Recent advances in magnetic fluid hyperthermia for cancer therapy

https://doi.org/10.1016/j.colsurfb.2018.10.051Get rights and content

Highlights

  • Theory of magnetic fluid hyperthermia to design an effective heat mediator.

  • Protocols for preparation of water-soluble biofunctional magnetic nanoparticle.

  • Recent pre-clinical studies of cancer treatment by magnetic fluid hyperthermia.

  • Combination of hyperthermia with stimulated chemotherapy for enhanced cancer therapy.

Abstract

Recently, magnetic fluid hyperthermia using biocompatible magnetic nanoparticles as heat mediators for cancer therapy has been extensively investigated due to its high efficiency and limited side effects. However, the development of more efficient heat nanomediators that exhibit very high specific absorption rate (SAR) value is essential for clinical application to overcome the several restrictions previously encountered due to the large quantity of nanomaterial required for effective treatment. In this review, we focus on the current progress in the development of magnetic nanoparticles based hyperthermia therapy as well as combined therapy harnessing hyperthermia with heat-mediated drug delivery for cancer treatment. We also address the fundamental principles of magnetic hyperthermia, basics of magnetism including the effect of several parameters on heating capacity, synthetic methods and nanoparticle surface chemistry needed to design and develop an ideal magnetic nanoparticle heat mediator suitable for clinical translation in cancer therapy.

Introduction

Cancer is a serious health issue in the world owing to a large number of cancer-related human deaths (8.8 million in 2015 worldwide) [1,2]. This is currently responsible for most of the deaths in the United States and Europe after heart disease as well as in the world after heart and infectious diseases [1,2]. Cancer rapidly spread to other parts of the human body because of uncontrolled growth of tumor cells, as long as their aptitude to invasion of adjacent tissue, metastasis, and immortality [3]. Thus, the diagnosis of cancer at an early stage is also essential from the current perspective of cancer therapy. For this purpose, several sensitive and selective bioassays including immunoassays, polymerase chain reaction, and fluorescence in situ hybridization, along with imaging techniques such as magnetic resonance imaging, fluorescence imaging, computed tomography, and ultrasound imaging have been well developed [[4], [5], [6], [7], [8], [9], [10], [11]]. At present, conventional approaches in use for cancer treatment include the removal of the tumor via surgery, radiation therapy, chemotherapy, or a combination of them. However, the toxicity to surrounding healthy cells, drug resistance of cancers, ineffectiveness against metastatic disease, difficulty in overcoming the biological barriers, and tumor relapse have limited the efficacy of common therapies [[12], [13], [14]]. Therefore, the development of new advanced techniques to replace or partner conventional treatments is strongly demanded. Nowadays, various new techniques based on nanomaterials that exhibit reduced side effects, including photothermal therapy, gene therapy, immunotherapy, photodynamic therapy, magnetic hyperthermia among others, have been developed in the laboratory and few of them are now under clinical investigation [11,[15], [16], [17], [18], [19]].

Magnetic fluid hyperthermia (MFH) is a favorable non-invasive technique for cancer therapy and has several advantages compared to traditional hyperthermia therapy [18,19]. This therapy involves selective administration of magnetic nanoparticles as a mediator of heat into the tumor followed by exposure of this tumor to an external alternating magnetic field (AMF). As a result, the temperature inside the tumor increases due to the generation of heat from internalized magnetic nanoparticles under high frequency AMF leading to magnetic energy dissipation for single-domain particles caused by internal Néel fluctuations of the nanoparticle magnetic moment and external Brownian fluctuations. Increased temperature kills cancer cells through various direct mechanisms, including denaturation, folding, and aggregation of proteins, apoptosis, necrosis and coagulation, and indirect response mediated by activation of the immune system promoted by overexpression of heat shock proteins [[18], [19], [20], [21]]. Magnetic hyperthermia has several advantages including higher penetration ability of magnetic field in the tissues and enhanced accumulation of magnetic nanoparticles in the tumor via magnetic targeting strategy for cancer treatment compared to NIR laser-based hyperthermia [15]. In addition, magnetic fluid hyperthermia based multimodal cancer therapies especially in combination with chemotherapy is more effective for cancer treatment due to their synergistic effects [[22], [23], [24]]. The efficiency of magnetic hyperthermia therapy is mainly determined by the specific absorption rate (SAR) value of heat mediator that further depends on the applied magnetic field, magnetic properties of nanoparticles, and the properties of the biological medium [18,19]. In general, the heating power of magnetic nanoparticles is highly sensitive to the nanocrystal size, the material composition, and the solvent properties [25]. In the last few decades, magnetic nanoparticles have been widely used for several biological applications including bioimaging and therapy because of their size-dependent magnetic properties and high biocompatibility [[26], [27], [28]]. Therefore, various methods have been well established for the synthesis of high-quality magnetic nanoparticles and also for their surface modifications to allow their utilization in a biological environment.

In this review, we begin with the basic principles of magnetism and magnetic heating in order to offer an insight into the essential elements needed for the design of magnetic nanoparticles useful for efficient hyperthermia agents for cancer therapy. We also provide a brief description of the synthetic methods and surface chemistry for the synthesis of water-soluble magnetic nanoparticles to develop an excellent heat mediator with high heating capacity. Finally, we summarize the recent studies (since 2013) on magnetic hyperthermia therapy as well as its combined effects with magnetothermal responsive released anticancer drug molecules for cancer treatment.

Section snippets

Magnetic fluid hyperthermia

Magnetic fluid hyperthermia involves the conversion of heat from magnetic nanoparticles via magnetic energy loss in the presence of an external AMF [18,19]. The produced heat is sufficient to kill the cancer cells and subsequently to destroy the tumor. Magnetic particles based hyperthermia was first introduced by Gilchrist et al. and its first implementation in the biological system was performed in 1979 [29,30]. In the last few decades, various pre-clinical and clinical research studies have

Basics of magnetism

The understanding of fundamental concepts about magnetic nanoparticles as well as the effect of physical and chemical properties on their magnetic properties is crucial to design optimal heat nanomediators. Magnetic nanomaterials are classified into several categories depending on their magnetic behavior, including for example diamagnetic, paramagnetic, ferromagnetic, ferrimagnetic and antiferromagnetic based on the arrangement of magnetic dipoles in absence or presence of an external magnetic

Magnetic hyperthermia therapy

In last decades, several pre-clinical magnetic hyperthermia studies have been performed to improve the cancer treatment aiming at minimizing the side effects on healthy cells. This section describes the advances in magnetic fluid hyperthermia for cancer therapy relative to the last five years (Table 1).

Majeed et al. synthesized silica-coated iron oxide (Fe3O4-SiO2) nanoparticles with tunable shell thickness [99]. The SAR value of these magnetic nanoparticles was enhanced after coating compared

Conclusions

Magnetic nanoparticles-based hyperthermia therapy is increasingly estimated to play an important role in cancer treatment. The combined effects of hyperthermia therapy with chemotherapy are more effective in the treatment and management of cancer compared to either hyperthermia therapy or chemotherapy alone. Moreover, magnetic resonance imaging of tumor using heat nanomediators as a contrast agent is also helpful to monitor the progress of treatment. Though the increased temperature of the

Acknowledgements

This work was partly supported by the Fondazione per la Ricerca Biomedica (FRRB) and by Academic Funding Unimib.

References (132)

  • H.M. Yang et al.

    A direct surface modification of iron oxide nanoparticles with various poly(amino acid)s for use as magnetic resonance probes

    J. Colloid Interface Sci.

    (2013)
  • S.H. Jalalian et al.

    Epirubicin loaded super paramagnetic iron oxide nanoparticle-aptamer bioconjugate for combined colon cancer therapy and imaging in vivo

    Eur. J. Pharm. Sci.

    (2013)
  • L. Wang et al.

    Multifunctional polyglycerol-grafted Fe3O4@SiO2 nanoparticles for targeting ovarian cancer cells

    Biomaterials

    (2011)
  • K. Hervé-Aubert et al.

    Impact of site-specific conjugation of ScFv to multifunctional nanomedicines using second generation maleimide

    Bioconjug. Chem.

    (2018)
  • J. Majeed et al.

    Enhanced specific absorption rate in silanol functionalized Fe3O4 core-shell nanoparticles: study of Fe leaching in Fe3O4 and hyperthermia in L929 and HeLa cells

    Colloids Surf. B

    (2014)
  • G. 2015 M et al.

    Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015

    Lancet

    (2016)
  • L.A. Torre et al.

    Global cancer statistics, 2012

    CA Cancer J. Clin.

    (2015)
  • L. Wu et al.

    Cancer biomarker detection: recent achievements and challenges

    Chem. Soc. Rev.

    (2015)
  • C.K. Dixit et al.

    Electrochemistry-based approaches to low cost, high sensitivity, automated, multiplexed protein immunoassays for cancer diagnostics

    Analyst

    (2016)
  • N. Goossens et al.

    Cancer biomarker discovery and validation

    Transl. Cancer Res.

    (2015)
  • S.B. Nimse et al.

    Biomarker detection technologies and future directions

    Analyst

    (2016)
  • D. Ni et al.

    Engineering of inorganic nanoparticles as magnetic resonance imaging contrast agents

    Chem. Soc. Rev.

    (2017)
  • H. Kobayashi et al.

    New strategies for fluorescent probe design in medical diagnostic imaging

    Chem. Rev.

    (2010)
  • E.B. Ehlerding et al.

    Big potential from small agents: nanoparticles for imaging-based companion diagnostics

    ACS Nano

    (2018)
  • Y. Huang et al.

    Biomedical nanomaterials for imaging-guided cancer therapy

    Nanoscale

    (2012)
  • K. Brindle

    New approaches for imaging tumour responses to treatment

    Nat. Rev. Cancer

    (2008)
  • K. Cho et al.

    Therapeutic nanoparticles for drug delivery in cancer

    Clin. Cancer Res.

    (2008)
  • G. Szakács et al.

    Targeting multidrug resistance in cancer

    Nat. Rev. Drug Discov.

    (2006)
  • W. Fan et al.

    Nanotechnology for multimodal synergistic cancer therapy

    Chem. Rev.

    (2017)
  • L. Gong et al.

    Two-dimensional transition metal dichalcogenide nanomaterials for combination cancer therapy

    J. Mater. Chem. B

    (2017)
  • L. Luo et al.

    Nanomaterial-based cancer immunotherapy

    J. Mater. Chem. B

    (2017)
  • N.K. Prasad et al.

    Mechanism of cell death induced by magnetic hyperthermia with nanoparticles of γ-MnxFe2–xO3 synthesized by a single step process

    J. Mater. Chem.

    (2007)
  • A. Ito et al.

    Heat shock protein 70 gene therapy combined with hyperthermia using magnetic nanoparticles

    Cancer Gene Ther.

    (2003)
  • R. Di Corato et al.

    Combining magnetic hyperthermia and photodynamic therapy for tumor ablation with photoresponsive magnetic liposomes

    ACS Nano

    (2015)
  • M. Gogoi et al.

    Biocompatibility and therapeutic evaluation of magnetic liposomes designed for self-controlled cancer hyperthermia and chemotherapy

    Integr. Biol.

    (2017)
  • E. Cazares-Cortes et al.

    Doxorubicin intracellular remote release from biocompatible oligo(ethylene glycol) methyl ether methacrylate-based magnetic nanogels triggered by magnetic hyperthermia

    ACS Appl. Mater. Interfaces

    (2017)
  • J.P. Fortin et al.

    Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia

    J. Am. Chem. Soc.

    (2007)
  • O.L. Gobbo et al.

    Magnetic nanoparticles in cancer theranostics

    Theranostics

    (2015)
  • L.-M. Lacroix et al.

    Magnetic nanoparticles as both imaging probes and therapeutic agents

    Curr. Top. Med. Chem.

    (2010)
  • M. Colombo et al.

    Biological applications of magnetic nanoparticles

    Chem. Soc. Rev.

    (2012)
  • R.K. Gilchrist et al.

    Selective inductive heating of lymph nodes

    Ann. Surg.

    (1957)
  • B. Thiesen et al.

    Clinical applications of magnetic nanoparticles for hyperthermia

    Int. J. Hyperthermia

    (2008)
  • P. Wust et al.

    Magnetic nanoparticles for interstitial thermotherapy-Feasibility, tolerance and achieved temperatures

    Int. J. Hyperthermia

    (2006)
  • J. Carrey et al.

    Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: application to magnetic hyperthermia optimization

    J. Appl. Phys.

    (2011)
  • M. Lévy et al.

    Magnetically induced hyperthermia: size-dependent heating power of γ-Fe2O3 nanoparticles

    J. Phys. Condens. Matter

    (2008)
  • S. Mornet et al.

    Magnetic nanoparticle design for medical diagnosis and therapy

    J. Mater. Chem.

    (2004)
  • U. Jeong et al.

    Superparamagnetic colloids: controlled synthesis and niche applications

    Adv. Mater.

    (2007)
  • L. Lartigue et al.

    Water-dispersible sugar-coated iron oxide nanoparticles. An evaluation of their relaxometric and magnetic hyperthermia properties

    J. Am. Chem. Soc.

    (2011)
  • C. Martinez-Boubeta et al.

    Learning from nature to improve the heat generation of iron-oxide nanoparticles for magnetic hyperthermia applications

    Sci. Rep.

    (2013)
  • P. Guardia et al.

    Water-soluble iron oxide nanocubes with high values of specific absorption rate for cancer cell hyperthermia treatment

    ACS Nano

    (2012)
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