Aneurysmal SAH Induced Vasospasm: Pathogenesis and Management

  • Chapter
  • First Online:
Endovascular Surgery of Cerebral Aneurysms
  • 539 Accesses

Abstract

Introduction: Vasospasm remains a major cause of poor outcome after subarachnoid hemorrhage (SAH) following rupture of intracranial aneurysms. The pathogenesis still remains misty due to its complexity even though a lot of progress has been made in understanding various causative mechanisms through intense clinical and experimental research.

Method: Study carried out by a review of English literature on topics related to pathogenesis and management of post SAH induced vasospasm.

Result: Evidence-based information available points toward multifactorial biochemical phenomena instigated by Ferrous Hemoglobin which revolve around:

  1. (a)

    Concept of early brain injury and evidence of cortical spreading depression

  2. (b)

    Effect of ischemia in pre-vasospasm period and blood–brain barrier disruption.

  3. (c)

    Role of Nitric oxide (NO), Endothelin-1 levels, and oxidative stress on smooth muscle cells.

  4. (d)

    Changes induced by free radical production, lipid peroxidation, and alteration of ionic channels.

  5. (e)

    Differential upregulation of genes.

Conclusion: To date the understanding of pathophysiology of delayed vasospasm has made significant stride for which the role of research using animal models cannot be overemphasized. The treatment of this complex condition still remains vague.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 69.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 89.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 119.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Vlak MH, Algra A, Brandenburg R, Rinkel GJ. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis the Lancet. Neurology. 2011 Jul;10(7):626–36. https://doi.org/10.1016/S1474-4422(11)70109-0.

    Article  PubMed  Google Scholar 

  2. Korja M, Lehto H, Juvela S. Lifelong rupture risk of intracranial aneurysms depends on risk factors: a prospective Finnish Cohort Study. Stroke. 2014;45:1958–63. https://doi.org/10.1161/STROKEAHA.114.005318.

    Article  PubMed  Google Scholar 

  3. Mensing LA, Greving JP, Verhoeff TA, Rinkel GJE, Ruigrok YM. Comparison of rupture risk of intracranial aneurysms between familial and sporadic patients. Stroke. 2019;50:1380–3. https://doi.org/10.1161/STROKEAHA.118.023783.

    Article  PubMed  Google Scholar 

  4. Karenberg A, Moog FP. Die Apoplexieimmedizinischen Schrifttum der Antike. Apoplexy in Ancient Medical Writings. Fortschritte der Neurologie-Psychiatrie. 1997;65(11):489–503. https://doi.org/10.1055/s-2007-996355.

    Article  CAS  PubMed  Google Scholar 

  5. Lawton MT, Vates GE. Subarachnoid hemorrhage. New Engl J Med. 2017;377:257–66. https://doi.org/10.1056/NEJMcp1605827.

    Article  PubMed  Google Scholar 

  6. Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke. 2008 Nov;39(11):3015–21. https://doi.org/10.1161/STROKEAHA.108.519942.

    Article  CAS  PubMed  Google Scholar 

  7. Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clip**: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol. 2011 Jul;10(7):618–25. https://doi.org/10.1016/S1474-4422(11)70108-9.

    Article  CAS  PubMed  Google Scholar 

  8. Dorsch N. Therapeutic approaches to vasospasm in subarachnoid hemorrhage. Curr Opin Crit Care. 2002 Apr;8(2):128–33. https://doi.org/10.1097/00075198-200204000-00007.

    Article  PubMed  Google Scholar 

  9. Ecker A, Rimenschneider P. Arteriographic demonstration of spasm of the intracranial arteries with special reference to saccular arterial aneurysms. J Neurosurg. 1951 Nov;8(6):660–7. https://doi.org/10.3171/jns.1951.8.6.0660.

    Article  CAS  PubMed  Google Scholar 

  10. Weir B, Grace M, Hansen J, et al. Time course of vasospasm in man. J Neurosurg. 1978 Feb;48(2):173–8. https://doi.org/10.3171/jns.1978.48.2.0173.

    Article  CAS  PubMed  Google Scholar 

  11. Nornes H. The role of intracranial pressure in the arrest of hemorrhage in patients with ruptured intracranial aneurysms. J Neurosurg. 1973;39:226–34. https://doi.org/10.3171/jns.1973.39.2.0226.

    Article  CAS  PubMed  Google Scholar 

  12. Trojanowski T. Blood Elsevier brain barrier changes after experimental subarachnoid hemorrhage. Acta Neurochirurgica (Wien). 1982;60(1–2):45–54. https://doi.org/10.1007/BF01401749.

    Article  CAS  Google Scholar 

  13. Baldwin ME, Loch Macdonald R, Huo D, Novakovia RL, Goldenberg FD, Frank JI, Rosengart AJ. Early vasospasm on admission angiography in patients with aneurysmal subarachnoid hemorrhage is a predictor for in-hospital complications and poor outcome. Stroke. 2004 Nov;35(11):2506–11. https://doi.org/10.1161/01.STR.0000144654.79393.cf.

    Article  PubMed  Google Scholar 

  14. Dreier JP, Ebert N, Priller J, Megow D, Lindauer U, Klee R, Reuter U, Imai Y, Einhäupl KM, Victorov I, Dirnagl U. Products of hemolysis in the subarachnoid space inducing spreading ischemia in the cortex and focal necrosis in rats: a model for delayed ischemic neurological deficits after subarachnoid hemorrhage? J Neurosurg. 2000 Oct;93(4):658–66. https://doi.org/10.3171/jns.2000.93.4.0658.

    Article  CAS  PubMed  Google Scholar 

  15. Ostrowski RP, Colohan AR, Zhang JH. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res. 2006 Jun;28(4):399–414. https://doi.org/10.1179/016164106X115008.

    Article  CAS  PubMed  Google Scholar 

  16. Geraghty JR, Testai FD. Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Curr Atheroscler Rep. 2017 Oct 23;19(12):50. https://doi.org/10.1007/s11883-017-0690-x.

    Article  CAS  PubMed  Google Scholar 

  17. Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet. 2017;389:655–66.

    Article  PubMed  Google Scholar 

  18. Fujii M, Yan J, Rolland WB, Soejima Y, Caner B, Zhang JH. Early brain injury, an evolving frontier in subarachnoid hemorrhage research. Transl Stroke Res. 2013 Aug;4(4):432–46. https://doi.org/10.1007/s12975-013-0257-2.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Seifert V, Löffler B-M, Zimmermann M, Roux S, Stolke D. Endothelin concentrations in patients with aneurysmal subarachnoid hemorrhage: correlation with cerebral vasospasm, delayed ischemic neurological deficits and volume of hematoma. J Neurosurg. 1995 Jan;82(1):55–62. https://doi.org/10.3171/jns.1995.82.1.0055.

    Article  CAS  PubMed  Google Scholar 

  20. Zuccarello M, Bonasso C, Lewis A, Sperelakis N, Rapoport RM. Relaxation of subarchnoid hemorrhage-induced spasm of rabbit basilar artery by the K+ channel activator cromakalim. Stroke. 1996 Feb;27(2):311–6. https://doi.org/10.1161/01.str.27.2.311.

    Article  CAS  PubMed  Google Scholar 

  21. Sehba F, Bederson J. Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res. 2006 Jun;28(4):381–98. https://doi.org/10.1179/016164106X114991.

    Article  CAS  PubMed  Google Scholar 

  22. Cahill WJ, Calvert JH, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006 Nov;26(11):1341–53. https://doi.org/10.1038/sj.jcbfm.9600283.

    Article  CAS  PubMed  Google Scholar 

  23. Turner C, Bergeron M, Matz P, et al. Heme oxygenase-1 is induced in glia throughout brain by subarachnoid hemoglobin. J Cereb Blood Flow Metab. 1998 Mar;18(3):257–73. https://doi.org/10.1097/00004647-199803000-00004.

    Article  CAS  PubMed  Google Scholar 

  24. Vikman P, Beg S, Khurana T, Hansen-Schwartz J, Edvinsson L. Gene expression and molecular changes in cerebral arteries following subarachnoid hemorrhage in the rat. J Neurosurg. 2006 Sep;105(3):438–44. https://doi.org/10.3171/jns.2006.105.3.438.

    Article  CAS  PubMed  Google Scholar 

  25. Dietrich H, Dacey R. Molecular keys to the problems of cerebral vasospasm. Neurosurgery. 2000 Mar;46(3):517–30. https://doi.org/10.1097/00006123-200003000-00001.

    Article  CAS  PubMed  Google Scholar 

  26. Clark JF, Sharp FR. Bilirubin oxidation products (BOXes) and their role in cerebral vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006 Oct;26(10):1223–33. https://doi.org/10.1038/sj.jcbfm.9600280.

    Article  CAS  PubMed  Google Scholar 

  27. Sharkey J, Butcher SP, Kelly JS. Endothelin-1 induced middle cerebral artery occlusion: pathological consequences and neuroprotective effects of MK801. J Auton Nerv Syst. 1994 Sep;49(Suppl):S177–85. https://doi.org/10.1016/0165-1838(94)90109-.

    Article  CAS  PubMed  Google Scholar 

  28. Gaetani P, Rodriguez y Baena R, Grignani G, Spanu G, Pacchiarini L and Paoletti P. Endothelin and aneurysmal subarachnoid haemorrhage: a study of subarachnoid cisternal cerebrospinal fluid. J Neurol Neurosurg Psychiatry. 1994;57:66–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hansen-Schwartz J, Hoel NL, Zhou M, Xu CB, Svendgaard NA, Edvinsson L. Subarachnoid hemorrhage enhances endothelin receptor expression and function in rat cerebral arteries. Neurosurgery. 2003 May;52(5):1188–94.

    PubMed  Google Scholar 

  30. Rothoerl RD, Ringel F. Molecular mechanisms of cerebral vasospasm following aneurysmal SAH. Neurol Res. 2007 Oct;29(7):636–42. https://doi.org/10.1179/016164107X240224.

    Article  CAS  PubMed  Google Scholar 

  31. Grassie ME, Moffat LD, Walsh MP, MacDonald JA. The myosin phosphatase targeting protein (MYPT) family: a regulated mechanism for achieving substrate specificity of the catalytic subunit of protein phosphatase type 1delta. Arch Biochem Biophys. 2011 Jun 15;510(2):147–59.

    Article  CAS  PubMed  Google Scholar 

  32. Miao L, Dai Y, Zhang J. Mechanism of RhoA/Rho kinase activation in endothelin-1-induced contraction in rabbit basilar artery. Am J Physiol Heart Circ Physiol. 2002 Sep;283(3):H983–9. https://doi.org/10.1152/ajpheart.00141.2002.

    Article  CAS  PubMed  Google Scholar 

  33. Kikkawa Y, Matsuo S, Kameda K, Hirano M, Nakamizo A, Sasaki T, Hirano K. Mechanisms underlying potentiation of endothelin-1-induced myofilament Ca(2+) sensitization after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2012 Feb;32(2):341–52. https://doi.org/10.1038/jcbfm.2011.132.

    Article  CAS  PubMed  Google Scholar 

  34. Nakamura K, Koga Y, Sakai H, Homma K, Ikebe M. cGMP-dependent relaxation of smooth muscle is coupled with the change in the phosphorylation of myosin phosphatase. Circ Res. 2 Aug 2007;(101):712–22. https://doi.org/10.1161/CIRCRESAHA.107.153981.

  35. Zhou C, Yamaguchi M, Kusaka G, Schonholz C, Nanda A, Zhang JH. Caspase inhibitors prevent endothelial apoptosis and cerebral vasospasm in dog model of experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004 Apr;24(4):419–31. https://doi.org/10.1097/00004647-200404000-00007.

    Article  CAS  PubMed  Google Scholar 

  36. Zubkov AY, Ogihara K, Bernanke DH, Parent AD, Zhang J. Apoptosis of endothelial cells in vessels affected by cerebral vasospasm. Surg Neurol. 2000 Mar;53(3):260–6. https://doi.org/10.1016/s0090-3019(99)00187-1.

    Article  CAS  PubMed  Google Scholar 

  37. Kimura H, Gules I, Meguro T, Zhang JH. Cytotoxicity of cytokines in cerebral microvascular endothelial cell. Brain Res. 2003 Nov 14;990(1–2):148–56. https://doi.org/10.1016/s0006-8993(03)03450-4.

    Article  CAS  PubMed  Google Scholar 

  38. Iseda K, Ono S, Onoda K, Satoh M, Manabe H, Nishiguchi M, Takahashi K, Tokunaga K, Sugiu K, Date I. Antivasospastic and antiinflammatory effects of caspase inhibitor in experimental subarachnoid hemorrhage. J Neurosurg. 2007 Jul;107(1):128–35. https://doi.org/10.3171/JNS-07/07/0128.

    Article  CAS  PubMed  Google Scholar 

  39. Satoh S, Suzuki Y, Harada T, Ikegaki I, Asano T, Shibuya M, Sugita K, Saito A. The role of platelets in the development of cerebral vasospasm. Brain Res Bull. 1991 Nov;27(5):663–8. https://doi.org/10.1016/0361-9230(91)90042-i.

    Article  CAS  PubMed  Google Scholar 

  40. Takeuchi H, Tanabe M, Okamoto H, Yamazaki M. Effects of thromboxane synthetase inhibitor (RS-5186) on experimentally-induced cerebral vasospasm. Neurol Res. 1999 Jul;21(5):513–6.

    Article  CAS  PubMed  Google Scholar 

  41. Fassbender K, Hodapp B, Rossol S, Bertsch T, Schmeck J, Schutt S, Fritzinger M, Horn P, Vajkoczy P, Wendel-Wellner M, Ragoschke A, Kuehl S, Brunner J, Schurer L, Schmiedeck P, Hennerici M. Endothelin-1 in subarachnoid hemorrhage: an acute-phase reactant produced by cerebrospinal fluid leukocytes. Stroke. 2000 Dec;31(12):2971–5. https://doi.org/10.1161/01.str.31.12.2971.

    Article  CAS  PubMed  Google Scholar 

  42. Polin RS, Bavbek M, Shaffrey ME, Billups K, Bogaev CA, Kassell NF, Lee KS. Detection of soluble E-selectin, ICAM-1, VCAM-1, and L-selectin in the cerebrospinal fluid of patients after subarachnoid hemorrhage. J Neurosurg. 1998 Oct;89(4):559–67. https://doi.org/10.3171/jns.1998.89.4.0559.

    Article  CAS  PubMed  Google Scholar 

  43. Bavbek M, Polin R, Kwan AL, Arthur AS, Kassell NF, Lee KS. Monoclonal antibodies against ICAM-1 and CD18 attenuate cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits. Stroke. 1998 Sep;29(9):1930–5. https://doi.org/10.1161/01.str.29.9.1930.

    Article  CAS  PubMed  Google Scholar 

  44. Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. Inflammation in the brain after experimental subarachnoid hemorrhage. Neurosurgery. 2005 May;56(5):1082–92.

    PubMed  Google Scholar 

  45. Allen BG, Walsh MP. The biochemical basis of the regulation of smooth-muscle contraction. Trends Biochem Sci. 1994 Sep;19(9):362–8. https://doi.org/10.1016/0968-0004(94)90112-0.

    Article  CAS  PubMed  Google Scholar 

  46. Hoffman WE, Wheeler P, Edelman G, Charbel FT, Torres NJ, Ausman JI. Hypoxic brain tissue following subarachnoid hemorrhage. Anesthesiology. 2000 Feb;92(2):442–6. https://doi.org/10.1097/00000542-200002000-00026.

    Article  CAS  PubMed  Google Scholar 

  47. Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke. 2004;35(2412–2417) https://doi.org/10.1161/01.STR.0000141162.29864.e9.

  48. Jan Claassen J, Carhuapoma R, Kreiter KT, Du EY, Sander Connolly E, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33:1225–32. https://doi.org/10.1161/01.STR.0000015624.29071.1F.

    Article  PubMed  Google Scholar 

  49. Semenza GL. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda, MD). 2009 Apr;24:97–106. https://doi.org/10.1152/physiol.00045.2008.

    Article  CAS  Google Scholar 

  50. Schmidt-Kastner R, Aguirre-Chen C, Kietzmann T, Saul I, Busto R, Ginsberg MD. Nuclear localization of the hypoxia-regulated pro-apoptotic protein BNIP3 after global brain ischemia in the rat hippocampus. Brain Res. 2004 Mar 19;1001(1–2):133–42. https://doi.org/10.1016/j.brainres.2003.11.065.

    Article  CAS  PubMed  Google Scholar 

  51. Yan J, Chen C, Lei J, Yang L, Wang K, Liu J, Zhou C. 2-methoxyestradiol reduces cerebral vasospasm after 48 hours of experimental subarachnoid hemorrhage in rats. Exp Neurol. 2006;202(2):348–56.

    Article  CAS  PubMed  Google Scholar 

  52. Cahill J, Calvert JW, Solaroglu I, Zhang JH. Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke. 2006 Jul;37(7):1868–74. https://doi.org/10.1161/01.STR.0000226995.27230.96.

    Article  PubMed  Google Scholar 

  53. Cahill J, Calvert JW, Marcantonio S, Zhang JH. p53 may play an orchestrating role in apoptotic cell death after experimental subarachnoid hemorrhage. Neurosurgery. 2007 Mar;60(3):531–45. https://doi.org/10.1227/01.NEU.0000249287.99878.9B.

    Article  PubMed  Google Scholar 

  54. Pearl JD, Macdonald RL. Vasospasm after aneurysmal subarachnoid hemorrhage: need for further study. Acta Neurochir Suppl. 2008;105:207–10.

    Article  CAS  PubMed  Google Scholar 

  55. Guney O, Erdi F, Esen H, Kiyici A, Kocaogullar Y. N-acetylcysteine prevents vasospasm after subarachnoid hemorrhage. World Neurosurg. 2010 Jan;73(1):42–9. https://doi.org/10.1016/j.surneu.2009.06.003.

    Article  PubMed  Google Scholar 

  56. Munakata A, Ohkuma H, Shimamura N. Effect of a free radical scavenger, edaravone, on free radical reactions: related signal transduction and cerebral vasospasm in the rabbit subarachnoid hemorrhage model. Acta Neurochir Suppl. 2011;110(Pt 2):17–22. https://doi.org/10.1007/978-3-7091-0356-2_4.17-22.

    Article  PubMed  Google Scholar 

  57. Hofmann F. The biology of cyclic GMP-dependent protein kinases. J Biol Chem. 2005 Jan;280(1):1–4. https://doi.org/10.1074/jbc.R400035200.

    Article  CAS  PubMed  Google Scholar 

  58. Kehl F, Cambj-Sapunar L, Maier KG, Miyata N, Kametani S, Okamoto H, Hudetz AG, Schulte ML, Zagorac D, Harder DR, Roman RJ. 20-HETE contributes to the acute fall in cerebral blood flow after subarachnoid hemorrhage in the rat. Am J Physiol Heart Circ Physiol. 2002 Apr;282(4):H1556–65. https://doi.org/10.1152/ajpheart.00924.200.

    Article  CAS  PubMed  Google Scholar 

  59. Kim DE, Suh YS, Lee MS, Kim KY, Lee JH, Lee HS, Hong KW, Kim CD. Vascular NAD(P)H oxidase triggers delayed cerebral vasospasm after subarachnoid hemorrhage in rats. Stroke. 2002 Nov;33(11):2687–91. https://doi.org/10.1161/01.str.0000033071.99143.9e.

    Article  CAS  PubMed  Google Scholar 

  60. Zheng JS, Zhan RY, Zheng SS, Zhou YQ, Tong Y, Wan S. Inhibition of NADPH oxidase attenuates vasospasm after experimental subarachnoid hemorrhage in rats. Stroke. 2005 May;36(5):1059–64. https://doi.org/10.1161/01.STR.0000163102.49888.b7.

    Article  CAS  PubMed  Google Scholar 

  61. Pyne-Geithman GJ, Caudell DN, Prakash P, Clark JF. Glutathione peroxidase and subarachnoid hemorrhage: implications for the role of oxidative stress in cerebral vasospasm. Neurol Res. 2009 Mar;31(2):195–9. https://doi.org/10.1179/174313209X393906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Pluta RM, Hansen-Schwartz J, Dreier J, et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res. 2009 Mar;31(2):151–8. https://doi.org/10.1179/174313209X393564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Andresen J, Shafi NI, Bryan RM Jr. Endothelial influences on cerebrovascular tone. J Appl Physiol. 2006 Jan;100(1):318–27. https://doi.org/10.1152/japplphysiol.00937.2005.

    Article  CAS  PubMed  Google Scholar 

  64. Kolias AG, Sen J, Belli A. Pathogenesis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: putative mechanisms and novel approaches. J Neurosci Res. 2009 Jan;87(1):1–11. https://doi.org/10.1002/jnr.21823.

    Article  CAS  PubMed  Google Scholar 

  65. Leao AA. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–90.

    Article  Google Scholar 

  66. Leao AA. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol. 1947 Nov;10(6):409–14. https://doi.org/10.1152/jn.1947.10.6.409.

    Article  CAS  PubMed  Google Scholar 

  67. Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann T-N, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006 Dec;129(Pt 12):3224–37. https://doi.org/10.1093/brain/awl297.

    Article  PubMed  Google Scholar 

  68. Sotero RC, Trujillo-Barreto NJ. Biophysical model for integrating neuronal activity, EEG, fMRI and metabolism. Neuroimage. https://doi.org/10.1016/j.neuroimage.2007.08.001.

  69. Filosa JA. Vascular tone and neurovascular coupling: considerations toward an improved in vitro model. Front Neuroenergetics. 2010;2:16. https://doi.org/10.3389/fnene.2010.00016.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Gardner-Medwin AR. Analysis of potassium dynamics in mammalian brain tissue. J Physiol. 1983 Feb;335:393–426. https://doi.org/10.1113/jphysiol.1983.sp014541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Orellana JA, Sáez PJ, Shoji KF, Schalper KA, Palacios-Prado N, Velarde V, Giaume C, Bennett MVL, Sáez JC. Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid Redox Signal. 2009;11:369–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Lindauer U, Kunz A, Schuh-Hofer S, Vogt J, Dreier JP, Dirnagl U. Nitric oxide from perivascular nerves modulates cerebral arterial pH reactivity. Am J Physiol Heart Circ Physiol. 2001 Sep;281(3):H1353–63. https://doi.org/10.1152/ajpheart.2001.281.3.H1353.

    Article  CAS  PubMed  Google Scholar 

  73. Horiuchi T, Dietrich HH, Hongo K, Goto T, Dacey RG Jr. Role of endothelial nitric oxide and smooth muscle potassium channels in cerebral arteriolar dilation in response to acidosis. Stroke. 2002;33:844–9. https://doi.org/10.1161/hs0302.104112.

    Article  CAS  PubMed  Google Scholar 

  74. Lindauer U, Vogt J, Schuh-Hofer S, Dreier JP, Dirnagl U. Cerebrovascular vasodilation to extraluminal acidosis occurs via combined activation of ATP-sensitive and Ca2+-activated potassium channels. J Cereb Blood Flow Metab. 2003;23:1227–38.

    Article  CAS  PubMed  Google Scholar 

  75. Celotto AC, Capellini VK, Baldo CF, Dalio MB, Rodrigues AJ, Evora PRB. Effects of acid-base imbalance on vascular reactivity. Braz J Med Biol Res. 2008 Jun;41(6):439–45. https://doi.org/10.1590/s0100-879x2008005000026.

    Article  CAS  PubMed  Google Scholar 

  76. Kleeberg J, Petzold GC, Major S, Dirnagl U, Dreier JP. ET-1 induces cortical spreading depression via activation of the ETA receptor/phospholipase C pathway in vivo. Am J Physiol Heart Circ Physiol. 2004;286:H1339–46.

    Article  CAS  PubMed  Google Scholar 

  77. Yufu K, Itoh T, Edamatsu R, Mori A, Hirakawa M. Effect of hyperbaric oxygenation on the Na+, K(+)-ATPase and membrane fluidity of cerebrocortical membranes after experimental subarachnoid hemorrhage. Neurochem Res. 1993;18:1033–9.

    Article  CAS  PubMed  Google Scholar 

  78. Mortimer AM, Steinfort B, Faulder K, Bradford C, Finfer S, Assaad N, Harrington T. The detrimental clinical impact of severe angiographic vasospasm may be diminished by maximal medical therapy and intensive endovascular treatment. J Neurointerv Surg. 2015 Dec;7(12):881–7. https://doi.org/10.1136/neurintsurg-2014-011403.

    Article  PubMed  Google Scholar 

  79. Chugh C, Agarwal H. Cerebral vasospasm and delayed cerebral ischemia: Review of literature and the management approach. Neurol India. 2019;67(1):185–200. https://doi.org/10.4103/0028-3886.253627.

    Article  PubMed  Google Scholar 

  80. Treggiari MM. Hemodynamic management of subarachnoid hemorrhage. Neurocrit Care. 2011 Sep;15(2):329–35. https://doi.org/10.1007/s12028-011-9589-5.

    Article  PubMed  Google Scholar 

  81. Lindegaard KF, Nornes H, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm after subarachnoid hemorrhage investigated by means of transcranial Doppler ultrasound. Acta Neurochir Suppl (Wien). 1988;42:81–4. https://doi.org/10.1007/978-3-7091-8975-7_16.

    Article  CAS  Google Scholar 

  82. Meyer R, Deem S, Yanez ND, Souter M, Lam A, Treggiari MM. Current practices of triple-H prophylaxis and therapy in patients with subarachnoid hemorrhage. Neurocrit Care. 2011 Feb;14(1):24–36. https://doi.org/10.1007/s12028-010-9437-z.

    Article  PubMed  Google Scholar 

  83. Soustiel JF, Shik V, Shreiber R, Tavor Y, Goldsher D. Basilar vasospasm diagnosis. Stroke. 2002;33:72–8.

    Article  PubMed  Google Scholar 

  84. Kassell NF, Haley EC Jr, Apperson-Hansen C, Alves WM. Randomized, double-blind, vehicle-controlled trial of tirilazad mesylate in patients with aneurysmal subarachnoid hemorrhage: a cooperative study in Europe, Australia, and New Zealand. J Neurosurg. 1996 Feb;84(2):221–8. https://doi.org/10.3171/jns.1996.84.2.0221.

    Article  CAS  PubMed  Google Scholar 

  85. Pollock DM, Keith TL, Highsmith RF. Endothelin receptors and calcium signaling. FASEB J. 1995 Sep;9(12):1196–204. https://doi.org/10.1096/fasebj.9.12.7672512.

    Article  CAS  PubMed  Google Scholar 

  86. Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, Vajkoczy P, Wanke I, Frey A, Marr A, Roux S, Kassell NF. Preventing vasospasm improves outcome after aneurysmal subarachnoid hemorrhage: rationale and design of CONSCIOUS-2 and CONSCIOUS-3 trials. Neurocrit Care. 2010 Dec;13(3):416–24. https://doi.org/10.1007/s12028-010.

    Article  PubMed  Google Scholar 

  87. Tseng MY. Summary of evidence on immediate statins therapy following aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2011 Sep;15(2):298–301. https://doi.org/10.1007/s12028-011-9596-6.

    Article  CAS  PubMed  Google Scholar 

  88. Kirkpatrick PJ, Turner CL, Christopher Smith PJ, Hutchinson PG, Murray D. Simvastatin in aneurysmal subarachnoid haemorrhage (STASH): a multicentre randomised phase 3 trial. Lancet. 2014;13:666–75.

    Article  CAS  Google Scholar 

  89. Kruuse C, Gupta S, Nilsson E, Kruse L, Edvinsson L. Differential vasoactive effects of sildenafil and tadalafil on cerebral arteries. Eur J Pharmacol. 2012 Jan 15;674(2–3):345–51. https://doi.org/10.1016/j.ejphar.2011.10.037.

    Article  CAS  PubMed  Google Scholar 

  90. Mukherjee KK, Singh SK, Khosla VK, Mohindra S, Salunke P. Safety and efficacy of sildenafil citrate in reversal of cerebral vasospasm: a feasibility study. Surg Neurol Int. 2012;3:3. https://doi.org/10.4103/2152-7806.92164.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Fathi AR, Bakhtian KD, Pluta RM. The role of nitric oxide donors in treating cerebral vasospasm after subarachnoid hemorrhage. Acta Neurochir Suppl. 2011;110(Pt 1):93–7. https://doi.org/10.1007/978-3-7091-0353-1_17.

    Article  PubMed  Google Scholar 

  92. Pathak A, Mathuriya SN, Khandelwal N, Verma K. Intermittent low dose intrathecal sodium nitroprusside therapy for treatment of symptomatic aneurysmal SAH-induced vasospasm. Br J Neurosurg. 2003 Aug;17(4):306–10. https://doi.org/10.1080/02688690310001601180.

    Article  CAS  PubMed  Google Scholar 

  93. Fathi AR, Pluta RM, Bakhtian KD, Qi M, Lonser RR. Reversal of cerebral vasospasm via intravenous sodium nitrite after subarachnoid hemorrhage in primates. J Neurosurg. 2011 Dec;115(6):1213–20. https://doi.org/10.3171/2011.7.JNS11390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Iseri LT, French JH. Magnesium: nature’s physiologic calcium blocker. Am Heart J. 1984;108:188–93.

    Article  CAS  PubMed  Google Scholar 

  95. Castanares-Zapatero D, Hantson P. Pharmacological treatment of delayed cerebral ischemia and vasospasm in subarachnoid hemorrhage. Ann Intens Care. 2011;1:12. https://doi.org/10.1186/2110-5820-1-12.

    Article  CAS  Google Scholar 

  96. Suarez JI. Magnesium sulfate administration in subarachnoid hemorrhage. Neurocrit Care. 2011 Sep;15(2):302–7. https://doi.org/10.1007/s12028-011-9603-y.

    Article  CAS  PubMed  Google Scholar 

  97. Wong GK, Poon WS, Chan MT, Boet R, Gin T, Ng SC, Zee BC. Intravenous magnesium sulphate for aneurysmal subarachnoid hemorrhage (IMASH): a randomized, double-blinded, placebo-controlled, multicenter phase III trial. Stroke. 2010 May;41(5):921–6. https://doi.org/10.1161/STROKEAHA.109.571125.

    Article  CAS  PubMed  Google Scholar 

  98. Vergouwen MD. Magnesium sulfate for aneurysmal subarachnoid hemorrhage: the end of the road or more trials? Crit Care (London, Engl). 2011;15(2):140. https://doi.org/10.1186/cc10055.

    Article  Google Scholar 

  99. Benedict CR, Loach AB. Sympathetic nervous system activity in patients with subarachnoid hemorrhage. Stroke. 1978;9(3):237–44. https://doi.org/10.1161/01.str.9.3.237.

    Article  CAS  PubMed  Google Scholar 

  100. Ogura T, Satoh A, Ooigawa H, Sugiyama T, Takeda R, Fushihara G, et al. Characteristics and prognostic value of acute catecholamine surge in patients with aneurysmal subarachnoid hemorrhage. Neurol Res. 2012 Jun;34(5):484–90. https://doi.org/10.1179/1743132812Y.0000000033.

    Article  CAS  PubMed  Google Scholar 

  101. Hall A, O’Kane R. The extracranial consequences of subarachnoid hemorrhage. World Neurosurg. 2018 Jan;109:381–92. https://doi.org/10.1016/j.wneu.2017.10.016.

    Article  PubMed  Google Scholar 

  102. Fernandez A, Schmidt JM, Claassen J, Pavlicova M, Huddleston D, Kreiter KT, Ostapkovich ND, Kowalski RG, Parra A, Sander Connolly E, Mayer SA. Fever after subarachnoid hemorrhage: risk factors and impact on outcome. Neurology. 2007 Mar 27;68(13):1013–9. https://doi.org/10.1212/01.wnl.0000258543.45879.f5.

    Article  CAS  PubMed  Google Scholar 

  103. Kramer CL, Pegoli M, Mandrekar J, Lanzino G, Rabinstein AA. Refining the association of fever with functional outcome in aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2017 Feb;26(1):41–7. https://doi.org/10.1007/s12028-016-0281-7.

    Article  PubMed  Google Scholar 

  104. Schubert GA, Poli S, Schilling L, Heiland S, Thomé C. Hypothermia reduces cytotoxic edema and metabolic alterations during the acute phase of massive SAH: a diffusion-weighted imaging and spectroscopy study in rats. J Neurotrauma. 2008;25:841–52.

    Article  PubMed  Google Scholar 

  105. Török E, Klopotowski M, Trabold R, Thal SC, Plesnila N, Schöller K. Mild hypothermia (33 °C) reduces intracranial hypertension and improves functional outcome after subarachnoid hemorrhage in rats. Neurosurgery. 2009;65:352–9.

    Article  PubMed  Google Scholar 

  106. Badjatia N, Fernandez L, Schmidt JM, Lee K, Claassen J, Connolly ES, Mayer SA. Impact of induced normothermia on outcome after subarachnoid hemorrhage: a case-control study. Neurosurgery. 2010;66(4):696–700. https://doi.org/10.1227/01.NEU.0000367618.42794.AA.

    Article  PubMed  Google Scholar 

  107. Kuramatsu JB, Kollmar R, Gerner ST, Madzar D, Pisarcikova A, Staykov D, et al. Is hypothermia helpful in severe subarachnoid hemorrhage? An exploratory study on macro vascular spasm, delayed cerebral infarction and functional outcome after prolonged hypothermia. Cerebrovasc Dis (Basel, Switzerland). 2015;40(5–6):228–35. https://doi.org/10.1159/000439178.

    Article  Google Scholar 

  108. Choi W, Kwon SC, Lee WJ, CheolWeon Y, Choi B, Lee H, Park ES, Ahn R. Feasibility and safety of mild therapeutic hypothermia in poor-grade subarachnoid hemorrhage: prospective pilot study. J Kor Med Sci. 2017 Aug;32(8):1337–44. https://doi.org/10.3346/jkms.2017.32.8.1337.

    Article  CAS  Google Scholar 

  109. Okazaki T, Hifumi T, Kawakita K, Shishido H, Ogawa D, Okauchi M. Atsushi Shindo, Masahiko Kawanishi, Takashi Tamiya, Yasuhiro Kuroda. Target serum sodium levels during intensive care unit management of aneurysmal subarachnoid hemorrhage. Shock. 2017 Nov;48(5):558–63. https://doi.org/10.1097/SHK.0000000000000897.

    Article  CAS  PubMed  Google Scholar 

  110. Shah K, Turgeon RD, Gooderham PA, Ensom MHH. Prevention and treatment of hyponatremia in patients with subarachnoid hemorrhage: a systematic review. World Neurosur. 2018;109:222–9.

    Article  Google Scholar 

  111. Beseoglu K, Etminan N, Steiger HJ, Hanggi D. The relation of early hypernatremia with clinical outcome in patients suffering from aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2014 Aug;123:164–8. https://doi.org/10.1016/j.clineuro.2014.05.022.

    Article  PubMed  Google Scholar 

  112. Spatenkova V, Bradac O, de Lacy P, Skrabalek P, Suchomel P. Dysnatremia as a poor prognostic indicator in patients with acute subarachnoid hemorrhage. J Neurosurg Sci. 2017 Aug;61(4):371–9. https://doi.org/10.23736/S0390-5616.16.03411-1.

    Article  PubMed  Google Scholar 

  113. Rabinstein AA, Lanzino G, Wijdicks EF. Multidisciplinary management and emerging therapeutic strategies in aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2010 May;9(5):504–19. https://doi.org/10.1016/S1474-4422(10)70087-9.

    Article  CAS  PubMed  Google Scholar 

  114. Wolf S. Routine management of volume status after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2011 Jul;10(7):626–36. https://doi.org/10.1016/S1474-4422(11)70109-0.

    Article  Google Scholar 

  115. Diringer MN, Bleck TP, Claude Hemphill J, Menon D, Shutter L, Vespa P, Bruder N, Connolly ES Jr, Citerio G, Gress D, Hanggi D, Hoh BL, Lanzino G, Le Roux P, Rabinstein A, Schmutzhard E, Stocchetti N, Suarez JI, Treggiari M, Tseng MY, Vergouwen MD, Wolf S, Zipfel G. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit Care. 2011;15:211–40.

    Article  PubMed  Google Scholar 

  116. Chittiboina P, Conrad S, McCarthy P, Nanda A, Guthikonda B. The evolving role of hemodilution in treatment of cerebral vasospasm: a historical perspective. World Neurosurg. 2011;75(5–6):660–4. https://doi.org/10.1016/j.wneu.2011.02.019.

    Article  PubMed  Google Scholar 

  117. Schanne FA, Kane AB, Young EE, Farber JL. Calcium dependence of toxic cell death: a final common pathway. Science (New York, NY). 1979 Nov 9;206(4419):700–2. https://doi.org/10.1126/science.386513.

    Article  CAS  Google Scholar 

  118. Auer LM. Pial arterial vasodilation by intravenous nimodipine in cats. Arzneimittelforschung. 1981;31(9):1423–5.

    CAS  PubMed  Google Scholar 

  119. Dale J, Landmark KH, Myhre E. The effects of nifedipine, a calcium antagonist, on platelet function. Am Heart J. 1983 Jan;105(1):103–5. https://doi.org/10.1016/0002-8703(83)90285-5.

    Article  CAS  PubMed  Google Scholar 

  120. Allen GS, Ahn HS, Preziosi TJ, Battye R, Boone SC, Boone SC. Cerebral arterial spasm: A controlled trial of nimodipine in patients with subarachnoid hemorrhage. New Engl J Med. 1983 Mar 17;308(11):619–24. https://doi.org/10.1056/NEJM198303173081103.

    Article  CAS  PubMed  Google Scholar 

  121. Mees SMD, Rinkel GJE, Feigin VL, Algra A, van den Bergh WM, Vermeulen M, van Gijn J. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2007 Jul 18;2007(3):CD000277. https://doi.org/10.1002/14651858.CD000277.

    Article  Google Scholar 

  122. Pickard JD, Murray GD, Illingworth R, Shaw MD, Teasdale GM, Foy PM, Humphrey PR, Lang DA, Nelson R, Richards P. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ. 1989 Mar 11;298(6674):636–42. https://doi.org/10.1136/bmj.298.6674.636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Murray GD. Surgical bleeding and calcium antagonists. British aneurysm nimodipine trial reported improved clinical outcome with nimodipine. Br Med J. 1995; https://doi.org/10.1136/bmj.311.7001.388c.

  124. Karinen P, Koivukangas P, Ohinmaa A, Koivukangas J, Ohman J. Cost-effectiveness analysis of nimodipine treatment after aneurysmal subarachnoid hemorrhage and surgery. J Neurosurg. 1988 Nov;69(5):683–6. https://doi.org/10.3171/jns.1988.69.5.0683.

    Article  Google Scholar 

  125. Bardutzky J, Witsch J, Juttler E, Schwab S, Vajkoczy P, Wolf S. EARLYDRAIN- outcome after early lumbar CSF-drainage in aneurysmal subarachnoid hemorrhage: study protocol for a randomized controlled trial. Randomized Controlled Trials. 2011;12:203.

    PubMed  Google Scholar 

  126. Al-Tamimi YZ, Bhargava D, Feltbower RG, Hall G, Goddard AJ, Quinn AC. Lumbar drainage of cerebrospinal fluid after aneurysmal subarachnoid hemorrhage: a prospective, randomized, controlled trial (LUMAS). Stroke. 2012 Mar;43(3):677–82. https://doi.org/10.1161/STROKEAHA.111.625731.

    Article  PubMed  Google Scholar 

  127. Yamamoto T, Esaki T, Nakao Y, Mori K. Efficacy of low-dose tissue-plasminogen activator intracisternal administration for the prevention of cerebral vasospasm after subarachnoid hemorrhage. World Neurosurg. 2010;73:675–82. https://doi.org/10.1016/j.wneu.2010.04.002.

    Article  PubMed  Google Scholar 

  128. Lu X, ChengyuanJi JW, You W, Wang W, Wang Z, Chen G. Intrathecal fibrinolysis for aneurysmal subarachnoid hemorrhage: evidence from randomized controlled trials and Cohort studies. Front Neurol. 2019;10:885. https://doi.org/10.3389/fneur.2019.00885.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Gaberel T. Intraventricular Fibrinolysis for Aneurysmal Subarachnoid Hemorrhage (FIVHeMA). Available online https://clinicaltrials.gov/ct2/show/NCT03187405. Accessed 01 February 2019.

  130. Kasuya H, Onda H, MikihikoTakeshita YO, Hori T. Efficacy and safety of nicardipine prolonged-release implants for preventing vasospasm in humans. Stroke. 2002 Apr;33(4):1011–105. https://doi.org/10.1161/01.str.0000014563.75483.22.

    Article  CAS  PubMed  Google Scholar 

  131. Kasuya H, Onda H, Sasahara A. Application of nicardipine prolonged-release implants: analysis of 97 consecutive patients with acute subarachnoid hemorrhage. Neurosurgery. 2005 May;56(5):895–902.

    PubMed  Google Scholar 

  132. Rosenwasser RH, Armonda RA, Thomas JE, Benitez RP, Gannon PM, Harrop J. Therapeutic modalities for the management of cerebral vasospasm: timing of endovascular options. Neurosurgery. 1999;44:975–9.

    Article  CAS  PubMed  Google Scholar 

  133. Zwienenberg-Lee M, Hartman J, Rudisill N, Madden LK, Smith K, Eskridge J. Effect of prophylactic transluminal balloon angioplasty on cerebral vasospasm and outcome in patients with Fisher grade III subarachnoid hemorrhage: results of a phase II multicenter, randomized, clinical trial. Stroke. 2008;39:1759–65.

    Article  PubMed  Google Scholar 

  134. Narayan V, Pendharkar H, Devi BI, Bhat DI, Shukla DP. Aggressive management of vasospasm with direct intra-arterial nimodipine therapy. Neurol India. 2018;66(2):416–22.

    Article  PubMed  Google Scholar 

  135. Vajkoczy P, Horn P, Bauhuf C, Munch E, Hubner U, Ing D, Thome C, Poeckler-Schoeninger C, Roth H, Schmiedek P. Effect of intra-arterial papaverine on regional cerebral blood flow in hemodynamically relevant cerebral vasospasm. Stroke. 2001;32:498–50. https://doi.org/10.1161/01.STR.32.2.498.

    Article  CAS  PubMed  Google Scholar 

  136. Firlik KS, Kaufmann AM, Firlik AD, Jungreis CA, Yonas H. Intra-arterial papaverine for the treatment of cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Surg Neurol. 1999 Jan;51(1):66–74. https://doi.org/10.1016/s0090-3019(97)00370-4.

    Article  CAS  PubMed  Google Scholar 

  137. Kerz T, Boor S, Beyer C, Welschehold S, Schuessler A, Oertel J. Effect of intraarterial papaverine or nimodipine on vessel diameter in patients with cerebral vasospasm after subarachnoid hemorrhage. Br J Neurosurg. 2012 Aug;26(4):517–24. https://doi.org/10.3109/02688697.2011.6507373.

    Article  PubMed  Google Scholar 

  138. Abulhasan YB, Jimenez JO, Teitelbaum J, Simoneau G, Angle MR. Milrinone for refractory cerebral vasospasm with delayed cerebral ischemia. J Neurosurg. 134(3):971–82.

    Google Scholar 

  139. Bejjani GK, Bank WO, Olan WJ, Sekhar LN. The efficacy and safety of angioplasty for cerebral vasospasm after subarachnoid hemorrhage. Neurosurgery. 1998;42:979–86.

    Article  CAS  PubMed  Google Scholar 

  140. Miley JT, Tariq N, Souslian FG, Qureshi N, Suri MF, Tummala RP. Comparison between angioplasty using compliant and noncompliant balloons for treatment of cerebral vasospasm associated with subarachnoid hemorrhage. Neurosurgery. 2011 Dec;69(2 Suppl):ons161-8. https://doi.org/10.1227/NEU.0b013e31822a8976.

    Article  Google Scholar 

  141. Kerz T, Boor S, Ulrich A, Beyer C, Hechtner M, Mueller-Forell W. Endovascular therapy for vasospasm after aneurysmatic subarachnoid hemorrhage. Br J Neurosurg. 2016 Oct;30(5):549–53. https://doi.org/10.3109/02688697.2016.1173193.

    Article  PubMed  Google Scholar 

  142. The invasive diagnostic and therapeutic management of cerebral vasospasm after aneurysmal subarachnoid haemorrhage trial (IMCVS) as cited by Chandril Chugh, Himanshu Agarwal in Cerebral vasospasm and delayed cerebral ischemia: Review of literature and the management approach. Neurol India. 2019; 67(1):185–200.

    Google Scholar 

  143. Sokolowski JD, Chen C-J, Ding D, Buell TJ, Raper DM, Ironside N, Taylor DG, Starke RM, Liu K. Endovascular treatment for cerebral vasospasm following aneurysmal subarachnoid hemorrhage: predictors of outcome and retreatment. J Interv Surg. 2018;10(4):367–74. https://doi.org/10.1136/neurintsurg-2017-013363.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Pathak, A. (2022). Aneurysmal SAH Induced Vasospasm: Pathogenesis and Management. In: Lv, X. (eds) Endovascular Surgery of Cerebral Aneurysms. Springer, Singapore. https://doi.org/10.1007/978-981-16-7102-9_2

Download citation

  • DOI: https://doi.org/10.1007/978-981-16-7102-9_2

  • Published:

  • Publisher Name: Springer, Singapore

  • Print ISBN: 978-981-16-7101-2

  • Online ISBN: 978-981-16-7102-9

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Navigation