Sonothrombolysis: An Emerging Modality for the Treatment of Acute Ischemic and Hemorrhagic Stroke

Translational Stroke Research

Volumn 2, Issue 2, 2011, Pages 159-170

  Soltani, Azita ^a   Clark, Wayne M ^b   Hansmann, Douglas R ^a  

^a EKOS Corporation   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Acute ischemic stroke; Endovascular sonothrombolysis; Hemorrhagic stroke; Transcranial sonothrombolysis

Indexed keywords

ABCIXIMAB; ACETYLSALICYLIC ACID; ALBUMIN; ALTEPLASE; DESMOTEPLASE; ECHO CONTRAST MEDIUM; EPTIFIBATIDE; HYPERTENSIVE AGENT; MAGNESIUM SULFATE; MINOCYCLINE; MRX 801; NORPHENAZONE; PERFLUTREN; SHU 508; SONOVUE; UNCLASSIFIED DRUG;

BLOOD CLOT LYSIS; BRAIN BLOOD FLOW; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CONTINUOUS INFUSION; DOPPLER ECHOGRAPHY; DRUG EFFICACY; HUMAN; MECHANICAL THROMBECTOMY; NEUROIMAGING; NEUROPROTECTION; PRIORITY JOURNAL; REVIEW; SONOTHROMBOLYSIS;

EID: 79955764407     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-011-0077-1     Document Type: Review

References (89)

1. Goldstein LB, Adams R, Alberts MJ, Appel LJ, Brass LM, Bushnell CD, et al. Primary prevention of ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council: cosponsored by the Atherosclerotic Peripheral Vascular Disease Interdisciplinary Working Group; Cardiovascular Nursing Council; Clinical Cardiology Council; Nutrition, Physical Activity, and Metabolism Council; and the Quality of Care and Outcomes Research Interdisciplinary Working Group. Stroke. 2006; 37: 1583-633.
2. MacKay J, Mensah G. Atlas of heart disease and stroke. Geneva: World Health Organization; 2004.
3. del Zoppo G, Poeck K, Pessin M, Wolpert SM, Furlan AJ, Ferbert A, et al. Recombinant tissue plasminogen activator in acute thrombotic and embolic stroke. Ann of Neurol. 1992; 32: 78-85.
4. Fieschi C, Argentino C, Lenzi G, Sacchetti M, Toni D, Bozzao L. Clinical and instrumental evaluation of patients with ischemic stroke within the first six hours. J Neurol Sci. 1989; 91: 311-22.
5. Watenberg KE, Mayer SA. Reducing the risk of ICH enlargement. J Neurol Sci. 2007; 261: 99-107.
6. Hallevi H, Albright KC, Aronowski J, Barreto AD, Martin-Schild S, Khaja AM, et al. Intraventricular hemorrhage: anatomic relationships and clinical implications. Neurology. 2008; 70: 848-52.
7. Young W, Lee KP, Pessin MS, Kwan ES, Rand WM, Caplan LR. Prognostic significance of ventricular blood in supratentorial hemorrhage: a volumetric study. Neurology. 1990; 40: 616-9.
8. Report of the Stroke Progress Review Group: National Institute of Health/National Institute of Neurological Disorders and Stroke. http://www. ninds. nih. gov/find_people/groups/stroke_prg/04_2002_stroke_prg_report. htm (2002). Accessed 7 Dec 2010.
9. Adams Jr HP, del Zoppo G, Alberts MJ, Bhatt DL, Brass L, Furlan A, et al. Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: the American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists. Stroke. 2007; 38: 1655-711.
10. Del Zoppo GJ, Saver JL, Jauch EC, Adams HP. Expansion of the time window for treatment of acute ischemic stroke with intravenous tissue plasminogen activator: a science advisory from the American Heart Association/American Stroke Association. Stroke. 2009; 40: 2945-8.
11. Ringleb PA, Bousser MG, Ford G, Bath P, Brainin M, Caso V, et al. Guidelines for management of ischemic stroke and transient ischemic attack 2008. Cerebrovasc Dis. 2008; 25: 457-507.
12. European Stroke Organization guideline update, January 2009. http://www. eso-stroke. org/pdf/ESOGuidelines_update_Jan_2009. pdf (2009). Accessed 1 Dec 2010.
13. Anonymous. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke, rt-PA Stroke Study Group. N Engl J Med. 1995; 333: 1581-7.
14. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D, et al. ECASS Investigators. Thrombolysis with alteplase 3 to 4. 5 hours after acute ischemic stroke. N Engl J Med. 2008; 359: 1317-29.
15. Smith WS, Sung G, Starkman S, Saver JL, Kidwell CS, Gobin YP, et al. Safety and efficacy of mechanical embolectomy in acute ischemic stroke: results of the MERCI trial. Stroke. 2005; 36: 1432-8.
16. Anonymous. CAST randomized placebo-controlled trial of early aspirin use in 20, 000 patients with acute ischaemic stroke. CAST (Chinese Acute Stroke Trial) Collaborative Group. Lancet. 1997; 349: 1641-9.
17. International Stroke Trial Collaborative Group. The International Stroke Trial (IST): a randomized trial of aspirin, subcutaneous heparin, both, or neither among 19, 435 patients with acute ischemic stroke. Lancet. 1997; 349: 1569-81.
18. Rordorf G, Koroshetz WJ, Ezzeddine MA, Segal AZ, Buonanno FS. A pilot study of drug-induced hypertension for treatment of acute stroke. Neurology. 2001; 56: 1210-3.
19. Hacke W, Albers G, Al-Rawi Y. The Desmoteplase in acute ischemic stroke trial (DIAS). A phase II MRI-based 9-hour window acute stroke thrombolysis trial with intravenous desmoteplase. Stroke. 2005; 36: 66-73.
20. Parsons MW, Miteff F, Bateman GA, Spratt N, Loiselle A, Attia J, et al. Acute ischemic stroke: imaging-guided tenecteplase treatment in an extended time window. Neurology. 2009; 72: 915-21.
21. Pancioli AM, Broderick J, Brott T, Tomsick T, Khoury J, Bean J, et al. The combined approach to lysis utilizing eptifibatide and rt-PA in acute ischemic stroke: the CLEAR stroke trial. Stroke. 2008; 39: 3268-76.
22. Ginsberg MD, Hill MD, Palesch YY, Ryckborst KJ, Tamariz D. The ALIAS Pilot Trial: a dose-escalation and safety study of albumin therapy for acute ischemic stroke-I: physiological responses and safety results. Stroke. 2006; 37: 2100-6.
23. Palesch YY, Hill MD, Ryckborst KJ, Tamariz D, Ginsberg MD. The ALIAS pilot trial: a dose-esclation and safety study of albumin therapy for acute ischemic stroke-II: neurologic outcome and efficacy analysis. Stroke. 2006; 37: 2107-14.
24. Fagan SC, Waller JL, Nichols FT, Edwards DJ, Pettigrew LC, Clark WM, et al. Minocycline to improve neurologic outcome in stroke (MINOS): a dose finding study. Stroke. 2010; 41: 2283-7.
25. Saver JL, Kidwell C, Eckstein M, Starkman S, FAST-MAG Pilot Trial Investigators. Prehospital neuroprotective therapy for acute stroke: results of the Field Administration of Stroke-Therapy Magnesium (FAST-MAG) pilot trial. Stroke. 2004; 35: e106-8.
26. Otomo E et al. Effect of a novel free radical scavenger, edaravone (MCI-186), on acute brain infarction. Randomized, placebo-controlled, double-blind study at multicenters. Cerebrovasc Dis. 2003; 15: 222-9.
27. Kulcsar Z, Bonvin C, Pereira VM, Altrichter S, Yilmaz H, Loevblad KO, et al. Penumbra system: a novel mechanical thrombectomy device for large-vessel occlusions in acute stroke. Am J Neuroradiol. 2010; 31: 628-33.
28. Castano C, Dorado L, Guerrero C, Millan M, Gomis M, Perez de la Ossa N, et al. Mechanical thrombectomy with the solitaire AB device in large artery occlusions of the anterior circulation. Stroke. 2010; 41: 1836-40.
29. Shuaib A, Sentis Steering Committee. SENTIS: a randomized trial evaluating vertebral perfusion augmentation via partial aortic occlusion in acute ischemic stroke. 7th World Stroke Congress; 2010 16 Oct 2010; Abstract 1154.
30. Gonzalez A, Mayol A, Martinez E, Gonzalez-Marcos JR, Gil-Peralta A. Mechanical thrombectomy with snare in patients with acute ischemic stroke. Neuroradiology. 2007; 49: 365-72.
31. Mayer TE, Hamann GF, Brueckmann HJ. Treatment of basilar artery embolism with a mechanical extraction device. Stroke. 2002; 33: 2232-5.
32. Hemmen TM, Raman R, Guluma KZ, Meyer BC, Gomes JA, Cruz-Flores S, et al. Intravenous thrombolysis plus hypothermia for acute treatment of ischemic stroke (ICTuS-L). Final results. Stroke. 2010; 41: 2265-70.
33. 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: 1359-64.
34. Morgenstern LB, Hemphill JC, Anderson C, Becker K, Broderick JP, Es Jr Connolly, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2010; 41: 2108-29.
35. Steiner T, Katse M, Forsting M, Mendelow D, Kwiecinski H, Szikora I, et al. Recommendations for the management of intracranial haemorrhage-part I: spontaneous intracerebral haemorrhage. The European Stroke Initiative Writing Committee and the Writing Committee for the EUSI Executive Committee. Cerebrovasc Dis. 2006; 22: 294-316.
36. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med. 2008; 358: 2127-37.
37. Morgan T, Awad I, Keyl P, Lane K, Hanley DF. Preliminary report of the clot lysis evaluating accelerated resolution of intraventricular hemorrhage (CLEAR-IVH) clinical trial. Acta Neurochir Suppl. 2008; 105: 217-20.
38. 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: 2897-902.
39. Rha JH, Saver JL. The impact of recanalization on ischemic stroke outcome: a meta-analysis. Stroke. 2007; 38: 967-73.
40. Kornowski R, Meltzer RS, Chernine A, Vered Z, Battler A. Does external ultrasound accelerate thrombolysis? Results from a rabbit model. Circulation. 1994; 89: 339-44.
41. Tachibana K, Tachibana S. Prototype therapeutic ultrasound emitting catheter for accelerating thromblolysis. J Ultrasound Med. 1997; 16: 529-35.
42. Olsson SB, Johansson B, Nilsson AM, Olsson Ch, Roijer A. Enhancement of thrombolysis by ultrasound. Ultrasound Med Biol. 1994; 20: 375-82.
43. Cintas P, Le Traon AP, Larrue V. High rate of recanalization of middle cerebral artery occlusion during 2-MHz transcranial color-coded Doppler continuous monitoring without thrombolytic drug. Stroke. 2002; 33: 626-8.
44. Francis CW, Oenunderson PT, Carstensen EL, Blinc A, Meltzer RS. Enhancement of fibrinolysis in vitro by ultrasound. J Clin Invest. 1992; 90: 2063-8.
45. Luo H, Nishioka T, Fishbein MC, Cercek B, Forrester JS, Kim CJ, et al. Transcutaneous ultrasound augments lysis of arterial thrombi in vivo. Circulation. 1996; 94: 775-8.
46. Anonymous. Assessment: transcranial Doppler. Report of the American Academy of Neurology, Therapeutics and Technology Assessment Subcommittee. Neurology. 1990; 40: 680-1.
47. Postert T, Federlein J, Przuntek H, Buettner T. Insufficient and absent acoustic temporal bone window: potential and limitations of transcranial contrast-enhanced color-coded sonography and contrast-enhanced power-based sonography. Ultrasound Med Biol. 1997; 23: 857-62.
48. Alexandrov AV, Demchuk AM, Felberg RA, Christou I, Barber PA, Burgin WS, et al. High rate of complete recanalization and dramatic clinical recovery during tPA infusion when continuously monitored with 2-MHz transcranial Doppler monitoring. Stroke. 2000; 31: 610-4.
49. Aexandrov AV, Demchuk AM, Burgin S, Robinson DJ, Grotta JC, et al. Ultrasound-enhanced thrombolysis for acute ischemic stroke: phase I. Finding of the CLOTBUST trial. J Neuroimaging. 2004; 14: 113-7.
50. 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: 2170-8.
51. Pfaffenberger S, Devcic-Kuhar B, Kollmann C, Kastl SP, Kaum C, Speidl WS, et al. Can a commercial diagnostic ultrasound device accelerate thrombolysis? An in vitro skull model. Stroke. 2005; 36: 124-8.
52. Swiercz M, Swiat M, Pawlak M, Weigele J, Tarasewicz R, Sobolewski A, et al. Narrowing of the middle cerebral artery: artificial intelligence methods and comparison of transcranial color coded duplex sonography with conventional TCD. Ultrasound Med Biol. 2010; 36: 17-28.
53. Eggers J, Koch B, Meyer K, König I, Seidel G. Effect of ultrasound on thromobolysis of middle cerebral artery occlusion. Ann Neurol. 2003; 53: 797-800.
54. Eggers J, Koenig 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. 2008; 39: 1470-5.
55. Eggers J, Sedel G, Koch B, König IR. Sonothrombolysis in acute ischemic stroke for patients ineligible for rt-PA. Neurology. 2005; 64: 1052-4.
56. Siddiqi F, Odrljin TM, Fay PJ, Cox C, Francis CW. Binding of tissue-plasminogen activator to fibrin: effect of ultrasound. Blood. 1998; 91: 2019-25.
57. Braaten JV, Goss RA, Francis CW. Ultrasound reversibly disaggregates fibrin fibers. Thromb Haemost. 1997; 78: 1063-8.
58. Daffertshofer M, Gass A, Ringleb P, Sitzer M, Sliwka U, Els T, et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemic: increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator: results of a phase II clinical trial. Stroke. 2005; 36: 1441-6.
59. Hölscher T, Wilkening WG, Molkenstruck S, Voit H, Koch C. Transcranial sound field characterization. Ultrasound Med Biol. 2008; 34: 973-80.
60. Apfel RE, Holland CK. Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound Med Biol. 1991; 17: 179-85.
61. Datta S, Coussios CC, McAdory LE, Porter T, De Courten-Myers G, et al. Correlation of cavitation with ultrasound enhancement of thrombolysis. Ultrasound Med Biol. 2006; 32: 1257-67.
62. Deng CX, Xu Q, Apfel Re, Holland CK. In vitro measurement of inertial cavitation thresholds in human blood. Ultrasound Med Biol. 1996; 22: 939-48.
63. Mahon BR, Nesbit GM, Barnwell SL, Clark W, Marotta TR, Weill A, et al. North American clinical experience with the EKOS MicroLysUS infusion catheter for the treatment of embolic stroke. Am J Neuroradiol. 2003; 24: 534-8.
64. Furlan AJ. Acute stroke therapy: beyond IV tPA. Cleve Clin J Med. 2002; 69: 730-4.
65. Jones MM, Nogajski JH, Faulder K, Harrington T, Ng P, Storey CE. Intra-arterial thrombolysis in acute ischemic stroke. Intern Med J. 2005; 35: 300-2.
66. IMS II trial investigators. The Interventional Management of Stroke (IMS) II Study. Stroke. 2007; 38: 2127-35.
67. Khatri P, Hill MD, Palesch YY, Spilker J, Jauch EC, Carrozzella JA, et al. Methodology of the interventional management of stroke III trial. Int J Stroke. 2008; 3: 130-7.
68. Newell DW, Shah M, Wilcox R, Hansmann D, Hanley DF. Sonothrombolysis is effective for minimally invasive evacuation of spontaneous Intracerebral hemorrhage. International Stroke Conference (ISC); 2010 25 Feb 2010; Abstract 192.
69. Tachibana K, Tachibana S. Albumin microbubble echo-contrast material as an enhancer or ultrasound accelerated thrombolysis. Circulation. 1995; 92: 1148-50.
70. Porter TR, Xie F, Kricsfeld A, Kilzer K. Noninvasive identification of acute myocardial ischemia and reperfusion with contrast ultrasound using intravenous perfluoropropane-exposed sonicated dextrose albumin. J Am Coll Cardiol. 1995; 26: 33-40.
71. Lou H, Nishioka T, Bar-Cohen Y, Berglund H, Kim CJ, Fishbein MC, et al. Transcutaneous ultrasound, low dose streptokinase and echogen are synergistic for the lysis of in vivo thrombotic occlusion. J Am Coll Cardiol. 1997; 29(Supplement 1): 478A-9A.
72. Wu Y, Unger EC, McCreery TP, Sweitzer RH, Shen D, Wu G, et al. Binding and lysing of blood clots using MRX-408. Invest Radiol. 1998; 33: 880-5.
73. Kondo I, Mizushige K, Ueda T, Masugata H, Ohmori K, Matsuo H. Histological observations and the process of ultrasound contrast agent enhancement of tissue plasminogen activator thrombolysis with ultrasound exposure. Jpn Circ J. 1999; 63: 478-84.
74. Mizushige K, Kondo I, Ohmori K, Hirao K, Matsuo H. Enhancement of ultrasound-accelerated thrombolysis by echo contrast agents: dependence on microbubble structure. Ultrasound Med Biol. 1999; 25: 1431-7.
75. Cintas P, Nguyen F, Boneu B, Larrue V. Enhancement of enzymatic fibrinolysis with 2-MHz ultrasound and microbubbles. J Thromb Haemost. 2004; 2: 1163-6.
76. Nishioka T, Luo H, Fishbein MC, Cercek B, Forrester JS, Kim CJ, et al. Dissolution of thrombotic arterial occlusion by high intensity, low frequency ultrasound and dodecafluoropentane emulsion: an in vitro and in vivo study. J Am Coll Cardiol. 1997; 30: 561-8.
77. Birnbaum Y, Luo H, Nagai T, Fishbein MC, Peterson TM, 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. 1998; 97: 130-4.
78. Culp WC, Porter TR, Lowery J, Xie F, Roberson PK, Marky L. Intracranial clot lysis with intravenous microbubbles and transcranial ultrasound in swine. Stroke. 2004; 35: 2407-11.
79. 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: 307-13.
80. Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol. 2004; 30: 979-89.
81. Meairs S, Alonso A. Ultrasound, microbubbles and the blood brain barrier. Prog Biophys Mol Biol. 2007; 93: 354-62.
82. 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 patients treated with intravenous tissue plasminogen activator. Stroke. 2006; 37: 425-9.
83. Rubiera M, Ribo M, Delgado-Mederos R, Santamarina E, Maisterra O, Delgado P, et al. Do bubble characteristics affect recanalization in stroke patients treated with microbubble-enhanced sonothrombolysis? Ultrasound Med Biol. 2008; 34: 1573-7.
84. Dinia L, Rubiera M, Ribo M, Maisterra O, Ortega G, del Sette M, et al. Reperfusion after stroke sonothrombolysis with microbubbles may predict intracranial bleeding. Neurology. 2009; 73: 775-80.
85. Alexandrov AV, Mikulik R, Ribo M, Sharma VK, Lao AY, Tsivgoulis G, et al. A pilot randomized clinical safety study of sonothrombolysis augmentation with ultrasound-activated perflutren-lipid microspheres for acute ischemic stroke. Stroke. 2008; 39: 1464-9.
86. Perren F, Loulidi J, Poglia D, Landis T, Sztajzel R. Microbubble potentiated transcranial duplex ultrasound enhances IV thrombolysis in acute stroke. J Thromb Thrombolysis. 2008; 25: 219-23.
87. 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.
88. Prokop AF, Soltani A, Roy RA. Cavitational mechanisms in ultrasound-accelerated fibrinolysis. Ultrasound Med Biol. 2007; 33: 942-33.
89. Hajri Z, Boukadoum M, Hamam H, Fontaine R. An investigation of the physical forces leading to thrombosis disruption by cavitation. J Thromb Thrombolysis. 2005; 20: 27-32.