Taboos and opportunities in sonothrombolysis for stroke

References

• Tsivgoulis G, Eggers J, Ribo M, Perren F, Saqqur M, Rubiera M, et al. Safety and efficacy of ultrasound-enhanced thrombolysis: A comprehensive review and meta-analysis of randomized and nonrandomized studies. Stroke 2010; 41: 280–287
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Barlinn K, Strong R, Alexandrov AW, Aronowski J. Low-power 2-MHz pulsed-wave transcranial ultrasound reduces ischemic brain damage in rats. Transl Stroke Res 2011; 2: 376–381, doi:10.1007/s12975-011-0080-6
   PubMed Web of Science ®Google Scholar
• Fatar M, Stroick M, Griebe M, Alonso A, Kreisel S, Kern R, et al. Effect of combined ultrasound and microbubbles treatment in an experimental model of cerebral ischemia. Ultrasound Med Biol 2008; 34: 1414–1420
   PubMed Web of Science ®Google Scholar
• Daffertshofer M, Huang Z, Fatar M, Popolo M, Schroeck H, Kuschinsky W, et al. Efficacy of sonothrombolysis in a rat model of embolic ischemic stroke. Neurosci Lett 2004; 361: 115–119
   PubMed Web of Science ®Google Scholar
• Kimura M, Iijima S, Kobayashi K, 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 1994; 17: 126–130
   PubMed Web of Science ®Google Scholar
• Francis CW, Blinc A, Lee S, Cox C. Ultrasound accelerates transport of recombinant tissue plasminogen activator into clots. Ultrasound Med Biol 1995; 21: 419–424
   PubMed Web of Science ®Google Scholar
• Luo H, Steffen W, Cercek B, Arunasalam S, Maurer G, Siegel RJ. Enhancement of thrombolysis by external ultrasound. Am Heart J. 1993; 125: 1564–1569
   PubMed Web of Science ®Google Scholar
• Lapchak PA, De Taboada L. Transcranial near infrared laser treatment (NILT) increases cortical adenosine-5′-triphosphate (ATP) content following embolic strokes in rabbits. Brain Res 2010; 1306: 100–105
   PubMed Web of Science ®Google Scholar
• Zivin JA, Albers GW, Bornstein N, Chippendale T, Dahlof B, Devlin T, et al. Effectiveness and safety of transcranial laser therapy for acute ischemic stroke. Stroke 2009; 40: 1359–1364
   PubMed Web of Science ®Google Scholar
• The Internet stroke center. Efficacy and safety trial of transcranial laser therapy within 24 hours from stroke onset (NEST-3). Clinical trials. http://www.strokecenter.org/trials/clinicalstudies/efficacy-and-safety-trial-of-transcranial-laser-therapy-within-24-hours-from-stroke-onset-nest-3. Accessed 16 October 2011
   Google Scholar
• Reith J, Jorgensen HS, Pedersen PM, Nakayama H, Raaschou HO, Jeppesen LL, et al. Body temperature in acute stroke: Relation to stroke severity, infarct size, mortality, and outcome. Lancet 1996; 347: 422–425
   PubMed Web of Science ®Google Scholar
• Hammer MD, Krieger DW. Hypothermia for acute ischemic stroke: Not just another neuroprotectant. Neurologist 2003; 9: 280–289
   PubMed Web of Science ®Google Scholar
• The internet stroke center. The intravascular cooling in the treatment of stroke 2/3 trial. Clinical trials. http://www.strokecenter.org/trials/clinicalstudies/the-intravascular-cooling-in-the-treatment-of-stroke-23-trial. Accessed 16 October 2011
   Google Scholar
• Barnett SB. Intracranial temperature elevation from diagnostic ultrasound. Ultrasound Med Biol 2001; 27: 883–888
   PubMed Web of Science ®Google Scholar
• Suchkova V, Siddiqi FN, Carstensen EL, Dalecki D, Child S, Francis CW. Enhancement of fibrinolysis with 40-kHz ultrasound. Circulation 1998; 98: 1030–1035
   PubMed Web of Science ®Google Scholar
• Steffen W, Cumberland D, Gaines P, Luo H, Nita H, Maurer G, et al. Catheter-delivered high intensity, low frequency ultrasound induces vasdodilation in vivo. Eur Heart J 1994; 15: 369–376
   PubMed Web of Science ®Google Scholar
• Saguchi T, Onoue H, Urashima M, Ishibashi T, Abe T, Furuhata H. Effective and safe conditions of low-frequency transcranial ultrasound thrombolysis for acute ischemic stroke. Neurologic and histologic evaluation in a rat middle cerebral artery stroke model. Stroke 2008; 39: 1007–1011
   Google Scholar
• Daffertshofer M, Gass A, Ringleb P, Sitzer M, Sliwka U, Els T, et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemia: Increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator: Results of a phase II clinical trial. Stroke 2005; 36: 1441–1446
   PubMed Web of Science ®Google Scholar
• Reinhard M, Hetzel A, Kruger S, Kretzer S, Talazko J, Ziyeh S, et al. Blood–brain barrier disruption by low frequency ultrasound. Stroke 2006; 37: 1546–1548
   PubMed Web of Science ®Google Scholar
• Wang Z, Moehring MA, Voie AH, Furuhata H. In vitro evaluation of dual mode ultrasonic thrombolysis method for transcranial application with an occlusive thrombosis model. Ultrasound Med Biol 2008; 34: 96–102
   PubMed Web of Science ®Google Scholar
• Daffertshofer M, Fatar M. Therapeutic ultrasound in ischemic stroke treatment: Experimental evidence. Eur J Ultrasound 2002; 16: 121–130
   PubMed Web of Science ®Google Scholar
• Pfaffenberger S, Devcic-Kuhar B, El-Rabadi K, Gröschl M, Speidl WS, Weiss TW, et al. 2MHz ultrasound enhances t-PA-mediated thrombolysis: Comparison of continuous versus pulsed ultrasound and standing versus travelling acoustic waves. Thromb Haemost 2003; 89: 583–589
   PubMed Web of Science ®Google Scholar
• Schneider F, Gerriets T, Walberer M, Mueller C, Rolke R, Eicke BM, et al. Brain edema and intracerebral necrosis caused by transcranial low-frequency 20-kHz ultrasound: A safety study in rats. Stroke 2006; 37: 1301–1306
   PubMed Web of Science ®Google Scholar
• Wilhelm-Schwenkmezger T, Pittermann P, Zajonz K, Kempski O, Dieterich M, Nedelmann M. Therapeutic application of 20-kHz transcranial ultrasound in an embolic middle cerebral artery occlusion model in rats: Safety concerns. Stroke 2007; 38: 1031–1035
   PubMed Web of Science ®Google Scholar
• Everbach EC, Francis CW. Cavitational mechanisms in ultrasound-accelerated thrombolysis at 1 MHz. Ultrasound Med Biol 2000; 26: 1153–1160
   PubMed Web of Science ®Google Scholar
• Hynynen K, McDannold N, Vykhodtseva N, et al. Focal disruption of the blood–brain barrier due to 260-kHz ultrasound bursts: A method for molecular imaging and targeted drug delivery. J Neurosurg 2006; 105: 445–454
   PubMed Web of Science ®Google Scholar
• Datta S, Coussios CC, McAdory LE, et al. Correlation of cavitation with ultrasound enhancement of thrombolysis. Ultrasound Med Biol 2006; 32: 1257–1267
   PubMed Web of Science ®Google Scholar
• Azuma T, Kawabata K-I, Umemura S-I, Ogihara M, Kubota J, Sasaki A, et al. Bubble generation by standing wave in water surrounded by cranium with transcranial ultrasonic beam. Jap Soc Appl Phys 2005; 44: 4625–4630
   Web of Science ®Google Scholar
• Gateau J, Aubry J-F, Chauvet D, Boch A-L, Fink M, Tanter M. In vivo bubble nucleation probability in sheep brain tissue. Phys Med Biol 2011; 56: 7001–7015
   PubMed Web of Science ®Google Scholar
• Dalecki D, Raeman CH, Child SZ, Cox C, Francis CW, Meltzer RS, et al. Hemolysis in vivo from exposure to pulsed ultrasound. Ultrasound Med Biol 1997; 23: 307–313
   PubMed Web of Science ®Google Scholar
• Sakharov DV, Rijken DC. The effect of flow on lysis of plasma clots in a plasma environment. Thromb Haemost 2000; 83: 469–474
   PubMed Web of Science ®Google Scholar
• Sakharov DV, Hekkenberg RT, Rijken DC. Acceleration of fibrinolysis by high frequency ultrasound: The contribution of acoustic streaming and temperature rise. Thromb Res 2000; 100: 333–340
   PubMed Web of Science ®Google Scholar
• Siddiqi F, Blinc A, Braaten J, Francis CW. Ultrasound increases flow through fibrin gels. Thromb Haemost 1995; 73: 495–498
   PubMed Web of Science ®Google Scholar
• Suchkova VN, Baggs RB, Sahni SK, Francis CW. Ultrasound improves tissue perfusion in ischemic tissue through a nitric oxide dependent mechanism. Thromb Haemost 2002; 88: 865–870
   PubMed Web of Science ®Google Scholar
• NCRPExposure Criteria for Medical, Diagnostic Ultrasound: II. Criteria Based on all Known Mechanisms, Report No. 140. Bethesda, MD:National Council on Radiation Protection and Measurements, 2002
   Google Scholar
• Pfaffenberger S, Devcic-Kuhar B, Kollmann C, Kastl SP, Kaun C, Speidl WS, et al. Can a commercial diagnostic ultrasound device accelerate thrombolysis? An in vitro skull model. Stroke 2005; 36: 124–128
   PubMed Web of Science ®Google Scholar
• Alexandrov AV. Ultrasound identification and lysis of clots. Stroke 2004; 35: 2722–2725
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Tsivgoulis G. Body weight, not thrombus-burden tissue plasminogen activator dosing: But still. Stroke 2010; 41: 2723–2724
   PubMed Web of Science ®Google Scholar
• Saqqur M, Uchino K, Demchuk AM, Molina CA, Garami Z, Calleja S, et al. Site of arterial occlusion identified by transcranial Doppler predicts the response to intravenous thrombolysis for stroke. Stroke 2007; 38: 948–954
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Burgin WS, Demchuk AM, El-Mitwalli A, Grotta JC. Speed of intracranial clot lysis with intravenous tissue plasminogen activator therapy: Sonographic classification and short-term improvement. Circulation 2001; 103: 2897–2902
   PubMed Web of Science ®Google Scholar
• National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 1995; 333: 1581–1587
   PubMed Web of Science ®Google Scholar
• Saqqur M, Tsivgoulis G, Molina CA, Demchuk AM, Siddiqui M, Alvarez-Sabín J, et al. Symptomatic intracerebral hemorrhage and recanalization after IV rt-PA: A multicenter study. Neurology 2008; 71: 1304–1312
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Molina CA, Grotta JC, Garami Z, Ford SR, Alvarez-Sabin J, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N Engl J Med 2004; 351: 2170–2178
   PubMed Web of Science ®Google Scholar
• Tiukinhoy-Laing SD, Huang S, Klegerman M, Holland CK, McPherson DD. Ultrasound-facilitated thrombolysis using tissue-plasminogen activator-loaded echogenic liposomes. Thromb Res 2007; 119: 777–784
   PubMed Web of Science ®Google Scholar
• Shaw GJ, Meunier JM, Huang SL, Lindsell CJ, McPherson DD, Holland CK. Ultrasound-enhanced thrombolysis with tPA-loaded echogenic liposomes. Thromb Res 2009; 124: 306–310
   PubMed Web of Science ®Google Scholar
• Hitchcock KE, Ivancevich NM, Haworth KJ, Caudell Stamper DN, Vela DC, Sutton JT, et al. Ultrasound-enhanced rt-PA thrombolysis in an ex vivo porcine carotid artery model. Ultrasound Med Biol 2011; 37: 1240–1251
   PubMed Web of Science ®Google Scholar
• Meunier JM, Holland CK, Pancioli AM, Lindsell CJ, Shaw GJ. Effect of low frequency ultrasound on combined rt-PA and eptifibatide thrombolysis in human clots. Thromb Res 2009; 123: 528–536
   PubMed Web of Science ®Google Scholar
• Collet JP, Montalescot G, Lesty C, Weisel JW. A structural and dynamic investigation of the facilitating effect of glycoprotein IIb/IIIa inhibitors in dissolving platelet-rich clots. Circ Res 2002; 90: 428–434
   PubMed Web of Science ®Google Scholar
• Medel R, Crowley RW, McKisic MS, Dumont AS, Kassell NF. Sonothrombolysis: An emerging modality for the management of stroke. Neurosurgery 2009; 65: 979–993
   PubMed Web of Science ®Google Scholar
• Frenkel V, Oberoi J, Stone MJ, Park M, Deng C, Wood BJ, et al. Pulsed high-intensity focused ultrasound enhances thrombolysis in an in vitro model. Radiology 2006; 239: 86–93
   PubMed Web of Science ®Google Scholar
• Stone MJ, Frenkel V, Dromi S, Thomas P, Lewis RP, Li KC, et al. Pulsed-high intensity focused ultrasound enhanced tPA mediated thrombolysis in a novel in vivo clot model: A pilot study. Thromb Res 2007; 121: 193–202
   PubMed Web of Science ®Google Scholar
• Molina CA, Barreto AD, Tsivgoulis G, Sierzenski P, Malkoff MD, Rubiera M, et al. Transcranial ultrasound in clinical sonothrombolysis (TUCSON) trial. Ann Neurol 2009; 66: 28–38
   PubMed Web of Science ®Google Scholar
• Molina CA, Ribo M, Rubiera M, Montaner J, Santamarina E, Delgado-Mederos R, et al. Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke subjects treated with intravenous tissue plasminogen activator. Stroke 2006; 37: 425–429
   PubMed Web of Science ®Google Scholar
• Hitchcock KE, Holland CK. Ultrasound-assisted thrombolysis for stroke therapy: Better thrombus break-up with bubbles. Stroke 2010; 41: S50–53
   PubMed Web of Science ®Google Scholar
• Meairs S, Culp W. Microbubbles for thrombolysis of acute ischemic stroke. Cerebrovasc Dis 2009; 27: S55–65
   PubMed Web of Science ®Google Scholar
• Newell DW, Shah MM, Wilcox R, Hansmann DR, Melnychuk E, Muschelli J, et al. Minimally invasive evacuation of spontaneous intracerebral hemorrhage using sonothrombolysis. Neurosurg 2011; 115: 592–601
   Web of Science ®Google Scholar
• Baron C, Aubry JF, Tanter M, Meairs S, Fink M. Simulation of intracranial acoustic fields in clinical trials of sonothrombolysis. Ultrasound Med Biol 2009; 35: 1148–1158
   PubMed Web of Science ®Google Scholar
• Adams HP, Jr, Effron MB, Torner J, Dávalos A, Frayne J, Teal P, et al. Emergency administration of abciximab for treatment of patients with acute ischemic stroke: Results of an international phase III trial: Abciximab in Emergency Treatment of Stroke Trial (AbESTT-II). Stroke 2008; 39: 87–99
   PubMed Web of Science ®Google Scholar
• Selvaraj P, Okita K, Matsumoto Y, Voie A, Hoelscher T, Weiss HJ, Szeri A. Effects of physical properties of the skull on high intensity focused ultrasound for transcranial sonothrombolysis. J Acoust Soc Am 2011; 130: 2538
   Google Scholar
• Moehring MA, Klepper JR. Pulse Doppler ultrasound detection, characterization and size estimation of emboli in flowing blood. IEEE Trans Biomed Eng 1994; 41: 35–44
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Tsivgoulis G, Rubiera M, Vadikolias K, Stamboulis E, Molina CA, et al. End-diastolic velocity increase predicts recanalization and neurological improvement in patients with ischemic stroke with proximal arterial occlusions receiving reperfusion therapies. Stroke 2010; 41: 948–952
   PubMed Web of Science ®Google Scholar
• Fischell TA, Abbas MA, Grant GW, Siegel RJ. Ultrasound energy: Effects on vascular function and integrity. Circulation 1991; 84: 1783–1795
   PubMed Web of Science ®Google Scholar
• Siegel RJ, Gaines P, Procter A, Fischell TA, Cumberland DC. Clinical demonstration that catheter-delivered ultrasound energy reverses arterial vasoconstriction. J Am Coll Cardiol 1992; 20: 732–735
   PubMed Web of Science ®Google Scholar
• Suchkova VN, Baggs RB, Francis CW. 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 2000; 101: 2296–2301
   PubMed Web of Science ®Google Scholar
• Davics PF. Flow-mediated endothelial mechanotransduction. Physiol Rev 1995; 75: 519–560
   PubMed Web of Science ®Google Scholar
• Sugita Y, Mizuno S, Nakayama N, Iwaki T, Murakami E, Wang Z, et al. Nitric oxide generation directly responds to ultrasound exposure. Ultrasound Med Biol 2008; 34: 487–493
   PubMed Web of Science ®Google Scholar
• The Internet Stroke Center. A randomized, active controlled, double-blinded trial of the combined lysis of thrombus with ultrasound and systemic tissue plasminogen activator (tPA) for emergent revascularization (CLOTBUSTER) in acute ischemic stroke. Clinical trials. http://www.strokecenter.org/trials/clinicalstudies/a-randomized-active-controlled-double-blinded-trial-of-the-combined-lysis-of-thrombus-with-ultrasound-and-systemic-tissue-plasminogen-activator-tpa-for-emergent-revascularization-clotbuster-in-acute-ischemic-stroke. Accessed 17 October 2011
   Google Scholar
• Fischer U, Arnold M, Nedeltchev K, Brekenfeld C, Ballinari P, Remonda L, et al. NIHSS score and arteriographic findings in acute ischemic stroke. Stroke 2005; 36: 2121–2125
   PubMed Web of Science ®Google Scholar
• Lewandowski CA, Frankel M, Tomsick TA, Broderick J, Frey J, Clark W, et al. Combined intravenous and intra-arterial r-TPA versus intra-arterial therapy of acute ischemic stroke: Emergency management of stroke (EMS) bridging trial. Stroke 1999; 30: 2598–2605
   PubMed Web of Science ®Google Scholar
• Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008; 359: 1317–1329
   PubMed Web of Science ®Google Scholar
• Wolpert SM, Bruckmann H, Greenlee R, Wechsler L, Pessin MS, del Zoppo GJ. The rt-PA Acute Stroke Study Group. Neuroradiologic evaluation of patients with acute stroke treated with recombinant tissue plasminogen activator. Am J Neuroradiol 1993; 14: 3–13
   Google Scholar
• Ammi AY, Mast TD, Huang I, Abruzzo TA, Coussios CC, Shaw GJ, et al. Characterization of ultrasound propagation through ex vivo human temporal bone. Ultrasound Med Biol 2008; 34: 1578–1589
   PubMed Web of Science ®Google Scholar
• Fry FJ, Barger JE. Acoustical properties of the human skull. J Acoust Soc Am 1978; 63: 1576–1590
   PubMed Web of Science ®Google Scholar
• Schafer M, First International Sonothrombolysis Conference 2008. Mannheim, Germany
   Google Scholar