Critical Appraisal of Neuroprotection Trials in Head Injury: What Have We Learned?

NeuroRx

Volumn 1, Issue 1, 2004, Pages 71-79

  Tolias, Christos M ^a   Bullock, M Ross ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Head injury; neuroprotection; translational research; trial design; trials

Indexed keywords

4 (3 PHOSPHONOALLYL) 2 PIPERAZINECARBOXYLIC ACID; 4 PHOSPHONOMETHYLPIPECOLIC ACID; ADENOSINE RECEPTOR BLOCKING AGENT; AMPA RECEPTOR ANTAGONIST; APTIGANEL; BAY 38 7271; BAY 44 2041; CANNABINOID RECEPTOR AGONIST; CORTICOSTEROID; CYCLOSPORIN A; DELTIBANT; DEXAMETHASONE; DEXANABINOL; ELIPRODIL; GLUTAMATE CARBOXYPEPTIDASE II INHIBITOR; LANICEMINE; MAGNESIUM SULFATE; NIMODIPINE; NS 1209; OMEGA CONOTOXIN MVIIA; PROGESTERONE; S 1746; SUPEROXIDE DISMUTASE; TIRILAZAD; TOPIRAMATE; TRAXOPRODIL; TRIAMCINOLONE; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT;

APOPTOSIS; ARTICLE; AXONAL INJURY; BRAIN EDEMA; BRAIN MITOCHONDRION; CLINICAL TRIAL; EXCITOTOXICITY; HEAD INJURY; HUMAN; INDUCED HYPOTHERMIA; NERVE CELL NECROSIS; NEUROPROTECTION; PATHOPHYSIOLOGY; TRAUMATIC BRAIN INJURY; ANIMAL; METHODOLOGY; REVIEW;

ANIMALS; CLINICAL TRIALS; CRANIOCEREBRAL TRAUMA; HUMANS; NEUROPROTECTIVE AGENTS; RESEARCH DESIGN;

EID: 5444245546     PISSN: 15455343     EISSN: 15455351     Source Type: Journal    
DOI: 10.1602/neurorx.1.1.71     Document Type: Article

References (79)

1. Kay A., and Teasdale G. Head injury in the United Kingdom. World J Surg 25 (2001) 1210-1220
2. Narayan R., Michael M., and The Clinical Trials in Head Injury Study Group. Clinical trials in head injury. J Neurotrauma 19 (2002) 503-557
3. Murray C., and Lopez A. Global mortality, disability and the contribution of the risk factors: global burden of disease study. Lancet 349 (1997) 1436-1442
4. Bullock R., Lyeth B., and Muizelaar J. Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery 45 (1999) 207-220
5. Choi D., Maulucci-Gedde M., and Kriegstein A. Glutamate neurotoxicity in cortical cell culture. J Neurosci 7 (1987) 357-368
6. Faden A., Demediuk P., Panter S., and Vink R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244 (1989) 798-800
7. Bredt D., and Snyder S. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86 (1989) 9030-9033
8. Yakovlev A., Knoblach S., Fan L., Fox G., Goodnight R., and Faden A. Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 17 (1997) 7415-7424
9. Zhang J., Dawson V., Dawson T., and Snyder S. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263 (1994) 687-689
10. Ha H., and Snyder S. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 96 (1999) 13978-13982
11. Mandir A., Poitras M., Berliner A., Herring W., Guastella D., Feldman A., et al. NMDA but not non-NMDA excitotoxicity is mediated by Poly(ADP-ribose) polymerase. J Neurosci 20 (2000) 8005-8011
12. Bullock R., Kuroda Y., Teasdale G., and McCulloch J. Prevention of post-traumatic excitotoxic brain damage with NMDA antagonist drugs: a new strategy for the nineties. Acta Neurochir Suppl (Wien) 55 (1992) 49-55
13. Choi D. Calcium and excitotoxic neuronal injury. Ann NY Acad Sci 747 (1994) 162-171
14. Unterberg A., and Baethmann A. The kallikrein-kinin system as mediator in vasogenic brain edema. Part 1: cerebral exposure to bradykinin and plasma. J Neurosurg 61 (1984) 87-96
15. Maier-Hauff K., Baethmann A., Lange M., Schurer L., and Unterberg A. The kallikrein-kinin system as mediator in vasogenic brain edema. Part 2: studies on kinin formation in focal and perifocal brain tissue. J Neurosurg 61 (1984) 97-106
16. Unterberg A., Dautermann C., Baethmann A., and Muller-Esterl W. The kallikrein-kinin system as mediator in vasogenic brain edema. Part 3: inhibition of the kallikrein-kinin system in traumatic brain swelling. J Neurosurg 64 (1986) 269-276
17. Marmarou A., Nichols J., Burgess J., Newell D., Troha J., Burnham D., and Pitts L. Effects of the bradykinin antagonist Bradycor (deltibant, CP-1027) in severe traumatic brain injury: results of a multi-center, randomized, placebo-controlled trial. American Brain Injury Consortium Study Group. J Neurotrauma 16 (1999) 431-444
18. Sahuquillo-Barris J., Lamarca-Ciuro J., Vilalta-Castan J., Rubio-Garcia E., and Rodriguez-Pazos M. Acute subdural hematoma and diffuse axonal injury after severe head trauma. J Neurosurg 68 (1988) 894-900
19. Gentleman S., Roberts G., Gennarelli T., Maxwell W., Adams J., Kerr S., et al. Axonal injury: a universal consequence of fatal closed head injury?. Acta Neuropathol (Berl) 89 (1995) 537-543
20. Reinert M., and Bullock R. Clinical trials in head injury. Neurol Res 21 (1999) 330-338
21. Smith D., Nonaka M., Miller R., Leoni M., Chen X., Alsop D., et al. Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J Neurosurg 93 (2000) 315-322
22. Maxwell W., Povlishock J., and Graham D. A mechanistic analysis of nondisruptive axonal injury: a review. J Neurotrauma 14 (1997) 419-440
23. Pettus E., Christman C., Giebel M., and Povlishock J. Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J Neurotrauma 11 (1994) 507-522
24. Okonkwo D., and Povlishock J. An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J Cereb Blood Flow Metab 19 (1999) 443-451
25. Lifshitz J., Friberg H., Neumar R., Raghupathi R., Welsh F., Janmey P., et al. Structural and functional damage sustained by mitochondria after traumatic brain injury in the rat: evidence for differentially sensitive populations in the cortex and hippocampus. J Cereb Blood Flow Metab 23 (2003) 219-231
26. Tigranian R., and Promyslov M. Peculiarities of oxidative phosphorylation in brain mitochondria with craniocerebral trauma. Ukr Biokhim Zh 41 (1969) 170-173
27. Arai C., and Ozawa K. Studies on the biochemical aspects of brain injuries and brain edema with special reference to functional changes of mitochondria in the brain. Shinkei Kenkyu No Shimpo 9 (1965) 611-622
28. Bakay L., Lee J., Lee G., and Peng J. Experimental cerebral concussion. Part 1: an electron microscopic study. J Neurosurg 47 (1977) 525-531
29. Yang M., DeWitt D., Becker D., and Hayes R. Regional brain metabolite levels following mild experimental head injury in the cat. J Neurosurg 63 (1985) 617-621
30. Ankarcrona M., Dypbukt J., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S., and Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15 (1995) 961-973
31. Uchino H., Elmer E., Uchino K., Lindvall O., and Siesjo B. Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischemia in the rat. Acta Physiol Scand 155 (1995) 469-471
32. Xiong Y., Gu Q., Peterson P., Muizelaar J., and Lee C. Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J Neurotrauma 14 (1997) 23-34
33. Clausen T., Zauner A., Levasseur J., Rice A., and Bullock R. Induced mitochondrial failure in the feline brain: implications for understanding acute post-traumatic metabolic events. Brain Res 908 (2001) 35-48
34. Verweij B., Muizelaar J., Vinas F., Peterson P., Xiong Y., and Lee C. Mitochondrial dysfunction after experimental and human brain injury and its possible reversal with a selective N-type calcium channel antagonist (SNX-111). Neurol Res 19 (1997) 334-339
35. Buki A., Okonkwo D., and Povlishock J. Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J Neurotrauma 16 (1999) 511-521
36. Alessandri B., Rice A., Levasseur J., DeFord M., Hamm R., and Bullock M. Cyclosporin A improves brain tissue oxygen consumption and learning/memory performance after lateral fluid percussion injury in rats. J Neurotrauma 19 (2002) 829-841
37. MacManus J., Buchan A., Hill I., Rasquinha I., and Preston E. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 164 (1993) 89-92
38. Beilharz E., Williams C., Dragunow M., Sirimanne E., and Gluckman P. Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Brain Res Mol Brain Res 29 (1995) 1-14
39. Rink A., Fung K., Trojanowski J., Lee V., Neugebauer E., and McIntosh T. Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 147 (1995) 1575-1583
40. Buki A., Okonkwo D., Wang K., and Povlishock J. Cytochrome c release and caspase activation in traumatic axonal injury. J Neurosci 20 (2000) 2825-2834
41. Sullivan P., Keller J., Bussen W., and Scheff S. Cytochrome c release and caspase activation after traumatic brain injury. Brain Res 949 (2002) 88-96
42. Yakovlev A., and Faden A. Caspase-dependent apoptotic pathways in CNS injury. Mol Neurobiol 24 (2001) 131-144
43. Bullock R., Zauner A., Myseros J., Marmarou A., Woodward J., and Young H. Evidence for prolonged release of excitatory amino acids in severe human head trauma. Relationship to clinical events. Ann NY Acad Sci 765 (1995) 290-297
44. Gopinath S., Valadka A., Goodman J., and Robertson C. Extracellular glutamate and aspartate in head injured patients. Acta Neurochir Suppl 76 (2000) 437-438
45. Tolias C., Richards D., Bowery N., and Sgouros S. Extracellular glutamate in the brains of children with severe head injuries: a pilot microdialysis study. Childs Nerv Syst 18 (2002) 368-374
46. Sarrafzadeh A., Sakowitz O., Callsen T., Lanksch W., and Unterberg A. Detection of secondary insults by brain tissue pO2 and bedside microdialysis in severe head injury. Acta Neurochir Suppl 81 (2002) 319-321
47. Khaldi A., Chiueh C., Bullock M., and Woodward J. The significance of nitric oxide production in the brain after injury. Ann NY Acad Sci 962 (2002) 53-59
48. Silberstein M., Lane D., Dodd S., and Opeskin K. Identification of a by-product of nitric oxide synthase activity in human acute brain injury with in vivo proton magnetic resonance spectroscopy. Am J Neuroradiol 23 (2002) 389-392
49. Kasprzak H., Wozniak A., Drewa G., and Wozniak B. Enhanced lipid peroxidation processes in patients after brain contusion. J Neurotrauma 18 (2001) 793-797
50. Reinert M., Hoelper B., Doppenberg E., Zauner A., and Bullock R. Substrate delivery and ionic balance disturbance after severe human head injury. Acta Neurochir Suppl 76 (2000) 439-444
51. Hutchinson P., Gupta A., Fryer T., Al-Rawi P., Chatfield D., Coles J., et al. Correlation between cerebral blood flow, substrate delivery, and metabolism in head injury: a combined microdialysis and triple oxygen positron emission tomography study. J Cereb Blood Flow Metab 22 (2002) 735-745
52. Robertson C. Management of cerebral perfusion pressure after traumatic brain injury. Anesthesiology 95 (2001) 1513-1517
53. Steiner L., Czosnyka M., Piechnik S., Smielewski P., Chatfield D., Menon D., et al. Continuous monitoring of cerebrovascular pressure reactivity allows determination of optimal cerebral perfusion pressure in patients with traumatic brain injury. Crit Care Med 30 (2002) 733-738
54. Czosnyka M., Smielewski P., Piechnik S., Steiner L., and Pickard J. Cerebral autoregulation following head injury. J Neurosurg 95 (2001) 756-763
55. Eker C., Asgeirsson B., Grande P., Schalen W., and Nordstrom C. Improved outcome after severe head injury with a new therapy based on principles for brain volume regulation and preserved microcirculation. Crit Care Med 26 (1998) 1881-1886
56. Povlishock J., Hayes R., Michel M., and McIntosh T. Workshop on animal models of traumatic brain injury. J Neurotrauma 11 (1994) 723-732
57. Statler K., Jenkins L., Dixon C., Claek R., Marion D., and Kochanek P. The simple model versus the super model: translating experimental traumatic brain injury research to the bedside. J Neurotrauma 18 (2001) 1195-1206
58. Faden A. Neuroprotection and traumatic brain injury: theoretical option or realistic proposition. Curr Opin Neurol 15 (2002) 707-712
59. Bramlett H., and Dietrich W. Neuropathological protection after traumatic brain injury in intact female rats versus males or ovariectomized females. J Neurotrauma 18 (2001) 891-900
60. Farin A., Deutsch R., Biegon A., and Marshall L. Sex-related differences in patients with severe head injury: greater susceptibility to brain swelling in female patients 50 years of age and younger. J Neurosurg 98 (2003) 32-36
61. Alves O., Doyle A., Gilman C., Sarkar M., Young H., and Bullock R. Evaluation of topiramate neuroprotective effect in severe TBI by using microdialysis. Abstract of oral presentation at AANS Meeting, San Diego, 2003. J Neurosurg 98 (2003) 712
62. Dickinson K., Bunn F., Wentz R., Edwards P., and Roberts I. Size and quality of randomized controlled trials in head injury: review of published studies. Br Med J 320 (2000) 1308-1311
63. MRC CRASH Trial National Coordinators. Update on progress in the international multicenter, randomized, controlled trial of corticosteroids after significant head injury (Medical Research Council CRASH Trial). Curr Opin Crit Care 9 (2003) 92-97
64. Clifton G., Miller E., Choi S., Levin H., McCauley S., Smith Jr. K., et al. Lack of effect of induction of hypothermia after acute brain injury. N Engl J Med 344 (2001) 556-563
65. Hukkelhoven C., Steyerberg E., Farace E., Habbema J., Marshall L., and Maas A. Regional differences in patient characteristics, case management, and outcomes in traumatic brain injury: experience from the tirilazad trials. J Neurosurg 97 (2002) 549-557
66. Clifton G., Choi S., Miller E., Levin H., Smith Jr. K., Muizelaar J., et al. Intercenter variance in clinical trials of head trauma-experience of the National Acute Brain Injury Study: Hypothermia. J Neurosurg 95 (2001) 751-755
67. Marshall L. Intercenter variance. J Neurosurg 95 (2001) 733-734
68. Teasdale G. Comment on Bullock R, Lyeth BG, Muizelaar JP. Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery 45 (1999) 207-220
69. Rothermundt M., Peters M., Prehn J., and Arolt V. S100B in brain damage and neurodegeneration. Mic Res Tech 60 (2003) 614-632
70. Anderson R., Hansson L., Nilsson O., Liska J., and Settegren G. High serum S100B levels for trauma patients without head injuries. Neurosurgery 48 (2001) 1255-1260
71. Alderson P., and Roberts I. Corticosteroids in acute traumatic brain injury: systematic review of randomized controlled trials. Br Med J 314 (1997) 1855-1859
72. Grumme T., Baethmann A., Kolodziejczyk D., Krimmer J., Fischer M., von Eisenhart Rothe B., et al. Treatment of patients with severe head injury by triamcinolone: a prospective, controlled multicenter clinical trial of 396 cases. Res Exp Med (Berl) 195 (1995) 217-229
73. Marshall L., Maas A., Marshall S., Bricolo A., Fearnside M., Iannotti F., et al. A multicenter trial on the efficacy of using tirilazad mesylate in cases of head injury. J Neurosurg 89 (1998) 519-525
74. Marmarou A., Nichols J., Burgess J., Newell D., Troha J., Burnham D., and Pitts L. Effects of the bradykinin antagonist Bradycor (deltibant, CP-1027) in severe traumatic brain injury: results of a multi-center, randomized, placebo-controlled trial. American Brain Injury Consortium Study Group. J Neurotrauma 16 (1999) 431-444
75. Knoller N., Levi L., Shoshan I., Reichenthal E., Razon N., Rappaport Z., et al. Dexanabinol (HU-211) in the treatment of severe closed head injury: a randomized, placebo-controlled, phase II clinical trial. Crit Care Med 30 (2002) 548-554
76. Robertson C., Valadka A., Hannay H., Contant C., Gopinath S., Cormio M., et al. Prevention of secondary ischemic insults after severe head injury. Crit Care Med 27 (1999) 2086-2095
77. Mauler F., Mittendorf J., Horvath E., and De Vry J. Characterization of the diarylether sulfonylester (-)-(R)-3-(2-hydroxymethylindanyl-4-oxy)phenyl-4,4,4-trifluoro-1-sulfonate (BAY 38-7271) as a potent cannabinoid receptor agonist with neuroprotective properties. J Pharmacol Exp Ther 302 (2002) 359-368
78. Fumoto N., Nakatsuka H., Ohta S., Kumon Y., and Ohnishi T. Hippocampal CA1 neuron survival and cytosolic FKBP12, the 12 kDa FK506-binding protein, after ischemia and tacrolimus treatment in gerbils. Neurosci Lett 339 (2003) 219-222
79. Jackson P., Tays K., Maclin K., Ko Y., Li W., Vitharana D., et al. Design and pharmacological activity of phosphinic acid based NAALADase inhibitors. J Med Chem 44 (2001) 4170-4175