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Erschienen in: Acta Neurochirurgica 1/2012

01.01.2012 | Experimental Research

The effect of common carotid artery occlusion on delayed brain tissue damage in the rat double subarachnoid hemorrhage model

verfasst von: Erdem Güresir, Nikos Vasiliadis, Santosh Dias, Peter Raab, Volker Seifert, Hartmut Vatter

Erschienen in: Acta Neurochirurgica | Ausgabe 1/2012

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Abstract

Objective

Delayed ischemic brain tissue damage in the time course of cerebral vasospasm in the rat double-subarachnoid hemorrhage (SAH) model has been described before. However, in order to enhance hemodynamic insufficiency during cerebral vasospasm (CVS), we performed—in a modification to the standard double-hemorrhage model—an additional unilateral common carotid artery occlusion (CCAO), expecting aggravation of brain-tissue damage in areas particularly sensitive to hypoxia.

Methods

CVS was induced by injection of 0.25 ml autologous blood twice in the cisterna magna of Sprague-Dawley rats with and without unilateral CCAO. The animals were examined on days 2, 3, 4 and 5, and compared with the sham-operated control group without SAH. The functional deficits were graded between 0 and 3. Perfusion weighted imaging (PWI) at 3 Tesla magnetic resonance (MR) tomography was performed to assess cerebral blood flow (CBF). The brains were fixed, stained and evaluated for histological changes.

Results

On day 5, the neurological state was significantly worse in rats with SAH. The relative CBF/muscle blood ratio was significantly decreased by SAH and lowest in rats with CCAO and SAH (4.5 ± 1.1 vs 2.7 ± 0.6) compared with sham (7.9 ± 1.5; p < 0.001). Basilar artery (BA) diameter was 79 ± 5 μm (SAH) vs 147 ± 4 μm (sham, p < 0.001). Neuronal cell count in the hippocampal areas CA1-CA4 was significantly reduced by SAH on day 5 (p < 0.001) and lowest in rats with SAH and CCAO.

Conclusions

CCAO leads to an aggravation of CVS-related delayed brain tissue damage in the modified rat double-SAH model.
Literatur
1.
Zurück zum Zitat Bederson JB, Germano IM, Guarino L (1995) Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 26:1086–1091PubMedCrossRef Bederson JB, Germano IM, Guarino L (1995) Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 26:1086–1091PubMedCrossRef
2.
Zurück zum Zitat Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL III, Vallabhajosyula P (1998) Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 42:352–360PubMedCrossRef Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL III, Vallabhajosyula P (1998) Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 42:352–360PubMedCrossRef
3.
Zurück zum Zitat Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H (1986) Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17:472–476PubMedCrossRef Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H (1986) Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17:472–476PubMedCrossRef
4.
Zurück zum Zitat Cahill J, Calvert JW, Solaroglu I, Zhang JH (2006) Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 37:1868–1874PubMedCrossRef Cahill J, Calvert JW, Solaroglu I, Zhang JH (2006) Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 37:1868–1874PubMedCrossRef
5.
Zurück zum Zitat Cambj-Sapunar L, Yu M, Harder DR, Roman RJ (2003) Contribution of 5-hydroxytryptamine1B receptors and 20-hydroxyeiscosatetraenoic acid to fall in cerebral blood flow after subarachnoid hemorrhage. Stroke 34:1269–1275PubMedCrossRef Cambj-Sapunar L, Yu M, Harder DR, Roman RJ (2003) Contribution of 5-hydroxytryptamine1B receptors and 20-hydroxyeiscosatetraenoic acid to fall in cerebral blood flow after subarachnoid hemorrhage. Stroke 34:1269–1275PubMedCrossRef
6.
Zurück zum Zitat de Ley G, Nshimyumuremyi JB, Leusen I (1985) Hemispheric blood flow in the rat after unilateral common carotid occlusion: evolution with time. Stroke 16:69–73PubMedCrossRef de Ley G, Nshimyumuremyi JB, Leusen I (1985) Hemispheric blood flow in the rat after unilateral common carotid occlusion: evolution with time. Stroke 16:69–73PubMedCrossRef
7.
Zurück zum Zitat Dittmar MS, Fehm NP, Vatankhah B, Horn M (2004) Ketamine/xylazine anesthesia for radiologic imaging of neurologically impaired rats: dose response, respiratory depression, and management of complications. Comp Med 54:652–655PubMed Dittmar MS, Fehm NP, Vatankhah B, Horn M (2004) Ketamine/xylazine anesthesia for radiologic imaging of neurologically impaired rats: dose response, respiratory depression, and management of complications. Comp Med 54:652–655PubMed
8.
Zurück zum Zitat Findlay JM, Deagle GM (1998) Causes of morbidity and mortality following intracranial aneurysm rupture. Can J Neurol Sci 25:209–215PubMed Findlay JM, Deagle GM (1998) Causes of morbidity and mortality following intracranial aneurysm rupture. Can J Neurol Sci 25:209–215PubMed
9.
Zurück zum Zitat Fujii K, Heistad DD, Faraci FM (1991) Flow-mediated dilatation of the basilar artery in vivo. Circ Res 69:697–705PubMed Fujii K, Heistad DD, Faraci FM (1991) Flow-mediated dilatation of the basilar artery in vivo. Circ Res 69:697–705PubMed
10.
Zurück zum Zitat Granstam E, Granstam SO (2003) Involvement of nitric oxide in the regulation of regional hemodynamics in streptozotocin-diabetic rats. Physiol Res 52:159–169PubMed Granstam E, Granstam SO (2003) Involvement of nitric oxide in the regulation of regional hemodynamics in streptozotocin-diabetic rats. Physiol Res 52:159–169PubMed
11.
Zurück zum Zitat Gules I, Satoh M, Clower BR, Nanda A, Zhang JH (2002) Comparison of three rat models of cerebral vasospasm. Am J Physiol Heart Circ Physiol 283:H2551–H2559PubMed Gules I, Satoh M, Clower BR, Nanda A, Zhang JH (2002) Comparison of three rat models of cerebral vasospasm. Am J Physiol Heart Circ Physiol 283:H2551–H2559PubMed
12.
Zurück zum Zitat Güresir E, Raabe A, Jaiimsin A, Dias S, Raab P, Seifert V, Vatter H (2010) Histological evidence of delayed ischemic brain tissue damage in the rat double-hemorrhage model. J Neurol Sci 293:18–22PubMedCrossRef Güresir E, Raabe A, Jaiimsin A, Dias S, Raab P, Seifert V, Vatter H (2010) Histological evidence of delayed ischemic brain tissue damage in the rat double-hemorrhage model. J Neurol Sci 293:18–22PubMedCrossRef
13.
Zurück zum Zitat Heros RC, Zervas NT, Varsos V (1983) Cerebral vasospasm after subarachnoid hemorrhage: an update. Ann Neurol 14:599–608PubMedCrossRef Heros RC, Zervas NT, Varsos V (1983) Cerebral vasospasm after subarachnoid hemorrhage: an update. Ann Neurol 14:599–608PubMedCrossRef
14.
Zurück zum Zitat Hop JW, Rinkel GJ, Algra A, van Gijn J (1997) Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 28:660–664PubMedCrossRef Hop JW, Rinkel GJ, Algra A, van Gijn J (1997) Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 28:660–664PubMedCrossRef
15.
Zurück zum Zitat Hossmann KA (1998) Experimental models for the investigation of brain ischemia. Cardiovasc Res 39:106–120PubMedCrossRef Hossmann KA (1998) Experimental models for the investigation of brain ischemia. Cardiovasc Res 39:106–120PubMedCrossRef
16.
Zurück zum Zitat Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL (1990) The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg 73:18–36PubMedCrossRef Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL (1990) The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg 73:18–36PubMedCrossRef
17.
Zurück zum Zitat 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 33:2687–2691PubMedCrossRef 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 33:2687–2691PubMedCrossRef
18.
Zurück zum Zitat Larsson E, Lindvall O, Kokaia Z (2001) Stereological assessment of vulnerability of immunocytochemically identified striatal and hippocampal neurons after global cerebral ischemia in rats. Brain Res 913:117–132PubMedCrossRef Larsson E, Lindvall O, Kokaia Z (2001) Stereological assessment of vulnerability of immunocytochemically identified striatal and hippocampal neurons after global cerebral ischemia in rats. Brain Res 913:117–132PubMedCrossRef
19.
Zurück zum Zitat Lee JY, Huang DL, Keep R, Sagher O (2008) Characterization of an improved double hemorrhage rat model for the study of delayed cerebral vasospasm. J Neurosci Methods 168:358–366PubMedCrossRef Lee JY, Huang DL, Keep R, Sagher O (2008) Characterization of an improved double hemorrhage rat model for the study of delayed cerebral vasospasm. J Neurosci Methods 168:358–366PubMedCrossRef
20.
Zurück zum Zitat Lei H, Grinberg O, Nwaigwe CI, Hou HG, Williams H, Swartz HM, Dunn JF (2001) The effects of ketamine-xylazine anesthesia on cerebral blood flow and oxygenation observed using nuclear magnetic resonance perfusion imaging and electron paramagnetic resonance oximetry. Brain Res 913:174–179PubMedCrossRef Lei H, Grinberg O, Nwaigwe CI, Hou HG, Williams H, Swartz HM, Dunn JF (2001) The effects of ketamine-xylazine anesthesia on cerebral blood flow and oxygenation observed using nuclear magnetic resonance perfusion imaging and electron paramagnetic resonance oximetry. Brain Res 913:174–179PubMedCrossRef
21.
Zurück zum Zitat Leifer D, Kowall NW (1993) Immunohistochemical patterns of selective cellular vulnerability in human cerebral ischemia. J Neurol Sci 119:217–228PubMedCrossRef Leifer D, Kowall NW (1993) Immunohistochemical patterns of selective cellular vulnerability in human cerebral ischemia. J Neurol Sci 119:217–228PubMedCrossRef
22.
Zurück zum Zitat Li F, Liu KF, Silva MD, Omae T, Sotak CH, Fenstermacher JD, Fisher M, Hsu CY, Lin W (2000) Transient and permanent resolution of ischemic lesions on diffusion-weighted imaging after brief periods of focal ischemia in rats: correlation with histopathology. Stroke 31:946–954PubMedCrossRef Li F, Liu KF, Silva MD, Omae T, Sotak CH, Fenstermacher JD, Fisher M, Hsu CY, Lin W (2000) Transient and permanent resolution of ischemic lesions on diffusion-weighted imaging after brief periods of focal ischemia in rats: correlation with histopathology. Stroke 31:946–954PubMedCrossRef
23.
Zurück zum Zitat Liu Y, Karonen JO, Vanninen RL, Ostergaard L, Roivainen R, Nuutinen J, Perkio J, Kononen M, Hamalainen A, Vanninen EJ, Soimakallio S, Kuikka JT, Aronen HJ (2000) Cerebral hemodynamics in human acute ischemic stroke: a study with diffusion- and perfusion-weighted magnetic resonance imaging and SPECT. J Cereb Blood Flow Metab 20:910–920PubMedCrossRef Liu Y, Karonen JO, Vanninen RL, Ostergaard L, Roivainen R, Nuutinen J, Perkio J, Kononen M, Hamalainen A, Vanninen EJ, Soimakallio S, Kuikka JT, Aronen HJ (2000) Cerebral hemodynamics in human acute ischemic stroke: a study with diffusion- and perfusion-weighted magnetic resonance imaging and SPECT. J Cereb Blood Flow Metab 20:910–920PubMedCrossRef
24.
Zurück zum Zitat Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, Frey A, Roux S, Pasqualin A (2008) Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 39:3015–3021PubMedCrossRef Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, Frey A, Roux S, Pasqualin A (2008) Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 39:3015–3021PubMedCrossRef
25.
Zurück zum Zitat Meguro T, Clower BR, Carpenter R, Parent AD, Zhang JH (2001) Improved rat model for cerebral vasospasm studies. Neurol Res 23:761–766PubMedCrossRef Meguro T, Clower BR, Carpenter R, Parent AD, Zhang JH (2001) Improved rat model for cerebral vasospasm studies. Neurol Res 23:761–766PubMedCrossRef
26.
Zurück zum Zitat Miyagi Y, Carpenter RC, Meguro T, Parent AD, Zhang JH (2000) Upregulation of rho A and rho kinase messenger RNAs in the basilar artery of a rat model of subarachnoid hemorrhage. J Neurosurg 93:471–476PubMedCrossRef Miyagi Y, Carpenter RC, Meguro T, Parent AD, Zhang JH (2000) Upregulation of rho A and rho kinase messenger RNAs in the basilar artery of a rat model of subarachnoid hemorrhage. J Neurosurg 93:471–476PubMedCrossRef
27.
Zurück zum Zitat Nau R, Haase S, Bunkowski S, Bruck W (2002) Neuronal apoptosis in the dentate gyrus in humans with subarachnoid hemorrhage and cerebral hypoxia. Brain Pathol 12:329–336PubMed Nau R, Haase S, Bunkowski S, Bruck W (2002) Neuronal apoptosis in the dentate gyrus in humans with subarachnoid hemorrhage and cerebral hypoxia. Brain Pathol 12:329–336PubMed
28.
Zurück zum Zitat Ostergaard L, Sorensen AG, Kwong KK, Weisskoff RM, Gyldensted C, Rosen BR (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part II: Experimental comparison and preliminary results. Magn Reson Med 36:726–736PubMedCrossRef Ostergaard L, Sorensen AG, Kwong KK, Weisskoff RM, Gyldensted C, Rosen BR (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part II: Experimental comparison and preliminary results. Magn Reson Med 36:726–736PubMedCrossRef
29.
Zurück zum Zitat Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn Reson Med 36:715–725PubMedCrossRef Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn Reson Med 36:715–725PubMedCrossRef
30.
Zurück zum Zitat Ostrowski RP, Colohan AR, Zhang JH (2005) Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J Cereb Blood Flow Metab 25:554–571PubMedCrossRef Ostrowski RP, Colohan AR, Zhang JH (2005) Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J Cereb Blood Flow Metab 25:554–571PubMedCrossRef
31.
Zurück zum Zitat Palmer GM, Cairns BE, Berkes SL, Dunning PS, Taylor GA, Berde CB (2002) The effects of lidocaine and adrenergic agonists on rat sciatic nerve and skeletal muscle blood flow in vivo. Anesth Analg 95:1080–6, tablePubMed Palmer GM, Cairns BE, Berkes SL, Dunning PS, Taylor GA, Berde CB (2002) The effects of lidocaine and adrenergic agonists on rat sciatic nerve and skeletal muscle blood flow in vivo. Anesth Analg 95:1080–6, tablePubMed
32.
Zurück zum Zitat Prunell GF, Mathiesen T, Svendgaard NA (2004) Experimental subarachnoid hemorrhage: cerebral blood flow and brain metabolism during the acute phase in three different models in the rat. Neurosurgery 54:426–436PubMedCrossRef Prunell GF, Mathiesen T, Svendgaard NA (2004) Experimental subarachnoid hemorrhage: cerebral blood flow and brain metabolism during the acute phase in three different models in the rat. Neurosurgery 54:426–436PubMedCrossRef
33.
Zurück zum Zitat Rabinstein AA, Pichelmann MA, Friedman JA, Piepgras DG, Nichols DA, McIver JI, Toussaint LG III, McClelland RL, Fulgham JR, Meyer FB, Atkinson JL, Wijdicks EF (2003) Symptomatic vasospasm and outcomes following aneurysmal subarachnoid hemorrhage: a comparison between surgical repair and endovascular coil occlusion. J Neurosurg 98:319–325PubMedCrossRef Rabinstein AA, Pichelmann MA, Friedman JA, Piepgras DG, Nichols DA, McIver JI, Toussaint LG III, McClelland RL, Fulgham JR, Meyer FB, Atkinson JL, Wijdicks EF (2003) Symptomatic vasospasm and outcomes following aneurysmal subarachnoid hemorrhage: a comparison between surgical repair and endovascular coil occlusion. J Neurosurg 98:319–325PubMedCrossRef
34.
Zurück zum Zitat Rousselle CH, Lefauconnier JM, Allen DD (1998) Evaluation of anesthetic effects on parameters for the in situ rat brain perfusion technique. Neurosci Lett 257:139–142PubMedCrossRef Rousselle CH, Lefauconnier JM, Allen DD (1998) Evaluation of anesthetic effects on parameters for the in situ rat brain perfusion technique. Neurosci Lett 257:139–142PubMedCrossRef
35.
Zurück zum Zitat Satoh M, Parent AD, Zhang JH (2002) Inhibitory effect with antisense mitogen-activated protein kinase oligodeoxynucleotide against cerebral vasospasm in rats. Stroke 33:775–781PubMedCrossRef Satoh M, Parent AD, Zhang JH (2002) Inhibitory effect with antisense mitogen-activated protein kinase oligodeoxynucleotide against cerebral vasospasm in rats. Stroke 33:775–781PubMedCrossRef
36.
Zurück zum Zitat Soehle M, Heimann A, Kempski O (1998) Postischemic application of lipid peroxidation inhibitor U-101033E reduces neuronal damage after global cerebral ischemia in rats. Stroke 29:1240–1246PubMedCrossRef Soehle M, Heimann A, Kempski O (1998) Postischemic application of lipid peroxidation inhibitor U-101033E reduces neuronal damage after global cerebral ischemia in rats. Stroke 29:1240–1246PubMedCrossRef
37.
Zurück zum Zitat Solomon RA, Antunes JL, Chen RY, Bland L, Chien S (1985) Decrease in cerebral blood flow in rats after experimental subarachnoid hemorrhage: a new animal model. Stroke 16:58–64PubMedCrossRef Solomon RA, Antunes JL, Chen RY, Bland L, Chien S (1985) Decrease in cerebral blood flow in rats after experimental subarachnoid hemorrhage: a new animal model. Stroke 16:58–64PubMedCrossRef
38.
Zurück zum Zitat Sugawara T, Lewen A, Noshita N, Gasche Y, Chan PH (2002) Effects of global ischemia duration on neuronal, astroglial, oligodendroglial, and microglial reactions in the vulnerable hippocampal CA1 subregion in rats. J Neurotrauma 19:85–98PubMedCrossRef Sugawara T, Lewen A, Noshita N, Gasche Y, Chan PH (2002) Effects of global ischemia duration on neuronal, astroglial, oligodendroglial, and microglial reactions in the vulnerable hippocampal CA1 subregion in rats. J Neurotrauma 19:85–98PubMedCrossRef
39.
Zurück zum Zitat Takeuchi K, Renic M, Bohman QC, Harder DR, Miyata N, Roman RJ (2005) Reversal of delayed vasospasm by an inhibitor of the synthesis of 20-HETE. Am J Physiol Heart Circ Physiol 289:H2203–H2211PubMedCrossRef Takeuchi K, Renic M, Bohman QC, Harder DR, Miyata N, Roman RJ (2005) Reversal of delayed vasospasm by an inhibitor of the synthesis of 20-HETE. Am J Physiol Heart Circ Physiol 289:H2203–H2211PubMedCrossRef
40.
Zurück zum Zitat Trandafir CC, Nishihashi T, Wang A, Murakami S, Ji X, Kurahashi K (2004) Participation of vasopressin in the development of cerebral vasospasm in a rat model of subarachnoid haemorrhage. Clin Exp Pharmacol Physiol 31:261–266PubMedCrossRef Trandafir CC, Nishihashi T, Wang A, Murakami S, Ji X, Kurahashi K (2004) Participation of vasopressin in the development of cerebral vasospasm in a rat model of subarachnoid haemorrhage. Clin Exp Pharmacol Physiol 31:261–266PubMedCrossRef
41.
Zurück zum Zitat Vatter H, Weidauer S, Konczalla J, Dettmann E, Zimmermann M, Raabe A, Preibisch C, Zanella FE, Seifert V (2006) Time course in the development of cerebral vasospasm after experimental subarachnoid hemorrhage: clinical and neuroradiological assessment of the rat double hemorrhage model. Neurosurgery 58:1190–1197PubMedCrossRef Vatter H, Weidauer S, Konczalla J, Dettmann E, Zimmermann M, Raabe A, Preibisch C, Zanella FE, Seifert V (2006) Time course in the development of cerebral vasospasm after experimental subarachnoid hemorrhage: clinical and neuroradiological assessment of the rat double hemorrhage model. Neurosurgery 58:1190–1197PubMedCrossRef
42.
Zurück zum Zitat Verlooy J, Van Reempts J, Haseldonckx M, Borgers M, Selosse P (1992) The course of vasospasm following subarachnoid haemorrhage in rats. A vertebrobasilar angiographic study. Acta Neurochir (Wien) 117:48–52CrossRef Verlooy J, Van Reempts J, Haseldonckx M, Borgers M, Selosse P (1992) The course of vasospasm following subarachnoid haemorrhage in rats. A vertebrobasilar angiographic study. Acta Neurochir (Wien) 117:48–52CrossRef
43.
Zurück zum Zitat Walsh EG, Minematsu K, Leppo J, Moore SC (1994) Radioactive microsphere validation of a volume localized continuous saturation perfusion measurement. Magn Reson Med 31:147–153PubMedCrossRef Walsh EG, Minematsu K, Leppo J, Moore SC (1994) Radioactive microsphere validation of a volume localized continuous saturation perfusion measurement. Magn Reson Med 31:147–153PubMedCrossRef
44.
Zurück zum Zitat Weir B, Grace M, Hansen J, Rothberg C (1978) Time course of vasospasm in man. J Neurosurg 48:173–178PubMedCrossRef Weir B, Grace M, Hansen J, Rothberg C (1978) Time course of vasospasm in man. J Neurosurg 48:173–178PubMedCrossRef
45.
Zurück zum Zitat 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 90:1098–1104PubMedCrossRef 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 90:1098–1104PubMedCrossRef
Metadaten
Titel
The effect of common carotid artery occlusion on delayed brain tissue damage in the rat double subarachnoid hemorrhage model
verfasst von
Erdem Güresir
Nikos Vasiliadis
Santosh Dias
Peter Raab
Volker Seifert
Hartmut Vatter
Publikationsdatum
01.01.2012
Verlag
Springer Vienna
Erschienen in
Acta Neurochirurgica / Ausgabe 1/2012
Print ISSN: 0001-6268
Elektronische ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-011-1191-2

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