Exacerbation of Thromboinflammation by Hyperglycemia Precipitates Cerebral Infarct Growth and Hemorrhagic Transformation

Stroke

Volumn 48, Issue 7, 2017, Pages 1932-1940

  Desilles, Jean Philippe ^a,b,c   Syvannarath, Varouna ^a   Ollivier, Véronique ^a   Journé, Clément ^d   Delbosc, Sandrine ^a   Ducroux, Célina ^a   Boisseau, William ^a,b   Louedec, Liliane ^a   DI Meglio, Lucas ^a   Loyau, Stéphane ^a   Jandrot Perrus, Martine ^a   Potier, Louis ^e   Michel, Jean Baptiste ^a   Mazighi, Mikael ^a,b,c   Ho Tin Noé, Benoit ^a  

^a Site Xavier Bichat and Département Hospitalo Universitaire Fibrosis Inflammation and Remodeling   (France)

^b FONDATION OPHTALMOLOGIQUE ADOLPHE DE ROTHSCHILD   (France)

^c DHU Neurovasc   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e BICHAT HOSPITAL   (France)

Author keywords

acute stroke; hyperglycemia; microvascular dysfunction; middle cerebral artery occlusion; polymorphonuclear neutrophils activation

Indexed keywords

GELATINASE B; SEROTONIN; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN HOMOGENATE; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN PERFUSION; CELL ADHESION; CONTROLLED STUDY; DIABETIC PATIENT; DISEASE EXACERBATION; DOWNSTREAM MICROVASCULAR THROMBOINFLAMMATION; ENDOTHELIUM CELL; HEMORRHAGIC TRANSFORMATION; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; INTRAVITAL MICROSCOPY; LEUKOCYTE ACTIVATION; MALE; MICROANGIOPATHY; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUTROPHIL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; RECANALIZATION; REPERFUSION INJURY; SEROTONIN BLOOD LEVEL; THROMBOCYTE; ANIMAL; BLOOD; CEREBRAL ARTERY DISEASE; CEREBRAL HEMORRHAGE; CEREBRAL INFARCTION; COMPLICATION; DIAGNOSTIC IMAGING; INFLAMMATION; INTRACRANIAL THROMBOSIS; MICROVASCULATURE; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD-BRAIN BARRIER; CEREBRAL HEMORRHAGE; CEREBRAL INFARCTION; HYPERGLYCEMIA; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INTRACRANIAL THROMBOSIS; MAGNETIC RESONANCE IMAGING; MALE; MICROVESSELS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85019609482     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.117.017080     Document Type: Article

References (35)

1. Desilles JP, Meseguer E, Labreuche J, Lapergue B, Sirimarco G, Gonzalez-Valcarcel J, et al. Diabetes mellitus, admission glucose, and outcomes after stroke thrombolysis: a registry and systematic review. Stroke. 2013;44:1915-1923. doi: 10.1161/STROKEAHA.111.000813.
2. Arnold M, Mattle S, Galimanis A, Kappeler L, Fischer U, Jung S, et al. Impact of admission glucose and diabetes on recanalization and outcome after intra-arterial thrombolysis for ischaemic stroke. Int J Stroke. 2014;9:985-991. doi: 10.1111/j.1747-4949.2012.00879.x.
3. Muir KW, McCormick M, Baird T, Ali M. Prevalence, predictors and prognosis of post-stroke hyperglycaemia in acute stroke trials: individual patient data pooled analysis from the Virtual International Stroke Trials Archive (VISTA). Cerebrovasc Dis Extra. 2011;1:17-27. doi: 10.1159/000324319.
4. Pulsinelli WA, Waldman S, Rawlinson D, Plum F. Moderate hyperglycemia augments ischemic brain damage: a neuropathologic study in the rat. Neurology. 1982;32:1239-1246.
5. Yip PK, He YY, Hsu CY, Garg N, Marangos P, Hogan EL. Effect of plasma glucose on infarct size in focal cerebral ischemia-reperfusion. Neurology. 1991;41:899-905.
6. McBride DW, Legrand J, Krafft PR, Flores J, Klebe D, Tang J, et al. Acute hyperglycemia is associated with immediate brain swelling and hemorrhagic transformation after middle cerebral artery occlusion in rats. Acta Neurochir Suppl. 2016;121:237-241. doi: 10.1007/978-3-319-18497-5-42.
7. Xing Y, Jiang X, Yang Y, Xi G. Hemorrhagic transformation induced by acute hyperglycemia in a rat model of transient focal ischemia. Acta Neurochir Suppl. 2011;111:49-54. doi: 10.1007/978-3-7091-0693-8-9.
8. Soejima Y, Hu Q, Krafft PR, Fujii M, Tang J, Zhang JH. Hyperbaric oxygen preconditioning attenuates hyperglycemia-enhanced hemorrhagic transformation by inhibiting matrix metalloproteinases in focal cerebral ischemia in rats. Exp Neurol. 2013;247:737-743. doi: 10.1016/j.expneurol.2013.03.019.
9. Kamada H, Yu F, Nito C, Chan PH. Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke. 2007;38:1044-1049. doi: 10.1161/01.STR.0000258041.75739. c.b.
10. Bémeur C, Ste-Marie L, Montgomery J. Increased oxidative stress during hyperglycemic cerebral ischemia. Neurochem Int. 2007;50:890-904. doi: 10.1016/j.neuint.2007.03.002.
11. Quast MJ, Wei J, Huang NC, Brunder DG, Sell SL, Gonzalez JM, et al. Perfusion deficit parallels exacerbation of cerebral ischemia/reperfusion injury in hyperglycemic rats. J Cereb Blood Flow Metab. 1997;17:553-559. doi: 10.1097/00004647-199705000-00009.
12. Venables GS, Miller SA, Gibson G, Hardy JA, Strong AJ. The effects of hyperglycaemia on changes during reperfusion following focal cerebral ischaemia in the cat. J Neurol Neurosurg Psychiatry. 1985;48:663-669.
13. Wong SL, Demers M, Martinod K, Gallant M, Wang Y, Goldfine AB, et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med. 2015;21:815-819. doi: 10.1038/nm.3887.
14. Jickling GC, Liu D, Ander BP, Stamova B, Zhan X, Sharp FR. Targeting neutrophils in ischemic stroke: translational insights from experimental studies. J Cereb Blood Flow Metab. 2015;35:888-901. doi: 10.1038/jcbfm.2015.45.
15. Justicia C, Salas-Perdomo A, Perez-de-Puig I, Deddens LH, van Tilborg GA, Castellvi C, et al. Uric acid is protective after cerebral ischemia/reperfusion in hyperglycemic mice. [published online ahead of print December 15, 2016]. Transl Stroke Res. doi: 10.1007/s12975-016-0515-1. http://link.springer.com/article/10.1007/s12975-016-0515-1. Accessed December 15, 2016.
16. Lin B, Ginsberg MD, Busto R, Li L. Hyperglycemia triggers massive neutrophil deposition in brain following transient ischemia in rats. Neurosci Lett. 2000;278:1-4.
17. Desilles JP, Loyau S, Syvannarath V, Gonzalez-Valcarcel J, Cantier M, Louedec L, et al. Alteplase reduces downstream microvascular thrombosis and improves the benefit of large artery recanalization in stroke. Stroke. 2015;46:3241-3248. doi: 10.1161/STROKEAHA.115.010721.
18. Lemhadri A, Hajji L, Michel JB, Eddouks M. Cholesterol and triglycerides lowering activities of caraway fruits in normal and streptozotocin diabetic rats. J Ethnopharmacol. 2006;106:321-326. doi: 10.1016/j.jep.2006.01.033.
19. Lu A, Clark JF, Broderick JP, Pyne-Geithman GJ, Wagner KR, Khatri P, et al. Mechanical reperfusion is associated with post-ischemic hemorrhage in rat brain. Exp Neurol. 2009;216:407-412. doi: 10.1016/j.expneurol.2008.12.020.
20. Goerge T, Ho-Tin-Noe B, Carbo C, Benarafa C, Remold-O'Donnell E, Zhao BQ, et al. Inflammation induces hemorrhage in thrombocytopenia. Blood. 2008;111:4958-4964. doi: 10.1182/blood-2007-11-123620.
21. De Meyer SF, Denorme F, Langhauser F, Geuss E, Fluri F, Kleinschnitz C. Thromboinflammation in stroke brain damage. Stroke. 2016;47:1165-1172. doi: 10.1161/STROKEAHA.115.011238.
22. Maestrini I, Strbian D, Gautier S, Haapaniemi E, Moulin S, Sairanen T, et al. Higher neutrophil counts before thrombolysis for cerebral ischemia predict worse outcomes. Neurology. 2015;85:1408-1416. doi: 10.1212/WNL.0000000000002029.
23. Liu J, Gao BB, Clermont AC, Blair P, Chilcote TJ, Sinha S, et al. Hyperglycemia-induced cerebral hematoma expansion is mediated by plasma kallikrein. Nat Med. 2011;17:206-210. doi: 10.1038/nm.2295.
24. Kleinschnitz C, Pozgajova M, Pham M, Bendszus M, Nieswandt B, Stoll G. Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intracranial bleeding. Circulation. 2007;115:2323-2330. doi: 10.1161/CIRCULATIONAHA.107.691279.
25. Deppermann C, Kraft P, Volz J, Schuhmann MK, Beck S, Wolf K, et al. Platelet secretion is crucial to prevent bleeding in the ischemic brain but not in the inflamed skin or lung in mice. Blood. 2017;129:1702-1706. doi: 10.1182/blood-2016-12-750711.
26. Mazighi M, Chaudhry SA, Ribo M, Khatri P, Skoloudik D, Mokin M, et al. Impact of onset-to-reperfusion time on stroke mortality: a collaborative pooled analysis. Circulation. 2013;127:1980-1985. doi: 10.1161/CIRCULATIONAHA.112.000311.
27. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med. 2010;16:887-896. doi: 10.1038/nm.2184.
28. von Brühl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med. 2012;209:819-835. doi: 10.1084/jem.20112322.
29. Ritter L, Davidson L, Henry M, Davis-Gorman G, Morrison H, Frye JB, et al. Exaggerated neutrophil-mediated reperfusion injury after ischemic stroke in a rodent model of type 2 diabetes. Microcirculation. 2011;18:552-561. doi: 10.1111/j.1549-8719.2011.00115.x.
30. Omi H, Okayama N, Shimizu M, Okouchi M, Ito S, Fukutomi T, et al. Participation of high glucose concentrations in neutrophil adhesion and surface expression of adhesion molecules on cultured human endothelial cells: effect of antidiabetic medicines. J Diabetes Complications. 2002;16:201-208.
31. Kruyt ND, Biessels GJ, Devries JH, Roos YB. Hyperglycemia in acute ischemic stroke: pathophysiology and clinical management. Nat Rev Neurol. 2010;6:145-155. doi: 10.1038/nrneurol.2009.231.
32. MacDougall NJ, Muir KW. Hyperglycaemia and infarct size in animal models of middle cerebral artery occlusion: systematic review and metaanalysis. J Cereb Blood Flow Metab. 2011;31:807-818. doi: 10.1038/jcbfm.2010.210.
33. Kummer U, Zobeley J, Brasen JC, Fahmy R, Kindzelskii AL, Petty AR, et al. Elevated glucose concentrations promote receptor-independent activation of adherent human neutrophils: an experimental and computational approach. Biophys J. 2007;92:2597-2607. doi: 10.1529/biophysj.106.086769.
34. Gentile NT, Vaidyula VR, Kanamalla U, DeAngelis M, Gaughan J, Rao AK. Factor VIIa and tissue factor procoagulant activity in diabetes mellitus after acute ischemic stroke: impact of hyperglycemia. Thromb Haemost. 2007;98:1007-1013.
35. Goyal M, Menon BK, van Zwam WH, Dippel DW, Mitchell PJ, Demchuk AM, et al; HERMES collaborators. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387:1723-1731. doi: 10.1016/S0140-6736(16)00163-X.