Skip to main content
Top
Published in: Experimental & Translational Stroke Medicine 1/2011

Open Access 01-12-2011 | Letter to the Editor

On the importance of long-term functional assessment after stroke to improve translation from bench to bedside

Authors: Thomas Freret, Pascale Schumann-Bard, Michel Boulouard, Valentine Bouet

Published in: Experimental & Translational Stroke Medicine | Issue 1/2011

Login to get access

Abstract

Despite extensive research efforts in the field of cerebral ischemia, numerous disappointments came from the translational step. Even if experimental studies showed a large number of promising drugs, most of them failed to be efficient in clinical trials. Based on these reports, factors that play a significant role in causing outcome differences between animal experiments and clinical trials have been identified; and latest works in the field have tried to discard them in order to improve the scope of the results. Nevertheless, efforts must be maintained, especially for long-term functional evaluations. As observed in clinical practice, animals display a large degree of spontaneous recovery after stroke. The neurological impairment, assessed by basic items, typically disappears during the firsts week following stroke in rodents. On the contrary, more demanding sensorimotor and cognitive tasks underline other deficits, which are usually long-lasting. Unfortunately, studies addressing such behavioral impairments are less abundant. Because the characterization of long-term functional recovery is critical for evaluating the efficacy of potential therapeutic agents in experimental strokes, behavioral tests that proved sensitive enough to detect long-term deficits are reported here. And since the ultimate goal of any stroke therapy is the restoration of normal function, an objective appraisal of the behavioral deficits should be done.
Literature
1.
go back to reference Virtanen T, Jolkkonen J, Sivenius J: Re: External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. Stroke 2004, 35: e9–10. author reply e9–10PubMedCrossRef Virtanen T, Jolkkonen J, Sivenius J: Re: External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. Stroke 2004, 35: e9–10. author reply e9–10PubMedCrossRef
2.
go back to reference Dittmar M, Spruss T, Schuierer G, Horn M: External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. Stroke 2003, 34: 2252–7. 10.1161/01.STR.0000083625.54851.9APubMedCrossRef Dittmar M, Spruss T, Schuierer G, Horn M: External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. Stroke 2003, 34: 2252–7. 10.1161/01.STR.0000083625.54851.9APubMedCrossRef
3.
go back to reference Tamura A, Graham DI, McCulloch J, Teasdale GM: 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: 53–60. 10.1038/jcbfm.1981.6PubMedCrossRef Tamura A, Graham DI, McCulloch J, Teasdale GM: 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: 53–60. 10.1038/jcbfm.1981.6PubMedCrossRef
4.
go back to reference Jonsson AC, Lindgren I, Norrving B, Lindgren A: Weight loss after stroke: a population-based study from the Lund Stroke Register. Stroke 2008, 918–23. Jonsson AC, Lindgren I, Norrving B, Lindgren A: Weight loss after stroke: a population-based study from the Lund Stroke Register. Stroke 2008, 918–23.
5.
go back to reference Wahlgren NG, Ahmed N: Neuroprotection in cerebral ischaemia: facts and fancies--the need for new approaches. Cerebrovasc Dis 2004,17(Suppl 1):153–66.PubMedCrossRef Wahlgren NG, Ahmed N: Neuroprotection in cerebral ischaemia: facts and fancies--the need for new approaches. Cerebrovasc Dis 2004,17(Suppl 1):153–66.PubMedCrossRef
6.
go back to reference Green AR: Why do neuroprotective drugs that are so promising in animals fail in the clinic? An industry perspective. Clin Exp Pharmacol Physiol 2002, 29: 1030–4. 10.1046/j.1440-1681.2002.03767.xPubMedCrossRef Green AR: Why do neuroprotective drugs that are so promising in animals fail in the clinic? An industry perspective. Clin Exp Pharmacol Physiol 2002, 29: 1030–4. 10.1046/j.1440-1681.2002.03767.xPubMedCrossRef
7.
go back to reference 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. 10.1161/01.STR.0000255951.37434.aaPubMedCrossRef 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. 10.1161/01.STR.0000255951.37434.aaPubMedCrossRef
8.
go back to reference Rothrock JF, Clark WM, Lyden PD: Spontaneous early improvement following ischemic stroke. Stroke 1995, 26: 1358–60. 10.1161/01.STR.26.8.1358PubMedCrossRef Rothrock JF, Clark WM, Lyden PD: Spontaneous early improvement following ischemic stroke. Stroke 1995, 26: 1358–60. 10.1161/01.STR.26.8.1358PubMedCrossRef
9.
go back to reference Hunter AJ, Mackay KB, Rogers DC: To what extent have functional studies of ischaemia in animals been useful in the assessment of potential neuroprotective agents? Trends Pharmacol Sci 1998, 19: 59–66. 10.1016/S0165-6147(97)01157-7PubMedCrossRef Hunter AJ, Mackay KB, Rogers DC: To what extent have functional studies of ischaemia in animals been useful in the assessment of potential neuroprotective agents? Trends Pharmacol Sci 1998, 19: 59–66. 10.1016/S0165-6147(97)01157-7PubMedCrossRef
10.
go back to reference Roof RL, Schielke GP, Ren X, Hall ED: A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke 2001, 32: 2648–57. 10.1161/hs1101.097397PubMedCrossRef Roof RL, Schielke GP, Ren X, Hall ED: A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke 2001, 32: 2648–57. 10.1161/hs1101.097397PubMedCrossRef
11.
go back to reference Zausinger S, Hungerhuber E, Baethmann A, Reulen H, Schmid-Elsaesser R: Neurological impairment in rats after transient middle cerebral artery occlusion: a comparative study under various treatment paradigms. Brain Res 2000, 863: 94–105. 10.1016/S0006-8993(00)02100-4PubMedCrossRef Zausinger S, Hungerhuber E, Baethmann A, Reulen H, Schmid-Elsaesser R: Neurological impairment in rats after transient middle cerebral artery occlusion: a comparative study under various treatment paradigms. Brain Res 2000, 863: 94–105. 10.1016/S0006-8993(00)02100-4PubMedCrossRef
12.
go back to reference Zhang L, Chen J, Li Y, Zhang ZG, Chopp M: Quantitative measurement of motor and somatosensory impairments after mild (30 min) and severe (2 h) transient middle cerebral artery occlusion in rats. J Neurol Sci 2000, 174: 141–6. 10.1016/S0022-510X(00)00268-9PubMedCrossRef Zhang L, Chen J, Li Y, Zhang ZG, Chopp M: Quantitative measurement of motor and somatosensory impairments after mild (30 min) and severe (2 h) transient middle cerebral artery occlusion in rats. J Neurol Sci 2000, 174: 141–6. 10.1016/S0022-510X(00)00268-9PubMedCrossRef
13.
go back to reference Valtysson J, Hillered L, Andine P, Hagberg H, Persson L: Neuropathological endpoints in experimental stroke pharmacotherapy: the importance of both early and late evaluation. Acta Neurochir (Wien) 1994, 129: 58–63. 10.1007/BF01400874CrossRef Valtysson J, Hillered L, Andine P, Hagberg H, Persson L: Neuropathological endpoints in experimental stroke pharmacotherapy: the importance of both early and late evaluation. Acta Neurochir (Wien) 1994, 129: 58–63. 10.1007/BF01400874CrossRef
14.
go back to reference Corbett D, Nurse S: The problem of assessing effective neuroprotection in experimental cerebral ischemia. Prog Neurobiol 1998, 54: 531–48. 10.1016/S0301-0082(97)00078-6PubMedCrossRef Corbett D, Nurse S: The problem of assessing effective neuroprotection in experimental cerebral ischemia. Prog Neurobiol 1998, 54: 531–48. 10.1016/S0301-0082(97)00078-6PubMedCrossRef
15.
go back to reference Biernaskie J, Corbett D: Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 2001, 21: 5272–80.PubMed Biernaskie J, Corbett D: Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 2001, 21: 5272–80.PubMed
16.
go back to reference Kawamata T, Alexis NE, Dietrich WD, Finklestein SP: Intracisternal basic fibroblast growth factor (bFGF) enhances behavioral recovery following focal cerebral infarction in the rat. J Cereb Blood Flow Metab 1996, 16: 542–7.PubMedCrossRef Kawamata T, Alexis NE, Dietrich WD, Finklestein SP: Intracisternal basic fibroblast growth factor (bFGF) enhances behavioral recovery following focal cerebral infarction in the rat. J Cereb Blood Flow Metab 1996, 16: 542–7.PubMedCrossRef
17.
go back to reference 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: 472–6. 10.1161/01.STR.17.3.472PubMedCrossRef 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: 472–6. 10.1161/01.STR.17.3.472PubMedCrossRef
18.
go back to reference De Ryck M, Van Reempts J, Borgers M, Wauquier A, Janssen PA: Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 1989, 20: 1383–90. 10.1161/01.STR.20.10.1383PubMedCrossRef De Ryck M, Van Reempts J, Borgers M, Wauquier A, Janssen PA: Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 1989, 20: 1383–90. 10.1161/01.STR.20.10.1383PubMedCrossRef
19.
go back to reference Bouet V, Freret T, Toutain J, Divoux D, Boulouard M, Schumann-Bard P: Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol 2007, 203: 555–67. 10.1016/j.expneurol.2006.09.006PubMedCrossRef Bouet V, Freret T, Toutain J, Divoux D, Boulouard M, Schumann-Bard P: Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol 2007, 203: 555–67. 10.1016/j.expneurol.2006.09.006PubMedCrossRef
20.
go back to reference Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, Freret T: The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009, 4: 1560–4. 10.1038/nprot.2009.125PubMedCrossRef Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, Freret T: The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009, 4: 1560–4. 10.1038/nprot.2009.125PubMedCrossRef
21.
go back to reference Modo M, Stroemer RP, Tang E, Veizovic T, Sowniski P, Hodges H: Neurological sequelae and long-term behavioural assessment of rats with transient middle cerebral artery occlusion. J Neurosci Methods 2000, 104: 99–109. 10.1016/S0165-0270(00)00329-0PubMedCrossRef Modo M, Stroemer RP, Tang E, Veizovic T, Sowniski P, Hodges H: Neurological sequelae and long-term behavioural assessment of rats with transient middle cerebral artery occlusion. J Neurosci Methods 2000, 104: 99–109. 10.1016/S0165-0270(00)00329-0PubMedCrossRef
22.
go back to reference Freret T, Bouet V, Leconte C, Roussel S, Chazalviel L, Divoux D, Schumann-Bard P, Boulouard M: Behavioral deficits after distal focal cerebral ischemia in mice: Usefulness of adhesive removal test. Behav Neurosci 2009, 123: 224–30.PubMedCrossRef Freret T, Bouet V, Leconte C, Roussel S, Chazalviel L, Divoux D, Schumann-Bard P, Boulouard M: Behavioral deficits after distal focal cerebral ischemia in mice: Usefulness of adhesive removal test. Behav Neurosci 2009, 123: 224–30.PubMedCrossRef
23.
go back to reference Freret T, Chazalviel L, Roussel S, Bernaudin M, Schumann-Bard P, Boulouard M: Long-term functional outcome following transient middle cerebral artery occlusion in the rat: correlation between brain damage and behavioral impairment. Behav Neurosci 2006, 120: 1285–98.PubMedCrossRef Freret T, Chazalviel L, Roussel S, Bernaudin M, Schumann-Bard P, Boulouard M: Long-term functional outcome following transient middle cerebral artery occlusion in the rat: correlation between brain damage and behavioral impairment. Behav Neurosci 2006, 120: 1285–98.PubMedCrossRef
24.
go back to reference Rogers DC, Campbell CA, Stretton JL, Mackay KB: Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 1997, 28: 2060–5. discussion 2066 10.1161/01.STR.28.10.2060PubMedCrossRef Rogers DC, Campbell CA, Stretton JL, Mackay KB: Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 1997, 28: 2060–5. discussion 2066 10.1161/01.STR.28.10.2060PubMedCrossRef
25.
go back to reference Grabowski M, Brundin P, Johansson BB: Paw-reaching, sensorimotor, and rotational behavior after brain infarction in rats. Stroke 1993, 24: 889–95. 10.1161/01.STR.24.6.889PubMedCrossRef Grabowski M, Brundin P, Johansson BB: Paw-reaching, sensorimotor, and rotational behavior after brain infarction in rats. Stroke 1993, 24: 889–95. 10.1161/01.STR.24.6.889PubMedCrossRef
26.
go back to reference Borlongan CV, Cahill DW, Sanberg PR: Locomotor and passive avoidance deficits following occlusion of the middle cerebral artery. Physiol Behav 1995, 58: 909–17. 10.1016/0031-9384(95)00103-PPubMedCrossRef Borlongan CV, Cahill DW, Sanberg PR: Locomotor and passive avoidance deficits following occlusion of the middle cerebral artery. Physiol Behav 1995, 58: 909–17. 10.1016/0031-9384(95)00103-PPubMedCrossRef
27.
go back to reference Winter B, Juckel G, Viktorov I, Katchanov J, Gietz A, Sohr R, Balkaya M, Hortnagl H, Endres M: Anxious and hyperactive phenotype following brief ischemic episodes in mice. Biol Psychiatry 2005, 57: 1166–75. 10.1016/j.biopsych.2005.02.010PubMedCrossRef Winter B, Juckel G, Viktorov I, Katchanov J, Gietz A, Sohr R, Balkaya M, Hortnagl H, Endres M: Anxious and hyperactive phenotype following brief ischemic episodes in mice. Biol Psychiatry 2005, 57: 1166–75. 10.1016/j.biopsych.2005.02.010PubMedCrossRef
28.
go back to reference DeVries AC, Nelson RJ, Traystman RJ, Hurn PD: Cognitive and behavioral assessment in experimental stroke research: will it prove useful? Neurosci Biobehav Rev 2001, 25: 325–42. 10.1016/S0149-7634(01)00017-3PubMedCrossRef DeVries AC, Nelson RJ, Traystman RJ, Hurn PD: Cognitive and behavioral assessment in experimental stroke research: will it prove useful? Neurosci Biobehav Rev 2001, 25: 325–42. 10.1016/S0149-7634(01)00017-3PubMedCrossRef
29.
go back to reference Virley D, Beech JS, Smart SC, Williams SC, Hodges H, Hunter AJ: A temporal MRI assessment of neuropathology after transient middle cerebral artery occlusion in the rat: correlations with behavior. J Cereb Blood Flow Metab 2000, 20: 563–82.PubMedCrossRef Virley D, Beech JS, Smart SC, Williams SC, Hodges H, Hunter AJ: A temporal MRI assessment of neuropathology after transient middle cerebral artery occlusion in the rat: correlations with behavior. J Cereb Blood Flow Metab 2000, 20: 563–82.PubMedCrossRef
30.
go back to reference Hudzik TJ, Borrelli A, Bialobok P, Widzowski D, Sydserff S, Howell A, Gendron P, Corbett D, Miller J, Palmer GC: Long-term functional end points following middle cerebral artery occlusion in the rat. Pharmacol Biochem Behav 2000, 65: 553–62. 10.1016/S0091-3057(99)00243-9PubMedCrossRef Hudzik TJ, Borrelli A, Bialobok P, Widzowski D, Sydserff S, Howell A, Gendron P, Corbett D, Miller J, Palmer GC: Long-term functional end points following middle cerebral artery occlusion in the rat. Pharmacol Biochem Behav 2000, 65: 553–62. 10.1016/S0091-3057(99)00243-9PubMedCrossRef
31.
go back to reference van Meer MP, van der Marel K, Wang K, Otte WM, El Bouazati S, Roeling TA, Viergever MA, Berkelbach van der Sprenkel JW, Dijkhuizen RM: Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci 2010, 30: 3964–72. 10.1523/JNEUROSCI.5709-09.2010PubMedCrossRef van Meer MP, van der Marel K, Wang K, Otte WM, El Bouazati S, Roeling TA, Viergever MA, Berkelbach van der Sprenkel JW, Dijkhuizen RM: Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci 2010, 30: 3964–72. 10.1523/JNEUROSCI.5709-09.2010PubMedCrossRef
32.
go back to reference Moore TL, Killiany RJ, Pessina MA, Moss MB, Finklestein SP, Rosene DL: Recovery from ischemia in the middle-aged brain: a nonhuman primate model. Neurobiol Aging 2011. Moore TL, Killiany RJ, Pessina MA, Moss MB, Finklestein SP, Rosene DL: Recovery from ischemia in the middle-aged brain: a nonhuman primate model. Neurobiol Aging 2011.
33.
go back to reference Encarnacion A, Horie N, Keren-Gill H, Bliss TM, Steinberg GK, Shamloo M: Long-term behavioral assessment of function in an experimental model for ischemic stroke. J Neurosci Methods 2011, 196: 247–57. 10.1016/j.jneumeth.2011.01.010PubMedCentralPubMedCrossRef Encarnacion A, Horie N, Keren-Gill H, Bliss TM, Steinberg GK, Shamloo M: Long-term behavioral assessment of function in an experimental model for ischemic stroke. J Neurosci Methods 2011, 196: 247–57. 10.1016/j.jneumeth.2011.01.010PubMedCentralPubMedCrossRef
34.
go back to reference Dijkhuizen RM, Ren J, Mandeville JB, Wu O, Ozdag FM, Moskowitz MA, Rosen BR, Finklestein SP: Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc Natl Acad Sci USA 2001, 98: 12766–71. 10.1073/pnas.231235598PubMedCentralPubMedCrossRef Dijkhuizen RM, Ren J, Mandeville JB, Wu O, Ozdag FM, Moskowitz MA, Rosen BR, Finklestein SP: Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc Natl Acad Sci USA 2001, 98: 12766–71. 10.1073/pnas.231235598PubMedCentralPubMedCrossRef
35.
go back to reference Rogalewski A, Dittgen T, Klugmann M, Kirsch F, Kruger C, Pitzer C, Minnerup J, Schabitz WR, Schneider A: Semaphorin 6A improves functional recovery in conjunction with motor training after cerebral ischemia. PLoS One 2010, 5: e10737. 10.1371/journal.pone.0010737PubMedCentralPubMedCrossRef Rogalewski A, Dittgen T, Klugmann M, Kirsch F, Kruger C, Pitzer C, Minnerup J, Schabitz WR, Schneider A: Semaphorin 6A improves functional recovery in conjunction with motor training after cerebral ischemia. PLoS One 2010, 5: e10737. 10.1371/journal.pone.0010737PubMedCentralPubMedCrossRef
36.
go back to reference Hicks AU, Hewlett K, Windle V, Chernenko G, Ploughman M, Jolkkonen J, Weiss S, Corbett D: Enriched environment enhances transplanted subventricular zone stem cell migration and functional recovery after stroke. Neuroscience 2007, 146: 31–40. 10.1016/j.neuroscience.2007.01.020PubMedCrossRef Hicks AU, Hewlett K, Windle V, Chernenko G, Ploughman M, Jolkkonen J, Weiss S, Corbett D: Enriched environment enhances transplanted subventricular zone stem cell migration and functional recovery after stroke. Neuroscience 2007, 146: 31–40. 10.1016/j.neuroscience.2007.01.020PubMedCrossRef
37.
go back to reference Reitmeir R, Kilic E, Kilic U, Bacigaluppi M, ElAli A, Salani G, Pluchino S, Gassmann M, Hermann DM: Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity. Brain 2011, 134: 84–99. 10.1093/brain/awq344PubMedCrossRef Reitmeir R, Kilic E, Kilic U, Bacigaluppi M, ElAli A, Salani G, Pluchino S, Gassmann M, Hermann DM: Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity. Brain 2011, 134: 84–99. 10.1093/brain/awq344PubMedCrossRef
38.
go back to reference Brown AW, Bjelke B, Fuxe K: Motor response to amphetamine treatment, task-specific training, and limited motor experience in a postacute animal stroke model. Exp Neurol 2004, 190: 102–8. 10.1016/j.expneurol.2004.07.005PubMedCrossRef Brown AW, Bjelke B, Fuxe K: Motor response to amphetamine treatment, task-specific training, and limited motor experience in a postacute animal stroke model. Exp Neurol 2004, 190: 102–8. 10.1016/j.expneurol.2004.07.005PubMedCrossRef
39.
go back to reference Hatinen S, Sairanen M, Sirvio J, Jolkkonen J: Improved sensorimotor function by rolipram following focal cerebral ischemia in rats. Restor Neurol Neurosci 2008, 26: 493–9.PubMed Hatinen S, Sairanen M, Sirvio J, Jolkkonen J: Improved sensorimotor function by rolipram following focal cerebral ischemia in rats. Restor Neurol Neurosci 2008, 26: 493–9.PubMed
40.
go back to reference Jin K, Wang X, Xie L, Mao XO, Greenberg DA: Transgenic ablation of doublecortin-expressing cells suppresses adult neurogenesis and worsens stroke outcome in mice. Proc Natl Acad Sci USA 2010, 107: 7993–8. 10.1073/pnas.1000154107PubMedCentralPubMedCrossRef Jin K, Wang X, Xie L, Mao XO, Greenberg DA: Transgenic ablation of doublecortin-expressing cells suppresses adult neurogenesis and worsens stroke outcome in mice. Proc Natl Acad Sci USA 2010, 107: 7993–8. 10.1073/pnas.1000154107PubMedCentralPubMedCrossRef
41.
go back to reference Ferrara A, El Bejaoui S, Seyen S, Tirelli E, Plumier JC: The usefulness of operant conditioning procedures to assess long-lasting deficits following transient focal ischemia in mice. Behav Brain Res 2009, 205: 525–34. 10.1016/j.bbr.2009.08.011PubMedCrossRef Ferrara A, El Bejaoui S, Seyen S, Tirelli E, Plumier JC: The usefulness of operant conditioning procedures to assess long-lasting deficits following transient focal ischemia in mice. Behav Brain Res 2009, 205: 525–34. 10.1016/j.bbr.2009.08.011PubMedCrossRef
42.
go back to reference Leconte C, Tixier E, Freret T, Toutain J, Saulnier R, Boulouard M, Roussel S, Schumann-Bard P, Bernaudin M: Delayed Hypoxic Postconditioning Protects Against Cerebral Ischemia in the Mouse. Stroke 2009. Leconte C, Tixier E, Freret T, Toutain J, Saulnier R, Boulouard M, Roussel S, Schumann-Bard P, Bernaudin M: Delayed Hypoxic Postconditioning Protects Against Cerebral Ischemia in the Mouse. Stroke 2009.
43.
go back to reference Freret T, Valable S, Chazalviel L, Saulnier R, Mackenzie ET, Petit E, Bernaudin M, Boulouard M, Schumann-Bard P: Delayed administration of deferoxamine reduces brain damage and promotes functional recovery after transient focal cerebral ischemia in the rat. Eur J Neurosci 2006, 23: 1757–65. 10.1111/j.1460-9568.2006.04699.xPubMedCrossRef Freret T, Valable S, Chazalviel L, Saulnier R, Mackenzie ET, Petit E, Bernaudin M, Boulouard M, Schumann-Bard P: Delayed administration of deferoxamine reduces brain damage and promotes functional recovery after transient focal cerebral ischemia in the rat. Eur J Neurosci 2006, 23: 1757–65. 10.1111/j.1460-9568.2006.04699.xPubMedCrossRef
44.
go back to reference Baird AL, Meldrum A, Dunnett SB: The staircase test of skilled reaching in mice. Brain Res Bull 2001, 54: 243–50. 10.1016/S0361-9230(00)00457-3PubMedCrossRef Baird AL, Meldrum A, Dunnett SB: The staircase test of skilled reaching in mice. Brain Res Bull 2001, 54: 243–50. 10.1016/S0361-9230(00)00457-3PubMedCrossRef
45.
go back to reference Tennant KA, Jones TA: Sensorimotor behavioral effects of endothelin-1 induced small cortical infarcts in C57BL/6 mice. J Neurosci Methods 2009, 181: 18–26. 10.1016/j.jneumeth.2009.04.009PubMedCrossRef Tennant KA, Jones TA: Sensorimotor behavioral effects of endothelin-1 induced small cortical infarcts in C57BL/6 mice. J Neurosci Methods 2009, 181: 18–26. 10.1016/j.jneumeth.2009.04.009PubMedCrossRef
46.
go back to reference Haelewyn B, Freret T, Pacary E, Schumann-Bard P, Boulouard M, Bernaudin M, Bouet V: Long-term evaluation of sensorimotor and mnesic behaviour following striatal NMDA-induced unilateral excitotoxic lesion in the mouse. Behav Brain Res 2007, 178: 235–43. 10.1016/j.bbr.2006.12.023PubMedCrossRef Haelewyn B, Freret T, Pacary E, Schumann-Bard P, Boulouard M, Bernaudin M, Bouet V: Long-term evaluation of sensorimotor and mnesic behaviour following striatal NMDA-induced unilateral excitotoxic lesion in the mouse. Behav Brain Res 2007, 178: 235–43. 10.1016/j.bbr.2006.12.023PubMedCrossRef
47.
go back to reference Wahl F, Allix M, Plotkine M, Boulu RG: Neurological and behavioral outcomes of focal cerebral ischemia in rats. Stroke 1992, 23: 267–72. 10.1161/01.STR.23.2.267PubMedCrossRef Wahl F, Allix M, Plotkine M, Boulu RG: Neurological and behavioral outcomes of focal cerebral ischemia in rats. Stroke 1992, 23: 267–72. 10.1161/01.STR.23.2.267PubMedCrossRef
48.
go back to reference Esneault E, Castagne V, Moser P, Bonny C, Bernaudin M: D-JNKi, a peptide inhibitor of c-Jun N-terminal kinase, promotes functional recovery after transient focal cerebral ischemia in rats. Neuroscience 2008, 152: 308–20. 10.1016/j.neuroscience.2007.12.036PubMedCrossRef Esneault E, Castagne V, Moser P, Bonny C, Bernaudin M: D-JNKi, a peptide inhibitor of c-Jun N-terminal kinase, promotes functional recovery after transient focal cerebral ischemia in rats. Neuroscience 2008, 152: 308–20. 10.1016/j.neuroscience.2007.12.036PubMedCrossRef
Metadata
Title
On the importance of long-term functional assessment after stroke to improve translation from bench to bedside
Authors
Thomas Freret
Pascale Schumann-Bard
Michel Boulouard
Valentine Bouet
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Experimental & Translational Stroke Medicine / Issue 1/2011
Electronic ISSN: 2040-7378
DOI
https://doi.org/10.1186/2040-7378-3-6

Other articles of this Issue 1/2011

Experimental & Translational Stroke Medicine 1/2011 Go to the issue