Fibrin degradation during sonothrombolysis - Effect of ultrasound, microbubbles and tissue plasminogen activator

Journal of Drug Delivery Science and Technology

Volumn 25, Issue February, 2015, Pages 29-35

  Petit, Bénédicte ^a   Yan, Feng ^b   Bussat, Philippe ^b   Bohren, Yannick ^b   Gaud, Emmanuel ^b   Fontana, Pierre ^c   Tranquart, Franc¸ois ^b   Allémann, Eric ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Bracco Suisse SA   (Switzerland)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Fibrinolysis; Ischemic stroke; Microbubbles; Recombinant tissue plasminogen activator; Sonothrombolysis; Ultrasound

Indexed keywords

ALTEPLASE; D DIMER; FIBRIN; FIBRIN DEGRADATION PRODUCT; FIBRINOGEN;

ARTICLE; BLOOD CLOT; BLOOD CLOT LYSIS; CONTROLLED STUDY; ECHOGRAPHY; FIBRINOLYSIS; HISTOLOGY; HUMAN; IN VITRO STUDY; MICROBUBBLE; RADIOACTIVITY; RADIOIODINATION;

EID: 84925390559     PISSN: 17732247     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jddst.2014.12.001     Document Type: Article

References (41)

1. K. Tachibana, S. Tachibana, Albumin microbubble echo-contrast material as an enhancer for ultrasound accelerated thrombolysis. Circulation 92 (5) (1995) 1148-1150.
2. S. Datta, C.C. Coussios, A.Y. Ammi, T.D. Mast, G. de Courten-Myers, C.K. Holland, Ultrasound-enhanced thrombolysis using definity as a cavitation nucleation agent, Ultrasound Med. Biol. 34 (9) (2008) 1421-1433.
3. A. Soltani, R. Singhal, M. Obtera, R.A. Roy, W.M. Clark, D.R. Hansmann, Potentiating intra-arterial sonothrombolysis for acute ischemic stroke by the addition of the ultrasound contrast agents (Optison & SonoVue), J. Thromb. Thrombolysis 31 (1) (2011) 71-84.
4. B. Petit, F. Yan, F. Tranquart, E. Allémann, Microbubbles and ultrasound-mediated thrombolysis: a review of recent in vitro studies, J. Drug Del. Sci. Tech. 22 (5) (2012) 381-392.
5. M. Nedelmann, N. Ritschel, S. Doenges, A.C. Langheinrich, T. Acker, P. Reuter, M. Yeniguen, J. Pukropski, M. Kaps, C. Mueller, G. Bachmann, T. Gerriets, Combined contrast-enhanced ultrasound and rt-PA treatment is safe and improves impaired microcirculation after reperfusion of middle cerebral artery occlusion, J. Cereb. Blood Flow. Metab. 30 (10) (2010) 1712-1720.
6. A.T. Brown, R. Flores, E. Hamilton, P.K. Roberson, M.J. Borrelli, W.C. Culp, Microbubbles improve sonothrombolysis in vitro and decrease hemorrhage in vivo in a rabbit stroke model, Invest Radiol. 46 (3) (2011) 202-207.
7. F. Xie, J. Lof, C. Everbach, A. He, R.M. Bennett, T. Matsunaga, J. Johanning, T.R. Porter, Treatment of acute intravascular thrombi with diagnostic ultrasound and intravenous microbubbles, JACC Cardiovasc. Imaging 2 (4) (2009) 511-518.
8. A. Amaral-Silva, S. Pineiro, C.A. Molina, Sonothrombolysis for the treatment of acute stroke: current concepts and future directions, Expert Rev. Neurother. 11 (2) (2011)265-273.
9. P. Cintas, F. Nguyen, B. Boneu, V. Larrue, Enhancement of enzymatic fibrinolysis with 2-MHz ultrasound and microbubbles, J. Thromb. Haemost. 2 (7) (2004) 1163-1166.
10. S. Meairs, W. Culp, Microbubbles for thrombolysis of acute ischemic stroke, Cerebrovasc. Dis. 27 (Suppl. 2) (2009) 55-65.
11. T.R. Porter, F. Xie, Ultrasound, microbubbles, and thrombolysis, Prog. Cardiovasc Dis. 44 (2) (2001) 101-110.
12. I. Kondo, K. Mizushige, T. Ueda, H. Masugata, K. Ohmori, H. Matsuo, Histological observations and the process of ultrasound contrast agent enhancement of tissue plasminogen activator thrombolysis with ultrasound exposure, Jpn. Circ. J. 63 (6) (1999) 478-484.
13. J.W. Weisel, Structure of fibrin: impact on clot stability, J. Thromb. Haemost. 5 (Suppl. 1) (2007) 116-124.
14. D.S. Liebeskind, N. Sanossian, W.H. Yong, S. Starkman, M.P. Tsang, A.L. Moya, D.D. Zheng, A.M. Abolian, D. Kim, L.K. Ali, S.H. Shah, A. Towfighi, B. Ovbiagele, C.S. Kidwell, S. Tateshima, R. Jahan, G.R. Duckwiler, F. Vinuela, N. Salamon, J.P. Villablanca, H.V. Vinters, V.J. Marder, J.L. Saver, CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke 42 (5) (2011) 1237-1243.
15. B. Petit, E. Gaud, D. Colevret, M. Arditi, F. Yan, F. Tranquart, E. Allémann, In vitro sonothrombolysis of human blood clots with BR38 microbubbles, Ultrasound Med. Biol. 38 (7) (2012) 1222-1233.
16. G.J. Shaw, M. Sperling, J.M. Meunier, Long-term stability of recombinant tissue plasminogen activator at -80 C, BMC Res. Notes. 2 (2009) 117.
17. L.C. Knight, A.Z. Budzynski, S.A. Olexa, Radiolabeling of fibrinogen using the iodogen technique, Thromb. Haemost. 46 (3) (1981) 593-596.
18. T. Ogata, K. Kimura, M. Nakajima, H. Naritomi, K. Minematsu, Diagnosis of middle cerebral artery occlusive lesions with contrast-enhanced transcranial color-coded real-time sonography in acute stroke. Neuroradiology 47 (4) (2005) 256-262.
19. P. Tanswell, U. Tebbe, K.L. Neuhaus, L. Glasle-Schwarz, J. Wojcik, E. Seifried, Pharmacokinetics and fibrin specificity of alteplase during accelerated infusions in acute myocardial infarction, J. Am. Coll. Cardiol 19 (5) (1992) 1071-1075.
20. M. Schneider, B. Anantharam, M. Arditi, D. Bokor, A. Broillet, P. Bussat, X. Fouillet, P. Frinking, I. Tardy, J. Terrettaz, R. Senior, F. Tranquart, BR38, a new ultrasound blood pool agent. Invest Radiol. 46 (8) (2011) 486-494.
21. S.S. Adam, N.S. Key, C.S. Greenberg, D-dimer antigen: current concepts and future prospects, Blood 113 (13) (2009) 2878-2887.
22. H.G. Yurka, R.N. Wissler, C.N. Zanghi, X. Liu, X. Tu, M.P. Eaton, The effective concentration of epsilon-aminocaproic acid for inhibition of fibrinolysis in neonatal plasma in vitro, Anesth. Analg 111 (1) (2010) 180-184.
23. V.G. Nielsen, L. Cankovic, B.L. Steenwyk, Epsilon-aminocaproic acid inhibition of fibrinolysis in vitro: should the 'therapeutic' concentration be reconsidered? Blood Coagul. Fibrinolysis 18 (1) (2007) 35-39.
24. C.G. Lauer, R. Burge, D.B. Tang, B.G. Bass, E.R. Gomez, B.M. Alving, Effect of ultrasound on tissue-type plasminogen activator-induced thrombolysis, Circulation 86 (4) (1992) 1257-1264.
25. D. Harpaz, X. Chen, C.W. Francis, V.J. Marder, R.S. Meltzer, Ultrasound enhancement of thrombolysis and reperfusion in vitro, J. Am. Coll. Cardiol. 21 (6) (1993) 1507-1511.
26. C.W. Francis, K. Doughney, B. Brenner, K. Klingbiel, V.J. Marder, Increased immunoreactivity of plasma after fibrinolytic activation in an anti-DD ELISA system. Role of soluble crosslinked fibrin polymers, Circulation 79 (3) (1989) 666-673.
27. J.L. Pittet, M.P. de, G. Reber, C. Durand, C. Villard, N. Piga, D. Rolland, S. Comby, G. Dupuy, VIDAS D-dimer: fast quantitative ELISA for measuring D-dimer in plasma, Clin. Chem. 42 (3) (1996) 410-415.
28. A.F. Prokop, A. Soltani, R.A. Roy, Cavitational mechanisms in ultrasound-accelerated fibrinolysis, Ultrasound Med. Biol. 33 (6) (2007) 924-933.
29. R. Flores, L.J. Hennings, J.D. Lowery, A.T. Brown, W.C. Culp, Microbubble-augmented ultrasound sonothrombolysis decreases intracranial hemorrhage in a rabbit model of acute ischemic stroke, Invest Radiol. 46 (7) (2011) 419-424.
30. C.A. Molina, M. Ribo, M. Rubiera, J. Montaner, E. Santamarina, R. Delgado-Mederos, J.F. Arenillas, R. Huertas, F. Purroy, P. Delgado, J. Alvarez-Sabin, Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke patients treated with intravenous tissue plasminogen activator, Stroke 37 (2) (2006) 425-429.
31. K.E. Hitchcock, N.M. Ivancevich, K.J. Haworth, D.N. Caudell Stamper, D.C. Vela, J.T. Sutton, G.J. Pyne-Geithman, C.K. Holland, Ultrasound-enhanced rt-PA thrombolysis in an ex vivo porcine carotid artery model, Ultrasound Med. Biol. 37 (8) (2011) 1240-1251.
32. A.D. Maxwell, C.A. Cain, A.P. Duryea, L. Yuan, H.S. Gurm, Z. Xu, Noninvasive thrombolysis using pulsed ultrasound cavitation therapy - histotripsy, Ultrasound Med. Biol. 35 (12) (2009) 1982-1994.
33. W.C. Culp, R. Flores, A.T. Brown, J.D. Lowery, P.K. Roberson, L.J. Hennings, S.D. Woods, J.H. Hatton, B.C. Culp, R.D. Skinner, M.J. Borrelli, Successful microbubble sonothrombolysis without tissue-type plasminogen activator in a rabbit model of acute ischemic stroke, Stroke 42 (8) (2011) 2280-2285.
34. M. Fatar, M. Stroick, M. Griebe, A. Alonso, S. Kreisel, R. Kern, M. Hennerici, S. Meairs, Effect of combined ultrasound and microbubbles treatment in an experimental model of cerebral ischemia, Ultrasound Med. Biol. 34 (9) (2008) 1414-1420.
35. J.J. Oliver, D.J. Webb, D.E. Newby, Stimulated tissue plasminogen activator release as a marker of endothelial function in humans, Arterioscler. Thromb. Vasc. Biol. 25 (12) (2005) 2470-2479.
36. A. Alonso, C.E. Dempfle, A. Della Martina, M. Stroick, M. Fatar, K. Zohsel, E. Allémann, M.G. Hennerici, S. Meairs, In vivo clot lysis of human thrombus with intravenous abciximab immunobubbles and ultrasound, Thromb. Res. 124 (1) (2009) 70-74.
37. F. Xie, J.M. Tsutsui, J. Lof, E.C. Unger, J. Johanning, W.C. Culp, T. Matsunaga, T. R. Porter, Effectiveness of lipid microbubbles and ultrasound in declotting thrombosis, Ultrasound Med. Biol. 31 (7) (2005) 979-985.
38. Y. Birnbaum, H. Luo, T. Nagai, M.C. Fishbein, T.M. Peterson, S. Li, D. Kricsfeld, T.R. Porter, R.J. Siegel, Noninvasive in vivo clot dissolution without a thrombolytic drug: recanalization of thrombosed iliofemoral arteries by transcutaneous ultrasound combined with intravenous infusion of microbubbles, Circulation 97 (2) (1998) 130-134.
39. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group, Tissue plasminogen activator for acute ischemic stroke, N. Engl. J. Med. 333 (24) (1995) 1581-1587.
40. F. Perren, J. Loulidi, D. Poglia, T. Landis, R. Sztajzel, Microbubble potentiated transcranial duplex ultrasound enhances IV thrombolysis in acute stroke, J. Thromb. Thrombolysis 25 (2) (2008) 219-223.
41. C.A. Molina, A.D. Barreto, G. Tsivgoulis, P. Sierzenski, M.D. Malkoff, M. Rubiera, N. Gonzales, R. Mikulik, G. Pate, J. Ostrem, W. Singleton, G. Manvelian, E.C. Unger, J.C. Grotta, P.D. Schellinger, A.V. Alexandrov, Transcranial ultrasound in clinical sonothrombolysis (TUCSON) trial, Ann. Neurol. 66 (1) (2009) 28-38.