The Rabbit Shunt Model of Subarachnoid Haemorrhage

Translational Stroke Research

Volumn 5, Issue 6, 2014, Pages 669-680

  Marbacher, Serge ^a,b   Nevzati, Edin ^a,b   Croci, Davide ^a,b   Erhardt, Salome ^a,b   Muroi, Carl ^a,b   Jakob, Stephan M ^a   Fandino, Javier ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b CANTONAL HOSPITAL AARAU   (Switzerland)

Author keywords

Animal models; Arterial blood shunt; Delayed cerebral vasospasm; Early brain injury; Microsurgery; Rabbit; Subarachnoid haemorrhage

Indexed keywords

ANESTHESIOLOGICAL PROCEDURE; ARTICLE; BRAIN; NONHUMAN; PATHOPHYSIOLOGY; PATIENT MONITORING; PERIOPERATIVE PERIOD; PRIORITY JOURNAL; RABBIT MODEL; RABBIT SHUNT MODEL; SUBARACHNOID HEMORRHAGE; ANASTOMOSIS; ANIMAL; CISTERNA MAGNA; DISEASE MODEL; FEMALE; INTRACRANIAL PRESSURE; MALE; RABBIT; VASOSPASM, INTRACRANIAL;

ANASTOMOSIS, SURGICAL; ANIMALS; BRAIN; CISTERNA MAGNA; DISEASE MODELS, ANIMAL; FEMALE; INTRACRANIAL PRESSURE; MALE; RABBITS; SUBARACHNOID HEMORRHAGE; VASOSPASM, INTRACRANIAL;

EID: 84922092153     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-014-0369-3     Document Type: Article

References (68)

1. Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009;8(7):635–42. doi:10.1016/S1474-4422(09)70126-7.
2. Malmivaara K, Juvela S, Hernesniemi J, Lappalainen J, Siironen J. Health-related quality of life and cost-effectiveness of treatment in subarachnoid haemorrhage. Eur J Neurol Off J Eur Fed Neurol Soc. 2012;19(11):1455–61. doi:10.1111/j.1468-1331.2012.03744.x.
3. Johnston SC, Selvin S, Gress DR. The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology. 1998;50(5):1413–8.
4. Ecker A, Riemenschneider PA. Arteriographic demonstration of spasm of the intracranial arteries, with special reference to saccular arterial aneurysms. J Neurosurg. 1951;8(6):660–7. doi:10.3171/jns.1951.8.6.0660.
5. Roux S, Breu V, Giller T, Neidhart W, Ramuz H, Coassolo P, et al. Ro 61–1790, a new hydrosoluble endothelin antagonist: general pharmacology and effects on experimental cerebral vasospasm. J Pharmacol Exp Ther. 1997;283(3):1110–8.
6. Wanebo JE, Louis HG, Arthur AS, Zhou J, Kassell NF, Lee KS et al. Attenuation of cerebral vasospasm by systemic administration of an endothelin-A receptor antagonist, TBC 11251, in a rabbit model of subarachnoid hemorrhage. Neurosurgical focus. 1997;3(4):ARTICLE.
7. Vajkoczy P, Meyer B, Weidauer S, Raabe A, Thome C, Ringel F, et al. Clazosentan (AXV-034343), a selective endothelin A receptor antagonist, in the prevention of cerebral vasospasm following severe aneurysmal subarachnoid hemorrhage: results of a randomized, double-blind, placebo-controlled, multicenter phase IIa study. J Neurosurg. 2005;103(1):9–17. doi:10.3171/jns.2005.103.1.0009.
8. Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke J Cereb Circ. 2008;39(11):3015–21. doi:10.1161/STROKEAHA.108.519942.
9. Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol. 2011;10(7):618–25. doi:10.1016/S1474-4422(11)70108-9.
10. Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins 3rd AL, et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery. 1998;42(2):352–60. discussion 60–2.
11. Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke J Cereb Circ. 2002;33(5):1225–32.
12. Siironen J, Porras M, Varis J, Poussa K, Hernesniemi J, Juvela S. Early ischemic lesion on computed tomography: predictor of poor outcome among survivors of aneurysmal subarachnoid hemorrhage. J Neurosurg. 2007;107(6):1074–9. doi:10.3171/JNS-07/12/1074.
13. Pluta RM, Hansen-Schwartz J, Dreier J, Vajkoczy P, Macdonald RL, Nishizawa S, et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res. 2009;31(2):151–8. doi:10.1179/174313209X393564.
14. Sehba FA, Pluta RM, Zhang JH. Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol. 2011;43(1):27–40. doi:10.1007/s12035-010-8155-z.
15. Cahill J, Zhang JH. Subarachnoid hemorrhage: is it time for a new direction? Stroke J Cereb Circ. 2009;40(3 Suppl):S86–7. doi:10.1161/STROKEAHA.108.533315.
16. Marbacher S, Fandino J, Kitchen ND. Standard intracranial in vivo animal models of delayed cerebral vasospasm. Br J Neurosurg. 2010;24(4):415–34. doi:10.3109/02688691003746274.
17. Edvinsson L, Egund N, Owman C, Sahlin C, Svendgaard NA. Reduced noradrenaline uptake and retention in cerebrovascular nerves associated with angiographically visible vasoconstriction following experimental subarachnoid hemorrhage in rabbits. Brain Res Bull. 1982;9(1–6):799–805.
18. Liszczak TM, Black PM, Tzouras A, Foley L, Zervas NT. Morphological changes of the basilar artery, ventricles, and choroid plexus after experimental SAH. J Neurosurg. 1984;61(3):486–93. doi:10.3171/jns.1984.61.3.0486.
19. Chan RC, Durity FA, Thompson GB, Nugent RA, Kendall M. The role of the prostacyclin-thromboxane system in cerebral vasospasm following induced subarachnoid hemorrhage in the rabbit. J Neurosurg. 1984;61(6):1120–8. doi:10.3171/jns.1984.61.6.1120.
20. Endo S, Branson PJ, Alksne JF. Experimental model of symptomatic vasospasm in rabbits. Stroke J Cereb Circ. 1988;19(11):1420–5.
21. Baker KF, Zervas NT, Pile-Spellman J, Vacanti FX, Miller D. Angiographic evidence of basilar artery constriction in the rabbit: a new model of vasospasm. Surg Neurol. 1987;27(2):107–12.
22. Spallone A, Pastore FS. Cerebral vasospasm in a double-injection model in rabbit. Surg Neurol. 1989;32(6):408–17.
23. Zhou ML, Shi JX, Zhu JQ, Hang CH, Mao L, Chen KF, et al. Comparison between one- and two-hemorrhage models of cerebral vasospasm in rabbits. J Neurosci Methods. 2007;159(2):318–24. doi:10.1016/j.jneumeth.2006.07.026.
24. Logothetis J, Karacostas D, Karoutas G, Artemis N, Mansouri A, Milonas I. A new model of subarachnoid hemorrhage in experimental animals with the purpose to examine cerebral vasospasm. Exp Neurol. 1983;81(2):257–78.
25. Egemen N, Sanlidilek U, Zorlutuna A, Baskaya M, Bilgic S, Caglar S, et al. Transclival approach to rabbit basilar artery for experimental induction of chronic vasospasm. Acta Neurochir. 1992;115(3–4):123–6.
26. Steiner L, Lofgren J, Zwetnow NN. Characteristics and limits of tolerance in repeated subarachnoid hemorrhage in dogs. Acta Neurol Scand. 1975;52(4):241–67.
27. McCormick PW, McCormick J, Zabramski JM, Spetzler RF. Hemodynamics of subarachnoid hemorrhage arrest. J Neurosurg. 1994;80(4):710–5. doi:10.3171/jns.1994.80.4.0710.
28. Trojanowski T. Experimental subarachnoid haemorrhage. Part I: a new approach to subarachnoid blood injection in cats. Acta Neurochir. 1982;62(3–4):171–5.
29. Offerhaus L, van Gool J. Electrocardiographic changes and tissue catecholamines in experimental subarachnoid haemorrhage. Cardiovasc Res. 1969;3(4):433–40.
30. Zhao W, Ujiie H, Tamano Y, Akimoto K, Hori T, Takakura K. Sudden death in a rat subarachnoid hemorrhage model. Neurol Med Chir. 1999;39(11):735–41. discussion 41–3.
31. Marbacher S, Sherif C, Neuschmelting V, Schlappi JA, Takala J, Jakob SM, et al. Extra-intracranial blood shunt mimicking aneurysm rupture: intracranial-pressure-controlled rabbit subarachnoid hemorrhage model. J Neurosci Methods. 2010;191(2):227–33. doi:10.1016/j.jneumeth.2010.07.004.
32. Marbacher S, Andereggen L, Neuschmelting V, Widmer HR, von Gunten M, Takala J, et al. A new rabbit model for the study of early brain injury after subarachnoid hemorrhage. J Neurosci Methods. 2012;208(2):138–45. doi:10.1016/j.jneumeth.2012.05.010.
33. Lin CL, Dumont AS, Su YF, Dai ZK, Cheng JT, Tsai YJ, et al. Attenuation of subarachnoid hemorrhage-induced apoptotic cell death with 17 beta-estradiol. Laboratory investigation. J Neurosurg. 2009;111(5):1014–22. doi:10.3171/2009.3.JNS081660.
34. Ondruska L, Rafay J, Okab AB, Ayoub MA, Al-Haidary AA, Samara EM, et al. Influence of elevated ambient temperature upon some physiological measurements of New Zealand white rabbits. Vet Med. 2011;56(4):180–6.
35. Nakajima M, Date I, Takahashi K, Ninomiya Y, Asari S, Ohmoto T. Effects of aging on cerebral vasospasm after subarachnoid hemorrhage in rabbits. Stroke J Cereb Circ. 2001;32(3):620–8.
36. Hockel K, Trabold R, Scholler K, Torok E, Plesnila N. Impact of anesthesia on pathophysiology and mortality following subarachnoid hemorrhage in rats. Exp Transl Stroke Med. 2012;4(1):5. doi:10.1186/2040-7378-4-5.
37. Barzago MM, Bortolotti A, Omarini D, Aramayona JJ, Bonati M. Monitoring of blood gas parameters and acid–base balance of pregnant and non-pregnant rabbits (Oryctolagus cuniculus) in routine experimental conditions. Lab Anim. 1992;26(2):73–9.
38. Schroeder CA, Smith LJ. Respiratory rates and arterial blood-gas tensions in healthy rabbits given buprenorphine, butorphanol, midazolam, or their combinations. J Am Assoc Lab Anim Sci. 2011;50(2):205–11.
39. Harper AM. Autoregulation of cerebral blood flow: influence of the arterial blood pressure on the blood flow through the cerebral cortex. J Neurol Neurosurg Psychiatry. 1966;29(5):398–403.
40. Markwalder TM, Grolimund P, Seiler RW, Roth F, Aaslid R. Dependency of blood flow velocity in the middle cerebral artery on end-tidal carbon dioxide partial pressure—a transcranial ultrasound Doppler study. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 1984;4(3):368–72. doi:10.1038/jcbfm.1984.54.
41. Hayakawa T, Waltz AG. Experimental subarachnoid hemorrhage from a middle cerebral artery. Neurologic deficits, intracranial pressures, blood pressures, and pulse rates. Stroke J Cereb Circ. 1977;8(4):421–6.
42. Andereggen L, Neuschmelting V, von Gunten M, Widmer HR, Takala J, Jakob S, et al. The rabbit blood-shunt model for the study of acute and late sequelae of subarachnoid hemorrhage: technical aspects. J Vis Exp. 2014.
43. Marbacher S, Milavec H, Neuschmelting V, Andereggen L, Erhardt S, Fandino J. Outer skull landmark-based coordinates for measurement of cerebral blood flow and intracranial pressure in rabbits. J Neurosci Methods. 2011;201(2):322–6. doi:10.1016/j.jneumeth.2011.08.009.
44. Levinger IM. Special features of the rabbit cerebroventricular system, studied by the casting method. J Anat. 1971;109(Pt 3):527–33.
45. Andereggen L, Neuschmelting V, Von Gunten M, Widmer HR, Fandino J, Marbacher S. The role of microclot formation in an acute subarachnoid hemorrhage model in the rabbit. BioMed Research International. 2014.
46. Sugawara T, Ayer R, Jadhav V, Zhang JH. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods. 2008;167(2):327–34. doi:10.1016/j.jneumeth.2007.08.004.
47. Marbacher S, Fathi AR, Muroi C, Coluccia D, Andereggen L, Neuschmelting V, et al. The rabbit blood shunt subarachnoid hemorrhage model. Acta neurochirurgica Supplement. 2014.
48. Bederson JB, Germano IM, Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke J Cereb Circ. 1995;26(6):1086–91. Discussion 91–2.
49. Kamii H, Kato I, Kinouchi H, Chan PH, Epstein CJ, Akabane A, et al. Amelioration of vasospasm after subarachnoid hemorrhage in transgenic mice overexpressing CuZn-superoxide dismutase. Stroke J Cereb Circ. 1999;30(4):867–71. discussion 72.
50. Brawley BW, Strandness Jr DE, Kelly WA. The biphasic response of cerebral vasospasm in experimental subarachnoid hemorrhage. J Neurosurg. 1968;28(1):1–8. doi:10.3171/jns.1968.28.1.0001.
51. Nagai H, Suzuki Y, Sugiura M, Noda S, Mabe H. Experimental cerebral vasospasm. 1: factors contributing to early spasm. J Neurosurg. 1974;41(3):285–92.
52. Weir B, Erasmo R, Miller J, McIntyre J, Secord D, Mielke B. Vasospasm in response to repeated subarachnoid hemorrhages in the monkey. J Neurosurg. 1970;33(4):395–406. doi:10.3171/jns.1970.33.4.0395.
53. Jakubowski J, Bell BA, Symon L, Zawirski MB, Francis DM. A primate model of subarachnoid hemorrhage: change in regional cerebral blood flow, autoregulation carbon dioxide reactivity, and central conduction time. Stroke J Cereb Circ. 1982;13(5):601–11.
54. Frosen J, Piippo A, Paetau A, Kangasniemi M, Niemela M, Hernesniemi J, et al. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: histological analysis of 24 unruptured and 42 ruptured cases. Stroke J Cereb Circ. 2004;35(10):2287–93. doi:10.1161/01.STR.0000140636.30204.da.
55. Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R. Structural fragility and inflammatory response of ruptured cerebral aneurysms. A comparative study between ruptured and unruptured cerebral aneurysms. Stroke J Cereb Circ. 1999;30(7):1396–401.
56. Jeon H, Ai J, Sabri M, Tariq A, Shang X, Chen G, et al. Neurological and neurobehavioral assessment of experimental subarachnoid hemorrhage. BMC Neurosci. 2009;10:103. doi:10.1186/1471-2202-10-103.
57. Buemi M, Grasso G, Corica F, Calapai G, Salpietro FM, Casuscelli T, et al. In vivo evidence that erythropoietin has a neuroprotective effect during subarachnoid hemorrhage. Eur J Pharmacol. 2000;392(1–2):31–4.
58. Marbacher S, Neuschmelting V, Graupner T, Jakob SM, Fandino J. Prevention of delayed cerebral vasospasm by continuous intrathecal infusion of glyceroltrinitrate and nimodipine in the rabbit model in vivo. Intensive Care Med. 2008;34(5):932–8. doi:10.1007/s00134-008-0995-x.
59. Neuschmelting V, Fathi AR, Hidalgo Staub ET, Marbacher S, Schroth G, Takala J, et al. Norepinephrine-induced hypertension dilates vasospastic basilar artery after subarachnoid haemorrhage in rabbits. Acta Neurochir. 2009;151(5):487–93. doi:10.1007/s00701-009-0287-4.
60. Fathi AR, Marbacher S, Graupner T, Wehrli F, Jakob SM, Schroth G, et al. Continuous intrathecal glyceryl trinitrate prevents delayed cerebral vasospasm in the single-SAH rabbit model in vivo. Acta Neurochir. 2011;153(8):1669–75. doi:10.1007/s00701-011-1049-7. discussion 75.
61. Chen G, Wu J, Sun C, Qi M, Hang C, Gong Y, et al. Potential role of JAK2 in cerebral vasospasm after experimental subarachnoid hemorrhage. Brain Res. 2008;1214:136–44. doi:10.1016/j.brainres.2008.03.085.
62. Zubkov AY, Aoki K, Parent AD, Zhang JH. Preliminary study of the effects of caspase inhibitors on vasospasm in dog penetrating arteries. Life Sci. 2002;70(25):3007–18.
63. Hart MN, O’Donnell SL. Effects of formaldehyde fixation on basilar artery caliber. Stroke J Cereb Circ. 1980;11(1):99–100.
64. Zheng B, Zheng T, Wang L, Chen X, Shi C, Zhao S. Aminoguanidine inhibition of iNOS activity ameliorates cerebral vasospasm after subarachnoid hemorrhage in rabbits via restoration of dysfunctional endothelial cells. J Neurol Sci. 2010;295(1–2):97–103. doi:10.1016/j.jns.2010.04.012.
65. Shao Z, Li J, Zhao Z, Gao C, Sun Z, Liu X. Effects of tetramethylpyrazine on nitric oxide/cGMP signaling after cerebral vasospasm in rabbits. Brain Res. 2010;1361:67–75. doi:10.1016/j.brainres.2010.09.011.
66. Laslo AM, Eastwood JD, Pakkiri P, Chen F, Lee TY. CT perfusion-derived mean transit time predicts early mortality and delayed vasospasm after experimental subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2008;29(1):79–85. doi:10.3174/ajnr.A0747.
67. Sasani M, Yazgan B, Celebi I, Aytan N, Catalgol B, Oktenoglu T, et al. Hypercholesterolemia increases vasospasm resulting from basilar artery subarachnoid hemorrhage in rabbits which is attenuated by vitamin E. Surg Neurol Int. 2011;2:29. doi:10.4103/2152-7806.77600.
68. Goksel HM, Ozum U, Oztoprak I. The therapeutic effect of continuous intracisternal l-Arginine infusion on experimental cerebral vasospasm. Acta Neurochir. 2001;143(3):277–85.