Ultrasound enhanced thrombolysis in acute arterial ischemia

Ultrasonics

Volumn 48, Issue 4, 2008, Pages 303-311

  Tsivgoulis, Georgios ^a,b   Culp, William C ^c   Alexandrov, Andrei V ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b NATIONAL AND KAPODISTRIAN UNIVERSITY OF ATHENS   (Greece)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Microspheres; Stroke; Thrombolysis; Tissue plasminogen activator; Transcranial Doppler

Indexed keywords

ABERRATIONS; ACOUSTIC WAVES; CHEMOTHERAPY; DRUG DELIVERY; DRUG DOSAGE; LIPIDS; MEDICAL IMAGING; MICROSPHERES; OPTICAL PROPERTIES; STABILIZERS (AGENTS); ULTRASONIC IMAGING; ULTRASONIC TRANSMISSION; ULTRASONICS; ULTRASONOGRAPHY; WAVES;

(1 1 0) SURFACE; (U ,V) OPERATOR; ACUTE ISCHEMIC STROKE (AIS); ANIMAL STUDIES; ARTERIAL OCCLUSIONS; ARTERIOVENOUS GRAFTS; BREAK-UP; CEREBRAL ISCHEMIA; CLINICAL TRIALS; DOSE ESCALATION; ELSEVIER (CO); IN-VITRO; INTERNATIONAL (CO); LOW-FREQUENCY ULTRASOUND; MECHANICAL PRESSURE; NON-INVASIVE TECHNIQUES; PERIPHERAL (SPI); PHASE I; PHASE II; POTENTIAL APPLICATIONS; PULSED WAVE ULTRASOUND; RANDOMIZED CLINICAL TRIALS; RECANALIZATION; SINGLE BEAMS; TARGETED MICROBUBBLES; THROMBOLYSIS; TISSUE PLASMINOGEN ACTIVATOR (TPA); TRANSCRANIAL; TRANSCRANIAL DOPPLER (TCD);

ULTRASONIC APPLICATIONS;

FIBRINOLYTIC AGENT; MICROSPHERE; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL; BRAIN ISCHEMIA; CLINICAL TRIAL; DOPPLER ECHOGRAPHY; EQUIPMENT; FIBRINOLYTIC THERAPY; HUMAN; INSTRUMENTATION; METHODOLOGY; MULTIMODALITY CANCER THERAPY; REVIEW; ULTRASOUND THERAPY;

ANIMALS; BRAIN ISCHEMIA; CLINICAL TRIALS AS TOPIC; COMBINED MODALITY THERAPY; EQUIPMENT SAFETY; FIBRINOLYTIC AGENTS; HUMANS; MICROSPHERES; THROMBOLYTIC THERAPY; TISSUE PLASMINOGEN ACTIVATOR; ULTRASONIC THERAPY; ULTRASONOGRAPHY, DOPPLER, TRANSCRANIAL;

EID: 48149110814     PISSN: 0041624X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultras.2007.11.008     Document Type: Review

References (64)

1. Trubestein R., Bernard H.R., Etzel F., Sobbe A., Cremer A., and Stumpff U. Thrombolysis by ultrasound. Clin. Sci. Mol. Med. 51 (1976) 697-698
2. Tachibana K., and Tachibana S. Ultrasonic vibration for boosting fibrinolytic effects of urokinase in vivo. Thromb. Haemost. 46 (1981) 211
3. Lauer C.G., Burge R., Tang D.B., Bass B.G., Gomez E.R., and Alving B.M. Effect of ultrasound on tissue-type plasminogen activator-induced thrombolysis. Circulation 86 (1992) 1257-1264
4. Kimura M., Iijima S., Kobayashi K., and Furuhata H. Evaluation of the thrombolytic effect of tissue-type plasminogen activator with ultrasound irradiation: in vitro experiment involving assay of the fibrin degradation products from the clot. Biol. Pharm. Bull. 17 (1994) 126-130
5. Akiyama M., Ishibashi T., Yamada T., and Furuhata H. Low-frequency ultrasound penetrates the cranium and enhances thrombolysis in vitro. Neurosurgery 43 (1998) 828-832
6. Suchkova V., Siddiqi F.N., Carstensen E.L., Dalecki D., Child S., and Francis C.W. Enhancement of fibrinolysis with 40-kHz ultrasound. Circulation 98 (1998) 1030-1035
7. Behrens S., Daffertshoffer M., Spiegel D., and Hennerici M. Low-frequency, low-intensity ultrasound accelerates thrombolysis through the skull. Ultrasound Med. Biol. 25 (1999) 269-273
8. Ishibashi T., Akiyama M., Onoue H., Abe T., and Furuhata H. Can transcranial ultrasonication increase recanalization flow with tissue plasminogen activator?. Stroke 33 (2002) 1399-1404
9. Francis C.W., Blinc A., Lee S., and Cox C. Ultrasound accelerates transport of recombinant tissue plasminogen activator into clots. Ultrasound Med. Biol. 21 (1995) 419-424
10. Sakharov D.V., Barrertt-Bergshoeff M., Hekkenberg R.T., and Rijken D.C. Fibrin-specificity of a plasminogen activator affects the efficiency of fibrinolysis and responsiveness to ultrasound: comparison of nine plasminogen activators in vitro. Thromb. Haemost. 81 (1999) 605-612
11. Spengos K., Behrens S., Daffertshofer M., Dempfle C.E., and Hennerici M. Acceleration of thrombolysis with ultrasound through the cranium in a flow model. Ultrasound Med. Biol. 26 (2000) 889-895
12. Behrens S., Spengos K., Daffertshofer M., Schroeck H., Dempfle C.E., and Hennerici M. Transcranial ultrasound-improved thrombolysis: diagnostic vs. therapeutic ultrasound. Ultrasound Med. Biol. 27 (2001) 1683-1689
13. Blinc A., Francis C.W., Trudnowski J.L., and Carstensen E.L. Characterization of ultrasound-potentiated fibrinolysis in vitro. Blood 81 (1993) 2636-2643
14. Kimura M., Iijima S., Kobayashi K., and Furuhata H. Evaluation of the thrombolytic effect of tissue-type plasminogen activator with ultrasonic irradiation: in vitro experiment involving assay of the fibrin degradation products from the clot. Biol. Pharm. Bull. 17 (1994) 126-130
15. Suchkova V.N., Baggs R.B., and Francis C.W. Effect of 40-kHz ultrasound on acute thrombotic ischemia in a rabbit femoral artery thrombosis model: enhancement of thrombolysis and improvement in capillary muscle perfusion. Circulation 101 (2000) 2296-2301
16. Polak J.F. Ultrasound energy and the dissolution of thrombus. New Engl. J. Med. 351 (2004) 2154-2155
17. Shaw G.J., Bavani N., Dhamija A., and Lindsell C.J. Effect of mild hypothermia on the thrombolytic efficacy of 120 kHz enhanced thrombolysis in an in vitro human clot model. Thromb. Res. 117 (2006) 603-608
18. Nahirnyak V., Mast D., and Holland C.K. Ultrasound-induced thermal elevation in clotted blood and cranial bone. Ultrasound Med. Biol. 33 (2007) 1285-1295
19. Tachibana K., and Tachibana S. Albumin microbubble echo-contrast material as an enhancer for ultrasound accelerated thrombolysis. Circulation 92 (1995) 1148-1150
20. Birnbaum Y., Luo H., Nagai T., Fishbein M.C., Peterson T.M., Li S., et al. 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 (1998) 130-134
21. Culp W.C., Porter T.R., Xie F., Goertzen T.C., McCowan T.C., Vonk B.N., et al. Microbubble potentiated ultrasound as a method of declotting thrombosed dialysis grafts: experimental study in dogs. Cardiovasc. Inter. Radiol. 24 (2001) 407-412
22. Culp W.C., Porter T.R., McCowan T.C., Roberson P.K., James C.A., Matchett W.J., et al. Microbubble-augmented ultrasound declotting of thrombosed arteriovenous dialysis grafts in dogs. J. Vasc. Interv. Radiol. 14 (2003) 343-347
23. Culp W.C., Erdem E., Roberson P.K., and Husain M.M. Microbubble-potentiated ultrasound as a method of stroke therapy in a pig model: preliminary findings. J. Vasc. Interv. Radiol. 14 (2003) 1433-1436
24. Culp W.C., Porter T.R., Lowery J., Xie F., Roberson P.K., and Marky L. Intracranial clot lysis with intravenous microbubbles and transcranial ultrasound in swine. Stroke 35 (2004) 2011-2407
25. Miller M.W., Miller D.L., and Brayman A.A. A review of in vitro bioeffects of inertial ultrasonic cavitation from a mechanistic perspective. Ultrasound Med. Biol. 22 (1996) 1131-1154
26. Holland C.K., and Apfel R.E. Thresholds for transient cavitation produced by pulsed ultrasound in a controlled nuclei environment. J. Acoust. Soc. Am. 88 (1990) 2059-2069
27. Schumann P.A., Christiansen J.P., Quigley R.M., McCreery T.P., Sweitzer R.H., Unger E.C., et al. Targeted-microbubble binding selectively to GPIIb IIIa receptors of platelet thrombi. Invest. Radiol. 37 (2002) 587-593
28. Atar S., Luo H., Birnbaum Y., Nagai T., and Siegel R.J. Augmentation of in vitro clot dissolution by low-frequency high-intensity ultrasound combined with antiplatelet and antithrombotic drugs. J. Thromb. Thrombolys. 11 (2001) 223-228
29. Alonso A., Della Martina A., Stroick M., Fatar M., Griebe M., Pochon S., et al. Molecular imaging of human thrombus with novel abciximab immunobubbles and ultrasound. Stroke 38 (2007) 1508-1514
30. Sonne C., Xie F., Lof J., Oberdorfer J., Phillips P., Carr Everbach E., et al. Differences in definity and optison microbubble destruction rates at a similar mechanical index with different real-time perfusion systems. J. Am. Soc. Echocardiog. 16 (2003) 1178-1185
31. Xie F., Tsutsui J.M., Lof J., Unger E.C., Johanning J., Culp W.C., et al. Effectiveness of lipid microbubbles and ultrasound in declotting thrombosis. Ultrasound Med. Biol. 31 (2005) 979-985
32. Alexandrov A.V., Molina C.A., Grotta J.C., et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. New Engl. J. Med. 351 (2004) 2170-2178
33. Eggers J., Koch B., Meyer K., Konig I., and Seidel G. Effect of ultrasound on thrombolysis of middle cerebral artery occlusion. Ann. Neurol. 53 (2003) 797-800
34. Eggers J., Seidel G., Koch B., and Konig I.R. Sonothrombolysis in acute ischemic stroke for patients ineligible for rt-PA. Neurology 64 (2005) 1052-1054
35. Cintas P., Le Traon A.P., and Larrue V. High rate of recanalization of middle cerebral artery occlusion during 2-MHz transcranial color-coded Doppler continuous monitoring without thrombolytic drug. Stroke 33 (2002) 626-628
36. D. Skoloudik, M. Bar, P. Hradilek, D. Vaclavik, O. Skoda, Safety and efficacy of thrombotripsy - acceleration of thrombolysis by TCCS, in: CD-ROM Proceedings of the NSRG 2003 Meeting, Germany.
37. Mahon B.R., Nesbit G.M., Barnwell S.L., Clark W., Marotta T.R., Weill A., et al. North American clinical experience with the EKOS MicroLysUS infusion catheter for the treatment of embolic stroke. AJNR Am. J. Neuroradiol. 24 (2003) 534-5348
38. The IMS Study Investigators, Combined intravenous and intra-arterial recanalization for acute ischemic stroke: the interventional management of stroke study, Stroke 35 (2004) 904-912.
39. IMS II Trial Investigators, The interventional management of stroke (IMS) II study, Stroke 38 (2007) 2127-2135.
40. Daffertshoffer M., and Hennerici M. Ultrasound in the treatment of ischaemic stroke. Lancet Neurol. 2 (2003) 283-290
41. Behrens S., Spengos K., Daffertshofer M., Wirth S., and Hennerici M. Potential use of therapeutic ultrasound in ischemic stroke treatment. Echocardiography 18 (2001) 259-263
42. Daffertshofer M., and Hennerici M. Sonothrombolysis: experimental evidence. Front Neurol. Neurosci. 21 (2006) 140-149
43. Daffertshofer M., Huang Z., Fatar M., Popolo M., Schroeck H., and Kuschinsky W. Efficacy of sonothrombolysis in a rat model of embolic ischemic stroke. Neurosci. Lett. 361 (2004) 115-119
44. Daffertshofer M., and Fatar M. Therapeutic ultrasound in ischemic stroke treatment: experimental evidence. Eur. J. Ultrasound 16 (2002) 121-130
45. Eggers J. Acute stroke: therapeutic transcranial color duplex sonography. Front Neurol. Neurosci. 21 (2006) 162-170
46. Daffertshofer M., Gass A., Ringleb P., et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemia: increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator. Stroke 36 (2005) 1441-1446
47. Reinhard M., Hetzel A., Kruger S., Kretzer S., Talazko J., Ziyeh S., et al. Blood-brain barrier disruption by low-frequency ultrasound. Stroke 37 (2006) 1546-1548
48. Unger E.C., Porter T., Culp W., Labell R., Matsunaga T., and Zutshi R. Therapeutic applications of lipid-coated microbubbles. Adv. Drug Deliver. Rev. 56 (2004) 1291-1314
49. Tsutsui J.M., Xie F., Johanning J., Lof J., Cory B., He A., et al. Treatment of deeply located acute intravascular thrombi with therapeutic ultrasound guided by diagnostic ultrasound and intravenous microbubbles. J. Ultrasound Med. 25 (2006) 1161-1168
50. Wu Y., Unger E.C., McCreery T.P., Sweitzer R.H., Shen D., Wu G., et al. Binding and lysing of blood clots using MRX-408. Invest. Radiol. 33 (1998) 880-885
51. Tiukinhoy-Laing S.D., Huang S., Klegerman M., Holland C.K., and McPherson D.D. Ultrasound-facilitated thrombolysis using tissue-plasminogen activator-loaded echogenic liposomes. Thromb. Res. 119 (2007) 777-784
52. Molina C.A., Ribo M., Arenillas J., et al. Microbubbles administration accelerates clot lysis during continuous 2 MHz ultrasound monitoring in stroke patients treated with intravenous tPA. Stroke 37 (2005) 425-429
53. Alexandrov A.V., Mikulik R., Ribo M., et al. A pilot randomized clinical safety study of thrombolysis augmentation with ultrasound-activated perflutren lipid microspheres. Stroke 38 (2007) LBP4
54. Larrue V., Viguier A., Arnaud C., et al. Trancranial ultrasound combined with intravenous microbubbles and tissue plasminogen activator for acute ischemic stroke: a randomized controlled study. Stroke 38 (2007) 472
55. F. Perren, J. Loulidi, D. Poglia, T. Landis, R. Sztajzel, Microbubble potentiated transcranial duplex ultrasound enhances IV thrombolysis in acute stroke, J. Thromb. Thrombolys. (2007) May 20 (epub ahead of print).
56. Sharma V.K., Tsivgoulis G., Lao A.Y., Malkoff M.D., Alexandrov A.W., and Alexandrov A.V. Quantification of microbubble appearance in brain vessels - implications for dose calculations and drug delivery. Stroke 38 (2007) 493
57. The NINDS t-PA Stroke Study Group, Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke, Stroke 28 (1997) 2109-2118.
58. Hacke W., Kaste M., Fieschi C., et al. Randomised double-blind placebo-controlled trial of thrombolytic therapy with intravenous alteplase in acute ischaemic stroke (ECASS II). Lancet 352 (1998) 1245-1251
59. .
60. Wissgott C., Richter A., Kamusella P., and Steinkamp H.J. Treatment of critical limb ischemia using ultrasound-enhanced thrombolysis (PARES trial): final results. J. Endovasc. Ther. 14 (2007) 438-443
61. Meairs S., Wahlgren N., Dirnagl U., et al. Stroke research priorities for the next decade - a representative view of the European scientific community. Cerebrovasc. Dis. 22 (2006) 75-82
62. Bekeredjian R., Chen S., Frenkel P.A., Grayburn P.A., and Shohet R.V. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 108 (2003) 1022-1026
63. Taniyama Y., Tachibana K., Hiraoka K., Namba T., Yamasaki K., Hashiya N., et al. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 105 (2002) 1233-1239
64. Alexandrov A.V. Ultrasound enhanced thrombolysis for stroke. Intl. J. Stroke 1 (2006) 26-29