Modelling the dynamics of microbubble undergoing stable and inertial cavitation: Delineating the effects of ultrasound and microbubble parameters on sonothrombolysis

• Autorzy: Tan Zhi Qi , Ooi Ean Hin , Chiew Yeong Shiong , Foo Ji Jinn , Ng Yin Kwee , Ooi Ean Tat

Identyfikatory

DOI

10.1016/j.bbe.2024.04.003

• Języki publikacji: EN

Abstrakty

EN

Sonothrombolysis induces clot breakdown using ultrasound waves to excite microbubbles. Despite the great potential, selecting optimal ultrasound (frequency and pressure) and microbubble (radius) parameters remains a challenge. To address this, a computational model was developed to investigate the bubble behaviour during sonothrombolysis. The blood and clot were assumed to be non-Newtonian and porous, respectively. The effects of ultrasound and microbubble parameters on flow-induced shear stress on the clot surface during stable and inertial cavitation were investigated. It was found that microbubble translation towards the clot and the shear stress on the clot surface during stable cavitation were significant when the bubble was about to undergo inertial cavitation. While insonation of large microbubble (radius of 1.65 μm) at low frequency (0.50 MHz) produced the highest shear stress during stable cavitation, selection of these parameters is not as intuitive for inertial cavitation due to the strong competing effect between jet velocity and translational distance. An increase in jet velocity is always accompanied by a decrease in the translational distance and vice versa. Therefore, a right balance between the jet velocity and the translational distance is critical to maximise the shear stress on the clot surface. A jet velocity of 303 m/s and a distance travelled of 5.12 μm at an initial bubble-clot separation of 10 μm produced the greatest clot surface shear stress. This is achievable by insonating a 0.55 μm microbubble using 0.50 MHz and 600 kPa ultrasound.

Słowa kluczowe

EN

acoustic wave; inertial cavitation; jet velocity; thrombolysis; shear stress

PL

fala akustyczna; kawitacja akustyczna; prędkość strumienia; naprężenie ścinające

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2024
• Tom: Vol. 44, no. 2
• Strony: 358--368
• Opis fizyczny: Bibliogr. 44 poz., rys., tab., wykr.

Twórcy

autor

Tan Zhi Qi

• Department of Mechanical Engineering, School of Engineering, Monash University Malaysia, Jalan Lagoon Selatan, 47500 Bandar Sunway, Selangor, Malaysia

autor

Ooi Ean Hin

• Department of Mechanical Engineering, School of Engineering, Monash University Malaysia, Jalan Lagoon Selatan, 47500 Bandar Sunway, Selangor, Malaysia

autor

Chiew Yeong Shiong

• Department of Mechanical Engineering, School of Engineering, Monash University Malaysia, Jalan Lagoon Selatan, 47500 Bandar Sunway, Selangor, Malaysia

autor

Foo Ji Jinn

• Department of Mechanical Engineering, School of Engineering, Monash University Malaysia, Jalan Lagoon Selatan, 47500 Bandar Sunway, Selangor, Malaysia

autor

Ng Yin Kwee

• School of Mechanical and Aerospace Engineering, College of Engineering, Nanyang Technological University, 50 Nanyang Avenue 639798, Singapore

autor

Ooi Ean Tat

• School of Engineering and Information Technology, Faculty of Science and Technology, Federation University, VIC 3350, Australia

Bibliografia

• [1] Xu S, Zong Y, Feng Y, Liu R, Liu X, Hu Y, et al. Dependence of pulsed focused ultrasound induced thrombolysis on duty cycle and cavitation bubble size distribution. Ultrason Sonochemistry 2015;22:160-6.
• [2] Goel L, Jiang X. Advances in sonothrombolysis techniques using piezoelectric transducers. Sensors 2020;20:1288.
• [3] Guo S, Du X, Wang X, Lu S, Shi A, Xu S, et al. Reduced clot debris size using standing waves formed via high intensity focused ultrasound. Appl Phys Lett 2017;111:123701.
• [4] Wu J, Xie F, Kumar T, Liu J, Lof J, Shi W, et al. Improved sonothrombolysis from a modified diagnostic transducer delivering impulses containing a longer pulse duration. Ultrasound Med Biol 2014;40:1545-53.
• [5] Xie F, Lof J, Everbach C, He A, Bennett RM, Matsunaga T, et al. Treatment of acute intravascular thrombi with diagnostic ultrasound and intravenous microbubbles. J Am Coll Cardiol Cardiovasc Imaging 2009;2:511-8.
• [6] Goel L, Wu H, Kim H, Zhang B, Kim J, Dayton PA, et al. Examining the influence of low-dose tissue plasminogen activator on microbubble-mediated forward-viewing intravascular sonothrombolysis. Ultrasound Med Biol 2020;46:1698-706.
• [7] Kim H, Kim J, Wu H, Zhang B, Dayton PA, Jiang X. A multi-pillar piezoelectric stack transducer for nanodroplet mediated intravascular sonothrombolysis. Ultrasonics 2021;116:106520.
• [8] Bader KB, Bouchoux G, Holland CK. Sonothrombolysis. Therapeutic Ultrasound 2016;880:339-62.
• [9] Weiss HL, Selvaraj P, Okita K, Matsumoto Y, Voie A, Hoelscher T, et al. Mechanical clot damage from cavitation during sonothrombolysis. J Acoust Soc Am 2013;133:3159-75.
• [10] Chen X, Leeman JE, Wang J, Pacella JJ, Villanueva FS. New insights into mechanisms of sonothrombolysis using ultra-high-speed imaging. Ultrasound Med Biol 2014;40:258-62.
• [11] Datta S, Coussios C, Ammi AY, Mast TD, de Courten-Myers GM, HollandK CK. Ultrasound-enhanced thrombolysis using definity® as a cavitation nucleation agent. Ultrasound Med Biol 2008;34:1421-33.
• [12] Kim J, Lindsey BD, Chang WY, Dai X, Stavas JM, Dayton PA, et al. Intravascular forward-looking ultrasound transducers for microbubble-mediated sonothrombolysis. Sci Rep 2017;7:1-10.
• [13] Borrelli MJ, O’Brien Jr WD, Hamilton E, Oelze ML, Wu J, Bernock LJ, et al. Influences of microbubble diameter and ultrasonic parameters on in vitro sonothrombolysis efficacy. J Vascular Intervent Radiol 2012;23:1677-84.
• [14] Zhang B, Wu H, Kim H, Welch PJ, Cornett A, Stocker G, et al. A model of high-speed endovascular sonothrombolysis with vortex ultrasound-induced shear stress to treat cerebral venous sinus thrombosis. Research 2023;6:0048.
• [15] Goel L, Wu H, Zhang B, Kim J, Dayton PA, Xu Z, et al. Safety evaluation of a forward-viewing intravascular transducer for sonothrombolysis: an in vitro and ex vivo study. Ultrasound Med Biol 2021;47:3231-9.
• [16] Petit B, Yan F, Tranquart F, Allémann E. Microbubbles and ultrasound-mediated thrombolysis: a review of recent in vitro studies. J Drug Deliv Sci Technol 2012;22:381-92.
• [17] Xie Y, Hu J, Lei W, Qian S. Prediction of vascular injury by cavitation microbubbles in a focused ultrasound field. Ultrason Sonochemistry 2022;88:106103.
• [18] Zeng Q, An H, Ohl CD. Wall shear stress from jetting cavitation bubbles: Influence of the stand-off distance and liquid viscosity. J Fluid Mech 2022;932:A14.
• [19] Wang S, Zhang A, Liu Y, Zeng D. Numerical simulation of bubble dynamics in an elastic vessel. Eur Phys J E 2013;36:119.
• [20] Hosseinkhah N, Goertz DE, Hynynen K. Microbubbles and blood-brain barrier opening: a numerical study on acoustic emissions and wall stress predictions. IEEE Trans Biomed Eng 2014;62:1293-304.
• [21] Khodabakhshi Z, Hosseinkhah N, Ghadiri H. Pulsating microbubble in a microvessel and mechanical effect on vessel wall: a simulation study. J Biomed Phys Eng 2021;11:629-40.
• [22] Hosseinkhah N, Chen H, Matula TJ, Burns PN, Hynynen K. Mechanisms of microbubble-vessel interactions and induced stresses: A numerical study. J Acoust Soc Am 2013;134:1875-85.
• [23] Gümmer J, Schenke S, Denner F. Modelling lipid-coated microbubbles in focused ultrasound applications at subresonance frequencies. Ultrasound Med Biol 2021;47:2958-79.
• [24] Qin D, Zou Q, Lei S, Wang W, Li Z. Cavitation dynamics and inertial cavitation threshold of lipid coated microbubbles in viscoelastic media with bubble–bubble interactions. Micromachines 2021;12:1125.
• [25] Mobadersany N, Sarkar K. The dynamic of contrast agent and surrounding fluid in the vicinity of a wall for sonoporation. In: Katz J, editor. 10th international symposium on cavitation - CAV2018. Baltimore, Maryland, USA: ASME Press; 2018, p. 257-62.
• [26] Mobadersany N, Sarkar K. The dynamic of contrast agent and surrounding fluid in the vicinity of a wall for sonoporation. 2018, arXiv preprint arXiv:1802.08652.
• [27] Acconcia C, Leung BYC, Hynynen K, Goertz DE. Interactions between ultrasound stimulated microbubbles and fibrin clots. Appl Phys Lett 2013;103:053701.
• [28] Treeby BE, Zhang EZ, Thomas AS, Cox BT. Measurement of the ultrasound attenuation and dispersion in whole human blood and its components from 0-70 MHz. Ultrasound Med Biol 2011;37:289-300.
• [29] Husain I, Labropulu F, Langdon C, Schwark J. A comparison of Newtonian and non-Newtonian models for pulsatile blood flow simulations. J Mech Behav Mater 2013;21:147-53.
• [30] Xu S, Xu Z, Kim OV, Litvinov RI, Weisel JW, Alber M. Model predictions of deformation, embolization and permeability of partially obstructive blood clots under variable shear flow. J R Soc Interface 2017;14:20170441.
• [31] Nield DA, Bejan A. Convection in porous media, vol. 3, New York: Springer; 2006.
• [32] Marmottant P, Van Der Meer S, Emmer M, Versluis M, De Jong N, Hilgenfeldt S, et al. A model for large amplitude oscillations of coated bubbles accounting for buckling and rupture. J Acoust Soc Am 2005;118:3499-505.
• [33] Yadav SS, Sikarwar BS, Ranjan P, Janardhanan R, Goyal A. Surface tension measurement of normal human blood samples by pendant drop method. J Med Eng Technol 2020;44:227-36.
• [34] Brujan EA. Jets from pulsed-ultrasound-induced cavitation bubbles near a rigid boundary. J Phys D: Appl Phys 2017;50:215302.
• [35] Paul S, Katiyar A, Sarkar K, Chatterjee D, Shi WT, Forsberg F. Material characterization of the encapsulation of an ultrasound contrast microbubble and its subharmonic response: Strain-softening interfacial elasticity model. J Acoust Soc Am 2010;127:3846-57.
• [36] Goel L, Wu H, Zhang B, Kim J, Dayton PA, Xu Z, et al. Nanodroplet-mediated catheter-directed sonothrombolysis of retracted blood clots. Microsyst Nanoeng 2021;7:1-7.
• [37] Tan ZQ, Ooi EH, Chiew YS, Foo JJ, Ng EYK, Ooi ET. A computational framework for the multiphysics simulation of microbubble-mediated sonothrombolysis using a forward-viewing intravascular transducer. Ultrasonics 2023;131:106961.
• [38] Wang X, Chen W, Zhou M, Zhang Z, Zhang L. Dynamics of double bubbles under the driving of burst ultrasound. Ultrason Sonochemistry 2022;84:105952.
• [39] Huang X, Wang QX, Zhang AM, Su J. Dynamic behaviour of a two-microbubble system under ultrasonic wave excitation. Ultrason Sonochemistry 2018;43:166-74.
• [40] Wang QX, Manmi K. Three dimensional microbubble dynamics near a wall subject to high intensity ultrasound. Phys Fluids 2014;26:032104.
• [41] Schmitt C, Henni AH, Cloutier G. Characterization of blood clot viscoelasticity by dynamic ultrasound elastography and modeling of the rheological behavior. J Biomech 2011;44:622-9.
• [42] Johnson S, Duffy S, Gunning G, Gilvarry M, McGarry JP, McHugh PE. Review of mechanical testing and modelling of thrombus material for vascular implant and device design. Ann Biomed Eng 2017;45:2494-508.
• [43] Sugerman GP, Kakaletsis S, Thakkar P, Chokshi A, Parekh SH, Rausch MK. A whole blood thrombus mimic: constitutive behavior under simple shear. J Mech Behav Biomed Mater 2021;115:104216.
• [44] Li H, Flé G, Bhatt M, Qu Z, Ghazavi S, Yazdani L, et al. Viscoelasticity imaging of biological tissues and single cells using shear wave propagation. Front Phys 2021;9:666192.