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Abstract
Remotely monitoring and regulating temperature in a small area are of vital importance for hyperthermia therapy. Herein, we report ~11 nm NaErF4 nanocrystal as the ultra-small nanoheater, which is highly safe for biological applications. Under 1530 nm photon excitation, upconversion intensity of NaErF4 is significantly enhanced as compared to the conventionally used 980 nm pumping source. Upconversion mechanisms are discussed on the basis of power dependence measurements. Importantly, light-to-heat transformation efficiency of NaErF4 through 1530 nm pumping is determined as high as 75%. Efficient NIR emission, centered at ~800 nm and thus within the biological window, is used for the temperature feedback. The potential applications of this highly efficient nanoheater for controlled photo-hyperthermia treatments are also demonstrated.
© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement
1. Introduction
Controlling and monitoring the temperature of small area are the fundamental preconditions for understanding and utilizing microscopic thermal processes, especially useful in some biological applications such as hyperthermia therapy [1]. Currently, hyperthermia treatments are usually mediated by ultrasounds [2], microwaves [3], magnetic fields [4] and lasers [5]. Among them, NIR photon induced nanoheaters play important roles as they can penetrate deeply into the human tissue and thus validate the subcutaneous treatment [6–10], and pioneering work of photothermal therapy has been carried out in vivo [11]. To date, nanoheaters with various compositions have been developed, including Au nanoshells, nanorods, and nanocages [12–14], Cu5S9 nanocrystals [15], Cu2-xSe nanoparticles [16], carbon nanoshells and naonotubes [17,18], graphene flakes [19], porous silicon [20] and so on. Although these nanoheaters have been proved to be efficient heat converter, lack of self-monitoring of temperature requires additional component to send signal for the temperature readout.
Alternatively, NIR light inducing Erbium based luminescent nanoheaters attract considerable attentions, as Er3+ with thermally coupled energy levels (2H11/2 and 4S3/2) are feasible for remote temperature sensing through fluorescence intensity ratio (FIR) technique [21–24]. In 2009, Tikhomirov et al. reported up to 800 °C heating temperature through 980 nm laser irradiating the Er3+/Yb3+ codoped oxyfluoride nanoparticles [25]. However, Er3+/Yb3+ based luminescent nanoheater have intrinsic drawbacks due to using 980 nm photon as excitation source as well as using green emission for temperature sensing. Specifically, excitation by 980 nm photon is not suitable for biological applications. It tends to arouse overheating and lower the penetration depth due to the strong absorption of water molecules in human tissue [26]. On the other hand, using Er3+ green emissions for temperature sensing also severely decrease the intensity of sensing signal due to strong absorption and scattering of human tissue within visible light region. Therefore, excitation and/or emission wavelengths falling in the so-called biological windows (BW, including І-BW spinning 650-950 nm, Π-BW covering 1000-1350 nm and Ш-BW within 1500-1750 nm [27]) are developed [8,16,18].
To make practically valuable nanoheaters for hyperthermia therapy, two factors should be focused. The first factor is the efficient light-to-heat conversion ability, which lowers the operating laser power corresponding to the lethal temperature of the nanoheater and thus suppresses the side effect of laser, that is, overheating effect. Second factor is the efficient photoluminescence signal of the nanoheater, specifically, detectable light signal dependent on the surrounding temperature. This signal should be strong enough to validate the non-invasive temperature sensing by monitoring the spectra of the nanoheater passing through the human tissue.
However, above mentioned factors are actually contradictory since the light-to-heat transformation and photoluminescence of rare earth are two ways consuming the absorbed energy and compete with each other. To simultaneously achieve effective heating and detectable photoluminescence, one feasible way is to enhance the absorption of incident light energy, including enlarging the absorption cross section of rare earth at the incident wavelength, as well as increasing the doping concentration of the nanoheater. Thus, one should choose rare earth with strong absorption at the incident wavelength and should increase the doping concentration, by adopting this method, the absorbed energy can be greatly enhanced [28].
Unfortunately, the effects of concentration quenching result in extremely weak emission under high doping situation and thus prevents heavily doping of rare earth [29–31]. In another word, although possessing efficient light-to-heat conversion, it remains formidable challenge to achieve detectable signal, falling in the BW, for temperature feedback in high doping nanoheaters.
Er3+ shows efficient energy absorption at 1530 nm (Ш-BW), as Er3+ possesses larger absorption cross section here. Most importantly, we found that the upconversion intensity of Er3+ heavily doped fluoride nanocrystals is highly enhanced under 1530 nm pumping source as compared to 980 nm excitation, especially for the NIR emission centered at ~800 nm (І-BW). This means one can simultaneously obtain efficient heat conversion and strong light signal within BW. Therefore, 1530 nm excited Er3+ heavily doped fluoride nanocrystals should be promising candidate for self-monitoring photothermal probe.
In this paper, we synthesized small NaErF4 nanocrystals as the photothermal nonoheater. Comparison of upconversion properties were carried out under 980 nm and 1530 nm excitation, and upconversion mechanisms were also investigated. Light-to-heat conversion efficiency was evaluated through monitoring one heating/cooling cycle of the nanoheater in liquid. In addition, FIR technique was utilized for the temperature feedback of the nanoheater and pork tissue was used to demonstrate the feasibility of the proposed nanoheater.
2. Results and discussion
NaErF4 (namely, 100 mol% Er3+ doping) nanocrystals are synthesized by a modified thermal decomposition method [32]. The TEM image in Fig. 1 shows the morphology of NaErF4 nanocrystals, which exhibit a mono-dispersed spherical shape with an average diameter of ~11 nm. Such small size is highly useful for biological applications, due to small nanoparticles can efficiently penetrate subcellular membranes, can be easily cleared from the human body, and would be more suitable for ex vivo diagnostics [33].
Fig. 1 TEM photograph of as-prepared NaErF4 nanocrystals, scale bar is 50 nm. Distribution of the particle size is given by measuring 100 particles, and the mean size is calculated to be ~11.3 nm.
Erbium (Ш) is the most commonly used upconversion activator and Yb3+ is usually added as the sensitizer to utilize its strong absorption at around 980 nm. Herein, strong absorption of Er3+ appears at 1.5 μm [Fig. 2(a)], providing solid foundation of efficient upconversion emissions upon 1.5 μm excitation by using Er3+ singly doped system. As expected, 1530 nm excitation leads to significant improvement on the upconversion intensity of NaErF4 as compared to 980 nm pumping source by using identical output power [Fig. 2(b)]. Importantly, the efficient NIR emission at around 800 nm validates the subcutaneous imaging and treatment as demonstrated later. As shown in our recent work [34], severe concentration quenching still occurs under 1530 nm excitation, indicating that the efficient energy harvest (due to 1530 nm pumping combined Er3+ heavily doping) is mainly responsible for the highly improved upconversion emission. Upconversion mechanisms of Er3+ excited by 1530 nm photon are investigated by power dependence measurements. It can be seen from Fig. 2(c) that green and red emissions are 3-photon processes, and NIR emission at 800 nm is 2-photon process, as detailed depicted in Fig. 2(d).
Fig. 2 Optical properties of NaErF4. (a) Absorption spectrum of Er3 + in the NIR region; (b) Comparison of upconversion spectra upon 980 nm and 1530 nm excitation; (c) Upconversion power dependence. Linear fitting lines and their slopes are given; (d) Energy levels and upconversion pathways of Er3 + under 980 nm and 1530 nm excitations.
As shown in Fig. 3(a), when the sample cell (a 10 × 10 mm2 quartz cuvette containing NaErF4/cyclohexane dispersed solution) is irradiated by 1530 nm laser, temperature of the solution raises gradually. The maximum temperature is achieved after 8-min heating and then another 10-min is needed to cool down to the ambient temperature without heating. In addition, 5 heating/cooling cycles are performed to show the good reproducibility of our nanoheater.
Fig. 3 Calculation of the light-to-heat conversion efficiency. (a) Heating and cooling processes of NaErF4 in cyclohexane; (b) Variation of t vs. T function, from which time constant can be calculated by the linear fitting.
Light-to-heat conversion efficiency is one of the most important parameter of the photo-heater. This efficiency can be calculated through monitoring one heating/cooling cycle of sample cell, using the following equation [18].
where Tmax = 34.3 °C is the equilibrium temperature; T0 = 19.6 °C is the initial ambient temperature [Fig. 3(a)]. Qb, expressing heat dissipated from 1530 nm light absorbed by the sample, was measured independently to be 97 mW by using a quartz cuvette containing pure cyclohexane without NaErF4 nanocrystals; I = 1 W is the incident laser power; A = 0.043 is the absorbance of Er3+ in the cuvette cell. To calculate hS, the heat transfer coefficient from quartz cuvette to the surroundings, time constant τs is introduced as follows [18].From Eq. (2), the obtained value of the time constant τs = 128 s is given, as shown in Fig. 3(b) by the linear fitting. According to the expression τs = mC/hS, where m = 0.80 g and C = 1.82 J/K·kg are the mass and heat capacity of cyclohexane in the cuvette, respectively, we obtained hS = 11.40 mW/K.
Hence, on the basis of the above mentioned parameters, the light-to-heat efficiency is calculated to be η = 75% by using Eq. (1). Due to the plenty of energy levels and thus multiple emission bands of Er3+, besides heat energy the residual of absorbed energy should be the summation of the light energy, including mainly the visible emissions and NIR emissions centered at around 800 nm, 980 nm, and 1550 nm, if one neglect the higher-order ultraviolet emissions. This conversion efficiency is much higher than the previously reported nanoheaters such as Au nanorods (21%) and nanoshells (13%), Cu9S5 (25.7%), and Carbon coating nanocrystals (38.1%) [15–17], and slightly higher than the NaNdF4@NaYF4@1Nd:NaYF4 core-shell nanoheater (72.7%) [28]. Although still lower than some gold nanorods with 100% heating efficiency [35,36], the presented nanoheater exhibits potential of self-monitoring due to its efficient NIR emission.
In addition, it is found that light-to-heat conversion efficiency drastically decreases by using 980 nm pumping source compared to 1530 nm excitation, due to the slump of light harvest. The estimated efficiencies of NaErF4 under 1530 nm and 980 nm excitation are 75% and 39%, respectively, evidencing the strong dependence of heat conversion on pumping wavelength. Similarly, decreasing the doping concentration of Er3+ also leads to evident decrease of the heat conversion efficiency (conversion efficiency of 80 mol% Er3+ doped NaGdF4 under 1530 nm excitation is evaluated to be 42%), due to the same reason as mentioned above.
To validate the temperature feedback, NIR emission band corresponding to the 4I9/2→4I15/2 transition is utilized for the temperature sensing. FIR (ratio of the luminescence intensities at 804 nm and 825 nm) increases with the ambient temperature and can be well fitted by a linear line [Figs. 4(a) and 4(b)] as follows.
where k = 0.00116 and b = 1.50843 are obtained by the fitting.Fig. 4 Sensing calibration and application demonstration of the NaErF4 nanoheater. (a) Normalized spectra (normalized at 825 nm) of NIR emission under lower and higher temperature; (b) Calibration of the temperature feedback in the nanoheater. Fitting function is given; (c) Schematic diagram of the experimental setup of the in ex vivo demonstration, showing the heating effect of the nanoheater through 2 mm thickness pork tissue; (d) Normalized spectra of NIR emission under different laser power excitation; (e) Heating effect under different laser powers, surface temperatures are monitored by the thermal camera and eigen temperatures are calculated from FIR sensing. The inset is the digital photograph of the scattered laser beam after passing through the pork tissue, the radius of the scattered beam is evaluated to be 0.4 cm, which is used for estimating the incident power density.
At the end, pork skin is used to demonstrate the ex vivo hyperthermia treatment. Experimental setup is depicted in Fig. 4(c), NaErF4 nanocrystals dispersed in cyclohexane are sprayed onto the back side of the pork skin (~2 mm of thickness). 1530 nm laser outputting various powers penetrate the pork skin and illuminate the nanocrystals. Upconversion signal, passing through the pork skin, is transmitted into the spectrometer to deduce the eigen temperature of NaErF4, using the calibration in Eq. (3) with determined parameters. Surface temperature of the skin is monitored by a thermal camera. The relative intensity at 804 nm and 825 nm evidently increases by increasing the pumping power [Fig. 4(d)], indicating the remarkable heating effect. As shown in Fig. 4(e), the heating temperature (increased temperature of NaErF4) approximately increases linearly with the incident laser power. The maximum temperature value goes above 100 °C and the surface heating of the pork skin is still weak when the power density is ~1 W/cm2, evidencing the high heat conversion efficiency of our nanoheater. The heating temperature is much higher than that reported in Nd3+/Yb3+ doped LaF3 core-shell nanocrystals [6], which can be attributed to the efficient light-to-heat transformation of NaErF4 (smaller size and core-only nature both benefit the heat accumulation), as well as the more concentrated nanocrystal used in the demonstration.
3. Conclusions
In summary, we have demonstrated a novel rare earth based nanoheater. Using NaErF4 optically excited with a single 1530 nm infrared beam, this nanoheater simultaneously achieved compact structure (core only nanocrystals), ultra-small particle size (~11 nm), efficient light-to-heat conversion (efficiency of ~75%) and temperature feedback (monitoring the heating). Luminescence mechanisms of the nanoheater were investigated on the basis of the power dependence variations. In addition, the application of NaErF4 nanoparticles for the achievement of fully controlled photo-hyperthermia processes under single infrared beam excitation through pork tissue has been demonstrated. The obtained results are going to open a new way for the development of biological nanoheater with enhanced efficiency and reduced risk.
Funding
Fundamental Research Funds for the Central Universities (HEUCF181114); Natural Science Foundation of Heilongjiang Province (LC2018026); 111 project (B13015) to the Harbin Engineering University; Postdoctoral Scientific Research Developmental Fund of Heilongjiang Province (LBH-Q17050).
Disclosures
The authors declare that there are no conflicts of interest related to this article.
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