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Clinical Neuroradiology

, Volume 27, Issue 2, pp 175–183 | Cite as

High-Resolution Vessel Wall Magnetic Resonance Imaging in Angiogram-Negative Non-Perimesencephalic Subarachnoid Hemorrhage

  • J. M. Coutinho
  • R. H. Sacho
  • J. D. Schaafsma
  • R. Agid
  • T. Krings
  • I. Radovanovic
  • C. C. Matouk
  • D. J. Mikulis
  • D. M. Mandell
Original Article

Abstract

Purpose

Standard magnetic resonance imaging (MRI) rarely identifies the cause of hemorrhage in patients with an angiogram-negative, non-perimesencephalic subarachnoid hemorrhage (SAH). Yet up to 10 % of these patients have recurrent hemorrhage. The aim of the study was to explore the potential role of high-resolution contrast-enhanced 3-Tesla vessel wall-MRI in patients with angiogram-negative SAH.

Methods

We performed intracranial vessel wall-MRI of the circle of Willis using a 3-Tesla scanner in consecutive patients presenting with a spontaneous, angiogram-negative, non-perimesencephalic SAH. Vessel wall-MRI included T1-, T2-, and gadolinium-enhanced T1-weighted two-dimensional black-blood sequences in multiple planes (voxel size 0.4 × 0.4 × 2.0 mm). Two neuroradiologists independently scored abnormalities of the arterial wall.

Results

In all, 11 patients (mean age 59 years) underwent vessel wall-MRI. A total of seven patients had vessel wall abnormalities despite normal catheter angiography. Two patients had focal abnormalities contiguous with the outer margin of the basilar artery wall for which we considered a differential of ruptured blood blister aneurysm, thrombosed aneurysm, and loculated extramural blood from elsewhere. Two patients had arterial wall enhancement involving multiple arteries, possibly secondary to SAH. Three patients had arterial wall enhancement at sites of dural penetration, remote from the SAH, likely related to age and atherosclerotic risk factors. Vessel wall-MRI did not alter patient management in this cohort.

Conclusion

Vessel wall-MRI showed abnormalities in seven patients with angiogram-negative SAH. These findings did not alter patient management, but the findings may be useful for other physicians who choose to perform vessel wall-MRI in this patient population.

Keywords

Subarachnoid Hemorrhage Intracranial aneurysm Magnetic resonance imaging High-resolution vessel wall magnetic resonance imaging 

References

  1. 1.
    van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain. 2001;124:249–78.CrossRefPubMedGoogle Scholar
  2. 2.
    Boswell S, Thorell W, Gogela S, Lyden E, Surdell D. Angiogram-negative subarachnoid hemorrhage: outcomes data and review of the literature. J Stroke Cerebrovasc Dis. 2013;22:750–7.CrossRefPubMedGoogle Scholar
  3. 3.
    Aviv RI, Shad A, Tomlinson G, Niemann D, Teddy PJ, Molyneux AJ, Byrne JV. Cervical dural arteriovenous fistulae manifesting as subarachnoid hemorrhage: report of two cases and literature review. AJNR Am J Neuroradiol. 2004;25:854–8.PubMedGoogle Scholar
  4. 4.
    Nicastro N, Schnider A, Leemann B. Anaplastic medullary ependymoma presenting as subarachnoid hemorrhage. Case Rep Neurol Med. 2013;2013:701820.PubMedPubMedCentralGoogle Scholar
  5. 5.
    van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369:306–18.CrossRefPubMedGoogle Scholar
  6. 6.
    Konczalla J, Schuss P, Platz J, Vatter H, Seifert V, Guresir 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.CrossRefPubMedGoogle Scholar
  7. 7.
    Maslehaty H, Barth H, Petridis AK, Doukas A, Maximilian Mehdorn H. Special features of subarachnoid hemorrhage of unknown origin: a review of a series of 179 cases. Neurol Res. 2012;34:91–7.CrossRefPubMedGoogle Scholar
  8. 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. 2014:1–8.Google Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 11.
    Woodfield J, Rane N, Cudlip S, Byrne JV. Value of delayed MRI in angiogram-negative subarachnoid haemorrhage. Clin Radiol. 2014;69:350–6.CrossRefPubMedGoogle Scholar
  12. 12.
    Andaluz N, Zuccarello M. Yield of further diagnostic work-up of cryptogenic subarachnoid hemorrhage based on bleeding patterns on computed tomographic scans. Neurosurgery. 2008;62:1040–6.CrossRefPubMedGoogle Scholar
  13. 13.
    Rogg JM, Smeaton S, Doberstein C, Goldstein JH, Tung GA, Haas RA. Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage. AJR Am J Roentgenol. 1999;172:201–6.CrossRefPubMedGoogle Scholar
  14. 14.
    Topcuoglu MA, Ogilvy CS, Carter BS, Buonanno FS, Koroshetz WJ, Singhal AB. Subarachnoid hemorrhage without evident cause on initial angiography studies: diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg. 2003;98:1235–40.CrossRefPubMedGoogle Scholar
  15. 15.
    Matouk CC, Mandell DM, Gunel 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.CrossRefPubMedGoogle Scholar
  16. 16.
    Mandell DM, Matouk CC, Farb RI, Krings T, Agid R, terBrugge K, Willinsky RA, Swartz RH, Silver FL, Mikulis DJ. Vessel wall MRI to differentiate between reversible cerebral vasoconstriction syndrome and central nervous system vasculitis: preliminary results. Stroke. 2012;43:860–2.CrossRefPubMedGoogle Scholar
  17. 17.
    Power S, Matouk C, Casaubon LK, Silver FL, Krings T, Mikulis DJ, Mandell DM. Vessel wall magnetic resonance imaging in acute ischemic stroke: effects of embolism and mechanical thrombectomy on the arterial wall. Stroke. 2014;45:2330–4.CrossRefPubMedGoogle Scholar
  18. 18.
    Obusez EC, Hui F, Hajj-Ali RA, Cerejo R, Calabrese LH, Hammad T, Jones SE. 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.CrossRefPubMedGoogle Scholar
  19. 19.
    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.CrossRefPubMedGoogle Scholar
  20. 20.
    Bradley WG Jr. MR appearance of hemorrhage in the brain. Radiology. 1993;189:15–26.CrossRefPubMedGoogle Scholar
  21. 21.
    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. J Neurosurg. 2011;115:1206–9.CrossRefPubMedGoogle Scholar
  22. 22.
    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.CrossRefPubMedGoogle Scholar
  23. 23.
    Aoki S, Shirouzu I, Sasaki Y, Okubo T, Hayashi N, Machida T, Hoshi E, Suzuki K, Funada N, Araki T. Enhancement of the intracranial arterial wall at MR imaging: relationship to cerebral atherosclerosis. Radiology. 1995;194:477–81.CrossRefPubMedGoogle Scholar
  24. 24.
    Mossa-Basha M, Hwang WD, De Havenon A, Hippe D, Balu N, Becker KJ, Tirschwell DT, Hatsukami T, Anzai Y, Yuan C. Multicontrast high-resolution vessel wall magnetic resonance imaging and its value in differentiating intracranial vasculopathic processes. Stroke. 2015;46:1567–73.CrossRefPubMedGoogle Scholar
  25. 25.
    van der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ. Venous drainage in perimesencephalic hemorrhage. Stroke. 2004;35:1614–8.CrossRefPubMedGoogle Scholar
  26. 26.
    Ambrose N, Pierce IT, Gatehouse PD, Haskard DO, Firmin DN. Magnetic resonance imaging of vein wall thickness in patients with Behcet’s syndrome. Clin Exp Rheumatol. 2014;32:S99–102.PubMedGoogle Scholar
  27. 27.
    Maslehaty H, Petridis AK, Barth H, Mehdorn HM. Diagnostic value of magnetic resonance imaging in perimesencephalic and nonperimesencephalic subarachnoid hemorrhage of unknown origin. J Neurosurg. 2011;114:1003–7.CrossRefPubMedGoogle Scholar
  28. 28.
    Qiao Y, Steinman DA, Qin Q, Etesami M, Schar M, Astor BC, Wasserman BA. Intracranial arterial wall imaging using three-dimensional high isotropic resolution black blood MRI at 3.0 T. J Magn Reson Imaging. 2011;34:22–30.CrossRefPubMedGoogle Scholar
  29. 29.
    Konczalla J, Platz J, Schuss P, Vatter H, Seifert V, Guresir E. Non-aneurysmal non-traumatic subarachnoid hemorrhage: patient characteristics, clinical outcome and prognostic factors based on a single-center experience in 125 patients. BMC Neurol. 2014;14:140.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wang Y, Lou X, Li Y, Sui B, Sun S, Li C, Jiang P, Siddiqui A, Yang X. Imaging investigation of intracranial arterial dissecting aneurysms by using 3 T high-resolution MRI and DSA: from the interventional neuroradiologists’ view. Acta Neurochir (Wien). 2014;156:515–25.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • J. M. Coutinho
    • 1
  • R. H. Sacho
    • 1
  • J. D. Schaafsma
    • 2
  • R. Agid
    • 1
  • T. Krings
    • 1
  • I. Radovanovic
    • 3
  • C. C. Matouk
    • 4
  • D. J. Mikulis
    • 1
  • D. M. Mandell
    • 1
  1. 1.Division of Neuroradiology, Department of Medical ImagingToronto Western Hospital, University Health Network and the University of TorontoTorontoCanada
  2. 2.Division of Neurology, Department of MedicineUniversity Health Network and the University of TorontoTorontoCanada
  3. 3.Division of Neurosurgery, Department of SurgeryUniversity Health Network and the University of TorontoTorontoCanada
  4. 4.Departments of Diagnostic Radiology and NeurosurgeryYale University School of MedicineNew HavenUSA

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