Abstract
A well-established method for treating cancerous tumors is magnetic hyperthermia, which uses localized heat generated by the relaxation mechanism of magnetic nanoparticles (MNPs) in a high-frequency alternating magnetic field. In this work, we investigate the heating efficiency of cylindrical NiFe MNPs, fabricated by template-assisted pulsed electrodeposition combined with differential chemical etching. The cylindrical geometry of the MNP enables the formation of the triple vortex state, which increases the heat generation efficiency by four times. Using time-dependent calorimetric measurements, the specific absorption rate (SAR) of the MNPs was determined and compared with the numerical calculations from micromagnetic simulations and vibrating sample magnetometer measurements. The magnetization reversal of high aspect ratios MNPs showed higher remanent magnetization and low-field susceptibility leading to higher hysteresis losses, which was reflected in higher experimental and theoretical SAR values. The SAR dependence on magnetic field strength exhibited small SAR values at low magnetic fields and saturates at high magnetic fields, which is correlated to the coercive field of the MNPs and a characteristic feature of ferromagnetic MNPs. The optimization of cylindrical NiFe MNPs will play a pivotal role in producing high heating performance and biocompatible magnetic hyperthermia agents.
Introduction
The applications for magnetic nanoparticles (MNPs) have been extensively researched in biomedical fields, such as magneto-mechanical cell destruction [1,2,3,4], magnetic resonance imaging [5,6,7], drug delivery [8,9,10], and magnetic hyperthermia [11,12,13,14], to compensate for the drawbacks of current diagnosis and therapy methods. The greatest advantage of MNPs is that they can be controlled remotely by an external magnetic field. The resultant magnetic response can be in the form of heat dissipation or magnetic torque, which is dependent on the applied magnetic field configuration and magnetization dynamics of the MNPs [15].
However, different biomedical applications require specific rotation mechanisms in diverse magnetic field configurations. Bio-sensors for cancer bio-markers use magnetic spectroscopy of the MNPs’ Brownian motion to measure the bound fraction and relaxation times of the MNPs within seconds [16]. In magnetic particle imaging for quantifying MNP concentrations, it requires Néel relaxation of the MNPs, while Brownian relaxation, caused by MNPs size distributions, should be minimized [17]. The two mechanisms that exist for the MNPs relaxation processes are Néel and Brownian relaxation, which results in either heat dissipation or spatial rotation of the MNPs. Néel relaxation is correlated to the re-orientation of the MNP magnetic moment to the magnetic field, while Brownian relaxation is correlated to the spatial rotation of the MNP [18,19,20].
Néel (tN) and Brownian (tB) relaxation time are given by:
where η is the viscosity coefficient, t0 is the inverse attempt frequency, K is the magnetic anisotropy constant, V is the volume of MNPs, kB is the Boltzmann constant, and T is the temperature. In principle, the faster mechanism dominates, but both Néel and Brownian mechanisms can occur concurrently, coupled through heat dissipation and magnetic torque [21]. The effective relaxation time (teff) is given by:
In smaller MNPs, the dominant mechanism is Néel relaxation, while for larger MNPs it is Brownian relaxation. In Néel relaxation, the MNP magnetization changes direction due to the reconfiguration of its magnetic moment and is dependent on the MNP size and the temperature. While in Brownian relaxation, the MNPs undergo a spatial rotation and are dependent on external conditions, such as viscosity and chemical binding [22,23,24]. Therefore, it is important to understand the contributions of these magnetic relaxation mechanisms in order to tune and adapt the design of the MNPs to obtain the optimal heat generation for magnetic hyperthermia or magnetic torque for magneto-actuated cell death.
Magnetic hyperthermia is a well-established cancer treatment technique which employs the use of localized heating by MNPs under a high-frequency alternating magnetic field, to induce cancer cell apoptosis and tumor regression [3, 25,26,27]. In an alternating magnetic field, the heat dissipated by the MNPs in one magnetic field cycle equals to the area of the hysteresis loop A, given by:
where M is the magnetization of MNPs, under an alternating magnetic field with frequency f and amplitude μ0Hmax [28,29,30]. To maintain a low MNPs dose and short treatment duration in magnetic hyperthermia, the MNPs heating efficiency must be maximized. The measurement of MNPs heating performance is referred to as specific absorption rate (SAR), which is given by the heat dissipated per unit of mass of MNPs (Wg− 1):
where ρ is the density of MNPs.
The efficiency of heat dissipation of MNPs can be experimentally measured in terms of SAR, which is the energy dissipated per unit of mass of MNPs (Wg− 1), and is given by:
where C is the specific heat of the medium (Cwater = 4.18 Jg− 1 °C− 1), ΔT/Δt is the initial slope of the time against temperature graph, and mMNP is the mass of the MNPs. However, SAR values are not fully representative of the heating efficiency of MNPs as heat dissipation is also influenced by frequency f and magnetic field strength H. Hence, effective specific absorption rate or intrinsic loss power (ILP) is used to characterize the MNPs heating efficiency, given by:
In cylindrical NiFe MNPs, a triple vortex state is formed, in which clockwise and anti-clockwise vortices are connected at the center of the MNP via a third vortex core, resulting in a three-dimensional magnetization configuration. The theoretical heat dissipation from the MNPs for magnetic hyperthermia applications was calculated from the simulated hysteresis loops and vibrating sample magnetometer measurements. Using time-dependent calorimetric measurements, the specific absorption rate and intrinsic loss power of the MNPs were determined and compared with the numerical calculations.
Methods
Fabrication of Magnetic Nanoparticles
Template-assisted pulsed electrodeposition with differential chemical etching is a simple and inexpensive fabrication method to produce MNPs of various compositions, Ni, Fe, or Co. Ni80Fe20, Permalloy, is a ferromagnetic material that displays exceptional magnetic properties such as high permeability, low coercivity, and near-zero magnetostriction. The fabrication of cylindrical MNPs starts by growing compositionally modulated cylindrical NiFe nanowires using anodic aluminum oxide (AAO) template-assisted pulsed electrodeposition in an electrolyte bath consisting of NiSO4, FeSO4, and H3BO3 [31,32,33,34,35]. Subsequently, the nanowires were released by dissolving the AAO template in NaOH. Finally, the Fe-rich regions in the nanowires were chemically etched by diluting HNO3 to form the MNPs. The diameter of the MNPs was determined by the AAO template pore size, while the length was controlled by the high-potential pulse VH duration Additional file 1.
Cell Viability
HeLa cells were seeded into 12-well microtiter plate at 8 × 104 cells/well and incubated in Dulbecco’s Modified Eagle’s medium supplemented with 4.5 g/L glucose, 2 mM L-glutamine, 10% fetal bovine serum, and 1% penicillin/streptomycin in a humidified atmosphere at 37 °C and 5% CO2. The cell viability was determined using PrestoBlue, a permeable resazurin-based cell viability reagent, which uses the reducing power of viable cells to quantitatively measure cell proliferation. HeLa cells treated with 0.1 mg/ml of MNPs were incubated with the PrestoBlue reagent at 37 °C and 5% CO2 for 2 h. The absorbance values at 570 nm and 600 nm were measured by Tecan Infinite M200 PRO Microplate Reader. The cell viability was expressed as a percentage relative to the cells unexposed to the MNPs. Each experiment was performed in quadruplicate sets of experimental and control assays.
Statistical Analysis
The results were represented as the mean ± standard deviation (SD). Statistical significance was analyzed using one-way analysis of variance (ANOVA) with OriginPro, OriginLab. A p value of < 0.05 was considered to be statistically significant.
Micromagnetic Simulations
The magnetization configurations of the MNPs were investigated using a GPU-accelerated micromagnetic simulation program, MuMax3, to solve the Landau–Lifshitz–Gilbert (LLG) equation in three dimensions [36]. These micromagnetic simulations provided insights into the magnetization configurations of the MNP at the microscopic level, which showed the correlation between analytical models and observations from experimental results. The total energy of a system is described by:
where \( {H}_{eff}=-\frac{1}{\mu_0}{\nabla}_ME \). The Landau–Lifshitz–Gilbert (LLG) equation describes the precession of magnetization M in an effective magnetic field Heff with damping α.
where γM(r) × Heff(r) is the precession of M(r) in a local field Heff(r) and \( \frac{\overline{\alpha}}{M_s}M(r)\times \left(M(r)\times {H}_{eff}(r)\right) \) is the empirical damping term. The material parameters for Permalloy Ni80Fe20 were used: saturation magnetization Ms of 860 × 103 A/m, exchange stiffness constant Aex of 1.3 × 10− 11 J/m, zero magneto-crystalline anisotropy k = 0, and Gilbert damping constant α of 0.01. A cell size of 5 nm × 5 nm × 5 nm was used for all simulations, which is sufficiently small as compared with the exchange length.
Experimental Setup for Magnetic Hyperthermia
SAR was experimentally obtained from time-dependent calorimetric measurements by exposing the MNPs to an alternating magnetic field generated by a high-frequency induction heater. MNPs in aqueous suspension with concentrations of 0.05–0.1 mg/ml were poured into a falcon tube, which was insulated by styrofoam and surrounded by the induction coils. The temperature of the coils was maintained at 28.0 ± 0.5 °C by a water recirculating chiller. The initial temperature of the suspension was maintained at 28.0 ± 0.5 °C for 1 min to eliminate any heat contributions from the induction coils. An alternating magnetic field range of 15.9 to 47.8 kAm− 1 and fixed frequency of 360 kHz were applied, within the criterion for clinical magnetic hyperthermia.
Results and Discussion
Characterization of Magnetic Nanoparticles
The composition of the fabricated cylindrical NiFe MNPs is determined by VH or the electrolyte composition. To show the large degree of control in the MNPs composition, various compositions of MNPs have fabricated (Ni88Fe12, Ni76Fe24, Ni52Fe48, and Ni36Fe64) and verified by energy-dispersive X-ray spectroscopy (EDX). Figure 1 shows the normalized hysteresis loop obtained by vibrating sample magnetometer (VSM) measurements for the NiFe MNPs with various compositions. The magnetic field is increased to a value that is sufficient to overcome the effective magnetic anisotropy such that the magnetization reaches saturation. The squareness ratio SQR is a basic measurement of how square the hysteresis loop is, given by:
The values of coercivity Hc and squareness SQR = Mr/Ms for in-plane and out-of-plane applied magnetic fields are tabulated in Table 1. In general, the trend of in-plane Hc is higher than the out-of-plane Hc for Ni-rich MNPs (Ni88Fe12, Ni76Fe24, and Ni52Fe48), but reversed for Fe-rich MNPs (Ni36Fe64), which is in agreement with the previous studies on anomalous co-deposition of NiFe nanowires [37].
Biocompatible Surface Coating
NiFe MNPs tend to aggregate due to the effects of strong dipole interactions between neighboring MNPs. Therefore, the surface modification of the MNPs using biocompatible and biodegradable polymer [38, 39], such as chitosan [40,41,42], polyvinyl alcohol [43,44,45], oleic acid [46,47,48], dextran [49, 50], and most commonly polyethylene glycol (PEG) [51,52,53,54,55,56], has been proposed. PEG is a hydrophilic polymer that has been widely used for improving blood circulation of liposomes and MNPs [57,58,59,60]. To disperse the cylindrical NiFe MNPs into water, a biocompatible 5000 g mol− 1 PEG was used as a stabilizer [61]. The scanning electron microscopy (SEM) image shows the formation of an oxide shell around the MNPs, shown in Fig. 2a. This oxide shell prevents oxidation of the magnetic materials in the MNPs. Previous research works on FeCo MNPs and Fe MNPs have shown severe oxidation from just exposure to the atmosphere [61, 62].
The X-ray diffraction (XRD) pattern peak was mainly indexed at the (111) crystal planes which corresponds to the face-centered cubic (fcc) structure of bulk NiFe, as shown in Fig. 2b. This indicates that the MNPs were electrodeposited with a preferred orientation of (111), which is also evident in NiFe nanowires fabricated by electrodeposition or sputtering [63, 64]. In addition, there was an absence of diffraction peaks corresponding to spinel oxide ((NiFe)3O4), which results from the formation of oxide phases due to the high concentration of Fe [65]. The high crystallinity of the NiFe MNPs led to negligible surface spin canting and hence retained the high saturation magnetization and small coercivity of the MNPs. Further characterizations for the PEG-coated NiFe MNPs were conducted using EDX measurement. As shown in Fig. 2c, mainly of Ni and Fe elements were detected, with the presence of a small percent of O element, an indication of the oxide shell formed around the MNPs.
From Fig. 2d, the cell viability of the HeLa cells exposed to uncoated and PEG-coated NiFe MNPs after 24 h is 82.2% and 82.6%, respectively. After 48 h, the cell viabilities decreased slightly to 79.9% and 82.1%, displaying slightly higher biocompatibility for PEG-coated MNPs. NiFe MNPs without any shells are toxic to mammalian cells and will affect cell viability. The PEG coating was highly biocompatible and can decrease the cytotoxicity and internalization of MNPs into the cells due to endocytosis [66, 67]. The cytotoxicity of the cylindrical NiFe MNPs to HeLa cells is comparable with other commercially available ferromagnetic NPs used in magnetic hyperthermia research [68].
Magnetization Dynamics
The composition of the MNPs was kept at Permalloy Ni80Fe20, while the length (l) and diameter (d) of the MNPs were varied. The exchange energy, demagnetization, or dipolar energy and Zeeman energy contributions to the total energy of the MNP are plotted as a function of applied magnetic field H along the MNP long axis in Fig. 3a–d, respectively. The MNP was first saturated by a strong magnetic field parallel to its long axis. At large magnetic fields, the Zeeman energy contribution predominates and the spins are mostly aligned in the magnetic field direction. This parallel arrangement of the spins to the field minimizes the exchange energy contribution to the total magnetic energy. As the applied magnetic field is reduced, a clockwise and an anti-clockwise vortex nucleation occur at the ends of the MNP, which progress towards the center of the MNP, leading to a gradual reduction of the parallel magnetization component that causes a drop in the Zeeman contribution, while other contributions become increasingly significant. The magnetization of the MNP tries to minimize the stray field, and thus reducing its demagnetization energy. At sufficiently low magnetic fields, the triple vortex state is formed, which is a stable magnetization configuration, with total energy kept at a minimum. As the magnetic field reverses, the sharp drop in exchange energy corresponds to the abrupt splitting of the two vortices.
MNPs with different lengths (l) were found to have significantly different magnetization configurations. At lengths l below 100 nm, only a single vortex was nucleated, which is an in-plane and closed flux domain structure, owing to the interaction between the magnetostatic energy and exchange energy. For l above 100 nm, a pair of anti-clockwise and clockwise vortex cores at the ends of the MNP were nucleated—double vortex state. When the magnetic field decreases, one of the vortex is annihilated, collapsing into the single vortex state. However, at l above 300 nm, there is no annihilation of vortex at low fields, instead an additional third vortex core was nucleated on the curved surface of the MNP—triple vortex state.
Calorimetric Measurements
The Ni80Fe20 MNPs, with l = 500 nm and d = 350 nm, were exposed to an alternating magnetic field of 15.9 to 47.8 kAm−1 (200 to 600 Oe), and the temperature-time curve is displayed in Fig. 4a. As characterized by the SAR equation, the SAR values were calculated to be 427 Wg− 1, 1054 Wg− 1, and 1742 Wg− 1, for 15.9 kAm− 1, 31.9 kAm− 1, and 47.8 kAm− 1, respectively. As predicted, the larger the magnetic field strength, the greater the SAR value, i.e., the SAR value was proportional to the magnetic field strength. Therefore, ILP was obtained to give a better evaluation of the heating efficiency of the MNPs for magnetic hyperthermia. As characterized by the ILP equation, the ILP values were calculated to be 4.69 nHm2kg− 1, 2.88 nHm2kg− 1, and 2.12 nHm2kg− 1, for 15.9 kAm− 1, 31.9 kAm− 1, and 47.8 kAm− 1 at 360 kHz, respectively.
Next, NiFe MNPs, with d = 350 nm and l = 100–500 nm, were exposed to an alternating magnetic field of 47.8 kAm− 1 (600 Oe), and the temperature-time curve is displayed in Fig. 4b. As characterized by the SAR equation, the SAR values were calculated to be 409 Wg− 1, 618 Wg− 1, and 1742 Wg− 1, for l = 100 nm, 200 nm, and 500 nm at 47.8 kAm− 1 and 360 kHz, respectively. As characterized by the ILP equation, the ILP values were calculated to be 0.50 nHm2kg− 1, 0.75 nHm2kg− 1, and 2.12 nHm2kg− 1 for l = 100 nm, 200 nm, and 500 nm at 47.8 kAm− 1 and 360 kHz, respectively.
MNPs with l = 500 nm had far greater heating efficiency than MNPs with l = 100 nm and 200 nm, leading to a more significant temperature rise. The highest SAR value of MNPs with l = 500 nm was 1742 Wg− 1 at 47.8 kAm− 1 and 360 kHz. For comparison, the SAR values for magnetic field of 15.9 to 31.9 kAm− 1 (200 to 400 Oe) and MNPs with d = 350 nm and l = 100–500 nm were tabulated in Fig. 4c. Under the same conditions, the SAR and ILP values of MNPs with l = 500 nm were four times higher than those with MNPs of smaller l. From micromagnetic simulations, it was observed that as l increases to > 300 nm, the magnetization reversal process of the MNP changed from a double vortex state to triple vortex state. At l < 300 nm, only a single vortex state or double vortex state was observed. The remanent magnetization Mr of the MNP was significantly higher for the triple vortex state as compared with the single or double vortex state.
For single domain MNPs, the theoretical model to calculate the dynamic hysteresis loop has been proposed by Carrey et al. [69] For multi-domains MNPs, the use of micromagnetic simulations to obtain static hysteresis loop for calculation was reasonable for MNPs with large sizes, above the critical size for superparamagnetism, as the switching time of the magnetization is in the order of 10− 9 s. Since the switching time of magnetic hyperthermia is in the order ~ 10− 6 s, the large MNPs are able to keep up with the alternating magnetic field. The area of hysteresis loops obtained from micromagnetic simulations of cylindrical NiFe MNPs and VSM measurements was used to theoretically calculate the SAR values and tabulated in Fig. 4d.
The SAR values of MNPs with l = 100 nm and 200 nm displayed a small SAR value at low magnetic fields below Hc and sharply increased until it reaches a saturation at high magnetic fields, which is a characteristic of the ferromagnetic regime. In contrast, the magnetic field dependence of the SAR value of l = 500 nm MNPs, with the triple vortex state, followed a non-linear relationship with SAR values that were ~ 6 times greater. The high remanent magnetization Mr of the triple vortex state in the l = 500 nm MNPs was evident in the non-zero SAR values at low magnetic fields. The comparison between calorimetric measurements (Fig. 4c) and numerical calculations (Fig. 4d) indicates a qualitative and quantitative agreement on the features of MNPs in the ferromagnetic regime, displaying small SAR values at low magnetic fields and saturation at high magnetic fields which was correlated to the Hc of the MNPs.
The heat dissipation of NiFe MNPs with triple vortex states was compared for d = 150–350 nm, under an alternating magnetic field of 47.8 kAm− 1 (600 Oe), and the temperature-time curve is displayed in Fig. 5a. The SAR and ILP values were calculated to be 1785 Wg− 1, 2073 Wg− 1, and 2750 Wg− 1 and 2.17 nHm2kg− 1, 2.52 nHm2kg− 1, and 3.34 nHm2kg− 1, for d = 350 nm, 250 nm, and 150 nm, respectively. The MNPs with d = 150 nm and 250 nm were able to reach the optimal therapeutic temperature of 43 °C in 4.92 min and 7.45 min at concentration of 0.1 mg/ml. Comparing MNPs with different aspect ratios, it was observed that the heating efficiency of d = 150 nm MNPs was 1.54 times greater than d = 350 nm MNPs. This was because MNPs with d = 150 nm possessed the highest low-field susceptibility and Mr. Therefore, the SAR value was closely correlated to the magnetization reversal process of the MNPs with both variations in l and d.
From micromagnetic simulations, it can be observed that the area of hysteresis A evolves significantly with the diameter (d) of the MNP. Therefore, the SAR value of the d = 150 nm MNPs increases so rapidly and saturates at a maximum SAR value of 6263 Wg− 1. The numerical calculations showed that the MNPs with higher aspect ratios have higher hysteresis losses, resulting in higher theoretical SAR values, as shown in Fig. 5b. The comparison between calorimetric measurements (Fig. 5a) and numerical calculations (Fig. 5b) was in good qualitative agreement, but there were quantitative disagreements in the values of hysteresis losses. The mismatch between the experimental and theoretical values arose from the NiFe MNPs being non-superparamagnetic and possessed non-negligible remanent magnetization, leading to unwanted agglomeration due to strong magnetic dipole interactions between neighboring MNPs [70, 71]. Since hydrodynamic volume of MNPs is a component governing the Brownian motion, the extent of aggregation of the MNPs will determine the dominating relaxation mechanism, i.e., Néel or Brownian relaxation. Hence, an aggregated group of MNPs versus a single free MNP will greatly differ in SAR values. Furthermore, an alternating magnetic field can induce nano-columns or nano-chains formation which exhibit dissimilar Brownian relaxation mechanism and hence accounted for the discrepancy between the experimental and theoretical values [72,73,74].
Conclusions
The high SAR values displayed by the cylindrical NiFe MNPs, comparable with iron oxide MNPs (IOMNPs) and superparamagnetic iron oxide nanoparticles (SPIONs) [28, 75], demonstrate the capability of these MNPs in heat dissipation under an alternating magnetic field. MNPs with the triple vortex state had far greater heating efficiency than MNPs with double or single vortex state, which have a SAR value of four times greater, attributed to the high Mr of the MNPs in the triple vortex state. Comparing MNPs with different aspect ratios, it was observed that the heating efficiency of d = 150 nm MNPs was 1.54 times greater than d = 350 nm MNPs due to a larger Mr and low-field susceptibility. Both calorimetric measurements and micromagnetic simulations showed the correlation between the magnetization reversal process and the higher hysteresis losses from d = 150 nm MNPs, resulting in higher experimental and theoretical SAR values. The easy control of the sizes of the MNPs and their magnetic properties indicate great potential for in vivo magnetic hyperthermia cancer therapy trials.
Availability of Data and Materials
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- d :
-
Diameter of magnetic nanoparticles
- EDX:
-
Energy-dispersive X-ray spectroscopy
- H c :
-
Coercivity
- ILP:
-
Intrinsic loss power
- l :
-
Length of magnetic nanoparticles
- MNPs:
-
Magnetic nanoparticles
- M r :
-
Remanent magnetization
- PEG:
-
Polyethylene glycol
- SAR:
-
Specific absorption rate
- SEM:
-
Scanning electron microscopy
- SQR:
-
Squareness ratio
- V H :
-
High-potential electrodeposition pulse
- VSM:
-
Vibrating sample magnetometer
- XRD:
-
X-ray diffraction spectroscopy
References
Kim D-H, Rozhkova EA, Ulasov IV, Bader SD, Rajh T, Lesniak MS et al (2010) Biofunctionalized magnetic-vortex microdiscs for targeted cancer-cell destruction. Nat Mater 9(2):165–171
Chiriac H, Radu E, Țibu M, Stoian G, Ababei G, Lăbușcă L et al (2018) Fe-Cr-Nb-B ferromagnetic particles with shape anisotropy for cancer cell destruction by magneto-mechanical actuation. Sci Rep 8(1):11538
Golovin YI, Gribanovsky SL, Golovin DY, Klyachko NL, Majouga AG, Master АM et al (2015) Towards nanomedicines of the future: remote magneto-mechanical actuation of nanomedicines by alternating magnetic fields. J Control Release 219:43–60
Martínez-Banderas AI, Aires A, Teran FJ, Perez JE, Cadenas JF, Alsharif N et al (2016) Functionalized magnetic nanowires for chemical and magneto-mechanical induction of cancer cell death. Sci Rep 6:35786
Lévy M, Lagarde F, Maraloiu V-A, Blanchin M-G, Gendron F, Wilhelm C et al (2010) Degradability of superparamagnetic nanoparticles in a model of intracellular environment: follow-up of magnetic, structural and chemical properties. Nanotechnology. 21(39):395103
Elias A, Tsourkas A (2009) Imaging circulating cells and lymphoid tissues with iron oxide nanoparticles. ASH Education Program Book 2009(1):720–726
Vitaliano G, Kim J, Mintzopoulos D, Adam C, Vitaliano F, Lukas S et al S262(2018) Novel targeted clathrin-based superparamagnetic iron oxide nanoparticles for CNS magnetic resonance imaging of dopamine transporters. Biol Psychiatry 83(9):S450
Tietze R, Zaloga J, Unterweger H, Lyer S, Friedrich RP, Janko C et al (2015) Magnetic nanoparticle-based drug delivery for cancer therapy. Biochem Biophys Res Commun 468(3):463–470
Chertok B, Moffat BA, David AE, Yu F, Bergemann C, Ross BD et al (2008) Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials 29(4):487–496
Inozemtseva OA, German SV, Navolokin NA, Bucharskaya AB, Maslyakova GN, Gorin DA (2018) Chapter 6 - encapsulated magnetite nanoparticles: preparation and application as multifunctional tool for drug delivery systems. In: Nikolelis DP (ed) Nikoleli G-P, editors. Elsevier, Nanotechnology and Biosensors, pp 175–192
Yang Y, Liu X, Lv Y, Herng TS, Xu X, Xia W et al (2015) Orientation mediated enhancement on magnetic hyperthermia of Fe3O4Nanodisc. Adv Funct Mater 25(5):812–820
Yang Y, Liu X, Yang Y, Xiao W, Li Z, Xue D et al (2013) Synthesis of nonstoichiometric zinc ferrite nanoparticles with extraordinary room temperature magnetism and their diverse applications. J Mater Chem C 1(16):2875
Bellizzi G, Bucci OM (2018) Magnetic nanoparticle hyperthermia. In: Crocco L, Karanasiou I, James ML, Conceição RC (eds) Emerging electromagnetic technologies for brain diseases diagnostics, monitoring and therapy. Springer International Publishing, Cham, pp 129–191
Thiesen B, Jordan A (2008) Clinical applications of magnetic nanoparticles for hyperthermia. Int J Hyperth 24(6):467–474
Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B et al (2011) Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neuro-Oncol 103(2):317–324
Zhang X, Reeves DB, Perreard IM, Kett WC, Griswold KE, Gimi B et al (2013) Molecular sensing with magnetic nanoparticles using magnetic spectroscopy of nanoparticle Brownian motion. Biosens Bioelectron 50:441–446
Reeves DB, Weaver JB (2015) Combined Neel and Brown rotational Langevin dynamics in magnetic particle imaging, sensing, and therapy. Appl Phys Lett 107(22):223106
Dieckhoff J, Eberbeck D, Schilling M, Ludwig F (2016) Magnetic-field dependence of Brownian and Néel relaxation times. J Appl Phys 119(4):043903
Reeves DB, Weaver JB (2015) Combined Néel and Brown rotational Langevin dynamics in magnetic particle imaging, sensing, and therapy. Appl Phys Lett 107(22):223106
Weaver JB, Zhang X, Kuehlert E, Toraya-Brown S, Reeves DB, Perreard IM et al (2013) Quantification of magnetic nanoparticles with low frequency magnetic fields: compensating for relaxation effects. Nanotechnology. 24(32):325502
Mamiya H, Jeyadevan B (2011) Hyperthermic effects of dissipative structures of magnetic nanoparticles in large alternating magnetic fields. Sci Rep 1:157
Adam MR, Eric WH, John BW (2009) Nanoparticle temperature estimation in combined ac and dc magnetic fields. Phys Med Biol 54(19):L51
Rauwerdink AM, Weaver JB (2010) Viscous effects on nanoparticle magnetization harmonics. J Magn Magn Mater 322(6):609–613
Rauwerdink AM, Weaver JB (2010) Measurement of molecular binding using the Brownian motion of magnetic nanoparticle probes. Appl Phys Lett 96(3):033702
Ling Y, Tang X, Wang F, Zhou X, Wang R, Deng L et al (2017) Highly efficient magnetic hyperthermia ablation of tumors using injectable polymethylmethacrylate–Fe3O4. RSC Adv 7(5):2913–2918
Zhang W, Zuo X, Niu Y, Wu C, Wang S, Guan S et al (2017) Novel nanoparticles with Cr3+ substituted ferrite for self-regulating temperature hyperthermia. Nanoscale 9(37):13929–13937
Cabrera D, Lak A, Yoshida T, Materia ME, Ortega D, Ludwig F et al (2017) Unraveling viscosity effects on the hysteresis losses of magnetic nanocubes. Nanoscale 9(16):5094–5101
Hervault A, Thanh NTK (2014) Magnetic nanoparticle-based therapeutic agents for thermo-chemotherapy treatment of cancer. Nanoscale 6(20):11553–11573
Shaterabadi Z, Nabiyouni G, Soleymani M (2017) Physics responsible for heating efficiency and self-controlled temperature rise of magnetic nanoparticles in magnetic hyperthermia therapy. Prog Biophys Mol Biol 133:9–19. https://doi.org/10.1016/j.pbiomolbio.2017.10.001
Delavari H, Hosseini HRM, Wolff M (2013) Modeling of self-controlling hyperthermia based on nickel alloy ferrofluids: proposition of new nanoparticles. J Magn Magn Mater 335:59–63
Gan WL, Chandra Sekhar M, Wong DW, Purnama I, Chiam SY, Wong LM et al (2014) Multi-vortex states in magnetic nanoparticles. Appl Phys Lett 105(15):152405
Wong DW, Chandra Sekhar M, Gan WL, Purnama I, Lew WS (2015) Dynamics of three-dimensional helical domain wall in cylindrical NiFe nanowires. J Appl Phys 117(17):17A747
Wong D, Purnama I, Lim G, Gan W, Murapaka C, Lew W (2016) Current-induced three-dimensional domain wall propagation in cylindrical NiFe nanowires. J Appl Phys 119(15):153902
Wong DW, Gan WL, Liu N, Lew WS (2017) Magneto-actuated cell apoptosis by biaxial pulsed magnetic field. Sci Rep 7(1):10919
Wong DW, Gan WL, Teo YK, Lew WS (2018) Interplay of cell death signaling pathways mediated by alternating magnetic field gradient. Cell Death Dis 4(1):49
Vansteenkiste A, Leliaert J, Dvornik M, Helsen M, Garcia-Sanchez F, Van Waeyenberge B (2014) The design and verification of MuMax3. AIP Adv 4(10):107133
Dragos O, Chiriac H, Lupu N, Grigoras M, Tabakovic I (2016) Anomalous codeposition of fcc NiFe nanowires with 5–55% Fe and their morphology, crystal structure and magnetic properties. J Electrochem Soc 163(3):D83–D94
Rai PK, Lee J, Kailasa SK, Kwon EE, Tsang YF, Ok YS et al (2018) A critical review of ferrate (VI)-based remediation of soil and groundwater. Environ Res 160:420–448
Azzouz A, Kailasa SK, Lee SS, Rascón AJ, Ballesteros E, Zhang M et al (2018) Review of nanomaterials as sorbents in solid-phase extraction for environmental samples. TrAC Trends Anal Chem 108:347–369. https://doi.org/10.1016/j.trac.2018.08.009
Luo L, Zhu L, Xu Y, Shen L, Wang X, Ding Y et al (2011) Hydrogen peroxide biosensor based on horseradish peroxidase immobilized on chitosan-wrapped NiFe2O4 nanoparticles. Microchim Acta 174(1–2):55–61
Luo L, Li Q, Xu Y, Ding Y, Wang X, Deng D et al (2010) Amperometric glucose biosensor based on NiFe2O4 nanoparticles and chitosan. Sensors Actuators B Chem 145(1):293–298
Zhou S, Li Y, Cui F, Jia M, Yang X, Wang Y et al (2014) Development of multifunctional folate-poly (ethylene glycol)-chitosan-coated Fe3O4 nanoparticles for biomedical applications. Macromol Res 22(1):58–66
Rana S, Gallo A, Srivastava R, Misra R (2007) On the suitability of nanocrystalline ferrites as a magnetic carrier for drug delivery: functionalization, conjugation and drug release kinetics. Acta Biomater 3(2):233–242
Sivakumar P, Ramesh R, Ramanand A, Ponnusamy S, Muthamizhchelvan C (2011) Synthesis and characterization of nickel ferrite magnetic nanoparticles. Mater Res Bull 46(12):2208–2211
Sivakumar P, Ramesh R, Ramanand A, Ponnusamy S, Muthamizhchelvan C (2011) Preparation of sheet like polycrystalline NiFe2O4 nanostructure with PVA matrices and their properties. Mater Lett 65(9):1438–1440
Tomitaka A, Koshi T, Hatsugai S, Yamada T, Takemura Y (2011) Magnetic characterization of surface-coated magnetic nanoparticles for biomedical application. J Magn Magn Mater 323(10):1398–1403
Kodama RH, Berkowitz AE, McNiff E Jr, Foner S (1996) Surface spin disorder in NiFe2O4 nanoparticles. Phys Rev Lett 77(2):394
Maaz K, Karim S, Mumtaz A, Hasanain S, Liu J, Duan J (2009) Synthesis and magnetic characterization of nickel ferrite nanoparticles prepared by co-precipitation route. J Magn Magn Mater 321(12):1838–1842
Ayala V, Herrera AP, Latorre-Esteves M, Torres-Lugo M, Rinaldi C (2013) Effect of surface charge on the colloidal stability and in vitro uptake of carboxymethyl dextran-coated iron oxide nanoparticles. J Nanopart Res 15(8):1874
Khot V, Salunkhe A, Thorat N, Ningthoujam R, Pawar S (2013) Induction heating studies of dextran coated MgFe2O4 nanoparticles for magnetic hyperthermia. Dalton Trans 42(4):1249–1258
Phadatare M, Khot V, Salunkhe A, Thorat N, Pawar S (2012) Studies on polyethylene glycol coating on NiFe2O4 nanoparticles for biomedical applications. J Magn Magn Mater 324(5):770–772
Islam MN, Abbas M, Kim C (2013) Synthesis of monodisperse and high moment nickel–iron (NiFe) nanoparticles using modified polyol process. Curr Appl Phys 13(9):2010–2013
Sertkol M, Köseoğlu Y, Baykal A, Kavas H, Başaran A (2009) Synthesis and magnetic characterization of Zn0. 6Ni0. 4Fe2O4 nanoparticles via a polyethylene glycol-assisted hydrothermal route. J Magn Magn Mater 321(3):157–162
Liu XL, Fan HM, Yi JB, Yang Y, Choo ESG, Xue JM et al (2012) Optimization of surface coating on Fe3O4 nanoparticles for high performance magnetic hyperthermia agents. J Mater Chem 22(17):8235–8244
Lee DH, Kang M, Lee HJ, Kim JA, Choi Y-K, Cho H et al (2015) Enhanced cellular uptake of silica-coated magnetite nanoparticles compared with peg-coated ones in stem cells. J Nanosci Nanotechnol 15(8):5512–5519
Jang D-H, Lee Y-I, Kim K-S, Park E-S, Kang S-C, Yoon T-J et al (2013) Induced heat property of polyethyleneglycol-coated iron oxide nanoparticles with dispersion stability for hyperthermia. J Nanosci Nanotechnol 13(9):6098–6102
Yu WW, Chang E, Falkner JC, Zhang J, Al-Somali AM, Sayes CM et al (2007) Forming biocompatible and nonaggregated nanocrystals in water using amphiphilic polymers. J Am Chem Soc 129(10):2871–2879
Sperling RA, Pellegrino T, Li JK, Chang WH, Parak WJ (2006) Electrophoretic separation of nanoparticles with a discrete number of functional groups. Adv Funct Mater 16(7):943–948
Torchilin VP (2005) Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov 4(2):145
Dubertret B, Skourides P, Norris DJ, Noireaux V, Brivanlou AH, Libchaber A (2002) In vivo imaging of quantum dots encapsulated in phospholipid micelles. Science. 298(5599):1759–1762
Abbas M, Islam MN, Rao BP, Ogawa T, Takahashi M, Kim C (2013) One-pot synthesis of high magnetization air-stable FeCo nanoparticles by modified polyol method. Mater Lett 91:326–329
Kura H, Takahashi M, Ogawa T (2010) Synthesis of monodisperse iron nanoparticles with a high saturation magnetization using an Fe (CO) x− Oleylamine reacted precursor. J Phys Chem C 114(13):5835–5838
Salem MS, Sergelius P, Zierold R, Moreno JMM, Görlitz D, Nielsch K (2012) Magnetic characterization of nickel-rich NiFe nanowires grown by pulsed electrodeposition. J Mater Chem 22(17):8549–8557
Nahrwold G, Scholtyssek JM, Motl-Ziegler S, Albrecht O, Merkt U, Meier G (2010) Structural, magnetic, and transport properties of Permalloy for spintronic experiments. J Appl Phys 108(1):013907
Chen Y, Luo X, Yue G-H, Luo X, Peng D-L (2009) Synthesis of iron–nickel nanoparticles via a nonaqueous organometallic route. Mater Chem Phys 113(1):412–416
Gupta AK, Gupta M (2005) Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials. 26(13):1565–1573
Gupta AK, Curtis AS (2004) Lactoferrin and ceruloplasmin derivatized superparamagnetic iron oxide nanoparticles for targeting cell surface receptors. Biomaterials. 25(15):3029–3040
Tomitaka A, Hirukawa A, Yamada T, Morishita S, Takemura Y (2009) Biocompatibility of various ferrite nanoparticles evaluated by in vitro cytotoxicity assays using HeLa cells. J Magn Magn Mater 321(10):1482–1484
Carrey J, Mehdaoui B, Respaud M (2011) Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: application to magnetic hyperthermia optimization. J Appl Phys 109(8):083921
Mehdaoui B, Meffre A, Carrey J, Lachaize S, Lacroix LM, Gougeon M et al (2011) Optimal size of nanoparticles for magnetic hyperthermia: a combined theoretical and experimental study. Adv Funct Mater 21(23):4573–4581
Serantes D, Baldomir D, Martinez-Boubeta C, Simeonidis K, Angelakeris M, Natividad E et al (2010) Influence of dipolar interactions on hyperthermia properties of ferromagnetic particles. J Appl Phys 108(7):073918
Klokkenburg M, Erné BH, Meeldijk JD, Wiedenmann A, Petukhov AV, Dullens RP et al (2006) In situ imaging of field-induced hexagonal columns in magnetite ferrofluids. Phys Rev Lett 97(18):185702
Liu C-M, Guo L, Wang R-M, Deng Y, Xu H-B, Yang S (2004) Magnetic nanochains of metal formed by assembly of small nanoparticles. Chem Commun 23:2726–2727
Mehdaoui B, Meffre A, Lacroix LM, Carrey J, Lachaize S, Gougeon M et al (2010) Large specific absorption rates in the magnetic hyperthermia properties of metallic iron nanocubes. J Magn Magn Mater 322(19):L49–L52
Iacovita C, Stiufiuc R, Radu T, Florea A, Stiufiuc G, Dutu A et al (2015) Polyethylene glycol-mediated synthesis of cubic iron oxide nanoparticles with high heating power. Nanoscale Res Lett 10(1):391
Acknowledgements
The work was supported by the Singapore National Research Foundation, Prime Minister’s Office under an Industry-IHL Partnership Program (NRF2015-IIP001-001). WSL is also a member of the Singapore Spintronics Consortium (SG-SPIN).
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D.W.W. and W.L.G. performed the micromagnetic simulations and calorimetric measurements. D.W.W and Y.K.T. performed the in vitro cell experiments. The project was supervised by W.S.L. All authors discussed the results and contributed to the manuscript. All authors read and approved the final manuscript.
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Wong, D.W., Gan, W.L., Teo, Y.K. et al. Heating Efficiency of Triple Vortex State Cylindrical Magnetic Nanoparticles. Nanoscale Res Lett 14, 376 (2019). https://doi.org/10.1186/s11671-019-3169-6
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DOI: https://doi.org/10.1186/s11671-019-3169-6