Ultrasound-enhanced drug delivery for cancer

Introduction: Ultrasound, which has traditionally been used as a diagnostic tool, is increasingly being used in non-invasive therapy and drug delivery. Areas covered: Of particular interest to this review is the rapidly accumulating evidence that ultrasound may have a key role to play both in improving the targeting and the efficacy of drug delivery for cancer. Currently available ultrasound-triggerable vehicles are first described, with particular reference to the ultrasonic mechanism that can activate release and the suitability of the size range of the vehicle used for drug delivery. Further mechanical and thermal effects of ultrasound that can enhance extravasation and drug distribution following release are then critically reviewed. Expert opinion: Acoustic cavitation is found to play a potentially key role both in achieving targeted drug release and enhanced extravasation at modest pressure amplitudes and acoustic energies, whilst simultaneously enabling real-time monitoring of the drug delivery process. The next challenge in ultrasound-enhanced drug delivery will thus be to develop a new generation of drug-carrying nanoparticles which are of the right size range for delivery to tumours, yet still capable of achieving initiation of cavitation activity and drug release at modest acoustic pressures and energies that have no safety implications for the patient.

[1]  D. Crossman,et al.  Microbubble-enhanced ultrasound for vascular gene delivery , 2000, Gene Therapy.

[2]  M. Chiao,et al.  Increased accumulation and retention of micellar paclitaxel in drug-sensitive and P-glycoprotein-expressing cell lines following ultrasound exposure. , 2012, Ultrasound in medicine & biology.

[3]  C. Arvanitis,et al.  Cavitation-enhanced extravasation for drug delivery. , 2011, Ultrasound in medicine & biology.

[4]  Michel Schneider,et al.  Characteristics of SonoVue™ , 1999 .

[5]  R. Vandenbroucke,et al.  Ultrasound assisted siRNA delivery using PEG-siPlex loaded microbubbles. , 2008, Journal of Controlled Release.

[6]  Samir Mitragotri,et al.  Healing sound: the use of ultrasound in drug delivery and other therapeutic applications , 2005, Nature Reviews Drug Discovery.

[7]  Katherine W Ferrara,et al.  Enhancement of vascular permeability with low-frequency contrast-enhanced ultrasound in the chorioallantoic membrane model. , 2007, Radiology.

[8]  J. Kuszak,et al.  Development of inherently echogenic liposomes as an ultrasonic contrast agent. , 1996, Journal of pharmaceutical sciences.

[9]  原田 慶美 Ultrasound activation of TiO₂ in melanoma tumors , 2011 .

[10]  Y. Negishi,et al.  Efficient siRNA delivery using novel siRNA-loaded Bubble liposomes and ultrasound. , 2012, International journal of pharmaceutics.

[11]  X. Liu,et al.  Torsional ultrasound modality for hard nucleus phacoemulsification cataract extraction , 2008, British Journal of Ophthalmology.

[12]  Mu-Yi Hua,et al.  Magnetic resonance monitoring of focused ultrasound/magnetic nanoparticle targeting delivery of therapeutic agents to the brain , 2010, Proceedings of the National Academy of Sciences.

[13]  A. Elshami,et al.  Retinoids augment the bystander effect in vitro and in vivo in herpes simplex virus thymidine kinase/ganciclovir-mediated gene therapy , 1997, Gene Therapy.

[14]  C. R. Hill,et al.  Physical Principles of Medical Ultrasonics, 2nd edition , 2004 .

[15]  Katherine W Ferrara,et al.  Ultrasound increases nanoparticle delivery by reducing intratumoral pressure and increasing transport in epithelial and epithelial-mesenchymal transition tumors. , 2012, Cancer research.

[16]  V. Frenkel,et al.  Delivery of liposomal doxorubicin (Doxil) in a breast cancer tumor model: investigation of potential enhancement by pulsed-high intensity focused ultrasound exposure. , 2006, Academic Radiology.

[17]  R. Esenaliev,et al.  Enhancement of Drug Delivery in Tumors by Using Interaction of Nanoparticles with Ultrasound Radiation , 2005, Technology in cancer research & treatment.

[18]  Manabu Kinoshita,et al.  A novel method for the intracellular delivery of siRNA using microbubble-enhanced focused ultrasound. , 2005, Biochemical and biophysical research communications.

[19]  Katherine W Ferrara,et al.  Driving delivery vehicles with ultrasound. , 2008, Advanced drug delivery reviews.

[20]  R. Guy,et al.  Ultrasound-mediated gene delivery: influence of contrast agent on transfection. , 2007, Bioconjugate chemistry.

[21]  Constantin Coussios,et al.  High intensity focused ultrasound: Physical principles and devices , 2007, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[22]  P. Dayton,et al.  Acoustic radiation force in vivo: a mechanism to assist targeting of microbubbles. , 1999, Ultrasound in medicine & biology.

[23]  H. Iijima,et al.  Enhanced laminin-derived peptide AG73-mediated liposomal gene transfer by bubble liposomes and ultrasound. , 2010, Molecular pharmaceutics.

[24]  Mark R Prausnitz,et al.  Mechanism of intracellular delivery by acoustic cavitation. , 2006, Ultrasound in medicine & biology.

[25]  T. Tagami,et al.  Efficient tumor regression by a single and low dose treatment with a novel and enhanced formulation of thermosensitive liposomal doxorubicin. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[26]  Ronald A. Roy,et al.  Applications of Acoustics and Cavitation to Noninvasive Therapy and Drug Delivery , 2008 .

[27]  D. Kirn Oncolytic virotherapy for cancer with the adenovirus dl1520 (Onyx-015): results of Phase I and II trials , 2001, Expert opinion on biological therapy.

[28]  W. Harvey,et al.  The stimulation of bone formation in vitro by therapeutic ultrasound. , 1997, Ultrasound in medicine & biology.

[29]  Katherine W Ferrara,et al.  Therapeutic effects of paclitaxel-containing ultrasound contrast agents. , 2006, Ultrasound in medicine & biology.

[30]  Douglas A Christensen,et al.  Drug-loaded nano/microbubbles for combining ultrasonography and targeted chemotherapy. , 2008, Ultrasonics.

[31]  R. Jain,et al.  Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Xiang Li,et al.  Preparation of nanobubbles for ultrasound imaging and intracelluar drug delivery. , 2010, International journal of pharmaceutics.

[33]  Miklós Gyöngy,et al.  Passive Spatial Mapping of Inertial Cavitation During HIFU Exposure , 2010, IEEE Transactions on Biomedical Engineering.

[34]  Sanjiv S Gambhir,et al.  Targeted microbubbles for imaging tumor angiogenesis: assessment of whole-body biodistribution with dynamic micro-PET in mice. , 2008, Radiology.

[35]  Robert C. Waag,et al.  Physical principles of medical ultrasonics , 1989 .

[36]  Zhong-gao Gao,et al.  Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy. , 2007, Journal of the National Cancer Institute.

[37]  Y. Negishi,et al.  Delivery of siRNA into the cytoplasm by liposomal bubbles and ultrasound. , 2008, Journal of controlled release : official journal of the Controlled Release Society.

[38]  M. Arora,et al.  Sonosensitive nanoparticle formulations for cavitation-mediated ultrasonic enhancement of local drug delivery , 2011 .

[39]  B. Raju,et al.  Focused ultrasound and microbubbles for enhanced extravasation. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[40]  J F Greenleaf,et al.  Ultrasound-mediated transfection of mammalian cells. , 1996, Human gene therapy.

[41]  W. Pitt,et al.  Ultrasonically activated chemotherapeutic drug delivery in a rat model. , 2002, Cancer research.

[42]  R K Jain,et al.  Openings between defective endothelial cells explain tumor vessel leakiness. , 2000, The American journal of pathology.

[43]  Flemming Forsberg,et al.  Ultrasound guided site specific gene delivery system using adenoviral vectors and commercial ultrasound contrast agents , 2006, Journal of cellular physiology.

[44]  Y. Taniyama,et al.  Development of safe and efficient novel nonviral gene transfer using ultrasound: enhancement of transfection efficiency of naked plasmid DNA in skeletal muscle , 2002, Gene Therapy.

[45]  P. Carson,et al.  The release of thrombin, using acoustic droplet vaporization (ADV), from perfluoropentane double emulsions , 2010, 2010 IEEE International Ultrasonics Symposium.

[46]  J. Shea,et al.  Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles. , 2009, Journal of controlled release : official journal of the Controlled Release Society.

[47]  Costas D Arvanitis,et al.  Ultrasound-induced cavitation enhances the delivery and therapeutic efficacy of an oncolytic virus in an in vitro model. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[48]  Zheng-Guo Cui,et al.  Regulation of gene expression in human prostate cancer cells with artificially constructed promoters that are activated in response to ultrasound stimulation. , 2013, Ultrasonics sonochemistry.

[49]  J. Kennedy High-intensity focused ultrasound in the treatment of solid tumours , 2005, Nature Reviews Cancer.

[50]  Shiro Mori,et al.  Herpes simplex virus thymidine kinase-mediated suicide gene therapy using nano/microbubbles and ultrasound. , 2008, Ultrasound in medicine & biology.

[51]  S. Homma,et al.  Effect of microbubble size on fundamental mode high frequency ultrasound imaging in mice. , 2010, Ultrasound in medicine & biology.

[52]  Hairong Zheng,et al.  Acoustically-active microbubbles conjugated to liposomes: characterization of a proposed drug delivery vehicle. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[53]  D. Belnap,et al.  Formation of eLiposomes as a drug delivery vehicle. , 2012, Colloids and surfaces. B, Biointerfaces.

[54]  M. Brandl,et al.  Ultrasound-mediated destabilization and drug release from liposomes comprising dioleoylphosphatidylethanolamine. , 2011, European journal of pharmaceutical sciences : official journal of the European Federation for Pharmaceutical Sciences.

[55]  Thierry Bettinger,et al.  Plasma membrane poration induced by ultrasound exposure: implication for drug delivery. , 2005, Journal of controlled release : official journal of the Controlled Release Society.

[56]  M. Okita,et al.  Effects of therapeutic ultrasound on joint mobility and collagen fibril arrangement in the endomysium of immobilized rat soleus muscle. , 2009, Ultrasound in medicine & biology.

[57]  Saurabh Datta,et al.  Correlation of cavitation with ultrasound enhancement of thrombolysis. , 2006, Ultrasound in medicine & biology.

[58]  Douglas L. Miller,et al.  Ultrasonic enhancement of gene transfection in murine melanoma tumors. , 1999, Ultrasound in medicine & biology.

[59]  Shao-ling Huang,et al.  Liposomes in ultrasonic drug and gene delivery. , 2008, Advanced drug delivery reviews.

[60]  F. T. ten Cate,et al.  Radionuclide tumour therapy with ultrasound contrast microbubbles. , 2004, Ultrasonics.

[61]  R K Jain,et al.  Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size. , 1995, Cancer research.

[62]  Timothy J Mason,et al.  Therapeutic ultrasound an overview. , 2011, Ultrasonics sonochemistry.

[63]  K. Tachibana,et al.  Ultrasound activation of TiO2 in melanoma tumors. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[64]  K. Tachibana,et al.  The Use of Ultrasound for Drug Delivery , 2001, Echocardiography.

[65]  R. Macdonald,et al.  Acoustically active liposomes for drug encapsulation and ultrasound-triggered release. , 2004, Biochimica et biophysica acta.

[66]  S. Kitamura,et al.  Nonviral delivery of siRNA into mesenchymal stem cells by a combination of ultrasound and microbubbles. , 2009, Journal of controlled release : official journal of the Controlled Release Society.

[67]  Douglas L. Miller,et al.  Sonoporation: Mechanical DNA Delivery by Ultrasonic Cavitation , 2002, Somatic cell and molecular genetics.

[68]  Diane Dalecki,et al.  Mechanical bioeffects of ultrasound. , 2004, Annual review of biomedical engineering.

[69]  L. Seymour Passive tumor targeting of soluble macromolecules and drug conjugates. , 1992, Critical reviews in therapeutic drug carrier systems.

[70]  O. Mykhaylyk,et al.  Targeted Endothelial Gene Delivery by Ultrasonic Destruction of Magnetic Microbubbles Carrying Lentiviral Vectors , 2012, Pharmaceutical Research.

[71]  Tom Leslie,et al.  Spatiotemporal monitoring of high-intensity focused ultrasound therapy with passive acoustic mapping. , 2012, Radiology.

[72]  E. Stride,et al.  Cavitation and contrast: The use of bubbles in ultrasound imaging and therapy , 2010, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[73]  Paul A Dayton,et al.  Formulation and acoustic studies of a new phase-shift agent for diagnostic and therapeutic ultrasound. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[74]  J. Schalken,et al.  Influence of high-intensity focused ultrasound on the development of metastases. , 1997, European urology.

[75]  H. Lipps,et al.  Towards safe, non-viral therapeutic gene expression in humans , 2005, Nature Reviews Genetics.

[76]  S. Libutti,et al.  Pulsed-High Intensity Focused Ultrasound and Low Temperature–Sensitive Liposomes for Enhanced Targeted Drug Delivery and Antitumor Effect , 2007, Clinical Cancer Research.

[77]  E. Wu,et al.  Preliminary in vitro study of ultrasound sonoporation cell labeling with superparamagnetic iron oxide particles for MRI cell tracking , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[78]  M. Brandl,et al.  Distearoylphosphatidylethanolamine-based liposomes for ultrasound-mediated drug delivery. , 2010, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[79]  K. Hynynen,et al.  Blood-brain barrier disruption induced by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index. , 2008, Ultrasound in medicine & biology.

[80]  Marilena Loizidou,et al.  Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. , 2009, Trends in pharmacological sciences.

[81]  K. Tachibana,et al.  Enhanced cytotoxic effect of Ara-C by low intensity ultrasound to HL-60 cells. , 2000, Cancer letters.

[82]  Ralf Seip,et al.  Ultrasound-triggered release of materials entrapped in microbubble-liposome constructs: a tool for targeted drug delivery. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[83]  Linda Lavery,et al.  Gene therapy of carcinoma using ultrasound-targeted microbubble destruction. , 2011, Ultrasound in medicine & biology.

[84]  J. Bai,et al.  Treatment of transplanted adriamycin-resistant ovarian cancers in mice by combination of adriamycin and ultrasound exposure. , 2004, Ultrasonics sonochemistry.

[85]  P. Fisher,et al.  Eradication of therapy-resistant human prostate tumors using an ultrasound-guided site-specific cancer terminator virus delivery approach. , 2010, Molecular therapy : the journal of the American Society of Gene Therapy.

[86]  J. Weinstein,et al.  Treatment of solid L1210 murine tumors with local hyperthermia and temperature-sensitive liposomes containing methotrexate. , 1980, Cancer research.

[87]  Richard Manasseh,et al.  Cavitation microstreaming patterns in single and multiple bubble systems , 2007, Journal of Fluid Mechanics.

[88]  Yun Zhou,et al.  The size of sonoporation pores on the cell membrane , 2008, 2008 IEEE Ultrasonics Symposium.

[89]  D. McPherson,et al.  Physical correlates of the ultrasonic reflectivity of lipid dispersions suitable as diagnostic contrast agents. , 2002, Ultrasound in medicine & biology.

[90]  Wen-zhi Chen,et al.  Circulating tumor cells in patients with solid malignancy treated by high-intensity focused ultrasound. , 2004, Ultrasound in medicine & biology.

[91]  R. Huebner,et al.  Studies on the use of viruses in the treatment of carcinoma of the cervix , 1956 .

[92]  R V Shohet,et al.  Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. , 2000, Circulation.

[93]  A. Kabalnov,et al.  Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory. , 1998, Ultrasound in medicine & biology.

[94]  M. Dewhirst,et al.  Efficacy of liposomes and hyperthermia in a human tumor xenograft model: importance of triggered drug release. , 2000, Cancer research.

[95]  Y Wu,et al.  Acoustically active lipospheres containing paclitaxel: a new therapeutic ultrasound contrast agent. , 1998, Investigative radiology.

[96]  N. Rainov,et al.  Ultrasound enhancement of liposome-mediated cell transfection is caused by cavitation effects. , 2000, Ultrasound in medicine & biology.

[97]  K. Tanaka,et al.  Tumor specific ultrasound enhanced gene transfer in vivo with novel liposomal bubbles. , 2008, Journal of controlled release : official journal of the Controlled Release Society.

[98]  K. Tanaka,et al.  Gene delivery by combination of novel liposomal bubbles with perfluoropropane and ultrasound. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[99]  L. Crum,et al.  Dual-pulse lithotripter accelerates stone fragmentation and reduces cell lysis in vitro. , 2003, Ultrasound in medicine & biology.

[100]  Y. Barenholz,et al.  Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes. , 1994, Cancer research.

[101]  W. Pitt,et al.  Ultrasonic drug delivery – a general review , 2004, Expert opinion on drug delivery.

[102]  S Otto,et al.  Dissolution of multicomponent microbubbles in the bloodstream: 2. Experiment. , 1998, Ultrasound in medicine & biology.

[103]  T. Sokoloski,et al.  Fibrin based drug delivery systems. , 1991, Journal of parenteral science and technology : a publication of the Parenteral Drug Association.

[104]  T Ikeda,et al.  Jet formation and shock wave emission during collapse of ultrasound-induced cavitation bubbles and their role in the therapeutic applications of high-intensity focused ultrasound , 2005, Physics in medicine and biology.

[105]  Roel Deckers,et al.  Ultrasound triggered, image guided, local drug delivery. , 2010, Journal of controlled release : official journal of the Controlled Release Society.