Experimental Subarachnoid Hemorrhage: Double Cisterna Magna Injection Rat Model—Assessment of Delayed Pathological Effects of Cerebral Vasospasm

Translational Stroke Research

Volumn 6, Issue 3, 2015, Pages 242-251

  Güresir, Erdem ^a   Schuss, Patrick ^a   Borger, Valeri ^a   Vatter, Hartmut ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Animal model; Cerebral vasospasm; Delayed ischemic neurologic deficit; Double hemorrhage model; Intracranial aneurysm; Subarachnoid hemorrhage

Indexed keywords

ANIMAL; BRAIN; CISTERNA MAGNA; COMPLICATION; DISEASE MODEL; FEMALE; FEMORAL ARTERY; MALE; MICROINJECTION; PATHOPHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; SUBARACHNOID HEMORRHAGE; SURGERY; VASCULARIZATION; VASOSPASM, INTRACRANIAL; WISTAR RAT;

ANIMALS; BRAIN; CISTERNA MAGNA; DISEASE MODELS, ANIMAL; FEMALE; FEMORAL ARTERY; MALE; MICROINJECTIONS; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; SUBARACHNOID HEMORRHAGE; VASOSPASM, INTRACRANIAL;

EID: 84940007921     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-015-0392-z     Document Type: Article

References (41)

1. Brawley BW, Strandness Jr DE, Kelly WA. The biphasic response of cerebral vasospasm in experimental subarachnoid hemorrhage. J Neurosurg. 1968;28(1):1–8.
2. Petruk KC, West GR, Marriott MR, McIntyre JW, Overton TR, Weib BK. Cerebral blood flow following induced subarachnoid hemorrhage in the monkey. J Neurosurg. 1972;37(3):316–24.
3. Umansky F, Kaspi T, Shalit MN. Regional cerebral blood flow in the acute stage of experimentally induced subarachnoid hemorrhage. J Neurosurg. 1983;58(2):210–6.
4. Barry KJ, Gogjian MA, Stein BM. Small animal model for investigation of subarachnoid hemorrhage and cerebral vasospasm. Stroke. 1979;10(5):538–41.
5. Delgado TJ, Brismar J, Svendgaard NA. Subarachnoid haemorrhage in the rat: angiography and fluorescence microscopy of the major cerebral arteries. Stroke. 1985;16(4):595–602.
6. Gules I, Satoh M, Clower BR, Nanda A, Zhang JH. Comparison of three rat models of cerebral vasospasm. Am J Physiol Heart Circ Physiol. 2002;283(6):H2551–9.
7. Meguro T, Clower BR, Carpenter R, Parent AD, Zhang JH. Improved rat model for cerebral vasospasm studies. Neurol Res. 2001;23(7):761–6.
8. Jackowski A, Crockard A, Burnstock G, Russell RR, Kristek F. The time course of intracranial pathophysiological changes following experimental subarachnoid haemorrhage in the rat. J Cereb Blood Flow Metab. 1990;10(6):835–49.
9. Suzuki H, Kanamaru K, Tsunoda H, Inada H, Kuroki M, Sun H, et al. Heme oxygenase-1 gene induction as an intrinsic regulation against delayed cerebral vasospasm in rats. J Clin Invest. 1999;104(1):59–66.
10. Verlooy J, Van Reempts J, Haseldonckx M, Borgers M, Selosse P. The course of vasospasm following subarachnoid haemorrhage in rats. A vertebrobasilar angiographic study. Acta Neurochir (Wien). 1992;117(1–2):48–52.
11. Rickels E, Zumkeller M. Vasospasm after experimentally induced subarachnoid haemorrhage and treatment with nimodipine. Neurochirurgia (Stuttg). 1992;35(4):99–102.
12. Ryba MS, Gordon-Krajcer W, Walski M, Chalimoniuk M, Chrapusta SJ. Hydroxylamine attenuates the effects of simulated subarachnoid hemorrhage in the rat brain and improves neurological outcome. Brain Res. 1999;850(1–2):225–33.
13. Widenka DC, Medele RJ, Stummer W, Bise K, Steiger HJ. Inducible nitric oxide synthase: a possible key factor in the pathogenesis of chronic vasospasm after experimental subarachnoid hemorrhage. J Neurosurg. 1999;90(6):1098–104.
14. Lefranc F, Golzarian J, Chevalier C, DeWitte O, Pochet R, Heizman C, et al. Expression of members of the calcium-binding s-100 protein family in a rat model of cerebral basilar artery vasospasm. J Neurosurg. 2002;97(2):408–15.
15. Miyagi Y, Carpenter RC, Meguro T, Parent AD, Zhang JH. Upregulation of rho a and rho kinase messenger RNAs in the basilar artery of a rat model of subarachnoid hemorrhage. J Neurosurg. 2000;93(3):471–6.
16. Satoh M, Parent AD, Zhang JH. Inhibitory effect with antisense mitogen-activated protein kinase oligodeoxynucleotide against cerebral vasospasm in rats. Stroke. 2002;33(3):775–81.
17. Güresir E, Raabe A, Jaiimsin A, Dias S, Raab P, Seifert V, et al. Histological evidence of delayed ischemic brain tissue damage in the rat double-hemorrhage model. J Neurol Sci. 2010;293(1–2):18–22.
18. Aladag MA, Turkoz Y, Ozcan C, Sahna E, Parlakpinar H, Akpolat N, et al. Caffeic acid phenethyl ester (cape) attenuates cerebral vasospasm after experimental subarachnoidal haemorrhage by increasing brain nitric oxide levels. Int J Dev Neurosci. 2006;24(1):9–14.
19. Lee JY, Huang DL, Keep R, Sagher O. Characterization of an improved double hemorrhage rat model for the study of delayed cerebral vasospasm. J Neurosci Methods. 2008;168(2):358–66.
20. Lu H, Shi JX, Chen HL, Hang CH, Wang HD, Yin HX. Expression of monocyte chemoattractant protein-1 in the cerebral artery after experimental subarachnoid hemorrhage. Brain Res. 2009;1262:73–80.
21. Takata K, Sheng H, Borel CO, Laskowitz DT, Warner DS, Lombard FW. Long-term cognitive dysfunction following experimental subarachnoid hemorrhage: new perspectives. Exp Neurol. 2008;213(2):336–44.
22. Vatter H, Weidauer S, Konczalla J, Dettmann E, Zimmermann M, Raabe A, 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(6):1190–7. discussion 1190–1197.
23. Cai J, Sun Y, Yuan F, Chen L, He C, Bao Y, et al. A novel intravital method to evaluate cerebral vasospasm in rat models of subarachnoid hemorrhage: a study with synchrotron radiation angiography. PLoS One. 2012;7(3):e33366.
24. Güresir E, Vasiliadis N, Dias S, Raab P, Seifert V, Vatter H. The effect of common carotid artery occlusion on delayed brain tissue damage in the rat double subarachnoid hemorrhage model. Acta Neurochir (Wien). 2012;154(1):11–9.
25. Güresir E, Vasiliadis N, Konczalla J, Raab P, Hattingen E, Seifert V, et al. Erythropoietin prevents delayed hemodynamic dysfunction after subarachnoid hemorrhage in a randomized controlled experimental setting. J Neurol Sci. 2013;332(1–2):128–35.
26. Hänggi D, Perrin J, Eicker S, Beseoglu K, Etminan N, Kamp MA, et al. Local delivery of nimodipine by prolonged-release microparticles-feasibility, effectiveness and dose-finding in experimental subarachnoid hemorrhage. PLoS One. 2012;7(9):e42597.
27. Konczalla J, Mrosek J, Wanderer S, Schuss P, Güresir E, Seifert V, et al. Functional effects of levosimendan in rat basilar arteries in vitro. Curr Neurovasc Res. 2013;10(2):126–33.
28. Raslan F, Albert-Weissenberger C, Westermaier T, Saker S, Kleinschnitz C, Lee JY. A modified double injection model of cisterna magna for the study of delayed cerebral vasospasm following subarachnoid hemorrhage in rats. Exp Transl Stroke Med. 2012;4(1):23.
29. Wang Z, Chen G, Zhu WW, Zhou D. Activation of nuclear factor-erythroid 2-related factor 2 (nrf2) in the basilar artery after subarachnoid hemorrhage in rats. Ann Clin Lab Sci. 2010;40(3):233–9.
30. Dittmar MS, Fehm NP, Vatankhah B, Horn M. Ketamine/xylazine anesthesia for radiologic imaging of neurologically impaired rats: dose response, respiratory depression, and management of complications. Comp Med. 2004;54(6):652–5.
31. Lee JY, Sagher O, Keep R, Hua Y, Xi G. Comparison of experimental rat models of early brain injury after subarachnoid hemorrhage. Neurosurgery. 2009;65(2):331–43. discussion 343.
32. Rousselle CH, Lefauconnier JM, Allen DD. Evaluation of anesthetic effects on parameters for the in situ rat brain perfusion technique. Neurosci Lett. 1998;257(3):139–42.
33. Lei H, Grinberg O, Nwaigwe CI, Hou HG, Williams H, Swartz HM, et al. 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. 2001;913(2):174–9.
34. Zausinger S, Baethmann A, Schmid-Elsaesser R. Anesthetic methods in rats determine outcome after experimental focal cerebral ischemia: mechanical ventilation is required to obtain controlled experimental conditions. Brain Res Brain Res Protocol. 2002;9(2):112–21.
35. Prunell GF, Mathiesen T, Diemer NH, Svendgaard NA. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery. 2003;52(1):165–75. discussion 175–166.
36. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke. 1986;17(3):472–6.
37. Weidauer S, Vatter H, Dettmann E, Seifert V, Zanella FE. Assessment of vasospasm in experimental subarachnoid hemorrhage in rats by selective biplane digital subtraction angiography. Neuroradiology. 2006;48(3):176–81.
38. Schilling L, Vatter H, Mursch K, Ehrenreich H, Schmiedek P. Characterization of the contractile and relaxant action of the endothelin-1 precursor, big endothelin-1, in the isolated rat basilar artery. Peptides. 2000;21(1):91–9.
39. Vatter H, Konczalla J, Weidauer S, Preibisch C, Zimmermann M, Raabe A, et al. Effect of delayed cerebral vasospasm on cerebrovascular endothelin a receptor expression and function. J Neurosurg. 2007;107(1):121–7.
40. 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(2):426–36. discussion 436–427.
41. Megyesi JF, Vollrath B, Cook DA, Findlay JM. In vivo animal models of cerebral vasospasm: a review. Neurosurgery. 2000;46(2):448–60. discussion 460–441.