Enhanced drug delivery in rabbit VX2 tumours using thermosensitive liposomes and MRI-controlled focused ultrasound hyperthermia

International Journal of Hyperthermia

Volumn 28, Issue 8, 2012, Pages 776-787

  Staruch, Robert M ^a,b   Ganguly, Milan ^a   Tannock, Ian F ^b,c   Hynynen, Kullervo ^a,b   Chopra, Rajiv ^a,b  

^a Sunnybrook Health Sciences Centre   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

Focused ultrasound; Heat targeted drug delivery; Image guided therapy; Magnetic resonance imaging; Non invasive thermometry

Indexed keywords

DOXORUBICIN; GADODIAMIDE; LIPOSOME; LYSO THERMOSENSITIVE LIPOSOMAL DOXORUBICIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CONTRAST ENHANCEMENT; CONTROLLED FOCUSED ULTRASOUND HYPERTHERMIA; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG ELIMINATION; DRUG RELEASE; DRUG TISSUE LEVEL; DRUG TUMOR LEVEL; EXPERIMENTAL RABBIT; FLUORESCENCE; FLUORESCENCE MICROSCOPY; HEAT TARGETED DRUG DELIVERY; HEATING; MAGNETIC RESONANCE THERMOMETRY; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; TEMPERATURE SENSITIVITY; THERMOMETRY; TISSUE HOMOGENATE; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR MODEL; TUMOR VOLUME; ULTRASOUND;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; DOXORUBICIN; DRUG DELIVERY SYSTEMS; LIPOSOMES; MAGNETIC RESONANCE IMAGING; MALE; NEOPLASMS; RABBITS; ULTRASONIC THERAPY;

EID: 84869421419     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2012.736670     Document Type: Article

References (48)

1. Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer 2006;6:583-592. (Pubitemid 44140857)
2. Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 2010;7:653-664.
3. Tredan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 2007;99:1441-1454.
4. Kong G, Braun RD, Dewhirst MW. Hyperthermia enables tumor-specific nanoparticle delivery: Effect of particle size. Cancer Res 2000;60:4440-4445. (Pubitemid 32103623)
5. Drummond DC, Noble CO, Hayes ME, Park JW, Kirpotin DB. Pharmacokinetics and In Vivo Drug Release Rates in Liposomal Nanocarrier Development. J Pharm Sci 2008;97:4696-4740.
6. Needham D, Dewhirst MW. The development and testing of a new temperature-sensitive drug delivery system for the treatment of solid tumors. Adv Drug Deliv Rev 2001;53:285-305. (Pubitemid 34024911)
7. Li L, ten Hagen TL, Schipper D, Wijnberg TM, van Rhoon GC, Eggermont AM, et al. Triggered content release from optimized stealth thermosensitive liposomes using mild hyperthermia. J Control Release 2010;143:274-279.
8. de Smet M, Heijman E, Langereis S, Hijnen NM, Grull H. Magnetic resonance imaging of high intensity focused ultrasound mediated drug delivery from temperature-sensitive liposomes: An in vivo proof-of-concept study. J Control Release 2011;150:102-110.
9. Tagami T, Ernsting MJ, Li S. Efficient tumor regression by a single and low dose treatment with a novel and enhanced formulation of thermosensitive liposomal doxorubicin. J Control Release 2011;152:303-309.
10. Chen Q, Krol A, Wright A, Needham D, Dewhirst MW, Yuan F. Tumor microvascular permeability is a key determinant for antivascular effects of doxorubicin encapsulated in a temperature sensitive liposome. Int J Hyperthermia 2008;24:475-482.
11. Yarmolenko PS, Zhao Y, Landon C, Spasojevic I, Yuan F, Needham D, et al. Comparative effects of thermosensitive doxorubicin-containing liposomes and hyperthermia in human and murine tumours. Int J Hyperthermia 2010;26:485-498.
12. Kong G, Anyarambhatla G, Petros WP, Braun RD, Colvin OM, Needham D, et al. Efficacy of liposomes and hyperthermia in a human tumor xenograft model: Importance of triggered drug release. Cancer Res 2000;60:6950-6957. (Pubitemid 32059168)
13. Gasselhuber A, Dreher MR, Negussie A, Wood BJ, Rattay F, Haemmerich D. Mathematical spatio-temporal model of drug delivery from low temperature sensitive liposomes during radiofrequency tumour ablation. Int J Hyperthermia 2010;26:499-513.
14. Poon RTP, Borys N. Lyso-thermosensitive liposomal doxorubicin: An adjuvant to increase the cure rate of radiofrequency ablation in liver cancer. Future Oncol 2011;7:937-945.
15. Celsion. Phase 1/2 study of ThermoDox with approved hyperthermia in treatment of breast cancer recurrence at the chest wall (DIGNITY). Available at: http://www. clinicaltrials.gov/ct2/show/NCT00826085 (accessed 19 March 2011).
16. Van Der Zee J, De Bruijne M, Mens JWM, Ameziane A, Broekmeyer-Reurink MP, Drizdal T, et al. Reirradiation combined with hyperthermia in breast cancer recurrences: Overview of experience in Erasmus MC. Int J Hyperthermia 2010;26:638-648.
17. Ahmed M, Brace CL, Lee FT, Goldberg SN. Principles of and advances in percutaneous ablation. Radiology 2011;258:351-369.
18. Hynynen K. MRIgHIFU: A tool for image-guided therapeutics. J Magn Reson Imaging 2011;34:482-493.
19. Salomir R, Vimeux FC, de Zwart JA, Grenier N, Moonen CTW. Hyperthermia by MR-guided focused ultrasound: Accurate temperature control based on fast MRI and a physical model of local energy deposition and heat conduction. Magn Reson Med 2000;43:342-347. (Pubitemid 30127519)
20. Smith NB, Merrilees NK, Dahleh M, Hynynen K. Control system for an MRI compatible intracavitary ultrasound array for thermal treatment of prostate disease. Int J Hyperthermia 2001;17:271-282. (Pubitemid 32421608)
21. Arora D, Cooley D, Perry T, Guo J, Richardson A, Moellmer J, et al. MR thermometry-based feedback control of efficacy and safety in minimum-time thermal therapies: Phantom and in-vivo evaluations. Int J Hyperthermia 2006;22:29-42. (Pubitemid 43158215)
22. Enholm JK, Kohler MO, Quesson B, Mougenot C, Moonen CT, Sokka SD. Improved volumetric MR-HIFU ablation by robust binary feedback control. IEEE Trans Biomed Eng 2010;57:103-113.
23. Negussie AH, Yarmolenko PS, Partanen A, Ranjan A, Jacobs G, Woods D, et al. Formulation and characterisation of magnetic resonance imageable thermally sensitive liposomes for use with magnetic resonance-guided high intensity focused ultrasound. Int J Hyperthermia 2011;27:140-155.
24. Tagami T, Foltz WD, Ernsting MJ, Lee CM, Tannock IF, May JP, et al. MRI monitoring of intratumoral drug delivery and prediction of the therapeutic effect with a multifunctional thermosensitive liposome. Biomaterials 2011;32:6570-6578.
25. Staruch R, Chopra R, Hynynen K. Localised drug release using MRI-controlled focused ultrasound hyperthermia. Int J Hyperthermia 2011;27:156-171.
26. Dromi S, Frenkel V, Luk A, Traughber B, Angstadt M, Bur M, et al. Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin Cancer Res 2007;13:2722-2727. (Pubitemid 46788041)
27. Ranjan A, Jacobs G, Woods DL, Negussie AH, Partanen A, Yarmolenko PS, et al. Image-guided drug delivery with magnetic resonance guided high intensity focused ultrasound and temperature sensitive liposomes in a rabbit VX2 tumor model. J Control Release 2011;158:487-494.
28. Chopra R, Curiel L, Staruch R, Morrison L, Hynynen K. An MRI-compatible system for focused ultrasound experiments in small animal models. Med Phys 2009;36:1867-1874.
29. Dudar TE, Jain RK. Differential response of normal and tumor microcirculation to hyperthermia. Cancer Res 1984;44:605-612. (Pubitemid 14187461)
30. McDannold NJ, King RL, Jolesz FA, Hynynen KH. Usefulness of MR imaging-derived thermometry and dosimetry in determining the threshold for tissue damage induced by thermal surgery in rabbits. Radiology 2000;216:517-523. (Pubitemid 30599876)
31. Staruch R, Chopra R, Hynynen K. MRI-controlled focused ultrasound hyperthermia for targeted drug delivery in bone: In vivo results. Radiology 2012;263:117-127.
32. Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys 1984;10:787-800. (Pubitemid 14094055)
33. Bachur NR, Moore AL, Bernstein JG, Liu A. Tissue distribution and disposition of daunomycin (NCS-82151) in mice: Fluorometric and isotopic methods. Cancer Chemother Rep 1970;54:89-94.
34. Primeau AJ, Rendon A, Hedley D, Lilge L, Tannock IF. The distribution of the anticancer drug doxorubicin in relation to blood vessels in solid tumors. Clin Cancer Res 2005;11:8782-8788. (Pubitemid 43005929)
35. Little RA. Changes in blood volume of rabbit with age. J Physiol 1970;208:485-497.
36. Robert J, Illiadis A, Hoerni B, Cano JP, Durand M, Lagarde C. Pharmacokinetics of Adriamycin in patients with breast cancer Y Correlation between pharmacokinetic parameters and clinical short-term response. Eur J Cancer Clin Oncol 1982;18:739-745. (Pubitemid 12033227)
37. Kidd JG, Rous P. A transplantable rabbit carcinoma originating in a virus-induced papilloma and containing the virus in masked or altered form. J Exp Med 1940;71:813-U22.
38. Purdie TG, Henderson E, Lee TY. Functional CT imaging of angiogenesis in rabbit VX2 soft-tissue tumour. Phys Med Biol 2001;46:3161-3175. (Pubitemid 34568065)
39. Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001;61:3027-3032. (Pubitemid 32691950)
40. Gasselhuber A, Dreher MR, Partanen A, Yarmolenko PS, Woods D, Wood BJ, et al. Targeted drug delivery by high intensity focused ultrasound mediated hyperthermia combined with temperature-sensitive liposomes: Computational modelling and preliminary in vivo validation. Int J Hyperthermia 2012;28:337-348.
41. Ponce AM, Viglianti BL, Yu D, Yarmolenko PS, Michelich CR, Woo J, et al. Magnetic resonance imaging of temperature-sensitive liposome release: Drug dose painting and antitumor effects. J Natl Cancer Inst 2007;99:53-63.
42. Patel P, Luk A, Durrani A, Dromi S, Cuesta J, Angstadt M, et al. In vitro and in vivo evaluations of increased effective beam width for heat deposition using a split focus high intensity ultrasound (HIFU) transducer. Int J Hyperthermia 2008;24:537-549.
43. Yarmolenko PS, Moon EJ, Landon C, Manzoor A, Hochman DW, Viglianti BL, et al. Thresholds for thermal damage to normal tissues: An update. Int J Hyperthermia 2011;27:320-343.
44. Marmor JB. Interactions of hyperthermia and chemotherapy in animals. Cancer Res 1979;39:2269-2276. (Pubitemid 9185422)
45. Kerr DJ, Kerr AM, Freshney RI, Kaye SB. Comparative intracellular uptake of Adriamycin and 4'-deoxydoxorubicin by non-small cell lung-tumor cells in culture and its relationship to cell-survival. Biochem Pharmacol 1986;35:2817-2823. (Pubitemid 16051530)
46. Kohler MO, Mougenot C, Quesson B, Enholm J, Le Bail B, Laurent C, et al. Volumetric HIFU ablation under 3D guidance of rapid MRI thermometry. Med Phys 2009;36:3521-3535.
47. Mougenot C, Quesson B, de Senneville BD, de Oliveira PL, Sprinkhuizen S, Palussiere J, et al. Three-dimensional spatial and temporal temperature control with MR thermometryguided focused ultrasound (MRgHIFU). Magn Reson Med 2009;61:603-614.
48. Partanen A, Yarmolenko PS, Viitala A, Appanaboyina S, Haemmerich D, Ranjan A, et al. Mild hyperthermia with magnetic resonance-guided high-intensity focused ultrasound for applications in drug delivery. Int J Hyperthermia 2012;28:320-336.