Photo-fluorescent and magnetic properties of iron oxide nanoparticles for biomedical applications.

Iron oxide exhibits fascinating physical properties especially in the nanometer range, not only from the standpoint of basic science, but also for a variety of engineering, particularly biomedical applications. For instance, Fe3O4 behaves as superparamagnetic as the particle size is reduced to a few nanometers in the single-domain region depending on the type of the material. The superparamagnetism is an important property for biomedical applications such as magnetic hyperthermia therapy of cancer. In this review article, we report on some of the most recent experimental and theoretical studies on magnetic heating mechanisms under an alternating (AC) magnetic field. The heating mechanisms are interpreted based on Néel and Brownian relaxations, and hysteresis loss. We also report on the recently discovered photoluminescence of Fe3O4 and explain the emission mechanisms in terms of the electronic band structures. Both optical and magnetic properties are correlated to the materials parameters of particle size, distribution, and physical confinement. By adjusting these parameters, both optical and magnetic properties are optimized. An important motivation to study iron oxide is due to its high potential in biomedical applications. Iron oxide nanoparticles can be used for MRI/optical multimodal imaging as well as the therapeutic mediator in cancer treatment. Both magnetic hyperthermia and photothermal effect has been utilized to kill cancer cells and inhibit tumor growth. Once the iron oxide nanoparticles are up taken by the tumor with sufficient concentration, greater localization provides enhanced effects over disseminated delivery while simultaneously requiring less therapeutic mass to elicit an equal response. Multi-modality provides highly beneficial co-localization. For magnetite (Fe3O4) nanoparticles the co-localization of diagnostics and therapeutics is achieved through magnetic based imaging and local hyperthermia generation through magnetic field or photon application. Here, Fe3O4 nanoparticles are shown to provide excellent conjugation bases for entrapment of therapeutic molecules, fluorescent agents, and targeting ligands; enhancement of solid tumor treatment is achieved through co-application of local hyperthermia with chemotherapeutic agents.

[1]  M. Hanson The frequency dependence of the complex susceptibility of magnetic liquids , 1991 .

[2]  Marc Respaud,et al.  Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: Application to magnetic hyperthermia optimization , 2011 .

[3]  V. Cabuil,et al.  Iron Oxide Monocrystalline Nanoflowers for Highly Efficient Magnetic Hyperthermia , 2012 .

[4]  Hidekazu Tanaka,et al.  Effect of ferrous/ferric ions molar ratio on reaction mechanism for hydrothermal synthesis of magnetite nanoparticles , 2008 .

[5]  W. Kaiser,et al.  Physical limits of hyperthermia using magnetite fine particles , 1998 .

[6]  P. Wachter,et al.  Optical properties of magnetite (Fe3O4) , 1979 .

[7]  S. Chakraborty,et al.  Detection of total count of Staphylococcus aureus using anti-toxin antibody labelled gold magnetite nanocomposites: a novel tool for capture, detection and bacterial separation , 2011 .

[8]  Andris F. Bakuzis,et al.  Effect of magnetic dipolar interactions on nanoparticle heating efficiency: Implications for cancer hyperthermia , 2013, Scientific Reports.

[9]  Rodney C. Ewing,et al.  Dual Surface‐Functionalized Janus Nanocomposites of Polystyrene/Fe3O4@SiO2 for Simultaneous Tumor Cell Targeting and Stimulus‐Induced Drug Release , 2013, Advanced materials.

[10]  P Wust,et al.  Clinical hyperthermia of prostate cancer using magnetic nanoparticles: Presentation of a new interstitial technique , 2005, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[11]  D. Pang,et al.  Fluorescent-magnetic-biotargeting multifunctional nanobioprobes for detecting and isolating multiple types of tumor cells. , 2011, ACS nano.

[12]  W. Wang,et al.  Quantum‐Dot‐Activated Luminescent Carbon Nanotubes via a Nano Scale Surface Functionalization for in vivo Imaging , 2007, Advanced Materials.

[13]  Hong Xu,et al.  Fluorescent, superparamagnetic nanospheres for drug storage, targeting, and imaging: a multifunctional nanocarrier system for cancer diagnosis and treatment. , 2010, ACS nano.

[14]  G. Kelsall,et al.  Photoelectrophoresis of colloidal iron oxides 1. Hematite (α-Fe2O3) , 1993 .

[15]  I. Baker,et al.  Surface Engineering of Core/Shell Iron/Iron Oxide Nanoparticles from Microemulsions for Hyperthermia. , 2010, Materials science & engineering. C, Materials for biological applications.

[16]  N. Gu,et al.  Near-infrared fluorescence labeling of iron nanoparticles and applications for cell labeling and in vivo imaging. , 2012, Methods in molecular biology.

[17]  W. Wang,et al.  Quantum dot conjugated hydroxylapatite nanoparticles for in vivo imaging , 2008, Nanotechnology.

[18]  A. Ganguli,et al.  Enhanced functionalization of Mn2O3@SiO2 core-shell nanostructures , 2011, Nanoscale research letters.

[19]  Chao Liu,et al.  Synthesis of bilayer oleic acid-coated Fe3O4 nanoparticles and their application in pH-responsive Pickering emulsions. , 2007, Journal of colloid and interface science.

[20]  Janusz Skowronek,et al.  Hyperthermia – description of a method and a review of clinical applications , 2007 .

[21]  D. Dunlop,et al.  Magnetic Properties of Hydrothermally Recrystallized Magnetite Crystals , 1987, Science.

[22]  Nerine J. Cherepy,et al.  Ultrafast Studies of Photoexcited Electron Dynamics in γ- and α-Fe2O3 Semiconductor Nanoparticles , 1998 .

[23]  V. Fazio,et al.  Sorafenib and locoregional deep electro-hyperthermia in advanced hepatocellular carcinoma: A phase II study , 2014, Oncology letters.

[24]  M. Grätzel,et al.  Ultrafast Charge Carrier Recombination and Trapping in Hematite Photoanodes under Applied Bias , 2014, Journal of the American Chemical Society.

[25]  Hong Xu,et al.  Photothermal effects and toxicity of Fe3O4 nanoparticles via near infrared laser irradiation for cancer therapy. , 2015, Materials science & engineering. C, Materials for biological applications.

[26]  Dar-Bin Shieh,et al.  Characterization of aqueous dispersions of Fe(3)O(4) nanoparticles and their biomedical applications. , 2005, Biomaterials.

[27]  P. C. Fannin Investigating magnetic fluids by means of complex susceptibility measurements , 2003 .

[28]  M. Erbudak,et al.  Final state effects in the 3d-photoelectron spectrum of Fe3O4 and comparison with FexO , 1977 .

[29]  M. Knobel,et al.  Effect of dipolar interaction observed in iron-based nanoparticles , 2005 .

[30]  A. Yaresko,et al.  Electronic structure and magneto-optical Kerr effect of Fe{sub 3}O{sub 4} and Mg{sup 2+}- or Al{sup 3+}-substituted Fe{sub 3}O{sub 4} , 2001 .

[31]  U. Nowak Thermally Activated Reversal in Magnetic Nanostructures , 2001 .

[32]  R. E. Rosensweig,et al.  Heating magnetic fluid with alternating magnetic field , 2002 .

[33]  L. Brus,et al.  Magnetite Fe3O4 Nanocrystals: Spectroscopic Observation of Aqueous Oxidation Kinetics† , 2003 .

[34]  Puneet Mishra,et al.  Resistive phase transition of the superconducting Si(111)-(7×3)-In surface , 2013, Nanoscale Research Letters.

[35]  P Jack Hoopes,et al.  Development of novel magnetic nanoparticles for hyperthermia cancer therapy , 2011, BiOS.

[36]  Jie Ren,et al.  Magnetocaloric effect in magnetothermally-responsive nanocarriers for hyperthermia-triggered drug release , 2012, Nanotechnology.

[37]  Shih-Chang Wang,et al.  Biodegradable magnetic-fluorescent magnetite/poly(dl-lactic acid-co-alpha,beta-malic acid) composite nanoparticles for stem cell labeling. , 2010, Biomaterials.

[38]  Xiangmin Zhang,et al.  Novel microwave-assisted digestion by trypsin-immobilized magnetic nanoparticles for proteomic analysis. , 2008, Journal of proteome research.

[39]  K. Pantopoulos,et al.  Iron metabolism and toxicity. , 2005, Toxicology and applied pharmacology.

[40]  Baoan Chen,et al.  Pharmacokinetic parameters and tissue distribution of magnetic Fe3O4 nanoparticles in mice , 2010, International journal of nanomedicine.

[41]  Hong Xu,et al.  Photoluminescence and photothermal effect of Fe3O4 nanoparticles for medical imaging and therapy , 2014 .

[42]  J. Dormann,et al.  A dynamic study of small interacting particles: superparamagnetic model and spin-glass laws , 1988 .

[43]  A. Bakuzis,et al.  Aggregate formation on polydisperse ferrofluids: A Monte Carlo analysis , 2005 .

[44]  Crispin R Dass,et al.  Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems , 2013, The Journal of pharmacy and pharmacology.

[45]  Hao Zeng,et al.  Size-controlled synthesis of magnetite nanoparticles. , 2002, Journal of the American Chemical Society.

[46]  H. Gu,et al.  Magnetite nanocrystal clusters with ultra-high sensitivity in magnetic resonance imaging. , 2012, Chemphyschem : a European journal of chemical physics and physical chemistry.

[47]  S. Shen,et al.  Monodisperse magnetites anchored onto carbon nanotubes: a platform for cell imaging, magnetic manipulation and enhanced photothermal treatment of tumors. , 2013, Journal of materials chemistry. B.

[48]  M. Hsiao,et al.  Biocompatibility of Fe3O4 nanoparticles evaluated by in vitro cytotoxicity assays using normal, glia and breast cancer cells , 2010, Nanotechnology.

[49]  Gennaro Bellizzi,et al.  Broadband spectroscopy of the electromagnetic properties of aqueous ferrofluids for biomedical applications , 2010 .

[50]  G. Trägårdh,et al.  Membrane emulsification — a literature review , 2000 .

[51]  Wei Wang,et al.  Luminescent hydroxylapatite nanoparticles by surface functionalization , 2006 .

[52]  Arturo Mediano,et al.  Influence of dipolar interactions on hyperthermia properties of ferromagnetic particles , 2010 .

[53]  R. Metselaar,et al.  Optical and magneto-optical polar Kerr spectra of Fe3O4 and Mg2+- or Al3+-substituted Fe3O4 , 1997 .

[54]  P. Jönsson,et al.  Relaxation in interacting nanoparticle systems , 2004 .

[55]  L. Lartigue,et al.  Mastering the Shape and Composition of Dendronized Iron Oxide Nanoparticles To Tailor Magnetic Resonance Imaging and Hyperthermia , 2014 .

[56]  Baoan Chen,et al.  Multifunctional magnetic Fe3O4 nanoparticles combined with chemotherapy and hyperthermia to overcome multidrug resistance , 2012, International journal of nanomedicine.

[57]  Qiang Wu,et al.  Pluronic-encapsulated natural chlorophyll nanocomposites for in vivo cancer imaging and photothermal/photodynamic therapies. , 2014, Biomaterials.

[58]  P. Maruthamuthu,et al.  Photogeneration of hydrogen using visible light with undoped/doped α-Fe2O3 in the presence of methyl viologen , 1995 .

[59]  J. Coey,et al.  One-Electron Energy Levels inFe3O4 , 1972 .

[60]  Mingyuan Gao,et al.  Facile synthesis of ultrasmall PEGylated iron oxide nanoparticles for dual-contrast T1- and T2-weighted magnetic resonance imaging , 2011, Nanotechnology.

[61]  Porto,et al.  Influence of dipolar interaction on magnetic properties of ultrafine ferromagnetic particles , 2000, Physical review letters.

[62]  H. P. Broida,et al.  Chemiluminescence and photoluminescence of diatomic iron oxide , 1975 .

[63]  R. K. Pandey,et al.  Dependence of pH and surfactant effect in the synthesis of magnetite (Fe3O4) nanoparticles and its properties , 2010 .

[64]  Jean-Paul Fortin,et al.  Intracellular heating of living cells through Néel relaxation of magnetic nanoparticles , 2008, European Biophysics Journal.

[65]  Y. Tokura,et al.  Charge-gap formation upon the Verwey transition in Fe 3 O 4 , 1998 .

[66]  Oliver T. Bruns,et al.  A highly effective, nontoxic T1 MR contrast agent based on ultrasmall PEGylated iron oxide nanoparticles. , 2009, Nano letters.

[67]  On the broadband measurement of the permittivity and magnetic susceptibility of ferrofluids , 1997 .

[68]  C. Robic,et al.  Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. , 2008, Chemical reviews.

[69]  Paul R. Stauffer,et al.  A pilot clinical trial of intravesical mitomycin-C and external deep pelvic hyperthermia for non-muscle-invasive bladder cancer , 2014, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[70]  A. Schrand,et al.  Fundamental examination of nanoparticle heating kinetics upon near infrared (NIR) irradiation. , 2011, ACS applied materials & interfaces.

[71]  Takeshi Kobayashi,et al.  Cancer hyperthermia using magnetic nanoparticles , 2011, Biotechnology journal.

[72]  M. E. Khosroshahi,et al.  Preparation and characterization of silica-coated iron-oxide bionanoparticles under N2 gas , 2010 .

[73]  M. F. Hansen,et al.  Models for the dynamics of interacting magnetic nanoparticles , 1998 .

[74]  O. Shebanova,et al.  Raman spectroscopic study of magnetite (FeFe2O4): a new assignment for the vibrational spectrum , 2003 .

[75]  Allen,et al.  Band gaps and electronic structure of transition-metal compounds. , 1985, Physical review letters.

[76]  S. Dutz,et al.  Effects of size distribution on hysteresis losses of magnetic nanoparticles for hyperthermia , 2008, Journal of physics. Condensed matter : an Institute of Physics journal.

[77]  U. Schwertmann,et al.  The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses , 2003 .

[78]  Hiroyuki Honda,et al.  Medical application of functionalized magnetic nanoparticles. , 2005, Journal of bioscience and bioengineering.

[79]  Hong Xu,et al.  Dipole-interaction mediated hyperthermia heating mechanism of nanostructured Fe3O4 composites , 2014 .

[80]  Kezheng Chen,et al.  Synthesis of magnetite-silica core-shell nanoparticles via direct silicon oxidation. , 2014, Journal of colloid and interface science.

[81]  T. Xia,et al.  Understanding biophysicochemical interactions at the nano-bio interface. , 2009, Nature materials.

[82]  R. Weissleder A clearer vision for in vivo imaging , 2001, Nature Biotechnology.

[83]  Hai-tao Yang,et al.  Exceeding natural resonance frequency limit of monodisperse Fe3O4 nanoparticles via superparamagnetic relaxation , 2013, Scientific Reports.

[84]  A. Mediano,et al.  Specific Absorption Rates and Magnetic Properties of Ferrofluids with Interaction Effects at Low Concentrations , 2010 .

[85]  G. Kelsall,et al.  Photoelectrophoresis of colloidal iron oxides. Part 2.—Magnetite (Fe3O4) , 1996 .

[86]  C. Röcker,et al.  Modeling receptor-mediated endocytosis of polymer-functionalized iron oxide nanoparticles by human macrophages. , 2011, Biomaterials.

[87]  R. Roe,et al.  Methods of X-ray and Neutron Scattering in Polymer Science , 2000 .

[88]  A. Bard,et al.  Photochemistry of colloidal semiconducting iron oxide polymorphs , 1987 .

[89]  Qingsheng Wu,et al.  Near-infrared laser light mediated cancer therapy by photothermal effect of Fe3O4 magnetic nanoparticles. , 2013, Biomaterials.

[90]  Matthias Zeisberger,et al.  Size-dependant heating rates of iron oxide nanoparticles for magnetic fluid hyperthermia. , 2009, Journal of magnetism and magnetic materials.

[91]  D. Dunlop Superparamagnetic and single‐domain threshold sizes in magnetite , 1973 .

[92]  E. Verwey,et al.  Physical Properties and Cation Arrangement of Oxides with Spinel Structures II. Electronic Conductivity , 1947 .

[93]  Rudolf Hergt,et al.  Magnetic particle hyperthermia—a promising tumour therapy? , 2014, Nanotechnology.

[94]  U. Nowak,et al.  Role of dipole-dipole interactions for hyperthermia heating of magnetic nanoparticle ensembles , 2012 .

[95]  Rujia Zou,et al.  Sub-10 nm Fe3O4@Cu(2-x)S core-shell nanoparticles for dual-modal imaging and photothermal therapy. , 2013, Journal of the American Chemical Society.

[96]  Werner A. Kaiser,et al.  Maghemite nanoparticles with very high AC-losses for application in RF-magnetic hyperthermia , 2004 .

[97]  S. Ropele,et al.  Tracking of Magnetite Labeled Nanoparticles in the Rat Brain Using MRI , 2014, PloS one.

[98]  Yan Hu,et al.  Effects of mesoporous SiO2 , Fe3 O4 , and TiO2 nanoparticles on the biological functions of endothelial cells in vitro. , 2014, Journal of biomedical materials research. Part A.

[99]  Jun Ma,et al.  Photothermal effect for Fe3O4 nanoparticles contained in micelles induced by near-infrared light , 2012 .

[100]  Heather Kalish,et al.  Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. , 2003, Radiology.

[101]  Zhuge Xi,et al.  Intraperitoneal injection of magnetic Fe3O4-nanoparticle induces hepatic and renal tissue injury via oxidative stress in mice , 2012, International journal of nanomedicine.

[102]  Werner A. Kaiser,et al.  Enhancement of AC-losses of magnetic nanoparticles for heating applications , 2004 .

[103]  P. Wachter,et al.  Evidence for 3dn to 3dn-14s transitions in magnetite and in lithium and magnesium ferrites , 1983 .

[104]  B. Berne,et al.  Dynamic Light Scattering: With Applications to Chemistry, Biology, and Physics , 1976 .

[105]  N. Gu,et al.  Manufacture of IRDye800CW-coupled Fe3O4 nanoparticles and their applications in cell labeling and in vivo imaging , 2010, Journal of nanobiotechnology.

[106]  E. Wohlfarth,et al.  A mechanism of magnetic hysteresis in heterogeneous alloys , 1948, Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences.

[107]  E. Paterson The Iron Oxides. Structure, Properties, Reactions, Occurrences and Uses , 1999 .

[108]  B. Scaife,et al.  The measurement of the frequency dependent susceptibility of magnetic colloids , 1988 .

[109]  R. Metselaar,et al.  A consistent interpretation of the magneto-optical spectra of spinel type ferrites( invited) , 1999 .

[110]  Hongchen Gu,et al.  Development of high magnetization Fe3O4/polystyrene/silica nanospheres via combined miniemulsion/emulsion polymerization. , 2006, Journal of the American Chemical Society.

[111]  K. O’Grady,et al.  Effect of the distribution of anisotropy constants on hysteresis losses for magnetic hyperthermia applications , 2013 .

[112]  I. Balberg,et al.  The optical absorption of iron oxides , 1978 .

[113]  N. Bedford,et al.  Engineered multifunctional nanocarriers for cancer diagnosis and therapeutics. , 2011, Small.

[114]  M. Peeters,et al.  The Treatment of Peritoneal Carcinomatosis of Colorectal Cancer with Complete Cytoreductive Surgery and Hyperthermic Intraperitoneal Peroperative Chemotherapy (HIPEC) with Oxaliplatin: A Belgian Multicentre Prospective Phase II Clinical Study , 2012, Annals of Surgical Oncology.

[115]  G. Pauletti,et al.  Rapidly disassembling nanomicelles with disulfide-linked PEG shells for glutathione-mediated intracellular drug delivery. , 2011, Chemical communications.

[116]  J. González,et al.  Transport properties of two finite armchair graphene nanoribbons , 2013, Nanoscale Research Letters.

[117]  Hong Xu,et al.  Fluorescent Polystyrene–Fe3O4 Composite Nanospheres for In Vivo Imaging and Hyperthermia , 2009 .

[118]  R. Amal,et al.  Nanoparticle-protein corona complexes govern the biological fates and functions of nanoparticles. , 2014, Journal of materials chemistry. B.

[119]  Yilong Wang,et al.  Enhanced adsorption of humic acid on amine functionalized magnetic mesoporous composite microspheres , 2012 .

[120]  Kan Wang,et al.  The potential of magnetic nanocluster and dual-functional protein-based strategy for noninvasive detection of HBV surface antibodies. , 2011, The Analyst.

[121]  D. Shieh,et al.  In vivo anti-cancer efficacy of magnetite nanocrystal--based system using locoregional hyperthermia combined with 5-fluorouracil chemotherapy. , 2013, Biomaterials.

[122]  W. Wang,et al.  In vivo Imaging and Drug Storage by Quantum‐Dot‐Conjugated Carbon Nanotubes , 2008 .

[123]  J. Bacri,et al.  Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. , 2007, Journal of the American Chemical Society.

[124]  Susceptibility of the disordered system of fine magnetic particles : a langevin-dynamics study , 2001 .

[125]  M. Respaud Magnetization process of noninteracting ferromagnetic cobalt nanoparticles in the superparamagnetic regime: Deviation from Langevin law , 1999 .

[126]  Zhongqiu Wang,et al.  One-pot facile synthesis of PEGylated superparamagnetic iron oxide nanoparticles for MRI contrast enhancement. , 2014, Materials science & engineering. C, Materials for biological applications.

[127]  Jinhu Yang,et al.  Spinous TiO₂ and Au@TiO₂ octahedral nanocages: amorphisity-to-crystallinity transition-driven surface structural construction and photocatalytic study. , 2014, Journal of colloid and interface science.

[128]  Hong Xu,et al.  Size-independent residual magnetic moments of colloidal Fe3O4-polystyrene nanospheres detected by ac susceptibility measurements , 2008 .

[129]  R Weissleder,et al.  Superparamagnetic iron oxide: pharmacokinetics and toxicity. , 1989, AJR. American journal of roentgenology.

[130]  Hong Xu,et al.  Effect of spatial confinement on magnetic hyperthermia via dipolar interactions in Fe₃O₄ nanoparticles for biomedical applications. , 2014, Materials science & engineering. C, Materials for biological applications.

[131]  Donglu Shi,et al.  Green synthetic, multifunctional hybrid micelles with shell embedded magnetic nanoparticles for theranostic applications. , 2013, ACS applied materials & interfaces.

[132]  L. Néel Some theoretical aspects of rock-magnetism , 1955 .

[133]  G. Goya,et al.  The influence of colloidal parameters on the specific power absorption of PAA-coated magnetite nanoparticles , 2011, Nanoscale research letters.

[134]  N. Usov,et al.  Hysteresis losses in a dense superparamagnetic nanoparticle assembly , 2012 .

[135]  W. Dewey,et al.  Thermal dose determination in cancer therapy. , 1984, International journal of radiation oncology, biology, physics.

[136]  K. Simeonidis,et al.  Size-Dependent Mechanisms in AC Magnetic Hyperthermia Response of Iron-Oxide Nanoparticles , 2012, IEEE Transactions on Magnetics.

[137]  Jon Timmis,et al.  Mechanisms of hyperthermia in magnetic nanoparticles , 2013 .

[138]  V. Banerjee,et al.  Ferromagnetism, hysteresis and enhanced heat dissipation in assemblies of superparamagnetic nanoparticles , 2012 .

[139]  D. Shi Integrated Multifunctional Nanosystems for Medical Diagnosis and Treatment , 2009 .