Secondary intracerebral hemorrhage due to early initiation of oral anticoagulation after ischemic stroke: An experimental study in mice

Stroke

Volumn 43, Issue 12, 2012, Pages 3352-3357

  Gliem, Michael ^a   Hermsen, Derik ^a   Van Rooijen, Nico ^b   Hartung, Hans Peter ^a   Jander, Sebastian ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Anticoagulation; Cerebral ischemia; Inflammation; Intracerebral hemorrhage; Macrophage

Indexed keywords

CLODRONIC ACID; DABIGATRAN ETEXILATE; LIPOSOME; PHENPROCOUMON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICOAGULATION; ARTICLE; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CONTROLLED STUDY; DRUG EFFECT; DRUG MEGADOSE; EXPERIMENTAL STUDY; LOW DRUG DOSE; MACROPHAGE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECONDARY INTRACEREBRAL HEMORRHAGE;

ADMINISTRATION, ORAL; ANIMALS; ANTICOAGULANTS; BENZIMIDAZOLES; BLOOD COAGULATION; BRAIN ISCHEMIA; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; INTRACRANIAL EMBOLISM; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PHENPROCOUMON; PYRIDINES; RISK FACTORS; STROKE; TIME FACTORS;

EID: 84870930023     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.112.666818     Document Type: Article

References (37)

1. Hart RG, Boop BS, Anderson DC. Oral anticoagulants and intracranial hemorrhage. Facts and hypotheses. Stroke. 1995;26:1471-1477.
2. Ferro JM. Cardioembolic stroke: an update. Lancet Neurol. 2003;2:177-188.
3. Beri A, Punnam SR. Anticoagulation in patients with acute ischemic stroke and atrial fiibrillation - a balance of risks and benefits. Cardiovasc Drugs Ther. 2008;22:419-425.
4. Hawryluk GW, Austin JW, Furlan JC, Lee JB, O'Kelly C, Fehlings MG. Management of anticoagulation following central nervous system hemorrhage in patients with high thromboembolic risk. J Thromb Haemost. 2010;8:1500-1508.
5. Connolly SJ, Ezekowitz MD, Yusuf S, Eikelboom J, Oldgren J, Parekh A, Pogue J, Reilly PA, Themeles E, Varrone J, Wang S, Alings M, Xavier D, Zhu J, Diaz R, Lewis BS, Darius H, Diener HC, Joyner CD, Wallentin L; RE-LY Steering Committee and Investigators. Dabigatran versus warfarin in patients with atrial fibrillation. N Engl J Med. 2009;361:1139-1151.
6. Diener HC, Connolly SJ, Ezekowitz MD, Wallentin L, Reilly PA, Yang S, Xavier D, Di Pasquale G, Yusuf S; RE-LY study group. Dabigatran compared with warfarin in patients with atrial fibrillation and previous transient ischaemic attack or stroke: a subgroup analysis of the RE-LY trial. Lancet Neurol. 2010;9:1157-1163.
7. Banfield DK, MacGillivray RT. Partial characterization of vertebrate prothrombin cDNAs: amplification and sequence analysis of the B chain of thrombin from nine different species. Proc Natl Acad Sci USA. 1992;89:2779-2783.
8. Pfeilschifter W, Spitzer D, Czech-Zechmeister B, Steinmetz H, Foerch C. Increased risk of hemorrhagic transformation in ischemic stroke occurring during warfarin anticoagulation: an experimental study in mice. Stroke. 2011;42:1116-1121.
9. Lauer A, Cianchetti FA, Van Cott EM, Schlunk F, Schulz E, Pfeilschifter W, Steinmetz H, Schaffer CB, Lo EH, Foerch C. Anticoagulation with the oral direct thrombin inhibitor dabigatran does not enlarge hematoma volume in experimental intracerebral hemorrhage. Circulation. 2011;124:1654-1662.
10. Pfeilschifter W, Bohmann F, Baumgarten P, Mittelbronn M, Pfeilschifter J, Lindhoff-Last E, Steinmetz H, Foerch C. Thrombolysis with recombinant tissue plasminogen activator under dabigatran anticoagulation in experimental stroke. Ann Neurol. 2012;71:624-633.
11. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci. 2003;4:399-415.
12. Dirnagl U. Inflammation in stroke: the good, the bad, and the unknown. Ernst Schering Res Found Workshop. 2004;47:87-99.
13. Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, Siler DA, Arumugam TV, Orthey E, Gerloff C, Tolosa E, Magnus T. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke. 2009;40:1849-1857.
14. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med. 2011;17:796-808.
15. Planas AM, Traystman RJ. Advances in translational medicine 2010. Stroke. 2011;42:283-284.
16. Strecker JK, Minnerup J, Gess B, Ringelstein EB, Schäbitz WR, Schilling M. Monocyte chemoattractant protein-1-deficiency impairs the expression of IL-6, IL-1ß and G-CSF after transient focal ischemia in mice. PLoS ONE. 2011;6:e25863.
17. Gliem M, Mausberg AK, Lee JI, Simiantonakis I, van Rooijen N, Hartung HP, Jander S. Macrophages prevent hemorrhagic infarct transformation in murine stroke models. Ann Neurol. 2012;71:743-752.
18. Clark WM, Lessov NS, Dixon MP, Eckenstein F. Monofilament intraluminal middle cerebral artery occlusion in the mouse. Neurol Res. 1997;19:641-648.
19. Stangier J, Stähle H, Rathgen K, Fuhr R. Pharmacokinetics and pharma-codynamics of the direct oral thrombin inhibitor dabigatran in healthy elderly subjects. Clin Pharmacokinet. 2008;47:47-59.
20. Zhou W, Schwarting S, Illanes S, Liesz A, Middelhoff M, Zorn M, Bendszus M, Heiland S, van Ryn J, Veltkamp R. Hemostatic therapy in experimental intracerebral hemorrhage associated with the direct thrombin inhibitor dabigatran. Stroke. 2011;42:3594-3599.
21. Van Rooijen N, Sanders A. Liposome mediated depletion of macro-phages: mechanism of action, preparation of liposomes and applications. J Immunol Methods. 1994;174:83-93.
22. Alves-Rosa F, Vermeulen M, Cabrera J, Stanganelli C, Capozzo A, Narbaitz M, van Rooijen N, Palermo M, Isturiz MA. Macrophage depletion following liposomal-encapsulated clodronate (LIP-CLOD) injection enhances megakaryocytopoietic and thrombopoietic activities in mice. Br J Haematol. 2003;121:130-138.
23. van Amerongen MJ, Harmsen MC, van Rooijen N, Petersen AH, van Luyn MJ. Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol. 2007;170:818-829.
24. Lucas T, Waisman A, Ranjan R, Roes J, Krieg T, Müller W, Roers A, Eming SA. Differential roles of macrophages in diverse phases of skin repair. J Immunol. 2010;184:3964-3977.
25. Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan WC, Fraser HM. Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction. 2011;141:821-831.
26. Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, Wang X, Lo EH. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med. 2006;12:441-445.
27. Stead LG, Jain A, Bellolio MF, Odufuye A, Gilmore RM, Rabinstein A, Chandra R, Dhillon R, Manivannan V, Serrano LA, Yerragondu N, Palamari B, Jain M, Decker WW. Emergency Department hyperglycemia as a predictor of early mortality and worse functional outcome after intracerebral hemorrhage. Neurocrit Care. 2010;13:67-74.
28. Lee SH, Kim BJ, Bae HJ, Lee JS, Lee J, Park BJ, Yoon BW. Effects of glucose level on early and long-term mortality after intracerebral haemorrhage: the Acute Brain Bleeding Analysis Study. Diabetologia. 2010;53:429-434.
29. Demchuk AM, Morgenstern LB, Krieger DW, Linda Chi T, Hu W, Wein TH, Hardy RJ, Grotta JC, Buchan AM. Serum glucose level and diabetes predict tissue plasminogen activator-related intracerebral hemorrhage in acute ischemic stroke. Stroke. 1999;30:34-39.
30. Ahmed N, Dávalos A, Eriksson N, Ford GA, Glahn J, Hennerici M, Mikulik R, Kaste M, Lees KR, Lindsberg PJ, Toni D; SITS Investigators. Association of admission blood glucose and outcome in patients treated with intravenous thrombolysis: results from the Safe Implementation of Treatments in Stroke International Stroke Thrombolysis Register (SITS-ISTR). Arch Neurol. 2010;67:1123-1130.
31. Liu J, Gao BB, Clermont AC, Blair P, Chilcote TJ, Sinha S, Flaumenhaft R, Feener EP. Hyperglycemia-induced cerebral hematoma expansion is mediated by plasma kallikrein. Nat Med. 2011;17:206-210.
32. Khanna S, Biswas S, Shang Y, Collard E, Azad A, Kauh C, Bhasker V, Gordillo GM, Sen CK, Roy S. Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS ONE. 2010;5:e9539.
33. Mirza R, Koh TJ. Dysregulation of monocyte/macrophage phenotype in wounds of diabetic mice. Cytokine. 2011;56:256-264.
34. Han KH, Ryu J, Hong KH, Ko J, Pak YK, Kim JB, Park SW, Kim JJ. HMG-CoA reductase inhibition reduces monocyte CC chemokine receptor 2 expression and monocyte chemoattractant protein-1-mediated monocyte recruitment in vivo. Circulation. 2005;111:1439-1447.
35. Stegbauer J, Lee DH, Seubert S, Ellrichmann G, Manzel A, Kvakan H, Muller DN, Gaupp S, Rump LC, Gold R, Linker RA. Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system. Proc Natl Acad Sci USA. 2009;106:14942-14947.
36. Gorter JW. Major bleeding during anticoagulation after cerebral ischemia: patterns and risk factors. Stroke Prevention In Reversible Ischemia Trial (SPIRIT). European Atrial Fibrillation Trial (EAFT) study groups. Neurology. 1999;53:1319-1327.
37. Hart RG, Tonarelli SB, Pearce LA. Avoiding central nervous system bleeding during antithrombotic therapy: recent data and ideas. Stroke. 2005;36:1588-1593.