Skip to main content
Top
Published in: Metabolic Brain Disease 1/2013

01-03-2013 | Original Paper

Dynamic change in cerebral microcirculation and focal cerebral metabolism in experimental subarachnoid hemorrhage in rabbits

Authors: Jin-Ning Song, Hu Chen, Ming Zhang, Yong-Lin Zhao, Xu-Dong Ma

Published in: Metabolic Brain Disease | Issue 1/2013

Login to get access

Abstract

Regional cerebral blood flow (rCBF) in the cerebral metabolism and energy metabolism measurements can be used to assess blood flow of brain cells and to detect cell activity. Changes of rCBF in the cerebral microcirculation and energy metabolism were determined in an experimental model of subarachnoid hemorrhage (SAH) model in 56 large-eared Japanese rabbits about 12 to 16-month old. Laser Doppler flowmetry was used to detect the blood supply to brain cells. Internal carotid artery and vein blood samples were used for duplicate blood gas analysis to assess the energy metabolism of brain cells. Cerebral blood flow (CBF) was detected by single photon emission computed tomography (SPECT) perfusion imaging using Tc-99m ethyl cysteinate dimer (Tc-99m ECD) as an imaging reagent. The percentage of injected dose per gram of brain tissue was calculated and analyzed. There were positive correlations between the percentage of radionuclide injected per gram of brain tissue and rCBF supply and cerebral metabolic rate for oxygen (P < 0.05). However, there was a negative correlation between radioactivity counts per unit volume detected on the SPECT rheoencephalogram and lactic acid concentration in the homolateral internal carotid artery and vein. In summary, this study found abnormal CBF in metabolism and utilization of brain cells after SAH, and also found that deterioration of energy metabolism of brain cells played a significant role in the development of SAH. There are matched reductions in CBF and metabolism. Thus, SPECT imaging could be used as a noninvasive method to detect CBF.
Literature
go back to reference Baechli H, Behzad M, Schreckenberger M, Hans-Georg B, Axel H, Oliver K, Beat A (2010) Blood constituents trigger brain swelling, tissue death, and reduction of glucose metabolism early after acute subdural hematoma in rats. J Cereb Blood Flow Metab 30:576–585PubMedCrossRef Baechli H, Behzad M, Schreckenberger M, Hans-Georg B, Axel H, Oliver K, Beat A (2010) Blood constituents trigger brain swelling, tissue death, and reduction of glucose metabolism early after acute subdural hematoma in rats. J Cereb Blood Flow Metab 30:576–585PubMedCrossRef
go back to reference Bederson JB, Levy AL, DiIlg WH, Kahn R, DiPerna CA, Jenkins AL, Vallabhajosyula P (1998) Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 42:352–360PubMedCrossRef Bederson JB, Levy AL, DiIlg WH, Kahn R, DiPerna CA, Jenkins AL, Vallabhajosyula P (1998) Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 42:352–360PubMedCrossRef
go back to reference Chrapusta G, Mrowiec G, Andrychowski R (2000) Immune abnormalities in aneurysmal subarachnoid haemorrhage patients: relation to delayed cerebral vasospasm. Scand J Immunol 51:400–407PubMedCrossRef Chrapusta G, Mrowiec G, Andrychowski R (2000) Immune abnormalities in aneurysmal subarachnoid haemorrhage patients: relation to delayed cerebral vasospasm. Scand J Immunol 51:400–407PubMedCrossRef
go back to reference Del ZG, Mabuchi T (2003) Cerebral microvessel responses to focal ischemia [J]. J Cereb Blood Flow Metab 23(8):879–894 Del ZG, Mabuchi T (2003) Cerebral microvessel responses to focal ischemia [J]. J Cereb Blood Flow Metab 23(8):879–894
go back to reference Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, Tolias C, Oliveira-Ferreira AI, Fabricius M, Hartings JA, Vajkoczy P, Lauritzen M, Dirnagl U, Bohner G, Strong AJ, COSBID study group (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132:1866–1881PubMedCrossRef Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, Tolias C, Oliveira-Ferreira AI, Fabricius M, Hartings JA, Vajkoczy P, Lauritzen M, Dirnagl U, Bohner G, Strong AJ, COSBID study group (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132:1866–1881PubMedCrossRef
go back to reference 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
go back to reference Hattingen E, Blasel S, Dettmann E, Vatter H, Pilatus U, Seifert V, Zanella FE, Weidauer S (2008) Perfusion-weighted MRI to evaluate cerebral autoregulation in aneurysmal subarachnoid haemorrhage. Neuroradiology 50:929–938PubMedCrossRef Hattingen E, Blasel S, Dettmann E, Vatter H, Pilatus U, Seifert V, Zanella FE, Weidauer S (2008) Perfusion-weighted MRI to evaluate cerebral autoregulation in aneurysmal subarachnoid haemorrhage. Neuroradiology 50:929–938PubMedCrossRef
go back to reference Hischam B, Rainer S, Hilmar D, Dietmar S, Gerd H (2007) The impact of subarachnoid hemorrhage on regional cerebral blood flow and large-vessel diameter in the canine model of chronic vasospasm. Surg Neurol 16:45–51 Hischam B, Rainer S, Hilmar D, Dietmar S, Gerd H (2007) The impact of subarachnoid hemorrhage on regional cerebral blood flow and large-vessel diameter in the canine model of chronic vasospasm. Surg Neurol 16:45–51
go back to reference Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J (2007) Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke 38:981–986PubMedCrossRef Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J (2007) Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke 38:981–986PubMedCrossRef
go back to reference Kozniewska E, Michalik R, Rafalowska J, Gadamski R, Walski M, Frontczak-Baniewicz M, Piotrowski P, Czernicki Z (2006) Mechanisms of vascular dysfunction after subarachnoid hemorrhage. J Physiol Pharmacol 57:145–160PubMed Kozniewska E, Michalik R, Rafalowska J, Gadamski R, Walski M, Frontczak-Baniewicz M, Piotrowski P, Czernicki Z (2006) Mechanisms of vascular dysfunction after subarachnoid hemorrhage. J Physiol Pharmacol 57:145–160PubMed
go back to reference Liszczak TM, Black PM, Tzouras A, Foley L, Zervas NT (1984) Morphological changes of the basilar artery, ventricles, and choroid plexus after experimental SAH. J Neurosurg 61:486–493PubMedCrossRef Liszczak TM, Black PM, Tzouras A, Foley L, Zervas NT (1984) Morphological changes of the basilar artery, ventricles, and choroid plexus after experimental SAH. J Neurosurg 61:486–493PubMedCrossRef
go back to reference Macdonald RL, Pluta RM, Zhang JH (2007) Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol 3(5):256–263PubMedCrossRef Macdonald RL, Pluta RM, Zhang JH (2007) Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol 3(5):256–263PubMedCrossRef
go back to reference Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, Frey A, Roux S, Pasqualin A, CONSCIOUS-1 Investigators (2008) Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial[J]. Stroke 39(11):3015–3021PubMedCrossRef Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, Frey A, Roux S, Pasqualin A, CONSCIOUS-1 Investigators (2008) Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial[J]. Stroke 39(11):3015–3021PubMedCrossRef
go back to reference Minhas PS, Menon DK, Smielewski P, Czosnyka M, Kirkpatrick P, Clark JC, Pickard JD (2003) Positron emission tomographic cerebral perfusion disturbances and transcranial Doppler findings among patients with neurological deterioration after subarachnoid hemorrhage. Neurosurgery 52:1017–1024PubMedCrossRef Minhas PS, Menon DK, Smielewski P, Czosnyka M, Kirkpatrick P, Clark JC, Pickard JD (2003) Positron emission tomographic cerebral perfusion disturbances and transcranial Doppler findings among patients with neurological deterioration after subarachnoid hemorrhage. Neurosurgery 52:1017–1024PubMedCrossRef
go back to reference Naderi S, Ozguven MA, Bayhan H, Gokalp H, Erdogan A, Egemen N (1994) Evaluation of cerebral vasospasm in patients with subarachnoid hemorrhage using single photon emission computed tomography. Neurosurg Rev 17:261–265PubMedCrossRef Naderi S, Ozguven MA, Bayhan H, Gokalp H, Erdogan A, Egemen N (1994) Evaluation of cerebral vasospasm in patients with subarachnoid hemorrhage using single photon emission computed tomography. Neurosurg Rev 17:261–265PubMedCrossRef
go back to reference Nakajima S, Kondoh T, Morishita A, Yamashita H, Kohmura E, Takashi S, Yokono K, Umetani K (2007) Loss of CO2-induced distensibility in cerebral arteries with chronic hypertension or vasospasm after subarachnoid hemorrhage. Kobe J Med Sci 53:317–326 Nakajima S, Kondoh T, Morishita A, Yamashita H, Kohmura E, Takashi S, Yokono K, Umetani K (2007) Loss of CO2-induced distensibility in cerebral arteries with chronic hypertension or vasospasm after subarachnoid hemorrhage. Kobe J Med Sci 53:317–326
go back to reference Niimi H, Komai Y, Yamaguchi S (2007) Blood flow regulation in the cerebral microvasculature with an arcadal network: A numerical simulation. Indian J Exp Biol 45:41–47PubMed Niimi H, Komai Y, Yamaguchi S (2007) Blood flow regulation in the cerebral microvasculature with an arcadal network: A numerical simulation. Indian J Exp Biol 45:41–47PubMed
go back to reference Ostrowski RP, Colohan AR, Zhang JH (2006) Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res 28:399–414PubMedCrossRef Ostrowski RP, Colohan AR, Zhang JH (2006) Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res 28:399–414PubMedCrossRef
go back to reference Poloyac SM, Zhang YQ, Bies RR, Kochanek PM, Graham SH (2006) Protective effect of the 20-HETE inhibitor HET0016 on brain damage after temporary focal ischemia 26: 1551–1561 Poloyac SM, Zhang YQ, Bies RR, Kochanek PM, Graham SH (2006) Protective effect of the 20-HETE inhibitor HET0016 on brain damage after temporary focal ischemia 26: 1551–1561
go back to reference Powsner RA, O'Tuama LA, Jabre A, Melhem ER (1998) SPECT imaging in cerebral vasospasm following subarachnoid hemorrhage. J Nucl Med 39:765–769PubMed Powsner RA, O'Tuama LA, Jabre A, Melhem ER (1998) SPECT imaging in cerebral vasospasm following subarachnoid hemorrhage. J Nucl Med 39:765–769PubMed
go back to reference Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251–256PubMedCrossRef Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251–256PubMedCrossRef
go back to reference Romano JG, Rabinstein AA, Arheart KL, Nathan S, Campo-Bustillo I, Koch S, Forteza AM (2008) Microemboli in aneurysmal subarachnoid hemorrhage. J Neuroimaging 18:396–401PubMedCrossRef Romano JG, Rabinstein AA, Arheart KL, Nathan S, Campo-Bustillo I, Koch S, Forteza AM (2008) Microemboli in aneurysmal subarachnoid hemorrhage. J Neuroimaging 18:396–401PubMedCrossRef
go back to reference Schlenk F, Nagel A, Graetz D, Sarrafzadeh AS (2008) Hyperglycemia and cerebral glucose in aneurysmal subarachnoid hemorrhage. Intensive Care Med 34:1200–1207PubMedCrossRef Schlenk F, Nagel A, Graetz D, Sarrafzadeh AS (2008) Hyperglycemia and cerebral glucose in aneurysmal subarachnoid hemorrhage. Intensive Care Med 34:1200–1207PubMedCrossRef
go back to reference Song JN, Zhang FR, Liu SX, Hu GY, Wang MD, Xie CH, Xie WF, Zhang XD (2004) Studies of regional cerebral blood flow after parent artery embolization in intracranial aneurysm. Chin J Neurosurg 20:463–466 Song JN, Zhang FR, Liu SX, Hu GY, Wang MD, Xie CH, Xie WF, Zhang XD (2004) Studies of regional cerebral blood flow after parent artery embolization in intracranial aneurysm. Chin J Neurosurg 20:463–466
go back to reference Song JN, Zhang M, Liang Q, Sui L, Xi L, Wang WB (2011) Correlation of calcitonin gene-related peptide and endothelin receptor A with subarachnoid hemorrhage. Neural Regen Res 6:47–54 Song JN, Zhang M, Liang Q, Sui L, Xi L, Wang WB (2011) Correlation of calcitonin gene-related peptide and endothelin receptor A with subarachnoid hemorrhage. Neural Regen Res 6:47–54
go back to reference Stein SC, Levine JM, Nagpal S, Leroux PD (2006) Vasospasm as the sole cause of cerebral ischemia: how strong is the evidence? Neurosurg Focus 21:E2PubMedCrossRef Stein SC, Levine JM, Nagpal S, Leroux PD (2006) Vasospasm as the sole cause of cerebral ischemia: how strong is the evidence? Neurosurg Focus 21:E2PubMedCrossRef
go back to reference Strong MJ, Wolff AV, Wakayama T, Garruto RM (1991) Aluminum-induced chronic myelopathy in rabbits. Neurotoxicology 12:9–21PubMed Strong MJ, Wolff AV, Wakayama T, Garruto RM (1991) Aluminum-induced chronic myelopathy in rabbits. Neurotoxicology 12:9–21PubMed
go back to reference Sukhotinsky I, Dilekoz E, Moskowitz MA, Ayata C (2008) Hypoxia and hypotension transform the blood flow response to cortical spreading depression from hyperemia into hypoperfusion in the rat. J Cerebr Blood Flow Metabol 28:1369–1376CrossRef Sukhotinsky I, Dilekoz E, Moskowitz MA, Ayata C (2008) Hypoxia and hypotension transform the blood flow response to cortical spreading depression from hyperemia into hypoperfusion in the rat. J Cerebr Blood Flow Metabol 28:1369–1376CrossRef
go back to reference Titova E, Ostrowski RP, Zhang JH, Tang J (2009) Experimental models of subarachnoid hemorrhage for studies of cerebral vasospasm. Neurol Res 31:568–581PubMedCrossRef Titova E, Ostrowski RP, Zhang JH, Tang J (2009) Experimental models of subarachnoid hemorrhage for studies of cerebral vasospasm. Neurol Res 31:568–581PubMedCrossRef
go back to reference Uhl E, Lehmberg J, Steiger HJ, Messmer K (2003) Intraoperative detection of early microvasospasm in patients with subarachnoid hemorrhage by using orthogonal polarization spectral imaging. Neurosurgery 52:1307–1317PubMedCrossRef Uhl E, Lehmberg J, Steiger HJ, Messmer K (2003) Intraoperative detection of early microvasospasm in patients with subarachnoid hemorrhage by using orthogonal polarization spectral imaging. Neurosurgery 52:1307–1317PubMedCrossRef
go back to reference 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
go back to reference Weidauer S, Lanfermann H, Raabe A, Zanella F, Seifert V, Beck J (2007) Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 38:1831–1836PubMedCrossRef Weidauer S, Lanfermann H, Raabe A, Zanella F, Seifert V, Beck J (2007) Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 38:1831–1836PubMedCrossRef
go back to reference Wu JM, Hua Y, Keep RF, Schallert T, Hoffa JT, Xi GH (2002) Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Res 953:45–52PubMedCrossRef Wu JM, Hua Y, Keep RF, Schallert T, Hoffa JT, Xi GH (2002) Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Res 953:45–52PubMedCrossRef
Metadata
Title
Dynamic change in cerebral microcirculation and focal cerebral metabolism in experimental subarachnoid hemorrhage in rabbits
Authors
Jin-Ning Song
Hu Chen
Ming Zhang
Yong-Lin Zhao
Xu-Dong Ma
Publication date
01-03-2013
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 1/2013
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-012-9369-8

Other articles of this Issue 1/2013

Metabolic Brain Disease 1/2013 Go to the issue