The role of imaging in the management of non-traumatic subarachnoid hemorrhage: a practical review

Abstract

The purpose of this review is to understand the role of imaging in the diagnosis and management of non-traumatic subarachnoid hemorrhage (SAH). SAH is a life-threatening emergency and a relatively common entity, the most common etiology being ruptured aneurysms. Multiple conundrums exist in literature at various steps of its imaging workup: diagnosis, management, and follow-up. We target our review to highlight the most effective practice and suggest efficient workup plans based on literature search, and describe in detail the clinical diagnostic and prognostic scales, role of CT scan, lumbar puncture, and MR, including angiography in the diagnosis and workup of SAH and its complications, and try to simplify the conundrums. Practical knowledge of imaging workup of SAH can help guide correct management of these patients, so as to reduce morbidity and mortality without resource overutilization.

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References

  1. 1.

    Cohen-Gadol AA, Bohnstedt BN (2013 Oct) Recognition and evaluation of nontraumatic subarachnoid hemorrhage and ruptured cerebral aneurysm. Am Fam Physician 88(7):451–456

    PubMed  Google Scholar 

  2. 2.

    Huhtakangas J, Lehto H, Seppä K, Kivisaari R, Niemelä M, Hernesniemi J, Lehecka M (2015) Long-term excess mortality after aneurysmal subarachnoid hemorrhage: patients with multiple aneurysms at risk. Stroke 46(7):1813–1818

    PubMed  Article  Google Scholar 

  3. 3.

    Marder CP, Narla V, Fink JR, Tozer Fink KR. Subarachnoid hemorrhage: beyond aneurysms. Am J Roentgenol [Internet]. 2013 26;202(1):25–37. Available from: https://doi.org/10.2214/AJR.12.9749, Subarachnoid Hemorrhage: Beyond Aneurysms

  4. 4.

    Carpenter CR, Raja AS, Brown MD (2015) Overtesting and the downstream consequences of overtreatment: implications of “preventing overdiagnosis” for emergency medicine. Acad Emerg Med Off J Soc Acad Emerg Med 22(12):1484–1492

    Article  Google Scholar 

  5. 5.

    Dubosh NM, Bellolio MF, Rabinstein AA, Edlow JA (2016) Sensitivity of early brain computed tomography to exclude aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Stroke 47(3):750–755

    PubMed  Article  Google Scholar 

  6. 6.

    Wu W-T, Pan H-Y, Wu K-H, Huang Y-S, Wu C-H, Cheng F-J (2020) The Ottawa subarachnoid hemorrhage clinical decision rule for classifying emergency department headache patients. Am J Emerg Med 38(2):198–202

    PubMed  Article  Google Scholar 

  7. 7.

    Rosen DS, Macdonald RL (2005) Subarachnoid hemorrhage grading scales: a systematic review. Neurocrit Care 2(2):110–118

    PubMed  Article  Google Scholar 

  8. 8.

    Salmela MB, Mortazavi S, Jagadeesan BD, Broderick DF, Burns J, Deshmukh TK, Harvey HB, Hoang J, Hunt CH, Kennedy TA, Khalessi AA, Mack W, Patel ND, Perlmutter JS, Policeni B, Schroeder JW, Setzen G, Whitehead MT, Cornelius RS, Corey AS (2017) ACR Appropriateness Criteria(®) cerebrovascular disease. J Am Coll Radiol 14(5S):S34–S61

    PubMed  Article  Google Scholar 

  9. 9.

    Dankbaar JW, de Rooij NK, Velthuis BK, Frijns CJM, Rinkel GJE, van der Schaaf IC (2009) Diagnosing delayed cerebral ischemia with different CT modalities in patients with subarachnoid hemorrhage with clinical deterioration. Stroke 40(11):3493–3498

    PubMed  Article  Google Scholar 

  10. 10.

    Backes D, Rinkel GJE, Kemperman H, Linn FHH, Vergouwen MDI (2012) Time-dependent test characteristics of head computed tomography in patients suspected of nontraumatic subarachnoid hemorrhage. Stroke. 43(8):2115–2119

    PubMed  Article  Google Scholar 

  11. 11.

    Mitchell P, Wilkinson ID, Hoggard N, Paley MN, Jellinek DA, Powell T, Romanowski C, Hodgson T, Griffiths PD (2001) Detection of subarachnoid haemorrhage with magnetic resonance imaging. J Neurol Neurosurg Psychiatry 70(2):205–211 Available from: https://pubmed.ncbi.nlm.nih.gov/11160469

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Cuvinciuc V, Viguier A, Calviere L, Raposo N, Larrue V, Cognard C et al (2010) Isolated acute nontraumatic cortical subarachnoid hemorrhage. Am J Neuroradiol 31(8):1355 LP–1351362 Available from: http://www.ajnr.org/content/31/8/1355.abstract

    Article  Google Scholar 

  13. 13.

    Perry JJ, Stiell IG, Sivilotti MLA, Bullard MJ, Lee JS, Eisenhauer M, Symington C, Mortensen M, Sutherland J, Lesiuk H, Wells GA (2010) High risk clinical characteristics for subarachnoid haemorrhage in patients with acute headache: prospective cohort study. BMJ 341:c5204

    PubMed  PubMed Central  Article  Google Scholar 

  14. 14.

    Sayer D, Bloom B, Fernando K, Jones S, Benton S, Dev S, Deverapalli S, Harris T (2015) An observational study of 2,248 patients presenting with headache, suggestive of subarachnoid hemorrhage, who received lumbar punctures following normal computed tomography of the head. Acad Emerg Med Off J Soc Acad Emerg Med 22(11):1267–1273

    Article  Google Scholar 

  15. 15.

    Lansley J, Selai C, Krishnan AS, Lobotesis K, Jäger HR (2016) Subarachnoid haemorrhage guidelines and clinical practice: a cross-sectional study of emergency department consultants’ and neurospecialists’ views and risk tolerances. BMJ Open 6(9):e012357

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Connolly ESJ, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT et al (2012) Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43(6):1711–1737

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    Shimoda M, Hoshikawa K, Shiramizu H, Oda S, Matsumae M (2010) Problems with diagnosis by fluid-attenuated inversion recovery magnetic resonance imaging in patients with acute aneurysmal subarachnoid hemorrhage. Neurol Med Chir (Tokyo) 50(7):530–537

    Article  Google Scholar 

  18. 18.

    Verma RK, Kottke R, Andereggen L, Weisstanner C, Zubler C, Gralla J, Kiefer C, Slotboom J, Wiest R, Schroth G, Ozdoba C, el-Koussy M (2013) Detecting subarachnoid hemorrhage: comparison of combined FLAIR/SWI versus CT. Eur J Radiol 82(9):1539–1545

    PubMed  Article  Google Scholar 

  19. 19.

    Weimer JM, Jones SE, Frontera JA (2017) Acute cytotoxic and vasogenic edema after subarachnoid hemorrhage: a quantitative MRI study. AJNR Am J Neuroradiol 38(5):928–934

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Maslehaty H, Petridis AK, Barth H, Mehdorn HM (2011 Apr) Diagnostic value of magnetic resonance imaging in perimesencephalic and nonperimesencephalic subarachnoid hemorrhage of unknown origin. J Neurosurg 114(4):1003–1007

    PubMed  Article  Google Scholar 

  21. 21.

    Bederson JB, Connolly ESJ, Batjer HH, Dacey RG, Dion JE, Diringer MN et al (2009) 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 40(3):994–1025

    PubMed  Google Scholar 

  22. 22.

    Sailer AMH, Wagemans BAJM, Nelemans PJ, de Graaf R, van Zwam WH (2014) Diagnosing intracranial aneurysms with MR angiography: systematic review and meta-analysis. Stroke 45(1):119–126

    PubMed  Article  Google Scholar 

  23. 23.

    Chen X, Liu Y, Tong H, Dong Y, Ma D, Xu L, Yang C (2018) Meta-analysis of computed tomography angiography versus magnetic resonance angiography for intracranial aneurysm. Medicine (Baltimore) [Internet] 97(20):e10771–e10771 Available from: https://pubmed.ncbi.nlm.nih.gov/29768368

    Article  Google Scholar 

  24. 24.

    Jang M, Kim JH, Park JW, Roh H, Lee H-J, Seo J, Hwang SH, Yoon JH, Yoon SH, Cho BK (2020) Features of “false positive” unruptured intracranial aneurysms on screening magnetic resonance angiography. PLoS One [Internet] 15(9):e0238597–e0238597 Available from: https://pubmed.ncbi.nlm.nih.gov/32881975

    CAS  Article  Google Scholar 

  25. 25.

    Edlow AJ (2007) Diagnosis of subarachnoid hemorrhage. Stroke [Internet] 38(4):1129–1131. Available from:. https://doi.org/10.1161/01.STR.0000259854.65818.57

    Article  Google Scholar 

  26. 26.

    Locksley HB (1966) Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the cooperative study. J Neurosurg 25(2):219–239

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    de Gans K, Nieuwkamp DJ, Rinkel GJE, Algra A (2002) Timing of aneurysm surgery in subarachnoid hemorrhage: a systematic review of the literature. Neurosurgery 50(2):332–336

    Google Scholar 

  28. 28.

    Delgado Almandoz JE, Jagadeesan BD, Refai D, Moran CJ, Cross DT 3rd, Chicoine MR et al (2012) Diagnostic yield of repeat catheter angiography in patients with catheter and computed tomography angiography negative subarachnoid hemorrhage. Neurosurgery. 70(5):1135–1142

    PubMed  Article  Google Scholar 

  29. 29.

    Jayaraman MV, Haas RA, Do HM, Meyers PM (2010) Should CT angiography be routinely used in patients suspected of having aneurysmal subarachnoid hemorrhage? Radiology. United States 254:314–316

  30. 30.

    Westerlaan HE, van Dijk JMC, Jansen-van der Weide MC, de Groot JC, RJM G, JJA M et al (2011) Intracranial aneurysms in patients with subarachnoid hemorrhage: CT angiography as a primary examination tool for diagnosis--systematic review and meta-analysis. Radiology. 258(1):134–145

    PubMed  Article  Google Scholar 

  31. 31.

    Moran CJ (2011) Aneurysmal subarachnoid hemorrhage: DSA versus CT angiography--is the answer available? Radiology. United States 258:15–17

  32. 32.

    Yeung R, Ahmad T, Aviv RI, de Tilly LN, Fox AJ, Symons SP (2009) Comparison of CTA to DSA in determining the etiology of spontaneous ICH. Can J Neurol Sci Le J Can des Sci Neurol 36(2):176–180

    Article  Google Scholar 

  33. 33.

    Wallace AN, Dines JN, Zipfel GJ, Derdeyn CP (2013) Yield of catheter angiography after computed tomography negative, lumbar puncture positive subarachnoid hemorrhage [corrected]. Stroke [Internet] 44(6):1729–1731 Available from: https://pubmed.ncbi.nlm.nih.gov/23619131

    CAS  Article  Google Scholar 

  34. 34.

    Horstman P, Linn FHH, Voorbij HAM, Rinkel GJE (2012) Chance of aneurysm in patients suspected of SAH who have a “negative” CT scan but a “positive” lumbar puncture. J Neurol 259(4):649–652

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    van Rooij WJ, Peluso JPP, Sluzewski M, Beute GN (2008) Additional value of 3D rotational angiography in angiographically negative aneurysmal subarachnoid hemorrhage: how negative is negative? AJNR Am J Neuroradiol 29(5):962–966

    PubMed  Article  Google Scholar 

  36. 36.

    Bechan RS, van Rooij SB, Sprengers ME, Peluso JP, Sluzewski M, Majoie CB, van Rooij WJ (2015) CT angiography versus 3D rotational angiography in patients with subarachnoid hemorrhage. Neuroradiology. 57(12):1239–1246

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Agid R, Lee SK, Willinsky RA, Farb RI, KG tB (2006) Acute subarachnoid hemorrhage: using 64-slice multidetector CT angiography to “triage” patients’ treatment. Neuroradiology 48(11):787–794

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    van Gelder JM (2003) Computed tomographic angiography for detecting cerebral aneurysms: implications of aneurysm size distribution for the sensitivity, specificity, and likelihood ratios. Neurosurgery 53(3):596–597

    Google Scholar 

  39. 39.

    White PM, Wardlaw JM, Easton V (2000) Can noninvasive imaging accurately depict intracranial aneurysms? A systematic review. Radiology. 217(2):361–370

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Romijn M, van Andel HAF G, van Walderveen MA, Sprengers ME, van Rijn JC, van Rooij WJ et al (2008) Diagnostic accuracy of CT angiography with matched mask bone elimination for detection of intracranial aneurysms: comparison with digital subtraction angiography and 3D rotational angiography. AJNR Am J Neuroradiol 29(1):134–139

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Watanabe Y, Uotani K, Nakazawa T, Higashi M, Yamada N, Hori Y, Kanzaki S, Fukuda T, Itoh T, Naito H (2009) Dual-energy direct bone removal CT angiography for evaluation of intracranial aneurysm or stenosis: comparison with conventional digital subtraction angiography. Eur Radiol 19(4):1019–1024

    PubMed  Article  Google Scholar 

  42. 42.

    Agid R, Andersson T, Almqvist H, Willinsky RA, Lee S-K, KG tB et al (2010) Negative CT angiography findings in patients with spontaneous subarachnoid hemorrhage: when is digital subtraction angiography still needed? AJNR Am J Neuroradiol 31(4):696–705

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Kern KC, Liebeskind DS (2019) Vessel wall imaging of cerebrovascular disorders. Curr Treat Options Cardiovasc Med 21(11):65

    PubMed  Article  Google Scholar 

  44. 44.

    Mossa-Basha M, Huynh TJ, Hippe DS, Fata P, Morton RP, Levitt MR (2018) Vessel wall MRI characteristics of endovascularly treated aneurysms: association with angiographic vasospasm. J Neurosurg 131(3):859–867

    PubMed  PubMed Central  Article  Google Scholar 

  45. 45.

    Hartman JB, Watase H, Sun J, Hippe DS, Kim L, Levitt M, Sekhar L, Balu N, Hatsukami T, Yuan C, Mossa-Basha M (2019) Intracranial aneurysms at higher clinical risk for rupture demonstrate increased wall enhancement and thinning on multicontrast 3D vessel wall MRI. Br J Radiol 92(1096):20180950

    PubMed  PubMed Central  Article  Google Scholar 

  46. 46.

    Dodick DW (2002) Thunderclap headache. J Neurol Neurosurg Psychiatry [Internet] 72(1):6–11 Available from: https://pubmed.ncbi.nlm.nih.gov/11784817

    CAS  Article  Google Scholar 

  47. 47.

    Ducros A, Bousser M-G (2013) Thunderclap headache. BMJ [Internet]:346 Available from: https://www.bmj.com/content/346/bmj.e8557

  48. 48.

    Dalyai R, Chalouhi N, Theofanis T, Jabbour PM, Dumont AS, Gonzalez LF et al (2013) 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 72(4):642–646

    Google Scholar 

  49. 49.

    Delgado Almandoz JE, Crandall BM, Fease JL, Scholz JM, Anderson RE, Kadkhodayan Y, Tubman DE (2013) Diagnostic yield of catheter angiography in patients with subarachnoid hemorrhage and negative initial noninvasive neurovascular examinations. AJNR Am J Neuroradiol 34(4):833–839

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Maslehaty H, Barth H, Petridis AK, Doukas A, Maximilian MH (2012) Special features of subarachnoid hemorrhage of unknown origin: a review of a series of 179 cases. Neurol Res 34(1):91–97

    PubMed  Article  Google Scholar 

  51. 51.

    van Gijn J, van Dongen KJ, Vermeulen M, Hijdra A (1985) Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology. 35(4):493–497

    PubMed  Article  Google Scholar 

  52. 52.

    Ruigrok YM, Rinkel GJ, Buskens E, Velthuis BK, van Gijn J (2000) Perimesencephalic hemorrhage and CT angiography: a decision analysis. Stroke 31(12):2976–2983

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Alg VS, Sofat R, Houlden H, Werring DJ (2013) Genetic risk factors for intracranial aneurysms: a meta-analysis in more than 116,000 individuals. Neurology 80(23):2154–2165

    PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Thompson BG, Brown RD, Amin-Hanjani S, Broderick JP, Cockroft KM, Connolly ES et al (2015) Guidelines for the management of patients with unruptured intracranial aneurysms. Stroke 46(8):2368–2400

    PubMed  Article  Google Scholar 

  55. 55.

    Williams LN, Brown RD Jr (2013) Management of unruptured intracranial aneurysms. Neurol Clin Pract [Internet] 3(2):99–108 Available from: https://pubmed.ncbi.nlm.nih.gov/23914319

    Article  Google Scholar 

  56. 56.

    Chen S, Luo J, Reis C, Manaenko A, Zhang J (2017) Hydrocephalus after subarachnoid hemorrhage: pathophysiology, diagnosis, and treatment. Biomed Res Int [Internet] 2017:8584753 Available from: https://pubmed.ncbi.nlm.nih.gov/28373987

    Google Scholar 

  57. 57.

    Kumar G, Alexandrov AV (2015) Vasospasm surveillance with transcranial doppler sonography in subarachnoid hemorrhage. J ultrasound Med Off J Am Inst Ultrasound Med 34(8):1345–1350

    Google Scholar 

  58. 58.

    Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, Ruefenacht D, Schmiedek P, Weidauer S, Pasqualin A, Macdonald RL (2011) Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke 42(4):919–923

    PubMed  Article  Google Scholar 

  59. 59.

    Mir DIA, Gupta A, Dunning A, Puchi L, Robinson CL, Epstein H-AB, Sanelli PC (2014) CT perfusion for detection of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. AJNR Am J Neuroradiol 35(5):866–871

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Cremers CHP, van der Schaaf IC, Wensink E, Greving JP, Rinkel GJE, Velthuis BK et al (2014) CT perfusion and delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab [Internet] 34(2):200–207 Available from: https://pubmed.ncbi.nlm.nih.gov/24281744

    Article  Google Scholar 

  61. 61.

    Tomycz L, Bansal NK, Hawley CR, Goddard TL, Ayad MJ, Mericle RA (2011) “Real-world” comparison of non-invasive imaging to conventional catheter angiography in the diagnosis of cerebral aneurysms. Surg Neurol Int 2:134

    PubMed  PubMed Central  Article  Google Scholar 

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Correspondence to Garvit D. Khatri.

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Khatri, G.D., Sarikaya, B., Cross, N.M. et al. The role of imaging in the management of non-traumatic subarachnoid hemorrhage: a practical review. Emerg Radiol (2021). https://doi.org/10.1007/s10140-021-01900-x

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Keywords

  • Aneurysmal subarachnoid hemorrhage
  • CT scans spiral
  • Angiography
  • Digital subtraction
  • MRI scan
  • Lumbar puncture