Thermally Modified Iron-Inserted Calcium Phosphate for Magnetic

Article Cite This: J. Phys. Chem. B 2019, 123, 5506−5513

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Thermally Modified Iron-Inserted Calcium Phosphate for Magnetic Hyperthermia in an Acceptable Alternating Magnetic Field Baskar Srinivasan,† Elayaraja Kolanthai,‡ Nivethaa Eluppai Asthagiri Kumaraswamy,† Ramana Ramya Jayapalan,# Durga Sankar Vavilapalli,† Luiz Henrique Catalani,‡ Goutam Singh Ningombam,§ Nehru Singh Khundrakpam,§ Nongmaithem Rajmuhon Singh,§ and Subbaraya Narayana Kalkura*,† †

Crystal Growth Centre, Anna University, Chennai, Tamil Nadu 600 025, India Departamento de Química Fundamental, Instituto de Química, University of São Paulo, Av. Prof. Lineu Prestes, 784, São Paulo 05508-000, Brazil # National Centre for Nanosciences and Nanotechnology, University of Madras, Chennai, Tamil Nadu 600 025, India § Department of Chemistry, Manipur University, Canchipur, Manipur 795003, India

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‡

S Supporting Information *

ABSTRACT: Magnetic hyperthermia treatment using calcium phosphate nanoparticles is an evolutionary choice because of its excellent biocompatibility. In the present work, Fe3+ is incorporated into HAp nanoparticles by thermal treatment at various temperatures. Induction heating was examined within the threshold Hf value of 4.58 × 106 kA m−1 s−1 (H is the strength of alternating magnetic field and f is the operating frequency) and sample concentration of 10 mg/mL. The temperature-dependent structural modifications are well correlated with the morphological, surface charge, and magnetic properties. Surface charge changes from +10 mV to −11 mV upon sintering because of the diffusion of iron in the HAp lattice. The saturation magnetization has been achieved by sintering the nanoparticles at 400 and 600 °C, which has led to the specific absorption rate of 12.2 and 37.2 W/g, respectively. Achievement of the hyperthermia temperature (42 °C) within 4 min is significant when compared with the existing magnetic calcium phosphate nanoparticles. The systematic investigation reveals that the HAp nanoparticles partially stabilized with FeOOH and biocompatible α-Fe2O3 exhibit excellent induction heating. In vitro tests confirmed the samples are highly hemocompatible. The importance of the present work lies in HAp nanoparticles exhibiting induction heating without compromising the factors such as Hf value, low sample concentration, and reduced duration of applied field.

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impact on the magnetic properties,9 and it can be modified by incorporating metal ions in it. HAp has an ionocovalent structure, and its anion (phosphate (PO4)3− and hydroxyl (OH−) groups can be replaced by substitution of F−, Cl−, B−, CO32−, and VO43−, and the cation (Ca2+) group can be replaced by metallic ions such as Fe2+, Ni2+, Co2+, Zn2+, Cu2+, Mg2+,Mn2+, Sr2+, Pb2+, and Cd2+,.10 There are also reports on Fe3+ insertion in the HAp lattice other than divalent cations, which demonstrates that temperature can be used as an effective tool to modify the structure and position of dopants in crystal lattice.11 Superparamagnetic iron-doped HAp nanoparticles with improved mechanical and biocompatible properties have been previously reported by our group.12 Magnetic properties were also modified by codoping Fe−Ag13 and Fe−Zn14 in HAp nanoparticles. It is found that

INTRODUCTION In recent years, magnetic nanoparticles are used in biomedical applications such as cell separation, targeted drug delivery, magnetic resonance imaging, and hyperthermia treatment of bone cancers. Synthetic hydroxyapatite (HAp) ((Ca10(PO4)6(OH)2) is widely used as a hard tissue replacement and in drug-delivery applications because of its high biocompatibility,1 osteoconductivity, and osteoinduction properties and also because it possesses a similar chemical structure to bone and teeth.2,3 Further, it is used in protein adsorption,4,5 as coating on implants made of titanium alloys as a thin layer,6 bioimaging,7 and treatment of cancer by magnetic hyperthermia.8 With respect to magnetic hyperthermia treatment, using HAp has attracted much interest despite its biocompatible nature, as the bone material with induction heating ability will be an evolutionary choice. For practical applications, the magnetic properties of HAp have to be modified without rescinding the biocompatibility. The chemical composition and crystal structure have a direct © 2019 American Chemical Society

Received: March 31, 2019 Revised: June 4, 2019 Published: June 5, 2019 5506

DOI: 10.1021/acs.jpcb.9b03015 J. Phys. Chem. B 2019, 123, 5506−5513

Article

The Journal of Physical Chemistry B

wavelength of 488 nm at 50 mW excitation power. The elemental compositions in as-synthesized Fe-doped HAp and samples sintered at various temperatures were analyzed using inductively coupled plasma-optical emission spectrometer (ICP-OES, Spectro Arcos instrument). The magnetic measurements of Fe-doped HAp and samples sintered at various temperatures were carried out by a vibrating sample magnetometer (VSM, Lakeshore VSM 7407) at room temperature. The particle size and surface morphology of the samples were examined using a field emission scanning electron microscope (FESEM, SUPRA 55 CARL ZEISS, Germany). Selected area electron diffraction (SAED) patterns were obtained using a high-resolution transmission electron microscope (HRTEM, FEI Tecnai TF-20 operating at 200 kV). Further, particle-size distribution and zeta potential of as-synthesized and sintered Fe-doped HAp were examined by dynamic light scattering (DLS, Malvern Zetasizer Nano-ZS) technique. The source of He−Ne diode laser with a wavelength of 633 nm was used to scatter the particles at a fixed angle of 90° at room temperature. Less than 1 mg of powder sample was dispersed in deionized water using a probe sonicator for 1 h. After sonication, the particle-dispersed (1.5 mL) solution was carefully transferred to a Malvern universal cell cuvette, and then the experiment was performed in triplicates. Induction Heating Measurement. The measurements of the induction heating ability of the nanoparticles were performed using Easy Heat 8310, Ambrell, U.K. The experimental procedure was followed from our previous report.20 The sample was heated using a current of 300 A up to 10 min (600 s), and 10 mg of the sample is dispersed in 1 mL of deionized water for the study. The resultant magnetic field (H) generated due to the applied current (i) was calculated by the following relation:

saturation magnetization (Ms) and retentivity (Mr) increases with increase in iron concentration. Iron doping in HAp has a great impact on physicochemical and biological properties, facilitating its use in various biomedical applications. Fe3+ and Fe2+ in HAp with Fe3O4 as a secondary phase exhibited induction heating.8 Efforts have been made to attain induction heating on calcium-phosphate-based materials for magnetic hyperthermia treatment of cancer. Magnetism has been induced, without altering the structure of β-tri calcium phosphate by incorporating iron and iron codoped cobalt and nickel into it, which exhibited induction heating.15−17 Since CaP-based materials with induction heating ability are very few, improvements are still needed for optimizing the factors like sample concentration, limit of magnetic field (H), frequency of applied ac magnetic field (f), and the duration of magnetic field required for the rise in temperature. Cancer cell destruction also depends on the quantity of nanoparticles and the duration of the applied field.18 The threshold limit of Hf value for clinical applications is 5 × 106 kA m−1 s−1.19 In the present work, iron-incorporated HAp nanoparticles synthesized by a wet precipitation technique were subsequently subjected to ultrasound and microwave irradiation. The obtained samples were sintered at various temperatures for modifying the structural and magnetic properties.11 Induction heating ability of the nanoparticles within the limit of Hf value and blood compatibility of the samples have been evaluated.

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EXPERIMENTAL METHOD Materials. Calcium nitrate tetrahydrate (Ca(NO3)2 4H2O, Merck), diammonium hydrogen phosphate ((NH4)2HPO4, Fisher Scientific), ferric chloride (FeCl3, Fisher Scientific), and ammonia solution (analytical grade) all having >99% purity were used for this experiment. All the experiments were performed using triple distilled water. Nanoparticle Synthesis. First, 1 M of calcium nitrate tetrahydrate along with 0.5 M of ferric chloride solutions were added dropwise into a 0.6 M diammonium hydrogen phosphate solution. The mixture was constantly stirred for 3 h, and the pH of the solution was maintained at 10 using ammonia solution throughout the reaction. Then the mixture was subjected to ultrasound for 1 h, (Sonics-Vibra Cell VCX750,750W) using a probe ultrasonicator. Subsequently, the mixture was subjected to microwave irradiation (household microwave oven, 900 W and 2.45 GHz) for a period of 30 min. Then the precipitate was washed using deionized water, centrifuged, and dried at 70 °C using a hot air oven. The obtained 0.5 M Fe-doped HAp nanoparticles were kept as control and further sintered at 200, 400, 600, 800, and 1000 °C for 2 h with a heating rate of 3.5 °C per min using a box furnace. Hereafter, the samples of 0.5 M Fe-doped HAp, sintered at 200, 400, 600, 800, and 1000 °C will be represented as Fe-0.5M, Fe-200, Fe-400, Fe-600, Fe-800, and Fe-1000, respectively. Characterization. Powder X-ray diffraction studies have been carried out using PANalytical X’Pert Powder XRD System Cu Kα radiation (0.154 nm) with a step size of 0.02° in the 2θ range of 10° to 80°. The functional groups of all the samples are identified using a Jasco Fourier transform infrared spectrometer (FTIR-6300) with the KBr pellet technique of wavenumber between 4000−400 cm−1 in transmission mode (64 scans for each samples). The Raman spectrum of all the samples are recorded in the LabRam-HR 800 Raman spectrometer equipped using an argon ion laser source

H=

1.257ni (in Oe) D

where n is the number of turns in the coil and D is the diameter of the turn in cm. The temperature of the system, where the sample was kept in the center of the coil was recorded using an optical temperature sensor (Photon R&D, Canada) with the accuracy of ±0.01 °C. AC field having a frequency (f) and magnetic field (H) is applied to the samples. In this work, f = 242 kHz was used to correspond to the measurement window time of 4.1× 10−6 s. The copper (Cu) coil labeled as C76 which has a diameter (D) of 7 cm, 6 numbers of turns (n), and its operating frequency (f) is 242 kHz can generate a field of Hf = 4.58 × 106 kA m−1 s−1. Blood Compatibility. Human blood was collected and immediately transferred to heparin coated tubes. The blood was consequently diluted with saline solution in order to bring UV−vis absorbance to one. Then the samples were added to 250 μL of the diluted blood. The samples were incubated for 20 min, which was followed by the addition of 2 mL of saline. This was left undisturbed for 1 h. Diluted blood along with 2 mL of saline in the absence of sample served as negative control. Diluted blood with deionized water served as positive control. The supernatant is collected after centrifugation, and the absorbance is measured using Jasco V-760 UV−visible spectrometer at 545 nm.21 Percentage of hemolysis is calculated using the formula 5507


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peaks of β-tcp are in good agreement with the standard JCPDS value (09-0169). Raman Spectroscopic Analysis. Raman spectrum of the samples is shown in Figure 2. The bands at 964 and 1124 cm−1

%hemolysis = OD for the test sample − OD for the negative control OD for the positive control − OD for the negative control

The calculated percentages of hemolysis for all the samples were compared with ASTM standard as highly hemocompatible (20% hemolysis).

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RESULTS AND DISCUSSION Powder X-ray Diffraction Analysis. Powder X-ray diffraction (XRD) patterns of the samples are shown in Figure 1. The peaks obtained from the XRD pattern for the control

Figure 2. Raman spectra of the samples synthesized at different temperatures.

correspond to the symmetric and asymmetric stretching modes of P−O respectively. The bands at 221, 246, 288, 407, 601, and 1301 cm−1 correspond to α-Fe2O3, and the band at 710 cm−1 corresponds to FeOOH.22−24 The control sample and Fe-200 contain P−O and α-Fe2O3 bands, whereas the XRD pattern reveals only HAp peaks. For Fe-400, the bands corresponding to P−O and FeOOH are present, and the XRD pattern reveals peak broadening and splitting of (211) plane, which confirms the interaction of iron with the hydroxyl group in HAp lattice. For Fe-600, the bands corresponding to HAp, α-Fe2O3, and FeOOH exist. The presence of α-Fe2O3 is also evident from the XRD analysis, confirming the occurrence of structural distortions. For Fe-800 and Fe-1000, bands corresponding to HAp and α-Fe2O3 exist, and the domination of hematite can also be seen from XRD analysis. At higher temperatures, FeOOH dehydrates and stabilizes in the form of hematite.25 A decrease in the intensity of the P−O bands on increasing the sintering temperature from 200 °C confirms the incorporation of iron in the HAp structure. The decrease in intensity and slight broadening of P−O bands for Fe-800 and Fe-1000 is due to the partial conversion of HAp to β-tcp.26,27

Figure 1. Powder X-ray diffraction pattern of the samples synthesized at different temperatures.

sample (Fe-0.5M) match well with the standard JCPDS (090432) pattern of HAp with a small decrease in lattice parameters. Sintering at 200 °C leads to an increase in the lattice parameter along the a-axis (Figure S1). At 400 °C, peak broadening occurs with the splitting of the major plane (211) along with a slight increase in the c axis (Figure 1 and S1 (Fe400)), indicating the structural distortion due to the diffusion of iron in HAp lattice. On sintering at 600 °C and above the presence of α-Fe2O3 (Hematite) is detected, the peaks of which match exactly with the JCPDS (33-0664) pattern of αFe2O3. Formation of small amount of β-tcp also occurs at 800 °C along with the dominant α-Fe2O3 phase. These crystalline 5508


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Figure 3. FESEM images of the samples synthesized at different temperatures.

Figure 4. High-resolution transmission electron microscopy of Fe-600. (a) Image. (b) Fringes. (c) SAED pattern.

present case, Fe3+ is coordinated along the inner axis for charge compensation. Fe3+ can be easily accommodated in the interstitial site of HAp because of its small ionic radii. The CO32− is prominently observed for Fe-0.5 M, and it is gradually reduced on increasing the sintering temperature (Figure S2). During sintering, Fe3+ diffuses into the HAp lattice and stabilizes in the form of FeOOH up to 400 °C. At 600 °C, dehydration of FeOOH takes place, and thus, partial stabilization of α-Fe2O3 occurs in HAp. At 800 and 1000 °C, FeOOH completely dehydrates, and thus, α-Fe2O3 is alone observed from XRD and Raman analyses. At higher temperatures, a band corresponding to CO2 at 2350 cm−1 is present, whereas bands corresponding to O−H at 1635 and 3400 cm−1

Inductively Coupled Plasma Optical Emission Spectroscopy (ICP-OES). The calculated Ca/P ratio for all the samples is 2.1 (Table S1), but for stoichiometric HAp it is 1.67. The increase in the ratio is due to the presence of carbonates in the HAp structure. The bands corresponding to carbonate are also observed in the FT-IR spectra at 876, 1421, 1458, and 1485 cm−128,29 (Figure S2). The carbonates are formed when CO2 from the atmosphere reacts with high pH solutions. The formation of carbonates is advantageous as 5 to 8 wt % of carbonate is found in natural bone. The presence of a phosphorus deficiency confirms the formation of B-type carbonate in the lattice.30 The presence of CO32− at PO43− in HAp removes Ca2+ for charge compensation, but in the 5509


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Figure 5. Room-temperature M−H curve of the samples sintered at different temperatures.

major plane (211) of HAp, and the SAED pattern also shows the planes corresponding to HAp (Figure 4b,c), which are well matched with the XRD pattern. Magnetic Study. The room-temperature M−H plot is shown in Figure 5. The magnetization values are less for Fe-0.5 M and Fe-200, and the loop indicates the paramagnetic property of the samples. For Fe-400 and Fe-600, magnetization is comparatively high, and saturation magnetization also occurs. The retentivity Mr for Fe-400 and Fe-600 is 4 and 6 memu/g, respectively. The coercivity Hc for Fe-400 and Fe600 is 300 and 347 G, respectively. The retentivity Mr for Fe800 and Fe-1000 are 0.4 and 0.7 memu/g, and the coercivity Hc is 1790 and 2835 G, respectively. The variations in magnetization Mr and Hc can be correlated with the structural properties of the samples. The magnetization gets saturated, and the coercivity is lowered for the samples containing FeOOH (Fe-400 and Fe-600) because it is superparamagnetic in nature. Agglomerates of spherical nanoparticles are observed from the FESEM micrograph, which is responsible for the existence of coercivity. The behavior of the magnetic transitions in nanoparticles is also due to the size effect.35,36 The magnetization is comparatively high for Fe-600, wherein FeOOH and α-Fe2O3 is partially stabilized in the HAp structure.

(Figure S2) are absent. This confirms that the coordination of iron with the carbonates has led to the formation of CO2 at higher temperatures. The bond energies of CO32− with Ca2+ is weaker than the PO43−; therefore, Fe3+ can be more easily located along the inner channel. According to Mayer et al., Fe3+ stabilizes in the form of FeOOH in the carbonated apatite.31 While sintering HAp in air, iron stabilizes in the form of hematite in HAp leading to a variation in lattice parameter, which has been reported.32 Morphological Analysis. FESEM micrographs of the samples are shown in Figure 3. The control sample (Fe-0.5M) shows irregular agglomerated spherical particles. An increase in the lattice parameter along the a axis on sintering at 200 °C, as discussed in the XRD analysis, leads to the texturing of the samples. At 400 and 600 °C, individual nanoparticles forming clusters of average size 300 nm has been observed. For Fe-800 and Fe-1000, irregular particles of larger size can be seen due to the diffusion of iron, leading to the phase change. During sintering, crystallization occurs by diffusion of ions from the surface into the lattice, which is dependent on temperature,33 and the diffused iron in HAp stabilizes in the form of hematite.34 The average size of Fe-600 is less than 50 nm as observed from the HRTEM image (Figure 4a). The fringe width was calculated as 0.29 nm, which corresponds to the 5510


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hyperthermia treatment.18,19 The existing CaP-based nanoparticles in colloidal suspensions require a comparatively much sample concentration and time to attain the hyperthermia temperature.15−17 The systematic investigation of iron incorporation reveals that FeOOH and α-Fe2O3 in HAp structure exhibits better induction heating. Iron oxide in the form of Fe3O4, embedded in HAp, exhibits good induction heating,39,40 but achievement of induction heating in α-Fe2O3 has more advantage than Fe3O4 because of its high biocompatibilty. α-Fe2O3 is the most stable phase among the iron oxides and is also less toxic. The high metabolic activity of α-Fe2O3 in HAp when compared to Fe3O4 in HAp has been proven by cell viability tests.41 In Vitro Hemocompatibility. The hemolysis percentage values obtained for various samples are shown in Figure S5. All the samples show less than 4% cell death, which reveals the highly hemocompatible nature of the samples. The cell death percentage for Fe-800 and Fe-1000 are comparatively higher than other samples, which may be due to α-Fe2O3 being dominantly observed than HAp from XRD and Raman analysis.

DLS and Zeta Potential. Particle-size distributions of the nanoparticles are shown in Figure S4. The size of the agglomerates of fine nanoparticles from FESEM reflects the hydrodynamic size obtained from DLS. The hydrodynamic diameter of the nanoparticles agrees well with the results from FESEM micrograph. The zeta potential value of the samples dispersed in water is shown in Figure S5. The control sample acquires a zeta potential of +10 mV, and during sintering, iron enters into the HAp and causes structural defects, leading to the negative surface charge. The surface charge turns to negative for Fe-400, affirming the interaction of Fe3+ in HAp, which is evidenced as a peak splitting in the XRD pattern. Zeta potential determines the colloidal stability, and relatively high colloidal stability is obtained for Fe-600 which is −11 mV. The surface charge of the nanoparticles has a direct impact on protein adsorption37 and interaction with polymers38 for synthesizing composite materials. Induction Heating Studies. Induction heating of the nanoparticles is examined with Hf field strength of 4.58 × 106 kA m−1 s−1, which is in the limit for therapeutic applications. The detailed information about the procedure is followed from our previous report.20 The sample concentration of 10 mg/mL is dispersed in water, and the duration of field is fixed at a maximum of 600 s. The samples Fe-400 and Fe-600 only exhibit induction heating at respective temperature of 35.8 and

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CONCLUSIONS The Fe3+ incorporation in HAp at various sintering temperature is systematically investigated. Iron in HAp alters the lattice parameters on both the axes. The presence of FeOOH and α-Fe2O3 in HAp is temperature-dependent and it is confirmed from the XRD and Raman studies. Surface charge of the nanoparticles turns to negative upon sintering. The saturation magnetization and low coercivity are obtained for the samples sintered at intermediate temperatures (400 and 600 °C). The induction heating tests were performed for the nanoparticles with an acceptable Hf field strength, and the temperature reaches a maximum of 48 °C in 10 min. The partial stabilization of FeOOH and α-Fe2O3 in carbonated HAp structure gives rise to better induction heating efficiency when compared with the already existing magnetic calcium phosphate nanoparticles. The samples are highly hemocompatible, and hence, the nanoparticles can be considered as a potential material for magnetic hyperthermia treatment.

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Figure 6. Induction heating (temperature versus time) profile of the Fe-HAp (Fe-400 and Fe-600) nanoparticles for 10 mg/mL concentration and magnetic field strength of Hf = 4.58 × 106 kA m−1s−1.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.9b03015. Variation in lattice parameter along a and c axis of FeHAp on sintering at different temperatures; presence of Ca, P, and Fe quantified using inductively coupled plasma optical emission spectroscopy; FT-IR spectra of the samples; particle-size distribution shows the hydrodynamic diameter of the nanoparticles; zeta potential of the samples showing variation upon sintering; and hemocompatibility of the samples (PDF)

48.7 °C (Figure 6). The specific absorption rate (SAR) of the samples is calculated by using the following relation. ΔT 1 W/g Δt m where C is the specific heat of water (4.18 J g1− K−1 mol−1), m is the mass of the iron inserted HAp per total amount of iron inserted HAp + water, and ΔT/Δt is the initial slope of the temperature versus time plot. The SAR values for the Fe-400 and Fe-600 are 12.2 and 37.2 W/g, respectively. The hyperthermia temperature for Fe-600 is attained in 210 s. The induction heating result substantiates with the magnetic properties such as saturation magnetization and also a comparatively low coercivity. The hyperthermia temperature is achieved in HAp at an acceptable Hf value, optimum sample concentration, and reduced duration of ac magnetic field, thus imparting a great advantage for magnetic SAR = C

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel.: 91-44-22358335. ORCID

Subbaraya Narayana Kalkura: 0000-0001-5777-2907 Notes

The authors declare no competing financial interest. 5511


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ACKNOWLEDGMENTS We acknowledge Department of Biotechnology (DBT), New Delhi for the sanction of project [no. (BT/515/NE/TBP/ 2013), dated: 11.12.2014]. The authors E.K. and L.H.C. acknowledge Fundaçaõ de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Brazil for the award of thematic project and postdoctoral fellowship (Grant for fellowship file No.: 2011/21442-6 and 2015/19694-8).

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Thermally Modified Iron-Inserted Calcium Phosphate for Magnetic

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