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Repeat Catheter Angiography in Patients with Aneurysmal-Pattern Angiographically Negative Subarachnoid Hemorrhage

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Abstract

Background

A significant proportion of patients with subarachnoid hemorrhage have a normal cerebral angiogram. Patients with angiographically negative subarachnoid hemorrhage (anSAH) with either perimesencephalic- (panSAH) or aneurysmal-pattern hemorrhage (aanSAH, also known as diffuse anSAH) have an excellent prognosis, but only if underlying vascular abnormalities are completely excluded. The rate of occult aneurysms in patients with aanSAH varies widely across studies. The purpose of this study was to quantify the value of repeat DSA in these patients.

Methods

We reviewed the records of all patients initially diagnosed with aanSAH after a screening DSA at a single tertiary neurovascular referral center from January 2006–April 2018. Patients with panSAH and traumatic SAH were excluded. We also performed a systematic review and meta-analysis of positive second DSAs in previously published case series of patients with aanSAH who underwent two serial DSAs. For meta-analysis, PubMed Central, MEDLINE and Cochrane Library databases were searched for pertinent studies up to November 2019. The rate of aneurysm detection on repeat angiography was extracted from each study. Pooled rates for positive second angiogram were calculated as untransformed proportions in a binary random-effects model meta-analysis. Inter-study heterogeneity was calculated using an I2 statistic.

Results

Three of 27 patients (11.1%) with aanSAH and at least two DSAs were subsequently found to have a cerebral aneurysm in our institutional dataset. Twenty-six studies in our systematic review met inclusion criteria, and the pooled rate of positive second angiogram was 10.4% (95% CI 7.3%—13.5%, P < 0.001). Substantial inter-study heterogeneity was observed in the meta-analysis (I2 = 61.7%, P < 0.001).

Conclusions

One in 10 patients with aanSAH has an occult ruptured aneurysm. A second-look DSA should be strongly considered in these cases.

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Abbreviations

anSAH:

Angiographically negative subarachnoid hemorrhage

DSA:

Digital subtraction angiography

SAH:

Subarachnoid hemorrhage

References

  1. Nesvick CL, Oushy S, Rinaldo L, et al. Clinical complications and outcomes of angiographically negative subarachnoid hemorrhage. Neurology. 2019;92:e2385-94.

    Article  PubMed  Google Scholar 

  2. Rinkel GJ, Wijdicks EF, Hasan D, et al. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet. 1991;338:964–8.

    Article  CAS  PubMed  Google Scholar 

  3. Rinkel GJ, Wijdicks EF, Vermeulen M, et al. The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol. 1991;29:463–8.

    Article  CAS  PubMed  Google Scholar 

  4. Mensing LA, Vergouwen MDI, Laban KG, et al. Perimesencephalic hemorrhage: a review of epidemiology, risk factors, presumed cause, clinical course, and outcome. Stroke. 2018;49:1363–70.

    Article  PubMed  Google Scholar 

  5. Kalra VB, Wu X, Matouk CC, et al. Use of follow-up imaging in isolated perimesencephalic subarachnoid hemorrhage: a meta-analysis. Stroke. 2015;46:401–6.

    Article  PubMed  Google Scholar 

  6. Geng B, Wu X, Brackett A, et al. Meta-analysis of recent literature on utility of follow-up imaging in isolated perimesencephalic hemorrhage. Clin Neurol Neurosurg. 2019;180:111–6.

    Article  PubMed  Google Scholar 

  7. Germans MR, Coert BA, Majoie CB, et al. Yield of spinal imaging in nonaneurysmal, nonperimesencephalic subarachnoid hemorrhage. Neurology. 2015;84:1337–40.

    Article  CAS  PubMed  Google Scholar 

  8. Khan AA, Smith JD, Kirkman MA, et al. Angiogram negative subarachnoid haemorrhage: outcomes and the role of repeat angiography. Clin Neurol Neurosurg. 2013;115:1470–5.

    Article  CAS  PubMed  Google Scholar 

  9. Kaim A, Proske M, Kirsch E, et al. Value of repeat-angiography in cases of unexplained subarachnoid hemorrhage (SAH). Acta Neurol Scand. 1996;93:366–73.

    Article  CAS  PubMed  Google Scholar 

  10. Connolly ES Jr, 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.

    Article  PubMed  Google Scholar 

  11. van Gijn J, van Dongen KJ, Vermeulen M, et al. Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology. 1985;35:493–7.

    Article  PubMed  Google Scholar 

  12. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Gupta SK, Gupta R, Khosla VK, et al. Nonaneurysmal nonperimesencephalic subarachnoid hemorrhage: is it a benign entity? Surg Neurol. 2009;71:566–71 (discussion 571, 571–562, 572).

    Article  PubMed  Google Scholar 

  14. Fontanella M, Rainero I, Panciani PP, et al. Subarachnoid hemorrhage and negative angiography: clinical course and long-term follow-up. Neurosurg Rev. 2011;34:477–84.

    Article  PubMed  Google Scholar 

  15. Bakker NA, Groen RJ, Foumani M, et al. Repeat digital subtraction angiography after a negative baseline assessment in nonperimesencephalic subarachnoid hemorrhage: a pooled data meta-analysis. J Neurosurg. 2014;120:99–103.

    Article  PubMed  Google Scholar 

  16. 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 (discussion 1047).

    Article  PubMed  Google Scholar 

  17. Delgado Almandoz JE, Jagadeesan BD, Refai D, et al. 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 

  18. Yu DW, Jung YJ, Choi BY, et al. Subarachnoid hemorrhage with negative baseline digital subtraction angiography: is repeat digital subtraction angiography necessary? J Cerebrovasc Endovasc Neurosurg. 2012;14:210–5.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Agid R, Andersson T, Almqvist H, et al. 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  CAS  PubMed  PubMed Central  Google Scholar 

  20. Little AS, Garrett M, Germain R, et al. Evaluation of patients with spontaneous subarachnoid hemorrhage and negative angiography. Neurosurgery. 2007;61:1139–50 (discussion 1150–1131).

    Article  PubMed  Google Scholar 

  21. Dalyai R, Chalouhi N, Theofanis T, et al. 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 651–642).

    PubMed  Google Scholar 

  22. Topcuoglu MA, Ogilvy CS, Carter BS, et al. Subarachnoid hemorrhage without evident cause on initial angiography studies: diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg. 2003;98:1235–40.

    Article  PubMed  Google Scholar 

  23. Rogg JM, Smeaton S, Doberstein C, et al. Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage. AJR Am J Roentgenol. 1999;172:201–6.

    Article  CAS  PubMed  Google Scholar 

  24. Jung JY, Kim YB, Lee JW, et al. Spontaneous subarachnoid haemorrhage with negative initial angiography: a review of 143 cases. J Clin Neurosci. 2006;13:1011–7.

    Article  PubMed  Google Scholar 

  25. Kumar R, Das KK, Sahu RK, et al. Angio negative spontaneous subarachnoid hemorrhage: Is repeat angiogram required in all cases? Surg Neurol Int. 2014;5:125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Moscovici S, Fraifeld S, Ramirez-de-Noriega F, et al. Clinical relevance of negative initial angiogram in spontaneous subarachnoid hemorrhage. Neurol Res. 2013;35:117–22.

    Article  PubMed  Google Scholar 

  27. Maslehaty H, Petridis AK, Barth H, et al. Diagnostic value of magnetic resonance imaging in perimesencephalic and nonperimesencephalic subarachnoid hemorrhage of unknown origin. J Neurosurg. 2011;114:1003–7.

    Article  PubMed  Google Scholar 

  28. Khan N, Schuknecht B, Yonekawa Y. Presentation and management of patients with initial negative 4-vessel cerebral angiography in subarachnoid hemorrhage. Acta Neurochir Suppl. 2002;82:71–81.

    CAS  PubMed  Google Scholar 

  29. Hashimoto H, Iida J, Hironaka Y, et al. Use of spiral computerized tomography angiography in patients with subarachnoid hemorrhage in whom subtraction angiography did not reveal cerebral aneurysms. J Neurosurg. 2000;92:278–83.

    Article  CAS  PubMed  Google Scholar 

  30. Canhao P, Ferro JM, Pinto AN, et al. Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms. Acta Neurochir (Wien). 1995;132:14–9.

    Article  CAS  Google Scholar 

  31. Zhong W, Zhao P, Wang D, et al. Different clinical characteristics between perimesencephalic subarachnoid hemorrhage and diffuse subarachnoid hemorrhage with negative initial angiography. Turk Neurosurg. 2014;24:327–32.

    PubMed  Google Scholar 

  32. Berdoz D, Uske A, de Tribolet N. Subarachnoid haemorrhage of unknown cause: clinical, neuroradiological and evolutive aspects. J Clin Neurosci. 1998;5:274–82.

    Article  CAS  PubMed  Google Scholar 

  33. Delgado Almandoz JE, Crandall BM, Fease JL, et al. Diagnostic yield of catheter angiography in patients with subarachnoid hemorrhage and negative initial noninvasive neurovascular examinations. AJNR Am J Neuroradiol. 2013;34:833–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bashir A, Mikkelsen R, Sorensen L, et al. Non-aneurysmal subarachnoid hemorrhage: when is a second angiography indicated? Neuroradiol J. 2018;31:244–52.

    Article  PubMed  Google Scholar 

  35. Yap L, Dyde RA, Hodgson TJ, et al. Spontaneous subarachnoid hemorrhage and negative initial vascular imaging–should further investigation depend upon the pattern of hemorrhage on the presenting CT? Acta Neurochir (Wien). 2015;157:1477–84.

    Article  CAS  Google Scholar 

  36. Rouchaud A, Lehman VT, Murad MH, et al. Nonaneurysmal perimesencephalic hemorrhage is associated with deep cerebral venous drainage anomalies: a systematic literature review and meta-analysis. AJNR Am J Neuroradiol. 2016;37:1657–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dietrich HH, Dacey RG Jr. Molecular keys to the problems of cerebral vasospasm. Neurosurgery. 2000;46:517–30.

    Article  CAS  PubMed  Google Scholar 

  38. Nishizawa S, Laher I. Signaling mechanisms in cerebral vasospasm. Trends Cardiovasc Med. 2005;15:24–34.

    Article  CAS  PubMed  Google Scholar 

  39. Ishiguro M, Morielli AD, Zvarova K, et al. Oxyhemoglobin-induced suppression of voltage-dependent K+ channels in cerebral arteries by enhanced tyrosine kinase activity. Circ Res. 2006;99:1252–60.

    Article  CAS  PubMed  Google Scholar 

  40. Schievink WI, Wijdicks EF. Origin of pretruncal nonaneurysmal subarachnoid hemorrhage: ruptured vein, perforating artery, or intramural hematoma? Mayo Clin Proc. 2000;75:1169–73.

    Article  CAS  PubMed  Google Scholar 

  41. Yue H, Ling W, Ou Y, et al. Intracranial subarachnoid hemorrhage resulting from non-cervical spinal arteriovenous lesions: analysis of possible cause of bleeding and literature review. Clin Neurol Neurosurg. 2019;184:105371.

    Article  PubMed  Google Scholar 

  42. Prestigiacomo CJ, Sabit A, He W, et al. Three dimensional CT angiography versus digital subtraction angiography in the detection of intracranial aneurysms in subarachnoid hemorrhage. J Neurointerv Surg. 2010;2:385–9.

    Article  PubMed  Google Scholar 

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Authors

Contributions

CLN, EFW, GL and AAR conceived the study and contributed to its design. CLN, SO, KR and LR collected the data. CLN and PK performed statistical analyses. CLN drafted the manuscript. All authors discussed the results and provided critical feedback on the final manuscript.

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Correspondence to Cody L. Nesvick.

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This study was performed with Institutional Review Board (IRB) approval for minimal-risk human studies research.

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Nesvick, C.L., Oushy, S., Ravindran, K. et al. Repeat Catheter Angiography in Patients with Aneurysmal-Pattern Angiographically Negative Subarachnoid Hemorrhage. Neurocrit Care 36, 52–60 (2022). https://doi.org/10.1007/s12028-021-01247-8

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  • DOI: https://doi.org/10.1007/s12028-021-01247-8

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