Plasmonic Photothermal Therapy in Third and Fourth Biological

Article pubs.acs.org/JPCC

Plasmonic Photothermal Therapy in Third and Fourth Biological Windows E. Doruk Onal* and Kaan Guven Department of Physics, Koc University, 34450 Istanbul, Turkey ABSTRACT: The recently reported third and fourth biological transparency windows located respectively at 1.6−1.9 μm and 2.1−2.3 μm promise deeper light penetration in many tissue types, yet they have not been utilized in photothermal therapy applications. Nanoparticle-assisted photothermal therapy poses a nontrivial optimization problem in which the light absorption efficiency of the nanoparticle has to be maximized subject to various constraints that are imposed by the application environment. Upscaling the typical absorberdominant nanoparticle designs (e.g., rod, sphere) that operate in the first and second transparency windows is not a viable option as they become increasingly inefficient absorbers, and their size can get prohibitively large for internalization into certain cell strains. The present study addresses this issue and suggests a versatile approach for designing both monolithic and self-assembling absorber dominant nanostructures for the new transparency windows. These nanoparticles are lithographically fabricatable; additionally, they are easily adaptable to low-cost, mass production compatible chemical growth methods. We demonstrate up to 40% size reduction and 2-fold increase in absorption efficiency compared to the conventional nanobar design. The overall photothermal performance in third and fourth windows is improved up to 55% per mass and 17-fold per nanoparticle compared to the second window.

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INTRODUCTION Hyperthermia therapy is based on increasing the temperature of a malignant tissue above its standard value(37 °C) to hinder cellular processes. In this context, incorporating metallic nanoparticles (NP) that convert electromagnetic radiation into heat via plasmonic resonances has been widely investigated in the past decade and became known as plasmonic photothermal therapy (PTT). The optical response of a NP is characterized by its scattering (σScat) and absorption cross sections (σAbs). The heating power of a metallic NP under continuous wave illumination is related to the incident light intensity and the absorption cross section of the NP: P = I × σAbs.1 The efficiency of PTT is determined by these two parameters. The amount of light intensity reaching the NP inside a human body is limited by the attenuation of biological tissue whereas the absorption cross section depends on the size, shape and material properties of the NP. Among various materials, gold is the dominant choice for NPs especially in biological applications due to its chemical inertness, biocompatibility and ability to support localized surface plasmon resonance(LSPR). Several studies indicate that a rod-like design is the most efficient geometry for PTT applications.2−4 More recently, NPs with large flat surfaces are shown to demonstrate better internalization properties which led us to replace nanorods with nanobar structures as potentially a more suitable geometry for PTT applications.5 The light penetration problem into the human body is overcome either by using optical fibers inserted through the © 2016 American Chemical Society

body to transmit light into tumors or by utilizing external illumination at specific wavelength bands where human body is most transparent. These wavelength bands are called the biological transparency windows and located in near-infrared (NIR) region of the spectrum. So far, PTT is experimentally demonstrated in NIR-I (700−950 nm)6 and NIR-II (1000− 1350 nm)7 which were discovered in 2001 and 2010 respectively. Recently, advancing photodetectors and optical instruments led to the discovery of new transparency windows at longer wavelengths: NIR-III (1600−1870 nm) and NIR-IV (2100−2300 nm) in 2014 and 2016.8,9 Although radiation in NIR-I and -II is successfully used in PTT applications, utilizing NIR-III and -IV provides significantly better light penetration in various tissue types compared to NIR-I and -II (Table 1). To the best of our knowledge, there is no published study exploring the NPs that can operate in the NIR-III and -IV for PTT applications. The objective of this article is to fill this gap by investigating NP designs that can efficiently operate in these bands. As revealed in this study, upscaling the existing NP designs of NIR-I or II to the NIR-III and -IV is not a feasible solution due to inefficiencies in photothermal conversion and cell intrusion. Received: October 4, 2016 Revised: December 16, 2016 Published: December 17, 2016 684

DOI: 10.1021/acs.jpcc.6b10060 J. Phys. Chem. C 2017, 121, 684−690

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The Journal of Physical Chemistry C Table 1. Comparison of Total Attenuation Length (μm) of Various Tissues in the Biological Transparency Windows total attenuation length (μm)

a

tissue type

NIR-I

NIR-II

NIR-III

NIR-IV

fibulaa prostate normalb prostate cancerc breast normalb breast cancerc rat brainc pig brainb

58 191 115 169 81 192 190

92 331 137 217 124 259 235

114 673 175 274 160 290 279

114 723 176 274 143 248 291

Sordillo et al.10 bSordillo et al.11 cShi et al.9

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COMPUTATIONAL DETAILS In this work we studied several NP designs from solid and contour-shaped gold nanobars to self-assembling gold nanodisk- and nanoring chains. The electromagnetic simulations are performed by a commercial software (Lumerical) which implements a high-frequency finite difference time domain (FDTD) solver. The light excitation is linearly polarized along the long axis of the NP. The frequency dependent complex dielectric function of gold is approximated by the Brendal− Bormann model which is shown to be in very good agreement with experimental observations in the studied wavelength range.12−14 The refractive index of the environment is set to 1.40 which corresponds to that of living cells.15

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RESULTS Gold Nanobars for Photothermal Therapy in NIR-III and NIR-IV. The LSPR of a NP can be adjusted spectrally across the biological transparency windows by modifying its size or geometry. For rod-like NPs, there is almost a linear relation between the NP length and its LSPR wavelength. However, simply scaling up the NP designs reported for PTT applications in NIR-I and II is not enough to adopt them to NIR-III and -IV because of two fundamental drawbacks. The first drawback is that scaling alters the NPs’ dominant response character at its LSPR: Solid gold nanobars (or nanospheres) that are good absorbers (absorb most of the incident radiation) in NIR-I become scatterers (absorb some of the incident radiation but scatter more of it) when scaled to NIR-III or IV. We show this in Figure 1d where the absorption efficiency coefficient (ϕAbs = σAbs/(σAbs + σScat)) of a solid gold nanobar (Figure 1a) is plotted as a function of its length and width. The majority of solid nanobars for NIR-III and -IV are scatterers (ϕAbs < 0.5). In a preceding work, we demonstrated that a contour nanobar which is obtained by introducing a hollow region to the solid nanobar enhances the ϕAbs significantly.16 This manifests itself here by the darkening of the entire plot region in Figure 1, parts e and f, as the colormapped ϕAbs shifts to higher values with increasing contour size. Even though the current research on the cell intrusion mechanism for NPs is not conclusive,17,18 decreasing the dimensions of the NP would likely ease this process in addition to increasing the spatial resolution for thermal spot generation. A comparison among parts d−f of Figure 1 also shows that the NIR-III and -IV active regions shift toward smaller nanobar lengths with increasing contour size which is particularly noticeable for narrower designs (see where the NIR-III and -IV active regions cross the x-axis in Figure 1d−f). Thus, the

Figure 1. Schematic of (a) solid (NB), (b) 50% contour (50% CNB), and (c) 70% contour nanobars (70% CNB) and (d−f) their respective absorption efficiency (ϕAbs) as a function of the nanobar dimensions. Black lines border respectively the regions where the nanobar is resonant in NIR-III or NIR-IV.

contour nanobar design aids in eliminating both of these drawbacks at once. Increasing the absorption efficiency (ϕAbs) is only one aspect as the absolute value of the absorption cross section (σAbs) is the key parameter in maximizing the heat generation. A recent experimental study of PTT in NIR-I employs small gold nanorods (L = 16−45 nm) that have almost 100% absorption efficiency and very high cellular uptake.19 However, due to the very small σAbs, in order to generate enough heat for cell ablation, high laser intensities around 12 W/cm2 were required which is well above the healthy limit (1−2 W/cm2). The intensity could be reduced by increasing the NP concentration but this causes further detrimental effects such as the elevated cytotoxicity. Evidently, designing a NP for PTT involves many trade-offs and requires a multidimensional optimization of absorption efficiency (ϕAbs), NP size and absorption cross section (σAbs). Figure 2 shows the scatter plot of a large number of solid and contour nanobars to benchmark these performance parameters and visually highlight the general strengths of the contour design. The contour nanobars resonant in NIR-III and -IV, on average, achieve 100−200% improvement in absorption efficiency (ϕAbs ∼ 0.4−0.6) depending on the contour percentage (Figure 2a). Furthermore, the contour nanobars provide 15−40% reduction in size compared to solid nanobars (Figure 2b). Regarding the absorption cross section, Figure 2c shows that the contour nanobars crowd along the maximum σAbs trendline. 685

DOI: 10.1021/acs.jpcc.6b10060 J. Phys. Chem. C 2017, 121, 684−690

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The Journal of Physical Chemistry C

Figure 2. Benchmarking the solid nanobar (NB, triangle) and contour nanobars (CNB,star, circle) in terms of absorption efficiency (ϕAbs), nanobar length, and absorption cross section (σAbs) in NIR-III and NIR-IV. The distribution of data due to a large number of solid and contour nanobars provides visual cues on the merits of contour design. Compared to the nanobars, the majority of the contour nanobars provide better ϕAbs (a) and smaller size (b) and accumulate more along the maximum σAbs trend (c). Note also that the maximum σAbs trend shows a universal behavior, independent of the nanobar design.

Figure 3. Comparison of the optical cross sections (absorption and scattering) of solid nanobar (NB), contour nanobar (CNB), nanodisk chain (NDC), nanoring chain (NRC), designed for NIR-III and NIR-IV, respectively. The change in the ordering of the cross section curves from part a to part b and from part e to part f indicates that the contour design transforms the dominant response of the solid nanobar from scatterer to absorber in both NIR III and IV. For the nanoring chains (d, h), scattering is almost completely suppressed, rendering them as highly efficient absorber nanoparticles.

This implies more freedom in design parameters while keeping the σAbs close to its maximum. Figure 2c also highlights the advantages of working in longer wavelength transparency windows (i.e., NIR-III and -IV) as the maximum of the σAbs linearly increases with resonance wavelength. Therefore, heat generation per particle is significantly higher in NIR-III (150%) and NIR-IV (250%) in comparison to NIR-II. As stated before, the relation between the NP size and the cellular uptake is not clearly understood and varies significantly with the cell type and the NP geometry due to the differing mechanisms of endocytosis.20,21 The internalization of a NP is a 2-step process which starts with the adherence of the NP to the cell surface, followed by membrane wrapping and endocytosis. NPs of different shapes and sizes interact differently with the cell membrane. Findings of a recent study show that NPs with large flat surface areas generate stronger adhesion forces between the NP and the cell membrane. Additionally,

geometrical regions with high local curvature promote membrane wrapping and accelerate cellular internalization.5 In the light of these findings, regarding cellular internalization, nanobars have a favorable advantage over the commonly used nanorod design in PTT applications. The internalization of gold NPs smaller than 100 nm for PTT in NIR-I and -II is well-known and reported by a number of studies.2−4,19,22 However, there is need for further experimental evidence to support internalization of the gold nanobars in the dimensions analyzed in this study (300−500 nm). Evidently, size is a less stringent condition for nonmetallic (e.g., polymer) and organic NPs as internalization of such nanostructures up to 3000 nm is experimentally observed.21,23 We decidedly propose an alternative solution to bypass the size limitation of monolithic nanobars: self-assembling NPs. These nanostructures are based on disk/ring shaped NPs with diameter smaller than 100 nm which can first be transferred 686

DOI: 10.1021/acs.jpcc.6b10060 J. Phys. Chem. C 2017, 121, 684−690

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The Journal of Physical Chemistry C

Table 2. Comparison of the Absorption Cross Section (σAbs) and Heating Efficiency per Mass (HEPM) of NPs for Biological Transparency Windowsa NIR window NIR-IV

NIR-III

NIR-II NIR-I

NP type NB 4 CNB 4 NDC 4 NRC 4 NB 3 CNB 3 NDC 3 NRC 3 RISb RISb rod-Ib rod-IIc rod-IIIc

σAbs (m2) 3.15 3.39 3.08 1.51 1.93 2.13 1.48 8.50 2.00 3.00 2.00 2.50 1.40

× × × × × × × × × × × × ×

average σAbs

−13

2.78 × 10

10 10−13 10−13 10−13 10−13 10−13 10−13 10−14 10−14 10−14 10−14 10−16 10−15

−13

1.60 × 10−13

2.00 × 10−14 1.29 × 10−14

HEPM (m2 g−1)

average HEPM

17.6 30.9 21.8 33.2 14.9 27.5 16.9 20.3 21.4 32.1 61.8 32.7 35.4

25.9

19.9

21.4 40.5

a c

Present work: NB, nanobar; CNB, contour nanobar; NDC, nanodisk chains; NRC, nanoring chains. Cited work: RIS, rod-in-shell. bWang et al.33 Jia et al.19

mass (HEPM) and the absorption cross section (σAbs) of NPs operating in NIR I−IV. Overall, longer wavelength transparency windows (NIR-III and -IV) enhance the heat generation per particle (see Avg σAbs in Table 2) by almost a full order of magnitude. On the other hand, HEPM is at its largest in NIR-I (see rightmost column in Table 2) partly due to an outlier data and partly because of the near 100% absorption efficiency of small NPs resonant in NIRI. Nevertheless, it is remarkable that the contour NPs in NIR-IV (i.e., CNB 4 and NRC 4) provide an HEPM value on par with the other NPs listed in NIR-I. Moreover, a comparison of NPs, both in NIR-III and -IV, shows that the contour NPs (CNBs and NRCs) provide 50−90% improvement in HEPM over the noncontoured ones (NBs and NDCs).

individually through the cell membrane and then assembled into a chain to construct a nanobar-like structure inside the cell. We investigate this approach in the next section. Self-Assembling NPs in NIR-III and NIR-IV: Nano Disk and Ring Chains. The self-assembly of nanodisks via DNA or protein assistance is well documented24−28 and was recently demonstrated in intracellular scale.29 A nanodisk chain (NDC) is smaller than its monolithic nanobar counterpart but still resonates at the same wavelength.30 Replacing nanodisks by nanorings would be a simple implementation of the contour design to the self-assembling NP chains. There are both topdown and bottom-up methods for fabricating these nanodisk and nanoring structures.31,32 Biological applications generally require vast number of NPs dispersed in solution and bottomup fabrication techniques can provide low-cost solutions that can easily be scaled for mass production. In our analysis, we utilized nanodisks/rings instead of nanospheres/shells to increase the flat surface area for superior surface adhesion and to create high local curvature for better membrane wrapping, both of which contribute positively to their rate of cellular uptake. For a comparison of the absorption properties of selfassembling nanodisk/nanoring−chains and monolithic solid/ contour nanobars, we picked a sample from each with the same resonance wavelength centered in the NIR-III and -IV. The scattering and absorption cross section spectra of these samples plotted respectively in Figure 3 and indicate that the NRC is the smallest in size and has the highest absorption efficiency both in NIR-III and -IV. If we were to set the size considerations aside, the best performing NP candidate among these would be the contour nanobar with highest absorption cross section among all (7% larger than the solid nanobar) and also providing a moderate reduction in size (18% smaller than the solid nanobar) and in the amount of gold used per NP (40% less than solid nanobar). Although cytotoxicity levels highly depend on particle size, shape and targeted cell type, a generic metric used in measuring the toxicity level is the internalized mass of gold. Normalizing the absorption cross section with the mass of the NP produces a figure-of-merit (heating efficiency per mass) that approximately measures the heating efficiency of various NPs at a normalized toxicity level. Table 2 lists the heating efficiency per

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DISCUSSION PTT is applicable to a wide range of cancer types in different tissues. Each tissue type has its own set of restrictions, from the choice of the transparency window for optimum light penetration to the NP size and shape for optimum cellular internalization. Because of these limitations, each treatment requires a tailored PTT scheme. For tissues that internalizes NPs under certain size limits (200/300 nm for NIR-III/-IV) self-assembling NP chains (NDCs and NRCs) propose a viable option. The self-assembling nanostructures such as NDCs and NRCs come at a cost of increased complexity due to the additional step of intracellular self-assembly. Besides, these selfassembling structures have lower heat generation per particle especially for the case of NRCs (see σAbs in Figure 3 and Table 2). However, in applications where the maximum absorption efficiency of the NP is of primary concern (e.g., photothermal imaging34), NRCs perform better than NDCs in suppressing the scattering induced noise and interference. Additionally, from the perspective of heat generated per mass of gold, NRCs quite effectively replicate even surpass the efficiency of monolithic contour nanobars (Table 2). One concern in utilizing larger wavelength transparency windows in PTT applications is the absorbance of human tissue and its effects on the selectivity of heating and peripheral photothermal damage. We quantify this by the selectivity contrast (μNP/μbrain) defined here as the ratio of the absorption coefficient of the cell doped with NPs to that of the bare cell. The absorption coefficient of an ensemble of randomly 687

DOI: 10.1021/acs.jpcc.6b10060 J. Phys. Chem. C 2017, 121, 684−690

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The Journal of Physical Chemistry C oriented NPs are estimated at a concentration of 25 pg per cell is calculated as done similar by Cole et al.35 The selectivity contrast gives a rough factor by which the temperature in the tumor cell can be increased compared to the ambient heating generated by the irradiation (Table 3). The contour NPs

dynamic tumor therapy) perform better than any single therapeutic approach.48−50 Another perspective on the multimodal approach is to utilize thermosensitive liposomes as drug delivery agents which are then triggered by the mild heating generated by the NPs.51

Table 3. Peripheral Heating and Selectivity: Comparing the Absorption Coefficients of Rat Brain Tissue with and without NPs

CONCLUSION The NIR-III and -IV biological transparency windows are promising candidates for the future of PTT applications in cancer treatment. These bands offer deeper tissue penetration (up to 2×) and, with well-engineered NP designs, more efficient heat generation. The contour nanobars and selfassembling nanodisk/ring chains presented in this study provide both size reduction and enhanced absorption efficiency, which are two of the critical parameters in the optimization of NPs for PTT. Evidently, NP size, cellular uptake mechanisms, and cytotoxicity impose nonlinear and often nonintuitive constraints that require experimental data to assert the true potential of these nanoparticles. The results reported here can open new opportunities in advancement of photothermal therapy applications by utilizing the newly discovered biological windows and also aid in development of nanoscale heat generation in general from nanocavitation and superheating to plasmonic photocatalysis and photothermal imaging applications.

NIR window

NP type

NIR-IV

NB 4 CNB 4 NDC 4 NRC 4 NB 3 CNB 3 NDC 3 NRC 3 RISb RISb rod-Ib rod-IIc rod-IIIc

NIR-III

NIR-II NIR-I

a

μbrain (mm−1)a μNP (mm−1) 1.44

0.54

0.07 0.004

73.5 128.9 91.0 138.4 62.1 114.4 70.6 84.4 89.0 133.6 257.4 136.2 147.5

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selectivity contrast 51 90 63 96 114 210 130 155 1198 36100 69576 36813 39852

Shi et al.9 bWang et al.33 cJia et al.19

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proposed for NIR-III and -IV can provide about 2 orders of magnitude selectivity contrast, which is sufficiently large. The selectivity contrast of NIR-I is extremely high (in this case, due mostly to the very small absorption coefficient of brain at NIR-I wavelengths). Unfortunately, this does not imply an ultimate photothermal performance in practice due to other relevant factors discussed previously. The chemical growth techniques for producing NPs provide several advantages compared to lithographic techniques. Chemical growth yields high morphological uniformity in mass production and produces single crystalline NPs which exhibit better plasmonic response. The sensitivity to growth conditions enables fine control on NP size and shape, but also introduces a challenge to preserve uniformity across different growth batches. Obviously, commercialization advantages such as lower cost and compatibility to industrial-scale production also introduce decisive factors in the layout.36 The nanodisk and nanoring building blocks are well suited and presently achievable by chemical growth techniques.31,32 While the present work highlights the potential use of the proposed NPs in PTT, they can be implemented in other applications. The enhanced absorption efficiency and size reduction achieved by the contour and self-assembling NP designs can be utilized in chemistry37−39 to improve localization of nanoscale heat generation in superheating and nanocavitation,40,41 plasmonic photocatalysis42,43 and plasmonassisted phase separation.44 Contour design can be exploited for more than increasing absorption efficiency of the NPs. The hollow regions of both the monolithic and the self-assembling nanostructures can be utilized as light triggered drug45 and gene46 delivery vehicles into to the cancer cells. The hollow region can also be filled with a photosensitizer that uses the absorbed energy to produce reactive oxygen species to kill cancer cells (photodynamic tumor therapy).47 Recent studies show that synergistic therapeutic strategies that use multimodal nanoplatforms (e.g., PTT + light-mediated chemotherapy, PTT + photo-

AUTHOR INFORMATION

Corresponding Author

*(E.D.O.) E-mail: [email protected]. ORCID

E. Doruk Onal: 0000-0001-9265-720X Kaan Guven: 0000-0002-1097-5106 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank Koc University for supporting this research. REFERENCES

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DOI: 10.1021/acs.jpcc.6b10060 J. Phys. Chem. C 2017, 121, 684−690

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DOI: 10.1021/acs.jpcc.6b10060 J. Phys. Chem. C 2017, 121, 684−690