Skip to main content

Vasospasm after spontaneous angiographically negative subarachnoid hemorrhage

Acta Neurochirurgica volume 154, pages 1127–1133 (2012)Cite this article

Abstract

Background

Vasospasm, delayed infarcts and clinical deterioration due to delayed cerebral ischemia (CD-DCI) following digital subtraction angiography (DSA)-negative, spontaneous subarachnoid hemorrhage (SAH) are infrequently and inconsistently described in the literature.

Methods

To quantify and characterize rates of each, we reviewed our own series of 77 patients with DSA-negative, spontaneous SAH. Employing a PubMed search, we reviewed the literature and calculated directly adjusted overall rates of vasospasm, delayed infarcts and CD-DCI.

Results

In our own patient cohort, 26 % of patients suffered vasospasm, 4 % delayed infarcts and 4 % CD-DCI. Higher Hunt-Hess grade and diffuse SAH pattern were associated with higher rates of each. Incorporating results from 18 studies in the literature, the directly adjusted overall rate of vasospasm following DSA-negative SAH was 16.3 % (95 % CI 12.3-21.1). Adjusted overall rates of delayed infarcts and CD-DCI were 3.4 % (95 % CI 1.9-5.5) and 6.8 % (95 % CI 5.0-9.1), respectively. For the subgroup of patients with diffuse SAH, the rates of vasospasm and CD-DCI were 31.3 % (95 % CI 21.6-43.9) and 9.7 % (95 % CI 7.0-13.0), respectively, while in patients with perimesencephalic SAH, respective rates were 13.1 % (95 % CI 7.7-20.7) and 2.4 % (95 % CI 1.0-4.8). A mixed-effects meta-analysis revealed an odds ratio for CD-DCI in diffuse SAH compared to perimesencephalic SAH of 3.79 (p = 0.009).

Conclusion

Although they are seen less frequently in patients with DSA-negative spontaneous SAH, vasospasm, delayed infarcts and CD-DCI do occur and may require endovascular therapy. Risk factors include a diffuse hemorrhage pattern and higher Hunt-Hess grade.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2

References

  1. Andaluz N, Zuccarello M (2008) Yield of further diagnostic work-up of cryptogenic subarachnoid hemorrhage based on bleeding patterns on computed tomographic scans. Neurosurgery 62:1040–1047

    PubMed  Article  Google Scholar 

  2. Artiola Fortuny L, Prieto-Valiente L (1981) Long-term prognosis in surgically treated intracranial aneurysms. Part 2: morbidity. J Neurosurg 54:35–43

    Article  CAS  Google Scholar 

  3. Barlow P (1992) Incidence of delayed cerebral ischemia following subarachnoid hemorrhage of unknown cause. J Neurol Neurosurg Psychiatry 48:132–136

    Article  Google Scholar 

  4. Brisman J, Sundbarg G (1985) Subarachnoid haemorrhage of unknown origin: prognosis and prognostic factors. J Neurosurg 63:349–354

    Article  Google Scholar 

  5. Canhao P, Ferro JM, Pinto AN, Melo TP, Campos JG (1995) Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms. Acta Neurochir (Wien) 132:14–19

    Article  CAS  Google Scholar 

  6. Cioffi F, Pasqualin A, Cavazzani P, Da Pian R (1989) Subarachnoid hemorrhage of unknown origin: clinical and tomographical aspects. Acta Neurochir (Wien) 97:31–39

    Article  CAS  Google Scholar 

  7. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    PubMed  Article  CAS  Google Scholar 

  8. Dorsch NWC, King MT (1994) A review of cerebral vasospasm in aneurysmal subarachnoid hemorrhage. Part 1: incidence and effects. J Clin Neurosci 1:19–26

    PubMed  Article  CAS  Google Scholar 

  9. Duong H, Melançon D, Tampieri D, Ethier R (1996) The negative angiogram in subarachnoid haemorrhage. Neuroradiology 38:15–19

    PubMed  Article  CAS  Google Scholar 

  10. Fisher CM, Roberson GH, Ojemann RG (1977) Cerebral vasospasm with ruptured saccular aneurysm—the clinical manifestations. Neurosurgery 1:245–248

    PubMed  Article  CAS  Google Scholar 

  11. Fontanella M, Rainero I, Panciani PP, Schatlo B, Benevello C, Garbossa D, Carlino C, Valfre W, Griva F, Bradac GB, Ducati A (2011) Subarachnoid hemorrhage and negative angiography: clinical course and long-term follow-up. Neurosurg Rev 34:477–484

    PubMed  Article  Google Scholar 

  12. Gupta SK, Gupta R, Khosla VK, Mohindra S, Chhabra R, Khandelwal N, Gupta V, Mukherjee KK, Tewari MK, Pathak A, Mathuriya SN (2009) Nonaneurysmal nonperimesecephalic subarachnoid hemorrhage: is it a benign entity? Surg Neurol 71:566–571

    PubMed  Article  Google Scholar 

  13. Hsu W, Pradilla G, Garonzik IM, Conway JE (2010) Pretruncal nonaneurysmal subarachnoid hemorrhage causing basilar artery vasospasm. Neurocrit Care 13:256–260

    PubMed  Article  Google Scholar 

  14. Hui FK, Tumialán LM, Tanaka T, Cawley CM, Zhang YJ (2009) Clinical differences between angiographically negative, diffuse subarachnoid hemorrhage and perimesencephalic subarachnoid hemorrhage. Neurocrit Care 11:64–70

    PubMed  Article  Google Scholar 

  15. Ildan F, Tuna M, Erman T, Gocer AI, Cetinalp E (2002) Prognosis and prognostic factors in nonaneurysmal perimesencephalic hemorrhage: a follow-up study in 29 patients. Surg Neurol 57:160–165

    PubMed  Article  Google Scholar 

  16. Kang DH, Park J, Lee SH, Park SH, Kim YS, Hamm IS (2009) Does non-perimesencephalic type non-aneurysmal subarachnoid hemorrhage have a benign prognosis? J Clin Neurosci 16:904–908

    PubMed  Article  Google Scholar 

  17. Kawamura S, Yasui N (1990) Clinical and long-term follow-up study in patients with spontaneous subarachnoid haemorrhage of unknown aetiology. Acta Neurochir 106:110–114

    Article  CAS  Google Scholar 

  18. Qureshi AI, Sung GY, Razumovsky AY, Lane K, Straw RN, Ulatowski JA (2000) Early identification of patients at risk for symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. Crit Care Med 28:984–990

    PubMed  Article  CAS  Google Scholar 

  19. Rinkel GJ, Wijdicks EFM, Hasan D, Kienstra GEM, Franke CL, Hageman LM, Vermeulen M, van Gijn J (1991) Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet 338:964–968

    PubMed  Article  CAS  Google Scholar 

  20. Ropper AH, Zervas NT (1984) Outcome 1 year after SAH from cerebral aneurysm. Management morbidity, mortality, and functional status in 112 consecutive good-risk patients. J Neurosurg 60:909–915

    PubMed  Article  CAS  Google Scholar 

  21. Schaller C, Rauseiser B, Rohde V, Hassler W (1996) Cerebral vasospasm after subarachnoid hemorrhage of unknown aetiology: a clinical and transcranial Doppler study. Acta Neurochir (Wien) 138:560–568

    Article  CAS  Google Scholar 

  22. Schievink WI, Wijdicks EF, Spetzler RF (2000) Diffuse vasospasm after pretruncal nonaneurysmal subarachnoid hemorrhage. AJNR Am J Neuroradiol 21:521–523

    PubMed  CAS  Google Scholar 

  23. Schwartz TH, Solomon RA (1996) Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery 39:433–440

    PubMed  CAS  Google Scholar 

  24. Sheehan JM, Cloft H, Kassell NF (2000) Symptomatic delayed arterial spasm following non-aneurysmal perimesencephalic subarachnoid hemorrhage: a case report and review of the literature. Acta Neurochir (Wien) 142:709–712

    Article  CAS  Google Scholar 

  25. Topcuoglu MA, Ogilvy CS, Carter BS, Buonanno FS, Koroshetz WJ, Singhal AB (2003) Subarachnoid hemorrhage without evident cause on initial angiography studies: diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg 98:1235–1240

    PubMed  Article  Google Scholar 

  26. Van Calenbergh F, Plets C, Goffin J, Velghe L (1993) Nonaneurysmal subarachnoid hemorrhage: prevalence of perimesencephalichemorrhage in a consecutive series. Surg Neurol 39:320–323

    PubMed  Article  Google Scholar 

  27. Vergouwen MDI, Vermeulen M, Gijn J, Rinkel GJE, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, Macdonald RL, Diringer MN, Broderick JP, Dreier JP, Roos Y (2010) Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies. Stroke 41:2391–2395

    PubMed  Article  Google Scholar 

  28. Whiting J, Reavey-Cantwell J, Velat G, Fautheree G, Firment C, Lewis S, Hoh B (2009) Clinical course of nontraumatic, nonaneurysmal subarachnoid hemorrhage: a single-institution experience. Neurosurg Focus 26:E21

    PubMed  Article  Google Scholar 

  29. Wijdicks EF, Schievink WI, Miller GM (1998) Pretruncal nonaneurysmal subarachnoid hemorrhage. Mayo Clin Proc 73:745–752

    PubMed  Article  CAS  Google Scholar 

Download references

Conflicts of interest

None.

Author information

Authors and Affiliations

  1. Department of Neurological Surgery, Brigham and Women’s Hospital and Harvard Medical School, 75 Francis St, Boston, MA, 02115, USA

    Bradley A. Gross, Ning Lin, Kai U. Frerichs & Rose Du

Authors
  1. Bradley A. Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ning Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kai U. Frerichs
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rose Du
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rose Du.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gross, B.A., Lin, N., Frerichs, K.U. et al. Vasospasm after spontaneous angiographically negative subarachnoid hemorrhage. Acta Neurochir 154, 1127–1133 (2012). https://doi.org/10.1007/s00701-012-1383-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-012-1383-4

Keywords

  • Angiogram negative SAH
  • SAH
  • Vasospasm
  • Infarction
  • Delayed cerebral ischemia