OJMI  Vol.5 No.2 , June 2015
Usefulness of Magnetic Particle Imaging for Predicting the Therapeutic Effect of Magnetic Hyperthermia
Abstract: Purpose: To investigate the usefulness of magnetic particle imaging (MPI) for predicting the therapeutic effect of magnetic hyperthermia (MH). Materials and Methods: First, we performed phantom experiments to investigate the relationship between the MPI value and the temperature rise of magnetic nanoparticles (MNPs) under an alternating magnetic field (AMF). The MPI value was defined as the pixel value of the transverse image reconstructed from the third-harmonic signals. Samples filled with various iron concentrations of MNPs (Resovist®) were prepared and were imaged using our MPI scanner. These samples were also heated using the AMF, and the specific loss power (SLP) and volume-specific loss power (vSLP) were calculated from the initial slope of the time-dependent temperature rise. Second, we performed animal experiments using tumor-bearing mice, which were divided into untreated (n = 10) and treated groups (n = 20). The tumors in the treated group were injected with Resovist® at an iron concentration of 250 mM (n = 10) or 500 mM (n = 10), and received MH for 20 min, during which the temperatures in the tumor and rectum were measured. The relative tumor volume growth (RTVG) was calculated from (V15 - V0)/V0, where V0 and V15 represented the tumor volume on day 0 and day 15 after MH, respectively. Results: In phantom experiments, the MPI value had significant correlations with the iron concentration of MNPs (r = 0.997), temperature rise (r = 0.981), and vSLP (r = 0.961). In animal experiments, the MPI value had significant correlations with the temperature rise in the tumor (r = 0.731) and RTVG (r = ﹣0.687). Conclusion: Our preliminary results suggest that MPI is useful for predicting the therapeutic effect of MH.
Cite this paper: Murase, K. , Aoki, M. , Banura, N. , Nishimoto, K. , Mimura, A. , Kuboyabu, T. and Yabata, I. (2015) Usefulness of Magnetic Particle Imaging for Predicting the Therapeutic Effect of Magnetic Hyperthermia. Open Journal of Medical Imaging, 5, 85-99. doi: 10.4236/ojmi.2015.52013.

[1]   Abe, M., Hiraoka, M., Takahashi, M., Egawa, S., Matsuda, C., Onoyama, Y., Morita, K., Kakehi, M. and Sugahara, T. (1986) Multi-Institutional Studies on Hyperthermia Using an 8-MHz Radiofrequency Capacitive Heating Device (Thermotron RF-8) in Combination with Radiation for Cancer Therapy. Cancer, 58, 1589-1595.<1589::AID-CNCR2820580802>3.0.CO;2-B

[2]   Oura, S., Tamaki, T., Hirai, I., Yoshimasu, T., Ohta, F., Nakamura, R. and Okamura, Y. (2007) Radiofrequency Ablation Therapy in Patients with Breast Cancers Two Centimeters or Less in Size. Breast Cancer, 14, 48-54.

[3]   Seip, R. and Ebbini, E.S. (1995) Noninvasive Estimation of Tissue Temperature Response to Heating Fields Using Diagnostic Ultrasound. IEEE Transactions on Biomedical Engineering, 42, 828-839.

[4]   Gilchrist, R.K., Medal, R., Shorey, W.D., Hanselman, R.C., Parrott, J.C. and Taylor, C.B. (1957) Selective Inductive Heating of Lymph Nodes. Annals of Surgery, 146, 596-606.

[5]   Jordan, A., Scholz, R., Maier-Hauff, K., Johannsen, M., Wust, P., Nodobny, J., Schirra, H., Schmidt, H., Deger, S. and Leoning, S. (2001) Presentation of a New Magnetic Field Therapy System for the Treatment of Human Solid Tumors with Magnetic Fluid Hyperthermia. Journal of Magnetism and Magnetic Materials, 225, 118-126.

[6]   Kozissnik, B., Bohorquez, A.C., Dobson, J. and Rinaldi, C. (2013) Magnetic Fluid Hyperthermia: Advances, Challenges, and Opportunity. International Journal of Hyperthermia, 29, 706-714.

[7]   Hilger, I. (2013) In Vivo Applications of Magnetic Nanoparticle Hyperthermia. International Journal of Hyperthermia, 29, 828-834.

[8]   Rosensweig, R.E. (2002) Heating Magnetic Fluid with Alternating Magnetic Field. Journal of Magnetism and Magnetic Materials, 252, 370-374.

[9]   Neuberger, T., Schopf, B., Hofmann, H., Hofmann, M. and von Rechenberg, B. (2005) Superparamagnetic Nanoparticles for Biomedical Applications: Possibilities and Limitations of a New Drug Delivery System. Journal of Magnetism and Magnetic Materials, 293, 483-496.

[10]   Grüttner, C., Müller, K., Teller, J. and Westphal, F. (2013) Synthesis and Functionalization of Magnetic Nanoparticles for Hyperthermia Applications. International Journal of Hyperthermia, 29, 777-789.

[11]   Ito, A., Shinkai, M., Honda, H. and Kobayashi, T. (2005) Medical Applications of Functionalized Magnetic Nanoparticles. Journal of Bioscience and Bioengineering, 100, 1-11.

[12]   Balivada, S., Rachakatla, R.S., Wang, H., Samarakoon, T.N., Dani, R.K., Pyle, M., Kroh, F.O., Walker, B., Leaym, X., Koper, O.B., Tamura, M., Chikan, V., Bossmann, S.H. and Troyer, D.L. (2010) A/C Magnetic Hyperthermia of Melanoma Mediated by Iron(0)/iron Oxide Core/shell Magnetic Nanoparticles: A Mouse Study. BMC Cancer, 10, 119-127.

[13]   Johannsen, M., Gneueckow, U., Thiesen, B., Taymoorian, K., Cho, C.H., Waldofner, N., Scholz, R., Jordan, A., Loening, S.A. and Wust, P. (2007) Thermotherapy of Prostate Cancer Using Magnetic Nanoparticles: Feasibility, Imaging, and Three-Dimensional Temperature Distribution. European Urology, 52, 1653-1662.

[14]   LeBrun, A., Manuchehrabadi, N., Attaluri, A., Wang, F., Ma, R. and Zhu, L. (2013) MicroCT Image-Generated Tumour Geometry and SAR Distribution for Tumour Temperature Elevation Simulations in Magnetic Nanoparticle Hyperthermia. International Journal of Hyperthermia, 29, 730-738.

[15]   Gleich, B. and Weizenecker, J. (2005) Tomographic Imaging Using the Nonlinear Response of Magnetic Particles. Nature, 435, 1214-1217.

[16]   Goodwill, P.W., Konkle, J.J., Zheng, B., Saritas, E.U. and Conolly, S.M. (2012) Projection X-Space Magnetic Particle Imaging. IEEE Transactions on Medical Imaging, 31, 1076-1085.

[17]   Murase, K., Hiratsuka, S., Song, R. and Takeuchi, Y. (2014) Development of a System for Magnetic Particle Imaging using Neodymium Magnets and Gradiometer. Japanese Journal of Applied Physics, 53, Article ID: 067001.

[18]   Murase, K., Song, R. and Hiratsuka, S. (2014) Magnetic Particle Imaging of Blood Coagulation. Applied Physics Letters, 104, Article ID: 252409.

[19]   Nishimoto, K., Mimura, A., Aoki, M., Banura, N. and Murase, K. (2015) Application of Magnetic Particle Imaging to Pulmonary Imaging Using Nebulized Magnetic Nanoparticles. Open Journal of Medical Imaging, 5, 49-55.

[20]   Murase, K., Mimura, A., Banura, N., Nishimoto, K. and Takata, H. (2015) Visualization of Magnetic Nanofibers Using Magnetic Particle Imaging. Open Journal of Medical Imaging, 5, 56-65.

[21]   Murase, K., Banura, N., Mimura, A. and Nishimoto, K. (2015) Simple and Practical Method for Correcting the Inhomogeneous Sensitivity of a Receiving Coil in Magnetic Particle Imaging. Japanese Journal of Applied Physics, 54, Article ID: 038001.

[22]   Murase, K., Oonoki, J., Takata, H., Song, R., Angraini, A., Ausanai, P. and Matsushita, T. (2011) Simulation and Experimental Studies on Magnetic Hyperthermia with Use of Superparamagnetic Iron Oxide Nanoparticles. Radiological Physics and Technology, 4, 194-202.

[23]   Biederer, S., Knopp, T., Sattel, T.F., Ludtke-Buzug, K., Gleich, B., Weizenecker, J., Borgert, J. and Buzug, T.M. (2009) Magnetization Response Spectroscopy of Superparamagnetic Nanoparticles for Magnetic Particle Imaging. Journal of Physics D: Applied Physics, 42, Article ID: 205007.

[24]   Markov, D.E., Boeve, H., Gleich, B., Borgert, J., Antonelli, A., Sfara, C. and Magnani, M. (2010) Human Erythrocytes as Nanoparticle Carriers for Magnetic Particle Imaging. Physics in Medicine and Biology, 55, 6461-6473.

[25]   Kallumadil, M., Tada, M., Nakagawa, T., Abe, M., Southern, P. and Pankhurst, Q.A. (2009) Suitability of Commercial Colloids for Magnetic Hyperthermia. Journal of Magnetism and Magnetic Materials, 321, 1509-1513.

[26]   Box, G.E.P. and Lucas, H.L. (1959) Design of Experiments in Nonlinear Situations. Biometrika, 46, 77-90.

[27]   Rodrigues, H.F., Mell, F.M., Branquinho, L.C., Zufelato, N., Silveira-Lacerda, E.P. and Bakuzis, A.F. (2013) Real- Time Infrared Thermography Detection of Magnetic Nanoparticle Hyperthermia in a Murine Model under a Non- Uniform Field Configuration. International Journal of Hyperthermia, 29, 752-767.

[28]   Andreu, I. and Natividad, E. (2013) Accuracy of Available Methods for Quantifying the Heat Power Generation of Nanoparticles for Magnetic Hyperthermia. International Journal of Hyperthermia, 29, 739-751.

[29]   Shinkai, M., Yanase, M., Honda, H., Wakabayashi, T., Yoshida, J. and Kobayashi, T. (1996) Intracellular Hyperthermia for Cancer Using Magnetite Cationic Liposomes: In Vitro Study. Japanese Journal of Cancer Research, 87, 1179- 1183.

[30]   Le, B., Shinkai, M., Kitade, T., Honda, H., Yoshida, J., Wakabayashi, T. and Kobayashi, T. (2001) Preparation of Tumor-Specific Magnetoliposomes and Their Application for Hyperthermia. Journal of Chemical Engineering of Japan, 34, 66-72.

[31]   Shinkai, M., Le, B., Honda, H., Yoshikawa, K., Shimizu, K., Saga, S., Wakabayashi, T., Yoshida, J. and Kobayashi, T. (2001) Targeting Hyperthermia for Renal Cell Carcinoma Using Human MN Antigen-specific Magnetoliposomes. Japanese Journal of Cancer Research, 92, 1138-1145.

[32]   Suzuki, M., Shinkai, M., Kamihira, M. and Kobayashi, T. (1995) Preparation and Characteristics of Magnetite-La- belled Antibody with the Use of Poly (Ethylene Glycol) Derivatives. Biotechnology and Applied Biochemistry, 21, 335-345.

[33]   Moroz, P., Jones, S.K., Winter, J. and Gray, B.N. (2001) Targeting Liver Tumors with Hyperthermia: Ferromagnetic Embolization in a Rabbit Liver Tumor Model. Journal of Surgical Oncology, 78, 22-29.

[34]   Jordan, A., Scholz, R., Wust, P., Fahling, H., Krause, J., Wlodarczyk, W., Sander, B., Vogl, T. and Felix, R. (1997) Effects of Magnetic Fluid Hyperthermia (MFH) on C3H Mammary Carcinoma in Vivo. International Journal of Hyperthermia, 13, 587-605.

[35]   Deng, Z.S. and Liu, J. (2002) Analytical Study on Bioheat Transfer Problems with Spatial or Transient Heating on Skin Surface or inside Biological Bodies. Journal of Biomechanical Engineering, 124, 638-649.

[36]   Pennes, H.H. (1998) Analysis of Tissue and Arterial Blood Temperatures in the Resting Human Forearm. Journal of Applied Physiology, 85, 5-34.

[37]   Shih, T.C., Kou, H.S., Liauh, C.T. and Lin, W.L. (2005) The Impact of Thermal Wave Characteristics on Thermal Dose Distribution during Thermal Therapy: A Numerical Study. Medical Physics, 32, 3029-3036.

[38]   Skeete, Z., Cheng, H., Crew, E., Lin, L., Zhao, W., Joseph, P., Shan, S., Cronk, H., Luo, J., Li, Y., Zhang, Q. and Zhong, C.J. (2014) Design of Functional Nanoparticles and Assemblies for Theranostic Applications. ACS Applied Materials and Interfaces, 6, 21752-21768.

[39]   Murase, K., Takata, H., Takeuchi, Y. and Saito, S. (2013) Control of the Temperature Rise in Magnetic Hyperthermia with Use of a Static Magnetic Field. Physica Medica, 29, 624-630.

[40]   Atsumi, T., Jeyadevan, B., Sato, Y. and Tohji, K. (2007) Heating Efficiency of Magnetite Particles Exposed to AC Magnetic Field. Journal of Magnetism and Magnetic Materials, 310, 2841-2843.

[41]   Hergt, R., Hiergeist, R., Hilger, I., Kaiser, W.A., Lapatnikov, Y., Margel, S. and Richter, U. (2004) Maghemite Nanoparticles with Very High AC-Losses for Application in RF-Magnetic Hyperthermia. Journal of Magnetism and Magnetic Materials, 270, 345-357.

[42]   Brezovich, I.A. and Meredith, R.F. (1989) Practical Aspects of Ferromagnetic Thermoseed Hyperthermia. Radiologic Clinics of North America, 27, 589-602.

[43]   Hergt, R. and Dutz, S. (2007) Magnetic Particle Hyperthermia—Biophysical Limitations of a Visionary Tumour Therapy. Journal of Magnetism and Magnetic Materials, 311, 187-192.

[44]   Robson, M.D., Gatehouse, P.D., Bydder, M. and Bydder, G.M. (2003) Magnetic Resonance: An Introduction to Ultrashort TE (UTE) Imaging. Journal of Computer Assisted Tomography, 27, 825-846.

[45]   Idiyatullin, D., Corum, C., Park, J.Y. and Garwood, M. (2006) Fast and Quiet MRI Using a Swept Radiofrequency. Journal of Magnetic Resonance, 181, 342-349.

[46]   Zhang, J., Chamberlain, R., Etheridge, M., Idiyatullin, D., Corum, C., Bischof, J. and Garwood, M. (2014) Quantifying Iron-Oxide Nanoparticles at High Concentration Based on Longitudinal Relaxation Using a Three-Dimensional SWIFT Look-Locker Sequence. Magnetic Resonance in Medicine, 71, 1982-1988.

[47]   Hoopes, P.J., Petryk, A.A., Tate, J.A., Savellano, M.S., Strawbridge, R.R., Giustini, A.J., Stan, R.V., Gimi, B. and Garwood, M. (2013) Imaging and Modification of the Tumor Vascular Barrier for Improvement in Magnetic Nanoparticle Uptake and Hyperthermia Treatment Efficacy. Proceedings of SPIE Energy-Based Treatment of Tissue and Assessment VII, 8584, Article ID: 858403.