CC BY-NC-ND 4.0 · Arquivos Brasileiros de Neurocirurgia: Brazilian Neurosurgery 2019; 38(03): 157-165
DOI: 10.1055/s-0039-1692124
Original Article | Artigo Original
Thieme Revinter Publicações Ltda Rio de Janeiro, Brazil

Angiographic Findings in Refractory Delayed Cerebral Ischemia

Achados angiográficos na isquemia cerebral tardia refratária
1   Department of Neurosurgery, Hospital Regional Rancagua, Rancagua, Chile
Alvaro Ruiz
2   Department of Neurosurgery, Institute of Neurosurgery Asenjo, Santiago, Chile
Jorge Mura
2   Department of Neurosurgery, Institute of Neurosurgery Asenjo, Santiago, Chile
› Author Affiliations
Source of Funding None.
Further Information

Publication History

29 December 2018

17 April 2019

Publication Date:
31 May 2019 (online)


Background Delayed cerebral ischemia (DCI) follows a refractory course in a subgroup of patients with aneurysmal subarachnoid hemorrhage (SAH), leading to diffuse ischemic injury. The role of angiographic vasospasm (AV) is unknown. Our goal is to study the angiographic alterations and the clinical profile of refractory DCI patients.

Methods Retrospective study of patients with SAH who presented with DCI treated with medical and endovascular therapy, with a refractory evolution, defined as multiple ischemic infarction and brain death.

Results Out of a cohort of 336 patients, 7 (2%) developed refractory DCI. The median age of the patients was 48 (38–60) years old. Five patients had ruptured anterior communicating artery (ACoA) aneurysms. Four patients were treated with coil embolization, and three with microsurgical clipping. Angiographic vasospasm was classified as severe in 5 cases. Compromise of bilateral circulation was detected in six patients. Distal circulation vasospasm occurred in five cases. Slow circulatory transit times were observed in three patients.

Conclusion Angiographic findings such as bilateral circulatory compromise and distal vasospasm were frequent alterations. Further studies are required to establish the association of these findings with the clinical outcomes.


Introdução A isquemia cerebral tardia (ICT) pode seguir um curso refratário em um subgrupo de pacientes com hemorragia subaracnoidea aneurismática (HSA), levando a uma lesão isquêmica difusa. O papel do vasoespasmo angiográfico (VA) ainda é desconhecido. Nosso objetivo é avaliar as alterações angiográficas e o perfil clínico dos pacientes com ICT refratária.

Métodos Estudo retrospectivo de pacientes com HSA que apresentaram ICT tratados com terapia médica e endovascular, com evolução refratária, definida como infarto isquêmico múltiplo e morte cerebral.

Resultados A partir de uma coorte de 336 pacientes, 7 (2%) desenvolveram ICT refratária. A mediana de idade foi de 48 (38–60) anos. Cinco pacientes tiveram ruptura de aneurisma da artéria comunicante anterior (ACoA). Quatro pacientes foram tratados com coiling e três com clipagem. O VA foi classificado como grave em cinco casos. Detectou-se acometimento da circulação bilateral em seis pacientes. A circulação distal do vasoespasmo aconteceu em cinco casos. Observou-se tempo de trânsito circulatório lento em três pacientes.

Conclusão Os achados angiográficos, como o acometimento circulatório bilateral e o vasoespasmo distal, foram alterações frequentes. Estudos adicionais serão necessários para confirmar as associações entre os achados angiográficos e os resultados clínicos.



  • References

  • 1 Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol 2014; 10 (01) 44-58
  • 2 Weidauer S, Lanfermann H, Raabe A, Zanella F, Seifert V, Beck J. Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 2007; 38 (06) 1831-1836
  • 3 Crowley RW, Medel R, Dumont AS. , et al. Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke 2011; 42 (04) 919-923
  • 4 Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJ, Rinkel GJ. Global and focal cerebral perfusion after aneurysmal subarachnoid hemorrhage in relation with delayed cerebral ischemia. Neuroradiology 2008; 50 (09) 813-820
  • 5 Aralasmak A, Akyuz M, Ozkaynak C, Sindel T, Tuncer R. CT angiography and perfusion imaging in patients with subarachnoid hemorrhage: correlation of vasospasm to perfusion abnormality. Neuroradiology 2009; 51 (02) 85-93
  • 6 Rosalind Lai PM, Du R. Role of Genetic Polymorphisms in Predicting Delayed Cerebral Ischemia and Radiographic Vasospasm After Aneurysmal Subarachnoid Hemorrhage: A Meta-Analysis. World Neurosurg 2015; 84 (04) 933-41.e2
  • 7 Brown RJ, Kumar A, Dhar R, Sampson TR, Diringer MN. The relationship between delayed infarcts and angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 2013; 72 (05) 702-707 , discussion 707–708
  • 8 Naraoka M, Matsuda N, Shimamura N, Asano K, Ohkuma H. The role of arterioles and the microcirculation in the development of vasospasm after aneurysmal SAH. BioMed Res Int 2014; 2014: 253746
  • 9 Frontera JA, Fernandez A, Schmidt JM. , et al. Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition?. Stroke 2009; 40 (06) 1963-1968
  • 10 Claassen J, Bernardini GL, Kreiter K. , et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 2001; 32 (09) 2012-2020
  • 11 Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale. J Neurosurg 1988; 68 (06) 985-986
  • 12 Mura J, Rojas-Zalazar D, Ruíz A, Vintimilla LC, Marengo JJ. Improved outcome in high-grade aneurysmal subarachnoid hemorrhage by enhancement of endogenous clearance of cisternal blood clots: a prospective study that demonstrates the role of lamina terminalis fenestration combined with modern microsurgical cisternal blood evacuation. Minim Invasive Neurosurg 2007; 50 (06) 355-362
  • 13 Komotar RJ, Olivi A, Rigamonti D, Tamargo RJ. Microsurgical fenestration of the lamina terminalis reduces the incidence of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 2002; 51 (06) 1403-1412 , discussion 1412–1413
  • 14 Dorhout Mees SM, Rinkel GJ, Feigin VL. , et al. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev 2007; (03) CD000277
  • 15 Kumar G, Shahripour RB, Harrigan MR. Vasospasm on transcranial Doppler is predictive of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Neurosurg 2016; 124 (05) 1257-1264
  • 16 Diringer MN, Bleck TP, Claude Hemphill III J. , et al; Neurocritical Care Society. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society's Multidisciplinary Consensus Conference. Neurocrit Care 2011; 15 (02) 211-240
  • 17 Connolly Jr ES, Rabinstein AA, Carhuapoma JR. , et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke 2012; 43 (06) 1711-1737
  • 18 Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wermer MJ, Rinkel GJ. Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology 2009; 51 (12) 813-819
  • 19 Lanterna LA, Lunghi A, Martchenko S, Gritti P, Bonaldi G, Biroli F. Cerebral watershed hypoperfusion in subarachnoid hemorrhage: computed tomography perfusion analysis. J Neurosurg 2011; 114 (04) 961-968
  • 20 Mortimer AM, Steinfort B, Faulder K, Harrington T. Delayed infarction following aneurysmal subarachnoid hemorrhage: Can the role of severe angiographic vasospasm really be dismissed?. J Neurointerv Surg 2016; 8 (08) 802-807
  • 21 Qureshi AI, Sung GY, Suri MA, Straw RN, Guterman LR, Hopkins LN. Prognostic value and determinants of ultraearly angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 1999; 44 (05) 967-973 , discussion 973–974
  • 22 Al-Mufti F, Roh D, Lahiri S. , et al. Ultra-early angiographic vasospasm associated with delayed cerebral ischemia and infarction following aneurysmal subarachnoid hemorrhage. J Neurosurg 2017; 126 (05) 1545-1551
  • 23 Phan K, Moore JM, Griessenauer CJ. , et al. Ultra-Early Angiographic Vasospasm After Aneurysmal Subarachnoid Hemorrhage: A Systematic Review and Meta-Analysis. World Neurosurg 2017; 102: 632-638.e1
  • 24 Abla AA, Wilson DA, Williamson RW. , et al. The relationship between ruptured aneurysm location, subarachnoid hemorrhage clot thickness, and incidence of radiographic or symptomatic vasospasm in patients enrolled in a prospective randomized controlled trial. J Neurosurg 2014; 120 (02) 391-397
  • 25 Dabus G, Nogueira RG. Current options for the management of aneurysmal subarachnoid hemorrhage-induced cerebral vasospasm: a comprehensive review of the literature. Intervent Neurol 2013; 2 (01) 30-51
  • 26 Pandey AS, Elias AE, Chaudhary N, Thompson BG, Gemmete JJ. Endovascular treatment of cerebral vasospasm: vasodilators and angioplasty. Neuroimaging Clin N Am 2013; 23 (04) 593-604
  • 27 Bauer AM, Rasmussen PA. Treatment of intracranial vasospasm following subarachnoid hemorrhage. Front Neurol 2014; 5: 72
  • 28 Hollingworth M, Chen PR, Goddard AJ, Coulthard A, Söderman M, Bulsara KR. Results of an International Survey on the Investigation and Endovascular Management of Cerebral Vasospasm and Delayed Cerebral Ischemia. World Neurosurg 2015; 83 (06) 1120-1126.e1
  • 29 Tuzgen S, Kucukyuruk B, Aydin S, Ozlen F, Kizilkilic O, Abuzayed B. Decompressive craniectomy in patients with cerebral infarction due to malignant vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosci Rural Pract 2012; 3 (03) 251-255
  • 30 Jain V, Rath GP, Dash HH, Bithal PK, Chouhan RS, Suri A. Stellate ganglion block for treatment of cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage - A preliminary study. J Anaesthesiol Clin Pharmacol 2011; 27 (04) 516-521
  • 31 Lylyk P, Vila JF, Miranda C, Ferrario A, Romero R, Cohen JE. Partial aortic obstruction improves cerebral perfusion and clinical symptoms in patients with symptomatic vasospasm. Neurol Res 2005; 27 (Suppl. 01) S129-S135
  • 32 Pradilla G, Chaichana KL, Hoang S, Huang J, Tamargo RJ. Inflammation and cerebral vasospasm after subarachnoid hemorrhage. Neurosurg Clin N Am 2010; 21 (02) 365-379
  • 33 Hockel K, Diedler J, Steiner J. , et al. Long-Term, Continuous Intra-Arterial Nimodipine Treatment of Severe Vasospasm After Aneurysmal Subarachnoid Hemorrhage. World Neurosurg 2016; 88: 104-112
  • 34 Von der Brelie C, Seifert M, Rot S. , et al. Sedation of Patients with Acute Aneurysmal Subarachnoid Hemorrhage with Ketamine Is Safe and Might Influence the Occurrence of Cerebral Infarctions Associated with Delayed Cerebral Ischemia. World Neurosurg 2017; 97: 374-382
  • 35 Durrant JC, Hinson HE. Rescue therapy for refractory vasospasm after subarachnoid hemorrhage. Curr Neurol Neurosci Rep 2015; 15 (02) 521