Animal Models of SAH and Their Translation to Clinical SAH

Chapter
Part of the Springer Series in Translational Stroke Research book series (SSTSR)

Abstract

Animal models of stroke may be useful for elucidating mechanisms of disease, but they have arguably not been particularly successful at predicting what treatments will be successful for ischemic stroke in humans. Animal models of subarachnoid hemorrhage also have been developed in rodents, dogs, and nonhuman primates. These models mimic angiographic vasospasm and some aspects of subarachnoid hemorrhage such as the transient global ischemia that sometimes occurs at the time of rupture of an aneurysm. Since the detailed acute and delayed pathologic effects of subarachnoid hemorrhage on human brain are not well delineated, how the animal models replicate this is unknown. Nevertheless, meta-analysis of the literature suggests that clinical trials of drugs for angiographic vasospasm in humans have been effective, and that some animal models accurately reflect what the effects of drugs are in humans. Analysis of animal models and comparison of drug effects on angiographic vasospasm in humans and animals suggest injection of autologous blood into the basal cisterns; assessment of vasospasm more than 3 days after the injection and intrathecal delivery of drugs may be better ways to study drugs in animals, in terms of translation to success in humans.

Keywords

Placebo Permeability Catheter Magnesium Ischemia 

References

  1. 1.
    Allen GS, Bahr AL. Cerebral arterial spasm: part 10. Reversal of acute and chronic spasm in dogs with orally administered nifedipine. Neurosurgery. 1979;4:43–7.PubMedGoogle Scholar
  2. 2.
    Altay T, Smithason S, Volokh N, et al. A novel method for subarachnoid hemorrhage to induce vasospasm in mice. J Neurosci Methods. 2009;183:136–40.PubMedGoogle Scholar
  3. 3.
    Barry KJ, Gogjian MA, Stein BM. Small animal model for investigation of subarachnoid hemorrhage and cerebral vasospasm. Stroke. 1979;10:538–41.PubMedGoogle Scholar
  4. 4.
    Brawley BW, Strandness DEJ, Kelly WA. The biphasic response of cerebral vasospasm in experimental subarachnoid hemorrhage. J Neurosurg. 1968;28:1–8.PubMedGoogle Scholar
  5. 5.
    Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2006;26:1341–53.PubMedGoogle Scholar
  6. 6.
    Clower BR, Smith RR, Haining JL, et al. Constrictive endarteropathy following experimental subarachnoid hemorrhage. Stroke. 1981;12:501–8.PubMedGoogle Scholar
  7. 7.
    Clower BR, Yamamoto Y, Cain L, et al. Endothelial injury following experimental subarachnoid hemorrhage in rats: effects on brain blood flow. Anat Rec. 1994;240:104–14.PubMedGoogle Scholar
  8. 8.
    Cosar M, Eser O, Fidan H, et al. The neuroprotective effect of dexmedetomidine in the hippocampus of rabbits after subarachnoid hemorrhage. Surg Neurol. 2009;71:54–9.PubMedGoogle Scholar
  9. 9.
    Delgado-Zygmunt T, Arbab MA, Shiokawa Y, et al. Cerebral blood flow and glucose metabolism in the squirrel monkey during the late phase of cerebral vasospasm. Acta Neurochir. 1993;121:166–73.Google Scholar
  10. 10.
    Delgado-Zygmunt TJ, Arbab MA, Shiokawa Y, et al. A primate model for acute and late cerebral vasospasm: angiographic findings. Acta Neurochir. 1992;118:130–6.Google Scholar
  11. 11.
    Dreier JP, Major S, Manning A, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain. 2009;132:1866–81.PubMedGoogle Scholar
  12. 12.
    Dreier JP, Windmuller O, Petzold G, et al. Ischemia triggered by red blood cell products in the subarachnoid space is inhibited by nimodipine administration or moderate volume expansion/hemodilution in rats. Neurosurgery. 2002;51:1457–65.PubMedGoogle Scholar
  13. 13.
    Eldevik OP, Kristiansen K, Torvik A. Subarachnoid hemorrhage and cerebrovascular spasm. Morphological study of intracranial arteries based on animal experiments and human autopsies. J Neurosurg. 1981;55:869–76.PubMedGoogle Scholar
  14. 14.
    Endo S, Branson PJ, Alksne JF. Experimental model of symptomatic vasospasm in rabbits. Stroke. 1988;19:1420–5.PubMedGoogle Scholar
  15. 15.
    Espinosa F, Weir B, Shnitka T, et al. A randomized placebo-controlled double-blind trial of nimodipine after SAH in monkeys. Part 2: pathological findings. J Neurosurg. 1984;60:1176–85.PubMedGoogle Scholar
  16. 16.
    Etminan N, Vergouwen MD, Ilodigwe D, et al. 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. 2011;31:1443–51.PubMedGoogle Scholar
  17. 17.
    Feiler S, Friedrich B, Scholler K, et al. Standardized induction of subarachnoid hemorrhage in mice by intracranial pressure monitoring. J Neurosci Methods. 2010;190:164–70.PubMedGoogle Scholar
  18. 18.
    Fein JM, Flor WJ, Cohan SL, et al. Sequential changes of vascular ultrastructure in experimental cerebral vasospasm. Myonecrosis of subarachnoid arteries. J Neurosurg. 1974;41:49–58.PubMedGoogle Scholar
  19. 19.
    Findlay JM, Weir BK, Kanamaru K, et al. Arterial wall changes in cerebral vasospasm. Neurosurgery. 1989;25:736–45.PubMedGoogle Scholar
  20. 20.
    Gao J, Wang H, Sheng H, et al. A novel apoE-derived therapeutic reduces vasospasm and improves outcome in a murine model of subarachnoid hemorrhage. Neurocrit Care. 2006;4:25–31.PubMedGoogle Scholar
  21. 21.
    Germano A, Costa C, DeFord SM, et al. Systemic administration of a calpain inhibitor reduces behavioral deficits and blood-brain barrier permeability changes after experimental subarachnoid hemorrhage in the rat. J Neurotrauma. 2002;19:887–96.PubMedGoogle Scholar
  22. 22.
    Grasso G, Buemi M, Alafaci C, et al. Beneficial effects of systemic administration of recombinant human erythropoietin in rabbits subjected to subarachnoid hemorrhage. Proc Natl Acad Sci USA. 2002;99:5627–31.PubMedGoogle Scholar
  23. 23.
    Gules I, Satoh M, Clower BR, et al. Comparison of three rat models of cerebral vasospasm. Am J Physiol Heart Circ Physiol. 2002;283:H2551–9.PubMedGoogle Scholar
  24. 24.
    Guresir E, Raabe A, Jaiimsin A, et al. Histological evidence of delayed ischemic brain tissue damage in the rat double-hemorrhage model. J Neurol Sci. 2010;293:18–22.PubMedGoogle Scholar
  25. 25.
    Hansen-Schwartz J, Hoel NL, Xu CB, et al. Subarachnoid hemorrhage-induced upregulation of the 5-HT1B receptor in cerebral arteries in rats. J Neurosurg. 2003;99:115–20.PubMedGoogle Scholar
  26. 26.
    Higgins J, Green S. Cochrane handbook for systematic reviews of interventions. In: The cochrane collaboration, 2008. Available at www.cochrane-handbook.org. Accessed Aug 8, 2011
  27. 27.
    Hop JW, Rinkel GJ, Algra A, et al. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28:660–4.PubMedGoogle Scholar
  28. 28.
    Ishiguro M, Puryear CB, Bisson E, et al. Enhanced myogenic tone in cerebral arteries from a rabbit model of subarachnoid hemorrhage. Am J Physiol Heart Circ Physiol. 2002;283:H2217–25.PubMedGoogle Scholar
  29. 29.
    Ishikawa M, Kusaka G, Yamaguchi N, et al. Platelet and leukocyte adhesion in the microvasculature at the cerebral surface immediately after subarachnoid hemorrhage. Neurosurgery. 2009;64:546–53.PubMedGoogle Scholar
  30. 30.
    Jackowski A, Crockard A, Burnstock G, et al. The time course of intracranial pathophysiological changes following experimental subarachnoid haemorrhage in the rat. J Cereb Blood Flow Metab. 1990;10:835–49.PubMedGoogle Scholar
  31. 31.
    Jadhav V, Sugawara T, Zhang J, et al. Magnetic resonance imaging detects and predicts early brain injury after subarachnoid hemorrhage in a canine experimental model. J Neurotrauma. 2008;25:1099–106.PubMedGoogle Scholar
  32. 32.
    Jeon H, Ai J, Sabri M, et al. Learning deficits after experimental subarachnoid hemorrhage in rats. Neuroscience. 2010;169:1805–14.PubMedGoogle Scholar
  33. 33.
    Jeon H, Ai J, Sabri M, et al. Neurological and neurobehavioral assessment of experimental subarachnoid hemorrhage. BMC Neurosci. 2009;10:103.PubMedGoogle Scholar
  34. 34.
    Josko J, Gwozdz B, Hendryk S, et al. Expression of vascular endothelial growth factor (VEGF) in rat brain after subarachnoid haemorrhage and endothelin receptor blockage with BQ-123. Folia Neuropathol. 2001;39:243–51.PubMedGoogle Scholar
  35. 35.
    Kamii H, Kato I, Kinouchi H, et al. Amelioration of vasospasm after subarachnoid hemorrhage in transgenic mice overexpressing CuZn-superoxide dismutase. Stroke. 1999;30:867–71.PubMedGoogle Scholar
  36. 36.
    Kanamaru K, Weir BK, Findlay JM, et al. Pharmacological studies on relaxation of spastic primate cerebral arteries in subarachnoid hemorrhage. J Neurosurg. 1989;71:909–15.PubMedGoogle Scholar
  37. 37.
    Kaoutzanis M, Yokota M, Sibilia R, et al. Neurologic evaluation in a canine model of single and double subarachnoid hemorrhage. J Neurosci Methods. 1993;50:301–7.PubMedGoogle Scholar
  38. 38.
    Kistler JP, Lees RS, Candia G, et al. Intravenous nitroglycerin in experimental cerebral vasospasm. A preliminary report. Stroke. 1979;10:26–9.PubMedGoogle Scholar
  39. 39.
    Kuwayama A, Zervas NT, Belson R, et al. A model for experimental cerebral arterial spasm. Stroke. 1972;3:49–56.PubMedGoogle Scholar
  40. 40.
    Laslo AM, Eastwood JD, Pakkiri P, et al. CT perfusion-derived mean transit time predicts early mortality and delayed vasospasm after experimental subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2008;29:79–85.PubMedGoogle Scholar
  41. 41.
    Lee JY, Huang DL, Keep R, et al. Characterization of an improved double hemorrhage rat model for the study of delayed cerebral vasospasm. J Neurosci Methods. 2008;168:358–66.PubMedGoogle Scholar
  42. 42.
    Lin CL, Calisaneller T, Ukita N, et al. A murine model of subarachnoid hemorrhage-induced cerebral vasospasm. J Neurosci Methods. 2003;123:89–97.PubMedGoogle Scholar
  43. 43.
    Liszczak TM, Varsos VG, Black PM, et al. Cerebral arterial constriction after experimental subarachnoid hemorrhage is associated with blood components within the arterial wall. J Neurosurg. 1983;58:18–26.PubMedGoogle Scholar
  44. 44.
    Lougheed WM, Tom M. A method of introducing blood into the subarachnoid space in the region of the circle of Willis in dogs. Can J Surg. 1961;4:329–37.PubMedGoogle Scholar
  45. 45.
    Macdonald RL, Weir B. Cerebral vasospasm. San Diego: Academic; 2001.Google Scholar
  46. 46.
    Marbacher S, Fandino J, Kitchen ND. Standard intracranial in vivo animal models of delayed cerebral vasospasm. Br J Neurosurg. 2010;24:415–34.PubMedGoogle Scholar
  47. 47.
    Marshman LA, Morice AH, Thompson JS. Increased efficacy of sodium nitroprusside in middle cerebral arteries following acute subarachnoid hemorrhage: indications for its use after rupture. J Neurosurg Anesthesiol. 1998;10:171–7.PubMedGoogle Scholar
  48. 48.
    Mayberg MR, Okada T, Bark DH. Morphologic changes in cerebral arteries after subarachnoid hemorrhage. Neurosurg Clin N Am. 1990;1:417–32.PubMedGoogle Scholar
  49. 49.
    McQueen JD, Jeanes LD. Influence of hypothermia on intracranial hypertension. J Neurosurg. 1962;19:277–88.Google Scholar
  50. 50.
    Meguro T, Chen B, Lancon J, et al. Oxyhemoglobin induces caspase-mediated cell death in cerebral endothelial cells. J Neurochem. 2001;77:1128–35.PubMedGoogle Scholar
  51. 51.
    Megyesi JF, Findlay JM, Vollrath B, et al. In vivo angioplasty prevents the development of vasospasm in canine carotid arteries. Pharmacological and morphological analyses. Stroke. 1997;28:1216–24.PubMedGoogle Scholar
  52. 52.
    Mignini LE, Khan KS. Methodological quality of systematic reviews of animal studies: a survey of reviews of basic research. BMC Med Res Methodol. 2006;6:10.PubMedGoogle Scholar
  53. 53.
    Miyamoto Y, Matsuda M. Cerebral blood flow and somatosensory evoked potentials in dogs with experimental vasospasm caused by double injection. Archiv Jpn Chirgurie. 1991;60:289–98.Google Scholar
  54. 54.
    Murakami K, Koide M, Dumont TM, et al. Subarachnoid hemorrhage induces gliosis and increased expression of the pro-inflammatory cytokine high mobility group box 1 protein. Transl Stroke Res. 2011;2:72–9.PubMedGoogle Scholar
  55. 55.
    Nagasawa S, Handa H, Naruo Y, et al. Experimental cerebral vasospasm arterial wall mechanics and connective tissue composition. Stroke. 1982;13:595–600.PubMedGoogle Scholar
  56. 56.
    Nakagomi T, Kassell NF, Sasaki T, et al. Impairment of endothelium-dependent vasodilation induced by acetylcholine and adenosine triphosphate following experimental subarachnoid hemorrhage. Stroke. 1987;18:482–9.PubMedGoogle Scholar
  57. 57.
    Nozaki K, Okamoto S, Uemura Y, et al. Changes of glycogen and ATP contents of the major cerebral arteries after experimentally produced subarachnoid haemorrhage in the dog. Acta Neurochir. 1990;104:38–41.Google Scholar
  58. 58.
    Nuki Y, Tsou TL, Kurihara C, et al. Elastase-induced intracranial aneurysms in hypertensive mice. Hypertension. 2009;54:1337–44.PubMedGoogle Scholar
  59. 59.
    Ohkuma H, Suzuki S, Ogane K. Phenotypic modulation of smooth muscle cells and vascular remodeling in intraparenchymal small cerebral arteries after canine experimental subarachnoid hemorrhage. Neurosci Lett. 2003;344:193–6.PubMedGoogle Scholar
  60. 60.
    Okada T, Harada T, Bark DH, et al. A rat femoral artery model for vasospasm. Neurosurgery. 1990;27:349–56.PubMedGoogle Scholar
  61. 61.
    Park IS, Meno JR, Witt CE, et al. Subarachnoid hemorrhage model in the rat: modification of the endovascular filament model. J Neurosci Methods. 2008;172:195–200.PubMedGoogle Scholar
  62. 62.
    Park S, Yamaguchi M, Zhou C, et al. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke. 2004;35:2412–7.PubMedGoogle Scholar
  63. 63.
    Parra A, McGirt MJ, Sheng H, et al. Mouse model of subarachnoid hemorrhage associated cerebral vasospasm: methodological analysis. Neurol Res. 2002;24:510–6.PubMedGoogle Scholar
  64. 64.
    Perkins E, Kimura H, Parent AD, et al. Evaluation of the microvasculature and cerebral ischemia after experimental subarachnoid hemorrhage in dogs. J Neurosurg. 2002;97:896–904.PubMedGoogle Scholar
  65. 65.
    Pluta RM, Hansen-Schwartz J, Dreier J, et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res. 2009;31:151–8.PubMedGoogle Scholar
  66. 66.
    Prunell GF, Mathiesen T, Diemer NH, et al. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery. 2003;52:165–75.PubMedGoogle Scholar
  67. 67.
    Prunell GF, Mathiesen T, Svendgaard NA. A new experimental model in rats for study of the pathophysiology of subarachnoid hemorrhage. Neuroreport. 2002;13:2553–6.PubMedGoogle Scholar
  68. 68.
    Prunell GF, Mathiesen T, Svendgaard NA. Experimental subarachnoid hemorrhage: cerebral blood flow and brain metabolism during the acute phase in three different models in the rat. Neurosurgery. 2004;54:426–36.PubMedGoogle Scholar
  69. 69.
    Prunell GF, Svendgaard NA, Alkass K, et al. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg. 2005;102:1046–54.PubMedGoogle Scholar
  70. 70.
    Rosengart AJ, Schultheiss KE, Tolentino J, et al. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007;38:2315–21.PubMedGoogle Scholar
  71. 71.
    Ryba MS, Gordon-Krajcer W, Walski M, et al. Hydroxylamine attenuates the effects of simulated subarachnoid hemorrhage in the rat brain and improves neurological outcome. Brain Res. 1999;850:225–33.PubMedGoogle Scholar
  72. 72.
    Sabri M, Ai J, Macdonald RL. Dissociation of vasospasm and secondary effects of experimental subarachnoid hemorrhage by clazosentan. Stroke. 2011;42:1454–60.PubMedGoogle Scholar
  73. 73.
    Sabri M, Ai J, Marsden PA, et al. Simvastatin re-couples dysfunctional endothelial nitric oxide synthase in experimental subarachnoid hemorrhage. PLoS One. 2011;6:e17062.PubMedGoogle Scholar
  74. 74.
    Sabri M, Jeon H, Ai J, et al. Anterior circulation mouse model of subarachnoid hemorrhage. Brain Res. 2009;1295:179–85.PubMedGoogle Scholar
  75. 75.
    Sabri M, Kawashima A, Ai J, et al. Neuronal and astrocytic apoptosis after subarachnoid hemorrhage: a possible cause for poor prognosis. Brain Res. 2008;1238:163–71.PubMedGoogle Scholar
  76. 76.
    Sahlin C, Owman C, Chang JY, et al. Changes in contractile response and effect of a calcium antagonist, nimodipine, in isolated intracranial arteries of baboon following experimental subarachnoid hemorrhage. Brain Res Bull. 1990;24:355–61.PubMedGoogle Scholar
  77. 77.
    Sasaki T, Murota SI, Wakai S, et al. Evaluation of prostaglandin biosynthetic activity in canine basilar artery following subarachnoid injection of blood. J Neurosurg. 1981;55:771–8.PubMedGoogle Scholar
  78. 78.
    Sasaki T, Wakai S, Asano T, et al. Prevention of cerebral vasospasm after SAH with a thromboxane synthetase inhibitor, OKY-1581. J Neurosurg. 1982;57:74–82.PubMedGoogle Scholar
  79. 79.
    Schatlo B, Dreier JP, Glasker S, et al. Report of selective cortical infarcts in the primate clot model of vasospasm after subarachnoid hemorrhage. Neurosurgery. 2010;67:721–8.PubMedGoogle Scholar
  80. 80.
    Schwartz AY, Masago A, Sehba FA, et al. Experimental models of subarachnoid hemorrhage in the rat: a refinement of the endovascular filament model. J Neurosci Methods. 2000;96:161–7.PubMedGoogle Scholar
  81. 81.
    Seckin H, Simsek S, Ozturk E, et al. Topiramate attenuates hippocampal injury after experimental subarachnoid hemorrhage in rabbits. Neurol Res. 2009;31:490–5.PubMedGoogle Scholar
  82. 82.
    Sehba FA, Flores R, Muller A, et al. Adenosine A(2A) receptors in early ischemic vascular injury after subarachnoid hemorrhage. Laboratory investigation. J Neurosurg. 2010;113:826–34.PubMedGoogle Scholar
  83. 83.
    Shiokawa K, Kasuya H, Miyajima M, et al. Prophylactic effect of papaverine prolonged-release pellets on cerebral vasospasm in dogs. Neurosurgery. 1998;42:109–15.PubMedGoogle Scholar
  84. 84.
    Silasi G, Colbourne F. Long-term assessment of motor and cognitive behaviours in the intraluminal perforation model of subarachnoid hemorrhage in rats. Behav Brain Res. 2009;198:380–7.PubMedGoogle Scholar
  85. 85.
    Simeone FA, Ryan KG, Cotter JR. Prolonged experimental cerebral vasospasm. J Neurosurg. 1968;29:357–66.PubMedGoogle Scholar
  86. 86.
    Solomon RA, Antunes JL, Chen RYZ, et al. Decrease in cerebral blood flow in rats after experimental subarachnoid hemorrhage: a new animal model. Stroke. 1985;16:58–64.PubMedGoogle Scholar
  87. 87.
    Sozen T, Tsuchiyama R, Hasegawa Y, et al. Role of interleukin-1beta in early brain injury after subarachnoid hemorrhage in mice. Stroke. 2009;40:2519–25.PubMedGoogle Scholar
  88. 88.
    Stein SC, Browne KD, Chen XH, et al. Thromboembolism and delayed cerebral ischemia after subarachnoid hemorrhage: an autopsy study. Neurosurgery. 2006;59:781–7.PubMedGoogle Scholar
  89. 89.
    Sugawara T, Ayer R, Jadhav V, et al. Simvastatin attenuation of cerebral vasospasm after subarachnoid hemorrhage in rats via increased phosphorylation of Akt and endothelial nitric oxide synthase. J Neurosci Res. 2008;86:3635–43.PubMedGoogle Scholar
  90. 90.
    Sugawara T, Ayer R, Jadhav V, et al. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods. 2008;167:327–34.PubMedGoogle Scholar
  91. 91.
    Svendgaard NA, Brismar J, Delgado T, et al. Late cerebral arterial spasm: the cerebrovascular response to hypercapnia, induced hypertension and the effect of nimodipine on blood flow autoregulation in experimental subarachnoid hemorrhage in primates. Gen Pharmacol. 1983;14:167–72.PubMedGoogle Scholar
  92. 92.
    Takata K, Sheng H, Borel CO, et al. Long-term cognitive dysfunction following experimental subarachnoid hemorrhage: new perspectives. Exp Neurol. 2008;213:336–44.PubMedGoogle Scholar
  93. 93.
    The Stroke Therapy Academic Industry Round Table (STAIR). Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke. 1999;30:2752–8.Google Scholar
  94. 94.
    Titova E, Ostrowski RP, Zhang JH, et al. Experimental models of subarachnoid hemorrhage for studies of cerebral vasospasm. Neurol Res. 2009;31(6):568–81.PubMedGoogle Scholar
  95. 95.
    van den Bergh WM, Schepers J, Veldhuis WB, et al. Magnetic resonance imaging in experimental subarachnoid haemorrhage. Acta Neurochir (Wien). 2005;147:977–83.Google Scholar
  96. 96.
    van der Worp HB, Howells DW, Sena ES, et al. Can animal models of disease reliably inform human studies? PLoS Med. 2010;7:e1000245.PubMedGoogle Scholar
  97. 97.
    Vatter H, Konczalla J, Weidauer S, et al. Characterization of the endothelin-B receptor expression and vasomotor function during experimental cerebral vasospasm. Neurosurgery. 2007;60:1100–8.PubMedGoogle Scholar
  98. 98.
    Vatter H, Weidauer S, Konczalla J, et al. Time course in the development of cerebral vasospasm after experimental subarachnoid hemorrhage: clinical and neuroradiological assessment of the rat double hemorrhage model. Neurosurgery. 2006;58:1190–7.PubMedGoogle Scholar
  99. 99.
    Veelken JA, Laing RJ, Jakubowski J. The Sheffield model of subarachnoid hemorrhage in rats. Stroke. 1995;26:1279–83.PubMedGoogle Scholar
  100. 100.
    Vergouwen MD, Vermeulen M, Coert BA, et al. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab. 2008;28:1761–70.PubMedGoogle Scholar
  101. 101.
    Vikman P, Beg S, Khurana T, et al. Gene expression and molecular changes in cerebral arteries following subarachnoid hemorrhage in the rat. J Neurosurg. 2006;105:438–44.PubMedGoogle Scholar
  102. 102.
    Vorkapic P, Bevan RD, Bevan JA. Longitudinal time course of reversible and irreversible components of chronic cerebrovasospasm of the rabbit basilar artery. J Neurosurg. 1991;74:951–5.PubMedGoogle Scholar
  103. 103.
    Wakade C, King MD, Laird MD, et al. Curcumin attenuates vascular inflammation and cerebral vasospasm after subarachnoid hemorrhage in mice. Antioxid Redox Signal. 2009;11:35–45.PubMedGoogle Scholar
  104. 104.
    Weir B, Erasmo R, Miller J, et al. Vasospasm in response to repeated subarachnoid hemorrhages in the monkey. J Neurosurg. 1970;33:395–406.PubMedGoogle Scholar
  105. 105.
    Wilkins RH, Levitt P. Intracranial arterial spasm in the dog. A chronic experimental model. J Neurosurg. 1970;33:260–9.PubMedGoogle Scholar
  106. 106.
    Yamamoto S, Teng W, Kakiuchi T, et al. Disturbance of cerebral blood flow autoregulation in hypertension is attributable to ischaemia following subarachnoid haemorrhage in rats: a PET study. Acta Neurochir. 1999;141:1213–9.Google Scholar
  107. 107.
    Yatsushige H, Yamaguchi M, Zhou C, et al. Role of c-Jun N-terminal kinase in cerebral vasospasm after experimental subarachnoid hemorrhage. Stroke. 2005;36:1538–43.PubMedGoogle Scholar
  108. 108.
    Zhou C, Yamaguchi M, Kusaka G, et al. Caspase inhibitors prevent endothelial apoptosis and cerebral vasospasm in dog model of experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004;24:419–31.PubMedGoogle Scholar
  109. 109.
    Zhou ML, Shi JX, Zhu JQ, et al. Comparison between one- and two-hemorrhage models of cerebral vasospasm in rabbits. J Neurosci Methods. 2007;159:318–24.PubMedGoogle Scholar
  110. 110.
    Zoerle T, Ilodigwe D, Wan H, et al. Pharmacologic prevention of cerebral vasospasm in experimental subarachnoid hemorrhage: systematic review and meta-analysis. Submitted 2011.Google Scholar
  111. 111.
    Zubkov AY, Aoki K, Parent AD, et al. Preliminary study of the effects of caspase inhibitors on vasospasm in dog penetrating arteries. Life Sci. 2002;70:3007–18.PubMedGoogle Scholar
  112. 112.
    Zuccarello M, Boccaletti R, Tosun M, et al. Role of extracellular Ca2+ in subarachnoid hemorrhage-induced spasm of the rabbit basilar artery. Stroke. 1996;27:1896–902.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Anesthesia and Critical Care MedicineUniversity of Milano, Neurosurgical Intensive Care Unit, Fondazione IRCCS Ca’ Granda–Ospedale Maggiore, PoliclinicoMilanItaly
  2. 2.Division of Neurosurgery, Labatt Family Centre of Excellence in Brain Injury and Trauma ResearchKeenan Research Centre of the Li Ka Shing Knowledge Institute of St. Michael’s HospitalTorontoCanada
  3. 3.Department of SurgeryUniversity of TorontoTorontoCanada

Personalised recommendations