Microbubble-mediated ultrasound drug-delivery and therapeutic monitoring

References

• Moonen C, Lentacker I. (Theme Editors). Ultrasound assisted drug delivery. Adv Drug Deliv Rev. 2014;72:1–154.
   PubMed Web of Science ®Google Scholar
• Becher H, Burns PN. Handbook of contrast echocardiography, Springer. Berlin, Germany: Springer; 2000.
   Google Scholar
• Simpson DH, Chin CT, Burns PN. Pulse inversion Doppler: a new method for detecting nonlinear echoes from microbubble contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control. 1999;46:372–382.
   PubMed Web of Science ®Google Scholar
• Harvey CJ, Blomley MJ, Eckersley RJ, et al. Pulse-inversion mode imaging of liver specific microbubbles: improved detection of sub centimetre metastases. Lancet. 2000;355:807–808.
   PubMed Web of Science ®Google Scholar
• Shapiro G, Wong AW, Bez M, et al. Multi-parameter evaluation of in vivo gene delivery using ultrasound-guided, microbubble-enhanced sonoporation. J Control Release. 2016;223:157–164.
   PubMed Web of Science ®Google Scholar
• Wang S, Olumolade O, Sun T, et al. Non-invasive, neuron-specific gene therapy can be facilitated by focused ultrasound and recombinant adeno-associated virus. Gene Ther. 2015;22:104–110.
   PubMed Web of Science ®Google Scholar
• Schneider M. Characteristics of SonoVuetrade mark. Echocardiography. 1999;16:743–746.
   PubMed Web of Science ®Google Scholar
• Lindner JR. Microbubbles in medical imaging: current applications and future directions. Nat Rev Drug Discov. 2004;3:527–533.
   PubMed Web of Science ®Google Scholar
• Klibanov AL. Targeted delivery of gas-filled microspheres, contrast agents for ultrasound imaging. Adv Drug Deliv Rev. 1999;37:139–157.
   PubMed Web of Science ®Google Scholar
• Yeh JSM, Sennoga CA, McConnell E, et al. A targeting microbubble for ultrasound molecular imaging. PLoS One. 2015;10:e0129681.
   PubMed Web of Science ®Google Scholar
• Escoffre J, Mannaris C, Geers B, et al. Doxorubicin liposome-loaded microbubbles for contrast imaging and ultrasound-triggered drug delivery. IEEE Trans Ultrason Ferroelectr Freq Control. 2013;60:78–87.
   PubMed Web of Science ®Google Scholar
• Deckers R, Rome C, Moonen CTW. The role of ultrasound and magnetic resonance in local drug delivery. J Magn Reson Imaging. 2008;27:400–409.
   PubMed Web of Science ®Google Scholar
• Blomley MJ, Albrecht T, Cosgrove DO, et al. Improved imaging of liver metastases with stimulated acoustic emission in the late phase of enhancement with the US contrast agent SH U 508A: early experience. Radiology. 1999;210:409–416.
   PubMed Web of Science ®Google Scholar
• Apfel RE, Holland CK. Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound Med Biol. 1991;17:179–185.
   PubMed Web of Science ®Google Scholar
• Alter J, Sennoga CA, Lopes DM, et al. Microbubble stability is a major determinant of the efficiency of ultrasound and microbubble mediated in vivo gene transfer. Ultrasound Med Biol. 2009;35:976–984.
   PubMed Web of Science ®Google Scholar
• Shohet RV, Chen S, Zhou YT, et al. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation. 2000;101:2554–2556.
   PubMed Web of Science ®Google Scholar
• Schumann PA, Christiansen JP, Quigley RM, et al. Targeted-microbubble binding selectively to GPIIb IIIa receptors of platelet thrombi. Invest Radiol. 2002;37:587–593.
   PubMed Web of Science ®Google Scholar
• Wu W, Wang Y, Shen S, et al. In vivo ultrasound molecular imaging of inflammatory thrombosis in arteries with cyclic Arg-Gly-Asp–modified microbubbles targeted to glycoprotein IIb/IIIa. Invest Radiol. 2013;48:803–812.
   PubMed Web of Science ®Google Scholar
• Caskey CF, Hu X, Ferrara KW. Leveraging the power of ultrasound for therapeutic design and optimization. J Control Release. 2011 Dec 20;156(3):297–306.
   PubMed Web of Science ®Google Scholar
• Correas J-M, Bridal L, Lesavre A, et al. Ultrasound contrast agents: properties, principles of action, tolerance, and artifacts. Eur Radiol. 2001;11:1316–1328.
   PubMed Web of Science ®Google Scholar
• Bartolotta TV, Midiri M, Galia M, et al. Characterization of benign hepatic tumors arising in fatty liver with SonoVue and pulse inversion US. Abdom Imaging. 2007;32:84–91.
   PubMedGoogle Scholar
• Patel DN, Bloch SH, Dayton PA, et al. Acoustic signatures of submicron contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control. 2004 Mar;51(3):293–301.
   PubMed Web of Science ®Google Scholar
• Rasmussen JH, Du Y, Jensen JA. Third harmonic imaging using pulse inversion. IEEE Int Ultrason Symp. 2011;2001:2269–2272.
   Google Scholar
• Wilson SR, Burns PN. Liver mass evaluation with ultrasound: the impact of microbubble contrast agents and pulse inversion imaging. Semin Liver Dis. 2001;21:147–160.
   PubMed Web of Science ®Google Scholar
• Mor-Avi V, Caiani E, Collins K, et al. Quantitative analysis of myocardial perfusion and regional left ventricular function from contrast-enhanced power modulation images. Comput Cardiol. 2001;28:97–100.
   Google Scholar
• Brock-Fisher GA, Poland MD, Rafter PG. Means for increasing sensitivity in non-linear ultrasound imaging systems. US5577505A (1996)
   Google Scholar
• Eckersley RJ, Chin CT, Burns PN. Optimizing phase and amplitude modulation schemes for imaging microbubble contrast agents at low acoustic power. Ultrasound Med Biol. 2005;31:213–219.
   PubMed Web of Science ®Google Scholar
• Haider B, Chiao RY. Higher order nonlinear ultrasonic imaging. IEEE Ultrason Symp Proceedings Int Symp. 1999;1999:1527–1531.
   Google Scholar
• Phillips PJ. Contrast pulse sequences (CPS): imaging nonlinear microbubbles. IEEE Ultrason Symp Proceedings Int Symp. 2001;2001:1739–1745.
   Google Scholar
• Tiemann K, Lohmeier S, Kuntz S, et al. Real-time contrast echo assessment of myocardial perfusion at low emission power: first experimental and clinical results using power pulse inversion imaging. Echocardiography. 1999;16:799–809.
   PubMed Web of Science ®Google Scholar
• Lammertink BHA, Bos C, Deckers R, et al. Sonochemotherapy: from bench to bedside. Front Pharmacol. 2015;6:138.
   PubMed Web of Science ®Google Scholar
• Novell A, Sennoga CA, Escoffre JM, et al. Evaluation of chirp reversal power modulation sequence for contrast agent imaging. Phys Med Biol. 2014;59:5101–5117.
   PubMed Web of Science ®Google Scholar
• Forsberg F, Piccoli CW, Merton DA, et al. Breast lesions: imaging with contrast-enhanced subharmonic US-initial experience. Radiology. 2007;244:718–726.
   PubMed Web of Science ®Google Scholar
• Chomas JE, Dayton P, May D, et al. Non-destructive subharmonic imaging. IEEE Trans Ultrason Ferroelectr Freq Control. 2002;49:883–892.
   PubMed Web of Science ®Google Scholar
• Gessner RC, Frederick CB, Foster FS, et al. Acoustic angiography: a new imaging modality for assessing microvasculature architecture. Int J Biomed Imaging. 2013;2013:1–9.
   Google Scholar
• Bouakaz A, Frigstad S, Ten CFJ, et al. Super harmonic imaging: a new imaging technique for improved contrast detection. Ultrasound Med Biol. 2002;28:59–68.
   PubMed Web of Science ®Google Scholar
• Fan C-H, Ting C-Y, Liu H-L, et al. Antiangiogenic-targeting drug-loaded microbubbles combined with focused ultrasound for glioma treatment. Biomaterials. 2013;34:2142–2155.
   PubMed Web of Science ®Google Scholar
• Burke CW, Alexander E, Timbie K, et al. Ultrasound-activated agents comprised of 5FU-bearing nanoparticles bonded to microbubbles inhibit solid tumour growth and improve survival. Mol Ther. 2014;22:321–328.
   PubMed Web of Science ®Google Scholar
• Sasaki N, Kudo N, Nakamura K, et al. Ultrasound image-guided therapy enhances antitumor effect of cisplatin. J Med Ultrason. 2013;41:11–21.
   PubMed Web of Science ®Google Scholar
• Shpak O, Verweij M, De Jong N, et al. Droplets, bubbles and ultrasound interactions. Adv Exp Med Biol. 2016;880:157–174.
   PubMed Web of Science ®Google Scholar
• Doinikov AA, Bouakaz A. Acoustic microstreaming around an encapsulated particle. J Acoust Soc Am. 2010;127:1218–1227.
   PubMed Web of Science ®Google Scholar
• Postema M, van Wamel A, Ten Cate FJ, et al. High-speed photography during ultrasound illustrates potential therapeutic applications of microbubbles. Med Phys. 2005;32:3707–3711.
   PubMed Web of Science ®Google Scholar
• Kooiman K, Emmer M, Foppen-Harteveld M, et al. Increasing the endothelial layer permeability through ultrasound-activated microbubbles. IEEE Trans Biomed Eng. 2010;57:29–32.
   PubMed Web of Science ®Google Scholar
• Derieppe M, Rojek K, Escoffre J-M, et al. Recruitment of endocytosis in sonopermeabilization-mediated drug delivery: a real-time study. Phys Biol. 2015;12:046010.
   PubMed Web of Science ®Google Scholar
• Zeghimi A, Escoffre J-M, Bouakaz A. Role of endocytosis in sonoporation-mediated membrane permeabilization and uptake of small molecules: a electron microscopy study. Phys Biol. 2015;12:066007.
   PubMed Web of Science ®Google Scholar
• Meijering BDM, Juffermans LJM, van Wamel A, et al. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ Res. 2009;104:679–687.
   PubMed Web of Science ®Google Scholar
• Tran TA, Roger S, Le Guennec JY, et al. Effect of ultrasound-activated microbubbles on the cell electrophysiological properties. Ultrasound Med Biol. 2007;33:158–163.
   PubMed Web of Science ®Google Scholar
• Bettinger T, Tranquart F. Design of microbubbles for gene/drug delivery. Adv Exp Med Biol. 2016;880:191–204.
   PubMed Web of Science ®Google Scholar
• Pu C, Chang S, Sun J, et al. Ultrasound-mediated destruction of LHRHa-targeted and paclitaxel-loaded lipid microbubbles for the treatment of intraperitoneal ovarian cancer xenografts. Mol Pharm. 2014;11:49–58.
   PubMed Web of Science ®Google Scholar
• Sirsi SR, Hernandez SL, Zielinski L, et al. Polyplex-microbubble hybrids for ultrasound-guided plasmid DNA delivery to solid tumours. J Control Release. 2012;157:224–234.
   PubMed Web of Science ®Google Scholar
• Matsuo M, Yamaguchi K, Feril LB, et al. Synergistic inhibition of malignant melanoma proliferation by melphalan combined with ultrasound and microbubbles. Ultrason Sonochem. 2011;18:1218–1224.
   PubMed Web of Science ®Google Scholar
• Song J, Chappell JC, Qi M, et al. Influence of injection site, microvascular pressure and ultrasound variables on microbubble-mediated delivery of microspheres to muscle. J Am Coll Cardiol. 2002;39:726–731.
   PubMed Web of Science ®Google Scholar
• Tzu-Yin W, Wilson KE, Machtaler S, et al. Ultrasound and microbubble guided drug delivery: mechanistic understanding and clinical implications. Curr Pharm Biotechnol. 2013;14:743–752.
   PubMed Web of Science ®Google Scholar
• Aryal M, Vykhodtseva N, Zhang Y-Z, et al. Multiple sessions of liposomal doxorubicin delivery via focused ultrasound mediated blood-brain barrier disruption: a safety study. J Control Release. 2015;204:60–69.
   PubMed Web of Science ®Google Scholar
• Escoffre J-M, Novell A, Serrière S, et al. Irinotecan delivery by microbubble-assisted ultrasound: in vitro validation and a pilot preclinical study. Mol Pharm. 2013;10:2667–2675.
   PubMed Web of Science ®Google Scholar
• Yan F, Li L, Deng Z, et al. Paclitaxel-liposome-microbubble complexes as ultrasound-triggered therapeutic drug delivery carriers. J Control Release. 2013;166:246–255.
   PubMed Web of Science ®Google Scholar
• Xie A, Belcik T, Qi Y, et al. Ultrasound-mediated vascular gene transfection by cavitation of endothelial-targeted cationic microbubbles. JACC Cardiovasc Imaging. 2012;5:1253–1262.
   PubMed Web of Science ®Google Scholar
• Escoffre J-M, Deckers R, Bos C, et al. Bubble-assisted ultrasound: application in immunotherapy and vaccination. Adv Exp Med Biol. 2016;880:243–261.
   PubMed Web of Science ®Google Scholar
• Jordão JF, Ayala-Grosso CA, Markham K, et al. Antibodies targeted to the brain with image-guided focused ultrasound reduces amyloid-beta plaque load in the TgCRND8 mouse model of Alzheimer’s disease. PLoS One. 2010;5:e10549.
   PubMed Web of Science ®Google Scholar
• Raymond SB, Treat LH, Dewey JD, et al. Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer’s disease mouse models. PLoS One. 2008;3:e2175.
   PubMed Web of Science ®Google Scholar
• McDannold N, Arvantis CD, Vykhodtseva N, et al. Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques. Cancer Res. 2012;72:3652–3663.
   PubMed Web of Science ®Google Scholar
• Kobus T, Vykhodtseva N, Pilatou M, et al. Safety validation of repeated blood-brain barrier disruption using focused ultrasound. Ultrasound Med Biol. 2016;42:481–492.
   PubMed Web of Science ®Google Scholar
• Downs ME, Buch A, Sierra C, et al. Long-term safety of repeated blood-brain barrier opening via focused ultrasound with microbubbles in non-human primates performing a cognitive task. PLoS One. 2015;10:e0125911.
   PubMed Web of Science ®Google Scholar
• Leong-Poi H. Contrast ultrasound and targeted microbubbles: diagnostic and therapeutic applications in progressive diabetic nephropathy. Semin Nephrol. 2012;32:494–504.
   PubMed Web of Science ®Google Scholar
• Castle J, Feinstein SB. Drug and gene delivery using sonoporation for cardiovascular disease. Adv Exp Med Biol. 2016;880:331–338.
   PubMed Web of Science ®Google Scholar
• Dixon AJ, Kilroy JP, Dhanaliwala AH, et al. Microbubble-mediated intravascular ultrasound imaging and therapy. IEEE Trans Ultrason Ferroelectr Freq Control. 2015;62:1674–1685.
   PubMed Web of Science ®Google Scholar
• Wang TY, Choe JW, Pu K, et al. Ultrasound-guided delivery of microRNA loaded nanoparticles into cancer. J Control Release. 2015;203:99–108.
   PubMed Web of Science ®Google Scholar
• Down ME, Buch A, Karakatsani ME, et al. Blood-brain barrier opening in behaving non-human primates via focused ultrasound with systemically administered microbubbles. Sci Rep. 2015;5:15076.
   PubMed Web of Science ®Google Scholar
• Wu J, Xie F, Kumar T, et al. Improved sonothrombolysis from a modified diagnostic transducer delivering impulses containing a longer pulse duration. Ultrasound Med Biol. 2014;40:1545–1553.
   PubMed Web of Science ®Google Scholar
• Kotopoulis S, Dimcevski G, Helge Gilja O, et al. Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med Phys. 2013;40:072902.
   PubMed Web of Science ®Google Scholar
• Kutty S, Xie F, Gao S, et al. Sonothrombolysis of intra-catheter aged venous thrombi using microbubble enhancement and guided three-dimensional ultrasound pulses. J Am Soc Echocardiogr. 2010 Sep;23(9):1001–1006.
   PubMed Web of Science ®Google Scholar
• The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med. 1995;333:1581–1588.
   PubMed Web of Science ®Google Scholar
• Kutty S, Wu J, Hammel JM, et al. Microbubble mediated thrombus dissolution with diagnostic ultrasound for the treatment of chronic venous thrombi. PLoS One. 2012;7(12):e51453.
   PubMed Web of Science ®Google Scholar
• Tachibana K, Tachibana S. Albumin microbubble echo-contrast material as an enhancer for ultrasound accelerated thrombolysis. Circulation. 1995;92:1148–1150.
   PubMed Web of Science ®Google Scholar
• Lauer CG, Burge R, Tang DB, et al. Effect of ultrasound on tissue-type plasminogen activator-induced thrombolysis. Circulation. 1992;86:1257–1264.
   PubMed Web of Science ®Google Scholar
• Datta S, Coussios CC, Ammi AY, et al. Ultrasound-enhanced thrombolysis using definity as a cavitation nucleation agent. Ultrasound Med Biol. 2008;34:1421–1433.
   PubMed Web of Science ®Google Scholar
• Rooney JA. Hemolysis near an ultrasonically pulsating gas bubble. Science. 1970;169:869–871.
   PubMed Web of Science ®Google Scholar
• Petit B, Bohren Y, Gaud E, et al. Sonothrombolysis: the contribution of stable and inertial cavitation to clot lysis. Ultrasound Med Biol. 2015;41:1402–1410.
   PubMed Web of Science ®Google Scholar
• Auboire L, Tranquart F, Ossant F, et al. Impact of sonothrombolysis on in vitro blood clot: pictographic validation with electron microscopy. Ultraschall Med. 2015. [cited 2015 Sep 2]. DOI:10.1055/s-0035-1553322
   PubMed Web of Science ®Google Scholar
• Luan Y, Lajoinie G, Gelderblom E, et al. Lipid shedding from single oscillating microbubbles. Ultrasound Med Biol. 2014;40:1834–1846.
   PubMed Web of Science ®Google Scholar
• Miao H, Gracewski SM, Dalecki D. Ultrasonic excitation of a bubble inside a deformable tube: implications for ultrasonically induced hemorrhage. J Acoust Soc Am. 2008;124:2374–2384.
   PubMed Web of Science ®Google Scholar
• Skyba DM, Price RJ, Linka AZ, et al. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation. 1998;98:290–293.
   PubMed Web of Science ®Google Scholar
• Hua X, Zhou L, Liu P, et al. In vivo thrombolysis with targeted microbubbles loading tissue plasminogen activator in a rabbit femoral artery thrombus model. J Thromb Thrombolysis. 2014;38:57–64.
   PubMed Web of Science ®Google Scholar
• Larrue V, Viguier A, Arnaud C, et al. Transcranial ultrasound combined with intravenous microbubbles and tissue plasminogen activator for acute ischemic stroke: a randomized controlled study. Stroke. 2007;38:472.
   Web of Science ®Google Scholar
• Alexandrov AV, Mikulik R, Ribo M, et al. A pilot randomized clinical safety study of sonothrombolysis augmentation with ultrasound-activated perflutren-lipid microspheres for acute ischemic stroke. Stroke. 2008;39:1464–1469.
   PubMed Web of Science ®Google Scholar
• Perren F, Loulidi J, Poglia D, et al. Microbubble potentiated transcranial duplex ultrasound enhances IV thrombolysis in acute stroke. J Thromb Thrombolysis. 2008;25:219–223.
   PubMed Web of Science ®Google Scholar
• Nicoli FJL, Squarcioni C, Grimaud L, et al. Microbubble administration during prolonged 2 MHz TCD improves recanalization and long-term functional outcome in acute stroke patients treated with iv thrombolysis for isolated mca m1 occlusion. Cerebro Vasc Dis. 2010;29:Q39.
   Google Scholar
• Nacu A, Kvistad CE, Logallo N, et al. A pragmatic approach to sonothrombolysis in acute ischaemic stroke: the Norwegian randomised controlled sonothrombolysis in acute stroke study (NOR-SASS). BMC Neurol. 2015;15:110–122.
   PubMed Web of Science ®Google Scholar
• Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285:1182–1186.
   PubMed Web of Science ®Google Scholar
• Lamuraglia M, Bridal SL, Santinet M, et al. Clinical relevance of contrast-enhanced ultrasound in monitoring anti-angiogenic therapy of cancer: current status and perspectives. Crit Rev Oncol Hematol. 2010;73:202–212.
   PubMed Web of Science ®Google Scholar
• Therasse P, Arbuck SG, Eisenhauer EA, et al. New guidelines to evaluate the response to treatment in solid tumors. European organization for research and treatment of cancer, national cancer institute of the United States, national cancer institute of Canada. J Natl Cancer Inst. 2000;92:205–216.
   PubMed Web of Science ®Google Scholar
• Smith AD, Lieber ML, Shah SN, et al. Assessing tumor response and detecting recurrence in metastatic renal cell carcinoma on targeted therapy: importance of size and attenuation on contrast-enhanced CT. AJR Am J Roentgenol. 2010;194:157–165.
   PubMed Web of Science ®Google Scholar
• Dietrich CF, Averkiou MA, Correas JM, et al. An EFSUMB introduction into Dynamic Contrast-Enhanced Ultrasound (DCE-US) for quantification of tumour perfusion. Ultraschall Med. 2012;33:344–351.
   PubMed Web of Science ®Google Scholar
• Tranquart F, Mercier L, Frinking P, et al. Perfusion quantification in contrast-enhanced ultrasound (CEUS)–ready for research projects and routine clinical use. Ultraschall Med. 2012;33:S31–8.
   PubMed Web of Science ®Google Scholar
• Williams R, Hudson JM, Lloyd BA, et al. Dynamic microbubble contrast-enhanced US to measure tumor response to targeted therapy: a proposed clinical protocol with results from renal cell carcinoma patients receiving antiangiogenic therapy. Radiology. 2011;260:581–590.
   PubMed Web of Science ®Google Scholar
• Lassau N, Koscielny S, Chami L, et al. Advanced hepatocellular carcinoma: early evaluation of response to bevacizumab therapy at dynamic contrast-enhanced US with quantification–preliminary results. Radiology. 2011;258:291–300.
   PubMed Web of Science ®Google Scholar
• Lassau N, Bonastre J, Kind M, et al. Validation of dynamic contrast-enhanced ultrasound in predicting outcomes of antiangiogenic therapy for solid tumors: the French multicenter support for innovative and expensive techniques study. Invest Radiol. 2014;49:794–800.
   PubMed Web of Science ®Google Scholar
• Piscaglia F, Nolsøe C, Dietrich C, et al. The EFSUMB guidelines and recommendations on the clinical practice of Contrast-Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med. 2012;33:33–59.
   PubMed Web of Science ®Google Scholar
• Anaye A, Perrenoud G, Rognin N. Differentiation of focal liver lesions: usefulness of parametric imaging with contrast-enhanced US. Radiology. 2011;261:300–310.
   PubMed Web of Science ®Google Scholar
• Yu T, Zhang Y, He H, et al. Anticancer potency of cytotoxic drugs after exposure to high-intensity focused ultrasound in the presence of microbubbles and hematoporphyrin. Mol Pharm. 2011;8:1408–1415.
   PubMed Web of Science ®Google Scholar
• Ojha T, Rizzo L, Storm G, et al. Image-guided drug delivery: preclinical applications and clinical translation. Expert Opin Drug Deliv. 2015;12:1203–1207.
   PubMed Web of Science ®Google Scholar
• Aw MS, Paniwnyk L, Losic D. The progressive role of acoustic cavitation for non-invasive therapies, contrast imaging and blood-tumor permeability enhancement. Expert Opin Drug Deliv. 2016;13:1383–1396.
   PubMed Web of Science ®Google Scholar
• Grundy M, Coussios C, Carlisle R. Advances in systemic delivery of anti-cancer agents for the treatment of metastatic cancer. Expert Opin Drug Deliv. 2016;13:999–1013.
   PubMed Web of Science ®Google Scholar
• Goins B, Phillips WT, Bao A. Strategies for improving the intratumoral distribution of liposomal drugs in cancer therapy. Expert Opin Drug Deliv. 2016;13:873–889.
   PubMed Web of Science ®Google Scholar
• Liu HL, Jan CK, Chu PC, et al. Design and experimental evaluation of a 256-channel dual-frequency ultrasound phased-array system for transcranial blood-brain barrier opening and brain drug delivery. IEEE Trans Biomed Eng. 2014;61:1350–1360.
   PubMed Web of Science ®Google Scholar
• Shih CP, Chen HC, Chen HK, et al. Ultrasound-aided microbubbles facilitate the delivery of drugs to the inner ear via the round window membrane. J Control Release. 2013;167:167–174.
   PubMed Web of Science ®Google Scholar
• Xie F, Boska MD, Lof J, et al. Effects of transcranial ultrasound and intravenous microbubbles on blood brain barrier permeability in a large animal model. Ultrasound Med Biol. 2008;34:2028–2034.
   PubMed Web of Science ®Google Scholar
• Horodyckid C, Canney M, Vignot A, et al. A. Safe long-term repeated disruption of the blood-brain barrier using an implantable ultrasound device: a multiparametric study in a primate model. J Neurosurg. 2016;10:1–11.
   Web of Science ®Google Scholar
• Wang F, Cheng Y, Mei J, et al. Focused ultrasound microbubble destruction-mediated changes in blood-brain barrier permeability assessed by contrast-enhanced magnetic resonance imaging. J Ultrasound Med. 2009;28(11):1501–1509.
   PubMed Web of Science ®Google Scholar