Skip to main content
SpringerLink
Log in

Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm

  • Conference paper
  • First Online:
Book cover Cerebral Vasospasm

Part of the book series: Acta Neurochirurgica Supplement ((NEUROCHIRURGICA,volume 104))

Abstract

Aneurismal subarachnoid haemorrhage (SAH) is a devastating disease that is associated with significant morbidity and mortality. The mortality is approximately 50%, with 30% of survivors having significant morbidity. There is substantial evidence to suggest that oxidative stress is significant in the development of acute brain injury and cerebral vasospasm following SAH. There are several sources for the excessive generation of free radicals following SAH, including disrupted mitochondrial respiration and extracellular hemoglobin. There is also the upregulation of free radical producing enzymes such as inducible nitric oxide synthase (iNOS), xanthine oxidase, NADPH oxidase (NOX), as well as enzymes involved in the metabolism of arachidonic acid. Additionally, intrinsic antioxidant systems such as superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) are inhibited. Experiments have linked free radicals to the apoptosis of neurons and endothelial cells, BBB breakdown and the altered contractile response of cerebral vessels following SAH. Antioxidant therapy has provided neuroprotection and antispasmotic effects in experimental SAH and some therapies have demonstrated improved outcomes in clinical trials. These studies have laid a foundation for the use of antioxidants in the treatment of aneurismal SAH.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arai T, Takeyama N, Tanaka T (1999) Glutathione monoethyl ester and inhibition of the oxyhemoglobin-induced increase in cytosolic calcium in cultured smooth-muscle cells. J Neurosurg 90: 527–532

    Article  CAS  PubMed  Google Scholar 

  2. Arthur AS, Fergus AH, Lanzino G, Mathys J, Kassell NF, Lee KS (1997) Systemic administration of the iron chelator deferiprone attenuates subarachnoid hemorrhage-induced cerebral vasospasm in the rabbit. Neurosurgery 41: 1385–1391

    Article  CAS  PubMed  Google Scholar 

  3. Asano T (1999) Oxyhemoglobin as the principal cause of cerebral vasospasm: a holistic view of its actions. Crit Rev Neurosurg 9: 303–318

    Article  CAS  PubMed  Google Scholar 

  4. Asano T, Matsui T (1999) Antioxidant therapy against cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Cell Mol Neurobiol 19: 31–44

    CAS  PubMed  Google Scholar 

  5. Asano T, Takakura K, Sano K, Kikuchi H, Nagai H, Saito I, Tamura A, Ochiai C, Sasaki T (1996) Effects of a hydroxyl radical scavenger on delayed ischemic neurological deficits following aneurysmal subarachnoid hemorrhage: results of a multicenter, placebo-controlled double-blind trial. J Neurosurg 84: 792–803

    Article  CAS  PubMed  Google Scholar 

  6. Baena R, Gaetani P, Marzatico F, Benzi G, Pacchiarini L, Paoletti P (1989) Effects of nicardipine on the ex vivo release of eicosanoids after experimental subarachnoid hemorrhage. J Neurosurg 71: 903–908

    Article  Google Scholar 

  7. Baena R, Gaetani P, Silvani V, Spanu G, Marzatico F (1988) Effect of nimodipine on mitochondrial respiration in different rat brain areas after subarachnoid haemorrhage. Acta Neurochir Suppl (Wien) 43: 177–181

    Google Scholar 

  8. Barbosa MD, Arthur AS, Louis RH, MacDonald T, Polin RS, Gazak C, Kassell NF (2001) The novel 5-lipoxygenase inhibitor ABT-761 attenuates cerebral vasospasm in a rabbit model of subarachnoid hemorrhage. Neurosurgery 49: 1205–1212

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Bilgihan A, Turkozkan N, Aricioglu A, Aykol S, Cevik C, Goksel M (1994) The effect of deferoxamine on brain lipid peroxide levels and Na-K ATPase activity following experimental subarachnoid hemorrhage. Gen Pharmacol 25: 495–497

    Article  CAS  PubMed  Google Scholar 

  11. Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A (1994) Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 25: 1342–1347

    Article  CAS  PubMed  Google Scholar 

  12. Calvert JW, Zhang JH (2005) Pathophysiology of an hypoxicischemic insult during the perinatal period. Neurol Res 27: 246–260

    Article  PubMed  Google Scholar 

  13. Caro AA, Cederbaum AI (2006) Role of cytochrome P450 in phospholipase A2-and arachidonic acid-mediated cytotoxicity. Free Radic Biol Med 40: 364–375

    Article  CAS  PubMed  Google Scholar 

  14. Clark JF, Sharp FR (2006) Bilirubin oxidation products (BOXes) and their role in cerebral vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 26: 1223–1233

    Article  CAS  PubMed  Google Scholar 

  15. Eliasson MJ, Huang Z, Ferrante RJ, Sasamata M, Molliver ME, Snyder SH, Moskowitz MA (1999) Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci 19: 5910–5918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Endo H, Nito C, Kamada H, Yu F, Chan PH (2006) Reduction in oxidative stress by superoxide dismutase overexpression attenuates acute brain injury after subarachnoid hemorrhage via activation of Akt/glycogen synthase kinase-3beta survival signaling. J Cereb Blood Flow Metab

    Google Scholar 

  17. Facchinetti F, Dawson VL, Dawson TM (1998) Free radicals as mediators of neuronal injury. Cell Mol Neurobiol 18: 667–682

    CAS  PubMed  Google Scholar 

  18. Figueroa S, Oset-Gasque MJ, Arce C, Martinez-Honduvilla CJ, Gonzalez MP (2006) Mitochondrial involvement in nitric oxideinduced cellular death in cortical neurons in culture. J Neurosci Res 83: 441–449

    Article  CAS  PubMed  Google Scholar 

  19. Fiskum G, Rosenthal RE, Vereczki V, Martin E, Hoffman GE, Chinopoulos C, Kowaltowski A (2004) Protection against ischemic brain injury by inhibition of mitochondrial oxidative stress. J Bioenerg Biomembr 36: 347–352

    Article  CAS  PubMed  Google Scholar 

  20. Forman LJ, Liu P, Nagele RG, Yin K, Wong PY (1998) Augmentation of nitric oxide, superoxide, and peroxynitrite production during cerebral ischemia and reperfusion in the rat. Neurochem Res 23: 141–148

    Article  CAS  PubMed  Google Scholar 

  21. Gaetani P, Lombardi D (1992) Brain damage following subarachnoid hemorrhage: the imbalance between anti-oxidant systems and lipid peroxidative processes. J Neurosurg Sci 36: 1–10

    CAS  PubMed  Google Scholar 

  22. Gaetani P, Marzatico F, Lombardi D, Adinolfi D, Baena R (1991) Effect of high-dose methylprednisolone and U74006F on eicosanoid synthesis after subarachnoid hemorrhage in rats. Stroke 22: 215–220

    Article  CAS  PubMed  Google Scholar 

  23. Gaetani P, Pasqualin A, Baena R, Borasio E, Marzatico F (1998) Oxidative stress in the human brain after subarachnoid hemorrhage. J Neurosurg 89: 748–754

    Article  CAS  PubMed  Google Scholar 

  24. Germano A, Imperatore C, d’Avella D, Costa G, Tomasello F (1998) Antivasospastic and brain-protective effects of a hydroxyl radical scavenger (AVS) after experimental subarachnoid hemorrhage. J Neurosurg 88: 1075–1081

    Article  CAS  PubMed  Google Scholar 

  25. Gilgun-Sherki Y, Rosenbaum Z, Melamed E, Offen D (2002) Antioxidant therapy in acute central nervous system injury: current state. Pharmacol Rev 54: 271–284

    Article  CAS  PubMed  Google Scholar 

  26. Goldman DW, Breyer RJ III, Yeh D, Brockner-Ryan BA, Alayash AI (1998) Acellular hemoglobin-mediated oxidative stress toward endothelium: a role for ferryl iron. Am J Physiol 275: H1046–H1053

    CAS  PubMed  Google Scholar 

  27. Griendling KK, Ushio-Fukai M (1998) Redox control of vascular smooth muscle proliferation. J Lab Clin Med 132: 9–15

    Article  CAS  PubMed  Google Scholar 

  28. Grote E, Hassler W (1988) The critical first minutes after subarachnoid hemorrhage. Neurosurgery 22: 654–661

    Article  CAS  PubMed  Google Scholar 

  29. Gursoy-Ozdemir Y, Can A, Dalkara T (2004) Reperfusion-induced oxidative/nitrative injury to neurovascular unit after focal cerebral ischemia. Stroke 35: 1449–1453

    Article  PubMed  CAS  Google Scholar 

  30. Gutteridge JM (1986) Iron promoters of the Fenton reaction and lipid peroxidation can be released from haemoglobin by peroxides. FEBS Lett 201: 291–295

    Article  CAS  PubMed  Google Scholar 

  31. Haley EC Jr, Kassell NF, Apperson-Hansen C, Maile MH, Alves WM (1997) A randomized, double-blind, vehicle-controlled trial of tirilazad mesylate in patients with aneurysmal subarachnoid hemorrhage: a cooperative study in North America. J Neurosurg 86: 467–474

    Article  CAS  PubMed  Google Scholar 

  32. Hall ED, Andrus PK, Smith SL, Oostveen JA, Scherch HM, Lutzke BS, Raub TJ, Sawada GA, Palmer JR, Banitt LS (1996) Neuroprotective efficacy of microvascularly-localized versus brain-penetrating antioxidants. Acta Neurochir Suppl 66: 107–113

    CAS  PubMed  Google Scholar 

  33. Halliwell B (1978) Superoxide-dependent formation of hydroxyl radicals in the presence of iron chelates: is it a mechanism for hydroxyl radical production in biochemical systems? FEBS Lett 92: 321–326

    Article  CAS  PubMed  Google Scholar 

  34. Halliwell B (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am J Med 91: 14S–22S

    Article  CAS  PubMed  Google Scholar 

  35. Handa Y, Kaneko M, Takeuchi H, Tsuchida A, Kobayashi H, Kubota T (2000) Effect of an antioxidant, ebselen, on development of chronic cerebral vasospasm after subarachnoid hemorrhage in primates. Surg Neurol 53: 323–329

    Article  CAS  PubMed  Google Scholar 

  36. Haorah J, Knipe B, Leibhart J, Ghorpade A, Persidsky Y (2005) Alcohol-induced oxidative stress in brain endothelial cells causes blood-brain barrier dysfunction. J Leukoc Biol 78: 1223–1232

    Article  CAS  PubMed  Google Scholar 

  37. Harada T, Mayberg MR (1992) Inhibition of delayed arterial narrowing by the iron-chelating agent deferoxamine. J Neurosurg 77: 763–767

    Article  CAS  PubMed  Google Scholar 

  38. Horky LL, Pluta RM, Boock RJ, Oldfield EH (1998) Role of ferrous iron chelator 2,2′-dipyridyl in preventing delayed vasospasm in a primate model of subarachnoid hemorrhage. J Neurosurg 88: 298–303

    Article  CAS  PubMed  Google Scholar 

  39. Imperatore C, Germano A, d’Avella D, Tomasello F, Costa G (2000) Effects of the radical scavenger AVS on behavioral and BBB changes after experimental subarachnoid hemorrhage. Life Sci 66: 779–790

    Article  CAS  PubMed  Google Scholar 

  40. Jarus-Dziedzic K, Czernicki Z, Kozniewska E (2003) Acute decrease of cerebrocortical microflow and lack of carbon dioxide reactivity following subarachnoid haemorrhage in the rat. Acta Neurochir Suppl 86: 473–476

    CAS  PubMed  Google Scholar 

  41. Kanamaru K, Weir BK, Findlay JM, Grace M, Macdonald RL (1990) A dosage study of the effect of the 21-aminosteroid U74006F on chronic cerebral vasospasm in a primate model. Neurosurgery 27: 29–38

    Article  CAS  PubMed  Google Scholar 

  42. Kanamaru K, Weir BK, Simpson I, Witbeck T, Grace M (1991) Effect of 21-aminosteroid U-74006F on lipid peroxidation in subarachnoid clot. J Neurosurg 74: 454–459

    Article  CAS  PubMed  Google Scholar 

  43. Kaptain GJ, Lanzino G, Kassell NF (2000) Subarachnoid haemorrhage: epidemiology, risk factors, and treatment options. Drugs Aging 17: 183–199

    Article  CAS  PubMed  Google Scholar 

  44. Kassell NF, Haley EC Jr, Apperson-Hansen C, Alves WM (1996) 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 84: 221–228

    Article  CAS  PubMed  Google Scholar 

  45. Katsuki H, Akino N, Okuda S, Saito H (1995) Antioxidants, but not cAMP or high K+, prevent arachidonic acid toxicity on neuronal cultures. Neuroreport 6: 1101–1104

    Article  CAS  PubMed  Google Scholar 

  46. Kaynar MY, Tanriverdi T, Kemerdere R, Atukeren P, Gumustas K (2005) Cerebrospinal fluid superoxide dismutase and serum malondialdehyde levels in patients with aneurysmal subarachnoid hemorrhage: preliminary results. Neurol Res 27: 562–567

    Article  CAS  PubMed  Google Scholar 

  47. Khaldi A, Zauner A, Reinert M, Woodward JJ, Bullock MR (2001) Measurement of nitric oxide and brain tissue oxygen tension in patients after severe subarachnoid hemorrhage. Neurosurgery 49: 33–38

    CAS  PubMed  Google Scholar 

  48. Kim DE, Suh YS, Lee MS, Kim KY, Lee JH, Lee HS, Hong KW, Kim CD (2002) Vascular NAD(P)H oxidase triggers delayed cerebral vasospasm after subarachnoid hemorrhage in rats. Stroke 33: 2687–2691

    Article  CAS  PubMed  Google Scholar 

  49. Kim DE, Suh YS, Lee MS, Kim KY, Lee JH, Lee HS, Hong KW, Kim CD (2002) Vascular NAD(P)H oxidase triggers delayed cerebral vasospasm after subarachnoid hemorrhage in rats. Stroke 33: 2687–2691

    Article  CAS  PubMed  Google Scholar 

  50. Kim P, Yaksh TL, Romero SD, Sundt TM Jr (1987) Production of uric acid in cerebrospinal fluid after subarachnoid hemorrhage in dogs: investigation of the possible role of xanthine oxidase in chronic vasospasm. Neurosurgery 21: 39–44

    Article  CAS  PubMed  Google Scholar 

  51. 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  CAS  PubMed  Google Scholar 

  52. Lanzino G, Kassell NF (1999) Double-blind, randomized, vehiclecontrolled study of high-dose tirilazad mesylate in women with aneurysmal subarachnoid hemorrhage. Part II. A cooperative study in North America. J Neurosurg 90: 1018–1024

    Article  CAS  PubMed  Google Scholar 

  53. Lanzino G, Kassell NF, Dorsch NW, Pasqualin A, Brandt L, Schmiedek P, Truskowski LL, Alves WM (1999) Double-blind, randomized, vehicle-controlled study of high-dose tirilazad mesylate in women with aneurysmal subarachnoid hemorrhage. Part I: A cooperative study in Europe, Australia, New Zealand, and South Africa. J Neurosurg 90: 1011–1017

    Article  CAS  PubMed  Google Scholar 

  54. Lassegue B, Clempus RE (2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277–R297

    Article  CAS  PubMed  Google Scholar 

  55. Leist M, Nicotera P (1998) Apoptosis, excitotoxicity, and neuropathology. Exp Cell Res 239: 183–201

    Article  CAS  PubMed  Google Scholar 

  56. Lewen A, Matz P, Chan PH (2000) Free radical pathways in CNS injury. J Neurotrauma 17: 871–890

    Article  CAS  PubMed  Google Scholar 

  57. Lipton SA, Singel DJ, Stamler JS (1994) Nitric oxide in the central nervous system. Prog Brain Res 103: 359–364

    Article  CAS  PubMed  Google Scholar 

  58. Lipton SA, Stamler JS (1994) Actions of redox-related congeners of nitric oxide at the NMDA receptor. Neuropharmacology 33: 1229–1233

    Article  CAS  PubMed  Google Scholar 

  59. Longstreth WT Jr, Nelson LM, Koepsell TD, van Belle G (1993) Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington. Neurology 43: 712–718

    Article  PubMed  Google Scholar 

  60. Macdonald RL, Weir BK (1994) Cerebral vasospasm and free radicals. Free Radic Biol Med 16: 633–643

    Article  CAS  PubMed  Google Scholar 

  61. Maeda Y, Hirano K, Nishimura J, Sasaki T, Kanaide H (2004) Endothelial dysfunction and altered bradykinin response due to oxidative stress induced by serum deprivation in the bovine cerebral artery. Eur J Pharmacol 491: 53–60

    Article  CAS  PubMed  Google Scholar 

  62. Marklund N, Ostman B, Nalmo L, Persson L, Hillered L (2000) Hypoxanthine, uric acid and allantoin as indicators of in vivo free radical reactions. Description of a HPLC method and human brain microdialysis data. Acta Neurochir (Wien) 142: 1135–1141

    Article  CAS  PubMed  Google Scholar 

  63. Marzatico F, Gaetani P, Baena R, Silvani V, Paoletti P, Benzi G (1988) Bioenergetics of different brain areas after experimental subarachnoid hemorrhage in rats. Stroke 19: 378–384

    Article  CAS  PubMed  Google Scholar 

  64. Marzatico F, Gaetani P, Cafe C, Spanu G, Baena R (1993) Antioxidant enzymatic activities after experimental subarachnoid hemorrhage in rats. Acta Neurol Scand 87: 62–66

    Article  CAS  PubMed  Google Scholar 

  65. Marzatico F, Gaetani P, Silvani V, Lombardi D, Sinforiani E, Baena R (1990) Experimental isobaric subarachnoid hemorrhage: regional mitochondrial function during the acute and late phase. Surg Neurol 34: 294–300

    Article  CAS  PubMed  Google Scholar 

  66. Marzatico F, Gaetani P, Tartara F, Bertorelli L, Feletti F, Adinolfi D, Tancioni F, Baena R (1998) Antioxidant status and alpha1-antiproteinase activity in subarachnoid hemorrhage patients. Life Sci 63: 821–826

    Article  CAS  PubMed  Google Scholar 

  67. Matsui T, Asano T (1994) Effects of new 21-aminosteroid tirilazad mesylate (U74006F) on chronic cerebral vasospasm in a “twohemorrhage” model of beagle dogs. Neurosurgery 34: 1035–1039

    CAS  PubMed  Google Scholar 

  68. Matz P, Weinstein P, States B, Honkaniemi J, Sharp FR (1996) Subarachnoid injections of lysed blood induce the hsp70 stress gene and produce DNA fragmentation in focal areas of the rat brain. Stroke 27: 504–512

    Article  CAS  PubMed  Google Scholar 

  69. Matz PG, Copin JC, Chan PH (2000) Cell death after exposure to subarachnoid hemolysate correlates inversely with expression of CuZn-superoxide dismutase. Stroke 31: 2450–2459

    Article  CAS  PubMed  Google Scholar 

  70. Matz PG, Fujimura M, Chan PH (2000) Subarachnoid hemolysate produces DNA fragmentation in a pattern similar to apoptosis in mouse brain. Brain Res 858: 312–319

    Article  CAS  PubMed  Google Scholar 

  71. Matz PG, Fujimura M, Lewen A, Morita-Fujimura Y, Chan PH (2001) Increased cytochrome c-mediated DNA fragmentation and cell death in manganese-superoxide dismutase-deficient mice after exposure to subarachnoid hemolysate. Stroke 32: 506–515

    Article  CAS  PubMed  Google Scholar 

  72. McCormick WF, Nofzinger JD (1965) Saccular intracranial aneuryms: an autopsy study. J Neurosurg 22: 155–159

    Article  CAS  PubMed  Google Scholar 

  73. McGirt MJ, Parra A, Sheng H, Higuchi Y, Oury TD, Laskowitz DT, Pearlstein RD, Warner DS (2002) Attenuation of cerebral vasospasm after subarachnoid hemorrhage in mice overexpressing extracellular superoxide dismutase. Stroke 33: 2317–2323

    Article  CAS  PubMed  Google Scholar 

  74. Miller AA, Drummond GR, Sobey CG (2006) Novel isoforms of NADPH-oxidase in cerebral vascular control. Pharmacol Ther 111: 928–948

    Article  CAS  PubMed  Google Scholar 

  75. Misra HP, Fridovich I (1972) The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem 247: 6960–6962

    Article  CAS  PubMed  Google Scholar 

  76. Miyata N, Seki T, Tanaka Y, Omura T, Taniguchi K, Doi M, Bandou K, Kametani S, Sato M, Okuyama S (2005) Beneficial effects of a new 20-hydroxyeicosatetraenoic acid synthesis inhibitor, TS-011 [N-(3-chloro-4-morpholin-4-yl) phenyl-N′-hydroxyimido formamide], on hemorrhagic and ischemic stroke. J Pharmacol Exp Ther 314: 77–85

    Article  CAS  PubMed  Google Scholar 

  77. Mori T, Nagata K, Town T, Tan J, Matsui T, Asano T (2001) Intracisternal increase of superoxide anion production in a canine subarachnoid hemorrhage model. Stroke 32: 636–642

    Article  CAS  PubMed  Google Scholar 

  78. Moro MA, Almeida A, Bolanos JP, Lizasoain I (2005) Mitochondrial respiratory chain and free radical generation in stroke. Free Radic Biol Med 39: 1291–1304

    Article  CAS  PubMed  Google Scholar 

  79. Muralikrishna AR, Hatcher JF (2006) Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic Biol Med 40: 376–387

    Article  CAS  Google Scholar 

  80. Murphy AN, Fiskum G, Beal MF (1999) Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J Cereb Blood Flow Metab 19: 231–245

    Article  CAS  PubMed  Google Scholar 

  81. Naoi M, Maruyama W, Shamoto-Nagai M, Yi H, Akao Y, Tanaka M (2005) Oxidative stress in mitochondria: decision to survival and death of neurons in neurodegenerative disorders. Mol Neurobiol 31: 81–93

    Article  CAS  PubMed  Google Scholar 

  82. Ng WH, Moochhala S, Yeo TT, Ong PL, Ng PY (2001) Nitric oxide and subarachnoid hemorrhage: elevated level in cerebrospinal fluid and their implications. Neurosurgery 49: 622–626

    CAS  PubMed  Google Scholar 

  83. Nishino T, Tamura I (1991) The mechanism of conversion of xanthine dehydrogenase to oxidase and the role of the enzyme in reperfusion injury. Adv Exp Med Biol 309A: 327–333

    Article  CAS  PubMed  Google Scholar 

  84. Ostrowski RP, Colohan AR, Zhang JH (2006) Neuroprotective effect of hyperbaric oxygen in a rat model of subarachnoid hemorrhage. Acta Neurochir Suppl 96: 188–193

    Article  CAS  PubMed  Google Scholar 

  85. Ostrowski RP, Tang J, Zhang JH (2006) Hyperbaric oxygen suppresses NADPH oxidase in a rat subarachnoid hemorrhage model. Stroke 37: 1314–1318

    Article  CAS  PubMed  Google Scholar 

  86. Osuka K, Suzuki Y, Watanabe Y, Takayasu M, Yoshida J (1998) Inducible cyclooxygenase expression in canine basilar artery after experimental subarachnoid hemorrhage. Stroke 29: 1219–1222

    Article  CAS  PubMed  Google Scholar 

  87. Osuka K, Watanabe Y, Yamauchi K, Nakazawa A, Usuda N, Tokuda M, Yoshida J (2006) Activation of the JAK-STAT signaling pathway in the rat basilar artery after subarachnoid hemorrhage. Brain Res 1072: 1–7

    Article  CAS  PubMed  Google Scholar 

  88. Paravicini TM, Sobey CG (2003) Cerebral vascular effects of reactive oxygen species: recent evidence for a role of NADPH-oxidase. Clin Exp Pharmacol Physiol 30: 855–859

    Article  CAS  PubMed  Google Scholar 

  89. Phillis JW, O’Regan MH (2003) The role of phospholipases, cyclooxygenases, and lipoxygenases in cerebral ischemic=traumatic injuries. Crit Rev Neurobiol 15: 61–90

    Article  CAS  PubMed  Google Scholar 

  90. Reeder BJ, Sharpe MA, Kay AD, Kerr M, Moore K, Wilson MT (2002) Toxicity of myoglobin and haemoglobin: oxidative stress in patients with rhabdomyolysis and subarachnoid haemorrhage. Biochem Soc Trans 30: 745–748

    Article  CAS  PubMed  Google Scholar 

  91. Rogers MS, Patel RP, Reeder BJ, Sarti P, Wilson MT, Alayash AI (1995) Pro-oxidant effects of cross-linked haemoglobins explored using liposome and cytochrome c oxidase vesicle model membranes. Biochem J 310 (Pt 3): 827–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Sadrzadeh SM, Anderson DK, Panter SS, Hallaway PE, Eaton JW (1987) Hemoglobin potentiates central nervous system damage. J Clin Invest 79: 662–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Saito I, Asano T, Sano K, Takakura K, Abe H, Yoshimoto T, Kikuchi H, Ohta T, Ishibashi S (1998) Neuroprotective effect of an antioxidant, ebselen, in patients with delayed neurological deficits after aneurysmal subarachnoid hemorrhage. Neurosurgery 42: 269–277

    Article  CAS  PubMed  Google Scholar 

  94. Sarti P, Hogg N, Darley-Usmar VM, Sanna MT, Wilson MT (1994) The oxidation of cytochrome-c oxidase vesicles by hemoglobin. Biochim Biophys Acta 1208: 38–44

    Article  CAS  PubMed  Google Scholar 

  95. Schievink WI (1997) Intracranial aneurysms. N Engl J Med 336: 28–40

    Article  CAS  PubMed  Google Scholar 

  96. Schievink WI, Riedinger M, Jhutty TK, Simon P (2004) Racial disparities in subarachnoid hemorrhage mortality: Los Angeles County, California, 1985-1998. Neuroepidemiology 23: 299–305

    Article  PubMed  Google Scholar 

  97. Schulz R, Jancar S, Cook DA (1990) Cerebral arteries can generate 5-and 15-hydroxyeicosatetraenoic acid from arachidonic acid. Can J Physiol Pharmacol 68: 807–813

    Article  CAS  PubMed  Google Scholar 

  98. Sehba FA, Bederson JB (2006) Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res 28: 381–398

    Article  CAS  PubMed  Google Scholar 

  99. Sehba FA, Chereshnev I, Maayani S, Friedrich V Jr, Bederson JB (2004) Nitric oxide synthase in acute alteration of nitric oxide levels after subarachnoid hemorrhage. Neurosurgery 55: 671–677

    Article  PubMed  Google Scholar 

  100. Serrano F, Kolluri NS, Wientjes FB, Card JP, Klann E (2003) NADPH oxidase immunoreactivity in the mouse brain. Brain Res 988: 193–198

    Article  CAS  PubMed  Google Scholar 

  101. Sharma HS, Drieu K, Westman J (2003) Antioxidant compounds EGB-761 and BN-52021 attenuate brain edema formation and hemeoxygenase expression following hyperthermic brain injury in the rat. Acta Neurochir Suppl 86: 313–319

    Article  CAS  PubMed  Google Scholar 

  102. Shimizu T, Watanabe T, Asano T, Seyama Y, Takakura K (1988) Activation of the arachidonate 5-lipoxygenase pathway in the canine basilar artery after experimental subarachnoidal hemorrhage. J Neurochem 51: 1126–1131

    Article  CAS  PubMed  Google Scholar 

  103. Shin HK, Lee JH, Kim CD, Kim YK, Hong JY, Hong KW (2003) Prevention of impairment of cerebral blood flow autoregulation during acute stage of subarachnoid hemorrhage by gene transfer of Cu/Zn SOD-1 to cerebral vessels. J Cereb Blood Flow Metab 23: 111–120

    Article  CAS  PubMed  Google Scholar 

  104. Shin HK, Lee JH, Kim KY, Kim CD, Lee WS, Rhim BY, Hong KW (2002) Impairment of autoregulatory vasodilation by NAD(P)H oxidase-dependent superoxide generation during acute stage of subarachnoid hemorrhage in rat pial artery. J Cereb Blood Flow Metab 22: 869–877

    Article  CAS  PubMed  Google Scholar 

  105. Sippell G, Lehmann P, Hollmann G (1975) Automation of multiple sephadex LH-20 column chromatography for the simultaneous separation of plasma corticosteroids. J Chromatogr 108: 305–312

    Article  CAS  PubMed  Google Scholar 

  106. Suzuki H, Kanamaru K, Tsunoda H, Inada H, Kuroki M, Sun H, Waga S, Tanaka T (1999) Heme oxygenase-1 gene induction as an intrinsic regulation against delayed cerebral vasospasm in rats. J Clin Invest 104: 59–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Takenaka K, Kassell NF, Foley PL, Lee KS (1993) Oxyhemoglobin-induced cytotoxicity and arachidonic acid release in cultured bovine endothelial cells. Stroke 24: 839–845

    Article  CAS  PubMed  Google Scholar 

  108. Tammariello SP, Quinn MT, Estus S (2000) NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J Neurosci 20: RC53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Tang J, Liu J, Zhou C, Ostanin D, Grisham MB, Neil GD, Zhang JH (2005) Role of NADPH oxidase in the brain injury of intrace-rebral hemorrhage. J Neurochem 94: 1342–1350

    Article  CAS  PubMed  Google Scholar 

  110. Toborek M, Malecki A, Garrido R, Mattson MP, Hennig B, Young B (1999) Arachidonic acid-induced oxidative injury to cultured spinal cord neurons. J Neurochem 73: 684–692

    Article  CAS  PubMed  Google Scholar 

  111. Tran Dinh YR, Jomaa A, Callebert J, Reynier-Rebuffel AM, Tedgui A, Savarit A, Sercombe R (2001) Overexpression of cyclooxygenase-2 in rabbit basilar artery endothelial cells after subarachnoid hemorrhage. Neurosurgery 48: 626–633

    Article  CAS  PubMed  Google Scholar 

  112. Turner CP, Panter SS, Sharp FR (1999) Anti-oxidants prevent focal rat brain injury as assessed by induction of heat shock proteins (HSP70, HO-1/HSP32, HSP47) following subarachnoid injections of lysed blood. Brain Res Mol Brain Res 65: 87–102

    Article  CAS  PubMed  Google Scholar 

  113. Vigne P, Frelin C (1994) Endothelins activate phospholipase A2 in brain capillary endothelial cells. Brain Res 651: 342–344

    Article  CAS  PubMed  Google Scholar 

  114. Vollmer DG, Hongo K, Ogawa H, Tsukahara T, Kassell NF (1991) A study of the effectiveness of the iron-chelating agent deferoxamine as vasospasm prophylaxis in a rabbit model of subarachnoid hemorrhage. Neurosurgery 28: 27–32

    Article  CAS  PubMed  Google Scholar 

  115. Vollmer DG, Kassell NF, Hongo K, Ogawa H, Tsukahara T (1989) Effect of the nonglucocorticoid 21-aminosteroid U74006F experimental cerebral vasospasm. Surg Neurol 31: 190–194

    Article  CAS  PubMed  Google Scholar 

  116. Vollrath B, Chan P, Findlay M, Cook D (1995) Lazaroids and deferoxamine attenuate the intracellular effects of oxyhaemoglobin in vascular smooth muscle. Cardiovasc Res 30: 619–626

    Article  CAS  PubMed  Google Scholar 

  117. von Holst H, Sollevi A (1985) Increased concentration of hypoxanthine in human central cerebrospinal fluid after subarachnoid haemorrhage. Acta Neurochir (Wien) 77: 52–59

    Article  Google Scholar 

  118. Warner DS, Sheng H, Batinic-Haberle I (2004) Oxidants, antioxidants and the ischemic brain. J Exp Biol 207: 3221–3231

    Article  CAS  PubMed  Google Scholar 

  119. Watanabe T, Asano T, Shimizu T, Seyama Y, Takakura K (1988) Participation of lipoxygenase products from arachidonic acid in the pathogenesis of cerebral vasospasm. J Neurochem 50: 1145–1150

    Article  CAS  PubMed  Google Scholar 

  120. Watanabe T, Nishiyama M, Hori T, Asano T, Shimizu T, Masayasu H (1997) Ebselen (DR3305) ameliorates delayed cerebral vasospasm in a canine two-hemorrhage model. Neurol Res 19: 563–565

    Article  CAS  PubMed  Google Scholar 

  121. Widenka DC, Medele RJ, Stummer W, Bise K, Steiger HJ (1999) Inducible nitric oxide synthase: a possible key factor in the pathogenesis of chronic vasospasm after experimental subarachnoid hemorrhage. J Neurosurg 90: 1098–1104

    Article  CAS  PubMed  Google Scholar 

  122. Won SJ, Kim DY, Gwag BJ (2002) Cellular and molecular pathways of ischemic neuronal death. J Biochem Mol Biol 35: 67–86

    CAS  PubMed  Google Scholar 

  123. Yamamoto S, Teng W, Nishizawa S, Kakiuchi T, Tsukada H (2000) Improvement in cerebral blood flow and metabolism following subarachnoid hemorrhage in response to prophylactic administration of the hydroxyl radical scavenger, AVS, (+/-)-N,N′-propylenedinicotinamide: a positron emission tomography study in rats. J Neurosurg 92: 1009–1015

    Article  CAS  PubMed  Google Scholar 

  124. Yang MF, Sun BL, Xia ZL, Zhu LZ, Qiu PM, Zhang SM (2003) Alleviation of brain edema by L-arginine following experimental subarachnoid hemorrhage in a rat model. Clin Hemorheol Microcirc 29: 437–443

    CAS  PubMed  Google Scholar 

  125. 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. Journal of Neurotrauma 23: 1874

    Article  PubMed  Google Scholar 

  126. Zhang X, Dong F, Ren J, Driscoll MJ, Culver B (2005) High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp Neurol 191: 318–325

    Article  CAS  PubMed  Google Scholar 

  127. Zheng JS, Zhan RY, Zheng SS, Zhou YQ, Tong Y, Wan S (2005) Inhibition of NADPH oxidase attenuates vasospasm after experimental subarachnoid hemorrhage in rats. Stroke 36: 1059–1064

    Article  PubMed  CAS  Google Scholar 

  128. Zuccarello M, Anderson DK (1989) Protective effect of a 21-aminosteroid on the blood-brain barrier following subarachnoid hemorrhage in rats. Stroke 20: 367–371

    Article  CAS  PubMed  Google Scholar 

  129. Zuccarello M, Marsch JT, Schmitt G, Woodward J, Anderson DK (1989) Effect of the 21-aminosteroid U-74006F on cerebral vasospasm following subarachnoid hemorrhage. J Neurosurg 71: 98–104

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology and Pharmacology, Loma Linda University Medical Center, Loma Linda, CA, USA

    R. E. Ayer & J. H. Zhang

  2. Department of Neurosurgery, Loma Linda University Medical Center, 11234 Anderson Street, Room 2562B, Loma Linda, CA, USA

    J. H. Zhang

  3. Department of Anesthesiology, Loma Linda University Medical Center, Loma Linda, CA, USA

    J. H. Zhang

Authors
  1. R. E. Ayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. H. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. H. Zhang .

Editor information

Editors and Affiliations

  1. Department of Neurosurgery, Medical Faculty of Istanbul, University of Istanbul, Istanbul, Turkey

    Talat Kırış

  2. Department of Neurosurgery, Loma Linda University Medical Center, Loma Linda, USA

    John H. Zhang

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag

About this paper

Cite this paper

Ayer, R.E., Zhang, J.H. (2008). Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm. In: Kırış, T., Zhang, J.H. (eds) Cerebral Vasospasm. Acta Neurochirurgica Supplement, vol 104. Springer, Vienna. https://doi.org/10.1007/978-3-211-75718-5_7

Download citation

  • DOI: https://doi.org/10.1007/978-3-211-75718-5_7

  • Published:

  • Publisher Name: Springer, Vienna

  • Print ISBN: 978-3-211-75717-8

  • Online ISBN: 978-3-211-75718-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation