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Current Pharmaceutical Biotechnology

Current Pharmaceutical Biotechnology

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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

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Review Article

Exploring the Theranostic Applications and Prospects of Nanobubbles

Author(s): Rahul Shahorcid of author, Niraj Phatakorcid of author, Ashok Choudhary, Sakshi Gadewar, Ajazuddinorcid of author and Sankha Bhattacharya*

Volume 25, Issue 9, 2024

Published on: 12 October, 2023

Page: [1167 - 1181] Pages: 15

DOI: 10.2174/0113892010248189231010085827

Price: $65

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Abstract

Anticancer medications as well as additional therapeutic compounds, have poor clinical effectiveness due to their diverse distribution, non-selectivity for malignant cells, and undesirable off-target side effects. As a result, ultrasound-based targeted delivery of therapeutic compounds carried in sophisticated nanocarriers has grown in favor of cancer therapy and control. Nanobubbles are nanoscale bubbles that exhibit unique physiochemical properties in both their inner core and outer shell. Manufacturing nanobubbles primarily aims to enhance therapeutic agents' bioavailability, stability, and targeted delivery. The small size of nanobubbles allows for their extravasation from blood vessels into surrounding tissues and site-specific release through ultrasound targeting. Ultrasound technology is widely utilized for therapy due to its speed, safety, and cost-effectiveness, and micro/nanobubbles, as ultrasound contrast agents, have numerous potential applications in disease treatment. Thus, combining ultrasound applications with NBs has recently demonstrated increased localization of anticancer molecules in tumor tissues with triggered release behavior. Consequently, an effective therapeutic concentration of drugs/genes is achieved in target tumor tissues with ultimately increased therapeutic efficacy and minimal side effects on other non-cancerous tissues. This paper provides a brief overview of the production processes for nanobubbles, along with their key characteristics and potential therapeutic uses.

Keywords: Nanobubbles, Magnetic Resonance Imaging (MRI), ultrasound, tumor imaging, gene delivery, non-cancerous tissues.

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Graphical Abstract

Graphical abstract illustrating key findings of the study

[1]
Thirumalaivasan, N.; Venkatesan, P.; Lai, P.S.; Wu, S.P. In vitro and in vivo approach of hydrogen-sulfide-responsive drug release driven by azide-functionalized mesoporous silica nanoparticles. ACS Appl. Bio Mater., 2019, 2(9), 3886-3896.
[http://dx.doi.org/10.1021/acsabm.9b00481] [PMID: 35021323]
[2]
Ketabat, Farinaz Controlled drug delivery systems for oral cancer treatment—current status and future perspectives. Pharmaceutics, 2019, 11(7), 302.
[http://dx.doi.org/10.3390/pharmaceutics11070302]
[3]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2019. CA Cancer J. Clin., 2019, 69(1), 7-34.
[http://dx.doi.org/10.3322/caac.21551] [PMID: 30620402]
[4]
Young-sun, K. Uterine fibroids: Semiquantitative perfusion MR imaging parameters associated with the intraprocedural and immediate postprocedural treatment efficiencies of MR imaging-guided high-intensity focused ultrasound ablation. Radiology, 2014, 273(2), 462-471.
[5]
Borregaard, R.; Lukac, P.; Gerdes, C.; Møller, D.; Mortensen, P.T.; Pedersen, L.; Nielsen, J.C.; Jensen, H.K. Radiofrequency ablation of accessory pathways in patients with the Wolff-Parkinson-White syndrome: The long-term mortality and risk of atrial fibrillation. Europace, 2015, 17(1), 117-122.
[http://dx.doi.org/10.1093/europace/euu176] [PMID: 25013013]
[6]
Taïeb, D.; Jha, A.; Treglia, G.; Pacak, K. Molecular imaging and radionuclide therapy of pheochromocytoma and paraganglioma in the era of genomic characterization of disease subgroups. Endocr. Relat. Cancer, 2019, 26(11), R627-R652.
[http://dx.doi.org/10.1530/ERC-19-0165] [PMID: 31561209]
[7]
Shen, Y.; Lv, W.; Yang, H.; Cai, W.; Zhao, P.; Zhang, L.; Zhang, J.; Yuan, L.; Duan, Y. FA-NBs-IR780: Novel multifunctional nanobubbles as molecule-targeted ultrasound contrast agents for accurate diagnosis and photothermal therapy of cancer. Cancer Lett., 2019, 455, 14-25.
[http://dx.doi.org/10.1016/j.canlet.2019.04.023] [PMID: 31018151]
[8]
Kiessling, F.; Fokong, S.; Bzyl, J.; Lederle, W.; Palmowski, M.; Lammers, T. Recent advances in molecular, multimodal and theranostic ultrasound imaging. Adv. Drug Deliv. Rev., 2014, 72, 15-27.
[http://dx.doi.org/10.1016/j.addr.2013.11.013] [PMID: 24316070]
[9]
Zhu, G.; Zhang, Y.; Wang, K.; Zhao, X.; Lian, H.; Wang, W.; Wang, H.; Wu, J.; Hu, Y.; Guo, H. Visualized intravesical floating hydrogel encapsulating vaporized perfluoropentane for controlled drug release. Drug Deliv., 2016, 23(8), 2820-2826.
[http://dx.doi.org/10.3109/10717544.2015.1101791] [PMID: 26515239]
[10]
Shagdarsuren, B.; Tamai, H.; Shingaki, N.; Mori, Y.; Maeshima, S.; Nuta, J.; Maeda, Y.; Moribata, K.; Niwa, T.; Deguchi, H.; Inoue, I.; Maekita, T.; Iguchi, M.; Kato, J.; Ichinose, M. Contribution of contrast-enhanced sonography with perfluorobutane microbubbles for diagnosis of recurrent hepatocellular carcinoma. J. Ultrasound Med., 2016, 35(7), 1383-1391.
[http://dx.doi.org/10.7863/ultra.15.08042] [PMID: 27208196]
[11]
Pathak, V.; Nolte, T.; Rama, E.; Rix, A.; Dadfar, S.M.; Paefgen, V.; Banala, S.; Buhl, E.M.; Weiler, M.; Schulz, V.; Lammers, T.; Kiessling, F. Molecular magnetic resonance imaging of Alpha-v-Beta-3 integrin expression in tumors with ultrasound microbubbles. Biomaterials, 2021, 275, 120896.
[http://dx.doi.org/10.1016/j.biomaterials.2021.120896] [PMID: 34090049]
[12]
Exner, A.A.; Kolios, M.C. Bursting microbubbles: How nanobubble contrast agents can enable the future of medical ultrasound molecular imaging and image-guided therapy. Curr. Opin. Colloid Interface Sci., 2021, 54, 101463.
[http://dx.doi.org/10.1016/j.cocis.2021.101463] [PMID: 34393610]
[13]
Lajoinie, G.; van Rooij, T.; Skachkov, I.; Blazejewski, E.; Veldhuis, G.; de Jong, N.; Kooiman, K.; Versluis, M. Laser-activated polymeric microcapsules for ultrasound imaging and therapy: In vitro feasibility. Biophys. J., 2017, 112(9), 1894-1907.
[http://dx.doi.org/10.1016/j.bpj.2017.03.033] [PMID: 28494960]
[14]
Cao, Yang Drug release from phase-changeable nanodroplets triggered by low-intensity focused ultrasound. Theranostics, 2018, 8(5), 1327.
[http://dx.doi.org/10.7150/thno.21492]
[15]
Wang, Shiying; Hossack, John .A.; Klibanov, Alexander .L Targeting of microbubbles: Contrast agents for ultrasound molecular imaging. J. Drug Target., 2018, 26(5-6), 420-434.
[http://dx.doi.org/10.1080/1061186X.2017.1419362]
[16]
Güvener, N.; Appold, L.; de Lorenzi, F.; Golombek, S.K.; Rizzo, L.Y.; Lammers, T.; Kiessling, F. Recent advances in ultrasound-based diagnosis and therapy with micro- and nanometer-sized formulations. Methods, 2017, 130, 4-13.
[http://dx.doi.org/10.1016/j.ymeth.2017.05.018] [PMID: 28552267]
[17]
Cai, Wen Bin The optimized fabrication of nanobubbles as ultrasound contrast agents for tumor imaging. Sci. Report., 2015, 5(1), 13725.
[http://dx.doi.org/10.1038/srep13725]
[18]
Deshpande, N.; Needles, A.; Willmann, J.K. Molecular ultrasound imaging: Current status and future directions. Clin. Radiol., 2010, 65(7), 567-581.
[http://dx.doi.org/10.1016/j.crad.2010.02.013] [PMID: 20541656]
[19]
Shakeri-Zadeh, A.; Zareyi, H.; Sheervalilou, R.; Laurent, S.; Ghaznavi, H.; Samadian, H. Gold nanoparticle-mediated bubbles in cancer nanotechnology. J. Control. Release, 2021, 330, 49-60.
[http://dx.doi.org/10.1016/j.jconrel.2020.12.022] [PMID: 33340564]
[20]
Duan, Lei Micro/nano-bubble-assisted ultrasound to enhance the EPR effect and potential theranostic applications. Theranostics, 2020, 10(2), 462.
[http://dx.doi.org/10.7150/thno.37593]
[21]
Yang, H.; Cai, W.; Xu, L.; Lv, X.; Qiao, Y.; Li, P.; Wu, H.; Yang, Y.; Zhang, L.; Duan, Y. Nanobubble–Affibody: Novel ultrasound contrast agents for targeted molecular ultrasound imaging of tumor. Biomaterials, 2015, 37, 279-288.
[http://dx.doi.org/10.1016/j.biomaterials.2014.10.013] [PMID: 25453958]
[22]
Damien, V.B. Nanobubbles for therapeutic delivery: Production, stability and current prospects. Curr. Opin. Coll. Interface Sci., 2021, 54, 101456.
[23]
Cavalli, R.; Soster, M.; Argenziano, M. Nanobubbles: A promising efficienft tool for therapeutic delivery. Ther. Deliv., 2016, 7(2), 117-138.
[http://dx.doi.org/10.4155/tde.15.92] [PMID: 26769397]
[24]
Roovers, S.; Segers, T.; Lajoinie, G.; Deprez, J.; Versluis, M.; De Smedt, S.C.; Lentacker, I. The role of ultrasound-driven microbubble dynamics in drug delivery: From microbubble fundamentals to clinical translation. Langmuir, 2019, 35(31), 10173-10191.
[http://dx.doi.org/10.1021/acs.langmuir.8b03779] [PMID: 30653325]
[25]
Abenojar, E.C.; Nittayacharn, P.; de Leon, A.C.; Perera, R.; Wang, Y.; Bederman, I.; Exner, A.A. Effect of bubble concentration on the in vitro and in vivo performance of highly stable lipid shell-stabilized micro-and nanoscale ultrasound contrast agents. Langmuir, 2019, 35(31), 10192-10202.
[http://dx.doi.org/10.1021/acs.langmuir.9b00462] [PMID: 30913884]
[26]
Lu, Shirui Mechanistic Insights and therapeutic delivery through micro/nanobubble-assisted ultrasound. Pharmaceutics, 2022, 14(3), 480.
[http://dx.doi.org/10.3390/pharmaceutics14030480]
[27]
Dichiarante, V.; Milani, R.; Metrangolo, P. Natural surfactants towards a more sustainable fluorine chemistry. Green Chem., 2018, 20(1), 13-27.
[http://dx.doi.org/10.1039/C7GC03081A]
[28]
Tehrani Fateh, S.; Moradi, L.; Kohan, E.; Hamblin, M.R.; Shiralizadeh Dezfuli, A. Comprehensive review on ultrasound-responsive theranostic nanomaterials: Mechanisms, structures and medical applications. Beilstein J. Nanotechnol., 2021, 12(1), 808-862.
[http://dx.doi.org/10.3762/bjnano.12.64] [PMID: 34476167]
[29]
Thomas, S.H. Ultrasonic encapsulation-A review. Ultrason. Sonochem., 2017, 35, 605-614.
[30]
Prasher, P.; Sharma, M.; Mehta, M.; Satija, S.; Aljabali, A.A.; Tambuwala, M.M.; Anand, K.; Sharma, N.; Dureja, H.; Jha, N.K.; Gupta, G.; Gulati, M.; Singh, S.K.; Chellappan, D.K.; Paudel, K.R.; Hansbro, P.M.; Dua, K. Current-status and applications of polysaccharides in drug delivery systems. Colloid Interface Sci. Commun., 2021, 42, 100418.
[http://dx.doi.org/10.1016/j.colcom.2021.100418]
[31]
Su, C.; Ren, X.; Nie, F.; Li, T.; Lv, W.; Li, H.; Zhang, Y. Current advances in ultrasound-combined nanobubbles for cancer-targeted therapy: A review of the current status and future perspectives. RSC Advances, 2021, 11(21), 12915-12928.
[http://dx.doi.org/10.1039/D0RA08727K] [PMID: 35423829]
[32]
Cao, Q.; Li, X.; Zhang, Q.; Zhou, K.; Yu, Y.; He, Z.; Xiang, Z.; Qiang, Y.; Qi, W. Big data analysis of manufacturing and preclinical studies of nanodrug-targeted delivery systems: A literature review. BioMed Res. Int., 2022, 2022, 1-10.
[http://dx.doi.org/10.1155/2022/1231446] [PMID: 35941977]
[33]
Mitragotri, Samir; Lahann, Joerg Materials for drug delivery: Innovative solutions to address complex biological hurdles. Adv. Mater., 2012, 24, 3717-3723.
[http://dx.doi.org/10.1002/adma.201202080]
[34]
Subhan, Md Abdus Recent advances in tumor targeting via EPR effect for cancer treatment. J. Personal Med., 2021, 11(6), 571.
[http://dx.doi.org/10.3390/jpm11060571]
[35]
Nazir, F.; Tabish, T.A.; Tariq, F.; Iftikhar, S.; Wasim, R.; Shahnaz, G. Stimuli-sensitive drug delivery systems for site-specific antibiotic release. Drug Discov. Today, 2022, 27(6), 1698-1705.
[http://dx.doi.org/10.1016/j.drudis.2022.02.014] [PMID: 35219858]
[36]
Li, T.; Zhou, J.; Zhang, C.; Zhi, X.; Niu, J.; Fu, H.; Song, J.; Cui, D. Surface-engineered nanobubbles with pH-/light-responsive drug release and charge-switchable behaviors for active NIR/MR/US imaging-guided tumor therapy. NPG Asia Mater., 2018, 10(11), 1046-1060.
[http://dx.doi.org/10.1038/s41427-018-0094-6]
[37]
Yasui, K.; Tuziuti, T.; Kanematsu, W. Mysteries of bulk nanobubbles (ultrafine bubbles); stability and radical formation. Ultrason. Sonochem., 2018, 48, 259-266.
[http://dx.doi.org/10.1016/j.ultsonch.2018.05.038] [PMID: 30080549]
[38]
Yasuda, K.; Matsushima, H.; Asakura, Y. Generation and reduction of bulk nanobubbles by ultrasonic irradiation. Chem. Eng. Sci., 2019, 195, 455-461.
[http://dx.doi.org/10.1016/j.ces.2018.09.044]
[39]
Nirmalkar, N.; Pacek, A.W.; Barigou, M.A.W. Pacek, and Mostafa Barigou. “On the existence and stability of bulk nanobubbles.”. Langmuir, 2018, 34(37), 10964-10973.
[http://dx.doi.org/10.1021/acs.langmuir.8b01163] [PMID: 30179016]
[40]
Cho, Sung-Ho Ultrasonic formation of nanobubbles and their zeta-potentials in aqueous electrolyte and surfactant solutions. Coll. Surf. A: Physicochem. Eng. Aspec., 2005, 269(1-3), 28-34.
[http://dx.doi.org/10.1016/j.colsurfa.2005.06.063]
[41]
Chen, Y.; Truong, V.N.T.; Bu, X.; Xie, G. A review of effects and applications of ultrasound in mineral flotation. Ultrason. Sonochem., 2020, 60, 104739.
[http://dx.doi.org/10.1016/j.ultsonch.2019.104739] [PMID: 31557697]
[42]
RAY. Nano bubbles: Concept & recent advances as therapeutic agent. Asian J. Adv. Res., 2021, 1085-1097.
[43]
An, H.; Liu, G.; Craig, V.S.J. Wetting of nanophases: Nanobubbles, nanodroplets and micropancakes on hydrophobic surfaces. Adv. Colloid Interface Sci., 2015, 222, 9-17.
[http://dx.doi.org/10.1016/j.cis.2014.07.008] [PMID: 25128452]
[44]
Xiao, Q.; Liu, Y.; Guo, Z.; Liu, Z.; Lohse, D.; Zhang, X. Solvent exchange leading to nanobubble nucleation: A molecular dynamics study. Langmuir, 2017, 33(32), 8090-8096.
[http://dx.doi.org/10.1021/acs.langmuir.7b01231] [PMID: 28742364]
[45]
Chen, M.; Peng, L.; Qiu, J.; Luo, K.; Liu, D.; Han, P. Monitoring of an ethanol-water exchange process to produce bulk nanobubbles based on dynamic light scattering. Langmuir, 2020, 36(34), 10069-10073.
[http://dx.doi.org/10.1021/acs.langmuir.0c01170] [PMID: 32787124]
[46]
Guan, M.; Guo, W.; Gao, L.; Tang, Y.; Hu, J.; Dong, Y. Investigation on the temperature difference method for producing nanobubbles and their physical properties. ChemPhysChem, 2012, 13(8), 2115-2118.
[http://dx.doi.org/10.1002/cphc.201100912] [PMID: 22505224]
[47]
Hao, R.; Fan, Y.; Howard, M.D.; Vaughan, J.C.; Zhang, B. Imaging nanobubble nucleation and hydrogen spillover during electrocatalytic water splitting. Proc. Natl. Acad. Sci. USA, 2018, 115(23), 5878-5883.
[http://dx.doi.org/10.1073/pnas.1800945115] [PMID: 29784824]
[48]
Nazari, Sabereh Recent developments in generation, detection and application of nanobubbles in flotation. Minerals, 2022, 12(4), 462.
[http://dx.doi.org/10.3390/min12040462]
[49]
Postnikov, A.V.; Uvarov, I.V.; Penkov, N.V.; Svetovoy, V.B. Collective behavior of bulk nanobubbles produced by alternating polarity electrolysis. Nanoscale, 2018, 10(1), 428-435.
[http://dx.doi.org/10.1039/C7NR07126D] [PMID: 29226935]
[50]
Hao, R.; Fan, Y.; Anderson, T.J.; Zhang, B. Imaging single nanobubbles of H2 and O2 during the overall water electrolysis with single-molecule fluorescence microscopy. Anal. Chem., 2020, 92(5), 3682-3688.
[http://dx.doi.org/10.1021/acs.analchem.9b04793] [PMID: 32024359]
[51]
Ranaweera, R.; Luo, L. Electrochemistry of nanobubbles. Curr. Opin. Electrochem., 2020, 22, 102-109.
[http://dx.doi.org/10.1016/j.coelec.2020.04.019]
[52]
Zhang, F.; Sun, L.; Yang, H.; Gui, X.; Schönherr, H.; Kappl, M.; Cao, Y.; Xing, Y. Recent advances for understanding the role of nanobubbles in particles flotation. Adv. Colloid Interface Sci., 2021, 291, 102403.
[http://dx.doi.org/10.1016/j.cis.2021.102403] [PMID: 33780858]
[53]
Theodorakis, P.E.; Che, Z. Surface nanobubbles: Theory, simulation, and experiment. A review. Adv. Colloid Interface Sci., 2019, 272, 101995.
[http://dx.doi.org/10.1016/j.cis.2019.101995] [PMID: 31394435]
[54]
Vu, Tri; Razansky, Daniel; Yao, Junjie Listening to tissues with new light: Recent technological advances in photoacoustic imaging. J. Opt., 2019, 21(10), 103001.
[http://dx.doi.org/10.1088/2040-8986/ab3b1a]
[55]
Ou, H.; Li, J.; Chen, C.; Gao, H.; Xue, X.; Ding, D. Organic/polymer photothermal nanoagents for photoacoustic imaging and photothermal therapy in vivo. Sci. China Mater., 2019, 62(11), 1740-1758.
[http://dx.doi.org/10.1007/s40843-019-9470-3]
[56]
Piperno, A.; Sciortino, M.T.; Giusto, E.; Montesi, M.; Panseri, S.; Scala, A. Recent advances and challenges in gene delivery mediated by polyester-based nanoparticles. Int. J. Nanomedicine, 2021, 16, 5981-6002.
[http://dx.doi.org/10.2147/IJN.S321329] [PMID: 34511901]
[57]
Wu, R.; Yang, X.; Li, X.; Dong, N.; Liu, Y.; Zhang, P. Nanobubbles for tumors: Imaging and drug carriers. J. Drug Deliv. Sci. Technol., 2021, 65, 102749.
[http://dx.doi.org/10.1016/j.jddst.2021.102749]
[58]
Shang, M.; Sun, X.; Guo, L.; Shi, D.; Liang, P.; Meng, D.; Zhou, X.; Liu, X.; Zhao, Y.; Li, J. pH-and ultrasound-responsive paclitaxel-loaded carboxymethyl chitosan nanodroplets for combined imaging and synergistic chemoradiotherapy. Int. J. Nanomedicine, 2020, 15, 537-552.
[http://dx.doi.org/10.2147/IJN.S233669] [PMID: 32021193]
[59]
Liu, J.; Shang, T.; Wang, F.; Cao, Y.; Hao, L.; Ren, J.; Ran, H.; Wang, Z.; Li, P.; Du, Z. Low-intensity focused ultrasound (LIFU)-induced acoustic droplet vaporization in phase-transition perfluoropentane nanodroplets modified by folate for ultrasound molecular imaging. Int. J. Nanomedicine, 2017, 12, 911-923.
[http://dx.doi.org/10.2147/IJN.S122667] [PMID: 28184161]
[60]
Wang, J.; Barback, C.V.; Ta, C.N.; Weeks, J.; Gude, N.; Mattrey, R.F.; Blair, S.L.; Trogler, W.C.; Lee, H.; Kummel, A.C. Extended lifetime in vivo pulse stimulated ultrasound imaging. IEEE Trans. Med. Imaging, 2018, 37(1), 222-229.
[http://dx.doi.org/10.1109/TMI.2017.2740784] [PMID: 28829305]
[61]
Wu, Jianrong A multifunctional biodegradable nanocomposite for cancer theranostics. Adv. Sci., 2019, 6(14), 1802001.
[http://dx.doi.org/10.1002/advs.201802001]
[62]
Li, Chunxiao Light‐responsive biodegradable nanorattles for cancer theranostics. Adv. Mater., 2018, 308, 1706150.
[http://dx.doi.org/10.1002/adma.201706150]
[63]
Hysi, E.; Fadhel, M.N.; Wang, Y.; Sebastian, J.A.; Giles, A.; Czarnota, G.J.; Exner, A.A.; Kolios, M.C. Photoacoustic imaging biomarkers for monitoring biophysical changes during nanobubble-mediated radiation treatment. Photoacoustics, 2020, 20, 100201.
[http://dx.doi.org/10.1016/j.pacs.2020.100201] [PMID: 32775198]
[64]
Kooiman, K.; Roovers, S.; Langeveld, S.A.G.; Kleven, R.T.; Dewitte, H.; O’Reilly, M.A.; Escoffre, J.M.; Bouakaz, A.; Verweij, M.D.; Hynynen, K.; Lentacker, I.; Stride, E.; Holland, C.K. Ultrasound-responsive cavitation nuclei for therapy and drug delivery. Ultrasound Med. Biol., 2020, 46(6), 1296-1325.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2020.01.002] [PMID: 32165014]
[65]
Power, S.; Slattery, M.M.; Lee, M.J. Nanotechnology and its relationship to interventional radiology. part II: Drug delivery, thermotherapy, and vascular intervention. Cardiovasc. Intervent. Radiol., 2011, 34(4), 676-690.
[http://dx.doi.org/10.1007/s00270-010-9967-y] [PMID: 20845040]
[66]
Hysi, E. Radiation-enhanced nanobubble therapy: Monitoring treatment effects using photoacoustic imaging. 2019 IEEE International Ultrasonics Symposium (IUS)., Glasgow, UK, 06-09 Oct, 2019
[http://dx.doi.org/10.1109/ULTSYM.2019.8925876]
[67]
Cheng, B.; Bing, C.; Xi, Y.; Shah, B.; Exner, A.A.; Chopra, R. Influence of nanobubble concentration on blood-brain barrier opening using focused ultrasound under real-time acoustic feedback control. Ultrasound Med. Biol., 2019, 45(8), 2174-2187.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2019.03.016] [PMID: 31072657]
[68]
Du, Jing Preparation and imaging investigation of dual-targeted C3F8-filled PLGA nanobubbles as a novel ultrasound contrast agent for breast cancer. Sci. Rep., 2018, 8(1), 3887.
[http://dx.doi.org/10.1038/s41598-018-21502-x]
[69]
Ding, Y.; Cao, Q.; Qian, S.; Chen, X.; Xu, Y.; Chen, J.; Shen, H. Optimized anti–prostate‐specific membrane antigen single‐chain variable fragment–loaded nanobubbles as a novel targeted ultrasound contrast agent for the diagnosis of prostate cancer. J. Ultrasound Med., 2020, 39(4), 761-773.
[http://dx.doi.org/10.1002/jum.15155] [PMID: 31702068]
[70]
Chan, M.H.; Chen, W.; Li, C.H.; Fang, C.Y.; Chang, Y.C.; Wei, D.H.; Liu, R.S.; Hsiao, M. An advanced in situ magnetic resonance imaging and ultrasonic theranostics nanocomposite platform: Crossing the blood-brain barrier and improving the suppression of glioblastoma using iron-platinum nanoparticles in nanobubbles. ACS Appl. Mater. Interfaces, 2021, 13(23), 26759-26769.
[http://dx.doi.org/10.1021/acsami.1c04990] [PMID: 34076419]
[71]
Alam, M.A.; Al Riyami, K. Shear strengthening of reinforced concrete beam using natural fibre reinforced polymer laminates. Constr. Build. Mater., 2018, 162, 683-696.
[http://dx.doi.org/10.1016/j.conbuildmat.2017.12.011]
[72]
Yang, M.; Zhang, N.; Zhang, T.; Yin, X.; Shen, J. Fabrication of doxorubicin-gated mesoporous polydopamine nanoplatforms for multimode imaging-guided synergistic chemophotothermal therapy of tumors. Drug Deliv., 2020, 27(1), 367-377.
[http://dx.doi.org/10.1080/10717544.2020.1730523] [PMID: 32091284]
[73]
Chen, S.; Liu, Y.; Zhu, S.; Chen, C.; Xie, W.; Xiao, L.; Zhu, Y.; Hao, L.; Wang, Z.; Sun, J.; Chang, S. Dual-mode imaging and therapeutic effects of drug-loaded phase-transition nanoparticles combined with near-infrared laser and low-intensity ultrasound on ovarian cancer. Drug Deliv., 2018, 25(1), 1683-1693.
[http://dx.doi.org/10.1080/10717544.2018.1507062] [PMID: 30343601]
[74]
Ben, O. The dose threshold for nanoparticle tumour delivery. Nat. Mater., 2020, 19(12), 1362-1371.
[75]
Wang, Y.; Lan, M.; Shen, D.; Fang, K.; Zhu, L.; Liu, Y.; Hao, L.; Li, P. Targeted nanobubbles carrying indocyanine green for ultrasound, photoacoustic and fluorescence imaging of prostate cancer. Int. J. Nanomedicine, 2020, 15, 4289-4309.
[http://dx.doi.org/10.2147/IJN.S243548] [PMID: 32606678]
[76]
Perera, R.H.; de Leon, A.; Wang, X.; Wang, Y.; Ramamurthy, G.; Peiris, P.; Abenojar, E.; Basilion, J.P.; Exner, A.A. Real time ultrasound molecular imaging of prostate cancer with PSMA-targeted nanobubbles. Nanomedicine, 2020, 28, 102213.
[http://dx.doi.org/10.1016/j.nano.2020.102213] [PMID: 32348874]
[77]
Zhang, J.; Chen, Y.; Deng, C.; Zhang, L.; Sun, Z.; Wang, J.; Yang, Y.; Lv, Q.; Han, W.; Xie, M. The optimized fabrication of a novel nanobubble for tumor imaging. Front. Pharmacol., 2019, 10, 610.
[http://dx.doi.org/10.3389/fphar.2019.00610] [PMID: 31214033]
[78]
Duan, S.; Guo, L.; Shi, D.; Shang, M.; Meng, D.; Li, J. Development of a novel folate-modified nanobubbles with improved targeting ability to tumor cells. Ultrason. Sonochem., 2017, 37, 235-243.
[http://dx.doi.org/10.1016/j.ultsonch.2017.01.013] [PMID: 28427629]
[79]
Gao, Y.; Hernandez, C.; Yuan, H.X.; Lilly, J.; Kota, P.; Zhou, H.; Wu, H.; Exner, A.A. Ultrasound molecular imaging of ovarian cancer with CA-125 targeted nanobubble contrast agents. Nanomedicine, 2017, 13(7), 2159-2168.
[http://dx.doi.org/10.1016/j.nano.2017.06.001] [PMID: 28603079]
[80]
VanOsdol, J.; Ektate, K.; Ramasamy, S.; Maples, D.; Collins, W.; Malayer, J.; Ranjan, A. Sequential HIFU heating and nanobubble encapsulation provide efficient drug penetration from stealth and temperature sensitive liposomes in colon cancer. J. Control. Release, 2017, 247, 55-63.
[http://dx.doi.org/10.1016/j.jconrel.2016.12.033] [PMID: 28042085]
[81]
Perera, R.H.; Hernandez, C.; Zhou, H.; Kota, P.; Burke, A.; Exner, A.A. Ultrasound imaging beyond the vasculature with new generation contrast agents. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2015, 7(4), 593-608.
[http://dx.doi.org/10.1002/wnan.1326] [PMID: 25580914]
[82]
de Leon, A.; Perera, R.; Hernandez, C.; Cooley, M.; Jung, O.; Jeganathan, S.; Abenojar, E.; Fishbein, G.; Sojahrood, A.J.; Emerson, C.C.; Stewart, P.L.; Kolios, M.C.; Exner, A.A. Contrast enhanced ultrasound imaging by nature-inspired ultrastable echogenic nanobubbles. Nanoscale, 2019, 11(33), 15647-15658.
[http://dx.doi.org/10.1039/C9NR04828F] [PMID: 31408083]
[83]
Wu, H.; Abenojar, E.C.; Perera, R.; De Leon, A.C.; An, T.; Exner, A.A. Time-intensity-curve analysis and tumor extravasation of nanobubble ultrasound contrast agents. Ultrasound Med. Biol., 2019, 45(9), 2502-2514.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2019.05.025] [PMID: 31248638]
[84]
Pellow, Carly Threshold-dependent nonlinear scattering from porphyrin nanobubbles for vascular and extravascular applications. Phys. Med. Biol., 2018, 63(21), 215001.
[http://dx.doi.org/10.1088/1361-6560/aae571]
[85]
Jafari, S. Theoretical and experimental investigation of the nonlinear dynamics of nanobubbles excited at clinically relevant ultrasound frequencies and pressures: The role oflipid shell buckling. 2017 IEEE International Ultrasonics Symposium (IUS)., Washington, DC, USA, 06-09 Sep, 2017
[86]
Miller, K.D.; Nogueira, L.; Mariotto, A.B.; Rowland, J.H.; Yabroff, K.R.; Alfano, C.M.; Jemal, A.; Kramer, J.L.; Siegel, R.L. Cancer treatment and survivorship statistics, 2019. CA Cancer J. Clin., 2019, 69(5), 363-385.
[http://dx.doi.org/10.3322/caac.21565] [PMID: 31184787]
[87]
Ramazanov, M.; Karimova, A.; Shirinova, H. Magnetism for drug delivery, MRI and hyperthermia applications: A review. Biointerface Res. Appl. Chem., 2021, 11, 8654-8668.
[88]
Gao, Y.; Ma, Q.; Cao, J.; Shi, Y.; Wang, J.; Ma, H.; Sun, Y.; Song, Y. Bifunctional alginate/chitosan stabilized perfluorohexane nanodroplets as smart vehicles for ultrasound and pH responsive delivery of anticancer agents. Int. J. Biol. Macromol., 2021, 191, 1068-1078.
[http://dx.doi.org/10.1016/j.ijbiomac.2021.09.166] [PMID: 34600955]
[89]
Zhang, L.; Yin, T.; Li, B.; Zheng, R.; Qiu, C.; Lam, K.S.; Zhang, Q.; Shuai, X. Size-modulable nanoprobe for high-performance ultrasound imaging and drug delivery against cancer. ACS Nano, 2018, 12(4), 3449-3460.
[http://dx.doi.org/10.1021/acsnano.8b00076] [PMID: 29634240]
[90]
Nakamura, Y.; Mochida, A.; Choyke, P.L.; Kobayashi, H. Nanodrug delivery: Is the enhanced permeability and retention effect sufficient for curing cancer? Bioconjug. Chem., 2016, 27(10), 2225-2238.
[http://dx.doi.org/10.1021/acs.bioconjchem.6b00437] [PMID: 27547843]
[91]
Tosetti, F.; Ferrari, N.; De Flora, S.; Albini, A. ‘Angioprevention’: Angiogenesis is a common and key target for cancer chemopreventive agents. FASEB J., 2002, 16(1), 2-14.
[http://dx.doi.org/10.1096/fj.01-0300rev] [PMID: 11772931]
[92]
Li, H.; Wu, Z.; Zhang, J.; Sun, X.; Duan, F.; Yao, J.; Sun, M.; Zhang, J.; Nie, L. Instant ultrasound-evoked precise nanobubble explosion and deep photodynamic therapy for tumors guided by molecular imaging. ACS Appl. Mater. Interfaces, 2021, 13(18), 21097-21107.
[http://dx.doi.org/10.1021/acsami.1c05517] [PMID: 33908256]
[93]
Gitler, A.D.; Dhillon, P.; Shorter, J. Neurodegenerative disease: Models, mechanisms, and a new hope. Dis. Model. Mech., 2017, 10(5), 499-502.
[http://dx.doi.org/10.1242/dmm.030205] [PMID: 28468935]
[94]
Lee, B.E.; Kim, H.Y.; Kim, H.J.; Jeong, H.; Kim, B.G.; Lee, H.E.; Lee, J.; Kim, H.B.; Lee, S.E.; Yang, Y.R.; Yi, E.C.; Hanover, J.A.; Myung, K.; Suh, P.G.; Kwon, T.; Kim, J.I. O-GlcNAcylation regulates dopamine neuron function, survival and degeneration in Parkinson disease. Brain, 2020, 143(12), 3699-3716.
[http://dx.doi.org/10.1093/brain/awaa320] [PMID: 33300544]
[95]
Kinfe, T.; Stadlbauer, A.; Winder, K.; Hurlemann, R.; Buchfelder, M. Incisionless MR-guided focused ultrasound: Technical considerations and current therapeutic approaches in psychiatric disorders. Expert Rev. Neurother., 2020, 20(7), 687-696.
[http://dx.doi.org/10.1080/14737175.2020.1779590] [PMID: 32511043]
[96]
Yan, Y.; Chen, Y.; Liu, Z.; Cai, F.; Niu, W.; Song, L.; Liang, H.; Su, Z.; Yu, B.; Yan, F. Brain delivery of curcumin through low-intensity ultrasound-induced blood–brain barrier opening via lipid-plga nanobubbles. Int. J. Nanomedicine, 2021, 16, 7433-7447.
[http://dx.doi.org/10.2147/IJN.S327737] [PMID: 34764649]
[97]
Suzuki, R.; Oda, Y.; Omata, D.; Nishiie, N.; Koshima, R.; Shiono, Y.; Sawaguchi, Y.; Unga, J.; Naoi, T.; Negishi, Y.; Kawakami, S.; Hashida, M.; Maruyama, K. Tumor growth suppression by the combination of nanobubbles and ultrasound. Cancer Sci., 2016, 107(3), 217-223.
[http://dx.doi.org/10.1111/cas.12867] [PMID: 26707839]
[98]
Maranhão, R.; Leite, A., Jr Development of anti-atherosclerosis therapy based on the inflammatory and proliferative aspects of the disease. Curr. Pharm. Des., 2015, 21(9), 1196-1204.
[http://dx.doi.org/10.2174/1381612820666141013150714] [PMID: 25312729]
[99]
Dong, L.; Li, N.; Wei, X.; Wang, Y.; Chang, L.; Wu, H.; Song, L.; Guo, K.; Chang, Y.; Yin, Y.; Pan, M.; Shen, Y.; Wang, F. A gambogic acid-loaded delivery system mediated by ultrasound-targeted microbubble destruction: A promising therapy method for malignant cerebral glioma. Int. J. Nanomedicine, 2022, 17, 2001-2017.
[http://dx.doi.org/10.2147/IJN.S344940] [PMID: 35535034]
[100]
Devulapally, R.; Lee, T.; Barghava-Shah, A.; Sekar, T.V.; Foygel, K.; Bachawal, S.V.; Willmann, J.K.; Paulmurugan, R. Ultrasound-guided delivery of thymidine kinase–nitroreductase dual therapeutic genes by PEGylated-PLGA/PEI nanoparticles for enhanced triple negative breast cancer therapy. Nanomedicine, 2018, 13(9), 1051-1066.
[http://dx.doi.org/10.2217/nnm-2017-0328] [PMID: 29790803]
[101]
Tan, J.K.Y.; Pham, B.; Zong, Y.; Perez, C.; Maris, D.O.; Hemphill, A.; Miao, C.H.; Matula, T.J.; Mourad, P.D.; Wei, H.; Sellers, D.L.; Horner, P.J.; Pun, S.H. Microbubbles and ultrasound increase intraventricular polyplex gene transfer to the brain. J. Control. Release, 2016, 231, 86-93.
[http://dx.doi.org/10.1016/j.jconrel.2016.02.003] [PMID: 26860281]
[102]
Manta, S.; Renault, G.; Delalande, A.; Couture, O.; Lagoutte, I.; Seguin, J.; Lager, F.; Houzé, P.; Midoux, P.; Bessodes, M.; Scherman, D.; Bureau, M.F.; Marie, C.; Pichon, C.; Mignet, N. Cationic microbubbles and antibiotic-free miniplasmid for sustained ultrasound–mediated transgene expression in liver. J. Control. Release, 2017, 262, 170-181.
[http://dx.doi.org/10.1016/j.jconrel.2017.07.015] [PMID: 28710005]
[103]
Endo-Takahashi, Yoko Efficient siRNA delivery using novel siRNA-loaded Bubble liposomes and ultrasound. Int. J. Pharm., 2012, 422(1-2), 504-509.
[http://dx.doi.org/10.1016/j.ijpharm.2011.11.023]
[104]
Endo-Takahashi, Yoko; Negishi, Yoichi Microbubbles and nanobubbles with ultrasound for systemic gene delivery. Pharmaceutics, 2020, 12(10), 964.
[http://dx.doi.org/10.3390/pharmaceutics12100964]
[105]
Song, Z.; Ye, Y.; Zhang, Z.; Shen, J.; Hu, Z.; Wang, Z.; Zheng, J. Noninvasive, targeted gene therapy for acute spinal cord injury using LIFU-mediated BDNF-loaded cationic nanobubble destruction. Biochem. Biophys. Res. Commun., 2018, 496(3), 911-920.
[http://dx.doi.org/10.1016/j.bbrc.2018.01.123] [PMID: 29360450]
[106]
Zhou, Q.; Deng, Q.; Hu, B.; Wang, Y.J.; Chen, J.L.; Cui, J.J.; Cao, S.; Song, H.N. Ultrasound combined with targeted cationic microbubble-mediated angiogenesis gene transfection improves ischemic heart function. Exp. Ther. Med., 2017, 13(5), 2293-2303.
[http://dx.doi.org/10.3892/etm.2017.4270] [PMID: 28565841]
[107]
Belcik, J.T.; Davidson, B.P.; Xie, A.; Wu, M.D.; Yadava, M.; Qi, Y.; Liang, S.; Chon, C.R.; Ammi, A.Y.; Field, J.; Harmann, L.; Chilian, W.M.; Linden, J.; Lindner, J.R. Augmentation of muscle blood flow by ultrasound cavitation is mediated by ATP and purinergic signaling. Circulation, 2017, 135(13), 1240-1252.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.116.024826] [PMID: 28174191]
[108]
Li, Hairui Diagnostic ultrasound and microbubbles treatment improves outcomes of coronary no-reflow in canine models by sonothrombolysis. Crit. Care Med., 2018, 46(9), e912.
[http://dx.doi.org/10.1097/CCM.0000000000003255]
[109]
Wang, C-H. Method and device for producing optimized lipidbased micro/nano-bubbles. U.S. Patent 9687570B2, 2022.
[110]
Hernandez, A.E.P. Stabilized crosslinked nanobubbles for diagnostic and therapeutic applications. W.O. Patent 2017210612A1, 2022.
[111]
Shailubhai, V.P. Compositions and method for the treatment and detection of colon cancer. C.A. Patent 3001727A1, 2022.
[112]
Wu, D.L. Multifunctional chemo- and mechanical therapeutics. W.O. Patent 2015163841A9, 2022.
[113]
Ultrasound-driven drug delivery platforms by the use of nanobubbles water prepared with drug-conjugated phospholipids via ester bonds and preparation method thereof. K.R. Patent 20200105299A, 2022.
[114]
Durmaz, M.E-S.Y.Y. Polymeric nanoparticles for ultrasound imaging and therapy. U.S. Patent 9415123B2, 2022.
[115]
Nittayacharn, A.E. Stabilized nanobubbles and microbubbles for diagnostic and therapeutic applications. E.P. Patent 3773752A1, 2022.
[116]
Oxford, U.o. Do Nanobubbles Improve Joint Hypoxia? N.C. Patent T04844008, 2022.
[117]
University of California. Micro/Nanobubbles (MNBs) for Treatment of Acute and Chronic Wounds. N.C. Patent T05169814, 2022.
[118]
Medicine, L.S. Feasibility of the vapor nanobubble technology for malaria diagnostics (malariasense). N.C. Patent T02672228, 2022.
[119]
Carolina, M.U.S. CEUS for intraoperative spinal cord injury. N.C. Patnet T05530798, 2022.
[120]
Research, M.N. The effect of RNS60 on ALS Biomarkers (RNS60). N.C. Patent T03456882, 2022.
[121]
Wang, Ye Preparation of nanobubbles for ultrasound imaging and intracelluar drug delivery. Int. J. Pharm., 2010, 384(1-2), 148-153.
[http://dx.doi.org/10.1016/j.ijpharm.2009.09.027]
[122]
Jin, J.; Yang, L.; Chen, F.; Gu, N. Drug delivery system based on nanobubbles. Interdiscip. Mater., 2022, 1(4), 471-494.
[http://dx.doi.org/10.1002/idm2.12050]
[123]
Babu, K.S.; Amamcharla, J.K. Generation methods, stability, detection techniques, and applications of bulk nanobubbles in agro-food industries: A review and future perspective. Crit. Rev. Food Sci. Nutr., 2022, 1-20.
[http://dx.doi.org/10.1080/10408398.2022.2067119] [PMID: 35467989]
[124]
Gupta, Vaibhav Nanotechnology in cosmetics and cosmeceuticals-A review of latest advancements. Gels, 2022, 8(3), 173.
[http://dx.doi.org/10.3390/gels8030173]
[125]
Alheshibri, M.; Craig, V.S.J. Differentiating between nanoparticles and nanobubbles by evaluation of the compressibility and density of nanoparticles. J. Phys. Chem. C, 2018, 122(38), 21998-22007.
[http://dx.doi.org/10.1021/acs.jpcc.8b07174]
[126]
Younis, S.A.; Kim, K-H.; Shaheen, S.M.; Antoniadis, V.; Tsang, Y.F.; Rinklebe, J.; Deep, A.; Brown, R.J.C. Advancements of nanotechnologies in crop promotion and soil fertility: Benefits, life cycle assessment, and legislation policies. Renew. Sustain. Energy Rev., 2021, 152, 111686.
[http://dx.doi.org/10.1016/j.rser.2021.111686]

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