Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Translational Stroke Research
Published in: Translational Stroke Research 3/2013

01-06-2013 | Original Article

In Vivo Animal Stroke Models

A Rationale for Rodent and Non-Human Primate Models

Authors: Naoki Tajiri, Travis Dailey, Christopher Metcalf, Yusef I. Mosley, Tsz Lau, Meaghan Staples, Harry van Loveren, Seung U. Kim, Tetsumori Yamashima, Takao Yasuhara, Isao Date, Yuji Kaneko, Cesario V. Borlongan

Published in: Translational Stroke Research | Issue 3/2013

Login to get access

Abstract

On average, every 4 min an individual dies from a stroke, accounting for one out of every 18 deaths in the United States. Approximately 795,000 Americans have a new or recurrent stroke each year, with just over 600,000 of these being first attack Roger et al. (Circulation, 125(1): 188–197, 2012). There have been multiple animal models of stroke demonstrating that novel therapeutics can help improve the clinical outcome. However, these results have failed to show the same outcomes when tested in human clinical trials. This review will discuss the current in vivo animal models of stroke, advantages and limitations, and the rationale for employing these animal models to satisfy translational gating items for examination of neuroprotective, as well as neurorestorative strategies in stroke patients. An emphasis in the present discussion of therapeutics development is given to stem cell therapy for stroke.
Literature
1.
Roger VL, et al. Executive summary: heart disease and stroke statistics—2012 update: a report from the American Heart Association. Circulation. 2012;125(1):188–97.PubMedCrossRef
2.
Davenport R, Dennis M. Neurological emergencies: acute stroke. J Neurol Neurosurg Psychiatry. 2000;68(3):277–88.PubMedCrossRef
3.
4.
Sudlow CL, Warlow CP. Comparing stroke incidence worldwide: what makes studies comparable? Stroke. 1996;27(3):550–8.PubMedCrossRef
5.
Fagan SC, et al. Cost-effectiveness of tissue plasminogen activator for acute ischemic stroke. NINDS rt-PA Stroke Study Group. Neurology. 1998;50(4):883–90.PubMedCrossRef
6.
Hess DC, et al. REACH: clinical feasibility of a rural telestroke network. Stroke. 2005;36(9):2018–20.PubMedCrossRef
7.
Wang S, et al. Remote evaluation of acute ischemic stroke in rural community hospitals in Georgia. Stroke. 2004;35(7):1763–8.PubMedCrossRef
8.
Borlongan CV, et al. Gene therapy, cell transplantation and stroke. Front Biosci. 2006;11:1090–101.PubMedCrossRef
9.
Pulsinelli WA, Brierley JB. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke. 1979;10(3):267–72.PubMedCrossRef
10.
Eklof B, Siesjo BK. The effect of bilateral carotid artery ligation upon the blood flow and the energy state of the rat brain. Acta Physiol Scand. 1972;86(2):155–65.PubMedCrossRef
11.
Eklof B, Siesjo BK. The effect of bilateral carotid artery ligation upon acid–base parameters and substrate levels in the rat brain. Acta Physiol Scand. 1972;86(4):528–38.PubMedCrossRef
12.
13.
Longa EZ, et al. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke. 1989;20(1):84–91.PubMedCrossRef
14.
Schmid-Elsaesser R, 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):2162–70.PubMedCrossRef
15.
Tamura A, et al. Focal cerebral ischaemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab. 1981;1(1):53–60.PubMedCrossRef
16.
Duverger D, MacKenzie ET. The quantification of cerebral infarction following focal ischemia in the rat: influence of strain, arterial pressure, blood glucose concentration, and age. J Cereb Blood Flow Metab. 1988;8(4):449–61.PubMedCrossRef
17.
Watson BD, et al. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol. 1985;17(5):497–504.PubMedCrossRef
18.
Markgraf CG, et al. Comparative histopathologic consequences of photothrombotic occlusion of the distal middle cerebral artery in Sprague–Dawley and Wistar rats. Stroke. 1993;24(2):92–286. discussion 292–3.CrossRef
19.
Zhang Z, et al. A new rat model of thrombotic focal cerebral ischemia. J Cereb Blood Flow Metab. 1997;17(2):123–35.PubMedCrossRef
20.
Pulsinelli WA, Buchan AM. The four-vessel occlusion rat model: method for complete occlusion of vertebral arteries and control of collateral circulation. Stroke. 1988;19(7):913–4.PubMedCrossRef
21.
Globus MY, et al. Intra-ischemic extracellular release of dopamine and glutamate is associated with striatal vulnerability to ischemia. Neurosci Lett. 1988;91(1):36–40.PubMedCrossRef
22.
Smith ML, et al. Models for studying long-term recovery following forebrain ischemia in the rat: 2. A 2-vessel occlusion model. Acta Neurol Scand. 1984;69(6):385–401.PubMedCrossRef
23.
de Crespigny AJ, et al. Acute studies of a new primate model of reversible middle cerebral artery occlusion. J Stroke Cerebrovasc Dis. 2005;14(2):80–7.PubMedCrossRef
24.
Sasaki M, et al. Development of a middle cerebral artery occlusion model in the nonhuman primate and a safety study of i.v. infusion of human mesenchymal stem cells. PLoS One. 2011;6(10):e26577.PubMedCrossRef
25.
Fisher M, et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009;40(6):2244–50.PubMedCrossRef
26.
Shi S, Morike K, Klotz U. The clinical implications of ageing for rational drug therapy. Eur J Clin Pharmacol. 2008;64(2):183–99.PubMedCrossRef
27.
Hurn PD, Vannucci SJ, Hagberg H. Adult or perinatal brain injury: does sex matter? Stroke. 2005;36(2):193–5.PubMedCrossRef
28.
Hattiangady B, Rao MS, Shetty AK. Plasticity of hippocampal stem/progenitor cells to enhance neurogenesis in response to kainate-induced injury is lost by middle age. Aging Cell. 2008;7(2):207–24.PubMedCrossRef
29.
The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med. 1995;333(24):1581–7.
30.
Iadecola C, Davisson RL. Hypertension and cerebrovascular dysfunction. Cell Metab. 2008;7(6):476–84.PubMedCrossRef
31.
Lindner MD, et al. Long-lasting functional disabilities in middle-aged rats with small cerebral infarcts. J Neurosci. 2003;23(34):10913–22.PubMed
32.
Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol. 2006;100(1):328–35.PubMedCrossRef
33.
Fisher M. Stroke and TIA: epidemiology, risk factors, and the need for early intervention. Am J Manage Care. 2008;14(6 Suppl 2):S204–11.
34.
Rewell SS, et al. Inducing stroke in aged, hypertensive, diabetic rats. J Cereb Blood Flow Metab. 2010;30(4):729–33.PubMedCrossRef
35.
Bruno A, et al. Admission glucose level and clinical outcomes in the NINDS rt-PA Stroke Trial. Neurology. 2002;59(5):669–74.PubMedCrossRef
36.
Martini SR, Kent TA. Hyperglycemia in acute ischemic stroke: a vascular perspective. J Cereb Blood Flow Metab. 2007;27(3):435–51.PubMedCrossRef
37.
Fan X, et al. A rat model of studying tissue-type plasminogen activator thrombolysis in ischemic stroke with diabetes. Stroke. 2012;43(2):567–70.PubMedCrossRef
38.
Kim E, et al. CD36 in the periphery and brain synergizes in stroke injury in hyperlipidemia. Ann Neurol. 2012;71(6):753–64.PubMedCrossRef
39.
Xu L, et al. Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion-reperfusion in rats. BMC Neurol. 2004;4:7.PubMedCrossRef
40.
Fagan SC, et al. Optimal delivery of minocycline to the brain: implication for human studies of acute neuroprotection. Exp Neurol. 2004;186(2):248–51.PubMedCrossRef
41.
Machado LS, et al. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 2006;7:56.PubMedCrossRef
42.
Matsukawa N, et al. Therapeutic targets and limits of minocycline neuroprotection in experimental ischemic stroke. BMC Neurosci. 2009;10:126.PubMedCrossRef
43.
Romero-Perez D, et al. Cardiac uptake of minocycline and mechanisms for in vivo cardioprotection. J Am Coll Cardiol. 2008;52(13):1086–94.PubMedCrossRef
44.
Matsumoto Y, Park IK, Kohyama K. Matrix metalloproteinase (MMP)-9, but not MMP-2, is involved in the development and progression of C protein-induced myocarditis and subsequent dilated cardiomyopathy. J Immunol. 2009;183(7):4773–81.PubMedCrossRef
45.
Glover LE, et al. A step-up approach for cell therapy in stroke: translational hurdles of bone marrow-derived stem cells. Transl Stroke Res. 2012;3(1):90–8.PubMedCrossRef
46.
Busch E, Kruger K, Hossmann KA. Improved model of thromboembolic stroke and rt-PA induced reperfusion in the rat. Brain Res. 1997;778(1):16–24.PubMedCrossRef
47.
Gerriets T, 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):201–11.PubMedCrossRef
48.
Belayev L, et al. Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke. 1996;27(9):1616–22. doi:discussion_​1623.PubMedCrossRef
49.
Garcia JH, et al. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation. Stroke. 1995;26(4):627–34. doi:discussion_​635.PubMedCrossRef
50.
Kawamura S, et al. Reversible middle cerebral artery occlusion in rats using an intraluminal thread technique. Surg Neurol. 1994;41(5):368–73.PubMedCrossRef
51.
Kawamura S, et al. Rat middle cerebral artery occlusion using an intraluminal thread technique. Acta Neurochir (Wien). 1991;109(3–4):126–32.CrossRef
52.
Memezawa H, Smith ML, Siesjo BK. Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats. Stroke. 1992;23(4):552–9.PubMedCrossRef
53.
Rink C, et al. Minimally invasive neuroradiologic model of preclinical transient middle cerebral artery occlusion in canines. Proc Natl Acad Sci U S A. 2008;105(37):14100–5.PubMedCrossRef
54.
Ginsberg MD BR. Small animal models of global and focal cerebral ischemia. In: Ginsberg MD, Bogousslavsky J, editors. Cerebrovascular disease: pathophysiology, diagnosis and management. Malden, MA: Blackwell Scientific Publications; 1998.
55.
van der Worp HB, et al. Can animal models of disease reliably inform human studies? PLoS Med. 2010;7(3):e1000245.PubMedCrossRef
56.
Lees JS, et al. Stem cell-based therapy for experimental stroke: a systematic review and meta-analysis. Int J Stroke. 2012;7(7):582–8.PubMedCrossRef
57.
Toda H, et al. Grafting neural stem cells improved the impaired spatial recognition in ischemic rats. Neurosci Lett. 2001;316(1):9–12.PubMedCrossRef
58.
Ferrari A, et al. Immature human NT2 cells grafted into mouse brain differentiate into neuronal and glial cell types. FEBS Lett. 2000;486(2):121–5.PubMedCrossRef
59.
Borlongan CV, et al. Transplantation of cryopreserved human embryonal carcinoma-derived neurons (NT2N cells) promotes functional recovery in ischemic rats. Exp Neurol. 1998;149(2):310–21.PubMedCrossRef
60.
Veizovic T, et al. Resolution of stroke deficits following contralateral grafts of conditionally immortal neuroepithelial stem cells. Stroke. 2001;32(4):1012–9.PubMedCrossRef
61.
Modo M, et al. Neurological sequelae and long-term behavioural assessment of rats with transient middle cerebral artery occlusion. J Neurosci Methods. 2000;104(1):99–109.PubMedCrossRef
62.
Englund U, et al. Grafted neural stem cells develop into functional pyramidal neurons and integrate into host cortical circuitry. Proc Natl Acad Sci U S A. 2002;99(26):17089–94.PubMedCrossRef
63.
Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A. 1999;96(19):10711–6.PubMedCrossRef
64.
Chen J, Li Y, Chopp M. Intracerebral transplantation of bone marrow with BDNF after MCAo in rat. Neuropharmacology. 2000;39(5):711–6.PubMedCrossRef
65.
Li Y, et al. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab. 2000;20(9):1311–9.PubMedCrossRef
66.
Woodbury D, et al. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000;61(4):364–70.PubMedCrossRef
67.
Munoz-Elias G, et al. Adult bone marrow stromal cells in the embryonic brain: engraftment, migration, differentiation, and long-term survival. J Neurosci. 2004;24(19):4585–95.PubMedCrossRef
68.
Borlongan CV, et al. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke. 2004;35(10):2385–9.PubMedCrossRef
69.
Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A. 1997;94(8):4080–5.PubMedCrossRef
70.
Hess DC, et al. Bone marrow as a source of endothelial cells and NeuN-expressing cells After stroke. Stroke. 2002;33(5):1362–8.PubMedCrossRef
71.
Li Y, et al. Treatment of stroke in rat with intracarotid administration of marrow stromal cells. Neurology. 2001;56(12):1666–72.PubMedCrossRef
72.
Chen J, et al. Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ Res. 2003;92(6):692–9.PubMedCrossRef
73.
Chen J, et al. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke. 2001;32(11):2682–8.PubMedCrossRef
74.
Willing AE, et al. Intravenous versus intrastriatal cord blood administration in a rodent model of stroke. J Neurosci Res. 2003;73(3):296–307.PubMedCrossRef
75.
Riess P, et al. Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery. 2002;51(4):1043–52. discussion 1052–4.PubMed
76.
Zhao LR, et al. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol. 2002;174(1):11–20.PubMedCrossRef
77.
Peled A, et al. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood. 2000;95(11):3289–96.PubMed
78.
Yamaguchi J, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation. 2003;107(9):1322–8.PubMedCrossRef
79.
Reyes M, et al. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest. 2002;109(3):337–46.PubMed
80.
Rajantie I, et al. Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood. 2004;104(7):2084–6.PubMedCrossRef
81.
Mahmood A, Lu D, Chopp M. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma. 2004;21(1):33–9.PubMedCrossRef
82.
Stroke Therapy Academic Industry Roundtable (STAIR). Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke. 1999;30(12):2752–8.
83.
Fukuda S, del Zoppo GJ. Models of focal cerebral ischemia in the nonhuman primate. ILAR J. 2003;44(2):96–104.PubMedCrossRef
84.
Neubuerger KT. Lesions of the human brain following circulatory arrest. J Neuropathol Exp Neurol. 1954;13(1):144–60.PubMedCrossRef
85.
Brierley JB, et al. Brain damage in the rhesus monkey resulting from profound arterial hypotension: I. Its nature, distribution and general physiological correlates. Brain Res. 1969;13(1):68–100.PubMedCrossRef
86.
87.
Wolin LR, Massopust Jr LC, Taslitz N. Tolerance to arrest of cerebral circulation in the rhesus monkey. Exp Neurol. 1971;30(1):103–15.PubMedCrossRef
88.
Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol. 1982;11(5):491–8.PubMedCrossRef
89.
Smith ML, Auer RN, Siesjo BK. The density and distribution of ischemic brain injury in the rat following 2–10 min of forebrain ischemia. Acta Neuropathol. 1984;64(4):319–32.PubMedCrossRef
90.
Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 1982;239(1):57–69.PubMedCrossRef
91.
Zola-Morgan S, Squire LR, Amaral DG. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci. 1986;6(10):2950–67.PubMed
92.
Rempel-Clower NL, et al. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci. 1996;16(16):5233–55.PubMed
93.
Petito CK, Lapinski RL. Postischemic alterations in ultrastructural cytochemistry of neuronal Golgi apparatus. Lab Investig. 1986;55(6):696–702.PubMed
94.
Fujioka M, et al. Hippocampal damage in the human brain after cardiac arrest. Cerebrovasc Dis. 2000;10(1):2–7.PubMedCrossRef
95.
Zola-Morgan S, et al. Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci. 1992;12(7):2582–96.PubMed
96.
Tabuchi E, et al. Hippocampal neuronal damage after transient forebrain ischemia in monkeys. Brain Res Bull. 1992;29(5):685–90.PubMedCrossRef
97.
Tabuchi E, et al. Ischemic neuronal damage specific to monkey hippocampus: histological investigation. Brain Res Bull. 1995;37(1):73–87.PubMedCrossRef
98.
Yamashima T. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog Neurobiol. 2000;62(3):273–95.PubMedCrossRef
99.
Yamashima T, et al. Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis'. Eur J Neurosci. 1998;10(5):1723–33.PubMedCrossRef
100.
Yamashima T, et al. Transient brain ischaemia provokes Ca2+, PIP2 and calpain responses prior to delayed neuronal death in monkeys. Eur J Neurosci. 1996;8(9):1932–44.PubMedCrossRef
101.
Yamashima T, et al. Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus. 2003;13(7):791–800.PubMedCrossRef
102.
Frykholm P, et al. Relationship between cerebral blood flow and oxygen metabolism, and extracellular glucose and lactate concentrations during middle cerebral artery occlusion and reperfusion: a microdialysis and positron emission tomography study in nonhuman primates. J Neurosurg. 2005;102(6):1076–84.PubMedCrossRef
103.
Nemoto EM, et al. Hyperthermia and hypermetabolism in focal cerebral ischemia. Adv Exp Med Biol. 2005;566:83–9.PubMedCrossRef
104.
Schmahmann JD, Rosene DL, Pandya DN. Ataxia after pontine stroke: insights from pontocerebellar fibers in monkey. Ann Neurol. 2004;55(4):585–9.PubMedCrossRef
105.
Vaitkevicius PV, et al. A cross-link breaker has sustained effects on arterial and ventricular properties in older rhesus monkeys. Proc Natl Acad Sci U S A. 2001;98(3):1171–5.PubMedCrossRef
106.
Tsukada T, Watanabe M, Yamashima T. Implications of CAD and DNase II in ischemic neuronal necrosis specific for the primate hippocampus. J Neurochem. 2001;79(6):1196–206.PubMedCrossRef
107.
Hara K, et al. Hippocampal CA1 cell loss in a non-human primate model of transient global ischemia: a pilot study. Brain Res Bull. 2007;74(1–3):164–71.PubMedCrossRef
108.
Nudo RJ, et al. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science. 1996;272(5269):1791–4.PubMedCrossRef
109.
Branston NM, et al. Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon. Exp Neurol. 1974;45(2):195–208.PubMedCrossRef
110.
Roitberg B, et al. Chronic ischemic stroke model in cynomolgus monkeys: behavioral, neuroimaging and anatomical study. Neurol Res. 2003;25(1):68–78.PubMedCrossRef
111.
112.
Del Zoppo GJ, et al. Experimental acute thrombotic stroke in baboons. Stroke. 1986;17(6):1254–65.PubMedCrossRef
113.
Marshall JW, Ridley RM. Assessment of cognitive and motor deficits in a marmoset model of stroke. ILAR J. 2003;44(2):153–60.PubMedCrossRef
114.
Yukie M, Yamaguchi K, Yamashima T. Impairments in recognition memory for object and for location after transient brain ischemia in monkeys. Rev Neurosci. 2006;17(1–2):201–14.PubMed
115.
Yoshida M, et al. Primate neurons show different vulnerability to transient ischemia and response to cathepsin inhibition. Acta Neuropathol. 2002;104(3):267–72.PubMed
116.
Borlongan CV. Cell therapy for stroke: remaining issues to address before embarking on clinical trials. Stroke. 2009;40(3 Suppl):S146–8.PubMedCrossRef
117.
Wechsler L, Steindler D, Borlongan C, Chopp M, et al. Stem Cell Therapies as an Emerging Paradigm in Stroke (STEPS): bridging basic and clinical science for cellular and neurogenic factor therapy in treating stroke. Stroke. 2009;40(2):510–5.
118.
Chopp M, et al. Who's in favor of translational cell therapy for stroke: STEPS forward please? Cell Transplant. 2009;18(7):691–3.PubMedCrossRef
119.
Borlongan CV, et al. Potential of stem/progenitor cells in treating stroke: the missing steps in translating cell therapy from laboratory to clinic. Regen Med. 2008;3(3):249–50.PubMedCrossRef
120.
121.
Crowell RM, et al. Temporary occlusion of the middle cerebral artery in the monkey: clinical and pathological observations. Stroke. 1970;1(6):439–48.
122.
Molinari GF, Moseley JI, Laurent JP. Segmental middle cerebral artery occlusion in primates: an experimental method requiring minimal surgery and anesthesia. Stroke. 1974;5(3):334–9.
123.
Symon L. Experimental model of stroke in the baboon. Adv Neurol. 1975;10:199–212.
124.
Spetzler RF, Selman WR. New design for an implantable vessel occluder. Surg Neurol. 1980;13(4):317–9.
125.
Crowell RM, Marcoux FW, DeGirolami U. Variability and reversibility of focal cerebral ischemia in unanesthetized monkeys. Neurology. 1981;31(10):1295–1302.
126.
Yonas H, et al. Stable xenon-enhanced CT measurement of cerebral blood flow in reversible focal ischemia in baboons. J Neurosurg. 1990;73(2):266–73.
Metadata
Title
In Vivo Animal Stroke Models
A Rationale for Rodent and Non-Human Primate Models
Authors
Naoki Tajiri
Travis Dailey
Christopher Metcalf
Yusef I. Mosley
Tsz Lau
Meaghan Staples
Harry van Loveren
Seung U. Kim
Tetsumori Yamashima
Takao Yasuhara
Isao Date
Yuji Kaneko
Cesario V. Borlongan
Publication date
01-06-2013
Publisher
Springer-Verlag
Published in
Translational Stroke Research / Issue 3/2013
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-012-0241-2

Other articles of this Issue 3/2013

Translational Stroke Research 3/2013 Go to the issue

Original Article

Distal Occlusion of the Middle Cerebral Artery in Mice: Are We Ready to Assess Long-Term Functional Outcome?

Special Report

RIGOR Guidelines: Escalating STAIR and STEPS for Effective Translational Research

BRIEF COMMUNICATIONS

Polymorphisms in ACVRL1 and Endoglin Genes are Not Associated with Sporadic and HHT-Related Brain AVMs in Dutch Patients

Original Article

Recommendations for Preclinical Research in Hemorrhagic Transformation

Original Article

SAHIT Investigators—on the Outcome of Some Subarachnoid Hemorrhage Clinical Trials

Original Article

Suppression of the Rho/Rho-Kinase Pathway and Prevention of Cerebral Vasospasm by Combination Treatment with Statin and Fasudil After Subarachnoid Hemorrhage in Rabbit