Abstract
Magnetic nanoparticles, including those formed of superparamagnetic iron oxides (SPIOs), are employed in various magnetic imaging and therapeutic techniques. In vivo imaging techniques based on the detection of magnetic nanoparticles inside the body include magnetic resonance imaging (MRI), magnetic particle imaging (MPI), magneto-motive ultrasonography (MMUS) and magneto-photoacoustic imaging (MPAI). Preclinical data indicate that the conditions required to heat up magnetic nanoparticles, including energy considerations, particle modifications, localization and exposure time, can be dynamically modulated during a single treatment procedure by monitoring imaging data acquired from the same magnetic nanoparticles. This Review explores the potential use of magnetic-nanoparticle-mediated imaging techniques combined with magnetic fluid hyperthermia (MFH) to selectively and precisely heat tumour locations while avoiding damage to surrounding healthy tissue. Imaging-guided MFH could provide individualized treatment plans based on information about the biodistribution of magnetic nanoparticles within the tumour and adjacent organs, as well as the volumetric distribution of the thermal dose. Requirements for the clinical translation of MFH-enabled magnetic imaging techniques are also discussed — the development of magnetic nanoparticle formulations with a favourable biosafety profile, optimal magnetic heating properties and maximal magnetic imaging signals; and the integration of magnetic imaging and heating hardware into a single platform.
Key points
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Multifunctional magnetic nanoparticles can be used as both therapeutic and diagnostic agents for multimodal cancer imaging and therapy.
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Combinations of magnetic imaging and hyperthermia could be used to provide individualized treatment plans based on magnetic nanoparticle biodistribution within the tumour and adjacent organs that provide guidance for an appropriate volumetric distribution of thermal dosing.
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A critical assessment of knowledge gaps in the field of precision hyperthermia is essential for increasing clinical translation.
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Navigation of complex regulations is essential for the manufacture of optimized magnetic nanoparticles for use with magnetic imaging-guided hyperthermia.
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References
Chhikara, B. S. & Parang, K. Global Cancer Statistics 2022: the trends projection analysis. Chem. Biol. Lett. 10, 451–451 (2023).
Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249 (2021).
Gao, Y. et al. Multifunctional nanoparticle for cancer therapy. MedComm 4, e187 (2023).
Ivkov, R. Magnetic nanoparticle hyperthermia: a new frontier in biology and medicine? Int. J. Hyperth. 29, 703–705 (2013).
Beola, L., Iturrioz-Rodríguez, N., Pucci, C., Bertorelli, R. & Ciofani, G. Drug-loaded lipid magnetic nanoparticles for combined local hyperthermia and chemotherapy against glioblastoma multiforme. ACS Nano 17, 18441–18455 (2023).
Hosseini, V. et al. Multimodal cancer cell therapy using Au@Fe2O3 core–shell nanoparticles in combination with photo-thermo-radiotherapy. Photodiagn. Photodyn. Ther. 24, 129–135 (2018).
Movahedi, M. M. et al. Investigating the photo-thermo-radiosensitization effects of folate-conjugated gold nanorods on KB nasopharyngeal carcinoma cells. Photodiagn. Photodyn. Ther. 24, 324–331 (2018).
Neshastehriz, A., Khosravi, Z., Ghaznavi, H. & Shakeri-Zadeh, A. Gold-coated iron oxide nanoparticles trigger apoptosis in the process of thermo-radiotherapy of U87-MG human glioma cells. Radiat. Environ. Biophys. 57, 405–418 (2018).
Mirrahimi, M. et al. Triple combination of heat, drug and radiation using alginate hydrogel co-loaded with gold nanoparticles and cisplatin for locally synergistic cancer therapy. Int. J. Biol. Macromol. 158, 617–626 (2020).
Alamzadeh, Z. et al. Gold nanoparticles promote a multimodal synergistic cancer therapy strategy by co-delivery of thermo-chemo-radio therapy. Eur. J. Pharm. Sci. 145, 105235 (2020).
Herrero de la Parte, B. et al. Proposal of new safety limits for in vivo experiments of magnetic hyperthermia antitumor therapy. Cancers 14, 3084 (2022).
Lenders, V. et al. Modulation of engineered nanomaterial interactions with organ barriers for enhanced drug transport. Chem. Soc. Rev. 52, 4672–4724 (2023).
Healy, S. et al. Clinical magnetic hyperthermia requires integrated magnetic particle imaging. Wiley Interdisc. Rev. Nanomed. Nanobiotechnol. 14, e1779 (2022).
Shakeri-Zadeh, A. et al. Folate receptor-targeted nanoprobes for molecular imaging of cancer: friend or foe? Nano Today 39, 101173 (2021).
Bulte, J. W. & Kraitchman, D. L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17, 484–499 (2004).
Abed, Z. et al. Iron oxide–gold core–shell nano-theranostic for magnetically targeted photothermal therapy under magnetic resonance imaging guidance. J. Cancer Res. Clin. Oncol. 145, 1213–1219 (2019).
Bulte, J. W. Superparamagnetic iron oxides as MPI tracers: a primer and review of early applications. Adv. Drug. Deliv. Rev. 138, 293–301 (2019).
Berezin, M. Y. Historical perspective on nanoparticles in imaging from 1895 to 2000. In Nanotechnology for Biomedical Imaging and Diagnostics: From Nanoparticle Design to Clinical Applications (ed. Berezin, M.Y.) (Wiley, 2014).
Johannsen, M. et al. Clinical hyperthermia of prostate cancer using magnetic nanoparticles: presentation of a new interstitial technique. Int. J. Hyperth. 21, 637–647 (2005).
Stark, D. D. et al. Superparamagnetic iron oxide: clinical application as a contrast agent for MR imaging of the liver. Radiology 168, 297–301 (1988).
Harisinghani, M. G. et al. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N. Engl. J. Med. 348, 2491–2499 (2003).
Xie, X. et al. Magnetic particle imaging: from tracer design to biomedical applications in vasculature abnormality. Adv. Mater. 36, e2306450 (2023).
Bulte, J. W. et al. Quantitative “hot-spot” imaging of transplanted stem cells using superparamagnetic tracers and magnetic particle imaging. Tomography 1, 91–97 (2015).
Jansson, T., Jansson, L., Mousavi, A., Persson, L. & Angenete, E. Detection of magnetomotive ultrasound signals from human tissue. Nanomed. Nanotechnol. Biol. Med. 47, 102621 (2023).
Sjöstrand, S. Evertsson, M. & Jansson, T. Contrast-enhanced magnetomotive ultrasound imaging (CE-MMUS) for colorectal cancer staging: assessment of sensitivity and resolution to detect alterations in tissue stiffness. In IEEE Int. Ultrasonics Symp. (IUS) 1077–1080 (IEEE, 2019).
Arsalani, S. et al. Hybrid nanoparticles of citrate-coated manganese ferrite and gold nanorods in magneto-optical imaging and thermal therapy. Nanomaterials 13, 434 (2023).
Bortot, B. et al. Image-guided cancer surgery: a narrative review on imaging modalities and emerging nanotechnology strategies. J. Nanobiotechnol. 21, 155 (2023).
Sharma, A. et al. Validation of a temperature-feedback controlled automated magnetic hyperthermia therapy device. Cancers 15, 327 (2023).
Mahmoudi, K., Bouras, A., Bozec, D., Ivkov, R. & Hadjipanayis, C. Magnetic hyperthermia therapy for the treatment of glioblastoma: a review of the therapy’s history, efficacy and application in humans. Int. J. Hyperth. 34, 1316–1328 (2018).
Gavilán, H. et al. Magnetic nanoparticles and clusters for magnetic hyperthermia: optimizing their heat performance and developing combinatorial therapies to tackle cancer. Chem. Soc. Rev. 50, 11614–11667 (2021).
Rodriguez, B. et al. Magnetic hyperthermia therapy for high-grade glioma: a state-of-the-art review. Pharmaceuticals 17, 300 (2024).
Adnan, A. et al. Hyperthermia and tumor immunity. Cancers 13, 2507 (2021).
Cazares-Cortes, E. et al. Recent insights in magnetic hyperthermia: from the “hot-spot” effect for local delivery to combined magneto-photo-thermia using magneto-plasmonic hybrids. Adv. Drug. Deliv. Rev. 138, 233–246 (2019).
Kaur, P., Aliru, M. L., Chadha, A. S., Asea, A. & Krishnan, S. Hyperthermia using nanoparticles—promises and pitfalls. Int. J. Hyperth. 32, 76–88 (2016).
Rahban, D., Doostan, M. & Salimi, A. Cancer therapy: prospects for application of nanoparticles for magnetic-based hyperthermia. Cancer Invest. 38, 507–521 (2020).
Beik, J. et al. Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J. Control. Rel. 235, 205–221 (2016).
Calderwood, S. K., Theriault, J. R. & Gong, J. How is the immune response affected by hyperthermia and heat shock proteins? Int. J. Hyperth. 21, 713–716 (2005).
Skitzki, J. J., Repasky, E. A. & Evans, S. S. Hyperthermia as an immunotherapy strategy for cancer. Curr. Opin. Invest. Drugs 10, 550–558 (2009).
Hadi, F. et al. Combinatorial effects of radiofrequency hyperthermia and radiotherapy in the presence of magneto‐plasmonic nanoparticles on MCF‐7 breast cancer cells. J. Cell. Physiol. 234, 20028–20035 (2019).
Beik, J. et al. Gold nanoparticle‐induced sonosensitization enhances the antitumor activity of ultrasound in colon tumor‐bearing mice. Med. Phys. 45, 4306–4314 (2018).
Curley, S. A., Palalon, F., Sanders, K. E. & Koshkina, N. V. The effects of non-invasive radiofrequency treatment and hyperthermia on malignant and nonmalignant cells. Int. J. Environ. Res. Public Health 11, 9142–9153 (2014).
Diederich, C. J. & Hynynen, K. Ultrasound technology for hyperthermia. Ultrasound Med. Biol. 25, 871–887 (1999).
Mensel, B., Weigel, C. & Hosten, N. Laser-induced thermotherapy. Recent Results Cancer Res. 167, 69–75 (2006).
Suriyanto, N. E. & Kumar, S. Physical mechanism and modeling of heat generation and transfer in magnetic fluid hyperthermia through Néelian and Brownian relaxation: a review. Biomed. Eng. Online 16, 36 (2017).
Gneveckow, U. et al. Description and characterization of the novel hyperthermia‐and thermoablation‐system for clinical magnetic fluid hyperthermia. Med. Phys. 31, 1444–1451 (2004).
Hergt, R., Dutz, S., Müller, R. & Zeisberger, M. Magnetic particle hyperthermia: nanoparticle magnetism and materials development for cancer therapy. J. Phys. Condens. Matter 18, S2919 (2006).
Huang, H. S. & Hainfeld, J. F. Intravenous magnetic nanoparticle cancer hyperthermia. Int. J. Nanomed. 8, 2521–2532 (2013).
Balivada, S. et al. A/C magnetic hyperthermia of melanoma mediated by iron(0)/iron oxide core/shell magnetic nanoparticles: a mouse study. BMC Cancer 10, 119 (2010).
Flores-Ramírez, A. et al. Physicochemical-electrochemical characterization of the nanocomposite chitosan-coated magnetite nanoparticles. J. Clust. Sci. 34, 1019–1035 (2023).
Choi, J.-G., Hasan, M., Akter, H. & Lee, S.-S. Characterization of dextran-coated magnetic nanoparticles (Fe3O4) conjugated with monoclonal antibody through low gradient magnet and centrifugation-based buffer separation processes. Curr. Appl. Phys. 48, 79–83 (2023).
Hasan, M., Choi, J.-G., Akter, H. & Lee, S.-S. Spleen distribution and serum immune responses after acute administration of silica-conjugated magnetite (Fe3O4) nanoparticles. AIP Adv. 13, 025135 (2023).
Gonzales-Weimuller, M., Zeisberger, M. & Krishnan, K. M. Size-dependent heating rates of iron oxide nanoparticles for magnetic fluid hyperthermia. J. Magn. Magn. Mater. 321, 1947–1950 (2009).
Nguyen, L. H. et al. The role of anisotropy in distinguishing domination of Néel or Brownian relaxation contribution to magnetic inductive heating: orientations for biomedical applications. Materials 14, 1875 (2021).
Mehak, Thummer, R. P. & Pandey, L. M. Surface modified iron-oxide based engineered nanomaterials for hyperthermia therapy of cancer cells. Biotechnol. Genet. Eng. Rev. 39, 1187–1233 (2023).
Mohammad, F. et al. Magnetically controlled drug delivery and hyperthermia effects of core-shell Cu@Mn3O4 nanoparticles towards cancer cells in vitro. Int. J. Biol. Macromol. 249, 126071 (2023).
Heydaryan, K., Mohammadalizadeh, M., Montazer, A. H. & Kashi, M. A. Reaction time-induced improvement in hyperthermia properties of cobalt ferrite nanoparticles with different sizes. Mater. Chem. Phys. 303, 127773 (2023).
Somvanshi, S. B., Jadhav, S. A., Gawali, S. S., Zakde, K. & Jadhav, K. Core-shell structured superparamagnetic Zn–Mg ferrite nanoparticles for magnetic hyperthermia applications. J. Alloy. Compd. 947, 169574 (2023).
Ali, I. et al. Comparison of copper-based Cu–Ni and Cu–Fe nanoparticles synthesized via laser ablation for magnetic hyperthermia and antibacterial applications. Phys. B 650, 414503 (2023).
Olusegun, S. J. et al. Synthesis and characterization of Sr2+ and Gd3+ doped magnetite nanoparticles for magnetic hyperthermia and drug delivery application. Ceram. Int. 49, 19851–19860 (2023).
Bulte, J. W., Wang, C. & Shakeri‐Zadeh, A. In vivo cellular magnetic imaging: labeled versus unlabeled cells. Adv. Funct. Mater. 32, 2207626 (2022).
Roumaih, K., Yehia, M. & Hassan, H. Synthesis and characterization of core–shell NiFe2O4@MgFe2O4 and ZnFe2O4@MgFe2O4 nanoferrites. J. Inorg. Organomet. Polym. 30, 3132–3142 (2020).
Patade, S. R. et al. Self-heating evaluation of superparamagnetic MnFe2O4 nanoparticles for magnetic fluid hyperthermia application towards cancer treatment. Ceram. Int. 46, 25576–25583 (2020).
Kharat, P. B., Somvanshi, S. B., Khirade, P. P. & Jadhav, K. Induction heating analysis of surface-functionalized nanoscale CoFe2O4 for magnetic fluid hyperthermia toward noninvasive cancer treatment. ACS Omega 5, 23378–23384 (2020).
Gasser, A. et al. Feasibility of superparamagnetic NiFe2O4 and GO-NiFe2O4 nanoparticles for magnetic hyperthermia. Mater. Sci. Eng. B 297, 116721 (2023).
Vatsalya, V. L. S., Sundari, G. S., Sridhar, C. S. & Lakshmi, C. S. Evidence of superparamagnetism in nano phased copper doped nickel zinc ferrites synthesized by hydrothermal method. Optik 247, 167874 (2021).
Rani, B. J., Mageswari, R., Ravi, G., Ganesh, V. & Yuvakkumar, R. Physico-chemical properties of pure and zinc incorporated cobalt nickel mixed ferrite (ZnxCo0.005−xNi0.005Fe2O4, where x = 0, 0.002, 0.004 M) nanoparticles. J. Mater. Sci. Mater. Electron. 28, 16450–16458 (2017).
Rezaei, B., Kermanpur, A. & Labbaf, S. Effect of Mn addition on the structural and magnetic properties of Zn–ferrite nanoparticles. J. Magn. Magn. Mater. 481, 16–24 (2019).
Sharma, R., Sharma, A., Chen, C. J., Kwon, S. & Hayek, S. S. Temperature and magnetic resonance characteristics of zinc, manganese, gadolinium, gold, iron magnetic nanoparticles and cytokine synergy in hyperthermia. J. Biomed. Sci. Eng. 1, 182–189 (2008).
Seo, W. S. et al. FeCo/graphitic-shell nanocrystals as advanced magnetic-resonance-imaging and near-infrared agents. Nat. Mater. 5, 971–976 (2006).
Muscas, G. et al. Magnetic interactions versus magnetic anisotropy in spinel ferrite nanoparticles. IEEE Magn. Lett. 10, 6110305 (2019).
Ma, Y. et al. Facile synthesis of ultrasmall MnFe2O4 nanoparticles with high saturation magnetization for magnetic resonance imaging. Ceram. Int. 47, 34005–34011 (2021).
Wang, Y. et al. Engineering ferrite nanoparticles with enhanced magnetic response for advanced biomedical applications. Mater. Today Adv. 8, 100119 (2020).
Schenck, J. F. The role of magnetic susceptibility in magnetic resonance imaging: MRI magnetic compatibility of the first and second kinds. Med. Phys. 23, 815–850 (1996).
Kalaiselvan, C. R. et al. Manganese ferrite (MnFe2O4) nanostructures for cancer theranostics. Coordin. Chem. Rev. 473, 214809 (2022).
Maier-Hauff, K. et al. Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme. J. Neurooncol. 81, 53–60 (2007).
Ahamed, M. et al. Oxidative stress mediated apoptosis induced by nickel ferrite nanoparticles in cultured A549 cells. Toxicology 283, 101–108 (2011).
Dadfar, S. M. et al. Size-isolation of superparamagnetic iron oxide nanoparticles improves MRI, MPI and hyperthermia performance. J. Nanobiotechnol. 18, 22 (2020).
Laurent, S. et al. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem. Rev. 108, 2064–2110 (2008).
Gavilán, H., Rizzo, G. M., Silvestri, N., Mai, B. T. & Pellegrino, T. Scale-up approach for the preparation of magnetic ferrite nanocubes and other shapes with benchmark performance for magnetic hyperthermia applications. Nat. Protoc. 18, 783–809 (2023).
Zou, L. et al. Microfluidic synthesis of magnetic nanoparticles in droplet-based microreactors. Mater. Chem. Phys. 276, 125384 (2022).
Blanco-Andujar, C. et al. Design of iron oxide-based nanoparticles for MRI and magnetic hyperthermia. Nanomedicine 11, 1889–1910 (2016).
Parat, A. et al. Dendrimer–nanoparticle conjugates in nanomedicine. Nanomedicine 10, 977–992 (2015).
Cheng, K.-W. & Hsu, S.-H. A facile method to prepare superparamagnetic iron oxide and hydrophobic drug-encapsulated biodegradable polyurethane nanoparticles. Int. J. Nanomed. 12, 1775–1789 (2017).
Schleich, N. et al. Dual anticancer drug/superparamagnetic iron oxide-loaded PLGA-based nanoparticles for cancer therapy and magnetic resonance imaging. Int. J. Pharm. 447, 94–101 (2013).
Chen, Y.-P. & Hsu, S.-H. Preparation and characterization of novel water-based biodegradable polyurethane nanoparticles encapsulating superparamagnetic iron oxide and hydrophobic drugs. J. Mater. Chem. B 2, 3391–3401 (2014).
Chan, N. et al. Multidentate block-copolymer-stabilized ultrasmall superparamagnetic iron oxide nanoparticles with enhanced colloidal stability for magnetic resonance imaging. Biomacromolecules 15, 2146–2156 (2014).
Li, Q. et al. Correlation between particle size/domain structure and magnetic properties of highly crystalline Fe3O4 nanoparticles. Sci. Rep. 7, 9894 (2017).
Liu, X. L. et al. Magnetic vortex nanorings: a new class of hyperthermia agent for highly efficient in vivo regression of tumors. Adv. Mater. 27, 1939–1944 (2015).
Yang, Y. et al. Orientation mediated enhancement on magnetic hyperthermia of Fe3O4 nanodisc. Adv. Funct. Mater. 25, 812–820 (2015).
Guardia, P. et al. Water-soluble iron oxide nanocubes with high values of specific absorption rate for cancer cell hyperthermia treatment. ACS Nano 6, 3080–3091 (2012).
Alphandéry, E. Biodistribution and targeting properties of iron oxide nanoparticles for treatments of cancer and iron anemia disease. Nanotoxicology 13, 573–596 (2019).
Nakamura, Y., Mochida, A., Choyke, P. L. & Kobayashi, H. Nanodrug delivery: is the enhanced permeability and retention effect sufficient for curing cancer? Bioconjug. Chem. 27, 2225–2238 (2016).
Huynh, N. T., Roger, E., Lautram, N., Benoît, J.-P. & Passirani, C. The rise and rise of stealth nanocarriers for cancer therapy: passive versus active targeting. Nanomedicine 5, 1415–1433 (2010).
Nguyen, L. N. M. et al. The exit of nanoparticles from solid tumours. Nat. Mater. 22, 1261–1272 (2023).
Bulte, J. W. et al. Specific MR imaging of human lymphocytes by monoclonal antibody‐guided dextran‐magnetite particles. Magn. Reson. Med. 25, 148–157 (1992).
Yu, N. et al. Transferrin-conjugated manganese dioxide/semiconducting polymer hybrid nanoparticles for targeted dual-model imaging of orthotopic glioblastoma. ACS Appl. Polym. Mater. 5, 4596–4603 (2023).
He, S., Du, Y., Tao, H. & Duan, H. Advances in aptamer-mediated targeted delivery system for cancer treatment. Int. J. Biol. Macromol. 124173 (2023).
Hashemian, A., Eshghi, H., Mansoori, G., Shakeri-Zadeh, A. & Mehdizadeh, A. Folate-conjugated gold nanoparticles (synthesis, characterization and design for cancer cells nanotechnology-based targeting). Int. J. Nanosci. Nanotechnol. 5, 25–34 (2009).
Dagogo-Jack, I. & Shaw, A. T. Tumour heterogeneity and resistance to cancer therapies. Nat. Rev. Clin. Oncol. 15, 81–94 (2018).
Schleich, N., Danhier, F. & Préat, V. Iron oxide-loaded nanotheranostics: major obstacles to in vivo studies and clinical translation. J. Control. Rel. 198, 35–54 (2015).
Shapiro, B. et al. Open challenges in magnetic drug targeting. Wiley Interdisc. Rev. Nanomed. Nanobiotechnol. 7, 446–457 (2015).
Almaki, J. H. et al. Trastuzumab-decorated nanoparticles for in vitro and in vivo tumor-targeting hyperthermia of HER2+ breast cancer. J. Mater. Chem. B 5, 7369–7383 (2017).
Sangnier, A. P. et al. Targeted thermal therapy with genetically engineered magnetite magnetosomes@ RGD: photothermia is far more efficient than magnetic hyperthermia. J. Control. Rel. 279, 271–281 (2018).
Mohammad, F., Raghavamenon, A. C., Claville, M. O., Kumar, C. S. & Uppu, R. M. Targeted hyperthermia-induced cancer cell death by superparamagnetic iron oxide nanoparticles conjugated to luteinizing hormone-releasing hormone. Nanotechnol. Rev. 3, 389–400 (2014).
Zhang, H. et al. Folic acid-targeted iron oxide nanoparticles as contrast agents for magnetic resonance imaging of human ovarian cancer. J. Ovarian Res. 9, 19 (2016).
Soleymani, M. et al. Effects of multiple injections on the efficacy and cytotoxicity of folate-targeted magnetite nanoparticles as theranostic agents for MRI detection and magnetic hyperthermia therapy of tumor cells. Sci. Rep. 10, 1695 (2020).
Yoo, M.-K. et al. Folate–PEG–superparamagnetic iron oxide nanoparticles for lung cancer imaging. Acta Biomater. 8, 3005–3013 (2012).
Ngen, E. J. et al. MRI assessment of prostate-specific membrane antigen (PSMA) targeting by a PSMA-targeted magnetic nanoparticle: potential for image-guided therapy. Mol. Pharm. 16, 2060–2068 (2019).
Majd, M. H. et al. Tamoxifen loaded folic acid armed PEGylated magnetic nanoparticles for targeted imaging and therapy of cancer. Colloids Surf. B 106, 117–125 (2013).
Wang, W. et al. M2 macrophage-targeted iron oxide nanoparticles for magnetic resonance image-guided magnetic hyperthermia therapy. J. Mater. Sci. Technol. 81, 77–87 (2021).
Zhu, N. et al. Surface modification of magnetic iron oxide nanoparticles. Nanomaterials 8, 810 (2018).
Dobrovolskaia, M. A., Shurin, M. & Shvedova, A. A. Current understanding of interactions between nanoparticles and the immune system. Toxicol. Appl. Pharmacol. 299, 78–89 (2016).
Lee, J. H. et al. Rod‐shaped iron oxide nanoparticles are more toxic than sphere‐shaped nanoparticles to murine macrophage cells. Environ. Toxicol. Chem. 33, 2759–2766 (2014).
Kedziorek, D. A. et al. Gene expression profiling reveals early cellular responses to intracellular magnetic labeling with superparamagnetic iron oxide nanoparticles. Magn. Reson. Med. 63, 1031–1043 (2010).
Liu, Y. et al. Genotoxicity assessment of magnetic iron oxide nanoparticles with different particle sizes and surface coatings. Nanotechnology 25, 425101 (2014).
Weissleder, R. Liver MR imaging with iron oxides: toward consensus and clinical practice. Radiology 193, 593–595 (1994).
Nowak-Jary, J. & Machnicka, B. Pharmacokinetics of magnetic iron oxide nanoparticles for medical applications. J. Nanobiotechnol. 20, 305 (2022).
Wang, Y.-X. J. Superparamagnetic iron oxide based MRI contrast agents: current status of clinical application. Quant. Imag. Med. Surg. 1, 35–40 (2011).
Solomon, S. B. & Silverman, S. G. Imaging in interventional oncology. Radiology 257, 624–640 (2010).
Cho, S., Park, W. & Kim, D.-H. Silica-coated metal chelating-melanin nanoparticles as a dual-modal contrast enhancement imaging and therapeutic agent. ACS Appl. Mater. Interf. 9, 101–111 (2017).
Tomitaka, A. et al. Development of magneto-plasmonic nanoparticles for multimodal image-guided therapy to the brain. Nanoscale 9, 764–773 (2017).
Tay, Z. W. et al. Magnetic particle imaging-guided heating in vivo using gradient fields for arbitrary localization of magnetic hyperthermia therapy. ACS Nano 12, 3699–3713 (2018).
Detappe, A. et al. Ultrasmall silica-based bismuth gadolinium nanoparticles for dual magnetic resonance–computed tomography image guided radiation therapy. Nano Lett. 17, 1733–1740 (2017).
Li, Y. et al. A smart and versatile theranostic nanomedicine platform based on nanoporphyrin. Nat. Commun. 5, 4712 (2014).
Park, W. et al. Immunomodulatory magnetic microspheres for augmenting tumor-specific infiltration of natural killer (NK) cells. ACS Appl. Mater. Interf. 9, 13819–13824 (2017).
Huang, P.-C. et al. Interstitial magnetic thermotherapy dosimetry based on shear wave magnetomotive optical coherence elastography. Biomed. Opt. Express 10, 539–551 (2019).
Mason, E. E. et al. Design analysis of an MPI human functional brain scanner. Int. J. Magn. Part. Imag. 3, 1703008 (2017).
Thieben, F. et al. System characterization of a human-sized 3D real-time magnetic particle imaging scanner for cerebral applications. Commun. Eng. 3, 47 (2024).
Senpan, A. et al. Conquering the dark side: colloidal iron oxide nanoparticles. ACS Nano 3, 3917–3926 (2009).
Park, S., Jang, J., Kim, J., Kim, Y. S. & Kim, C. Real-time triple-modal photoacoustic, ultrasound, and magnetic resonance fusion imaging of humans. IEEE Trans. Med. Imaging 36, 1912–1921 (2017).
Chan, M.-H., Hsieh, M.-R., Liu, R.-S., Wei, D.-H. & Hsiao, M. Magnetically guided theranostics: optimizing magnetic resonance imaging with sandwich-like kaolinite-based iron/platinum nanoparticles for magnetic fluid hyperthermia and chemotherapy. Chem. Mater. 32, 697–708 (2019).
Buchholz, O. et al. In situ theranostic platform combining highly localized magnetic fluid hyperthermia, magnetic particle imaging, and thermometry in 3D. Theranostics 14, 324–340 (2024).
Behrends, A. et al. Integrable magnetic fluid hyperthermia systems for 3D magnetic particle imaging. Nanotheranostics 8, 163–178 (2024).
Nakamura, H., Ito, N., Kotake, F., Mizokami, Y. & Matsuoka, T. Tumor-detecting capacity and clinical usefulness of SPIO-MRI in patients with hepatocellular carcinoma. J. Gastroenterol. 35, 849–855 (2000).
Asadi, M. et al. MRI-based numerical modeling strategy for simulation and treatment planning of nanoparticle-assisted photothermal therapy. Phys. Med. 66, 124–132 (2019).
Lin, Y. et al. Magnetic nanoparticles applied in targeted therapy and magnetic resonance imaging: crucial preparation parameters, indispensable pre-treatments, updated research advancements and future perspectives. J. Mater. Chem. B 8, 5973–5991 (2020).
Chu, W. et al. Magnetic resonance-guided high-intensity focused ultrasound hyperthermia for recurrent rectal cancer: MR thermometry evaluation and preclinical validation. Int. J. Radiat. Oncol. Biol. Phys. 95, 1259–1267 (2016).
Wang, X., Pan, F., Xiang, Z., Jia, W. & Lu, W. Magnetic Fe3O4@PVP nanotubes with high heating efficiency for MRI-guided magnetic hyperthermia applications. Mater. Lett. 262, 127187 (2020).
Beik, J. et al. Simulation-guided photothermal therapy using MRI-traceable iron oxide-gold nanoparticle. J. Photochem. Photobiol. B 199, 111599 (2019).
Lozano-Pedraza, C. et al. Assessing the parameters modulating optical losses of iron oxide nanoparticles under near infrared irradiation. Nanoscale Adv. 3, 6490–6502 (2021).
Rieke, V. in Interventional Magnetic Resonance Imaging (eds Kahn, T. & Busse, H.) 271–288 (Springer, 2011).
Shakeri-Zadeh, A. et al. MPI of SuperSPIO20-labeled ALS patient-derived, genome-edited iPSCs and iPSC-derived motor neurons. Int. J. Magn. Part. Imag. 8, 203003 (2022).
Shakeri-Zadeh, A., Kuddannaya, S., Bibic, A., Walczak, P. & Bulte, J. Fast dynamic MPI cytometry. Int. J. Magn. Part. Imag. 9, 577 (2023).
Wang, C., Shakeri-Zadeh, A., Kuddannaya, S., Arifin, D. & Bulte, J. Versatile superparamagnetic radiopaque nanocomplex for in vivo MPI, MRI, and CT stem cell tracking. Int. J. Magn. Part. Imag. 9, 576 (2023).
Ghaemi, B. et al. Smart intratumoral delivery of theranostic gold-iron oxide nanoflowers in prostate cancer using tumor-tropic mesenchymal stem cells. Int. J. Magn. Part. Imag. 9, 573 (2023).
Carlton, H. et al. HYPER: pre-clinical device for spatially-confined magnetic particle hyperthermia. Int. J. Hyperth. 40, 2272067 (2023).
Tay, Z. W. et al. A high-throughput, arbitrary-waveform, MPI spectrometer and relaxometer for comprehensive magnetic particle optimization and characterization. Sci. Rep. 6, 34180 (2016).
Lüdtke-Buzug, K. et al. Comparison of commercial iron oxide-based MRI contrast agents with synthesized high-performance MPI tracers. Biomed. Tech. 58, 527–533 (2013).
Kranemann, T. C. et al. An MPI-compatible HIFU transducer: experimental evaluation of interferences. Int. J. Magn. Part. Imag. 4, 1811003 (2018).
Oh, J. et al. Detection of magnetic nanoparticles in tissue using magneto-motive ultrasound. Nanotechnology 17, 4183 (2006).
Mehrmohammadi, M. et al. In vivo pulsed magneto-motive ultrasound imaging using high-performance magnetoactive contrast nanoagents. Nanoscale 5, 11179–11186 (2013).
Mallidi, S., Larson, T., Aaron, J., Sokolov, K. & Emelianov, S. Molecular specific optoacoustic imaging with plasmonic nanoparticles. Opt. Express 15, 6583–6588 (2007).
Mehrmohammadi, M., Yoon, K., Qu, M., Johnston, K. & Emelianov, S. Enhanced pulsed magneto-motive ultrasound imaging using superparamagnetic nanoclusters. Nanotechnology 22, 045502 (2010).
Kubelick, K. P. & Mehrmohammadi, M. Magnetic particles in motion: magneto-motive imaging and sensing. Theranostics 12, 1783 (2022).
Pope, A. G. et al. Contrast-enhanced imaging of SPIO-labeled platelets using magnetomotive ultrasound. Phys. Med. Biol. 58, 7277 (2013).
Ruohonen, J. & Ilmoniemi, R. Focusing and targeting of magnetic brain stimulation using multiple coils. Med. Biol. Eng. Comput. 36, 297–301 (1998).
Qu, M. et al. Magneto-photo-acoustic imaging. Biomed. Opt. Express 2, 385–396 (2011).
Li, J. et al. Magnetically responsive optical modulation: from anisotropic nanostructures to emerging applications. Adv. Funct. Mat. 34, 2308293 (2023).
Fan, Y. et al. The LMIT: light-mediated minimally-invasive theranostics in oncology. Theranostics 14, 341–362 (2024).
Kallumadil, M. et al. Suitability of commercial colloids for magnetic hyperthermia. J. Magn. Magn. Mater. 321, 1509–1513 (2009).
Bauer, L. M., Situ, S. F., Griswold, M. A. & Samia, A. C. S. Magnetic particle imaging tracers: state-of-the-art and future directions. J. Phys. Chem. Lett. 6, 2509–2517 (2015).
Brandt, C. & Schmidt, C. Modeling magnetic particle imaging for dynamic tracer distributions. Sens. Imag. 22, 45 (2021).
Eberbeck, D., Wiekhorst, F., Wagner, S. & Trahms, L. How the size distribution of magnetic nanoparticles determines their magnetic particle imaging performance. Appl. Phys. Lett. 98, 182502 (2011).
Ferguson, R. M., Khandhar, A. P. & Krishnan, K. M. Tracer design for magnetic particle imaging. J. Appl. Phys. 111, 07B318 (2012).
Khandhar, A. P., Ferguson, R. M., Arami, H. & Krishnan, K. M. Monodisperse magnetite nanoparticle tracers for in vivo magnetic particle imaging. Biomaterials 34, 3837–3845 (2013).
Du, Y., Lai, P. T., Leung, C. H. & Pong, P. W. Design of superparamagnetic nanoparticles for magnetic particle imaging (MPI). Int. J. Mol. Sci. 14, 18682–18710 (2013).
Mahdavi, M. et al. Synthesis, surface modification and characterisation of biocompatible magnetic iron oxide nanoparticles for biomedical applications. Molecules 18, 7533–7548 (2013).
Paysen, H. et al. Towards quantitative magnetic particle imaging: a comparison with magnetic particle spectroscopy. AIP Adv. 8, 056712 (2018).
Riedinger, A. et al. Subnanometer local temperature probing and remotely controlled drug release based on azo-functionalized iron oxide nanoparticles. Nano Lett. 13, 2399–2406 (2013).
Dong, J. & Zink, J. I. Taking the temperature of the interiors of magnetically heated nanoparticles. ACS Nano 8, 5199–5207 (2014).
Zhang, J. et al. Magnetic particle imaging deblurring with dual contrastive learning and adversarial framework. Comput. Biol. Med. 165, 107461 (2023).
Csóka, I., Ismail, R., Jójárt-Laczkovich, O. & Pallagi, E. Regulatory considerations, challenges and risk-based approach in nanomedicine development. Curr. Med. Chem. 28, 7461–7476 (2021).
Ali, F., Neha, K. & Parveen, S. Current regulatory landscape of nanomaterials and nanomedicines: a global perspective. J. Drug. Deliv. Sci. Technol. 80, 104118 (2022).
Foulkes, R. et al. The regulation of nanomaterials and nanomedicines for clinical application: current and future perspectives. Biomater. Sci. 8, 4653–4664 (2020).
Banala, V. T., Mukherjee, D., Mahajan, S. & Singh, P. K. in Multifunctional Nanocarriers (eds Mehra, N. K. et al.) 501–521 (Elsevier, 2022).
Paradise, J. Regulating nanomedicine at the food and drug administration. AMA J. Ethics 21, E347–355 (2019).
Liu, Y., Zhu, S., Gu, Z., Chen, C. & Zhao, Y. Toxicity of manufactured nanomaterials. Particuology 69, 31–48 (2022).
Dahnke, H. & Schaeffter, T. Limits of detection of SPIO at 3.0 T using T2* relaxometry. Magn. Reson. Med. 53, 1202–1206 (2005).
Yu, E. Y. et al. Magnetic particle imaging: a novel in vivo imaging platform for cancer detection. Nano Lett. 17, 1648–1654 (2017).
Ding, N. et al. Sensitive photoacoustic/magnetic resonance dual imaging probe for detection of malignant tumors. J. Pharm. Sci. 109, 3153–3159 (2020).
van Wijk, D. F. et al. Increasing spatial resolution of 3T MRI scanning improves reproducibility of carotid arterial wall dimension measurements. MAGMA 27, 219–226 (2014).
Gleich, B. & Weizenecker, J. Tomographic imaging using the nonlinear response of magnetic particles. Nature 435, 1214–1217 (2005).
Qu, M. et al. Contrast-enhanced magneto-photo-acoustic imaging in vivo using dual-contrast nanoparticles. Photoacoustics 2, 55–62 (2014).
Ohgushi, M., Nagayama, K. & Wada, A. Dextran-magnetite: a new relaxation reagent and its application to T2 measurements in gel systems. J. Magn. Reson. 29, 599–601 (1978).
De Vries, I. J. M. et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat. Biotechnol. 23, 1407–1413 (2005).
Carey, R., Newman, D. & Thomas, B. Photo-acoustic detection of magneto-optic absorption (MPAS) in thin iron films. J. Phys. D 15, 343 (1982).
Oldenburg, A. L., Gunther, J. R. & Boppart, S. A. Imaging magnetically labeled cells with magnetomotive optical coherence tomography. Opt. Lett. 30, 747–749 (2005).
Gilchrist, R. et al. Selective inductive heating of lymph nodes. Ann. Surg. 146, 596 (1957).
Jordan, A. et al. Presentation of a new magnetic field therapy system for the treatment of human solid tumors with magnetic fluid hyperthermia. J. Magn. Magn. Mater. 225, 118–126 (2001).
Sun, Y. et al. Superparamagnetic PLGA-iron oxide microcapsules for dual-modality US/MR imaging and high intensity focused US breast cancer ablation. Biomaterials 33, 5854–5864 (2012).
Fu, G. et al. Magnetic Prussian blue nanoparticles for targeted photothermal therapy under magnetic resonance imaging guidance. Bioconjug. Chem. 25, 1655–1663 (2014).
Song, G. et al. Carbon-coated FeCo nanoparticles as sensitive magnetic-particle-imaging tracers with photothermal and magnetothermal properties. Nat. Biomed. Eng. 4, 325–334 (2020).
Bui, M. P., Le, T.-A. & Yoon, J. A magnetic particle imaging-based navigation platform for magnetic nanoparticles using interactive manipulation of a virtual field free point to ensure targeted drug delivery. IEEE Trans. Industr. Electron. 68, 12493–12503 (2020).
Wang, Q. et al. Ultrasound Doppler-guided real-time navigation of a magnetic microswarm for active endovascular delivery. Sci. Adv. 7, eabe5914 (2021).
Yang, H. Y., Li, Y. & Lee, D. S. Multifunctional and stimuli‐responsive magnetic nanoparticle‐based delivery systems for biomedical applications. Adv. Ther. 1, 1800011 (2018).
Jalili, N. A., Jaiswal, M. K., Peak, C. W., Cross, L. M. & Gaharwar, A. K. Injectable nanoengineered stimuli-responsive hydrogels for on-demand and localized therapeutic delivery. Nanoscale 9, 15379–15389 (2017).
Castro-Torres, J. L., Méndez, J., Torres-Lugo, M. & Juan, E. Development of handheld induction heaters for magnetic fluid hyperthermia applications and in-vitro evaluation on ovarian and prostate cancer cell lines. Biomed. Phys. Eng. Express 9, 035010 (2023).
Son, S. et al. Cancer therapeutics based on diverse energy sources. Chem. Soc. Rev. 51, 8201–8215 (2022).
Chitnis, P. V., Mamou, J., McLaughlan, J., Murray, T. & Roy, R. A. Photoacoustic thermometry for therapeutic hyperthermia. In IEEE Int. Ultrasonics Symp. (IUS) 1757–1760 (IEEE, 2009).
Acknowledgements
A.S.-Z. and J.W.M.B. are supported by National Institutes of Health (NIH) grants R01 CA257557 and S10 OD026740.
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A.S.-Z. composed the initial draft, made illustrations and performed a literature search. J.W.M.B. contributed to the writing, overall outline and revisions. Both authors reviewed and approved all versions of this manuscript.
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Shakeri-Zadeh, A., Bulte, J.W.M. Imaging-guided precision hyperthermia with magnetic nanoparticles. Nat Rev Bioeng (2024). https://doi.org/10.1038/s44222-024-00257-3
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DOI: https://doi.org/10.1038/s44222-024-00257-3