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Review

Development of transcranial sonothrombolysis as an alternative stroke therapy: incremental scientific advances toward overcoming substantial barriers

Paul A Lapchak Cedars-Sinai Medical Center, Departments of Neurology and Neurosurgery, Davis Research Building, D-2091, 110 N. George Burns Road, Los Angeles, CA 90048, USA. [email protected]; Cedars-Sinai Medical Center, Departments of Neurology and Neurosurgery, Davis Research Building, D-2091, 110 N. George Burns Road, Los Angeles, CA 90048, USA. [email protected]
,
Kiyoshi Kikuchi Cedars-Sinai Medical Center, Department of Neurology, Davis Research Building, D-2094, 110 N. George Burns Road, Los Angeles, CA 90048, USA; Department of Physiology, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan; Department of Neurosurgery, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan; Cedars-Sinai Medical Center, Department of Neurology, Davis Research Building, D-2094, 110 N. George Burns Road, Los Angeles, CA 90048, USA; Department of Physiology, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan; Department of Neurosurgery, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan
,
Pramod Butte Cedars-Sinai Medical Center, Department of Neurosurgery, Davis Research Building, D-2056, 110 N. George Burns Road, Los Angeles, CA 90048, USA; Cedars-Sinai Medical Center, Department of Neurosurgery, Davis Research Building, D-2056, 110 N. George Burns Road, Los Angeles, CA 90048, USA
&
Thilo Hölscher Brain Ultrasound Research Laboratory, Departments of Radiology and Neurosciences, University of California, San Diego, 200 West Arbor Drive, San Diego, CA 92103-8756, USA; Brain Ultrasound Research Laboratory, Departments of Radiology and Neurosciences, University of California, San Diego, 200 West Arbor Drive, San Diego, CA 92103-8756, USA
Pages 201-213 | Published online: 09 Jan 2014

References

  • Lloyd-Jones D, Adams RJ, Brown TM et al. Heart disease and stroke statistics – 2010 update: a report from the American Heart Association. Circulation 121(7), e46–e215 (2010).
  • Lloyd-Jones D, Adams RJ, Brown TM et al.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics – 2010 update: a report from the American Heart Association. Circulation 121(7), 948–954 (2010).
  • Boudreau DM, Guzauskas G, Villa KF, Fagan SC, Veenstra DL. A model of cost–effectiveness of tissue plasminogen activator in patient subgroups 3 to 4.5 hours after onset of acute ischemic stroke. Ann. Emerg. Med. 61(1), 46–55 (2013).
  • Roger VL, Go AS, Lloyd-Jones DM et al.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics – 2011 update: a report from the American Heart Association. Circulation 123(4), e18–e209 (2011).
  • Roger VL, Go AS, Lloyd-Jones DM et al.; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics – 2012 update: a report from the American Heart Association. Circulation 125(1), e2–e220 (2012).
  • Hacke W, Kaste M, Bluhmki E et al.; ECASS Investigators. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 359(13), 1317–1329 (2008).
  • Lansberg MG, Bluhmki E, Thijs VN. Efficacy and safety of tissue plasminogen activator 3 to 4.5 hours after acute ischemic stroke: a metaanalysis. Stroke 40(7), 2438–2441 (2009).
  • Sandercock P, Wardlaw JM, Lindley RI et al; IST-3 collaborative group. The benefits and harms of intravenous thrombolysis with recombinant tissue plasminogen activator within 6 h of acute ischaemic stroke (the third international stroke trial [IST-3]): a randomised controlled trial. Lancet 379(9834), 2352–2363 (2012).
  • Fang MC, Cutler DM, Rosen AB. Trends in thrombolytic use for ischemic stroke in the United States. J. Hosp. Med. 5(7), 406–409 (2010).
  • Francis CW, Onundarson PT, Carstensen EL et al. Enhancement of fibrinolysis in vitro by ultrasound. J. Clin. Invest. 90(5), 2063–2068 (1992).
  • Braaten JV, Goss RA, Francis CW. Ultrasound reversibly disaggregates fibrin fibers. Thromb. Haemost. 78(3), 1063–1068 (1997).
  • Siddiqi F, Odrljin TM, Fay PJ, Cox C, Francis CW. Binding of tissue-plasminogen activator to fibrin: effect of ultrasound. Blood 91(6), 2019–2025 (1998).
  • Sakharov DV, Rijken DC. The effect of flow on lysis of plasma clots in a plasma environment. Thromb. Haemost. 83(3), 469–474 (2000).
  • Datta S, Coussios CC, McAdory LE et al. Correlation of cavitation with ultrasound enhancement of thrombolysis. Ultrasound Med. Biol. 32(8), 1257–1267 (2006).
  • Prokop AF, Soltani A, Roy RA. Cavitational mechanisms in ultrasound-accelerated fibrinolysis. Ultrasound Med. Biol. 33(6), 924–933 (2007).
  • Everbach EC, Francis CW. Cavitational mechanisms in ultrasound-accelerated thrombolysis at 1 MHz. Ultrasound Med. Biol. 26(7), 1153–1160 (2000).
  • Harvey EN. Biological aspects of ultrasonic waves, a general survey. Biol. Bull. 59, 306–325 (1930).
  • Lynn JG, Zwemer RL, Chick AJ, Miller AE. A new method for the generation and use of focused ultrasound in experimental biology. J. Gen. Physiol. 26(2), 179–193 (1942).
  • Fry WJ, Barnard JW, Fry EJ, Krumins RF, Brennan JF. Ultrasonic lesions in the mammalian central nervous system. Science 122(3168), 517–518 (1955).
  • Fry WJ, Barnard JW, Fry FJ, Brennan JF. Ultrasonically produced localized selective lesions in the central nervous system. Am. J. Phys. Med. 34(3), 413–423 (1955).
  • Bakay L, Ballantine HT Jr, Hueter TF, Sosa D. Ultrasonically produced changes in the blood–brain barrier. AMA Arch. Neurol. Psychiatry 76(5), 457–467 (1956).
  • Fry WJ, Fry FJ. Fundamental neurological research and human neurosurgery using intense ultrasound. IRE Trans. Med. Electron. ME-7, 166–181 (1960).
  • Fry FJ, Kossoff G, Eggleton RC, Dunn F. Threshold ultrasonic dosages for structural changes in the mammalian brain. J. Acoust. Soc. Am. 48(6), Suppl. 2, 1413+ (1970).
  • Fry FJ, Goss SA. Further studies of the transkull transmission of an intense focused ultrasonic beam: lesion production at 500 kHz. Ultrasound Med. Biol. 6(1), 33–38 (1980).
  • Clement GT, Hynynen K. A noninvasive method for focusing ultrasound through the human skull. Phys. Med. Biol. 47(8), 1219–1236 (2002).
  • Hynynen K, Vykhodtseva NI, Chung AH, Sorrentino V, Colucci V, Jolesz FA. Thermal effects of focused ultrasound on the brain: determination with MR imaging. Radiology 204(1), 247–253 (1997).
  • Clement GT, White PJ, King RL, McDannold N, Hynynen K. A magnetic resonance imaging-compatible, large-scale array for trans-skull ultrasound surgery and therapy. J. Ultrasound Med. 24(8), 1117–1125 (2005).
  • Lapchak PA. Recommendations and practices to optimize stroke therapy: developing effective translational research programs. Stroke doi:10.1007/s12975-012-0209-2 (2013) (Epub ahead of print).
  • Schäfer S, Kliner S, Klinghammer L et al. Influence of ultrasound operating parameters on ultrasound-induced thrombolysis in vitro. Ultrasound Med. Biol. 31(6), 841–847 (2005).
  • Meunier JM, Holland CK, Lindsell CJ, Shaw GJ. Duty cycle dependence of ultrasound enhanced thrombolysis in a human clot model. Ultrasound Med. Biol. 33(4), 576–583 (2007).
  • 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 38(3), 1031–1035 (2007).
  • Daffertshofer M, Huang Z, Fatar M et al. Efficacy of sonothrombolysis in a rat model of embolic ischemic stroke. Neurosci. Lett. 361(1–3), 115–119 (2004).
  • Rosenschein U, Furman V, Kerner E, Fabian I, Bernheim J, Eshel Y. Ultrasound imaging-guided noninvasive ultrasound thrombolysis: preclinical results. Circulation 102(2), 238–245 (2000).
  • Frenkel V, Oberoi J, Stone MJ et al. Pulsed high-intensity focused ultrasound enhances thrombolysis in an in vitro model. Radiology 239(1), 86–93 (2006).
  • Stone MJ, Frenkel V, Dromi S et al. Pulsed-high intensity focused ultrasound enhanced tPA mediated thrombolysis in a novel in vivo clot model, a pilot study. Thromb. Res. 121(2), 193–202 (2007).
  • Williams AR, Chater BV, Allen KA, Sherwood MR, Sanderson JH. Release of beta-thromboglobulin from human platelets by therapeutic intensities of ultrasound. Br. J. Haematol. 40(1), 133–142 (1978).
  • Kornowski R, Meltzer RS, Chernine A, Vered Z, Battler A. Does external ultrasound accelerate thrombolysis? Results from a rabbit model. Circulation 89(1), 339–344 (1994).
  • Poliachik SL, Chandler WL, Mourad PD et al. Effect of high-intensity focused ultrasound on whole blood with and without microbubble contrast agent. Ultrasound Med. Biol. 25(6), 991–998 (1999).
  • Hademenos GJ, Massoud TF. Biophysical mechanisms of stroke. Stroke 28(10), 2067–2077 (1997).
  • Marder VJ, Chute DJ, Starkman S et al. Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke. Stroke 37(8), 2086–2093 (2006).
  • Saguchi T, Onoue H, Urashima M, Ishibashi T, Abe T, Furuhata H. Effective and safe conditions of low-frequency transcranial ultrasonic thrombolysis for acute ischemic stroke: neurologic and histologic evaluation in a rat middle cerebral artery stroke model. Stroke 39(3), 1007–1011 (2008).
  • Culp WC, Flores R, Brown AT et al. Successful microbubble sonothrombolysis without tissue-type plasminogen activator in a rabbit model of acute ischemic stroke. Stroke 42(8), 2280–2285 (2011).
  • Flores R, Hennings LJ, Lowery JD, Brown AT, Culp WC. Microbubble-augmented ultrasound sonothrombolysis decreases intracranial hemorrhage in a rabbit model of acute ischemic stroke. Invest. Radiol. 46(7), 419–424 (2011).
  • Burgess A, Huang Y, Waspe AC et al. High-intensity focused ultrasound (HIFU) for dissolution of clots in a rabbit model of embolic stroke. PLoS ONE 7(8), e42311 (2012).
  • Shimizu J, Fukuda T, Abe T et al. Ultrasound safety with midfrequency transcranial sonothrombolysis: preliminary study on normal macaca monkey brain. Ultrasound Med. Biol. 38(6), 1040–1050 (2012).
  • Culp WC, Erdem E, Roberson PK, Husain MM. Microbubble potentiated ultrasound as a method of stroke therapy in a pig model: preliminary findings. J. Vasc. Interv. Radiol. 14(11), 1433–1436 (2003).
  • Alexandrov AV, Mikulik R, Ribo M et al. A pilot randomized clinical safety study of sonothrombolysis augmentation with ultrasound-activated perflutren-lipid, microspheres for acute ischemic stroke. Stroke 39(5), 1464–1469 (2008).
  • Alexandrov AV, Molina CA, Grotta JC et al.; CLOTBUST Investigators. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N. Engl. J. Med. 351(21), 2170–2178 (2004).
  • Molina CA, Barreto AD, Tsivgoulis G et al. Transcranial ultrasound in clinical sonothrombolysis (TUCSON) trial. Ann. Neurol. 66(1), 28–38 (2009).
  • Eggers J, König IR, Koch B, Händler G, Seidel G. Sonothrombolysis with transcranial color-coded sonography and recombinant tissue-type plasminogen activator in acute middle cerebral artery main stem occlusion: results from a randomized study. Stroke 39(5), 1470–1475 (2008).
  • Eggers J, Seidel G, Koch B, König IR. Sonothrombolysis in acute ischemic stroke for patients ineligible for rt-PA. Neurology 64(6), 1052–1054 (2005).
  • Devcic-Kuhar B, Pfaffenberger S, Gherardini L et al. Ultrasound affects distribution of plasminogen and tissue-type plasminogen activator in whole blood clots in vitro. Thromb. Haemost. 92(5), 980–985 (2004).
  • Pfaffenberger S, Devcic-Kuhar B, El-Rabadi K et al. 2MHz ultrasound enhances tPA-mediated thrombolysis: comparison of continuous versus pulsed ultrasound and standing versus travelling acoustic waves. Thromb. Haemost. 89(3), 583–589 (2003).
  • Datta S, Coussios CC, Ammi AY, Mast TD, de Courten-Myers GM, Holland CK. Ultrasound-enhanced thrombolysis using Definity as a cavitation nucleation agent. Ultrasound Med. Biol. 34(9), 1421–1433 (2008).
  • Behrens S, Daffertshofer M, Spiegel D, Hennerici M. Low-frequency, low-intensity ultrasound accelerates thrombolysis through the skull. Ultrasound Med. Biol. 25(2), 269–273 (1999).
  • Holscher T, Raman R, Ernström K et al. In vitro sonothrombolysis with duplex ultrasound: first results using a simplified model. Cerebrovasc. Dis. 28(4), 365–370 (2009).
  • Alonso A, Dempfle CE, Della Martina A et al. In vivo clot lysis of human thrombus with intravenous abciximab immunobubbles and ultrasound. Thromb. Res. 124(1), 70–74 (2009).
  • Dijkmans PA, Juffermans LJ, Musters RJ et al. Microbubbles and ultrasound: from diagnosis to therapy. Eur. J. Echocardiogr. 5(4), 245–256 (2004).
  • 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: results of a Phase II clinical trial. Stroke 36(7), 1441–1446 (2005).
  • Siegel RJ, Atar S, Fishbein MC et al. Noninvasive transcutaneous low frequency ultrasound enhances thrombolysis in peripheral and coronary arteries. Echocardiography 18(3), 247–257 (2001).
  • STAIR. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30(12), 2752–2758 (1999).
  • Wang Z, Fukuda T, Azuma T, Furuhata H. Safety of low-frequency transcranial ultrasound in permanent middle cerebral artery occlusion in spontaneously hypertensive rats. Cerebrovasc. Dis. 33(1), 23–29 (2012).
  • Fatar M, Stroick M, Griebe M, Alonso A, Hennerici MG, Daffertshofer M. Brain temperature during 340-kHz pulsed ultrasound insonation: a safety study for sonothrombolysis. Stroke 37(7), 1883–1887 (2006).
  • Schneider F, Gerriets T, Walberer M et al. Brain edema and intracerebral necrosis caused by transcranial low-frequency 20-kHz ultrasound: a safety study in rats. Stroke 37(5), 1301–1306 (2006).
  • Casals JB, Pieri NC, Feitosa ML et al. The use of animal models for stroke research: a review. Comp. Med. 61(4), 305–313 (2011).
  • Lapchak PA. Translational stroke research using a rabbit embolic stroke model: a correlative analysis hypothesis for novel therapy development. Transl. Stroke Res. 1(2), 96–107 (2010).
  • Turner RJ, Jickling GC, Sharp FR. Are underlying assumptions of current animal models of human stroke correct: from STAIRs to High Hurdles? Transl. Stroke Res. 2(2), 138–143 (2011).
  • Donnan GA. The 2007 Feinberg lecture: a new road map for neuroprotection. Stroke 39(1), 242 (2008).
  • Tsivgoulis G, Eggers J, Ribo M et al. Safety and efficacy of ultrasound-enhanced thrombolysis: a comprehensive review and meta-analysis of randomized and nonrandomized studies. Stroke. 41(2), 280–287 (2010).
  • Ricci S, Dinia L, Del Sette M et al. Sonothrombolysis for acute ischaemic stroke. Cochrane Database Syst. Rev. 10, CD008348 (2012).
  • Tsivgoulis G, Culp WC, Alexandrov AV. Ultrasound enhanced thrombolysis in acute arterial ischemia. Ultrasonics 48(4), 303–311 (2008).
  • Tsivgoulis G, Alexandrov AV. Ultrasound-enhanced thrombolysis in acute ischemic stroke: potential, failures, and safety. Neurotherapeutics 4(3), 420–427 (2007).
  • Meairs S, Alonso A, Hennerici MG. Progress in sonothrombolysis for the treatment of stroke. Stroke 43(6), 1706–1710 (2012).
  • Eggers J, Koch B, Meyer K, König I, Seidel G. Effect of ultrasound on thrombolysis of middle cerebral artery occlusion. Ann. Neurol. 53(6), 797–800 (2003).
  • Alexandrov AV, Wojner AW, Grotta JC; CLOTBUST Investigators. CLOTBUST: design of a randomized trial of ultrasound-enhanced thrombolysis for acute ischemic stroke. J. Neuroimaging 14(2), 108–112 (2004).
  • Saver JL. Improving reperfusion therapy for acute ischaemic stroke. J. Thromb. Haemost. 9(Suppl. 1), 333–343 (2011).
  • Baron C, Aubry JF, Tanter M, Meairs S, Fink M. Simulation of intracranial acoustic fields in clinical trials of sonothrombolysis. Ultrasound Med. Biol. 35(7), 1148–1158 (2009).
  • Kobayashi N, Yasu T, Yamada S et al. Influence of contrast ultrasonography with perflutren lipid microspheres on microvessel injury. Circ. J. 67(7), 630–636 (2003).
  • Alexandrov AV, Tsivgoulis G, Rubiera M et al.; TUCSON Investigators. End-diastolic velocity increase predicts recanalization and neurological improvement in patients with ischemic stroke with proximal arterial occlusions receiving reperfusion therapies. Stroke 41(5), 948–952 (2010).
  • Barlinn K, Tsivgoulis G, Molina CA et al.; for the TUCSON Investigators. Exploratory analysis of estimated acoustic peak rarefaction pressure, recanalization, and outcome in the transcranial ultrasound in clinical sonothrombolysis trial. J. Clin. Ultrasound doi:10.1002/jcu.21978 (2012) (Epub ahead of print).
  • Perren F, Loulidi J, Poglia D, Landis T, Sztajzel R. Microbubble potentiated transcranial duplex ultrasound enhances IV thrombolysis in acute stroke. J. Thromb. Thrombolysis 25(2), 219–223 (2008).
  • Hölscher T, Fisher DJ, Ahadi G, Voie A. Introduction of a rabbit carotid artery model for sonothrombolysis research. Transl. Stroke Res. 3(3), 397–407 (2012).
  • Meairs S, Culp W. Microbubbles for thrombolysis of acute ischemic stroke. Cerebrovasc. Dis. 27(Suppl. 2), 55–65 (2009).
  • Molina CA, Ribo M, Rubiera M et al. Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke patients treated with intravenous tissue plasminogen activator. Stroke 37(2), 425–429 (2006).
  • Borrelli MJ, O’Brien WD Jr, Hamilton E et al. Influences of microbubble diameter and ultrasonic parameters on in vitro sonothrombolysis efficacy. J. Vasc. Interv. Radiol. 23(12), 1677–1684.e1 (2012).
  • Leeman JE, Kim JS, Yu FT et al. Effect of acoustic conditions on microbubble-mediated microvascular sonothrombolysis. Ultrasound Med. Biol. 38(9), 1589–1598 (2012).
  • Martin E, Jeanmonod D, Morel A, Zadicario E, Werner B. High-intensity focused ultrasound for noninvasive functional neurosurgery. Ann. Neurol. 66(6), 858–861 (2009).
  • Damianou C, Ioannides K, Hadjisavvas V, Mylonas N, Couppis A, Iosif D. In vitro and in vivo brain ablation created by high-intensity focused ultrasound and monitored by MRI. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 56(6), 1189–1198 (2009).
  • ter Haar GR. High intensity focused ultrasound for the treatment of tumors. Echocardiography 18(4), 317–322 (2001).
  • Jolesz FA, McDannold N. Current status and future potential of MRI-guided focused ultrasound surgery. J. Magn. Reson. Imaging 27(2), 391–399 (2008).
  • Maxwell AD, Cain CA, Duryea AP, Yuan L, Gurm HS, Xu Z. Noninvasive thrombolysis using pulsed ultrasound cavitation therapy – histotripsy. Ultrasound Med. Biol. 35(12), 1982–1994 (2009).
  • Spengos K, Behrens S, Daffertshofer M, Dempfle CE, Hennerici M. Acceleration of thrombolysis with ultrasound through the cranium in a flow model. Ultrasound Med. Biol. 26(5), 889–895 (2000).

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