An overview of the influence of therapeutic ultrasound exposures on the vasculature: High intensity ultrasound and microbubble-mediated bioeffects

References

• Fowlkes JB, Abramowicz JS, Church CC, Holland CK, Miller DL, O’Brien WD, et al. American institute of ultrasound in medicine consensus report on potential bioeffects of diagnostic ultrasound. J Ultrasound Med 2008;27:503–15
   PubMed Web of Science ®Google Scholar
• Dalecki D. Mechanical bioeffects of ultrasound. Ann Rev Biomed Eng 2004;6:229–48
   PubMed Web of Science ®Google Scholar
• Hynynen K, Chung AH, Colucci V, Jolesz FA. Potential adverse effects of high-intensity focused ultrasound exposure on blood vessels in vivo. Ultrasound Med Biol 1996;22:193–201
   PubMed Web of Science ®Google Scholar
• Vaezy S, Martin R, Kaczkowski P, Keilman G, Goldman B, Yaziji H, et al. Use of high-intensity focused ultrasound to control bleeding. J Vasc Surg 1999;29:533–42
   PubMed Web of Science ®Google Scholar
• Shaw CJ, ter Haar GR, Rivens IH, Giussani DA, Lees CC. Pathophysiological mechanisms of high-intensity focused ultrasound-mediated vascular occlusion and relevance to non-invasive fetal surgery. J R Soc Interface 2014;11. Article ID: 20140029
   PubMed Web of Science ®Google Scholar
• Kooiman K, Vos HJ, Versluis M, de Jong N. Acoustic behavior of microbubbles and implications for drug delivery. Adv Drug Del Rev 2014;72:28–48
   PubMed Web of Science ®Google Scholar
• Bakay L, Hueter TF, Ballantine HT, Sosa D. Ultrasonically produced changes in the blood–brain barrier. AMA Arch NeurPsych 1956;76:457–67
   PubMedGoogle Scholar
• Skyba DM, Price RJ, Linka AZ, Skalak TC, Kaul S. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation 1998;98:290–3
   PubMed Web of Science ®Google Scholar
• Fallon JT, Eggleton RC, Stehbens WE. Effect of ultrasound on arteries. Arch Pathol 1972;94:380–8
   PubMedGoogle Scholar
• Hynynen K, Colucci V, Chung A, Jolesz F. Noninvasive arterial occlusion using MRI-guided focused ultrasound. Ultrasound Med Biol 1996;22:1071–7
   PubMed Web of Science ®Google Scholar
• Nyborg WL. Acoustic streaming. In: Mason WP, ed. Physical acoustics: Principles and methods. 1. New York: Academic Press, 1964, pp: 265–331
   Google Scholar
• Konofagou EE, Hynynen K. Localized harmonic motion imaging: Theory, simulations and experiments. Ultrasound Med Biol 2003;29:1405–13
   PubMed Web of Science ®Google Scholar
• Lizzi FL, Muratore R, Deng CX, Ketterling JA, Alam SK, Mikaelian S, et al. Radiation-force technique to monitor lesions during ultrasonic therapy. Ultrasound Med Biol 2003;29:1593–605
   PubMed Web of Science ®Google Scholar
• Hynynen K. The threshold for thermally significant cavitation in dog thigh muscle in vivo. Ultrasound Med Biol 1991;17:157–69
   PubMed Web of Science ®Google Scholar
• Holland CK, Deng CX, Apfel RE, Alderman JL, Fernandez LA, Taylor KJW. Direct evidence of cavitation in vivo from diagnostic ultrasound. Ultrasound Med Biol 1996;22:917–25
   PubMed Web of Science ®Google Scholar
• Ter Haar G, Coussios C. High intensity focused ultrasound: Physical principles and devices. Int J Hyperthermia 2007;23:89–104
   PubMed Web of Science ®Google Scholar
• Clarke RL, ter Haar GR. Temperature rise recorded during lesion formation by high-intensity focused ultrasound. Ultrasound Med Biol 1997;23:299–306
   PubMed Web of Science ®Google Scholar
• Leighton TG. The Acoustic Bubble. London: Academic Press, 1994
   Google Scholar
• Prosperetti A. Nonlinear oscillations of gas-bubbles in liquids – Transient solutions and connection between subharmonic signal and cavitation. J Acoust Soc Am 1975;57:810–21
   Web of Science ®Google Scholar
• Suslick KS, Flannigan DJ. Inside a collapsing bubble: Sonoluminescence and the conditions during cavitation. Ann Rev Phys Chem 2008;59:659–83
   PubMed Web of Science ®Google Scholar
• Roberts WW, Hall TL, Ives K, Wolf JS, Fowlkes JB, Cain CA. Pulsed cavitational ultrasound: A noninvasive technology for controlled tissue ablation (histotripsy) in the rabbit kidney. J Urol 2006;175:734–8
   PubMed Web of Science ®Google Scholar
• Coleman AJ SJ, Crum LA, Dyson M. Acoustic cavitation generated by an extracorporeal shockwave lithotripter. Ultrasound Med Biol 1987;13:69–76
   PubMed Web of Science ®Google Scholar
• Yang F-Y, Chiu W-H, Liu S-H, Lin G-L, Ho F-M. Functional changes in arteries induced by pulsed high-intensity focused ultrasound. IEEE Trans Ultrason Ferroelectr Freq Control 2009;56:2643–9
   PubMed Web of Science ®Google Scholar
• Hwang JH, Zhou Y, Warren C, Brayman AA, Crum LA. Targeted venous occlusion using pulsed high-intensity focused ultrasound. IEEE Trans Biomed Eng 2010;57:37–40
   PubMed Web of Science ®Google Scholar
• Fry FJ, Kossoff G, Eggleton RC, Dunn F. Threshold ultrasonic dosages for structural changes in the mammalian brain. J Acoust Soc Am 1970;48:1413–17
   Google Scholar
• Vykhodtseva NI, Hynynen K, Damianou C. Histologic effects of high-intensity pulsed-ultrasound exposure with subharmonic emission in rabbit brain in-vivo. Ultrasound Med Biol 1995;21:969–79
   PubMed Web of Science ®Google Scholar
• McDannold N, Vykhodtseva N, Hynynen K. Targeted disruption of the blood–brain barrier with focused ultrasound: Association with cavitation activity. Phys Med Biol 2006;51:793–807
   PubMed Web of Science ®Google Scholar
• Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001;61:3027–32
   PubMed Web of Science ®Google Scholar
• McDannold N, Vykhodtseva N, Jolesz FA, Hynynen K. MRI investigation of the threshold for thermally induced blood–brain barrier disruption and brain tissue damage in the rabbit brain. Magn Reson Med 2004;51:913–23
   PubMed Web of Science ®Google Scholar
• Staruch R, Chopra R, Hynynen K. Localised drug release using MRI-controlled focused ultrasound hyperthermia. Int J Hyperthermia 2011;27:156–71
   PubMed Web of Science ®Google Scholar
• Yang R, Reilly CR, Rescorla FJ, Faught PR, Sanghvi NT, Fry FJ, et al. High-intensity focussed ultrasound in the treatment of experimental liver cancer. Arch Surg 1991;126:1002–10
   PubMedGoogle Scholar
• Dorr LN, Hynynen K. The effects of tissue heterogeneities and large blood vessels on the thermal exposure induced by short high-power ultrasound pulses. Int J Hyperthermia 1992;8:45–59
   PubMed Web of Science ®Google Scholar
• Delonmartin C, Vogt C, Chignier E, Guers C, Chapelon JY, Cathignol D. Venous thrombosis generation by means of high-intensity focussed ultrasound. Ultrasound Med Biol 1995;21:113–19
   PubMed Web of Science ®Google Scholar
• Rivens IH, Rowland IJ, Denbow M, Fisk NM, ter Haar GR, Leach MO. Vascular occlusion using focused ultrasound surgery for use in fetal medicine. Eur J Ultrasound 1999;9:89–97
   PubMedGoogle Scholar
• Denbow ML, Rivens IH, Rowland IJ, Leach MO, Fisk NM, ter Haar GR. Preclinical development of noninvasive vascular occlusion with focused ultrasonic surgery for fetal therapy. Am J Obstet Gynecol 2000;182:387–92
   PubMed Web of Science ®Google Scholar
• Hwang JH, Vaezy S, Martin RW, Cho MY, Noble ML, Crum LA, et al. High-intensity focused US: A potential new treatment for GI bleeding. Gastrointest Endosc 2003;58:111–15
   PubMed Web of Science ®Google Scholar
• Ishikawa T, Okai T, Sasaki K, Umemura S, Fujiwara R, Kushima M, et al. Functional and histological changes in rat femoral arteries by HIFU exposure. Ultrasound Med Biol 2003;29:1471–7
   PubMed Web of Science ®Google Scholar
• Ichihara M, Sasaki K, Umemura S-I, Kushima M, Okai T. Blood flow occlusion via ultrasound image-guided high-intensity focused ultrasound and its effect on tissue perfusion. Ultrasound Med Biol 2007;33:452–9
   PubMed Web of Science ®Google Scholar
• Mahoney K, Martin H, Hynynen K. Focused ultrasound effects on blood vessels in vivo – Limits for vascular interventions. In: Schneider SC, Levy M, McAvoy BR, eds. Proc IEEE Ultrason Symp 2000;1–2:1405–8
   Google Scholar
• Colman RW, Hirsh J, Marder VJ, Clowes AA, Goerge JN. Hemostasis and thrombosis: Basic principles and clinical practice. 4th ed. Philadelphia: Lippincott Williams and Wilkins, 2001
   Google Scholar
• Hwang JH, Tu J, Brayman AA, Matula TJ, Crum LA. Correlation between inertial cavitation dose and endothelial cell damage in vivo. Ultrasound Med Biol 2006;32:1611–19
   PubMed Web of Science ®Google Scholar
• Stieger SM, Caskey CF, Adamson RH, Qin S, Curry F-RE, Wisner ER, et al. Enhancement of vascular permeability with low-frequency contrast-enhanced ultrasound in the chorioallantoic membrane model. Radiology 2007;243:112–21
   PubMed Web of Science ®Google Scholar
• Poliachik SL, Chandler WL, Mourad PD, Ollos RJ, Crum LA. Activation, aggregation and adhesion of platelets exposed to high-intensity focused ultrasound. Ultrasound Med Biol 2001;27:1567–76
   PubMed Web of Science ®Google Scholar
• Poliachik SL, Chandler WL, Ollos RJ, Bailey MR, Crum LA. The relation between cavitation and platelet aggregation during exposure to high-intensity focused ultrasound. Ultrasound Med Biol 2004;30:261–9
   PubMed Web of Science ®Google Scholar
• Vaezy S, Martin R, Schmiedl U, Caps M, Taylor S, Beach K, et al. Liver hemostasis using high-intensity focused ultrasound. Ultrasound Med Biol 1997;23:1413–20
   PubMed Web of Science ®Google Scholar
• Vaezy S, Martin R, Yaziji H, Kaczkowski P, Keilman G, Carter S, et al. Hemostasis of punctured blood vessels using high-intensity focused ultrasound. Ultrasound Med Biol 1998;24:903–10
   PubMed Web of Science ®Google Scholar
• Zderic V, Keshavarzi A, Noble ML, Paun M, Sharar SR, Crum LA, et al. Hemorrhage control in arteries using high-intensity focused ultrasound: A survival study. Ultrasonics 2006;44:46–53
   PubMed Web of Science ®Google Scholar
• Zhou Y, Zia J, Warren C, Starr FL, Brayman AA, Crum LA, et al. Targeted long-term venous occlusion using pulsed high-intensity focussed ultrasound combined with a pro-thrombotic inflammatory agent. Ultrasound Med Biol 2011;37:1653–8
   PubMed Web of Science ®Google Scholar
• Xu Z, Ludomirsky A, Eun LY, Hall TL, Tran BC, Fowlkes JB, et al. Controlled ultrasound tissue erosion. IEEE Trans Ultrason Ferroelectr Freq Control 2004;51:726–36
   PubMed Web of Science ®Google Scholar
• Xu Z, Fowlkes JB, Rothman ED, Levin AM, Cain CA. Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity. J Acoust Soc Am 2005;117:424–35
   PubMed Web of Science ®Google Scholar
• Vlaisavljevich E, Maxwell A, Warnez M, Johnsen E, Cain CA, Xu Z. Histotripsy-induced cavitation cloud initiation thresholds in tissues of different mechanical properties. IEEE Trans Ultrason Ferroelectr Freq Control 2014;61:341–52
   PubMed Web of Science ®Google Scholar
• Chaussy C Brendel W, Schmiedt E. Extracorporeally induced destruction of kidney stones by shock waves. Lancet 1980;2(8207):1265–8
   PubMed Web of Science ®Google Scholar
• Dalecki D, Child SZ, Raeman CH, Penney DP, Mayer R, Cox C, et al. Thresholds for fetal hemorrhages produced by a piezoelectric lithotripter. Ultrasound Med Biol 1997;23:287–97
   PubMed Web of Science ®Google Scholar
• Nishida T, Shimokawa H, Oi K, Tatewaki H, Uwatoku T, Abe K, et al. Extracorporeal cardiac shock wave therapy markedly ameliorates ischemia-induced myocardial dysfunction in pigs in vivo. Circulation 2004;110:3055–61
   PubMed Web of Science ®Google Scholar
• Uwatoku T, Ito K, Abe K, Oi K, Hizume T, Sunagawa K, et al. Extracorporeal cardiac shock wave therapy improves left ventricular remodeling after acute myocardial infarction in pigs. Coronary Artery Dis 2007;18:397–404
   PubMed Web of Science ®Google Scholar
• Ito Y, Ito K, Shiroto T, Tsuburaya R, Yi GJ, Takeda M, et al. Cardiac shock wave therapy ameliorates left ventricular remodeling after myocardial ischemia-reperfusion injury in pigs in vivo. Coronary Artery Dis 2010;21:304–11
   PubMed Web of Science ®Google Scholar
• Yang P, Guo T, Wang W, Peng Y-Z, Wang Y, Zhou P, et al. Randomized and double-blind controlled clinical trial of extracorporeal cardiac shock wave therapy for coronary heart disease. Heart Vessels 2013;28:284–91
   PubMed Web of Science ®Google Scholar
• Nazer B, Gerstenfeld EP, Hata A, Crum LA, Matula TJ. Cardiovascular applications of therapeutic ultrasound. J Intervent Cardiac Electrophysiol 2014;39:287–94
   PubMed Web of Science ®Google Scholar
• Ciampa AR, de Prati AC, Amelio E, Cavalieri E, Persichini T, Colasanti M, et al. Nitric oxide mediates anti-inflammatory action of extracorporeal shock waves. Febs Lett 2005;579:6839–45
   PubMed Web of Science ®Google Scholar
• Mariotto S, Cavalieri F, Amelio E, Ciampa AR, de Prati AC, Marlinghaus E, et al. Extracorporeal shock waves: From lithotripsy to anti-inflammatory action by NO production. Nitric Oxide Biol Chem 2005;12:89–96
   PubMed Web of Science ®Google Scholar
• Dayton PA, Ferrara KW. Targeted imaging using ultrasound. J Magn Reson Imaging 2002;16:362–77
   PubMed Web of Science ®Google Scholar
• ter Haar G. Safety and bio-effects of ultrasound contrast agents. Med Biol Eng Comput 2009;47:893–900
   PubMed Web of Science ®Google Scholar
• Bouakaz A, de Jong N. WFUMB safety symposium on echo-contrast agents: Nature and types of ultrasound contrast agents. Ultrasound Med Biology 2007;33:187–96
   PubMed Web of Science ®Google Scholar
• Qin S, Caskey CF, Ferrara KW. Ultrasound contrast microbubbles in imaging and therapy: Physical principles and engineering. Physics Med Biol 2009;54:R27–57
   PubMed Web of Science ®Google Scholar
• Unger E, Porter T, Lindner J, Grayburn P. Cardiovascular drug delivery with ultrasound and microbubbles. Adv Drug Deliv Rev 2014;72:110–26
   PubMed Web of Science ®Google Scholar
• Aryal M, Arvanitis CD, Alexander PM, McDannold N. Ultrasound-mediated blood–brain barrier disruption for targeted drug delivery in the central nervous system. Adv Drug Deliv Rev 2014;72:94–109
   PubMed Web of Science ®Google Scholar
• Deckers R, Moonen CTW. Ultrasound triggered, image guided, local drug delivery. J Control Release 2010;148:25–33
   PubMed Web of Science ®Google Scholar
• Unger EC, Porter T, Culp W, Labell R, Matsunaga T, Zutshi R. Therapeutic applications of lipid-coated microbubbles. Adv Drug Deliv Rev 2004;56:1291–314
   PubMed Web of Science ®Google Scholar
• Burgess A, Hynynen K. Noninvasive and targeted drug delivery to the brain using focused ultrasound. ACS Chem Neurosci 2013;4:519–26
   PubMed Web of Science ®Google Scholar
• Miller DL, Dou CY, Armstrong WF. The influence of agent delivery mode on cardiomyocyte injury induced by myocardial contrast echocardiography in rats. Ultrasound Med Biol 2005;31:1257–63
   PubMed Web of Science ®Google Scholar
• Vancraeynest D, Havaux X, Pouleur AC, Pasquet A, Gerber B, Beauloye C, et al. Myocardial delivery of colloid nanoparticles using ultrasound-targeted microbubble destruction. Eur Heart J 2006;27:237–45
   PubMed Web of Science ®Google Scholar
• Chappell JC, Klibanov AL, Price RJ. Ultrasound-microbubble-induced neovascularization in mouse skeletal muscle. Ultrasound Med Biol 2005;31:1411–22
   PubMed Web of Science ®Google Scholar
• Chappell JC, Song J, Klibanov AL, Price RJ. Ultrasonic microbubble destruction stimulates therapeutic arteriogenesis via the CD18-dependent recruitment of bone marrow-derived cells. Arterioscler Thromb Vasc Biol 2008;28:1117–22
   PubMed Web of Science ®Google Scholar
• Wood AKW, Ansaloni S, Ziemer LS, Lee WMF, Feldman MD, Sehgal CM. The antivascular action of physiotherapy ultrasound on murine tumors. Ultrasound Med Biol 2005;31:1403–10
   PubMed Web of Science ®Google Scholar
• McDannold N, Zhang Y-Z, Power C, Jolesz F, Vykhodtseva N. Nonthermal ablation with microbubble-enhanced focused ultrasound close to the optic tract without affecting nerve function Laboratory investigation. J Neurosurg 2013;119:1208–20
   PubMed Web of Science ®Google Scholar
• Chopra R, Vykhodtseva N, Hynynen K. Influence of exposure time and pressure amplitude on blood–brain-barrier opening using transcranial ultrasound exposures. ACS Chem Neurosci 2010;1:391–8
   PubMed Web of Science ®Google Scholar
• Burke CW, Klibanov AL, Sheehan JP, Price RJ. Inhibition of glioma growth by microbubble activation in a subcutaneous model using low duty cycle ultrasound without significant heating. J Neurosurg 2011;114:1654–61
   PubMed Web of Science ®Google Scholar
• Goertz DE, Todorova M, Mortazavi O, Agache V, Chen B, Karshafian R, et al. Antitumor effects of combining docetaxel (Taxotere) with the antivascular action of ultrasound stimulated microbubbles. Plos One 2012;7. Article ID: e52307
   PubMed Web of Science ®Google Scholar
• Czarnota GJ, Karshafian R, Burns PN, Wong S, Al Mahrouki A, Lee JW, et al. Tumor radiation response enhancement by acoustical stimulation of the vasculature. Proc Natl Acad Sci USA 2012;109:E2033–41
   PubMed Web of Science ®Google Scholar
• Dollet B, van der Meer SM, Garbin V, de Jong N, Lohse D, Versluis M. Nonspherical oscillations of ultrasound contrast agent-microbubbles. Ultrasound Med Biol 2008;34:1465–73
   PubMed Web of Science ®Google Scholar
• van der Meer SM, Dollet B, Voormolen MM, Chin CT, Bouakaz A, de Jong N, et al. Microbubble spectroscopy of ultrasound contrast agents. J Acoust Soc Am 2007;121:648–56
   PubMed Web of Science ®Google Scholar
• Juffermans LJM, van Dijk A, Jongenelen CAM, Drukarch B, Reijerkerk A, de Vries HE, et al. Ultrasound and microbubble induced intra- and intercellular bioeffects in primary endothelial cells. Ultrasound Med Biol 2009;35:1917–27
   PubMed Web of Science ®Google Scholar
• Xu Z, Hall TL, Fowlkes JB, Cain CA. Effects of acoustic parameters on bubble cloud dynamics in ultrasound tissue erosion (histotripsy). J Acoust Soc Am 2007;122:229–36
   PubMed Web of Science ®Google Scholar
• Dayton PA, Allen JS, Ferrara KW. The magnitude of radiation force on ultrasound contrast agents. J Acoust Soc Am 2002;112:2183–92
   PubMed Web of Science ®Google Scholar
• Chomas JE, Dayton P, Allen J, Morgan K, Ferrara KW. Mechanisms of contrast agent destruction. IEEE Trans Ultrason Ferroelec Freq Control 2001;48:232–48
   PubMed Web of Science ®Google Scholar
• Borden MA, Kruse DE, Caskey CF, Zhao SK, Dayton PA, Ferrara KW. Influence of lipid shell physicochemical properties on ultrasound-induced microbubble destruction. IEEE Trans Ultrason Ferroelec Freq Control 2005;52:1992–2002
   PubMed Web of Science ®Google Scholar
• Luan Y, Lajoinie G, Gelderblom E, Skachkov I, van der Steen AFW, Vos HJ, et al. Lipid shedding from single oscillating microbubbles. Ultrasound Med Biol 2014;40:1834–46
   PubMed Web of Science ®Google Scholar
• Klotz AR, Lindvere L, Stefanovic B, Hynynen K. Temperature change near microbubbles within a capillary network during focused ultrasound. Phys Med Biol 2010;55:1549–61
   PubMed Web of Science ®Google Scholar
• O’Reilly MA, Hynynen K. Blood–brain barrier: Real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology 2012;263:96–106
   PubMed Web of Science ®Google Scholar
• Jensen CR, Ritchie RW, Gyoengy M, Collin JRT, Leslie T, Coussios C-C. Spatiotemporal monitoring of high-intensity focused ultrasound therapy with passive acoustic mapping. Radiology 2012;262:252–61
   PubMed Web of Science ®Google Scholar
• Hosseinkhah N, Chen H, Matula TJ, Burns PN, Hynynen K. Mechanisms of microbubble-vessel interactions and induced stresses: A numerical study. J Acoust Soc Am 2013;134:1875–85
   PubMed Web of Science ®Google Scholar
• Qin SP, Ferrara KW. Acoustic response of compliable microvessels containing ultrasound contrast agents. Phys Med Biol 2006;51:5065–88
   PubMed Web of Science ®Google Scholar
• Martynov S, Stride E, Saffari N. The natural frequencies of microbubble oscillation in elastic vessels. J Acoust Soc Am 2009;126:2963–72
   PubMed Web of Science ®Google Scholar
• van Wamel A, Kooiman K, Harteveld M, Emmer M, ten Cate FJ, Versluis M, et al. Vibrating microbubbles poking individual cells: Drug transfer into cells via sonoporation. J Control Release 2006;112:149–55
   PubMed Web of Science ®Google Scholar
• Elder SA. Cavitation microstreaming. J Acoust Soc Am 1959;31:54–64
   Web of Science ®Google Scholar
• Garbin V, Cojoc D, Ferrari E, Di Fabrizio E, Overvelde MLJ, van der Meer SM, et al. Changes in microbubble dynamics near a boundary revealed by combined optical micromanipulation and high-speed imaging. Appl Phys Lett 2007;90:3
   Web of Science ®Google Scholar
• Prentice P, Cuschierp A, Dholakia K, Prausnitz M, Campbell P. Membrane disruption by optically controlled microbubble cavitation. Nature Phys 2005;1:107–10
   Web of Science ®Google Scholar
• Caskey CF, Kruse DE, Dayton PA, Kitano TK, Ferrara KW. Microbubble oscillation in tubes with diameters of 12, 25, and 195 microns. Appl Phys Lett 2006;88:3
   Web of Science ®Google Scholar
• Qin S, Ferrara KW. Acoustic response of compliable microvessels containing ultrasound contrast agents. Phys Med Biol 2006;51:5065–88
   PubMed Web of Science ®Google Scholar
• Sassaroli E, Hynynen K. Resonance frequency of microbubbles in small blood vessels: A numerical study. Phys Med Biol 2005;50:5293–305
   PubMed Web of Science ®Google Scholar
• Sassaroli E, Hynynen K. Cavitation threshold of microbubbles in gel tunnels by focused ultrasound. Ultrasound Med Biol 2007;33:1651–60
   PubMed Web of Science ®Google Scholar
• Faez T, Skachkov I, Versluis M, Kooiman K, de Jong N. In vivo characterization of microbubble contrast agents: Microbubble spectroscopy in a chicken embryo. Ultrasound Med Biol 2012;38:1608–17
   PubMed Web of Science ®Google Scholar
• Hosseinkhah N, Hynynen K. A three-dimensional model of an ultrasound contrast agent gas bubble and its mechanical effects on microvessels. Phys Med Biol 2012;57:785–808
   PubMed Web of Science ®Google Scholar
• Chen H, Kreider W, Brayman AA, Bailey MR, Matula TJ. Blood vessel deformations on microsecond time scales by ultrasonic cavitation. Phys Rev Lett 2011;106:034301
   PubMed Web of Science ®Google Scholar
• Chen H, Brayman AA, Kreider W, Bailey MR, Matula TJ. Observations of translation and jetting of ultrasound-activated microbubbles in mesenteric microvessels. Ultrasound Med Biol 2011;37:2139–48
   PubMed Web of Science ®Google Scholar
• Price RJ, Skyba DM, Kaul S, Skalak TC. Delivery of colloidal, particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound. Circulation 1998;98:1264–7
   PubMed Web of Science ®Google Scholar
• Tokarczyk A, Rivens I, van Bavel E, Symonds-Tayler R, ter Haar G. An experimental system for the study of ultrasound exposure of isolated blood vessels. Phys Med Biol 2013;58:2281–304
   PubMed Web of Science ®Google Scholar
• Stieger SM, Caskey CF, Adamson RH, Qin SP, Curry FRE, Wisner ER, et al. Enhancement of vascular permeability with low-frequency contrast-enhanced ultrasound in the chorioallantoic membrane model. Radiology 2007;243:112–21
   PubMed Web of Science ®Google Scholar
• Raymond SB, Skoch J, Hynynen K, Bacskai BJ. Multiphoton imaging of ultrasound/Optison mediated cerebrovascular effects in vivo. J Cereb Blood Flow Metab 2007;27:393–403
   PubMed Web of Science ®Google Scholar
• Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K. Cellular mechanisms of the blood–brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 2004;30:979–89
   PubMed Web of Science ®Google Scholar
• Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. Noninvasive MR imaging-guided focal opening of the blood–brain barrier in rabbits. Radiology 2001;220:640–6
   PubMed Web of Science ®Google Scholar
• Cho EE, Drazic J, Ganguly M, Stefanovic B, Hynynen K. Two-photon fluorescence microscopy study of cerebrovascular dynamics in ultrasound-induced blood–brain barrier opening. J Cereb Blood Flow Metab 2011;31:1852–62
   PubMed Web of Science ®Google Scholar
• Heath CH, Sorace A, Knowles J, Rosenthal E, Hoyt K. Microbubble therapy enhances anti-tumor properties of cisplatin and cetuximab in vitro and in vivo. Otolaryngol Head Neck Surg 2012;146:938–45
   PubMed Web of Science ®Google Scholar
• Wright C, Hynynen K, Goertz D. An investigation of high intensity focused ultrasound thrombolysis. AIP Conf Proc 2011;1359:246–50
   Google Scholar
• Bazan-Peregrino M, Arvanitis CD, Rifai B, Seymour LW, Coussios C-C. Ultrasound-induced cavitation enhances the delivery and therapeutic efficacy of an oncolytic virus in an in vitro model. J Control Release 2012;157:235–42
   PubMed Web of Science ®Google Scholar
• Sheikov N, McDannold N, Jolesz F, Zhang YZ, Tam K, Hynynen K. Brain arterioles show more active vesicular transport of blood-borne tracer molecules than capillaries and venules after focused ultrasound-evoked opening of the blood–brain barrier. Ultrasound Med Biol 2006;32:1399–409
   PubMed Web of Science ®Google Scholar
• Bao SP, Thrall BD, Miller DL. Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med Biol 1997;23:953–9
   PubMed Web of Science ®Google Scholar
• Meijering BDM, Juffermans LJM, van Wamel A, Henning RH, Zuhorn IS, Emmer M, et al. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ Res 2009;104:679–87
   PubMed Web of Science ®Google Scholar
• Juffermans LJ, Meijering BD, Kooiman K, Emmer M, van Wamel A, Musters RJ, et al. Targeted delivery of macromolecules using ultrasound and microbubbles is regulated by induction of endocytosis and pore formation. Circulation 2008;118:S643
   Web of Science ®Google Scholar
• Deng J, Huang Q, Wang F, Liu Y, Wang Z, Wang Z, et al. The role of caveolin-1 in blood–brain barrier disruption induced by focused ultrasound combined with microbubbles. J Mol Neurosci 2012;46:677–87
   PubMed Web of Science ®Google Scholar
• Huang Y, Vykhodtseva NI, Hynynen K. Creating brain lesions with low-intensity focused ultrasound with microbubbles: A rat study at half a megahertz. Ultrasound Med Biol 2013;39:1420–8
   PubMed Web of Science ®Google Scholar
• Vykhodtseva N, McDannold N, Hynynen K. Induction of apoptosis in vivo in the rabbit brain with focused ultrasound and Optison (R). Ultrasound Med Biol 2006;32:1923–9
   PubMed Web of Science ®Google Scholar
• McDannold NJ, Vykhodtseva NI, Hynynen K. Microbubble contrast agent with focused ultrasound to create brain lesions at low power levels: MR imaging and histologic study in rabbits. Radiology 2006;241:95–106
   PubMed Web of Science ®Google Scholar
• Wood AKW, Bunte RM, Price HE, Deitz MS, Tsai JH, Lee WMF, et al. The disruption of murine tumor neovasculature by low-intensity ultrasound – Comparison between 1- and 3-MHz sonication frequencies. Acad Radiol 2008;15:1133–41
   PubMed Web of Science ®Google Scholar
• Goertz DE, Karshafian R, Hynynen K. IEEE. Antivascular effects of pulsed low intensity ultrasound and microbubbles in mouse tumors. IEEE Ultrason Symp 2008;1–4:670–3
   Google Scholar
• Hu X, Kheirolomoom A, Mahakian LM, Beegle JR, Kruse DE, Lam KS, et al. Insonation of targeted microbubbles produces regions of reduced blood flow within tumor vasculature. Invest Radiol 2012;47:398–405
   PubMed Web of Science ®Google Scholar
• Al-Mahrouki AA, Iradji S, Tran WT, Czarnota GJ. Cellular characterization of ultrasound-stimulated microbubble radiation enhancement in a prostate cancer xenograft model. Dis Model Mech 2014;7:363–72
   PubMed Web of Science ®Google Scholar
• Todorova M, Agache V, Mortazavi O, Chen B, Karshafian R, Hynynen K, et al. Antitumor effects of combining metronomic chemotherapy with the antivascular action of ultrasound stimulated microbubbles. Int J Cancer 2013;132:2956–66
   PubMed Web of Science ®Google Scholar
• Lin C-Y, Tseng H-C, Shiu H-R, Wu M-F, Chou C-Y, Lin W-L. Ultrasound sonication with microbubbles disrupts blood vessels and enhances tumor treatments of anticancer nanodrug. Int J Nanomed 2012;7:2143–52
   PubMed Web of Science ®Google Scholar
• Wood AKW, Schultz SM, Lee WMF, Bunte RM, Sehgal CM. Antivascular ultrasound extends survival of mice with implanted melanomas. Ultrasound Med Biol 2010;36:853–7
   PubMed Web of Science ®Google Scholar
• Siemann DW. The unique characteristics of tumor vasculature and preclinical evidence for its selective disruption by tumor-vascular disrupting agents. Cancer Treat Rev 2011;37:63–74
   PubMed Web of Science ®Google Scholar
• Hwang JH, Brayman AA, Reidy MA, Matula TJ, Kimmey MB, Crum LA. Vascular effects induced by combined 1-MHz ultrasound and microbubble contrast agent treatments in vivo. Ultrasound Med Biol 2005;31:553–64
   PubMed Web of Science ®Google Scholar
• Miller DL, Gies RA. Enhancement of ultrasonically-induced hemolysis by perfluorocarbon-based compared to air-based echo-contrast agents. Ultrasound Med Biol 1998;24:285–92
   PubMed Web of Science ®Google Scholar
• Miller DL, Quddus J. Diagnostic ultrasound activation of contrast agent gas bodies induces capillary rupture in mice. Proc Natl Acad Sci USA 2000;97:10179–84
   PubMed Web of Science ®Google Scholar
• Li P, Cao LQ, Dou CY, Armstrong WF, Miller D. Impact of myocardial contrast echocardiography on vascular permeability: An in vivo dose response study of delivery mode, pressure amplitude and contrast dose. Ultrasound Med Biol 2003;29:1341–9
   PubMed Web of Science ®Google Scholar
• Thorsen T, Lie RT, Holmsen H. Induction of platelet aggegation in vitro by microbubbles of nitrogen. Undersea Biomed Res 1989;16:453–64
   PubMedGoogle Scholar
• Shigeta K, Taniguchi N, Omoto K, Madoiwa S, Sakata Y, Mori M, et al. In vitro platelet activation by an echo contrast agent. J Ultrasound Med 2003;22:365–73
   PubMed Web of Science ®Google Scholar
• Song J, Qi M, Kaul S, Price RJ. Stimulation of arteriogenesis in skeletal muscle by microbubble destruction with ultrasound. Circulation 2002;106:1550–5
   PubMed Web of Science ®Google Scholar
• Song J, Cottler PS, Klibanov AL, Kaul S, Price RJ. Microvascular remodeling and accelerated hyperemia blood flow restoration in arterially occluded skeletal muscle exposed to ultrasonic microbubble destruction. Am J Physiol Heart Circ Physiol 2004;287:H2754–61
   PubMed Web of Science ®Google Scholar
• Yoshida J, Ohmori K, Takeuchi H, Shinomiya K, Namba T, Kondo I, et al. Treatment of ischemic limbs based on local recruitment of vascular endothelial growth factor-producing inflammatory cells with ultrasonic microbubble destruction. J Am Coll Cardiol 2005;46:899–905
   PubMed Web of Science ®Google Scholar
• Imada T, Tatsumi T, Mori Y, Nishiue T, Yoshida M, Masaki H, et al. Targeted delivery of bone marrow mononuclear cells by ultrasound destruction of microbubbles induces both angiogenesis and arteriogenesis response. Arterioscler Thromb Vasc Biol 2005;25:2128–34
   PubMed Web of Science ®Google Scholar
• Leong-Poi H, Kuliszewski MA, Lekas M, Sibbald M, Teichert-Kuliszewska K, Klibanov AL, et al. Therapeutic arteriogenesis by ultrasound-mediated VEGF(165) plasmid gene delivery to chronically ischemic skeletal muscle. Circ Res 2007;101:295–303
   PubMed Web of Science ®Google Scholar
• Pfaffenberger S, Devcic-Kuhar B, Kastl SP, Huber K, Maurer G, Wojta J, et al. Ultrasound thrombolysis. Thromb Haemost 2005;94:26–36
   PubMed Web of Science ®Google Scholar
• Blinc A, Francis CW, Trudnowski JL, Carstensen EL. Characgerization of ultrasound potentiated fibrinolysis in vivo. Blood 1993;81:2636–43
   PubMed Web of Science ®Google Scholar
• Porter TR, LeVeen RF, Fox R, Kricsfeld A, Xie F. Thrombolytic enhancement with perfluorocarbon-exposed sonicated dextrose albumin microbubbles. Am Heart J 1996;132:964–8
   PubMed Web of Science ®Google Scholar
• Datta S, Coussios C-C, McAdory LE, Tan J, Porter T, De Courten-Myers G, et al. Correlation of cavitation with ultrasound enhancement of thrombolysis. Ultrasound Med Biol 2006;32:1257–67
   PubMed Web of Science ®Google Scholar
• Culp WC, Porter TR, Xie F, Goertzen TC, McCowan TC, Vonk BN, et al. Microbubble potentiated ultrasound as a method of declotting thrombosed dialysis grafts: Experimental study in dogs. Cardiovasc Intervent Radiol 2001;24:407–12
   PubMed Web of Science ®Google Scholar
• Leeman JE, Kim JS, Yu FTH, Chen X, Kim K, Wang J, et al. Effect of acoustic conditions on microbubble mediated microvascular sonothrombolysis. Ultrasound Med Biol 2012;38:1589–98
   PubMed Web of Science ®Google Scholar
• Alexandrov AV, Molina CA, Grotta JC, Garami Z, Ford SR, Alvarez-Sabin J, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. New Engl J Med 2004;351:2170–8
   PubMed Web of Science ®Google Scholar
• Burgess A, Huang Y, Waspe AC, Ganguly M, Goertz DE, Hynynen K. High-intensity focused ultrasound (HIFU) for dissolution of clots in a rabbit model of embolic stroke. Plos One 2012;7:e43211
   PubMed Web of Science ®Google Scholar
• Maxwell AD, Owens G, Gurm HS, Ives K, Myers DD, Jr. Xu Z. Noninvasive treatment of deep venous thrombosis using pulsed ultrasound cavitation therapy (histotripsy) in a porcine model. J Vasc Interv Radiol 2011;22:369–77
   PubMed Web of Science ®Google Scholar
• Rosenschein U, Furman V, Kerner E, Fabian I, Bernheim J, Eshel Y. Ultrasound imaging-guided noninvasive ultrasound thrombolysis – Preclinical results. Circulation 2000;102:238–45
   PubMed Web of Science ®Google Scholar