Radial extracorporeal shock wave promotes the enhanced permeability and retention effect to reinforce cancer nanothermotherapeutics
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摘要
Since most cancer nanomedicine relies on the enhanced permeability and retention(EPR) effect to eradicate tumors, strategies that are able to promote nanoparticle(NP) delivery and extravasation are presupposed to elevate the EPR effect for more effective cancer therapeutics. However, nanothermotherapeutics still suffers from limited drug delivery into tumor sites, for even though numerous efforts have been made to enhance the selective tumor targeting of NPs. In this study, we uncovered that radial extracorporeal shock wave therapy(rESWT), an important approach in physical therapy that has been overlooked in cancer treatment in the past, can largely improve the EPR-dependent tumor uptake of NPs. We here defined the optimal low dosage and desirable combinatory manner for rESWT in driving NP accumulation towards tumors. Two underlying biophysical mechanisms responsible for the rESWT-enhanced EPR effect were proposed. On one hand, rESWT-conducted compressive and tensile forces could relieve high intra-tumoral pressure; on the other hand, rESWT-induced cavitation bubbles could directly distend and disrupt tumor blood vessels. All these together synergistically promoted vessel vasodilation, tumor perfusion and NP extravasation. Further experiments revealed that the combinatory therapeutics between rESWT and nanothermotherapeutics greatly improved the tumor-killing efficacy. Thus, our findings open a new path to improve EPR-mediated drug delivery with the assistance of rESWT.
Since most cancer nanomedicine relies on the enhanced permeability and retention(EPR) effect to eradicate tumors, strategies that are able to promote nanoparticle(NP) delivery and extravasation are presupposed to elevate the EPR effect for more effective cancer therapeutics. However, nanothermotherapeutics still suffers from limited drug delivery into tumor sites, for even though numerous efforts have been made to enhance the selective tumor targeting of NPs. In this study, we uncovered that radial extracorporeal shock wave therapy(rESWT), an important approach in physical therapy that has been overlooked in cancer treatment in the past, can largely improve the EPR-dependent tumor uptake of NPs. We here defined the optimal low dosage and desirable combinatory manner for rESWT in driving NP accumulation towards tumors. Two underlying biophysical mechanisms responsible for the rESWT-enhanced EPR effect were proposed. On one hand, rESWT-conducted compressive and tensile forces could relieve high intra-tumoral pressure; on the other hand, rESWT-induced cavitation bubbles could directly distend and disrupt tumor blood vessels. All these together synergistically promoted vessel vasodilation, tumor perfusion and NP extravasation. Further experiments revealed that the combinatory therapeutics between rESWT and nanothermotherapeutics greatly improved the tumor-killing efficacy. Thus, our findings open a new path to improve EPR-mediated drug delivery with the assistance of rESWT.
Since most cancer nanomedicine relies on the enhanced permeability and retention(EPR) effect to eradicate tumors, strategies that are able to promote nanoparticle(NP) delivery and extravasation are presupposed to elevate the EPR effect for more effective cancer therapeutics. However, nanothermotherapeutics still suffers from limited drug delivery into tumor sites, for even though numerous efforts have been made to enhance the selective tumor targeting of NPs. In this study, we uncovered that radial extracorporeal shock wave therapy(rESWT), an important approach in physical therapy that has been overlooked in cancer treatment in the past, can largely improve the EPR-dependent tumor uptake of NPs. We here defined the optimal low dosage and desirable combinatory manner for rESWT in driving NP accumulation towards tumors. Two underlying biophysical mechanisms responsible for the rESWT-enhanced EPR effect were proposed. On one hand, rESWT-conducted compressive and tensile forces could relieve high intra-tumoral pressure; on the other hand, rESWT-induced cavitation bubbles could directly distend and disrupt tumor blood vessels. All these together synergistically promoted vessel vasodilation, tumor perfusion and NP extravasation. Further experiments revealed that the combinatory therapeutics between rESWT and nanothermotherapeutics greatly improved the tumor-killing efficacy. Thus, our findings open a new path to improve EPR-mediated drug delivery with the assistance of rESWT.
引文
[1]Golombek SKMJ,Theek B,Appold L,et al.Tumor targeting via EPR:strategies to enhance patient responses.Adv Drug Deliv Rev 2018;130:17-38.
[2]Lang TDX,Zheng Z,Liu Y,et al.Tumor microenvironment-responsive docetaxel-loaded micelle combats metastatic breast cancer.Sci Bull2019;64:91-100.
[3]Deng L,Sun C,Yun B,et al.Functionalization of small black phosphorus nanoparticles for targeted imaging and photothermal therapy of cancer.Sci Bull 2018;63:917-24.
[4]Ac D.Tumor endothelial cells.Cold Spring Harb Perspect Med 2012;2:a006536.
[5]Ojha TPV,Shi Y,Hennink WE,et al.Pharmacological and physical vessel modulation strategies to improve epr-mediated drug targeting to tumors.Adv Drug Deliv Rev 2017;15:44-60.
[6]Shi JKP,Wooster R,Farokhzad OC.Cancer nanomedicine:progress,challenges and opportunities.Nat Rev Cancer 2017;17:20-37.
[7]Blanco ESH,Ferrari M.Principles of nanoparticle design for overcoming biological barriers to drug delivery.Nat Biotechnol 2015;33:941-51.
[8]Wilhelm STA,Dai Q,Ohta S,et al.Analysis of nanoparticle delivery to tumours.Nat Rev Mater 2016;1:16014.
[9]Chauhan VPMJ,Liu H,Lacorre DA,et al.Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumour blood vessels.Nat Commun 2013;4:2516.
[10]Stylianopoulos TJR.Combining two strategies to improve perfusion and drug delivery in solid tumors.Proc Natl Acad Sci USA 2013;110:18632-7.
[11]Stylianopoulos TMJ,Chauhan VP,Jain SR,et al.Causes,consequences,and remedies for growth-induced solid stress in murine and human tumors.Proc Natl Acad Sci USA 2012;109:15101-8.
[12]Dai QWS,Ding D,Syed AM,et al.Quantifying the ligand-coated nanoparticle delivery to cancer cells in solid tumors.ACS Nano 2018;12:8423-35.
[13]Cj W.Extracorporeal shockwave therapy in musculoskeletal disorders.JOrthop Surg Res 2012;7:11.
[14]Mariotto SdPA,Cavalieri E,Amelio E,et al.Extracorporeal shock wave therapy in inflammatory diseases:molecular mechanism that triggers antiinflammatory action.Curr Med Chem 2009;16:2366-72.
[15]Schmitz CCN,Milz S,Schieker M,et al.Efficacy and safety of extracorporeal shock wave therapy for orthopedic conditions:a systematic review on studies listed in the pedro database.Br Med Bull 2015;116:115-38.
[16]Yip HKLF,Chen KH,Sung PH,et al.Preclinical and clinical application of extracorporeal shockwave for ischemic cardiovascular disease.Transl Res Biomed Basel,Karger 2018;6:87-101.
[17]Zhang LFX,Chen S,Zhao ZB,et al.Efficacy and safety of extracorporeal shock wave therapy for acute and chronic soft tissue wounds:a systematic review and meta-analysis.Int Wound J 2018;15:590-9.
[18]Kobayashi HWR,Choyke PL.Improving conventional enhanced permeability and retention(epr)effects;what is the appropriate target?Theranostics2013;4:81-9.
[19]Romeo PLV,Pagani D,Sansone V.Extracorporeal shock wave therapy in musculoskeletal disorders:a review.Med Princ Pract 2014;23:7-13.
[20]Sirsi SRBM.State-of-the-art materials for ultrasound-triggered drug delivery.Adv Drug Deliv Rev 2014;72:3-14.
[21]Frairia RBL,Catalano MG.Extracorporeal shock waves:perspectives in malignant tumor treatment.J Biol Regul Homeost Agents 2016;30:641-8.
[22]López-Marín LM,Millán-Chiu BE,Casta?o-González K,et al.Shock waveinduced damage and poration in eukaryotic cell membranes.J Membrane Biol2017;250:41-52.
[23]López-Marín LMRA,Fernández F,Loske A.Shock wave-induced permeabilization of mammalian cells.Phys Life Rev 2018;26-27:1-38.
[24]Chen QXL,Chen J,Yang Z,et al.Tumor vasculature normalization by orally fed erlotinib to modulate the tumor microenvironment for enhanced cancer nanomedicine and immunotherapy.Biomaterials 2017;148:69-80.
[25]Feng LCL,Dong Z,Tao D,et al.Theranostic liposomes with hypoxia-activated prodrug to effectively destruct hypoxic tumors post-photodynamic therapy.ACS Nano 2017;11:927-37.
[26]Feng LTD,Dong Z,Chen Q,et al.Near-infrared light activation of quenched liposomal ce6 for synergistic cancer phototherapy with effective skin protection.Biomaterials 2017;127:13-24.
[27]Guo M,Liu Z,Liu J,et al.Direct site-specific treatment of skin cancer using doxorubicin-loaded nanofibrous membranes.Sci Bull 2018;63:92-100.
[28]Gao JS-PM,Huang H,et al.Synthesis of different-sized gold nanostars for Raman bioimaging and photothermal therapy in cancer nanotheranostics.Sci China Chem 2017;60:1219-29.
[29]Song XFL,Liang C,Yang K,et al.Ultrasound triggered tumor oxygenation with oxygen-shuttle nanoperfluorocarbon to overcome hypoxia-associated resistance in cancer therapies.Nano Lett 2016;16:6145-53.
[30]Zhang RFL,Dong Z,Wang L,et al.Glucose&oxygen exhausting liposomes for combined cancer starvation and hypoxia-activated therapy.Biomaterials2018;162:123-31.
[31]Lukes PZJ,Horak V,Hoffer P,et al.In vivo effects of focused shock waves on tumor tissue visualized by fluorescence staining techniques.Bioelectrochemistry 2015;103:103-10.
[32]W?rle KSP,Hofst?dter F.The combined effects of high-energy shock waves and cytostatic drugs or cytokines on human bladder cancer cells.Br J Cancer1994;69:58-65.
[33]Liu YCX,Guo A,Liu S,Hu G.Quantitative assessments of mechanical responses upon radial extracorporeal shock wave therapy.Adv Sci 2017;5:1700797.
[34]Chang YS,McDonald DM,Jones R,et al.Mosaic blood vessels in tumors:frequency of cancer cells in contact with flowing blood.Proc Natl Acad Sci USA2000;97:14608-13.
[35]Cabral HMY,Mizuno K,Chen Q,et al.Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size.Nat Nanotechnol2011;6:815-23.
[36]Yokota K,Akiyama Y,Mimura T.Detection of synovial inflammation in rheumatic diseases using superb microvascular imaging:comparison with conventional power doppler imaging.Mod Rheumatol 2018;28:327-33.
[37]Gong H,Xiang J,Han X,et al.Hyaluronidase to enhance nanoparticle-based photodynamic tumor therapy.Nano Lett 2016;16:2512-21.
[38]Dolor ASFJ.Digesting a path forward:the utility of collagenase tumor treatment for improved drug delivery.Mol Pharm 2018;15:2069-83.
[39]Wang JY,Lu X,He X.Nanoparticle systems reduce systemic toxicity in cancer treatment.Nanomedicine 2016;11:103-6.
[40]Zhou H,Deng J,Lemons PK,et al.Hyaluronidase embedded in nanocarrier peg shell for enhanced tumor penetration and highly efficient antitumor efficacy.Nano Lett 2016;16:3268-77.
[41]Coussios CC.Applications of acoustics and cavitation to noninvasive therapy and drug delivery.Annu Rev Fluid Mech 2008;40:395-420.
[42]Dasgupta ALM,Ojha T,Storm G,et al.Ultrasound-mediated drug delivery to the brain:principles,progress and prospects.Drug Discov Today Technol2016;20:41-8.
[43]Császár NB,Milz S,Sprecher CM,et al.Radial shock wave devices generate cavitation.PLoS One 2015;10:0140541.
[44]Caskey CF,Qin S,Dayton PA,et al.Direct observations of ultrasound microbubble contrast agent interaction with the microvessel wall.J Acoust Soc Am 2007;122:1191-200.
[45]Chen HKW,Brayman AA,Bailey MR,et al.Blood vessel deformations on microsecond time scales by ultrasonic cavitation.Phys Rev Lett 2011;106:034301.
[46]Sirsi SR,Borden BM.Advances in ultrasound mediated gene therapy using microbubble contrast agents.Theranostics 2012;2:1208-22.
[47]Brujan EANK,Schmidt P,Vogel A.Dynamics of laser-induced cavitation bubbles near elastic boundaries:influence of the elastic modulus.J Fluid Mech2001;433:283-314.
[48]Liang CCY,Yi X,Xu J,et al.Nanoparticle-mediated internal radioisotope therapy to locally increase the tumor vasculature permeability for synergistically improved cancer therapies.Biomaterials 2019;197:368-79.
[49]Cherukuri PGE,Curley SA.Targeted hyperthermia using metal nanoparticles.Adv Drug Deliv Rev 2010;62:339-45.
[50]Theek BBM,Ojha T,M?ckel D,et al.Sonoporation enhances liposome accumulation and penetration in tumors with low epr.J Control Release2016;231:77-85.
[51]Liao JWX,Ran B,Peng J,et al.Polymer hybrid magnetic nanocapsules encapsulating ir820 and ptx for external magnetic field-guided tumor targeting and multifunctional theranostics.Nanoscale 2017;9:2479-91.
[52]Marano FAM,Frairia R,Adamini A,et al.Doxorubicin-loaded nanobubbles combined with extracorporeal shock waves:basis for a new drug delivery tool in anaplastic thyroid cancer.Thyroid 2016;26:706-16.
[53]Marano FFR,Rinella L,Argenziano M,et al.Combining doxorubicinnanobubbles and shockwaves for anaplastic thyroid cancer treatment:preclinical study in a xenograft mouse model.Endocr Relat Cancer2017;24:275-86.
[54]Varchi GFF,Canaparo R,Ballestri M,et al.Engineered porphyrin loaded coreshell nanoparticles for selective sonodynamic anticancer treatment.Nanomedicine 2015;10:3483-94.
[55]Canaparo RVG,Ballestri M,Foglietta F,et al.Polymeric nanoparticles enhance the sonodynamic activity of meso-tetrakis(4-sulfonatophenyl)porphyrin in an in vitro neuroblastoma model.Int J Nanomed 2013;8:4247-63.
[56]Dollet BMP,Garbin V.Bubble dynamics in soft and biological matter.Annu Rev Fluid Mech 2019;51:331-55.
[57]Ji QWP,He C.Extracorporeal shockwave therapy as a novel and potential treatment for degenerative cartilage and bone disease:osteoarthritis.Aqualitative analysis of the literature.Prog Biophys Mol Biol 2016;121:255-65.
[2]Lang TDX,Zheng Z,Liu Y,et al.Tumor microenvironment-responsive docetaxel-loaded micelle combats metastatic breast cancer.Sci Bull2019;64:91-100.
[3]Deng L,Sun C,Yun B,et al.Functionalization of small black phosphorus nanoparticles for targeted imaging and photothermal therapy of cancer.Sci Bull 2018;63:917-24.
[4]Ac D.Tumor endothelial cells.Cold Spring Harb Perspect Med 2012;2:a006536.
[5]Ojha TPV,Shi Y,Hennink WE,et al.Pharmacological and physical vessel modulation strategies to improve epr-mediated drug targeting to tumors.Adv Drug Deliv Rev 2017;15:44-60.
[6]Shi JKP,Wooster R,Farokhzad OC.Cancer nanomedicine:progress,challenges and opportunities.Nat Rev Cancer 2017;17:20-37.
[7]Blanco ESH,Ferrari M.Principles of nanoparticle design for overcoming biological barriers to drug delivery.Nat Biotechnol 2015;33:941-51.
[8]Wilhelm STA,Dai Q,Ohta S,et al.Analysis of nanoparticle delivery to tumours.Nat Rev Mater 2016;1:16014.
[9]Chauhan VPMJ,Liu H,Lacorre DA,et al.Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumour blood vessels.Nat Commun 2013;4:2516.
[10]Stylianopoulos TJR.Combining two strategies to improve perfusion and drug delivery in solid tumors.Proc Natl Acad Sci USA 2013;110:18632-7.
[11]Stylianopoulos TMJ,Chauhan VP,Jain SR,et al.Causes,consequences,and remedies for growth-induced solid stress in murine and human tumors.Proc Natl Acad Sci USA 2012;109:15101-8.
[12]Dai QWS,Ding D,Syed AM,et al.Quantifying the ligand-coated nanoparticle delivery to cancer cells in solid tumors.ACS Nano 2018;12:8423-35.
[13]Cj W.Extracorporeal shockwave therapy in musculoskeletal disorders.JOrthop Surg Res 2012;7:11.
[14]Mariotto SdPA,Cavalieri E,Amelio E,et al.Extracorporeal shock wave therapy in inflammatory diseases:molecular mechanism that triggers antiinflammatory action.Curr Med Chem 2009;16:2366-72.
[15]Schmitz CCN,Milz S,Schieker M,et al.Efficacy and safety of extracorporeal shock wave therapy for orthopedic conditions:a systematic review on studies listed in the pedro database.Br Med Bull 2015;116:115-38.
[16]Yip HKLF,Chen KH,Sung PH,et al.Preclinical and clinical application of extracorporeal shockwave for ischemic cardiovascular disease.Transl Res Biomed Basel,Karger 2018;6:87-101.
[17]Zhang LFX,Chen S,Zhao ZB,et al.Efficacy and safety of extracorporeal shock wave therapy for acute and chronic soft tissue wounds:a systematic review and meta-analysis.Int Wound J 2018;15:590-9.
[18]Kobayashi HWR,Choyke PL.Improving conventional enhanced permeability and retention(epr)effects;what is the appropriate target?Theranostics2013;4:81-9.
[19]Romeo PLV,Pagani D,Sansone V.Extracorporeal shock wave therapy in musculoskeletal disorders:a review.Med Princ Pract 2014;23:7-13.
[20]Sirsi SRBM.State-of-the-art materials for ultrasound-triggered drug delivery.Adv Drug Deliv Rev 2014;72:3-14.
[21]Frairia RBL,Catalano MG.Extracorporeal shock waves:perspectives in malignant tumor treatment.J Biol Regul Homeost Agents 2016;30:641-8.
[22]López-Marín LM,Millán-Chiu BE,Casta?o-González K,et al.Shock waveinduced damage and poration in eukaryotic cell membranes.J Membrane Biol2017;250:41-52.
[23]López-Marín LMRA,Fernández F,Loske A.Shock wave-induced permeabilization of mammalian cells.Phys Life Rev 2018;26-27:1-38.
[24]Chen QXL,Chen J,Yang Z,et al.Tumor vasculature normalization by orally fed erlotinib to modulate the tumor microenvironment for enhanced cancer nanomedicine and immunotherapy.Biomaterials 2017;148:69-80.
[25]Feng LCL,Dong Z,Tao D,et al.Theranostic liposomes with hypoxia-activated prodrug to effectively destruct hypoxic tumors post-photodynamic therapy.ACS Nano 2017;11:927-37.
[26]Feng LTD,Dong Z,Chen Q,et al.Near-infrared light activation of quenched liposomal ce6 for synergistic cancer phototherapy with effective skin protection.Biomaterials 2017;127:13-24.
[27]Guo M,Liu Z,Liu J,et al.Direct site-specific treatment of skin cancer using doxorubicin-loaded nanofibrous membranes.Sci Bull 2018;63:92-100.
[28]Gao JS-PM,Huang H,et al.Synthesis of different-sized gold nanostars for Raman bioimaging and photothermal therapy in cancer nanotheranostics.Sci China Chem 2017;60:1219-29.
[29]Song XFL,Liang C,Yang K,et al.Ultrasound triggered tumor oxygenation with oxygen-shuttle nanoperfluorocarbon to overcome hypoxia-associated resistance in cancer therapies.Nano Lett 2016;16:6145-53.
[30]Zhang RFL,Dong Z,Wang L,et al.Glucose&oxygen exhausting liposomes for combined cancer starvation and hypoxia-activated therapy.Biomaterials2018;162:123-31.
[31]Lukes PZJ,Horak V,Hoffer P,et al.In vivo effects of focused shock waves on tumor tissue visualized by fluorescence staining techniques.Bioelectrochemistry 2015;103:103-10.
[32]W?rle KSP,Hofst?dter F.The combined effects of high-energy shock waves and cytostatic drugs or cytokines on human bladder cancer cells.Br J Cancer1994;69:58-65.
[33]Liu YCX,Guo A,Liu S,Hu G.Quantitative assessments of mechanical responses upon radial extracorporeal shock wave therapy.Adv Sci 2017;5:1700797.
[34]Chang YS,McDonald DM,Jones R,et al.Mosaic blood vessels in tumors:frequency of cancer cells in contact with flowing blood.Proc Natl Acad Sci USA2000;97:14608-13.
[35]Cabral HMY,Mizuno K,Chen Q,et al.Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size.Nat Nanotechnol2011;6:815-23.
[36]Yokota K,Akiyama Y,Mimura T.Detection of synovial inflammation in rheumatic diseases using superb microvascular imaging:comparison with conventional power doppler imaging.Mod Rheumatol 2018;28:327-33.
[37]Gong H,Xiang J,Han X,et al.Hyaluronidase to enhance nanoparticle-based photodynamic tumor therapy.Nano Lett 2016;16:2512-21.
[38]Dolor ASFJ.Digesting a path forward:the utility of collagenase tumor treatment for improved drug delivery.Mol Pharm 2018;15:2069-83.
[39]Wang JY,Lu X,He X.Nanoparticle systems reduce systemic toxicity in cancer treatment.Nanomedicine 2016;11:103-6.
[40]Zhou H,Deng J,Lemons PK,et al.Hyaluronidase embedded in nanocarrier peg shell for enhanced tumor penetration and highly efficient antitumor efficacy.Nano Lett 2016;16:3268-77.
[41]Coussios CC.Applications of acoustics and cavitation to noninvasive therapy and drug delivery.Annu Rev Fluid Mech 2008;40:395-420.
[42]Dasgupta ALM,Ojha T,Storm G,et al.Ultrasound-mediated drug delivery to the brain:principles,progress and prospects.Drug Discov Today Technol2016;20:41-8.
[43]Császár NB,Milz S,Sprecher CM,et al.Radial shock wave devices generate cavitation.PLoS One 2015;10:0140541.
[44]Caskey CF,Qin S,Dayton PA,et al.Direct observations of ultrasound microbubble contrast agent interaction with the microvessel wall.J Acoust Soc Am 2007;122:1191-200.
[45]Chen HKW,Brayman AA,Bailey MR,et al.Blood vessel deformations on microsecond time scales by ultrasonic cavitation.Phys Rev Lett 2011;106:034301.
[46]Sirsi SR,Borden BM.Advances in ultrasound mediated gene therapy using microbubble contrast agents.Theranostics 2012;2:1208-22.
[47]Brujan EANK,Schmidt P,Vogel A.Dynamics of laser-induced cavitation bubbles near elastic boundaries:influence of the elastic modulus.J Fluid Mech2001;433:283-314.
[48]Liang CCY,Yi X,Xu J,et al.Nanoparticle-mediated internal radioisotope therapy to locally increase the tumor vasculature permeability for synergistically improved cancer therapies.Biomaterials 2019;197:368-79.
[49]Cherukuri PGE,Curley SA.Targeted hyperthermia using metal nanoparticles.Adv Drug Deliv Rev 2010;62:339-45.
[50]Theek BBM,Ojha T,M?ckel D,et al.Sonoporation enhances liposome accumulation and penetration in tumors with low epr.J Control Release2016;231:77-85.
[51]Liao JWX,Ran B,Peng J,et al.Polymer hybrid magnetic nanocapsules encapsulating ir820 and ptx for external magnetic field-guided tumor targeting and multifunctional theranostics.Nanoscale 2017;9:2479-91.
[52]Marano FAM,Frairia R,Adamini A,et al.Doxorubicin-loaded nanobubbles combined with extracorporeal shock waves:basis for a new drug delivery tool in anaplastic thyroid cancer.Thyroid 2016;26:706-16.
[53]Marano FFR,Rinella L,Argenziano M,et al.Combining doxorubicinnanobubbles and shockwaves for anaplastic thyroid cancer treatment:preclinical study in a xenograft mouse model.Endocr Relat Cancer2017;24:275-86.
[54]Varchi GFF,Canaparo R,Ballestri M,et al.Engineered porphyrin loaded coreshell nanoparticles for selective sonodynamic anticancer treatment.Nanomedicine 2015;10:3483-94.
[55]Canaparo RVG,Ballestri M,Foglietta F,et al.Polymeric nanoparticles enhance the sonodynamic activity of meso-tetrakis(4-sulfonatophenyl)porphyrin in an in vitro neuroblastoma model.Int J Nanomed 2013;8:4247-63.
[56]Dollet BMP,Garbin V.Bubble dynamics in soft and biological matter.Annu Rev Fluid Mech 2019;51:331-55.
[57]Ji QWP,He C.Extracorporeal shockwave therapy as a novel and potential treatment for degenerative cartilage and bone disease:osteoarthritis.Aqualitative analysis of the literature.Prog Biophys Mol Biol 2016;121:255-65.