Multi-resolution simulation of focused ultrasound propagation through ovine skull from a single-element transducer

Transcranial focused ultrasound (tFUS) is emerging as a non-invasive brain stimulation modality. Complicated interactions between acoustic pressure waves and osseous tissue introduce many challenges in the accurate targeting of an acoustic focus through the cranium. Image-guidance accompanied by a numerical simulation is desired to predict the intracranial acoustic propagation through the skull; however, such simulations typically demand heavy computation, which warrants an expedited processing method to provide on-site feedback for the user in guiding the acoustic focus to a particular brain region. In this paper, we present a multi-resolution simulation method based on the finite-difference time-domain formulation to model the transcranial propagation of acoustic waves from a single-element transducer (250 kHz). The multi-resolution approach improved computational efficiency by providing the flexibility in adjusting the spatial resolution. The simulation was also accelerated by utilizing parallelized computation through the graphic processing unit. To evaluate the accuracy of the method, we measured the actual acoustic fields through ex vivo sheep skulls with different sonication incident angles. The measured acoustic fields were compared to the simulation results in terms of focal location, dimensions, and pressure levels. The computational efficiency of the presented method was also assessed by comparing simulation speeds at various combinations of resolution grid settings. The multi-resolution grids consisting of 0.5 and 1.0 mm resolutions gave acceptable accuracy (under 3 mm in terms of focal position and dimension, less than 5% difference in peak pressure ratio) with a speed compatible with semi real-time user feedback (within 30 s). The proposed multi-resolution approach may serve as a novel tool for simulation-based guidance for tFUS applications.

[1]  Max Wintermark,et al.  A pilot study of focused ultrasound thalamotomy for essential tremor. , 2013, The New England journal of medicine.

[2]  Jing Chen,et al.  Rapid MR‐ARFI method for focal spot localization during focused ultrasound therapy , 2011, Magnetic resonance in medicine.

[3]  M. Tanter,et al.  Low intensity focused ultrasound modulates monkey visuomotor behavior , 2013, Current Biology.

[4]  T. Namiki 3-D ADI-FDTD method-unconditionally stable time-domain algorithm for solving full vector Maxwell's equations , 2000 .

[5]  Kullervo Hynynen,et al.  A numerical study of transcranial focused ultrasound beam propagation at low frequency , 2005, Physics in medicine and biology.

[6]  M. Fink,et al.  Influence of the pressure field distribution in transcranial ultrasonic neurostimulation. , 2013, Medical physics.

[7]  B. Strand,et al.  Solving inverse electromagnetic problems using FDTD and gradient‐based minimization , 2006 .

[8]  K. Bathe Finite Element Procedures , 1995 .

[9]  K. Hynynen,et al.  Transcranial Magnetic Resonance Imaging– Guided Focused Ultrasound Surgery of Brain Tumors: Initial Findings in 3 Patients , 2010, Neurosurgery.

[10]  K. Bathe,et al.  An explicit time integration scheme for the analysis of wave propagations , 2013 .

[11]  S. Yoo,et al.  Focused Ultrasound-mediated Non-invasive Brain Stimulation: Examination of Sonication Parameters , 2014, Brain Stimulation.

[12]  Gábor Székely,et al.  Full-wave acoustic and thermal modeling of transcranial ultrasound propagation and investigation of skull-induced aberration correction techniques: a feasibility study , 2015, Journal of therapeutic ultrasound.

[13]  Natalia Vykhodtseva,et al.  Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery. , 2006, Journal of neurosurgery.

[14]  W. Lauriks,et al.  Ultrasonic wave propagation in human cancellous bone: application of Biot theory. , 2004, The Journal of the Acoustical Society of America.

[15]  Xu Xiao,et al.  An integrated model-based software for FUS in moving abdominal organs , 2015, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[16]  A Hosokawa Simulation of ultrasound propagation through bovine cancellous bone using elastic and Biot's finite-difference time-domain methods. , 2005, The Journal of the Acoustical Society of America.

[17]  Xu Xue,et al.  An Effective Finite Difference Method for Simulation of Bioheat Transfer in Irregular Tissues , 2013 .

[18]  Sungon Lee,et al.  Development of a Wearable Robotic Positioning System for Noninvasive Transcranial Focused Ultrasound Stimulation , 2016, IEEE/ASME Transactions on Mechatronics.

[19]  Allen Taflove,et al.  Computational Electrodynamics the Finite-Difference Time-Domain Method , 1995 .

[20]  Huiling Jiang,et al.  3D FDTD analysis by using non-uniform mesh , 1998, ICMMT'98. 1998 International Conference on Microwave and Millimeter Wave Technology. Proceedings (Cat. No.98EX106).

[21]  Jong-Hwan Lee,et al.  Transcranial focused ultrasound stimulation of human primary visual cortex , 2016, Scientific Reports.

[22]  Kullervo Hynynen,et al.  Uterine leiomyomas: MR imaging-based thermometry and thermal dosimetry during focused ultrasound thermal ablation. , 2006, Radiology.

[23]  Thomas Dreyer,et al.  Full wave modeling of therapeutic ultrasound: efficient time-domain implementation of the frequency power-law attenuation. , 2004, The Journal of the Acoustical Society of America.

[24]  Purang Abolmaesumi,et al.  Point-Based Rigid-Body Registration Using an Unscented Kalman Filter , 2007, IEEE Transactions on Medical Imaging.

[25]  Jong-Hwan Lee,et al.  Focused ultrasound modulates region-specific brain activity , 2011, NeuroImage.

[26]  Jay B. West,et al.  Designing optically tracked instruments for image-guided surgery , 2004, IEEE Transactions on Medical Imaging.

[27]  Yun Jing,et al.  Verification of the westervelt equation for focused transducers , 2011, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[28]  M. Marberger,et al.  High-energy shockwaves and extracorporeal high-intensity focused ultrasound. , 2003, Journal of endourology.

[29]  Richard A. Fournier,et al.  A multi-resolution satellite imagery approach for large area mapping of ericaceous shrubs in Northern Quebec, Canada , 2009, Int. J. Appl. Earth Obs. Geoinformation.

[30]  Charles R. G. Guttmann,et al.  Multiresolution Data Acquisition and Detection in Functional MRI , 2001, NeuroImage.

[31]  B T Cox,et al.  k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields. , 2010, Journal of biomedical optics.

[32]  Ioannis T. Rekanos,et al.  Inverse scattering in the time domain: an iterative method using an FDTD sensitivity analysis scheme , 2002 .

[33]  S. Yoo,et al.  Noninvasive transcranial stimulation of rat abducens nerve by focused ultrasound. , 2012, Ultrasound in medicine & biology.

[34]  Kullervo Hynynen,et al.  Ultrasound for drug and gene delivery to the brain. , 2008, Advanced drug delivery reviews.

[35]  J. Barger,et al.  Acoustical properties of the human skull. , 1978, The Journal of the Acoustical Society of America.

[36]  F Dunn,et al.  Ultrasonic absorption and attenuation in mammalian tissues. , 1979, Ultrasound in medicine & biology.

[37]  Natalia Vykhodtseva,et al.  500‐element ultrasound phased array system for noninvasive focal surgery of the brain: A preliminary rabbit study with ex vivo human skulls , 2004, Magnetic resonance in medicine.

[38]  Mickael Tanter,et al.  Simulation of intracranial acoustic fields in clinical trials of sonothrombolysis. , 2009, Ultrasound in medicine & biology.

[39]  Lei Zhao,et al.  Real-Time Adaptive Functional MRI , 1999, NeuroImage.

[40]  Seung-Schik Yoo,et al.  PET∕CT imaging evidence of FUS-mediated (18)F-FDG uptake changes in rat brain. , 2013, Medical physics.

[41]  S. Yoo,et al.  Suppression of EEG visual-evoked potentials in rats through neuromodulatory focused ultrasound , 2015, Neuroreport.

[42]  Pierre-Olivier Bouchard,et al.  Crack propagation modelling using an advanced remeshing technique , 2000 .

[43]  Mickael Tanter,et al.  Attenuation, scattering, and absorption of ultrasound in the skull bone. , 2011, Medical physics.

[44]  J. A. Evans,et al.  Ultrasonic attenuation and velocity in bone. , 1990, Physics in medicine and biology.

[45]  Wonhye Lee,et al.  Image-Guided Focused Ultrasound-Mediated Regional Brain Stimulation in Sheep. , 2016, Ultrasound in medicine & biology.

[46]  J. Kennedy High-intensity focused ultrasound in the treatment of solid tumours , 2005, Nature Reviews Cancer.

[47]  A. Morel,et al.  High‐intensity focused ultrasound for noninvasive functional neurosurgery , 2009, Annals of neurology.

[48]  Win-Li Lin,et al.  Feasibility of transrib focused ultrasound thermal ablation for liver tumors using a spherically curved 2D array: a numerical study. , 2007, Medical physics.

[49]  Vincent P. Ferrera,et al.  Long-Term Safety of Repeated Blood-Brain Barrier Opening via Focused Ultrasound with Microbubbles in Non-Human Primates Performing a Cognitive Task , 2015, PloS one.

[50]  Wonhye Lee,et al.  Focused ultrasound brain stimulation to anesthetized rats induces long‐term changes in somatosensory evoked potentials , 2018, Int. J. Imaging Syst. Technol..

[51]  T Deffieux,et al.  Numerical study of a simple transcranial focused ultrasound system applied to blood-brain barrier opening , 2010, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[52]  Bradley E. Treeby,et al.  Simulating Focused Ultrasound Transducers Using Discrete Sources on Regular Cartesian Grids , 2016, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[53]  Mathieu Pernot,et al.  Targeting accuracy of transcranial magnetic resonance-guided high-intensity focused ultrasound brain therapy: a fresh cadaver model. , 2013, Journal of neurosurgery.

[54]  Yao-Sheng Tung,et al.  Contrast-agent-enhanced ultrasound thermal ablation. , 2006, Ultrasound in medicine & biology.

[55]  A. Williams,et al.  Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans , 2014, Nature Neuroscience.

[56]  Gregory T. Clement,et al.  Longitudinal and shear mode ultrasound propagation in human skull bone. , 2006, Ultrasound in medicine & biology.

[57]  Shinsuk Park,et al.  Estimation of the spatial profile of neuromodulation and the temporal latency in motor responses induced by focused ultrasound brain stimulation , 2013, Neuroreport.

[58]  Yiqiang Yu,et al.  A 3-D Radial Point Interpolation Method for Meshless Time-Domain Modeling , 2009, IEEE Transactions on Microwave Theory and Techniques.

[59]  Kullervo Hynynen,et al.  MRI evaluation of thermal ablation of tumors with focused ultrasound , 1998, Journal of magnetic resonance imaging : JMRI.

[60]  Laehyun Kim,et al.  Non-invasive transmission of sensorimotor information in humans using an EEG/focused ultrasound brain-to-brain interface , 2017, PloS one.

[61]  Aki Pulkkinen,et al.  Numerical simulations of clinical focused ultrasound functional neurosurgery , 2014, Physics in medicine and biology.

[62]  P. J. Westervelt,et al.  Scattering of Sound by Sound , 1957 .

[63]  Ben Cox,et al.  Sensitivity of simulated transcranial ultrasound fields to acoustic medium property maps , 2017, Physics in medicine and biology.

[64]  Guirong Liu,et al.  Smoothed Particle Hydrodynamics: A Meshfree Particle Method , 2003 .

[65]  André Stumpf,et al.  Hierarchical extraction of landslides from multiresolution remotely sensed optical images , 2014 .

[66]  K Hynynen,et al.  A focused ultrasound method for simultaneous diagnostic and therapeutic applications--a simulation study. , 2001, Physics in medicine and biology.

[67]  M Tanter,et al.  Experimental demonstration of noninvasive transskull adaptive focusing based on prior computed tomography scans. , 2003, The Journal of the Acoustical Society of America.

[68]  Marc Thiriet,et al.  Simulation of nonlinear Westervelt equation for the investigation of acoustic streaming and nonlinear propagation effects. , 2013, The Journal of the Acoustical Society of America.

[69]  G Montaldo,et al.  Non-invasive transcranial ultrasound therapy based on a 3D CT scan: protocol validation and in vitro results , 2009, Physics in medicine and biology.

[70]  Natalia Vykhodtseva,et al.  Blood-brain barrier disruption and vascular damage induced by ultrasound bursts combined with microbubbles can be influenced by choice of anesthesia protocol. , 2011, Ultrasound in medicine & biology.

[71]  Jay B. West,et al.  Predicting error in rigid-body point-based registration , 1998, IEEE Transactions on Medical Imaging.

[72]  F A Jolesz,et al.  MR imaging-guided focused ultrasound surgery of fibroadenomas in the breast: a feasibility study. , 2001, Radiology.

[73]  Bradley E Treeby,et al.  Accurate simulation of transcranial ultrasound propagation for ultrasonic neuromodulation and stimulation. , 2017, The Journal of the Acoustical Society of America.

[74]  Priya Bansal,et al.  Numerical evaluation of the skull for human neuromodulation with transcranial focused ultrasound , 2017, Journal of neural engineering.

[75]  U Pietrzyk,et al.  An interactive technique for three-dimensional image registration: validation for PET, SPECT, MRI and CT brain studies. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[76]  T G Leighton,et al.  Empirical angle-dependent Biot and MBA models for acoustic anisotropy in cancellous bone , 2007, Physics in medicine and biology.

[77]  Gangming Luo,et al.  Ultrasound simulation in bone , 2008, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[78]  In-Uk Song,et al.  Simultaneous acoustic stimulation of human primary and secondary somatosensory cortices using transcranial focused ultrasound , 2016, BMC Neuroscience.

[79]  J. Fandino,et al.  First noninvasive thermal ablation of a brain tumor with MR-guided focused ultrasound , 2014, Journal of therapeutic ultrasound.

[80]  S. Yoo,et al.  Image-Guided Transcranial Focused Ultrasound Stimulates Human Primary Somatosensory Cortex , 2015, Scientific Reports.

[81]  M J Ackerman,et al.  The Visible Human Project , 1998, Proc. IEEE.

[82]  E. Francomano,et al.  A smoothed particle interpolation scheme for transient electromagnetic simulation , 2006, IEEE Transactions on Magnetics.

[83]  K. Hynynen,et al.  Blood-brain barrier disruption induced by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index. , 2008, Ultrasound in medicine & biology.

[84]  Thomas Deffieux,et al.  Transcranial ultrasonic stimulation modulates single-neuron discharge in macaques performing an antisaccade task , 2017, Brain Stimulation.

[85]  Hyungmin Kim,et al.  Image‐guided navigation of single‐element focused ultrasound transducer , 2012, Int. J. Imaging Syst. Technol..

[86]  M. Krumpholz,et al.  MRTD: new time-domain schemes based on multiresolution analysis , 1996 .

[87]  Gregory T. Clement,et al.  A Magnetic Resonance Imaging–Compatible, Large‐Scale Array for Trans‐Skull Ultrasound Surgery and Therapy , 2005, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[88]  G. Trahey,et al.  A heterogeneous nonlinear attenuating full- wave model of ultrasound , 2009, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[89]  K. Kuroda,et al.  A precise and fast temperature mapping using water proton chemical shift , 1995, Magnetic resonance in medicine.

[90]  K. Hynynen,et al.  Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. , 2004, Ultrasound in medicine & biology.

[91]  Yun Jing,et al.  Time-reversal transcranial ultrasound beam focusing using a k-space method , 2012, Physics in medicine and biology.