Intracranial hemorrhage: Mechanisms of secondary brain injury

Acta Neurochirurgica, Supplementum

Volumn , Issue 111, 2011, Pages 63-69

  Lok, Josephine ^a   Leung, Wendy ^a   Murphy, Sarah ^a   Butler, William ^a   Noviski, Natan ^a   Lo, Eng H ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Coagulation; Heme toxicity; Inflammation; Intracranial hemorrhage; Iron toxicity; Vascular response

Indexed keywords

BILIRUBIN; HAPTOGLOBIN; HEME; MATRIX METALLOPROTEINASE; OXYHEMOGLOBIN; THROMBIN;

ASTROCYTE; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; BLOOD TOXICITY; BLOOD VESSEL REACTIVITY; BRAIN HEMORRHAGE; BRAIN INJURY; CELL ACTIVATION; CONFERENCE PAPER; ENDOTHELIAL MICROPARTICLE; ENDOTHELIUM CELL; HUMAN; HYPERCOAGULABILITY; LEUKOCYTE; LEUKOCYTE ACTIVATION; MICROGLIA; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; SECONDARY BRAIN INJURY; SPONTANEOUS INTRACRANIAL HEMORRHAGE; THROMBOCYTE; THROMBOCYTE ACTIVATION; TRAUMATIC INTRACRANIAL HEMORRHAGE; ANIMAL; BLOOD VESSEL; GLIA; METABOLISM; NERVE TRACT; PATHOLOGY; PATHOPHYSIOLOGY; REVIEW;

ANIMALS; BLOOD COAGULATION DISORDERS; BLOOD PLATELETS; BLOOD VESSELS; BRAIN INJURIES; HEME; HUMANS; INTRACRANIAL HEMORRHAGES; LEUKOCYTES; NEURAL PATHWAYS; NEUROGLIA;

EID: 79960665602     PISSN: 00651419     EISSN: 00016268     Source Type: Book Series    
DOI: 10.1007/978-3-7091-0693-8_11     Document Type: Conference Paper

References (65)

1. Narayan RK, Maas AI, Servadei F, Skolnick BE, Tillinger MN, Marshall LF (2008) Progression of traumatic intracerebral hemor¬rhage: a prospective observational study. J Neurotrauma 25: 629-639 (Pubitemid 351918434)
2. White CL, Griffth S, Caron JL (2009) Early progression of traumatic cerebral contusions: characterization and risk factors. J Trauma 67:508-514, discussion 514-505
3. Park JH, Park SW, Kang SH, Nam TK, Min BK, Hwang SN (2009) Detection of traumatic cerebral microbleeds by susceptibility-weighted image of MRI. J Korean Neurosurg Soc 46:365-369
4. Wu HM, Huang SC, Hattori N, Glenn TC, Vespa PM, Hovda DA, Bergsneider M (2004) Subcortical white matter metabolic changes remote from focal hemorrhagic lesions suggest diffuse injury after human traumatic brain injury. Neurosurgery 55:1306-1315, discus¬sion 1316-1307 (Pubitemid 39612873)
5. Immonen RJ, Kharatishvili I, Grohn H, Pitkanen A, Grohn OH (2009) Quantitative MRI predicts long-term structural and func¬tional outcome after experimental traumatic brain injury. Neuro-image 45:1-9
6. Narayan RK, Maas AI, Marshall LF, Servadei F, Skolnick BE, Tillinger MN (2008) Recombinant factor VIIA in traumatic intrac-erebral hemorrhage: results of a dose-escalation clinical trial. Neurosurgery 62:776-786, discussion 786-778
7. Chang EF, Claus CP, Vreman HJ, Wong RJ, Noble-Haeusslein LJ (2005) Heme regulation in traumatic brain injury: relevance to the adult and developing brain. J Cereb Blood Flow Metab 25:1401-1417 (Pubitemid 41541951)
8. Wagner KR, Sharp FR, Ardizzone TD, Lu A, Clark JF (2003) Heme and iron metabolism: role in cerebral hemorrhage. J Cereb Blood Flow Metab 23:629-652 (Pubitemid 36713668)
9. Sharp FR, Massa SM, Swanson RA (1999) Heat-shock protein pro¬tection. Trends Neurosci 22:97-99
10. O'Brien PJ, Little C (1969) Intracellular mechanisms for the decom¬position of a lipid peroxide. II. Decomposition of a lipid peroxide by subcellular fractions. Can J Biochem 47:493-499
11. Zhao X, Song S, Sun G, Strong R, Zhang J, Grotta JC, Aronowski J (2009) Neuroprotective role of haptoglobin after intracerebral hem¬orrhage. J Neurosci 29:15819-15827
12. Wang X, Mori T, Sumii T, Lo EH (2002) Hemoglobin-induced cytotoxicity in rat cerebral cortical neurons: caspase activation and oxidative stress. Stroke 33:1882-1888 (Pubitemid 34761080)
13. Keep RF, Xiang J, Ennis SR, Andjelkovic A, Hua Y, Xi G, Hoff JT (2008) Blood-brain barrier function in intracerebral hemorrhage. Acta Neurochir Suppl 105:73-77
14. Thiex R, Tsirka SE (2007) Brain edema after intracerebral hemor¬rhage: mechanisms, treatment options, management strategies, and operative indications. Neurosurg Focus 22:E6
15. Bhasin RR, Xi G, Hua Y, Keep RF, Hoff JT (2002) Experimental intracerebral hemorrhage: effect of lysed erythrocytes on brain edema and blood-brain barrier permeability. Acta Neurochir Suppl 81:249-251
16. Ferris CD, Jaffrey SR, Sawa A, Takahashi M, Brady SD, Barrow RK, Tysoe SA, Wolosker H, Baranano DE, Dore S, Poss KD, Snyder SH (1999) Haem oxygenase-1 prevents cell death by regu¬lating cellular iron. Nat Cell Biol 1:152-157 (Pubitemid 129656019)
17. Regan RF, Chen J, Benvenisti-Zarom L (2004) Heme oxygenase-2 gene deletion attenuates oxidative stress in neurons exposed to extracellular hemin. BMC Neurosci 5:34. doi:10.1186/1471-2202-5-34 (Pubitemid 40177047)
18. Rogers B, Yakopson V, Teng ZP, Guo Y, Regan RF (2003) Heme oxygenase-2 knockout neurons are less vulnerable to hemoglobin toxicity. Free Radic Biol Med 35:872-881 (Pubitemid 37211441)
19. Baranano DE, Rao M, Ferris CD, Snyder SH (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci USA 99:16093-16098 (Pubitemid 35462754)
20. Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2004) Deferoxamine-induced attenuation of brain edema and neurological defcits in a rat model of intracerebral hemorrhage. J Neurosurg 100:672-678 (Pubitemid 38372849)
21. Xi G, Keep RF, Hoff JT (1998) Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J Neurosurg 89:991-996 (Pubitemid 28544054)
22. Wada T, Oara H, Watanabe K, Kinoshita H, Yachi A (1970) Autoradiographic study on the site of uptake of the haptoglobin-hemoglobin complex. J Reticuloendothel Soc 8:185-193
23. Allison AC, Rees WA (1957) The binding of haemoglobin by plasma proteins (haptoglobins); its bearing on the renal threshold for haemoglobin and the aetiology of haemoglobinuria. Br Med J 2:1137-1143
24. Wang Y, Kinzie E, Berger FG, Lim SK, Baumann H (2001) Haptoglobin, an infammation-inducible plasma protein. Redox Rep 6:379-385
25. Buehler PW, Abraham B, Vallelian F, Linnemayr C, Pereira CP, Cipollo JF, Jia Y, Mikolajczyk M, Boretti FS, Schoedon G, Alayash AI, Schaer DJ (2009) Haptoglobin preserves the CD163 hemoglo¬bin scavenger pathway by shielding hemoglobin from peroxidative modifcation. Blood 113:2578-2586
26. Stein SC, Smith DH (2004) Coagulopathy in traumatic brain injury. Neurocrit Care 1:479-488 (Pubitemid 41278339)
27. Keimowitz RM, Annis BL (1973) Disseminated intravascular coagu¬lation associated with massive brain injury. J Neurosurg 39:178-180
28. Morel N, Morel O, Petit L, Hugel B, Cochard JF, Freyssinet JM, Sztark F, Dabadie P (2008) Generation of procoagulant micropar-ticles in cerebrospinal fuid and peripheral blood after traumatic brain injury. J Trauma 64:698-704 (Pubitemid 351366895)
29. Cohen MJ, Brohi K, Ganter MT, Manley GT, Mackersie RC, Pittet JF (2007) Early coagulopathy after traumatic brain injury: the role of hypoperfusion and the protein C pathway. J Trauma 63:1254-1261, discussion 1261-1252
30. Halpern CH, Reilly PM, Turtz AR, Stein SC (2008) Traumatic coagulopathy: the effect of brain injury. J Neurotrauma 25: 997-1001
31. Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB (2008) Microthrombosis after aneurysmal subarachnoid hemor¬rhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab 28:1761-1770
32. Sugawara T, Jadhav V, Ayer R, Chen W, Suzuki H, Zhang JH (2009) Thrombin inhibition by argatroban ameliorates early brain injury and improves neurological outcomes after experimental subarach-noid hemorrhage in rats. Stroke 40:1530-1532
33. Morel O, Morel N, Freyssinet JM, Toti F (2008) Platelet micropar-ticles and vascular cells interactions: a checkpoint between the hae¬mostatic and thrombotic responses. Platelets 19:9-23 (Pubitemid 351171554)
34. Kai Y, Maeda Y, Sasaki T, Kanaide H, Hirano K (2008) Basic and translational research on proteinase-activated receptors: the role of thrombin receptor in cerebral vasospasm in subarachnoid hemor¬rhage. J Pharmacol Sci 108:426-432
35. Xi G, Reiser G, Keep RF (2003) The role of thrombin and throm-bin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective? J Neurochem 84:3-9. doi:10.1046/j.1471-4159.2003.01268.x [pii] (Pubitemid 36182060)
36. Akopov S, Sercombe R, Seylaz J (1996) Cerebrovascular reactivity: role of endothelium/platelet/leukocyte interactions. Cerebrovasc Brain Metab Rev 8:11-94
37. Auer LM, Leber K, Sayama I (1985) Effect of serotonin and its antagonist ketanserin on pial vessels. J Cereb Blood Flow Metab 5:517-522 (Pubitemid 16218225)
38. Muhonen MG, Robertson SC, Gerdes JS, Loftus CM (1997) Effects of serotonin on cerebral circulation after middle cerebral artery occlusion. J Neurosurg 87:301-306 (Pubitemid 27349118)
39. Khalil Z, Helme RD (1990) Serotonin modulates substance P-induced plasma extravasation and vasodilatation in rat skin by an action through capsaicin-sensitive primary afferent nerves. Brain Res 527:292-298. doi:0006-8993(90)91149-B [pii] (Pubitemid 20290609)
40. Gecse A, Kis B, Mezei Z, Telegdy G (1999) Effects of infamma-tory neuropeptides on the arachidonate cascade of platelets. Int Arch Allergy Immunol 118:166-170 (Pubitemid 29195495)
41. Wang J, Dore S (2007) Infammation after intracerebral hemor¬rhage. J Cereb Blood Flow Metab 27:894-908
42. Weiss SJ (1989) Tissue destruction by neutrophils. N Engl J Med 320:365-376 (Pubitemid 19106873)
43. Stern M, Savill J, Haslett C (1996) Human monocyte-derived mac-rophage phagocytosis of senescent eosinophils undergoing apopto-sis. Mediation by alpha v beta 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am J Pathol 149: 911-921 (Pubitemid 26334175)
44. Lee PY, Pearce FL (1990) Histamine secretion from mast cells stimulated with bradykinin. Agents Actions 30:67-69 (Pubitemid 20142242)
45. Ishikawa M, Zhang JH, Nanda A, Granger DN (2004) Infammatory responses to ischemia and reperfusion in the cerebral microcircula-tion. Front Biosci 9:1339-1347 (Pubitemid 39060847)
46. Gregersen R, Lambertsen K, Finsen B (2000) Microglia and mac-rophages are the major source of tumor necrosis factor in permanent middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 20:53-65 (Pubitemid 30019830)
47. Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40:140-155. doi:10.1002/glia.10161 (Pubitemid 35337372)
48. Stoll G, Schroeter M, Jander S, Siebert H, Wollrath A, Kleinschnitz C, Bruck W (2004) Lesion-associated expression of transforming growth factor-beta-2 in the rat nervous system: evidence for down-regulating the phagocytic activity of microglia and macrophages. Brain Pathol 14:51-58 (Pubitemid 38200589)
49. Min KJ, Yang MS, Kim SU, Jou I, Joe EH (2006) Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain infammation. J Neurosci 26: 1880-1887 (Pubitemid 43237001)
50. Wang J, Tsirka SE (2005) Tuftsin fragment 1-3 is benefcial when delivered after the induction of intracerebral hemorrhage. Stroke 36:613-618 (Pubitemid 40344165)
51. Mander P, Borutaite V, Moncada S, Brown GC (2005) Nitric oxide from infammatory-activated glia synergizes with hypoxia to induce neuronal death. J Neurosci Res 79:208-215 (Pubitemid 40116437)
52. Khan M, Sekhon B, Giri S, Jatana M, Gilg AG, Ayasolla K, Elango C, Singh AK, Singh I (2005) S-Nitrosoglutathione reduces infammation and protects brain against focal cerebral ischemia in a rat model of experimental stroke. J Cereb Blood Flow Metab 25:177-192 (Pubitemid 40171200)
53. Van Den Bosch L, Tilkin P, Lemmens G, Robberecht W (2002) Minocycline delays disease onset and mortality in a transgenic model of ALS. NeuroReport 13:1067-1070 (Pubitemid 34587742)
54. Canolle B, Masmejean F, Melon C, Nieoullon A, Pisano P, Lortet S (2004) Glial soluble factors regulate the activity and expression of the neuronal glutamate transporter EAAC1: implication of cholesterol. J Neurochem 88:1521-1532. doi:10.1046/j.1471-4159.2003.02301.x [pii] (Pubitemid 38366928)
55. Sercombe R, Dinh YR, Gomis P (2002) Cerebrovascular infammation following subarachnoid hemorrhage. Jpn J Pharmacol 88:227-249 (Pubitemid 34302973)
56. Uemura Y, Sugimoto T, Okamoto S, Handa H, Mizuno N (1987) Changes of neuropeptide immunoreactivity in cerebrovascular nerve fbers after experimentally produced SAH. Immunohistochemical study in the dog. J Neurosurg 66:741-747 (Pubitemid 17072994)
57. Fein JM, Flor WJ, Cohan SL, Parkhurst J (1974) Sequential changes of vascular ultrastructure in experimental cerebral vasospasm. Myonecrosis of subarachnoid arteries. J Neurosurg 41:49-58
58. Mayberg MR, Okada T, Bark DH (1990) The signifcance of mor¬phological changes in cerebral arteries after subarachnoid hemor¬rhage. J Neurosurg 72:626-633 (Pubitemid 20113691)
59. Gomis P, Kacem K, Sercombe C, Seylaz J, Sercombe R (2000) Confocal microscopic evidence of decreased alpha-actin expression within rabbit cerebral artery smooth muscle cells after subarachnoid haemorrhage. Histochem J 32:673-678 (Pubitemid 32147000)
60. Yamamoto Y, Bernanke DH, Smith RR (1990) Accelerated non-muscle contraction after subarachnoid hemorrhage: cere-brospinal fluid testing in a culture model. Neurosurgery 27: 921-928
61. Grossetete M, Phelps J, Arko L, Yonas H, Rosenberg GA (2009) Elevation of matrix metalloproteinases 3 and 9 in cerebrospinal fuid and blood in patients with severe traumatic brain injury. Neurosurgery 65:702-708
62. Jung KH, Chu K, Lee ST, Kim SJ, Song EC, Kim EH, Park DK, Sinn DI, Kim JM, Kim M, Roh JK (2007) Blockade of AT1 receptor reduces apoptosis, infammation, and oxidative stress in normoten-sive rats with intracerebral hemorrhage. J Pharmacol Exp Ther 322:1051-1058 (Pubitemid 47295814)
63. Simard JM, Kilbourne M, Tsymbalyuk O, Tosun C, Caridi J, lvanova S, Keledjian K, Bochicchio E, Gerzanich V (2009) Key role of sulfonylurea receptor 1 in progressive secondary hemor¬rhage after brain confusion. J Neurotrauma 26(12): 2257-2267
64. Armin SS, Colohan AR, Zhang JH (2006) Traumatic subarachnoid hemorrhage: our current understanding and its evolution over the past half century. Neurol Res 28:445-452 (Pubitemid 43967792)
65. Armin SS, Colohan AR, Zhang JH (2008) Vasospasm in traumatic brain injury. Acta Neurochir Suppl 104:421-425