Ultrasound-assisted intravascular therapy: history and future perspectives of development. A review

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Abstract

The first use of ultrasound in treating vascular disorders dates back to 1976. Since then, numerous original studies have been published, offering various concepts of its use. Many technical solutions have been developed and used with variable success, some of which have been developed in modern medicine. This article discusses the development of ultrasound therapeutic technologies in treating vascular disorders. The history of methods is described, available data on promising future areas are presented, and information on existing methods and devices is given.

About the authors

Anton I. Analeev

Sechenov First Moscow State Medical University (Sechenov University)

Email: semitko_s_p@staff.sechenov.ru
ORCID iD: 0000-0002-8500-5569

Res. Assist.

Russian Federation, Moscow

Sergey P. Semitko

Sechenov First Moscow State Medical University (Sechenov University)

Author for correspondence.
Email: semitko_s_p@staff.sechenov.ru
ORCID iD: 0000-0002-1268-5145

D. Sci. (Med.)

Russian Federation, Moscow

Irina E. Chernysheva

Sechenov First Moscow State Medical University (Sechenov University)

Email: chernysheva_i_e@staff.sechenov.ru
ORCID iD: 0000-0002-9707-0691

Cand. Sci. (Med.)

Russian Federation, Moscow

Nikita V. Belikov

Sechenov First Moscow State Medical University (Sechenov University)

Email: belikov_n_v@staff.sechenov.ru
ORCID iD: 0000-0001-6564-6441

Cand. Sci. (Techn.)

Russian Federation, Moscow

Irina V. Khaydukova

Sechenov First Moscow State Medical University (Sechenov University)

Email: khaydukova_i_v@staff.sechenov.ru
ORCID iD: 0000-0003-4591-5506

Cand. Sci. (Techn.)

Russian Federation, Moscow

Anna S. Borde

Sechenov First Moscow State Medical University (Sechenov University)

Email: borde_a_s@staff.sechenov.ru
ORCID iD: 0000-0001-8359-1819

Cand. Sci. (Techn.)

Russian Federation, Moscow

David G. Ioseliani

Sechenov First Moscow State Medical University (Sechenov University)

Email: davidgi@mail.ru
ORCID iD: 0000-0001-6425-7428

D. Sci. (Med.), Prof., Acad. RAS

Russian Federation, Moscow

Peter S. Timashev

Sechenov First Moscow State Medical University (Sechenov University)

Email: timashev_p_s@staff.sechenov.ru
ORCID iD: 0000-0001-7773-2435

D. Sci. (Chem.), Prof.

Russian Federation, Moscow

Victor V. Fomin

Sechenov First Moscow State Medical University (Sechenov University)

Email: fomin_v_v_1@staff.sechenov.ru
ORCID iD: 0000-0002-2682-4417

D. Sci. (Med.), Prof., Corr. Memb. RAS

Russian Federation, Moscow

References

  1. Manbachi A, Cobbold RS. Development and application of piezoelectric materials for ultrasound generation and detection. Ultrasound. 2011;19(4):187-96. doi: 10.1258/ult.2011.011027
  2. Zimmerman D. Paul Langevin and the discovery of active sonar or asdic. The Northern Mariner. 2002;12(1):39-52. doi: 10.25071/2561-546572
  3. Соколов С.Я. Ультраакустические колебания и их применение. Заводская лаборатория. 1935;(5):527-38 [Sokolov SIa. Ul'traakusticheskie kolebaniia i ikh primenenie. Zavodskaia Laboratoriia. 1935;(5):527-38 (in Russian)].
  4. Kaproth-Joslin KA, Nicola R, Dogra VS. The History of US: From Bats and Boats to the Bedside and Beyond: RSNA Centennial Article. Radiographics. 2015;35(3):960-70. doi: 10.1148/rg.2015140300
  5. Stouffer JR. History of ultrasound in animal science. J Ultrasound Med. 2004;23(5):577-84. doi: 10.7863/jum.2004.23.5.577
  6. Siegel RJ, Luo H. Ultrasound thrombolysis. Ultrasonics. 2008;48(4):312-20. doi: 10.1016/j.ultras.2008.03.010
  7. Payne MM. Charles Theodore Dotter. The father of intervention. Tex Heart Inst J. 2001;28(1):28-38.
  8. Кесов П.Г., Рейтблат О.М., Сафиуллина З.М., Шалаев С.В. Эволюция тромболитической терапии в лечении инфаркта миокарда. Рациональная фармакотерапия в кардиологии. 2014;10(5):554-8 [Kesov PG, Reytblat OM, Safiullina ZM, Shalaev SV. Evolution of thrombolytic therapy in the treatment of myocardial infarction. Ration Pharmacother Cardio. 2014;10(5):554-8 (in Russian)].
  9. Olsson SB, Johansson B, Nilsson AM, et al. Enhancement of thrombolysis by ultrasound. Ultrasound Med Biol. 1994;20(4):375-82. doi: 10.1016/0301-5629(94)90006-x
  10. Harpaz D, Chen X, Francis CW, et al. Ultrasound enhancement of thrombolysis and reperfusion in vitro. J Am Coll Cardiol. 1993;21(6):1507-11. doi: 10.1016/0735-1097(93)90331-t
  11. Ariani M, Fishbein MC, Chae JS, et al. Dissolution of peripheral arterial thrombi by ultrasound. Circulation. 1991;84(4):1680-8. doi: 10.1161/01.cir.84.4.1680
  12. Rosenschein U, Bernstein JJ, DiSegni E, et al. Experimental ultrasonic angioplasty: disruption of atherosclerotic plaques and thrombi in vitro and arterial recanalization in vivo. J Am Coll Cardiol. 1990;15(3):711-7. doi: 10.1016/0735-1097(90)90651-5
  13. Hamm CW, Steffen W, Terres W, et al. Intravascular therapeutic ultrasound thrombolysis in acute myocardial infarctions. Am J Cardiol. 1997;80(2):200-4. doi: 10.1016/s0002-9149(97)00318-4
  14. Rosenschein U, Roth A, Rassin T, et al. Analysis of coronary ultrasound thrombolysis endpoints in acute myocardial infarction (ACUTE trial). Results of the feasibility phase. Circulation. 1997;95(6):1411-6. doi: 10.1161/01.cir.95.6.1411
  15. Luo H, Steffen W, Cercek B, et al. Enhancement of thrombolysis by external ultrasound. Am Heart J. 1993;125(6):1564-9. doi: 10.1016/0002-8703(93)90741-q
  16. Luo H, Nishioka T, Berglund H, et al. Effect of External Ultrasound Frequency on Thrombus Disruption in Vitro. J Thromb Thrombolysis. 1996;3(1):63-6. doi: 10.1007/BF00226413
  17. Luo H, Nishioka T, Fishbein MC, et al. Transcutaneous ultrasound augments lysis of arterial thrombi in vivo. Circulation. 1996;94(4):775-8. doi: 10.1161/01.cir.94.4.775
  18. Alexandrov AV, Demchuk AM, Felberg RA, 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(3):610-4. doi: 10.1161/01.str.31.3.610
  19. Eggers J, Koch B, Meyer K, et al. Effect of ultrasound on thrombolysis of middle cerebral artery occlusion. Ann Neurol. 2003;53(6):797-800. doi: 10.1002/ana.10590
  20. Tsivgoulis G, Alexandrov AV. Ultrasound-enhanced thrombolysis in acute ischemic stroke: potential, failures, and safety. Neurotherapeutics. 2007;4(3):420-7. doi: 10.1016/j.nurt.2007.05.012
  21. Hoksbergen AW, Legemate DA, Ubbink DT, Jacobs MJ. Success rate of transcranial color-coded duplex ultrasonography in visualizing the basal cerebral arteries in vascular patients over 60 years of age. Stroke. 1999;30(7):1450-5. doi: 10.1161/01.str.30.7.1450
  22. Barreto AD, Alexandrov AV, Shen L, et al. CLOTBUST-Hands Free: pilot safety study of a novel operator-independent ultrasound device in patients with acute ischemic stroke. Stroke. 2013;44(12):3376-81. doi: 10.1161/STROKEAHA.113.002713
  23. Molina CA, Barreto AD, Tsivgoulis G, et al. Transcranial ultrasound in clinical sonothrombolysis (TUCSON) trial. Ann Neurol. 2009;66(1):28-38. doi: 10.1002/ana.21723
  24. 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. 2005;36(7):1441-6. doi: 10.1161/01.STR.0000170707.86793.1a
  25. Cohen MG, Tuero E, Bluguermann J, et al. Transcutaneous ultrasound-facilitated coronary thrombolysis during acute myocardial infarction. Am J Cardiol. 2003;92(4):454-7. doi: 10.1016/s0002-9149(03)00666-0
  26. Hudson M, Greenbaum A, Brenton L, et al. Adjunctive transcutaneous ultrasound with thrombolysis: results of the PLUS (Perfusion by ThromboLytic and UltraSound) trial. JACC Cardiovasc Interv. 2010;3(3):352-9. doi: 10.1016/j.jcin.2009.11.020
  27. Goel L, Jiang X. Advances in Sonothrombolysis Techniques Using Piezoelectric Transducers. Sensors (Basel). 2020;20(5):1288. doi: 10.3390/s20051288
  28. Frenkel V, Oberoi J, Stone MJ, et al. Pulsed high-intensity focused ultrasound enhances thrombolysis in an in vitro model. Radiology. 2006;239(1):86-93. doi: 10.1148/radiol.2391042181
  29. Francis CW, Blinc A, Lee S, Cox C. Ultrasound accelerates transport of recombinant tissue plasminogen activator into clots. Ultrasound Med Biol. 1995;21(3):419-24. doi: 10.1016/0301-5629(94)00119-x
  30. 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(4):333-40. doi: 10.1016/s0049-3848(00)00319-4
  31. Riesz P, Kondo T. Free radical formation induced by ultrasound and its biological implications. Free Radic Biol Med. 1992;13(3):247-70. doi: 10.1016/0891-5849(92)90021-8
  32. Brujan EA, Ikeda T, Matsumoto Y. Jet formation and shock wave emission during collapse of ultrasound-induced cavitation bubbles and their role in the therapeutic applications of high-intensity focused ultrasound. Phys Med Biol. 2005;50(20):4797-809. doi: 10.1088/0031-9155/50/20/004
  33. Weiss HL, Selvaraj P, Okita K, et al. Mechanical clot damage from cavitation during sonothrombolysis. J Acoust Soc Am. 2013;133(5):3159-75. doi: 10.1121/1.4795774
  34. Chuang YH, Cheng PW, Chen SC, et al. Effects of ultrasound-induced inertial cavitation on enzymatic thrombolysis. Ultrason Imaging. 2010;32(2):81-90. doi: 10.1177/016173461003200202
  35. Wu J, Xie F, Kumar T, et al. Improved sonothrombolysis from a modified diagnostic transducer delivering impulses containing a longer pulse duration. Ultrasound Med Biol. 2014;40(7):1545-53. doi: 10.1016/j.ultrasmedbio.2014.01.015
  36. Bader KB, Holland CK. Gauging the likelihood of stable cavitation from ultrasound contrast agents. Phys Med Biol. 2013;58(1):127-44. doi: 10.1088/0031-9155/58/1/127
  37. Porter TR, Xie F, Li S, et al. Increased ultrasound contrast and decreased microbubble destruction rates with triggered ultrasound imaging. J Am Soc Echocardiogr. 1996;9(5):599-605. doi: 10.1016/s0894-7317(96)90054-1
  38. Nishioka T, Luo H, Fishbein MC, 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(2):561-8. doi: 10.1016/s0735-1097(97)00182-4
  39. 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. 2008;39(5):1464-9. doi: 10.1161/STROKEAHA.107.505727
  40. Shaw GJ, Meunier JM, Huang SL, et al. Ultrasound-enhanced thrombolysis with tPA-loaded echogenic liposomes. Thromb Res. 2009;124(3):306-10. doi: 10.1016/j.thromres.2009.01.008
  41. Laing ST, Moody M, Smulevitz B, et al. Ultrasound-enhanced thrombolytic effect of tissue plasminogen activator-loaded echogenic liposomes in an in vivo rabbit aorta thrombus model – brief report. Arterioscler Thromb Vasc Biol. 2011;31(6):1357-9. doi: 10.1161/ATVBAHA.111.225938
  42. Wang X, Gkanatsas Y, Palasubramaniam J, et al. Thrombus-Targeted Theranostic Microbubbles: A New Technology towards Concurrent Rapid Ultrasound Diagnosis and Bleeding-free Fibrinolytic Treatment of Thrombosis. Theranostics. 2016;6(5):726-38. doi: 10.7150/thno.14514
  43. Hua X, Liu P, Gao YH, et al. Construction of thrombus-targeted microbubbles carrying tissue plasminogen activator and their in vitro thrombolysis efficacy: a primary research. J Thromb Thrombolysis. 2010;30(1):29-35. doi: 10.1007/s11239-010-0450-z
  44. Hua X, Zhou L, Liu P, et al. In vivo thrombolysis with targeted microbubbles loading tissue plasminogen activator in a rabbit femoral artery thrombus model. J Thromb Thrombolysis. 2014;38(1):57-64. doi: 10.1007/s11239-014-1071-8
  45. Zhu Y, Guan L, Mu Y. Combined Low-Frequency Ultrasound and Urokinase-Containing Microbubbles in Treatment of Femoral Artery Thrombosis in a Rabbit Model. PLoS One. 2016;11(12):e0168909. doi: 10.1371/journal.pone.0168909
  46. Zhu X, Guo J, He C, et al. Ultrasound triggered image-guided drug delivery to inhibit vascular reconstruction via paclitaxel-loaded microbubbles. Sci Rep. 2016;6:21683. doi: 10.1038/srep21683
  47. De Saint Victor M, Carugo D, Barnsley LC, et al. Magnetic targeting to enhance microbubble delivery in an occluded microarterial bifurcation. Phys Med Biol. 2017;62(18):7451-70. doi: 10.1088/1361-6560/aa858f
  48. Pajek D, Burgess A, Huang Y, Hynynen K. High-intensity focused ultrasound sonothrombolysis: the use of perfluorocarbon droplets to achieve clot lysis at reduced acoustic power. Ultrasound Med Biol. 2014;40(9):2151-61. doi: 10.1016/j.ultrasmedbio.2014.03.026
  49. Guo S, Guo X, Wang X, et al. Reduced clot debris size in sonothrombolysis assisted with phase-change nanodroplets. Ultrason Sonochem. 2019;54:183-91. doi: 10.1016/j.ultsonch.2019.02.001
  50. Aguiar MOD, Tavares BG, Tsutsui JM, et al. Sonothrombolysis Improves Myocardial Dynamics and Microvascular Obstruction Preventing Left Ventricular Remodeling in Patients With ST Elevation Myocardial Infarction. Circ Cardiovasc Imaging. 2020;13(4):e009536. doi: 10.1161/CIRCIMAGING.119.009536
  51. Chiang HP, Aguiar MOD, Tavares BG, et al. The Impact of Sonothrombolysis on Left Ventricular Diastolic Function and Left Atrial Mechanics Preventing Left Atrial Remodeling in Patients With ST Elevation Acute Myocardial Infarction. J Am Soc Echocardiogr. 2023;36(5):504-13. doi: 10.1016/j.echo.2022.12.010
  52. Owens CA. Ultrasound-Enhanced Thrombolysis: EKOS EndoWave Infusion Catheter System. Semin Intervent Radiol. 2008;25(1):37-41. doi: 10.1055/s-2008-1052304
  53. Wissgott C, Richter A, Kamusella P, Steinkamp HJ. Treatment of critical limb ischemia using ultrasound-enhanced thrombolysis (PARES Trial): final results. J Endovasc Ther. 2007;14(4):438-43. doi: 10.1177/152660280701400402
  54. Ouriel K, Veith FJ, Sasahara AA. A comparison of recombinant urokinase with vascular surgery as initial treatment for acute arterial occlusion of the legs. Thrombolysis or Peripheral Arterial Surgery (TOPAS) Investigators. N Engl J Med. 1998;338(16):1105-11. doi: 10.1056/NEJM199804163381603
  55. Kucher N, Boekstegers P, Müller OJ, et al. Randomized, controlled trial of ultrasound-assisted catheter-directed thrombolysis for acute intermediate-risk pulmonary embolism. Circulation. 2014;129(4):479-86. doi: 10.1161/CIRCULATIONAHA.113.005544
  56. Piazza G, Hohlfelder B, Jaff MR, et al; SEATTLE II Investigators. A Prospective, Single-Arm, Multicenter Trial of Ultrasound-Facilitated, Catheter-Directed, Low-Dose Fibrinolysis for Acute Massive and Submassive Pulmonary Embolism: The SEATTLE II Study. JACC Cardiovasc Interv. 2015;8(10):1382-92. doi: 10.1016/j.jcin.2015.04.020
  57. Tapson VF, Sterling K, Jones N, et al. A Randomized Trial of the Optimum Duration of Acoustic Pulse Thrombolysis Procedure in Acute Intermediate-Risk Pulmonary Embolism: The OPTALYSE PE Trial. JACC Cardiovasc Interv. 2018;11(14):1401-10. doi: 10.1016/j.jcin.2018.04.008
  58. Goldhaber S, Konstantinides SV, Meneveau N, et al. International EkoSonic Registry of the Treatment and Clinical Outcomes of Patients with Pulmonary Embolism Prospective Cohort 3-month Data Release. Available at: https://www.bostonscientific.com/content/dam/bostonscientific/pi/portfolio-group/vascular-surgery/ekos/campaign/clinical-evidence/ekos-knocout-data-summary.pdf.coredownload.pdf. Accessed: 12.09.2023
  59. Klok FA, Piazza G, Sharp ASP, et al. Ultrasound-facilitated, catheter-directed thrombolysis vs anticoagulation alone for acute intermediate-high-risk pulmonary embolism: Rationale and design of the HI-PEITHO study. Am Heart J. 2022;251:43-53. doi: 10.1016/j.ahj.2022.05.011
  60. Bock J. Treating pulmonary embolism with EKOSTM Endovascular System: A clinician’s perpective. Digital Insert Endovascular Today. 2023;22(9):1-3.
  61. Forero MNT, Daemen J. The Coronary Intravascular Lithotripsy System. Interv Cardiol. 2019;14(3):174-81. doi: 10.15420/icr.2019.18.R1
  62. Wilson SJ, Spratt JC, Hill J, et al. Incidence of „shocktopics“ and asynchronous cardiac pacing in patients undergoing coronary intravascular lithotripsy. EuroIntervention. 2020;15(16):1429-35. doi: 10.4244/EIJ-D-19-00484
  63. Messas E, IJsselmuiden A, Goudot G, et al. Feasibility and Performance of Noninvasive Ultrasound Therapy in Patients With Severe Symptomatic Aortic Valve Stenosis: A First-in-Human Study. Circulation. 2021;143(9):968-70. doi: 10.1161/CIRCULATIONAHA.120.050672
  64. Messas E, Ijsselmuiden A, Trifunović-Zamaklar D, et al. Treatment of severe symptomatic aortic valve stenosis using non-invasive ultrasound therapy: A cohort study. Lancet. 2023;402(10419):2317-25. doi: 10.1016/S0140-6736(23)01518-0

Supplementary files

Supplementary Files
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1. JATS XML
2. Fig. 1. The first model of the EKOS catheter - EKOS EndoWave. Given with permission of C. Owens [52].

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3. Fig. 2. EKOS+ catheter (image from the device manufacturer, Boston Scientific).

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4. Fig. 3. Shockwave device (image from the manufacturer of the Shockwave Medical device).

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