Acoustic behavior of microbubbles and implications for drug delivery

Advanced Drug Delivery Reviews

Volumn 72, Issue , 2014, Pages 28-48

  Kooiman, Klazina ^a,b   Vos, Hendrik J ^a,c   Versluis, Michel ^d   De Jong, Nico ^a,b,c  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

Acoustic cavitation; Acoustic microstreaming; Co administration; Drug carrier system; Drug release; Drug uptake; Microcapsule; Ultrasound contrast agent

Indexed keywords

CONTROLLED DRUG DELIVERY; MICROSTRUCTURE; SHEAR STRESS; ULTRASONIC IMAGING;

ACOUSTIC CAVITATIONS; ACOUSTIC MICROSTREAMING; DRUG CARRIER SYSTEMS; DRUG RELEASE; DRUG UPTAKE; MICROCAPSULES; ULTRASOUND CONTRAST AGENT;

TARGETED DRUG DELIVERY;

ALBUMIN; DRUG CARRIER; ECHO CONTRAST MEDIUM; LIPID; POLYMER;

ACOUSTIC ANALYSIS; ACOUSTIC CAVITATION; ACOUSTIC MICROSTREAMING; DRUG DELIVERY SYSTEM; DRUG RELEASE; DRUG UPTAKE; HUMAN; MATERIAL COATING; MICROBUBBLE; MICROCAPSULE; MICROSTREAMING; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RADIATION FORCE; RADIOLOGICAL PARAMETERS; REVIEW; SHEAR STRESS; THEORY; ACOUSTICS; ANIMAL;

ACOUSTICS; ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; MICROBUBBLES;

EID: 84901587139     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.03.003     Document Type: Review

References (232)

1. Gramiak R., Shah P.M. Echocardiography of the aortic root. Invest. Radiol. 1968, 3:356-366.
2. Goldberg B.B., Liu J.-B., Forsberg F. Ultrasound contrast agents: a review. Ultrasound Med. Biol. 1994, 20:319-333.
3. Cosgrove D. Ultrasound contrast agents: an overview. Eur. J. Radiol. 2006, 60:324-330.
4. Postema M., Gilja O.H. Contrast-enhanced and targeted ultrasound. World J. Gastroenterol. 2011, 17:28.
5. Kaul S. Myocardial contrast echocardiography: a 25-year retrospective. Circulation 2008, 118:291-308.
6. Klibanov A.L. Ultrasound contrast agents: development of the field and current status. Top. Curr. Chem. 2002, 222:73-105.
7. Greis C. Ultrasound contrast agents as markers of vascularity and microcirculation. Clin. Hemorheol. Microcirc. 2009, 43:1-9.
8. Faez T., Emmer M., Kooiman K., Versluis M., van der Steen A.F., de Jong N. 20years of ultrasound contrast agent modeling. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2013, 60:7-20.
9. Wu J., Nyborg W.L. Ultrasound, cavitation bubbles and their interaction with cells. Adv. Drug Deliv. Rev. 2008, 60:1103-1116.
10. Hernot S., Klibanov A.L. Microbubbles in ultrasound-triggered drug and gene delivery. Adv. Drug Deliv. Rev. 2008, 60:1153-1166.
11. Klibanov A.L. Microbubble contrast agents: targeted ultrasound imaging and ultrasound-assisted drug-delivery applications. Invest. Radiol. 2006, 41:354-362.
12. Ferrara K.W. Driving delivery vehicles with ultrasound. Adv. Drug Deliv. Rev. 2008, 60:1097-1102.
13. Dijkmans P.A., Juffermans L.J., Musters R.J., van Wamel A., ten Cate F.J., van Gilst W., Visser C.A., de Jong N., Kamp O. Microbubbles and ultrasound: from diagnosis to therapy. Eur. J. Echocardiogr. 2004, 5:245-256.
14. Ferrara K.W., Borden M.A., Zhang H. Lipid-shelled vehicles: engineering for ultrasound molecular imaging and drug delivery. Acc. Chem. Res. 2009, 42:881-892.
15. ICUS, What is CEUS?, in:. http://www.icus-society.org/about-ceus/.
16. Correas J.M., Helenon O., Pourcelot L., Moreau J.F. Ultrasound contrast agents. Examples of blood pool agents. Acta Radiol. Suppl. 1997, 412:101-112.
17. Leighton T.G. The Acoustic Bubble 1994, Academic Press, London.
18. Medwin H. Counting Bubbles acoustically: a review. Ultrasonics 1977, 7-13.
19. Holland C.K., Deng C.X., Apfel R.E., Alderman J.L., Fernandez L.A., Taylor K.J. Direct evidence of cavitation in vivo from diagnostic ultrasound. Ultrasound Med. Biol. 1996, 22:917-925.
20. Vignon F., Shi W.T., Powers J.E., Everbach E.C., Liu J., Gao S., Xie F., Porter T.R. Microbubble cavitation imaging. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2013, 60:661-670.
21. Kamiyama N., Moriyasu F., Mine Y., Goto Y. Analysis of flash echo from contrast agent for designing optimal ultrasound diagnostic systems. Ultrasound Med. Biol. 1999, 25:411-420.
22. Rayleigh L. VIII. On the pressure developed in a liquid during the collapse of a spherical cavity, The London, Edinburgh, and Dublin Philosophical. Mag. J. Sci. 1917, 34:94-98.
23. Plesset M. The dynamics of cavitation bubbles. J. Appl. Mech. 1949, 16:227-282.
24. Noltingk B.E., Neppiras E.A. Cavitation produced by ultrasonics. Proc. Phys. Soc. Sec. B 1950, 63:674-685.
25. Neppiras E., Noltingk B. Cavitation produced by ultrasonics: theoretical conditions for the onset of cavitation. Proc. Phys. Soc. Sec. B 1951, 64:1032-1038.
26. Poritsky H. The collapse or growth of a spherical bubble or cavity in a viscous fluid. Proc. First Nat. Cong. Appl. Math. 1952, 813-821.
27. Brennen C.E. Cavitation and Bubble Dynamics 1995, Oxford University Press.
28. Hilgenfeldt S., Lohse D., Zomack M. Response of bubbles to diagnostic ultrasound: a unifying theoretical approach. Eur. Phys. J. B 1998, 4:247-255.
29. de Jong N., Bouakaz A., Frinking P. Basic acoustic properties of microbubbles. Echocardiogr. 2002, 19:229-240.
30. van der Meer S.M., Dollet B., Voormolen M.M., Chin C.T., Bouakaz A., de Jong N., Versluis M., Lohse D. Microbubble spectroscopy of ultrasound contrast agents. J. Acoust. Soc. Am. 2007, 121:648-656.
31. Tsiglifis K., Pelekasis N.A. Nonlinear radial oscillations of encapsulated microbubbles subject to ultrasound: The effect of membrane constitutive law. J. Acoust. Soc. Am. 2008, 123:4059-4070.
32. Morgan K.E., Allen J.S., Dayton P.A., Chomas J.E., Klibanov A.L., Ferrara K.W. Experimental and theoretical evaluation of microbubble behavior: effect of transmitted phase and bubble size. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2000, 47:1494-1509.
33. Doinikov A.A., Haac J.F., Dayton P.A. Modeling of nonlinear viscous stress in encapsulating shells of lipid-coated contrast agent microbubbles. Ultrasonics 2009, 49:269-275.
34. Minnaert M. On musical air-bubbles and the sound of running water. Philos. Mag. 1933, 16:235-248.
35. Wagai T. Studies on the foundation and development of diagnostic ultrasound. P. Jpn. Acad. B Phys. 2007, 83:256-265.
36. McLaughlan J., Ingram N., Smith P.R., Harput S., Coletta P.L., Evans S., Freear S. Increasing the sonoporation efficiency of targeted polydisperse microbubble populations using chirp excitation. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2013, 60:2511-2520.
37. Chetty K., Stride E., Sennoga C.A., Hajnal J.V., Eckersley R.J. High-speed optical observations and simulation results of SonoVue microbubbles at low-pressure insonation. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2008, 55:1333-1342.
38. Church C.C. The effects of an elastic solid surface layer on the radial pulsations of gas bubbles. J. Acoust. Soc. Am. 1995, 97:1510-1521.
39. Sarkar K., Shi W.T., Chatterjee D., Forsberg F. Characterization of ultrasound contrast microbubbles using in vitro experiments and viscous and viscoelastic interface models for encapsulation. J. Acoust. Soc. Am. 2005, 118:539-550.
40. Hoff L., Sontum P.C., Hovem J.M. Oscillations of polymeric microbubbles: effect of the encapsulating shell. J. Acoust. Soc. Am. 2000, 107:2272-2280.
41. Marmottant P., van der Meer S., Emmer M., Versluis M., de Jong N., Hilgenfeldt S., Lohse D. A model for large amplitude oscillations of coated bubbles accounting for buckling and rupture. J. Acoust. Soc. Am. 2005, 118:3499-3505.
42. Doinikov A.A., Dayton P.A. Maxwell rheological model for lipid-shelled ultrasound microbubble contrast agents. J. Acoust. Soc. Am. 2007, 121:3331-3340.
43. Tu J., Guan J., Qiu Y., Matula T.J. Estimating the shell parameters of SonoVue microbubbles using light scattering. J. Acoust. Soc. Am. 2009, 126:2954.
44. Emmer M., Vos H., Versluis M., de Jong N. Radial modulation of single microbubbles. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2009, 56:2370-2379.
45. Vos H.J., Emmer M., de Jong N. Oscillation of single microbubbles at room versus body temperature. IEEE Ultrasonics symposium, Beijing, China 2008, 982-984.
46. Dayton P.A., Allen J.S., Ferrara K.W. The Magnitude of radiation force on ultrasound contrast agents. J. Acoust. Soc. Am. 2002, 112:2183-2192.
47. Borden M.A., Martinez G.V., Ricker J., Tsvetkova N., Longo M., Gillies R.J., Dayton P.A., Ferrara K.W. Lateral phase separation in lipid-coated microbubbles. Langmuir 2006, 22:4291-4297.
48. Overvelde M., Garbin V., Dollet B., de Jong N., Lohse D., Versluis M. Dynamics of coated microbubbles adherent to a wall. Ultrasound Med. Biol. 2011, 37:1500-1508.
49. Caskey C.F., Stieger S.M., Qin S., Dayton P.A., Ferrara K.W. Direct observations of ultrasound microbubble contrast agent interaction with the microvessel wall. J. Acoust. Soc. Am. 2007, 122:1191-1200.
50. Miller D.L., Averkiou M.A., Brayman A.A., Everbach E.C., Holland C.K., Wible J.H., Wu J. Bioeffects considerations for diagnostic ultrasound contrast agents. J. Ultrasound Med. 2008, 27:611-632.
51. Kooiman K., Böhmer M.R., Emmer M., Vos H.J., Chlon C., Shi W.T., Hall C.S., de Winter S.H., Schroen K., Versluis M., de Jong N., van Wamel A. Oil-filled polymer microcapsules for ultrasound-mediated delivery of lipophilic drugs. J. Control. Release 2009, 133:109-118.
52. Bjerknes V. Fields of Force 1906, Columbia University Press, New York.
53. Vos H.J., Guidi F., Boni E., Tortoli P. Method for microbubble characterization using primary radiation force. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2007, 54:1333-1345.
54. Marmottant P., Versluis M., de Jong N., Hilgenfeldt S., Lohse D. High-speed imaging of an ultrasound-driven bubble in contact with a wall: "Narcissus" effect and resolved acoustic streaming. Exp. Fluids 2005, 10.1007/s00348-00005-00080-y.
55. Vos H.J., Dollet B., Versluis M., de Jong N. Nonspherical shape oscillations of coated microbubbles in contact with a wall. Ultrasound Med. Biol. 2011, 37:935-948.
56. Postema M.A.B., Van Wamel A., Lancée C.T., de Jong N. Ultrasound-induced encapsulated microbubble phenomena. Ultrasound Med. Biol. 2004, 30:827-840.
57. Doinikov A.A., Zhao S., Dayton P.A. Modeling of the acoustic response from contrast agent microbubbles near a rigid wall. Ultrasonics 2009, 49:195-201.
58. de Jong N., Hoff L., Skotland T., Bom N. Absorption and scatter of encapsulated gas filled microspheres: theoretical considerations and some measurements. Ultrasonics 1992, 30:95-103.
59. Guidi F., Vos H.J., Mori R., de Jong N., Tortoli P. Microbubble characterization through acoustically induced deflation. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2010, 57:193-202.
60. Sijl J., Vos H.J., Rozendal T., de Jong N., Lohse D., Versluis M. Combined optical and acoustical detection of single microbubble dynamics. J. Acoust. Soc. Am. 2011, 130:3271-3281.
61. Maresca D., Emmer M., van Neer P.L.M.J., Vos H.J., Versluis M., Muller M., de Jong N., van der Steen A.F.W. Acoustic sizing of an ultrasound contrast agent. Ultrasound Med. Biol. 2010, 36:1713-1721.
62. Kuribayashi K., Kudo N., Natori M., Yamamoto K. A high-magnification and high-speed system for the observation of microbubbles under ultrasound exposure. IEEE Ultrasonics symposium, Lake Tahoe, Nevada 1999, 1755-1758.
63. Chin C.T., Lancée C.T., Borsboom J.M.G., Mastik F., Frijlink M.E., de Jong N., Versluis M., Lohse D. Brandaris 128: A 25 million frames per second digital camera with 128 highly sensitive frames. Rev. Sci. Instrum. 2003, 74:5026-5034.
64. Gelderblom E.C., Vos H.J., Mastik F., Faez T., Luan Y., Kokhuis T.J., van der Steen A.F., Lohse D., de Jong M N., Versluis M. Brandaris 128 ultra-high-speed imaging facility: 10years of operation, updates, and enhanced features. Rev. Sci. Instrum. 2012, 83. (103706-103706-103711).
65. Chen X., Wang J., Versluis M., de Jong N., Villanueva F.S. Ultra-fast bright field and fluorescence imaging of the dynamics of micrometer-sized objects. Rev. Sci. Instrum. 2013, 84:063701.
66. Pu G., Borden M.A., Longo M.L. Collapse and shedding transitions in binary lipid monolayers coating microbubbles. Langmuir 2006, 22:2993-2999.
67. Emmer M., van Wamel A., Goertz D.E., de Jong N. The onset of microbubble vibration. Ultrasound Med. Biol. 2007, 33:941-949.
68. Overvelde M., Garbin V., Sijl J., Dollet B., de Jong N., Lohse D., Versluis M. Nonlinear shell behavior of phospholipid-coated microbubbles. Ultrasound Med. Biol. 2010, 36:2080-2092.
69. Goertz D.E., de Jong N., van der Steen A.F.W. Attenuation and size distribution measurements of Definity and manipulated Definity populations. Ultrasound Med. Biol. 2007, 33:1376-1388.
70. de Jong N., Cornet R., Lancée C. Higher harmonics of vibrating gas-filled microspheres. Part two: measurements. Ultrasonics 1994, 32:455-459.
71. Eller A., Flynn H.G. Generation of subharmonics of order one-half by bubbles in a sound field. J. Acoust. Soc. Am. 1969, 46:727-772.
72. Prosperetti A. Nonlinear oscillations of gas bubbles in liquids: transient solutions and the connection between subharmonic signal and cavitation. J. Acoust. Soc. Am. 1975, 57:810-821.
73. Sijl J., Dollet B., Overvelde M., Garbin V., Rozendal T., de Jong N., Lohse D., Versluis M. Subharmonic behavior of phospholipid-coated ultrasound contrast agent microbubbles. J. Acoust. Soc. Am. 2010, 128:3239.
74. de Jong N., Emmer M., Chin C.T., Bouakaz A., Mastik F., Lohse D., Versluis M. "Compression-only" behavior of phospholipid-coated contrast bubbles. Ultrasound Med. Biol. 2007, 33:653-656.
75. Dollet B., Van der Meer S.M., Garbin V., de Jong N., Lohse D., Versluis M. Nonspherical oscillations of ultrasound contrast agent microbubbles. Ultrasound Med. Biol. 2008, 34:1465-1473.
76. Fong S.W., Klaseboer E., Turangan C.K., Khoo B.C., Hung K.C. Numerical Analysis of a gas bubble near bio-materials in an ultrasound field. Ultrasound Med. Biol. 2006, 32:925-942.
77. Zhao S., Ferrara K.W., Dayton P.A. Asymmetric oscillation of adherent targeted ultrasound contrast agents. Appl. Phys. Lett. 2005, 87. (ref. 134103).
78. Prentice P., Cuschieri A., Dholakia K., Prausnitz M., Campbell P. Membrane disruption by optically controlled microbubble cavitation. Nat. Phys. 2005, 1:107-110.
79. Blake J.R., Taib B.B., Doherty G. Transient cavities near boundaries. Part 1. Rigid boundary. J. Fluid Mech. 1986, 170:479-497.
80. Vos H.J., Dollet B., Bosch J.G., Versluis M., de Jong N. Nonspherical vibrations of microbubbles in contact with a wall - a pilot study at low mechanical index. Ultrasound Med. Biol. 2008, 34:685-688.
81. Marmottant P., Hilgenfeldt S. Controlled vesicle deformation and lysis by single oscillating bubbles. Nature 2003, 423:153-156.
82. May D.J., Allen J.S., Ferrara K.W. Dynamics and fragmentation of thick-shelled microbubbles. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2002, 49:1400-1410.
83. Chomas J.E., Dayton P.A., Allen J.S., Morgan K.E., Ferrara K.W. Mechanisms of contrast agent destruction. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2001, 48:232-248.
84. Tögel R., Luther S., Lohse D. Viscosity Destablizes Sonoluminescing Bubbles 2005, University of Twente, The Netherlands.
85. Putterman S., Weninger K. Sonoluminescence: how bubbles turn sound into light. Annu. Rev. Fluid Mech. 2000, 32:445-476.
86. Versluis M., Schmitz B., von der Heydt A., Lohse D. How snapping shrimp snap: through cavitating bubbles. Science 2000, 289:2114-2117.
87. Hallow D.M., Mahajan A.D., McCutchen T.E., Prausnitz M.R. Measurement and correlation of acoustic cavitation with cellular bioeffects. Ultrasound Med. Biol. 2006, 32:1111-1122.
88. Coussios C.C., Roy R.A. Applications of acoustics and cavitation to noninvasive therapy and drug delivery. Annu. Rev. Fluid Mech. 2008, 40:395-420.
89. Plesset M.S., Mitchell T.P. On the Stability of the Spherical Shape of a Vapor Cavity in a Liquid. Quarterly Appl. Math. 1956, 12(4).
90. Chomas J.E., Dayton P., May D., Ferrara K. Threshold of fragmentation for ultrasonic contrast agents. J. Biomed. Opt. 2001, 6:141-150.
91. de Jong N., Emmer M., van Wamel A., Versluis M. Ultrasonic characterization of ultrasound contrast agents. Med. Biol. Eng. Comput. 2009, 47:861-873.
92. Marmottant P., Bouakaz A., de Jong N., Quilliet C. Buckling resistance of solid shell bubbles under ultrasound. J. Acoust. Soc. Am. 2011, 129:1231-1239.
93. Lensen D., Gelderblom E.C., Vriezema D.M., Marmottant P., Verdonschot N., Versluis M., de Jong N., Van Hest J.C. Biodegradable polymeric microcapsules for selective ultrasound-triggered drug release. Soft Matter 2011, 7:5417-5422.
94. Bouakaz A., Versluis M., de Jong N. High-speed optical observations of contrast agent destruction. Ultrasound Med. Biol. 2005, 31:391-399.
95. van Wamel A., Kooiman K., Harteveld M., Emmer M., Ten Cate F.J., Versluis M., de Jong N. Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation. J. Control. Release 2006, 112:149-155.
96. Rooney J.A. Hemolysis near an ultrasonically pulsating gas bubble. Science 1970, 169:869-871.
97. Elder S.A. Cavitation microstreaming. J. Acoust. Soc. Am. 1959, 31:54-64.
98. Collis J., Manasseh R., Liovic P., Tho P., Ooi A., Petkovic-Duran K., Zhu Y. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics 2010, 50:273-279.
99. Gelderblom E.C. Ultra-High-Speed Fluorescence Imaging 2012, Universiteit Twente.
100. Forbes M.M., O'Brien W.D. Development of a theoretical model describing sonoporation activity of cells exposed to ultrasound in the presence of contrast agents. J. Acoust. Soc. Am. 2012, 131:2723-2729.
101. Doinikov A.A., Bouakaz A. Theoretical investigation of shear stress generated by a contrast microbubble on the cell membrane as a mechanism for sonoporation. J. Acoust. Soc. Am. 2010, 128:11-19.
102. Wu J. Theoretical study on shear stress generated by microstreaming surrounding contrast agents attached to living cells. Ultrasound Med. Biol. 2002, 28:125-129.
103. Dijkink R., Ohl C.-D. Measurement of cavitation induced wall shear stress. Appl. Phys. Lett. 2008, 93. (254107-254107-254103).
104. Malek A.M., Alper S.L., Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999, 282:2035-2042.
105. Ohl C.-D., Arora M., Ikink R., de Jong N., Versluis M., Delius M., Lohse D. Sonoporation from jetting cavitation bubbles. Biophys. J. 2006, 91:4285-4295.
106. Brujan E.-A., Nahen K., Schmidt P., Vogel A. Dynamics of laser-induced cavitation bubbles near elastic boundaries: influence of the elastic modulus. J. Fluid Mech. 2001, 433:283-314.
107. Chen H., Kreider W., Brayman A.A., Bailey M.R., Matula T.J. Blood vessel deformations on microsecond time scales by ultrasonic cavitation. Phys. Rev. Lett. 2011, 106:034301.
108. Garbin V., Cojoc D., Ferrari E., Di Fabrizio E., Overvelde M.L.J., van der Meer S.M., de Jong N., Lohse D., Versluis M. Changes in microbubble dynamics near a boundary revealed by combined optical micromanipulation and high-speed imaging. Appl. Phys. Lett. 2007, 90:114103.
109. Doinikov A.A., Aired L., Bouakaz A. Acoustic response from a bubble pulsating near a fluid layer of finite density and thickness. J. Acoust. Soc. Am. 2011, 129:616-621.
110. Hay T.A., Ilinskii Y.A., Zabolotskaya E.A., Hamilton M.F. Model for bubble pulsation in liquid between parallel viscoelastic layers. J. Acoust. Soc. Am. 2012, 132:124.
111. Leighton T. The inertial terms in equations of motion for bubbles in tubular vessels or between plates. J. Acoust. Soc. Am. 2011, 130:3333-3338.
112. Thomas D.H., Sboros V., Emmer M., Vos H., de Jong N. Microbubble oscillations in capillary tubes. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2013, 60:105-114.
113. Faez T., Skachkov I., Versluis M., Kooiman K., de Jong N. In vivo characterization of ultrasound contrast agents: microbubble spectroscopy in a chicken embryo. Ultrasound Med. Biol. 2012, 38:1608-1617.
114. Bao S., Thrall B.D., Miller D.L. Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med. Biol. 1997, 23:953-959.
115. Kotopoulis S., Dimcevski G., Gilja O.H., Hoem D., Postema M. Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med. Phys. 2013, 40:072902.
116. Lai C.Y., Wu C.H., Chen C.C., Li P.C. Quantitative relations of acoustic inertial cavitation with sonoporation and cell viability. Ultrasound Med. Biol. 2006, 32:1931-1941.
117. Qiu Y., Luo Y., Zhang Y., Cui W., Zhang D., Wu J., Zhang J., Tu J. The correlation between acoustic cavitation and sonoporation involved in ultrasound-mediated DNA transfection with polyethylenimine (PEI) in vitro. J. Control. Release 2010, 145:40-48.
118. Forbes M.M., Steinberg R.L., O'Brien W.D. Examination of inertial cavitation of Optison in producing sonoporation of chinese hamster ovary cells. Ultrasound Med. Biol. 2008, 34:2009-2018.
119. Kinoshita M., Hynynen K. Key factors that affect sonoporation efficiency in in vitro settings: the importance of standing wave in sonoporation. Biochem. Biophys. Res. Commun. 2007, 359:860-865.
120. Delalande A., Kotopoulis S., Rovers T., Pichon C., Postema M. Sonoporation at a low mechanical index. Bubble Sci. Eng. Technol. 2011, 3:3-12.
121. Hu Y., Wan J.M.F., Yu A.C.H. Membrane perforation and recovery dynamics in microbubble-mediated sonoporation. Ultrasound Med. Biol. 2013, 39:2393-2405.
122. Krasovitski B., Frenkel V., Shoham S., Kimmel E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3258-3263.
123. Wrenn S.P., Small E., Dan N. Bubble nucleation in lipid bilayers: a mechanism for low frequency ultrasound disruption. Biochim. Biophys. Acta 2013, 1828:1192-1197.
124. Rappaport S.M., Berezhkovskii A.M., Zimmerberg J., Bezrukov S.M. Thermodynamics of interleaflet cavitation in lipid bilayer membranes. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 2013, 87:022715.
125. Pua E.C., Zhong P. Ultrasound-mediated drug delivery. IEEE Eng. Med. Biol. Mag. 2009, 28:64-75.
126. Karshafian R., Bevan P.D., Williams R., Samac S., Burns P.N. Sonoporation by ultrasound-activated microbubble contrast agents: effect of acoustic exposure parameters on cell membrane permeability and cell viability. Ultrasound Med. Biol. 2009, 35:847-860.
127. Schlicher R.K., Radhakrishna H., Tolentino T.P., Apkarian R.P., Zarnitsyn V., Prausnitz M.R. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med. Biol. 2006, 32:915-924.
128. Meijering B.D., Juffermans L.J., van Wamel A., Henning R.H., Zuhorn I.S., Emmer M., Versteilen A.M., Paulus W., van Gilst W.H., Kooiman K., de Jong N., Musters R.J., Deelman L.E., Kamp O. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ. Res. 2009, 104:679-687.
129. Chen X., Wan J.M., Yu A.C. Sonoporation as a cellular stress: induction of morphological repression and developmental delays. Ultrasound Med. Biol. 2013, 39:1075-1086.
130. Mehier-Humbert S., Bettinger T., Yan F., Guy R.H. Plasma membrane poration induced by ultrasound exposure: Implication for drug delivery. J. Control. Release 2005, 104:213-222.
131. Zhou Y., Cui J.M., Deng C.X. Dynamics of sonoporation correlated with acoustic cavitation activities. Biophys. J. 2008, 94:L51-L53.
132. Tran T.A., Roger S., Le Guennec J.Y., Tranquart F., Bouakaz A. Effect of ultrasound-activated microbubbles on the cell electrophysiological properties. Ultrasound Med. Biol. 2007, 33:158-163.
133. Meijering B.D.M., Henning R.H., van Gilst W.H., Gavrilovic I., van Wamel A., Deelman L.E. Optimization of ultrasound and microbubbles targeted gene delivery to cultured primary endothelial cells. J. Drug Target. 2007, 15:664-671.
134. van Wamel A., Bouakaz A., Versluis M., de Jong N. Micromanipulation of endothelial cells: ultrasound-microbubble-cell interaction. Ultrasound Med. Biol. 2004, 30:1255-1258.
135. Kudo N., Okada K., Yamamoto K. Sonoporation by single-shot pulsed ultrasound with microbubbles adjacent to cells. Biophys. J. 2009, 96:4866-4876.
136. Sheikov N., McDannold N., Sharma S., Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med. Biol. 2008, 34:1093-1104.
137. Liu Y., Yi S., Zhang J., Fang Z., Zhou F., Jia W., Liu Z., Ye G. Effect of microbubble-enhanced ultrasound on prostate permeability: a potential therapeutic method for prostate disease. Urology 2013, 81:e921-e927. (921).
138. Fan Z., Liu H., Mayer M., Deng C.X. Spatiotemporally controlled single cell sonoporation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:16486-16491.
139. Yang F., Gu N., Chen D., Xi X., Zhang D., Li Y., Wu J. Experimental study on cell self-sealing during sonoporation. J. Control. Release 2008, 131:205-210.
140. Jin L.F., Li F., Wang H.P., Wei F., Qin P., Du L.F. Ultrasound targeted microbubble destruction stimulates cellular endocytosis in facilitation of adeno-associated virus delivery. Int. J. Mol. Sci. 2013, 14:9737-9750.
141. Sundqvist T., Liu S.M. Hydrogen peroxide stimulates endocytosis in cultured bovine aortic endothelial cells. Acta Physiol. Scand. 1993, 149:127-131.
142. MacDonald P.E., Eliasson L., Rorsman P. Calcium increases endocytotic vesicle size and accelerates membrane fission in insulin-secreting INS-1 cells. J. Cell Sci. 2005, 118:5911-5920.
143. Saliez J., Bouzin C., Rath G., Ghisdal P., Desjardins F., Rezzani R., Rodella L.F., Vriens J., Nilius B., Feron O., Balligand J.L., Dessy C. Role of caveolar compartmentation in endothelium-derived hyperpolarizing factor-mediated relaxation: Ca2+ signals and gap junction function are regulated by caveolin in endothelial cells. Circulation 2008, 117:1065-1074.
144. Fan Z., Kumon R.E., Park J., Deng C.X. Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J. Control. Release 2010, 142:31-39.
145. Juffermans L.J., van Dijk A., Jongenelen C.A., Drukarch B., Reijerkerk A., de Vries H.E., Kamp O., Musters R.J. Ultrasound and microbubble-induced intra- and intercellular bioeffects in primary endothelial cells. Ultrasound Med. Biol. 2009, 35:1917-1927.
146. Juffermans L.J., Dijkmans P.A., Musters R.J., Visser C.A., Kamp O. Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H1595-H1601.
147. Tran T.A., Le Guennec J.Y., Bougnoux P., Tranquart F., Bouakaz A. Characterization of cell membrane response to ultrasound activated microbubbles. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2008, 55:44-49.
148. Juffermans L.J., Kamp O., Dijkmans P.A., Visser C.A., Musters R.J. Low-intensity ultrasound-exposed microbubbles provoke local hyperpolarization of the cell membrane via activation of BK(Ca) channels. Ultrasound Med. Biol. 2008, 34:502-508.
149. Guyton A.C., Hall J.E. Medical Physiology 2006, Elsevier Saunders, London.
150. Kumon R.E., Aehle M., Sabens D., Parikh P., Han Y.W., Kourennyi D., Deng C.X. Spatiotemporal effects of sonoporation measured by real-time calcium imaging. Ultrasound Med. Biol. 2009, 35:494-506.
151. Davies P.F. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 1995, 75:519-560.
152. Nilius B., Droogmans G., Wondergem R. Transient receptor potential channels in endothelium: solving the calcium entry puzzle?. Endothelium 2003, 10:5-15.
153. Apodaca G. Modulation of membrane traffic by mechanical stimuli. Am. J. Physiol. Ren. Physiol. 2002, 282:F179-F190.
154. Niwa K., Sakai J., Karino T., Aonuma H., Watanabe T., Ohyama T., Inanami O., Kuwabara M. Reactive oxygen species mediate shear stress-induced fluid-phase endocytosis in vascular endothelial cells. Free Radic. Res. 2006, 40:167-174.
155. Yudina A., Lepetit-Coiffé C.T.W.Moonen Evaluation of the temporal windown for drug delivery following ultrasound-mediated membrane permeability enhancement. Mol. Imaging Biol. 2011, 13:239-249.
156. Kooiman K., Emmer M., Foppen-Harteveld M., van Wamel A., de Jong N. Increasing the endothelial layer permeability through ultrasound-activated microbubbles. IEEE Trans. Biomed. Eng. 2010, 57:29-32.
157. Kooiman K., van der Steen A.F.W., de Jong N. Role of intracellular calcium and reactive oxygen species in microbubble-mediated alterations of endothelial layer permeability. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2013, 60:1811-1815.
158. Walker D.C., MacKenzie A., Hosford S. The structure of the tricellular region of endothelial tight junctions of pulmonary capillaries analyzed by freeze-fracture. Microvasc. Res. 1994, 48:259-281.
159. Burns A.R., Walker D.C., Brown E.S., Thurmon L.T., Bowden R.A., Keese C.R., Simon S.I., Entman M.L., Smith C.W. Neutrophil transendothelial migration is independent of tight junctions and occurs preferentially at tricellular corners. J. Immunol. 1997, 159:2893-2903.
160. Ushio-Fukai M., Frey R.S., Fukai T., Malik A.B. Reactive oxygen species and endothelial permeability. Free Radical Effects on Membranes 2008, 147-189. Elsevier Academic Press Inc., San Diego.
161. Birukov K.G. Cyclic stretch, reactive oxygen species, and vascular remodeling. Antioxid. Redox Signal. 2009, 11:1651-1667.
162. Mehta D., Malik A.B. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 2006, 86:279-367.
163. Kooiman K., Foppen-Harteveld M., van der Steen A.F.W., de Jong N. Sonoporation of endothelial cells by vibrating targeted microbubbles. J. Control. Release 2011, 154:35-41.
164. Lindner J.R. Molecular imaging of cardiovascular disease with contrast-enhanced ultrasonography. Nat. Rev. Cardiol. 2009, 6:475-481.
165. Mauldin F.W., Dhanaliwala A.H., Patil A.V., Hossack J.A. Real-time targeted molecular imaging using singular value spectra properties to isolate the adherent microbubble signal. Phys. Med. Biol. 2012, 57:5275-5293.
166. Needles A., Couture O., Foster F.S. A method for differentiating targeted microbubbles in real time using subharmonic micro-ultrasound and interframe filtering. Ultrasound Med. Biol. 2009, 35:1564-1573.
167. Zhao S., Kruse D.E., Ferrara K.W., Dayton P.A. Acoustic response from adherent targeted contrast agents. J. Acoust. Soc. Am. 2006, 120:EL63-EL69.
168. Escoffre J.M., Piron J., Novell A., Bouakaz A. Doxorubicin delivery into tumor cells with ultrasound and microbubbles. Mol. Pharm. 2011, 8:799-806.
169. Sternberg A., Amar M., Alfici R., Groisman G. Conclusions from a study of venous invasion in stage IV colorectal adenocarcinoma. J. Clin. Pathol. 2002, 55:17-21.
170. Eguchi S., Takatsuki M., Hidaka M., Soyama A., Tomonaga T., Muraoka I., Kanematsu T. Predictor for histological microvascular invasion of hepatocellular carcinoma: a lesson from 229 consecutive cases of curative liver resection. World J. Surg. 2010, 34:1034-1038.
171. Chang S., Guo J., Sun J., Zhu S., Yan Y., Zhu Y., Li M., Wang Z., Xu R.X. Targeted microbubbles for ultrasound mediated gene transfection and apoptosis induction in ovarian cancer cells. Ultrason. Sonochem. 2013, 20:171-179.
172. Cagol P.P., Pasqual E., Bacchetti S. Natural history of the neoplastic locoregional disease: clinical and pathological patterns. J. Exp. Clin. Cancer Res. 2003, 22:1-4.
173. Delalande A., Bouakaz A., Renault G., Tabareau F., Kotopoulis S., Midoux P., Arbeille B., Uzbekov R., Chakravarti S., Postema M., Pichon C. Ultrasound and microbubble-assisted gene delivery in Achilles tendons: long lasting gene expression and restoration of fibromodulin KO phenotype. J. Control. Release 2011, 156:223-230.
174. Park J., Fan Z., Deng C.X. Effects of shear stress cultivation on cell membrane disruption and intracellular calcium concentration in sonoporation of endothelial cells. J. Biomech. 2011, 44:164-169.
175. Mehier-Humbert S., Yan F., Frinking P., Schneider M., Guy R.H., Bettinger T. Ultrasound-mediated gene delivery: influence of contrast agent on transfection. Bioconjug. Chem. 2007, 18:652-662.
176. Cochran M., Wheatley M.A. In vitro gene delivery with ultrasound-triggered polymer microbubbles. Ultrasound Med. Biol. 2013, 39:1102-1119.
177. Böhmer M.R., Chlon C.H.T., Raju B.I., Chin C.T., Shevchenko T., Klibanov A.L. Focused ultrasound and microbubbles for enhanced extravasation. J. Control. Release 2010, 148:18-24.
178. Zhang Y., Tachibana R., Okamoto A., Azuma T., Sasaki A., Yoshinaka K., Tei Y., Takagi S., Matsumoto Y. Ultrasound-mediated gene transfection in vitro: effect of ultrasonic parameters on efficiency and cell viability. Int. J. Hyperth. 2012, 28:290-299.
179. Phillips L.C., Klibanov A.L., Wamhoff B.R., Hossack J.A. Localized ultrasound enhances delivery of rapamycin from microbubbles to prevent smooth muscle proliferation. J. Control. Release 2011, 154:42-49.
180. Phillips L.C., Klibanov A.L., Wamhoff B.R., Hossack J.A. Targeted gene transfection from microbubbles into vascular smooth muscle cells using focused, ultrasound-mediated delivery. Ultrasound Med. Biol. 2010, 36:1470-1480.
181. Chen S., Shohet R.V., Bekeredjian R., Frenkel P., Grayburn P.A. Optimization of ultrasound parameters for cardiac gene delivery of adenoviral or plasmid deoxyribonucleic acid by ultrasound-targeted microbubble destruction. J. Am. Coll. Cardiol. 2003, 42:301-308.
182. Unger E.C., McCreery T.P., Sweitzer R.H., Caldwell V.E., Wu Y. Acoustically active lipospheres containing paclitaxel: a new therapeutic ultrasound contrast agent. Invest. Radiol. 1998, 33:886-892.
183. Tartis M.S., McCallan J., Lum A.F.H., LaBell R., Stieger S.M., Matsunaga T.O., Ferrara K.W. Therapeutic effects of paclitaxel-containing ultrasound contrast agents. Ultrasound Med. Biol. 2006, 32:1771-1780.
184. Shortencarier M.J., Dayton P.A., Bloch S.H., Schumann P.A., Matsunaga T.O., Ferrara K.W. A method for radiation-force localized drug delivery using gas-filled lipospheres. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2004, 51:822-831.
185. Kheirolomoom A., Dayton P.A., Lum A.F., Little E., Paoli E.E., Zheng H., Ferrara K.W. Acoustically-active microbubbles conjugated to liposomes: characterization of a proposed drug delivery vehicle. J. Control. Release 2007, 118:275-284.
186. Luan Y., Faez T., Gelderblom E., Skachkov I., Geers B., Lentacker I., van der Steen T., Versluis M., de Jong N. Acoustical properties of individual liposome-loaded microbubbles. Ultrasound Med. Biol. 2012, 38:2174-2185.
187. McLaughlan J., Ingram N., Abou-Saleh R., Harput S., Evans T., Evens S., Coletta L., Freear S. High-frequency subharmonic imaging of liposome-loaded microbubbles. IEEE Ultrasonics Symposium Proceedings, Czech Republic, Prague 2013, (IUS1-PC3-2).
188. Luan Y., Lajoinie G., Gelderblom E., Skachkov I., Dewitte H., Lentacker I., van Rooij T., Vos H.J., van der Steen A.F.W., Versluis M., de Jong N. Liposome shedding from a vibrating microbubble on nanoseconds timescale. IEEE Ultrasonics Symposium Proceedings, Czech Republic, Prague 2013, (IUS1-B1-2).
189. Tlaxca J.L., Rychak J.J., Ernst P.B., Konkalmatt P.R., Shevchenko T.I., Pizzaro T.T., Rivera-Nieves J., Klibanov A.L., Lawrence M.B. Ultrasound-based molecular imaging and specific gene delivery to mesenteric vasculature by endothelial adhesion molecule targeted microbubbles in a mouse model of Crohn's disease. J. Control. Release 2013, 165:216-225.
190. Xie A., Belcik T., Qi Y., Morgan T.K., Champaneri S.A., Taylor S., Davidson B.P., Zhao Y., Klibanov A.L., Kuliszewski M.A., Leong-Poi H., Ammi A., Lindner J.R. Ultrasound-mediated vascular gene transfection by cavitation of endothelial-targeted cationic microbubbles. Jacc Cardiovasc. Imaging 2012, 5:1253-1262.
191. Phillips L.C., Klibanov A.L., Wamhoff B.R., Hossack J.A. Intravascular ultrasound detection and delivery of molecularly targeted microbubbles for gene delivery. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2012, 59:1596-1601.
192. Fan C.H., Ting C.Y., Liu H.L., Huang C.Y., Hsieh H.Y., Yen T.C., Wei K.C., Yeh C.K. Antiangiogenic-targeting drug-loaded microbubbles combined with focused ultrasound for glioma treatment. Biomaterials 2013, 34:2142-2155.
193. Lum A.F., Borden M.A., Dayton P.A., Kruse D.E., Simon S.I., Ferrara K.W. Ultrasound radiation force enables targeted deposition of model drug carriers loaded on microbubbles. J. Control. Release 2006, 111:128-134.
194. Lentacker I., de Smedt S.C., Demeester J., van Marck V., Bracke M., Sanders N.N. Lipoplex-loaded microbubbles for gene delivery: a Trojan horse controlled by ultrasound. Adv. Funct. Mater. 2007, 17:1910-1916.
195. Lentacker I., Geers B., Demeester J., de Smedt S.C., Sanders N.N. Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved. Mol. Ther. 2010, 18:101-108.
196. Geers B., Lentacker I., Sanders N.N., Demeester J., Meairs S., De Smedt S.C. Self-assembled liposome-loaded microbubbles: the missing link for safe and efficient ultrasound triggered drug-delivery. J. Control. Release 2011, 152:249-256.
197. Yang D., Gao Y.H., Tan K.B., Zuo Z.X., Yang W.X., Hua X., Li P.J., Zhang Y., Wang G. Inhibition of hepatic fibrosis with artificial microRNA using ultrasound and cationic liposome-bearing microbubbles. Gene Ther. 2013, 20:1140-1148.
198. Klibanov A.L., Shevchenko T.I., Raju B.I., Seip R., Chin C.T. Ultrasound-triggered release of materials entrapped in microbubble-liposome constructs: a tool for targeted drug delivery. J. Control. Release 2010, 148:13-17.
199. Borden M.A., Caskey C.F., Little E., Gillies R.J., Ferrara K.W. DNA and polylysine adsorption and multilayer construction onto cationic lipid-coated microbubbles. Langmuir 2007, 23:9401-9408.
200. Christiansen J.P., French B.A., Klibanov A.L., Kaul S., Lindner J.R. Targeted tissue transfection with ultrasound destruction of plasmid-bearing cationic microbubbles. Ultrasound Med. Biol. 2003, 29:1759-1767.
201. Vannan M., McCreery T., Li P., Han Z., Unger E., Kuersten B., Nabel E., Rajagopalan S. Ultrasound-mediated transfection of canine myocardium by intravenous administration of cationic microbubble-linked plasmid DNA. J. Am. Soc. Echocardiogr. 2002, 15:214-218.
202. Carson A.R., McTiernan C.F., Lavery L., Hodnick A., Grata M., Leng X., Wang J., Chen X., Modzelewski R.A., Villanueva F.S. Gene therapy of carcinoma using ultrasound-targeted microbubble destruction. Ultrasound Med. Biol. 2011, 37:393-402.
203. Porter T.R., Hiser W.L., Kricsfeld D., Deligonul U., Xie F., Iversen P., Radio S. Inhibition of carotid artery neointimal formation with intravenous microbubbles. Ultrasound Med. Biol. 2001, 27:259-265.
204. Taniyama Y., Tachibana K., Hiraoka K., Namba T., Yamasaki K., Hashiya N., Aoki M., Ogihara T., Yasufumi K., Morishita R. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002, 105:1233-1239.
205. Shohet R.V., Chen S., Zhou Y.T., Wang Z., Meidell R.S., Unger R.H., Grayburn P.A. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 2000, 101:2554-2556.
206. Lentacker I., de Geest B.G., Vandenbroucke R.E., Peeters L., Demeester J., de Smedt S.C., Sanders N.N. Ultrasound-responsive polymer-coated microbubbles that bind and protect DNA. Langmuir 2006, 22:7273-7278.
207. Tinkov S., Winter G., Coester C., Bekeredjian R. New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: Part I-Formulation development and in-vitro characterization. J. Control. Release 2010, 143:143-150.
208. Kang J., Wu X., Wang Z., Ran H., Xu C., Wu J., Wang Z., Zhang Y. Antitumor effect of docetaxel-loaded lipid microbubbles combined with ultrasound-targeted microbubble activation on VX2 rabbit liver tumors. J. Ultrasound Med. 2010, 29:61-70.
209. Xing W., Gang W.Z., Yong Z., Yi Z.Y., Shan X.C., Tao R.H. Treatment of xenografted ovarian carcinoma using paclitaxel-loaded ultrasound microbubbles. Acad. Radiol. 2008, 15:1574-1579.
210. Li P., Zheng Y., Ran H., Tan J., Lin Y., Zhang Q., Ren J., Wang Z. Ultrasound triggered drug release from 10-hydroxycamptothecin-loaded phospholipid microbubbles for targeted tumor therapy in mice. J. Control. Release 2012, 162:349-354.
211. Ting C.Y., Fan C.H., Liu H.L., Huang C.Y., Hsieh H.Y., Yen T.C., Wei K.C., Yeh C.K. Concurrent blood-brain barrier opening and local drug delivery using drug-carrying microbubbles and focused ultrasound for brain glioma treatment. Biomaterials 2012, 33:704-712.
212. Phillips L.C., Dhanaliwala A.H., Klibanov A.L., Hossack J.A., Wamhoff B.R. Focused ultrasound-mediated drug delivery from microbubbles reduces drug dose necessary for therapeutic effect on neointima formation-brief report. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2853-2855.
213. Carson A.R., McTiernan C.F., Lavery L., Grata M., Leng X., Wang J., Chen X., Villanueva F.S. Ultrasound-targeted microbubble destruction to deliver siRNA cancer therapy. Cancer Res. 2012, 72:6191-6199.
214. Ren J., Xu C., Zhou Z., Zhang Y., Li X., Zheng Y., Ran H., Wang Z. A novel ultrasound microbubble carrying gene and Tat peptide: preparation and characterization. Acad. Radiol. 2009, 16:1457-1465.
215. Bekeredjian R., Chen S., Frenkel P.A., Grayburn P.A., Shohet R.V. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 2003, 108:1022-1026.
216. Liao A.H., Li Y.K., Lee W.J., Wu M.F., Liu H.L., Kuo M.L. Estimating the delivery efficiency of drug-loaded microbubbles in cancer cells with ultrasound and bioluminescence imaging. Ultrasound Med. Biol. 2012, 38:1938-1948.
217. Wheatley M.A., Cochran M.C., Eisenbrey J.R., Oum K.L. Cellular signal transduction can be induced by TRAIL conjugated to microcapsules. J. Biomed. Mater. Res. A 2012, 100:2602-2611.
218. Eisenbrey J.R., Huang P., Hsu J., Wheatley M.A. Ultrasound triggered cell death in vitro with doxorubicin loaded poly lactic-acid contrast agents. Ultrasonics 2009, 49:628-633.
219. Eisenbrey J.R., Burstein O.M., Kambhampati R., Forsberg F., Liu J.B., Wheatley M.A. Development and optimization of a doxorubicin loaded poly(lactic acid) contrast agent for ultrasound directed drug delivery. J. Control. Release 2010, 143:38-44.
220. Fokong S., Theek B., Wu Z., Koczera P., Appold L., Jorge S., Resch-Genger U., van Zandvoort M., Storm G., Kiessling F., Lammers T. Image-guided, targeted and triggered drug delivery to tumors using polymer-based microbubbles. J. Control. Release 2012, 163:75-81.
221. Cochran M.C., Eisenbrey J., Ouma R.O., Soulen M., Wheatley M.A. Doxorubicin and paclitaxel loaded microbubbles for ultrasound triggered drug delivery. Int. J. Pharm. 2011, 414:161-170.
222. Niu C., Wang Z., Lu G., Krupka T.M., Sun Y., You Y., Song W., Ran H., Li P., Zheng Y. Doxorubicin loaded superparamagnetic PLGA-iron oxide multifunctional microbubbles for dual-mode US/MR imaging and therapy of metastasis in lymph nodes. Biomaterials 2013, 34:2307-2317.
223. Zheng Y., Zhang Y., Ao M., Zhang P., Zhang H., Li P., Qing L., Wang Z., Ran H. Hematoporphyrin encapsulated PLGA microbubble for contrast enhanced ultrasound imaging and sonodynamic therapy. J. Microencapsul. 2012, 29:437-444.
224. Seemann S., Hauff P., Schultze-Mosgau M., Lehmann C., Reszka R. Pharmaceutical evaluation of gas-filled microparticles as gene delivery system. Pharm. Res. 2002, 19:250-257.
225. Wheatley M.A., Forsberg F., Oum K., Ro R., El-Sherif D. Comparison of in vitro and in vivo acoustic response of a novel 50:50 PLGA contrast agent. Ultrasonics 2006, 44:360-367.
226. Eisenbrey J.R., Soulen M.C., Wheatley M.A. Delivery of encapsulated doxorubicin by ultrasound-mediated size reduction of drug-loaded polymer contrast agents. IEEE Trans. Biomed. Eng. 2010, 57:24-28.
227. Maeda H., Wu J., Sawa T., Matsumura Y., Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J. Control. Release 2000, 65:271-284.
228. Anderson J.M., Shive M.S. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv. Drug Deliv. Rev. 1997, 28:5-24.
229. Cochran M.C., Eisenbrey J.R., Soulen M.C., Schultz S.M., Ouma R.O., White S.B., Furth E.E., Wheatley M.A. Disposition of ultrasound sensitive polymeric drug carrier in a rat hepatocellular carcinoma model. Acad. Radiol. 2011, 18:1341-1348.
230. Shi W.T., Böhmer M., van Wamel A., Celebi M., Klibanov A.L., Chin C.T., Chlon C., Emmer M., Kooiman K., de Jong N., Hall C.S. Ultrasound therapy with drug loaded microcapsules. IEEE Ultrasonics Symposium Proceedings, New York, USA 2007, 773-776.
231. Skyba D.M., Price R.J., Linka A.Z., Skalak T.C., Kaul S. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation 1998, 98:290-293.
232. Price R.J., Skyba D.M., Kaul S., Skalak T.C. Delivery of colloidal particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound. Circulation 1998, 98:1264-1267.