Liposomes in Active, Passive and Acoustically-Triggered Drug Delivery

Author(s): Sara Al Basha, Najla Salkho, Sarah Dalibalta, Ghaleb Adnan Husseini*.

Journal Name: Mini-Reviews in Medicinal Chemistry

Volume 19 , Issue 12 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Cancer has become one of the most deadly noncommunicable diseases globally. Several modalities used to treat cancer patients exist today yet many have failed to prove high efficacy with low side effects. The most common example of such modalities is the use of chemotherapeutic drugs to treat cancerous cells and deter their uncontrolled proliferation. In addition to the destruction of cancerous tissues, chemotherapy destroys healthy tissues as it lacks the specificity to annihilate cancerous cells only and preferentially, which result in adverse side effects including nausea, hair fall and myocardial infarction. To prevent the side effects of non-selective chemotherapy, cancer therapy research has been focused on the implementation of nanocarrier systems that act as vehicles to encapsulate drugs and selectively transport their agent to the tumor site. In this paper, we shed light on liposomes along with three anticancer drug delivery approaches: passive, active and ultrasound-triggered drug delivery.

Keywords: Drug delivery, passive targeting, active targeting, triggered targeting, ultrasound, liposomes.

[1]
Ferlay, J.; Soerjomataram, I.; Ervik, M.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. GLOBOCAN 2012: Estimated cancer incidence, mortality and prevalence worldwide in 2012.IARC cancer base No. 11IARC Sci Pub[Online]2012, http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx (Accessed August 11, 2018).
[2]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2018. CA Cancer J. Clin., 2018, 68(1), 7-30.
[3]
Dickens, E.; Ahmed, S. Principles of cancer treatment by chemotherapy. Surgery, 2018, 36(3), 134-138.
[4]
Symonds, R.P.; Foweraker, K. Principles of chemotherapy and radiotherapy. Curr. Obstet. Gynaecol., 2006, 16(2), 100-106.
[5]
Types of cancer treatment. J. Nat. Cancer Inst., https://www.cancer.gov/about-cancer/treatment/types (Accessed August 11, 2018).
[6]
Pastorino, F.; Brignole, C.; Di Paolo, D.; Nico, B.; Pezzolo, A.; Marimpietri, D.; Pagnan, G.; Piccardi, F.; Cilli, M.; Longhi, R.; Ribatti, D.; Corti, A.; Allen, T.M.; Ponzoni, M. Targeting liposomal chemotherapy via both tumors cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy. Cancer Res., 2006, 66(20), 10073-10082.
[7]
Monsuez, J.J.; Charniot, J.C.; Vignat, N.; Artigou, J.Y. Cardiac side-effects of cancer chemotherapy. Int. J. Cardiol., 2010, 144(1), 3-15.
[8]
Elkhodiry, M.A.; Momah, C.C.; Suwaidi, S.R.; Gadalla, D.; Martins, A.M.; Vitor, R.F.; Husseini, G.A. Synergistic nanomedicine: Passive, active, and ultrasound-triggered drug delivery in cancer treatment. J. Nanosci. Nanotechnol., 2016, 16(1), 1-18.
[9]
Pitt, W.G.; Husseini, G.A.; Roeder, B.L.; Dickinson, D.J.; Warden, D.R.; Hartley, J.M.; Jones, P.W. Preliminary results of combining low frequency low intensity ultrasound and liposomal drug delivery to treat tumors in rats. J. Nanosci. Nanotechnol., 2011, 11(3), 1866-1870.
[10]
Husseini, G.A.; Pitt, W.G.; Martins, A.M. Ultrasonically triggered drug delivery: breaking the barrier. Colloids Surf. B Biointerfaces, 2014, 123, 364-386.
[11]
Collins, I.; Workman, P. New approaches to molecular cancer therapeutics. Nat. Chem. Biol., 2006, 2(12), 689-700.
[12]
Dua, J.S.; Rana, A.C.; Bhandari, A.K. Liposome: Methods of preparation and applications. Intl. J. Pharm. Stud. Res., 2012, 3(2), 14-20.
[13]
Deamer, D.W. From “banghasomes” to liposomes: a memoir of Alec Bangham, 1921-2010. FASEB J., 2010, 24(5), 1308-1310.
[14]
Wagner, A.; Vorauer-Uhl, K. Liposome technology for industrial purposes. J. Drug Deliv., 2011, 2011, 1-9.
[15]
Monteiro, N.; Martins, A.; Reis, R.L.; Neves, N.M. Liposomes in tissue engineering and regenerative medicine. J. R. Soc. Interface, 2014, 11(101)
[http://dx.doi.org/10.1098/rsif.2014.0459]
[16]
Willis, M.; Forssen, E. Ligand-targeted liposomes. Adv. Drug Deliv. Rev., 1998, 29(3), 249-271.
[17]
Brey, R.N.; Liang, L. Polymerizable fatty acids, phospholipids and polymerized liposomes therefrom. U.S. Patent US6187335B1, February 13, 2001.
[18]
Leung, S.J.; Romanowski, M. Light-activated content release from liposomes. Theranostics, 2012, 2(10), 1020-1036.
[19]
Gabizon, A.A. Stealth liposomes and tumor targeting: One step further in the quest for the magic bullet. Clin. Cancer Res., 2001, 7(2), 223-225.
[20]
Juliano, R.L.; Stamp, D. The effect of particle size and charge on the clearance rates of liposomes and liposome encapsulated drugs. Biochem. Biophys. Res. Commun., 1975, 63(3), 651-658.
[21]
Magin, R.L.; Hunter, J.M.; Niesman, M.R.; Bark, G.A. Effect of vesicle size on the clearance, distribution, and tumor uptake of temperature-sensitive liposomes. Cancer Drug Deliv., 1986, 3(4), 223-237.
[22]
Fenske, D.B.; Cullis, P.R. Entrapment of small molecules and nucleic acid-based drugs in liposomes. Methods Enzymol., 2005, 391, 7-40.
[23]
Noble, G.T.; Stefanick, J.F.; Ashley, J.D.; Kiziltepe, T.; Bilgicer, B. Ligand-targeted liposome design: Challenges and fundamental considerations. Trends Biotechnol., 2014, 32(1), 32-45.
[24]
Karanth, H.; Murthy, R.S. pH-sensitive liposomes-principle and application in cancer therapy. J. Pharm. Pharmacol., 2007, 59(4), 469-483.
[25]
Barenholz, Y. Doxil®—The first FDA-approved nano-drug: Lessons learned. J. Control. Release, 2012, 160(2), 117-134.
[26]
Delivered by stealth® technology home page. https://www.doxil.com/ (Accessed August 16, 2018).
[27]
Wong, A.D.; Ye, M.; Ulmschneider, M.B.; Searson, P.C. Quantitative analysis of the enhanced permeation and retention (EPR) effect. PLoS One, 2015, 10(5)e0123461
[28]
Bulbake, U.; Doppalapudi, S.; Kommineni, N.; Khan, W. Liposomal formulations in clinical use: An updated review. Pharmaceutics, 2017, 9(2), 12.
[29]
Prescribing Myocet®. http://www.tevauk.com/hcp/myocet (Accessed August 16, 2018).
[30]
Swenson, C.E.; Perkins, W.R.; Roberts, P.; Janoff, A.S. Liposome technology and the development of Myocet™ (liposomal doxorubicin citrate). Breast, 2001, 10, 1-7.
[31]
Myocet https://www.drugs.com/uk/myocet.html (Accessed August 16, 2018).
[32]
Amreddy, N.; Babu, A.; Muralidharan, R.; Panneerselvam, J.; Srivastava, A.; Ahmed, R.; Mehta, M.; Munshi, A.; Ramesh, R. Recent advances in nanoparticle-based cancer drug and gene delivery. Adv. Cancer Res., 2018, 137, 115-170.
[33]
Mepact home page. http://www.mepact.net/ (Accessed August 16, 2018).
[34]
Silverman, J.A.; Deitcher, S.R. Marqibo® (vincristine sulfate liposome injection) improves the pharmacokinetics and pharmacodynamics of vincristine. Cancer Chemother. Pharmacol., 2013, 71(3), 555-564.
[35]
The first and only liposome-encapsulated vincristine. http://www.marqibo.com/ (Accessed August 16, 2018).
[36]
Burade, V.; Bhowmick, S.; Maiti, K.; Zalawadia, R.; Ruan, H.; Thennati, R. Lipodox® (generic doxorubicin hydrochloride liposome injection): In vivo efficacy and bioequivalence versus Caelyx® (doxorubicin hydrochloride liposome injection) in human mammary carcinoma (MX-1) xenograft and syngeneic fibrosarcoma (WEHI 164) mouse mode. BMC Cancer, 2017, 17(1), 405.
[37]
Understanding therapy with ONIVYDE® (Irinotecan Liposome Injection). https://www.onivyde.com/for-patients/ (Accessed August 26, 2018).
[39]
Kim, M.; Williams, S. Daunorubicin and cytarabine liposome in newly diagnosed therapy-related acute myeloid leukemia (AML) or AML with myelodysplasia-related changes. Ann. Pharmacother., 2018, 52(8), 792-800.
[40]
Drug approval package: VYXEOS (daunorubicin and cytarabine). https://www.accessdata.fda.gov/drugsatfda_docs/nda/2017/209401Orig1s000ChemR.pdf (Accessed August 27, 2018).
[41]
Park, K. Facing the truth about nanotechnology in drug delivery. ACS Nano, 2013, 7(9), 7442-7447.
[42]
Lattin, J.R.; Pitt, W.G.; Belnap, D.M.; Husseini, G.A. Ultrasound-induced calcein release from eLiposomes. Ultrasound Med. Biol., 2012, 38(12), 2163-2173.
[43]
Staples, B.J.; Pitt, W.G.; Roeder, B.L.; Husseini, G.A.; Rajeev, D.; Schaalje, G.B. Distribution of doxorubicin in rats undergoing ultrasonic drug delivery. J. Pharm. Sci., 2010, 99(7), 3122-3131.
[44]
Moussa, H.G.; Martins, A.M.; Husseini, G.A. Review on triggered liposomal drug delivery with a focus on ultrasound. Curr. Cancer Drug Targets, 2015, 15(4), 282-313.
[45]
Khokhlova, T.D.; Haider, Y.; Hwang, J.H. Therapeutic potential of ultrasound microbubbles in gastrointestinal oncology: Recent advances and future prospects. Therap. Adv. Gastroenterol., 2015, 8(6), 384-394.
[46]
Lentacker, I.; Geers, B.; Demeester, J.; De Smedt, S.C.; Sanders, N.N. Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: Cytotoxicity and mechanisms involved. Mol. Ther., 2010, 18(1), 101-108.
[47]
Lattin, J.R.; Pitt, W.G. Factors affecting ultrasonic release from eLiposomes. J. Pharm. Sci., 2015, 104(4), 1373-1384.
[48]
Byrne, J.D.; Betancourt, T.; Brannon-Peppas, L. Active targeting schemes for nanoparticle systems in cancer therapeutics. Adv. Drug Deliv. Rev., 2008, 60(15), 1615-1626.
[49]
Torchilin, V.P. Multifunctional nanocarriers. Adv. Drug Deliv. Rev., 2006, 58(14), 1532-1555.
[50]
Hillen, F.; Griffioen, A.W. Tumour vascularization: sprouting angiogenesis and beyond. Cancer Metastasis Rev., 2007, 26(3-4), 489-502.
[51]
Zetter, B.R. Angiogenesis and tumor metastasis. Annu. Rev. Med., 1998, 49, 407-424.
[52]
Greish, K. Enhanced permeability and retention (EPR) effect for anticancer nanomedicine drug targeting. Methods Mol. Biol., 2010, 624, 25-37.
[53]
Aggarwal, P.; Hall, J.B.; McLeland, C.B.; Dobrovolskaia, M.A.; McNeil, S.E. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv. Drug Deliv. Rev., 2009, 61(6), 428-437.
[54]
Greish, K. Enhanced permeability and retention of macromolecular drugs in solid tumors: A royal gate for targeted anticancer nanomedicines. J. Drug Target., 2007, 15(7-8), 457-464.
[55]
Fang, J.; Sawa, T.; Maeda, H. Factors and mechanism of “EPR” effect and the enhanced antitumor effects of macromolecular drugs including SMANCS. Adv. Exp. Med. Biol., 2003, 519, 29-49.
[56]
Jhaveri, A.M.; Torchilin, V.P. Multifunctional polymeric micelles for delivery of drugs and siRNA. Front. Pharmacol., 2014, 5, 1-26.
[57]
Vaage, J.; Donovan, D.; Uster, P.; Working, P. Tumour uptake of doxorubicin in polyethylene glycol-coated liposomes and therapeutic effect against a xenografted human pancreatic carcinoma. Br. J. Cancer, 1997, 75(4), 482-486.
[58]
Maeda, H.; Bharate, G.Y.; Daruwalla, J. Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect. Eur. J. Pharm. Biopharm., 2009, 71(3), 409-419.
[59]
Harrington, K.J.; Mohammadtaghi, S.; Uster, P.S.; Glass, D.; Peters, A.M.; Vile, R.G.; Stewart, J.S. Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes. Clin. Cancer Res., 2001, 7(2), 243-254.
[60]
Dams, E.T.; Laverman, P.; Oyen, W.J.; Storm, G.; Scherphof, G.L.; van Der Meer, J.W.; Corstens, F.H.; Boerman, O.C. Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharmacol. Exp. Ther., 2000, 292(3), 1071-1079.
[61]
Ishida, T.; Maeda, R.; Ichihara, M.; Irimura, K.; Kiwada, H. Accelerated clearance of PEGylated liposomes in rats after repeated injections. J. Control. Release, 2003, 88(1), 35-42.
[62]
Ishida, T.; Harada, M.; Wang, X.Y.; Ichihara, M.; Irimura, K.; Kiwada, H. Accelerated blood clearance of PEGylated liposomes following preceding liposome injection: Effects of lipid dose and PEG surface-density and chain length of the first-dose liposomes. J. Control. Release, 2005, 105(3), 305-317.
[63]
Laverman, P.; Carstens, M.G.; Boerman, O.C.; Dams, E.T.; Oyen, W.J.; van Rooijen, N.; Corstens, F.H.; Storm, G. Factors affecting the accelerated blood clearance of polyethylene glycol-liposomes upon repeated injection. J. Pharmacol. Exp. Ther., 2001, 298(2), 607-612.
[64]
Hossen, M.N.; Kajimoto, K.; Tatsumi, R.; Hyodo, M.; Harashima, H. Comparative assessments of crucial factors for a functional ligand-targeted nanocarrier. J. Drug Target., 2014, 22(7), 600-609.
[65]
Carlsson, J.; Kullberg, E.B.; Capala, J.; Sjöberg, S.; Edwards, K.; Gedda, L. Ligand liposomes and boron neutron capture therapy. J. Neurooncol., 2003, 62(1-2), 47-59.
[66]
Steichen, S.D.; Caldorera-Moore, M.; Peppas, N.A. A review of current nanoparticle and targeting moieties for the delivery of cancer therapeutics. Eur. J. Pharm. Sci., 2013, 48(3), 416-427.
[67]
Park, J.W. Liposome-based drug delivery in breast cancer treatment. Breast Cancer Res., 2002, 4(3), 95-99.
[68]
Park, J.W.; Hong, K.; Carter, P.; Asgari, H.; Guo, L.Y.; Keller, G.A.; Wirth, C.; Shalaby, R.; Kotts, C.; Wood, W.I. Development of anti-p185HER2 immunoliposomes for cancer therapy. Proc. Natl. Acad. Sci. USA, 1995, 92(5), 1327-1331.
[69]
Kirpotin, D.; Park, J.W.; Hong, K.; Zalipsky, S.; Li, W.L.; Carter, P.; Benz, C.C.; Papahadjopoulos, D. Sterically stabilized anti-HER2 immunoliposomes: Design and targeting to human breast cancer cells in vitro. Biochemistry, 1997, 36(1), 66-75.
[70]
Yuan, M.; Qiu, Y.; Zhang, L.; Gao, H.; He, Q. Targeted delivery of transferrin and TAT co-modified liposomes encapsulating both paclitaxel and doxorubicin for melanoma. Drug Deliv., 2016, 23(4), 1171-1183.
[71]
Tang, J.; Zhang, L.; Liu, Y.; Zhang, Q.; Qin, Y.; Yin, Y.; Yuan, W.; Yang, Y.; Xie, Y.; Zhang, Z.; He, Q. Synergistic targeted delivery of payload into tumor cells by dual-ligand liposomes co-modified with cholesterol anchored transferrin and TAT. Int. J. Pharm., 2013, 454(1), 31-40.
[72]
Wang, R.H.; Cao, H.M.; Tian, Z.J.; Jin, B.; Wang, Q.; Ma, H.; Wu, J. Efficacy of dual-functional liposomes containing paclitaxel for treatment of lung cancer. Oncol. Rep., 2015, 33(2), 783-791.
[73]
Sharma, G.; Modgil, A.; Layek, B.; Arora, K.; Sun, C.; Law, B.; Singh, J. Cell penetrating peptide tethered bi-ligand liposomes for delivery to brain in vivo: Biodistribution and transfection. J. Control. Release, 2013, 167(1), 1-10.
[74]
ClinicalTrials.gov registry. Study of MBP-426 in patients with second line gastric, gastroesophageal, or esophageal adenocarcinoma. US Nat. Lib. Med. , 2014.
[75]
van der Meel, R.; Vehmeijer, L.J.C.; Kok, R.J.; Storm, G.; van Gaal, E.V.B. Ligand-targeted particulate nanomedicines undergoing clinical evaluation: Current Status. In: Intracellular Delivery III: Market Entry Barriers of Nanomedicines; Prokop, A.; Weissig, V., Eds.; Springer: Switzerland, 2016; pp. 163-200.
[76]
Liu, R.; Xiao, K.; Luo, J.; Lam, K.S. Development of cancer-targeting ligands and ligand-drug conjugates. In: Drug Delivery in Oncology: From Basic Research to Cancer Therapy; Kratz, F.; Senter, P., Eds.; Wiley-VCH: Germany, 2012; pp. 121-168.
[77]
Matsumura, Y.; Gotoh, M.; Muro, K.; Yamada, Y.; Shirao, K.; Shimada, Y.; Okuwa, M.; Matsumoto, S.; Miyata, Y.; Ohkura, H.; Chin, K.; Baba, S.; Yamao, T.; Kannami, A.; Takamatsu, Y.; Ito, K.; Takahashi, K. Phase I and pharmacokinetic study of MCC-465, a doxorubicin (DXR) encapsulated in PEG immunoliposome, in patients with metastatic stomach cancer. Ann. Oncol., 2004, 15(3), 517-525.
[78]
Broderick, J.M. MM-302 falls short in phase II HER2+ breast cancer trial. OncLive [Online], December 21 2016.https://www.onclive.com/web-exclusives/mm302-falls-short-in-phase-ii-her2-breast-cancer-trial (Accessed August 30, 2018).
[79]
ClinicalTrials.gov registry. A phase I study of systemic gene therapy with SGT-94 in patients with solid tumors (SGT94-01). U.S. National Library of Medicine. 2017.https://clinicaltrials.gov/ct2/ show/NCT01517464 (Accessed August 30, 2018).
[80]
National Institutes of Health. Retargeting FDA approved anticancer liposomal drugs to cancer stem cells. Department of Health and Human Services 2015.https://www.sbir.gov/sbirsearch/detail/1043275 (Accessed August 30, 2018).
[81]
Shih, Y-H.; Luo, T-Y.; Chiang, P-F.; Yao, C-J.; Lin, W-J.; Peng, C-L.; Shieh, M-J. EGFR-targeted micelles containing near-infrared dye for enhanced photothermal therapy in colorectal cancer. J. Control. Release, 2017, 258, 196-207.
[82]
Ahn, J.; Miura, Y.; Yamada, N.; Chida, T.; Liu, X.; Kim, A.; Sato, R.; Tsumura, R.; Koga, Y.; Yasunaga, M.; Nishiyama, N.; Matsumura, Y.; Cabral, H.; Kataoka, K. Antibody fragment-conjugated polymeric micelles incorporating platinum drugs for targeted therapy of pancreatic cancer. Biomaterials, 2015, 39, 23-30.
[83]
Cui, M.Y.; Dong, Z.; Cai, H.; Huang, K.; Liu, Y.; Fang, Z.; Li, X.; Luo, Y. Folate-targeted polymeric micelles loaded with superparamagnetic iron oxide as a contrast agent for magnetic resonance imaging of a human tongue cancer cell line. Mol. Med. Rep., 2017, 16(5), 7597-7602.
[84]
Wu, G.; Barth, R.F.; Yang, W.; Chatterjee, M.; Tjarks, W.; Ciesielski, M.J.; Fenstermaker, R.A. Site-specific conjugation of boron-containing dendrimers to anti-EGF receptor monoclonal antibody cetuximab (IMC-C225) and its evaluation as a potential delivery agent for neutron capture therapy. Bioconjug. Chem., 2004, 15(1), 185-194.
[85]
Poh, S.; Putt, K.S.; Low, P.S. Folate-targeted dendrimers selectively accumulate at sites of inflammation in mouse models of ulcerative colitis and atherosclerosis. Biomacromolecules, 2017, 18(10), 3082-3088.
[86]
Skyba, D.M.; Price, R.J.; Linka, A.Z.; Skalak, T.C.; Kaul, S. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation, 1998, 98(4), 290-293.
[87]
Ta, T.; Porter, T.M. Thermosensitive liposomes for localized delivery and triggered release of chemotherapy. J. Control. Release, 2013, 169(1-2), 112-125.
[88]
Mura, S.; Nicolas, J.; Couvreur, P. Stimuli-responsive nanocarriers for drug delivery. Nat. Mater., 2013, 12(11), 991-1003.
[89]
Kneidl, B.; Peller, M.; Winter, G.; Lindner, L.H.; Hossann, M. Thermosensitive liposomal drug delivery systems: State of the art review. Int. J. Nanomedicine, 2014, 9, 4387-4398.
[90]
Forbes, N.A.; Zasadzinski, J.A. Localized photothermal heating of temperature sensitive liposomes. Biophys. J., 2010, 98(3), 274a.
[91]
de la Rica, R.; Aili, D.; Stevens, M.M. Enzyme-responsive nanoparticles for drug release and diagnostics. Adv. Drug Deliv. Rev., 2012, 64(11), 967-978.
[92]
He, X.; Li, J.; An, S.; Jiang, C. pH-sensitive drug-delivery systems for tumor targeting. Ther. Deliv., 2013, 4(12), 1499-1510.
[93]
Ellens, H. Bentz, J.; Szoka, F.C. H+- and Ca2+-induced fusion and destabilization of liposomes. Biochemistry, 1985, 24(13), 3099-3106.
[94]
Ferreira, D.S.; Lopes, S.C.; Franco, M.S.; Oliveira, M.C. pH-sensitive liposomes for drug delivery in cancer treatment. Ther. Deliv., 2013, 4(9), 1099-1123.
[95]
Yavlovich, A.; Singh, A.; Blumenthal, R.; Puri, A. A novel class of phototriggerable liposomes containing DPPC: DC (8,9) PC as vehicles for delivery of doxorubicin to cells. Biochim. Biophys. Acta, 2011, 1808(1), 117-126.
[96]
Pradhan, P.; Giri, J.; Rieken, F.; Koch, C.; Mykhaylyk, O.; Döblinger, M.; Banerjee, R.; Bahadur, D.; Plank, C. Targeted temperature sensitive magnetic liposomes for thermo-chemotherapy. J. Control. Release, 2010, 142(1), 108-121.
[97]
Jain, A.; Tiwari, A.; Verma, A.; Jain, S.K. Ultrasound-based triggered drug delivery to tumors. Drug Deliv. Transl. Res., 2018, 8(1), 150-164.
[98]
Dromi, S.; Frenkel, V.; Luk, A.; Traughber, B.; Angstadt, M.; Bur, M.; Poff, J.; Xie, J.; Libutti, S.K.; Li, K.C.; Wood, B.J. Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin. Cancer Res., 2007, 13(9), 2722-2727.
[99]
Ranjan, A.; Jacobs, G.C.; Woods, D.L.; Negussie, A.H.; Partanen, A.; Yarmolenko, P.S.; Gacchina, C.E.; Sharma, K.V.; Frenkel, V.; Wood, B.J.; Dreher, M.R. 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(3), 487-494.
[100]
Lyon, P.C.; Griffiths, L.F.; Lee, J.; Chung, D.; Carlisle, R.; Wu, F.; Middleton, M.R.; Gleeson, F.V.; Coussios, C.C. Clinical trial protocol for TARDOX: A phase I study to investigate the feasibility of targeted release of lyso-thermosensitive liposomal doxorubicin (ThermoDox®) using focused ultrasound in patients with liver tumours. J. Ther. Ultrasound, 2017, 5, 28.
[101]
Lyon, P.C.; Gray, M.D.; Mannaris, C.; Folkes, L.K.; Stratford, M.; Campo, L.; Chung, D.Y.F.; Scott, S.; Anderson, M.; Goldin, R.; Carlisle, R.; Wu, F.; Middleton, M.R.; Gleeson, F.V.; Coussios, C.C. Safety and feasibility of ultrasound-triggered targeted drug delivery of doxorubicin from thermosensitive liposomes in liver tumors (TARDOX): A single-centre, open-label, phase 1 trial. Lancet Oncol., 2018, 19(8), 1027-1039.
[102]
Pitt, W.G.; Husseini, G.A.; Staples, B.J. Ultrasonic drug delivery – a general review. Expert Opin. Drug Deliv., 2004, 1(1), 37-56.
[103]
Smith, N.B. Perspectives on transdermal ultrasound mediated drug delivery. Int. J. Nanomedicine, 2007, 2(4), 585-594.
[104]
Ahmed, S.E.; Martins, A.M.; Husseini, G.A. The use of ultrasound to release chemotherapeutic drugs from micelles and liposomes. J. Drug Target., 2015, 23(1), 16-42.
[105]
Staples, B.J.; Roeder, B.J.; Husseini, G.A.; Badamjav, O.; Schaalje, G.B.; Pitt, W.G. Role of frequency and mechanical index in ultrasonic-enhanced chemotherapy in rats. Cancer Chemother. Pharmacol., 2009, 64(3), 593-600.
[106]
Ueda, H.; Mutoh, M.; Seki, T.; Kobayashi, D.; Morimoto, Y. Acoustic cavitation as an enhancing mechanism of low-frequency sonophoresis for transdermal drug delivery. Biol. Pharm. Bull., 2009, 32(5), 916-920.
[107]
Stringham, S.B.; Viskovska, M.A.; Richardson, E.S.; Ohmine, S.; Husseini, G.A.; Murray, B.K.; Pitt, W.G. Over-pressure suppresses ultrasonic-induced drug uptake. Ultrasound Med. Biol., 2009, 35(3), 409-415.
[108]
Yang, F.; Gu, N.; Chen, D.; Xi, X.; Zhang, D.; Li, Y.; Wu, J. Experimental study on cell self-sealing during sonoporation. J. Control. Release, 2008, 131(3), 205-210.
[109]
Karshafian, R.; Bevan, P.D.; Williams, R.; Samac, S.; Burns, P.N. Sonoporation by ultrasound-activated microbubble contrast agents: Effect of acoustic exposure parameters on cell membrane permeability and cell viability. Ultrasound Med. Biol., 2009, 35(5), 847-860.
[110]
Rapoport, N. Drug-loaded perfluorocarbon nanodroplets for ultrasound-mediated drug delivery. Adv. Exp. Med. Biol., 2016, 880, 221-241.
[111]
Nomikou, N.; McHale, A.P. Exploiting ultrasound-mediated effects in delivering targeted, site-specific cancer therapy. Cancer Lett., 2010, 296(2), 133-143.
[112]
Park, D.; Park, H.; Seo, J.; Lee, S. Sonophoresis in transdermal drug delivery. Ultrasonics, 2014, 54(1), 56-65.
[113]
Apfel, R.E.; Holland, C.K. Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound Med. Biol., 1991, 17(2), 179-185.
[114]
Williams, J.B.; Buchanan, C.M.; Husseini, G.A.; Pitt, W.G. Cytosolic delivery of doxorubicin from liposomes to multidrug resistant cells via the vaporization of perfluoropentane droplets. J. Nanomed. Res., 2017, 5(4), 00122.
[115]
Pitt, W.G.; Singh, R.N.; Perez, K.X.; Husseini, G.A.; Jack, D.R. Phase transitions of perfluorocarbon nanoemulsion induced with ultrasound: a mathematical model. Ultrason. Sonochem., 2014, 21(2), 879-891.
[116]
Singh, R.; Husseini, G.A.; Pitt, W.G. Phase Transitions of Nanoemulsions using ultrasound: Experimental observations. Ultrason. Sonochem., 2012, 19(5), 1120-1125.
[117]
Husseini, G.A.; Pitt, W.G.; Javadi, M. Investigating the stability of eLiposomes at elevated temperatures. Technol. Cancer Res. Treat., 2015, 14(4), 379-382.
[118]
Husseini, G.A.; Pitt, W.G.; Williams, J.B.; Javadi, M. Investigating the release mechanism of calcein from eLiposomes at higher temperatures. J. Coll. Sci. Biotechnol., 2014, 3(3), 239-244.
[119]
Salkho, N.M.; Paul, V.; Kawak, P.; Vitor, R.F.; Martins, A.M.; Al Sayah, M.; Husseini, G.A. Ultrasonically controlled estrone-modified liposomes for estrogen-positive breast cancer therapy. Artif. Cells Nanomed. Biotechnol., 2018, 46(Suppl. 2), 462-472.
[120]
Salkho, N.M.; Turki, R.Z.; Guessoum, O.; Martins, A.M.; Vitor, R.F.; Husseini, G.A. Liposomes and ultrasound as a promising drug delivery system in cancer treatment. Curr. Mol. Med., 2017, 17(10), 668-688.
[121]
Ahmed, S.E.; Moussa, H.G.; Martins, A.M.; Al-Sayah, M.; Husseini, G.A. Effect of pH, ultrasound frequency and power density on the release of calcein from stealth liposome. Eur. J. Nanomed., 2016, 8(1), 31-43.
[122]
Moussa, H.G.; Husseini, G.A.; Abdel-Jabbar, N.M.; Ahmad, S.E. The use of model predictive control and artificial neural networks to optimize the ultrasonic release of a model drug from liposomes. IEEE Trans. Nanobioscience, 2017, 16(3), 149-156.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 12
Year: 2019
Page: [961 - 969]
Pages: 9
DOI: 10.2174/1389557519666190408155251
Price: $58

Article Metrics

PDF: 22
HTML: 4