Magnetic Particle Imaging-Guided Heating in Vivo Using Gradient Fields for Arbitrary Localization of Magnetic Hyperthermia Therapy
Open accessAbstract
Image-guided treatment of cancer enables physicians to localize and treat tumors with great precision. Here, we present in vivo results showing that an emerging imaging modality, magnetic particle imaging (MPI), can be combined with magnetic hyperthermia into an image-guided theranostic platform. MPI is a noninvasive 3D tomographic imaging method with high sensitivity and contrast, zero ionizing radiation, and is linearly quantitative at any depth with no view limitations. The same superparamagnetic iron oxide nanoparticle (SPIONs) tracers imaged in MPI can also be excited to generate heat for magnetic hyperthermia. In this study, we demonstrate a theranostic platform, with quantitative MPI image guidance for treatment planning and use of the MPI gradients for spatial localization of magnetic hyperthermia to arbitrarily selected regions. This addresses a key challenge of conventional magnetic hyperthermia-SPIONs delivered systemically accumulate in off-target organs ( e.g., liver and spleen), and difficulty in localizing hyperthermia results in collateral heat damage to these organs. Using a MPI magnetic hyperthermia workflow, we demonstrate image-guided spatial localization of hyperthermia to the tumor while minimizing collateral damage to the nearby liver (1-2 cm distance). Localization of thermal damage and therapy was validated with luciferase activity and histological assessment. Apart from localizing thermal therapy, the technique presented here can also be extended to localize actuation of drug release and other biomechanical-based therapies. With high contrast and high sensitivity imaging combined with precise control and localization of the actuated therapy, MPI is a powerful platform for magnetic-based theranostics.
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Magnetic drug targeting needs very strong magnetic fields for successful application in humans, increasing hardware cost and making it less attractive for clinical implementation.
“Furthermore, magnetic drug targeting needs very strong magnetic fields for successful application in humans, which increases the cost of the hardware setup, and which makes it less attractive for clinical implementation [199].”
From Iron oxide nanoparticles: Diagnostic, therapeutic and theranostic applications (2019) · cites this paper as [199]
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“(a) Localized hyperthermia guided by the magnetic particle imaging technique (Reproduced with permission from [54].”
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“have recently demonstrated spatially specific, tumor targeted hyperthermia with 7 mm resolution in small animal models (Figure 5b) (Tay et al., 2018).”
BackgroundInfluentialMultifunctional phototheranostic nanomedicine for cancer imaging and treatment
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“Moreover, there have already been several ways to accelerate the enhancement of tissue temperatures, such as light irradiation, the action of an alternating magnetic field (magnetic hyperthermia) [45], and microwave radiation (microwave hyperthermia) [46].”
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Superparamagnetic iron oxides as MPI tracers: A primer and review of early applications
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“To proof this, localization of thermal damage and therapy was validated with luciferase activity and histological assessment [55].”
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“using gradient magnetic field, heating of SPIO particles can be achieved only at the location of the FFR [1, 65, 66].”
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BackgroundPhotothermal conversion and transfer in photothermal therapy: From macroscale to nanoscale
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Magnetic Hyperthermia and Radiation Therapy: Radiobiological Principles and Current Practice †
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“(h) Stimulation of the MNPs can be spatially varying, resulting in non-uniform temperature distributions by design [210,211], similar to “dose painting” in RT.”
BackgroundA mitochondria-targeting magnetothermogenic nanozyme for magnet-induced synergistic cancer therapy
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Bioorthogonal chemistry for prodrug activation in vivo
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“Adapted with permission from Reference [15].”
InfluentialTriggering antitumoural drug release and gene expression by magnetic hyperthermia
Moros, M., Idiago-López, J., Asín, L., Antolín, E. M., Beola, L., Grazú, V., Fratila, R. M., Gutiérrez, L., & de la Fuente, J. M. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.10.004 · Cited by 142 · see citing works
Thermo-Sensitive Nanomaterials: Recent Advance in Synthesis and Biomedical Applications
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“The methods used for the generation of hyperthermia are microwave [159], ultrasound [160], magnetic [161], near-infrared (NIR) laser, known as photo-thermal therapy (PTT) [162], and radiofrequency [163].”
MethodWhither Magnetic Hyperthermia? A Tentative Roadmap
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BackgroundImprovement of Hyperthermia Properties of Iron Oxide Nanoparticles by Surface Coating
Vassallo, M., Martella, D., Barrera, G., Celegato, F., Coïsson, M., Ferrero, R., Olivetti, E. S., Troia, A., Sozeri, H., Parmeggiani, C., et al. (2023) · ACS Omega · doi:10.1021/acsomega.2c06244 · Cited by 137 · see citing works
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Magnetic Particle Imaging: Current Applications in Biomedical Research
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Non‐Invasive Thermal Therapy for Tissue Engineering and Regenerative Medicine
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“Additionally, MNPs can be utilized in magnetic hyperthermia to destroy cancer cells and decrease tumour volume via a targeted approach [86].”
BackgroundMonitoring Intracranial Cerebral Hemorrhage Using Multicontrast Real-Time Magnetic Particle Imaging
Szwargulski, P., Wilmes, M., Javidi, E., Thieben, F., Graeser, M., Koch, M., Gruettner, C., Adam, G., Gerloff, C. P., Magnus, T. U., et al. (2020) · ACS Nano · doi:10.1021/acsnano.0c06326 · Cited by 118 · see citing works
Chemodynamic nanomaterials for cancer theranostics
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“This enabled localized treatment of tumors (potentially lung tumors) while sparing other tissues with non-specific SPION uptake [47,50].”
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A review on numerical modeling for magnetic nanoparticle hyperthermia: Progress and challenges
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“P r oo f - o f - c o n c e p t h a s a l r e a d y b ee n d e m o n s t r a t e d [ 80 ] , a n d i s u s e f u l f o r M N P l o c a l i z a t i o n .”
TranSMS: Transformers for Super-Resolution Calibration in Magnetic Particle Imaging
Güngör, A., Askin, B., Soydan, D. A., Sarıtaş, E. Ü., Top, C. B., & Çukur, T. (2022) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2022.3189693 · Cited by 115 · see citing works
Imaging-guided precision hyperthermia with magnetic nanoparticles
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“To ensure the safety of MFH procedures, heating must be induced only in the tumour, which might be feasible with imaging guidance 13,122 (Fig.”
InfluentialChang, X., Wu, Q., Wu, Y., Xi, X., Cao, J., Chu, H., Liu, Q., Li, Y., Wu, W., Fang, X., et al. (2022) · Nano Letters · doi:10.1021/acs.nanolett.2c03260 · Cited by 109 · see citing works
A Magneto-Optical Nanoplatform for Multimodality Imaging of Tumors in Mice
Song, G., Zheng, X., Wang, Y., Xia, X., Chu, S., & Rao, J. (2019) · ACS Nano · doi:10.1021/acsnano.9b01436 · Cited by 109 · see citing works
Real-Time Magnetic Navigation of a Rotating Colloidal Microswarm Under Ultrasound Guidance
Wang, Q., Yang, L., Yu, J., Chiu, P. W. Y., Zheng, Y., & Zhang, L. (2020) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2020.2987045 · Cited by 108 · see citing works
“Among them, magnetite nanoparticles are treated as promising candidates and have been applied in medical imaging and biosensing [42], [43].”
BackgroundMeasles and rubella elimination in the WHO Region for Europe: progress and challenges
O’Connor, P. M., Jankovic, D., Muscat, M., Mamou, M. C. B., Reef, S. E., Papania, M. J., Singh, S., Kaloumenos, T., Butler, R., & Datta, S. S. (2017) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2017.01.003 · Cited by 123 · see citing works
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“[13] utilized MPI to guide MFH in vivo and found that MPI was able to accurately quantify amounts of iron oxide administered.”
BackgroundMethodInfluentialStimuli‐Responsive Materials for Biomedical Applications
do Nascimento, A. T., Stoddart, P. R., Goris, T., Kael, M., Manasseh, R., Alt, K., Tashkandi, J., Kim, B. C., & Moulton, S. E. (2025) · Advanced Materials · doi:10.1002/adma.202507559 · Cited by 100 · see citing works
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“[55] reported an emerging magnetic particle imaging (MPI)-induced hyperthermia therapy, by which the spatial localization of thermal damage to the tumor was realized while minimizing the collateral damage to the nearby liver with 1–2 cm distance.”
BackgroundChen, J., Liu, J., Hu, Y., Tian, Z., & Zhu, Y. (2019) · Science and Technology of Advanced Materials · doi:10.1080/14686996.2019.1682467 · Cited by 97 · see citing works
Advances in Magnetic Nanoparticle‐Mediated Cancer Immune‐Theranostics
Cheng, H., Tsao, H., Chiang, C., & Chen, S. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202001451 · Cited by 98 · see citing works
Harvell-Smith, S., Tung, L. D., & Thanh, N. T. K. (2021) · Nanoscale · doi:10.1039/d1nr05670k · Cited by 96 · see citing works
Clinical magnetic hyperthermia requires integrated magnetic particle imaging
Healy, S., Bakuzis, A. F., Goodwill, P. W., Attaluri, A., Bulte, J. W. M., & Ivkov, R. (2022) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1779 · Cited by 95 · see citing works
Aspects of high-performance and bio-acceptable magnetic nanoparticles for biomedical application
Kush, P., Kumar, P., Singh, R., & Kaushik, A. K. (2021) · Asian Journal of Pharmaceutical Sciences · doi:10.1016/j.ajps.2021.05.005 · Cited by 96 · see citing works
Nanoparticle-based Cell Trackers for Biomedical Applications
Ni, J., Li, Y., Yue, W., Liu, B., & Li, K. (2020) · Theranostics · doi:10.7150/thno.39915 · Cited by 87 · see citing works
“As compared to MRI, MPI only requires non-ionizing and low frequency magnetic fields that are safer for clinical translation.”
BackgroundInfluentialTay, Z. W., Chandrasekharan, P., Fellows, B. D., Rodrigo, I., Yu, E. Y., Olivo, M., & Conolly, S. (2021) · Cancers · doi:10.3390/cancers13215285 · Cited by 84 · see citing works
“This ideal workflow was demonstrated in a rodent cancer model by Tay et al. 2018 (Figure 7a), where the efficacy of precision MHT and mitigation of collateral thermal damage to the liver was validated in vivo [15] (Figure 7c–e).”
BackgroundMethodInfluentialRajendrakumar, S. K., Uthaman, S., Cho, C.-S., & Park, I. (2018) · Biomacromolecules · doi:10.1021/acs.biomac.8b00460 · Cited by 83 · see citing works
Externally Triggered Heat and Drug Release from Magnetically Controlled Nanocarriers
Fuller, E. G., Sun, H. R., Dhavalikar, R., Unni, M., Scheutz, G. M., Sumerlin, B. S., & Rinaldi, C. (2019) · ACS Applied Polymer Materials · doi:10.1021/acsapm.8b00100 · Cited by 81 · see citing works
Infrared‐Emitting Multimodal Nanostructures for Controlled In Vivo Magnetic Hyperthermia
Ximendes, E. C., Marin, R., Shen, Y., Ruiz, D., Gómez‐Cerezo, D., Rodríguez‐Sevilla, P., Lifante, J., Viveros-Méndez, P. X., Gámez, F., García‐Soriano, D., et al. (2021) · Advanced Materials · doi:10.1002/adma.202100077 · Cited by 80 · see citing works
A Perspective on Cell Tracking with Magnetic Particle Imaging
Sehl, O. C., Gevaert, J. J., Melo, K. P., Knier, N. N., & Foster, P. J. (2020) · Tomography · doi:10.18383/j.tom.2020.00043 · Cited by 79 · see citing works
“MP gradients can be used to target an ROI by aligning the FFR with a heating target and magnetically restrict SPIONs in surrounding tissue (71).”
MethodMagnetic Strategies for Nervous System Control
Christiansen, M. G., Senko, A. W., & Anikeeva, P. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050241 · Cited by 76 · see citing works
“…(Gould et al. 1978, Walcott et al. 1979, Kirschvink et al. 1985), including humans (Kirschvink et al. 1992, Gilder et al. 2018), it likely serves a metabolic rather than a sensory function, and evidence of magnetitedependent cell signaling remains elusive (Treiber et al. 2012, Edelman et al. 2015).”
BackgroundPMMA-Fe 3 O 4 for internal mechanical support and magnetic thermal ablation of bone tumors
Yu, K., Liang, B., Zheng, Y., Exner, A. A., Kolios, M. C., Xu, T., Guo, D., Cai, X., Wang, Z., Ran, H., et al. (2019) · Theranostics · doi:10.7150/thno.34157 · Cited by 76 · see citing works
“shaped magnetic fields to "gate" the heating only to selected regions under MRI guidance [45].”
The Effects of Localized Heat on the Hallmarks of Cancer
Hannon, G., Tansi, F. L., Hilger, I., & Prina‐Mello, A. (2021) · Advanced Therapeutics · doi:10.1002/adtp.202000267 · Cited by 76 · see citing works
Magnetic systems for cancer immunotherapy
Day, N. B., Wixson, W. C., & Shields, C. W. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.03.023 · Cited by 76 · see citing works
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Long circulating tracer tailored for magnetic particle imaging
Liu, S., Chiu‐Lam, A., Rivera‐Rodriguez, A., DeGroff, R., Savliwala, S., Sarna, N. S., & Rinaldi, C. (2021) · Nanotheranostics · doi:10.7150/ntno.58548 · Cited by 73 · see citing works
“In addition, because SPIONs can be used to label cells and other biomaterials, MPI has tremendous potential for applications such as cell tracking [3], nanoparticle drug delivery [4], image-guided procedures [5], monitoring tissue regeneration scaffolds [6], monitoring the brain [7], and blood pool imaging [8, 9].”
BackgroundUsing small-angle scattering to guide functional magnetic nanoparticle design
Honecker, D., Bersweiler, M., Erokhin, S., Berkov, D. V., Chesnel, K., Venero, D. A., Qdemat, A., Disch, S., Jochum, J. K., Michels, A., et al. (2022) · Nanoscale Advances · doi:10.1039/d1na00482d · Cited by 73 · see citing works
Review: Remotely controlled magneto-regulation of therapeutics from magnetoelastic gel matrices
Ganguly, S., & Margel, S. (2020) · Biotechnology Advances · doi:10.1016/j.biotechadv.2020.107611 · Cited by 72 · see citing works
Brero, F., Albino, M., Antoccia, A., Arosio, P., Avolio, M., Berardinelli, F., Bettega, D., Calzolari, P., Ciocca, M., Corti, M., et al. (2020) · Nanomaterials · doi:10.3390/nano10101919 · Cited by 74 · see citing works
The application of nanoparticles-based ferroptosis, pyroptosis and autophagy in cancer immunotherapy
Deng, W., Shang, H., Tong, Y., Liu, X., Huang, Q., He, Y. T., Wu, J., Ba, X., Chen, Z., Chen, Y., et al. (2024) · Journal of Nanobiotechnology · doi:10.1186/s12951-024-02297-8 · Cited by 74 · see citing works
“In general, compared with traditional treatment methods, PTT based on nanomaterials mediated by external laser stimulation has greater advantages [145–148].”
ResultLu, Y., Rivera‐Rodriguez, A., Tay, Z. W., Hensley, D. W., Fung, B. K., Colson, C., Saayujya, C., Huynh, Q., Kabuli, L., Fellows, B. D., et al. (2020) · International Journal of Hyperthermia · doi:10.1080/02656736.2020.1853252 · Cited by 71 · see citing works
“Though more dosage and temperature can be accessed by calculation, in vivo temperature feedback can provide the most accurate assessment of thermal therapy and dosage [22].”
InfluentialLak, A., Cassani, M., Binh, T., Winckelmans, N., Cabrera, D. M., Sadrollahi, E., Marras, S., Remmer, H., Fiorito, S., Cremades‐Jimeno, L., et al. (2018) · Nano Letters · doi:10.1021/acs.nanolett.8b02722 · Cited by 71 · see citing works
Recent developments of the reconstruction in magnetic particle imaging
Yin, L., Li, W., Du, Y., Wang, K., Liu, Z., Hui, H., & Tian, J. (2022) · Visual Computing for Industry Biomedicine and Art · doi:10.1186/s42492-022-00120-5 · Cited by 70 · see citing works
Tomographic Field Free Line Magnetic Particle Imaging With an Open-Sided Scanner Configuration
Top, C. B., & Güngör, A. (2020) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2020.3014197 · Cited by 70 · see citing works
“In vivo and phantom studies have demonstrated the potential use of MPI for a diverse range of clinical applications including: real time cardiac imaging [21]–[23]; instrument visualization for cardiovascular interventions [24]–[27]; catheter steering [28]; assessment of aneursym hydrodynamics [29]; stenosis quantifica…”
BackgroundThe Applications of Magnetic Particle Imaging: From Cell to Body
Han, X. H., Li, Y., Liu, W., Chen, X., Song, Z., Wang, X., Deng, Y., Tang, X., & Jiang, Z. (2020) · Diagnostics · doi:10.3390/diagnostics10100800 · Cited by 68 · see citing works
Systemically Delivered Magnetic Hyperthermia for Prostate Cancer Treatment
Albarqi, H. A., Demessie, A. A., Sabei, F. Y., Moses, A. S., Hansen, M. N., Dhagat, P., Taratula, O. R., & Taratula, O. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12111020 · Cited by 68 · see citing works
Magnetite Nanoparticle Co-precipitation Synthesis, Characterization, and Applications: Mini Review
Al‐Madhagi, H., Yazbik, V., Abdelwahed, W., & Alchab, L. (2023) · BioNanoScience · doi:10.1007/s12668-023-01113-1 · Cited by 67 · see citing works
Optimization of Drive Parameters for Resolution, Sensitivity and Safety in Magnetic Particle Imaging
Tay, Z. W., Hensley, D. W., Chandrasekharan, P., Zheng, B., & Conolly, S. (2019) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2019.2957041 · Cited by 66 · see citing works
“Other important applications include stem cell tracking [5], cancer imaging [10], acute gut bleed detection [11],lung imaging [12], [13], stroke and brain imaging [14], [15], and imageguided hyperthermia-therapy [16], [17].”
BackgroundJiang, Z., Han, X., Du, Y., Li, Y., Li, Y., Li, J., Tian, J., & Wu, A. (2021) · Nano Letters · doi:10.1021/acs.nanolett.0c04455 · Cited by 66 · see citing works
Magnetism-mediated targeting hyperthermia-immunotherapy in “cold” tumor with CSF1R inhibitor
Fang, Y., He, Y., Wu, C., Zhang, M., Gu, Z., Zhang, J., Liu, E., Xu, Q., Asrorov, A. M., & Huang, Y. (2021) · Theranostics · doi:10.7150/thno.57511 · Cited by 66 · see citing works
“Unlike photothermal therapy that is typically applied in superficial tumors owing to the limited penetrating ability of beams in human tissues, magnetic hyperthermia (MHT) can work remotely in the deep parts of the body [7, 8].”
BackgroundWychowaniec, J. K., & Brougham, D. F. (2022) · Advanced Science · doi:10.1002/advs.202202278 · Cited by 66 · see citing works
Chandrasekharan, P., Tay, Z. W., Zhou, X. Y., Yu, E. Y., Orendorff, R. D., Hensley, D. W., Huynh, Q., Fung, B. K., Colson, C., Goodwill, P. W., et al. (2018) · British Journal of Radiology · doi:10.1259/bjr.20180326 · Cited by 67 · see citing works
Multifunctional theranostic nanoparticles for biomedical cancer treatments - A comprehensive review
Kandasamy, G., & Maity, D. (2021) · Materials Science and Engineering C · doi:10.1016/j.msec.2021.112199 · Cited by 65 · see citing works
Egea-Benavente, D., Ovejero, J. G., Morales, M. P., & Barber, D. F. (2021) · Cancers · doi:10.3390/cancers13184583 · Cited by 63 · see citing works
“All this makes this technique an excellent non-invasive 3D tomographic imaging method to be combined with MHT for a real-time therapy image guided [15,87].”
MethodOrigin and Shell-Driven Optimization of the Heating Power in Core/Shell Bimagnetic Nanoparticles
Lavorato, G. C., Das, R., Xing, Y. T., Robles, J., Litterst, F. J., Baggio‐Saitovitch, E., Phan, M., & Srikanth, H. (2020) · ACS Applied Nano Materials · doi:10.1021/acsanm.9b02449 · Cited by 62 · see citing works
DEQ-MPI: A Deep Equilibrium Reconstruction With Learned Consistency for Magnetic Particle Imaging
Güngör, A., Askin, B., Soydan, D. A., Top, C. B., Sarıtaş, E. Ü., & Çukur, T. (2023) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2023.3300704 · Cited by 61 · see citing works
“M AGNETIC particle imaging (MPI) is a powerful modality with high clinical prospect in applications such as angiography, cell tracking, cancer imaging, and neurovascular imaging [1], [2], [3], [4], [5], [6], [7], [8], [9].”
Background
- Authors
- Tay, Z. W., Chandrasekharan, P., Chiu-Lam, A., Hensley, D. W., Dhavalikar, R., Zhou, X. Y., Yu, E. Y., Goodwill, P. W., Zheng, B., Rinaldi, C., & Conolly, S. M.
- Affiliations
- University of California, Berkeley (US)
- Department of Chemical Engineering, University of Florida, Gainesville, Florida 32611, United States
- Magnetic Insight, Inc., Alameda, California 94501, United States
- University of Florida (US)
- Corresponding author
- Tay, Zhi Wei
- ORCID
- Venue
- ACS Nano
- Publisher
- American Chemical Society (ACS)
- Published
- 2018-03-23
- Volume
- 12
- Issue
- 4
- Pages
- 3699-3713
- ISSN
- 1936-0851 (ISSN-L)
- 1936-086X
- PMC
- PMC6007035
- OpenAlex
- W2793607796
- Cited by
- 459
- References
- 80
- Citations by year
- 2026: 44 · 2025: 65 · 2024: 48 · 2023: 59 · 2022: 59 · 2021: 65 · 2020: 58 · 2019: 42 · 2018: 18 · 2017: 1
- FWCI
- 18.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- ACS Nano (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of California Berkeley (26IP-0049)
- Agency for Science, Technology and Research
- National Institute of Biomedical Imaging and Bioengineering (1R21 EB018453-01A1, 5R43 EB020463-02, R01 EB024578, R01 EB019458)
- Thomas and Stacey Siebel Foundation
- National Institute on Drug Abuse (1R43 DA041814-01A1)
- University of Florida Health Cancer Center
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Characterization and Applications of Magnetic Nanoparticles
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Physical Sciences › Engineering › Biomedical Engineering › Photoacoustic and Ultrasonic Imaging
- Keywords
- magnetic particle imaging, magnetic hyperthermia, superparamagnetic iron oxide nanoparticles, theranostics, liver, tumor targeting, cancer therapy
- MeSH terms
- Animals, Antineoplastic Agents, Female, Heating, Humans, Hyperthermia, Induced, Mammary Neoplasms, Experimental, Mice, Nude, Apoptosis, Cell Line, Tumor, Mice, Magnetite Nanoparticles, Magnetic Fields, Optical Imaging
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