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Current diagnostic approaches to subarachnoid haemorrhage

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Abstract

Over the past decade, significant advances have been made in the field of subarachnoid haemorrhage (SAH). Prompt diagnosis with high-resolution CT and intensive critical care support remain key aspects of good patient management. Early identification and definitive treatment of underlying ruptured aneurysms is generally advocated to reduce the risk of re-bleeding, a complication with high mortality and morbidity. Although intra-arterial digital subtraction angiography (DSA) is still considered the gold standard for sourcing aneurysms, CT angiography, especially with the evolution of multi-slice technology, is slowly gaining acceptance as a rapid, accessible and minimally invasive method which appears likely to replace DSA as first-line modality in the future. Furthermore, the advent of Guglielmi detachable coils and the ISAT trial have revolutionised the treatment of ruptured aneurysms, with a significant trend towards endovascular coiling away from operative clipping. Improvements in clinical experience, coiling technology and assistive devices now allow interventionalists to potentially treat the majority of aneurysms, including wide-necked or complex lesions. The uncertain long-term results of coiling, however, still fuel strong debate and controversy. This review summarises current diagnostic approaches to SAH from a radiological perspective, with an emphasis on aneurysmal SAH and an evidence-based approach to the role of imaging and interventional radiology in diagnosis, treatment and follow-up.

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References

  1. Menghini VV, Brown RD Jr, Sicks JD, O’Fallon WM, Wiebers DO (1998) Incidence and prevalence of intracranial aneurysms and hemorrhage in Olmsted County, Minnesota, 1965 to 1995. Neurology 51:405–411

    Google Scholar 

  2. Linn FH, Rinkel GJ, Algra A, van Gijn J (1996) Incidence of subarachnoid hemorrhage: role of region, year, and rate of computed tomography: a meta-analysis. Stroke 27:625–629

    CAS  PubMed  Google Scholar 

  3. Lanzino G, Kassell NF, Germanson TP, Kongable GL, Truskowski LL, Torner JC, Jane JA (1996) Age and outcome after aneurysmal subarachnoid hemorrhage: why do older patients fare worse? J Neurosurg 85:410–418

    Google Scholar 

  4. Kirkpatrick PJ (2002) Subarachnoid haemorrhage and intracranial aneurysms: what neurologists need to know. J Neurol Neurosurg Psychiatry 73(Suppl 1):i28–i33

    Google Scholar 

  5. Sudlow CL, Warlow CP (1997) Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. International Stroke Incidence Collaboration. Stroke 28:491–499

    Google Scholar 

  6. Johnston SC, Selvin S, Gress DR (1998) The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology 50:1413–1418

    Google Scholar 

  7. Hop JW, Rinkel GJ, Algra A, van Gijn J (1997) Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 28:660–664

    CAS  PubMed  Google Scholar 

  8. van Gijn J, Rinkel GJ (2001) Subarachnoid haemorrhage: diagnosis, causes and management. Brain 124:249–278

    Google Scholar 

  9. Frizzell RT, Kuhn F, Morris R, Quinn C, Fisher WS III (1997) Screening for ocular hemorrhages in patients with ruptured cerebral aneurysms: a prospective study of 99 patients. Neurosurgery 41:529–533, discussion 533–534

    Google Scholar 

  10. Reijneveld JC, Wermer M, Boonman Z, van Gijn J, Rinkel GJ (2000) Acute confusional state as presenting feature in aneurysmal subarachnoid hemorrhage: frequency and characteristics. J Neurol 247:112–116

    Google Scholar 

  11. Ross N, Hutchinson PJ, Seeley H, Kirkpatrick PJ (2002) Timing of surgery for supratentorial aneurysmal subarachnoid haemorrhage: report of a prospective study. J Neurol Neurosurg Psychiatry 72:480–484

    Google Scholar 

  12. van der Wee N, Rinkel GJ, Hasan D, van Gijn J (1995) Detection of subarachnoid haemorrhage on early CT: is lumbar puncture still needed after a negative scan? J Neurol Neurosurg Psychiatry 58:357–359

    Google Scholar 

  13. van Gijn J, van Dongen KJ (1982) The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 23:153–156

    PubMed  Google Scholar 

  14. Vermeulen M, van Gijn J (1990) The diagnosis of subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 53:365–372

    Google Scholar 

  15. Rabinstein AA, Pittock SJ, Miller GM, Schindler JJ, Wijdicks EF (2003) Pseudosubarachnoid haemorrhage in subdural haematoma. J Neurol Neurosurg Psychiatry 74:1131–1132

    Google Scholar 

  16. Noguchi K, Ogawa T, Inugami A, Toyoshima H, Okudera T, Uemura K (1994) MR of acute subarachnoid hemorrhage: a preliminary report of fluid-attenuated inversion-recovery pulse sequences. Am J Neuroradiol 15:1940–1943

    Google Scholar 

  17. Ogawa T, Inugami A, Fujita H, Hatazawa J, Shimosegawa E, Noguchi K, Okudera T, Kanno I, Uemura K, Suzuki A et al. (1995) MR diagnosis of subacute and chronic subarachnoid hemorrhage: comparison with CT. Am J Roentgenol 165:1257–1262

    Google Scholar 

  18. Noguchi K, Ogawa T, Seto H, Inugami A, Hadeishi H, Fujita H, Hatazawa J, Shimosegawa E, Okudera T, Uemura K (1997) Subacute and chronic subarachnoid hemorrhage: diagnosis with fluid-attenuated inversion-recovery MR imaging. Radiology 203:257–262

    Google Scholar 

  19. Mohamed M, Heasly DC, Yagmurlu B, Yousem DM, Heasely DC (2004) Fluid-attenuated inversion recovery MR imaging and subarachnoid hemorrhage: not a panacea. Am J Neuroradiol 25:545–550

    Google Scholar 

  20. Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251–256

    CAS  PubMed  Google Scholar 

  21. Longstreth WT Jr, Koepsell TD, Yerby MS, van Belle G (1985) Risk factors for subarachnoid hemorrhage. Stroke 16:377–385

    Google Scholar 

  22. Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP (1990) The international cooperative study on the timing of aneurysm surgery. Part 2: surgical results. J Neurosurg 73:37–47

    Google Scholar 

  23. Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL (1990) The international cooperative study on the timing of aneurysm surgery. Part 1: overall management results. J Neurosurg 73:18–36

    Google Scholar 

  24. Johnston SC, Higashida RT, Barrow DL, Caplan LR, Dion JE, Hademenos G, Hopkins LN, Molyneux A, Rosenwasser RH, Vinuela F, Wilson CB (2002) Recommendations for the endovascular treatment of intracranial aneurysms: a statement for healthcare professionals from the Committee on Cerebrovascular Imaging of the American Heart Association Council on Cardiovascular Radiology. Stroke 33:2536–2544

    Google Scholar 

  25. Guglielmi G, Vinuela F, Dion J, Duckwiler G (1991) Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: preliminary clinical experience. J Neurosurg 75:8–14

    CAS  PubMed  Google Scholar 

  26. Macdonald RL, Mojtahedi S, Johns L, Kowalczuk A (1998) Randomized comparison of Guglielmi detachable coils and cellulose acetate polymer for treatment of aneurysms in dogs. Stroke 29:478–485, discussion 485–486

    CAS  PubMed  Google Scholar 

  27. Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R (2002) International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:1267–1274

    Article  PubMed  Google Scholar 

  28. Kirkpatrick PJ, Kirollos RW, Higgins N, Matta B (2003) Lessons to be learnt from the International Subarachnoid Haemorrhage Trial (ISAT). Br J Neurosurg 17:5–7

    Google Scholar 

  29. Heros RC (2003) Guglielmi detachable coil technology. J Neurosurg 98:945–947, discussion 947

    Google Scholar 

  30. Maurice-Williams RS (2004) Aneurysm surgery after the International Subarachnoid Aneurysm Trial (ISAT). J Neurol Neurosurg Psychiatry 75:807–808

    Google Scholar 

  31. Benitez RP, Silva MT, Klem J, Veznedaroglu E, Rosenwasser RH (2004) Endovascular occlusion of wide-necked aneurysms with a new intracranial microstent (Neuroform) and detachable coils. Neurosurgery 54:1359–1368

    Article  Google Scholar 

  32. Cottier JP, Pasco A, Gallas S, Gabrillargues J, Cognard C, Drouineau J, Brunereau L, Herbreteau D (2001) Utility of balloon-assisted Guglielmi detachable coiling in the treatment of 49 cerebral aneurysms: a retrospective, multicenter study. Am J Neuroradiol 22:345–351

    CAS  PubMed  Google Scholar 

  33. Raymond J, Roy D, Leblanc P, Roorda S, Janicki C, Normandeau L, Morel F, Gevry G, Bahary JP, Chagnon M, Guilbert F, Weill A (2003) Endovascular treatment of intracranial aneurysms with radioactive coils: initial clinical experience. Stroke 34:2801–2806

    Google Scholar 

  34. Mawad ME, Cekirge S, Ciceri E, Saatci I (2002) Endovascular treatment of giant and large intracranial aneurysms by using a combination of stent placement and liquid polymer injection. J Neurosurg 96:474–482

    Google Scholar 

  35. van der Jagt M, Hasan D, Bijvoet HW, Pieterman H, Dippel DW, Vermeij FH, Avezaat CJ (1999) Validity of prediction of the site of ruptured intracranial aneurysms with CT. Neurology 52:34–39

    Google Scholar 

  36. Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W (2003) Neurologic complications of cerebral angiography: prospective analysis of 2,899 procedures and review of the literature. Radiology 227:522–528

    PubMed  Google Scholar 

  37. Cloft HJ, Joseph GJ, Dion JE (1999) Risk of cerebral angiography in patients with subarachnoid hemorrhage, cerebral aneurysm, and arteriovenous malformation: a meta-analysis. Stroke 30:317–320

    CAS  PubMed  Google Scholar 

  38. Sugahara T, Korogi Y, Nakashima K, Hamatake S, Honda S, Takahashi M (2002) Comparison of 2D and 3D digital subtraction angiography in evaluation of intracranial aneurysms. Am J Neuroradiol 23:1545–1552

    Google Scholar 

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

    Google Scholar 

  40. White PM, Wardlaw JM, Teasdale E, Sloss S, Cannon J, Easton V (2001) Power transcranial Doppler ultrasound in the detection of intracranial aneurysms. Stroke 32:1291–1297

    Google Scholar 

  41. Turner CL, Kirkpatrick PJ (2000) Detection of intracranial aneurysms with unenhanced and echo contrast enhanced transcranial power Doppler. J Neurol Neurosurg Psychiatry 68:489–495

    Article  CAS  PubMed  Google Scholar 

  42. Turner CL, Higgins JN, Kirkpatrick PJ (2003) Assessment of transcranial color-coded duplex sonography for the surveillance of intracranial aneurysms treated with Guglielmi detachable coils. Neurosurgery 53:866–871, discussion 871–872

    Google Scholar 

  43. White PM, Teasdale EM, Wardlaw JM, Easton V (2001) Intracranial aneurysms: CT angiography and MR angiography for detection prospective blinded comparison in a large patient cohort. Radiology 219:739–749

    Google Scholar 

  44. Willinek WA, Gieseke J, von Falkenhausen M, Born M, Hadizadeh D, Manka C, Textor HJ, Schild HH, Kuhl CK (2004) Sensitivity encoding (SENSE) for high spatial resolution time-of-flight MR angiography of the intracranial arteries at 3.0 T. Rofo 176:21–26

    Google Scholar 

  45. Parker DL, Goodrich KC, Alexander AL, Buswell HR, Blatter DD, Tsuruda JS (1998) Optimized visualization of vessels in contrast enhanced intracranial MR angiography. Magn Reson Med 40:873–882

    Google Scholar 

  46. Metens T, Rio F, Baleriaux D, Roger T, David P, Rodesch G (2000) Intracranial aneurysms: detection with gadolinium-enhanced dynamic three-dimensional MR angiography—initial results. Radiology 216:39–46

    Google Scholar 

  47. Leclerc X, Navez JF, Gauvrit JY, Lejeune JP, Pruvo JP (2002) Aneurysms of the anterior communicating artery treated with Guglielmi detachable coils: follow-up with contrast-enhanced MR angiography. Am J Neuroradiol 23:1121–1127

    PubMed  Google Scholar 

  48. Boulin A, Pierot L (2001) Follow-up of intracranial aneurysms treated with detachable coils: comparison of gadolinium-enhanced 3D time-of-flight MR angiography and digital subtraction angiography. Radiology 219:108–113

    CAS  PubMed  Google Scholar 

  49. Raaymakers TW, Buys PC, Verbeeten B Jr, Ramos LM, Witkamp TD, Hulsmans FJ, Mali WP, Algra A, Bonsel GJ, Bossuyt PM, Vonk CM, Buskens E, Limburg M, van Gijn J, Gorissen A, Greebe P, Albrecht KW, Tulleken CA, Rinkel GJ (1999) MR angiography as a screening tool for intracranial aneurysms: feasibility, test characteristics, and interobserver agreement. Am J Roentgenol 173:1469–1475

    CAS  PubMed  Google Scholar 

  50. Chappell ET, Moure FC, Good MC (2003) Comparison of computed tomographic angiography with digital subtraction angiography in the diagnosis of cerebral aneurysms: a meta-analysis. Neurosurgery 52:624–631, discussion 630–631

    Google Scholar 

  51. Tomandl BF, Kostner NC, Schempershofe M, Huk WJ, Strauss C, Anker L, Hastreiter P (2004) CT angiography of intracranial aneurysms: a focus on postprocessing. Radiographics 24:637–655

    Google Scholar 

  52. Velthuis BK, van Leeuwen MS, Witkamp TD, Boomstra S, Ramos LM, Rinkel GJ (1997) CT angiography: source images and postprocessing techniques in the detection of cerebral aneurysms. Am J Roentgenol 169:1411–1417

    CAS  PubMed  Google Scholar 

  53. Wintermark M, Uske A, Chalaron M, Regli L, Maeder P, Meuli R, Schnyder P, Binaghi S (2003) Multislice computerized tomography angiography in the evaluation of intracranial aneurysms: a comparison with intraarterial digital subtraction angiography. J Neurosurg 98:828–836

    Google Scholar 

  54. Kangasniemi M, Makela T, Koskinen S, Porras M, Poussa K, Hernesniemi J (2004) Detection of intracranial aneurysms with two-dimensional and three-dimensional multislice helical computed tomographic angiography. Neurosurgery 54:336–340, discussion 340–331

    Article  Google Scholar 

  55. Jayaraman MV, Mayo-Smith WW, Tung GA, Haas RA, Rogg JM, Mehta NR, Doberstein CE (2004) Detection of intracranial aneurysms: multi-detector row CT angiography compared with DSA. Radiology 230:510–518

    Google Scholar 

  56. Velthuis BK, van Leeuwen MS, Witkamp TD, Ramos LM, Berkelbach van der Sprenkel JW, Rinkel GJ (2001) Surgical anatomy of the cerebral arteries in patients with subarachnoid hemorrhage: comparison of computerized tomography angiography and digital subtraction angiography. J Neurosurg 95:206–212

    Google Scholar 

  57. Velthuis BK, Van Leeuwen MS, Witkamp TD, Ramos LM, Berkelbach van Der Sprenkel JW, Rinkel GJ (1999) Computerized tomography angiography in patients with subarachnoid hemorrhage: from aneurysm detection to treatment without conventional angiography. J Neurosurg 91:761–767

    Google Scholar 

  58. Hoh BL, Cheung AC, Rabinov JD, Pryor JC, Carter BS, Ogilvy CS (2004) Results of a prospective protocol of computed tomographic angiography in place of catheter angiography as the only diagnostic and pretreatment planning study for cerebral aneurysms by a combined neurovascular team. Neurosurgery 54:1329–1342

    Google Scholar 

  59. Hijdra A, Van Gijn J, Stefanko S, Van Dongen KJ, Vermeulen M, Van Crevel H (1986) Delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: clinicoanatomic correlations. Neurology 36:329–333

    Google Scholar 

  60. Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1–9

    Google Scholar 

  61. van der Jagt M, Hasan D, Bijvoet HW, Pieterman H, Koudstaal PJ, Avezaat CJ (2000) Interobserver variability of cisternal blood on CT after aneurysmal subarachnoid hemorrhage. Neurology 54:2156–2158

    Google Scholar 

  62. Sloan MA, Alexandrov AV, Tegeler CH, Spencer MP, Caplan LR, Feldmann E, Wechsler LR, Newell DW, Gomez CR, Babikian VL, Lefkowitz D, Goldman RS, Armon C, Hsu CY, Goodin DS (2004) Assessment: transcranial Doppler ultrasonography: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 62:1468–1481

    Google Scholar 

  63. Vora YY, Suarez-Almazor M, Steinke DE, Martin ML, Findlay JM (1999) Role of transcranial Doppler monitoring in the diagnosis of cerebral vasospasm after subarachnoid hemorrhage. Neurosurgery 44:1237–1247, discussion 1247–1248

    Google Scholar 

  64. Lysakowski C, Walder B, Costanza MC, Tramer MR (2001) Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review. Stroke 32:2292–2298

    Google Scholar 

  65. Anderson GB, Ashforth R, Steinke DE, Findlay JM (2000) CT angiography for the detection of cerebral vasospasm in patients with acute subarachnoid hemorrhage. Am J Neuroradiol 21:1011–1015

    Google Scholar 

  66. Otawara Y, Ogasawara K, Ogawa A, Sasaki M, Takahashi K (2002) Evaluation of vasospasm after subarachnoid hemorrhage by use of multislice computed tomographic angiography. Neurosurgery 51:939–942, discussion 942–943

    Google Scholar 

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

    Google Scholar 

  68. Van Der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ (2004) Venous drainage in perimesencephalic hemorrhage. Stroke (in press)

  69. Rinkel GJ, Wijdicks EF, Vermeulen M, Hasan D, Brouwers PJ, van Gijn J (1991) The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol 29:463–468

    Google Scholar 

  70. Rinkel GJ, Wijdicks EF, Hasan D, Kienstra GE, 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

    Google Scholar 

  71. Hashimoto H, Iida J, Hironaka Y, Okada M, Sakaki T (2000) Use of spiral computerized tomography angiography in patients with subarachnoid hemorrhage in whom subtraction angiography did not reveal cerebral aneurysms. J Neurosurg 92:278–283

    Google Scholar 

  72. Yamada M, Kitahara T, Kurata A, Fujii K, Miyasaka Y (2004) Intracranial vertebral artery dissection with subarachnoid hemorrhage: clinical characteristics and outcomes in conservatively treated patients. J Neurosurg 101:25–30

    Google Scholar 

  73. Rinkel GJ, van Gijn J, Wijdicks EF (1993) Subarachnoid hemorrhage without detectable aneurysm. A review of the causes. Stroke 24:1403–1409

    Google Scholar 

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Acknowledgements

We are grateful to Professor David Yousem from John Hopkins University and Carole Turner from Addenbrooke’s Hospital for providing some of the images in this review.

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Correspondence to Jonathan H. Gillard.

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U-King-Im, J.M., Koo, B., Trivedi, R.A. et al. Current diagnostic approaches to subarachnoid haemorrhage. Eur Radiol 15, 1135–1147 (2005). https://doi.org/10.1007/s00330-005-2665-5

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