Targeted drug delivery by high intensity focused ultrasound mediated hyperthermia combined with temperature-sensitive liposomes: Computational modelling and preliminary in vivovalidation

References

• Allen TM, Cullis PR. Drug delivery systems: Entering the mainstream. Science 2004; 303: 1818–1822
   PubMed Web of Science ®Google Scholar
• Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer-chemotherapy – Mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS. Cancer Res 1986; 46: 6387–6392
   PubMed Web of Science ®Google Scholar
• Poon RT, Ng KK, Yuen J, Hahne W, Prabhakar R, Eugeni M, et al. A Phase I Dose Escalation Tolerability Study of ThermoDox™ (Thermally Sensitive Liposomal Doxorubicin) in Combination With Radiofrequency Ablation (RFA) of Primary and Metastatic Tumors of the Liver. Celsion Corporation, Columbia, MD
   Google Scholar
• Celsion. A, phase III, randomized, double-blinded, dummy-controlled study of the efficacy and safety of ThermoDox® (thermally sensitive liposomal doxorubicin) in combination with radiofrequency ablation (RFA) compared to RFA-alone in the treatment of non-resectable hepatocellular carcinoma. Clinical trial
   Google Scholar
• National Cancer Institute. A phase I dose escalation study of heat activated liposome delivery of doxorubicin and radiofrequency ablation of primary and metastatic tumors of the liver. Clinical trial. National Institutes of Health.
   Google Scholar
• Duke University Cancer Institute and National Cancer Institute. A phase I, dose escalation and pharmacokinetics study of temperature sensitive liposome encapsulated doxorubicin (ThermoDox™) and hyperthermia in patients with local-regionally recurrent breast cancer. Clinical trial. National Institutes of Health.
   Google Scholar
• Poon RT, Borys N. Lyso-thermosensitive liposomal doxorubicin: A novel approach to enhance efficacy of thermal ablation of liver cancer. Expert Opin Pharmacother 2009; 10: 333–3343
   PubMed Web of Science ®Google Scholar
• Yatvin MB, Weinstein JN, Dennis WH, Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science 1978; 202: 1290–1293
   PubMed Web of Science ®Google Scholar
• Merlin JL. Encapsulation of doxorubicin in thermosensitive small unilamellar vesicle liposomes. Eur J Cancer 1991; 27: 1026–1030
   PubMed Web of Science ®Google Scholar
• Gaber MH, Hong K, Huang SK, Papahadjopoulos D. Thermosensitive sterically stabilized liposomes: Formulation and in vitro studies on mechanism of doxorubicin release by bovine serum and human plasma. Pharm Res 1995; 12: 1407–1416
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001; 61: 3027–3032
   PubMed Web of Science ®Google Scholar
• Hossann M, Wiggenhorn M, Schwerdt A, Wachholz K, Teichert N, Eibl H, et al. In vitro stability and content release properties of phosphatidylglyceroglycerol containing thermosensitive liposomes. Biochim Biophys Acta 2007; 1768: 2491–2499
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Rumboldt Z, Al-Okaili R, Deveikis JP. Perfusion CT for head and neck tumors: Pilot study. Am J Neuroradiol 2005; 26: 1178–1185
   PubMed Web of Science ®Google Scholar
• Abdullah SS, Pialat JB, Wiart M, Duboeuf F, Mabrut JY, Bancel B, et al. Characterization of hepatocellular carcinoma and colorectal liver metastasis by means of perfusion MRI. J Magn Reson Imaging 2008; 28: 390–395
   PubMed Web of Science ®Google Scholar
• Ludemann L, Prochnow D, Rohlfing T, Franiel T, Warmuth C, Taupitz M, et al. Simultaneous quantification of perfusion and permeability in the prostate using dynamic contrast-enhanced magnetic resonance imaging with an inversion-prepared dual-contrast sequence. Ann Biomed Eng 2009; 37: 749–762
   PubMed Web of Science ®Google Scholar
• Hokland SL, Pedersen M, Salomir R, Quesson B, Stodkilde-Jorgensen H, Moonen CT. MRI-guided focused ultrasound: Methodology and applications. IEEE Trans Med Imaging 2006; 25: 723–731
   PubMed Web of Science ®Google Scholar
• ter Haar G, Coussios C. High intensity focused ultrasound: Physical principles and devices. Int J Hyperthermia 2007; 23: 89–104
   PubMed Web of Science ®Google Scholar
• Staruch R, Chopra R, Hynynen K. MRI-controlled ultrasound thermal therapy. IEEE Pulse 2011; 2: 39–47
   PubMed Web of Science ®Google Scholar
• Tempany CM, McDannold NJ, Hynynen K, Jolesz FA. Focused ultrasound surgery in oncology: Overview and principles. Radiology 2011; 259: 39–56
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Staruch R, Chopra R, Hynynen K. Localised drug release using MRI-controlled focused ultrasound hyperthermia. Int J Hyperthermia 2010; 27: 156–171
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Gasselhuber A, Appanaboyina S, Dreher MR, Partanen A, Wood BJ, Rattay F. Computational modeling of high-intensity focused ultrasound mediated drug delivery. Proc SPIE 2011; 7901: 7910F
   Google Scholar
• Ranjan A, Jacobs GC, 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 2012; 158: 487–494
   PubMed Web of Science ®Google Scholar
• El-Kareh AW, Secomb TW. Theoretical models for drug delivery to solid tumors. Crit Rev Biomed Eng 1997; 25: 503–571
   PubMed Web of Science ®Google Scholar
• El-Kareh AW, Secomb TW. A mathematical model for comparison of bolus injection, continuous infusion, and liposomal delivery of doxorubicin to tumor cells. Neoplasia 2000; 2: 325–338
   PubMed Web of Science ®Google Scholar
• Zhang A, Mi X, Yang G, Xu LX. Numerical study of thermally targeted liposomal drug delivery in tumor. J Heat Transfer 2009; 131: 043209–0432010
   Web of Science ®Google Scholar
• Pennes HH. Analysis of tissue and arterial blood temperatures in the resting human forearm. J Appl Physiol 1948; 1: 93–122
   PubMed Web of Science ®Google Scholar
• Partanen A, Mougenot C, Vaara T. Feasibility of agar-silica phantoms in quality assurance of MRgHIFU. AIP Conference Proceedings 2009; 1113: 296–300
   Google Scholar
• Ishihara Y, Calderon A, Watanabe H, Okamoto K, Suzuki Y, Kuroda K. A precise and fast temperature mapping using water proton chemical shift. Magn Reson Med 1995; 34: 814–823
   PubMed Web of Science ®Google Scholar
• Brown SL, Hunt JW, Hill RP. Differential thermal sensitivity of tumour and normal tissue microvascular response during hyperthermia. Int J Hyperthermia 1992; 8: 501–514
   PubMed Web of Science ®Google Scholar
• Breen MS, Breen M, Butts K, Chen L, Saidel GM, Wilson DL. MRI-guided thermal ablation therapy: Model and parameter estimates to predict cell death from mr thermometry images. Ann Biomed Eng 2007; 35: 1391–1403
   PubMed Web of Science ®Google Scholar
• Duck FA. Chapter 2: Thermal properties of tissue. Physical properties of tissue. Academic Press, London 1990; 167–223
   Google Scholar
• Van Beers BE, Leconte I, Materne R, Smith AM, Jamart J, Horsmans Y. Hepatic perfusion parameters in chronic liver disease: Dynamic CT measurements correlated with disease severity. Am J Roentgenol 2001; 176: 667–673
   PubMed Web of Science ®Google Scholar
• Gustafson DL, Rastatter JC, Colombo T, Long ME. Doxorubicin pharmacokinetics: Macromolecule binding, metabolism, and excretion in the context of a physiologic model. J Pharm Sci 2002; 91: 1488–1501
   PubMed Web of Science ®Google Scholar
• El-Kareh AW, Secomb TW. Two-mechanism peak concentration model for cellular pharmacodynamics of doxorubicin. Neoplasia 2005; 7: 705–713
   PubMed Web of Science ®Google Scholar
• Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, et al. Estimating kinetic parameters from dynamic contrast-enhanced t(1)-weighted MRI of a diffusable tracer: Standardized quantities and symbols. J Magn Reson Imaging 1999; 10: 223–232
   PubMed Web of Science ®Google Scholar
• Brizel DM, Klitzman B, Cook JM, Edwards J, Rosner G, Dewhirst MW. A comparison of tumor and normal tissue microvascular hematocrits and red cell fluxes in a rat window chamber model. Int J Radiat Oncol Biol Phys 1993; 25: 269–276
   PubMed Web of Science ®Google Scholar
• Sparano JA, Speyer J, Gradishar WJ, Liebes L, Sridhara R, Mendoza S, et al. Phase I trial of escalating doses of paclitaxel plus doxorubicin and dexrazoxane in patients with advanced breast cancer. J Clin Oncol 1999; 17: 880–886
   PubMed Web of Science ®Google Scholar
• Jackson TL. Intracellular accumulation and mechanism of action of doxorubicin in a spatio-temporal tumor model. J Theor Biol 2003; 220: 201–213
   PubMed Web of Science ®Google Scholar
• Brown RP, Delp MD, Lindstedt SL, Rhomberg LR, Beliles RP. Physiological parameter values for physiologically based pharmacokinetic models. Toxicol Ind Health 1997; 13: 407–484
   PubMed Web of Science ®Google Scholar
• Yuan F, Leunig M, Berk DA, Jain RK. Microvascular permeability of albumin, vascular surface area, and vascular volume measured in human adenocarcinoma LS174T using dorsal chamber in SCID mice. Microvasc Res 1993; 45: 269–289
   PubMed Web of Science ®Google Scholar
• Jain RK. Transport of molecules in the tumor interstitium: A review. Cancer Res 1987; 47: 3039–3051
   PubMed Web of Science ®Google Scholar
• Qian F, Stowe N, Liu EH, Saidel GM, Gao J. Quantification of in vivo doxorubicin transport from PLGA millirods in thermoablated rat livers. J Control Release 2003; 91: 157–166
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Partanen A, Yarmolenko PS, Viitala A, Appanaboyina S, Haemmmerich D, Ranjan A, et al. Mild hyperthermia with magnetic resonance guided high intensity focused ultrasound for applications in drug delivery. Int J Hyperthermia 2012
   Web of Science ®Google Scholar
• Patel PR, 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
   PubMed Web of Science ®Google Scholar
• 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 thermometry-guided focused ultrasound (MRGHIFU). Magn Reson Med 2009; 61: 603–614
   PubMed Web of Science ®Google Scholar
• Kawai H, Minamiya Y, Kitamura M, Matsuzaki I, Hashimoto M, Suzuki H, Abo S. Direct measurement of doxorubicin concentration in the intact, living single cancer cell during hyperthermia. Cancer 1997; 79: 214–219
   PubMed Web of Science ®Google Scholar
• Goldberg SN, Saldinger PF, Gazelle GS, Huertas JC, Stuart KE, Jacobs T, et al. Percutaneous tumor ablation: Increased necrosis with combined radio-frequency ablation and intratumoral doxorubicin injection in a rat breast tumor model. Radiology 2001; 220: 420–427
   PubMed Web of Science ®Google Scholar