Mechanisms of microthrombi formation after experimental subarachnoid hemorrhage

Neuroscience

Volumn 224, Issue , 2012, Pages 26-37

  Sabri, M ^b   Ai, J ^a   Lakovic, K ^b   D'abbondanza, J ^b   Ilodigwe, D ^a   MacDonald, R L ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Microthrombosis; Mouse; Nitric oxide; Scanning electron microscopy; Subarachnoid hemorrhage; Transmission electron microscopy

Indexed keywords

FIBRINOGEN; NITRIC OXIDE; PADGEM PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERIOLE; ARTICLE; BLOOD CLOTTING; BLOOD VESSEL WALL; BRAIN INJURY; BRAIN NERVE CELL; BRAIN TISSUE; CELL MEMBRANE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOTHELIUM; IMMUNOHISTOCHEMISTRY; MALE; MICROTHROMBUS; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUBARACHNOID HEMORRHAGE; TRANSMISSION ELECTRON MICROSCOPY; VASOCONSTRICTION;

ANIMALS; APOPTOSIS; ARTERIOLES; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTRACRANIAL THROMBOSIS; MALE; MICE; MICROSCOPY, ELECTRON; NEURONS; NITRIC OXIDE; P-SELECTIN; SUBARACHNOID HEMORRHAGE; VASOCONSTRICTION;

EID: 84866010248     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.002     Document Type: Article

References (63)

1. Al-Khindi T., Macdonald R.L., Schweizer T.A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 2010, 41:e519-e536.
2. Baldwin M.E., Macdonald R.L., Huo D., Novakovic R.L., Goldenberg F.D., Frank J.I., Rosengart A.J. Early vasospasm on admission angiography in patients with aneurysmal subarachnoid hemorrhage is a predictor for in-hospital complications and poor outcome. Stroke 2004, 35:2506-2511.
3. Bederson J.B., Germano I.M., Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 1995, 26:1086-1091.
4. Bederson J.B., Levy A.L., Ding W.H., Kahn R., DiPerna C.A., Jenkins A.L., Vallabhajosyula P. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998, 42:352-360.
5. Bevilacqua M.P., Nelson R.M. Selectins. J Clin Invest 1993, 91:379-387.
6. Clower B.R., Yoshioka J., Honma T., Smith R.R. Blood platelets and early intimal changes in cerebral arteries following experimental subarachnoid hemorrhage. Cerebral vasospasm 1988, 335-341. Raven, New York. R.H. Wilkins (Ed.).
7. Davenpeck K.L., Gauthier T.W., Lefer A.M. Inhibition of endothelial-derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology 1994, 107:1050-1058.
8. Diringer M.N., Kirsch J.R., Traystman R.J. Reduced cerebral blood flow but intact reactivity to hypercarbia and hypoxia following subarachnoid hemorrhage in rabbits. J Cereb Blood Flow Metab 1994, 14:59-63.
9. Fein J.M., Flor W.J., Cohan S.L., Parkhurst J. Sequential changes of vascular ultrastructure in experimental cerebral vasospasm. Myonecrosis of subarachnoid arteries. J Neurosurg 1974, 41:49-58.
10. Findlay J.M., Weir B.K., Kanamaru K., Espinosa F. Arterial wall changes in cerebral vasospasm. Neurosurgery 1989, 25:736-745.
11. Friedrich B., Muller F., Feiler S., Scholler K., Plesnila N. Experimental subarachnoid hemorrhage causes early and long-lasting microarterial constriction and microthrombosis: an in-vivo microscopy study. J Cereb Blood Flow Metab 2012, 32:447-455.
12. Friedrich V., Flores R., Muller A., Bi W., Peerschke E.I., Sehba F.A. Reduction of neutrophil activity decreases early microvascular injury after subarachnoid haemorrhage. J Neuroinflammation 2011, 8:103.
13. Frijns C.J., Kasius K.M., Algra A., Fijnheer R., Rinkel G.J. Endothelial cell activation markers and delayed cerebral ischaemia in patients with subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 2006, 77:863-867.
14. Furie B., Furie B.C., Flaumenhaft R. A journey with platelet P-selectin: the molecular basis of granule secretion, signalling and cell adhesion. Thromb Haemost 2001, 86:214-221.
15. Grubb R.L.J., Raichle M.E., Eichling J.O., Gado M.H. Effects of subarachnoid hemorrhage on cerebral blood volume, blood flow, and oxygen utilization in humans. J Neurosurg 1977, 46:446-453.
16. Hatsuoka M., Makita T. Scanning electron microscopy of experimental thrombus formation in canine lateral saphena vein. Scan Electron Microsc 1981, 4:189-194.
17. Herz D.A., Baez S., Shulman K. Pial microcirculation in subarachnoid hemorrhage. Stroke 1975, 6:417-424.
18. Ishikawa M., Kusaka G., Yamaguchi N., Sekizuka E., Nakadate H., Minamitani H., Shinoda S., Watanabe E. Platelet and leukocyte adhesion in the microvasculature at the cerebral surface immediately after subarachnoid hemorrhage. Neurosurgery 2009, 64:546-553.
19. Jakobsen M., Overgaard J., Marcussen E., Enevoldsen E.M. Relation between angiographic cerebral vasospasm and regional CBF in patients with SAH. Acta Neurol Scand 1990, 82:109-115.
20. Larsen E., Celi A., Gilbert G.E., Furie B.C., Erban J.K., Bonfanti R., Wagner D.D., Furie B. PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell 1989, 59:305-312.
21. Lee J.Y., Huang D.L., Keep R., Sagher O. Characterization of an improved double hemorrhage rat model for the study of delayed cerebral vasospasm. J Neurosci Methods 2008, 168:358-366.
22. Lin C.L., Calisaneller T., Ukita N., Dumont A.S., Kassell N.F., Lee K.S. A murine model of subarachnoid hemorrhage-induced cerebral vasospasm. J Neurosci Methods 2003, 123:89-97.
23. Liszczak T.M., Varsos V.G., Black P.M., Kistler J.P., Zervas N.T. Cerebral arterial constriction after experimental subarachnoid hemorrhage is associated with blood components within the arterial wall. J Neurosurg 1983, 58:18-26.
24. Macdonald R.L., Higashida R.T., Keller E., Mayer S.A., Molyneux A., Raabe A., Vajkoczy P., Wanke I., Bach D., Frey A., Marr A., Roux S., Kassell N. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol 2011, 10:618-625.
25. Macdonald R.L., Kassell N.F., Mayer S., Ruefenacht D., Schmiedek P., Weidauer S., Frey A., Roux S., Pasqualin A. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 2008, 39:3015-3021.
26. Macdonald R.L., Pluta R.M., Zhang J.H. Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol 2007, 3:256-263.
27. McEver R.P. GMP-140: a receptor for neutrophils and monocytes on activated platelets and endothelium. J Cell Biochem 1991, 45:156-161.
28. Murohara T., Parkinson S.J., Waldman S.A., Lefer A.M. Inhibition of nitric oxide biosynthesis promotes P-selectin expression in platelets. Role of protein kinase C. Arterioscler Thromb Vasc Biol 1995, 15:2068-2075.
29. Nieuwkamp D.J., Setz L.E., Algra A., Linn F.H., de Rooij N.K., Rinkel G.J. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 2009, 8:635-642.
30. Nissen J.J., Mantle D., Gregson B., Mendelow A.D. Serum concentration of adhesion molecules in patients with delayed ischaemic neurological deficit after aneurysmal subarachnoid haemorrhage: the immunoglobulin and selectin superfamilies. J Neurol Neurosurg Psychiatry 2001, 71:329-333.
31. Ohkuma H., Itoh K., Shibata S., Suzuki S. Morphological changes of intraparenchymal arterioles after experimental subarachnoid hemorrhage in dogs. Neurosurgery 1997, 41:230-235.
32. Palabrica T., Lobb R., Furie B.C., Aronovitz M., Benjamin C., Hsu Y.M., Sajer S.A., Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992, 359:848-851.
33. Pennings F.A., Albrecht K.W., Muizelaar J.P., Schuurman P.R., Bouma G.J. Abnormal responses of the human cerebral microcirculation to papaverin during aneurysm surgery. Stroke 2009, 40:317-320.
34. Pennings F.A., Bouma G.J., Ince C. Direct observation of the human cerebral microcirculation during aneurysm surgery reveals increased arteriolar contractility. Stroke 2004, 35:1284-1288.
35. Pluta R.M., Hansen-Schwartz J., Dreier J., Vajkoczy P., Macdonald R.L., Nishizawa S., Kasuya H., Wellman G., Keller E., Zauner A., Dorsch N., Clark J., Ono S., Kiris T., Leroux P., Zhang J.H. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res 2009, 31:151-158.
36. Prunell G.F., Mathiesen T., Svendgaard N.A. A new experimental model in rats for study of the pathophysiology of subarachnoid hemorrhage. Neuroreport 2002, 13:2553-2556.
37. Rabinstein A.A., Friedman J.A., Weigand S.D., McClelland R.L., Fulgham J.R., Manno E.M., Atkinson J.L., Wijdicks E.F. Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 2004, 35:1862-1866.
38. Romano J.G., Forteza A.M., Concha M., Koch S., Heros R.C., Morcos J.J., Babikian V.L. Detection of microemboli by transcranial Doppler ultrasonography in aneurysmal subarachnoid hemorrhage. Neurosurgery 2002, 50:1026-1030.
39. Sabri M., Ai J., Knight B., Tariq A., Jeon H., Shang X., Marsden P.A., Loch M.R. Uncoupling of endothelial nitric oxide synthase after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 2011, 31:190-199.
40. Sabri M., Ai J., Macdonald R.L. Dissociation of vasospasm and secondary effects of experimental subarachnoid hemorrhage by clazosentan. Stroke 2011, 42:1454-1460.
41. Sabri M., Ai J., Marsden P.A., Macdonald R.L. Simvastatin re-couples dysfunctional endothelial nitric oxide synthase in experimental subarachnoid hemorrhage. PLoS One 2011, 6:e17062.
42. Sabri M., Jeon H., Ai J., Tariq A., Shang X., Chen G., Macdonald R.L. Anterior circulation mouse model of subarachnoid hemorrhage. Brain Res 2009, 1295:179-185.
43. Salary M., Quigley M.R., Wilberger J.E. Relation among aneurysm size, amount of subarachnoid blood, and clinical outcome. J Neurosurg 2007, 107:13-17.
44. Sehba F.A., Ding W.H., Chereshnev I., Bederson J.B. Effects of S-nitrosoglutathione on acute vasoconstriction and glutamate release after subarachnoid hemorrhage. Stroke 1999, 30:1955-1961.
45. Sehba F.A., Friedrich V., Makonnen G., Bederson J.B. Acute cerebral vascular injury after subarachnoid hemorrhage and its prevention by administration of a nitric oxide donor. J Neurosurg 2007, 106:321-329.
46. Sehba F.A., Mostafa G., Friedrich V., Bederson J.B. Acute microvascular platelet aggregation after subarachnoid hemorrhage. J Neurosurg 2005, 102:1094-1100.
47. Sehba F.A., Schwartz A.Y., Chereshnev I., Bederson J.B. Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2000, 20:604-611.
48. Stein S.C., Browne K.D., Chen X.H., Smith D.H., Graham D.I. Thromboembolism and delayed cerebral ischemia after subarachnoid hemorrhage: an autopsy study. Neurosurgery 2006, 59:781-787.
49. Sun B.L., Zheng C.B., Yang M.F., Yuan H., Zhang S.M., Wang L.X. Dynamic alterations of cerebral pial microcirculation during experimental subarachnoid hemorrhage. Cell Mol Neurobiol 2009, 29:235-241.
50. Suzuki S., Kimura M., Souma M., Ohkima H., Shimizu T., Iwabuchi T. Cerebral microthrombosis in symptomatic cerebral vasospasm - a quantitative histological study in autopsy cases. Neurol Med Chir (Tokyo) 1990, 30:309-316.
51. Suzuki S., Suzuki M., Iwabuchi T., Kamata Y. Role of multiple cerebral microthrombosis in symptomatic cerebral vasospasm: with a case report. Neurosurgery 1983, 13:199-203.
52. Tanabe Y., Sakata K., Yamada H., Ito T., Takada M. Cerebral vasospasm and ultrastructural changes in cerebral arterial wall. An experimental study. J Neurosurg 1978, 49:229-238.
53. Tani E., Yamagata S., Maeda Y., Ito Y. Cytochemical demonstration of adenylate and guanylate cyclases in vascular smooth muscle of circle of Willis. J Neurosurg 1978, 49:239-248.
54. Taylor T.N., Davis P.H., Torner J.C., Holmes J., Meyer J.W., Jacobson M.F. Lifetime cost of stroke in the United States. Stroke 1996, 27:1459-1466.
55. Uhl E., Lehmberg J., Steiger H.J., Messmer K. Intraoperative detection of early microvasospasm in patients with subarachnoid hemorrhage by using orthogonal polarization spectral imaging. Neurosurgery 2003, 52:1307-1315.
56. Vandendries E.R., Furie B.C., Furie B. Role of P-selectin and PSGL-1 in coagulation and thrombosis. Thromb Haemost 2004, 92:459-466.
57. Varsos V.G., Liszczak T.M., Han D.H., Kistler J.P., Vielma J., Black P.M., Heros R.C., Zervas N.T. Delayed cerebral vasospasm is not reversible by aminophylline, nifedipine, or papaverine in a "two-hemorrhage" canine model. J Neurosurg 1983, 58:11-17.
58. Vergouwen M.D., Vermeulen M., Coert B.A., Stroes E.S., Roos Y.B. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab 2008, 28:1761-1770.
59. Vollmer D.G., Takayasu M., Dacey R.G. An in vitro comparative study of conducting vessels and penetrating arterioles after experimental subarachnoid hemorrhage in the rabbit. J Neurosurg 1992, 77:113-119.
60. Weidauer S., Lanfermann H., Raabe A., Zanella F., Seifert V., Beck J. Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 2007, 38:1831-1836.
61. Weidauer S., Vatter H., Beck J., Raabe A., Lanfermann H., Seifert V., Zanella F. Focal laminar cortical infarcts following aneurysmal subarachnoid haemorrhage. Neuroradiology 2008, 50:1-8.
62. Yundt K.D., Grubb R.L., Diringer M.N., Powers W.J. Autoregulatory vasodilation of parenchymal vessels is impaired during cerebral vasospasm. J Cereb Blood Flow Metab 1998, 18:419-424.
63. Zimmerman G.A., Prescott S.M., McIntyre T.M. Endothelial cell interactions with granulocytes: tethering and signaling molecules. Immunol Today 1992, 13:93-100.