Remotely Activated Nanoparticles for Anticancer Therapy
Corresponding Author: Valentina Cauda
Nano-Micro Letters,
Vol. 13 (2021), Article Number: 11
Abstract
Cancer has nowadays become one of the leading causes of death worldwide. Conventional anticancer approaches are associated with different limitations. Therefore, innovative methodologies are being investigated, and several researchers propose the use of remotely activated nanoparticles to trigger cancer cell death. The idea is to conjugate two different components, i.e., an external physical input and nanoparticles. Both are given in a harmless dose that once combined together act synergistically to therapeutically treat the cell or tissue of interest, thus also limiting the negative outcomes for the surrounding tissues. Tuning both the properties of the nanomaterial and the involved triggering stimulus, it is possible furthermore to achieve not only a therapeutic effect, but also a powerful platform for imaging at the same time, obtaining a nano-theranostic application. In the present review, we highlight the role of nanoparticles as therapeutic or theranostic tools, thus excluding the cases where a molecular drug is activated. We thus present many examples where the highly cytotoxic power only derives from the active interaction between different physical inputs and nanoparticles. We perform a special focus on mechanical waves responding nanoparticles, in which remotely activated nanoparticles directly become therapeutic agents without the need of the administration of chemotherapeutics or sonosensitizing drugs.
Highlights:
1 The present review highlights the importance of remotely activated nanoparticles for anticancer purposes.
2 For each physical input, we present its possible active synergy with several nanomaterials.
3 We report examples and the mechanism of action when clarified.
4 Clinical trials involving remotely triggered nanoparticles are discussed.
Keywords
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- International Agency for Research in Cancer, Latest Global Cancer Data (World Health Organization, Geneva, 2018)
- D. Hanahan, R.A. Weinberg, Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011). https://doi.org/10.1016/j.cell.2011.02.013
- S. Tran, P.-J. DeGiovanni, B. Piel, P. Rai, Cancer nanomedicine: a review of recent success in drug delivery. Clin. Transl. Med. 6, e44 (2017). https://doi.org/10.1186/s40169-017-0175-0
- S. Soares, J. Sousa, A. Pais, C. Vitorino, Nanomedicine: principles, properties, and regulatory issues. Front. Chem. 6, 1–15 (2018). https://doi.org/10.3389/fchem.2018.00360
- J. Shi, P.W. Kantoff, R. Wooster, O.C. Farokhzad, Cancer nanomedicine: progress, challenges and opportunities. Nat. Rev. 17, 20–37 (2017). https://doi.org/10.1038/nrc.2016.108.Cancer
- C. Yan, Z. Guo, Y. Shen, Y. Chen, H. Tian, W.H. Zhu, Molecularly precise self-assembly of theranostic nanoprobes within a single-molecular framework for: in vivo tracking of tumor-specific chemotherapy. Chem. Sci. 9, 4959–4969 (2018). https://doi.org/10.1039/c8sc01069b
- P. Dong, K.P. Rakesh, H.M. Manukumar, Y.H.E. Mohammed, C.S. Karthik et al., Innovative nano-carriers in anticancer drug delivery—a comprehensive review. Bioorg. Chem. 85, 325–336 (2019). https://doi.org/10.1016/j.bioorg.2019.01.019
- J. Zhang, Q. Wang, J. Liu, Z. Guo, J. Yang et al., Saponin-based near-infrared nanoparticles with aggregation-induced emission behavior: enhancing cell compatibility and permeability. ACS Appl. Bio Mater. 2, 943–951 (2019). https://doi.org/10.1021/acsabm.8b00812
- X. Ji, C. Wang, M. Tang, D. Guo, F. Peng et al., Biocompatible protamine sulfate@silicon nanoparticle-based gene nanocarriers featuring strong and stable fluorescence. Nanoscale 10, 14455–14463 (2018). https://doi.org/10.1039/c8nr03107j
- L. Racca, M. Canta, B. Dumontel, A. Ancona, T. Limongi et al., Zinc oxide nanostructures in biomedicine. Smart Nanoparticles Biomed. (2018). https://doi.org/10.1016/b978-0-12-814156-4.00012-4
- V. De Matteis, M. Cascione, C.C. Toma, S. Leporatti, Silver nanoparticles: synthetic routes, in vitro toxicity and theranostic applications for cancer disease. Nanomaterials 8(5), 319 (2018). https://doi.org/10.3390/nano8050319
- T. Limongi, M. Canta, L. Racca, A. Ancona, S. Tritta, V. Vighetto, V. Cauda, Improving dispersal of therapeutic nanoparticles in the human body. Nanomedicine 14, 797–801 (2019). https://doi.org/10.2217/nnm-2019-0070
- Y.S. Youn, Y.H. Bae, Perspectives on the past, present, and future of cancer nanomedicine. Adv. Drug Deliv. Rev. 130, 3–11 (2018). https://doi.org/10.1016/j.addr.2018.05.008
- A. Albanese, P.S. Tang, W.C.W. Chan, The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 14, 1–16 (2012). https://doi.org/10.1146/annurev-bioeng-071811-150124
- A. Sukhanova, S. Bozrova, P. Sokolov, M. Berestovoy, A. Karaulov, I. Nabiev, Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Res. Lett. 13, 44 (2018). https://doi.org/10.1186/s11671-018-2457-x
- G. Canavese, A. Ancona, L. Racca, M. Canta, B. Dumontel et al., Nanoparticle-assisted ultrasound: a special focus on sonodynamic therapy against cancer. Chem. Eng. J. 340, 155–172 (2018). https://doi.org/10.1016/j.cej.2018.01.060
- D. Kwatra, A. Venugopal, S. Anant, Nanoparticles in radiation therapy: a summary of various approaches to enhance radiosensitization in cancer. Transl. Cancer Res. 2, 330–342 (2013). https://doi.org/10.3978/j.issn.2218-676X.2013.08.06
- D. Chang, M. Lim, J.A.C.M. Goos, R. Qiao, Y.Y. Ng et al., Biologically targeted magnetic hyperthermia: potential and limitations. Front. Pharmacol. 9, 831 (2018). https://doi.org/10.3389/fphar.2018.00831
- R. Zhang, F. Yan, Y. Chen, Exogenous physical irradiation on titania semiconductors: materials chemistry and tumor-specific nanomedicine. Adv. Sci. 5, 1801175 (2018). https://doi.org/10.1002/advs.201801175
- C.B. Collins, R.S. McCoy, B.J. Ackerson, G.J. Collins, C.J. Ackerson, Radiofrequency heating pathways for gold nanoparticles. Nanoscale 6, 8459–8472 (2014). https://doi.org/10.1039/c4nr00464g
- B. McWilliams, H. Wang, V. Binns, S. Curto, S. Bossmann, P. Prakash, Experimental investigation of magnetic nanoparticle-enhanced microwave hyperthermia. J. Funct. Biomater. 8, 21 (2017). https://doi.org/10.3390/jfb8030021
- Z. Yang, Z. Sun, Y. Ren, X. Chen, W. Zhang et al., Advances in nanomaterials for use in photothermal and photodynamic therapeutics (review). Mol. Med. Rep. 20, 5–15 (2019). https://doi.org/10.3892/mmr.2019.10218
- J.B. Vines, J.H. Yoon, N.E. Ryu, D.J. Lim, H. Park, Gold nanoparticles for photothermal cancer therapy. Front. Chem. 7, 1–16 (2019). https://doi.org/10.3389/fchem.2019.00167
- D. Howard, S. Sebastian, Q.V.C. Le, B. Thierry, I. Kempson, Chemical mechanisms of nanoparticle radiosensitization and radioprotection: a review of structure-function relationships influencing reactive oxygen species. Int. J. Mol. Sci. 21, 579 (2020). https://doi.org/10.3390/ijms21020579
- L. Racca, T. Limongi, V. Vighetto, B. Dumontel, A. Ancona et al., Zinc oxide nanocrystals and high-energy shock waves: a new synergy for the treatment of cancer cells. Front. Bioeng. Biotechnol. 8, 577 (2020). https://doi.org/10.3389/fbioe.2020.00577
- H. Xiang, Y. Chen, Energy-converting nanomedicine. Small 15, e1805339 (2019). https://doi.org/10.1002/smll.201805339
- A.K. Parchur, J.M. Jagtap, G. Sharma, V. Gogineni, S.B. White, A. Joshi, Remotely triggered nanotheranostics. Nanotheranostics 1, 1–22 (2019). https://doi.org/10.1007/978-3-030-01775-0_17
- A. Sneider, D. Vandyke, S. Paliwal, P. Rai, Remotely triggered nano-theranostics for cancer applications. Nanotheranostics 1, 1–22 (2017). https://doi.org/10.7150/ntno.17109
- W. Fan, B. Yung, P. Huang, X. Chen, Nanotechnology for multimodal synergistic cancer therapy. Chem. Rev. 117, 13566–13638 (2017). https://doi.org/10.1021/acs.chemrev.7b00258
- G. Pizzino, N. Irrera, M. Cucinotta, G. Pallio, F. Mannino, V. Arcoraci, F. Squadrito, D. Altavilla, A. Bitto, Oxidative stress: harms and benefits for human health. Oxid. Med. Cell Longev. 2017, 1–13 (2017). https://doi.org/10.1155/2017/8416763
- V. Vighetto, A. Ancona, L. Racca, T. Limongi, A. Troia, G. Canavese, V. Cauda, The synergistic effect of nanocrystals combined with ultrasound in the generation of reactive oxygen species for biomedical applications. Front. Bioeng. Biotechnol. 7, 1–10 (2019). https://doi.org/10.3389/fbioe.2019.00374
- W. Fan, W. Tang, J. Lau, Z. Shen, J. Xie, J. Shi, X. Chen, Breaking the depth dependence by nanotechnology-enhanced x-ray-excited deep cancer theranostics. Adv. Mater. 31, 1806381 (2019). https://doi.org/10.1002/adma.201806381
- C. Verry, L. Sancey, S. Dufort, G. Le Duc, C. Mendoza et al., Treatment of multiple brain metastases using gadolinium nanoparticles and radiotherapy: NANO-RAD, a phase I study protocol. BMJ Open 9, 1–6 (2019). https://doi.org/10.1136/bmjopen-2018-023591
- J. Deng, S. Xu, W. Hu, X. Xun, L. Zheng, M. Su, Tumor targeted, stealthy and degradable bismuth nanoparticles for enhanced X-ray radiation therapy of breast cancer. Biomaterials 154, 24–33 (2018). https://doi.org/10.1016/j.biomaterials.2017.10.048
- Z. Kuncic, S. Lacombe, Nanoparticle radio-enhancement: principles, progress and application to cancer treatment. Phys. Med. Biol. 63, 02TR01 (2018). https://doi.org/10.1088/1361-6560/aa99ce
- J. Zhao, M. Zhou, C. Li, Synthetic nanoparticles for delivery of radioisotopes and radiosensitizers in cancer therapy. Cancer Nanotechnol. 7, 9 (2016). https://doi.org/10.1186/s12645-016-0022-9
- P. Retif, S. Pinel, M. Toussaint, C. Frochot, R. Chouikrat, T. Bastogne, M. Barberi-Heyob, Nanoparticles for radiation therapy enhancement: the key parameters. Theranostics 5, 1030–1044 (2015). https://doi.org/10.7150/thno.11642
- Y. Liu, P. Zhang, F. Li, X. Jin, J. Li, W. Chen, Q. Li, Metal-based nanoenhancers for future radiotherapy: radiosensitizing and synergistic effects on tumor cells. Theranostics 8, 1824–1849 (2018). https://doi.org/10.7150/thno.22172
- S. Bonvalot, P.L. Rutkowski, J. Thariat, S. Carrère, A. Ducassou et al., NBTXR3, a first-in-class radioenhancer hafnium oxide nanoparticle, plus radiotherapy versus radiotherapy alone in patients with locally advanced soft-tissue sarcoma (Act. In. Sarc): a multicentre, phase 2–3, randomised, controlled trial. Lancet Oncol. 20, 1148–1159 (2019). https://doi.org/10.1016/S1470-2045(19)30326-2
- A.K. Hauser, M.I. Mitov, E.F. Daley, R.C. McGarry, K.W. Anderson, J.Z. Hilt, Targeted iron oxide nanoparticles for the enhancement of radiation therapy. Biomaterials 105, 127–135 (2016). https://doi.org/10.1016/j.biomaterials.2016.07.032
- F. Chen, X.H. Zhang, X.D. Hu, P.D. Liu, H.Q. Zhang, The effects of combined selenium nanoparticles and radiation therapy on breast cancer cells in vitro. Artif. Cells Nanomed. Biotechnol. 46, 937–948 (2018). https://doi.org/10.1080/21691401.2017.1347941
- T.J. Meyer, A. Scherzad, H. Moratin, T.E. Gehrke, J. Killisperger et al., The radiosensitizing effect of zinc oxide nanoparticles in sub-cytotoxic dosing is associated with oxidative stress in vitro. Materials 12, 4062 (2019). https://doi.org/10.3390/MA12244062
- J. Xie, N. Wang, X. Dong, C. Wang, Z. Du et al., Graphdiyne nanoparticles with high free radical scavenging activity for radiation protection. ACS Appl. Mater. Interfaces. 11, 2579–2590 (2019). https://doi.org/10.1021/acsami.8b00949
- N. Abdi Goushbolagh, B. Farhood, A. Astani, A. Nikfarjam, M. Kalantari, M.H. Zare, Quantitative cytotoxicity, cellular uptake and radioprotection effect of cerium oxide nanoparticles in MRC-5 normal cells and MCF-7 cancerous cells. Bionanoscience 8, 769–777 (2018). https://doi.org/10.1007/s12668-018-0538-z
- Y. Gao, K. Chen, J.L. Ma, F. Gao, Cerium oxide nanoparticles in cancer. Onco Targets Ther. 7, 835–840 (2014). https://doi.org/10.2147/ott.s62057
- A.Z. Abbasi, C.R. Gordijo, M.A. Amini, A. Maeda, A.M. Rauth, R.S. DaCosta, X.Y. Wu, Hybrid manganese dioxide nanoparticles potentiate radiation therapy by modulating tumor hypoxia. Cancer Res. 76, 6643–6656 (2016). https://doi.org/10.1158/0008-5472.CAN-15-3475
- M. Durante, R. Orecchia, J.S. Loeffler, Charged-particle therapy in cancer: clinical uses and future perspectives. Nat. Rev. Clin. Oncol. 14, 483–495 (2017). https://doi.org/10.1038/nrclinonc.2017.30
- S. Lacombe, E. Porcel, E. Scifoni, Particle therapy and nanomedicine: state of art and research perspectives. Cancer Nanotechnol. 8, 9 (2017). https://doi.org/10.1186/s12645-017-0029-x
- P. Symonds, G.D.D. Jones, FLASH radiotherapy: the next technological advance in radiation therapy? Clin. Oncol. 31, 405–406 (2019). https://doi.org/10.1016/j.clon.2019.05.011
- A. Degiovanni, U. Amaldi, History of hadron therapy accelerators. Phys. Med. 31, 322–332 (2015). https://doi.org/10.1016/j.ejmp.2015.03.002
- M.I. Khot, H. Andrew, H.S. Svavarsdottir, G. Armstrong, A.J. Quyn, D.G. Jayne, A review on the scope of photothermal therapy-based nanomedicines in preclinical models of colorectal cancer. Clin. Colorectal Cancer 18, e200–e209 (2019). https://doi.org/10.1016/j.clcc.2019.02.001
- A. Bettaieb, P.K. Wrzal, D.A. Averill-Bates, Hyperthermia: Cancer Treatment and Beyond. Cancer treatment-conventional and innovative approaches. https://doi.org/10.5772/55795
- J. Wang, J. Qiu, A review of organic nanomaterials in photothermal cancer therapy. Cancer Res. Front. 2, 67–84 (2016). https://doi.org/10.17980/2016.67
- M.G. Lubner, C.L. Brace, J.L. Hinshaw, F.T. Lee, Microwave tumor ablation: mechanism of action, clinical results and devices. J. Vasc. Interv. Radiol. 21, S192–S203 (2010). https://doi.org/10.1038/jid.2014.371
- B. Zhang, M.A.J. Moser, E.M. Zhang, Y. Luo, C. Liu, W. Zhang, A review of radiofrequency ablation: large target tissue necrosis and mathematical modelling. Phys. Med. 32, 961–971 (2016). https://doi.org/10.1016/j.ejmp.2016.07.092
- M. Barajas, T. Fraga, M. Acevedo, R.G. Cabrera, Radiofrequency ablation: a review of current knowledge, therapeutic perspectives, complications, and contraindications. Int. J. Biosens. Bioelectron. 4, 53–55 (2018). https://doi.org/10.15406/ijbsbe.2018.04.00098
- P. Pantano, C.D. Harrison, J. Poulose, D. Urrabazo, T.Q. Norman et al., Factors affecting the 13.56-MHz radio-frequency-mediated heating of gold nanoparticles. Appl. Spectrosc. Rev. 52, 821–836 (2017). https://doi.org/10.1080/05704928.2017.1314299
- J. Beyk, H. Tavakoli, Selective radiofrequency ablation of tumor by magnetically targeting of multifunctional iron oxide-gold nanohybrid. J. Cancer Res. Clin. Oncol. 145, 2199–2209 (2019). https://doi.org/10.1007/s00432-019-02969-1
- J. Beik, Z. Abed, F.S. Ghoreishi, S. Hosseini-Nami, S. Mehrzadi, A. Shakeri-Zadeh, S.K. Kamrava, Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J. Control. Release 235, 205–221 (2016). https://doi.org/10.1016/j.jconrel.2016.05.062
- P. Das, M. Colombo, D. Prosperi, Recent advances in magnetic fluid hyperthermia for cancer therapy. Colloids Surf. B Biointerfaces 174, 42–55 (2019). https://doi.org/10.1016/j.colsurfb.2018.10.051
- S.K. Sharma, N. Shrivastava, F. Rossi, L.D. Tung, N.T.K. Thanh, Nanoparticles-based magnetic and photo induced hyperthermia for cancer treatment. Nano Today 100, 795 (2019). https://doi.org/10.1016/j.nantod.2019.100795
- J. Dulińska-Litewka, A. Łazarczyk, P. Hałubiec, O. Szafrański, K. Karnas, A. Karewicz, Superparamagnetic iron oxide nanoparticles-current and prospective medical applications. Materials 12, 617 (2019). https://doi.org/10.3390/ma12040617
- Z. Ashikbayeva, D. Tosi, D. Balmassov, E. Schena, P. Saccomandi, V. Inglezakis, Application of nanoparticles and nanomaterials in thermal ablation therapy of cancer. Nanomaterials 9, 1195 (2019). https://doi.org/10.3390/nano9091195
- G. Hemery, C. Genevois, F. Couillaud, S. Lacomme, E. Gontier et al., Monocore: vs. multicore magnetic iron oxide nanoparticles: uptake by glioblastoma cells and efficiency for magnetic hyperthermia. Mol. Syst. Des. Eng. 2, 629–639 (2017). https://doi.org/10.1039/c7me00061h
- L. Kafrouni, O. Savadogo, Recent progress on magnetic nanoparticles for magnetic hyperthermia. Prog. Biomater. 5, 147–160 (2016). https://doi.org/10.1007/s40204-016-0054-6
- S. Kalia, S. Kango, A. Kumar, Y. Haldorai, B. Kumari, R. Kumar, Magnetic polymer nanocomposites for environmental and biomedical applications. Colloid Polym. Sci. 292, 2025–2052 (2014). https://doi.org/10.1007/s00396-014-3357-y
- G. Lavorato, E. Lima, M. Vasquez Mansilla, H. Troiani, R. Zysler, E. Winkler, Bifunctional CoFe2O4/ZnO core/shell nanoparticles for magnetic fluid hyperthermia with controlled optical response. J. Phys. Chem. C 122, 3047–3057 (2018). https://doi.org/10.1021/acs.jpcc.7b11115
- S.V. Jadhav, P.S. Shewale, B.C. Shin, M.P. Patil, G.D. Kim et al., Study of structural and magnetic properties and heat induction of gadolinium-substituted manganese zinc ferrite nanoparticles for in vitro magnetic fluid hyperthermia. J. Colloid Interface Sci. 541, 192–203 (2019). https://doi.org/10.1016/j.jcis.2019.01.063
- M. Coşkun, M. Korkmaz, The effect of SiO2 shell thickness on the magnetic properties of ZnFe2O4 nanoparticles. J. Nanoparticle Res. 16, 2316 (2014). https://doi.org/10.1007/s11051-014-2316-3
- L. León Félix, B. Sanz, V. Sebastián, T.E. Torres, M.H. Sousa et al., Gold-decorated magnetic nanoparticles design for hyperthermia applications and as a potential platform for their surface-functionalization. Sci. Rep. 9, 1–11 (2019). https://doi.org/10.1038/s41598-019-40769-2
- K. Wu, D. Su, J. Liu, R. Saha, J.P. Wang, Magnetic nanoparticles in nanomedicine: a review of recent advances. Nanotechnology 30, 502003 (2019). https://doi.org/10.1088/1361-6528/ab4241
- S. Hatamie, B. Parseh, M.M. Ahadian, F. Naghdabadi, R. Saber, M. Soleimani, Heat transfer of PEGylated cobalt ferrite nanofluids for magnetic fluid hyperthermia therapy: in vitro cellular study. J. Magn. Magn. Mater. 462, 185–194 (2018). https://doi.org/10.1016/j.jmmm.2018.05.020
- G. Kandasamy, A. Sudame, T. Luthra, K. Saini, D. Maity, Functionalized hydrophilic superparamagnetic iron oxide nanoparticles for magnetic fluid hyperthermia application in liver cancer treatment. ACS Omega 3, 3991–4005 (2018). https://doi.org/10.1021/acsomega.8b00207
- P.M. Price, W.E. Mahmoud, A.A. Al-Ghamdi, L.M. Bronstein, Magnetic drug delivery: where the field is going. Front. Chem. 6, 1–7 (2018). https://doi.org/10.3389/fchem.2018.00619
- J. Cardinal, J.R. Klune, E. Chory, G. Jeyabalan, J.S. Kanzius, M. Nalesnik, D.A. Geller, Non-invasive radiofrequency ablation of cancer targeted by gold nanoparticles. Surgery 144, 125–132 (2008). https://doi.org/10.1016/j.surg.2008.03.036.NON-INVASIVE
- S.M. Amini, S. Kharrazi, S.M. Rezayat, K. Gilani, Radiofrequency electric field hyperthermia with gold nanostructures: role of particle shape and surface chemistry. Artif. Cells Nanomed. Biotechnol. 46, 1452–1462 (2018). https://doi.org/10.1080/21691401.2017.1373656
- Y.L. Shao, B. Arjun, H.L. Leo, K.J. Chua, Nano-assisted radiofrequency ablation of clinically extracted irregularly-shaped liver tumors. J. Therm. Biol 66, 101–113 (2017). https://doi.org/10.1016/j.jtherbio.2017.04.005
- C.J. Gannon, P. Cherukuri, B.I. Yakobson, L. Cognet, J.S. Kanzius et al., Carbon nanotube-enhanced thermal destruction of cancer cells in a noninvasive radiofrequency field. Cancer 110, 2654–2665 (2007). https://doi.org/10.1002/cncr.23155
- D. Bijukumar, C.M. Girish, A. Sasidharan, S. Nair, M. Koyakutty, Transferrin-conjugated biodegradable graphene for targeted radiofrequency ablation of hepatocellular carcinoma. ACS Biomater. Sci. Eng. 1, 1211–1219 (2015). https://doi.org/10.1021/acsbiomaterials.5b00184
- G. Raniszewski, A. Miaskowski, S. Wiak, The application of carbon nanotubes in magnetic fluid hyperthermia. J. Nanomater. 2015, 527652 (2015). https://doi.org/10.1155/2015/527652
- H. Wu, G. Liu, X. Wang, J. Zhang, Y. Chen et al., Solvothermal synthesis of cobalt ferrite nanoparticles loaded on multiwalled carbon nanotubes for magnetic resonance imaging and drug delivery. Acta Biomater. 7, 3496–3504 (2011). https://doi.org/10.1016/j.actbio.2011.05.031
- R. Singh, S.V. Torti, Carbon nanotubes in hyperthermia therapy. Adv. Drug Deliv. Rev. 65, 2045–2060 (2013). https://doi.org/10.1016/j.addr.2013.08.001
- F. Saghatchi, M. Mohseni-Dargah, S. Akbari-Birgani, S. Saghatchi, B. Kaboudin, Cancer therapy and imaging through functionalized carbon nanotubes decorated with magnetite and gold nanoparticles as a multimodal tool. Appl. Biochem. Biotechnol. 191, 1280–1293 (2020). https://doi.org/10.1007/s12010-020-03280-3
- K.P. Tamarov, L.A. Osminkina, S.V. Zinovyev, K.A. Maximova, J.V. Kargina et al., Radio frequency radiation-induced hyperthermia using Si nanoparticle-based sensitizers for mild cancer therapy. Sci. Rep. 4, 7034 (2014). https://doi.org/10.1038/srep07034
- M. Gongalsky, G. Gvindzhiliia, K. Tamarov, O. Shalygina, A. Pavlikov et al., Radiofrequency hyperthermia of cancer cells enhanced by silicic acid ions released during the biodegradation of porous silicon nanowires. ACS Omega 4, 10662–10669 (2019). https://doi.org/10.1021/acsomega.9b01030
- A. Ashokan, V.H. Somasundaram, G.S. Gowd, I.M. Anna, G.L. Malarvizhi et al., Biomineral nano-theranostic agent for magnetic resonance image guided, augmented radiofrequency ablation of liver tumor. Sci. Rep. 7, 1–15 (2017). https://doi.org/10.1038/s41598-017-14976-8
- E.S. Glazer, S.A. Curley, Non-invasive radiofrequency ablation of malignancies mediated by quantum dots, gold nanoparticles and carbon nanotubes. Ther. Deliv. 2, 1325–1330 (2011). https://doi.org/10.1038/jid.2014.371
- E.S. Glazer, S.A. Curley, Radiofrequency field-induced thermal cytotoxicity in cancer cells treated with fluorescent nanoparticles. Cancer 116, 3285–3293 (2010). https://doi.org/10.1002/cncr.25135
- L. Sidoff, D.E. Dupuy, Clinical experiences with microwave thermal ablation of lung malignancies. Int. J. Hyperth. 33, 25–33 (2017). https://doi.org/10.1080/02656736.2016.1204630
- C. Kim, Understanding the nuances of microwave ablation for more accurate post-treatment assessment. Future Oncol. 14, 1755–1764 (2018). https://doi.org/10.2217/fon-2017-0736
- L. Tan, W. Tang, T. Liu, X. Ren, C. Fu et al., Biocompatible hollow polydopamine nanoparticles loaded ionic liquid enhanced tumor microwave thermal ablation in vivo. ACS Appl. Mater. Interfaces. 8, 11237–11245 (2016). https://doi.org/10.1021/acsami.5b12329
- B. Beckler, A. Cowan, N. Farrar, A. Murawski, A. Robinson et al., Microwave Heating of antibody-functionalized carbon nanotubes as a feasible cancer treatment. Biomed. Phys. Eng. Exp. 4, 831 (2018). https://doi.org/10.1088/2057-1976/aac9fe
- L. Wen, W. Ding, S. Yang, D. Xing, Microwave pumped high-efficient thermoacoustic tumor therapy with single wall carbon nanotubes. Biomaterials 75, 163–173 (2016). https://doi.org/10.1016/j.biomaterials.2015.10.028
- L. Wen, S. Yang, J. Zhong, Q. Zhou, D. Xing, Thermoacoustic imaging and therapy guidance based on ultra-short pulsed microwave pumped thermoelastic effect induced with superparamagnetic iron oxide nanoparticles. Theranostics 7, 1976–1989 (2017). https://doi.org/10.7150/thno.17846
- M. Jelbuldina, A. Korobeinyk, S. Korganbayev, D. Tosi, K. Dukenbayev, V.J. Inglezakis, Real-time temperature monitoring in liver during magnetite nanoparticle-enhanced microwave ablation with fiber bragg grating sensors: ex vivo analysis. IEEE Sens. J. 18, 8005–8011 (2018). https://doi.org/10.1109/JSEN.2018.2865100
- T. Tang, X. Xu, Z. Wang, J. Tian, Y. Yang, C. Ou, H. Bao, T. Liu, Cu2ZnSnS4 nanocrystals for microwave thermal and microwave dynamic combination tumor therapy. Chem. Commun. 55, 13148–13151 (2019). https://doi.org/10.1039/c9cc07762f
- H. Peng, J. Ouyang, Y. Peng, A simple approach for the synthesis of bi-functional Fe3O4@WO3-x core–shell nanoparticles with magnetic-microwave to heat responsive properties. Inorg. Chem. Commun. 84, 138–143 (2017). https://doi.org/10.1016/j.inoche.2017.08.004
- N.R. Paudel, D. Shvydka, E.I. Parsai, A novel property of gold nanoparticles: free radical generation under microwave irradiation. Med. Phys. 43, 1598–1602 (2016). https://doi.org/10.1118/1.4942811
- B. Kioko, T. Ogundolie, M. Adebiyi, Y. Ettinoffe, C. Rhodes et al., De-crystallization of uric acid crystals in synovial fluid using gold colloids and microwave heating. Nano Biomed. Eng. 6, 104–110 (2014). https://doi.org/10.5101/nbe.v6i4.p104-110
- G.L. McLemore, S. Toker, Z. Boone-Kukoyi, H. Ajifa, C. Lansiquot et al., Microwave heating of crystals with gold nanoparticles and synovial fluid under synthetic skin patches. ACS Omega 2, 5992–6002 (2017). https://doi.org/10.1021/acsomega.7b00816
- F.H. Ghahremani, A. Sazgarnia, M.H. Bahreyni-Toosi, O. Rajabi, A. Aledavood, Efficacy of microwave hyperthermia and chemotherapy in the presence of gold nanoparticles: an in vitro study on osteosarcoma. Int. J. Hyperth. 27, 625–636 (2011). https://doi.org/10.3109/02656736.2011.587363
- R. Moradpoor, S.A. Aledavood, O. Rajabi, J.K. Chamani, A. Sazgarnia, Enhancement of cisplatin efficacy by gold nanoparticles or microwave hyperthermia? An in vitro study on a melanoma cell line. Int. J. Cancer Manag. 10, 1–8 (2017). https://doi.org/10.17795/ijcp-5925
- X. Chu, L. Mao, O. Johnson, K. Li, J. Phan, Y. Zhang et al., Exploration of TiO2 nanoparticle mediated microdynamic therapy on cancer treatment. Nanomed. Nanotechnol. Biol. Med. 18, 272–281 (2019). https://doi.org/10.1016/j.nano.2019.02.016
- S. Wang, X.G. Mei, S.N. Goldberg, M. Ahmed, J.C. Lee et al., Does thermosensitive liposomal vinorelbine improve end-point survival after percutaneous radiofrequency ablation of liver tumors in a mouse model? Radiology 279, 762–772 (2016). https://doi.org/10.1148/radiol.2015150787
- S. Wu, D. Zhang, J. Yu, J. Dou, X. Li, M. Mu, P. Liang, Chemotherapeutic nanoparticle-based liposomes enhance the efficiency of mild microwave ablation in hepatocellular carcinoma therapy. Front. Pharmacol. 11, 1–9 (2020). https://doi.org/10.3389/fphar.2020.00085
- J.P. Dou, Q. Wu, C.H. Fu, D.Y. Zhang, J. Yu, X.W. Meng, P. Liang, Amplified intracellular Ca2+ for synergistic anti-tumor therapy of microwave ablation and chemotherapy. J. Nanobiotechnol. 17, 1–17 (2019). https://doi.org/10.1186/s12951-019-0549-0
- A.C.V. Doughty, A.R. Hoover, E. Layton, C.K. Murray, E.W. Howard, W.R. Chen, Nanomaterial applications in photothermal therapy for cancer. Materials 12, 779 (2019). https://doi.org/10.3390/ma12050779
- J. Liang, H. Liu, J. Yu, L. Zhou, J. Zhu, Plasmon-enhanced solar vapor generation. Nanophotonics 8, 771–786 (2019). https://doi.org/10.1515/nanoph-2019-0039
- M. Kim, J.H. Lee, J.M. Nam, Plasmonic photothermal nanoparticles for biomedical applications. Adv. Sci. 6, 1900471 (2019). https://doi.org/10.1002/advs.201900471
- W. Wei, X. Zhang, S. Zhang, G. Wei, Z. Su, Biomedical and bioactive engineered nanomaterials for targeted tumor photothermal therapy: a review. Mater. Sci. Eng., C 104, 109891 (2019). https://doi.org/10.1016/j.msec.2019.109891
- W. Yang, H. Liang, S. Ma, D. Wang, J. Huang, Gold nanoparticle based photothermal therapy: development and application for effective cancer treatment. Sustain. Mater. Technol. 22, e00109 (2019). https://doi.org/10.1016/j.susmat.2019.e00109
- M.R.K. Ali, Y. Wu, M.A. El-Sayed, Gold-nanoparticle-assisted plasmonic photothermal therapy advances toward clinical application. J. Phys. Chem. C 123, 15375–15393 (2019). https://doi.org/10.1021/acs.jpcc.9b01961
- M. Sancho-Albero, N. Navascués, G. Mendoza, V. Sebastián, M. Arruebo, P. Martín-Duque, J. Santamaría, Exosome origin determines cell targeting and the transfer of therapeutic nanoparticles towards target cells. J. Nanobiotechnol. 17, 1–13 (2019). https://doi.org/10.1186/s12951-018-0437-z
- J. Estelrich, M. Antònia Busquets, Iron oxide nanoparticles in photothermal therapy. Molecules 23, 1567 (2018). https://doi.org/10.3390/molecules23071567
- G.H. Lu, W.T. Shang, H. Deng, Z.Y. Han, M. Hu et al., Targeting carbon nanotubes based on IGF-1R for photothermal therapy of orthotopic pancreatic cancer guided by optical imaging. Biomaterials 195, 13–22 (2019). https://doi.org/10.1016/j.biomaterials.2018.12.025
- J. Mou, T. Lin, F. Huang, H. Chen, J. Shi, Black titania-based theranostic nanoplatform for single NIR laser induced dual-modal imaging-guided PTT/PDT. Biomaterials 84, 13–24 (2016). https://doi.org/10.1016/j.biomaterials.2016.01.009
- J.B. Vines, D.J. Lim, H. Park, Contemporary polymer-based nanoparticle systems for photothermal therapy. Polymers 10, 1–16 (2018). https://doi.org/10.3390/polym10121357
- J. Wang, R. Yan, F. Guo, M. Yu, F. Tan, N. Li, Targeted lipid-polyaniline hybrid nanoparticles for photoacoustic imaging guided photothermal therapy of cancer. Nanotechnology 27, 285102 (2016). https://doi.org/10.1088/0957-4484/27/28/285102
- A.F. Dos Santos, D.R.Q. De Almeida, L.F. Terra, M.S. Baptista, L. Labriola, Photodynamic therapy in cancer treatment—an update review. J. Cancer Metastasis Treat 5, 25 (2019). https://doi.org/10.20517/2394-4722.2018.83
- S. Mallidi, S. Anbil, A.L. Bulin, G. Obaid, M. Ichikawa, T. Hasan, Beyond the barriers of light penetration: strategies, perspectives and possibilities for photodynamic therapy. Theranostics 6, 2458–2487 (2016). https://doi.org/10.7150/thno.16183
- D. van Straten, V. Mashayekhi, H.S. de Bruijn, S. Oliveira, D.J. Robinson, Oncologic photodynamic therapy: basic principles, current clinical status and future directions. Cancers 9, 1–54 (2017). https://doi.org/10.3390/cancers9020019
- X. Li, J.F. Lovell, J. Yoon, X. Chen, Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol. (2020). https://doi.org/10.1038/s41571-020-0410-2
- R. Baskaran, J. Lee, S.-G. Yang, Clinical development of photodynamic agents and therapeutic applications. Biomater. Res. 22, 1–8 (2018). https://doi.org/10.1186/s40824-018-0140-z
- M. Lismont, L. Dreesen, S. Wuttke, Metal-organic framework nanoparticles in photodynamic therapy: current status and perspectives. Adv. Funct. Mater. 27, 1–16 (2017). https://doi.org/10.1002/adfm.201606314
- S.S. Lucky, K.C. Soo, Y. Zhang, Nanoparticles in photodynamic therapy. Chem. Rev. 115, 1990–2042 (2015). https://doi.org/10.1021/cr5004198
- D. Lu, R. Tao, Z. Wang, Carbon-based materials for photodynamic therapy: a mini-review. Front. Chem. Sci. Eng. 13, 310–323 (2019). https://doi.org/10.1007/s11705-018-1750-7
- J. Bogdan, J. Pławińska-Czarnak, J. Zarzyńska, Nanoparticles of titanium and zinc oxides as novel agents in tumor treatment: a review. Nanoscale Res. Lett. 12, 225 (2017). https://doi.org/10.1186/s11671-017-2007-y
- Z. Youssef, R. Vanderesse, L. Colombeau, F. Baros, T. Roques-Carmes et al., The application of titanium dioxide, zinc oxide, fullerene, and graphene nanoparticles in photodynamic therapy. Cancer Nanotechnol. 8, 6 (2017). https://doi.org/10.1186/s12645-017-0032-2
- A. Grebinyk, S. Grebinyk, S. Prylutska, U. Ritter, O. Matyshevska, T. Dandekar, M. Frohme, C 60 fullerene accumulation in human leukemic cells and perspectives of LED-mediated photodynamic therapy. Free Radic. Biol. Med. 124, 319–327 (2018). https://doi.org/10.1016/j.freeradbiomed.2018.06.022
- A. Ancona, B. Dumontel, N. Garino, B. Demarco, D. Chatzitheodoridou et al., Lipid-coated zinc oxide nanoparticles as innovative ROS-generators for photodynamic therapy in cancer cells. Nanomaterials 8, 143 (2018). https://doi.org/10.3390/nano8030143
- F.U. Rehman, C. Zhao, H. Jiang, X. Wang, Biomedical applications of nano-titania in theranostics and photodynamic therapy. Biomater. Sci. 4, 40–54 (2016). https://doi.org/10.1039/c5bm00332f
- D. Ziental, B. Czarczynska-Goslinska, D.T. Mlynarczyk, A. Glowacka-Sobotta, B. Stanisz, T. Goslinski, L. Sobotta, Titanium dioxide nanoparticles: prospects and applications in medicine. Nanomaterials 10, 387 (2020). https://doi.org/10.3390/nano10020387
- W. Ni, M. Li, J. Cui, Z. Xing, Z. Li et al., 808 nm light triggered black TiO2 nanoparticles for killing of bladder cancer cells. Mater. Sci. Eng., C 81, 252–260 (2017). https://doi.org/10.1016/j.msec.2017.08.020
- C. Yi, Z. Yu, Q. Ren, X. Liu, Y. Wang et al., Nanoscale ZnO-based photosensitizers for photodynamic therapy. Photodiagnosis Photodyn. Ther. 30, 101694 (2020). https://doi.org/10.1016/j.pdpdt.2020.101694
- J. Gupta, D. Bahadur, Visible light sensitive mesoporous cu-substituted zno nanoassembly for enhanced photocatalysis, bacterial inhibition, and noninvasive tumor regression. ACS Sustain. Chem. Eng. 5, 8702–8709 (2017). https://doi.org/10.1021/acssuschemeng.7b01433
- M. Sivasubramanian, Y.C. Chuang, L.W. Lo, Evolution of nanoparticle-mediated photodynamic therapy: from superficial to deep-seated cancers. Molecules 24, 520 (2019). https://doi.org/10.3390/molecules24030520
- C. Zhang, K. Zhao, W. Bu, D. Ni, Y. Liu, J. Feng, J. Shi, Marriage of scintillator and semiconductor for synchronous radiotherapy and deep photodynamic therapy with diminished oxygen dependence. Angew. Chem. Int. Ed. 127, 1790–1794 (2015). https://doi.org/10.1002/ange.201408472
- G.M.F. Calixto, J. Bernegossi, L.M. De Freitas, C.R. Fontana, M. Chorilli, A.M. Grumezescu, Nanotechnology-based drug delivery systems for photodynamic therapy of cancer: a review. Molecules 21, 1–18 (2016). https://doi.org/10.3390/molecules21030342
- G. Yi, S.H. Hong, J. Son, J. Yoo, C. Park, Y. Choi, H. Koo, Recent advances in nanoparticle carriers for photodynamic therapy. Quant. Imaging Med. Surg. 8, 433–443 (2018). https://doi.org/10.21037/qims.2018.05.04
- G. Yang, L. Xu, Y. Chao, J. Xu, X. Sun et al., Hollow MnO2 as a tumor-microenvironment-responsive biodegradable nano-platform for combination therapy favoring antitumor immune responses. Nat. Commun. 8, 902 (2017). https://doi.org/10.1038/s41467-017-01050-0
- H. Shibaguchi, H. Tsuru, M. Kuroki, M. Kuroki, Sonodynamic cancer therapy: a non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer Res. 31, 2425–2430 (2011)
- Z. Izadifar, P. Babyn, D. Chapman, Mechanical and biological effects of ultrasound: a review of present knowledge. Ultrasound Med. Biol. 43, 1085–1104 (2017). https://doi.org/10.1016/j.ultrasmedbio.2017.01.023
- H. Xu, X. Zhang, R. Han, P. Yang, H. Ma et al., Nanoparticles in sonodynamic therapy: state of the art review. RSC Adv. 6, 50697–50705 (2016). https://doi.org/10.1039/c6ra06862f
- G.Y. Wan, Y. Liu, B.W. Chen, Y.Y. Liu, Y.S. Wang, N. Zhang, Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol. Med. 13, 325–338 (2016). https://doi.org/10.20892/j.issn.2095-3941.2016.0068
- A.P. Sviridov, L.A. Osminkina, A.L. Nikolaev, A.A. Kudryavtsev, A.N. Vasiliev, V.Y. Timoshenko, Lowering of the cavitation threshold in aqueous suspensions of porous silicon nanoparticles for sonodynamic therapy applications. Appl. Phys. Lett. 107, 123107 (2015). https://doi.org/10.1063/1.4931728
- L.A. Osminkina, A.L. Nikolaev, A.P. Sviridov, N.V. Andronova, K.P. Tamarov et al., Porous silicon nanoparticles as efficient sensitizers for sonodynamic therapy of cancer. Microporous Mesoporous Mater. 210, 169–175 (2015). https://doi.org/10.1016/j.micromeso.2015.02.037
- J.T. Seil, T.J. Webster, Antibacterial effect of zinc oxide nanoparticles combined with ultrasound. Nanotechnology 23, 495101 (2012). https://doi.org/10.1088/0957-4484/23/49/495101
- A. Ebrahimi Fard, A. Zarepour, A. Zarrabi, A. Shanei, H. Salehi, Synergistic effect of the combination of triethylene-glycol modified Fe3O4 nanoparticles and ultrasound wave on MCF-7 cells. J. Magn. Magn. Mater. 394, 44–49 (2015). https://doi.org/10.1016/j.jmmm.2015.06.040
- A. Marino, M. Battaglini, D. De Pasquale, A. Degl’Innocenti, G. Ciofani, Ultrasound-activated piezoelectric nanoparticles inhibit proliferation of breast cancer cells. Sci. Rep. 8, 1–13 (2018). https://doi.org/10.1038/s41598-018-24697-1
- M. Lafond, S. Yoshizawa, S. Ichiro Umemura, Sonodynamic therapy: advances and challenges in clinical translation. J. Ultrasound Med. 38, 567–580 (2019). https://doi.org/10.1002/jum.14733
- X. Wang, H. Chen, Y. Zheng, M. Ma, Y. Chen et al., Au-nanoparticle coated mesoporous silica nanocapsule-based multifunctional platform for ultrasound mediated imaging, cytoclasis and tumor ablation. Biomaterials 34, 2057–2068 (2013). https://doi.org/10.1016/j.biomaterials.2012.11.044
- C. Brazzale, R. Canaparo, L. Racca, F. Foglietta, G. Durando et al., Enhanced selective sonosensitizing efficacy of ultrasound-based anticancer treatment by targeted gold nanoparticles. Nanomedicine 12, 3053–3070 (2016). https://doi.org/10.2217/nnm-2016-0293
- V. Bernard, V. Mornstein, J. Jaroš, M. Sedláčková, J. Škorpíková, Combined effect of silver nanoparticles and therapeutical ultrasound on ovarian carcinoma cells A2780. J. Appl. Biomed. 12, 137–145 (2014). https://doi.org/10.1016/j.jab.2014.01.002
- X. Han, J. Huang, X. Jing, D. Yang, H. Lin et al., Oxygen-deficient black titania for synergistic/enhanced sonodynamic and photoinduced cancer therapy at near infrared-II biowindow. ACS Nano 12, 4545–4555 (2018). https://doi.org/10.1021/acsnano.8b00899
- S.A.R. Dibaji, M.F. Al-Rjoub, M.R. Myers, R.K. Banerjee, Enhanced heat transfer and thermal dose using magnetic nanoparticles during HIFU thermal ablation-an in vitro study. J. Nanotechnol. Eng. Med. 4, 040902 (2013). https://doi.org/10.1115/1.4027340
- O.K. Kosheleva, T.C. Lai, N.G. Chen, M. Hsiao, C.H. Chen, Selective killing of cancer cells by nanoparticle-assisted ultrasound. J. Nanobiotechnol. 14, 46 (2016). https://doi.org/10.1186/s12951-016-0194-9
- F. Gong, L. Cheng, N. Yang, O. Betzer, L. Feng et al., Ultrasmall oxygen-deficient bimetallic oxide mnwox nanoparticles for depletion of endogenous gsh and enhanced sonodynamic cancer therapy. Adv. Mater. 31, 1–9 (2019). https://doi.org/10.1002/adma.201900730
- A. Sviridov, K. Tamarov, I. Fesenko, W. Xu, V. Andreev, V. Timoshenko, V.P. Lehto, Cavitation induced by Janus-like mesoporous silicon nanoparticles enhances ultrasound hyperthermia. Front. Chem. 7, 1–12 (2019). https://doi.org/10.3389/fchem.2019.00393
- A. Kharin, O. Syshchyk, A. Geloen, S. Alekseev, A. Rogov, V. Lysenko, V. Timoshenko, Carbon fluoroxide nanoparticles as fluorescent labels and sonosensitizers for theranostic applications. Sci. Technol. Adv. Mater. 16, 44601 (2015). https://doi.org/10.1088/1468-6996/16/4/044601
- X. Pan, L. Bai, H. Wang, Q. Wu, H. Wang et al., Metal–organic-framework-derived carbon nanostructure augmented sonodynamic cancer therapy. Adv. Mater. 30, 1–9 (2018). https://doi.org/10.1002/adma.201800180
- A. Marino, E. Almici, S. Migliorin, C. Tapeinos, M. Battaglini et al., Piezoelectric barium titanate nanostimulators for the treatment of glioblastoma multiforme. J. Colloid Interface Sci. 538, 449–461 (2019). https://doi.org/10.1016/j.jcis.2018.12.014
- M.C. d’Agostino, K. Craig, E. Tibalt, S. Respizzi, Shock wave as biological therapeutic tool: from mechanical stimulation to recovery and healing, through mechanotransduction. Int. J. Surg. 24, 147–153 (2015). https://doi.org/10.1016/j.ijsu.2015.11.030
- F. Foglietta, S. Duchi, R. Canaparo, G. Varchi, E. Lucarelli, B. Dozza, L. Serpe, Selective sensitiveness of mesenchymal stem cells to shock waves leads to anticancer effect in human cancer cell co-cultures. Life Sci. 173, 28–35 (2017). https://doi.org/10.1016/j.lfs.2017.01.009
- F. Marano, R. Frairia, L. Rinella, M. Argenziano, B. Bussolati et al., Combining doxorubicin-nanobubbles and shockwaves for anaplastic thyroid cancer treatment: preclinical study in a xenograft mouse model. Endocr. Relat. Cancer 24, 275–286 (2017). https://doi.org/10.1530/ERC-17-0045
- R. Canaparo, L. Serpe, G.P. Zara, R. Chiarle, L. Berta, R. Frairia, High energy shock waves (HESW) increase paclitaxel efficacy in a syngeneic model of breast cancer. Technol. Cancer Res. Treat. 7, 117–124 (2008). https://doi.org/10.1177/153303460800700204
- J. Zhang, S. Shrivastava, R.O. Cleveland, T.H. Rabbitts, Lipid-mRNA nanoparticle designed to enhance intracellular delivery mediated by shock waves. ACS Appl. Mater. Interfaces. 11, 10481–10491 (2019). https://doi.org/10.1021/acsami.8b21398
- L.M. López-Marín, A.L. Rivera, F. Fernández, A.M. Loske, Shock wave-induced permeabilization of mammalian cells. Phys. Life Rev. 26–27, 1–38 (2018). https://doi.org/10.1016/j.plrev.2018.03.001
- R. Canaparo, L. Serpe, M.G. Catalano, O. Bosco, G.P. Zara, L. Berta, R. Frairia, High energy shock waves (HESW) for sonodynamic therapy: effects on HT-29 human colon cancer cells. Anticancer Res. 26, 3337–3342 (2006)
- L. Serpe, R. Canaparo, L. Berta, A. Bargoni, G.P. Zara, R. Frairia, High energy shock waves and 5-aminolevulinic for sonodynamic therapy: effects in a syngeneic model of colon cancer. Technol. Cancer Res. Treat. 10, 85–93 (2011). https://doi.org/10.7785/tcrt.2012.500182
- F. Foglietta, R. Canaparo, A. Francovich, F. Arena, S. Civera et al., Sonodynamic treatment as an innovative bimodal anticancer approach: shock wave-mediated tumor growth inhibition in a syngeneic breast cancer model. Discov. Med. 20, 197–205 (2015)
- G. Varchi, F. Foglietta, R. Canaparo, M. Ballestri, F. Arena et al., Engineered porphyrin loaded core-shell nanoparticles for selective sonodynamic anticancer treatment. Nanomedicine 10, 3483–3494 (2015). https://doi.org/10.2217/nnm.15.150
- R. Canaparo, G. Varchi, M. Ballestri, F. Foglietta, G. Sotgiu et al., Polymeric nanoparticles enhance the sonodynamic activity of meso-tetrakis (4-sulfonatophenyl) porphyrin in an in vitro neuroblastoma model. Int. J. Nanomed. 8, 4247–4263 (2013). https://doi.org/10.2147/IJN.S51070
- L. Wang, D. Meng, Y. Hao, Y. Zhao, D. Li et al., Gold nanostars mediated combined photothermal and photodynamic therapy and X-ray imaging for cancer theranostic applications. J. Biomater. Appl. 30, 547–557 (2015). https://doi.org/10.1177/0885328215594481
- A. Shanei, H. Akbari-Zadeh, Investigating the sonodynamic-radiosensitivity effect of gold nanoparticles on HeLa cervical cancer cells. J. Korean Med. Sci. 34, 1–15 (2019). https://doi.org/10.3346/jkms.2019.34.e243
- Z. Behrouzkia, Z. Joveini, B. Keshavarzi, N. Eyvazzadeh, R.Z. Aghdam, Hyperthermia: how can it be used? Oman Med. J. 31, 89–97 (2016). https://doi.org/10.5001/omj.2016.19
- P.S. Jiang, H.Y. Tsai, P. Drake, F.N. Wang, C.S. Chiang, Gadolinium-doped iron oxide nanoparticles induced magnetic field hyperthermia combined with radiotherapy increases tumour response by vascular disruption and improved oxygenation. Int. J. Hyperth. 6736, 1–9 (2017). https://doi.org/10.1080/02656736.2017.1308019
- M. Li, Q. Zhao, X. Yi, X. Zhong, G. Song et al., Au@MnS@ZnS core/shell/shell nanoparticles for magnetic resonance imaging and enhanced cancer radiation therapy. ACS Appl. Mater. Interfaces. 8, 9557–9564 (2016). https://doi.org/10.1021/acsami.5b11588
- N. Ma, Y.W. Jiang, X. Zhang, H. Wu, J.N. Myers et al., Enhanced radiosensitization of gold nanospikes via hyperthermia in combined cancer radiation and photothermal therapy. ACS Appl. Mater. Interfaces. 8, 28480–28494 (2016). https://doi.org/10.1021/acsami.6b10132
- J.F. Hainfeld, L. Lin, L. Slatkin, F. Avraham Dilmanian, T.M. Vadas, H.M. Smilowitz, Gold nanoparticle hyperthermia reduces radiotherapy dose. Nanomed. Nanotechnol. Biol. Med. 10, 1609–1617 (2014). https://doi.org/10.1016/j.nano.2014.05.006
- X. Yu, A. Li, C. Zhao, K. Yang, X. Chen, W. Li, Ultrasmall semimetal nanoparticles of bismuth for dual-modal computed tomography/photoacoustic imaging and synergistic thermoradiotherapy. ACS Nano 11, 3990–4001 (2017). https://doi.org/10.1021/acsnano.7b00476
- F. Daneshvar, F. Salehi, M. Karimi, R.D. Vais, M.A. Mosleh-Shirazi, N. Sattarahmady, Combined X-ray radiotherapy and laser photothermal therapy of melanoma cancer cells using dual-sensitization of platinum nanoparticles. J. Photochem. Photobiol. B Biol. 203, 111737 (2020). https://doi.org/10.1016/j.jphotobiol.2019.111737
- M. Zhou, Y. Chen, M. Adachi, X. Wen, B. Erwin et al., Single agent nanoparticle for radiotherapy and radio-photothermal therapy in anaplastic thyroid cancer. Biomaterials 57, 41–49 (2015). https://doi.org/10.1016/j.biomaterials.2015.04.013
- V. Hosseini, M. Mirrahimi, A. Shakeri-Zadeh, F. Koosha, B. Ghalandari et al., Multimodal cancer cell therapy using Au@Fe2O3 core–shell nanoparticles in combination with photo-thermo-radiotherapy. Photodiagnosis Photodyn. Ther. 24, 129–135 (2018). https://doi.org/10.1016/j.pdpdt.2018.08.003
- M.M. Movahedi, Z. Alamzadeh, S. Hosseini-Nami, A. Shakeri-Zadeh, G. Taheripak et al., Investigating the mechanisms behind extensive death in human cancer cells following nanoparticle assisted photo-thermo-radiotherapy. Photodiagnosis Photodyn. Ther. 29, 101600 (2020). https://doi.org/10.1016/j.pdpdt.2019.101600
- J. Liu, Y. Yang, W. Zhu, X. Yi, Z. Dong et al., Nanoscale metal-organic frameworks for combined photodynamic and radiation therapy in cancer treatment. Biomaterials 97, 1–9 (2016). https://doi.org/10.1016/j.biomaterials.2016.04.034
- C. Western, D. Hristov, J. Schlosser, Ultrasound imaging in radiation therapy: from interfractional to intrafractional guidance. Cureus 7, 1–19 (2015). https://doi.org/10.7759/cureus.280
- R. Cirincione, F.M. Di Maggio, G.I. Forte, L. Minafra, V. Bravatà et al., High-intensity focused ultrasound- and radiation therapy-induced immuno-modulation: comparison and potential opportunities. Ultrasound Med. Biol. 43, 398–411 (2017). https://doi.org/10.1016/j.ultrasmedbio.2016.09.020
- X. Liu, Y. Zhang, Y. Wang, W. Zhu, G. Li et al., Comprehensive understanding of magnetic hyperthermia for improving antitumor therapeutic efficacy. Theranostics 10, 3793–3815 (2020). https://doi.org/10.7150/thno.40805
- A. Espinosa, R. Di Corato, J. Kolosnjaj-Tabi, P. Flaud, T. Pellegrino, C. Wilhelm, Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment. ACS Nano 10, 2436–2446 (2016). https://doi.org/10.1021/acsnano.5b07249
- X. Ma, Y. Wang, X.L. Liu, H. Ma, G. Li et al., Fe3O4-Pd Janus nanoparticles with amplified dual-mode hyperthermia and enhanced ROS generation for breast cancer treatment. Nanoscale Horiz. 4, 1450–1459 (2019). https://doi.org/10.1039/c9nh00233b
- R. Di Corato, G. Béalle, J. Kolosnjaj-Tabi, A. Espinosa, O. Clément et al., Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes. ACS Nano 9, 2904–2916 (2015). https://doi.org/10.1021/nn506949t
- A. Curcio, A.K.A. Silva, S. Cabana, A. Espinosa, B. Baptiste et al., Iron oxide nanoflowers@CuS hybrids for cancer tri-therapy: interplay of photothermal therapy, magnetic hyperthermia and photodynamic therapy. Theranostics 9, 1288–1302 (2019). https://doi.org/10.7150/thno.30238
- A. Józefczak, K. Kaczmarek, T. Hornowski, M. Kubovčíková, Z. Rozynek, M. Timko, A. Skumiel, Magnetic nanoparticles for enhancing the effectiveness of ultrasonic hyperthermia. Appl. Phys. Lett. 108, 1–5 (2016). https://doi.org/10.1063/1.4955130
- E. Beguin, M.D. Gray, K.A. Logan, H. Nesbitt, Y. Sheng et al., Magnetic microbubble mediated chemo-sonodynamic therapy using a combined magnetic-acoustic device. J. Control Release 317, 23–33 (2020). https://doi.org/10.1016/j.jconrel.2019.11.013
- S. Xiao, Z. Hu, Y. He, H. Jin, Y. Yang et al., Enhancement effect of microbubble-enhanced ultrasound in microwave ablation in rabbit VX2 liver tumors. Biomed. Res. Int. 2020, 1–10 (2020). https://doi.org/10.1155/2020/3050148
- Z. Zhou, Y. Wang, S. Song, W. Wu, S. Wu, P.H. Tsui, Monitoring microwave ablation using ultrasound echo decorrelation imaging: an ex vivo study. Sensors 19, 977 (2019). https://doi.org/10.3390/s19040977
- D. Gebreel, T. Shalaby, Y. Yousef, M. Mohamed, H. Badawy, Magnetic fluid based on Fe3O4 nanoparticles: preparation and hyperthermia application. Int. J. Chem. Appl. Biol. Sci. 1, 24 (2014). https://doi.org/10.4103/2348-0734.131792
- X. Li, Y. Liu, F. Fu, M. Cheng, Y. Liu et al., Single NIR laser-activated multifunctional nanoparticles for cascaded photothermal and oxygen-independent photodynamic therapy. Nano-Micro Lett. 11, 68 (2019). https://doi.org/10.1007/s40820-019-0298-5
- S. Luo, Z. Yang, X. Tan, Y. Wang, Y. Zeng et al., Multifunctional photosensitizer grafted on polyethylene glycol and polyethylenimine dual-functionalized nanographene oxide for cancer-targeted near-infrared imaging and synergistic phototherapy. ACS Appl. Mater. Interfaces. 8, 17176–17186 (2016). https://doi.org/10.1021/acsami.6b05383
- C. Yao, L. Zhang, J. Wang, Y. He, J. Xin et al., Gold nanoparticle mediated phototherapy for cancer. J. Nanomater. 7, 167 (2016). https://doi.org/10.1155/2016/5497136
- Q. Li, L. Hong, H. Li, C. Liu, Graphene oxide-fullerene C60 (GO-C60) hybrid for photodynamic and photothermal therapy triggered by near-infrared light. Biosens. Bioelectron. 89, 477–482 (2017). https://doi.org/10.1016/j.bios.2016.03.072
- J. Lee, Y.H. Lee, C.B. Jeong, J.S. Choi, K.S. Chang, M. Yoon, Gold nanorods-conjugated TiO2 nanoclusters for the synergistic combination of phototherapeutic treatments of cancer cells. J. Nanobiotechnol. 16, 1–12 (2018). https://doi.org/10.1186/s12951-018-0432-4
- A. Sazgarnia, A. Shanei, A.R. Taheri, N. Tayyebi Meibodi, H. Eshghi, N. Attaran, M. Shanei, The therapeutic effect of acoustic cavitation on breast carcinoma tumor model in BALB/c mice in the presence of gold nanoparticles. J. Ultrasound Med. 32, 475–483 (2013). https://doi.org/10.22122/jims.v37i531.11968
- C. Dai, S. Zhang, Z. Liu, R. Wu, Y. Chen, Two-dimensional graphene augments nanosonosensitized sonocatalytic tumor eradication. ACS Nano 11, 9467–9480 (2017). https://doi.org/10.1021/acsnano.7b05215
- F. Gao, G. He, H. Yin, J. Chen, Y. Liu et al., Titania-coated 2D gold nanoplates as nanoagents for synergistic photothermal/sonodynamic therapy in the second near-infrared window. Nanoscale 11, 2374–2384 (2019). https://doi.org/10.1039/C8NR07188H
- A.C. Anselmo, S. Mitragotri, Nanoparticles in the clinic. Bioeng. Transl. Med. 1, 10–29 (2016). https://doi.org/10.1002/btm2.10003
- N. Garino, T. Limongi, B. Dumontel, M. Canta, L. Racca et al., A microwave-assisted synthesis of zinc oxide nanocrystals finely tuned for biological applications. Nanomaterials 9, 212 (2019). https://doi.org/10.3390/nano9020212
- A.C. Anselmo, S. Mitragotri, Nanoparticles in the clinic: an update. Bioeng. Transl. Med. 4, e10143 (2019). https://doi.org/10.1002/btm2.10143
- J.M. Stern, V.V. Kibanov Solomonov, E. Sazykina, J.A. Schwartz, S.C. Gad, G.P. Goodrich, Initial evaluation of the safety of nanoshell-directed photothermal therapy in the treatment of prostate disease. Int. J. Toxicol. 35, 38–46 (2016). https://doi.org/10.1177/1091581815600170
- A.R. Rastinehad, H. Anastos, E. Wajswol, J.S. Winoker, J.P. Sfakianos et al., Gold nanoshell-localized photothermal ablation of prostate tumors in a clinical pilot device study. Proc. Natl. Acad. Sci. U.S.A. 116, 18590–18596 (2019). https://doi.org/10.1073/pnas.1906929116
References
International Agency for Research in Cancer, Latest Global Cancer Data (World Health Organization, Geneva, 2018)
D. Hanahan, R.A. Weinberg, Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011). https://doi.org/10.1016/j.cell.2011.02.013
S. Tran, P.-J. DeGiovanni, B. Piel, P. Rai, Cancer nanomedicine: a review of recent success in drug delivery. Clin. Transl. Med. 6, e44 (2017). https://doi.org/10.1186/s40169-017-0175-0
S. Soares, J. Sousa, A. Pais, C. Vitorino, Nanomedicine: principles, properties, and regulatory issues. Front. Chem. 6, 1–15 (2018). https://doi.org/10.3389/fchem.2018.00360
J. Shi, P.W. Kantoff, R. Wooster, O.C. Farokhzad, Cancer nanomedicine: progress, challenges and opportunities. Nat. Rev. 17, 20–37 (2017). https://doi.org/10.1038/nrc.2016.108.Cancer
C. Yan, Z. Guo, Y. Shen, Y. Chen, H. Tian, W.H. Zhu, Molecularly precise self-assembly of theranostic nanoprobes within a single-molecular framework for: in vivo tracking of tumor-specific chemotherapy. Chem. Sci. 9, 4959–4969 (2018). https://doi.org/10.1039/c8sc01069b
P. Dong, K.P. Rakesh, H.M. Manukumar, Y.H.E. Mohammed, C.S. Karthik et al., Innovative nano-carriers in anticancer drug delivery—a comprehensive review. Bioorg. Chem. 85, 325–336 (2019). https://doi.org/10.1016/j.bioorg.2019.01.019
J. Zhang, Q. Wang, J. Liu, Z. Guo, J. Yang et al., Saponin-based near-infrared nanoparticles with aggregation-induced emission behavior: enhancing cell compatibility and permeability. ACS Appl. Bio Mater. 2, 943–951 (2019). https://doi.org/10.1021/acsabm.8b00812
X. Ji, C. Wang, M. Tang, D. Guo, F. Peng et al., Biocompatible protamine sulfate@silicon nanoparticle-based gene nanocarriers featuring strong and stable fluorescence. Nanoscale 10, 14455–14463 (2018). https://doi.org/10.1039/c8nr03107j
L. Racca, M. Canta, B. Dumontel, A. Ancona, T. Limongi et al., Zinc oxide nanostructures in biomedicine. Smart Nanoparticles Biomed. (2018). https://doi.org/10.1016/b978-0-12-814156-4.00012-4
V. De Matteis, M. Cascione, C.C. Toma, S. Leporatti, Silver nanoparticles: synthetic routes, in vitro toxicity and theranostic applications for cancer disease. Nanomaterials 8(5), 319 (2018). https://doi.org/10.3390/nano8050319
T. Limongi, M. Canta, L. Racca, A. Ancona, S. Tritta, V. Vighetto, V. Cauda, Improving dispersal of therapeutic nanoparticles in the human body. Nanomedicine 14, 797–801 (2019). https://doi.org/10.2217/nnm-2019-0070
Y.S. Youn, Y.H. Bae, Perspectives on the past, present, and future of cancer nanomedicine. Adv. Drug Deliv. Rev. 130, 3–11 (2018). https://doi.org/10.1016/j.addr.2018.05.008
A. Albanese, P.S. Tang, W.C.W. Chan, The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 14, 1–16 (2012). https://doi.org/10.1146/annurev-bioeng-071811-150124
A. Sukhanova, S. Bozrova, P. Sokolov, M. Berestovoy, A. Karaulov, I. Nabiev, Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Res. Lett. 13, 44 (2018). https://doi.org/10.1186/s11671-018-2457-x
G. Canavese, A. Ancona, L. Racca, M. Canta, B. Dumontel et al., Nanoparticle-assisted ultrasound: a special focus on sonodynamic therapy against cancer. Chem. Eng. J. 340, 155–172 (2018). https://doi.org/10.1016/j.cej.2018.01.060
D. Kwatra, A. Venugopal, S. Anant, Nanoparticles in radiation therapy: a summary of various approaches to enhance radiosensitization in cancer. Transl. Cancer Res. 2, 330–342 (2013). https://doi.org/10.3978/j.issn.2218-676X.2013.08.06
D. Chang, M. Lim, J.A.C.M. Goos, R. Qiao, Y.Y. Ng et al., Biologically targeted magnetic hyperthermia: potential and limitations. Front. Pharmacol. 9, 831 (2018). https://doi.org/10.3389/fphar.2018.00831
R. Zhang, F. Yan, Y. Chen, Exogenous physical irradiation on titania semiconductors: materials chemistry and tumor-specific nanomedicine. Adv. Sci. 5, 1801175 (2018). https://doi.org/10.1002/advs.201801175
C.B. Collins, R.S. McCoy, B.J. Ackerson, G.J. Collins, C.J. Ackerson, Radiofrequency heating pathways for gold nanoparticles. Nanoscale 6, 8459–8472 (2014). https://doi.org/10.1039/c4nr00464g
B. McWilliams, H. Wang, V. Binns, S. Curto, S. Bossmann, P. Prakash, Experimental investigation of magnetic nanoparticle-enhanced microwave hyperthermia. J. Funct. Biomater. 8, 21 (2017). https://doi.org/10.3390/jfb8030021
Z. Yang, Z. Sun, Y. Ren, X. Chen, W. Zhang et al., Advances in nanomaterials for use in photothermal and photodynamic therapeutics (review). Mol. Med. Rep. 20, 5–15 (2019). https://doi.org/10.3892/mmr.2019.10218
J.B. Vines, J.H. Yoon, N.E. Ryu, D.J. Lim, H. Park, Gold nanoparticles for photothermal cancer therapy. Front. Chem. 7, 1–16 (2019). https://doi.org/10.3389/fchem.2019.00167
D. Howard, S. Sebastian, Q.V.C. Le, B. Thierry, I. Kempson, Chemical mechanisms of nanoparticle radiosensitization and radioprotection: a review of structure-function relationships influencing reactive oxygen species. Int. J. Mol. Sci. 21, 579 (2020). https://doi.org/10.3390/ijms21020579
L. Racca, T. Limongi, V. Vighetto, B. Dumontel, A. Ancona et al., Zinc oxide nanocrystals and high-energy shock waves: a new synergy for the treatment of cancer cells. Front. Bioeng. Biotechnol. 8, 577 (2020). https://doi.org/10.3389/fbioe.2020.00577
H. Xiang, Y. Chen, Energy-converting nanomedicine. Small 15, e1805339 (2019). https://doi.org/10.1002/smll.201805339
A.K. Parchur, J.M. Jagtap, G. Sharma, V. Gogineni, S.B. White, A. Joshi, Remotely triggered nanotheranostics. Nanotheranostics 1, 1–22 (2019). https://doi.org/10.1007/978-3-030-01775-0_17
A. Sneider, D. Vandyke, S. Paliwal, P. Rai, Remotely triggered nano-theranostics for cancer applications. Nanotheranostics 1, 1–22 (2017). https://doi.org/10.7150/ntno.17109
W. Fan, B. Yung, P. Huang, X. Chen, Nanotechnology for multimodal synergistic cancer therapy. Chem. Rev. 117, 13566–13638 (2017). https://doi.org/10.1021/acs.chemrev.7b00258
G. Pizzino, N. Irrera, M. Cucinotta, G. Pallio, F. Mannino, V. Arcoraci, F. Squadrito, D. Altavilla, A. Bitto, Oxidative stress: harms and benefits for human health. Oxid. Med. Cell Longev. 2017, 1–13 (2017). https://doi.org/10.1155/2017/8416763
V. Vighetto, A. Ancona, L. Racca, T. Limongi, A. Troia, G. Canavese, V. Cauda, The synergistic effect of nanocrystals combined with ultrasound in the generation of reactive oxygen species for biomedical applications. Front. Bioeng. Biotechnol. 7, 1–10 (2019). https://doi.org/10.3389/fbioe.2019.00374
W. Fan, W. Tang, J. Lau, Z. Shen, J. Xie, J. Shi, X. Chen, Breaking the depth dependence by nanotechnology-enhanced x-ray-excited deep cancer theranostics. Adv. Mater. 31, 1806381 (2019). https://doi.org/10.1002/adma.201806381
C. Verry, L. Sancey, S. Dufort, G. Le Duc, C. Mendoza et al., Treatment of multiple brain metastases using gadolinium nanoparticles and radiotherapy: NANO-RAD, a phase I study protocol. BMJ Open 9, 1–6 (2019). https://doi.org/10.1136/bmjopen-2018-023591
J. Deng, S. Xu, W. Hu, X. Xun, L. Zheng, M. Su, Tumor targeted, stealthy and degradable bismuth nanoparticles for enhanced X-ray radiation therapy of breast cancer. Biomaterials 154, 24–33 (2018). https://doi.org/10.1016/j.biomaterials.2017.10.048
Z. Kuncic, S. Lacombe, Nanoparticle radio-enhancement: principles, progress and application to cancer treatment. Phys. Med. Biol. 63, 02TR01 (2018). https://doi.org/10.1088/1361-6560/aa99ce
J. Zhao, M. Zhou, C. Li, Synthetic nanoparticles for delivery of radioisotopes and radiosensitizers in cancer therapy. Cancer Nanotechnol. 7, 9 (2016). https://doi.org/10.1186/s12645-016-0022-9
P. Retif, S. Pinel, M. Toussaint, C. Frochot, R. Chouikrat, T. Bastogne, M. Barberi-Heyob, Nanoparticles for radiation therapy enhancement: the key parameters. Theranostics 5, 1030–1044 (2015). https://doi.org/10.7150/thno.11642
Y. Liu, P. Zhang, F. Li, X. Jin, J. Li, W. Chen, Q. Li, Metal-based nanoenhancers for future radiotherapy: radiosensitizing and synergistic effects on tumor cells. Theranostics 8, 1824–1849 (2018). https://doi.org/10.7150/thno.22172
S. Bonvalot, P.L. Rutkowski, J. Thariat, S. Carrère, A. Ducassou et al., NBTXR3, a first-in-class radioenhancer hafnium oxide nanoparticle, plus radiotherapy versus radiotherapy alone in patients with locally advanced soft-tissue sarcoma (Act. In. Sarc): a multicentre, phase 2–3, randomised, controlled trial. Lancet Oncol. 20, 1148–1159 (2019). https://doi.org/10.1016/S1470-2045(19)30326-2
A.K. Hauser, M.I. Mitov, E.F. Daley, R.C. McGarry, K.W. Anderson, J.Z. Hilt, Targeted iron oxide nanoparticles for the enhancement of radiation therapy. Biomaterials 105, 127–135 (2016). https://doi.org/10.1016/j.biomaterials.2016.07.032
F. Chen, X.H. Zhang, X.D. Hu, P.D. Liu, H.Q. Zhang, The effects of combined selenium nanoparticles and radiation therapy on breast cancer cells in vitro. Artif. Cells Nanomed. Biotechnol. 46, 937–948 (2018). https://doi.org/10.1080/21691401.2017.1347941
T.J. Meyer, A. Scherzad, H. Moratin, T.E. Gehrke, J. Killisperger et al., The radiosensitizing effect of zinc oxide nanoparticles in sub-cytotoxic dosing is associated with oxidative stress in vitro. Materials 12, 4062 (2019). https://doi.org/10.3390/MA12244062
J. Xie, N. Wang, X. Dong, C. Wang, Z. Du et al., Graphdiyne nanoparticles with high free radical scavenging activity for radiation protection. ACS Appl. Mater. Interfaces. 11, 2579–2590 (2019). https://doi.org/10.1021/acsami.8b00949
N. Abdi Goushbolagh, B. Farhood, A. Astani, A. Nikfarjam, M. Kalantari, M.H. Zare, Quantitative cytotoxicity, cellular uptake and radioprotection effect of cerium oxide nanoparticles in MRC-5 normal cells and MCF-7 cancerous cells. Bionanoscience 8, 769–777 (2018). https://doi.org/10.1007/s12668-018-0538-z
Y. Gao, K. Chen, J.L. Ma, F. Gao, Cerium oxide nanoparticles in cancer. Onco Targets Ther. 7, 835–840 (2014). https://doi.org/10.2147/ott.s62057
A.Z. Abbasi, C.R. Gordijo, M.A. Amini, A. Maeda, A.M. Rauth, R.S. DaCosta, X.Y. Wu, Hybrid manganese dioxide nanoparticles potentiate radiation therapy by modulating tumor hypoxia. Cancer Res. 76, 6643–6656 (2016). https://doi.org/10.1158/0008-5472.CAN-15-3475
M. Durante, R. Orecchia, J.S. Loeffler, Charged-particle therapy in cancer: clinical uses and future perspectives. Nat. Rev. Clin. Oncol. 14, 483–495 (2017). https://doi.org/10.1038/nrclinonc.2017.30
S. Lacombe, E. Porcel, E. Scifoni, Particle therapy and nanomedicine: state of art and research perspectives. Cancer Nanotechnol. 8, 9 (2017). https://doi.org/10.1186/s12645-017-0029-x
P. Symonds, G.D.D. Jones, FLASH radiotherapy: the next technological advance in radiation therapy? Clin. Oncol. 31, 405–406 (2019). https://doi.org/10.1016/j.clon.2019.05.011
A. Degiovanni, U. Amaldi, History of hadron therapy accelerators. Phys. Med. 31, 322–332 (2015). https://doi.org/10.1016/j.ejmp.2015.03.002
M.I. Khot, H. Andrew, H.S. Svavarsdottir, G. Armstrong, A.J. Quyn, D.G. Jayne, A review on the scope of photothermal therapy-based nanomedicines in preclinical models of colorectal cancer. Clin. Colorectal Cancer 18, e200–e209 (2019). https://doi.org/10.1016/j.clcc.2019.02.001
A. Bettaieb, P.K. Wrzal, D.A. Averill-Bates, Hyperthermia: Cancer Treatment and Beyond. Cancer treatment-conventional and innovative approaches. https://doi.org/10.5772/55795
J. Wang, J. Qiu, A review of organic nanomaterials in photothermal cancer therapy. Cancer Res. Front. 2, 67–84 (2016). https://doi.org/10.17980/2016.67
M.G. Lubner, C.L. Brace, J.L. Hinshaw, F.T. Lee, Microwave tumor ablation: mechanism of action, clinical results and devices. J. Vasc. Interv. Radiol. 21, S192–S203 (2010). https://doi.org/10.1038/jid.2014.371
B. Zhang, M.A.J. Moser, E.M. Zhang, Y. Luo, C. Liu, W. Zhang, A review of radiofrequency ablation: large target tissue necrosis and mathematical modelling. Phys. Med. 32, 961–971 (2016). https://doi.org/10.1016/j.ejmp.2016.07.092
M. Barajas, T. Fraga, M. Acevedo, R.G. Cabrera, Radiofrequency ablation: a review of current knowledge, therapeutic perspectives, complications, and contraindications. Int. J. Biosens. Bioelectron. 4, 53–55 (2018). https://doi.org/10.15406/ijbsbe.2018.04.00098
P. Pantano, C.D. Harrison, J. Poulose, D. Urrabazo, T.Q. Norman et al., Factors affecting the 13.56-MHz radio-frequency-mediated heating of gold nanoparticles. Appl. Spectrosc. Rev. 52, 821–836 (2017). https://doi.org/10.1080/05704928.2017.1314299
J. Beyk, H. Tavakoli, Selective radiofrequency ablation of tumor by magnetically targeting of multifunctional iron oxide-gold nanohybrid. J. Cancer Res. Clin. Oncol. 145, 2199–2209 (2019). https://doi.org/10.1007/s00432-019-02969-1
J. Beik, Z. Abed, F.S. Ghoreishi, S. Hosseini-Nami, S. Mehrzadi, A. Shakeri-Zadeh, S.K. Kamrava, Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J. Control. Release 235, 205–221 (2016). https://doi.org/10.1016/j.jconrel.2016.05.062
P. Das, M. Colombo, D. Prosperi, Recent advances in magnetic fluid hyperthermia for cancer therapy. Colloids Surf. B Biointerfaces 174, 42–55 (2019). https://doi.org/10.1016/j.colsurfb.2018.10.051
S.K. Sharma, N. Shrivastava, F. Rossi, L.D. Tung, N.T.K. Thanh, Nanoparticles-based magnetic and photo induced hyperthermia for cancer treatment. Nano Today 100, 795 (2019). https://doi.org/10.1016/j.nantod.2019.100795
J. Dulińska-Litewka, A. Łazarczyk, P. Hałubiec, O. Szafrański, K. Karnas, A. Karewicz, Superparamagnetic iron oxide nanoparticles-current and prospective medical applications. Materials 12, 617 (2019). https://doi.org/10.3390/ma12040617
Z. Ashikbayeva, D. Tosi, D. Balmassov, E. Schena, P. Saccomandi, V. Inglezakis, Application of nanoparticles and nanomaterials in thermal ablation therapy of cancer. Nanomaterials 9, 1195 (2019). https://doi.org/10.3390/nano9091195
G. Hemery, C. Genevois, F. Couillaud, S. Lacomme, E. Gontier et al., Monocore: vs. multicore magnetic iron oxide nanoparticles: uptake by glioblastoma cells and efficiency for magnetic hyperthermia. Mol. Syst. Des. Eng. 2, 629–639 (2017). https://doi.org/10.1039/c7me00061h
L. Kafrouni, O. Savadogo, Recent progress on magnetic nanoparticles for magnetic hyperthermia. Prog. Biomater. 5, 147–160 (2016). https://doi.org/10.1007/s40204-016-0054-6
S. Kalia, S. Kango, A. Kumar, Y. Haldorai, B. Kumari, R. Kumar, Magnetic polymer nanocomposites for environmental and biomedical applications. Colloid Polym. Sci. 292, 2025–2052 (2014). https://doi.org/10.1007/s00396-014-3357-y
G. Lavorato, E. Lima, M. Vasquez Mansilla, H. Troiani, R. Zysler, E. Winkler, Bifunctional CoFe2O4/ZnO core/shell nanoparticles for magnetic fluid hyperthermia with controlled optical response. J. Phys. Chem. C 122, 3047–3057 (2018). https://doi.org/10.1021/acs.jpcc.7b11115
S.V. Jadhav, P.S. Shewale, B.C. Shin, M.P. Patil, G.D. Kim et al., Study of structural and magnetic properties and heat induction of gadolinium-substituted manganese zinc ferrite nanoparticles for in vitro magnetic fluid hyperthermia. J. Colloid Interface Sci. 541, 192–203 (2019). https://doi.org/10.1016/j.jcis.2019.01.063
M. Coşkun, M. Korkmaz, The effect of SiO2 shell thickness on the magnetic properties of ZnFe2O4 nanoparticles. J. Nanoparticle Res. 16, 2316 (2014). https://doi.org/10.1007/s11051-014-2316-3
L. León Félix, B. Sanz, V. Sebastián, T.E. Torres, M.H. Sousa et al., Gold-decorated magnetic nanoparticles design for hyperthermia applications and as a potential platform for their surface-functionalization. Sci. Rep. 9, 1–11 (2019). https://doi.org/10.1038/s41598-019-40769-2
K. Wu, D. Su, J. Liu, R. Saha, J.P. Wang, Magnetic nanoparticles in nanomedicine: a review of recent advances. Nanotechnology 30, 502003 (2019). https://doi.org/10.1088/1361-6528/ab4241
S. Hatamie, B. Parseh, M.M. Ahadian, F. Naghdabadi, R. Saber, M. Soleimani, Heat transfer of PEGylated cobalt ferrite nanofluids for magnetic fluid hyperthermia therapy: in vitro cellular study. J. Magn. Magn. Mater. 462, 185–194 (2018). https://doi.org/10.1016/j.jmmm.2018.05.020
G. Kandasamy, A. Sudame, T. Luthra, K. Saini, D. Maity, Functionalized hydrophilic superparamagnetic iron oxide nanoparticles for magnetic fluid hyperthermia application in liver cancer treatment. ACS Omega 3, 3991–4005 (2018). https://doi.org/10.1021/acsomega.8b00207
P.M. Price, W.E. Mahmoud, A.A. Al-Ghamdi, L.M. Bronstein, Magnetic drug delivery: where the field is going. Front. Chem. 6, 1–7 (2018). https://doi.org/10.3389/fchem.2018.00619
J. Cardinal, J.R. Klune, E. Chory, G. Jeyabalan, J.S. Kanzius, M. Nalesnik, D.A. Geller, Non-invasive radiofrequency ablation of cancer targeted by gold nanoparticles. Surgery 144, 125–132 (2008). https://doi.org/10.1016/j.surg.2008.03.036.NON-INVASIVE
S.M. Amini, S. Kharrazi, S.M. Rezayat, K. Gilani, Radiofrequency electric field hyperthermia with gold nanostructures: role of particle shape and surface chemistry. Artif. Cells Nanomed. Biotechnol. 46, 1452–1462 (2018). https://doi.org/10.1080/21691401.2017.1373656
Y.L. Shao, B. Arjun, H.L. Leo, K.J. Chua, Nano-assisted radiofrequency ablation of clinically extracted irregularly-shaped liver tumors. J. Therm. Biol 66, 101–113 (2017). https://doi.org/10.1016/j.jtherbio.2017.04.005
C.J. Gannon, P. Cherukuri, B.I. Yakobson, L. Cognet, J.S. Kanzius et al., Carbon nanotube-enhanced thermal destruction of cancer cells in a noninvasive radiofrequency field. Cancer 110, 2654–2665 (2007). https://doi.org/10.1002/cncr.23155
D. Bijukumar, C.M. Girish, A. Sasidharan, S. Nair, M. Koyakutty, Transferrin-conjugated biodegradable graphene for targeted radiofrequency ablation of hepatocellular carcinoma. ACS Biomater. Sci. Eng. 1, 1211–1219 (2015). https://doi.org/10.1021/acsbiomaterials.5b00184
G. Raniszewski, A. Miaskowski, S. Wiak, The application of carbon nanotubes in magnetic fluid hyperthermia. J. Nanomater. 2015, 527652 (2015). https://doi.org/10.1155/2015/527652
H. Wu, G. Liu, X. Wang, J. Zhang, Y. Chen et al., Solvothermal synthesis of cobalt ferrite nanoparticles loaded on multiwalled carbon nanotubes for magnetic resonance imaging and drug delivery. Acta Biomater. 7, 3496–3504 (2011). https://doi.org/10.1016/j.actbio.2011.05.031
R. Singh, S.V. Torti, Carbon nanotubes in hyperthermia therapy. Adv. Drug Deliv. Rev. 65, 2045–2060 (2013). https://doi.org/10.1016/j.addr.2013.08.001
F. Saghatchi, M. Mohseni-Dargah, S. Akbari-Birgani, S. Saghatchi, B. Kaboudin, Cancer therapy and imaging through functionalized carbon nanotubes decorated with magnetite and gold nanoparticles as a multimodal tool. Appl. Biochem. Biotechnol. 191, 1280–1293 (2020). https://doi.org/10.1007/s12010-020-03280-3
K.P. Tamarov, L.A. Osminkina, S.V. Zinovyev, K.A. Maximova, J.V. Kargina et al., Radio frequency radiation-induced hyperthermia using Si nanoparticle-based sensitizers for mild cancer therapy. Sci. Rep. 4, 7034 (2014). https://doi.org/10.1038/srep07034
M. Gongalsky, G. Gvindzhiliia, K. Tamarov, O. Shalygina, A. Pavlikov et al., Radiofrequency hyperthermia of cancer cells enhanced by silicic acid ions released during the biodegradation of porous silicon nanowires. ACS Omega 4, 10662–10669 (2019). https://doi.org/10.1021/acsomega.9b01030
A. Ashokan, V.H. Somasundaram, G.S. Gowd, I.M. Anna, G.L. Malarvizhi et al., Biomineral nano-theranostic agent for magnetic resonance image guided, augmented radiofrequency ablation of liver tumor. Sci. Rep. 7, 1–15 (2017). https://doi.org/10.1038/s41598-017-14976-8
E.S. Glazer, S.A. Curley, Non-invasive radiofrequency ablation of malignancies mediated by quantum dots, gold nanoparticles and carbon nanotubes. Ther. Deliv. 2, 1325–1330 (2011). https://doi.org/10.1038/jid.2014.371
E.S. Glazer, S.A. Curley, Radiofrequency field-induced thermal cytotoxicity in cancer cells treated with fluorescent nanoparticles. Cancer 116, 3285–3293 (2010). https://doi.org/10.1002/cncr.25135
L. Sidoff, D.E. Dupuy, Clinical experiences with microwave thermal ablation of lung malignancies. Int. J. Hyperth. 33, 25–33 (2017). https://doi.org/10.1080/02656736.2016.1204630
C. Kim, Understanding the nuances of microwave ablation for more accurate post-treatment assessment. Future Oncol. 14, 1755–1764 (2018). https://doi.org/10.2217/fon-2017-0736
L. Tan, W. Tang, T. Liu, X. Ren, C. Fu et al., Biocompatible hollow polydopamine nanoparticles loaded ionic liquid enhanced tumor microwave thermal ablation in vivo. ACS Appl. Mater. Interfaces. 8, 11237–11245 (2016). https://doi.org/10.1021/acsami.5b12329
B. Beckler, A. Cowan, N. Farrar, A. Murawski, A. Robinson et al., Microwave Heating of antibody-functionalized carbon nanotubes as a feasible cancer treatment. Biomed. Phys. Eng. Exp. 4, 831 (2018). https://doi.org/10.1088/2057-1976/aac9fe
L. Wen, W. Ding, S. Yang, D. Xing, Microwave pumped high-efficient thermoacoustic tumor therapy with single wall carbon nanotubes. Biomaterials 75, 163–173 (2016). https://doi.org/10.1016/j.biomaterials.2015.10.028
L. Wen, S. Yang, J. Zhong, Q. Zhou, D. Xing, Thermoacoustic imaging and therapy guidance based on ultra-short pulsed microwave pumped thermoelastic effect induced with superparamagnetic iron oxide nanoparticles. Theranostics 7, 1976–1989 (2017). https://doi.org/10.7150/thno.17846
M. Jelbuldina, A. Korobeinyk, S. Korganbayev, D. Tosi, K. Dukenbayev, V.J. Inglezakis, Real-time temperature monitoring in liver during magnetite nanoparticle-enhanced microwave ablation with fiber bragg grating sensors: ex vivo analysis. IEEE Sens. J. 18, 8005–8011 (2018). https://doi.org/10.1109/JSEN.2018.2865100
T. Tang, X. Xu, Z. Wang, J. Tian, Y. Yang, C. Ou, H. Bao, T. Liu, Cu2ZnSnS4 nanocrystals for microwave thermal and microwave dynamic combination tumor therapy. Chem. Commun. 55, 13148–13151 (2019). https://doi.org/10.1039/c9cc07762f
H. Peng, J. Ouyang, Y. Peng, A simple approach for the synthesis of bi-functional Fe3O4@WO3-x core–shell nanoparticles with magnetic-microwave to heat responsive properties. Inorg. Chem. Commun. 84, 138–143 (2017). https://doi.org/10.1016/j.inoche.2017.08.004
N.R. Paudel, D. Shvydka, E.I. Parsai, A novel property of gold nanoparticles: free radical generation under microwave irradiation. Med. Phys. 43, 1598–1602 (2016). https://doi.org/10.1118/1.4942811
B. Kioko, T. Ogundolie, M. Adebiyi, Y. Ettinoffe, C. Rhodes et al., De-crystallization of uric acid crystals in synovial fluid using gold colloids and microwave heating. Nano Biomed. Eng. 6, 104–110 (2014). https://doi.org/10.5101/nbe.v6i4.p104-110
G.L. McLemore, S. Toker, Z. Boone-Kukoyi, H. Ajifa, C. Lansiquot et al., Microwave heating of crystals with gold nanoparticles and synovial fluid under synthetic skin patches. ACS Omega 2, 5992–6002 (2017). https://doi.org/10.1021/acsomega.7b00816
F.H. Ghahremani, A. Sazgarnia, M.H. Bahreyni-Toosi, O. Rajabi, A. Aledavood, Efficacy of microwave hyperthermia and chemotherapy in the presence of gold nanoparticles: an in vitro study on osteosarcoma. Int. J. Hyperth. 27, 625–636 (2011). https://doi.org/10.3109/02656736.2011.587363
R. Moradpoor, S.A. Aledavood, O. Rajabi, J.K. Chamani, A. Sazgarnia, Enhancement of cisplatin efficacy by gold nanoparticles or microwave hyperthermia? An in vitro study on a melanoma cell line. Int. J. Cancer Manag. 10, 1–8 (2017). https://doi.org/10.17795/ijcp-5925
X. Chu, L. Mao, O. Johnson, K. Li, J. Phan, Y. Zhang et al., Exploration of TiO2 nanoparticle mediated microdynamic therapy on cancer treatment. Nanomed. Nanotechnol. Biol. Med. 18, 272–281 (2019). https://doi.org/10.1016/j.nano.2019.02.016
S. Wang, X.G. Mei, S.N. Goldberg, M. Ahmed, J.C. Lee et al., Does thermosensitive liposomal vinorelbine improve end-point survival after percutaneous radiofrequency ablation of liver tumors in a mouse model? Radiology 279, 762–772 (2016). https://doi.org/10.1148/radiol.2015150787
S. Wu, D. Zhang, J. Yu, J. Dou, X. Li, M. Mu, P. Liang, Chemotherapeutic nanoparticle-based liposomes enhance the efficiency of mild microwave ablation in hepatocellular carcinoma therapy. Front. Pharmacol. 11, 1–9 (2020). https://doi.org/10.3389/fphar.2020.00085
J.P. Dou, Q. Wu, C.H. Fu, D.Y. Zhang, J. Yu, X.W. Meng, P. Liang, Amplified intracellular Ca2+ for synergistic anti-tumor therapy of microwave ablation and chemotherapy. J. Nanobiotechnol. 17, 1–17 (2019). https://doi.org/10.1186/s12951-019-0549-0
A.C.V. Doughty, A.R. Hoover, E. Layton, C.K. Murray, E.W. Howard, W.R. Chen, Nanomaterial applications in photothermal therapy for cancer. Materials 12, 779 (2019). https://doi.org/10.3390/ma12050779
J. Liang, H. Liu, J. Yu, L. Zhou, J. Zhu, Plasmon-enhanced solar vapor generation. Nanophotonics 8, 771–786 (2019). https://doi.org/10.1515/nanoph-2019-0039
M. Kim, J.H. Lee, J.M. Nam, Plasmonic photothermal nanoparticles for biomedical applications. Adv. Sci. 6, 1900471 (2019). https://doi.org/10.1002/advs.201900471
W. Wei, X. Zhang, S. Zhang, G. Wei, Z. Su, Biomedical and bioactive engineered nanomaterials for targeted tumor photothermal therapy: a review. Mater. Sci. Eng., C 104, 109891 (2019). https://doi.org/10.1016/j.msec.2019.109891
W. Yang, H. Liang, S. Ma, D. Wang, J. Huang, Gold nanoparticle based photothermal therapy: development and application for effective cancer treatment. Sustain. Mater. Technol. 22, e00109 (2019). https://doi.org/10.1016/j.susmat.2019.e00109
M.R.K. Ali, Y. Wu, M.A. El-Sayed, Gold-nanoparticle-assisted plasmonic photothermal therapy advances toward clinical application. J. Phys. Chem. C 123, 15375–15393 (2019). https://doi.org/10.1021/acs.jpcc.9b01961
M. Sancho-Albero, N. Navascués, G. Mendoza, V. Sebastián, M. Arruebo, P. Martín-Duque, J. Santamaría, Exosome origin determines cell targeting and the transfer of therapeutic nanoparticles towards target cells. J. Nanobiotechnol. 17, 1–13 (2019). https://doi.org/10.1186/s12951-018-0437-z
J. Estelrich, M. Antònia Busquets, Iron oxide nanoparticles in photothermal therapy. Molecules 23, 1567 (2018). https://doi.org/10.3390/molecules23071567
G.H. Lu, W.T. Shang, H. Deng, Z.Y. Han, M. Hu et al., Targeting carbon nanotubes based on IGF-1R for photothermal therapy of orthotopic pancreatic cancer guided by optical imaging. Biomaterials 195, 13–22 (2019). https://doi.org/10.1016/j.biomaterials.2018.12.025
J. Mou, T. Lin, F. Huang, H. Chen, J. Shi, Black titania-based theranostic nanoplatform for single NIR laser induced dual-modal imaging-guided PTT/PDT. Biomaterials 84, 13–24 (2016). https://doi.org/10.1016/j.biomaterials.2016.01.009
J.B. Vines, D.J. Lim, H. Park, Contemporary polymer-based nanoparticle systems for photothermal therapy. Polymers 10, 1–16 (2018). https://doi.org/10.3390/polym10121357
J. Wang, R. Yan, F. Guo, M. Yu, F. Tan, N. Li, Targeted lipid-polyaniline hybrid nanoparticles for photoacoustic imaging guided photothermal therapy of cancer. Nanotechnology 27, 285102 (2016). https://doi.org/10.1088/0957-4484/27/28/285102
A.F. Dos Santos, D.R.Q. De Almeida, L.F. Terra, M.S. Baptista, L. Labriola, Photodynamic therapy in cancer treatment—an update review. J. Cancer Metastasis Treat 5, 25 (2019). https://doi.org/10.20517/2394-4722.2018.83
S. Mallidi, S. Anbil, A.L. Bulin, G. Obaid, M. Ichikawa, T. Hasan, Beyond the barriers of light penetration: strategies, perspectives and possibilities for photodynamic therapy. Theranostics 6, 2458–2487 (2016). https://doi.org/10.7150/thno.16183
D. van Straten, V. Mashayekhi, H.S. de Bruijn, S. Oliveira, D.J. Robinson, Oncologic photodynamic therapy: basic principles, current clinical status and future directions. Cancers 9, 1–54 (2017). https://doi.org/10.3390/cancers9020019
X. Li, J.F. Lovell, J. Yoon, X. Chen, Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol. (2020). https://doi.org/10.1038/s41571-020-0410-2
R. Baskaran, J. Lee, S.-G. Yang, Clinical development of photodynamic agents and therapeutic applications. Biomater. Res. 22, 1–8 (2018). https://doi.org/10.1186/s40824-018-0140-z
M. Lismont, L. Dreesen, S. Wuttke, Metal-organic framework nanoparticles in photodynamic therapy: current status and perspectives. Adv. Funct. Mater. 27, 1–16 (2017). https://doi.org/10.1002/adfm.201606314
S.S. Lucky, K.C. Soo, Y. Zhang, Nanoparticles in photodynamic therapy. Chem. Rev. 115, 1990–2042 (2015). https://doi.org/10.1021/cr5004198
D. Lu, R. Tao, Z. Wang, Carbon-based materials for photodynamic therapy: a mini-review. Front. Chem. Sci. Eng. 13, 310–323 (2019). https://doi.org/10.1007/s11705-018-1750-7
J. Bogdan, J. Pławińska-Czarnak, J. Zarzyńska, Nanoparticles of titanium and zinc oxides as novel agents in tumor treatment: a review. Nanoscale Res. Lett. 12, 225 (2017). https://doi.org/10.1186/s11671-017-2007-y
Z. Youssef, R. Vanderesse, L. Colombeau, F. Baros, T. Roques-Carmes et al., The application of titanium dioxide, zinc oxide, fullerene, and graphene nanoparticles in photodynamic therapy. Cancer Nanotechnol. 8, 6 (2017). https://doi.org/10.1186/s12645-017-0032-2
A. Grebinyk, S. Grebinyk, S. Prylutska, U. Ritter, O. Matyshevska, T. Dandekar, M. Frohme, C 60 fullerene accumulation in human leukemic cells and perspectives of LED-mediated photodynamic therapy. Free Radic. Biol. Med. 124, 319–327 (2018). https://doi.org/10.1016/j.freeradbiomed.2018.06.022
A. Ancona, B. Dumontel, N. Garino, B. Demarco, D. Chatzitheodoridou et al., Lipid-coated zinc oxide nanoparticles as innovative ROS-generators for photodynamic therapy in cancer cells. Nanomaterials 8, 143 (2018). https://doi.org/10.3390/nano8030143
F.U. Rehman, C. Zhao, H. Jiang, X. Wang, Biomedical applications of nano-titania in theranostics and photodynamic therapy. Biomater. Sci. 4, 40–54 (2016). https://doi.org/10.1039/c5bm00332f
D. Ziental, B. Czarczynska-Goslinska, D.T. Mlynarczyk, A. Glowacka-Sobotta, B. Stanisz, T. Goslinski, L. Sobotta, Titanium dioxide nanoparticles: prospects and applications in medicine. Nanomaterials 10, 387 (2020). https://doi.org/10.3390/nano10020387
W. Ni, M. Li, J. Cui, Z. Xing, Z. Li et al., 808 nm light triggered black TiO2 nanoparticles for killing of bladder cancer cells. Mater. Sci. Eng., C 81, 252–260 (2017). https://doi.org/10.1016/j.msec.2017.08.020
C. Yi, Z. Yu, Q. Ren, X. Liu, Y. Wang et al., Nanoscale ZnO-based photosensitizers for photodynamic therapy. Photodiagnosis Photodyn. Ther. 30, 101694 (2020). https://doi.org/10.1016/j.pdpdt.2020.101694
J. Gupta, D. Bahadur, Visible light sensitive mesoporous cu-substituted zno nanoassembly for enhanced photocatalysis, bacterial inhibition, and noninvasive tumor regression. ACS Sustain. Chem. Eng. 5, 8702–8709 (2017). https://doi.org/10.1021/acssuschemeng.7b01433
M. Sivasubramanian, Y.C. Chuang, L.W. Lo, Evolution of nanoparticle-mediated photodynamic therapy: from superficial to deep-seated cancers. Molecules 24, 520 (2019). https://doi.org/10.3390/molecules24030520
C. Zhang, K. Zhao, W. Bu, D. Ni, Y. Liu, J. Feng, J. Shi, Marriage of scintillator and semiconductor for synchronous radiotherapy and deep photodynamic therapy with diminished oxygen dependence. Angew. Chem. Int. Ed. 127, 1790–1794 (2015). https://doi.org/10.1002/ange.201408472
G.M.F. Calixto, J. Bernegossi, L.M. De Freitas, C.R. Fontana, M. Chorilli, A.M. Grumezescu, Nanotechnology-based drug delivery systems for photodynamic therapy of cancer: a review. Molecules 21, 1–18 (2016). https://doi.org/10.3390/molecules21030342
G. Yi, S.H. Hong, J. Son, J. Yoo, C. Park, Y. Choi, H. Koo, Recent advances in nanoparticle carriers for photodynamic therapy. Quant. Imaging Med. Surg. 8, 433–443 (2018). https://doi.org/10.21037/qims.2018.05.04
G. Yang, L. Xu, Y. Chao, J. Xu, X. Sun et al., Hollow MnO2 as a tumor-microenvironment-responsive biodegradable nano-platform for combination therapy favoring antitumor immune responses. Nat. Commun. 8, 902 (2017). https://doi.org/10.1038/s41467-017-01050-0
H. Shibaguchi, H. Tsuru, M. Kuroki, M. Kuroki, Sonodynamic cancer therapy: a non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer Res. 31, 2425–2430 (2011)
Z. Izadifar, P. Babyn, D. Chapman, Mechanical and biological effects of ultrasound: a review of present knowledge. Ultrasound Med. Biol. 43, 1085–1104 (2017). https://doi.org/10.1016/j.ultrasmedbio.2017.01.023
H. Xu, X. Zhang, R. Han, P. Yang, H. Ma et al., Nanoparticles in sonodynamic therapy: state of the art review. RSC Adv. 6, 50697–50705 (2016). https://doi.org/10.1039/c6ra06862f
G.Y. Wan, Y. Liu, B.W. Chen, Y.Y. Liu, Y.S. Wang, N. Zhang, Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol. Med. 13, 325–338 (2016). https://doi.org/10.20892/j.issn.2095-3941.2016.0068
A.P. Sviridov, L.A. Osminkina, A.L. Nikolaev, A.A. Kudryavtsev, A.N. Vasiliev, V.Y. Timoshenko, Lowering of the cavitation threshold in aqueous suspensions of porous silicon nanoparticles for sonodynamic therapy applications. Appl. Phys. Lett. 107, 123107 (2015). https://doi.org/10.1063/1.4931728
L.A. Osminkina, A.L. Nikolaev, A.P. Sviridov, N.V. Andronova, K.P. Tamarov et al., Porous silicon nanoparticles as efficient sensitizers for sonodynamic therapy of cancer. Microporous Mesoporous Mater. 210, 169–175 (2015). https://doi.org/10.1016/j.micromeso.2015.02.037
J.T. Seil, T.J. Webster, Antibacterial effect of zinc oxide nanoparticles combined with ultrasound. Nanotechnology 23, 495101 (2012). https://doi.org/10.1088/0957-4484/23/49/495101
A. Ebrahimi Fard, A. Zarepour, A. Zarrabi, A. Shanei, H. Salehi, Synergistic effect of the combination of triethylene-glycol modified Fe3O4 nanoparticles and ultrasound wave on MCF-7 cells. J. Magn. Magn. Mater. 394, 44–49 (2015). https://doi.org/10.1016/j.jmmm.2015.06.040
A. Marino, M. Battaglini, D. De Pasquale, A. Degl’Innocenti, G. Ciofani, Ultrasound-activated piezoelectric nanoparticles inhibit proliferation of breast cancer cells. Sci. Rep. 8, 1–13 (2018). https://doi.org/10.1038/s41598-018-24697-1
M. Lafond, S. Yoshizawa, S. Ichiro Umemura, Sonodynamic therapy: advances and challenges in clinical translation. J. Ultrasound Med. 38, 567–580 (2019). https://doi.org/10.1002/jum.14733
X. Wang, H. Chen, Y. Zheng, M. Ma, Y. Chen et al., Au-nanoparticle coated mesoporous silica nanocapsule-based multifunctional platform for ultrasound mediated imaging, cytoclasis and tumor ablation. Biomaterials 34, 2057–2068 (2013). https://doi.org/10.1016/j.biomaterials.2012.11.044
C. Brazzale, R. Canaparo, L. Racca, F. Foglietta, G. Durando et al., Enhanced selective sonosensitizing efficacy of ultrasound-based anticancer treatment by targeted gold nanoparticles. Nanomedicine 12, 3053–3070 (2016). https://doi.org/10.2217/nnm-2016-0293
V. Bernard, V. Mornstein, J. Jaroš, M. Sedláčková, J. Škorpíková, Combined effect of silver nanoparticles and therapeutical ultrasound on ovarian carcinoma cells A2780. J. Appl. Biomed. 12, 137–145 (2014). https://doi.org/10.1016/j.jab.2014.01.002
X. Han, J. Huang, X. Jing, D. Yang, H. Lin et al., Oxygen-deficient black titania for synergistic/enhanced sonodynamic and photoinduced cancer therapy at near infrared-II biowindow. ACS Nano 12, 4545–4555 (2018). https://doi.org/10.1021/acsnano.8b00899
S.A.R. Dibaji, M.F. Al-Rjoub, M.R. Myers, R.K. Banerjee, Enhanced heat transfer and thermal dose using magnetic nanoparticles during HIFU thermal ablation-an in vitro study. J. Nanotechnol. Eng. Med. 4, 040902 (2013). https://doi.org/10.1115/1.4027340
O.K. Kosheleva, T.C. Lai, N.G. Chen, M. Hsiao, C.H. Chen, Selective killing of cancer cells by nanoparticle-assisted ultrasound. J. Nanobiotechnol. 14, 46 (2016). https://doi.org/10.1186/s12951-016-0194-9
F. Gong, L. Cheng, N. Yang, O. Betzer, L. Feng et al., Ultrasmall oxygen-deficient bimetallic oxide mnwox nanoparticles for depletion of endogenous gsh and enhanced sonodynamic cancer therapy. Adv. Mater. 31, 1–9 (2019). https://doi.org/10.1002/adma.201900730
A. Sviridov, K. Tamarov, I. Fesenko, W. Xu, V. Andreev, V. Timoshenko, V.P. Lehto, Cavitation induced by Janus-like mesoporous silicon nanoparticles enhances ultrasound hyperthermia. Front. Chem. 7, 1–12 (2019). https://doi.org/10.3389/fchem.2019.00393
A. Kharin, O. Syshchyk, A. Geloen, S. Alekseev, A. Rogov, V. Lysenko, V. Timoshenko, Carbon fluoroxide nanoparticles as fluorescent labels and sonosensitizers for theranostic applications. Sci. Technol. Adv. Mater. 16, 44601 (2015). https://doi.org/10.1088/1468-6996/16/4/044601
X. Pan, L. Bai, H. Wang, Q. Wu, H. Wang et al., Metal–organic-framework-derived carbon nanostructure augmented sonodynamic cancer therapy. Adv. Mater. 30, 1–9 (2018). https://doi.org/10.1002/adma.201800180
A. Marino, E. Almici, S. Migliorin, C. Tapeinos, M. Battaglini et al., Piezoelectric barium titanate nanostimulators for the treatment of glioblastoma multiforme. J. Colloid Interface Sci. 538, 449–461 (2019). https://doi.org/10.1016/j.jcis.2018.12.014
M.C. d’Agostino, K. Craig, E. Tibalt, S. Respizzi, Shock wave as biological therapeutic tool: from mechanical stimulation to recovery and healing, through mechanotransduction. Int. J. Surg. 24, 147–153 (2015). https://doi.org/10.1016/j.ijsu.2015.11.030
F. Foglietta, S. Duchi, R. Canaparo, G. Varchi, E. Lucarelli, B. Dozza, L. Serpe, Selective sensitiveness of mesenchymal stem cells to shock waves leads to anticancer effect in human cancer cell co-cultures. Life Sci. 173, 28–35 (2017). https://doi.org/10.1016/j.lfs.2017.01.009
F. Marano, R. Frairia, L. Rinella, M. Argenziano, B. Bussolati et al., Combining doxorubicin-nanobubbles and shockwaves for anaplastic thyroid cancer treatment: preclinical study in a xenograft mouse model. Endocr. Relat. Cancer 24, 275–286 (2017). https://doi.org/10.1530/ERC-17-0045
R. Canaparo, L. Serpe, G.P. Zara, R. Chiarle, L. Berta, R. Frairia, High energy shock waves (HESW) increase paclitaxel efficacy in a syngeneic model of breast cancer. Technol. Cancer Res. Treat. 7, 117–124 (2008). https://doi.org/10.1177/153303460800700204
J. Zhang, S. Shrivastava, R.O. Cleveland, T.H. Rabbitts, Lipid-mRNA nanoparticle designed to enhance intracellular delivery mediated by shock waves. ACS Appl. Mater. Interfaces. 11, 10481–10491 (2019). https://doi.org/10.1021/acsami.8b21398
L.M. López-Marín, A.L. Rivera, F. Fernández, A.M. Loske, Shock wave-induced permeabilization of mammalian cells. Phys. Life Rev. 26–27, 1–38 (2018). https://doi.org/10.1016/j.plrev.2018.03.001
R. Canaparo, L. Serpe, M.G. Catalano, O. Bosco, G.P. Zara, L. Berta, R. Frairia, High energy shock waves (HESW) for sonodynamic therapy: effects on HT-29 human colon cancer cells. Anticancer Res. 26, 3337–3342 (2006)
L. Serpe, R. Canaparo, L. Berta, A. Bargoni, G.P. Zara, R. Frairia, High energy shock waves and 5-aminolevulinic for sonodynamic therapy: effects in a syngeneic model of colon cancer. Technol. Cancer Res. Treat. 10, 85–93 (2011). https://doi.org/10.7785/tcrt.2012.500182
F. Foglietta, R. Canaparo, A. Francovich, F. Arena, S. Civera et al., Sonodynamic treatment as an innovative bimodal anticancer approach: shock wave-mediated tumor growth inhibition in a syngeneic breast cancer model. Discov. Med. 20, 197–205 (2015)
G. Varchi, F. Foglietta, R. Canaparo, M. Ballestri, F. Arena et al., Engineered porphyrin loaded core-shell nanoparticles for selective sonodynamic anticancer treatment. Nanomedicine 10, 3483–3494 (2015). https://doi.org/10.2217/nnm.15.150
R. Canaparo, G. Varchi, M. Ballestri, F. Foglietta, G. Sotgiu et al., Polymeric nanoparticles enhance the sonodynamic activity of meso-tetrakis (4-sulfonatophenyl) porphyrin in an in vitro neuroblastoma model. Int. J. Nanomed. 8, 4247–4263 (2013). https://doi.org/10.2147/IJN.S51070
L. Wang, D. Meng, Y. Hao, Y. Zhao, D. Li et al., Gold nanostars mediated combined photothermal and photodynamic therapy and X-ray imaging for cancer theranostic applications. J. Biomater. Appl. 30, 547–557 (2015). https://doi.org/10.1177/0885328215594481
A. Shanei, H. Akbari-Zadeh, Investigating the sonodynamic-radiosensitivity effect of gold nanoparticles on HeLa cervical cancer cells. J. Korean Med. Sci. 34, 1–15 (2019). https://doi.org/10.3346/jkms.2019.34.e243
Z. Behrouzkia, Z. Joveini, B. Keshavarzi, N. Eyvazzadeh, R.Z. Aghdam, Hyperthermia: how can it be used? Oman Med. J. 31, 89–97 (2016). https://doi.org/10.5001/omj.2016.19
P.S. Jiang, H.Y. Tsai, P. Drake, F.N. Wang, C.S. Chiang, Gadolinium-doped iron oxide nanoparticles induced magnetic field hyperthermia combined with radiotherapy increases tumour response by vascular disruption and improved oxygenation. Int. J. Hyperth. 6736, 1–9 (2017). https://doi.org/10.1080/02656736.2017.1308019
M. Li, Q. Zhao, X. Yi, X. Zhong, G. Song et al., Au@MnS@ZnS core/shell/shell nanoparticles for magnetic resonance imaging and enhanced cancer radiation therapy. ACS Appl. Mater. Interfaces. 8, 9557–9564 (2016). https://doi.org/10.1021/acsami.5b11588
N. Ma, Y.W. Jiang, X. Zhang, H. Wu, J.N. Myers et al., Enhanced radiosensitization of gold nanospikes via hyperthermia in combined cancer radiation and photothermal therapy. ACS Appl. Mater. Interfaces. 8, 28480–28494 (2016). https://doi.org/10.1021/acsami.6b10132
J.F. Hainfeld, L. Lin, L. Slatkin, F. Avraham Dilmanian, T.M. Vadas, H.M. Smilowitz, Gold nanoparticle hyperthermia reduces radiotherapy dose. Nanomed. Nanotechnol. Biol. Med. 10, 1609–1617 (2014). https://doi.org/10.1016/j.nano.2014.05.006
X. Yu, A. Li, C. Zhao, K. Yang, X. Chen, W. Li, Ultrasmall semimetal nanoparticles of bismuth for dual-modal computed tomography/photoacoustic imaging and synergistic thermoradiotherapy. ACS Nano 11, 3990–4001 (2017). https://doi.org/10.1021/acsnano.7b00476
F. Daneshvar, F. Salehi, M. Karimi, R.D. Vais, M.A. Mosleh-Shirazi, N. Sattarahmady, Combined X-ray radiotherapy and laser photothermal therapy of melanoma cancer cells using dual-sensitization of platinum nanoparticles. J. Photochem. Photobiol. B Biol. 203, 111737 (2020). https://doi.org/10.1016/j.jphotobiol.2019.111737
M. Zhou, Y. Chen, M. Adachi, X. Wen, B. Erwin et al., Single agent nanoparticle for radiotherapy and radio-photothermal therapy in anaplastic thyroid cancer. Biomaterials 57, 41–49 (2015). https://doi.org/10.1016/j.biomaterials.2015.04.013
V. Hosseini, M. Mirrahimi, A. Shakeri-Zadeh, F. Koosha, B. Ghalandari et al., Multimodal cancer cell therapy using Au@Fe2O3 core–shell nanoparticles in combination with photo-thermo-radiotherapy. Photodiagnosis Photodyn. Ther. 24, 129–135 (2018). https://doi.org/10.1016/j.pdpdt.2018.08.003
M.M. Movahedi, Z. Alamzadeh, S. Hosseini-Nami, A. Shakeri-Zadeh, G. Taheripak et al., Investigating the mechanisms behind extensive death in human cancer cells following nanoparticle assisted photo-thermo-radiotherapy. Photodiagnosis Photodyn. Ther. 29, 101600 (2020). https://doi.org/10.1016/j.pdpdt.2019.101600
J. Liu, Y. Yang, W. Zhu, X. Yi, Z. Dong et al., Nanoscale metal-organic frameworks for combined photodynamic and radiation therapy in cancer treatment. Biomaterials 97, 1–9 (2016). https://doi.org/10.1016/j.biomaterials.2016.04.034
C. Western, D. Hristov, J. Schlosser, Ultrasound imaging in radiation therapy: from interfractional to intrafractional guidance. Cureus 7, 1–19 (2015). https://doi.org/10.7759/cureus.280
R. Cirincione, F.M. Di Maggio, G.I. Forte, L. Minafra, V. Bravatà et al., High-intensity focused ultrasound- and radiation therapy-induced immuno-modulation: comparison and potential opportunities. Ultrasound Med. Biol. 43, 398–411 (2017). https://doi.org/10.1016/j.ultrasmedbio.2016.09.020
X. Liu, Y. Zhang, Y. Wang, W. Zhu, G. Li et al., Comprehensive understanding of magnetic hyperthermia for improving antitumor therapeutic efficacy. Theranostics 10, 3793–3815 (2020). https://doi.org/10.7150/thno.40805
A. Espinosa, R. Di Corato, J. Kolosnjaj-Tabi, P. Flaud, T. Pellegrino, C. Wilhelm, Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment. ACS Nano 10, 2436–2446 (2016). https://doi.org/10.1021/acsnano.5b07249
X. Ma, Y. Wang, X.L. Liu, H. Ma, G. Li et al., Fe3O4-Pd Janus nanoparticles with amplified dual-mode hyperthermia and enhanced ROS generation for breast cancer treatment. Nanoscale Horiz. 4, 1450–1459 (2019). https://doi.org/10.1039/c9nh00233b
R. Di Corato, G. Béalle, J. Kolosnjaj-Tabi, A. Espinosa, O. Clément et al., Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes. ACS Nano 9, 2904–2916 (2015). https://doi.org/10.1021/nn506949t
A. Curcio, A.K.A. Silva, S. Cabana, A. Espinosa, B. Baptiste et al., Iron oxide nanoflowers@CuS hybrids for cancer tri-therapy: interplay of photothermal therapy, magnetic hyperthermia and photodynamic therapy. Theranostics 9, 1288–1302 (2019). https://doi.org/10.7150/thno.30238
A. Józefczak, K. Kaczmarek, T. Hornowski, M. Kubovčíková, Z. Rozynek, M. Timko, A. Skumiel, Magnetic nanoparticles for enhancing the effectiveness of ultrasonic hyperthermia. Appl. Phys. Lett. 108, 1–5 (2016). https://doi.org/10.1063/1.4955130
E. Beguin, M.D. Gray, K.A. Logan, H. Nesbitt, Y. Sheng et al., Magnetic microbubble mediated chemo-sonodynamic therapy using a combined magnetic-acoustic device. J. Control Release 317, 23–33 (2020). https://doi.org/10.1016/j.jconrel.2019.11.013
S. Xiao, Z. Hu, Y. He, H. Jin, Y. Yang et al., Enhancement effect of microbubble-enhanced ultrasound in microwave ablation in rabbit VX2 liver tumors. Biomed. Res. Int. 2020, 1–10 (2020). https://doi.org/10.1155/2020/3050148
Z. Zhou, Y. Wang, S. Song, W. Wu, S. Wu, P.H. Tsui, Monitoring microwave ablation using ultrasound echo decorrelation imaging: an ex vivo study. Sensors 19, 977 (2019). https://doi.org/10.3390/s19040977
D. Gebreel, T. Shalaby, Y. Yousef, M. Mohamed, H. Badawy, Magnetic fluid based on Fe3O4 nanoparticles: preparation and hyperthermia application. Int. J. Chem. Appl. Biol. Sci. 1, 24 (2014). https://doi.org/10.4103/2348-0734.131792
X. Li, Y. Liu, F. Fu, M. Cheng, Y. Liu et al., Single NIR laser-activated multifunctional nanoparticles for cascaded photothermal and oxygen-independent photodynamic therapy. Nano-Micro Lett. 11, 68 (2019). https://doi.org/10.1007/s40820-019-0298-5
S. Luo, Z. Yang, X. Tan, Y. Wang, Y. Zeng et al., Multifunctional photosensitizer grafted on polyethylene glycol and polyethylenimine dual-functionalized nanographene oxide for cancer-targeted near-infrared imaging and synergistic phototherapy. ACS Appl. Mater. Interfaces. 8, 17176–17186 (2016). https://doi.org/10.1021/acsami.6b05383
C. Yao, L. Zhang, J. Wang, Y. He, J. Xin et al., Gold nanoparticle mediated phototherapy for cancer. J. Nanomater. 7, 167 (2016). https://doi.org/10.1155/2016/5497136
Q. Li, L. Hong, H. Li, C. Liu, Graphene oxide-fullerene C60 (GO-C60) hybrid for photodynamic and photothermal therapy triggered by near-infrared light. Biosens. Bioelectron. 89, 477–482 (2017). https://doi.org/10.1016/j.bios.2016.03.072
J. Lee, Y.H. Lee, C.B. Jeong, J.S. Choi, K.S. Chang, M. Yoon, Gold nanorods-conjugated TiO2 nanoclusters for the synergistic combination of phototherapeutic treatments of cancer cells. J. Nanobiotechnol. 16, 1–12 (2018). https://doi.org/10.1186/s12951-018-0432-4
A. Sazgarnia, A. Shanei, A.R. Taheri, N. Tayyebi Meibodi, H. Eshghi, N. Attaran, M. Shanei, The therapeutic effect of acoustic cavitation on breast carcinoma tumor model in BALB/c mice in the presence of gold nanoparticles. J. Ultrasound Med. 32, 475–483 (2013). https://doi.org/10.22122/jims.v37i531.11968
C. Dai, S. Zhang, Z. Liu, R. Wu, Y. Chen, Two-dimensional graphene augments nanosonosensitized sonocatalytic tumor eradication. ACS Nano 11, 9467–9480 (2017). https://doi.org/10.1021/acsnano.7b05215
F. Gao, G. He, H. Yin, J. Chen, Y. Liu et al., Titania-coated 2D gold nanoplates as nanoagents for synergistic photothermal/sonodynamic therapy in the second near-infrared window. Nanoscale 11, 2374–2384 (2019). https://doi.org/10.1039/C8NR07188H
A.C. Anselmo, S. Mitragotri, Nanoparticles in the clinic. Bioeng. Transl. Med. 1, 10–29 (2016). https://doi.org/10.1002/btm2.10003
N. Garino, T. Limongi, B. Dumontel, M. Canta, L. Racca et al., A microwave-assisted synthesis of zinc oxide nanocrystals finely tuned for biological applications. Nanomaterials 9, 212 (2019). https://doi.org/10.3390/nano9020212
A.C. Anselmo, S. Mitragotri, Nanoparticles in the clinic: an update. Bioeng. Transl. Med. 4, e10143 (2019). https://doi.org/10.1002/btm2.10143
J.M. Stern, V.V. Kibanov Solomonov, E. Sazykina, J.A. Schwartz, S.C. Gad, G.P. Goodrich, Initial evaluation of the safety of nanoshell-directed photothermal therapy in the treatment of prostate disease. Int. J. Toxicol. 35, 38–46 (2016). https://doi.org/10.1177/1091581815600170
A.R. Rastinehad, H. Anastos, E. Wajswol, J.S. Winoker, J.P. Sfakianos et al., Gold nanoshell-localized photothermal ablation of prostate tumors in a clinical pilot device study. Proc. Natl. Acad. Sci. U.S.A. 116, 18590–18596 (2019). https://doi.org/10.1073/pnas.1906929116