Potential and problems in ultrasound-responsive drug delivery systems

International Journal of Nanomedicine

Volumn 8, Issue , 2013, Pages 1621-1633

  Zhao, Ying Zheng ^a,c   Du, Li Na ^b   Lu, Cui Tao ^a   Jin, Yi Guang ^b   Ge, Shu Ping ^c  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^c ST CHRISTOPHER'S HOSPITAL FOR CHILDREN   (United States)

Author keywords

Clinical application; Targeted therapy; Ultrasound

Indexed keywords

ALBUNEX; BISPHERES; CARMUSTINE; CONTRAST MEDIUM; CURCUMIN; DOXORUBICIN; DRUG CARRIER; FIBROBLAST GROWTH FACTOR 1; MACROGOL; NANOBUBBLE; NANODROPLET; PACLITAXEL; PERFLEXANE; PERFLUBUTANE; PERFLUTREN; POLYMERIC MICELLE; SHU 508; SONOVUE; TISSUE PLASMINOGEN ACTIVATOR; UNCLASSIFIED DRUG; UROKINASE;

APOPTOSIS; BLOOD BRAIN BARRIER; BREAST TUMOR; CANCER TISSUE; CELL MEMBRANE PERMEABILITY; CLINICAL PRACTICE; DNA DAMAGE; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DOSAGE FORM COMPARISON; DRUG FORMULATION; DRUG HALF LIFE; DRUG PENETRATION; DRUG RELEASE; DRUG TRANSPORT; ENCAPSULATION; ENZYME PHOSPHORYLATION; FLUORESCENCE MICROSCOPY; HEART PROTECTION; HUMAN; ISCHEMIC HEART DISEASE; MEDICAL PROCEDURES; MICROBUBBLE; MICROEMULSION; MOLECULARLY TARGETED THERAPY; NONHUMAN; OVARY TUMOR; PANCREAS TUMOR; REVIEW; THERANOSTIC; THROMBOSIS; ULTRASOUND; ULTRASOUND RESPONSIVE DRUG DELIVERY SYSTEM; VASCULAR DISEASE;

CLINICAL APPLICATION; TARGETED THERAPY; ULTRASOUND;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; NANOMEDICINE; SONICATION; ULTRASONICS; ULTRASONOGRAPHY, INTERVENTIONAL;

EID: 84876720445     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S43589     Document Type: Review

References (127)

1. Timko B P, Dvir T, Kohane DS. Remotely triggerable drug delivery systems. Adv Mater. 2010;2:4925-4943.
2. Mulvagh SL, DeMaria AN, Feinstein SB, et al. Contrast echocardiography: current and future applications. J Am Soc Echocardiogr. 2000;13:331-342.
3. Bouakaz A, Versluis M, de Jong N. High-speed optical observations of contrast agent destruction. Ultrasound Med Biol. 2005;31:391-399.
4. Torchilin V P. Targeted pharmaceutical nanocarriers for cancer therapy and imaging. AAPS J. 2007;9:E128-E147.
5. Schroeder A, Honen R, Turjeman K, Gabizon A, Kost J, Barenholz Y. Ultrasound triggered release of cisplatin from liposomes in murine tumors. J Control Release. 2009;137:63-68.
6. Zhao YZ, Luo YK, Lu CT, et al. Phospholipids-based microbubbles sonoporation pore size and reseal of cell membrane cultured in vitro. J Drug Target. 2008;16:18-25.
7. Rapoport NY, Christensen DA, Fain HD, Barrows L, Gao Z. Ultrasound-triggered drug targeting of tumor in vitro and in vivo. Ultrasonics. 2004;42:943-950.
8. Otani K, Yamahara K, Ohnishi S, Obata H, Kitamura S, Nagaya N. Nonviral delivery of siRNA into mesenchymal stem cells by a combination of ultrasound and microbubbles. J Control Release. 2009;133:146-153.
9. Suzuki R, Oda Y, Utoguchi N, Maruyama K. Progress in the development of ultrasound-mediated gene delivery systems utilizing nano- and microbubbles. J Control Release. 2011;149:36-41.
10. Zhao Y, Lu C, Fu H, et al. Phospholipid-based ultrasonic microbubbles for loading protein and ultrasound-triggered release. Drug Dev Ind Pharm. 2009;35:1121-1127.
11. Wang Y, Li X, Zhou Y, Huang P, Xu Y. Preparation of nanobubbles for ultrasound imaging and intracelluar drug delivery. Int J Pharm. 2010;384:148-153.
12. Suzuki M, Koshiyama K, Shinohara F, et al. Nanobubbles enhanced drug susceptibility of cancer cells using ultrasound. International Congress Series. 2005;1284:338-339.
13. Du L, Jin Y, Zhou W, Zhao J. Ultrasound-triggered drug release and enhanced anticancer effect of doxorubicin-loaded poly (D,L-lactide-co-glycolide)-methoxy-poly(ethylene glycol) nanodroplets. Ultrasound Med Biol. 2011;37:1252-1258.
14. Ibsen S, Benchimol M, Simberg D, Schutt C, Steiner J, Esener S. A novel nested liposome drug delivery vehicle capable of ultrasound triggered release of its payload. J Control Release. 2011;155:358-366.
15. Zhao Y, Dai D, Lu C, et al. Using acoustic cavitation to enhance chemotherapy of DOX liposomes: experiment in vitro and in vivo. Drug Dev Ind Pharm. 2012;38:1090-1098.
16. Medina J, Salvado A, del Pozo A. Use of ultrasound to prepare lipid emulsions of lorazepam for intravenous injection. Int J Pharm. 2001;216:1-8.
17. Marin A, Muniruzzaman M, Rapoport N. Acoustic activation of drug delivery from polymeric micelles: effect of pulsed ultrasound. J Control Release. 2001;71:239-249.
18. Rapoport N. Combined cancer therapy by micellar-encapsulated drug and ultrasound. Int J Pharm. 2004;277:155-162.
19. Marin A, Sun H, Husseini GA, Pitt WG, Christensena DA, Rapoport N Y. Drug delivery in Pluronic micelles: effect of high-frequency ultrasound on drug release from micelles and intracellular uptake. J Control Release. 2002;84:39-47.
20. Suzuki R, Namai E, Oda Y, et al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release. 2010;142:245-250.
21. Negishi Y, Endo Y, Fukuyama T, et al. Delivery of siRNA into the cytoplasm by liposomal bubbles and ultrasound. J Control Release. 2008;132:124-130.
22. Rapoport NY, Kennedy AM, Shea JE, Scaife CL, Nam K-H. Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles. J Control Release. 2009;138:268-276.
23. Harada Y, Ogawa K, Irie Y, et al. Ultrasound activation of TiO2 in melanoma tumors. J Control Release. 2011;149:190-195.
24. Lee M-H, Lin H-Y, Chen H-C, Thomas JL. Ultrasound mediates the release of curcumin from microemulsions. Langmuir. 2008;24: 1707-1713.
25. Eisenbrey JR, Burstein OM, Kambhampati R, Forsberg F, Liu JB, Wheatley MA. Development and optimization of a doxorubicin loaded poly(lactic acid) contrast agent for ultrasound directed drug delivery. J Control Release. 2010;143:38-44.
26. Lu C, Zhao Y, Wu Y, et al. Experiment on enhancing antitumor effect of intravenous epirubicin hydrochloride by acoustic cavitation in situ combined with phospholipid-based microbubbles. Cancer Chemother Pharmacol. 2011;68:343-348.
27. Li P, Zheng Y, Ran H, et al. Ultrasound triggered drug release from 10-hydroxycamptothecin-loaded phospholipid microbubbles for targeted tumor therapy in mice. J Control Release. 2012;162:349-354.
28. Lu C, Zhao Y, Gao H, et al. Comparing encapsulation effciency and ultrasound-triggered release for protein between phospholipid-based microbubbles and liposomes. J Microencapsul. 2010;27:115-121.
29. Zhao Y, Lu C, Li X, et al. Improving the cardio protective effect of aFGF in ischemic myocardium with ultrasound-mediated cavitation of heparin modifed microbubbles: preliminary experiment. J Drug Target. 2012;20:623-631.
30. Yoon CS, Park JH. Ultrasound-mediated gene delivery. Expert Opin Drug Deliv. 2010;7:321-330.
31. Haag P, Frauscher F, Gradl J, et al. Microbubble-enhanced ultrasound to deliver an antisense oligodeoxynucleotide targeting the human androgen receptor into prostate tumours. J Steroid Biochem Mol Biol. 2006;102: 103-113.
32. Zhao Y, Lu C. Factors that affect the efficiency of antisense oligodeoxyribonucleotide transfection by insonated gas-flled lipid microbubbles. J Nanopart Res. 2008;10:449-454.
33. Nomikou N, McHale A P. Exploiting ultrasound-mediated effects in delivering targeted, site-specifc cancer therapy. Cancer Lett. 2010;296: 133-143.
34. Bioley G, Lassus A, Bussat P, Terrettaz J, Tranquart F, Corthésy B. Gas-flled microbubble-mediated delivery of antigen and the induction of immune responses. Biomaterials. 2012;33:5935-5946.
35. Lima EG, Durney KM, Sirsi SR, et al. Microbubbles as biocompatible porogens for hydrogel scaffolds. Acta Biomater. 2012;8:4334-4341.
36. Seto JE, Polat BE, Lopez RFV, Blankschtein D, Langer R. Effects of ultrasound and sodium lauryl sulfate on the transdermal delivery of hydrophilic permeants: comparative in vitro studies with full-thickness and split-thickness pig and human skin. J Control Release. 2010;145: 26-32.
37. Polat BE, Hart D, Langer R, Blankschtein D. Ultrasound-mediated transdermal drug delivery: mechanisms, scope, and emerging trends. J Control Release. 2011;152:330-348.
38. Burgess A, Huang Y, Querbes W, Sah DW, Hynynen K. Focused ultrasound for targeted delivery of siRNA and effcient knockdown of Htt expression. J Control Release. 2012;163:125-129.
39. Jin H, Tan H, Zhao L, et al. Ultrasound-triggered thrombolysis using urokinase-loaded nanogels. Int J Pharm. 2012;434:384-390.
40. Zhou XB, Qin H, Li J, et al. Platelet-targeted microbubbles inhibit re-occlusion after thrombolysis with transcutaneous ultrasound and microbubbles. Ultrasonics. 2011;51:270-274.
41. Vykhodtseva N, McDannold N, Hynynen K. Progress and problems in the application of focused ultrasound for blood-brain barrier disruption. Ultrasonics. 2008;48:279-296.
42. Liu H-L, Hua M-Y, Chen P-Y, et al. Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment. Radiology. 2010;255:415-425.
43. Rapoport N, Kennedy AM, Shea JE, Scaife CL, Nam K-H. Ultrasonic nanotherapy of pancreatic cancer: lessons from ultrasound imaging. Mol Pharm. 2009;7:22-31.
44. Ferrara K, Pollard R, Borden M. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng. 2007;9:415-447.
45. Kabalnov A, Klein D, Pelura T, Schutt E, Weers J. Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory. Ultrasound Med Biol. 1998;24:739-749.
46. Korenaga K, Korenaga M, Furukawa M, Yamasaki T, Sakaida I. Usefulness of Sonazoid contrast-enhanced ultrasonography for hepatocellular carcinoma: comparison with pathological diagnosis and superparamagnetic iron oxide magnetic resonance images. J Gastroenterol. 2009;44:733-741.
47. Watanabe R, Matsumura M, Munemasa T, Fujimaki M, Suematsu M. Mechanism of hepatic parenchyma-specifc contrast of microbubble-based contrast agent for ultrasonography: microscopic studies in rat liver. Invest Radiol. 2007;42:643-651.
48. Qin S, Caskey CF, Ferrara K W. Ultrasound contrast microbubbles in imaging and therapy: physical principles and engineering. Phys Med Biol. 2009;54:R27-R57.
49. Azmin M, Mohamedi G, Edirisinghe M, Stride E P. Dissolution of coated microbubbles: the effect of nanoparticles and surfactant concentration. Mater Sci Eng C Mater Biol Appl. 2012;32:2654-2658.
50. Rapoport N, Nam KH, Gupta R, et al. Ultrasound-mediated tumor imaging and nanotherapy using drug loaded, block copolymer stabilized perfuorocarbon nanoemulsions. J Control Release. 2011;153:4-15.
51. Sheeran PS, Luois S, Dayton PA, Matsunaga TO. Formulation and acoustic studies of a new phase-shift agent for diagnostic and therapeutic ultrasound. Langmuir. 2011;27:10412-10420.
52. Fang J, Nakamura H, Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv Drug Deliv Rev. 2011;63:136-151.
53. Sheeran PS, Wong V P, Luois S, et al. Decafuorobutane as a phase-change contrast agent for low-energy extravascular ultrasonic imaging. Ultrasound Med Biol. 2011;37:1518-1530.
54. Zhao Y, Sun C, Lu C, et al. Characterization and anti-tumor activity of chemical conjugation of doxorubicin in polymeric micelles (DOX-P) in vitro. Cancer Lett. 2011;311:187-194.
55. Mitragotri S. Sonophoresis: a 50-year journey. Drug Discov Today. 2004;9:735-736.
56. Mitragotri S, Blankschtein D, Langer R. Transdermal drug delivery using low frequency sonophoresis. Pharm Res. 1996;13:411-420.
57. Gaertner W. Frequency dependence of ultrasonic cavitation. J Acoust Soc Am. 1954;26:977-980.
58. Kushner J, Kim D, So P, Blankschtein D, Langer R. Dual-channel two-photon microscopy study of transdermal transport in skin treated with low-frequency ultrasound and a chemical enhancer. J Invest Dermatol. 2007;127:2832-2846.
59. Alvarez-Román R, Merino G, Kalia Y, Naik A, Guy R. Skin permeability enhancement by low frequency sonophoresis: lipid extraction and transport pathways. J Pharm Sci. 2003;92:1138-1146.
60. Polat B, Figueroa P, Blankschtein D, Langer R. Transport pathways and enhancement mechanisms within localized and non-localized transport regions in skin treated with low-frequency sonophoresis and sodium lauryl sulfate. J Pharm Sci. 2011;100:512-529.
61. Wolloch L, Kost J. The importance of microjet vs shock wave formation in sonophoresis. J Control Release. 2010;148:204-211.
62. Lee S, Choi K, Menon G, et al. Penetration pathways induced by low-frequency sonophoresis with physical and chemical enhancers: iron oxide nanoparticles versus lanthanum nitrates. J Invest Dermatol. 2010;130:1063-1072.
63. Ueda H, Mutoh M, Seki T, Kobayashi D, Morimoto Y. Acoustic cavitation as an enhancing mechanism of low-frequency sonophoresis for transdermal drug delivery. Biol Pharm Bull. 2009;32:916-920.
64. Lavon I, Grossman N, Kost J, Kimmel E, Enden G. Bubble growth within the skin by rectifed diffusion might play a signifcant role in sonophoresis. J Control Release. 2007;117:246-255.
65. Morimoto Y, Mutoh M, Ueda H, et al. Elucidation of the transport pathway in hairless rat skin enhanced by low frequency sonophoresis based on the solute-water transport relationship and confocal microscopy. J Control Release. 2005;103:587-597.
66. Spierings E, Brevard J, Katz N. Two-minute skin anesthesia through ultrasound pretreatment and iontophoretic delivery of a topical anesthetic: a feasibility study. Pain Med. 2008;9:55-59.
67. Brown M, Martin G, Jones S, Akomeah F. Dermal and transdermal drug delivery systems: current and future prospects. Drug Deliv. 2006;13: 175-187.
68. Tang H, Blankschtein D, Langer R. Prediction of steady-state skin permeabilities of polar and nonpolar permeants across excised pig skin based on measurements of transient diffusion: characterization of hydration effects on the skin porous pathway. J Pharm Sci. 2002;91: 1891-1907.
69. Pardridge WM. Advances in cell biology of blood-brain barrier transport. Semin Cell Biol. 1991;2:419-426.
70. McDannold N, Arvanitis CD, Vykhodtseva N, Livingstone MS. Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and effcacy evaluation in rhesus macaques. Cancer Res. 2012;72:3652-3663.
71. Uesugi Y, Kawata H, Jo J-i, Saito Y, Tabata Y. An ultrasound-responsive nano delivery system of tissue-type plasminogen activator for thrombolytic therapy. J Control Release. 2010;147:269-277.
72. Diederich CJ, Hynynen K. Ultrasound technology for hyperthermia. Ultrasound Med Biol. 1999;25:871-887.
73. Chapelon JY, Ribault M, Vernier F, Souchon R, Gelet A. Treatment of localised prostate cancer with transrectal high intensity focused ultrasound. Eur J Ultrasound. 1999;9:31-38.
74. Gelet A, Chapelon J Y, Poissonnier L, et al. Local recurrence of prostate cancer after external beam radiotherapy: early experience of salvage therapy using high-intensity focused ultrasonography. Urology. 2004;63:625-629.
75. Kohrmann KU, Michel MS, Gaa J, Marlinghaus E, Alken P. High intensity focused ultrasound as noninvasive therapy for multifocal renal cell carcinoma: case study and review of the literature. J Urol. 2002;167:2397-2403.
76. Wu F, Wang ZB, Chen WZ, et al. Extracorporeal high intensity focused ultrasound ablation in the treatment of patients with large hepatocellular carcinoma. Ann Surg Oncol. 2004;11:1061-1069.
77. Wu F, Wang ZB, Cao YD, et al. A randomised clinical trial of high-intensity focused ultrasound ablation for the treatment of patients with localised breast cancer. Br J Cancer. 2003;89:2227-2233.
78. Chen W, Wang Z, Wu F, et al. High intensity focused ultrasound in the treatment of primary malignant bone tumor. Zhonghua Zhong Liu Za Zhi. 2002;24:612-615. Chinese.
79. Chan AH, Fujimoto VY, Moore DE, Martin RW, Vaezy S. An image-guided high intensity focused ultrasound device for uterine fbroids treatment. Med Phys. 2002;29:2611-2620.
80. Vaezy S, Noble ML, Keshavarzi A, et al. Liver hemostasis with high-intensity ultrasound: repair and healing. J Ultrasound Med Biol. 2004;23:217-225.
81. Afadzi M, Davies CD, Hansen YH, et al. Effect of ultrasound parameters on the release of liposomal calcein. Ultrasound Med Biol. 2012;38: 476-486.
82. Ohl CD, Arora M, Ikink R, et al. Sonoporation from jetting cavitation bubbles. Biophys J. 2006;91:4285-4295.
83. Lentacker I, Wang N, Vandenbroucke RE, Demeester J, Smedt SCD, Sanders NN. Ultrasound exposure of lipoplex loaded microbubbles facilitates direct cytoplasmic entry of the lipoplexes. Mol Pharm. 2009;6:457-467.
84. Geers B, Lentacker I, Alonso A, et al. Elucidating the mechanisms behind sonoporation with adeno-associated virus-loaded microbubbles. Mol Pharm. 2011;8:2244-2251.
85. Meijering BD, Juffermans LJ, 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.
86. Unger EC, Hersh E, Vannan M, Matsunaga TO, McCreery T. Local drug and gene delivery through microbubbles. Prog Cardiovasc Dis. 2001;44:45-54.
87. Kalantarinia K, Belcik JT, Patrie JT, Wei K. Real-time measurement of renal blood fow in healthy subjects using contrast-enhanced ultrasound. Am J Physiol Renal Physiol. 2009;297:F1129-F1134.
88. Taniyama Y, Tachibana K, Hiraoka K, et al. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation. 2002;105: 1233-1239.
89. Mannaris C, Averkiou MA. Investigation of microbubble response to long pulses used in ultrasound-enhanced drug delivery. Ultrasound Med Biol. 2012;38:681-691.
90. Ye h CK, Su SY. Effects of acoustic insonation parameters on ultrasound contrast agent destruction. Ultrasound Med Biol. 2008;34: 1281-1291.
91. Xu Z, Fowlkes JB, Cain CA. A new strategy to enhance cavitational tissue erosion using a high-intensity, initiating sequence. IEEE Trans Ultrason Ferroelectr Freq Control. 2006;53:1412-1424.
92. Zhu C, He S, Shan M, Chen J. Study of a peak in cavitation activity from HIFU exposures using TA fuorescence. Ultrasonics. 2006; 44 Suppl 1:e349-e351.
93. Chen H, Li X, Wan M. The inception of cavitation bubble clouds induced by high-intensity focused ultrasound. Ultrasonics. 2006; 44 Suppl 1:e427-e429.
94. Chen WS, Brayman AA, Matula TJ, Crum LA. Inertial cavitation dose and hemolysis produced in vitro with or without Optison. Ultrasound Med Biol. 2003;29:725-737.
95. Tu J, Matula TJ, Brayman AA, Crum LA. Inertial cavitation dose produced in ex vivo rabbit ear arteries with Optison by 1-MHz pulsed ultrasound. Ultrasound Med Biol. 2006;32:281-288.
96. Chen WS, Matula TJ, Brayman AA, Crum LA. A comparison of the fragmentation thresholds and inertial cavitation doses of different ultrasound contrast agents. J Acoust Soc Am. 2003;113:643-651.
97. McDannold N, Vykhodtseva N, Hynynen K. Use of ultrasound pulses combined with defnity for targeted blood-brain barrier disruption: a feasibility study. Ultrasound Med Biol. 2007;33: 584-590.
98. Duvshani-Eshet M, Machluf M. Therapeutic ultrasound optimization for gene delivery: a key factor achieving nuclear DNA localization. J Control Release. 2005;108:513-528.
99. Miller M W, Everbach EC, Miller WM, Battaglia L F. Biological and environmental factors affecting ultrasound-induced hemolysis in vitro: 2. Medium dissolved gas (pO2) content. Ultrasound Med Biol. 2003;29:93-102.
100. Brotchie A, Statham T, Zhou M, Dharmarathne L, Grieser F, Ashokkumar M. Acoustic bubble sizes, coalescence, and sonochemical activity in aqueous electrolyte solutions saturated with different gases. Langmuir. 2010;26:12690-12695.
101. Chappell JC, Song J, Burke C W, Klibanov AL, Price RJ. Targeted delivery of nanoparticles bearing fibroblast growth factor-2 by ultrasonic microbubble destruction for therapeutic arteriogenesis. Small. 2008;4:1769-1777.
102. Hynynen K, Clement G, McDannold N, Vykhodtseva N. The feasibility of noninvasive image-guided treatments of brain disodereds by focused ultrasound. J Acoust Soc Am. 2004;115:24-46.
103. Furusawa Y, Fujiwara Y, Hassan MA, et al. Inhibition of DNA-dependent protein kinase promotes ultrasound-induced cell death including apoptosis in human leukemia cells. Cancer Lett. 2012;322: 107-112.
104. Furusawa Y, Fujiwara Y, Campbell P, et al. DNA double-strand breaks induced by cavitational mechanical effects of ultrasound in cancer cell lines. PLoS One. 2012;7:e29012.
105. Lammers T, Aime S, Hennink WE, Storm G, Kiessling F. Theranostic nanomedicine. Acc Chem Res. 2011;44:1029-1038.
106. Liu Z, Lammers T, Ehling J, et al. Iron oxide nanoparticle-containing microbubble composites as contrast agents for MR and ultrasound dual-modality imaging. Biomaterials. 2011;32:6155-6163.
107. Lim YT, Cho MY, Kang JH, et al. Perfuorodecalin/[InGaP/ZnS quantum dots] nanoemulsions as 19F MR/optical imaging nanoprobes for the labeling of phagocytic and nonphagocytic immune cells. Biomaterials. 2010;31:4964-4971.
108. Pochon S, Tardy I, Bussat P, et al. BR55: a lipopeptide-based VEGFR2-targeted ultrasound contrast agent for molecular imaging of angiogen-esis. Invest Radiol. 2010;45:89-95.
109. Sundaram J, Mellein BR, Mitragotri S. An experimental and theoretical analysis of ultrasound-induced permeabilization of cell membranes. Biophys J. 2003;84:3087-3101.
110. Schlicher RK, Hutcheson JD, Radhakrishna H, Apkarian R P, Prausnitz MR. Changes in cell morphology due to plasma membrane wounding by acoustic cavitation. Ultrasound Med Biol. 2010;36: 677-692.
111. van Wamel A, Kooiman K, Emmer M, ten Cate FJ, Versluis M, de Jong N. Ultrasound microbubble induced endothelial cell permeability. J Control Release. 2006;116:e100-e102.
112. Yudina A, Lepetit-Coiffe M, Moonen CT. Evaluation of the temporal window for drug delivery following ultrasound-mediated membrane permeability enhancement. Mol Imaging Biol. 2011;13:239-249.
113. Yudina A, de Smet M, Lepetit-Coiffé M, et al. Ultrasound-mediated intracellular drug delivery using microbubbles and temperature-sensitive liposomes. J Control Release. 2011;155:442-448.
114. Maxwell AD, Cain CA, Duryea AP, Yuan L, Gurm HS, Xu Z. Noninvasive thrombolysis using pulsed ultrasound cavitation therapy - histotripsy. Ultrasound Med Biol. 2009;35:1982-1994.
115. Yoshizawa S, Ikeda T, Ito A, Ota R, Takagi S, Matsumoto Y. High intensity focused ultrasound lithotripsy with cavitating microbubbles. Med Biol Eng Comput. 2009;47:851-860.
116. Gourevich D, Gerold B, Arditti F, et al. Ultrasound activated nano-encapsulated targeted drug delivery and tumour cell poration. Adv Exp Med Biol. 2012;733:135-144.
117. Askari AT, Unzek S, Popovic ZB, et al. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet. 2003;362:697-703.
118. Ghanem A, Steingen C, Brenig F, et al. Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mesenchymal stem cells after acute myocardial infarction. J Mol Cell Cardiol. 2009;47:411-418.
119. Zhong S, Shu S, Wang Z, et al. Enhanced homing of mesenchymal stem cells to the ischemic myocardium by ultrasound-targeted microbubble destruction. Ultrasonics. 2012;52:281-286.
120. Pinton G, Aubry J F, Fink M, Tanter M. Numerical prediction of frequency dependent 3D maps of mechanical index thresholds in ultrasonic brain therapy. Med Phys. 2012;39:455-467.
121. Tezel A, Mitragotri S. Interactions of inertial cavitation bubbles with stratum corneum lipid bilayers during low-frequency sonophoresis. Biophys J. 2003;85:3502-3512.
122. Sharma D, Hanesh M, Yahya A, Mohamed M. Phonophoresis with diclofenac versus ketoprofen for knee joint injuries. Middle East J Int Med. 2009;2:9-12.
123. Meshali M, Abdel-Aleem H, Sakr F, Nazzal S, El-Malah Y. Effect of gel composition and phonophoresis on the transdermal delivery of ibuprofen: in vitro and in vivo evaluation. Pharm Dev Technol. 2011;16:93-101.
124. Kaya K, Delialouglu S, Babadag M, et al. Combined physiotherapy in patients with arthrogenous pain of temporomandibular joint. J Phys Med Rehab Sci. 2010;13:6-14.
125. Yang JH, Kim TY, Lee JH, Yoon SW, Yang KH, Shin SC. Antihyperalgesic and anti-inflammatory effects of ketorolac tromethamine gel using pulsed ultrasound in infamed rats. Arch Pharm Res. 2008;31:511-517.
126. Meshali M, Abdel-Aleem H, Sakr F, Nazzal S, El-Malah Y. In vitro phonophoresis: effect of ultrasound intensity and mode at high frequency on NSAIDs transport across cellulose and rabbit skin membranes. Pharmazie. 2008;63:49-53.
127. Rainsford KD. Profle and mechanisms of gastrointestinal and other side effects of nonsteroidal anti-infammatory drugs (NSAIDs). Am J Med. 1999;107:27-35.