Very early-initiated physical rehabilitation protects against ischemic brain injury

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 7, 2012, Pages 2476-2489

  Zhang, Pengyue ^a   Zhang, Qi ^a   Pu, Hongjian ^a   Wu, Yi ^a   Bai, Yulong ^a   Vosler, Peter S ^b   Chen, Jun ^a,b   Shi, Hong ^a   Gao, Yanqin ^a   Hu, Yongshan ^a  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytosis; Functional recovery; In vivo ischemia; Neuroinflammation; VEIPR

Indexed keywords

CELL ADHESION MOLECULE; CYCLOOXYGENASE 2; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BLOOD BRAIN BARRIER; BRAIN DAMAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN WATER; CONTROLLED STUDY; CYTOKINE PRODUCTION; EARLY INTERVENTION; ENCEPHALITIS; HUMAN; IMMUNOFLUORESCENCE; INFLAMMATION; MALE; MAZE TEST; MICROGLIA; MOTOR PERFORMANCE; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; REHABILITATION CARE; SPATIAL LEARNING; SPATIAL MEMORY; VERY EARLY INITIATED PHYSICAL REHABILITATION; ANIMAL; ANIMAL BEHAVIOR; FLUORESCENT ANTIBODY TECHNIQUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; BEHAVIOR, ANIMAL; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MALE; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84867322560     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: None     Document Type: Article

References (80)

1. D. Lloyd-Jones, R. Adams, M. Carnethon, G. De Simone , T. B. Ferguson, K. Flegal, E. Ford, K. Furie, A. Go, K. Greenlund, N. Haase, S. Hailpern, M. Ho, V. Howard, B. Kissela, S. Kittner, D. Lackland, L. Lisabeth, A. Marelli, M. McDermott, J. Meigs, D., Mozaffarian, G. Nichol, C. O'Donnell, V. Roger, W. Rosamond, R. Sacco, P. Sorlie, R. Stafford, J. Steinberger, T. Thom, S. Wasserthiel-Smoller, N. Wong, J. Wylie-Rosett, and Y. Hong: Heart disease and stroke statistics-2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 119, 480-486 (2009))
2. S. Zinn, H. B. Bosworth, H. M. Hoenig, and H. S. Swartzwelder: Executive function deficits in acute stroke. Arch Phys Med Rehabil 88, 173-180 (2007)) (Pubitemid 46161331)
3. S. K. Saxena, T. P. Ng, G. Koh, D. Yong, and N. P. Fong: Is improvement in impaired cognition and depressive symptoms in post-stroke patients associated with recovery in activities of daily living? Acta Neurol Scand 115, 339-346 (2007)) (Pubitemid 46699425)
4. V. E. O'Collins, M. R. Macleod, G. A. Donnan, L. L. Horky, B. H. van der Worp and D. W. Howells: 1,026 experimental treatments in acute stroke. Ann Neurol 59, 467-477 (2006)) (Pubitemid 43358067)
5. D. L. O. N. Perez and A. Davalos:Neuroprotection in cerebral infarction: the opportunity of new studies. Cerebrovasc Dis 24 Suppl 1, 153-156 (2007)) (Pubitemid 350035862)
6. E. H. Lo, J. P. Broderickand, M. A. Moskowitz: tPA and proteolysis in the neurovascular unit. Stroke 35, 354-356 (2004)) (Pubitemid 38174404)
7. M. I. Weintraub: Thrombolysis (tissue plasminogen activator) in stroke: a medicolegal quagmire. Stroke 37, 1917-1922 (2006)) (Pubitemid 44297752)
8. T. Liu-Ambrose, J. J. Eng, L. A. Boyd, C. Jacova, J. C. Davis, S. Bryan, P. Lee, P. Brasher and G. Y. Hsiung: Promotion of the mind through exercise (PROMoTE): a proof-of-concept randomized controlled trial of aerobic exercise training in older adults with vascular cognitive impairment. BMC Neurol 10, 14 (2010))
9. B. M. Quaney, L. A. Boyd, J. M. McDowd, L. H. Zahner, J. He, M. S. Mayo and R. F. Macko: Aerobic exercise improves cognition and motor function poststroke. Neurorehabil Neural Repair23, 879-885 (2009))
10. L. Ada, C. M. Dean, J. M. Hall, J. Bampton and S. Crompton: A treadmill and overground walking program improves walking in persons residing in the community after stroke: a placebo-controlled, randomized trial. Arch Phys Med Rehabil 84, 1486 -1491(2003)) (Pubitemid 37237257)
11. D. F. E. A. Alexander W. Dromerick: Does the application of constraint-induced movement therapy during acute rehabilitation reduce arm impairment after ischemic stroke. Stroke 31, 2984-2988 (2000))
12. M. D. Chen and J. H. Rimmer: Effects of exercise on quality of life in stroke survivors: a meta-analysis. Stroke 42(3), 832-837 (2011))
13. R. Galvin, T. Cusack, E. O'Grady, TB. Murphy, E.Stokes: Family-mediated exercise intervention (FAME): evaluation of a novel form of exercise delivery after stroke. Stroke 42(3), 681-686(2011))
14. Y. J. Sim, S. S. Kim, J. Y. Kim, M. S. Shin and C. J. Kim: Treadmill exercise improves short-term memory by suppressing ischemia-induced apoptosis of neuronal cells in gerbils. Neurosci Lett 372, 256-261 (2004))
15. H. Chang, Y. Yang, S. P. Wang and R. Wang: Effects of treadmill training on motor performance and extracellular glutamate level in striatum in rats with or without transient middle cerebral artery occlusion. Behavioural Brain Research 299, 37 -40(2009))
16. T. A. Jones, R. P. Allred, D. L. Adkins, J. E. Hsu, A. O'Bryant and M. A. Maldonado: Remodeling the brain with behavioral experience after stroke. Stroke 40, S136-138 (2009))
17. Y. F. Liu, H. I. Chen, C. L. Wu, Y. M. Kuo, L. Yu, A. M. Huang, F. S. Wu, J. I. Chuang and C. J. Jen: Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol 587, 3221-3231 (2009))
18. M. Ploughman, V. Windle, C. L. MacLellan, N. White, J. J. Dore and D. Corbett: Brain-derived neurotrophic factor contributes to recovery of skilled reaching after focal ischemia in rats. Stroke 40, 1490-1495 (2009))
19. A. M. Stranahan, D. Khalil and E. Gould: Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus 17, 1017-1022 (2007)) (Pubitemid 350156815)
20. Z. Ying, R. R. Roy, H. Zhong, S. Zdunowski, V. R. Edgerton and F. Gomez-Pinilla: BDNF-exercise interactions in the recovery of symmetrical stepping after a cervical hemisection in rats. Neuroscience 155, 1070-1078 (2008))
21. S. S. Vaynman, Z. Ying, D. Yin and F. Gomez-Pinilla: Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Res 1070, 124-130 (2006)) (Pubitemid 43247751)
22. C. X. Luo, J. Jiang, Q. G. Zhou, X. J. Zhu, W. Wang, Z. J. Zhang, X. Han and D. Y. Zhu: Voluntary exerciseinduced neurogenesis in the postischemic dentate gyrus is associated with spatial memory recovery from stroke. J Neurosci Res 85, 1637-1646 (2007)) (Pubitemid 46849611)
23. Y. R. Yang, R. Y. Wang and P. S. Wang: Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 339, 91-94 (2003)) (Pubitemid 36254784)
24. J. Bernhardt, M. N. Thuy, J. M. Collier and L. A. Legg: Very Early Versus Delayed Mobilization after Stroke. Stroke 40, e489-490 (2009))
25. S. T. Bland, T. Schallert, R. Strong, J. Aronowski, J. C. Grotta and D. M. Feeney: Early exclusive use of the affected forelimb after moderate transient focal ischemia in rats: functional and anatomic outcome. Stroke 31, 1144-1152(2000)) (Pubitemid 30253539)
26. A. Risedal, J. Zeng and B. B. Johansson: Early training may exacerbate brain damage after focal brain ischemia in the rat.J Cereb Blood Flow Metab 19, 997-1003 (1999)) (Pubitemid 30173722)
27. Y. Yagita, K. Kitagawa, T. Sasaki, Y. Terasaki, K. Todo, E. Omura-Matsuoka, M. Matsumoto and M. Hori: Postischemic exercise decreases neurogenesis in the adult rat dentate gyrus.Neurosci Lett 409, 24-29 (2006)) (Pubitemid 44585114)
28. R. P. Allred and T. A. Jones: Maladaptive effects of learning with the less-affected forelimb after focal cortical infarcts in rats. Exp Neurol 210, 172-181 (2008)) (Pubitemid 351258078)
29. X. Hu, H. Zheng, T. Yan, S. Pan, J. Fang, R. Jiang and S. Ma: Physical exercise induces expression of CD31 and facilitates neural function recovery in rats with focal cerebral infarction. Neurol Res 32, 397-402 (2010))
30. S. U. Lee, D. Y. Kim, S. H. Park, D. H. Choi, H. W. Park and T. R., Han: Mild to moderate early exercise promotes recovery from cerebral ischemia in rats. Can J Neurol Sci 36, 443-449 (2009).
31. J. Bernhardt, H. Dewey, A. Thrift, J. Collier and G. Donnan: A very early rehabilitation trial for stroke (AVERT): phase II safety and feasibility. Stroke 39, 390-396 (2008)) (Pubitemid 351619461)
32. J., Bernhardt: Very early mobilization following acute stroke: Controversies, the unknowns, and a way forward. Ann Indian Acad Neurol 11, 88-98 (2008))
33. National Stroke Foundation. Clinical guidelines for acute stroke management, http://www.strokefoundation.com.au/news/welcome/clinicalguidelines- for-acute-stroke-management.
34. E. Z. Longa, P. R. Weinstein, S. Carlson and R. Cummins: Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20, 84-91 (1989)) (Pubitemid 19040218)
35. D. A. Dawson and J. M. Hallenbeck: Acute focal ischemia-induced alterations in MAP2 immunostaining: description of temporal changes and utilization as a marker for volumetric assessment of acute brain injury. J Cereb Blood Flow Metab 16, 170-174 (1996)) (Pubitemid 26007962)
36. Y. Liu, F. S. Silverstein, R. Skoff and J. D. Barks: Hypoxic-ischemic oligodendroglial injury in neonatal rat brain. Pediatr Res 51, 25-33 (2002)) (Pubitemid 34008206)
37. K. J Livak and T. D Schmittgen:Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25,402-408(2001)) (Pubitemid 34164012)
38. T. N. Lin, Y. Y. He, G. Wu, M. Khan and C. Y. Hsu: Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24, 117-121 (1993)) (Pubitemid 23014393)
39. C. H. Chen, T. J. Toung, A. Sapirstein and A. Bhardwaj: Effect of duration of osmotherapy on bloodbrain barrier disruption and regional cerebral edema after experimental stroke. J Cereb Blood Flow Metab 26, 951-958 (2006)) (Pubitemid 43980411)
40. E. R. Migliati, M. Amiry-Moghaddam, S. C. Froehner, M. E. Adams, O. P. Ottersen and A. Bhardwaj: Na (+)-K (+)-2Cl (-) cotransport inhibitor attenuates cerebral edema following experimental stroke via the perivascular pool of aquaporin-4. Neurocrit Care 13, 123-131 (2010))
41. D. C. Rogers, C. A. Campbell, J. L. Stretton and K. B. Mackay: Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 28, 2060-2066 (1997)) (Pubitemid 27459019)
42. G. A Metz, and I. Q Whishaw,: Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore-and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115(2), 169-179(2002)) (Pubitemid 34461965)
43. C. V. Vorhees and M. T. Williams: Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1, 848-858 (2006))
44. F Block: Global ischemia and behavioural deficits. Prog Neurobiol 58(3), 279-295(1999)) (Pubitemid 29193058)
45. T. Takano, N. Oberheim, ML. Cotrina and M. Nedergaard: Astrocytes and ischemic injury. Stroke 40, S8-12(2009))
46. AG. Ceulemans,T. Zgavc, R. Kooijman, S. Hachimi-Idrissi, S. Sarreand Y.Michotte : The dual role of the neuroinflammatory response after ischemic stroke: modulatory effects of hypothermia. J Neuroinflammation 7, 74(2010))
47. B. Rossi, S. Angiari, E. Zenaro, SL. Budui, G.Constantin: Vascular inflammation in central nervous system diseases: adhesion receptors controlling leukocyteendothelial interactions. J Leukoc Biol 289, 539-556(2011))
48. Y. Chen, RA.Swanson : Astrocytes and brain injury. J Cereb Blood Flow Metab 23, 137-149(2003)) (Pubitemid 36188452)
49. D. Tanne, R. Tsabari, O. Chechik, A. Toledano, D. Orion, Y. Schwammenthal, T. Philips, E. Schwammenthal and Y. Adler: Improved exercise capacity in patients after minor ischemic stroke undergoing a supervised exercise training program. Isr Med Assoc J 10, 113-116 (2008)) (Pubitemid 351649634)
50. A. M. Auriat and F. Colbourne: Delayed rehabilitation lessens brain injury and improves recovery after intracerebral hemorrhage in rats. Brain Res 1251, 262-268 (2009))
51. F. Cechetti, C. Fochesatto, D. Scopel, P. Nardin, C. A. Goncalves, C. A. Netto and I. R. Siqueira: Effect of a neuroprotective exercise protocol on oxidative state and BDNF levels in the rat hippocampus. Brain Res 1188, 182-188 (2008))
52. M. Arias and L. N. Smith: Early mobilization of acute stroke patients. J Clin Nurs 16, 282-288 (2007))
53. C. J. Brown, R. J. Friedkin and S. K. Inouye: Prevalence and outcomes of low mobility in hospitalized older patients. J Am Geriatr Soc 52, 1263-1270 (2004)) (Pubitemid 39038197)
54. C. Allen, P. Glasziou and M. C. Del: Bed rest: a potentially harmful treatment needing more careful evaluation. Lancet354, 1229-1233 (1999)) (Pubitemid 29469350)
55. G. Vangeisonand DA.Rempe: The Janus-faced effects of hypoxia on astrocyte function. Neuroscientist 15,579-588(2009))
56. I .Aksu, A. Topcu, UM. Camsari and O .Acikgoz Effect of acute and chronic exercise on oxidant-antioxidant equilibrium in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 452(3), 281-285(2009))
57. F. C.Barone and G. Z. Feuerstein: Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19(8), 819-834 (1999)) (Pubitemid 30173383)
58. Q. Wang, X. N. Tang and M A. Yenari:The inflammatory response in stroke.J Neuroimmunol 184,53-68(2007)) (Pubitemid 46365991)
59. S. M. Lucas, N. J. Rothwell and R. M. Gibson: The role of inflammation in CNS injury and disease. Br J Pharmacol 147 S232-240 (2006)) (Pubitemid 43077281)
60. J. Correale and A. Villa: The neuroprotective role of inflammation in nervous system injuries.J Neurol 251, 1304-1316 (2004))
61. C. Szabo, B. Zingarelli, M. O'Connor and A. L. Salzman: DNA strand breakage, activation of poly (ADPribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite.Proc Natl Acad Sci 93, 1753-1758 (1996)) (Pubitemid 26079829)
62. M. Minami, T. Katayama and M. Satoh: Brain cytokines and chemokines: roles in ischemic injury and pain. J Pharmacol Sci 100, 461-470 (2006)) (Pubitemid 44609536)
63. H. Offner, S. Subramanian, S. M. Parker, M. E. Afentoulis, A. A. Vandenbark and P. D. Hurn: Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 26, 654-665 (2006))
64. B. Fogal, J. A. Hewett and S. J. Hewett, Interleukin-1beta potentiates neuronal injury in a variety of injury models involving energy deprivation. J Neuroimmunol 161, 93-100 (2005)) (Pubitemid 40340877)
65. C. Iadecola, F.Zhang, R. Casey, M. Nagayama and M. E. Ross: Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17, 9157-9164 (1997)) (Pubitemid 27498443)
66. M. Guo, B. Cox, S. Mahale, W. Davis, A. Carranza, K. Hayes, S. Sprague, D. Jimenez and Y. Ding: Preischemic exercise reduces matrix metalloproteinase-9 expression and ameliorates blood-brain barrier dysfunction in stroke. Neuroscience 151, 340-351 (2008))
67. Y. H. Ding, C. N. Young, X. Luan, J. Li, J. A. Rafols, J. C. Clark, J. N. McAllister and Y. Ding: Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol 109, 237-246 (2005)) (Pubitemid 41166592)
68. G. Stoll and S. Jander: The role of microglia and macrophages in the pathophysiology of the CNS.Prog Neurobiol 58, 233-247 (1999)) (Pubitemid 29193056)
69. K. Nakajima, S. Yamamoto, S. Kohsaka and T. Kurihara: Neuronal stimulation leading to upregulation of glutamate transporter-1 (GLT-1) in rat microglia in vitro.Neurosci Lett 436, 331-334 (2008))
70. A. Tuttolomondo: Citokines and inflammation markers in ischemic stroke. Curr Pharm Des 14, 3547-3548 (2008))
71. C. L. Gibson, T. C. Coughlan and S. P. Murphy: Glial nitric oxide and ischemia. Glia 50, 417-426 (2005)) (Pubitemid 40780845)
72. S. W. Barger, M. E. Goodwin, M. M. Porter and M. L. Beggs: Glutamate release from activated microglia requires the oxidative burst and lipid peroxidation.J Neurochem 101, 1205-1213 (2007)) (Pubitemid 46718822)
73. S. T. Dheen, C. Kaur and E. A. Ling: Microglial activation and its implications in the brain diseases. Curr Med Chem 14, 1189-1197 (2007)) (Pubitemid 46739320)
74. K. A. Hewlett and D. Corbett: Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neuroscience 141, 27-33 (2006))
75. X. Liu, A. J. Bolteus, D. M. Balkin, O. Henschel and A. Bordey: GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 54, 394-410 (2006)) (Pubitemid 44422941)
76. M. Ploughman, S. Granter-Button, G. Chernenko, Z. Attwood, B. A. Tucker, K. M. Mearow and D. Corbett: Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Res 1150, 207-216 (2007)) (Pubitemid 46702117)
77. K. Hayes, S. Sprague, M. Guo, W. Davis, A. Friedman, A. Kumar, D. F. Jimenez and Y. Ding: Forced, not voluntary, exercise effectively induces neuroprotection in stroke. Acta Neuropathol 115, 289-296 (2008))
78. F. Cechetti, A. Rhod, F. Simao, K. Santin, C. Salbego, C. A. Netto and I. R. Siqueira: Effect of treadmill exercise on cell damage in rat hippocampal slices submitted to oxygen and glucose deprivation. Brain Res 1157, 121-125 (2007)) (Pubitemid 46957518)
79. J. L. Humm, D. A. Kozlowski, D. C. James, J. E. Gotts and T. Schallert: Use-dependent exacerbation of brain damage occurs during an early post-lesion vulnerable period. Brain Res 783, 286-292 (1998)) (Pubitemid 28131409)
80. D. Scopel, C. Fochesatto, H. Cimarosti, M. Rabbo, A. Bello-Klein, C. Salbego, C. A. Netto and I. R. Siqueira: Exercise intensity influences cell injury in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Res Bull 71, 155-159 (2006)) (Pubitemid 44750432)