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A review of ultrasound-mediated microbubbles technology for cancer therapy: a vehicle for chemotherapeutic drug delivery

Published online by Cambridge University Press:  22 August 2019

Ernest Osei*
Affiliation:
Department of Medical Physics, Grand River Regional Cancer Centre, Kitchener, ON, Canada Department of Physics and Astronomy, University of Waterloo, Waterloo, ON, Canada Department of Systems Design Engineering, University of Waterloo, Waterloo, ON, Canada Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ONCanada
Aladdin Al-Asady
Affiliation:
Department of Medical Physics, Grand River Regional Cancer Centre, Kitchener, ON, Canada
*
Author for Correspondence: Ernest Osei, Department of Medical Physics, Grand River Regional Cancer Centre, 835 King Street West, Kitchener, N2G 1G3 Ontario, Canada. E-mail: [email protected]

Abstract

Background:

The unique behaviour of microbubbles under ultrasound acoustic pressure makes them useful agents for drug and gene delivery. Several studies have demonstrated the potential application of microbubbles as a non-invasive, safe and effective technique for targeted delivery of drugs and genes. The drugs can be incorporated into the microbubbles in several different approaches and then carried to the site of interest where it can be released by destruction of the microbubbles using ultrasound to achieve the required therapeutic effect.

Methods:

The objective of this article is to report on a review of the recent advances of ultrasound-mediated microbubbles as a vehicle for delivering drugs and genes and its potential application for the treatment of cancer.

Conclusion:

Ultrasound-mediated microbubble technology has the potential to significantly improve chemotherapy drug delivery to treatment sites with minimal side effects. Moreover, the technology can induce temporary and reversible changes in the permeability of cells and vessels, thereby allowing for drug delivery in a spatially localised region which can improve the efficiency of drugs with poor bioavailability due to their poor absorption, rapid metabolism and rapid systemic elimination.

Type
Literature Review
Copyright
© Cambridge University Press 2019

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References

Canadian Cancer Society’s Advisory Committee on Cancer Statistics. Canadian Cancer Statistics 2017. Toronto, ON: Canadian Cancer Society; 2017. http://www.cancer.ca/~/media/cancer.ca/CW/cancer%20information/cancer%20101/Canadian%20cancer%20statistics/Canadian-Cancer-Statistics-2017-EN.pdf. Accessed on June 2019.Google Scholar
Kaliberov, S A, Buchsbaum, D J.Cancer treatment with gene therapy and radiation therapy. Adv Cancer Res 2012; 115: 221263. doi: 10.1016/B978-0-12-398342-8.00007-0.CrossRefGoogle ScholarPubMed
Raghunandan, R, Voll, M, Osei, Eet al. A review of applications of principles of quantum physics in oncology: do quantum physics principles have any role in oncology research and applications? J Radiother Pract 2019; 112. doi: 10.1017/S1460396919000153.CrossRefGoogle Scholar
Nambiar, S, Osei, E, Fleck, Aet al. Synthesis of curcumin-functionalized gold nanoparticles and cytotoxicity studies in human prostate cancer cell line, Applied Nanoscience 2018; 8 (3): 347357. doi: 10.1007/s13204-018-0728-6.CrossRefGoogle Scholar
Tu, J, Zhang, H, Yu, Jet al. Ultrasound-mediated microbubble destruction: a new method in cancer immunotherapy. OncoTargets Ther 2018; 11: 57635775.CrossRefGoogle Scholar
Unger, E C, McCreery, T P, Sweitzer, R Het al. Acoustically active lipospheres containing paclitaxel: a new therapeutic ultrasound contrast agent. Invest Radiol 1998; 33: 886892.CrossRefGoogle Scholar
Fritz, T A, Unger, E C, Sutherland, Get al. Phase I clinical trials of MRX-115. A new ultrasound contrast agent. Invest Radiol 1997; 32: 735740.CrossRefGoogle ScholarPubMed
Shohet, R V, Chen, S, Zhou, Y Tet al. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 2000; 101 (22): 25542556.CrossRefGoogle ScholarPubMed
Teupe, C, Richter, S, Fisslthaler, Bet al. Vascular gene transfer of phosphomimetic endothelial nitric oxide synthase (S1177D) using ultrasound-enhanced destruction of plasmid-loaded microbubbles improves vasoreactivity. Circulation 2002; 105: 11041109.CrossRefGoogle ScholarPubMed
Ng, K Y, Liu, Y.Therapeutic ultrasound: its application in drug delivery. Med Res Rev 2002; 22 (2): 204223.CrossRefGoogle ScholarPubMed
Kennedy, J E.High-intensity focused ultrasound in the treatment of solid tumours. Nat Rev Cancer 2005; 5 (4): 321327.CrossRefGoogle ScholarPubMed
Rassweiler, J J, Knoll, T, Kohrmann, K Uet al. Shock wave technology and application: an update. Eur Urol 2011; 59 (5): 784796.CrossRefGoogle ScholarPubMed
Borden, M A, Caskey, C F, Little, Eet al. DNA and polylysine adsorption and multilayer construction onto cationic lipid-coated microbubbles Langmuir 2007; 23 (18):94019408.CrossRefGoogle ScholarPubMed
Hoff, L, Acoustic Characterization of Contrast Agents for Medical Ultrasound Imaging. Springer, 2001 (eBook).CrossRefGoogle Scholar
Correas, J M, Bridal, L, Lesavre, Aet al. Ultrasound contrast agents: properties, principles of action, tolerance, and artifacts. Eur Radiol 2001; 11 (8): 13161328.CrossRefGoogle ScholarPubMed
Wei, K, Mulvagh, S L, Carson, Let al.The safety of Definity and Optison for ultrasound image enhancement: a retrospective analysis of 78,383 administered contrast doses. J Am Soc Echocardiogr 2008; 21 (11): 12021206.CrossRefGoogle ScholarPubMed
Sirsi, S, Borden, M.Microbubble compositions, properties and biomedical applications. Bubble Sci Eng Technol 2009; 1 (1–2): 317. doi: 10.1179/175889709X446507.CrossRefGoogle ScholarPubMed
Christiansen, J P, French, B A, Klibanov, A Let al. Targeted tissue transfection with ultrasound destruction of plasmid-bearing cationic microbubbles. Ultrasound Med Biol 2003; 29 (12): 17591767.CrossRefGoogle ScholarPubMed
Bekeredjian, R, Chen, S, Grayburn, P Aet al. Augmentation of cardiac protein delivery using ultrasound targeted microbubble destruction. Ultrasound Med Biol 2005; 31: 687691.CrossRefGoogle ScholarPubMed
Kheirolomoom, A, Dayton, P A, Lum, A Fet al.Acoustically-active microbubbles conjugated to liposomes: characterization of a proposed drug delivery vehicle. J Control Release 2007; 118: 275284.CrossRefGoogle ScholarPubMed
Seemann, S, Hauff, P, Schultze-Mosgau, Met al. Pharmaceutical evaluation of gas-filled microparticles as gene delivery system. Pharm Res 2002; 19: 250257.CrossRefGoogle ScholarPubMed
Marmottant, P, van der Meer, S, Emmer, Met al. A model for large amplitude oscillations of coated bubbles accounting for buckling and rupture. J Acoust Soc Am 2005; 118: 34993505.CrossRefGoogle Scholar
Stride, E, Saffari, N.Microbubble ultrasound contrast agents: a review. J Eng Med 2003; 217: 429. doi: 10.1243/09544110360729072.CrossRefGoogle ScholarPubMed
Tachibana, K, Tachibana, S.The use of ultrasound for drug delivery. Echocardiography 2001; 18 (4): 323e8.CrossRefGoogle ScholarPubMed
Dijkmans, P A, Juffermans, L J M, Musters, R J Pet al. Microbubbles and ultrasound: from diagnosis to therapy. Eur J Echocardiograph 2004; 5: 245e256.CrossRefGoogle Scholar
Skyba, D M, Price, R J, Linka, A Zet al. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation 1998; 98: 290293.CrossRefGoogle ScholarPubMed
Price, R J, Skyba, D M, Kaul, Set al. Delivery of colloidal particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound. Circulation 1998; 98: 12641267.CrossRefGoogle ScholarPubMed
Taniyama, Y, Tachibana, K, Hiraoka, Ket al. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002; 105: 12331239.CrossRefGoogle Scholar
Mukherjee, D, Wong, J, Griffin, Bet al.Tenfold augmentation of endothelial uptake of vascular endothelial growth factor with ultrasound after systemic administration. J Am Coll Cardiol 2000; 35 (6): 16781686.CrossRefGoogle Scholar
Unger, E C, Hersh, E, Vannan, Met al. Local drug and gene delivery through microbubbles. Prog Cardiovasc Dis 2001; 44 (1): 4554.CrossRefGoogle ScholarPubMed
Villanueva, F S, Jankowski, R J, Manaugh, Cet al. Albumin microbubble adherence to human coronary endothelium: implications for assessment of endothelial function using myocardial contrast echocardiography. J Am Coll Cardiol 1997; 30: 689693.CrossRefGoogle ScholarPubMed
Porter, T R, Hiser, W L, Kricsfeld, Det al.Inhibition of carotid artery neointimal formation with intravenous microbubbles. Ultrasound Med Biol 2001; 27: 259265.CrossRefGoogle ScholarPubMed
Porter, T R, Knnap, D, Venneri, Let al.Increased suppression of intracoronary c-myc protein synthesis within the stent or balloon injury site using an intravenous microbubble delivery system containing antisense to C-myc: comparison with direct intracoronary injection. J Am Coll Cardiol 2003; 41 (6): 431A. doi: 10.1016/S0735-1097(03)81290-1.Google Scholar
Basta, G, Venneri, L, Lazzerini, Get al. In vitro modulation of intracellular oxidative stress of endothelial cells by diagnostic cardiac ultrasound. Cardiovasc Res 2003; 58 (1): 156161.CrossRefGoogle ScholarPubMed
Grüll, H, Langereis, S.Hyperthermia-triggered drug delivery from temperature-sensitive liposomes using MRI-guided high intensity focused ultrasound. J Control Release Off J Control Release Soc 2012; 161 (2): 317327.CrossRefGoogle ScholarPubMed
Oerlemans, C, Deckers, R, Storm, Get al. Evidence for a new mechanism behind HIFU-triggered release from liposomes. J Control Release Off J Control Release Soc 2013; 168 (3): 327333.CrossRefGoogle ScholarPubMed
Liang, H-D, Tang, J, Halliwell, M.Sonoporation, drug delivery, and gene therapy. Proc Inst Mech Eng [H] 2010; 224: 343361.CrossRefGoogle ScholarPubMed
Uchida, T, Nakano, M, Hongo, Set al. High-intensity focused ultrasound therapy for prostate cancer. Int J Urol Off J Jpn Urol Assoc 2012; 19: 187201.Google ScholarPubMed
Focused Ultrasound Foundation’s website (www.fusfoundation.org): An Overview of the Biological Effects of Focused Ultrasound. https://d3nqfeqdtaoni.cloudfront.net/images/pdf/Bioeffects_Paper_July_2015.pdf. Accessed on June 2019.CrossRefGoogle Scholar
Couture, O, Foley, J, Kassell, N Fet al. Review of ultrasound mediated drug delivery for cancer treatment: updates from preclinical studies. Transl Cancer Res 2014; 3: 494511.Google Scholar
Tan, S, Wu, T, Zhang, Det al. Cell or cell membrane-based drug delivery systems. Theranostics 2015; 5 (8): 863881.CrossRefGoogle ScholarPubMed
Suzuki, M, Koshiyama, K, Shinohara, Fet al. Nanobubbles enhanced drug susceptibility of cancer cells using ultrasound. International Congress Series 2005; 1284: 338339.CrossRefGoogle Scholar
Suzuki, R, Namai, E, Oda, Yet al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release 2010; 142: 245250.CrossRefGoogle ScholarPubMed
Suzuki, R, Oda, Y, Utoguchi, Net al. Progress in the development of ultrasound-mediated gene delivery systems utilizing nano- and microbubbles. J Control Release 2011; 149: 3641.CrossRefGoogle ScholarPubMed
Foley, J L, Eames, M, Snell, Jet al. Image-guided focused ultrasound: State of the technology and the challenges that lie ahead. Imaging Med 2013; 5: 357370.CrossRefGoogle Scholar
Al-Bataineh, O, Jenne, J, Huber, P.Clinical and future applications of high intensity focused ultrasound in cancer. Cancer Treat Rev 2012; 38: 346353.CrossRefGoogle ScholarPubMed
Jang, H J, Lee, J-Y, Lee, D-Het al. Current and future clinical applications of High-Intensity Focused Ultrasound (HIFU) for pancreatic cancer. Gut Liver 2010; 4: S57–S61.CrossRefGoogle ScholarPubMed
Wang, T-Y, Wilson, K E, Machtaler, Set al. Ultrasound and microbubble guided drug delivery: mechanistic understanding and clinical implications. Curr Pharm Biotechnol. 2014; 14 (8): 743752.CrossRefGoogle Scholar
Webb, H, Lubner, M G, Hinshaw, J L.Thermal ablation. Semin Roentgenol 2011; 46: 133141.CrossRefGoogle ScholarPubMed
Chen, C-J, Hsu, H-C, Chung, W-Set al. Clinical experience with ultrasound-based real-time tracking lithotripsy in the single renal stone treatment. J Endourol 2009; 23: 18111815.CrossRefGoogle ScholarPubMed
Deng, C X.Targeted drug delivery across the blood-brain barrier using ultrasound technique. Ther Deliv 2010; 1: 819848.CrossRefGoogle ScholarPubMed
Uchida, T, Nakano, M, Hongo, Set al. High-intensity focused ultrasound therapy for prostate cancer. Int J Urol Off J Jpn Urol Assoc 2012; 19: 187201.Google ScholarPubMed
Dewitte, H, Van Lint, S, Heirman, Cet al. The potential of antigen and TriMix sonoporation using mRNA-loaded microbubbles for ultrasound triggered cancer immunotherapy. J Control Release 2014; 194 (12): 2836.CrossRefGoogle ScholarPubMed
Un, K, Kawakami, S, Suzuki, Ret al. Suppression of melanoma growth and metastasis by DNA vaccination using an ultrasound-responsive and mannose-modified gene carrier. Mol Pharm 2011; 8 (2): 543554.CrossRefGoogle ScholarPubMed
Ishijima, A, Minamihata, K, Yamaguchi, Set al. Selective intracellular vaporisation of antibody conjugated phase-change nano-droplets in vitro. Sci Rep 2017; 7: 44077.CrossRefGoogle ScholarPubMed
Kobus, T, Zervantonakis, I K, Zhang, Yet al. Growth inhibition in a brain metastasis model by antibody delivery using focused ultrasound-mediated blood-brain barrier disruption. J Control Release 2016; 238: 281288.CrossRefGoogle Scholar
Miller, M W.Gene transfection and drug delivery. Ultrasound Med Biol 2000, 26 (suppl 1): S59S62.CrossRefGoogle ScholarPubMed
Lindner, J R, Song, J, Christiansen, Jet al. Ultrasound assessment of inflammation and renal tissue injury with microbubbles targeted to P-selectin. Circulation 2001, 104: 21072112.CrossRefGoogle ScholarPubMed
Weller, G E, Lu, E, Csikari, M Met al.Ultrasound imaging of acute cardiac transplant rejection with microbubbles targeted to intercellular adhesion molecule-1. Circulation 2003; 108: 218224.CrossRefGoogle ScholarPubMed
Oda, Y, Suzuki, R, Otake, Set al. Prophylactic immunization with Bubble liposomes and ultrasound-treated dendritic cells provided a four-fold decrease in the frequency of melanoma lung metastasis. J Control Release 2012; 160 (2): 362366.CrossRefGoogle ScholarPubMed
Ji, Y, Han, Z, Shao, Let al. Evaluation of in vivo antitumor effects of low-frequency ultrasound-mediated miRNA-133a microbubble delivery in breast cancer. Cancer Med 2016; 5: 25342543. 10.1002/cam4.840.CrossRefGoogle ScholarPubMed
Lentacker, I, Geers, B, Demeester, Jet al. Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved. Mol Ther 2010; 18: 101108. 10.1038/mt.2009.160.CrossRefGoogle ScholarPubMed
Kotopoulis, S, Dimcevski, G, Gilja, O Het al.Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med Phys 2013; 40: 072902. Accessed on 10th August 2018.CrossRefGoogle ScholarPubMed
Liu, H, Chang, S, Sun, Jet al.Ultrasound-mediated destruction of LHRHa targeted and paclitaxel loaded lipid microbubbles induces proliferation inhibition and apoptosis in ovarian cancer cells. Mol Pharm 2014; 11: 4048. doi: 10.1021/mp4005244.CrossRefGoogle ScholarPubMed
Florinas, S, Kim, J, Nam, Ket al. Ultrasound-assisted zsiRNA delivery via arginine-grafted bioreducible polymer and microbubbles targeting VEGF for ovarian cancer treatment. J Control Release 2014; 183: 18. doi: 10.1016/j.jconrel.2014.03.025.CrossRefGoogle ScholarPubMed
Blum, N T, Yildirim, A, Chattaraj, Ret al. Nanoparticles formed by acoustic destruction of microbubbles and their utilization for imaging and effects on therapy by high intensity focused ultrasound. Theranostics 2017; 7 (3): 694702.CrossRefGoogle ScholarPubMed
Hou, R, Xu, Y, Lu, Qet al. Effect of low-frequency low-intensity ultrasound with microbubbles on prostate cancer hypoxia. Tumour Biol 2017; 39 (10): 1010428317719275.CrossRefGoogle ScholarPubMed
Xu, L, Osei, B, Osei, E.A review of radiation genomics: integrating patient radiation response with genomics for personalised and targeted radiation therapy. J Radiother Prac 2019; 18: 198209. doi: 10.1017/S1460396918000547.CrossRefGoogle Scholar
Fellinger, K, Schmid, J. Klinik und Therapie des chronischen Gelenkreumatismus. Vienna, Austria, Wien, 1954: 549552.Google Scholar
Al-Asady, A. Assembling Ultrasound Contrast Agent from Commonly Available Resources in Iraqi Hospitals (simulated and in vitro study). PhD. Thesis, University of Mustansiriyah, Iraq, 2017.Google Scholar
Gramiak, R, Shah, P. Echocardiography of the aortic root. Invest Radiol 1968; 3 (5): 356366. ISSN:0020-9996.CrossRefGoogle ScholarPubMed
Sijl, J, Vos, H J, de Jong, Net al. Combined optical and acoustical characterization of individual US contrast microbubbles. 19th International Congress on Acoustics, ICA2007 MADRID, Symposium Proceedings, 2007.Google Scholar
Dolan, MS, Gala, SS, Dodla, Set al.Safety and efficacy of commercially available ultrasound contrast agents for rest and stress echocardiography. A multicenter experience. J Am Coll Cardiol 2009; 53 (1): 3238.CrossRefGoogle ScholarPubMed
Main, M L, Ryan, A C, Davis, T Eet al. Acute mortality in hospitalized patients undergoing echocardiography with and without an ultrasound contrast agent (multicenter registry results in 4,300,966 consecutive patients). Am J Cardiol 2008; 102 (12): 17421746.CrossRefGoogle Scholar
Weiss, R J, Ahmad, M, Villanueva, Fet al. CaRES (Contrast Echocardiography Registry for Safety Surveillance): a prospective multicenter study to evaluate the safety of the ultrasound contrast agent density in clinical practice. J Am Soc Echocardiogr 2012; 25 (7): 790795CrossRefGoogle Scholar
Shchukin, D G, Kohler, K, Mohwald, Het al. Gas-filled polyelectrolyte capsules. Angew Chem Int Ed 2005; 44 (21): 33103314.CrossRefGoogle ScholarPubMed