Theranostics in the vasculature: bioeffects of ultrasound and microbubbles to induce vascular shutdown

Ultrasound-triggered microbubbles destruction leading to vascular shutdown have resulted in preclinical studies in tumor growth delay or inhibition, lesion formation, radio-sensitization and modulation of the immune micro-environment. Antivascular ultrasound aims to be developed as a focal, targeted, non-invasive, mechanical and non-thermal treatment, alone or in combination with other treatments, and this review positions these treatments among the wider therapeutic ultrasound domain. Antivascular effects have been reported for a wide range of ultrasound exposure conditions, and evidence points to a prominent role of cavitation as the main mechanism. At relatively low peak negative acoustic pressure, predominantly non-inertial cavitation is most likely induced, while higher peak negative pressures lead to inertial cavitation and bubbles collapse. Resulting bioeffects start with inflammation and/or loose opening of the endothelial lining of the vessel. The latter causes vascular access of tissue factor, leading to platelet aggregation, and consequent clotting. Alternatively, endothelium damage exposes subendothelial collagen layer, leading to rapid adhesion and aggregation of platelets and clotting. In a pilot clinical trial, a prevalence of tumor response was observed in patients receiving ultrasound-triggered microbubble destruction along with transarterial radioembolization. Two ongoing clinical trials are assessing the effectiveness of ultrasound-stimulated microbubble treatment to enhance radiation effects in cancer patients. Clinical translation of antivascular ultrasound/microbubble approach may thus be forthcoming.

[1]  J. Hossack,et al.  Quantitative analysis of in-vivo microbubble distribution in the human brain , 2021, Scientific Reports.

[2]  K. Hynynen,et al.  MR-guided focused ultrasound liquid biopsy enriches circulating biomarkers in patients with brain tumors , 2021, Neuro-oncology.

[3]  Ji-Bin Liu,et al.  US-triggered Microbubble Destruction for Augmenting Hepatocellular Carcinoma Response to Transarterial Radioembolization: A Randomized Pilot Clinical Trial. , 2020, Radiology.

[4]  K. Hynynen,et al.  Comparing rapid short-pulse to tone burst sonication sequences for focused ultrasound and microbubble-mediated blood-brain barrier permeability enhancement. , 2020, Journal of controlled release : official journal of the Controlled Release Society.

[5]  W. Tran,et al.  Effect of Treatment Sequencing on the Tumor Response to Combined Treatment With Ultrasound‐Stimulated Microbubbles and Radiotherapy , 2020, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[6]  C. Pacia,et al.  Focused ultrasound for safe and effective release of brain tumor biomarkers into the peripheral circulation , 2020, PloS one.

[7]  E. Leuthardt,et al.  Feasibility and safety of focused ultrasound-enabled liquid biopsy in the brain of a porcine model , 2020, Scientific Reports.

[8]  Mark Borden,et al.  Microbubble Agents: New Directions. , 2020, Ultrasound in medicine & biology.

[9]  G. Miller,et al.  Sonoselective transfection of cerebral vasculature without blood–brain barrier disruption , 2020, Proceedings of the National Academy of Sciences.

[10]  Hai Jin,et al.  Enhancement Effect of Microbubble-Enhanced Ultrasound in Microwave Ablation in Rabbit VX2 Liver Tumors , 2020, BioMed research international.

[11]  Y. Liao,et al.  Therapeutic ultrasound combined with microbubbles improves atherosclerotic plaque stability by selectively destroying the intraplaque neovasculature , 2020, Theranostics.

[12]  Mickael Tanter,et al.  Super-resolution Ultrasound Imaging. , 2020, Ultrasound in medicine & biology.

[13]  P. Frinking,et al.  Three Decades of Ultrasound Contrast Agents: A Review of the Past, Present and Future Improvements. , 2020, Ultrasound in medicine & biology.

[14]  R. Price,et al.  Perspectives on Recent Progress in Focused Ultrasound Immunotherapy , 2019, Theranostics.

[15]  Nir Lipsman,et al.  First-in-human trial of blood–brain barrier opening in amyotrophic lateral sclerosis using MR-guided focused ultrasound , 2019, Nature Communications.

[16]  J. Frank,et al.  The Proteomic Effects of Pulsed Focused Ultrasound on Tumor Microenvironments of Murine Melanoma and Breast Cancer Models. , 2019, Ultrasound in medicine & biology.

[17]  Yongping Lu,et al.  The effects of ultrasound-targeted microbubble destruction (UTMD) carrying IL-8 monoclonal antibody on the inflammatory responses and stability of atherosclerotic plaques. , 2019, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[18]  Douglas L. Miller,et al.  Capillary Hemorrhage Induced by Contrast-Enhanced Diagnostic Ultrasound in Rat Intestine. , 2019, Ultrasound in medicine & biology.

[19]  J. Tu,et al.  Low-intensity pulsed ultrasound promotes apoptosis and inhibits angiogenesis via p38 signaling-mediated endoplasmic reticulum stress in human endothelial cells , 2019, Molecular medicine reports.

[20]  Jiao Peng,et al.  Berberine nanoparticles for promising sonodynamic therapy of a HeLa xenograft tumour , 2019, RSC advances.

[21]  E. Stride,et al.  Microbubbles, Nanodroplets and Gas-Stabilizing Solid Particles for Ultrasound-Mediated Extravasation of Unencapsulated Drugs: An Exposure Parameter Optimization Study. , 2019, Ultrasound in medicine & biology.

[22]  James J. Choi,et al.  Rapid Short-pulse Ultrasound Delivers Drugs Uniformly across the Murine Blood-Brain Barrier with Negligible Disruption. , 2019, Radiology.

[23]  K. Hynynen,et al.  Enhancing Checkpoint Inhibitor Therapy with Ultrasound Stimulated Microbubbles. , 2019, Ultrasound in medicine & biology.

[24]  Nir Lipsman,et al.  Blood-Brain Barrier Opening in Primary Brain Tumors with Non-invasive MR-Guided Focused Ultrasound: A Clinical Safety and Feasibility Study , 2019, Scientific Reports.

[25]  K. Hynynen,et al.  Ultrasound-responsive droplets for therapy: A review. , 2019, Journal of controlled release : official journal of the Controlled Release Society.

[26]  C. Moonen,et al.  Sonopermeation to improve drug delivery to tumors: from fundamental understanding to clinical translation , 2018, Expert opinion on drug delivery.

[27]  K. Hynynen,et al.  Microbubble-assisted MRI-guided focused ultrasound for hyperthermia at reduced power levels , 2018, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[28]  K. Hynynen,et al.  Angiogenic response of rat hippocampal vasculature to focused ultrasound-mediated increases in blood-brain barrier permeability , 2018, Scientific Reports.

[29]  M. Borden,et al.  State-of-the-art of microbubble-assisted blood-brain barrier disruption , 2018, Theranostics.

[30]  E. Leuthardt,et al.  Focused Ultrasound-enabled Brain Tumor Liquid Biopsy , 2018, Scientific Reports.

[31]  S. Delorme,et al.  Motion model ultrasound localization microscopy for preclinical and clinical multiparametric tumor characterization , 2018, Nature Communications.

[32]  G. Czarnota,et al.  Role of Acid Sphingomyelinase and Ceramide in Mechano-Acoustic Enhancement of Tumor Radiation Responses , 2018, Journal of the National Cancer Institute.

[33]  F. Orsi,et al.  Focused ultrasound: tumour ablation and its potential to enhance immunological therapy to cancer. , 2018, The British journal of radiology.

[34]  W. Tran,et al.  Tumour Vascular Shutdown and Cell Death Following Ultrasound-Microbubble Enhanced Radiation Therapy , 2018, Theranostics.

[35]  Ji-Bin Liu,et al.  Localized microbubble cavitation-based antivascular therapy for improving HCC treatment response to radiotherapy. , 2017, Cancer letters.

[36]  Chanikarn Power,et al.  Closed-loop control of targeted ultrasound drug delivery across the blood–brain/tumor barriers in a rat glioma model , 2017, Proceedings of the National Academy of Sciences.

[37]  C. Yeh,et al.  Current progress in antivascular tumor therapy. , 2017, Drug discovery today.

[38]  Kullervo Hynynen,et al.  Acute Inflammatory Response Following Increased Blood-Brain Barrier Permeability Induced by Focused Ultrasound is Dependent on Microbubble Dose , 2017, Theranostics.

[39]  Colleen T. Curley,et al.  Focused Ultrasound Immunotherapy for Central Nervous System Pathologies: Challenges and Opportunities , 2017, Theranostics.

[40]  T. Bettinger,et al.  Characteristics and Echogenicity of Clinical Ultrasound Contrast Agents: An In Vitro and In Vivo Comparison Study , 2017, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[41]  K. Hynynen,et al.  Acute effects of focused ultrasound-induced increases in blood-brain barrier permeability on rat microvascular transcriptome , 2017, Scientific Reports.

[42]  J. Frank,et al.  Improving the therapeutic efficacy of mesenchymal stromal cells to restore perfusion in critical limb ischemia through pulsed focused ultrasound , 2017, Scientific Reports.

[43]  Xinmai Yang,et al.  High-precision, non-invasive anti-microvascular approach via concurrent ultrasound and laser irradiation , 2017, Scientific Reports.

[44]  M. Borden,et al.  Microbubble gas volume: A unifying dose parameter in blood-brain barrier opening by focused ultrasound , 2017, Theranostics.

[45]  Neekita Jikaria,et al.  Disrupting the blood–brain barrier by focused ultrasound induces sterile inflammation , 2016, Proceedings of the National Academy of Sciences.

[46]  A. Molven,et al.  A human clinical trial using ultrasound and microbubbles to enhance gemcitabine treatment of inoperable pancreatic cancer. , 2016, Journal of controlled release : official journal of the Controlled Release Society.

[47]  James J. Choi,et al.  Rapid short-pulse sequences enhance the spatiotemporal uniformity of acoustically driven microbubble activity during flow conditions. , 2016, The Journal of the Acoustical Society of America.

[48]  K. Hoang-Xuan,et al.  Clinical trial of blood-brain barrier disruption by pulsed ultrasound , 2016, Science Translational Medicine.

[49]  Natalia Vykhodtseva,et al.  Cavitation-enhanced nonthermal ablation in deep brain targets: feasibility in a large animal model. , 2016, Journal of neurosurgery.

[50]  Ari Partanen,et al.  Low-Intensity Focused Ultrasound Induces Reversal of Tumor-Induced T Cell Tolerance and Prevents Immune Escape , 2016, The Journal of Immunology.

[51]  N. McDannold,et al.  Nonthermal ablation in the rat brain using focused ultrasound and an ultrasound contrast agent: long-term effects. , 2016, Journal of neurosurgery.

[52]  F. DiMeco,et al.  Intraoperative Navigated Angiosonography for Skull Base Tumor Surgery. , 2015, World neurosurgery.

[53]  M. Tanter,et al.  Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging , 2015, Nature.

[54]  C. Dietrich,et al.  Benefit of Contrast-Enhanced Ultrasound (CEUS) in the Follow-Up Care of Patients with Colon Cancer: A Prospective Multicenter Study , 2015, Ultraschall in der Medizin.

[55]  Yini Chen,et al.  Optimization of low-frequency low-intensity ultrasound-mediated microvessel disruption on prostate cancer xenografts in nude mice using an orthogonal experimental design. , 2015, Oncology letters.

[56]  Fabian Kiessling,et al.  Evolution of contrast agents for ultrasound imaging and ultrasound-mediated drug delivery , 2015, Front. Pharmacol..

[57]  Eleanor Stride,et al.  Ultrasound-Propelled Nanocups for Drug Delivery , 2015, Small.

[58]  Y. Liao,et al.  Selective depletion of tumor neovasculature by microbubble destruction with appropriate ultrasound pressure , 2015, International journal of cancer.

[59]  T. Liang,et al.  Enhanced antitumor efficacy of ultrasonic cavitation with up-sized microbubbles in pancreatic cancer , 2015, Oncotarget.

[60]  J. Frank,et al.  Pulsed Focused Ultrasound Pretreatment Improves Mesenchymal Stromal Cell Efficacy in Preventing and Rescuing Established Acute Kidney Injury in Mice , 2015, Stem cells.

[61]  Chandra M Sehgal,et al.  A review of low-intensity ultrasound for cancer therapy. , 2015, Ultrasound in medicine & biology.

[62]  G. Czarnota,et al.  Biomechanical effects of microbubbles: from radiosensitization to cell death. , 2015, Future oncology.

[63]  David E Goertz,et al.  An overview of the influence of therapeutic ultrasound exposures on the vasculature: High intensity ultrasound and microbubble-mediated bioeffects , 2015, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[64]  L. Solbiati,et al.  INTRAOPERATIVE CONTRAST ENHANCED ULTRASOUND IN BRAIN TUMOR SURGERY , 2014 .

[65]  L. Solbiati,et al.  Intraoperative Cerebral Glioma Characterization with Contrast Enhanced Ultrasound , 2014, BioMed research international.

[66]  Luigi Solbiati,et al.  Intraoperative contrast-enhanced ultrasound for brain tumor surgery. , 2014, Neurosurgery.

[67]  G. Czarnota,et al.  Dll4-Notch Signalling Blockade Synergizes Combined Ultrasound-Stimulated Microbubble and Radiation Therapy in Human Colon Cancer Xenografts , 2014, PloS one.

[68]  Chih-Kuang Yeh,et al.  Combining Microbubbles and Ultrasound for Drug Delivery to Brain Tumors: Current Progress and Overview , 2014, Theranostics.

[69]  W. Tran,et al.  Cellular characterization of ultrasound-stimulated microbubble radiation enhancement in a prostate cancer xenograft model , 2014, Disease Models & Mechanisms.

[70]  W. Pitt,et al.  Acoustic Droplet Vaporization in Biology and Medicine , 2013, BioMed research international.

[71]  F. Jolesz,et al.  Nonthermal ablation with microbubble-enhanced focused ultrasound close to the optic tract without affecting nerve function. , 2013, Journal of neurosurgery.

[72]  H. Ran,et al.  Ultrasound targeted microbubble destruction promotes angiogenesis and heart function by inducing myocardial microenvironment change. , 2013, Ultrasound in medicine & biology.

[73]  Sheldon J. J. Kwok,et al.  Ultrasound-mediated microbubble enhancement of radiation therapy studied using three-dimensional high-frequency power Doppler ultrasound. , 2013, Ultrasound in medicine & biology.

[74]  Jonathan A. Kopechek,et al.  Relationship between cavitation and loss of echogenicity from ultrasound contrast agents , 2013, Physics in medicine and biology.

[75]  G. Czarnota,et al.  Effects of biophysical parameters in enhancing radiation responses of prostate tumors with ultrasound-stimulated microbubbles. , 2013, Ultrasound in medicine & biology.

[76]  K. Hynynen,et al.  Creating brain lesions with low-intensity focused ultrasound with microbubbles: a rat study at half a megahertz. , 2013, Ultrasound in medicine & biology.

[77]  F. Stuart Foster,et al.  Acoustic Angiography: A New Imaging Modality for Assessing Microvasculature Architecture , 2013, Int. J. Biomed. Imaging.

[78]  Kullervo Hynynen,et al.  Antitumor effects of combining metronomic chemotherapy with the antivascular action of ultrasound stimulated microbubbles , 2013, International journal of cancer.

[79]  S. Wong,et al.  Ultrasound-Activated Microbubble Cancer Therapy: Ceramide Production Leading to Enhanced Radiation Effect in vitro , 2013, Technology in cancer research & treatment.

[80]  Kullervo Hynynen,et al.  Antitumor Effects of Combining Docetaxel (Taxotere) with the Antivascular Action of Ultrasound Stimulated Microbubbles , 2012, PloS one.

[81]  S. Crouzet,et al.  Prostate focused ultrasound focal therapy—imaging for the future , 2012, Nature Reviews Clinical Oncology.

[82]  Wen-zhi Chen,et al.  Clinical utility of a microbubble-enhancing contrast ("SonoVue") in treatment of uterine fibroids with high intensity focused ultrasound: a retrospective study. , 2012, European journal of radiology.

[83]  Robert Carlisle,et al.  Ultrasound-enhanced drug delivery for cancer , 2012, Expert opinion on drug delivery.

[84]  Hao-Li Liu,et al.  Low-pressure pulsed focused ultrasound with microbubbles promotes an anticancer immunological response , 2012, Journal of Translational Medicine.

[85]  James J. Choi,et al.  Spatiotemporal evolution of cavitation dynamics exhibited by flowing microbubbles during ultrasound exposure. , 2012, The Journal of the Acoustical Society of America.

[86]  Raffi Karshafian,et al.  Bioeffects of ultrasound-stimulated microbubbles on endothelial cells: gene expression changes associated with radiation enhancement in vitro. , 2012, Ultrasound in medicine & biology.

[87]  M. Livingstone,et al.  Controlled Ultrasound-Induced Blood-Brain Barrier Disruption Using Passive Acoustic Emissions Monitoring , 2012, PloS one.

[88]  Paul A Dayton,et al.  Mapping microvasculature with acoustic angiography yields quantifiable differences between healthy and tumor-bearing tissue volumes in a rodent model. , 2012, Radiology.

[89]  W. Tran,et al.  Microbubble and ultrasound radioenhancement of bladder cancer , 2012, British Journal of Cancer.

[90]  Gregory J. Czarnota,et al.  Tumor radiation response enhancement by acoustical stimulation of the vasculature , 2012, Proceedings of the National Academy of Sciences.

[91]  Katherine W Ferrara,et al.  Insonation of Targeted Microbubbles Produces Regions of Reduced Blood Flow Within Tumor Vasculature , 2012, Investigative radiology.

[92]  Win-Li Lin,et al.  Ultrasound sonication with microbubbles disrupts blood vessels and enhances tumor treatments of anticancer nanodrug , 2012, International journal of nanomedicine.

[93]  Kullervo Hynynen,et al.  Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. , 2012, Radiology.

[94]  P. Li,et al.  Disruption of tumor neovasculature by microbubble enhanced ultrasound: a potential new physical therapy of anti-angiogenesis. , 2012, Ultrasound in medicine & biology.

[95]  C. Sehgal,et al.  Modeling of thermal effects in antivascular ultrasound therapy. , 2012, The Journal of the Acoustical Society of America.

[96]  Elisa E Konofagou,et al.  Noninvasive and localized neuronal delivery using short ultrasonic pulses and microbubbles , 2011, Proceedings of the National Academy of Sciences.

[97]  M. Arditi,et al.  BR38, a New Ultrasound Blood Pool Agent , 2011, Investigative radiology.

[98]  J. Sheehan,et al.  Inhibition of glioma growth by microbubble activation in a subcutaneous model using low duty cycle ultrasound without significant heating. , 2011, Journal of neurosurgery.

[99]  J. Chapelon,et al.  Prostate cancer ablation with transrectal high-intensity focused ultrasound: assessment of tissue destruction with contrast-enhanced US. , 2011, Radiology.

[100]  Wayne Kreider,et al.  Blood vessel deformations on microsecond time scales by ultrasonic cavitation. , 2011, Physical review letters.

[101]  P. Carson,et al.  Initial investigation of acoustic droplet vaporization for occlusion in canine kidney. , 2010, Ultrasound in medicine & biology.

[102]  Yao-Sheng Tung,et al.  Multi-modality safety assessment of blood-brain barrier opening using focused ultrasound and definity microbubbles: a short-term study. , 2010, Ultrasound in medicine & biology.

[103]  Paul A Dayton,et al.  High-resolution, high-contrast ultrasound imaging using a prototype dual-frequency transducer: In vitro and in vivo studies , 2010, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[104]  S. Homma,et al.  Effect of microbubble size on fundamental mode high frequency ultrasound imaging in mice. , 2010, Ultrasound in medicine & biology.

[105]  Susan M. Schultz,et al.  Antivascular ultrasound therapy extends survival of mice with implanted melanomas. , 2010, Ultrasound in medicine & biology.

[106]  Alexander R. Klotz,et al.  Temperature change near microbubbles within a capillary network during focused ultrasound , 2010, Physics in medicine and biology.

[107]  E. Stride,et al.  Cavitation and contrast: The use of bubbles in ultrasound imaging and therapy , 2010, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[108]  Chien Ting Chin,et al.  Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mesenchymal stem cells after acute myocardial infarction. , 2009, Journal of molecular and cellular cardiology.

[109]  B. Raju,et al.  Control and reversal of tumor growth by ultrasound activated microbubbles , 2009, 2009 IEEE International Ultrasonics Symposium.

[110]  Joseph L Bull,et al.  An ex vivo study of the correlation between acoustic emission and microvascular damage. , 2009, Ultrasound in medicine & biology.

[111]  Zvi Friedman,et al.  Quantitative evaluation of local myocardial blood volume in contrast echocardiography , 2009, Medical Image Anal..

[112]  C. Sehgal,et al.  The disruption of murine tumor neovasculature by low-intensity ultrasound-comparison between 1- and 3-MHz sonication frequencies. , 2008, Academic radiology.

[113]  Kenneth S Suslick,et al.  Inside a collapsing bubble: sonoluminescence and the conditions during cavitation. , 2008, Annual review of physical chemistry.

[114]  T. Kim,et al.  Enhancement patterns of hepatocellular carcinoma at contrast-enhanced US: comparison with histologic differentiation. , 2007, Radiology.

[115]  M. Okusa,et al.  Ultrasound Contrast Agents in the Study of Kidney Function in Health and Disease. , 2007, Drug discovery today. Disease mechanisms.

[116]  Paul A Dayton,et al.  Direct observations of ultrasound microbubble contrast agent interaction with the microvessel wall. , 2007, The Journal of the Acoustical Society of America.

[117]  Katherine W Ferrara,et al.  Enhancement of vascular permeability with low-frequency contrast-enhanced ultrasound in the chorioallantoic membrane model. , 2007, Radiology.

[118]  D. Dalecki WFUMB Safety Symposium on Echo-Contrast Agents: bioeffects of ultrasound contrast agents in vivo. , 2007, Ultrasound in medicine & biology.

[119]  K. Hynynen,et al.  Induction of apoptosis in vivo in the rabbit brain with focused ultrasound and Optison. , 2006, Ultrasound in Medicine and Biology.

[120]  Xiaodong Zhou,et al.  Enhancement of ultrasound contrast agent in High-Intensity focused ultrasound ablation , 2006, Advances in therapy.

[121]  Kullervo Hynynen,et al.  Microbubble contrast agent with focused ultrasound to create brain lesions at low power levels: MR imaging and histologic study in rabbits. , 2006, Radiology.

[122]  A. Brayman,et al.  Correlation between inertial cavitation dose and endothelial cell damage in vivo. , 2006, Ultrasound in medicine & biology.

[123]  C. Sehgal,et al.  Histopathological observations of the antivascular effects of physiotherapy ultrasound on a murine neoplasm. , 2006, Ultrasound in medicine & biology.

[124]  Michael D Feldman,et al.  The antivascular action of physiotherapy ultrasound on murine tumors. , 2005, Ultrasound in medicine & biology.

[125]  A. Klibanov,et al.  Ultrasound-microbubble-induced neovascularization in mouse skeletal muscle. , 2005, Ultrasound in medicine & biology.

[126]  P. Carson,et al.  Acoustic droplet vaporization for temporal and spatial control of tissue occlusion: a kidney study , 2005, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[127]  Lawrence A Crum,et al.  Vascular effects induced by combined 1-MHz ultrasound and microbubble contrast agent treatments in vivo. , 2005, Ultrasound in medicine & biology.

[128]  Gregory T. Clement,et al.  Perspectives in clinical uses of high-intensity focused ultrasound. , 2004, Ultrasonics.

[129]  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.

[130]  C. Cain,et al.  Microbubble-enhanced cavitation for noninvasive ultrasound surgery , 2003, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[131]  K. Ley,et al.  Journal of Thrombosis and Haemostasis, 1: 1699±1709 REVIEW ARTICLE The role of in¯ammation in vascular injury and repair , 2022 .

[132]  Zvi Fuks,et al.  Tumor Response to Radiotherapy Regulated by Endothelial Cell Apoptosis , 2003, Science.

[133]  K. Hynynen,et al.  Optical monitoring of ultrasound-induced bioeffects in glass catfish. , 2003, Ultrasound in medicine & biology.

[134]  A. Klibanov,et al.  Microbubbles induce renal hemorrhage when exposed to diagnostic ultrasound in anesthetized rats. , 2002, Ultrasound in medicine & biology.

[135]  Ji Song,et al.  Stimulation of Arteriogenesis in Skeletal Muscle by Microbubble Destruction With Ultrasound , 2002, Circulation.

[136]  Satoshi Yamada,et al.  Endothelial cell injury in venule and capillary induced by contrast ultrasonography. , 2002, Ultrasound in medicine & biology.

[137]  S. Umemura,et al.  Enhancement of ultrasonic absorption by microbubbles for therapeutic application , 2001, 2001 IEEE Ultrasonics Symposium. Proceedings. An International Symposium (Cat. No.01CH37263).

[138]  E. Carstensen,et al.  Bioeffects of positive and negative acoustic pressures in mice infused with microbubbles. , 2000, Ultrasound in medicine & biology.

[139]  D. Miller,et al.  Diagnostic Ultrasound Activation of Contrast Agent Gas Bodies Induces Capillary Rupture in Mice. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[141]  D. Miller,et al.  The influence of ultrasound frequency and gas-body composition on the contrast agent-mediated enhancement of vascular bioeffects in mouse intestine. , 2000, Ultrasound in medicine & biology.

[142]  D. Miller,et al.  Consequences of lithotripter shockwave interaction with gas body contrast agent in mouse intestine. , 1999, The Journal of urology.

[143]  D. Miller,et al.  Gas-body-based contrast agent enhances vascular bioeffects of 1.09 MHz ultrasound on mouse intestine. , 1998, Ultrasound in medicine & biology.

[144]  T C Skalak,et al.  Delivery of colloidal particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound. , 1998, Circulation.

[145]  T C Skalak,et al.  Direct In Vivo Visualization of Intravascular Destruction of Microbubbles by Ultrasound and Its Local Effects on Tissue. , 1998, Circulation.

[146]  A. Kabalnov,et al.  Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory. , 1998, Ultrasound in medicine & biology.

[147]  Robert E. Apfel,et al.  Sonic effervescence: A tutorial on acoustic cavitation , 1997 .

[148]  Andrea Prosperetti,et al.  Nonlinear oscillations of gas bubbles in liquids. Transient solutions and the connection between subharmonic signal and cavitation , 1975 .

[149]  K. Hynynen,et al.  Opening the Blood-Brain Barrier with MR Imaging-guided Focused Ultrasound: Preclinical Testing on a Trans-Human Skull Porcine Model. , 2017, Radiology.

[150]  Christian Greis,et al.  Quantitative evaluation of microvascular blood flow by contrast-enhanced ultrasound (CEUS). , 2011, Clinical hemorheology and microcirculation.

[151]  Xiaodong Zhou,et al.  Transmission electron microscopy of VX2 liver tumors after high-intensity focused ultrasound ablation enhanced with SonoVue® , 2009, Advances in therapy.

[152]  Douglas L. Miller Overview of experimental studies of biological effects of medical ultrasound caused by gas body activation and inertial cavitation. , 2007, Progress in biophysics and molecular biology.

[153]  P. Dayton,et al.  Mechanisms of contrast agent destruction , 2001, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[154]  Y. Nishimura,et al.  Increased heating efficiency of hyperthermia using an ultrasound contrast agent: a phantom study. , 1998, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[155]  E. Carstensen,et al.  The influence of contrast agents on hemorrhage produced by lithotripter fields. , 1997, Ultrasound in medicine & biology.

[156]  G. Haar The Acoustic Bubble , 1996 .

[157]  E. Carstensen,et al.  A test for cavitation as a mechanism for intestinal hemorrhage in mice exposed to a piezoelectric lithotripter. , 1996, Ultrasound in medicine & biology.

[158]  E. Carstensen,et al.  Intestinal hemorrhage from exposure to pulsed ultrasound. , 1995, Ultrasound in medicine & biology.

[159]  R. M. Thomas,et al.  Thresholds for hemorrhages in mouse skin and intestine induced by lithotripter shock waves. , 1995, Ultrasound in medicine & biology.

[160]  E. Carstensen,et al.  Thresholds for intestinal hemorrhage in mice exposed to a piezoelectric lithotripter. , 1995, Ultrasound in medicine & biology.