MR-guided transcranial brain HIFU in small animal models

Recent studies have demonstrated the feasibility of transcranial high-intensity focused ultrasound (HIFU) therapy in the brain using adaptive focusing techniques. However, the complexity of the procedures imposes provision of accurate targeting, monitoring and control of this emerging therapeutic modality in order to ensure the safety of the treatment and avoid potential damaging effects of ultrasound on healthy tissues. For these purposes, a complete workflow and setup for HIFU treatment under magnetic resonance (MR) guidance is proposed and implemented in rats. For the first time, tissue displacements induced by the acoustic radiation force are detected in vivo in brain tissues and measured quantitatively using motion-sensitive MR sequences. Such a valuable target control prior to treatment assesses the quality of the focusing pattern in situ and enables us to estimate the acoustic intensity at focus. This MR-acoustic radiation force imaging is then correlated with conventional MR-thermometry sequences which are used to follow the temperature changes during the HIFU therapeutic session. Last, pre- and post-treatment magnetic resonance elastography (MRE) datasets are acquired and evaluated as a new potential way to non-invasively control the stiffness changes due to the presence of thermal necrosis. As a proof of concept, MR-guided HIFU is performed in vitro in turkey breast samples and in vivo in transcranial rat brain experiments. The experiments are conducted using a dedicated MR-compatible HIFU setup in a high-field MRI scanner (7 T). Results obtained on rats confirmed that both the MR localization of the US focal point and the pre- and post-HIFU measurement of the tissue stiffness, together with temperature control during HIFU are feasible and valuable techniques for efficient monitoring of HIFU in the brain. Brain elasticity appears to be more sensitive to the presence of oedema than to tissue necrosis.

[1]  C. Moonen,et al.  Image-guided, noninvasive, spatiotemporal control of gene expression , 2009, Proceedings of the National Academy of Sciences.

[2]  W. Dewey,et al.  Arrhenius relationships from the molecule and cell to the clinic , 2009, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[3]  D. Grenier,et al.  Transient MR elastography (t‐MRE) using ultrasound radiation force: Theory, safety, and initial experiments in vitro , 2008, Magnetic resonance in medicine.

[4]  Thomas Deffieux,et al.  Quantitative assessment of breast lesion viscoelasticity: initial clinical results using supersonic shear imaging. , 2008, Ultrasound in medicine & biology.

[5]  J Brian Fowlkes,et al.  Histotripsy: minimally invasive technology for prostatic tissue ablation in an in vivo canine model. , 2008, Urology.

[6]  Stephan E Maier,et al.  Magnetic resonance acoustic radiation force imaging. , 2008, Medical physics.

[7]  Ralph Sinkus,et al.  In vivo brain viscoelastic properties measured by magnetic resonance elastography , 2008, NMR in biomedicine.

[8]  G. Navon,et al.  A new MRI method, tested in vitro for the assessment of thermal coagulation and demonstrated in vivo on focused ultrasound ablation , 2008, NMR in biomedicine.

[9]  I. Roberts,et al.  High-intensity focused ultrasound ablation of liver tumours: can radiological assessment predict the histological response? , 2008, The British journal of radiology.

[10]  Ralph Sinkus,et al.  Magnetic resonance elastography for the noninvasive staging of liver fibrosis. , 2008, Gastroenterology.

[11]  Dieter Klatt,et al.  Non‐invasive measurement of brain viscoelasticity using magnetic resonance elastography , 2008, NMR in biomedicine.

[12]  Philip V Bayly,et al.  Measurement of the dynamic shear modulus of mouse brain tissue in vivo by magnetic resonance elastography. , 2008, Journal of biomechanical engineering.

[13]  Mathieu Pernot,et al.  Potential of MRI and Ultrasound Radiation Force in Elastography: Applications to Diagnosis and Therapy , 2008, Proceedings of the IEEE.

[14]  Roel Deckers,et al.  The role of ultrasound and magnetic resonance in local drug delivery , 2008, Journal of magnetic resonance imaging : JMRI.

[15]  J. Trobaugh,et al.  In vivo change in ultrasonic backscattered energy with temperature in motion-compensated images , 2008, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[16]  Clifford R. Jack,et al.  Magnetic resonance elastography of the brain , 2008, NeuroImage.

[17]  Mickael Tanter,et al.  MR elastography of breast lesions: Understanding the solid/liquid duality can improve the specificity of contrast‐enhanced MR mammography , 2007, Magnetic resonance in medicine.

[18]  J. Chapelon,et al.  Ultrasound surgery with a toric transducer allows the treatment of large volumes over short periods of time , 2007 .

[19]  Fabrice Marquet,et al.  In vivo transcranial brain surgery with an ultrasonic time reversal mirror. , 2007, Journal of neurosurgery.

[20]  Eyal Zadicario,et al.  MAGNETIC RESONANCE IMAGING‐GUIDED FOCUSED ULTRASOUND FOR THERMAL ABLATION IN THE BRAIN: A FEASIBILITY STUDY IN A SWINE MODEL , 2007, Neurosurgery.

[21]  M. Abolhassani,et al.  Noninvasive Temperature Estimation Using Sonographic Digital Images , 2007, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[22]  Y. Kaji,et al.  Magnetic resonance-guided focused ultrasound surgery for uterine fibroids: relationship between the therapeutic effects and signal intensity of preexisting T2-weighted magnetic resonance images. , 2007, American journal of obstetrics and gynecology.

[23]  Constantin Coussios,et al.  High intensity focused ultrasound: Physical principles and devices , 2007, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[24]  G Montaldo,et al.  Compensating for bone interfaces and respiratory motion in high-intensity focused ultrasound , 2007, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[25]  M. Bikson,et al.  Bio-heat transfer model of deep brain stimulation-induced temperature changes , 2006, Conference proceedings : ... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Annual Conference.

[26]  K. Wårdell,et al.  Radio-frequency lesioning in brain tissue with coagulation-dependent thermal conductivity: modelling, simulation and analysis of parameter influence and interaction , 2006, Medical and Biological Engineering and Computing.

[27]  Kullervo Hynynen,et al.  Pre-clinical testing of a phased array ultrasound system for MRI-guided noninvasive surgery of the brain--a primate study. , 2006, European journal of radiology.

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

[29]  Kiyoshi Namba,et al.  Breast Focused Ultrasound Surgery With Magnetic Resonance Guidance , 2006, Topics in magnetic resonance imaging : TMRI.

[30]  Fiona M. Fennessy,et al.  A Review of Magnetic Resonance Imaging-Guided Focused Ultrasound Surgery of Uterine Fibroids , 2006, Topics in magnetic resonance imaging : TMRI.

[31]  Chris J. Diederich,et al.  Magnetic Resonance-Guided High-Intensity Ultrasound Ablation of the Prostate , 2006, Topics in magnetic resonance imaging : TMRI.

[32]  F V Gleeson,et al.  The safety and feasibility of extracorporeal high-intensity focused ultrasound (HIFU) for the treatment of liver and kidney tumours in a Western population , 2005, British Journal of Cancer.

[33]  C. Moonen,et al.  Magnetic resonance temperature imaging , 2005, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[34]  M. Jacobs,et al.  Uterine fibroids: diffusion-weighted MR imaging for monitoring therapy with focused ultrasound surgery--preliminary study. , 2005, Radiology.

[35]  K. M. Bograchev,et al.  Ultrasonic temperature imaging for guiding focused ultrasound surgery: effect of angle between imaging beam and therapy beam. , 2005, Ultrasound in medicine & biology.

[36]  Michel Bertrand,et al.  Monitoring the formation of thermal lesions with heat-induced echo-strain imaging: a feasibility study. , 2005, Ultrasound in medicine & biology.

[37]  M Fink,et al.  Imaging anisotropic and viscous properties of breast tissue by magnetic resonance‐elastography , 2005, Magnetic resonance in medicine.

[38]  Mickael Tanter,et al.  The role of viscosity in the impulse diffraction field of elastic waves induced by the acoustic radiation force , 2004, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[39]  M. Fink,et al.  Supersonic shear imaging: a new technique for soft tissue elasticity mapping , 2004, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[40]  M. Fink,et al.  Temperature estimation using ultrasonic spatial compound imaging , 2004, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[41]  K. Hynynen,et al.  MRI investigation of the threshold for thermally induced blood–brain barrier disruption and brain tissue damage in the rabbit brain , 2004, Magnetic resonance in medicine.

[42]  J Bercoff,et al.  Monitoring Thermally-Induced Lesions with Supersonic Shear Imaging , 2004, Ultrasonic imaging.

[43]  M Pernot,et al.  High power transcranial beam steering for ultrasonic brain therapy. , 2003, Physics in medicine and biology.

[44]  Eduardo G Moros,et al.  Noninvasive temperature estimation based on the energy of backscattered ultrasound. , 2003, Medical physics.

[45]  M. Hennerici,et al.  Ultrasound in the treatment of ischaemic stroke , 2003, The Lancet Neurology.

[46]  J A de Zwart,et al.  Spatial and temporal control of transgene expression in vivo using a heat‐sensitive promoter and MRI‐guided focused ultrasound , 2003, The journal of gene medicine.

[47]  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.

[48]  Gregg Trahey,et al.  Observations of Tissue Response to Acoustic Radiation Force: Opportunities for Imaging , 2002, Ultrasonic imaging.

[49]  Kullervo Hynynen,et al.  Magnetic resonance image-guided focused ultrasound surgery. , 2002, Cancer journal.

[50]  H. Winn,et al.  High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo. , 2002, Ultrasound in medicine & biology.

[51]  A. Giuliano,et al.  Advances in FDG PET probes in surgical oncology. , 2002, Cancer journal.

[52]  K. Hynynen,et al.  Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. , 2001, Radiology.

[53]  J. Felmlee,et al.  Assessment of thermal tissue ablation with MR elastography , 2001, Magnetic resonance in medicine.

[54]  F A Jolesz,et al.  MRI detection of the thermal effects of focused ultrasound on the brain. , 2000, Ultrasound in medicine & biology.

[55]  R M Henkelman,et al.  Proton‐resonance frequency shift MR thermometry is affected by changes in the electrical conductivity of tissue , 2000, Magnetic resonance in medicine.

[56]  J Ophir,et al.  The feasibility of elastographic visualization of HIFU-induced thermal lesions in soft tissues. Image-guided high-intensity focused ultrasound. , 1999, Ultrasound in medicine & biology.

[57]  Roy W. Martin,et al.  Detection of High-Intensity Focused Ultrasound Liver Lesions Using Dynamic Elastometry , 1999, Ultrasonic imaging.

[58]  S. Emelianov,et al.  Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. , 1998, Ultrasound in medicine & biology.

[59]  J. Chapelon,et al.  Differential Attenuation Imaging for the Characterization of High Intensity Focused Ultrasound Lesions , 1998, Ultrasonic imaging.

[60]  J. L. Thomas,et al.  Focusing and steering through absorbing and aberrating layers: application to ultrasonic propagation through the skull. , 1998, The Journal of the Acoustical Society of America.

[61]  J. Greenleaf,et al.  Ultrasound-stimulated vibro-acoustic spectrography. , 1998, Science.

[62]  J.-L. Thomas,et al.  Ultrasonic beam focusing through tissue inhomogeneities with a time reversal mirror: application to transskull therapy , 1996, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[63]  K. Boone,et al.  Effect of skin impedance on image quality and variability in electrical impedance tomography: a model study , 1996, Medical and Biological Engineering and Computing.

[64]  R. Ehman,et al.  Magnetic resonance elastography , 1996, Nature Medicine.

[65]  A. Manduca,et al.  Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. , 1995, Science.

[66]  R. Seip,et al.  Noninvasive estimation of tissue temperature response to heating fields using diagnostic ultrasound , 1995, IEEE Transactions on Biomedical Engineering.

[67]  W. Dewey,et al.  Thermal dose determination in cancer therapy. , 1984, International journal of radiation oncology, biology, physics.

[68]  K M Sekins,et al.  Determination of perfusion field during local hyperthermia with the aid of finite element thermal models. , 1982, Journal of biomechanical engineering.

[69]  F. Dunn,et al.  Compilation of empirical ultrasonic properties of mammalian tissues. II. , 1980, The Journal of the Acoustical Society of America.

[70]  F. Dunn,et al.  Comprehensive compilation of empirical ultrasonic properties of mammalian tissues. , 1978, The Journal of the Acoustical Society of America.

[71]  J. O'brien,et al.  Lipid composition of the normal human brain: gray matter, white matter, and myelin. , 1965, Journal of lipid research.

[72]  Gail ter Haar,et al.  Therapeutic applications of ultrasound. , 2007, Progress in biophysics and molecular biology.

[73]  Gail ter Haar,et al.  Therapeutic applications of ultrasound. , 2007 .

[74]  R Willinger,et al.  Shear linear behavior of brain tissue over a large frequency range. , 2005, Biorheology.

[75]  M Pernot,et al.  High power transcranial beam steering for ultrasonic brain therapy , 2003 .

[76]  L. Crum,et al.  Image-guided acoustic therapy. , 2001, Annual review of biomedical engineering.

[77]  K. Hynynen,et al.  Trans-skull ultrasound therapy: the feasibility of using image-derived skull thickness information to correct the phase distortion , 1999, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[78]  P. VanBaren,et al.  Two-dimensional temperature estimation using diagnostic ultrasound , 1998, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[79]  K. Hynynen,et al.  Thermal dose optimization via temporal switching in ultrasound surgery , 1998, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[80]  J. Arendt Paper presented at the 10th Nordic-Baltic Conference on Biomedical Imaging: Field: A Program for Simulating Ultrasound Systems , 1996 .

[81]  J. Jensen,et al.  Calculation of pressure fields from arbitrarily shaped, apodized, and excited ultrasound transducers , 1992, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[82]  Francis A. Duck,et al.  Physical properties of tissue : a comprehensive reference book , 1990 .