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Early Events After Aneurysmal Subarachnoid Hemorrhage

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Neurovascular Events After Subarachnoid Hemorrhage

Part of the book series: Acta Neurochirurgica Supplement ((NEUROCHIRURGICA,volume 120))

Abstract

The first 72 h after aneurysmal subarachnoid hemorrhage (SAH) is a critical period for the patient. Most of the deaths in the SAH patient population occur during this time, and a number of key events activate and trigger mechanisms that not only contribute to early brain injury but evolve over time and participate in the delayed complications. This review highlights the contribution of key events to the early brain injury and to overall outcome after SAH.

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References

  1. Le Roux PD, Winn HR (1998) Management of the ruptured aneurysm. Neurosurg Clin N Am 9:525–540

    PubMed  Google Scholar 

  2. Macdonald RL, Weir BK (1991) A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 22:971–982

    Article  PubMed  CAS  Google Scholar 

  3. Simeone FA, Ryan KG, Cotter JR (1968) Prolonged experimental cerebral vasospasm. J Neurosurg 29:357–366

    Article  PubMed  CAS  Google Scholar 

  4. Dupont S, Rabinstein AA (2013) Extent of acute hydrocephalus after subarachnoid hemorrhage as a risk factor for poor functional outcome. Neurol Res 35:107–110

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Ishiguro M, Murakami K, Link T, Zvarova K, Tranmer BI, Morielli AD, Wellman GC (2008) Acute and chronic effects of oxyhemoglobin on voltage-dependent ion channels in cerebral arteries. Acta Neurochir Suppl 104:99–102

    Article  PubMed  CAS  Google Scholar 

  7. Sehba FA, Friedrich V (2013) Cerebral microvasculature is an early target of subarachnoid hemorrhage. Acta Neurochir Suppl 115:199–205

    PubMed  Google Scholar 

  8. Kajikawa H, Ohta T, Yoshikawa Y, Funatsu N, Yamamoto M, Someda K (1979) Cerebral vasospasm and hemoglobins – clinical and experimental studies. Neurol Med Chir (Tokyo) 19:61–71

    Article  CAS  Google Scholar 

  9. Meguro T, Chen B, Lancon J, Zhang JH (2001) Oxyhemoglobin induces caspase-mediated cell death in cerebral endothelial cells. J Neurochem 77:1128–1135

    Article  PubMed  CAS  Google Scholar 

  10. Rollins S, Perkins E, Mandybur G, Zhang JH (2002) Oxyhemoglobin produces necrosis, not apoptosis, in astrocytes. Brain Res 945:41–49

    Article  PubMed  CAS  Google Scholar 

  11. Sehba FA, Schwartz AY, Chereshnev I, Bederson JB (2000) Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. J Cereb Blood Flow Metab 20:604–611

    Article  PubMed  CAS  Google Scholar 

  12. Ishiguro M, Morielli AD, Zvarova K, Tranmer BI, Penar PL, Wellman GC (2006) Oxyhemoglobin-induced suppression of voltage-dependent K+ channels in cerebral arteries by enhanced tyrosine kinase activity. Circ Res 99:1252–1260

    Article  PubMed  CAS  Google Scholar 

  13. Ohlstein EH, Storer BL (1992) Oxyhemoglobin stimulation of endothelin production in cultured endothelial cells. J Neurosurg 77:274–278

    Article  PubMed  CAS  Google Scholar 

  14. Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517–554

    Article  PubMed  CAS  Google Scholar 

  15. Ozawa H, Nishida A, Mito T, Takashima S (1994) Immunohistochemical study of ferritin-positive cells in the cerebellar cortex with subarachnoidal hemorrhage in neonates. Brain Res 651:345–348

    Article  PubMed  CAS  Google Scholar 

  16. Ono S, Zhang ZD, Marton LS, Yamini B, Windmeyer E, Johns L, Kowalczuk A, Lin G, Macdonald RL (2000) Heme oxygenase-1 and ferritin are increased in cerebral arteries after subarachnoid hemorrhage in monkeys. J Cereb Blood Flow Metab 20:1066–1076

    Article  PubMed  CAS  Google Scholar 

  17. Petzold A, Worthington V, Appleby I, Kerr ME, Kitchen N, Smith M (2011) Cerebrospinal fluid ferritin level, a sensitive diagnostic test in late-presenting subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 20:489–493

    Article  PubMed  PubMed Central  Google Scholar 

  18. Lee JY, Keep RF, He Y, Sagher O, Hua Y, Xi G (2010) Hemoglobin and iron handling in brain after subarachnoid hemorrhage and the effect of deferoxamine on early brain injury. J Cereb Blood Flow Metab 30:1793–1803

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  19. Kranc KR, Pyne GJ, Tao L, Claridge TD, Harris DA, Cadoux-Hudson TA, Turnbull JJ, Schofield CJ, Clark JF (2000) Oxidative degradation of bilirubin produces vasoactive compounds. Eur J Biochem 267:7094–7101

    Article  PubMed  CAS  Google Scholar 

  20. Pyne-Geithman GJ, Morgan CJ, Wagner K, Dulaney EM, Carrozzella J, Kanter DS, Zuccarello M, Clark JF (2005) Bilirubin production and oxidation in CSF of patients with cerebral vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 25:1070–1077

    Article  PubMed  CAS  Google Scholar 

  21. Brinker T, Seifert V, Dietz H (1992) Cerebral blood flow and intracranial pressure during experimental subarachnoid haemorrhage. Acta Neurochir 115:47–52

    Article  PubMed  CAS  Google Scholar 

  22. Lee VH, Oh JK, Mulvagh SL, Wijdicks EF (2006) Mechanisms in neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage. Neurocrit Care 5:243–249

    Article  PubMed  Google Scholar 

  23. Brouwers PJ, Wijdicks EF, Hasan D, Vermeulen M, Wever EF, Frericks H, van Gijn J (1989) Serial electrocardiographic recording in aneurysmal subarachnoid hemorrhage. Stroke 20:1162–1167

    Article  PubMed  CAS  Google Scholar 

  24. Eisalo A, Perasalo J, Halonen PI (1972) Electrocardiographic abnormalities and some laboratory findings in patients with subarachnoid haemorrhage. Br Heart J 34:217–226

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. Frontera JA, Parra A, Shimbo D, Fernandez A, Schmidt JM, Peter P, Claassen J, Wartenberg KE, Rincon F, Badjatia N, Naidech A, Connolly ES, Mayer SA (2008) Cardiac arrhythmias after subarachnoid hemorrhage: risk factors and impact on outcome. Cerebrovasc Dis 26:71–78

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sakr YL, Lim N, Amaral AC, Ghosn I, Carvalho FB, Renard M, Vincent JL (2004) Relation of ECG changes to neurological outcome in patients with aneurysmal subarachnoid hemorrhage. Int J Cardiol 96:369–373

    Article  PubMed  Google Scholar 

  27. van der Kleij FG, Henselmans JM, van de Loosdrecht AA (1999) Cardiac arrhythmia as initial presentation of aneurysmal subarachnoid hemorrhage. Neth J Med 55:242–246

    Article  PubMed  Google Scholar 

  28. Norris JW, Hachinski VC, Myers MG, Callow J, Wong T, Moore RW (1979) Serum cardiac enzymes in stroke. Stroke 10:548–553

    Article  PubMed  CAS  Google Scholar 

  29. Fabinyi G, Hunt D, McKinley L (1977) Myocardial creatine kinase isoenzyme in serum after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 40:818–820

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Zhu BL, Ishikawa T, Michiue T, Li DR, Zhao D, Bessho Y, Kamikodai Y, Tsuda K, Okazaki S, Maeda H (2007) Postmortem cardiac troponin I and creatine kinase MB levels in the blood and pericardial fluid as markers of myocardial damage in medicolegal autopsy. Leg Med (Tokyo) 9:241–250

    Article  CAS  Google Scholar 

  31. Kolin A, Norris JW (1984) Myocardial damage from acute cerebral lesions. Stroke 15:990–993

    Article  PubMed  CAS  Google Scholar 

  32. Sato K, Masuda T, Izumi T (1999) Subarachnoid hemorrhage and myocardial damage clinical and experimental studies. Jpn Heart J 40:683–701

    Article  PubMed  CAS  Google Scholar 

  33. Masuda T, Sato K, Yamamoto S, Matsuyama N, Shimohama T, Matsunaga A, Obuchi S, Shiba Y, Shimizu S, Izumi T (2002) Sympathetic nervous activity and myocardial damage immediately after subarachnoid hemorrhage in a unique animal model. Stroke 33:1671–1676

    Article  PubMed  Google Scholar 

  34. Muroi C, Keller M, Pangalu A, Fortunati M, Yonekawa Y, Keller E (2008) Neurogenic pulmonary edema in patients with subarachnoid hemorrhage. J Neurosurg Anesthesiol 20:188–192

    Article  PubMed  Google Scholar 

  35. McLaughlin N, Bojanowski MW, Girard F, Denault A (2005) Pulmonary edema and cardiac dysfunction following subarachnoid hemorrhage. Can J Neurol Sci 32:178–185

    PubMed  Google Scholar 

  36. Walder B, Brundler MA, Totsch M, Elia N, Morel DR (2002) Influence of the type and rate of subarachnoid fluid infusion on lethal neurogenic pulmonary edema in rats. J Neurosurg Anesthesiol 14:194–203

    Article  PubMed  Google Scholar 

  37. Sehba FA, Pluta RM, Zhang JH (2011) Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol 43:27–40

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  38. Sehba FA, Hou J, Pluta RM, Zhang JH (2012) The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol 97:14–37

    Article  PubMed  PubMed Central  Google Scholar 

  39. Fein JM (1976) Brain energetics and circulatory control after subarachnoid hemorrhage. J Neurosurg 45:498–507

    Article  PubMed  CAS  Google Scholar 

  40. Fein JM (1978) Brain energetics and cerebral death. Ann N Y Acad Sci 315:97–104

    Article  PubMed  CAS  Google Scholar 

  41. Gewirtz RJ, Dhillon HS, Goes SE, DeAtley SM, Scheff SW (1999) Lactate and free fatty acids after subarachnoid hemorrhage. Brain Res 840:84–91

    Article  PubMed  CAS  Google Scholar 

  42. Sarrafzadeh AS, Sakowitz OW, Kiening KL, Benndorf G, Lanksch WR, Unterberg AW (2002) Bedside microdialysis: a tool to monitor cerebral metabolism in subarachnoid hemorrhage patients? Crit Care Med 30:1062–1070

    Article  PubMed  Google Scholar 

  43. Dreier JP, Drenckhahn C, Woitzik J, Major S, Offenhauser N, Weber-Carstens S, Wolf S, Strong AJ, Vajkoczy P, Hartings JA (2013) Spreading ischemia after aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl 115:125–129

    PubMed  Google Scholar 

  44. Kohno K, Sakaki S, Ohue S, Kumon Y, Matsuoka K (1991) Intracellular calcium levels in canine basilar artery smooth muscle following experimental subarachnoid hemorrhage: an electron microscopic cytochemical study. Acta Neuropathol 81:664–669

    Article  PubMed  CAS  Google Scholar 

  45. Wang J, Ohta S, Sakaki S, Araki N, Matsuda S, Sakanaka M (1994) Changes in Ca(++)-ATPase activity in smooth-muscle cell membranes of the canine basilar artery with experimental subarachnoid hemorrhage. J Neurosurg 80:269–275

    Article  PubMed  CAS  Google Scholar 

  46. Hubschmann OR (1987) The role of calcium in parenchymal cell injury in subarachnoid haemorrhage. Neurol Res 9:265–269

    PubMed  CAS  Google Scholar 

  47. Sakaki S, Ohue S, Kohno K, Takeda S (1989) Impairment of vascular reactivity and changes in intracellular calcium and calmodulin levels of smooth muscle cells in canine basilar arteries after subarachnoid hemorrhage. Neurosurgery 25:753–761

    Article  PubMed  CAS  Google Scholar 

  48. Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL 3rd, Vallabhajosyula P (1998) Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 42:352–360

    Article  PubMed  CAS  Google Scholar 

  49. Sehba FA, Ding WH, Chereshnev I, Bederson JB (1999) Effects of S-nitrosoglutathione on acute vasoconstriction and glutamate release after subarachnoid hemorrhage. Stroke 30:1955–1961

    Article  PubMed  CAS  Google Scholar 

  50. Yatsushige H, Calvert JW, Cahill J, Zhang JH (2006) Limited role of inducible nitric oxide synthase in blood-brain barrier function after experimental subarachnoid hemorrhage. J Neurotrauma 23:1874–1882

    Article  PubMed  Google Scholar 

  51. Durmaz R, Ozkara E, Kanbak G, Arslan O, Dokumacioğlu A, Kartkaya K, Atasoy M (2008) Nitric oxide level and adenosine deaminase activity in cerebrospinal fluid of patients with subarachnoid hemorrhage. Turk Neurosurg 18:157–164

    PubMed  Google Scholar 

  52. Jung CS, Oldfield EH, Harvey-White J, Espey MG, Zimmermann M, Seifert V, Pluta RM (2007) Association of an endogenous inhibitor of nitric oxide synthase with cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 107:945–950

    Article  PubMed  CAS  Google Scholar 

  53. Wang X, Zhu C, Zhang G, Lu Y (1995) Changes of endothelin during cerebral vasospasm after experimental subarachnoid hemorrhage. Chin Med J (Engl) 108:586–590

    CAS  Google Scholar 

  54. Kramer A, Fletcher J (2009) Do endothelin-receptor antagonists prevent delayed neurological deficits and poor outcomes after aneurysmal subarachnoid hemorrhage?: a meta-analysis. Stroke 40:3403–3406

    Article  PubMed  CAS  Google Scholar 

  55. Etminan N, Vergouwen MD, Ilodigwe D, Macdonald RL (2011) Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab 31:1443–1451

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  56. Mathiesen T, Edner G, Ulfarsson E, Andersson B (1997) Cerebrospinal fluid interleukin-1 receptor antagonist and tumor necrosis factor-alpha following subarachnoid hemorrhage. J Neurosurg 87:215–220

    Article  PubMed  CAS  Google Scholar 

  57. Dumont AS, Dumont RJ, Chow MM, Lin CL, Calisaneller T, Ley KF, Kassell NF, Lee KS (2003) Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery 53:123–133; discussion 133–135

    Article  PubMed  Google Scholar 

  58. Kaynar MY, Tanriverdi T, Kafadar AM, Kacira T, Uzun H, Aydin S, Gumustas K, Dirican A, Kuday C (2004) Detection of soluble intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in both cerebrospinal fluid and serum of patients after aneurysmal subarachnoid hemorrhage. J Neurosurg 101:1030–1036

    Article  PubMed  CAS  Google Scholar 

  59. Gaetani P, Marzatico F, Rodriguez Y, Baena R, Pacchiarini L, Vigano T, Grignani G, Crivellari MT, Benzi G (1990) Arachidonic acid metabolism and pathophysiologic aspects of subarachnoid hemorrhage in rats. Stroke 21:328–332

    Article  PubMed  CAS  Google Scholar 

  60. Lin CL, Hsu YT, Lin TK, Morrow JD, Hsu JC, Hsu YH, Hsieh TC, Tsay PK, Yen HC (2006) Increased levels of F2-isoprostanes following aneurysmal subarachnoid hemorrhage in humans. Free Radic Biol Med 40:1466–1473

    Article  PubMed  CAS  Google Scholar 

  61. Kamezaki T, Yanaka K, Nagase S, Fujita K, Kato N, Nose T (2002) Increased levels of lipid peroxides as predictive of symptomatic vasospasm and poor outcome after aneurysmal subarachnoid hemorrhage. J Neurosurg 97:1302–1305

    Article  PubMed  CAS  Google Scholar 

  62. Hsieh YP, Lin CL, Shiue AL, Yin H, Morrow JD, Hsu JC, Hsieh TC, Wei HJ, Yen HC (2009) Correlation of F4-neuroprostanes levels in cerebrospinal fluid with outcome of aneurysmal subarachnoid hemorrhage in humans. Free Radic Biol Med 47:814–824

    Article  PubMed  CAS  Google Scholar 

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Sehba, F.A., Friedrich, V. (2015). Early Events After Aneurysmal Subarachnoid Hemorrhage. In: Fandino, J., Marbacher, S., Fathi, AR., Muroi, C., Keller, E. (eds) Neurovascular Events After Subarachnoid Hemorrhage. Acta Neurochirurgica Supplement, vol 120. Springer, Cham. https://doi.org/10.1007/978-3-319-04981-6_4

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  • DOI: https://doi.org/10.1007/978-3-319-04981-6_4

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