1(School of Life Science and Technology, Xinxiang Medical University, Xinxiang 453003, Henan, China) 2(Institute of Biomedical Engineering, Chinese Academy of Medical Sciences, Tianjin 300192, China)
Abstract：Magnetic hyperthermia is a new non-invasive tumor therapy following radiotherapy and chemotherapy, in which, magnetic nanoparticles were targeted delivered to the lesion sites under the applied magnetic fields and generated heat rapidly in the alternating magnetic fields. Magnetic hyperthermia made the protein denaturation, DNA damage or immune system activation in tumor microenvironment, which killed tumor cells safely and effectively in a short time. This paper reviewed the heat generation mechanisms of magnetic nanoparticles, the interactions of magnetic nanoparticles and cells in tumor therapy progress, and the synergistic effects between magnetic hyperthermia and other tumor therapies, such as chemotherapy, radiotherapy, photodynamic therapy, immune therapy. The biosafety of magnetic nanomaterials was also discussed from the aspects of cytotoxicity and clinical side effects.
[1] Gilchrist RK, Medal R, Shorey WD, et al. Selective inductive heating of lymph nodes [J]. Annals of Surgery, 1957, 146(4): 596-606. [2] Carrey J, Mehdaoui B, Respaud M. Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: Application to magnetic hyperthermia optimization [J]. Journal of Applied Physics, 2011, 109: 083921. [3] Hergt R, Dutz S, Zeisberger M. Validity limits of the Néel relaxation model of magnetic nanoparticles for hyperthermia [J]. Nanotechnology, 2010, 21(1): 015706. [4] 刘丹. 磁流体热疗的磁场分析和温度场分析[D]. 天津: 河北工业大学, 2015. [5] 许黄涛, 任伟, 潘永信. 纳米铁氧化物磁热疗相关机制研究进展[J]. 生物化学与生物物理进展, 2019, 46(4): 369-378. [6] 张俊武, 王红理, 黄丽清. 铁磁材料交流磁化曲线及磁滞回线的观测[J]. 物理实验, 2017, 37(8): 17-21. [7] Dutz S, Hergt R. Magnetic nanoparticle heating and heat transfer on a microscale: Basic principles, realities and physical limitations of hyperthermia for tumour therapy [J]. International Journal of Hyperthermia, 2013, 29(8): 790-800. [8] Yang SM, Jo JY, Kim TH, et al. AC dynamics of ferroelectric domains from an investigation of the frequency dependence of hysteresis loops [J]. Physical Review B, 2010, 82: 174125. [9] Eiji K, Yanagihara H, Hashimoto S, et al. Hysteresis power-loss heating of ferromagnetic nanoparticles designed for magnetic thermoablation[J]. IEEE Transactions on Magnetics, 2008, 44(11):4452-4455. [10] 冯本珍. 铁磁材料磁滞回线的研究[J]. 中国科技信息, 2006, 22: 307-311. [11] 戴京营, 汪敢. 电源铁氧体中的磁滞损耗和涡流损耗的研究[J]. 磁性材料及器件, 1994, 25(2): 12-14. [12] Xie LQ, Jin WW, Zuo XR, et al. Construction of small-sized superparamagnetic Janus nanoparticles and their application in cancer combined chemotherapy and magnetic hyperthermia [J]. Biomaterials Science, 2020, 8: 1431-1441. [13] Deatsch AE, Evans BA. Heating efficiency in magnetic nanoparticle hyperthermia [J]. Journal of Magnetism and Magnetic Materials, 2014, 354: 163-172. [14] 李康. 磁流体肿瘤热疗的理论与实验研究[D]. 北京: 北京交通大学, 2017. [15] Rovers SA, Hoogenboom R, Kemmere MF, et al. Relaxation processes of superparamagnetic iron oxide nanoparticles in liquid and incorporated in poly(methyl methacrylate)[J]. Journal of Physical Chemistry C, 2008, 112: 15643-15646. [16] Jeun M, Kim YJ, Park KH, et al. Physical contribution of Néel and Brown relaxation to interpreting intracellular hyperthermia characteristics using superparamagnetic nanofluids [J]. Journal of Nanoscience and Nanotechnology, 2013, 13: 5719-5725. [17] Deissler RJ, Wu Y, Martens MA. Dependence of Brownian and Néel relaxation times on magnetic field strength [J]. Medical Physics, 2014, 41 (1): 012301. [18] Dieckhoff J, Eberbeck D, Schilling M, et al. Magnetic-field dependence of Brownian and Néel relaxation times [J]. Journal of Applied Physics, 2016, 119: 043903. [19] 王煦漫, 古宏晨, 杨正强, 等. 磁热疗用Fe3O4在交变磁场中的热效应[J]. 上海交通大学学报, 2005, 39(2): 275-278. [20] 陈小勇, 刘晓丽, 樊海明. 磁性纳米材料的生物医学应用[J]. 物理, 2020, 49(6), 381-389. [21] Lee JH, Jang J, Choi J, et al. Exchange-coupled magnetic nanoparticles for efficient heat induction [J]. Nature Nanotechnology, 2011, 6: 418-422. [22] 江小莉, 王燕云, 王英泽, 等. 调制磁性纳米颗粒提高磁热性能的研究[J]. 生物化学与生物物理进展, 2019, 46(3): 248-255. [23] Xie LQ, Jin WW, Chen HL,et al. Superparamagnetic iron oxide nanoparticles for cancer diagnosis and therapy [J]. Journal of Biomedical Nanotechnology, 2019, 15: 215-235. [24] Laurent S, Dutz S, Hfeli UO, et al. Magnetic fluid hyperthermia: Focus on superparamagnetic iron oxide nanoparticle s[J]. Advances in Colloid and Interface Science, 2011, 166: 8-23. [25] Bakoglidis KD, Simeonidis K, Sakellari D, et al. Size-dependent mechanisms in AC magnetic hyperthermia response of iron-oxide nanoparticles [J]. IEEE Transactions on Magnetics, 2012, 48(4): 1320-1323. [26] 韩栋, 张宝林, 苏礼超, 等. 不同粒径超顺磁性氧化铁纳米粒子的合成及其在交变磁场中的磁热效[J]. 材料工程, 2019, 47(4): 84-90. [27] Nemati Z, Salili SM, Alonso J, et al. Superparamagnetic iron oxide nanodiscs for hyperthermia therapy: does size matter [J]. Journal of Alloys and Compounds, 2017, 714: 709-714. [28] Kumar CSSR, Mohammad F. Magnetic nanomaterials for hyperthermia-based therapy and controlled drug delivery [J]. Advanced Drug Delivery Reviews, 2011, 63: 789-808. [29] Pradhan P, Giri J, Samanta G, et al. Comparative evaluation of heating ability and biocompatibility of different ferrite-based magnetic fluids for hyperthermia application [J]. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2006, 81B(1):12-22. [30] Corato RD, Espinosa A, Lartigue L, et al. Magnetic hyperthermia efficiency in the cellular environment for different nanoparticle designs [J]. Biomaterials, 2014, 35: 6400-6411. [31] Patade SR, Andhare DD, Somvanshi SB, et al. Self-heating evaluation of superparamagnetic MnFe2O4 nanoparticles formagnetic fluid hyperthermia application towards cancer treatment [J]. Ceramics International, 2020, 46: 25576-25583. [32] Ota S, Yamada T, Takemura Y. Magnetization reversal and specific loss power of magnetic nanoparticles in cellular environment evaluated by AC hysteresis measurement [J]. Journal of Nanomaterials, 2015, 2015:836761. [33] Gobbo OL, Sjaastad K, Radomski MW, et al. Magnetic nanoparticles in cancer theranostics [J]. Theranostics, 2015, 5(11): 1249-1263. [34] 丁琪. Fe3O4@Ag复合纳米结构的可控制备及其磁致热疗的基础研究[D]. 南京: 东南大学, 2018. [35] Albarqi HA, Wong LH, Schumann C, et al. Biocompatible nanoclusters with high heating efficiency for systemically delivered magnetic hyperthermia [J]. ACS Nano, 2019, 13(6): 6383-6395. [36] 赵印敏, 栗波, 杨晓君, 等. 靶向血管新生肽修饰的氧化铁纳米粒对荷瘤裸鼠磁热疗的研究[J]. 肿瘤, 2010, 30(5): 450-454. [37] 苏展. CD44靶向磁性纳米粒子在交变磁场下对肿瘤干细胞作用的研究[D]. 济南: 山东大学, 2019. [38] Sadhukha T, Wiedmann TS, Panyam J. Inhalable magnetic nanoparticles for targeted hyperthermia in lung cancer therapy [J]. Biomaterials, 2013, 34(21): 5163-5171. [39] Ling D, Lee N, Hyeon T. Chemical synthesis and assembly of uniformly sized iron oxide nanoparticles for medical applications [J]. Accounts of Chemical Research, 2015, 48: 1276-1285. [40] Li Y, Wang N, Huang X, et al. Polymer-assisted magnetic nanoparticle assemblies for biomedical applications[J]. ACS Applied Bio Materials, 2020, 3(1): 121-142. [41] 齐宝宁, 王小平, 王希楠, 等. 热疗对免疫细胞的影响及机制[J]. 现代肿瘤医学, 2018, 26(16): 2635-2639. [42] Lepock JR. Involvement of membranes in cellular responses to hyperthermia [J]. Radiation Research, 1982, 92(3): 433-438. [43] Sanz B, Calatayud MP, Torres TE, et al. Magnetic hyperthermia enhances cell toxicity with respect to exogenous heating [J]. Biomaterials, 2017, 114: 62-70. [44] Calatayud MP, Soler E, Torres TE, et al. Cell damage produced by magnetic fluid hyperthermia on microglial BV2 cells [J]. Scientific Reports, 2017, 7(1): 8627. [45] Prasad NK, Rathinasamy K, Panda D, et al. Mechanism of cell death induced by magnetic hyperthermia with nanoparticles of gamma-MnxFe2-xO3synthesized by a single step process [J]. Journal of Materials Chemistry, 2007, 17(48): 5042-5051. [46] Hilger I, Rapp A, Greulich KO, et al. Assessment of DNA damage in target tumor cells after thermoablation in mice [J]. Radiology, 2005, 237(2): 500-506. [47] 徐云钊, 奚庆华, 张玉泉. 磁性纳米顺铂微球联合磁流体热疗对卵巢癌skov-3细胞增殖、凋亡及侵袭的影响[J]. 山东医药, 2013, 53(28): 13-16. [48] Petryk AA, Giustini AJ, Gottesman RE, et al. Magnetic nanoparticle hyperthermia enhancement of cisplatin chemotherapy cancer treatment [J]. International Journal of Hyperthermia, 2013, 29(8): 845-851. [49] 冷曙光, 何云, 庄志雄, 等. 外源性化学物致机体DNA损伤与修复的生物标志物研究进展[J]. 中华预防医学杂志, 2005, 3: 210-212. [50] Cellai F, Munnia A, Viti J, et al. Magnetic hyperthermia and oxidative damage to DNA of human hepatocarcinoma cells [J]. International Journal of Molecular Sciences, 2017, 18: 939. [51] Yang CT, Li KY, Meng FQ, et al. ROS-induced HepG2 cell death from hyperthermia using magnetic hydroxyapatite nanoparticles [J]. Nanotechnology, 2018, 29(37): 375101. [52] Kobayashi T, Kakimi K, Nakayama E, et al. Antitumor immunity by magnetic nanoparticle-mediated hyperthermia [J]. Nanomedicine, 2014, 9(11): 1715-1726. [53] Chen T, Guo J, Han C, et al. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway [J]. Journal of Immunology, 2009, 182(3): 1449-1459. [54] Shi H, Cao T, Connolly JE, et al. Hyperthermia enhances CTL cross-priming [J]. Journal of Immunology, 2006, 176(4): 2134-2141. [55] 王锐. 磁流体热疗结合HSR1反义寡核苷酸抑制人脑膜瘤增殖和诱导细胞凋亡的体外实验研究[D]. 福州: 福建医科大学, 2008. [56] 黄芳玲. Cp6-0DNs在小鼠黑色素细胞瘤磁流体热疗中免疫增强效应的研究[D]. 长沙:中南大学, 2013. [57] 李凤武. 核酸适配体修饰的铁纳米材料对肿瘤热疗及免疫治疗的靶向调节作用[D]. 北京: 北京协和医学院, 2014. [58] 欧阳伟炜. 磁感应热疗及热化疗治疗大鼠乳腺癌的疗效及对免疫功能的影响[D]. 长沙: 中南大学, 2010. [59] Chao Y, Chen GB, Liang C, et al. Iron nanoparticles for low-power local magnetic hyperthermia in combination with immune checkpoint blockade for systemic antitumor therapy [J]. Nano Letter, 2019, 19(7): 4287-4296. [60] Wang Z, Zhang F, Shao D, et al. Janus nanobullets combine photodynamic therapy and magnetic hyperthermia to potentiate synergetic anti-metastatic immunotherapy[J]. Advanced Science, 2019, 6: 1901690. [61] Chang D, Lim M, Goos JACM, et al. Biologically targeted magnetic hyperthermia: Potential and limitations [J]. Frontiers in Pharmacology, 2018, 9: 831. [62] 王力. 核壳结构铁酸盐纳米立方块的制备及其靶向磁热疗与化疗协同治疗研究[D]. 上海: 上海师范大学, 2015. [63] Ferjaoui Z, Dine EJA, Kulmukhamedova A, et al. Doxorubicin-loaded thermoresponsive superparamagnetic nanocarriers for controlled drug delivery and magnetic hyperthermia application [J]. ACS Applied Materials & Interfaces, 2019, 11(34): 30610-30620. [64] Cazares-Cortes E, Espinosa A, Guigner JM, et al. Doxorubicin intracellular remote release from biocompatible oligo(ethylene glycol) methyl ether methacrylate-based magnetic nanogels triggered by magnetic hyperthermia [J]. ACS Applied Materials & Interfaces, 2017, 9(31): 25775-25788. [65] Mai BT, Balakrishnan PB, Barthel MJ, et al. Thermoresponsive iron oxide nanocubes for an effective clinical translation of magnetic hyperthermia and heat-mediated chemotherapy [J]. ACS Applied Materials & Interfaces, 2019, 11(6): 5727-5739. [66] 杨扬. 载顺铂的PLGA/Fe3O4原位植入物磁热消融联合化疗增效兔VX2肿瘤实验研究[D]. 重庆: 重庆医科大学, 2017. [67] Shen JM, Yin T, Tian XZ, et al. Surface charge-switchable polymeric magnetic nanoparticles for the controlled release of anticancer drug [J]. ACS Applied Materials & Interfaces, 2013, 5(15): 7014-7024. [68] Pramanik N, Ranganathan S, Rao S, et al. A composite of hyaluronic acid-modified graphene oxide and iron oxide nanoparticles for targeted drug delivery and magnetothermal therapy [J]. ACS Omega, 2019, 4(5): 9284-9293. [69] Ognjanovic′ M, Radovic′ M, Mirkovic′ M, et al.Iron oxide nanoflowers designed for potential use in dual magnetic hyperthermia/radionuclide cancer therapy and diagnosis [J]. ACS Applied Materials & Interfaces, 2019, 11(44): 41109-41117. [70] Ni D, Ferreira CA, Barnhart TE, et al. Magnetic targeting of nanotheranostics enhances cerenkov radiation-induced photodynamic therapy [J]. Journal of the American Chemical Society, 2018, 140(44): 14971-14979. [71] Spirou SV, Basini M, Lascialfari A, et al. Magnetic hyperthermia and radiation therapy: radiobiological principles and current practice [J]. Nanomaterials, 2018, 8: 401. [72] Spirou SV, Lima SAC, Bouziotis P, et al. Recommendations for in vitro and in vivo testing of magnetic nanoparticle hyperthermia combined with radiation therapy [J]. Nanomaterials, 2018, 8: 306. [73] 谭曼曼, 刘燕玲, 张瑜娟, 等.纳米载体-近红外光热疗法在肿瘤治疗中的研究进展[J]. 南昌大学学报(医学版), 2020, 60(1): 88-93. [74] Espinosa A, Corato RD, Kolosnjaj-Tabi J, et al. Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment [J]. ACS Nano, 2016, 10(2): 2436-2446. [75] Corato RD, Béalle G, Kolosnjaj-Tabi J, et al. Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes [J]. ACS Nano, 2015, 9(3): 2904-2916. [76] Das R, Rinaldi-Montes N, Alonso J, et al. Boosted hyperthermia therapy by combined AC magnetic and photothermal exposures in Ag/Fe3O4 nanoflowers [J]. ACS Applied Materials & Interfaces, 2016, 8(38): 25162-25169. [77] 刘庆祖, 杨慧恺, 刘建恒, 等. 磁性纳米颗粒在肿瘤药物及肿瘤治疗中的研究进展[J]. 解放军医学院学报, 2020, 41(4): 409-412. [78] Pan J, Hu P, Guo Y, et al.Combined magnetic hyperthermia and immune therapy for primary and metastatic tumor treatments [J].ACS Nano, 2020, 14(1): 1033-1044. [79] Liu X, Zheng J, Sun W, et al. Ferrimagnetic vortex nanoring-mediated mild magnetic hyperthermia imparts potent immunological effect for treating cancer metastasis [J]. ACS Nano, 2019, 13(8): 8811-8825. [80] Saeed M, Xu Z, Geest BGD, et al. Molecular imaging for cancer immunotherapy: Seeing is believing [J]. Bioconjugate Chemistry, 2020, 31(2): 404-415. [81] 李毅斌, 胡喜钢, 吴钢, 等. 基于检查点阻断抗体的肿瘤靶向免疫治疗研究进展[J]. 广东医学, 2015, 3: 484-487. [82] Andra W, Nowak H, Magnetism in Medicine: A Handbook [M] (2nd Edition). Bristol: IOP Publishing Ltd, 2007: 550-567. [83] 严文辉, 周汉新, 李富荣. 纳米磁靶向药物载体在肿瘤治疗中的研究进展[J]. 中国药房, 2007, 18(4), 305-307. [84] 黄琴琴, 王永禄, 李学明. 纳米载体材料毒理学效应及其作用机制研究进展[J]. 中国药房, 2011, 22(21), 2004-2007. [85] Kim JS, Yoon TJ, Yu KN, et al. Toxicity and tissue distribution of magnetic nanoparticles in mice [J]. Toxicological Science, 2006, 89(1): 338-347. [86] Coricovac DE, Moacǎ EA, Pinzaru I, et al. Magnetic resonance imaging contrast agents based on iron oxide superparamagnetic ferrofluids [J]. Chemistry of Materials, 2010, 22(5):1739-1748. [87] Agotegaray MA, Campelo AE, Zysler RD, et al. Magnetic nanoparticles for drug targeting: from design to insights into systemic toxicity. Preclinical evaluation of hematological, vascular and neurobehavioral toxicology [J]. Biomaterials Science, 2017, 5(4):772-783. [88] Hfeli UO, Riffle JS, Harris-Shekhawat L, et al. Cell uptake and in vitro toxicity of magnetic nanoparticles suitable for drug delivery [J]. Molecular Pharmaceutics, 2009, 6(5): 1417-1428. [89] Wu X, Tan Y, Mao H, et al. Toxic effects of iron oxide nanoparticles on human umbilical vein endothelial cells [J]. International Journal of Nanomedicine, 2010, 5: 385-399. [90] Sadeghi L, Yousefi BV, Espanani HR, Toxic effects of the Fe2O3 nanoparticles on the liver and lung tissue [J]. Bratislavske Lekarske Listy, 2015, 116 (6): 373-378. [91] Kim JE, Shin JY, Cho MH. Magnetic nanoparticles: an update of application for drug delivery and possible toxic effects [J]. Archives of Toxicology, 2011, 86(5): 685-700. [92] Agotegaray MA, Lassalle VL. Silica-coated magnetic nanoparticles: An insight into targeted drug delivery and toxicology [M]// Springer Briefs in Molecular Science. Berlin: Springer Nature, 2017: 76-78.
