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Current Pharmaceutical Design


ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Photo- and Sono-Dynamic Therapy: A Review of Mechanisms and Considerations for Pharmacological Agents Used in Therapy Incorporating Light and Sound

Author(s): Yanye Yang, Juan Tu*, Dongxin Yang, Jason L. Raymond*, Ronald A. Roy and Dong Zhang

Volume 25 , Issue 4 , 2019

Page: [401 - 412] Pages: 12

DOI: 10.2174/1381612825666190123114107

Price: $65


As irreplaceable energy sources of minimally invasive treatment, light and sound have, separately, laid solid foundations in their clinic applications. Constrained by the relatively shallow penetration depth of light, photodynamic therapy (PDT) typically involves involves superficial targets such as shallow seated skin conditions, head and neck cancers, eye disorders, early-stage cancer of esophagus, etc. For ultrasound-driven sonodynamic therapy (SDT), however, to various organs is facilitated by the superior... transmission and focusing ability of ultrasound in biological tissues, enabling multiple therapeutic applications including treating glioma, breast cancer, hematologic tumor and opening blood-brain-barrier (BBB). Considering the emergence of theranostics and precision therapy, these two classic energy sources and corresponding sensitizers are worth reevaluating. In this review, three typical therapies using light and sound as a trigger, PDT, SDT, and combined PDT and SDT are introduced. The therapeutic dynamics and current designs of pharmacological sensitizers involved in these therapies are presented. By introducing both the history of the field and the most up-to-date design strategies, this review provides a systemic summary on the development of PDT and SDT and fosters inspiration for researchers working on ‘multi-modal’ therapies involving light and sound.

Keywords: Photodynamic therapy, sonodynamic therapy, sono-photodynamic therapy, perfluorocarbon, photosensitizer, sonosensitier, ultrasound contrast agents.

Kennedy J. High-intensity focused ultrasound in the treatment of solid tumours. Nat Rev Cancer 2005; 5(4): 321-7.
Nikfarjam M, Christophi C. Interstitial laser thermotherapy for liver tumours. Br J Surg 2003; 90(9): 1033-47.
Lismont M, Dreesen L, Wuttke S. Metal-organic framework nanoparticles in photodynamic therapy: current status and perspectives. Adv Funct Mater 2017; 27(14): 1606314.
Dolmans D, Fukumura D, Jain R. Photodynamic therapy for cancer. Nat Rev Cancer 2003; 3(5): 380-7.
Nesi-Reis V, Lera-Nonose D, Oyama J, et al. Contribution of photodynamic therapy in wound healing: a systematic review. Photodiagn Photodyn Ther 2018; 21: 294-305.
Wen X, Li Y, Hamblin MR. Photodynamic therapy in dermatology beyond non-melanoma cancer: An update. Photodiagn Photodyn Ther 2017; 19: 140-52.
Bashkatov AN, Genina EA, Kochubey VI, Tuchin VV. Optical properties of human skin, subcutaneous and mucous tissues in the wavelength range from 400 to 2000 nm. J Phys D Appl Phys 2005; 38(15): 2543-55.
Mironova KE, Proshkina GM, Ryabova AV, et al. Genetically Encoded Immunophotosensitizer 4D5scFv-miniSOG is a Highly Selective Agent for Targeted Photokilling of Tumor Cells in vitro. Theranostics 2013; 3(11): 831-40.
Grebenik EA, Kostyuk AB, Deyev SM. Upconversion nanoparticles and their hybrid assemblies for biomedical applications. Russ Chem Rev 2016; 85(12): 1277-96.
Yumita N, Nishigaki R, Umemura K, Umemura SI. Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Jpn J Cancer Res 1989; 80(3): 219-22.
Yumita NN, Nishigaki R, Umemura K, Umemura S. Synergistic Effect of Ultrasound and Hematoporphyrin on Sarcoma 180. Jpn J Cancer Res 1990; 81(3): 304-8.
Jin ZH, Miyoshi N, Ishiguro K, et al. Combination effect of photodynamic and sonodynamic therapy on experimental skin squamous cell carcinoma in C3H/HeN mice. J Dermatol 2000; 27(5): 294-306.
Tserkovsky DA, Alexandrova EN, Chalau VN, Istomin YP. Effects of combined sonodynamic and photodynamic therapies with photolon on a glioma C6 tumor model. Exp Oncol 2012; 34(4): 332-5.
Sirsi SR, Borden MA. Advances in ultrasound mediated gene therapy using microbubble contrast agents. Theranostics 2012; 2(12): 1208-22.
Wu Y, Lu CT, Li WF, et al. Preparation and antitumor activity of bFGF-mediated active targeting doxorubicin microbubbles. Drug Dev Ind Pharm 2013; 39(11): 1712-9.
Abrahamse H, Hamblin MR. New photosensitizers for photodynamic therapy. Biochem J 2016; 473(4): 347-64.
van Straten D, Mashayekhi V, de Bruijn H, et al. Oncologic photodynamic therapy: basic principles, current clinical status and future directions. Cancers (Basel) 2017; 9(2): 19.
Castano AP, Demidova TN, Hamblin MR. Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization. Photodiagn Photodyn Ther 2004; 1(4): 279-93.
Castano AP, Demidova TN, Hamblin MR. Mechanisms in photodynamic therapy: part two-cellular signaling, cell metabolism and modes of cell death. Photodiagn Photodyn Ther 2005; 2(1): 1-23.
Lafond M, Yoshizawa S, Umemura SI. Sonodynamic therapy: advances and challenges in clinical translation. J Ultrasound Med 2018; 1-14.
Pan X, Wang H, Wang S, et al. Sonodynamic therapy (SDT): a novel strategy for cancer nanotheranostics. Sci China Life Sci 2018; 61(4): 415-26.
Rengeng L, Qianyu Z, Yuehong L, et al. Sonodynamic therapy, a treatment developing from photodynamic therapy. Photodiagn Photodyn Ther 2017; 19: 159-66.
Wang X, Jia Y, Wang P, et al. Current status and future perspectives of sonodynamic therapy in glioma treatment. Ultrason Sonochem 2017; 37: 592-9.
Liu Y, Wang P, Liu Q, Wang X. Sinoporphyrin sodium triggered sono-photodynamic effects on breast cancer both in vitro and in vivo. Ultrason Sonochem 2016; 31: 437-48.
Saito M, Iida T, Nagayama D. Photodynamic therapy with verteporfin for age-related macular degeneration or polypoidal choroidal vasculopathy: comparison of the presence of serous retinal pigment epithelial detachment. Br J Ophthalmol 2008; 92(12): 1642-7.
Shavkuta BS, Gerasimov MY, Minaev NV, et al. Highly effective 525 nm femtosecond laser crosslinking of collagen and strengthening of a human donor cornea. Laser Phys Lett 2018; 15(1): 015602.
Robertson CA, Evans DH, Abrahamse H. Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT. J Photochem Photobiol B 2009; 96(1): 1-8.
Juzeniene A, Moan J. The history of PDT in Norway Part one: Identification of basic mechanisms of general PDT. Photodiagn Photodyn Ther 2007; 4(1): 3-11.
Agostinis PBE, Breyssens H. Regulatory pathways in photodynamic therapy induced apoptosis. In: 10th Congress of the European-Society-for-Photobiology. Vienna, Austria. Photochem Photobiol Sci 2004; 3(8): 721-9.
Li X, Kolemen S, Yoon J, Akkaya EU. Activatable photosensitizers: agents for selective photodynamic therapy. Adv Funct Mater 2017; 27(5): 1604053.
Fan W, Huang P, Chen X. Overcoming the Achilles’ heel of photodynamic therapy. Chem Soc Rev 2016; (45): 6488-519.
Tian J, Zhou J, Shen Z, Ding L, Yu J-S, Ju H. A pH-activatable and aniline-substituted photosensitizer for near-infrared cancer theranostics. Chem Sci 2015; (6): 5969-77.
Battogtokh GK, Ko YT. Active-targeted pH-responsive albumin-photosensitizer conjugate nanoparticles as theranostic agents. J Mater Chem B 2015; 3(48): 9349-59.
Cottrell WJ, Paquette AD, Keymel KR, et al. Irradiance-dependent photobleaching and pain in delta-aminolevulinic acid-photodynamic therapy of superficial basal cell carcinomas. Clin Cancer Res 2008; (14): 4475-83.
Foster TH, Murant RS, Bryant RG, Knox RS, Gibson SL, Hilf R. Oxygen consumption and diffusion effects in photodynamic therapy. Radiat Res 1991; 126(3): 296-303.
Wang W, Moriyama LT, Bagnato VS. Photodynamic therapy induced vascular damage: an overview of experimental PDT. Laser Phys Lett 2013; 10: 023001.
Sitnik TH. BW. The effect of fluence rate on tumor and normal tissue responses to photodynamic therapy. Photochem Photobiol 1998; 67: 462-6.
Sitnik TH, Hampton JA, Henderson BW. Reduction of tumour oxygenation during and after photodynamic therapy in vivo: effects of fluence rate. Br J Cancer 1998; 77: 1386-94.
Song. C. W. SA, Osborn J. L., & Iwata K. Tumour oxygenation is increased by hyperthermia at mild temperatures. Int J Hyperthermia 2009; 25: 91-5.
Bolfarini GC, Siqueira-Moura MP, Demets GJF, et al. In vitro evaluation of combined hyperthermia and photodynamic effects using magnetoliposomes loaded with cucurbituril zinc phthalocyanine complex on melanoma. J Photochem Photobiol B 2012; 115: 1-4.
Di Corato R, Béalle G, Kolosnjaj-Tabi J, et al. Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes. ACS Nano 2015; 9: 2904-16.
Matzi V, Maier A, Sankin O, et al. Photodynamic therapy enhanced by hyperbaric oxygenation in palliation of malignant pleural mesothelioma: clinical experience. Photodiagn Photodyn Ther 2004; 1: 57-64.
Chen Q, Huang Z, Chen H, et al. Improvement of tumor response by manipulation of tumor oxygenation during photodynamic therapy. Photochem Photobiol 2002; 76: 197-203.
Day RA, Estabrook DA, Logan JK, Sletten EM. Fluorous photosensitizers enhance photodynamic therapy with perfluorocarbon nanoemulsions. Chem Commun (Camb) 2017; 53: 13043-6.
Cheng Y, Cheng H, Jiang C, et al. Perfluorocarbon nanoparticles enhance reactive oxygen levels and tumour growth inhibition in photodynamic therapy. Nat Commun 2015; 6: 8785.
Clark L, Gollan F. Survival of mammals breathing organic liquids equilibrated with oxygen at atmospheric pressure. Science 1966; 152(3730): 1755-6.
Castro CI, Briceno JC. Perfluorocarbon-based oxygen carriers: review of products and trials. Artif Organs 2010; 34(8): 622-34.
Jahr J, Walker V, Manoochehri K. Blood substitutes as pharmacotherapies in clinical practice. Curr Opin Anaesthesiol 2007; 20: 325-30.
Fingar VHMT, Henderson BW. Modification of photodynamic therapy-induced hypoxia by fluosol-DA (20%) and carbogen breathing in mice. Cancer Res 1988; 48: 3350-4.
Wang YG, Kim H, Mun S, et al. Indocyanine green-loaded perfluorocarbon nanoemulsions for bimodal (19)F-magnetic resonance/nearinfrared fluorescence imaging and subsequent phototherapy. Quant Imaging Med Surg 2013; 3: 132-40.
Ren H, Liu J, Su F, et al. Relighting photosensitizers by synergistic integration of albumin and perfluorocarbon for enhanced photodynamic therapy. ACS Appl Mater Interfaces 2017; 9: 3463-73.
Sheng D, Liu T, Deng L, et al. Perfluorooctyl bromide & indocyanine green co-loaded nanoliposomes for enhanced multimodal imaging-guided phototherapy. Biomaterials 2018; 165: 1-13.
Wang J, Liu L, You Q, et al. All-in-one theranostic nanoplatform based on hollow MoSx for photothermally-maneuvered oxygen self-enriched photodynamic therapy. Theranostics 2018; 8: 955-71.
Song X, Feng L, Liang C, et al. Ultrasound triggered tumor oxygenation with oxygen-shuttle nanoperfluorocarbon to overcome hypoxia-associated resistance in cancer therapies. Nano Lett 2016; 16: 6145-53.
Chen H, Zhou X, Gao Y, et al. Recent progress in development of new sonosensitizers for sonodynamic cancer therapy. Drug Discov Today 2014; 19: 502-9.
Tachibana K, Feril Jr L.B., Ikeda-Dantsuji Y. Sonodynamic therapy. Ultrasonics 2008; 48(4): 253-9.
Rosenthal I, Sostaric JZ, Riesz P. Sonodynamic therapy--a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem 2004; 11(6): 349-63.
Hirschberg H, Madsen S. Synergistic efficacy of ultrasound, sonosensitizers and chemotherapy: a review. Ther Deliv 2017; 8(5): 331-42.
Chen J, Luo H, Liu Y, et al. Oxygen-self-produced nanoplatform for relieving hypoxia and breaking resistance to sonodynamic treatment of pancreatic cancer. ACS Nano 2017; 11(12): 12849-62.
Ju D, Yamaguchi F, Zhan G, et al. Hyperthermotherapy enhances antitumor effect of 5-aminolevulinic acid-mediated sonodynamic therapy with activation of caspase-dependent apoptotic pathway in human glioma. Tumour Biol 2016; 37: 10415-26.
Umemura SYN, Nishigaki R, Umemura K. Mechanism of cell damage by ultrasound in combination with hematoporphyrin. Jpn J Cancer Res 1990; 81: 962-6.
Kessel DJR, Fowlkes JB, Cain C. Porphyrin-induced enhancement of ultrasound cytotoxicity. Int J Radiat Biol 1994; 66: 221-8.
Tang W, Liu Q, Zhang J, et al. In vitro activation of mitochondria-caspase signaling pathway in sonodynamic therapy-induced apoptosis in sarcoma 180 cells. Ultrasonics 2010; 50: 567-76.
Li JH, Song DY, Xu YG, et al. In vitro study of haematoporphyrin monomethyl ether-mediated sonodynamic effects on C6 glioma cells. Neurol Sci 2008; 29: 229-35.
Su X, Wang P, Wang X, et al. Apoptosis of U937 cells induced by hematoporphyrin monomethyl ether-mediated sonodynamic action. Cancer Biother Radiopharm 2013; 28: 207-17.
Feng Q, Zhang W, Yang X, et al. pH/Ultrasound dual-responsive gas generator for ultrasound imaging-guided therapeutic inertial cavitation and sonodynamic therapy. Adv Healthc Mater 2017; 7(5): Epub
Yan S, Lu M, Ding X, et al. HematoPorphyrin monomethyl ether polymer contrast agent for ultrasound/photoacoustic dual-modality imaging-guided synergistic high intensity focused ultrasound (HIFU) therapy. Sci Rep 2016; 6: 31833.
Su X, Wang X, Zhang K, et al. Sonodynamic therapy induces apoptosis of human leukemia HL-60 cells in the presence of protoporphyrin IX. Gen Physiol Biophys 2016; 35(2): 155-64.
Huang P, Qian X, Chen Y, et al. Metalloporphyrin-encapsulated biodegradable nanosystems for highly efficient magnetic resonance imaging-guided sonodynamic cancer therapy. J Am Chem Soc 2017; 139: 1275-84.
Umemura KY. N; Nishigaki, R; Umemura, Si. Sonodynamically induced antitumor effect of pheophorbide a. Cancer Lett 1996; 102: 151-7.
Xu ZY, Wang K, Li XQ, et al. The ABCG2 transporter is a key molecular determinant of the efficacy of sonodynamic therapy with Photofrin in glioma stem-like cells. Ultrasonics 2013; 53: 232-8.
Yumita NNR, Umemura S. Sonodynamically induced antitumor effect of Photofrin II on colon 26 carcinoma. J Cancer Res Clin Oncol 2000; 126: 601-6.
Tachibana K, Kimura N, Okumura M, Eguchi H, Tachibana S. Enhancement of cell killing of HL-60 cells by ultrasound in the presence of the photosensitizing drug Photofrin II. Cancer Lett 1993; 72(3): 195-9.
Yumita N, Okudaira K, Momose Y, Umemura S. Sonodynamically induced apoptosis and active oxygen generation by gallium-porphyrin complex, ATX-70. Cancer Chemother Pharmacol 2010; 66: 1071-8.
Umemura Si. Yumita NN, R. Enhancement of ultrasonically induced cell damage by a gallium-porphyrin complex, ATX-70. Jpn J Cancer Res 1993; 84: 582-8.
Abe HKM, Tachibana K. Targeted sonodynamic therapy of cancer using a photosensitizer conjugated with antibody against carcinoembryonic antigen. Anticancer Res 2002; (22): 1575-80.
Yumita NNR, Sakata I. Sonodynamically induced antitumor effect of 4-formyloximethylidene-3-hydroxy-2-vinyl-deuterio-porphynyl(IX)-6,7-diaspartic acid (ATX-S10). Jpn J Cancer Res 2000; 91: 255-60.
Yumita N, Sakata I, Nakajima S, Umemura S. Ultrasonically induced cell damage and active oxygen generation by 4-formyloximeetylidene-3-hydroxyl-2-vinyl-deuterio-porphynyl(IX)-6-7-diaspartic acid: on the mechanism of sonodynamic activation. Biochim Biophys Acta, Gen Subj 2003; 1620(1-3): 179-84.
Yumita N, Han QS, Kitazumi I, Umemura S. Sonodynamically-induced apoptosis, necrosis, and active oxygen generation by mono-l-aspartyl chlorin e6. Cancer Sci 2008; 99(1): 166-72.
Yumita N, Iwase Y, Nishi K, et al. Involvement of reactive oxygen species in sonodynamically induced apoptosis using a novel porphyrin derivative. Theranostics 2012; 2(9): 880-8.
Hachimine K, Shibaguchi H, Kuroki M, et al. Sonodynamic therapy of cancer using a novel porphyrin derivative, DCPH-P-Na(I), which is devoid of photosensitivity. Cancer Sci 2007; 98(6): 916-20.
Yumita NKK, Sasaki K. Sonodynamic effect of erythrosin B on sarcoma 180 cells in vitro. Ultrason Sonochem 2002; 9: 259-65.
Umemura SYN, Umemura K, Nishigaki R. Sonodynamically induced effect of rose bengal on isolated sarcoma 180 cells. Cancer Chemother Pharmacol 1999; 43: 389-93.
Nonaka M, Yamamoto M, Yoshino S, Umemura S, Sasaki K, Fukushima T. Sonodynamic therapy consisting of focused ultrasound and a photosensitizer causes a selective antitumor effect in a rat intracranial glioma model. Anticancer Res 2009; 29(3): 943-50.
Sugita N, Kawabata K, Sasaki K, Sakata I, Umemura S. Synthesis of amphiphilic derivatives of rose bengal and their tumor accumulation. Bioconjug Chem 2007; 18(3): 866-73.
Sugita N, Iwase Y, Yumita N, Ikeda T, Umemura S. Sonodynamically induced cell damage using rose bengal derivative. Anticancer Res 2010; 30(9): 3361-6.
Chen Z, Li J, Song X, Wang Z, Yue W. Use of a novel sonosensitizer in sonodynamic therapy of U251 glioma cells in vitro. Exp Ther Med 2012; (3): 273-8.
Sviridov AP, Andreev VG, Ivanova EM, Osminkina LA, Tamarov KP, Timoshenko VYu. Porous silicon nanoparticles as sensitizers for ultrasonic hyperthermia. Appl Phys Lett 2013; 103: 193110.
Yumita N, Watanabe T, Chen FS, Momose Y, Umemura S. Induction of apoptosis by functionalized fullerene-based sonodynamic therapy in HL-60 cells. Anticancer Res 2016; 36(6): 2665-74.
Qian J, Gao Q. Sonodynamic therapy mediated by emodin induces the oxidation of microtubules to facilitate the sonodynamic effect. Ultrasound Med Biol 2018; 44(4): 853-60.
Gao Q, Wang F, Guo S, et al. Sonodynamic effect of an anti-inflammatory agent--emodin on macrophages. Ultrasound Med Biol 2011; 37(9): 1478-85.
Qian X, Zheng Y, Chen Y. Micro/nanoparticle-augmented sonodynamic therapy (SDT): breaking the depth shallow of photoactivation. Adv Mater 2016; 28(37): 8097-129.
Harada Y, Ogawa K, Irie Y, et al. Ultrasound activation of TiO2 in melanoma tumors. J Control Release 2011; 149(2): 190-5.
Yamaguchi S, Kobayashi H, Narita T, et al. Sonodynamic therapy using water-dispersed TiO2-polyethylene glycol compound on glioma cells: comparison of cytotoxic mechanism with photodynamic therapy. Ultrason Sonochem 2011; 18(5): 1197-204.
Shen S, Wu L, Liu J, et al. Core-shell structured Fe3O4@TiO2-doxorubicin nanoparticles for targeted chemo-sonodynamic therapy of cancer. Int J Pharm 2015; 486(1-2): 380-8.
Shen S, Guo X, Wu L, et al. Dual-core@shell-structured Fe3O4–NaYF4@TiO2 nanocomposites as a magnetic targeting drug carrier for bioimaging and combined chemo-sonodynamic therapy. J Mater Chem B 2014; 2(35): 5775-84.
Lentacker I, De Cock I, Deckers R, et al. Understanding ultrasound induced sonoporation: definitions and underlying mechanisms. Adv Drug Deliv Rev 2014; 72: 49-64.
Ward M, Wu J, Chiu J-F. Ultrasound-induced cell lysis and sonoporation enhanced by contrast agents. J Acoust Soc Am 1999; 105(5): 2951-7.
Lakshmanan S, Gupta GK, Avci P, et al. Physical energy for drug delivery; poration, concentration and activation. Adv Drug Deliv Rev 2014; 71: 98-114.
Wu J, Nyborg WL. Ultrasound, cavitation bubbles and their interaction with cells. Adv Drug Deliv Rev 2008; 60(10): 1103-16.
Kooiman K, Foppen-Harteveld M, van der Steen AF, de Jong N. Sonoporation of endothelial cells by vibrating targeted microbubbles. J Control Release 2011; 154(1): 35-41.
Fan Z, Liu H, Mayer M, Deng CX. Spatiotemporally controlled single cell sonoporation. Proc Natl Acad Sci USA 2012; 109(41): 16486-91.
van Wamel A, Kooiman K, Harteveld M, et al. Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation. J Control Release 2006; 112(2): 149-55.
Fan P, Zhang Y, Guo X, et al. Cell-cycle-specific cellular responses to sonoporation. Theranostics 2017; 7(19): 4894-908.
Hu Y, Wan JM, Yu AC. Membrane perforation and recovery dynamics in microbubble-mediated sonoporation. Ultrasound Med Biol 2013; 39(12): 2393-405.
Spurny P, Oberst J, Heinlein D. Photographic observations of Neuschwanstein, a second meteorite from the orbit of the Pribram chondrite. Nature 2003; 423: 151-3.
Lauterborn W, Kurz T. Physics of bubble oscillations. Rep Prog Phys 2010; 73(10): 106501.
Allen J, Roy R, Church C. On the role of shear viscosity in mediating inertial cavitation from short-pulse, megahertz-frequency ultrasound. IEEE Trans Ultrason Ferroelectr Freq Control 1997; 44(4): 743-51.
Ohl CD, Arora M, Ikink R, et al. Sonoporation from jetting cavitation bubbles. Biophys J 2006; 91(11): 4285-95.
Prentice P, Cuschieri A, Dholakia K, et al. Membrane disruption by optically controlled microbubble cavitation. Nat Phys 2005; 1: 107-10.
Nishikawa M, Huang L. Nonviral vectors in the new millennium: delivery barriers in gene transfer. Hum Gene Ther 2001; 12(8): 861-70.
Lentacker I, De Geest B, Vandenbroucke R, et al. Ultrasound-responsive polymer-coated microbubbles that bind and protect DNA. Langmuir 2006; 22(17): 7273-8.
Frenkel P, 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.
Bekeredjian R, Chen S, Grayburn PA, Shohet RV. Augmentation of cardiac protein delivery using ultrasound targeted microbubble destruction. Ultrasound Med Biol 2005; 31(5): 687-91.
Wilson K, Homan K, Emelianov S. Biomedical photoacoustics beyond thermal expansion using triggered nanodroplet vaporization for contrast-enhanced imaging. Nat Commun 2012; 3: 618.
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.
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.
Haag P, Frauscher F, Gradl J, et al. Microbubble-enhanced ultrasound to deliver an antisense oligodeoxynucleotide targeting the human androgen receptor into prostate tumours. J Steroid Biochem Mol Biol 2006; 102(1-5): 103-13.
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.
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.
Tinkov S, Winter G, Coester C, Bekeredjian R. New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: Part I--Formulation development and in vitro characterization. J Control Release 2010; 143(1): 143-50.
De Cock I, Lajoinie G, Versluis M, De Smedt SC, Lentacker I. Sonoprinting and the importance of microbubble loading for the ultrasound mediated cellular delivery of nanoparticles. Biomaterials 2016; 83: 294-307.
Cosgrove D, Harvey C. Clinical uses of microbubbles in diagnosis and treatment. Med Biol Eng Comput 2009; 47(8): 813-26.
Weissleder R, Mahmood U. Molecular imaging. Radiology 2001; 219(2): 316-33.
Quaia E. Microbubble ultrasound contrast agents: an update. Eur Radiol 2007; 17(8): 1995-2008.
Bartolotta TV, Vernuccio F, Taibbi A, Lagalla R. Contrast-enhanced ultrasound in focal liver lesions: where do we stand? Semin Ultrasound CT MR 2016; 37(6): 573-86.
Wu Q, Wang Y, Li Y, Hu B, He ZY. Diagnostic value of contrast-enhanced ultrasound in solid thyroid nodules with and without enhancement. Endocrine 2016; 53(2): 480-8.
Mori N, Mugikura S, Takahashi S, et al. Quantitative analysis of contrast-enhanced ultrasound imaging in invasive breast cancer: a novel technique to obtain histopathologic information of microvessel density. Ultrasound Med Biol 2017; 43(3): 607-14.
Porter TR, Xie F. Myocardial perfusion imaging with contrast ultrasound. JACC Cardiovasc Imaging 2010; 3(2): 176-87.
Hoffmann R, Barletta G, von Bardeleben S, et al. Analysis of left ventricular volumes and function: a multicenter comparison of cardiac magnetic resonance imaging, cine ventriculography, and unenhanced and contrast-enhanced two-dimensional and three-dimensional echocardiography. J Am Soc Echocardiogr 2014; 27(3): 292-301.
Madani A, Beletsky V, Tamayo A, Munoz C, Spence JD. High-risk asymptomatic carotid stenosis Ulceration on 3D ultrasound vs. TCD microemboli. Neurology 2011; 77(8): 744-50.
Eisenbrey JR, Burstein OM, Kambhampati R, Forsberg F, Liu JB, Wheatley MA. Development and optimization of a doxorubicin loaded poly(lactic acid) contrast agent for ultrasound directed drug delivery. J Control Release 2010; 143(1): 38-44.
Cochran MC, Eisenbrey J, Ouma RO, Soulen M, Wheatley MA. Doxorubicin and paclitaxel loaded microbubbles for ultrasound triggered drug delivery. Int J Pharm 2011; 414(1-2): 161-70.
Holt RG, Roy RA. Measurements of bubble-enhanced heating from focused, mhz-frequency ultrasound in a tissue-mimicking material. Ultrasound Med Biol 2001; 27(10): 1399-412.
Watmough DJ, Lakshmi R, Ghezzi F, et al. The effect of gas bubbles on the production of ultrasound hyperthermia at 0.75 MHz: A phantom study. Ultrasound Med Biol 1993; 19(3): 231-41.
Li C, Zhang Y, Li Z, et al. Light-responsive biodegradable nanorattles for cancer theranostics. Adv Mater 2018; 30(8): 1-8.
Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 2004; 30(7): 979-89.
Lammers T, Koczera P, Fokong S, et al. Theranostic USPIO-loaded microbubbles for mediating and monitoring blood-brain barrier permeation. Adv Funct Mater 2015; 25(1): 36-43.
Bleeker H, Shung K, Barnhart J. Ultrasonic characterization of Albunex©, a new contrast agent. J Acoust Soc Am 1990; 87(4): 1792-7.
Guvener N, Appold L, de Lorenzi F, et al. Recent advances in ultrasound-based diagnosis and therapy with micro- and nanometer-sized formulations. Methods 2017; 130: 4-13.
Li H, Yang Y, Zhang M, et al. Acoustic characterization and enhanced ultrasound imaging of long-circulating lipid-coated microbubbles. J Ultrasound Med 2018; 37(5): 1243-56.
Lindner JR. Microbubbles in medical imaging: current applications and future directions. Nat Rev Drug Discov 2004; 3(6): 527-32.
Hernot S, Klibanov AL. Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev 2008; 60(10): 1153-66.
Wang S, Hossack JA, Klibanov AL. Targeting of microbubbles: contrast agents for ultrasound molecular imaging. J Drug Target 2018; 26(5-6): 420-34.
DeJong N, Hoff L, Skotland T, Bom N. Absorption and scatter of encapsulated gas filled microspheres: theoretical considerations and some measurements. Ultrasonics 1992; 30(2): 95-103.
Hoff L, Sontum PC, Hovem JM. Oscillations of polymeric microbubbles: Effect of the encapsulating shell. J Acoust Soc Am 2000; 107(4): 2272-80.
Qin S, Ferrara K. A model for the dynamics of ultrasound contrast agents in vivo. J Acoust Soc Am 2010; 128(3): 1511-21.
Church C. The effects of an elastic solid surface layer on the radial pulsations of gas bubbles. J Acoust Soc Am 1995; 97(3): 1510-21.
Guo X, Li Q, Zhang Z, Zhang D. Tu. Investigation on the inertial cavitation threshold and shell properties of commercialized ultrasound contrast agent microbubbles. J Acoust Soc Am 2013; 134(2): 1622-31.
Sheeran PS, Dayton PA. Improving the performance of phase-change perfluorocarbon droplets for medical ultrasonography: current progress, challenges, and prospects. Scientifica (Cairo) 2014; 2014: 579684.
Sheeran PS, Luois S, Dayton PA, Matsunaga TO. Formulation and acoustic studies of a new phase-shift agent for diagnostic and therapeutic ultrasound. Langmuir 2011; 27(17): 10412-20.
Sheeran PS, Luois SH, Mullin LB, Matsunaga TO, Dayton PA. Design of ultrasonically-activatable nanoparticles using low boiling point perfluorocarbons. Biomaterials 2012; 33(11): 3262-9.
Sheeran PS, Matsunaga TO, Dayton PA. Phase change events of volatile liquid perfluorocarbon contrast agents produce unique acoustic signatures. Phys Med Biol 2014; 59(2): 379-401.
Kripfgans OD, Fowlkes JB, Woydt M, Eldevik OP, Carson PL. In vivo droplet vaporization for occlusion therapy and phase aberration correction. IEEE Trans Ultrason Ferroelectr Freq Control 2002; 49(6): 726-38.
Zhang M, Fabiilli ML, Haworth KJ, et al. Initial investigation of acoustic droplet vaporization for occlusion in canine kidney. Ultrasound Med Biol 2010; 36(10): 1691-703.
Haworth K, Fowlkes J, Carson P, Kripfgans O. Towards aberration correction of transcranial ultrasound using acoustic droplet vaporization. Ultrasound Med Biol 2008; 34(3): 435-45.
Huang J, Xu JS, Xu RX. Heat-sensitive microbubbles for intraoperative assessment of cancer ablation margins. Biomaterials 2010; 31(6): 1278-86.
Kang ST, Lin YC, Yeh CK. Mechanical bioeffects of acoustic droplet vaporization in vessel-mimicking phantoms. Ultrason Sonochem 2014; 21(5): 1866-74.
Miyoshi N, Kundu SK, Tuziuti T, Yasui K, Shimada I, Ito Y. Combination of Sonodynamic and Photodynamic Therapy against Cancer Would Be Effective through Using a Regulated Size of Nanoparticles. Nanosci Nanoeng 2016; 4(1): 1-11.
Abd El-Kaream SA, Abd Elsamie GH, Abd-Alkareem AS. Sono-photodynamic modality for cancer treatment using bio-degradable bio-conjugated sonnelux nanocomposite in tumor-bearing mice: Activated cancer therapy using light and ultrasound. Biochem Biophys Res Commun 2018; 503(2): 1075-86.
Wang P, Li C, Wang X, et al. Anti-metastatic and pro-apoptotic effects elicited by combination photodynamic therapy with sonodynamic therapy on breast cancer both in vitro and in vivo. Ultrason Sonochem 2015; 23: 116-27.
Wang H, Wang P, Zhang K, Wang X, Liu Q. Changes in cell migration due to the combined effects of sonodynamic therapy and photodynamic therapy on MDA-MB-231 cells. Laser Phys Lett 2015; 12(3): 035603.
Li Q, Wang X, Wang P, et al. Efficacy of chlorin e6-mediated sono-photodynamic therapy on 4T1 cells. Cancer Biother Radiopharm 2014; 29(1): 42-52.
Chen HJ, Zhou XB, Wang AL, Zheng BY, Yeh CK, Huang JD. Synthesis and biological characterization of novel rose bengal derivatives with improved amphiphilicity for sono-photodynamic therapy. Eur J Med Chem 2018; 145: 86-95.
Nomikou N, Curtis K, McEwan C, et al. A versatile, stimulus-responsive nanoparticle-based platform for use in both sonodynamic and photodynamic cancer therapy. Acta Biomater 2017; 49: 414-21.

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