Early outcome and blood-brain barrier integrity after co-administered thrombolysis and hyperbaric oxygenation in experimental stroke

Experimental and Translational Stroke Medicine

Volumn 3, Issue 1, 2011, Pages

  Michalski, Dominik ^a   Pelz, Johann ^a   Weise, Christopher ^a   Kacza, Johannes ^a   Boltze, Johannes ^a,b   Grosche, Jens ^a   Kamprad, Manja ^a   Schneider, Dietmar ^a   Hobohm, Carsten ^a   Härtig, Wolfgang ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALTEPLASE; FLUORESCEIN ISOTHIOCYANATE; GELATINASE A; GELATINASE B; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BLOOD CLOT LYSIS; BLOOD SAMPLING; CONTROLLED STUDY; FUNCTIONAL DISEASE; HYPERBARIC OXYGEN; HYPEROXIA; MALE; MEMBRANE PERMEABILITY; MENZIES SCORE; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; NONHUMAN; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SHAM PROCEDURE; STROKE; SURVIVAL; THROMBOEMBOLISM; TREATMENT OUTCOME;

EID: 79960660332     PISSN: None     EISSN: 20407378     Source Type: Journal    
DOI: 10.1186/2040-7378-3-5     Document Type: Article

References (42)

1. Endres M, Engelhardt B, Koistinaho J, Lindvall O, Meairs S, Mohr JP, Planas A, Rothwell N, Schwaninger M, Schwab ME, Vivien D, Wieloch T, Dirnagl U. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc Dis 2008, 25:268-278. 10.1159/000118039, 18292653.
2. Bechmann I, Galea I, Perry VH. What is the blood-brain barrier (not)?. Trends Immunol 2007, 28:5-11. 10.1016/j.it.2006.11.007, 17140851.
3. Kaur C, Ling EA. Blood brain barrier in hypoxic-ischemic conditions. Curr Neurovasc Res 2008, 5:71-81. 10.2174/156720208783565645, 18289024.
4. del Zoppo GJ. The neurovascular unit in the setting of stroke. J Intern Med 2010, 267:156-171. 10.1111/j.1365-2796.2009.02199.x, 3001328, 20175864.
5. Young AR, Ali C, Duretête A, Vivien D. Neuroprotection and stroke: time for a compromise. J Neurochem 2007, 103:1302-1309. 10.1111/j.1471-4159.2007.04866.x, 17727635.
6. Li F, Tatlisumak T. Focal brain ischemia models in rodents. Handbook of Experimental Neurology 2006, 212-228. Cambridge: Cambridge University Press, Tatlisumak T, Fisher M.
7. Belayev L, Busto R, Zhao W, Ginsberg MD. Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res 1996, 739:88-96. 10.1016/S0006-8993(96)00815-3, 8955928.
8. Pillai DR, Dittmar MS, Baldaranov D, Heidemann RM, Henning EC, Schuierer G, Bogdahn U, Schlachetzki F. Cerebral ischemia-reperfusion injury in rats-a 3 T MRI study on biphasic blood-brain barrier opening and the dynamics of edema formation. J Cereb Blood Flow Metab 2009, 29:1846-1855. 10.1038/jcbfm.2009.106, 2848453, 19654585.
9. Candelario-Jalil E, Yang Y, Rosenberg GA. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 2009, 158:983-994. 10.1016/j.neuroscience.2008.06.025, 18621108.
10. Rosell A, Lo EH. Multiphasic roles for matrix metalloproteinases after stroke. Curr Opin Pharmacol 2008, 8:82-89. 10.1016/j.coph.2007.12.001, 18226583.
11. Schäbitz WR, Schade H, Heiland S, Kollmar R, Bardutzky J, Henninger N, Müller H, Carl U, Toyokuni S, Sommer C, Schwab S. Neuroprotection by hyperbaric oxygenation after experimental focal cerebral ischemia monitored by MRI. Stroke 2004, 35:1175-1179. 10.1161/01.STR.0000125868.86298.8e, 15060313.
12. Liu W, Hendren J, Qin XJ, Liu KJ. Normobaric hyperoxia reduces the neurovascular complications associated with delayed tissue plasminogen activator treatment in a rat model of focal cerebral ischemia. Stroke 2009, 40:2526-2531. 10.1161/STROKEAHA.108.545483, 2714253, 19478225.
13. Sun L, Zhou W, Mueller C, Sommer C, Heiland S, Bauer AT, Marti HH, Veltkamp R. Oxygen therapy reduces secondary hemorrhage after thrombolysis in thromboembolic cerebral ischemia. J Cereb Blood Flow Metab 2010, 30:1651-1660. 10.1038/jcbfm.2010.50, 20424638.
14. Qin Z, Karabiyikoglu M, Hua Y, Silbergleit R, He Y, Keep RF, Xi G. Hyperbaric oxygen-induced attenuation of hemorrhagic transformation after experimental focal transient cerebral ischemia. Stroke 2007, 38:1362-1367. 10.1161/01.STR.0000259660.62865.eb, 17322079.
15. Veltkamp R, Bieber K, Wagner S, Beynon C, Siebing DA, Veltkamp C, Schwaninger M, Marti HH. Hyperbaric oxygen reduces basal lamina degradation after transient focal cerebral ischemia in rats. Brain Res 2006, 1076:231-237. 10.1016/j.brainres.2006.01.013, 16480689.
16. Veltkamp R, Siebing DA, Sun L, Heiland S, Bieber K, Marti HH, Nagel S, Schwab S, Schwaninger M. Hyperbaric oxygen reduces blood-brain barrier damage and edema after transient focal cerebral ischemia. Stroke 2005, 36:1679-1683. 10.1161/01.STR.0000173408.94728.79, 16020761.
17. Michalski D, Härtig W, Schneider D, Hobohm C. Use of normobaric and hyperbaric oxygen in acute focal cerebral ischemia - a preclinical and clinical review. Acta Neurol Scand 2011, 123:85-97.
18. Singhal AB. A review of oxygen therapy in ischemic stroke. Neurol Res 2007, 29:173-183. 10.1179/016164107X181815, 17439702.
19. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D, Larrue V, Lees KR, Medeghri Z, Machnig T, Schneider D, von Kummer R, Wahlgren N, Toni D, . ECASS Investigators Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008, 359:1317-1329. 10.1056/NEJMoa0804656, 18815396, ECASS Investigators.
20. Burggraf D, Martens HK, Dichgans M, Hamann GF. rt-PA causes a dose-dependent increase in the extravasation of cellular and non-cellular blood elements after focal cerebral ischemia. Brain Res 2007, 1164:55-62.
21. Adibhatla RM, Hatcher JF. Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies. CNS Neurol Disord Drug Targets 2008, 7:243-253. 10.2174/187152708784936608, 2562687, 18673209.
22. Jin R, Yang G, Li G. Molecular insights and therapeutic targets for blood-brain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator. Neurobiol Dis 2010, 38:376-385. 10.1016/j.nbd.2010.03.008, 2862862, 20302940.
23. Michalski D, Küppers-Tiedt L, Weise C, Laignel F, Härtig W, Raviolo M, Schneider D, Hobohm C. Long-term functional and neurological outcome after simultaneous treatment with tissue-plasminogen activator and hyperbaric oxygen in early phase of embolic stroke in rats. Brain Res 2009, 1303:161-168.
24. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR. A rat model of focal embolic cerebral ischemia. Brain Res 1997, 766:83-92. 10.1016/S0006-8993(97)00580-5, 9359590.
25. Menzies SA, Hoff JT, Betz AL. Middle cerebral artery occlusion in rats: a neurological and pathological evaluation of a reproducible model. Neurosurgery 1992, 31:100-106. 10.1227/00006123-199207000-00014, 1641086.
26. Michalski D, Grosche J, Pelz J, Schneider D, Weise C, Bauer U, Kacza J, Gärtner U, Hobohm C, Härtig W. A novel quantification of blood-brain barrier damage and histochemical typing after embolic stroke in rats. Brain Res 2010, 1359:186-200.
27. Sternberger NH, Sternberger LA. Blood-brain barrier protein recognized by monoclonal antibody. Proc Natl Acad Sci USA 1987, 84:8169-8173. 10.1073/pnas.84.22.8169, 299500, 3500474.
28. Fujiwara N, Murata Y, Arai K, Egi Y, Lu J, Wu O, Singhal AB, Lo EH. Combination therapy with normobaric oxygen (NBO) plus thrombolysis in experimental ischemic stroke. BMC Neurosci 2009, 10:79. 10.1186/1471-2202-10-79, 2714858, 19604385.
29. Henninger N, Bratane BT, Bastan B, Bouley J, Fisher M. Normobaric hyperoxia and delayed tPA treatment in a rat embolic stroke model. J Cereb Blood Flow Metab 2009, 29:119-129. 10.1038/jcbfm.2008.104, 18766195.
30. Gasche Y, Fujimura M, Morita-Fujimura Y, Copin JC, Kawase M, Massengale J, Chan PH. Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. J Cereb Blood Flow Metab 1999, 19:1020-1028.
31. Strbian D, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E, Abo-Ramadan U, Tatlisumak T. The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 2008, 153:175-181. 10.1016/j.neuroscience.2008.02.012, 18367342.
32. Chen B, Friedman B, Cheng Q, Tsai P, Schim E, Kleinfeld D, Lyden PD. Severe blood-brain barrier disruption and surrounding tissue injury. Stroke 2009, 40:e666-e674. 10.1161/STROKEAHA.109.551341, 2819286, 19893002.
33. Abo-Ramadan U, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E, Soinne L, Strbian D, Tatlisumak T. Post-ischemic leakiness of the blood-brain barrier: a quantitative and systematic assessment by Patlak plots. Exp Neurol 2009, 219:328-333. 10.1016/j.expneurol.2009.06.002, 19520075.
34. Kelly MA, Shuaib A, Todd KG. Matrix metalloproteinase activation and blood-brain barrier breakdown following thrombolysis. Exp Neurol 2006, 200:38-49. 10.1016/j.expneurol.2006.01.032, 16624294.
35. Park KP, Rosell A, Foerch C, Xing C, Kim WJ, Lee S, Opdenakker G, Furie KL, Lo EH. Plasma and brain matrix metalloproteinase-9 after acute focal cerebral ischemia in rats. Stroke 2009, 40:2836-2842. 10.1161/STROKEAHA.109.554824, 19556529.
36. Fukuda S, Fini CA, Mabuchi T, Koziol JA, Eggleston LL, del Zoppo GJ. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 2004, 35:998-1004. 10.1161/01.STR.0000119383.76447.05, 2979008, 15001799.
37. Bauer AT, Bürgers HF, Rabie T, Marti HH. Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab 2010, 30:837-848. 10.1038/jcbfm.2009.248, 2949161, 19997118.
38. Heo JH, Lucero J, Abumiya T, Koziol JA, Copeland BR, del Zoppo GJ. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab 1999, 19:624-633.
39. Tsuji K, Aoki T, Tejima E, Arai K, Lee SR, Atochin DN, Huang PL, Wang X, Montaner J, Lo EH. Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke 2005, 36:1954-1959. 10.1161/01.STR.0000177517.01203.eb, 16051896.
40. Planas AM, Solé S, Justicia C. Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol Dis 2001, 8:834-846. 10.1006/nbdi.2001.0435, 11592852.
41. Ethell IM, Ethell DW. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 2007, 85:2813-2823. 10.1002/jnr.21273, 17387691.
42. 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. 10.1038/nm1387, 16565723.