In vivo magnetic nanoparticle hyperthermia: a review on preclinical studies, low-field nano-heaters, noninvasive thermometry and computer simulations for treatment planning

References

• Moros E. Physics of thermal therapy fundamentals and clinical applications. Boca Raton (FL): CRC/Taylor & Francis; 2013.
   Google Scholar
• Jordan A, Wust P, Fahling H, et al. Inductive heating of ferrimagnetic particles and magnetic fluids: physical evaluation of their potential for hyperthermia. Int J Hyperthermia. 1993;9(1):51–68.
   PubMed Web of Science ®Google Scholar
• Rastinehad AR, Anastos H, Wajswol E, et al. Gold nanoshell-localized photothermal ablation of prostate tumors in a clinical pilot device study. Proc Natl Acad Sci USA. 2019;116(37):18590–18596.
   PubMed Web of Science ®Google Scholar
• Toraya-Brown S, Sheen MR, Zhang P, et al. Local hyperthermia treatment of tumors induces CD8(+) T cell-mediated resistance against distal and secondary tumors. Nanomedicine. 2014;10(6):1273–1285.
   PubMed Web of Science ®Google Scholar
• Bertotti G. Hysteresis in magnetism: for physicists, materials scientists, and engineers. San Diego (CA): Academic Press; 1998.
   Google Scholar
• Rosensweig RE. Heating magnetic fluid with alternating magnetic field. J Magn Magn Mater. 2002;252:370–374.
   Web of Science ®Google Scholar
• Verde EL, Landi GT, Gomes JA, et al. Magnetic hyperthermia investigation of cobalt ferrite nanoparticles: comparison between experiment, linear response theory, and dynamic hysteresis simulations. J Appl Phys. 2012;111:123902.
   Web of Science ®Google Scholar
• Carrey J, Mehdaoui B, Respaud M. Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: application to magnetic hyperthermia optimization. J Appl Phys. 2011;109(8):083921.
   Web of Science ®Google Scholar
• Verde EL, Landi GT, Carrião MS, et al. Field dependent transition to the non-linear regime in magnetic hyperthermia experiments: comparison between maghemite, copper, zinc, nickel and cobalt ferrite nanoparticles of similar sizes. AIP Adv. 2012;2:032120.
   Web of Science ®Google Scholar
• Jordan A, Scholz R, Wust P, et al. Effects of magnetic fluid hyperthermia (MFH) on C3H mammary carcinoma in vivo. Int J Hyperth. 1997;13(6):587–605.
   PubMed Web of Science ®Google Scholar
• Hilger I, Andrä W, Hergt R, et al. Electromagnetic heating of breast tumors in interventional radiology: in vitro and in vivo studies in human cadavers and mice. Radiology. 2001;218(2):570–575.
   PubMed Web of Science ®Google Scholar
• Johannsen M, Thiesen B, Jordan A, et al. Magnetic fluid hyperthermia (MFH)reduces prostate cancer growth in the orthotopic Dunning R3327 rat model. Prostate. 2005;64(3):283–292.
   PubMed Web of Science ®Google Scholar
• Ito A, Honda H, Kobayashi T. Cancer immunotherapy based on intracellular hyperthermia using magnetite nanoparticles: a novel concept of “heat-controlled necrosis” with heat shock protein expression. Cancer Immunol Immunother. 2006;55(3):320–328.
   PubMed Web of Science ®Google Scholar
• Dennis CL, Jackson AJ, Borchers JA, et al. Nearly complete regression of tumors via collective behavior of magnetic nanoparticles in hyperthermia. Nanotechnology. 2009;20(39):395103.
   PubMed Web of Science ®Google Scholar
• Hou C-H, Hou S-M, Hsueh Y-S, et al. The in vivo performance of biomagnetic hydroxyapatite nanoparticles in cancer hyperthermia therapy. Biomaterials. 2009;30(23–24):3956–3960.
   PubMed Web of Science ®Google Scholar
• Lee J-H, Jang J, Choi J, et al. Exchange-coupled magnetic nanoparticles for efficient heat induction. Nat Nanotechnol. 2011;6(7):418–422.
   PubMed Web of Science ®Google Scholar
• Candido N, Calmon M, Taboga S, et al. High efficacy in hyperthermia-associated with polyphosphate magnetic nanoparticles for oral cancer treatment. J Nanomed Nanotechnol. 2014;5:206.
   Google Scholar
• Kossatz S, Grandke J, Couleaud P, et al. Efficient treatment of breast cancer xenografts with multifunctionalized iron oxide nanoparticles combining magnetic hyperthermia and anti-cancer drug delivery. Breast Cancer Res. 2015;17:66.
   PubMed Web of Science ®Google Scholar
• Liu XL, Yang Y, Ng CT, Zhao LY, et al. Magnetic vortex nanorings: a new class of hyperthermia agent for highly efficient in vivo regression of tumors. Adv Mater Weinheim. 2015;27(11):1939–1944.
   PubMed Web of Science ®Google Scholar
• Alphandéry E, Idbaih A, Adam C, et al. Chains of magnetosomes with controlled endotoxin release and partial tumor occupation induce full destruction of intracranial U87-Luc glioma in mice under the application of an alternating magnetic field. J Control Release. 2017;262:259–272.
   PubMed Web of Science ®Google Scholar
• Jang J, Lee J, Seon J, et al. Giant magnetic heat induction of magnesium-doped γ-Fe2O3 superparamagnetic nanoparticles for completely killing tumors. Adv Mater. 2018;30(6):1704362.
   Web of Science ®Google Scholar
• Ma X, Wang Y, Liu X-L, et al. Fe3O4–Pd Janus nanoparticles with amplified dual-mode hyperthermia and enhanced ROS generation for breast cancer treatment. Nanoscale Horiz. 2019;4(6):1450–1459.
   Web of Science ®Google Scholar
• Mai BT, Balakrishnan PB, Barthel MJ, et al. Thermoresponsive iron oxide nanocubes for an effective clinical translation of magnetic hyperthermia and heat-mediated chemotherapy. ACS Appl Mater Interfaces. 2019;11(6):5727–5739.
   PubMed Web of Science ®Google Scholar
• Atkinson WJ, Brezovich IA, Chakraborty DP. Usable frequencies in hyperthermia with thermal seeds. IEEE Trans Biomed Eng. 1984;31(1):70–75.
   PubMed Web of Science ®Google Scholar
• Dutz S, Hergt R. Magnetic nanoparticle heating and heat transfer on a microscale: Basic principles, realities and physical limitations of hyperthermia for tumour therapy. Int J Hyperthermia. 2013;29(8):790–800.
   PubMed Web of Science ®Google Scholar
• Dutz S, Hergt R. Magnetic particle hyperthermia-a promising tumour therapy? Nanotechnology. 2014;25(45):452001.
   PubMed Web of Science ®Google Scholar
• Wust P, Hildebrandt B, Sreenivasa G, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol. 2002;3(8):487–497.
   PubMed Web of Science ®Google Scholar
• van den Tempel N, Horsman MR, Kanaar R. Improving efficacy of hyperthermia in oncology by exploiting biological mechanisms. Int J Hyperthermia. 2016;32(4):446–454.
   PubMed Web of Science ®Google Scholar
• Bull JMC. A review of immune therapy in cancer and a question: can thermal therapy increase tumor response? Int J Hyperthermia. 2018;34(6):840–852.
   PubMed Web of Science ®Google Scholar
• Sweeney EE, Cano-Mejia J, Fernandes R. Photothermal therapy generates a thermal window of immunogenic cell death in neuroblastoma. Small. 2018;14(20):e1800678.
   PubMed Web of Science ®Google Scholar
• Hirsch LR, Stafford RJ, Bankson JA, et al. Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance. Proc Natl Acad Sci USA. 2003;100(23):13549–13554.
   PubMed Web of Science ®Google Scholar
• Mehdaoui B, Carrey J, Stadler M, et al. Influence of a transverse static magnetic field on the magnetic hyperthermia properties and high-frequency hysteresis loops of ferromagnetic FeCo nanoparticles. Appl Phys Lett. 2012;100(5):052403.
   Web of Science ®Google Scholar
• MagForce USA, Inc. MagForce announces enrollment of first patient in its pivotal, three-stage, single-arm study of focal ablation of prostate cancer with nanotherm therapy. n.d. [cited 2020 April 10]. https://magforce.com.
   Google Scholar
• Hilger I. In vivo applications of magnetic nanoparticle hyperthermia. Int J Hyperthermia. 2013;29(8):828–834.
   PubMed Web of Science ®Google Scholar
• Vorotnikova E, Ivkov R, Foreman A, et al. The magnitude and time-dependence of the apoptotic response of normal and malignant cells subjected to ionizing radiation versus hyperthermia. Int J Radiat Biol. 2006;82(8):549–559.
   PubMed Web of Science ®Google Scholar
• Duval KEA, Vernice NA, Wagner RJ, et al. Immunogenetic effects of low dose (CEM43 30) magnetic nanoparticle hyperthermia and radiation in melanoma cells. Int J Hyperthermia. 2019;36(sup1):37–46.
   PubMed Web of Science ®Google Scholar
• Petryk AA, Giustini AJ, Gottesman RE, et al. Magnetic nanoparticle hyperthermia enhancement of cisplatin chemotherapy cancer treatment. Int J Hyperthermia. 2013;29(8):845–851.
   PubMed Web of Science ®Google Scholar
• Johannsen M, Thiesen B, Wust P, et al. Magnetic nanoparticle hyperthermia for prostate cancer. Int J Hyperthermia. 2010;26(8):790–795.
   PubMed Web of Science ®Google Scholar
• Attaluri A, Kandala SK, Wabler M, et al. Magnetic nanoparticle hyperthermia enhances radiation therapy: a study in mouse models of human prostate cancer. Int J Hyperthermia. 2015;31(4):359–374.
   PubMed Web of Science ®Google Scholar
• Oei AL, Korangath P, Mulka K, et al. Enhancing the abscopal effect of radiation and immune checkpoint inhibitor therapies with magnetic nanoparticle hyperthermia in a model of metastatic breast cancer. Int J Hyperthermia. 2019;36(sup1):47–63.
   PubMed Web of Science ®Google Scholar
• Rieke V, Butts Pauly K. MR thermometry. J Magn Reson Imaging. 2008;27(2):376–390.
   PubMed Web of Science ®Google Scholar
• Carter DL, MacFall JR, Clegg ST, et al. Magnetic resonance thermometry during hyperthermia for human high-grade sarcoma. Int J Radiat Oncol Biol Phys. 1998;40(4):815–822.
   PubMed Web of Science ®Google Scholar
• Wiekhorst F, Trahms L. Use of magnetic nanoparticles in biomedical applications. In: Van de Voorde M, Fermon C, editors. Nanomagnetism: applications and perspectives. Weinheim (Germany): Wiley-VCH Verlag GmbH & Co. KGaA; 2017. p. 137–164.
   Google Scholar
• Stephen ZR, Kievit FM, Zhang M. Magnetite nanoparticles for medical MR imaging. Mater Today (Kidlington). 2011;14(7–8):330–338.(11)70163-8.
   PubMedGoogle Scholar
• Hilger I, Kaiser WA. Iron oxide-based nanostructures for MRI and magnetic hyperthermia. Nanomedicine (Lond). 2012;7(9):1443–1459.
   PubMed Web of Science ®Google Scholar
• Ferrari M. Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer. 2005;5(3):161–171.
   PubMed Web of Science ®Google Scholar
• Wickline SA, Neubauer AM, Winter PM, et al. Molecular imaging and therapy of atherosclerosis with targeted nanoparticles. J Magn Reson Imaging. 2007;25(4):667–680.
   PubMed Web of Science ®Google Scholar
• Harisinghani MG, Barentsz J, Hahn PF, et al. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med. 2003;348(25):2491–2499.
   PubMed Web of Science ®Google Scholar
• Roberts TPL, Chuang N, Roberts HC. Neuroimaging: do we really need new contrast agents for MRI? Eur J Radiol. 2000;34(3):166–178.
   PubMed Web of Science ®Google Scholar
• Paysen H, Loewa N, Weber K, et al. Imaging and quantification of magnetic nanoparticles: Comparison of magnetic resonance imaging and magnetic particle imaging. J Magn Magn Mater. 2019;475:382–388.
   Web of Science ®Google Scholar
• Gneveckow U, Jordan A, Scholz R, et al. Description and characterization of the novel hyperthermia- and thermoablation-system MFH 300F for clinical magnetic fluid hyperthermia . Med Phys. 2004;31(6):1444–1451.
   PubMed Web of Science ®Google Scholar
• Maier-Hauff K, Ulrich F, Nestler D, et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol. 2011;103(2):317–324.
   PubMed Web of Science ®Google Scholar
• Maier-Hauff K, Rothe R, Scholz R, et al. Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme. J Neurooncol. 2007;81(1):53–60.
   PubMed Web of Science ®Google Scholar
• Mahmoudi K, Bouras A, Bozec D, et al. Magnetic hyperthermia therapy for the treatment of glioblastoma: a review of the therapy’s history, efficacy and application in humans. Int J Hyperthermia. 2018;34(8):1316–1328.
   PubMed Web of Science ®Google Scholar
• LeBrun A, Manuchehrabadi N, Attaluri A, et al. MicroCT image-generated tumour geometry and SAR distribution for tumour temperature elevation simulations in magnetic nanoparticle hyperthermia. Int J Hyperthermia. 2013;29(8):730–738.
   PubMed Web of Science ®Google Scholar
• LeBrun A, Ma R, Zhu L. MicroCT image based simulation to design heating protocols in magnetic nanoparticle hyperthermia for cancer treatment. J Therm Biol. 2016;62(Pt B):129–137.
   PubMed Web of Science ®Google Scholar
• Attaluri A, Ma R, Qiu Y, et al. Nanoparticle distribution and temperature elevations in prostatic tumours in mice during magnetic nanoparticle hyperthermia. Int J Hyperthermia. 2011;27(5):491–502.
   PubMed Web of Science ®Google Scholar
• Attaluri A, Ma R, Zhu L. Using MicroCT imaging technique to quantify heat generation distribution induced by magnetic nanoparticles for cancer treatments. J Heat Transf. 2010;133:011003–011003.
   Web of Science ®Google Scholar
• Rhoon G. v. Is CEM43 still a relevant thermal dose parameter for hyperthermia treatment monitoring? Int J Hyperthermia. 2016;32:50–62.
   PubMed Web of Science ®Google Scholar
• Wilhelm S, Tavares AJ, Dai Q, et al. Analysis of nanoparticle delivery to tumours. Nat Rev Mater. 2016;1(5):16014.
   Web of Science ®Google Scholar
• LeBrun A, Joglekar T, Bieberich C, et al. Identification of infusion strategy for achieving repeatable nanoparticle distribution and quantification of thermal dosage using micro-CT Hounsfield unit in magnetic nanoparticle hyperthermia. Int J Hyperthermia. 2016;32(2):132–143.
   PubMed Web of Science ®Google Scholar
• Jordan A, Scholz R, Wust P, et al. Magnetic fluid hyperthermia (MFH): Cancer treatment with AC magnetic field induced excitation of biocompatible superparamagnetic nanoparticles. J Magn Magn Mater. 1999;201:413–419.
   Web of Science ®Google Scholar
• Rodrigues HF, Mello FM, Branquinho LC, Zufelato N, et al. Real-time infrared thermography detection of magnetic nanoparticle hyperthermia in a murine model under a non-uniform field configuration. Int J Hyperthermia. 2013;29(8):752–767.
   PubMed Web of Science ®Google Scholar
• Ma M, Chen H, Chen Y, et al. Au capped magnetic core/mesoporous silica shell nanoparticles for combined photothermo-/chemo-therapy and multimodal imaging. Biomaterials. 2012;33(3):989–998.
   PubMed Web of Science ®Google Scholar
• Di Corato R, Béalle G, Kolosnjaj-Tabi J, et al. Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes. ACS Nano. 2015;9(3):2904–2916.
   PubMed Web of Science ®Google Scholar
• Espinosa A, Di Corato R, Kolosnjaj-Tabi J, et al. Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment. ACS Nano. 2016;10(2):2436–2446.
   PubMed Web of Science ®Google Scholar
• Chanmugam A, Hatwar R, Herman C. Thermal analysis of cancerous breast model. Int Mech Eng Congress Expo. 2012;2012:134–143.
   PubMedGoogle Scholar
• Bhargava A, Chanmugam A, Herman C. Heat transfer model for deep tissue injury: a step towards an early thermographic diagnostic capability. Diagn Pathol. 2014;9:36.
   PubMed Web of Science ®Google Scholar
• Hatwar R, Herman C. Inverse method for quantitative characterisation of breast tumours from surface temperature data. Int J Hyperthermia. 2017;33(7):741–757.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Herman C. Optimization of skin cooling by computational modeling for early thermographic detection of breast cancer. Int J Heat Mass Transf. 2018;126:864–876.
   Web of Science ®Google Scholar
• Herman C. The role of dynamic infrared imaging in melanoma diagnosis. Expert Rev Dermatol. 2013;8(2):177–184.
   PubMedGoogle Scholar
• Kateb B, Yamamoto V, Yu C, et al. Infrared thermal imaging: a review of the literature and case report. NeuroImage. 2009;47:T154–T162.
   PubMed Web of Science ®Google Scholar
• Nishikawa K, Matsudaira H, Suzuki H, et al. Intraoperative thermal imaging in esophageal replacement: its use in the assessment of gastric tube viability. Surg Today. 2006;36(9):802–806.
   PubMed Web of Science ®Google Scholar
• Santos HDA, Ximendes EC, Iglesias-de la Cruz M del C, et al. In vivo early tumor detection and diagnosis by infrared luminescence transient nanothermometry. Adv Funct Mater. 2018;28(43):1803924.
   Web of Science ®Google Scholar
• Kolosnjaj-Tabi J, Di Corato R, Lartigue L, et al. Heat-generating iron oxide nanocubes: subtle “destructurators” of the tumoral microenvironment. ACS Nano. 2014;8(5):4268–4283.
   PubMed Web of Science ®Google Scholar
• Rodrigues HF, Capistrano G, Mello FM, et al. Precise determination of the heat delivery during in vivo magnetic nanoparticle hyperthermia with infrared thermography. Phys Med Biol. 2017;62(10):4062–4082.
   PubMed Web of Science ®Google Scholar
• Hadadian Y, Uliana JH, Oliveira Carneiro AA, et al. A novel theranostic platform: integration of magnetomotive and thermal ultrasound imaging with magnetic hyperthermia. IEEE Trans Biomed Eng. 2020. DOI: 10.1109/TBME.2020.2990873
   PubMed Web of Science ®Google Scholar
• Lewis MA, Staruch RM, Chopra R. Thermometry and ablation monitoring with ultrasound. Int J Hyperthermia. 2015;31(2):163–181.
   PubMed Web of Science ®Google Scholar
• Ortgies DH, Teran FJ, Rocha U, et al. Optomagnetic nanoplatforms for in situ controlled hyperthermia. Adv Funct Mater. 2018;28(11):1704434.
   Web of Science ®Google Scholar
• Tay ZW, Chandrasekharan P, Chiu-Lam A, et al. Magnetic particle imaging-guided heating in vivo using gradient fields for arbitrary localization of magnetic hyperthermia therapy. ACS Nano. 2018;12(4):3699–3713.
   PubMed Web of Science ®Google Scholar
• Weaver JB, Rauwerdink AM, Hansen EW. Magnetic nanoparticle temperature estimation. Med Phys. 2009;36(5):1822–1829.
   PubMed Web of Science ®Google Scholar
• Mahnken AH, Bruners P. CT thermometry: will it ever become ready for use? Int J Clin Pract. 2011;65:1–2.
   PubMed Web of Science ®Google Scholar
• Fani F, Schena E, Saccomandi P, et al. CT-based thermometry: an overview. Int J Hyperthermia. 2014;30(4):219–227.
   PubMed Web of Science ®Google Scholar
• Saccomandi P, Schena E, Silvestri S. Techniques for temperature monitoring during laser-induced thermotherapy: an overview. Int J Hyperthermia. 2013;29(7):609–619.
   PubMed Web of Science ®Google Scholar
• Oh J, Feldman MD, Kim J, et al. Detection of magnetic nanoparticles in tissue using magneto-motive ultrasound. Nanotechnology. 2006;17(16):4183–4190.
   PubMed Web of Science ®Google Scholar
• Dhavalikar R, Rinaldi C. Theoretical predictions for spatially-focused heating of magnetic nanoparticles guided by magnetic particle imaging field gradients. J Magn Magn Mater. 2016;419:267–273.
   PubMed Web of Science ®Google Scholar
• Wells J, Löwa N, Paysen H, et al. Probing particle-matrix interactions during magnetic particle spectroscopy. J Magn Magn Mater. 2019;475:421–428.
   Web of Science ®Google Scholar
• Fatima A, Kratkiewicz K, Manwar R, et al. Review of cost reduction methods in photoacoustic computed tomography. Photoacoustics. 2019;15:100112–100137.
   Web of Science ®Google Scholar
• Capistrano G, Rodrigues HF, Zufelato N, et al. Non-invasive intratumoral thermal dose determination during in vivo magnetic nanoparticle hyperthermia: combining surface temperature measurements and computer simulations. Manuscript submitted for publication. 2020.
   Google Scholar
• Dewhirst MW, Viglianti BL, Lora-Michiels M, et al. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int J Hyperthermia. 2003;19(3):267–294.
   PubMed Web of Science ®Google Scholar
• van Rhoon G, Pearce J, Corry P, et al. The house believes that measurement of thermal dose is essential for thermal therapy. 12th International Congress of Hyperthermic Oncology. New Orleans, LA: 2016.
   Google Scholar
• Sapareto SA, Hopwood LE, Dewey WC, et al. Effects of hyperthermia on survival and progression of Chinese hamster ovary cells. Cancer Res. 1978;38(2):393–400.
   PubMed Web of Science ®Google Scholar
• Perez CA, Sapareto SA. Thermal dose expression in clinical hyperthermia and correlation with tumor response/control. Cancer Res. 1984;44(10 Suppl):4818s–4825s.
   PubMed Web of Science ®Google Scholar
• Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol. 1984;10(6):787–800.(84)90379-1.
   PubMed Web of Science ®Google Scholar
• Pearce JA. Comparative analysis of mathematical models of cell death and thermal damage processes. Int J Hyperthermia. 2013;29(4):262–280.
   PubMed Web of Science ®Google Scholar
• Yarmolenko PS, Moon EJ, Landon C, et al. Thresholds for thermal damage to normal tissues: An update. Int J Hyperthermia. 2011;27(4):320–343.
   PubMed Web of Science ®Google Scholar
• Dewey WC. Arrhenius relationships from the molecule and cell to the clinic. Int J Hyperthermia. 2009;25(1):3–20.
   PubMed Web of Science ®Google Scholar
• Field SB, Morris CC. The relationship between heating time and temperature: its relevance to clinical hyperthermia. Radiother Oncol J Eur Soc Ther Radiol Oncol. 1983;1(2):179–186.
   PubMedGoogle Scholar
• Pearce JA. Relationship between Arrhenius models of thermal damage and the CEM 43 thermal dose. In: Ryan TP, editor. 2009. p. 718104.
   Google Scholar
• Moritz AR, Henriques FC. Studies of thermal injury: II. The relative importance of time and surface temperature in the causation of cutaneous burns. Am J Pathol. 1947;23(5):695–720.
   PubMed Web of Science ®Google Scholar
• Feng Y, Tinsley Oden J, Rylander MN. A two-state cell damage model under hyperthermic conditions: theory and in vitro experiments. J Biomech Eng. 2008;130(4):041016.
   PubMed Web of Science ®Google Scholar
• Pearce JA. Improving accuracy in Arrhenius models of cell death: adding a temperature-dependent time delay. J Biomech Eng. 2015;137(12):121006.
   PubMed Web of Science ®Google Scholar
• Gilchrist RK, Medal R, Shorey WD, et al. Selective inductive heating of lymph nodes. Ann Surg. 1957;146(4):596–606.
   PubMed Web of Science ®Google Scholar
• Ivkov R. Magnetic nanoparticle hyperthermia: a new frontier in biology and medicine? Int J Hyperthermia. 2013;29(8):703–705.
   PubMed Web of Science ®Google Scholar
• Danhier F. To exploit the tumor microenvironment: since the EPR effect fails in the clinic, what is the future of nanomedicine? J Control Release. 2016;244(Pt A):108–121.
   PubMed Web of Science ®Google Scholar
• Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Am Assoc Cancer Res. 1986;46:6387–6392.
   Google Scholar
• Maeda H, Tsukigawa K, Fang J. A retrospective 30 years after discovery of the enhanced permeability and retention effect of solid tumors: next-generation chemotherapeutics and photodynamic therapy-problems, solutions, and prospects. Microcirculation. 2016;23(3):173–182.
   PubMed Web of Science ®Google Scholar
• Petros RA, DeSimone JM. Strategies in the design of nanoparticles for therapeutic applications. Nat Rev Drug Discov. 2010;9(8):615–627.
   PubMed Web of Science ®Google Scholar
• Kozissnik B, Bohorquez AC, Dobson J, et al. Magnetic fluid hyperthermia: advances, challenges, and opportunity. Int J Hyperthermia. 2013;29(8):706–714.
   PubMed Web of Science ®Google Scholar
• Sindhwani S, Syed AM, Ngai J, et al. The entry of nanoparticles into solid tumours. Nat Mater. 2020;19(5):566–575.
   PubMed Web of Science ®Google Scholar
• Gratton SEA, Ropp PA, Pohlhaus PD, et al. The effect of particle design on cellular internalization pathways. Proc Natl Acad Sci USA. 2008;105(33):11613–11618.
   PubMed Web of Science ®Google Scholar
• Rabin Y. Is intracellular hyperthermia superior to extracellular hyperthermia in the thermal sense? Int J Hyperthermia. 2002;18(3):194–202.
   PubMed Web of Science ®Google Scholar
• Williams DF. On the mechanisms of biocompatibility. Biomaterials. 2008;29(20):2941–2953.
   PubMed Web of Science ®Google Scholar
• Williams DF. There is no such thing as a biocompatible material. Biomaterials. 2014;35(38):10009–10014.
   PubMed Web of Science ®Google Scholar
• Malvindi MA, De Matteis V, Galeone A, et al. Toxicity assessment of silica coated iron oxide nanoparticles and biocompatibility improvement by surface engineering. PLoS ONE. 2014;9(1):e85835.
   PubMed Web of Science ®Google Scholar
• Reddy LH, Arias JL, Nicolas J, et al. Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem Rev. 2012;112(11):5818–5878.
   PubMed Web of Science ®Google Scholar
• Huang D-M, Chung T-H, Hung Y, et al. Internalization of mesoporous silica nanoparticles induces transient but not sufficient osteogenic signals in human mesenchymal stem cells. Toxicol Appl Pharmacol. 2008;231(2):208–215.
   PubMed Web of Science ®Google Scholar
• Jain TK, Reddy MK, Morales MA, et al. Biodistribution, clearance, and biocompatibility of iron oxide magnetic nanoparticles in rats. Mol Pharm. 2008;5(2):316–327.
   PubMed Web of Science ®Google Scholar
• Weissleder R, Stark D, Engelstad B, et al. Superparamagnetic iron oxide: pharmacokinetics and toxicity. AJR Am J Roentgenol. 1989;152(1):167–173.
   PubMed Web of Science ®Google Scholar
• Bourrinet P, Bengele HH, Bonnemain B, et al. Preclinical safety and pharmacokinetic profile of ferumoxtran-10, an ultrasmall superparamagnetic iron oxide magnetic resonance contrast agent. Invest Radiol. 2006;41(3):313–324.
   PubMed Web of Science ®Google Scholar
• Weissleder R, Nahrendorf M, Pittet MJ. Imaging macrophages with nanoparticles. Nat Mater. 2014;13(2):125–138.
   PubMed Web of Science ®Google Scholar
• Kut C, Zhang Y, Hedayati M, et al. Preliminary study of injury from heating systemically delivered, nontargeted dextran-superparamagnetic iron oxide nanoparticles in mice. Nanomedicine (Lond). 2012;7(11):1697–1711.
   PubMed Web of Science ®Google Scholar
• Yu M, Zheng J. Clearance pathways and tumor targeting of imaging nanoparticles. ACS Nano. 2015;9(7):6655–6674.
   PubMed Web of Science ®Google Scholar
• Quini CC, Matos JF, Próspero AG, et al. Renal perfusion evaluation by alternating current biosusceptometry of magnetic nanoparticles. J Magn Magn Mater. 2015;380:2–6.
   Web of Science ®Google Scholar
• Sousa-Junior AA, Mendanha SA, Carrião MS, et al. Predictive model for delivery efficiency: erythrocyte membrane-camouflaged Magnetofluorescent Nanocarriers Study. Mol Pharm. 2020;17(3):837–851.
   PubMed Web of Science ®Google Scholar
• U.S. Food and Drug Administration - FDA. MRI (Magnetic Resonance Imaging). FDA 2019. [cited 2020 June 19]. https://www.fda.gov/radiation-emitting-products/medical-imaging/mri-magnetic-resonance-imaging
   Google Scholar
• International Commission on Non-Ionizing Radiation Protection (ICNIRP). Guidelines for limiting exposure to electromagnetic fields (100 kHz to 300 GHz). Health Phys. 2020;118:483–524.
   PubMed Web of Science ®Google Scholar
• Oleson JR. A review of magnetic induction methods for hyperthermia treatment of cancer. IEEE Trans Biomed Eng. 1984;31(1):91–97.
   PubMed Web of Science ®Google Scholar
• Cheshire WP. Thermoregulatory disorders and illness related to heat and cold stress. Auton Neurosci. 2016;196:91–104.
   PubMed Web of Science ®Google Scholar
• Young JH, Wang M-T, Brezovich IA. Frequency/depth-penetration considerations in hyperthermia by magnetically induced currents. Electron Lett. 1980;16(10):358.
   Web of Science ®Google Scholar
• van Rhoon GC, Samaras T, Yarmolenko PS, et al. CEM43 °C thermal dose thresholds: a potential guide for magnetic resonance radiofrequency exposure levels? Eur Radiol. 2013;23(8):2215–2227.
   PubMed Web of Science ®Google Scholar
• Andreuccetti D, Fossi R, Petrucci C. An Internet resource for the calculation of the dielectric properties of body tissues in the frequency range 10 Hz - 100 GHz. Based on data published by Gabriel C et al. in 1996. 1997. [cited 2017 March 7]. http://niremf.ifac.cnr.it/tissprop/
   Google Scholar
• Gabriel C, Gabriel S, Corthout E. The dielectric properties of biological tissues: I. Literature survey. Phys Med Biol. 1996;41(11):2231–2249.
   PubMed Web of Science ®Google Scholar
• Gabriel S, Lau RW, Gabriel C. The dielectric properties of biological tissues: II. Measurements in the frequency range 10 Hz to 20 GHz. Phys Med Biol. 1996;41(11):2251–2269.
   PubMed Web of Science ®Google Scholar
• Gabriel S, Lau RW, Gabriel C. The dielectric properties of biological tissues: III. Parametric models for the dielectric spectrum of tissues. Phys Med Biol. 1996;41(11):2271–2293.
   PubMed Web of Science ®Google Scholar
• Wust P, Gneveckow U, Johannsen M, et al. Magnetic nanoparticles for interstitial thermotherapy-feasibility, tolerance and achieved temperatures. Int J Hyperthermia. 2006;22(8):673–685.
   PubMed Web of Science ®Google Scholar
• Singh MP, Sethuraman SN, Ritchey J, et al. In-situ vaccination using focused ultrasound heating and anti-CD-40 agonistic antibody enhances T-cell mediated local and abscopal effects in murine melanoma. Int J Hyperthermia. 2019;36(sup1):64–73.
   PubMed Web of Science ®Google Scholar
• Wennerberg E, Lhuillier C, Vanpouille-Box C, et al. Barriers to radiation-induced in situ tumor vaccination. Front Immunol. 2017;8:211–229.
   PubMed Web of Science ®Google Scholar
• Ngwa W, Irabor OC, Schoenfeld JD, et al. Using immunotherapy to boost the abscopal effect. Nat Rev Cancer. 2018;18(5):313–322.
   PubMed Web of Science ®Google Scholar
• Daguenet E, Louati S, Wozny A-S, et al. Radiation-induced bystander and abscopal effects: important lessons from preclinical models. Br J Cancer. 2020. Doi:10.1038/s41416-020-0942-3
   PubMed Web of Science ®Google Scholar
• Toraya-Brown S, Fiering S. Local tumour hyperthermia as immunotherapy for metastatic cancer. Int J Hyperthermia. 2014;30(8):531–539.
   PubMed Web of Science ®Google Scholar
• Sheen MR, Fiering S. In situ vaccination: harvesting low hanging fruit on the cancer immunotherapy tree. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2019;11(1):e1524.
   PubMed Web of Science ®Google Scholar
• Fiering SN, Evans S. Introduction to thermal therapy and immunotherapy: at the crossroads of new discovery. Int J Hyperthermia. 2019;36(sup1):1–2.
   PubMed Web of Science ®Google Scholar
• Carrião MS, Bakuzis AF. Mean-field and linear regime approach to magnetic hyperthermia of core-shell nanoparticles: can tiny nanostructures fight cancer? Nanoscale. 2016;8(15):8363–8377.
   PubMed Web of Science ®Google Scholar
• Issels RD, Lindner LH, Verweij J, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: a randomised phase 3 multicentre study. Lancet Oncol. 2010;11(6):561–570.
   PubMed Web of Science ®Google Scholar
• Horsman MR, Overgaard J. The impact of hypoxia and its modification of the outcome of radiotherapy. J Radiat Res. 2016;57(S1):i90–i98.
   PubMed Web of Science ®Google Scholar
• Aquino VRR, Figueiredo LC, Coaquira JAH, et al. Magnetic interaction and anisotropy axes arrangement in nanoparticle aggregates can enhance or reduce the effective magnetic anisotropy. J Magn Magn Mater. 2020;498:166170.
   Web of Science ®Google Scholar
• Aquino VRR, Vinícius-Araújo M, Shrivastava N, et al. Role of the fraction of blocked nanoparticles on the hyperthermia efficiency of Mn-based ferrites at clinically relevant conditions. J Phys Chem C. 2019;123(45):27725–27734.
   Web of Science ®Google Scholar
• MagForce AG, Inc. Since 2011, MagForce AG holds the European CE certificate and thus official approval of NanoTherm® therapy for the treatment of brain tumors in Germany and all member states of the European Union. n.d. [cited 2020 April 10]. https://magforce.com
   Google Scholar
• Southern P, Pankhurst QA. Commentary on the clinical and preclinical dosage limits of interstitially administered magnetic fluids for therapeutic hyperthermia based on current practice and efficacy models. Int J Hyperthermia. 2018;34(6):671–686.
   PubMed Web of Science ®Google Scholar
• Freeman AC, Platt SR, Holmes S, et al. Convection-enhanced delivery of cetuximab conjugated iron-oxide nanoparticles for treatment of spontaneous canine intracranial gliomas. J Neurooncol. 2018;137(3):653–663.
   PubMed Web of Science ®Google Scholar
• Dennis CL, Jackson AJ, Borchers JA, et al. The influence of collective behavior on the magnetic and heating properties of iron oxide nanoparticles. J Appl Phys. 2008;103(7):07A319.
   Web of Science ®Google Scholar
• Lartigue L, Hugounenq P, Alloyeau D, et al. Cooperative organization in iron oxide multi-core nanoparticles potentiates their efficiency as heating mediators and MRI contrast agents. ACS Nano. 2012;6(12):10935–10949.
   PubMed Web of Science ®Google Scholar
• Hugounenq P, Levy M, Alloyeau D, et al. Iron oxide monocrystalline nanoflowers for highly efficient magnetic hyperthermia. J Phys Chem C. 2012;116(29):15702–15712.
   Web of Science ®Google Scholar
• Liu XL, Choo ESG, Ahmed AS, et al. Magnetic nanoparticle-loaded polymer nanospheres as magnetic hyperthermia agents. J Mater Chem B. 2014;2(1):120–128.
   PubMed Web of Science ®Google Scholar
• Dennis CL, Krycka KL, Borchers JA, et al. Internal magnetic structure of nanoparticles dominates time-dependent relaxation processes in a magnetic field. Adv Funct Mater. 2015;25(27):4300–4311.
   Web of Science ®Google Scholar
• Shubitidze F, Kekalo K, Stigliano R, et al. Magnetic nanoparticles with high specific absorption rate of electromagnetic energy at low field strength for hyperthermia therapy. J Appl Phys. 2015;117(9):094302.
   PubMed Web of Science ®Google Scholar
• Das R, Rinaldi-Montes N, Alonso J, et al. Boosted hyperthermia therapy by combined AC magnetic and photothermal exposures in Ag/Fe3O4 nanoflowers. ACS Appl Mater Interfaces. 2016;8(38):25162–25169.
   PubMed Web of Science ®Google Scholar
• Soleymani M, Edrissi M, Alizadeh AM. Tailoring La1-xSrxMnO3 (0.25 ≤x≤ 0.35) nanoparticles for self-regulating magnetic hyperthermia therapy: an in vivo study. J Mater Chem B. 2017;5(24):4705–4712.
   PubMed Web of Science ®Google Scholar
• Hemery G, Genevois C, Couillaud F, et al. Monocore vs. multicore magnetic iron oxide nanoparticles: uptake by glioblastoma cells and efficiency for magnetic hyperthermia. Mol Syst Des Eng. 2017;2(5):629–639.
   Web of Science ®Google Scholar
• Gavilán H, Sánchez EH, Brollo MEF, et al. Formation mechanism of maghemite nanoflowers synthesized by a polyol-mediated process. ACS Omega. 2017;2(10):7172–7184.
   PubMed Web of Science ®Google Scholar
• Phong PT, Nam PH, Manh DH, et al. Mn0.5Zn0.5Fe2O4 nanoparticles with high intrinsic loss power for hyperthermia therapy. J Magn Magn Mater. 2017;433:76–83.
   Web of Science ®Google Scholar
• Bender P, Fock J, Hansen MF, et al. Influence of clustering on the magnetic properties and hyperthermia performance of iron oxide nanoparticles. Nanotechnology. 2018;29(42):425705.
   PubMed Web of Science ®Google Scholar
• He S, Zhang H, Liu Y, et al. Maximizing specific loss power for magnetic hyperthermia by hard-soft mixed ferrites. Small. 2018;14(29):1800135.
   Web of Science ®Google Scholar
• Bender P, Honecker D, Fernández Barquín L. Supraferromagnetic correlations in clusters of magnetic nanoflowers. Appl Phys Lett. 2019;115(13):132406.
   Web of Science ®Google Scholar
• Curcio A, Silva AKA, Cabana S, et al. Iron oxide nanoflowers @ CuS hybrids for cancer tri-therapy: interplay of photothermal therapy, magnetic hyperthermia and photodynamic therapy. Theranostics. 2019;9(5):1288–1302.
   PubMed Web of Science ®Google Scholar
• Del Sol-Fernández S, Portilla-Tundidor Y, Gutiérrez L, et al. Flower-like Mn-doped magnetic nanoparticles functionalized with αvβ3-integrin-ligand to efficiently induce intracellular heat after alternating magnetic field exposition, triggering glioma cell death . ACS Appl Mater Interfaces. 2019;11(30):26648–26663.
   PubMed Web of Science ®Google Scholar
• Ognjanović M, Radović M, Mirković M, et al. 99mTc-, 90Y-, and 177Lu-labeled iron oxide nanoflowers designed for potential use in dual magnetic hyperthermia/radionuclide cancer therapy and diagnosis. ACS Appl Mater Interfaces. 2019;11(44):41109–41117.
   PubMed Web of Science ®Google Scholar
• Attaluri A, Seshadri M, Mirpour S, et al. Image-guided thermal therapy with a dual-contrast magnetic nanoparticle formulation: a feasibility study. Int J Hyperthermia. 2016;32(5):543–557.
   PubMed Web of Science ®Google Scholar
• Zadnik PL, Molina CA, Sarabia-Estrada R, et al. Characterization of intratumor magnetic nanoparticle distribution and heating in a rat model of metastatic spine disease. J Neurosurg Spine. 2014;20(6):740–750.
   PubMed Web of Science ®Google Scholar
• Branquinho LC, Carrião MS, Costa AS, et al. Effect of magnetic dipolar interactions on nanoparticle heating efficiency: implications for cancer hyperthermia. Sci Rep. 2013;3:2887.
   PubMed Web of Science ®Google Scholar
• Pavel M, Gradinariu G, Stancu A. Study of the optimum dose of ferromagnetic nanoparticles suitable for cancer therapy using MFH. IEEE Trans Magn. 2008;44(11):3205–3208.
   Web of Science ®Google Scholar
• Pavel M, Stancu A. Study of the optimum injection sites for a multiple metastases region in cancer therapy by using MFH. IEEE Trans Magn. 2009;45(10):4825–4828.
   Web of Science ®Google Scholar
• Pavel M, Stancu A. Ferromagnetic nanoparticles dose based on tumor size in magnetic fluid hyperthermia cancer therapy. IEEE Trans Magn. 2009;45(11):5251–5254.
   Web of Science ®Google Scholar
• Pearce JA, Petryk AA, Hoopes PJ. Numerical model study of in vivo magnetic nanoparticle tumor heating. IEEE Trans Biomed Eng. 2017;64(12):2813–2823.
   PubMed Web of Science ®Google Scholar
• Li J, Yao H, Lei Y, et al. Numerical simulation of magnetic fluid hyperthermia based on multiphysics coupling and recommendation on preferable treatment conditions. Curr Appl Phys. 2019;19(9):1031–1039.
   Web of Science ®Google Scholar
• Tang Y, Flesch RCC, Jin T. Numerical method to evaluate the survival rate of malignant cells considering the distribution of treatment temperature field for magnetic hyperthermia. J Magn Magn Mater. 2019;490:165458.
   Web of Science ®Google Scholar
• Pennes HH. Analysis of tissue and arterial blood temperatures in the resting human forearm. J Appl Physiol. 1948;1(2):93–122.
   PubMed Web of Science ®Google Scholar
• Wissler EH. Pennes’ 1948 paper revisited. J Appl Physiol. 1998;85(1):35–41.
   PubMed Web of Science ®Google Scholar
• Javidi M, Heydari M, Karimi A, et al. Evaluation of the effects of injection velocity and different gel concentrations on nanoparticles in hyperthermia therapy. J Biomed Phys Eng. 2014;4(4):151–162.
   PubMedGoogle Scholar
• Kandala SK, Liapi E, Whitcomb LL, et al. Temperature-controlled power modulation compensates for heterogeneous nanoparticle distributions: a computational optimization analysis for magnetic hyperthermia. Int J Hyperthermia. 2019;36(1):115–129.
   PubMed Web of Science ®Google Scholar
• Johannsen M, Gneveckow U, Thiesen B, et al. Thermotherapy of prostate cancer using magnetic nanoparticles: feasibility, imaging, and three-dimensional temperature distribution. Eur Urol. 2007;52(6):1653–1661.
   PubMed Web of Science ®Google Scholar
• Lang J, Erdmann B, Seebass M. Impact of nonlinear heat transfer on temperature control in regional hyperthermia. IEEE Trans Biomed Eng. 1999;46(9):1129–1138.
   PubMed Web of Science ®Google Scholar
• Solberg OV, Lindseth F, Torp H, et al. Freehand 3D ultrasound reconstruction algorithms-a review. Ultrasound Med Biol. 2007;33(7):991–1009.
   PubMed Web of Science ®Google Scholar
• Weissleder R, Pittet MJ. Imaging in the era of molecular oncology. Nature. 2008;452(7187):580–589.
   PubMed Web of Science ®Google Scholar
• Rocha U, Upendra Kumar K, Jacinto C, et al. Nd3+ doped LaF3 nanoparticles as self-monitored photo-thermal agents. Appl Phys Lett. 2014;104(5):053703.
   Web of Science ®Google Scholar
• Shah J, Park S, Aglyamov S, et al. Photoacoustic imaging and temperature measurement for photothermal cancer therapy. J Biomed Opt. 2008;13(3):034024.
   PubMed Web of Science ®Google Scholar
• Marques JP, Simonis FFJ, Webb AG. Low-field MRI: an MR physics perspective. J Magn Reson Imaging. 2019;49(6):1528–1542.
   PubMed Web of Science ®Google Scholar
• Gleich B, Weizenecker J. Tomographic imaging using the nonlinear response of magnetic particles. Nature. 2005;435(7046):1214–1217.
   PubMed Web of Science ®Google Scholar
• Goodwill PW, Saritas EU, Croft LR, et al. X-Space MPI: magnetic nanoparticles for safe medical imaging. Adv Mater. 2012;24(28):3870–3877.
   PubMed Web of Science ®Google Scholar
• Hensley D, Tay ZW, Dhavalikar R, et al. A theranostic platform for localized magnetic fluid hyperthermia and magnetic particle imaging. Proceedings of the SPIE 10066, Energy-based Treatment of Tissue and Assessment IX, 1006603; 2017.
   Google Scholar
• Bender P, Fock J, Frandsen C, et al. Relating magnetic properties and high hyperthermia performance of iron oxide nanoflowers. J Phys Chem C. 2018;122(5):3068–3077.
   Web of Science ®Google Scholar
• Graeser M, Thieben F, Szwargulski P, et al. Human-sized magnetic particle imaging for brain applications. Nat Commun. 2019;10(1):1936.
   PubMed Web of Science ®Google Scholar
• Foiret J, Ferrara KW. Spatial and temporal control of hyperthermia using real time ultrasonic thermal strain imaging with motion compensation, phantom study. PLoS One. 2015;10(8):e0134938.
   PubMed Web of Science ®Google Scholar