Emerging experimental therapies for intracerebral hemorrhage: Targeting mechanisms of secondary brain injury

Neurosurgical Focus

Volumn 34, Issue 5, 2013, Pages

  Belur, Praveen K ^a   Chang, Jason J ^b   He, Shuhan ^a   Emanuel, Benjamin A ^b   Mack, William J ^c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Division of Neurocritical Care Stroke   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Animal model; Intracerebral hemorrhage; Neuroprotection; Pathophysiology; Secondary brain injury; Therapeutic intervention

Indexed keywords

ANTICOAGULANT AGENT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR;

BRAIN HEMORRHAGE; BRAIN INJURY; EXPERIMENTAL THERAPY; HUMAN; REVIEW; BRAIN INJURIES; CEREBRAL HEMORRHAGE; COMPLICATION;

ANTICOAGULANTS; BRAIN INJURIES; CEREBRAL HEMORRHAGE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; THERAPIES, INVESTIGATIONAL;

EID: 84879005737     PISSN: None     EISSN: 10920684     Source Type: Journal    
DOI: 10.3171/2013.2.FOCUS1317     Document Type: Article

References (96)

1. Anderson CS, Huang Y, Arima H, Heeley E, Skulina C, Parsons MW, et al: Effects of early intensive blood pressure-lowering treatment on the growth of hematoma and perihematomal edema in acute intracerebral hemorrhage: the Intensive Blood Pressure Reduction in Acute Cerebral Haemorrhage Trial (INTERACT). Stroke 41:307-312, 2010
2. Anderson CS, Huang Y, Wang JG, Arima H, Neal B, Peng B, et al: Intensive blood pressure reduction in acute cerebral haemorrhage trial (INTERACT): a randomised pilot trial. Lancet Neurol 7:391-399, 2008
3. Auriat AM, Silasi G, Wei Z, Paquette R, Paterson P, Nichol H, et al: Ferric iron chelation lowers brain iron levels after intracerebral hemorrhage in rats but does not improve outcome. Exp Neurol 234:136-143, 2012
4. Babu R, Bagley JH, Di C, Friedman AH, Adamson C: Thrombin and hemin as central factors in the mechanisms of intracerebral hemorrhage-induced secondary brain injury and as potential targets for intervention. Neurosurg Focus 32(4):E8, 2012
5. Barone FC, Feuerstein GZ: Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19:819-834, 1999
6. Beray-Berthat V, Delifer C, Besson VC, Girgis H, Coqueran B, Plotkine M, et al: Long-term histological and behavioural characterisation of a collagenase-induced model of intracerebral haemorrhage in rats. J Neurosci Methods 191:180-190, 2010
7. Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, et al: Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med 346:557-563, 2002
8. Broderick JP, Brott TG, Tomsick T, Barsan W, Spilker J: Ultraearly evaluation of intracerebral hemorrhage. J Neurosurg 72: 195-199, 1990
9. Colbourne F, Corbett D: Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection. J Neurosci 15:7250-7260, 1995
10. Colbourne F, Corbett D, Zhao Z, Yang J, Buchan AM: Prolonged but delayed postischemic hypothermia: a long-term outcome study in the rat middle cerebral artery occlusion model. J Cereb Blood Flow Metab 20:1702-1708, 2000
11. Cui JJ, Wang D, Gao F, Li YR: Effects of atorvastatin on pathological changes in brain tissue and plasma MMP-9 in rats with intracerebral hemorrhage. Cell Biochem Biophys 62: 87-90, 2012
12. Daverat P, Castel JP, Dartigues JF, Orgogozo JM: Death and functional outcome after spontaneous intracerebral hemorrhage. A prospective study of 166 cases using multivariate analysis. Stroke 22:1-6, 1991
13. Deinsberger W, Vogel J, Kuschinsky W, Auer LM, Böker DK: Experimental intracerebral hemorrhage: description of a double injection model in rats. Neurol Res 18:475-477, 1996
14. Fayad PB, Awad IA: Surgery for intracerebral hemorrhage. Neurology 51 (3 Suppl 3):S69-S73, 1998
15. Fingas M, Clark DL, Colbourne F: The effects of selective brain hypothermia on intracerebral hemorrhage in rats. Exp Neurol 208:277-284, 2007
16. Fingas M, Penner M, Silasi G, Colbourne F: Treatment of intracerebral hemorrhage in rats with 12 h, 3 days and 6 days of selective brain hypothermia. Exp Neurol 219:156-162, 2009
17. 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 40:2244- 2250, 2009
18. Giancotti FG, Ruoslahti E: Integrin signaling. Science 285: 1028-1032, 1999
19. Gong Y, Hua Y, Keep RF, Hoff JT, Xi G: Intracerebral hemorrhage: effects of aging on brain edema and neurological deficits. Stroke 35:2571-2575, 2004
20. Görgen I, Hartung T, Leist M, Niehörster M, Tiegs G, Uhlig S, et al: Granulocyte colony-stimulating factor treatment protects rodents against lipopolysaccharide-induced toxicity via suppression of systemic tumor necrosis factor-alpha. J Immunol 149:918-924, 1992
21. Grasso G, Graziano F, Sfacteria A, Carletti F, Meli F, Maugeri R, et al: Neuroprotective effect of erythropoietin and darbepoetin alfa after experimental intracerebral hemorrhage. Neurosurgery 65:763-770, 2009
22. Gu Y, Hua Y, He Y, Wang L, Hu H, Keep RF, et al: Iron accumulation and DNA damage in a pig model of intracerebral hemorrhage. Acta Neurochir Suppl 111:123-128, 2011
23. Gu Y, Hua Y, Keep RF, Morgenstern LB, Xi G: Deferoxamine reduces intracerebral hematoma-induced iron accumulation and neuronal death in piglets. Stroke 40:2241-2243, 2009
24. Hankey GJ, Hon C: Surgery for primary intracerebral hemorrhage: is it safe and effective? A systematic review of case series and randomized trials. Stroke 28:2126-2132, 1997
25. Hartung T, Döcke WD, Gantner F, Krieger G, Sauer A, Stevens P, et al: Effect of granulocyte colony-stimulating factor treatment on ex vivo blood cytokine response in human volunteers. Blood 85:2482-2489, 1995
26. Hatakeyama T, Okauchi M, Hua Y, Keep RF, Xi G: Deferoxamine reduces cavity size in the brain after intracerebral hemorrhage in aged rats. Acta Neurochir Suppl 111:185-190, 2011
27. Hua Y, Keep RF, Gu Y, Xi G: Thrombin and brain recovery after intracerebral hemorrhage. Stroke 40 (3 SuppL):S88-S89, 2009
28. Hua Y, Keep RF, Hoff JT, Xi G: Brain injury after intracerebral hemorrhage: the role of thrombin and iron. Stroke 38 (2 Suppl):759-762, 2007
29. Hua Y, Wu J, Keep RF, Nakamura T, Hoff JT, Xi G: Tumor necrosis factor-alpha increases in the brain after intracerebral hemorrhage and thrombin stimulation. Neurosurgery 58: 542-550, 2006
30. Hua Y, Xi G, Keep RF, Hoff JT: Complement activation in the brain after experimental intracerebral hemorrhage. J Neurosurg 92:1016-1022, 2000
31. Hwang BY, Appelboom G, Ayer A, Kellner CP, Kotchetkov IS, Gigante PR, et al: Advances in neuroprotective strategies: potential therapies for intracerebral hemorrhage. Cerebrovasc Dis 31:211-222, 2011
32. Jung KH, Chu K, Jeong SW, Han SY, Lee ST, Kim JY, et al: HMG-CoA reductase inhibitor, atorvastatin, promotes sensorimotor recovery, suppressing acute inflammatory reaction after experimental intracerebral hemorrhage. Stroke 35:1744- 1749, 2004
33. Karki K, Knight RA, Han Y, Yang D, Zhang J, Ledbetter KA, et al: Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage. Stroke 40: 3384-3389, 2009
34. Katsuki H: Exploring neuroprotective drug therapies for intracerebral hemorrhage. J Pharmacol Sci 114:366-378, 2010
35. Kawai N, Kawanishi M, Okauchi M, Nagao S: Effects of hypothermia on thrombin-induced brain edema formation. Brain Res 895:50-58, 2001
36. Kawanishi M, Kawai N, Nakamura T, Luo C, Tamiya T, Nagao S: Effect of delayed mild brain hypothermia on edema formation after intracerebral hemorrhage in rats. J Stroke Cerebrovasc Dis 17:187-195, 2008
37. Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T: Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course. Stroke 27:1783-1787, 1996
38. Keberle H: The biochemistry of desferrioxamine and its relation to iron metabolism. Ann N Y Acad Sci 119:758-768, 1964
39. Keep RF, Xi G, Hua Y, Hoff JT: The deleterious or beneficial effects of different agents in intracerebral hemorrhage: think big, think small, or is hematoma size important? Stroke 36: 1594-1596, 2005
40. Kirkman MA, Allan SM, Parry-Jones AR: Experimental intracerebral hemorrhage: avoiding pitfalls in translational research. J Cereb Blood Flow Metab 31:2135-2151, 2011
41. Kitaoka T, Hua Y, Xi G, Hoff JT, Keep RF: Delayed argatroban treatment reduces edema in a rat model of intracerebral hemorrhage. Stroke 33:3012-3018, 2002
42. Knight RA, Han Y, Nagaraja TN, Whitton P, Ding J, Chopp M, et al: Temporal MRI assessment of intracerebral hemorrhage in rats. Stroke 39:2596-2602, 2008
43. Leonardo CC, Robbins S, Doré S: Translating basic science research to clinical application: models and strategies for intracerebral hemorrhage. Front Neurol 3:85, 2012
44. MacLellan CL, Girgis J, Colbourne F: Delayed onset of prolonged hypothermia improves outcome after intracerebral hemorrhage in rats. J Cereb Blood Flow Metab 24:432-440, 2004
45. Manaenko A, Chen H, Zhang JH, Tang J: Comparison of different preclinical models of intracerebral hemorrhage. Acta Neurochir Suppl 111:9-14, 2011
46. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al: Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 358:2127-2137, 2008
47. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al: Recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 352:777-785, 2005
48. Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, et al: Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial. Lancet 365:387-397, 2005
49. Nagatsuna T, Nomura S, Suehiro E, Fujisawa H, Koizumi H, Suzuki M: Systemic administration of argatroban reduces secondary brain damage in a rat model of intracerebral hemorrhage: histopathological assessment. Cerebrovasc Dis 19:192- 200, 2005
50. Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G: Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg 100:672-678, 2004
51. Nakamura T, Kuroda Y, Hosomi N, Okabe N, Kawai N, Tamiya T, et al: Serine protease inhibitor attenuates intracerebral hemorrhage-induced brain injury and edema formation in rat. Acta Neurochir Suppl 106:307-310, 2010
52. Naval NS, Abdelhak TA, Urrunaga N, Zeballos P, Mirski MA, Carhuapoma JR: An association of prior statin use with decreased perihematomal edema. Neurocrit Care 8:13-18, 2008
53. Naval NS, Abdelhak TA, Zeballos P, Urrunaga N, Mirski MA, Carhuapoma JR: Prior statin use reduces mortality in intracerebral hemorrhage. Neurocrit Care 8:6-12, 2008
54. Okauchi M, Hua Y, Keep RF, Morgenstern LB, Schallert T, Xi G: Deferoxamine treatment for intracerebral hemorrhage in aged rats: therapeutic time window and optimal duration. Stroke 41:375-382, 2010
55. Okauchi M, Hua Y, Keep RF, Morgenstern LB, Xi G: Effects of deferoxamine on intracerebral hemorrhage-induced brain injury in aged rats. Stroke 40:1858-1863, 2009
56. Park HK, Chu K, Lee ST, Jung KH, Kim EH, Lee KB, et al: Granulocyte colony-stimulating factor induces sensorimotor recovery in intracerebral hemorrhage. Brain Res 1041:125- 131, 2005
57. Plane JM, Shen Y, Pleasure DE, Deng W: Prospects for minocycline neuroprotection. Arch Neurol 67:1442-1448, 2010
58. Qing WG, Dong YQ, Ping TQ, Lai LG, Fang LD, Min HW, et al: Brain edema after intracerebral hemorrhage in rats: the role of iron overload and aquaporin 4. Laboratory investigation. J Neurosurg 110:462-468, 2009
59. Qureshi AI: Antihypertensive Treatment of Acute Cerebral Hemorrhage (ATACH): rationale and design. Neurocrit Care 6:56-66, 2007
60. Qureshi AI, Palesch YY: Antihypertensive Treatment of Acute Cerebral Hemorrhage (ATACH) II: design, methods, and rationale. Neurocrit Care 15:559-576, 2011
61. Rosenberg GA: Matrix metalloproteinases in neuroinflammation. Glia 39:279-291, 2002
62. Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M: Collagenase- induced intracerebral hemorrhage in rats. Stroke 21: 801-807, 1990
63. Sangha N, Gonzales NR: Treatment targets in intracerebral hemorrhage. Neurotherapeutics 8:374-387, 2011
64. Schäbitz WR, Kollmar R, Schwaninger M, Juettler E, Bardutzky J, Schölzke MN, et al: Neuroprotective effect of granulocyte colony-stimulating factor after focal cerebral ischemia. Stroke 34:745-751, 2003
65. Schneider A, Krüger C, Steigleder T, Weber D, Pitzer C, Laage R, et al: The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest 115:2083-2098, 2005
66. Selim M, Yeatts S, Goldstein JN, Gomes J, Greenberg S, Morgenstern LB, et al: Safety and tolerability of deferoxamine mesylate in patients with acute intracerebral hemorrhage. Stroke 42:3067-3074, 2011
67. Seyfried D, Han Y, Lu D, Chen J, Bydon A, Chopp M: Improvement in neurological outcome after administration of atorvastatin following experimental intracerebral hemorrhage in rats. J Neurosurg 101:104-107, 2004
68. Shi W, Wang Z, Pu J, Wang R, Guo Z, Liu C, et al: Changes of blood-brain barrier permeability following intracerebral hemorrhage and the therapeutic effect of minocycline in rats. Acta Neurochir Suppl 110:61-67, 2011
69. Siesjö BK: Mechanisms of ischemic brain damage. Crit Care Med 16:954-963, 1988
70. Sinar EJ, Mendelow AD, Graham DI, Teasdale GM: Experimental intracerebral hemorrhage: effects of a temporary mass lesion. J Neurosurg 66:568-576, 1987
71. Sobrino T, Arias S, Rodríguez-González R, Brea D, Silva Y, de la Ossa NP, et al: High serum levels of growth factors areassociated with good outcome in intracerebral hemorrhage. J Cereb Blood Flow Metab 29:1968-1974, 2009
72. Song S, Hua Y, Keep RF, Hoff JT, Xi G: A new hippocampal model for examining intracerebral hemorrhage-related neuronal death: effects of deferoxamine on hemoglobin-induced neuronal death. Stroke 38:2861-2863, 2007
73. Staykov D, Wagner I, Volbers B, Doerfler A, Schwab S, Kollmar R: Mild prolonged hypothermia for large intracerebral hemorrhage. Neurocrit Care 18:178-183, 2013
74. Sun Z, Zhao Z, Zhao S, Sheng Y, Zhao Z, Gao C, et al: Recombinant hirudin treatment modulates aquaporin-4 and aquaporin- 9 expression after intracerebral hemorrhage in vivo. Mol Biol Rep 36:1119-1127, 2009
75. Szymanska A, Biernaskie J, Laidley D, Granter-Button S, Corbett D: Minocycline and intracerebral hemorrhage: influence of injury severity and delay to treatment. Exp Neurol 197:189-196, 2006
76. Tapia-Perez H, Sanchez-Aguilar M, Torres-Corzo JG, Rodriguez- Leyva I, Gonzalez-Aguirre D, Gordillo-Moscoso A, et al: Use of statins for the treatment of spontaneous intracerebral hemorrhage: results of a pilot study. Cent Eur Neurosurg 70:15-20, 2009
77. Thiex R, Tsirka SE: Brain edema after intracerebral hemorrhage: mechanisms, treatment options, management strategies, and operative indications. Neurosurg Focus 22(5):E6, 2007
78. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ: Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol 9:167-176, 2010
79. Vespa P, McArthur D, Miller C, O'Phelan K, Frazee J, Kidwell C, et al: Frameless stereotactic aspiration and thrombolysis of deep intracerebral hemorrhage is associated with reduction of hemorrhage volume and neurological improvement. Neurocrit Care 2:274-281, 2005
80. Wang J, Fields J, Zhao C, Langer J, Thimmulappa RK, Kensler TW, et al: Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic Biol Med 43: 408-414, 2007
81. Wang J, Tsirka SE: Tuftsin fragment 1-3 is beneficial when delivered after the induction of intracerebral hemorrhage. Stroke 36:613-618, 2005
82. Warkentin LM, Auriat AM, Wowk S, Colbourne F: Failure of deferoxamine, an iron chelator, to improve outcome after collagenase-induced intracerebral hemorrhage in rats. Brain Res 1309:95-103, 2010
83. Wasserman JK, Schlichter LC: Minocycline protects the blood-brain barrier and reduces edema following intracerebral hemorrhage in the rat. Exp Neurol 207:227-237, 2007
84. Wasserman JK, Schlichter LC: Neuron death and inflammation in a rat model of intracerebral hemorrhage: effects of delayed minocycline treatment. Brain Res 1136:208-218, 2007
85. Wasserman JK, Zhu X, Schlichter LC: Evolution of the inflammatory response in the brain following intracerebral hemorrhage and effects of delayed minocycline treatment. Brain Res 1180:140-154, 2007
86. Wu H, Wu T, Xu X, Wang J, Wang J: Iron toxicity in mice with collagenase-induced intracerebral hemorrhage. J Cereb Blood Flow Metab 31:1243-1250, 2011
87. Wu J, Yang S, Hua Y, Liu W, Keep RF, Xi G: Minocycline attenuates brain edema, brain atrophy and neurological deficits after intracerebral hemorrhage. Acta Neurochir Suppl 106: 147-150, 2010
88. Wu J, Yang S, Xi G, Fu G, Keep RF, Hua Y: Minocycline reduces intracerebral hemorrhage-induced brain injury. Neurol Res 31:183-188, 2009
89. Xi G, Keep RF, Hoff JT: Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5:53-63, 2006
90. Yang D, Knight RA, Han Y, Karki K, Zhang J, Ding C, et al: Vascular recovery promoted by atorvastatin and simvastatin after experimental intracerebral hemorrhage: magnetic resonance imaging and histological study. Laboratory investigation. J Neurosurg 114:1135-1142, 2011
91. Yang GY, Betz AL, Chenevert TL, Brunberg JA, Hoff JT: Experimental intracerebral hemorrhage: relationship between brain edema, blood flow, and blood-brain barrier permeability in rats. J Neurosurg 81:93-102, 1994
92. Yang S, Song S, Hua Y, Nakamura T, Keep RF, Xi G: Effects of thrombin on neurogenesis after intracerebral hemorrhage. Stroke 39:2079-2084, 2008
93. Zacco A, Togo J, Spence K, Ellis A, Lloyd D, Furlong S, et al: 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors protect cortical neurons from excitotoxicity. J Neurosci 23:11104-11111, 2003
94. Zazulia AR, Diringer MN, Videen TO, Adams RE, Yundt K, Aiyagari V, et al: Hypoperfusion without ischemia surrounding acute intracerebral hemorrhage. J Cereb Blood Flow Metab 21:804-810, 2001
95. Zhang L, Shu XJ, Zhou HY, Liu W, Chen Y, Wang CL, et al: Protective effect of granulocyte colony-stimulating factor on intracerebral hemorrhage in rat. Neurochem Res 34:1317- 1323, 2009
96. Zhao F, Hua Y, He Y, Keep RF, Xi G: Minocycline-induced attenuation of iron overload and brain injury after experimental intracerebral hemorrhage. Stroke 42:3587-3593, 2011