Review Article

Microbubbles Contrast Agents: General Overview as Diagnostics and Therapeutic Agent

Author(s): Shivani K. Gharat*, Shilpa C. Godiyal, Pranali P. Malusare, Kisan R. Jadhav and Vilasrao J. Kadam

Volume 23, Issue 10, 2022

Published on: 14 June, 2022

Page: [960 - 977] Pages: 18

DOI: 10.2174/1573399818666220421123142

Price: $65

Abstract

Recent discoveries have unfolded many powerful emerging applications in the field of drug delivery science. For the past few years, ultrasound mediated microbubble contrast agents have been an emerging modality for diagnostic and drug delivery applications. Microbubbles are small spherical bubbles composed of a gas core encapsulated by a shell with different materials. The composition of the microbubble determines its stiffness, encapsulation efficiency, stability, and clearance from the system. A gas-filled microbubble, when activated by an acoustic pulse, can produce large volumetric oscillations and, once administered intravenously, can act as a cavitating nuclei, allowing for a wide range of ultrasound-assisted drug delivery applications. Microbubbles offer a fantastic approach to ultrasound triggered drug delivery with various drug loading techniques and targeting strategies for the uptake of bioactive substances such as polynucleotides, proteins, genes, and small-molecule drugs. Microbubbles can be used for several diagnostic and therapeutic purposes for accurate detection and treatment of various life-threatening diseases.

Keywords: Ultrasound contrast agents, microbubbles, cavitation nuclei, theranostic agents, volumetric Oscillations, diagnostics, targeted delivery.

« Previous
Graphical Abstract
[1]
Nanda NC, Carstensen C. Echo-enhancing agents: Safety. In: Nanda NC, Schlief R, Goldberg BB, Eds. Advances in echo imaging using contrast enhancers. Dordrecht: Kluwer 1997; pp. 115-31.
[http://dx.doi.org/10.1007/978-94-011-5704-9_6]
[2]
Jangjou A, Meisami AH, Jamali K, et al. The promising shadow of microbubble over medical sciences: from fighting wide scope of prevalence disease to cancer eradication. J Biomed Sci 2021; 28(1): 49.
[http://dx.doi.org/10.1186/s12929-021-00744-4] [PMID: 34154581]
[3]
Martin JK. Blomley, Jennifer C Cooke, Evan C Unger, Mark J Monaghan, David O Cosgrove. Microbubble contrast agents: A new era in ultrasound. BMJ 2001; 322: 1222-5.
[4]
Gramiak R, Shah PM. Echocardiography of the aortic root. Invest Radiol 1968; 3(5): 356-66.
[http://dx.doi.org/10.1097/00004424-196809000-00011] [PMID: 5688346]
[5]
Kassan DG, Lynch AM, Stiller MJ. Physical enhancement of dermatologic drug delivery: iontophoresis and phonophoresis. J Am Acad Dermatol 1996; 34(4): 657-66.
[http://dx.doi.org/10.1016/S0190-9622(96)80069-7] [PMID: 8601657]
[6]
Russell SJ. Science, medicine, and the future. Gene therapy. BMJ 1997; 315(7118): 1289-92.
[http://dx.doi.org/10.1136/bmj.315.7118.1289] [PMID: 9390059]
[7]
Hernot S, Klibanov AL. Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev 2008; 60(10): 1153-66.
[http://dx.doi.org/10.1016/j.addr.2008.03.005] [PMID: 18486268]
[8]
William G. Pitt, Ghaleb A Husseini, Bryant J Staples. Ultrasonic drug delivery-a general review. Expert Opin Drug Deliv 2004; 1(1): 37-56.
[http://dx.doi.org/10.1517/17425247.1.1.37] [PMID: 16296719]
[9]
Kabalnov A, Klein D, Pelura T, Schutt E, Weers J. Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory. Ultrasound Med Biol 1998; 24(5): 739-49.
[http://dx.doi.org/10.1016/S0301-5629(98)00034-9] [PMID: 9695277]
[10]
Lee S, Kim DH, Needham D. Equilibrium and dynamic interfacial tension measurements at microscopic interfaces using a micropipet technique. 2. Dynamics of phospholipid monolayer formation and equilibrium tensions at the water-air interface. Langmuir 2001; 17(18): 5544-50.
[http://dx.doi.org/10.1021/la0103261]
[11]
Frinking P, Segers T, Luan Y, Tranquart F. Three decades of ultrasound contrast agents: a review of the past, Present and future improvements. Ultrasound Med Biol 2020; 46(4): 892-908.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2019.12.008] [PMID: 31941587]
[12]
Chow AM, Wu EX. Microbubbles: Contrast agents for ultrasound and MRI. In: Long N, Wong W-T, Eds. The chemistry of molecular imaging. John Wiley & Sons, Inc. 2015; pp. 321-34.
[13]
Kirsten Christensen-Jeffries, Robert J Eckersley. Physics of Microbubble Contrast Agents. In: Sidhu PS, Sellars ME, Deganello A, Eds. Contrast-Enhanced Ultrasound in Pediatric Imaging. Springer Nature Switzerland AG 2021; pp. 1-1.
[http://dx.doi.org/10.1007/978-3-030-49691-3_1]
[14]
Prajapati J, Agrawal Y. Synthesis, characterization and application of microbubbles: A review. IJPSR 2012; 3(6): 1532-43.
[15]
Quaia E. Classification and safety of microbubble-based contrast agents. In: Contrast media in ultrasonography. Berlin: Springer-Verlag 2005; pp. 3-14.
[http://dx.doi.org/10.1007/3-540-27214-3_1]
[16]
Faez T, Emmer M, Kooiman K, Versluis M, van der Steen A, de Jong N. 20 years of ultrasound contrast agent modeling. IEEE Trans Ultrason Ferroelectr Freq Control 2013; 60(1): 7-20.
[http://dx.doi.org/10.1109/TUFFC.2013.2533] [PMID: 23287909]
[17]
Christiansen C, Kryvi H, Sontum PC, Skotland T. Physical and biochemical characterization of Albunex, a new ultrasound contrast agent consisting of air-filled albumin microspheres suspended in a solution of human albumin. Biotechnol Appl Biochem 1994; 19(3): 307-20.
[PMID: 8031506]
[18]
Myrset AH, Nicolaysen H, Toft K, Christiansen C, Skotland T. Structure and organization of albumin molecules forming the shell of air-filled microspheres: evidence for a monolayer of albumin molecules of multiple orientations stabilizing the enclosed air. Biotechnol Appl Biochem 1996; 24(2): 145-53.
[PMID: 8865606]
[19]
Grinstaff MW, Suslick KS. Air-filled proteinaceous microbubbles: synthesis of an echo-contrast agent. Proc Natl Acad Sci USA 1991; 88(17): 7708-10.
[http://dx.doi.org/10.1073/pnas.88.17.7708] [PMID: 1652761]
[20]
D’Arrigo JS. Stable gas-in-liquid emulsions: production in natural waters and artificial media. New York, NY: Elsevier Science Pub. Co 1986.
[21]
Epstein PS, Plesset MS. On the stability of gas bubbles in liquid gas solutions. J Chem Phys 1950; 18(11): 1505-9.
[http://dx.doi.org/10.1063/1.1747520]
[22]
Duncan PB, Needham D. Test of the Epstein-Plesset model for gas microparticle dissolution in aqueous media: effect of surface tension and gas undersaturation in solution. Langmuir 2004; 20(7): 2567-78.
[http://dx.doi.org/10.1021/la034930i] [PMID: 15835125]
[23]
Kim DH, Costello MJ, Duncan PB, Needham D. Mechanical properties and microstructure of polycrystalline phospholipid monolayer shells: Novel solid microparticles. Langmuir 2003; 19(20): 8455-66.
[http://dx.doi.org/10.1021/la034779c]
[24]
Stride E, Edirisinghe M. Novel microbubble preparation technologies. Soft Matter 2008; 4(12): 2350-9.
[http://dx.doi.org/10.1039/b809517p]
[25]
Singhal S, Moser CC, Wheatley MA. Surfactant-stabilized microbubbles as ultrasound contrast agents: stability study of Span 60 and Tween 80 mixtures using a Langmuir trough. Langmuir ACS pub 1993; 9: 2426-9.
[http://dx.doi.org/10.1021/la00033a027]
[26]
Wang WH, Moser CC, Wheatley MA. Langmuir trough study of surfactant mixtures used in the production of a new ultrasound contrast agent consisting of stabilized microbubbles. J Phys Chem 1996; 100(32): 13815-21.
[http://dx.doi.org/10.1021/jp9613549]
[27]
Dressaire E, Bee R, Bell DC, Lips A, Stone HA. Interfacial polygonal nanopatterning of stable microbubbles. Science 2008; 320(5880): 1198-201.
[http://dx.doi.org/10.1126/science.1154601] [PMID: 18511685]
[28]
Bloch SH, Wan M, Dayton PA, Ferrara KW. Optical observation of lipid- and polymer shelled ultrasound microbubble contrast agents. Appl Phys Lett 2004; 84(4): 631-3.
[http://dx.doi.org/10.1063/1.1643544]
[29]
Wheatley MA, Schrope B, Shen P. Contrast agents for diagnostic ultrasound: development and evaluation of polymer-coated microbubbles. Biomaterials 1990; 11(9): 713-7.
[http://dx.doi.org/10.1016/0142-9612(90)90033-M] [PMID: 2090309]
[30]
Bohmer MR, Schroeders R, Steenbakkers JAM, et al. Preparation of monodisperse polymer particles and capsules by ink-jet printing. Colloids Surf A Physicochem Eng Asp 2006; 289(1-3): 96-104.
[http://dx.doi.org/10.1016/j.colsurfa.2006.04.011]
[31]
Shchukin DG, Köhler K, Möhwald H, Sukhorukov GB. Gas-filled polyelectrolyte capsules. Angew Chem Int Ed 2005; 44(21): 3310-4.
[http://dx.doi.org/10.1002/anie.200462889] [PMID: 15844113]
[32]
Borden MA, Caskey CF, Little E, Gillies RJ, Ferrara KW. DNA and polylysine adsorption and multilayer construction onto cationic lipid-coated microbubbles. Langmuir 2007; 23(18): 9401-8.
[http://dx.doi.org/10.1021/la7009034] [PMID: 17665937]
[33]
Eniola AO, Willcox PJ, Hammer DA. Interplay between rolling and firm adhesion elucidated with a cell-free system engineered with two distinct receptor-ligand pairs. Biophys J 2003; 85(4): 2720-31.
[http://dx.doi.org/10.1016/S0006-3495(03)74695-5] [PMID: 14507735]
[34]
Postema M, Schmitz G. Bubble dynamics involved in ultrasonic imaging. Expert Rev Mol Diagn 2006; 6(3): 493-502.
[http://dx.doi.org/10.1586/14737159.6.3.493] [PMID: 16706749]
[35]
Becher H, Burns PN. Contrast agents for echocardiography: Principles and instrumentation. In: Becher H, Burns PN, Eds. Handbook of contrast echocardiography LV function and myocardial perfusion. Berlin: Springer-Verlag 2000; pp. 2-44.
[36]
Cosgrove D, Lassau N. Imaging of perfusion using ultrasound. Eur J Nucl Med Mol Imaging 2010; 37(S1)(Suppl. 1): S65-85.
[http://dx.doi.org/10.1007/s00259-010-1537-7] [PMID: 20640418]
[37]
Fan Z, Kumon RE, Deng CX. Mechanisms of microbubble-facilitated sonoporation for drug and gene delivery. Ther Deliv 2014; 5(4): 467-86.
[http://dx.doi.org/10.4155/tde.14.10] [PMID: 24856171]
[38]
Collis J, Manasseh R, Liovic P, et al. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics 2010; 50(2): 273-9.
[http://dx.doi.org/10.1016/j.ultras.2009.10.002] [PMID: 19896683]
[39]
de Jong N, Emmer M, Chin CT, et al. “Compression-only” behavior of phospholipid-coated contrast bubbles. Ultrasound Med Biol 2007; 33(4): 653-6.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2006.09.016] [PMID: 17320268]
[40]
Cui W, Bei J, Wang S, et al. Preparation and evaluation of poly(L-lactide-co-glycolide) (PLGA) microbubbles as a contrast agent for myocardial contrast echocardiography. J Biomed Mater Res B Appl Biomater 2005; 73(1): 171-8.
[http://dx.doi.org/10.1002/jbm.b.30189] [PMID: 15678494]
[41]
Cavalieri F, El Hamassi A, Chiessi E, Paradossi G. Langmuir. Stable polymeric microballoons as multifunctional device for biomedical uses. Synthesis and Characterization 2005; 21: 8758-64.
[42]
Sirsi S, Borden M. Microbubble Compositions, Properties and Biomedical Applications. Bubble Sci Eng Technol 2009; 1(1-2): 3-17.
[http://dx.doi.org/10.1179/175889709X446507] [PMID: 20574549]
[43]
Zhao YZ, Liang HD, Mei XG, Halliwell M. Preparation, characterization and in vivo observation of phospholipid-based gas-filled microbubbles containing hirudin. Ultrasound Med Biol 2005; 31(9): 1237-43.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2005.05.007] [PMID: 16176790]
[44]
Suslick KS, Didenko Y, Fang MM, et al. Acoustic cavitation and its chemical consequences. Philos Trans- Royal Soc, Math Phys Eng Sci 1999; 357(1751): 335-53.
[http://dx.doi.org/10.1098/rsta.1999.0330]
[45]
Nyborg WL. Biological effects of ultrasound: development of safety guidelines. Part II: general review. Ultrasound Med Biol 2001; 27(3): 301-33.
[http://dx.doi.org/10.1016/S0301-5629(00)00333-1] [PMID: 11369117]
[46]
Bjerknes K, Dyrstad K, Smistad G, Agerkvist I. Preparation of polymeric microcapsules: formulation studies. Drug Dev Ind Pharm 2000; 26(8): 847-56.
[http://dx.doi.org/10.1081/DDC-100101308] [PMID: 10900541]
[47]
Jiang B, Gao C, Shen J. Polylactide hollow spheres fabricated by interfacial polymerization in an oil-in-water emulsion system. Colloid Polym Sci 2006; 284(5): 513-9.
[http://dx.doi.org/10.1007/s00396-005-1415-1]
[48]
Lee M, Lee EY, Lee D, Park BJ. Stabilization and fabrication of microbubbles: applications for medical purposes and functional materials. Soft Matter 2015; 11(11): 2067-79.
[http://dx.doi.org/10.1039/C5SM00113G] [PMID: 25698443]
[49]
Kukizaki M, Goto M. Size control of nanobubbles generated from Shirasu-porous-glass membranes. J Membr Sci 2006; 281(1-2): 386-96.
[http://dx.doi.org/10.1016/j.memsci.2006.04.007]
[50]
Kukizakia M, Goto M. Spontaneous formation behavior of uniform-sized microbubbles from Shirasu porous glass (SPG) membranes in the absence of water-phase flow. Colloids Surf A Physicochem Eng Asp 2007; 296(1-3): 174-81.
[http://dx.doi.org/10.1016/j.colsurfa.2006.09.042]
[51]
Farook U, Zhang HB, Edirisinghe MJ, Stride E, Saffari N. Preparation of microbubble suspensions by co-axial electrohydrodynamic atomization. Med Eng Phys 2007; 29(7): 749-54.
[http://dx.doi.org/10.1016/j.medengphy.2006.08.009] [PMID: 17035065]
[52]
Farook U, Stride E, Edirisinghe MJ, Moaleji R. Microbubbling by co-axial electrohydrodynamic atomization. Med Biol Eng Comput 2007; 45(8): 781-9.
[http://dx.doi.org/10.1007/s11517-007-0210-1] [PMID: 17624564]
[53]
Teng W, Huneiti Z, Machowski W, Evans JRG, Edirisinghe MJ, Balachandran W. Towards particle-by particle deposition of ceramics using electrostatic atomization. J Mater Sci Lett 1997; 16(12): 1017-9.
[http://dx.doi.org/10.1023/A:1018506103880]
[54]
Hettiarachchi K, Talu E, Longo ML, Dayton PA, Lee AP. On-chip generation of microbubbles as a practical technology for manufacturing contrast agents for ultrasonic imaging. Lab Chip 2007; 7(4): 463-8.
[http://dx.doi.org/10.1039/b701481n] [PMID: 17389962]
[55]
Pancholi KP, Farook U, Moaleji R, Stride E, Edirisinghe MJ. Novel methods for preparing phospholipid coated microbubbles. Eur Biophys J 2008; 37(4): 515-20.
[http://dx.doi.org/10.1007/s00249-007-0211-x] [PMID: 17687548]
[56]
Dollet B, van Hoeve W, Raven JP, Marmottant P, Versluis M. Role of the channel geometry on the bubble pinch-off in flow-focusing devices. Phys Rev Lett 2008; 100(3): 034504.
[http://dx.doi.org/10.1103/PhysRevLett.100.034504] [PMID: 18232987]
[57]
Pancholi K, Stride E, Edirisinghe M. Dynamics of bubble formation in highly viscous liquids. Langmuir 2008; 24(8): 4388-93.
[http://dx.doi.org/10.1021/la703849x] [PMID: 18331069]
[58]
Stride E. The influence of surface adsorption on microbubble dynamics. Philos Trans- Royal Soc, Math Phys Eng Sci 2008; 366(1873): 2103-15.
[http://dx.doi.org/10.1098/rsta.2008.0001] [PMID: 18348975]
[59]
Schmidt W, Roessling G. Novel manufacturing process of hollow polymer microspheres. Chem Eng Sci 2006; 61(15): 4973-81.
[http://dx.doi.org/10.1016/j.ces.2006.03.021]
[60]
O’Brien WD Jr. Ultrasound-biophysics mechanisms. Prog Biophys Mol Biol 2007; 93(1-3): 212-55.
[http://dx.doi.org/10.1016/j.pbiomolbio.2006.07.010] [PMID: 16934858]
[61]
Information for manufacturers seeking marketing clearance of diagnostic ultrasound systems and transducers. 2008. Available from: https://www.fda.gov/media/71100/download
[62]
Christiansen JP, French BA, Klibanov AL, Kaul S, Lindner JR. Targeted tissue transfection with ultrasound destruction of plasmid-bearing cationic microbubbles. Ultrasound Med Biol 2003; 29(12): 1759-67.
[http://dx.doi.org/10.1016/S0301-5629(03)00976-1] [PMID: 14698343]
[63]
Bekeredjian R, Chen S, Frenkel PA, Grayburn PA, Shohet RV. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 2003; 108(8): 1022-6.
[http://dx.doi.org/10.1161/01.CIR.0000084535.35435.AE] [PMID: 12912823]
[64]
Chen S, Shohet RV, Bekeredjian R, Frenkel P, Grayburn PA. Optimization of ultrasound parameters for cardiac gene delivery of adenoviral or plasmid deoxyribonucleic acid by ultrasound-targeted microbubble destruction. J Am Coll Cardiol 2003; 42(2): 301-8.
[http://dx.doi.org/10.1016/S0735-1097(03)00627-2] [PMID: 12875768]
[65]
Frenkel PA, Chen S, Thai T, Shohet RV, Grayburn PA. DNA-loaded albumin microbubbles enhance ultrasound-mediated transfection in vitro. Ultrasound Med Biol 2002; 28(6): 817-22.
[http://dx.doi.org/10.1016/S0301-5629(02)00518-5] [PMID: 12113794]
[66]
Klibanov AL. Targeted delivery of gas-filled microspheres, contrast agents for ultrasound imaging. Adv Drug Deliv Rev 1999; 37(1-3): 139-57.
[http://dx.doi.org/10.1016/S0169-409X(98)00104-5] [PMID: 10837732]
[67]
Lentacker I, De Geest BG, Vandenbroucke RE, et al. Ultrasound-responsive polymer-coated microbubbles that bind and protect DNA. Langmuir 2006; 22(17): 7273-8.
[http://dx.doi.org/10.1021/la0603828] [PMID: 16893226]
[68]
Zwiorek K, Kloeckner J, Wagner E, Coester C. Gelatin nanoparticles as a new and simple gene delivery system. J Pharm Pharm Sci 2005; 7(4): 22-8.
[PMID: 15850545]
[69]
Chomas JE, Dayton P, Allen J, Morgan K, Ferrara KW. Mechanisms of contrast agent destruction. IEEE Trans Ultrason Ferroelectr Freq Control 2001; 48(1): 232-48.
[http://dx.doi.org/10.1109/58.896136] [PMID: 11367791]
[70]
Chomas JE, Dayton P, May D, Ferrara K. Threshold of fragmentation for ultrasonic contrast agents. J Biomed Opt 2001; 6(2): 141-50.
[http://dx.doi.org/10.1117/1.1352752] [PMID: 11375723]
[71]
Miller MW. Gene transfection and drug delivery. Ultrasound Med Biol 2000; 26(Suppl. 1): S59-62.
[http://dx.doi.org/10.1016/S0301-5629(00)00166-6] [PMID: 10794877]
[72]
Skyba DM, Price RJ, Linka AZ, Skalak TC, Kaul S. Direct in vivo visualization of intravascular destruction of microbubbles by ultra-sound and its local effects on tissue. Circulation 1998; 98(4): 290-3.
[http://dx.doi.org/10.1161/01.CIR.98.4.290] [PMID: 9711932]
[73]
Taniyama Y, Tachibana K, Hiraoka K, et al. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002; 105(10): 1233-9.
[http://dx.doi.org/10.1161/hc1002.105228] [PMID: 11889019]
[74]
Christiansen JP, Leong-Poi H, Klibanov AL, Kaul S, Lindner JR. Noninvasive imaging of myocardial reperfusion injury using leukocyte-targeted contrast echocardiography. Circulation 2002; 105(15): 1764-7.
[http://dx.doi.org/10.1161/01.CIR.0000015466.89771.E2] [PMID: 11956115]
[75]
Lindner JR, Coggins MP, Kaul S, Klibanov AL, Brandenburger GH, Ley K. Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin- and complement-mediated adherence to activated leukocytes. Circulation 2000; 101(6): 668-75.
[http://dx.doi.org/10.1161/01.CIR.101.6.668] [PMID: 10673260]
[76]
Rapoport N, Gao Z, Kennedy A. Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy. J Natl Cancer Inst 2007; 99(14): 1095-106.
[http://dx.doi.org/10.1093/jnci/djm043] [PMID: 17623798]
[77]
Siwak DR, Tari AM, Lopez-Berestein G. The potential of drug-carrying immunoliposomes as anticancer agents. Commentary re: J. W. Park et al., Anti-HER2 immunoliposomes: enhanced efficacy due to targeted delivery. Clin. Cancer Res., 8: 1172-1181, 2002. Clin Cancer Res 2002; 8(4): 955-6.
[PMID: 11948099]
[78]
Shi M, Wosnick JH, Ho K, Keating A, Shoichet MS. Immuno-polymeric nanoparticles by Diels-Alder chemistry. Angew Chem Int Ed 2007; 46(32): 6126-31.
[http://dx.doi.org/10.1002/anie.200701032] [PMID: 17628481]
[79]
Lim AKP, Patel N, Eckersley RJ, Taylor-Robinson SD, Cosgrove DO, Blomley MJ. Evidence for spleen-specific uptake of a microbubble contrast agent: A quantitative study in healthy volunteers. Radiology 2004; 231(3): 785-8.
[http://dx.doi.org/10.1148/radiol.2313030544] [PMID: 15118114]
[80]
Nalini kurup, Prajakta naik. Microbubbles: A novel delivery system. Jprhc 2010; 2(3): 228-34.
[81]
Janzen N, Zisman A, Pantuck AJ, Perry K, Schulam P, Belldegrun AS. Minimally invasive ablative approaches in the treatment of renal cell carcinoma. Curr Urol Rep 2002; 3: 13-20.
[82]
ter Haar GR. High intensity focused ultrasound for the treatment of tumors. Echocardiography 2001; 18(4): 317-22.
[http://dx.doi.org/10.1046/j.1540-8175.2001.00317.x] [PMID: 11415504]
[83]
Cheung JS, Chow AM, Guo H, Wu EX. Microbubbles as a novel contrast agent for brain MRI. Neuroimage 2009; 46(3): 658-64.
[http://dx.doi.org/10.1016/j.neuroimage.2009.02.037] [PMID: 19269337]
[84]
Alexander AL, McCreery TT, Barrette TR, Gmitro AF, Unger EC. Microbubbles as novel pressure-sensitive MR contrast agents. Magn Reson Med 1996; 35(6): 801-6.
[http://dx.doi.org/10.1002/mrm.1910350603] [PMID: 8744005]
[85]
Dharmakumar R, Plewes DB, Wright GA. On the parameters affecting the sensitivity of MR measures of pressure with microbubbles. Magn Reson Med 2002; 47(2): 264-73.
[http://dx.doi.org/10.1002/mrm.10075] [PMID: 11810669]
[86]
Yang F, Li Y, Chen Z, Zhang Y, Wu J, Gu N. Superparamagnetic iron oxide nanoparticle-embedded encapsulated microbubbles as dual contrast agents of magnetic resonance and ultrasound imaging. Biomaterials 2009; 30(23-24): 3882-90.
[http://dx.doi.org/10.1016/j.biomaterials.2009.03.051] [PMID: 19395082]
[87]
Park JI, Jagadeesan D, Williams R, et al. Microbubbles loaded with nanoparticles: A route to multiple imaging modalities. ACS Nano 2010; 4(11): 6579-86.
[http://dx.doi.org/10.1021/nn102248g] [PMID: 20968309]
[88]
Chow AM, Wu EX. Microbubbles: Contrast agents for ultrasound and MRI The chemistry of molecular imaging. 1st ed. John Wiley & Sons, Inc. 2015.
[89]
Tartis MS, Kruse DE, Zheng H, et al. Dynamic microPET imaging of ultrasound contrast agents and lipid delivery. J Control Release 2008; 131(3): 160-6.
[http://dx.doi.org/10.1016/j.jconrel.2008.07.030] [PMID: 18718854]
[90]
Willmann JK, Cheng Z, Davis C, et al. Targeted microbubbles for imaging tumor angiogenesis: Assessment of whole-body biodistribution with dynamic micro-PET in mice. Radiology 2008; 249(1): 212-9.
[http://dx.doi.org/10.1148/radiol.2491072050] [PMID: 18695212]
[91]
Zhang L, Hu C, Zhao T, Luo S. Noninvasive visualization of microvessels using diffraction enhanced imaging. Eur J Radiol 2011; 80(1): 158-62.
[http://dx.doi.org/10.1016/j.ejrad.2010.08.019] [PMID: 20833491]
[92]
Arfelli F, Rigon L, Menk RH. Microbubbles as x-ray scattering contrast agents using analyzer-based imaging. Phys Med Biol 2010; 55(6): 1643-58.
[http://dx.doi.org/10.1088/0031-9155/55/6/008] [PMID: 20182004]
[93]
Gong Q, Gao X, Liu W, Hong T, Chen C. Drug-loaded microbubbles combined with ultrasound for thrombolysis and malignant tumor therapy. BioMed Research International 2019; 11.
[http://dx.doi.org/10.1155/2019/6792465]
[94]
Molina CA, Ribo M, Rubiera M, et al. Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke patients treated with intravenous tissue plasminogen activator. Stroke 2006; 37(2): 425-9.
[http://dx.doi.org/10.1161/01.STR.0000199064.94588.39] [PMID: 16373632]
[95]
Wang X, Gkanatsas Y, Palasubramaniam J, et al. Thrombus-targeted theranostic microbubbles: A new technology towards concurrent rapid ultrasound diagnosis and bleeding-free fibrinolytic treatment of thrombosis. Theranostics 2016; 6(5): 726-38.
[http://dx.doi.org/10.7150/thno.14514] [PMID: 27022419]
[96]
Hagisawa K, Nishioka T, Suzuki R, et al. Thrombus-targeted perfluorocarbon-containing liposomal bubbles for enhancement of ultrasonic thrombolysis: In vitro and in vivo study. J Thromb Haemost 2013; 11(8): 1565-73.
[http://dx.doi.org/10.1111/jth.12321] [PMID: 23773778]
[97]
Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 2001; 220(3): 640-6.
[http://dx.doi.org/10.1148/radiol.2202001804] [PMID: 11526261]
[98]
Burgess A, Shah K, Hough O, Hynynen K. Focused ultrasound-mediated drug delivery through the blood-brain barrier. Expert Rev Neurother 2015; 15(5): 477-91.
[http://dx.doi.org/10.1586/14737175.2015.1028369] [PMID: 25936845]
[99]
Sheikov N, McDannold N, Sharma S, Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med Biol 2008; 34(7): 1093-104.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2007.12.015] [PMID: 18378064]
[100]
Tung YS, Vlachos F, Feshitan JA, Borden MA, Konofagou EE. The mechanism of interaction between focused ultrasound and microbubbles in blood-brain barrier opening in mice. J Acoust Soc Am 2011; 130(5): 3059-67.
[http://dx.doi.org/10.1121/1.3646905] [PMID: 22087933]
[101]
Lipsman N, Meng Y, Bethune AJ, et al. Blood-brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound. Nat Commun 2018; 9(1): 2336.
[http://dx.doi.org/10.1038/s41467-018-04529-6] [PMID: 30046032]
[102]
Verma IM, Somia N. Gene therapy - promises, problems and prospects. Nature 1997; 389(6648): 239-42.
[http://dx.doi.org/10.1038/38410] [PMID: 9305836]
[103]
Newman KD, Dunn PF, Owens JW, et al. Adenovirus-mediated gene transfer into normal rabbit arteries results in prolonged vascular cell activation, inflammation, and neointimal hyperplasia. J Clin Invest 1995; 96(6): 2955-65.
[http://dx.doi.org/10.1172/JCI118367] [PMID: 8675667]
[104]
Felgner PL. Nonviral strategies for gene therapy. Sci Am 1997; 276(6): 102-6.
[http://dx.doi.org/10.1038/scientificamerican0697-102] [PMID: 9163942]
[105]
Porter TR, Iversen PL, Li S, Xie F. Interaction of diagnostic ultrasound with synthetic oligonucleotide-labeled perfluorocarbon-exposed sonicated dextrose albumin microbubbles. J Ultrasound Med 1996; 15(8): 577-84.
[http://dx.doi.org/10.7863/jum.1996.15.8.577] [PMID: 8839405]
[106]
Bao S, Thrall BD, Miller DL. Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med Biol 1997; 23(6): 953-9.
[http://dx.doi.org/10.1016/S0301-5629(97)00025-2] [PMID: 9300999]
[107]
Shohet RV, Chen S, Zhou YT, et al. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 2000; 101(22): 2554-6.
[http://dx.doi.org/10.1161/01.CIR.101.22.2554] [PMID: 10840004]
[108]
Li W, Liu S, Ren J, Xiong H, Yan X, Wang Z. Gene transfection to retinal ganglion cells mediated by ultrasound microbubbles in vitro. Acad Radiol 2009; 16(9): 1086-94.
[http://dx.doi.org/10.1016/j.acra.2009.03.019] [PMID: 19541507]
[109]
Kaneko OF, Willmann JK. Ultrasound for molecular imaging and therapy in cancer. Quant Imaging Med Surg 2012; 2(2): 87-97.
[PMID: 23061039]
[110]
Escoffre JM, Mannaris C, Geers B, et al. Doxorubicin liposome-loaded microbubbles for contrast imaging and ultrasound-triggered drug delivery. IEEE Trans Ultrason Ferroelectr Freq Control 2013; 60(1): 78-87.
[http://dx.doi.org/10.1109/TUFFC.2013.2539] [PMID: 23287915]
[111]
Kang J, Wu X, Wang Z, et al. Antitumor effect of docetaxel-loaded lipid microbubbles combined with ultrasound-targeted microbubble activation on VX2 rabbit liver tumors. J Ultrasound Med 2010; 29(1): 61-70.
[http://dx.doi.org/10.7863/jum.2010.29.1.61] [PMID: 20040776]
[112]
Tinkov S, Coester C, Serba S, et al. New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: In-vivo characterization. J Control Release 2010; 148(3): 368-72.
[http://dx.doi.org/10.1016/j.jconrel.2010.09.004] [PMID: 20868711]
[113]
Ramaswamy K, Marx V, Laser D, et al. Targeted microbubbles: a novel application for the treatment of kidney stones. BJU Int 2015; 116(1): 9-16.
[http://dx.doi.org/10.1111/bju.12996] [PMID: 25402588]
[114]
Lan HY, Mu W, Tomita N, et al. Inhibition of renal fibrosis by gene transfer of inducible Smad7 using ultrasound-microbubble system in rat UUO model. J Am Soc Nephrol 2003; 14(6): 1535-48.
[http://dx.doi.org/10.1097/01.ASN.0000067632.04658.B8] [PMID: 12761254]
[115]
Newhouse MT. Tennis anyone? The lungs as a new court for systemic therapy. CMAJ 1999; 161(10): 1287-8.
[PMID: 10584092]
[116]
Edwards DA, Hanes J, Caponetti G, et al. Large porous particles for pulmonary drug delivery. Science 1997; 276(5320): 1868-71.
[http://dx.doi.org/10.1126/science.276.5320.1868] [PMID: 9188534]
[117]
Musante CJ, Schroeter JD, Rosati JA, Crowder TM, Hickey AJ, Martonen TB. Factors affecting the deposition of inhaled porous drug particles. J Pharm Sci 2002; 91(7): 1590-600.
[http://dx.doi.org/10.1002/jps.10152] [PMID: 12115821]
[118]
Edwards DA, Ben-Jebria A, Langer R. Recent advances in pulmonary drug delivery using large, porous inhaled particles. J Appl Physiol 1998; 85(2): 379-85.
[http://dx.doi.org/10.1152/jappl.1998.85.2.379] [PMID: 9688708]
[119]
Greenleaf WJ, Bolander ME, Sarkar G, Goldring MB, Greenleaf JF. Artificial cavitation nuclei significantly enhance acoustically induced cell transfection. Ultrasound Med Biol 1998; 24(4): 587-95.
[http://dx.doi.org/10.1016/S0301-5629(98)00003-9] [PMID: 9651968]
[120]
Miller DL, Pislaru SV, Greenleaf JE. Sonoporation: mechanical DNA delivery by ultrasonic cavitation. Somat Cell Mol Genet 2002; 27(1-6): 115-34.
[http://dx.doi.org/10.1023/A:1022983907223] [PMID: 12774945]
[121]
Porter TR, Xie F. Therapeutic ultrasound for gene delivery. Echocardiography 2001; 18(4): 349-53.
[http://dx.doi.org/10.1046/j.1540-8175.2001.00349.x] [PMID: 11415508]
[122]
Lu QL, Liang HD, Partridge T, Blomley MJ. Microbubble ultrasound improves the efficiency of gene transduction in skeletal muscle in vivo with reduced tissue damage. Gene Ther 2003; 10(5): 396-405.
[http://dx.doi.org/10.1038/sj.gt.3301913] [PMID: 12601394]
[123]
Teupe C, Richter S, Fisslthaler B, et al. Vascular gene transfer of phosphomimetic endothelial nitric oxide synthase (S1177D) using ultrasound-enhanced destruction of plasmid-loaded microbubbles improves vasoreactivity. Circulation 2002; 105(9): 1104-9.
[http://dx.doi.org/10.1161/hc0902.104720] [PMID: 11877363]
[124]
Bloch SH, Wan M, Dayton PA, Ferrara KW. Optical observation of lipid- and polymer-shelled ultrasound microbubble contrast agents. Appl Phys Lett 2004; 84(4): 631-3.
[http://dx.doi.org/10.1063/1.1643544]
[125]
Min KH, Min HS, Lee HJ, et al. pH-controlled gas-generating mineralized nanoparticles: A theranostic agent for ultrasound imaging and therapy of cancers. ACS Nano 2015; 9(1): 134-45.
[http://dx.doi.org/10.1021/nn506210a] [PMID: 25559896]
[126]
Zhang N, Li J, Hou R, et al. Bubble-generating nano-lipid carriers for ultrasound/CT imaging-guided efficient tumor therapy. Int J Pharm 2017; 534(1-2): 251-62.
[http://dx.doi.org/10.1016/j.ijpharm.2017.07.081] [PMID: 28803939]
[127]
Mikhail G. Shapiro, Patrick W. he, Arkosnato Neogy, Melissa Yin, F. Stuart Foster, David V. Schaffer. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat Nanotechnol 2014; 9: 311-6.
[128]
Farhadi A, Ho GH, Sawyer DP, Bourdeau RW, Shapiro MG. Ultrasound imaging of gene expression in mammalian cells. Science 2019; 365(6460): 1469-75.
[http://dx.doi.org/10.1126/science.aax4804] [PMID: 31604277]
[129]
Fix SM, Borden MA, Dayton PA. Therapeutic gas delivery via microbubbles and liposomes. J Control Release 2015; 209: 139-49.
[http://dx.doi.org/10.1016/j.jconrel.2015.04.027] [PMID: 25913365]
[130]
Fix SM, Papadopoulou V, Velds H, et al. Oxygen microbubbles improve radiotherapy tumor control in a rat fibrosarcoma model - A preliminary study. PLoS One 2018; 13(4): e0195667.
[http://dx.doi.org/10.1371/journal.pone.0195667] [PMID: 29630640]
[131]
Lu X. Impact of IL-12 in Cancer. Curr Cancer Drug Targets 2017; 17(8): 682-97.
[http://dx.doi.org/10.2174/1568009617666170427102729] [PMID: 28460617]
[132]
Brunda MJ. Interleukin-12. J Leukoc Biol 1994; 55(2): 280-8.
[http://dx.doi.org/10.1002/jlb.55.2.280] [PMID: 7905508]
[133]
Suzuki R, Namai E, Oda Y, et al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release 2010; 142(2): 245-50.
[http://dx.doi.org/10.1016/j.jconrel.2009.10.027] [PMID: 19883708]
[134]
Munakata L, Tanimoto Y, Osa A, et al. Lipid nanoparticles of Type-A CpG D35 suppress tumor growth by changing tumor immune-microenvironment and activate CD8 T cells in mice. J Control Release 2019; 313: 106-19.
[http://dx.doi.org/10.1016/j.jconrel.2019.09.011] [PMID: 31629036]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy