Crucial factors and emerging concepts in ultrasound-triggered drug delivery

Journal of Controlled Release

Volumn 164, Issue 3, 2012, Pages 248-255

  Geers, Bart ^a   Dewitte, Heleen ^a   De Smedt, Stefaan C ^a   Lentacker, Ine ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Image guided drug delivery; Microbubbles; Ultrasound

Indexed keywords

CONTRAST AGENT; DRUG CARRIER; ENCAPSULATED DRUGS; GAS BUBBLE; IMAGE-GUIDED; MAJOR FACTORS; MICROBUBBLES; ULTRASOUND GUIDED; ULTRASOUND IMAGING; ULTRASOUND WAVES;

CELL MEMBRANES; CONTROLLED DRUG DELIVERY; CYTOLOGY; ULTRASONIC IMAGING; ULTRASONIC WAVES; ULTRASONICS;

BUBBLES (IN FLUIDS);

CONTRAST MEDIUM; DOXORUBICIN; DRUG CARRIER; LIPOSOME; PACLITAXEL;

ACOUSTIC ANALYSIS; ANTIGEN PRESENTING CELL; CANCER IMMUNIZATION; CELL MEMBRANE; CONFERENCE PAPER; DRUG DELIVERY SYSTEM; ENCAPSULATION; HEART INFARCTION; HUMAN; IMAGING; MICROBUBBLE; NONHUMAN; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; ULTRASOUND;

CELL MEMBRANE PERMEABILITY; DOXORUBICIN; DRUG CARRIERS; HUMANS; LIPOSOMES; MICROBUBBLES; PHARMACEUTICAL PREPARATIONS; SOLUBILITY; ULTRASONICS;

EID: 84870249845     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.08.014     Document Type: Conference Paper

References (88)

1. B.P. Timko, T. Dvir, and D.S. Kohane Remotely triggerable drug delivery systems Adv. Mater. 22 2010 4925 4943
2. S.L. Mulvagh, A.N. DeMaria, S.B. Feinstein, P.N. Burns, S. Kaul, J.G. Miller, M. Monaghan, T.R. Porter, L.J. Shaw, and F.S. Villanueva Contrast echocardiography: current and future applications J. Am. Soc. Echocardiogr. 13 2000 331 342
3. S. Qin, C.F. Caskey, and K.W. Ferrara Ultrasound contrast microbubbles in imaging and therapy: physical principles and engineering Phys. Med. Biol. 54 2009 R27 R57
4. A. Bouakaz, M. Versluis, and N. de Jong High-speed optical observations of contrast agent destruction Ultrasound Med. Biol. 31 2005 391 399
5. J. Wu, and W.L. Nyborg Ultrasound, cavitation bubbles and their interaction with cells Adv. Drug Deliv. Rev. 60 2008 1103 1116
6. E. Quaia Assessment of tissue perfusion by contrast-enhanced ultrasound Eur. Radiol. 21 2011 604 615
7. Y. Qiu, Y. Luo, Y. Zhang, W. Cui, D. Zhang, J. Wu, J. Zhang, and J. Tu The correlation between acoustic cavitation and sonoporation involved in ultrasound-mediated DNA transfection with polyethylenimine (PEI) in vitro J. Control. Release 145 2010 40 48
8. I. Lentacker, S.C. De Smedt, and N.N. Sanders Drug loaded microbubble design for ultrasound triggered delivery Soft Matter 5 2009 2161 2170
9. S. Tinkov, R. Bekeredjian, G. Winter, and C. Coester Microbubbles as ultrasound triggered drug carriers J. Pharm. Sci. 98 2009 1935 1961
10. P.A. Frenkel, S. Chen, T. Thai, R.V. Shohet, and P.A. Grayburn DNA-loaded albumin microbubbles enhance ultrasound-mediated transfection in vitro Ultrasound Med. Biol. 28 2002 817 822
11. M.A. Borden, C.F. Caskey, E. Little, R.J. Gillies, and K.W. Ferrara DNA and polylysine adsorption and multilayer construction onto cationic lipid-coated microbubbles Langmuir 23 2007 9401 9408
12. S.R. Sirsi, S.L. Hernandez, L. Zielinski, H. Blomback, A. Koubaa, M. Synder, S. Homma, J.J. Kandel, D.J. Yamashiro, and M.A. Borden Polyplex-microbubble hybrids for ultrasound-guided plasmid DNA delivery to solid tumors J. Control. Release 157 2012 224 234
13. L.C. Phillips, A.L. Klibanov, B.R. Wamhoff, and J.A. Hossack Targeted gene transfection from microbubbles into vascular smooth muscle cells using focused, ultrasound-mediated delivery Ultrasound Med. Biol. 36 2010 1470 1480
14. S. Tinkov, G. Winter, C. Coester, and R. Bekeredjian New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: part I - Formulation development and in-vitro characterization J. Control. Release 143 2010 143 150
15. C.Y. Ting, C.H. Fan, H.L. Liu, C.Y. Huang, H.Y. Hsieh, T.C. Yen, K.C. Wei, and C.K. Yeh Concurrent blood-brain barrier opening and local drug delivery using drug-carrying microbubbles and focused ultrasound for brain glioma treatment Biomaterials 33 2012 704 712
16. A.C. Camarozano, F.Z. Garcia de Almeida Cyrino, D.A. Bottino, and E. Bouskela Effects of microbubbles and ultrasound on the microcirculation: observation on the hamster cheek pouch J. Am. Soc. Echocardiogr. 23 2010 1323 1330
17. K. Kooiman, M.R. Bohmer, M. Emmer, H.J. Vos, C. Chlon, W.T. Shi, C.S. Hall, S.H. de Winter, K. Schroen, M. Versluis, N. de Jong, and A. van Wamel Oil-filled polymer microcapsules for ultrasound-mediated delivery of lipophilic drugs J. Control. Release 133 2009 109 118
18. M.S. Tartis, J. McCallan, A.F. Lum, R. LaBell, S.M. Stieger, T.O. Matsunaga, and K.W. Ferrara Therapeutic effects of paclitaxel-containing ultrasound contrast agents Ultrasound Med. Biol. 32 2006 1771 1780
19. S. Hernot, and A.L. Klibanov Microbubbles in ultrasound-triggered drug and gene delivery Adv. Drug Deliv. Rev. 60 2008 1153 1166
20. I. Lentacker, B. Geers, J. Demeester, S.C. De Smedt, and N.N. Sanders Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved Mol. Ther. 18 2010 101 108
21. M.L. De Temmerman, H. Dewitte, R.E. Vandenbroucke, B. Lucas, C. Libert, J. Demeester, S.C. De Smedt, I. Lentacker, and J. Rejman mRNA-Lipoplex loaded microbubble contrast agents for ultrasound-assisted transfection of dendritic cells Biomaterials 32 2011 9128 9135
22. I. Lentacker, N. Wang, R.E. Vandenbroucke, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound exposure of lipoplex loaded microbubbles facilitates direct cytoplasmic entry of the lipoplexes Mol. Pharm. 6 2009 457 467
23. R.E. Vandenbroucke, I. Lentacker, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound assisted siRNA delivery using PEG-siPlex loaded microbubbles J. Control. Release 126 2008 265 273
24. P. Caliceti, M. Chinol, M. Roldo, F.M. Veronese, A. Semenzato, S. Salmaso, and G. Paganelli Poly(ethylene glycol)-avidin bioconjugates: suitable candidates for tumor pretargeting J. Control. Release 83 2002 97 108
25. B. Geers, I. Lentacker, N.N. Sanders, J. Demeester, S. Meairs, and S.C. De Smedt Self-assembled liposome-loaded microbubbles: the missing link for safe and efficient ultrasound triggered drug-delivery J. Control. Release 152 2011 249 256
26. Y.C. Barenholz Doxil(R) - the first FDA-approved nano-drug: lessons learned J. Control. Release 2012 [Electronic publication ahead of print]
27. A. Gabizon, R. Catane, B. Uziely, B. Kaufman, T. Safra, R. Cohen, F. Martin, A. Huang, and Y. Barenholz Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes Cancer Res. 54 1994 987 992
28. S. Tinkov, C. Coester, S. Serba, N.A. Geis, H.A. Katus, G. Winter, and R. Bekeredjian New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: in-vivo characterization J. Control. Release 148 2010 368 372
29. R. Suzuki, E. Namai, Y. Oda, N. Nishiie, S. Otake, R. Koshima, K. Hirata, Y. Taira, N. Utoguchi, Y. Negishi, S. Nakagawa, and K. Maruyama Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure J. Control. Release 142 2010 245 250
30. Y. Wang, X. Li, Y. Zhou, P. Huang, and Y. Xu Preparation of nanobubbles for ultrasound imaging and intracelluar drug delivery Int. J. Pharm. 384 2010 148 153
31. M.S. Tartis, D.E. Kruse, H. Zheng, H. Zhang, A. Kheirolomoom, J. Marik, and K.W. Ferrara Dynamic microPET imaging of ultrasound contrast agents and lipid delivery J. Control. Release 131 2008 160 166
32. F.Y. Yang, T.T. Wong, M.C. Teng, R.S. Liu, M. Lu, H.F. Liang, and M.C. Wei Focused ultrasound and interleukin-4 receptor-targeted liposomal doxorubicin for enhanced targeted drug delivery and antitumor effect in glioblastoma multiforme J. Control. Release 2012 [Electronic publication ahead of print]
33. C.H. Wang, Y.F. Huang, and C.K. Yeh Aptamer-conjugated nanobubbles for targeted ultrasound molecular imaging Langmuir 27 2011 6971 6976
34. Z. Gao, A.M. Kennedy, D.A. Christensen, and N.Y. Rapoport Drug-loaded nano/microbubbles for combining ultrasonography and targeted chemotherapy Ultrasonics 48 2008 260 270
35. N. Rapoport, K.H. Nam, R. Gupta, Z. Gao, P. Mohan, A. Payne, N. Todd, X. Liu, T. Kim, J. Shea, C. Scaife, D.L. Parker, E.K. Jeong, and A.M. Kennedy Ultrasound-mediated tumor imaging and nanotherapy using drug loaded, block copolymer stabilized perfluorocarbon nanoemulsions J. Control. Release 153 2011 4 15
36. P.S. Sheeran, S. Luois, P.A. Dayton, and T.O. Matsunaga Formulation and acoustic studies of a new phase-shift agent for diagnostic and therapeutic ultrasound Langmuir 27 2011 10412 10420
37. J. Fang, H. Nakamura, and H. Maeda 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. 63 2011 136 151
38. P.S. Sheeran, V.P. Wong, S. Luois, R.J. McFarland, W.D. Ross, S. Feingold, T.O. Matsunaga, and P.A. Dayton Decafluorobutane as a phase-change contrast agent for low-energy extravascular ultrasonic imaging Ultrasound Med. Biol. 37 2011 1518 1530
39. X. Wang, H. Chen, Y. Chen, M. Ma, K. Zhang, F. Li, Y. Zheng, D. Zeng, Q. Wang, and J. Shi Perfluorohexane-encapsulated mesoporous silica nanocapsules as enhancement agents for highly efficient high intensity focused ultrasound (HIFU) Adv. Mater. 24 2012 785 791
40. C.E. Ashley, E.C. Carnes, G.K. Phillips, D. Padilla, P.N. Durfee, P.A. Brown, T.N. Hanna, J. Liu, B. Phillips, M.B. Carter, N.J. Carroll, X. Jiang, D.R. Dunphy, C.L. Willman, D.N. Petsev, D.G. Evans, A.N. Parikh, B. Chackerian, W. Wharton, D.S. Peabody, and C.J. Brinker The targeted delivery of multicomponent cargos to cancer cells by nanoporous particle-supported lipid bilayers Nat. Mater. 10 2011 389 397
41. B.A. Kaufmann, J.M. Sanders, C. Davis, A. Xie, P. Aldred, I.J. Sarembock, and J.R. Lindner Molecular imaging of inflammation in atherosclerosis with targeted ultrasound detection of vascular cell adhesion molecule-1 Circulation 116 2007 276 284
42. S. Hernot, S. Unnikrishnan, Z. Du, T. Shevchenko, B. Cosyns, A. Broisat, J. Toczek, V. Caveliers, S. Muyldermans, T. Lahoutte, A.L. Klibanov, and N. Devoogdt Nanobody-coupled microbubbles as novel molecular tracer J. Control. Release 158 2012 346 353
43. E.A. Ferrante, J.E. Pickard, J. Rychak, A. Klibanov, and K. Ley Dual targeting improves microbubble contrast agent adhesion to VCAM-1 and P-selectin under flow J. Control. Release 140 2009 100 107
44. L. Yang, X. Zhang, M. Ye, J. Jiang, R. Yang, T. Fu, Y. Chen, K. Wang, C. Liu, and W. Tan Aptamer-conjugated nanomaterials and their applications Adv. Drug Deliv. Rev. 63 2011 1361 1370
45. C.H. Wang, S.T. Kang, Y.H. Lee, Y.L. Luo, Y.F. Huang, and C.K. Yeh Aptamer-conjugated and drug-loaded acoustic droplets for ultrasound theranosis Biomaterials 33 2012 1939 1947
46. K. Kooiman, M. Foppen-Harteveld, A.F. van der Steen, and N. de Jong Sonoporation of endothelial cells by vibrating targeted microbubbles J. Control. Release 154 2011 35 41
47. I. Lentacker, B.G. De Geest, R.E. Vandenbroucke, L. Peeters, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound-responsive polymer-coated microbubbles that bind and protect DNA Langmuir 22 2006 7273 7278
48. A. Ghanem, C. Steingen, F. Brenig, F. Funcke, Z.Y. Bai, C. Hall, C.T. Chin, G. Nickenig, W. Bloch, and K. Tiemann Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mesenchymal stem cells after acute myocardial infarction J. Mol. Cell. Cardiol. 47 2009 411 418
49. H. Leong-Poi, M.A. Kuliszewski, M. Lekas, M. Sibbald, K. Teichert-Kuliszewska, A.L. Klibanov, D.J. Stewart, and J.R. Lindner Therapeutic arteriogenesis by ultrasound-mediated VEGF(165) plasmid gene delivery to chronically ischemic skeletal muscle Circ. Res. 101 2007 295 303
50. A. van Wamel, K. Kooiman, M. Harteveld, M. Emmer, F.J. ten Cate, M. Versluis, and N. de Jong Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation J. Control. Release 112 2006 149 155
51. M. Figueiredo, and R. Esenaliev PLGA nanoparticles for ultrasound-mediated gene delivery to solid tumors J. Drug Deliv. 2012 2012 767839
52. T.B. Brismar, D. Grishenkov, B. Gustafsson, J. Harmark, A. Barrefelt, S.V. Kothapalli, S. Margheritelli, L. Oddo, K. Caidahl, H. Hebert, and G. Paradossi Magnetite nanoparticles can be coupled to microbubbles to support multimodal imaging Biomacromolecules 13 5 2012 1390 1399
53. I. Lentacker, R.E. Vandenbroucke, B. Lucas, J. Demeester, S.C. De Smedt, and N.N. Sanders New strategies for nucleic acid delivery to conquer cellular and nuclear membranes J. Control. Release 132 2008 279 288
54. M. Seo, I. Gorelikov, R. Williams, and N. Matsuura Microfluidic assembly of monodisperse, nanoparticle-incorporated perfluorocarbon microbubbles for medical imaging and therapy Langmuir 26 2010 13855 13860
55. M. Afadzi, C.D. Davies, Y.H. Hansen, T. Johansen, O.K. Standal, R. Hansen, S.E. Masoy, E.A. Nilssen, and B. Angelsen Effect of ultrasound parameters on the release of liposomal calcein Ultrasound Med. Biol. 38 2012 476 486
56. C.D. Ohl, and R. Ikink Shock-wave-induced jetting of micron-size bubbles Phys. Rev. Lett. 90 2003 214502
57. C.D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse Sonoporation from jetting cavitation bubbles Biophys. J. 91 2006 4285 4295
58. R. Karshafian, P.D. Bevan, R. Williams, S. Samac, and P.N. Burns Sonoporation by ultrasound-activated microbubble contrast agents: effect of acoustic exposure parameters on cell membrane permeability and cell viability Ultrasound Med. Biol. 35 2009 847 860
59. R. Karshafian, S. Samac, P.D. Bevan, and P.N. Burns Microbubble mediated sonoporation of cells in suspension: clonogenic viability and influence of molecular size on uptake Ultrasonics 50 2010 691 697
60. S. Mehier-Humbert, T. Bettinger, F. Yan, and R.H. Guy Plasma membrane poration induced by ultrasound exposure: implication for drug delivery J. Control. Release 104 2005 213 222
61. B. Geers, I. Lentacker, A. Alonso, N.N. Sanders, J. Demeester, S. Meairs, and S.C. De Smedt Elucidating the mechanisms behind sonoporation with adeno-associated virus-loaded microbubbles Mol. Pharm. 8 2011 2244 2251
62. B.D. Meijering, L.J. Juffermans, A. van Wamel, R.H. Henning, I.S. Zuhorn, M. Emmer, A.M. Versteilen, W.J. Paulus, W.H. van Gilst, K. Kooiman, N. de Jong, R.J. Musters, L.E. Deelman, and O. Kamp Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation Circ. Res. 104 2009 679 687
63. C. Mannaris, and M.A. Averkiou Investigation of microbubble response to long pulses used in ultrasound-enhanced drug delivery Ultrasound Med. Biol. 38 2012 681 691
64. R. Seip, C.T. Chin, C.S. Hall, B.I. Raju, A. Ghanem, and K. Tiemann Targeted ultrasound-mediated delivery of nanoparticles: on the development of a new HIFU-based therapy and imaging device IEEE Trans. Biomed. Eng. 57 2010 61 70
65. L.H. Treat, N. McDannold, N. Vykhodtseva, Y. Zhang, K. Tam, and K. Hynynen Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound Int. J. Cancer 121 2007 901 907
66. F. Marquet, Y.S. Tung, T. Teichert, V.P. Ferrera, and E.E. Konofagou Noninvasive, transient and selective blood-brain barrier opening in non-human primates in vivo PLoS One 6 2011 e22598
67. M.R. Bohmer, C.H. Chlon, B.I. Raju, C.T. Chin, T. Shevchenko, and A.L. Klibanov Focused ultrasound and microbubbles for enhanced extravasation J. Control. Release 148 2010 18 24
68. N. Vykhodtseva, N. McDannold, and K. Hynynen Progress and problems in the application of focused ultrasound for blood-brain barrier disruption Ultrasonics 48 2008 279 296
69. N. Rapoport, Z. Gao, and A. Kennedy Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy J. Natl. Cancer Inst. 99 2007 1095 1106
70. K. Un, S. Kawakami, M. Yoshida, Y. Higuchi, R. Suzuki, K. Maruyama, F. Yamashita, and M. Hashida The elucidation of gene transferring mechanism by ultrasound-responsive unmodified and mannose-modified lipoplexes Biomaterials 32 2011 4659 4669
71. O. Mueller, S. Schinkel, J. Kleinschmidt, H. Katus, and R. Bekeredjian Augmentation of AAV-mediated cardiac gene transfer after systemic administration in adult rats Gene Ther. 15 2008 1558 1565
72. T. Lammers, S. Aime, W.E. Hennink, G. Storm, and F. Kiessling Theranostic nanomedicine Acc. Chem. Res. 44 2011 1029 1038
73. T. Lammers, F. Kiessling, W.E. Hennink, and G. Storm Nanotheranostics and image-guided drug delivery: current concepts and future directions Mol. Pharm. 7 2010 1899 1912
74. F. Kiessling, S. Fokong, P. Koczera, W. Lederle, and T. Lammers Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics J. Nucl. Med. 53 2012 345 348
75. Z. Liu, T. Lammers, J. Ehling, S. Fokong, J. Bornemann, F. Kiessling, and J. Gatjens Iron oxide nanoparticle-containing microbubble composites as contrast agents for MR and ultrasound dual-modality imaging Biomaterials 32 2011 6155 6163
76. Y.T. Lim, M.Y. Cho, J.H. Kang, Y.W. Noh, J.H. Cho, K.S. Hong, J.W. Chung, and B.H. Chung Perfluorodecalin/[InGaP/ZnS quantum dots] nanoemulsions as 19F MR/optical imaging nanoprobes for the labeling of phagocytic and nonphagocytic immune cells Biomaterials 31 2010 4964 4971
77. R.K. Schlicher, J.D. Hutcheson, H. Radhakrishna, R.P. Apkarian, and M.R. Prausnitz Changes in cell morphology due to plasma membrane wounding by acoustic cavitation Ultrasound Med. Biol. 36 2010 677 692
78. A. van Wamel, K. Kooiman, M. Emmer, F.J. ten Cate, M. Versluis, and N. de Jong Ultrasound microbubble induced endothelial cell permeability J. Control. Release 116 2006 e100 e102
79. A. Yudina, M. Lepetit-Coiffe, and C.T. Moonen Evaluation of the temporal window for drug delivery following ultrasound-mediated membrane permeability enhancement Mol. Imaging Biol. 13 2011 239 249
80. A. Yudina, M. de Smet, M. Lepetit-Coiffe, S. Langereis, L. Van Ruijssevelt, P. Smirnov, V. Bouchaud, P. Voisin, H. Grull, and C.T. Moonen Ultrasound-mediated intracellular drug delivery using microbubbles and temperature-sensitive liposomes J. Control. Release 155 2011 442 448
81. E. Chavakis, M. Koyanagi, and S. Dimmeler Enhancing the outcome of cell therapy for cardiac repair: progress from bench to bedside and back Circulation 121 2010 325 335
82. S.M. Herbst, M.E. Klegerman, H. Kim, J. Qi, H. Shelat, M. Wassler, M.R. Moody, C.M. Yang, X. Ge, Y. Zou, J.A. Kopechek, F.J. Clubb, D.C. Kraemer, S. Huang, C.K. Holland, D.D. McPherson, and Y.J. Geng Delivery of stem cells to porcine arterial wall with echogenic liposomes conjugated to antibodies against CD34 and intercellular adhesion molecule-1 Mol. Pharm. 7 2010 3 11
83. X. Song, H. Zhu, L. Jin, J. Wang, Q. Yang, P. Jin, and X. Li Ultrasound-mediated microbubble destruction enhances the efficacy of bone marrow mesenchymal stem cell transplantation and cardiac function Clin. Exp. Pharmacol. Physiol. 36 2009 267 271
84. S. Zhong, S. Shu, Z. Wang, J. Luo, W. Zhong, H. Ran, Y. Zheng, Y. Yin, and Z. Ling Enhanced homing of mesenchymal stem cells to the ischemic myocardium by ultrasound-targeted microbubble destruction Ultrasonics 52 2012 281 286
85. A.T. Askari, S. Unzek, Z.B. Popovic, C.K. Goldman, F. Forudi, M. Kiedrowski, A. Rovner, S.G. Ellis, J.D. Thomas, P.E. DiCorleto, E.J. Topol, and M.S. Penn Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy Lancet 362 2003 697 703
86. K. Un, S. Kawakami, R. Suzuki, K. Maruyama, F. Yamashita, and M. Hashida Enhanced transfection efficiency into macrophages and dendritic cells by a combination method using mannosylated lipoplexes and bubble liposomes with ultrasound exposure Hum. Gene Ther. 21 2010 65 74
87. S. Kreiter, A. Selmi, M. Diken, M. Koslowski, C.M. Britten, C. Huber, O. Tuereci, and U. Sahin Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity Cancer Res. 70 2010 9031 9040
88. A. Sever, S. Jones, K. Cox, J. Weeks, P. Mills, and P. Jones Preoperative localization of sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasonography in patients with breast cancer Br. J. Surg. 96 2009 1295 1299