Secondary pathology following contusion, dislocation, and distraction spinal cord injuries

Experimental Neurology

Volumn 212, Issue 2, 2008, Pages 490-506

  Choo, Anthony M ^a,b   Liu, Jie ^b   Dvorak, Marcel ^b   Tetzlaff, Wolfram ^b   Oxland, Thomas R ^a,b  

^a VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Contusion; Dextran; Dislocation; Distraction; Injury mechanisms; Membrane compromise; Ramification index; Secondary injury

Indexed keywords

3 NITROTYROSINE; AMYLOID BETA PROTEIN; CYTOCHROME C; DEXTRAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CONTUSION; GRAY MATTER; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MITOCHONDRION; NERVE CELL; NERVE FIBER DEGENERATION; NERVE FIBER MEMBRANE; NEUROFILAMENT; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION;

ANIMALS; ASTROCYTES; BIOMECHANICS; CELL MEMBRANE PERMEABILITY; CONTUSIONS; DEXTRANS; DISEASE MODELS, ANIMAL; DISLOCATIONS; FLUORESCEIN; MALE; NERVE TISSUE PROTEINS; RATS; SPINAL CORD INJURIES;

EID: 47349105023     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.04.038     Document Type: Article

References (103)

1. Arundine M., Aarts M., Lau A., and Tymianski M. Vulnerability of central neurons to secondary insults after in vitro mechanical stretch. J. Neurosci. 24 (2004) 8106-8123
2. Banik N.L., Hogan E.L., Powers J.M., and Whetstine L.J. Degradation of cytoskeletal proteins in experimental spinal cord injury. Neurochem. Res. 7 (1982) 1465-1475
3. Banik N.L., Shields D.C., Ray S., Davis B., Matzelle D., Wilford G., and Hogan E.L. Role of calpain in spinal cord injury: effects of calpain and free radical inhibitors. Ann. N. Y. Acad. Sci. 844 (1998) 131-137
4. Basso D.M., Beattie M.S., and Bresnahan J.C. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp. Neurol. 139 (1996) 244-256
5. Block M.L., and Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76 (2005) 77-98
6. Borgens R.B., and Shi R. Immediate recovery from spinal cord injury through molecular repair of nerve membranes with polyethylene glycol. FASEB J. 14 (2000) 27-35
7. Bracken M.B., Shepard M.J., Collins W.F., Holford T.R., Young W., Baskin D.S., Eisenberg H.M., Flamm E., Leo-Summers L., Maroon J., et al. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury. Results of the Second National Acute Spinal Cord Injury Study. N. Engl. J. Med. 322 (1990) 1405-1411
8. Bracken M.B., Shepard M.J., Holford T.R., Leo-Summers L., Aldrich E.F., Fazl M., Fehlings M., Herr D.L., Hitchon P.W., Marshall L.F., Nockels R.P., Pascale V., Perot Jr. P.L., Piepmeier J., Sonntag V.K., Wagner F., Wilberger J.E., Winn H.R., and Young W. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the third National Acute Spinal Cord Injury randomized controlled trial. National Acute Spinal Cord Injury Study. Jama 277 (1997) 1597-1604
9. Breig A. Overstretching of and circumscribed pathological tension in the spinal cord-a basic cause of symptoms in cord disorders. J. Biomech. 3 (1970) 7-9
10. Bye N., Habgood M.D., Callaway J.K., Malakooti N., Potter A., Kossmann T., and Morganti-Kossmann M.C. Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp. Neurol. 204 (2007) 220-233
11. Chen X.H., Meaney D.F., Xu B.N., Nonaka M., McIntosh T.K., Wolf J.A., Saatman K.E., and Smith D.H. Evolution of neurofilament subtype accumulation in axons following diffuse brain injury in the pig. J. Neuropathol. Exp. Neurol. 58 (1999) 588-596
12. Choo A.M., Liu J., Lam C.K., Dvorak M., Tetzlaff W., and Oxland T.R. Contusion, dislocation and distraction: primary hemorrhage and membrane permeability in distinct mechanisms of spinal cord injury. J. Neurosurg. Spine 6 (2007) 255-266
13. Cornish R., Blumbergs P.C., Manavis J., Scott G., Jones N.R., and Reilly P.L. Topography and severity of axonal injury in human spinal cord trauma using amyloid precursor protein as a marker of axonal injury. Spine 25 (2000) 1227-1233
14. Cullen D.K., and LaPlaca M.C. Neuronal response to high rate shear deformation depends on heterogeneity of the local strain field. J. Neurotrauma 23 (2006) 1304-1319
15. Deng Y., Thompson B.M., Gao X., and Hall E.D. Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp. Neurol. 205 (2007) 154-165
16. Diaz-Ruiz A., Rios C., Duarte I., Correa D., Guizar-Sahagun G., Grijalva I., and Ibarra A. Cyclosporin-A inhibits lipid peroxidation after spinal cord injury in rats. Neurosci. Lett. 266 (1999) 61-64
17. Faden A.I., Lemke M., Simon R.P., and Noble L.J. N-methyl-D-aspartate antagonist MK801 improves outcome following traumatic spinal cord injury in rats: behavioral, anatomic, and neurochemical studies. J. Neurotrauma 5 (1988) 33-45
18. Farkas O., Lifshitz J., and Povlishock J.T. Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury?. J. Neurosci. 26 (2006) 3130-3140
19. Galbraith J.A., Thibault L.E., and Matteson D.R. Mechanical and electrical responses of the squid giant axon to simple elongation. J. Biomech. Eng. 115 (1993) 13-22
20. Gaviria M., Privat A., d'Arbigny P., Kamenka J., Haton H., and Ohanna F. Neuroprotective effects of a novel NMDA antagonist, Gacyclidine, after experimental contusive spinal cord injury in adult rats. Brain Res. 874 (2000) 200-209
21. Gaviria M., Privat A., d'Arbigny P., Kamenka J.M., Haton H., and Ohanna F. Neuroprotective effects of gacyclidine after experimental photochemical spinal cord lesion in adult rats: dose-window and time-window effects. J. Neurotrauma 17 (2000) 19-30
22. Geddes-Klein D.M., Schiffman K.B., and Meaney D.F. Mechanisms and consequences of neuronal stretch injury in vitro differ with the model of trauma. J. Neurotrauma 23 (2006) 193-204
23. Geddes D.M., Cargill II R.S., and LaPlaca M.C. Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J. Neurotrauma 20 (2003) 1039-1049
24. Geisler F.H., Coleman W.P., Grieco G., and Poonian D. The Sygen multicenter acute spinal cord injury study. Spine 26 (2001) S87-98
25. Gensel J.C., Tovar C.A., Hamers F.P., Deibert R.J., Beattie M.S., and Bresnahan J.C. Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J. Neurotrauma 23 (2006) 36-54
26. Glenn J.A., Ward S.A., Stone C.R., Booth P.L., and Thomas W.E. Characterisation of ramified microglial cells: detailed morphology, morphological plasticity and proliferative capability. J. Anat. 180 Pt 1 (1992) 109-118
27. Gomes-Leal W., Corkill D.J., and Picanco-Diniz C.W. Systematic analysis of axonal damage and inflammatory response in different white matter tracts of acutely injured rat spinal cord. Brain Res. 1066 (2005) 57-70
28. Gris D., Marsh D.R., Oatway M.A., Chen Y., Hamilton E.F., Dekaban G.A., and Weaver L.C. Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J. Neurosci. 24 (2004) 4043-4051
29. Gruner J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9 (1992) 123-126 discussion 126-128
30. Guha A., Tator C.H., and Rochon J. Spinal cord blood flow and systemic blood pressure after experimental spinal cord injury in rats. Stroke 20 (1989) 372-377
31. Gulyas A.I., Buzsaki G., Freund T.F., and Hirase H. Populations of hippocampal inhibitory neurons express different levels of cytochrome c. Eur. J. Neurosci. 23 (2006) 2581-2594
32. Hall E.D., and Springer J.E. Neuroprotection and acute spinal cord injury: a reappraisal. NeuroRx 1 (2004) 80-100
33. Harwood S.M., Yaqoob M.M., and Allen D.A. Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Ann. Clin. Biochem. 42 (2005) 415-431
34. Hedel H.J., and Curt A. Fighting for each segment: estimating the clinical value of cervical and thoracic segments in SCI. J. Neurotrauma 23 (2006) 1621-1631
35. Hendriks W.T., Eggers R., Ruitenberg M.J., Blits B., Hamers F.P., Verhaagen J., and Boe G.J. Profound differences in spontaneous long-term functional recovery after defined spinal tract lesions in the rat. J. Neurotrauma 23 (2006) 18-35
36. Howard C.V., and Reed M.G. Unbiased Stereology - Three Dimensional Measurement in Microscopy (1998), Springer-Verlag, New York
37. Hurlbert R.J. Methylprednisolone for acute spinal cord injury: an inappropriate standard of care. J. Neurosurg. 93 (2000) 1-7
38. Iizuka H., Yamamoto H., Iwasaki Y., Yamamoto T., and Konno H. Evolution of tissue damage in compressive spinal cord injury in rats. J. Neurosurg. 66 (1987) 595-603
39. Imai Y., Ibata I., Ito D., Ohsawa K., and Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 224 (1996) 855-862
40. Inoue K. Microglial activation by purines and pyrimidines. Glia 40 (2002) 156-163
41. Ito D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., and Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res. Mol. Brain Res. 57 (1998) 1-9
42. Jafari S.S., Nielson M., Graham D.I., and Maxwell W.L. Axonal cytoskeletal changes after nondisruptive axonal injury. II. Intermediate sized axons. J. Neurotrauma 15 (1998) 955-966
43. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19 (1996) 312-318
44. Lalancette-Hebert M., Gowing G., Simard A., Weng Y.C., and Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27 (2007) 2596-2605
45. Li G.L., Farooque M., Holtz A., and Olsson Y. Changes of beta-amyloid precursor protein after compression trauma to the spinal cord: an experimental study in the rat using immunohistochemistry. J. Neurotrauma 12 (1995) 269-277
46. Loy D.N., Magnuson D.S., Zhang Y.P., Onifer S.M., Mills M.D., Cao Q.L., Darnall J.B., Fajardo L.C., Burke D.A., and Whittemore S.R. Functional redundancy of ventral spinal locomotor pathways. J. Neurosci. 22 (2002) 315-323
47. Lusardi T.A., Wolf J.A., Putt M.E., Smith D.H., and Meaney D.F. Effect of acute calcium influx after mechanical stretch injury in vitro on the viability of hippocampal neurons. J. Neurotrauma 21 (2004) 61-72
48. Marar B.C. The pattern of neurological damage as an aid to the diagnosis of the mechanism in cervical-spine injuries. J. Bone Jt. Surg. Am. 56 (1974) 1648-1654
49. Matsumoto H., Kumon Y., Watanabe H., Ohnishi T., Shudou M., Ii C., Takahashi H., Imai Y., and Tanaka J. Antibodies to CD11b, CD68, and lectin label neutrophils rather than microglia in traumatic and ischemic brain lesions. J. Neurosci. Res. 85 (2007) 994-1009
50. Maxwell W.L., Povlishock J.T., and Graham D.L. A mechanistic analysis of nondisruptive axonal injury: a review. J. Neurotrauma 14 (1997) 419-440
51. Maxwell W.L., Domleo A., McColl G., Jafari S.S., and Graham D.I. Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. J. Neurotrauma 20 (2003) 151-168
52. Myklebust J.B., Maiman D.J., and Cusick J.F. Axial tension model of spinal cord injury. J. Am. Parapleg. Soc. 11 (1988) 50-55
53. Nehrt A., Rodgers R., Shapiro S., Borgens R., and Shi R. The critical role of voltage-dependent calcium channel in axonal repair following mechanical trauma. Neuroscience 146 (2007) 1504-1512
54. Nikolaidis N., and Pitas I. 3-D Image Processing Algorithms (2001), John Wiley & Sons, New York
55. Norenberg M.D., Smith J., and Marcillo A. The pathology of human spinal cord injury: defining the problems. J. Neurotrauma 21 (2004) 429-440
56. Okonkwo D.O., Pettus E.H., Moroi J., and Povlishock J.T. Alteration of the neurofilament sidearm and its relation to neurofilament compaction occurring with traumatic axonal injury. Brain Res. 784 (1998) 1-6
57. Pant H.C. Dephosphorylation of neurofilament proteins enhances their susceptibility to degradation by calpain. Biochem. J. 256 (1988) 665-668
58. Pearse D.D., Lo Jr. T.P., Cho K.S., Lynch M.P., Garg M.S., Marcillo A.E., Sanchez A.R., Cruz Y., and Dietrich W.D. Histopathological and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J. Neurotrauma 22 (2005) 680-702
59. Pettus E.H., Christman C.W., Giebel M.L., and Povlishock J.T. Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J. Neurotrauma 11 (1994) 507-522
60. Pickett G.E., Campos-Benitez M., Keller J.L., and Duggal N. Epidemiology of traumatic spinal cord injury in Canada. Spine 31 (2006) 799-805
61. Pointillart V., Petitjean M.E., Wiart L., Vital J.M., Lassie P., Thicoipe M., and Dabadie P. Pharmacological therapy of spinal cord injury during the acute phase. Spinal Cord 38 (2000) 71-76
62. Prado G.R., and LaPlaca M.C. Neuronal plasma membrane is transiently disrupted by mechanical trauma: an insight into the in mechanisms involved. Journal of Neurotrauma 21 (2004) 1331
63. Rivlin A.S., and Tator C.H. Effect of duration of acute spinal cord compression in a new acute cord injury model in the rat. Surg. Neurol. 10 (1978) 38-43
64. Rosenberg L.J., and Wrathall J.R. Time course studies on the effectiveness of tetrodotoxin in reducing consequences of spinal cord contusion. J. Neurosci. Res. 66 (2001) 191-202
65. Saatman K.E., Abai B., Grosvenor A., Vorwerk C.K., Smith D.H., and Meaney D.F. Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J. Cereb. Blood Flow Metab. 23 (2003) 34-42
66. Scheff S.W., Rabchevsky A.G., Fugaccia I., Main J.A., and Lumpp Jr. J.E. Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J. Neurotrauma 20 (2003) 179-193
67. Schrimsher G.W., and Reier P.J. Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat. Exp. Neurol. 120 (1993) 264-276
68. Schucht P., Raineteau O., Schwab M.E., and Fouad K. Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp. Neurol. 176 (2002) 143-153
69. Schumacher P.A., Eubanks J.H., and Fehlings M.G. Increased calpain I-mediated proteolysis, and preferential loss of dephosphorylated NF200, following traumatic spinal cord injury. Neuroscience 91 (1999) 733-744
70. Schumacher P.A., Siman R.G., and Fehlings M.G. Pretreatment with calpain inhibitor CEP-4143 inhibits calpain I activation and cytoskeletal degradation, improves neurological function, and enhances axonal survival after traumatic spinal cord injury. J Neurochem 74 (2000) 1646-1655
71. Schwartz M. Macrophages and microglia in central nervous system injury: are they helpful or harmful?. J. Cereb. Blood Flow Metab. 23 (2003) 385-394
72. Sekhon L.H., and Fehlings M.G. Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine 26 (2001) S2-12
73. Shi R., and Pryor J.D. Temperature dependence of membrane sealing following transection in mammalian spinal cord axons. Neuroscience 98 (2000) 157-166
74. Shi R., and Pryor J.D. Pathological changes of isolated spinal cord axons in response to mechanical stretch. Neuroscience 110 (2002) 765-777
75. Shi R., and Whitebone J. Conduction deficits and membrane disruption of spinal cord axons as a function of magnitude and rate of strain. J. Neurophysiol. 95 (2006) 3384-3390
76. Shi R., Asano T., Vining N.C., and Blight A.R. Control of membrane sealing in injured mammalian spinal cord axons. J. Neurophysiol. 84 (2000) 1763-1769
77. Silberstein M., and McLean K. Non-contiguous spinal injury: clinical and imaging features, and postulated mechanism. Paraplegia 32 (1994) 817-823
78. Singleton R.H., and Povlishock J.T. Identification and characterization of heterogeneous neuronal injury and death in regions of diffuse brain injury: evidence for multiple independent injury phenotypes. J. Neurosci. 24 (2004) 3543-3553
79. Smith D.H., Wolf J.A., Lusardi T.A., Lee V.M., and Meaney D.F. High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J. Neurosci. 19 (1999) 4263-4269
80. Smith D.H., Chen X.H., Iwata A., and Graham D.I. Amyloid beta accumulation in axons after traumatic brain injury in humans. J. Neurosurg. 98 (2003) 1072-1077
81. Soltys Z., Ziaja M., Pawlinski R., Setkowicz Z., and Janeczko K. Morphology of reactive microglia in the injured cerebral cortex. Fractal analysis and complementary quantitative methods. J. Neurosci. Res. 63 (2001) 90-97
82. Springer J.E., Azbill R.D., Kennedy S.E., George J., and Geddes J.W. Rapid calpain I activation and cytoskeletal protein degradation following traumatic spinal cord injury: attenuation with riluzole pretreatment. J Neurochem 69 (1997) 1592-1600
83. Springer J.E., Azbill R.D., and Knapp P.E. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat. Med. 5 (1999) 943-946
84. Stence N., Waite M., and Dailey M.E. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33 (2001) 256-266
85. Sternberger L.A., and Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 6126-6130
86. Stirling D.P., Khodarahmi K., Liu J., McPhail L.T., McBride C.B., Steeves J.D., Ramer M.S., and Tetzlaff W. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J. Neurosci. 24 (2004) 2182-2190
87. Stokes B.T., Noyes D.H., and Behrmann D.L. An electromechanical spinal injury technique with dynamic sensitivity. J. Neurotrauma 9 (1992) 187-195
88. Stone J.R., Rubin D.G., Dialo A.O., Okonkwo D.O., and Helm G.A. Relationship of 40 kD, 10 kD, and 3 kD fluorescent indicators of alterted axolemmal permeability to impaired axoplasmic transport in traumatic axonal injury. J. Neurotrauma 19 (2002) 1278 (Abstract)
89. Stone J.R., Okonkwo D.O., Dialo A.O., Rubin D.G., Mutlu L.K., Povlishock J.T., and Helm G.A. Impaired axonal transport and altered axolemmal permeability occur in distinct populations of damaged axons following traumatic brain injury. Exp. Neurol. 190 (2004) 59-69
90. Sugawara T., Lewen A., Gasche Y., Yu F., and Chan P.H. Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. FASEB J. 16 (2002) 1997-1999
91. Tadie M., Gaviria M., Mathe J.-F., Menthonnex P., Loubert G., Lagarrigue J., Saint-Marc C., Argenson C., Kempf C., D'Arbigny P., Kamenka J.M., Privat A., and Carli P. Early care and treatment with a neuroprotective drug, Gacyclidine, in patients with acute spinal cord injury. Rachis 15 (2003) 363-376
92. Tator C.H. Spine-spinal cord relationships in spinal cord trauma. Clin. Neurosurg. 30 (1983) 479-494
93. Tator C.H. Hemodynamic issues and vascular factors in acute experimental spinal cord injury. J. Neurotrauma 9 (1992) 139-140 discussion 141
94. Tator C.H. Review of treatment trials in human spinal cord injury: issues, difficulties, and recommendations. Neurosurgery 59 (2006) 957-982 discussion 982-957
95. Tator C.H., and Fehlings M.G. Review of clinical trials of neuroprotection in acute spinal cord injury. Neurosurg. Focus 6 (1999) e8
96. Teng Y.D., Choi H., Onario R.C., Zhu S., Desilets F.C., Lan S., Woodard E.J., Snyder E.Y., Eichler M.E., and Friedlander R.M. Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 3071-3076
97. Vanderluit J.L., McPhail L.T., Fernandes K.J., Kobayashi N.R., and Tetzlaff W. In vivo application of mitochondrial pore inhibitors blocks the induction of apoptosis in axotomized neonatal facial motoneurons. Cell Death Differ. 10 (2003) 969-976
98. Vercelli A., Repici M., Garbossa D., and Grimaldi A. Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res. Bull. 51 (2000) 11-28
99. Wrathall J.R., Teng Y.D., and Choiniere D. Amelioration of functional deficits from spinal cord trauma with systemically administered NBQX, an antagonist of non-N-methyl-D-aspartate receptors. Exp. Neurol. 137 (1996) 119-126
100. Wrathall J.R., Teng Y.D., and Marriott R. Delayed antagonism of AMPA/kainate receptors reduces long-term functional deficits resulting from spinal cord trauma. Exp. Neurol. 145 (1997) 565-573
101. Xiong Y., Rabchevsky A.G., and Hall E.D. Role of peroxynitrite in secondary oxidative damage after spinal cord injury. J. Neurochem. 100 (2007) 639-649
102. Xu J., Fan G., Chen S., Wu Y., Xu X.M., and Hsu C.Y. Methylprednisolone inhibition of TNF-alpha expression and NF-kB activation after spinal cord injury in rats. Brain Res. Mol. Brain Res. 59 (1998) 135-142
103. Zar J.H. Biostatistical Analysis (1999), Prentice Hall, New Jersey