-019-00843-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00062-019-00843-8

Keywords

Navigation