Doxorubicin liposome-loaded microbubbles for contrast imaging and ultrasound-triggered drug delivery

IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control

Volumn 60, Issue 1, 2013, Pages 78-87

  Escoffre, Jean Michel ^a   Mannaris, Christophoros ^b   Geers, Bart ^c   Novell, Anthony ^a   Lentacker, Ine ^c   Averkiou, Michalakis ^b   Bouakaz, Ayache ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITY OF CYPRUS   (Cyprus)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CELL VIABILITY; CONTRAST AGENT; CONTRAST IMAGING; DIAGNOSTIC ULTRASOUND; DOXORUBICIN; ENHANCED UPTAKE; GLIOBLASTOMA CELLS; IMAGE GUIDANCES; IMAGE-GUIDED; IN-VITRO; IN-VIVO; MECHANICAL INDEXES; MICROBUBBLES; NON-LINEAR ULTRASOUND; REAL TIME; TARGETED DRUG DELIVERY; THERAPEUTIC PROPERTIES;

DRUG DELIVERY; LIPOSOMES; ULTRASONIC IMAGING;

ULTRASONICS;

CONTRAST MEDIUM; DOXORUBICIN; LIPOSOME;

ARTICLE; CELL SURVIVAL; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG EFFECT; GLIOBLASTOMA; HUMAN; IMAGE QUALITY; KINETICS; METABOLISM; METHODOLOGY; MICROBUBBLE; NONPARAMETRIC TEST; TUMOR CELL LINE; ULTRASOUND;

CELL LINE, TUMOR; CELL SURVIVAL; CONTRAST MEDIA; DOXORUBICIN; DRUG DELIVERY SYSTEMS; GLIOBLASTOMA; HUMANS; KINETICS; LIPOSOMES; MICROBUBBLES; PHANTOMS, IMAGING; STATISTICS, NONPARAMETRIC; ULTRASONICS;

MLCS; MLOWN;

EID: 84872048869     PISSN: 08853010     EISSN: None     Source Type: Journal    
DOI: 10.1109/TUFFC.2013.2539     Document Type: Article

References (47)

1. C. Carvalho, R. X. Santos, S. Cardoso, S. Correia, P. J. Oliveira, M. S. Santos, and P. I. Moreira, "Doxorubicin: The good, the bad and the ugly effect," Curr. Med. Chem., vol. 16, no. 25, pp. 3267-3285, 2009.
2. A. A. Gabizon, "Pegylated liposomal doxorubicin: Metamorphosis of an old drug into a new form of chemotherapy," Cancer Invest., vol. 19, no. 4, pp. 424-436, 2001. (Pubitemid 32525189)
3. Y. C. Barenholz, "Doxil-The first FDA -approved nano-drug: Lessons learned," J. Control. Release, vol. 160, no. 2, pp. 117-134, 2012.
4. C. L. Bennett and E. A. Calhoun, "Pharmacoeconomics of liposomal anthracycline therapy," Semin. Oncol., vol. 31, no. 6, suppl. 13, pp. 191-195, 2004. (Pubitemid 40023248)
5. M. E. O'Brien, N. Wigler, M. Inbar, R. Rosso, E. Grischke, A. Santoro, R. Catane, D. G. Kieback, P. Tomczak, S. P. Ackland, F. Oriandi, L. Mellars, L. Alland, C. Tendler; CAELY X Breast Cancer Study Group, "Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELY X/ Doxil) versus conventional for first-line treatment of metastatic breast cancer," Ann. Oncol., vol. 15, no. 3, pp. 440-449, 2004. (Pubitemid 38444547)
6. R. R. Patil, S. A. Guhagarkar, and P. V. Devarajan, "Engineered nanocarriers of doxorubicin: A current update," Crit. Rev. Ther. Drug Carrier Syst., vol. 25, no. 1, pp. 1-61, 2008. (Pubitemid 351363756)
7. R. Deckers and C. T. Moonen, "Ultrasound triggered, image guided, local drug delivery," J. Control. Release, vol. 148, no. 1, pp. 25-33, 2010.
8. A. Fernandez-Fernandez, R. Manchanda, and A. J. McGoron, "Theranostic applications of nanomaterials in cancer: drug delivery, image-guided therapy, and multifunctional platforms," Appl. Biochem. Biotechnol., vol. 165, no. 7-8, pp. 1628-1651, 2011.
9. A. V. Patil, J. J. Rychak, A. L. Klibanov, and J. A. Hossack, "Realtime technique for improving molecular imaging and guiding drug delivery in large blood vessels: In vitro and ex vivo results," Mol. Imaging, vol. 10, no. 4, pp. 238-247, 2011.
10. V. Frenkel, "Ultrasound mediated delivery of drugs and genes to solid tumors," Adv. Drug Deliv. Rev., vol. 60, no. 10, pp. 1193-1208, 2008.
11. 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., vol. 6, no. 2, pp. 457-467, 2009.
12. J.-M. Escoffre, K. Kaddur, M.-P. Rols, and A. Bouakaz, "In vitro gene transfer by electro-sonoporation," Ultrasound Med. Biol., vol. 36, no. 10, pp. 1746-1755, 2010.
13. K. Iwanaga, K. Tominaga, K. Yamaoto, M. Habu, H. Maeda, S. Akifusa, T. Tsujisawa, T. Okinaga, J. Fukuda, and T. Nishihara, "Local delivery system of cytotoxic agents to tumors by focused sonoporation," Cancer Gene Ther., vol. 14, no. 4, pp. 354-363, 2007. (Pubitemid 46425785)
14. Y. Ueno, S. Sonoda, R. Suzuki, M. Yokouchi, Y. Kawasoe, K. Tachibana, K. Maruyama, T. Sakamoto, and S. Komiva, "Combination of ultrasound and bubble liposomes enhance the effect of doxorubicin and inhibit murine osteosarcoma growth," Cancer Biol. Ther., vol. 12, no. 4, pp. 270-277, 2011.
15. J. Wu, "Theoretical study on shear stress generated by microstreaming surrounding contrast agents attached to living cells," Ultrasound Med. Biol., vol. 28, no. 1, pp. 125-129, 2002. (Pubitemid 34202308)
16. A. A. Doinikov and A. Bouakaz, "Acoustic microstreaming around an encapsulated particule," J. Acoust. Soc. Am., vol. 127, no. 3, pp. 1218-1227, 2010.
17. C. D. Ohl and B. Wolfrum, "Detachment and sonoporation of adherent HeLa-cells by shock waves-induced cavitation," Biochim. Biophys. Acta, vol. 1624, no. 1-3, pp. 131-138, 2003. (Pubitemid 37464950)
18. C. D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, "Sonoporation from jetting cavitation bubbles," Biophys. J., vol. 91, no. 11, pp. 4285-4295, 2006. (Pubitemid 44887286)
19. B. D. M. Meijering, L. J. M. Juffermans, A. van Wamel, R. H. Henning, I. S. Zuhorn, M. Emmer, A. M. G. Versteilen, W. J. Paulus, W. H. van Gilst, K. Kooiman, N. de Jong, R. J. P. 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., vol. 104, no. 5, pp. 679-687, 2009.
20. A. A. Doinikov and A. Bouakaz, "Theoretical investigation of shear stress generated by a contrast microbubble on the cell membrane as a mechanism for sonoporation," J. Acoust. Soc. Am., vol. 128, no. 1, pp. 11-19, 2010.
21. C. Greis, "Technology overview: SonoVue (Bracco, Milan)," Eur. Radiol., vol. 14, suppl. 8, pp. 11-15, 2004.
22. T. Yoshida, T. Kondo, R. Ogawa, L. B. Feril Jr., Q. L. Zhao, A. Watanabe, and K. Tsukada, "Combination of doxorubicin and lowintensity ultrasound causes a synergistic enhancement in cell killing and an additive enhancement in apoptosis induction in human lymphoma U937 cells," Cancer Chemother. Pharmacol., vol. 61, no. 4, pp. 559-567, 2008.
23. V. Frenkel, A. Etherington, M. Greene, J. Quijano, J. Xie, F. Hunter, S. Dromi, and K. C. Li, "Delivery of liposomal doxorubicin (Doxil) in breast cancer tumor model: Investigation of potential enhancement by pulsed-high intensity focused ultrasound exposure," Acad. Radiol., vol. 13, no. 4, pp. 469-479, 2006.
24. E. Hagtvet, T. J. Evjen, D. R. Olsen, S. L. Fossheim, and E. A. Nilssen, "Ultrasound enhanced antitumor activity of liposomal doxorubicin in mice," J. Drug Target., vol. 19, no. 8, pp. 701-708, 2011.
25. P. Mohan and N. Rapoport, "Doxorubicin as a molecular nanotheranostic agent: Effect of doxorubicin encapsulation in micelles or nanoemulsions on the ultrasound-mediated intracellular delivery and nuclear trafficking," Mol. Pharm., vol. 7, no. 6, pp. 1959-1973, 2010.
26. 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 drugdelivery," J. Control. Release, vol. 152, no. 2, pp. 249-256, 2011.
27. J.-M. Escoffre, J. Piron, A. Novell, and A. Bouakaz, "Doxorubicin delivery into tumor cells with ultrasound and microbubbles," Mol. Pharm., vol. 8, no. 3, pp. 799-806, 2011.
28. C. Y. Lin, J. R. Li, H. C. Tseng, M. F. Wu, and W. L. Lin, "Enhancement of focused ultrasound with microbubbles on the treatments of anticancer nanodrug in mouse tumors," Nanomedicine, vol. 8, pp. 900-907, 2012.
29. M. C. Cochran, J. R. Eisenbrey, M. C. Soulen, S. M. Schultz, R. O. Ouama, S. B. White, E. E. Furth, and M. A. Wheatley, "Disposition of ultrasound sensitive polymeric drug carrier in a rat hepatocellular carcinoma model," Acad. Radiol., vol. 18, no. 11, pp. 1341-1348, 2011.
30. F. Yan, L. Li, Z. Deng, Q. Jin, and H. Zheng, "Paclitaxel-liposome loaded microbubbles for ultrasound-triggered drug delivery in vitro and in vivo," J. Acoust. Soc. Am., vol. 131, no. 4, p. 3366, 2012.
31. A. F. Lum, M. A. Borden, P. A. Dayton, D. E. Kruse, S. I. Simon, and K. W. Ferrara, "Ultrasound radiation force enables targeted deposition of model drug carriers loaded on microbubbles," J. Control. Release, vol. 111, no. 1-2, pp. 128-134, 2006. (Pubitemid 43290001)
32. 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., vol. 18, no. 1, pp. 101-108, 2010.
33. M. Lampaskis and M. Averkiou, "Investigation of the relationship of nonlinear backscattered ultrasound intensity with microbubble concentration at low MI," Ultrasound Med. Biol., vol. 36, no. 2, pp. 306-312, 2010.
34. G. A. Brock-Fischer, M. D. Poland, and P. G. Rafter, "Means for increasing sensitivity in non-linear ultrasound imaging systems." US Patent 5 577 505, Nov. 26, 1996.
35. M. Averkiou, J. Powers, D. Skyba, M. Bruce, and S. Jensen, "Ultrasound contrast imaging research," Ultrasound Q., vol. 19, no. 1, pp. 27-37, 2003. (Pubitemid 36547040)
36. M. de Smet, S. Langereis, S. van den Bosch, and H. Grüll, "Temperature- sensitive liposomes for doxorubicin delivery under MRI guidance," J. Control. Release, vol. 143, no. 1, pp. 120-127, 2010.
37. R. Bekeredjian, R. D. Kroll, E. Fein, S. Tinkov, C. Coester, G. Winter, H. A. Katus, and H. Kulaksiz, "Ultrasound targeted microbubble destruction increases capillary permeability in hepatomas," Ultrasound Med. Biol., vol. 33, no. 10, pp. 1592-1598, 2007. (Pubitemid 47444492)
38. M. R. Böhmer, C. H. T. Chlon, B. I. Raju, C. T. Chin, T. Shevchenko, and A. L. Klibanov, "Focused ultrasound and microbubbles for enhanced extravasation," J. Control. Release, vol. 148, no. 1, pp. 18-24, 2010.
39. S. M. Stieger, C. F. Caskey, R. H. Adamson, S. Qin, F. R. E. Curry, E. R. Wisner, and K. W. Ferrara, "Enhancement of vascular permeability with low-ferquency contrast-enhanced ultrasound in the chorioallantoic membrane model," Radiology, vol. 243, no. 1, pp. 112-121, 2007. (Pubitemid 46579701)
40. M. S. Gordon, D. S. Mendelson, and G. Kato, "Tumor angiogenesis and novel antiangiogenic strategies," Int. J. Cancer, vol. 126, no. 8, pp. 1777-1787, 2010.
41. S. T. Duggan and G. M. Keating, "Pegylated liposomal doxorubicin: A review of its use in metastatic breast cancer, ovarian cancer, multiple myeloma and AIDS-related Kaposi's sarcoma," Drugs, vol. 71, no. 18, pp. 2531-2558, 2011.
42. T. Fritz, M. McKeon, and E. Unger, "Preclinical studies of MRX- 115: Safety evaluations of myocardium perfusion agent," Acad. Radiol., vol. 3, suppl. 2, pp. S185-S187, 1996.
43. S. E. Grauer, G. Sutherland, and T. Fritz, "Safety and echo contrast efficacy of multiple doses of Aerosomes MRX-115 in a phase I clinical trial," in AHA, 69th Scientific Sessions, 1996, Abs. 1857, Circulation, vol. 94, pp. I316-I319.
44. D. Bokor, "Diagnostic efficacy of SonoVue," Am. J. Cardiol., vol. 86, no. 4A, pp. 19G-24G, 2000. (Pubitemid 30645928)
45. D. Bokor, J. B. Chambers, P. J. Rees, T. G. Mant, F. Luzzani, and A. Spinazzi, "Clinical safety of SonoVue, a new contrast agent for ultrasound imaging, in healthy volunteers and in patients with chronic obstrutive pulmonary disease," Invest. Radiol., vol. 36, no. 2, pp. 104-109, 2001. (Pubitemid 32147857)
46. E. C. Unger, T. Porter, W. Culp, R. Labell, T. Matsunaga, and R. Zutshi, "Therapeutic applications of lipid-coated microbubbles," Adv. Drug Deliv. Rev., vol. 56, no. 9, pp. 1291-1314, 2004. (Pubitemid 38510475)
47. Y. Y. Zhao, C. T. Lu, Z. C. Zhou, Z. Jin, L. Zhang, C. Z. Sun, Y. Y. Xu, H. S. Gao, J. L. Tian, F. H. Gao, Q. Q. Tang, W. Li, Q. Xiang, X. Li, and W. F. Li, "Enhancing chemotherapeutic drug inhibition on tumor growth by ultrasound: An in vivo experiment," J. Drug Target., vol. 19, no. 2, pp. 154-160, 2011.