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Expert Opinion on Drug Delivery Volume 10, 2013 - Issue 5
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Ultrasound-mediated drug delivery for cardiovascular disease

Jonathan T SuttonUniversity of Cincinnati, College of Engineering and Applied Science, Biomedical Engineering Program, Cincinnati, OH, USA
, BS,
Kevin J HaworthUniversity of Cincinnati, College of Medicine, Internal Medicine, Division of Cardiovascular Diseases, 3935 Cardiovascular Center 231 Albert Sabin Way Cincinnati, OH 45267-0586, USA+1 5135585675; +1 5135586102; [email protected];University of Cincinnati, College of Engineering and Applied Science, Biomedical Engineering Program, Cincinnati, OH, USA
, PhD,
Gail Pyne-GeithmanUniversity of Cincinnati, College of Medicine, Department of Neurosurgery and the University of Cincinnati Neuroscience Institute, Cincinnati, OH, USA;Mayfield Clinic, Cincinnati, OH, USA
, DPhil &
Christy K HollandUniversity of Cincinnati, College of Medicine, Internal Medicine, Division of Cardiovascular Diseases, 3935 Cardiovascular Center 231 Albert Sabin Way Cincinnati, OH 45267-0586, USA+1 5135585675; +1 5135586102; [email protected];University of Cincinnati, College of Engineering and Applied Science, Biomedical Engineering Program, Cincinnati, OH, USA
, PhD
Pages 573-592 | Published online: 01 Mar 2013

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Melvin E. Klegerman, Melanie R. Moody, Shao-Ling Huang, Tao Peng, Susan T. Laing, Vijay Govindarajan, Delia Danila, Amirali Tahanan, Mohammad H. Rahbar, Deborah Vela, Curtis Genstler, Kevin J. Haworth, Christy K. Holland, David D. McPherson & Patrick H. Kee. (2023) Demonstration of ultrasound-mediated therapeutic delivery of fibrin-targeted pioglitazone-loaded echogenic liposomes into the arterial bed for attenuation of peri-stent restenosis. Journal of Drug Targeting 31:1, pages 109-118.
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Dallan McMahon, Charissa Poon & Kullervo Hynynen. (2019) Evaluating the safety profile of focused ultrasound and microbubble-mediated treatments to increase blood-brain barrier permeability. Expert Opinion on Drug Delivery 16:2, pages 129-142.
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J. T. Sutton, K. J. Haworth, S. K. Shanmukhappa, M. R. Moody, M. E. Klegerman, J. K. Griffin, D. M. Patton, D. D. McPherson & C. K. Holland. (2016) Delivery of bevacizumab to atheromatous porcine carotid tissue using echogenic liposomes. Drug Delivery 23:9, pages 3594-3605.
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Baljeet Singh, Tarun Garg, Amit K. Goyal & Goutam Rath. (2016) Recent advancements in the cardiovascular drug carriers. Artificial Cells, Nanomedicine, and Biotechnology 44:1, pages 216-225.
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JT Sutton, JL Raymond, MC Verleye, GJ Pyne-Geithman & CK Holland. (2014) Pulsed ultrasound enhances the delivery of nitric oxide from bubble liposomes to ex vivo porcine carotid tissue. International Journal of Nanomedicine 9, pages 4671-4683.
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. (2023) AIUM Official Statement for the Statement on Biological Effects of Therapeutic Ultrasound . Journal of Ultrasound in Medicine 42:12.
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Daniel Suarez Escudero, Kevin J. Haworth, Curtis Genstler & Christy K. Holland. (2023) Quantifying the Effect of Acoustic Parameters on Temporal and Spatial Cavitation Activity: Gauging Cavitation Dose. Ultrasound in Medicine & Biology 49:11, pages 2388-2397.
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Melvin E. Klegerman, Tao Peng, Shao-Ling Huang, Brion Frierson, Melanie R. Moody, Hyunggun Kim & David D. McPherson. (2023) Storage Stability of Atheroglitatide, an Echogenic Liposomal Formulation of Pioglitazone Targeted to Advanced Atheroma with a Fibrin-Binding Peptide. Pharmaceutics 15:9, pages 2288.
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Xin Yin & Li-Hong Jiang. (2023) Extracellular vesicles: Targeting the heart. Frontiers in Cardiovascular Medicine 9.
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Mahdieh Darroudi, Seyedeh Elnaz Nazari, Prashant Kesharwani, Majid Rezayi, Majid Khazaei & Amirhossein Sahebkar. 2023. Emerging Applications of Carbon Nanotubes in Drug and Gene Delivery. Emerging Applications of Carbon Nanotubes in Drug and Gene Delivery 1 35 .
Junhui Tang, Jiawei Tang, Qiong Zhu, Yiyi Liao, Luhua Bai, Tingting Luo, Shuang Feng & Zheng Liu. (2022) A minimally invasive strategy to evacuate hematoma by synergy of an improved ultrasonic horn with urokinase: An in vitro study. Medical Physics 49:3, pages 1333-1343.
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Prabir Kumar Kulabhusan, Jaison Jeevanandam, Caleb Acquah & Michael K. Danquah. 2022. Combination Drug Delivery Approach as an Effective Therapy for Various Diseases. Combination Drug Delivery Approach as an Effective Therapy for Various Diseases 107 127 .
Yi-Ju Ho, Chih-Chung Huang, Ching-Hsiang Fan, Hao-Li Liu & Chih-Kuang Yeh. (2021) Ultrasonic technologies in imaging and drug delivery. Cellular and Molecular Life Sciences 78:17-18, pages 6119-6141.
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Yi Wang, Avani V. Pisapati, X. Frank Zhang & Xuanhong Cheng. (2021) Recent Developments in Nanomaterial‐Based Shear‐Sensitive Drug Delivery Systems. Advanced Healthcare Materials 10:13.
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Xiaoqian Su, Moumita Rakshit, Prativa Das, Ipshita Gupta, Dhiman Das, Manojit Pramanik, Kee Woei Ng & James Kwan. (2021) Ultrasonic Implantation and Imaging of Sound-Sensitive Theranostic Agents for the Treatment of Arterial Inflammation. ACS Applied Materials & Interfaces 13:21, pages 24422-24430.
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Robert T. Kleven, Kunal B. Karani, Nicole Hilvert, Samantha M. Ford, Karla P. Mercado-Shekhar, John M. Racadio, Marepalli B. Rao, Todd A. Abruzzo & Christy K. Holland. (2021) Accelerated sonothrombolysis with Definity in a xenographic porcine cerebral thromboembolism model. Scientific Reports 11:1.
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Annika Hess, James T. Thackeray, Kai C. Wollert & Frank M. Bengel. (2020) Radionuclide Image-Guided Repair of the Heart. JACC: Cardiovascular Imaging 13:11, pages 2415-2429.
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Claude Inserra, Gabriel Regnault, Sarah Cleve, Cyril Mauger & Alexander A. Doinikov. (2020) Acoustic microstreaming produced by nonspherical oscillations of a gas bubble. IV. Case of modes and . Physical Review E 102:4.
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Inés Beekers, Frits Mastik, Robert Beurskens, Phoei Ying Tang, Merel Vegter, Antonius F.W. van der Steen, Nico de Jong, Martin D. Verweij & Klazina Kooiman. (2020) High-Resolution Imaging of Intracellular Calcium Fluctuations Caused by Oscillating Microbubbles. Ultrasound in Medicine & Biology 46:8, pages 2017-2029.
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Lina Guan, Chunmei Wang, Xue Yan, Liyun Liu, Yanhong Li & Yuming Mu. (2020) A thrombolytic therapy using diagnostic ultrasound combined with RGDS-targeted microbubbles and urokinase in a rabbit model. Scientific Reports 10:1.
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Klazina Kooiman, Silke Roovers, Simone A.G. Langeveld, Robert T. Kleven, Heleen Dewitte, Meaghan A. O'Reilly, Jean-Michel Escoffre, Ayache Bouakaz, Martin D. Verweij, Kullervo Hynynen, Ine Lentacker, Eleanor Stride & Christy K. Holland. (2020) Ultrasound-Responsive Cavitation Nuclei for Therapy and Drug Delivery. Ultrasound in Medicine & Biology 46:6, pages 1296-1325.
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Cameron A.B. Smith & Constantin C. Coussios. (2020) Spatiotemporal Assessment of the Cellular Safety of Cavitation-Based Therapies by Passive Acoustic Mapping. Ultrasound in Medicine & Biology 46:5, pages 1235-1243.
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Amir Shamloo, Sina Ebrahimi, Ali Amani & Famida Fallah. (2020) Targeted Drug Delivery of Microbubble to Arrest Abdominal Aortic Aneurysm Development: A Simulation Study Towards Optimized Microbubble Design. Scientific Reports 10:1.
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Kirby R. Lattwein, Himanshu Shekhar, Joop J.P. Kouijzer, Willem J.B. van Wamel, Christy K. Holland & Klazina Kooiman. (2020) Sonobactericide: An Emerging Treatment Strategy for Bacterial Infections. Ultrasound in Medicine & Biology 46:2, pages 193-215.
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Patrick H. Kee, Melanie R. Moody, Shao-Ling Huang, Hyunggun Kim, Xing Yin, Tao Peng, Susan T. Laing, Melvin E. Klegerman, Mohammad H. Rahbar, Deborah Vela, Curtis Genstler, Kevin J. Haworth, Christy K. Holland & David D. McPherson. (2020) Stabilizing Peri-Stent Restenosis Using a Novel Therapeutic Carrier. JACC: Basic to Translational Science 5:1, pages 1-11.
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Qiong Zhu, Gang Dong, Zhiwei Wang, Lulu Sun, Shunji Gao & Zheng Liu. (2019) Intra-clot Microbubble-Enhanced Ultrasound Accelerates Catheter-Directed Thrombolysis for Deep Vein Thrombosis: A Clinical Study. Ultrasound in Medicine & Biology 45:9, pages 2427-2433.
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Robert T Kleven, Kunal B Karani, Nuria G Salido, Himanshu Shekhar, Kevin J Haworth, T Douglas Mast, Dawit G Tadesse & Christy K Holland. (2019) The effect of 220 kHz insonation scheme on rt-PA thrombolytic efficacy in vitro . Physics in Medicine & Biology 64:16, pages 165015.
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Bhavana Joshi & Abhijeet Joshi. 2019. Bioelectronics and Medical Devices. Bioelectronics and Medical Devices 241 260 .
Kyle T. Rich, Christy K. Holland, Marepalli B. Rao & T. Douglas Mast. (2018) Characterization of cavitation-radiated acoustic power using diffraction correction. The Journal of the Acoustical Society of America 144:6, pages 3563-3574.
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Paul Boulos, Franois Varray, Adrien Poizat, Alessandro Ramalli, Bruno Gilles, Jean-Christophe Bera & Christian Cachard. (2018) Weighting the Passive Acoustic Mapping Technique With the Phase Coherence Factor for Passive Ultrasound Imaging of Ultrasound-Induced Cavitation. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control 65:12, pages 2301-2310.
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Ilya Skachkov, Ying Luan, Sandra T. van Tiel, Antonius F. W. van der Steen, Nico de Jong, Monique R. Bernsen & Klazina Kooiman. (2018) SPIO labeling of endothelial cells using ultrasound and targeted microbubbles at diagnostic pressures. PLOS ONE 13:9, pages e0204354.
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Martin P. Stewart, Robert Langer & Klavs F. Jensen. (2018) Intracellular Delivery by Membrane Disruption: Mechanisms, Strategies, and Concepts. Chemical Reviews 118:16, pages 7409-7531.
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Yadong Shi, Wanyin Shi, Liang Chen & Jianping Gu. (2018) A systematic review of ultrasound-accelerated catheter-directed thrombolysis in the treatment of deep vein thrombosis. Journal of Thrombosis and Thrombolysis 45:3, pages 440-451.
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Kirby R. Lattwein, Himanshu Shekhar, Willem J. B. van Wamel, Tammy Gonzalez, Andrew B. Herr, Christy K. Holland & Klazina Kooiman. (2018) An in vitro proof-of-principle study of sonobactericide. Scientific Reports 8:1.
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Michael D. Gray, Erasmia Lyka & Constantin C. Coussios. (2018) Diffraction Effects and Compensation in Passive Acoustic Mapping. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control 65:2, pages 258-268.
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Peng Qin, Tao Han, Alfred C.H. Yu & Lin Xu. (2018) Mechanistic understanding the bioeffects of ultrasound-driven microbubbles to enhance macromolecule delivery. Journal of Controlled Release 272, pages 169-181.
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Nihan Güvener, Lia Appold, Federica de Lorenzi, Susanne K. Golombek, Larissa Y. Rizzo, Twan Lammers & Fabian Kiessling. (2017) Recent advances in ultrasound-based diagnosis and therapy with micro- and nanometer-sized formulations. Methods 130, pages 4-13.
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Ran Peng, Yang Luo, Zhangyong Li, Wei Wang & Yu Pang. (2017) Design of an ultrasonic physiotherapy system with pulse wave feedback control. Technology and Health Care 25, pages 305-315.
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Tuantuan Wang, Chuxiao Yuan, Bingyang Dai, Yang Liu, Mingxi Li, Zhenqiang Feng, Qing Jiang, Zhihong Xu, Ningwei Zhao, Ning Gu & Fang Yang. (2017) Click-Chemistry-Mediated Rapid Microbubble Capture for Acute Thrombus Ultrasound Molecular Imaging. ChemBioChem 18:14, pages 1364-1368.
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Klazina Kooiman, Tom van Rooij, Bin Qin, Frits Mastik, Hendrik J. Vos, Michel Versluis, Alexander L. Klibanov, Nico de Jong, Flordeliza S. Villanueva & Xucai Chen. (2017) Focal areas of increased lipid concentration on the coating of microbubbles during short tone-burst ultrasound insonification. PLOS ONE 12:7, pages e0180747.
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Shenwen Huang, Himanshu Shekhar & Christy K. Holland. (2017) Comparative lytic efficacy of rt-PA and ultrasound in porcine versus human clots. PLOS ONE 12:5, pages e0177786.
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Caleb Abshire, Hakm Y. Murad, Jaspreet S. Arora, James Liu, Sree Harsha Mandava, Vijay T. John, Damir B. Khismatullin & Benjamin R. Lee. (2017) Focused Ultrasound–Triggered Release of Tyrosine Kinase Inhibitor From Thermosensitive Liposomes for Treatment of Renal Cell Carcinoma. Journal of Pharmaceutical Sciences 106:5, pages 1355-1362.
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Algimantas Bubulis, Vida Garalienė, Vytautas Jurėnas, Jonas Navickas & Saulius Giedraitis. (2017) Effect of Low-Intensity Cavitation on the Isolated Human Thoracic Artery In Vitro. Ultrasound in Medicine & Biology 43:5, pages 1040-1047.
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Uche A. K. Chude-Okonkwo, Reza Malekian, B. T. Maharaj & Athanasios V. Vasilakos. (2017) Molecular Communication and Nanonetwork for Targeted Drug Delivery: A Survey. IEEE Communications Surveys & Tutorials 19:4, pages 3046-3096.
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Dario Carugo, Miles Aron, Erdinc Sezgin, Jorge Bernardino de la Serna, Marina K. Kuimova, Christian Eggeling & Eleanor Stride. (2017) Modulation of the molecular arrangement in artificial and biological membranes by phospholipid-shelled microbubbles. Biomaterials 113, pages 105-117.
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Julia Wang, Jonah A. Kaplan, Yolonda L. Colson & Mark W. Grinstaff. (2017) Mechanoresponsive materials for drug delivery: Harnessing forces for controlled release. Advanced Drug Delivery Reviews 108, pages 68-82.
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Jason L Raymond, Ying Luan, Tao Peng, Shao-Ling Huang, David D McPherson, Michel Versluis, Nico de Jong & Christy K Holland. (2016) Loss of gas from echogenic liposomes exposed to pulsed ultrasound. Physics in Medicine and Biology 61:23, pages 8321-8339.
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Yuqi Zhang, Jicheng Yu, Hunter N. Bomba, Yong Zhu & Zhen Gu. (2016) Mechanical Force-Triggered Drug Delivery. Chemical Reviews 116:19, pages 12536-12563.
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Tom van Rooij, Ilya Skachkov, Inés Beekers, Kirby R. Lattwein, Jason D. Voorneveld, Tom J.A. Kokhuis, Deep Bera, Ying Luan, Antonius F.W. van der Steen, Nico de Jong & Klazina Kooiman. (2016) Viability of endothelial cells after ultrasound-mediated sonoporation: Influence of targeting, oscillation, and displacement of microbubbles. Journal of Controlled Release 238, pages 197-211.
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Aris Xie, Melinda D. Wu, Gabriella Cigarroa, J. Todd Belcik, Azzdine Ammi, Federico Moccetti & Jonathan R. Lindner. (2016) Influence of DNA-Microbubble Coupling on Contrast Ultrasound–Mediated Gene Transfection in Muscle and Liver. Journal of the American Society of Echocardiography 29:8, pages 812-818.
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Madhuvanthi A. Kandadai, Prithviraj Mukherjee, Himanshu Shekhar, George J. Shaw, Ian Papautsky & Christy K. Holland. (2016) Microfluidic manufacture of rt-PA -loaded echogenic liposomes. Biomedical Microdevices 18:3.
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Xucai Chen, Jianjun Wang, John J. Pacella & Flordeliza S. Villanueva. (2016) Dynamic Behavior of Microbubbles during Long Ultrasound Tone-Burst Excitation: Mechanistic Insights into Ultrasound-Microbubble Mediated Therapeutics Using High-Speed Imaging and Cavitation Detection. Ultrasound in Medicine & Biology 42:2, pages 528-538.
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Kevin J. Haworth, Jason L. Raymond, Kirthi Radhakrishnan, Melanie R. Moody, Shao-Ling Huang, Tao Peng, Himanshu Shekhar, Melvin E. Klegerman, Hyunggun Kim, David D. McPherson & Christy K. Holland. (2016) Trans-Stent B-Mode Ultrasound and Passive Cavitation Imaging. Ultrasound in Medicine & Biology 42:2, pages 518-527.
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Francois T. H. Yu, Xucai Chen, Jianjun Wang, Bin Qin & Flordeliza S. Villanueva. (2015) Low Intensity Ultrasound Mediated Liposomal Doxorubicin Delivery Using Polymer Microbubbles. Molecular Pharmaceutics 13:1, pages 55-64.
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Kenneth B. Bader, Guillaume Bouchoux & Christy K. Holland. 2016. Therapeutic Ultrasound. Therapeutic Ultrasound 339 362 .
Natalya Rapoport. 2016. Therapeutic Ultrasound. Therapeutic Ultrasound 221 241 .
Renae Waters, Ryan Maloney, Sudhir H. Ranganath, Hsin-Yi Hsieh & Arghya Paul. 2016. Microscale Technologies for Cell Engineering. Microscale Technologies for Cell Engineering 269 289 .
Kirthi Radhakrishnan, Kevin J. Haworth, Tao Peng, David D. McPherson & Christy K. Holland. (2015) Loss of Echogenicity and Onset of Cavitation from Echogenic Liposomes: Pulse Repetition Frequency Independence. Ultrasound in Medicine & Biology 41:1, pages 208-221.
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Kenneth B. Bader, Matthew J. Gruber & Christy K. Holland. (2015) Shaken and Stirred: Mechanisms of Ultrasound-Enhanced Thrombolysis. Ultrasound in Medicine & Biology 41:1, pages 187-196.
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Ilya Skachkov, Ying Luan, Antonius F.W. van der Steen, Nico de Jong & Klazina Kooiman. (2014) Targeted microbubble mediated sonoporation of endothelial cells in vivo. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control 61:10, pages 1661-1667.
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Klazina Kooiman, Tom J. A. Kokhuis, Tom van Rooij, Ilya Skachkov, Alex Nigg, Johannes G. Bosch, Antonius F. W. van der Steen, Wiggert A. van Cappellen & Nico de Jong. (2014) DSPC or DPPC as main shell component influences ligand distribution and binding area of lipid‐coated targeted microbubbles. European Journal of Lipid Science and Technology 116:9, pages 1217-1227.
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Xing Hua, Lina Zhou, Ping Liu, Yun He, Kaibin Tan, Qinghai Chen, Yuejuan Gao & Yunhua Gao. (2014) In vivo thrombolysis with targeted microbubbles loading tissue plasminogen activator in a rabbit femoral artery thrombus model. Journal of Thrombosis and Thrombolysis 38:1, pages 57-64.
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Himanshu Shekhar, Ivy Awuor, Keri Thomas, Joshua J. Rychak & Marvin M. Doyley. (2014) The Delayed Onset of Subharmonic and Ultraharmonic Emissions from a Phospholipid-Shelled Microbubble Contrast Agent. Ultrasound in Medicine & Biology 40:4, pages 727-738.
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Jason L. Raymond, Kevin J. Haworth, Kenneth B. Bader, Kirthi Radhakrishnan, Joseph K. Griffin, Shao-Ling Huang, David D. McPherson & Christy K. Holland. (2014) Broadband Attenuation Measurements of Phospholipid-Shelled Ultrasound Contrast Agents. Ultrasound in Medicine & Biology 40:2, pages 410-421.
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Zhi-Yi Chen, Yi-Xiang Wang, Yan Lin, Jin-Shan Zhang, Feng Yang, Qiu-Lan Zhou & Yang-Ying Liao. (2014) Advance of Molecular Imaging Technology and Targeted Imaging Agent in Imaging and Therapy. BioMed Research International 2014, pages 1-12.
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Scott J. Satinover, Jacob D. Dove & Mark A. Borden. (2014) Single-Particle Optical Sizing of Microbubbles. Ultrasound in Medicine & Biology 40:1, pages 138-147.
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Fang Yang, Qing Wang, Zhuxiao Gu, Kun Fang, Gerard Marriott & Ning Gu. (2013) Silver Nanoparticle-Embedded Microbubble as a Dual-Mode Ultrasound and Optical Imaging Probe. ACS Applied Materials & Interfaces 5:18, pages 9217-9223.
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Kirthi Radhakrishnan, Kenneth B Bader, Kevin J Haworth, Jonathan A Kopechek, Jason L Raymond, Shao-Ling Huang, David D McPherson & Christy K Holland. (2013) Relationship between cavitation and loss of echogenicity from ultrasound contrast agents. Physics in Medicine and Biology 58:18, pages 6541-6563.
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Ali H Dhanaliwala, Johnny L Chen, Joseph P Kilroy, Linsey C Phillips, Adam J Dixon, Alexander L Klibanov, Brian R Wamhoff & John A Hossack. (2013) Intravascular ultrasound-based imaging and drug delivery. Intravascular ultrasound-based imaging and drug delivery.

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