In vivo experimental models of focal ischemic stroke

Thrombus and Stroke

Volumn , Issue , 2008, Pages 39-56

  Gounis, Matthew J ^a   Sicard, Kenneth M ^a   Wakhloo, Ajay K ^a   Fisher, Marc ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78650701847     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (98)

1. Sacco RL, Wolf PA, Gorelick PB. Risk factors and their management for stroke prevention: outlook for 1999 and beyond. Neurology 1999; 53 (7 suppl 4): S15-S24.
2. del Zoppo GJ, Poeck K, Pessin MS, et al. Recombinant tissue plasminogen activator in acute thrombotic and embolic stroke. Ann Neurol 1992; 32 (1): 78-86.
3. Hsu CY. Criteria for valid preclinical trials using animal stroke models. Stroke 1993; 24 (5): 633-636.
4. Yamori Y, Horie R, Handa H, et al. Pathogenetic similarity of strokes in stroke-prone spontaneously hypertensive rats and humans. Stroke 1976; 7 (1): 46-53.
5. Coyle P. Middle cerebral artery occlusion in the young rat. Stroke 1982; 13 (6): 855-859.
6. Ginsberg MD, Busto R. Rodent models of cerebral ischemia. Stroke 1989; 20 (12): 1627-1642.
7. Hoyte L, Kaur J, Buchan AM. Lost in translation: taking neuroprotection from animal models to clinical trials. Exp Neurol 2004; 188 (2): 200-204.
8. Koizumi J, Yoshida Y, Nakazawa T, et al. Experimental studies of ischemic brain edema. I: a new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area. Jap J Stroke 1986; 8: 1-8.
9. Belayev L, Alonso OF, Busto R, et al. Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 1996; 27 (9): 1616-1622; discussion 1623.
10. Takano K, Tatlisumak T, Bergmann AG, et al. Reproducibility and reliability of middle cerebral artery occlusion using a silicone-coated suture (Koizumi) in rats. J Neurol Sci 1997; 153 (1): 8-11.
11. Longa EZ, Weinstein PR, Carlson S, et al. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20 (1): 84-91.
12. Nagasawa H, Kogure K. Correlation between cerebral blood flow and histologic changes in a new rat model of middle cerebral artery occlusion. Stroke 1989; 20 (8): 1037-1043.
13. Li F, Han S, Tatlisumak T, et al. A new method to improve in-bore middle cerebral artery occlusion in rats: demonstration with diffusion-and perfusion-weighted imaging. Stroke 1998; 29 (8): 1715-1719; discussion 1719-1720.
14. Li F, Tatlisumak T. Focal brain ischemia models in rodents. In: Tatlisumak T, Fisher M, eds. Handbook of Experimental Neurology: Methods and Techniques in Animal Research. Cambridge: Cambridge University Press, 2006: 311-328.
15. Meng X, Fisher M, Shen Q, et al. Characterizing the diffusion/perfusion mismatch in experimental focal cerebral ischemia. Ann Neurol 2004; 55 (2): 207-212.
16. Kuge Y, Minematsu K, Yamaguchi T, et al. Nylon monofilament for intraluminal middle cerebral artery occlusion in rats. Stroke 1995; 26 (9): 1655-1657.
17. Zarow GJ, Karibe H, States BA, et al. Endovascular suture occlusion of the middle cerebral artery in rats: effect of suture insertion distance on cerebral blood flow, infarct distribution and infarct volume. Neurol Res 1997; 19 (4): 409-416.
18. Oliff HS, Weber E, Miyazaki B, et al. Infarct volume varies with rat strain and vendor in focal cerebral ischemia induced by transcranial middle cerebral artery occlusion. Brain Res 1995; 699 (2): 329-331.
19. Schmid-Elsaesser R, Zausinger S, Hungerhuber E, et al. A critical reevaluation of the intraluminal thread model of focal cerebral ischemia: evidence of inadvertent premature reperfusion and subarachnoid hemorrhage in rats by laser-Doppler flowmetry. Stroke 1998; 29 (10): 2162-2170.
20. Zhao Q, Memezawa H, Smith ML, et al. Hyperthermia complicates middle cerebral artery occlusion induced by an intraluminal filament. Brain Res 1994; 649 (1-2): 253-259.
21. Li F, Omae T, Fisher M. Spontaneous hyperthermia and its mechanism in the intraluminal suture middle cerebral artery occlusion model of rats. Stroke 1999; 30 (11): 2464-2470.
22. Sicard KM, Henninger N, Fisher M, et al. Differential recovery of multimodal MRI and behavior after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 2006; 26 (11): 1451-1462.
23. Sicard KM, Henninger N, Fisher M, et al. Long-term changes of functional MRI-based brain function, behavioral status, and histopathology after transient focal cerebral ischemia in rats. Stroke 2006; 37 (10): 2593-2600.
24. Futrell N, Watson BD, Dietrich WD, et al. A new model of embolic stroke produced by photochemical injury to the carotid artery in the rat. Ann Neurol 1988; 23 (3): 251-257.
25. Hill NC, Millikan CH, Wakim KG, et al. Studies in cerebrovascular disease. VII. Experimental production of cerebral infarction by intracarotid injection of homologous blood clot: preliminary report. Mayo Clin Proc 1955; 30 (26): 625-633.
26. Kudo M, Aoyama A, Ichimori S, et al. An animal model of cerebral infarction. Homologous blood clot emboli in rats. Stroke 1982; 13 (4): 505-508.
27. Henninger N, Sicard KM, Schmidt KF, et al. Comparison of ischemic lesion evolution in embolic versus mechanical middle cerebral artery occlusion in Sprague Dawley rats using diffusion and perfusion imaging. Stroke 2006; 37 (5): 1283-1287.
28. Albers GW. Antithrombotic agents in cerebral ischemia. Am J Cardiol 1995; 75 (6): 34B-38B.
29. NINDS Study Investigators. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke t-PA stroke study group. N Engl J Med 1995; 333 (24): 1581-1587.
30. Savitz SI, Fisher M. Future of neuroprotection for acute stroke: in the aftermath of the saint trials. Ann Neurol 2007; 61 (5): 396-402.
31. Busch E, Kruger K, Hossmann KA. Improved model of thromboembolic stroke and t-PA induced reperfusion in the rat. Brain Res 1997; 778 (1): 16-24.
32. Takano K, Carano RA, Tatlisumak T, et al. Efficacy of intra-arterial and intravenous prourokinase in an embolic stroke model evaluated by diffusion-perfusion magnetic resonance imaging. Neurology 1998; 50 (4): 870-875.
33. Henninger N, Sicard KM, Fisher M, et al. Spectacular shrinking deficit: insights from multimodal magnetic resonance imaging after embolic middle cerebral artery occlusion in Sprague-Dawley rats. J Cereb Blood Flow Metab 2007; 27 (10): 1756-1763.
34. Siegel BA, Meidinger R, Elliott AJ, et al. Experimental cerebral microembolism. Multiple tracer assessment of brain edema. Arch Neurol 1972; 26 (1): 73-77.
35. Garcia JH. Experimental ischemic stroke: a review. Stroke 1984; 15 (1): 5-14.
36. Takeda T, Shima T, Okada Y, et al. Pathophysiological studies of cerebral ischemia produced by silicone cylinder embolization in rats. J Cereb Blood Flow 1987; 7 (suppl): S66.
37. Fukuchi K, Kusuoka H, Watanabe Y, et al. Correlation of sequential MR images of microsphere-induced cerebral ischemia with histologic changes in rats. Invest Radiol 1999; 34 (11): 698-703.
38. Gerriets T, Li F, Silva MD, et al. The macrosphere model: evaluation of a new stroke model for permanent middle cerebral artery occlusion in rats. J Neurosci Methods 2003; 122 (2): 201-211.
39. Watson BD, Dietrich WD, Busto R, et al. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 1985; 17 (5): 497-504.
40. Dietrich WD, Ginsberg MD, Busto R, et al. Photochemically induced cortical infarction in the rat. 2. Acute and subacute alterations in local glucose utilization. J Cereb Blood Flow Metab 1986; 6 (2): 195-202.
41. Sugimori H, Yao H, Ooboshi H, et al. Krypton laser-induced photothrombotic distal middle cerebral artery occlusion without craniectomy in mice. Brain Res Brain Res Protoc 2004; 13 (3): 189-196.
42. Schneider G, Fries P, Wagner-Jochem D, et al. Pathophysiological changes after traumatic brain injury: comparison of two experimental animal models by means of MRI. MAGMA 2002; 14 (3): 233-241.
43. Carmichael ST. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2005; 2 (3): 396-409.
44. Heilman CB, Kwan ES, Wu JK. Aneurysm recurrence following endovascular balloon occlusion. J Neurosur 1992; 77 (2): 260-264.
45. Korninger C, Collen D. Studies on the specific fibrinolytic effect of human extrinsic (tissue-type) plasminogen activator in human blood and in various animal species in vitro. Thromb Haemost 1981; 46 (2): 561-565.
46. Zivin JA, Fisher M, DeGirolami U, et al. Tissue plasminogen activator reduces neurological damage after cerebral embolism. Science 1985; 230 (4731): 1289-1292.
47. Zhang SM, Ramirez-Lassepas M, Hernandez LA, et al. A new model of experimental cerebral infarction in New Zealand white rabbits. J Tongji Med Univ 1995; 15 (1): 5-9.
48. Lapchak PA, Araujo DM, Song D, et al. Neuroprotective effects of the spin trap agent disodium-[(tert-butylimino)methyl]benzene-1,3-disulfonate N-oxide (generic NXY-059) in a rabbit small clot embolic stroke model: combination studies with the thrombolytic tissue plasminogen activator. Stroke 2002; 33 (5): 1411-1415.
49. Maher P, Salgado KF, Zivin JA, et al. A novel approach to screening for new neuroprotective compounds for the treatment of stroke. Brain Res 2007; 1173: 117-125.
50. Lapchak PA, Araujo DM, Pakola S, et al. Microplasmin: a novel thrombolytic that improves behavioral outcome after embolic strokes in rabbits. Stroke 2002; 33 (9): 2279-2284.
51. Lyden PD, Madden KP, Clark WM, et al. Incidence of cerebral hemorrhage after treatment with tissue plasminogen activator or streptokinase following embolic stroke in rabbits. Stroke 1990; 21 (11): 1589-1593.
52. Lee JS, Hamilton MG, Zabramski JM. Variations in the anatomy of the rabbit cervical carotid artery. Stroke 1994; 25 (2): 501-503.
53. Bednar MM, McAuliffe T, Raymond S, et al. Tissue plasminogen activator reduces brain injury in a rabbit model of thromboembolic stroke. Stroke 1990; 21 (12): 1705-1709.
54. Benes V, Zabramski JM, Boston M, et al. Effect of intra-arterial tissue plasminogen activator and urokinase on autologous arterial emboli in the cerebral circulation of rabbits. Stroke 1990; 21 (11): 1594-1599.
55. Lapchak PA, Chapman DF, Zivin JA. Pharmacological effects of the spin trap agents N-t-butyl-phenylnitrone (PBN) and 2,2,6, 6-tetramethylpiperidine-N-oxyl (TEMPO) in a rabbit thromboembolic stroke model: combination studies with the thrombolytic tissue plasminogen activator. Stroke 2001; 32 (1): 147-153.
56. Lapchak PA, Chapman DF, Zivin JA. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke 2000; 31 (12): 3034-3040.
57. Russell D, Madden KP, Clark WM, et al. Tissue plasminogen activator cerebrovascular thrombolysis in rabbits is dependent on the rate and route of administration. Stroke 1992; 23 (3): 388-393.
58. O’Brien MD, Waltz AG. Transorbital approach for occluding the middle cerebral artery without craniectomy. Stroke 1973; 4 (2): 201-206.
59. Sundt TM, Waltz AG. Experimental cerebral infarction: retro-orbital, extradural approach for occluding the middle cerebral artery. Mayo Clin Proc 1966; 41 (3): 159-168.
60. Hossmann KA, Mies G, Paschen W, et al. Multiparametric imaging of blood flow and metabolism after middle cerebral artery occlusion in cats. J Cereb Blood Flow Metab 1985; 5 (1): 97-107.
61. Berkelbach van der Sprenkel JW, Tulleken CA. The postorbital approach to the middle cerebral artery in cats. Stroke 1988; 19 (4): 503-506.
62. Bose B, Osterholm JL, Berry R. A reproducible experimental model of focal cerebral ischemia in the cat. Brain Res 1984; 311 (2): 385-391.
63. Davis DO, Rumbaugh CL. Cerebral angiography in the dog. Method for consistent results. Invest Radiol 1967; 2 (5): 323-325.
64. Purdy PD, Devous MD Sr., Batjer HH, et al. Microfibrillar collagen model of canine cerebral infarction. Stroke 1989; 20 (10): 1361-1367.
65. Corbett RJ, Purdy PD, Laptook AR, et al. Noninvasive measurement of brain temperature after stroke. AJNR Am J Neuroradiol 1999; 20 (10): 1851-1857.
66. Molinari GF. Experimental cerebral infarction. II. Clinicopathological model of deep cerebral infarction. Stroke 1970; 1 (4): 232-244.
67. Molinari GF. Experimental cerebral infarction. I. Selective segmental occlusion of intracranial arteries in the dog. Stroke 1970; 1 (4): 224-231.
68. Bell RD, Alexander GM, Nguyen T, et al. Quantification of cerebral infarct size by creatine kinase BB isoenzyme. Stroke 1986; 17 (2): 254-260.
69. Levinthal R, Moseley JI, Brown WJ, et al. Effect of STA-MCA anastomosis on the course of experimental acute MCA embolic occlusion. Stroke 1979; 10 (4): 371-375.
70. Dujovny M, Osgood CP, Barrionuevo PJ, et al. Middle cerebral artery microneurosurgical embolectomy. Surgery 1976; 80 (3): 336-339.
71. Laha RK, Israeli J, Dujovny M, et al. Low molecular weight dextran in experimental embolectomy. Stroke 1980; 11 (1): 59-63.
72. Suzuki T, Kazui T, Yamamoto S, et al. Effect of prophylactically administered edaravone during antegrade cerebral perfusion in a canine model of old cerebral infarction. J Thorac Cardiovasc Surg 2007; 133 (3): 710-716.
73. Purdy PD, Horowitz MB, Mathews D, et al. Calcium 45 autoradiography and dualisotope single-photon emission CT in a canine model of cerebral ischemia and middle cerebral artery occlusion. AJNR Am J Neuroradiol 1996; 17 (6): 1161-1170.
74. Asari S, Kinugasa K, Fujisawa H, et al. Extracranial-intracranial bypass in experimental cerebral infarction in dogs. Stroke 1978; 9 (5): 461-464.
75. Lawner PM, Laurent JP, Simeone FA, et al. Hemodynamic and clinicopathologic verification of a stroke model in the dog. Stroke 1981; 12 (3): 313-316.
76. Lawner PM, Laurent JP, Simeone FA, et al. Effect of extracranial-intracranial bypass and pentobarbital on acute stroke in dogs. J Neurosurg 1982; 56 (1): 92-96.
77. Seki H, Yoshimoto T, Ogawa A, et al. Hemodynamics in hemorrhagic infarction—an experimental study. Stroke 1985; 16 (4): 647-651.
78. Suzuki J, Tanaka S, Yoshimoto T. Suppression of brain swelling with mannitol and perfluorochemicals. An experimental study. Acta Neurochir (Wien) 1981; 58 (3-4): 149-160.
79. Shaibani A, Khawar S, Shin W, et al. First results in an MR imaging—compatible canine model of acute stroke. AJNR Am J Neuroradiol 2006; 27 (8): 1788-1793.
80. Levy EI, Sauvageau E, Hanel RA, et al. Self-expanding versus balloon-mounted stents for vessel recanalization following embolic occlusion in the canine model: technical feasibility study. AJNR Am J Neuroradiol 2006; 27 (10): 2069-2072.
81. Qureshi AI, Boulos AS, Hanel RA, et al. Randomized comparison of intra-arterial and intravenous thrombolysis in a canine model of acute basilar artery thrombosis. Neuroradiol 2004; 46 (12): 988-995.
82. Osterman FA, Bell WR, Montali RJ, et al. Natural history of autologous blood clot embolization in swine. Invest Radiol 1976; 11 (4): 267-276.
83. Imai H, Konno K, Nakamura M, et al. A new model of focal cerebral ischemia in the miniature pig. J Neurosurg 2006; 104 (2 suppl): 123-132.
84. Zhang L, Cheng H, Shi J, et al. Focal epidural cooling reduces the infarction volume of permanent middle cerebral artery occlusion in swine. Surg Neurol 2007; 67 (2): 117-121.
85. Rohl L, Sakoh M, Simonsen CZ, et al. Time evolution of cerebral perfusion and apparent diffusion coefficient measured by magnetic resonance imaging in a porcine stroke model. J Magn Reson Imaging 2002; 15 (2): 123-129.
86. Sakoh M, Gjedde A. Neuroprotection in hypothermia linked to redistribution of oxygen in brain. Am J Physiol Heart Circ Physiol 2003; 285 (1): H17-H25.
87. Sakoh M, Ohnishi T, Ostergaard L, et al. Prediction of tissue survival after stroke based on changes in the apparent diffusion of water (cytotoxic edema). Acta Neurochir Suppl 2003; 86: 137-140.
88. Sakoh M, Ostergaard L, Gjedde A, et al. Prediction of tissue survival after middle cerebral artery occlusion based on changes in the apparent diffusion of water. J Neurosurg 2001; 95 (3): 450-458.
89. Sakoh M, Ostergaard L, Røhl L, et al. Relationship between residual cerebral blood flow and oxygen metabolism as predictive of ischemic tissue viability: sequential multitracer positron emission tomography scanning of middle cerebral artery occlusion during the critical first 6 hours after stroke in pigs. J Neurosurg 2000; 93 (4): 647-657.
90. Culp WC, Porter TR, Lowery J, et al. Intracranial clot lysis with intravenous microbubbles and transcranial ultrasound in swine. Stroke 2004; 35 (10): 2407-2411.
91. Gralla J, Schroth G, Remonda L, et al. Mechanical thrombectomy for acute ischemic stroke: thrombus-device interaction, efficiency, and complications in vivo. Stroke 2006; 37 (12): 3019-3024.
92. Gralla J, Burkhardt M, Schroth G, et al. Occlusion length is a crucial determinant of efficiency and complication rate in thrombectomy for acute ischemic stroke. AJNR Am J Neuroradiol 2008; Epub ahead of print: 1-6.
93. Kuluz JW, Prado R, He D, et al. New pediatric model of ischemic stroke in infant piglets by photothrombosis: acute changes in cerebral blood flow, microvasculature, and early histopathology. Stroke 2007; 38 (6): 1932-1937.
94. Tanaka Y, Imai H, Konno K, et al. Experimental model of lacunar infarction in the gyrencephalic brain of the miniature pig: neurological assessment and histological, immunohistochemical, and physiological evaluation of dynamic corticospinal tract deformation. Stroke 2008; 39 (1): 205-212.
95. Zhang A, Altura BT, Altura BM. Ethanol-induced contraction of cerebral arteries in diverse mammals and its mechanism of action. Eur J Pharmacol 1993; 248 (3): 229-236.
96. Dirnagl U. Bench to bedside: the quest for quality in experimental stroke research. J Cereb Blood Flow Metab 2006; 26 (12): 1465-1478.
97. Fisher M, Tatlisumak T. Use of animal models has not contributed to development of acute stroke therapies: con. Stroke 2005; 36 (10): 2324-2325.
98. Kaste M. Use of animal models has not contributed to development of acute stroke therapies: pro. Stroke 2005; 36 (10): 2323-2324.