Skip to main content

Advertisement

SpringerLink
Log in

Usefulness of 3D High-resolution Vessel Wall MRI in Diffuse Nonaneurysmal SAH Patients

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

Abstract

Purpose

In 15–20% of patients with nontraumatic diffuse subarachnoid hemorrhage (SAH), the initial conventional angiography does not reveal a causative vascular abnormality, such as intracranial aneurysm. In this study, we evaluated clinical utility of 3D high-resolution vessel wall magnetic resonance imaging (HR-VWI) in patients with diffuse nonaneurysmal SAH.

Methods

A total of 17 patients with diffuse nonaneurysmal SAH were included in this retrospective study. We characterized demographics and HR-VWI findings and reviewed the clinical management and outcomes.

Results

Of the patients 14 (14/17; 82.4%,) showed abnormal findings on HR-VWI, including 5 with intracranial dissections (29.4%), 3 with blood blister-like aneurysm (17.6%), 1 with ruptured fusiform aneurysm (5.9%), and 5 with focal nodular wall enhancement without unclassified pathology (29.4%). Of these patients were treated with endovascular management. Most patients (16/17) had a favorable modified Rankin scale scores of 0–2 on discharge.

Conclusion

The 3D HR-VWI revealed various hidden pathologies, such as intracranial arterial dissection, blood blister-like aneurysm, and fusiform aneurysm in patients with diffuse nonaneurysmal SAH. In addition, 3D HR-VWI had an impact on the management of SAH. The 3D HR-VWI can be a complementary diagnostic method for patients with diffuse nonaneurysmal SAH in a research or clinical setting.

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

Abbreviations

BBA:

Blood blister-like aneurysm

HR-VWI:

High-resolution vessel wall magnetic resonance imaging

mRS:

Modified Rankin scale

WFNS:

World Federation of Neurosurgical Societies

References

  1. Bederson JB, Connolly ES Jr, Batjer HH, Dacey RG, Dion JE, Diringer MN, Duldner JE Jr, Harbaugh RE, Patel AB, Rosenwasser RH; American Heart Association. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40:994–1025. Erratum in: Stroke. 2009;40:e518.

    Article  PubMed  Google Scholar 

  2. van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain. 2001;124:249–78.

    Article  PubMed  Google Scholar 

  3. Rinkel GJ, Wijdicks EF, Hasan D, Kienstra GE, Franke CL, Hageman LM, Vermeulen M, van Gijn J. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet. 1991;338:964–8.

    Article  PubMed  CAS  Google Scholar 

  4. Duong H, Melançon D, Tampieri D, Ethier R. The negative angiogram in subarachnoid haemorrhage. Neuroradiology. 1996;38:15–9.

    Article  PubMed  CAS  Google Scholar 

  5. Zolnourian A, Borg N, Akhigbe T, Macdonald J, Bulters D. Vessel wall imaging after subarachnoid hemorrhage in patients with multiple Intracranial aneurysms: a cautionary case. World Neurosurg. 2019;127:414–7.

    Article  PubMed  Google Scholar 

  6. Konczalla J, Schuss P, Platz J, Vatter H, Seifert V, Güresir E. Clinical outcome and prognostic factors of patients with angiogram-negative and non-perimesencephalic subarachnoid hemorrhage: benign prognosis like perimesencephalic SAH or same risk as aneurysmal SAH? Neurosurg Rev. 2015;38:121–7; discussion 127.

    Article  PubMed  Google Scholar 

  7. Maslehaty H, Barth H, Petridis AK, Doukas A, Mehdorn HM. Special features of subarachnoid hemorrhage of unknown origin: a review of a series of 179 cases. Neurol Res. 2012;34:91–7.

    Article  PubMed  Google Scholar 

  8. Elhadi AM, Zabramski JM, Almefty KK, Mendes GA, Nakaji P, McDougall CG, Albuquerque FC, Preul MC, Spetzler RF. Spontaneous subarachnoid hemorrhage of unknown origin: hospital course and long-term clinical and angiographic follow-up. J Neurosurg. 2015;122:663–70.

    PubMed  Google Scholar 

  9. Bakker NA, Groen RJ, Foumani M, Uyttenboogaart M, Eshghi OS, Metzemaekers JD, Lammers N, Luijckx GJ, Van Dijk JM. Repeat digital subtraction angiography after a negative baseline assessment in nonperimesencephalic subarachnoid hemorrhage: a pooled data meta-analysis. J Neurosurg. 2014;120:99–103.

    PubMed  Google Scholar 

  10. Agid R, Andersson T, Almqvist H, Willinsky RA, Lee SK, terBrugge KG, Farb RI, Söderman M. Negative CT angiography findings in patients with spontaneous subarachnoid hemorrhage: When is digital subtraction angiography still needed? AJNR Am J Neuroradiol. 2010;31:696–705.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Kaufmann TJ, Huston J 3rd, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF. Complications of diagnostic cerebral angiography: evaluation of 19,826 consecutive patients. Radiology. 2007;243:812–9.

    Article  PubMed  Google Scholar 

  12. Steven AJ, Milburn JM, Gulotta P, Gandhi D. Clinical images: vessel wall imaging in the management of subarachnoid hemorrhage and multiple intracranial aneurysms. Ochsner J. 2016;16:199–202.

    PubMed  PubMed Central  Google Scholar 

  13. 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 

  14. Kondo R, Yamaki T, Mouri W, Sato S, Saito S, Nagahata M, Nagahata S, Kayama T. Magnetic resonance vessel wall imaging reveals rupture site in subarachnoid hemorrhage with multiple cerebral aneurysms. No Shinkei Geka. 2014;42:1147–50.

    PubMed  Google Scholar 

  15. Nagahata S, Nagahata M, Obara M, Kondo R, Minagawa N, Sato S, Sato S, Mouri W, Saito S, Kayama T. Wall Enhancement of the Intracranial Aneurysms Revealed by Magnetic Resonance Vessel Wall Imaging Using Three-Dimensional Turbo Spin-Echo Sequence with Motion-Sensitized Driven-Equilibrium: A Sign of Ruptured Aneurysm? Clin Neuroradiol. 2016;26:277–83.

    Article  PubMed  CAS  Google Scholar 

  16. Coutinho JM, Sacho RH, Schaafsma JD, Agid R, Krings T, Radovanovic I, Matouk CC, Mikulis DJ, Mandell DM. High-Resolution Vessel Wall Magnetic Resonance Imaging in Angiogram-Negative Non-Perimesencephalic Subarachnoid Hemorrhage. Clin Neuroradiol. 2017;27:175–83.

    Article  PubMed  CAS  Google Scholar 

  17. Qiao Y, Steinman DA, Qin Q, Etesami M, Schär M, Astor BC, Wasserman BA. Intracranial arterial wall imaging using three-dimensional high isotropic resolution black blood MRI at 3.0 Tesla. J Magn Reson Imaging. 2011;34:22–30.

    Article  PubMed  Google Scholar 

  18. Eiden S, Beck C, Venhoff N, Elsheikh S, Ihorst G, Urbach H, Meckel S. 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:e0213514.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Shigeta H, Kyoshima K, Nakagawa F, Kobayashi S. Dorsal internal carotid artery aneurysms with special reference to angiographic presentation and surgical management. Acta Neurochir (Wien). 1992;119:42–8.

    Article  CAS  Google Scholar 

  20. Gaughen JR Jr., Raghavan P, Jensen ME, Hasan D, Pfeffer AN, Evans AJ. Utility of CT angiography in the identification and characterization of supraclinoid internal carotid artery blister aneurysms. AJNR Am J Neuroradiol. 2010;31:640–4.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Han M, Rim NJ, Lee JS, Kim SY, Choi JW. Feasibility of high-resolution MR imaging for the diagnosis of intracranial vertebrobasilar artery dissection. Eur Radiol. 2014;24:3017–24.

    Article  PubMed  Google Scholar 

  22. Naggara O, Louillet F, Touzé E, Roy D, Leclerc X, Mas JL, Pruvo JP, Meder JF, Oppenheim C. Added value of high-resolution MR imaging in the diagnosis of vertebral artery dissection. AJNR Am J Neuroradiol. 2010;31:1707–12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Rodallec MH, Marteau V, Gerber S, Desmottes L, Zins M. Craniocervical arterial dissection: spectrum of imaging findings and differential diagnosis. Radiographics. 2008;28:1711–28.

    Article  PubMed  Google Scholar 

  24. Lubicz B, Collignon L, Lefranc F, Bruneau M, Brotchi J, Balériaux D, De Witte O. Circumferential and fusiform intracranial aneurysms: reconstructive endovascular treatment with self-expandable stents. Neuroradiology. 2008;50:499–507.

    Article  PubMed  Google Scholar 

  25. Delgado Almandoz JE, Jagadeesan BD, Refai D, Moran CJ, Cross DT 3rd, Chicoine MR, Rich KM, Diringer MN, Dacey RG Jr, Derdeyn CP, Zipfel GJ. Diagnostic yield of repeat catheter angiography in patients with catheter and computed tomography angiography negative subarachnoid hemorrhage. Neurosurgery. 2012;70:1135–42.

    Article  PubMed  Google Scholar 

  26. Dalyai R, Chalouhi N, Theofanis T, Jabbour PM, Dumont AS, Gonzalez LF, Gordon DS, Thakkar V, Rosenwasser RH, Tjoumakaris SI. Subarachnoid hemorrhage with negative initial catheter angiography: a review of 254 cases evaluating patient clinical outcome and efficacy of short- and long-term repeat angiography. Neurosurgery. 2013;72:646–52; discussion 651–2. Erratum in: Neurosurgery. 2013;73:E913.

    PubMed  Google Scholar 

  27. Xie Y, Yang Q, Xie G, Pang J, Fan Z, Li D. Improved black-blood imaging using DANTE-SPACE for simultaneous carotid and intracranial vessel wall evaluation. Magn Reson Med. 2016;75:2286–94.

    Article  PubMed  Google Scholar 

  28. Lindenholz A, van der Kolk AG, Zwanenburg JJM, Hendrikse J. The use and pitfalls of Intracranial vessel wall imaging: how we do it. Radiology. 2018;286:12–28.

    Article  PubMed  Google Scholar 

  29. Mohan M, Islim AI, Rasul FT, Rominiyi O, deSouza RM, Poon MTC, Jamjoom AAB, Kolias AG, Woodfield J, Patel K, Chari A, Kirollos R; British Neurosurgical Trainee Research Collaborative. Subarachnoid haemorrhage with negative initial neurovascular imaging: a systematic review and meta-analysis. Acta Neurochir (Wien). 2019;161:2013–26.

    Article  Google Scholar 

  30. Khan AA, Smith JD, Kirkman MA, Robertson FJ, Wong K, Dott C, Grieve JP, Watkins LD, Kitchen ND. Angiogram negative subarachnoid haemorrhage: outcomes and the role of repeat angiography. Clin Neurol Neurosurg. 2013;115:1470–5.

    Article  PubMed  CAS  Google Scholar 

  31. Canneti B, Mosqueira AJ, Nombela F, Gilo F, Vivancos J. Spontaneous subarachnoid hemorrhage with negative angiography managed in a stroke unit: clinical and prognostic characteristics. J Stroke Cerebrovasc Dis. 2015;24:2484–90.

    Article  PubMed  Google Scholar 

  32. Moscovici S, Fraifeld S, Ramirez-de-Noriega F, Rosenthal G, Leker RR, Itshayek E, Cohen JE. Clinical relevance of negative initial angiogram in spontaneous subarachnoid hemorrhage. Neurol Res. 2013;35:117–22.

    Article  PubMed  Google Scholar 

  33. Little AS, Garrett M, Germain R, Farhataziz N, Albuquerque FC, McDougall CG, Zabramski JM, Nakaji P, Spetzler RF. Evaluation of patients with spontaneous subarachnoid hemorrhage and negative angiography. Neurosurgery. 2007;61:1139–50; discussion 1150–1.

    Article  PubMed  Google Scholar 

  34. Debette S, Compter A, Labeyrie MA, Uyttenboogaart M, Metso TM, Majersik JJ, Goeggel-Simonetti B, Engelter ST, Pezzini A, Bijlenga P, Southerland AM, Naggara O, Béjot Y, Cole JW, Ducros A, Giacalone G, Schilling S, Reiner P, Sarikaya H, Welleweerd JC, Kappelle LJ, de Borst GJ, Bonati LH, Jung S, Thijs V, Martin JJ, Brandt T, Grond-Ginsbach C, Kloss M, Mizutani T, Minematsu K, Meschia JF, Pereira VM, Bersano A, Touzé E, Lyrer PA, Leys D, Chabriat H, Markus HS, Worrall BB, Chabrier S, Baumgartner R, Stapf C, Tatlisumak T, Arnold M, Bousser MG. Epidemiology, pathophysiology, diagnosis, and management of intracranial artery dissection. Lancet Neurol. 2015;14:640–54.

    Article  PubMed  Google Scholar 

  35. Sasaki O, Ogawa H, Koike T, Koizumi T, Tanaka R. A clinicopathological study of dissecting aneurysms of the intracranial vertebral artery. J Neurosurg. 1991;75:874–82.

    PubMed  CAS  Google Scholar 

  36. Ro A, Kageyama N, Abe N, Takatsu A, Fukunaga T. Intracranial vertebral artery dissection resulting in fatal subarachnoid hemorrhage: clinical and histopathological investigations from a medicolegal perspective. J Neurosurg. 2009;110:948–54.

    PubMed  Google Scholar 

  37. Sakurai K, Miura T, Sagisaka T, Hattori M, Matsukawa N, Mase M, Kasai H, Arai N, Kawai T, Shimohira M, Yamawaki T, Shibamoto Y. Evaluation of luminal and vessel wall abnormalities in subacute and other stages of intracranial vertebrobasilar artery dissections using the volume isotropic turbo-spin-echo acquisition (VISTA) sequence: a preliminary study. J Neuroradiol. 2013;40:19–28.

    PubMed  Google Scholar 

  38. Natori T, Sasaki M, Miyoshi M, Ohba H, Oura MY, Narumi S, Harada T, Kabasawa H, Terayama Y. Detection of vessel wall lesions in spontaneous symptomatic vertebrobasilar artery dissection using T1-weighted 3-dimensional imaging. J Stroke Cerebrovasc Dis. 2014;23:2419–24.

    Article  PubMed  Google Scholar 

  39. Arai D, Satow T, Komuro T, Kobayashi A, Nagata H, Miyamoto S. Evaluation of the arterial wall in vertebrobasilar artery dissection using high-resolution magnetic resonance vessel wall imaging. J Stroke Cerebrovasc. 2016;25:1444–50.

    Article  Google Scholar 

  40. Alexander MD, Yuan C, Rutman A, Tirschwell DL, Palagallo G, Gandhi D, Sekhar LN, Mossa-Basha M. High-resolution intracranial vessel wall imaging: imaging beyond the lumen. J Neurol Neurosurg Psychiatry. 2016;87:589–97.

    Article  PubMed  Google Scholar 

  41. Chung JW, Kim BJ, Choi BS, Sohn CH, Bae HJ, Yoon BW, Lee SH. High-resolution magnetic resonance imaging reveals hidden etiologies of symptomatic vertebral arterial lesions. J Stroke Cerebrovasc Dis. 2014;23:293–302.

    Article  PubMed  Google Scholar 

  42. Andaluz N, Zuccarello M. Blister-like aneurysms of the anterior communicating artery: a retrospective review of diagnosis and treatment in five patients. Neurosurgery. 2008;62:807–11; discussion 811.

    Article  PubMed  Google Scholar 

  43. Horie N, Morikawa M, Fukuda S, Hayashi K, Suyama K, Nagata I. Detection of blood blister-like aneurysm and intramural hematoma with high-resolution magnetic resonance imaging: case report. J Neurosurg. 2011;115:1206–9.

    Article  PubMed  Google Scholar 

  44. Gonzalez AM, Narata AP, Yilmaz H, Bijlenga P, Radovanovic I, Schaller K, Lovblad KO, Pereira VM. Blood blister-like aneurysms: single center experience and systematic literature review. Eur J Radiol. 2014;83:197–205.

    PubMed  Google Scholar 

  45. Lehman VT, Brinjikji W, Mossa-Basha M, Lanzino G, Rabinstein AA, Kallmes DF, Huston J. Conventional and high-resolution vessel wall MRI of intracranial aneurysms: current concepts and new horizons. J Neurosurg. 2018;128:969–81.

    PubMed  Google Scholar 

  46. Mitobe Y, Kondo R, Yamaki T, Saito G, Saito S, Sonoda Y. Magnetic Resonance Vessel Wall Imaging Reveals a Ruptured Blood Blister-like Aneurysm: A Case Report. No Shinkei Geka. 2018;46:1087–91.

    PubMed  Google Scholar 

  47. Nakatomi H, Segawa H, Kurata A, Shiokawa Y, Nagata K, Kamiyama H, Ueki K, Kirino T. Clinicopathological study of intracranial fusiform and dolichoectatic aneurysms: insight on the mechanism of growth. Stroke. 2000;31:896–900.

    Article  PubMed  CAS  Google Scholar 

  48. Saito A, Fujimura M, Endo H, Omodaka S, Kanoke A, Sato K, Tominaga T. Diagnostic Value of Contrast-Enhanced Magnetic Resonance Vessel Wall Imaging on the Onset Type of Vertebral Artery Dissection. Cerebrovasc Dis. 2019;48:124–31.

    Article  PubMed  Google Scholar 

  49. Sakata N, Takebayashi S, Kojima M, Masawa N, Suzuki K, Takatama M. Pathology of a dissecting intracranial aneurysm. Neuropathology. 2000;20:104–8.

    Article  PubMed  CAS  Google Scholar 

  50. Ishikawa T, Nakamura N, Houkin K, Nomura M. Pathological consideration of a “blister-like” aneurysm at the superior wall of the internal carotid artery: case report. Neurosurgery. 1997;40:403–5. discussion 5–6.

    Article  PubMed  CAS  Google Scholar 

  51. Mizutani T, Miki Y, Kojima H, Suzuki H. Proposed classification of nonatherosclerotic cerebral fusiform and dissecting aneurysms. Neurosurgery. 1999;45:253–9. discussion 9–60.

    Article  PubMed  CAS  Google Scholar 

  52. Endo S, Takaba M, Ogiichi T, Kurimoto M, Nishijima M, Takaku A. Pathological study of Intracranial artery dissection with subarachnoid hemorrhage. Surg Cereb Stroke. 1997;25:169–76.

    Article  Google Scholar 

  53. Park SH, Yim MB, Lee CY, Kim E, Son EI. Intracranial fusiform aneurysms: it’s pathogenesis, clinical characteristics and managements. J Korean Neurosurg Soc. 2008;44:116–23.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Day AL, Gaposchkin CG, Yu CJ, Rivet DJ, Dacey RG Jr.. Spontaneous fusiform middle cerebral artery aneurysms: characteristics and a proposed mechanism of formation. J Neurosurg. 2003;99:228–40.

    Article  PubMed  Google Scholar 

  55. Sim SY, Chung J, Shin YS. Are blood blister-like aneurysms a specific type of dissection? A comparative study of blood blister-like aneurysms and ruptured mizutani type 4 vertebral artery dissections. J Korean Neurosurg Soc. 2014;56:395–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

The study was supported by a Korea University Guro Hospital “KOREA RESEARCH-DRIVEN HOSPITALS” Grant (O1903981).

Author Contributions

Conception and design: Hye Na Jung, Sang-il Suh; acquisition of data: all authors; analysis and interpretation of the data: Hye Na Jung, Sang-il Suh; drafting the article: Hye Na Jung; critically revising the article: Sang-il Suh; reviewing the submitted version of the manuscript: all authors. Approving the final version of the manuscript on behalf of all authors: Sang-il Suh.

Author information

Authors and Affiliations

  1. Department of Radiology, Guro Hospital, Korea University College of Medicine, 148 Guro-dong, 08308, Guro-gu, Seoul, Korea (Republic of)

    Hye Na Jung, Sang-il Suh & Inseon Ryoo

  2. Siemens Healthineers Ltd., Seoul, Korea (Republic of)

    InSeong Kim

Authors
  1. Hye Na Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sang-il Suh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Inseon Ryoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. InSeong Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sang-il Suh.

Ethics declarations

Conflict of interest

H.N. Jung, S. Suh, I. Ryoo and I. Kim declare that they have no competing interests.

Ethical standards

For this article no studies with human participants or animals were performed by any of the authors. All studies mentioned were in accordance with the ethical standards indicated in each case. This retrospective study was performed after consultation with the institutional ethics committee and in accordance with national legal requirements. Ethics approval 2020GR0195. Consent to participate waived for this retrospective review.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jung, H.N., Suh, Si., Ryoo, I. et al. Usefulness of 3D High-resolution Vessel Wall MRI in Diffuse Nonaneurysmal SAH Patients. Clin Neuroradiol 31, 1071–1081 (2021). https://doi.org/10.1007/s00062-021-01018-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00062-021-01018-0

Keywords

Search

Navigation