Photothermal Effect of Superparamagnetic Fe<sub>3</sub>O<sub>4</sub> Nanoparticles Irradiated by Near-Infrared Laser

Fu, Shawei; Man, Yuchun; Jia, Fuquan

doi:https://doi.org/10.1155/2020/2832347

Journal of Nanomaterials

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Abstract Introduction Materials and Methods Results and Discussion Conclusions Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

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Smart Design, Controllable Synthesis, and Functional Applications of Low-Dimensional Hetero-Structured Materials

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Volume 2020 | Article ID 2832347 | https://doi.org/10.1155/2020/2832347

Photothermal Effect of Superparamagnetic Fe₃O₄ Nanoparticles Irradiated by Near-Infrared Laser

Shawei Fu,¹Yuchun Man,¹and Fuquan Jia¹

Guest Editor: Zhenyi Zhang

Received13 Jul 2020

Accepted03 Aug 2020

Published14 Oct 2020

Abstract

Fe₃O₄ nanoparticles (NPs) have been widely used in biomedicine due to their unique magnetism, biocompatibility, and biodegradability. Magnetic hyperthermia of Fe₃O₄ NPs for cancer treatment has attracted more attention. However, it could interfere with magnetic field-sensitive devices of patients, such as pacemakers. Therefore, it is necessary to find a new method for clinical therapy. In this study, the superparamagnetic Fe₃O₄ NPs were fabricated. Visible-near-infrared absorption spectra indicated that the Fe₃O₄ NPs have near-infrared absorption. The influences of Fe₃O₄ NP concentrations, power density, and wavelength of near-infrared laser irradiation on the photothermal performance of Fe₃O₄ NPs were investigated. The results revealed that high concentrations, large power density, and short irradiation wavelength could improve the photothermal performance of Fe₃O₄ NPs. The temperature variation and the absorption intensity simultaneously determined the photothermal transduction efficiency of Fe₃O₄ NPs. The application of the photothermal performance of Fe₃O₄ NPs would provide a new opportunity for clinic cancer treatment.

1. Introduction

In recent years, nanomaterials have been widely used in photocatalysis [1–3] and electrochemical applications [4]. With recent nanotechnology developments, more and more nanomaterials find their practical as well as potential applications in biomedicine [5–9]. One of such example is the application of superparamagnetic Fe₃O₄ NPs for cell targeting, drug delivery, magnetic resonance imaging, and magnetic hyperthermal cancer therapy, all of which rely on unique magnetic properties of Fe₃O₄ as well as its biocompatibility and biodegradability [10–14]. Specially designed Fe₃O₄ NPs and their composites demonstrating diverse performance characteristics are promising prospects for theranostic applications [15–19]. However, using magnetic hyperthermia for cancer treatment might not be applicable to a wide-enough extent. For example, patients with implanted devices sensitive to magnetic fields (e.g., pacemakers) cannot be treated by the external magnetic field [20]. High-intensity magnetic fields might bring other potential risks to patients.

Photothermal therapy (PTT) recently emerged as a promising strategy to battle cancer [21–24]. It uses photothermal agents to ablate cancer cells in combination with near-infrared (NIR) irradiation to raise local temperature around the tumour. Comparing with magnetic hyperthermal therapy, PTT is more convenient and safer. Heat generated from photothermal nanoagents irradiated by a laser is directed exactly and precisely at the cancer cells, which significantly reduces potential damage to surrounding healthy cells and tissues. Ideal PTT agents not only absorb NIR but also have high photothermal conversion efficiency. Numerous PTT agents were extensively studied by other research groups, such as noble metals (Au and Ag), carbon-based material, and polymers [25]. All of these agents can absorb NIR irradiation and convert it into heat.

Fe₃O₄ NPs absorb light in a wider range: from the visible to the NIR part of the light spectrum. The energy absorption of Fe₃O₄ NPs in the NIR region can be exploited. In addition, electron nonradiative transition of Fe₃O₄ NPs in the NIR region also releases thermal energy. The absorption at the NIR region of Fe₃O₄ NPs is attributed to the indirect band gap transition of Fe(III) 3d electrons. The electronic transitions may contribute to the absorption of Fe₃O₄, namely, d-d transitions of the Fe(II) and Fe(III) ions in the visible-NIR wavelength range [11, 26]. Thus, Fe₃O₄ NPs might become next-generation photothermal agents for cancer therapy. At present, a lot of effort was dedicated to combine Fe₃O₄ NPs with other photothermal agents to achieve photothermal cancer therapy [10, 15, 23, 27]. In these nanocomposites, Fe₃O₄ was only implemented to enhance magnetic targeting and imaging of the composite. The photothermal effect of Fe₃O₄ NPs was not considered at all. However, we believe that individual Fe₃O₄ NPs acting as photothermal agents could simultaneously achieve multiple functions, which will help to avoid complex preparation of composites for cancer therapy. Another very important aspect is superior biosafety of Fe₃O₄ NPs in comparison to other photothermal agents [28]. Fe₃O₄ NPs have excellent biocompatibility and can be easily excreted from the body.

In this work, Fe₃O₄ NPs were fabricated by the thermal decomposition method, after which water soluble nanocrystals were obtained using the surface ligand exchange technique. Photothermal performance of the Fe₃O₄ NPs was studied. Fe₃O₄ NPs were used for magnetic targeting photothermal therapy against cancer cells using NIR irradiation.

2. Materials and Methods

2.1. Initial Chemicals

All initial compounds were analytically pure and used without any further treatment. We purchased 1,2-hexadecanediol (90% pure), iron acetylacetonate (Fe(acac)₃, 99.9% pure), benzyl ether (99% pure), oleylamine (OLA, 70% pure), branched polyethylenimine (PEI, 25000 kDa), oleic acid (OA, 90% pure), and chloroform from Sigma Chemical Company (USA). Hexyl hydride was obtained from Sinopharm Chemical Reagent (China).

2.2. Synthesis

Fe₃O₄ NPs were synthesized using the thermal decomposition technique [29]. For this purpose, 2 mmol of Fe(acac)₃, 10 mmol of 1,2-hexadecanediol, and 6 mmol of OA and OLA were mixed in 20 mL of benzyl ether in a three-neck flask. The resulting solution was stirred under N₂ atmosphere. The solution was heated to 200°C and kept at this temperature for 30 min, after which it was heated to 300°C and refluxed for 1 h. The resulting solution was gradually cooled to room temperature. Fe₃O₄ NPs were rinsed with ethanol several times and then suspended in chloroform. 0.004 mM Fe₃O₄-chloroform suspension was then diluted again in 1 mM PEI-chloroform solution under constant stirring at room temperature. After 48 h, hexyl hydride was added into the suspension. The final product was PEI-capped Fe₃O₄ precipitates, which were washed three times with water and then dispersed in deionized water.

2.3. Photothermal Tests

Fe₃O₄ NP suspensions with different concentrations were placed into centrifuge tubes. These suspensions were then irradiated by lasers with different power densities. Temperatures of these suspensions were recorded every minute for 15 consecutive minutes. We also irradiated Fe₃O₄ NPs that were placed in a thin plastic bag using a similar empty bag as a reference.

2.4. Cytotoxicity Assay

Cells of 4T1 mouse breast cancer cells were cultured at 37°C in 5% CO₂ atmosphere using RPMI-1640 as a medium with addition of fetal bovine serum (10%), streptomycin (100 μg/mL), and penicillin (100 U/mL). Prior to the assay, 4T1 cells were seeded in a 96-well plate (10⁴ cells/well) for 12 h, after which Fe₃O₄ NPs with different concentrations were added to each well. Cultivation was performed at 37°C for 24 h, after which 20 μL of 5 mg/mL methyl thiazolyl tetrazolium (MTT) was added, and the cells were incubated for another 4 h. MTT assay was performed to determine cell viabilities (relative to the control), which was expressed as a percentage of the control. The final value represents an average one. The measurement error represents standard deviation (SD).

2.5. Photothermal Treatment of Breast Cancer 4T1 Cells

4T1 cells were incubated with 0.1 mg/mL Fe₃O₄ NPs at 37°C for 1 h. After the treatment, excess Fe₃O₄ was removed by rinsing with phosphate buffer saline, after which a standard MTT assay (performed as described above) was implemented to examine how Fe₃O₄ presence affected 4T1 cells. Another series of 4T1 cells after incubation was irradiated by an 808 nm laser for 10 min with 1 W/cm² power density with or without an applied magnetic field. After the irradiation, cell viability was also analyzed by MTT assay.

2.6. Characterization

Micromorphologies of the resulting samples were obtained by transmission electron microscopy (TEM) using an FEI Tecnai G2 S-Twin. Phase compositions as well as their crystallinity degree were determined by X-ray diffraction (XRD) using a D/MAX-RA XRD Rigaku system with Cu Kα radiation at 50 kV and 300 mA operating voltage and current, respectively. Effect of the magnetic field on the samples was obtained at 300 K using an MPMS-XL-5 5QUID magnetometer. The magnetic field was cycled between −30 and +30 kOe. UV-vis-near-IR absorption spectra were recorded using a PerkinElmer UV WinLab spectrophotometer.

3. Results and Discussion

TEM analysis showed uniform monodispersed Fe₃O₄ NPs (see Figure 1(a)) in diameter. XRD analysis confirmed that the resulting NPs were pure Fe₃O₄ with a cubic inverse spinel structure (according to JCPDS 75-1610), as shown in Figure 1(b).

(a)

(b)

Magnetic properties Fe₃O₄ NPs were obtained using a field-dependent magnetization technique. Hysteresis loop of Fe₃O₄ NPs at room temperature showed no hysteresis; thus, our resulting Fe₃O₄ NPs were superparamagnetic (see Figure 2(a)). Saturation magnetization of Fe₃O₄ NPs was ~39.5 emu/g, which indicates strong magnetism. Figure 2(b) shows Fe₃O₄ NPs in an aqueous solution with and without application of an external magnetic field. When suspended Fe₃O₄ NPs were not subjected to the magnetic field, they were well-dispersed and suitable for biological applications. When a magnet was in contact with one side of the vial, Fe₃O₄ NPs quickly separated from the aqueous solution and attached to the vial wall near the magnet. As a result, the solution became clear.

(a)

(b)

The absorption spectrum of the 0.1 mg/mL suspension of Fe₃O₄ NPs showed higher absorption intensity in the visible region than in the NIR region (see Figure 3). However, the penetrability of visible light is not strong; it was not to be used for biomedical applications. Although the absorption intensity in the NIR region is not as strong as that in the visible region, it is enough to produce excellent photothermal performance, as shown in the following photothermal test.

Photothermal performance of Fe₃O₄ NPs was tested by measuring the temperature of aqueous suspensions containing different contents of Fe₃O₄ NPs. These suspensions were irradiated using different laser power densities and wavelengths (see Figure 4). When the suspensions were irradiated by an 808 nm laser, higher temperatures were observed in suspensions with higher Fe₃O₄ NPs contents (see Figure 4(a)). For example, when a suspension containing 0.05 mg/mL of Fe₃O₄ NPs was irradiated by an 808 nm laser for 10 min, temperature increased 29.4°C. However, in the case of 1 mg/mL Fe₃O₄ NP suspensions, laser irradiation increased suspension temperature by 46.3°C. More significant temperature increase for suspensions with higher Fe₃O₄ NP contents was attributed to more absorbed irradiation (because there were more particles in the suspension), which was then converted into heat. Our control experiments with aqueous solutions containing no Fe₃O₄ NPs showed only up to 4.4°C temperature increase upon the same laser irradiation conditions.

(a)

(b)

(c)

Laser power density also affected temperature increase. Laser power density equal to 0.4 W/cm² was not enough to produce significantly increased temperature of Fe₃O₄ NP suspensions (see Figure 4(b)). Temperatures of the 0.1 mg/mL Fe₃O₄ NP suspension upon its 10 min irradiation with an 808 nm laser at 1 and 2 W/cm² power densities were increased 33.9 and 46.1°C, respectively.

We also studied temperature changes of Fe₃O₄ NP suspensions upon their irradiation by lasers with different wavelengths (see Figure 4(c)). Irradiation by lasers with shorter wavelengths increased suspension temperatures more than irradiation with laser with longer wavelengths, which corresponds to the results of our light-absorption experiments: more energy was absorbed in the visible part of the spectrum than in the NIR. However, the main reason of popularity of photothermal treatments using NIR irradiation for biomedical applications is its strong penetrability into the tissues and biological/physiological systems.

Photothermal conversion efficiency is an important parameter to evaluate the photothermal properties of materials. To calculate the photothermal conversion efficiency of Fe₃O₄ NPs, an energy balance on the system is required [18, 26, 30]. The total energy balance for the system is where is the heat generated by the material under laser irradiation, is the heat generated by water under laser irradiation, is the heat transferred from the system to the environment, is the mass, and is the heat capacity. where is the laser power, is the absorption intensity at the excitation wavelength of (nm), and is the photothermal conversion efficiency. where is the heat transfer coefficient, is the surface area of the container, is the solution temperature, and is the ambient surrounding temperature. In order to calculate , the cooling stage is studied. After removing the laser excitation, the heat generated by the system is stopped. Equation (1) becomes

Rearranging Equation (3) then integrating

Let be the time constant for heat transfer from the system

During solution cooling, the temperature decrease was monitored. is calculated according to the temperature changes of the solution as a function of time. Thus, can be computed.

At the maximum steady-state temperature, the heat transfer between the system and the environment reaches equilibrium. The temperature is a constant.

Equation (1) gives the expression

Then, Equations (3) and (4) give the expression

In order to further study the photothermal performance of the Fe₃O₄ NPs, we recorded the temperature change of the 1 mL Fe₃O₄ NP suspensions at different concentrations as a function of time under continuous different power densities of the 808 nm laser irradiation until the suspensions reached a steady-state temperature. Then, the laser was turned off and the suspension was cooled (see Figure 5(a)). The linear time data versus negative natural logarithm of the temperature driving force is obtained by the cooling process as shown in Figures 5(b)–5(d). According to the obtained data, the time constant of 0.1 mg/mL Fe₃O₄ NP suspensions with an 808 nm laser irradiation at 2 W/cm² power densities is determined to be . The time constant of 0.5 mg/mL Fe₃O₄ NP suspensions with an 808 nm laser irradiation at 1 W/cm² power densities is determined to be s. The time constant of 0.1 mg/mL Fe₃O₄ NP suspensions with an 808 nm laser irradiation at 1 W/cm² power densities is determined to be s. According to Equations (7) and (10), the relevant parameters are inputted into the formula. The photothermal conversion efficiency is about 2.23%, 4.64%, and 6.57%, respectively. It can be seen that the photothermal performance of NPs is not only contributed by absorption, but also determined by photothermal conversion efficiency.

(a)

(b)

(c)

(d)

The mouse 4T1 breast cancer cells were selected to investigate the toxicity of Fe₃O₄ NPs by standard MTT assay. The 4T1 cells were incubated with different mass concentrations of the Fe₃O₄ NP suspension at 37°C for 24 h. As displayed in Figure 6, the viability of cancer cells was about 97.6% when the concentration of the Fe₃O₄ NP suspension was 0.01 mg/mL. With the increase of the Fe₃O₄ NP concentration, the viabilities of cancer cells were gradually decreased. But even when the concentration of the Fe₃O₄ NP suspension was 1 mg/mL, the viabilities of cancer cells were still about 94.1%. It indicates the low cellular toxicity of the Fe₃O₄ NPs.

To demonstrate the photothermal effect of Fe₃O₄ NP suspensions for cancer treatment, we used mouse 4T1 breast cancer cells (see Figure 7). The cells with the 808 nm laser irradiation at the power density of 1 W/cm² or 2 W/cm² for 10 min had no significant cellular death. As discussed above, the Fe₃O₄ NPs of 0.1 mg/mL have little cellular toxicity. However, after the 808 nm laser irradiation at the power density of 1 W/cm² for 10 min, the cell viability reduced to 50.5% for 4T1 cells incubated with Fe₃O₄ NPs. It reduced even more after application of an external magnetic field. Under the external magnetic field, the viability further reduced to 24.1% for the cells incubated with Fe₃O₄ NPs. Thus, application of a magnetic field significantly enhanced the photothermal effect of Fe₃O₄ NPs.

4. Conclusions

We successfully prepared superparamagnetic Fe₃O₄ NPs by the thermal decomposition method. These Fe₃O₄ NPs demonstrated absorption in both the visible and NIR spectra and were able to convert light energy into heat. High concentration of Fe₃O₄ NPs in an aqueous suspension and high power density as well as shorter wavelengths of a laser resulted in a significantly more enhanced photothermal effect of Fe₃O₄ NPs. Photothermal destruction of cancer cells had the best efficiency when it was performed with the application of an external magnetic field.

Data Availability

All data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

Acknowledgments

This work was supported by the Jilin Provincial Education Department “13th Five-Year” Science and Technology Research Planning Project (JJKH20180584KJ).

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Copyright © 2020 Shawei Fu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Journal of Nanomaterials

Smart Design, Controllable Synthesis, and Functional Applications of Low-Dimensional Hetero-Structured Materials

Photothermal Effect of Superparamagnetic Fe3O4 Nanoparticles Irradiated by Near-Infrared Laser

Abstract

1. Introduction

2. Materials and Methods

2.1. Initial Chemicals

2.2. Synthesis

2.3. Photothermal Tests

2.4. Cytotoxicity Assay

2.5. Photothermal Treatment of Breast Cancer 4T1 Cells

2.6. Characterization

3. Results and Discussion

4. Conclusions

Data Availability

Conflicts of Interest

Acknowledgments

References

Copyright

Photothermal Effect of Superparamagnetic Fe₃O₄ Nanoparticles Irradiated by Near-Infrared Laser