BaO–Fe2O3 containing bioactive glasses

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BaO–Fe2O3 containing bioactive glasses: A potential candidate for cancer hyperthermia

Article in Materials Chemistry and Physics · November 2019

DOI: 10.1016/j.matchemphys.2019.122439

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Materials Chemistry and Physics 241 (2020) 122439

Available online 8 November 2019

BaO – Fe ₂ O ₃ containing bioactive glasses: A potential candidate for cancer hyperthermia

D. Bizari

^a^,^*

, A. Yazdanpanah

^b

, F. Moztarzadeh

^b

aTrauma Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran

bBiomaterials Group, Faculty of Biomedical Engineering (Center of Excellence), Amirkabir University of Technology, P.O. Box 15875-4413, Tehran, Iran

H I G H L I G H T S

�Synthesis of CaO/P2O5/SiO2/BaO/Fe2O3 magnetic bioactive glasses.

�The narrow distribution of particle sizes between 30 and 70 nm.

�Addition of BaO–Fe2O3 generate enough heat for application of these materials in cancer hyperthermia.

�These materials suggested as new magnetic and bioactive biomaterials for cancer treatment with hyperthermia.

A R T I C L E I N F O Keywords:

Bioactive glass Hyperthermia Barium–iron Magnetic properties

A B S T R A C T

A series of BaO–Fe2O3 bioactive glasses synthesized with the sol-gel technique. In this research, the magnetic properties of prepared bioactive glass were examined to study the potential application of these materials in cancer hyperthermia. To this goal, physical, morphological and, magnetic behavior of synthesized magnetic bioactive glass, were examined. Scanning Electron Microscopy, X-ray Powder Diffraction, and also Transmission Electron Microscopy used to characterize the composition and morphology of the glass nanoparticles. The size of glass particles studied by Laser Particle Size Analyzer (LPSA). Thermal analysis was used to determine the final heat treatment temperature via Differential Thermal Analysis (DTA). To evaluate the magnetic properties of synthesized glasses, Vibrating Sample Magnetometer, and Calorimetric test used.

The results of this research showed that BaO–Fe2O3 addition in the glass structure affects the magnetic behavior of the bioactive glass. VSM (Vibrating Sample Magnetometer) and calorimetric test results prove that the magnetic behavior of the glasses increases with the increase of magnetic content. Results showed that BG1010 and BG0515 generate enough heat for the application of these materials in cancer hyperthermia.

Considering Cytocompatibility, Bioactivity, and magnetic properties, it seems the BG1010 sample is the best candidate to use in hyperthermia treatments. Finally, this study proves that the prepared bioactive glasses with magnetic content are good candidates in cancer hyperthermia applications.

1. Introduction

The application of small particles in the AC magnetic field for cancer hyperthermia started in the late 1950s. Three decades later, a specific absorption rate (SAR) of colloidal dispersions of superparamagnetic iron oxide nanoparticles was found to be significantly higher at clinically acceptable mixtures comparing larger multi-domain particles. The mentioned phenomenon was a surprise in this technique, and it has attracted lots of attention in the last few years [1–4]. Researchers extensively used the ferromagnetic materials in the hyperthermia

technique as an alternative method to eradicate cancer cells, specifically deep-seated cancers such as bone tumors [5]. Once granular seeds of glass-ceramics are implanted in the vicinity of tumors, and they exposed to alternating magnetic fields, the produced heat from magnetic loss will kill the tumors. Most often, the induced temperature is between 42 and 45 ^�C in which healthy tissue survives [6,7].

In 1983 for the first time, Luderer et al. [8] utilized the ferrimagnetic glass-ceramic as a thermoseed for use in the hyperthermia technique.

Their glass-ceramic contained lithium ferrite (LiFe5O8) and hematite (Fe2O3) crystallites in the system Al2O3–SiO2–P2O5, but, was not

* Corresponding author.

E-mail addresses: [email protected], [email protected] (D. Bizari).

Contents lists available at ScienceDirect

Materials Chemistry and Physics

journal homepage: www.elsevier.com/locate/matchemphys

https://doi.org/10.1016/j.matchemphys.2019.122439

Received 14 June 2019; Received in revised form 3 November 2019; Accepted 7 November 2019

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Materials Chemistry and Physics 241 (2020) 122439

2 bioactive. Besides, the heat generation of the materials was not sufficient to destroy the malignant carcinoma [8]. So, ferrimagnetic thermoseeds must exhibit higher heat-generating capacity. Magnetite (Fe3O4) is a well-known ferrimagnetic material and also used for the synthesis of magnetite-containing glass ceramics, which had been previously reported by several researchers [9,10]. Later, Ebisawa et al. in 1991 synthesized another non-bioactive ferrimagnetic glass-ceramic with Fe3O4

in a matrix of CaO.SiO2-based glass [11]. The magnetic properties of this glass-ceramic arise from magnetite crystallized from hematite present in the glass during heat treatment [11]. In their next study [12], they proved that ferrimagnetic Fe2O3-containing CaO–SiO2 glass-ceramics could show bioactivity if small amounts of Na2O, B2O3, and P2O5

added to the composition of the parent glass [12]. In another work [13], this group investigates in vitro bioactivities of ferrimagnetic glass-ceramics with the compositions 60CaOSiO₂-40(FeO, Fe₂O₃) added with 3Na2O, 3B2O3, and 3P2O5 in weight ratio. They found that glass-ceramics with Na2O or B2O3 added in combination with P2O5 show bioactivity [13]. It is clear from the results that glass-ceramics of the system FeO–Fe2O3–CaO–SiO2 indeed do show bioactivity as well as ferrimagnetism, achieved through small addition of certain oxides [13].

More magnetic bioactive glass-ceramics based on CaO–SiO₂glasses, which contain iron oxide were reported since [14–16].

In the study by Leenakul et al. [17], ferrimagnetic bioactive glass-ceramics were synthesized in the system of BaFe12O19(BG) SiO2

CaO Na2O P2O5 using the incorporation method [17]. They detected sodium calcium silicate and barium iron oxide in all of their samples [17]. The magnetic hysteresis loops of their glasses showed that the Ms (saturation magnetization) enhanced with BG contents increase in the glass structure. Alternatively, the results showed that the coercivity of the samples decreases as the BG content of the glasses increase. This phenomenon occurs because of the multi-domain structure of the BG crystalline structure.

Furthermore, the results proved that with an alternating magnetic field (�10 kOe), the increase of BG from 5 wt % to 40 wt % caused a rise in the area of the hysteresis loops [17]. The In-vitro bioactivity tests in simulated body fluid proved that all of the prepared samples are bioactive. Also, they reported an increase in the bioactivity of the glasses as the BG content of the glasses increase [17]. Therefore, they concluded that the addition of BaFe12O19 to 45s5 glasses enhanced both the magnetic and bioactivity of these glasses [17].

In this research, we prepared a new BaO–Fe2O3 containing BG using the sol-gel technique. We reported the effect of magnetic content on structural, physical features, and bioactivity of the BGs in our previous paper [18]. The results proved that the BaO–Fe₂O₃addition in the BG structure caused several changes in glass behavior. Results also showed different apatite morphologies on the bioactive glass surfaces. The Fe2O3

content harms bioactivity, but the BaO content increased the bioactivity of the samples. However, all of the BGs are extremely bioactive. It also demonstrated that the BGs are highly biocompatible. In this paper, to demonstrate the potential of these nanoparticles to be used as thermoseeds of cancer hyperthermia, we studied the magnetic properties of obtained glasses.

2. Experimental

2.1. Preparation of magnetic bioactive glasses

Bioactive glasses (60% (SiO2, Fe2O3, and BaO), 36% CaO, and 4%

P2O5 (mol %) prepared with the sol-gel approach. The procedure of synthesis is reported before in Ref. [18]. Briefly, the diluted HNO₃, the water solution of Tetraethylorthosilicate (TEOS, Sigma Aldrich), and triethyl phosphate (TEP, Sigma Aldrich) mixed for 1 h. Then, barium chloride, iron nitrate, and calcium nitrate (based on BG composition) introduced to the mixture. The achieved sol aged for seven days. The samples then dried at 70 and 140 ^�C for one day. Lastly, all samples synthesized at 700 ^�C for 2 h. Glass composition and their contents listed

in Table 1.

2.2. Characterization of magnetic bioactive glasses (MBG) 2.2.1. Physical properties of MBG

In this study, we used DTA analysis (A Netzsch STA 409 PC/PG) to determine the proper temperature for thermal treatment. The magnetic BGs also studied using the XRD analysis with Siemens-Brucker D5000 diffractometer and Fourier Transform Infrared (FTIR) spectroscopy. The particle size and the morphology of the synthesized nanoparticles are examined using Laser Particle Size Analyzer (LPSA, Coulter LS 230, Coulter Electronics, USA), Scanning Electron Microscope (SEM-Philips XL30) and also Transmission Electron Microscopy (TEM, Philips CM120).

2.2.2. Magnetic properties evaluations

2.2.2.1. Vibrating sample magnetometer (VSM). Vibrating sample magnetometer (VSM: Lake Shore, Model 7404) at the field range of 10000 (Oe) to 10000 (Oe) at room temperature (25 ^�C) used to characterize the magnetic properties of the magnetic bioactive glasses.

2.2.2.2. Calorimetric test. To study the heating ability of the synthesized magnetic bioactive glasses, they were exposed to calorimetric measurements by an alternate magnetic field to detect the temperature variations of a water suspension of samples. The experiment conducted with an induction coil producing a magnetic field with the intensity between 0 and 50 mT at the 300 kHz frequency. Each glass composition (BG010, BG1010, BG0515, and BG100) samples put in the container.

The powders suspended in 10 ml of distilled water using PVA (polyvinyl alcohol) as a stabilizer. After that, the samples put in the middle of the coils of the inductor, and then an alternative magnetic field was applied to the samples. The temperature was monitored using an IR temperature sensor.

2.2.2.3. Statistical analysis. The experiments conducted in the fifth replicate. The experiment results provided as means, standard error (SE). Statistical analysis carried out by using a one-way ANOVA and Tukey test with significance reported if P <0.05. As for normalizing group study, the Kolmogorov–Smirnov test method used.

3. Results and discussions 3.1. DTA characterization

Fig. 1a displays the DTA results of the BG. The DTA result showed several endothermic and exothermic peaks. The first endothermic peak begins at room temperature, which relates to the water release and the evaporation of the polycondensation reaction by-products. The first exothermic, which is between 250 and 350 ^�C, is related to the burning of the surfactants. The second endothermic peak between 450 and 650 ^�C is because of the silanol condensation and the nitrate removal from the structure. The result of the DTA trace proves that the BG structure transformed at higher temperatures. The results prove that the glass transition temperature (TG) is amid 800 to 900 ^�C. The last peak relates to the crystallization of the BG. The BG crystallization Table 1

Chemical content and sample numbers of different MBG.

Sample Number Fe2O3 P2O5 CaO BaO SiO2

BG 00 0 4 36 0 60

BG 100 0 4 36 10 50

BG 010 10 4 36 0 50

BG 1010 10 4 36 10 40

BG 0515 15 4 36 5 40

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temperature, Tc, is between 890 and 900 ^�C. According to the DTA results, there is no significant weight loss beyond 700 ^�C. The results also proved that the residuals and by-products removed under 700 ^�C.

Therefore 700 ^�C is a proper temperature for the final heat treatment and stabilization of the glasses.

3.2. FTIR spectra of MBG

The FTIR spectra of magnetic bioactive glasses showed in Fig. 1b.

Most absorption bands around 460 cm ¹were related to the Si–O–Si bending vibration mode and symmetric stretching of the Si–O–Si band, respectively. The absorption band located at (1000–1200) cm ¹attributed to Si–O–Si asymmetric stretching in the SiO4 group [14,18–20].

The peaks around 1639 cm ¹-1648cm ¹confirmed the bending vibration modes of water (O–H) groups [14,18,19]. The band observed at 569 cm ¹in Fe BG, Ba BG, and BaFe BG was related to metal-oxygen (metal-O) bond, which could confirm the formation of magnetic iron oxide (Fe–O) or (Ba–O) [21]. These peaks prove the existence of the ferrite in the glass composition. Additionally, the absorption bands at 3550 cm ¹were attributed to –OH group and confirmed the formation of silanol groups on the surface of glasses groups [22]. Finally, the IR data confirmed the possibility of the formation of a silica framework (glass) [14,18].

3.3. Size analysis of MBG

In this study, the LPSA was used to characterize the size distribution of the glass particles. The result of the LPSA showed in Fig. 2a. The size of synthesized glass nanoparticles is mostly 30–70 nm, and the Particles’

Average Xsv ¼D [2,3] is 0.045 μm.

As shown in Fig. 2a, particles have a fine size distribution, and therefore no size scattering is detected. Synthesized glass nanoparticles are mono-dispersed and homogenous. The particle sizes and also the particle size distributions play an essential role in the magnetic features of the final product.

3.4. TEM results of MBG

The TEM micrograph of the synthesized glass particles showed in Fig. 2b. Particle morphology of the nanoparticles are nearly elliptical, and the size of the nanoparticles is in 40–70 nm range.

It must be mentioned that the magnetic nanoparticles have a very more significant magnetization than the bulk materials. In nanoparticles, a large portion of the material composition is on the surface [23]. Besides, in nanoparticles, the nano-grains, and also the large portion of grain boundaries caused better biocompatibility. These structures can induce cell adhesion and proliferation [24–26]. Based on these facts, it seems that the nanostructured magnetic bioactive glasses have even improved magnetic features and biocompatibility over traditional crystals.

3.5. SEM results of MBG

SEM examination used to study and evaluate the BG particle sizes.

The SEM image of the BG NPs showed in Fig. 3. Homogenous surfaces, including fine-sized particles, are detected. Additionally, the particle size of the BG particles is 100–200 nm. However, because the samples grounded for 10 h, agglomerated particles are observed, yet these BG particles can be detached.

3.6. Phase analysis of MBG using XRD

The X-ray diffraction patterns of the MBG showed in Fig. 4. Fig. 4a shows the BG00 sample results. It does not show a diffraction peak, so we can conclude that we have an amorphous structure of bioactive glass without barium and ferrite contents. Fig. 4b shows the results of the BG010 sample (10% ferrite). The pattern shows the presence of the peaks related to magnetite according to the reference PDF 89–0951 and also larnite according to the reference PDF 83–0461. Fig. 4c shows the results for the sample BG100 (10% barium). In this pattern, the existence of two crystalline phases detected. These phases are calcium silicate according to the reference PDF 29–0369 and also barium calcium silicate according to the reference PDF 36–1449.

Fig. 4d shows the results for sample BG1010 (10% barium and 10%

ferrite). The curve exhibits the presence of two crystalline barium sili- cates. The identified parts are Ba3SiO5 according to the reference PDF 19–0175 and also BaSiO3, according to the reference PDF 30–0151.

Fig. 4e exhibits the result of the XRD pattern of the BG0515 (5% barium, 15% ferrite). The absence of diffraction peaks in the XRD patterns confirms an amorphous structure. It is well known that Fe2O3 acts as a glass modifier at low concentrations while at higher concentrations, it acts partially as a network former [27,28]. So, in silicate glasses, the presence of transition metal ions in low doping percent is not expected to form separate structural units. Therefore we can assume the transition metal ions at a low level behave as a network modifier. A decrease of glass nucleation and crystallization temperature of the bioactive glass with the addition of Fe₂O₃can be related to lower structural bonding in BG010, BG1010 [29].

Nevertheless, in BG0515, the Fe2O3 content acts as a network former.

Therefore, an increase in the glass crystallization temperature can Fig. 1. (a) DTA of BG (b) FTIR Curves of magnetic bioactive glasses.

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4 happen as the Fe2O3 content increase. In this study, in order to better characterization of the Fe2O3 and BaO addition effect on the magnetic properties, we decide to limit the variable parameters and set 700 ^�C for all of the final thermal treatment temperatures of the glasses.

3.7. Magnetic properties

3.7.1. Vibrating sample magnetometer (VSM) of MBG

The magnetization hysteresis loops of the MBG collected at 300 kHz showed in Fig. 5. All BGs showed similar magnetic properties. BG showed low coercivity (Hc) near soft magnetic materials. The magnetic features of the MBG showed in Table 2. The coercivity (Hc) and also the remanence magnetization (Mr) of the MBG are 40, 20, 950, 980 Oe, and 0.001377, 0.0025547, 0.046718, 0.03773 emu/g for BG010, BG100, BG1010 and BG0515 respectively. The saturation magnetization of the samples also reported in Table 2. It shows that the BG010 sample exhibits the highest value.

Generally, the remanence magnetization of the MBG improved with

the higher barium-ferrite part, and the BG1010 had the highest remanence magnetization among samples. Usually, the area of hysteresis loops was used to calculate the magnetic loss of the material. The loss amounts of MBG presented in Table 2. The area of the hysteresis loops grows bigger as the content of barium-ferrite increase from BG100 to BG0515. The maximum area gained for the BG1010 MBG, which exhibited the highest magnetic part.

Ferrimagnetic and ferromagnetic NPs (multi-domain or single domain) produce heat with an alternating external magnetic field. The below formula can be used to calculate the amount of produced heat [30]:

PFM¼μ₀f Z

Hdm

This formula shows the total produced heat per volume. The produced heat is proportional to the frequency and also the area of the hysteresis loop. In this formula, eddy currents and also resonance properties neglected. For magnetic NPs, PFM calculated by integrating Fig. 2. (a) Size distribution of bioactive glass particles. (b) TEM images of the BG particles.

Fig. 3. SEM images of bioactive glasses.

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the hysteresis loop area from the VSM test. Generally, the produced heat from magnetic NPs estimated by the SAR (specific absorption rate). The heat produced per volume also can be achieved using the SAR and the density of the NPs. Because it is nearly difficult to reach fully saturated loops in vivo, it is practical to assume about 25% of the maximum amount for accidently aligned NPs [30]. We used the above formula and VSM results to calculate the heat generated by our MBG. The results of the calculations showed in Fig. 6a. With the above assumptions and our estimates BG100, BG010, BG1010, and BG0515 samples must produce the temperatures around 5, 10, 84, and 67 ^�C within 720 s time under an external alternating magnetic field with 300 kHz frequency. These results show that BG1010 and BG0515 are producing enough temperature for magnetic hyperthermia. The best temperatures range for magnetic hyperthermia treatment is 41–43^�C.

3.8. Heat generation of MBG under alternate magnetic field

Fig. 6b shows the heat generation of glass samples under the external alternating magnetic field (300 kHz). For each type of magnetic bioactive glass, the temperature increase as a function of time. The tendency of diagrams is not linear due to the heat dissipation effect. This event is further noticeable in the BG0515 and BG1010 diagrams. Because in these samples, we have higher temperatures, and therefore there must be also higher heat dispersions. Ideally, the temperature of the ferrofluid must increase with the time until the produced and dissipated heat are almost equivalent. This value is helpful in hyperthermia application because this phenomenon led to a self-limiting effect in temperature.

With a single-domain particle, like the superparamagnetic NP, the

alternating magnetic field induces Brown and N�eel relaxation in order to produce the heat. Brown relaxation is the accidental spin of the mo- mentum via the motion of particles, and N�eel relaxation is the flipping movement of the magnetic moment of the particles [31,32]. It proved that particle aggregations affect Brown relaxation [6,31]. The SAR values also are size-dependent. In this study, the produced nanoparticles are uniform with particle size ranging from 40 to 70 nm in all samples, and we also use stabilizers in preparation of magnetic Ferro-fluids to avoid particle aggregations. The results show the temperature rises under alternative magnetic field (300 kHz) to 4.4, 10.4, 44.8 and 56.4 ^�C for BG100, BG010, BG1010, and BG0515 samples after 720 s, respectively. BG100 showed the lowest temperature, given that the particle sizes and the particle aggregations controlled in the process, this result is probably caused by the absence of ferrite compounds in the structure and also the small magnetic part of the bioactive glass. BG010 also reached 10.4 ^�C, which is not enough for magnetic cancer hyperthermia.

It seems the magnetic component in this bioactive glass sample is small, too.

Some researchers point out the effect of crystallinity and crystal sizes on the magnetic properties of the materials. Chia et al. [33] study the effect of crystallinity and crystal sizes on the magnetic properties of CoFe2O4. They report that the higher calcination temperature results in a higher degree of crystallinity and a larger mean crystallite size of CoFe2O4. Their results show that the magnetic properties (Ms and Hc) of the nanocrystals have considerably increased with the increase of mean crystallite size.

Some other researchers proved that amorphous magnetic nanoparticles could even show better magnetic properties. Yang et al. [34]

Fig. 4. XRD patterns of: (a) BG00 (b) BG010 (c) BG100 (d) BG1010 (e) BG0515.

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6 investigate the magnetic properties of fluids based on amorphous particles. They point out the Fe-based amorphous have uniquely high magnetic properties due to the short-range ordered and long-range disordered atomic structures. They synthesize three kinds of functional magnetic fluids: Fe73.5Nb3Cu1Si13.5B9 fluid (amorphous), CoFe2O4, and Fe3O4 (crystalline). They reported that the Ms (saturation magnetization) of metallic amorphous particles is nearly 75% and 50% higher than CoFe2O4 and Fe3O4, respectively.

Also, several researchers samples with higher magnetic content result in higher magnetic properties [17].

As XRD results showed, almost all bioactive glasses have amorphous natures, and we have amorphous Fe2O3 and BaO in the bioactive glass structure. So among two compositions with the highest magnetic content (BG1010 and BG0515), BG0515 is entirely amorphous. In our study, amorphous BG0515 shows the highest magnetic behavior in the alternating field, and it is similar to the previous study by Yang et al. [34].

In contrast with the first two samples, BG1010 and BG0515 Samples showed a very higher ability to produce heat. Higher magnetic part ratio and also the existence of ferrite and barium, which forms a capable

paramagnetic nanoparticle, caused higher heat generation ability in these two bioactive glasses. These results also confirm by calculated temperatures using VSM results. As Fig. 6 shows, all samples showed similar behavior in a calculated and calorimetric test. We also detected a decrease at temperatures in the calorimetric test comparing calculated temperatures. For example, BG0515 showed 56.4 ^�C in calorimetric test after 720s while the calculated results showed 67 ^�C. This decrease is even more in the BG1010 sample. The results showed 44.8 ^�C for calorimetric test and 84 ^�C for the calculated temperature using VSM results.

This decrease is maybe because of the ensemble of randomly aligned ferromagnetic particles and the difficulty of reaching fully saturated loops.

4. Conclusion

In this research, several different bioactive glasses (BG00, BG010, BG100, BG1010, ‘and BG0515) have been synthesized and character- ized. In our previous paper [18], the structural properties, Bioactivity, and biocompatibility of these glasses reported. In this paper, we report the physical and magnetic features of the synthesized glasses. The prepared magnetic bioactive glasses are good candidates for cancer hyperthermia. LPSA and also TEM proved that we have fine nanoparticle with 30–70 nm size. The VSM and calorimetric tests showed BG1010 and BG0515 generate enough heat for the application of these materials in cancer hyperthermia. Considering Cytocompatibility and Bioactivity results [18] and the magnetic properties form VSM and calorimetric tests, it seems the BG1010 sample is the best candidate to use in hyperthermia treatments since this composition presented the best agree- ment between magnetic behavior of glass, bioactivity of the glass and Fig. 5.Room temperature hysteresis loops of MBG (a) BG1010 (b) BG0515 (c) BG010 (d) BG100.

Table 2

Magnetic properties of the synthesized bioactive glasses.

BG010 BG100 BG1010 BG0515

Remanence Magnetization

(Mr) (emu/g) 0.001377 0.0025547 0.046718 0.03773

Coercivity (Hc) (Oe) 40 20 950 980

Saturation Magnetization

(Ms) (emu/g) 2.275471 0.0406311 0.31105 0.23186 Interpolated hysteresis area 80.16 41.35 658.46 526.94

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also biocompatibility of the samples.

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BaO–Fe2O3 containing bioactive glasses