Inertial cavitation to non-invasively trigger and monitor intratumoral release of drug from intravenously delivered liposomes

Journal of Controlled Release

Volumn 178, Issue 1, 2014, Pages 101-107

  Graham, Susan M ^a   Carlisle, Robert ^a   Choi, James J ^a   Stevenson, Mark ^a   Shah, Apurva R ^a   Myers, Rachel S ^a   Fisher, Kerry ^a   Peregrino, Miriam Bazan ^b   Seymour, Len ^a   Coussios, Constantin C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

Author keywords

Cancer; Drug delivery; Inertial cavitation; Liposomes; Ultrasound

Indexed keywords

ACOUSTIC EMISSION TESTING; CAVITATION; CONTROLLED DRUG DELIVERY; DIAGNOSIS; DRUG DELIVERY; LIPOSOMES; NONINVASIVE MEDICAL PROCEDURES; TUMORS; ULTRASONICS;

CANCER; DIAGNOSTIC ULTRASOUND; FOCUSED ULTRASOUND; INERTIAL CAVITATION; NONINVASIVE METHODS; PHOSPHOETHANOLAMINE; TRIGGERED RELEASE; ULTRASOUND EXPOSURE;

TARGETED DRUG DELIVERY;

1,2 DISTEAROYL SN GLYCERO 3 PHOSPHOETHANOLAMINE; DOXORUBICIN; GLYCEROPHOSPHOETHANOLAMINE; LIPOSOME; SONOVUE; UNCLASSIFIED DRUG;

ACOUSTICS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHEMICAL COMPOSITION; CONTROLLED STUDY; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG FORMULATION; DRUG RELEASE; ECHOGRAPHY; EMBRYO; FEMALE; HUMAN; IN VITRO STUDY; INTRATUMORAL DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; LIPOSOMAL DELIVERY; MICROBUBBLE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

CANCER; DRUG DELIVERY; INERTIAL CAVITATION; LIPOSOMES; ULTRASOUND;

ANIMALS; FEMALE; FIREFLY LUCIFERIN; INJECTIONS, INTRAVENOUS; LIPOSOMES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROBUBBLES; PHOSPHATIDYLETHANOLAMINES; PHOSPHOLIPIDS; SULFUR HEXAFLUORIDE; TISSUE DISTRIBUTION; ULTRASONIC THERAPY;

EID: 84893877010     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.12.016     Document Type: Article

References (37)

1. H. Maeda The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting Adv. Enzyme Regul. 41 2001 189 207
2. Y. Barenholz Doxil(R)-the first FDA-approved nano-drug: lessons learned J. Control. Release 160 2012 117 134
3. A.J. Coukell, and C.M. Spencer Polyethylene glycol-liposomal doxorubicin. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic efficacy (Pubitemid 27117367)
4. T.D. Tailor, G. Hanna, P.S. Yarmolenko, M.R. Dreher, A.S. Betof, A.B. Nixon, I. Spasojevic, and M.W. Dewhirst Effect of pazopanib on tumor microenvironment and liposome delivery Mol. Cancer Ther. 9 2010 1798 1808
5. K.M. Laginha, S. Verwoert, G.J. Charrois, and T.M. Allen Determination of doxorubicin levels in whole tumor and tumor nuclei in murine breast cancer tumors Clin. Cancer Res. 11 2005 6944 6949 (Pubitemid 41428752)
6. F. Yuan, M. Dellian, D. Fukumura, M. Leunig, D.A. Berk, V.P. Torchilin, and R.K. Jain Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size Cancer Res. 55 1995 3752 3756
7. H. Karanth, and R.S. Murthy pH-sensitive liposomes-principle and application in cancer therapy J. Pharm. Pharmacol. 59 2007 469 483 (Pubitemid 47051120)
8. B. Goldenbogen, N. Brodersen, A. Gramatica, M. Loew, J. Liebscher, A. Herrmann, H. Egger, B. Budde, and A. Arbuzova Reduction-sensitive liposomes from a multifunctional lipid conjugate and natural phospholipids: reduction and release kinetics and cellular uptake Langmuir 27 2011 10820 10829
9. S. Dromi, V. Frenkel, A. Luk, B. Traughber, M. Angstadt, M. Bur, J. Poff, J. Xie, S.K. Libutti, K.C. Li, and B.J. Wood Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect Clin. Cancer Res. 13 2007 2722 2727 (Pubitemid 46788041)
10. A. Kheirolomoom, D.E. Kruse, S. Qin, K.E. Watson, C.Y. Lai, L.J. Young, R.D. Cardiff, and K.W. Ferrara Enhanced in vivo bioluminescence imaging using liposomal luciferin delivery system J. Control. Release 141 2010 128 136
11. T.J. Evjen, E.A. Nilssen, S. Rognvaldsson, M. Brandl, and S.L. Fossheim Distearoylphosphatidylethanolamine-based liposomes for ultrasound-mediated drug delivery Eur. J. Pharm. Biopharm. 75 2010 327 333
12. S. Mo, C.C. Coussios, L. Seymour, and R. Carlisle Ultrasound-enhanced drug delivery for cancer Expert Opin. Drug Deliv. 9 2012 1525 1538
13. P. Giustetto, D.D. Castelli, C. Boffa, S. Rizzitelli, D. Durando, J.C. Cutrin, S. Aime, and E. Terreno Release of a paramagnetic magnetic resonance imaging agent from liposomes triggered by low intensity non-focused ultrasound J. Med. Imaging Health Inform. 3 2013 356 366
14. T.J. Evjen, E. Hagtvet, A. Moussatov, S. Rognvaldsson, J.L. Mestas, R.A. Fowler, C. Lafon, and E.A. Nilssen In vivo monitoring of liposomal release in tumours following ultrasound stimulation Eur. J. Pharm. Biopharm. 84 2013 526 531
15. C.D. Arvanitis, M. Bazan-Peregrino, B. Rifai, L.W. Seymour, and C.C. Coussios Cavitation-enhanced extravasation for drug delivery Ultrasound Med. Biol. 37 2011 1838 1852
16. M. Bazan-Peregrino, B. Rifai, R.C. Carlisle, J. Choi, C.D. Arvanitis, L.W. Seymour, and C.C. Coussios Cavitation-enhanced delivery of a replicating oncolytic adenovirus to tumors using focused ultrasound J. Control. Release 169 2013 40 47
17. C.H. Farny, R.G. Holt, and R.A. Roy Temporal and spatial detection of HIFU-induced inertial and hot-vapor cavitation with a diagnostic ultrasound system Ultrasound Med. Biol. 35 2009 603 615
18. M. Gyongy, and C.C. Coussios Passive spatial mapping of inertial cavitation during HIFU exposure IEEE Trans. Biomed. Eng. 57 2010 48 56
19. J.J. Choi, and C.C. Coussios Spatiotemporal evolution of cavitation dynamics exhibited by flowing microbubbles during ultrasound exposure J. Acoust. Soc. Am. 132 2012 3538 3549
20. R. Carlisle, L.W. Seymour, and C.C. Coussios Targeting of Liposomes via PSGL1 for Enhanced Tumor Accumulation Pharm. Res. 30 2013 352 361
21. A. Ryan, and H. Scrable Visualization of the dynamics of gene expression in the living mouse Mol. Imaging 3 2004 33 42
22. M. Stevenson, R. Carlisle, B. Davies, C. Preece, M. Hammett, W.L. Liu, K.D. Fisher, A. Ryan, H. Scrable, and L.W. Seymour Development of a positive-readout mouse model of siRNA pharmacodynamics Mol. Ther. Nucleic Acids 2 2013 e133
23. N. Hockham, C.C. Coussios, and M. Arora A real-time controller for sustaining thermally relevant acoustic cavitation during ultrasound therapy IEEE Trans. Ultrason. Ferroelectr. Freq. Control 57 2010 2685 2694
24. M. Bazan-Peregrino, B. Rifai, R.C. Carlisle, J. Choi, C.D. Arvanitis, L.W. Seymour, and C.C. Coussios Cavitation-enhanced delivery of a replicating oncolytic adenovirus to tumors using focused ultrasound J. Control. Release 169 2013 40 47
25. E. Wisse, F. Jacobs, B. Topal, P. Frederik, and B. De Geest The size of endothelial fenestrae in human liver sinusoids: implications for hepatocyte-directed gene transfer Gene Ther. 15 2008 1193 1199
26. J.J. Choi, K. Selert, F. Vlachos, A. Wong, and E.E. Konofagou Noninvasive and localized neuronal delivery using short ultrasonic pulses and microbubbles Proc. Natl. Acad. Sci. U. S. A. 108 2011 16539 16544
27. M. Bazan-Peregrino, C.D. Arvanitis, B. Rifai, L.W. Seymour, and C.C. Coussios Ultrasound-induced cavitation enhances the delivery and therapeutic efficacy of an oncolytic virus in an in vitro model J. Control. Release 157 2012 235 242
28. R.K. Jain Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy Science 307 2005 58 62 (Pubitemid 40093472)
29. D.L. Miller, and J. Song Tumor growth reduction and DNA transfer by cavitation-enhanced high-intensity focused ultrasound in vivo Ultrasound Med. Biol. 29 2003 887 893 (Pubitemid 36808641)
30. S. Mitragotri Healing sound: the use of ultrasound in drug delivery and other therapeutic applications Nat. Rev. Drug Discov. 4 2005 255 260 (Pubitemid 40372559)
31. R. Carlisle, J. Choi, M. Bazan-Peregrino, R. Laga, V. Subr, L. Kostka, K. Ulbrich, C.C. Coussios, and L.W. Seymour Enhanced Tumor Uptake and Penetration of Virotherapy Using Polymer Stealthing and Focused Ultrasound J. Natl. Cancer Inst. 105 2013 1701 1710
32. L.H. Treat, N. McDannold, Y. Zhang, N. Vykhodtseva, and K. Hynynen Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma Ultrasound Med. Biol. 38 2012 1716 1725
33. 31P NMR spectroscopy and x-ray diffraction Biochim. Biophys. Acta 690 1982 117 123
34. R.S. Cobbold Foundations of biomedical ultrasound 2007 Oxford University Press New York
35. T.J. Evjen, S. Hupfeld, S. Barnert, S. Fossheim, R. Schubert, and M. Brandl Physicochemical characterization of liposomes after ultrasound exposure - mechanisms of drug release J. Pharm. Biomed. Anal. 78-79 2013 118 122
36. L.T. Baxter, and R.K. Jain Transport of fluid and macromolecules in tumors. II. Role of heterogeneous perfusion and lymphatics Microvasc. Res. 40 1990 246 263 (Pubitemid 20327678)
37. E. Mylonopoulou, M. Bazan-Peregrino, C.D. Arvanitis, and C.C. Coussios A non-exothermic cell-embedding tissue-mimicking material for studies of ultrasound-induced hyperthermia and drug release Int. J. Hyperthermia 29 2013 133 144