Are Underlying Assumptions of Current Animal Models of Human Stroke Correct: From STAIRs to High Hurdles?

Translational Stroke Research

Volumn 2, Issue 2, 2011, Pages 138-143

  Turner, Renée J ^a,b,c   Jickling, Glen C ^a,b   Sharp, Frank R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Animal models; Cerebral ischemia; Neuroprotection; Rabbit; Stroke; Tissue plasminogen activator

Indexed keywords

TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ATHEROSCLEROSIS; BLOOD CLOT; CONTROLLED STUDY; DEATH; DRUG EFFICACY; HUMAN; IMMUNE SYSTEM; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RABBIT; REVIEW; STROKE;

EID: 79955725794     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-011-0067-3     Document Type: Review

References (76)

1. Diener HC, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, et al. NXY-059 for the treatment of acute stroke: pooled analysis of the SAINT I and II Trials. Stroke. 2008; 39: 1751-8.
2. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, et al. NXY-059 for the treatment of acute ischemic stroke. N Engl J Med. 2007; 357: 562-71.
3. Fisher M. Recommendations for advancing development of acute stroke therapies: Stroke Therapy Academic Industry Roundtable 3. Stroke. 2003; 34: 1539-46.
4. Fisher M, Albers GW, Donnan GA, Furlan AJ, Grotta JC, Kidwell CS, et al. Enhancing the development and approval of acute stroke therapies: Stroke Therapy Academic Industry Roundtable. Stroke. 2005; 36: 1808-13.
5. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI, et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009; 40: 2244-50.
6. Fisher M, Hanley DF, Howard G, Jauch EC, Warach S. Recommendations from the STAIR V meeting on acute stroke trials, technology and outcomes. Stroke. 2007; 38: 245-8.
7. Saver JL, Albers GW, Dunn B, Johnston KC, Fisher M. Stroke Therapy Academic Industry Roundtable (STAIR) recommendations for extended window acute stroke therapy trials. Stroke. 2009; 40: 2594-600.
8. STAIR. Recommendations for clinical trial evaluation of acute stroke therapies. Stroke. 2001; 32: 1598-606.
9. Dirnagl U. Bench to bedside: the quest for quality in experimental stroke research. J Cereb Blood Flow Metab. 2006; 26: 1465-78.
10. Endres M, Engelhardt B, Koistinaho J, Lindvall O, Meairs S, Mohr JP, et al. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc Dis. 2008; 25: 268-78.
11. Ginsberg MD, Busto R. Rodent models of cerebral ischemia. Stroke. 1989; 20: 1627-42.
12. Lang JT, McCullough LD. Pathways to ischemic neuronal cell death: are sex differences relevant? J Transl Med. 2008; 6: 33.
13. Herson PS, Koerner IP, Hurn PD. Sex, sex steroids, and brain injury. Semin Reprod Med. 2009; 27: 229-39.
14. Howells DW, Porritt MJ, Rewell SS, O'Collins V, Sena ES, van der Worp HB, et al. Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia. J Cereb Blood Flow Metab. 2010; 30: 1412-31.
15. Liu S, Zhen G, Meloni BP, Campbell K, Winn HR. Rodent Stroke Model Guidelines for Preclinical Stroke Trials (1st Edition). J Exp Stroke Transl Med. 2009; 2: 2-27.
16. Lo EH. Experimental models, neurovascular mechanisms and translational issues in stroke research. Br J Pharmacol. 2008; 153 Suppl 1: S396-405.
17. Macleod MR, Fisher M, O'Collins V, Sena ES, Dirnagl U, Bath PM, et al. Reprint: good laboratory practice: preventing introduction of bias at the bench. J Cereb Blood Flow Metab. 2009; 29: 221-3.
18. Savitz SI. A critical appraisal of the NXY-059 neuroprotection studies for acute stroke: a need for more rigorous testing of neuroprotective agents in animal models of stroke. Exp Neurol. 2007; 205: 20-5.
19. Sena ES, van der Worp HB, Bath PM, Howells DW, Macleod MR. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol. 2010; 8: e1000344.
20. Willing AE. Experimental models: help or hindrance. Stroke. 2009; 40: S152-4.
21. Zivin JA, Fisher M, DeGirolami U, Hemenway CC, Stashak JA. Tissue plasminogen activator reduces neurological damage after cerebral embolism. Science. 1985; 230: 1289-92.
22. NINDS. 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: 1581-7.
23. Busch E, Kruger K, Allegrini PR, Kerskens CM, Gyngell ML, Hoehn-Berlage M, et al. Reperfusion after thrombolytic therapy of embolic stroke in the rat: magnetic resonance and biochemical imaging. J Cereb Blood Flow Metab. 1998; 18: 407-18.
24. Jiang Q, Zhang RL, Zhang ZG, Ewing JR, Divine GW, Chopp M. Diffusion-, T2-, and perfusion-weighted nuclear magnetic resonance imaging of middle cerebral artery embolic stroke and recombinant tissue plasminogen activator intervention in the rat. J Cereb Blood Flow Metab. 1998; 18: 758-67.
25. Papadopoulos SM, Chandler WF, Salamat MS, Topol EJ, Sackellares JC. Recombinant human tissue-type plasminogen activator therapy in acute thromboembolic stroke. J Neurosurg. 1987; 67: 394-8.
26. Asahi M, Asahi K, Wang X, Lo EH. Reduction of tissue plasminogen activator-induced hemorrhage and brain injury by free radical spin trapping after embolic focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 2000; 20: 452-7.
27. Kano T, Harada T, Katayama Y. Attenuation of extravasation of tissue plasminogen activator by the free radical scavenger, edaravone: evaluation in a rat thromboembolic stroke model. Neurol Res. 2005; 27: 499-502.
28. Kano T, Katayama Y, Tejima E, Lo EH. Hemorrhagic transformation after fibrinolytic therapy with tissue plasminogen activator in a rat thromboembolic model of stroke. Brain Res. 2000; 854: 245-8.
29. Overgaard K, Sereghy T, Pedersen H, Boysen G. Effect of delayed thrombolysis with rt-PA in a rat embolic stroke model. J Cereb Blood Flow Metab. 1994; 14: 472-7.
30. Zhang L, Zhang ZG, Zhang RL, Lu M, Adams J, Elliott PJ, et al. Postischemic (6-Hour) treatment with recombinant human tissue plasminogen activator and proteasome inhibitor PS-519 reduces infarction in a rat model of embolic focal cerebral ischemia. Stroke. 2001; 32: 2926-31.
31. Chehrazi BB, Seibert JA, Kissel P, Hein L, Brock JM. Evaluation of recombinant tissue plasminogen activator in embolic stroke. Neurosurgery. 1989; 24: 355-60.
32. Phillips DA, Davis MA, Fisher M. Selective embolization and clot dissolution with tPA in the internal carotid artery circulation of the rabbit. AJNR Am J Neuroradiol. 1988; 9: 899-902.
33. Phillips DA, Fisher M, Smith TW, Davis MA. The safety and angiographic efficacy of tissue plasminogen activator in a cerebral embolization model. Ann Neurol. 1988; 23: 391-4.
34. Sicard KM, Fisher M. Animal models of focal brain ischemia. Exp Transl Stroke Med. 2009; 1: 7.
35. Savitz SI, Fisher M. Future of neuroprotection for acute stroke: in the aftermath of the SAINT trials. Ann Neurol. 2007; 61: 396-402.
36. Kudo M, Aoyama A, Ichimori S, Fukunaga N. An animal model of cerebral infarction. Homologous blood clot emboli in rats. Stroke. 1982; 13: 505-8.
37. Meng W, Wang X, Asahi M, Kano T, Asahi K, Ackerman RH, et al. Effects of tissue type plasminogen activator in embolic versus mechanical models of focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 1999; 19: 1316-21.
38. Zhang RL, Zhang L, Jiang Q, Zhang ZG, Goussev A, Chopp M. Postischemic intracarotid treatment with TNK-tPA reduces infarct volume and improves neurological deficits in embolic stroke in the unanesthetized rat. Brain Res. 2000; 878: 64-71.
39. Elkind MS, Sacco RL. Stroke risk factors and stroke prevention. Semin Neurol. 1998; 18: 429-40.
40. Sacco RL. Newer risk factors for stroke. Neurology. 2001; 57: S31-4.
41. Dornas WC, Oliveira TT, Augusto LE, Nagem TJ. Experimental atherosclerosis in rabbits. Arq Bras Cardiol. 2010; 95: 272-8.
42. Moghadasian MH, Frohlich JJ, McManus BM. Advances in experimental dyslipidemia and atherosclerosis. Lab Invest. 2001; 81: 1173-83.
43. Yanni AE. The laboratory rabbit: an animal model of atherosclerosis research. Lab Anim. 2004; 38: 246-56.
44. Daugherty A, Lu H, Howatt DA, Rateri DL. Modes of defining atherosclerosis in mouse models: relative merits and evolving standards. Methods Mol Biol. 2009; 573: 1-15.
45. Russell JC, Proctor SD. Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis. Cardiovasc Pathol. 2006; 15: 318-30.
46. Verbeuren TJ. Experimental models of thrombosis and atherosclerosis. Therapie. 2006; 61: 379-87.
47. Hayashi T, Kamada H, Jin G, Deguchi K, Nagotani S, Sehara Y, et al. Different expression of low density lipoprotein receptor and ApoE between young adult and old rat brains after ischemia. Neurol Res. 2006; 28: 822-5.
48. Mostaza JM, Martin-Jadraque R, Vicente I, San Martin MA, Lahoz C. Patients at high risk of cerebrovascular disease: the REACH study. Cerebrovasc Dis. 2009; 27 Suppl 1: 77-81.
49. Qureshi AI, Taylor RA. Research priorities for intracranial atherosclerotic diseases. J Neuroimaging. 2009; 19 Suppl 1: 39S-42S.
50. Zhang GY, Chen ZQ, Ling F, Li YJ, Wang Y, Gu BX. Establishment of a novel hemodynamic cerebral ischemia model of atherosclerotic rabbit. Neurol India. 2010; 58: 191-4.
51. Jordan J, Segura T, Brea D, Galindo MF, Castillo J. Inflammation as therapeutic objective in stroke. Curr Pharm Des. 2008; 14: 3549-64.
52. Tanasescu R, Nicolau A, Ticmeanu M, Luca D, Caraiola S, Cojocaru IM, et al. An immunological approach to cerebral ischemia (I). Immune cells and adhesion molecules. Rom J Intern Med. 2008; 46: 3-8.
53. Tuttolomondo A, Di Sciacca R, Di Raimondo D, Renda C, Pinto A, Licata G. Inflammation as a therapeutic target in acute ischemic stroke treatment. Curr Top Med Chem. 2009; 9: 1240-60.
54. Enlimomab. Use of anti-ICAM-1 therapy in ischemic stroke: results of the Enlimomab Acute Stroke Trial. Neurology. 2001; 57: 1428-34.
55. Furuya K, Takeda H, Azhar S, McCarron RM, Chen Y, Ruetzler CA, et al. Examination of several potential mechanisms for the negative outcome in a clinical stroke trial of enlimomab, a murine anti-human intercellular adhesion molecule-1 antibody: a bedside-to-bench study. Stroke. 2001; 32: 2665-74.
56. Shah IM, Macrae IM, Di Napoli M. Neuroinflammation and neuroprotective strategies in acute ischaemic stroke-from bench to bedside. Curr Mol Med. 2009; 9: 336-54.
57. Fauci AS, Braunwald E, Kasper DL, Hauser SL, Longo DL, Jameson JL, et al. Laboratory Values of Clinical Importance. 2009.
58. Fox JG, Anderson LC, Leow FM, Quimby FW. Laboratory Animal Medicine. Academic Press; 2002.
59. Jickling GC, Xu H, Stamova B, Ander BP, Zhan X, Tian Y, et al. Signatures of cardioembolic and large-vessel ischemic stroke. Ann Neurol. 2010; 68: 681-92.
60. Moore DF, Li H, Jeffries N, Wright V, Cooper Jr RA, Elkahloun A, et al. Using peripheral blood mononuclear cells to determine a gene expression profile of acute ischemic stroke: a pilot investigation. Circulation. 2005; 111: 212-21.
61. Stamova B, Xu H, Jickling G, Bushnell C, Tian Y, Ander BP, et al. Gene expression profiling of blood for the prediction of ischemic stroke. Stroke. 2010; 41: 2171-7.
62. Tang Y, Lu A, Aronow BJ, Sharp FR. Blood genomic responses differ after stroke, seizures, hypoglycemia, and hypoxia: blood genomic fingerprints of disease. Ann Neurol. 2001; 50: 699-707.
63. Tang Y, Xu H, Du X, Lit L, Walker W, Lu A, et al. Gene expression in blood changes rapidly in neutrophils and monocytes after ischemic stroke in humans: a microarray study. J Cereb Blood Flow Metab. 2006; 26: 1089-102.
64. Callaway JK, Knight MJ, Watkins DJ, Beart PM, Jarrott B. Delayed treatment with AM-36, a novel neuroprotective agent, reduces neuronal damage after endothelin-1-induced middle cerebral artery occlusion in conscious rats. Stroke. 1999; 30: 2704-12. discussion 2712.
65. Huang SS, Tsai SK, Chih CL, Chiang LY, Hsieh HM, Teng CM, et al. Neuroprotective effect of hexasulfobutylated C60 on rats subjected to focal cerebral ischemia. Free Radic Biol Med. 2001; 30: 643-9.
66. Sharkey J, Ritchie IM, Kelly PA. Perivascular microapplication of endothelin-1: a new model of focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab. 1993; 13: 865-71.
67. Head BP, Patel P. Anesthetics and brain protection. Curr Opin Anaesthesiol. 2007; 20: 395-9.
68. Kirsch JR, Traystman RJ, Hurn PD. Anesthetics and cerebroprotection: experimental aspects. Int Anesthesiol Clin. 1996; 34: 73-93.
69. Koerner IP, Brambrink AM. Brain protection by anesthetic agents. Curr Opin Anaesthesiol. 2006; 19: 481-6.
70. Wang L, Jing W, Hang YN. Glutamate-induced c-Jun expression in neuronal PC12 cells: the effects of ketamine and propofol. J Neurosurg Anesthesiol. 2008; 20: 124-30.
71. Gelb AW, Bayona NA, Wilson JX, Cechetto DF. Propofol anesthesia compared to awake reduces infarct size in rats. Anesthesiology. 2002; 96: 1183-90.
72. Hsia AW, Sachdev HS, Tomlinson J, Hamilton SA, Tong DC. Efficacy of IV tissue plasminogen activator in acute stroke: does stroke subtype really matter? Neurology. 2003; 61: 71-5.
73. Bailey EL, McCulloch J, Sudlow C, Wardlaw JM. Potential animal models of lacunar stroke: a systematic review. Stroke. 2009; 40: e451-8.
74. Hainsworth AH, Markus HS. Do in vivo experimental models reflect human cerebral small vessel disease? A systematic review. J Cereb Blood Flow Metab. 2008; 28: 1877-91.
75. Lapchak P. Translational stroke research using a rabbit embolic stroke model: a correlative analysis hypothesis for novel therapy development. Transl Stroke Res. 2010; 1: 96-107.
76. Wardlaw JM, Murray V, Berge E, Del Zoppo GJ. Thrombolysis for acute ischaemic stroke. Cochrane Database Syst Rev 2009: CD000213.