Porphyrins as efficient ratiometric and lifetime-based contactless optical thermometers

Materials and Design 184 (2019) 108188

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Porphyrins as efficient ratiometric and lifetime-based contactless optical thermometers I.E. Kolesnikov a,b,⁎, A.A. Kalinichev a, M.A. Kurochkin a, E. Yu Kolesnikov c, E. Lähderanta b a b c

Saint Petersburg State University, St. Petersburg 199034, Russia LUT University, Lappeenranta 53850, Finland Volga State University of Technology, Yoshkar-Ola 424000, Russia

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Tetraphenylporphyrins were firstly used as contactless luminescence temperature sensors. • Fluorescence intensity ratio and luminescence lifetime were utilized for thermal sensing. • Thermal sensitivity of 0.25% °C−1 and temperature resolution of 0.2 °C were achieved. • Photobleaching does not affect thermal sensing abilities of studied porphyrins.

a r t i c l e

i n f o

Article history: Received 7 July 2019 Received in revised form 1 September 2019 Accepted 4 September 2019 Available online 05 September 2019 Keywords: Porphyrins Thermometry Luminescence Lifetime Sensor

a b s t r a c t Numerous attempts to develop an efficient anti-cancer agent are focusing on the design of multifunctional objects with synergistic theranostic treatments and minimal side effects. The most prospective treatments which can be used in combination are chemotherapy, photothermal therapy, and photodynamic therapy. To avoid collateral damage, it is important to control local temperature during the treatment procedure. In this work, we demonstrate how free-based and zinc-containing porphyrins can be used as contactless luminescence thermometers. Thermal sensing was provided based on two approaches: ratiometric and lifetime-based techniques. Thermometric performances of suggested temperature sensors including relative sensitivity and temperature resolution were calculated and compared. © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Data availability: The raw/processed data required to reproduce these findings cannot be shared at this time as the data also forms part of an ongoing study.

1. Introduction

⁎ Corresponding author at: Saint Petersburg State University, St. Petersburg 199034, Russia. E-mail address: [email protected] (I.E. Kolesnikov).

Porphyrins are an important class of naturally occurring compounds featuring a planar tetrapyrrolic macrocycle with strong aromaticity. Porphyrins can be called one of the cornerstones of biological life because they play a very important role in the metabolism process. Some of the best examples are metalloporphyrins such as the

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magnesium-containing reduced porphyrin (or chlorine) found in chlorophyll and the iron-containing porphyrins found as heme [1]. Chlorophylls play pivotal roles in photosynthesis as both light harvesting antennae and charge separation reaction systems. Hemes are one of the key components for biocatalysts and oxygen carriers in the blood [2]. Moreover, porphyrins are the archetypal functional molecules, playing an important role in diverse areas of scientific research owing to its unique electronic and optical properties. Therefore, porphyrin research has a long history, covering a wide variety of disciplines of natural sciences, including photosynthesis, P450-related biocatalysis, organic photovoltaic cells, photodynamic therapeutic agents, bioimaging probes, chemosensors, conductive organic materials, lightemitting materials, near-infrared dyes, nonlinear optical materials, information storage, molecular wires, metal ligands, supramolecules, and so forth [3–7]. Currently, cancer is still a major threat to human health around the world [8,9]. Surgery, chemotherapy and radiation are the most commonly used therapeutic clinical methods in the fight against cancer. However, these methods have a serious drawback: cancer cells and normal cells are simultaneously killed, which gives rise to a new disease that may cause the patient's death [10]. So, nowadays many scientific groups are making efforts to develop efficient and noninvasive tools for early cancer detection and therapy [11,12]. Phototherapy, which includes photodynamic therapy (PDT) and photothermal therapy (PTT), is an experimental technique for the treatment of malignant tissues [13]. Compared with conventional treatments, phototherapy has many advantages such as the minimal invasion, low toxicity and spatial and temporal control [14,15]. PDT induces cancer cell death by apoptosis, necrosis, and autophagy, and these mechanisms can concurrently occur. PDT destroys cancer cells by inducing apoptosis through diverse signaling pathways coupled with Bcl-2 family members, caspases, and an apoptosis-inducing factor. When the apoptotic pathway is unavailable, PDT can cause cancer cell death through induction of a necrotic or autophagic mechanism. Cell death mechanisms are dependent on a variety of parameters including the nature of the photosensitizer, PDT dose, and cell genotype [16]. PDT rapidly eliminates local tumors, resulting in the cure of early disease and palliation of advanced cases, being associated with an enhanced antitumor immunity [17]. Nowadays, approved use of PDT is quite widespread in such countries as United Kingdom, Netherlands, Israel and Japan. PTT is a novel clinical treatment using laser-induced temperature increase to above 42 °C to eliminate tumor cells [18–20]. The main principle of PTT is to “burn” cancer cells while the surrounding normal tissue survives [21,22]. Efficiency of PTT is strongly dependent on the magnitude of the heating as well as the treatment duration [23,24]. Therefore, it is mandatory to have high-resolution real-time monitoring of the temperature in order to minimize collateral damage in healthy tissues surrounding the tumor [25]. Compared with traditional single therapeutic treatments, combination treatment joins merits from each approach, which results in minimization of side effects and improves therapeutic efficacy [26,27]. Thus, designing such multifunctional therapeutic agents with high performance, high stability and good biocompatibility has become a hot spot of cancer phototherapy. Recently, several types of such synergistic agents for antitumor treatment were synthesized and tested [10]. Despite obtaining good results of combination treatment, PTT was provided without temperature control, which can result in overheating and as a result the collateral damage of healthy tissues. To overcome this problem, broadening of the porphyrins functionality (wide-known PDT agents) by using them as contactless optical thermal sensors was suggested. To our knowledge, it is the first demonstration of temperature sensing via porphyrins emission properties. In this paper, the optical and photoluminescence properties of freebased and zinc-containing tetraphenylporphyrins in different (non-

polar and polar) solvents were studied. The possibility of accurate temperature sensing using ratiometric and lifetime approaches was demonstrated for both synthesized samples. Thermometric performance was calculated including relative thermal sensitivity and temperature resolution as well as photostability. The obtained results open up an avenue for design new class of multifunctional therapeutic agents combining PDT action and thermal sensing. 2. Experimental Tetraphenylporphyrin (TPP) and zinc-containing tetraphenylporphyrin (ZnTPP) have been synthesized according to a previously reported method [28]. Absorption spectra were measured using spectrophotometer Lambda 1050 (Perkin Elmer). Photoluminescence spectroscopy was carried out at modular fluorimeter Fluorolog-3 (Horiba Jobin Yvon) equipped with 450 W Xe lamp as an excitation source. Fluorescence decay curves were performed with time correlated single photon counting (TCSPC) technique at modular fluorimeter Fluorolog-3. Light emission diode (λem = 390 nm, pulse duration 1.1 ns) excited luminescence of porphyrins. Typical experimental conditions for TCSPC measurement were: spectral slit – 3 nm, repetition rate – 1 MHz, TAC range – 50 or 100 ns. Fluorescence lifetimes were obtained via standard deconvolution procedure using DAS 6 software developed by Horiba Jobin Yvon. Temperature was controlled using chiller ThermoTek T255P (set point resolution 0.1 °C) during thermal measurements. Average power during photobleaching experiments was 350 μW (power density 9 μW/mm2). 3. Results and discussion Fig. 1a and b show absorption and excitation spectra of TPP solution in benzene. Absorption spectrum consists of strong Soret band (S0–S2 transition) centered at 419 nm and four weak bands called the Q bands indicating S0–S1 transitions: Qy(0,1) (514 nm), Qy(0,0) (549 nm), Qx(0,1) (589 nm), and Qx(0,0) (647 nm). Excitation spectrum was monitored at emission line attributed to the Q(0,1) (λem = 719 nm). The positions of excitation bands were determined to be 418 nm, 513 nm, 547 nm, 591 nm, and 647 nm, which match well with absorption lines positions. Fig. 1c presents emission spectrum of TPP solution in benzene measured upon 418 nm excitation radiation. The obtained spectrum consists of two bands which corresponds to the Q(0,0) (651 nm) and Q(0,1) (719 nm) bands. Both aforementioned lines are assigned to the S1–S0 transition. Noteworthy, that Q(0,0) line is stronger than Q(0,1) one in TPP emission spectrum. The temperature effect on the TPP emission spectrum is shown in Fig. 2a. Temperature was varied within physiological range (20–45 °C). As can be seen, both emission lines gradually decline along with temperature growth. Such behavior is typical for many phosphors and can be explained by thermal quenching effect. Utilizing the fluorescence intensity ratio (FIR) between Q(0,0) and Q(0,1) bands were suggested as an indication of temperature (Fig. 2b). As can be seen, FIR demonstrates monotonic pseudo-linear trend allowing to define information about local temperature from calculated FIR value. To provide optical ratiometric thermometry, two thermally-coupled energy levels are usually required. Nowadays, there are two mechanisms of ratiometric thermometry based on thermally-coupled levels: the first mechanism is based on the thermoequilibrium between excited energy levels, whereas the second one on the thermoequilibrium between two ground energy levels [29,30]. Moreover, recently several scientific groups reported successful ratiometric temperature sensing based on non-thermally coupled levels [31–33]. Both sensing approaches deal with emission lines originated from different excited levels (in case of thermally-coupled ground energy levels, different excitation transition are used to monitor emission intensity). Here, FIR is calculated between emission lines attributed to the transitions from the same excited level, therefore the observed temperature dependence

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Fig. 1. a) Absorption spectrum of TPP solution in benzene; b) excitation spectrum of TPP solution in benzene (λem = 719 nm); c) emission spectrum of TPP solution in benzene (λex = 418 nm); d) TPP energy level diagram.

cannot be explained by the thermal redistribution of electron population of vibrational levels. Uttamlal et al. reported that TPP demonstrates tautomerism in the excited state (internal conversion of trans to cis to trans) [34]. The shift of equilibrium between tautomers along with temperature growth can cause change of emission lines' intensity and, as a result, FIR value. Besides steady state photoluminescence properties, temperature affects also the luminescence lifetime, therefore lifetime can be used for

thermal sensing. Decay curves of the both observed lines centered at 651 nm (Q(0,0)) and 719 nm (Q(0,1)) were measured at different temperatures. It should be noted that all decays demonstrated monoexponential behavior. Luminescence lifetimes as a function of temperature are shown in Fig. 2c and d. One can see that temperature growth results in gradual decline of lifetime, which is monotonic and pseudo-linear. Thus, it can be concluded that TPP can be potentially used as ther

Fig. 2. a) Emission spectra of TPP solution in benzene measured at different temperatures (λex = 418 nm); temperature dependence of b) FIR and c), d) lifetime of TPP solution in benzene.

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mal sensor through two various strategies based on FIR and lifetime measurements. To prove that not only TPP can be used for thermal sensing, metalsubstituted TPP has been also studied. ZnTPP was chosen as an example of metal-substituted tetraphenylporphyrin due to its wide-spreading. Absorption, excitation and emission spectra of ZnTPP solution in benzene were measured (Fig. 3). Absorption spectrum consists of strong Soret band (S0–S2 transition) centered at 422 nm and two weak Q bands indicating S0–S1 transitions: Q(0,1) (550 nm), Q(0,0) (597 nm). Excitation spectrum was monitored at emission line attributed to the Q(0,1) (λem = 646 nm). The positions of excitation bands were determined to be 422, 548, and 589 nm, which match well with absorption lines positions. It should be noted that only two Q-bands were observed in absorption and excitation spectra for ZnTPP sample, whereas TPP demonstrates four Q-bands (Fig. 1). This fact can be explained by higher point symmetry in case of ZnTPP (D4h) comparing with TPP (D2h), which leads to degeneration of excited energy levels. Fig. 3c shows emission spectrum of ZnTPP solution in benzene obtained upon 422 nm excitation radiation. This spectrum consists of two bands corresponding to the Q(0,0) and Q(0,1) bands with maxima at 598 nm and 646 nm, respectively. In ZnTPP solution Q(0,1) line has higher intensity than Q(0,0). Emission spectra of ZnTPP solution in benzene measured at different temperatures are presented in Fig. 4a. Similar to TPP solution, both emission lines demonstrated gradual decline along with temperature growth. Temperature dependence of FIR between Q(0,0) and Q(0,1) bands is shown in Fig. 4b. One can see that FIR displays monotonic pseudo-linear trend, which allows to determine the local temperature in a simple way. Temperature dependence of luminescence lifetimes of ZnTPP solution in benzene is presented in Fig. 4c and d. The fluorescence decay curves were measured for both emission band at 646 nm (Q(0,1)) and 598 nm (Q(0,0)). Similar to TPP sample, all luminescence decays were fitted with single exponential function. As can be seen from Fig. 4c and d, temperature growth leads to monotonic linear decline of lifetime

from 1.92 ns at 20 °C to 1.83 ns at 45 °C (λem = 646 nm) and from 1.95 ns at 20 °C to 1.86 ns at 45 °C (λem = 598 nm). The organic chromophores usually suffered from photobleaching [35]. The evolution of emission intensity was studied as a function of time upon constant excitation radiation (λex = 418 nm). Photobleaching of TPP in benzene was measured for liquid phase and for drops of solution on the cover slip. During 30 min radiation, a slight monotonic decline of emission intensity was observed in both cases (Fig. S1). As can be seen, the total emission intensity decreased by 3% and 9% for TPP solution and TPP drops on cover slip, respectively. Comparing with widely-used organic chromophores (e.g. fluorescein, rhodamine 6 g, coumarin) [36–38], TPP demonstrates a much lower photobleaching effect. As the photobleaching effect is typical for organic chromophores including porphyrins, it is important to study, how it can affect thermal sensing features. Temperature of TPP solution in benzene was calculated using FIR, which was obtained from emission spectra measured during the photobleaching study. From Fig. S2a, which shows plot of temperature versus irradiation time, one can conclude that observed photobleaching does not interfere in temperature determination via FIR technique. This fact can be explained by the total emission intensity decrease without redistribution upon irradiation. Average calculated temperature of TPP solution in benzene during the photobleaching experiment was determined to be 23.1 °C, which matches well with real temperature of 23 °C (Fig. S2b). Optical properties of porphyrin solutions strongly depend on solvents [39]. Therefore, it was checked whether the thermal sensing ability is maintained for solutions in polar solvent. Acetone was chosen as an example of a polar solvent. Absorption and photoluminescence studies of TPP and ZnTPP solutions in acetone were carried out. Absorption spectrum of TPP solution in acetone included strong Soret band (414 nm) and four weak Q-bands (511, 548, 589, and 650 nm) (Fig. S3a). Excitation spectrum was monitored at emission line attributed to the Q(0,1) (λem = 716 nm) (Fig. S3b). It consisted of following bands: Soret band (414 nm), Qy(0,1) (510 nm), Qy(0,0) (544 nm), Qx

Fig. 3. a) Absorption spectrum of ZnTPP solution in benzene; b) excitation spectrum of ZnTPP solution in benzene (λem = 646 nm); c) emission spectrum of ZnTPP solution in benzene (λex = 422 nm); d) ZnTPP energy level diagram.

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Fig. 4. a) Emission spectra of ZnTPP solution in benzene measured at different temperatures (λex = 422 nm); temperature dependence of b) FIR and c), d) lifetime of ZnTPP solution in benzene.

(0,1) (588 nm), and Qx(0,0) (643 nm). Two strong emission lines centered at 648 (Q(0,0)) and 716 nm (Q(0,1)) were observed in emission spectrum of TPP solution in acetone (Fig. S3c). Comparing with TPP in benzene, emission bands of TPP in acetone demonstrated small blue shift. Emission spectra of TPP solution in acetone measured at different temperatures (20–45 °C) upon 414 nm radiation are presented in Fig. S4a. Temperature affected TPP in acetone the same way as TPP in benzene. FIR between Q(0,0) and Q(0,1) bands showed monotonic pseudo-linear decline along with temperature increase (Fig. S4b). The lifetime of TPP solution in acetone as a function of temperature is presented in Fig. S4c. The fluorescence decay curves were obtained by monitoring the most intense emission band at 648 nm (Q(0,1)). All experimental fluorescence decay curves were fitted with single exponential function irrespective temperature. Surprisingly, the obtained lifetime of TPP solution in acetone increased along with temperature growth (from 9.36 ns at 20 °C to 10.22 ns at 45 °C), which contradicts the results obtained for TPP solution in benzene. This phenomenon can be explained by the fact of that TPP is less soluble in acetone than in benzene and that TPP forms aggregates. Along with temperature increase two opposite processes take place in TPP solution in acetone: thermal quenching and disaggregation [40]. So, it can be concluded that only the FIR technique can be exploited for thermal sensing using a TPP solution in acetone. The absorption spectrum of ZnTPP solution in acetone consisted of strong Soret band (422 nm) and two weak Q-bands (549 and 597 nm) (Fig. S5a). Excitation spectrum monitored at emission band of 653 nm includes Soret band (420 nm), Q(0,1) (550 nm) and Q(0,0) (592 nm) (Fig. S5b). Emission spectrum of ZnTPP solution in acetone is composed from two bands centered at 601 (Q(0,0)) and 653 nm (Q (0,1)) (Fig. S5c). Emission lines of ZnTPP solution in acetone shifts to longer wavelength comparing with emission lines of ZnTPP solution in benzene. Fig. S6a shows the dependence of emission spectra of ZnTPP solution in acetone on temperature. Evolution of FIR between Q(0,0) and Q(0,1) bands demonstrates monotonic pseudo-linear decrease along with

temperature growth (Fig. S6b). Fluorescence decay measurements of ZnTPP solution (λem = 653 nm) in acetone performed at different temperatures revealed mono-exponential behavior independent on temperature. One can see that temperature growth results in a gradual decrease of lifetime from 2.11 ns at 20 °C to 2.05 ns at 45 °C (Fig. S6c). One of the key parameters of luminescence thermometers is sensitivity, which is defined as a quotient of the change in a monitoring parameter and the change in the temperature value [41]: ∂Q S ¼ ∂T

ð1Þ

Sensitivity depends on the value of the measured quantity, so it could not be used for the comparison of results obtained using different measuring systems. Even with the same measuring system, sensitivity can change if different detection amplification gains or different excitation intensities are used. To overcome this problem and to compare the thermal performances between different thermometers irrespective of their nature and sensing parameter, the relative sensitivity should be Table 1 Relative sensitivity (Sr) and temperature resolution (ΔT) of TPP and ZnTPP luminescence thermometers based on FIR and lifetime approaches. Material FIR TPP ZnTPP

Lifetime TPP ZnTPP

Solvent

Sr (% °C−1)

ΔT (°C)

Benzene Acetone Benzene Acetone

0.15 0.15 0.25 0.14

0.9 0.2 0.8 0.8

Benzene Acetone Benzene Acetone

0.24 – 0.18 0.12

0.5 – 0.9 1.6

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Fig. 5. Thermal heating-cooling cycles of TPP solution in benzene. Temperature was determined using a) FIR and lifetimes measured at b) 651 nm, c) 719 nm.

calculated: 1 ∂Q ∙100% Sr ¼ Q ∂T

ð2Þ

The relative sensitivities of TPP and ZnTPP in benzene and acetone utilizing FIR and lifetime as temperature dependent parameter were calculated. The variations of the Sr values with temperature from 20 to 45 °C for FIR and lifetime techniques are shown in Fig. S7, whereas Sr values obtained at T = 20 °C are listed in Table 1. It should be noted that Sr demonstrates monotonic increase along with temperature growth independently on sensing parameter, used substance and solvent. Besides relative sensitivity, temperature resolution (ΔT) defines quality of luminescence thermometer [42,43]. ΔT indicates the smallest change in a temperature that causes an observable change in the monitored parameter. The temperature resolution can be determined using several methods, which were performed and compared in our earlier paper [44]. Here, the temperature resolution was obtained from calibration curve: ΔT ¼

1 δQ Sr Q

ð3Þ

where δQ/Q is the relative uncertainty in the determination of the temperature dependent parameter. ΔT values calculated for T = 20 °C are presented in Table 1. From Table 1, one can see that the best relative sensitivity was found to be 0.25% °C−1, whereas FIR and lifetime sensing techniques demonstrated similar sensitivities. TPP in acetone has the best temperature resolution of 0.2 °C. Noteworthy, almost all regarded thermometers possess sub-degree resolution, which makes them prospective candidates for precise contactless thermal sensing. Repeatability is another important parameter for thermal sensors. It defines stability of temperature measurements carried out with the same experimental conditions [45]. Fig. 5 presents the thermal cycling experiment with TPP solution in benzene, where the temperature was varied in consecutive heating-cooling cycles (20–40 °C). FIR and lifetimes were used as a temperature dependent parameter. It should be noted that FIR and lifetimes as well as the control method gives similar results taking into account thermal uncertainties. Thus, contactless temperature detection using luminescence of porphyrins is repeatable and reversible after several cycles, which indicates the reliability of such sensing technique. 4. Conclusions In summary, it was demonstrated that free-based and metalsubstituted tetraphenylporphyrins can be used as non-contact luminescence temperature sensors. Thermal sensing can be provided based on any of following temperature dependent parameters: FIR and lifetime. Both FIR and lifetime demonstrated a linear decline along with temperature increase within biological temperature range, which facilitates

thermal sensing. Thermometric performance of TPP and ZnTPP solutions was discussed in terms of relative sensitivity and temperature resolution. The maximal sensitivity was found to be 0.25% °C−1 and the best temperature resolution was 0.2 °C. TPP solution decreased emission intensity by 3% during 30 min radiation, which makes it suitable for long luminescence measurements. It was verified that a change in solvent did not affect the thermal sensing ability of TPP and ZnTPP solutions. Thus, the obtained results open an avenue towards the design and use of water-soluble porphyrins for accurate non-contact luminescence thermometry. CRediT authorship contribution statement I.E. Kolesnikov:Conceptualization, Methodology, Investigation, Writing - original draft.A.A. Kalinichev:Conceptualization, Investigation, Visualization.M.A. Kurochkin:Investigation, Visualization.E. Yu Kolesnikov:Validation, Formal analysis.E. Lähderanta:Conceptualization, Supervision, Writing - review & editing. Acknowledgments The authors are grateful to Dr. A. Konev for providing TPP and ZnTPP samples. The experimental measurements were carried out in «Center for Optical and Laser materials research». Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.matdes.2019.108188. References [1] R. Giovannetti, The use of spectrophotometry UV–vis for the study of porphyrins, Macro to Nano Spectrosc, IntechOpen, 2012. [2] S. Hiroto, Y. Miyake, H. Shinokubo, Synthesis and functionalization of porphyrins through organometallic methodologies, Chem. Rev. 117 (2016) 2910–3043. [3] K. Kadish, K.M. Smith, R. Guilard, The Porphyrin Handbook, Elsevier, 2000. [4] D. Dolphin, The Porphyrins V7: Biochemistry, Elsevier, 2012. [5] Z. Wang, C.-Y. Zhu, H.-S. Zhao, S.-Y. Yin, S.-J. Wang, J.-H. Zhang, J.-J. Jiang, M. Pan, C.Y. Su, Record high cationic dye separation performance for water sanitation using a neutral coordination framework, J. Mater. Chem. A 7 (2019) 4751–4758. [6] Z. Wang, J.-H. Zhang, C.-Y. Zhu, S.-Y. Yin, M. Pan, Tunable luminescence and white light emission of porphyrin-zinc coordination assemblies, J. Porphyr. Phthalocyanines. 22 (2018) 821–830. [7] Z. Wang, J.-H. Zhang, J.-J. Jiang, H.-P. Wang, Z.-W. Wei, X. Zhu, M. Pan, C.-Y. Su, A stable metal cluster-metalloporphyrin MOF with high capacity for cationic dye removal, J. Mater. Chem. A 6 (2018) 17698–17705. [8] D. Yang, G. Yang, P. Yang, R. Lv, S. Gai, C. Li, F. He, J. Lin, Assembly of Au plasmonic photothermal agent and iron oxide nanoparticles on ultrathin black phosphorus for targeted photothermal and photodynamic cancer therapy, Adv. Funct. Mater. 27 (2017), 1700371. [9] M. Pei, X. Jia, P. Liu, Design of Janus-like PMMA-PEG-FA grafted fluorescent carbon dots and their nanoassemblies for leakage-free tumor theranostic application, Mater. Des. 155 (2018) 288–296. [10] Z. Wang, S. Gai, C. Wang, G. Yang, C. Zhong, Y. Dai, F. He, D. Yang, P. Yang, Selfassembled zinc phthalocyanine nanoparticles as excellent photothermal/photodynamic synergistic agent for antitumor treatment, Chem. Eng. J. 361 (2019) 117–128. [11] S. Gai, G. Yang, P. Yang, F. He, J. Lin, D. Jin, B. Xing, Recent advances in functional nanomaterials for light–triggered cancer therapy, Nano Today 19 (2018) 146–187.

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