Abstract

Innovative biophotonic modalities such as photoacoustic imaging (PAI) have the potential to provide enhanced sensitivity and molecule-specific detection when used with nanoparticles. However, high peak irradiance levels generated by pulsed lasers can lead to modification of plasmonic nanoparticles. Thus, there is an outstanding need to develop practical methods to effectively predict the onset nanoparticle photomodification as well as a need to better understand the process during PAI. To address this need, we studied pulsed laser damage of gold nanorods (GNRs) using turbid phantoms and a multi-spectral near-infrared PAI system, comparing results with spectrophotometric measurements of non-scattering samples. Transmission electron microscopy and Monte Carlo modeling were also performed to elucidate damage processes. In the phantoms, shifts in PAI-detected spectra indicative of GNR damage were initiated at exposure levels one-third of that seen in non-scattering samples, due to turbidity-induced enhancement of subsurface fluence. For exposures approaching established safety limits, damage was detected at depths of up to 12.5 mm. Typically, GNR damage occurred rapidly, over the course of a few laser pulses. This work advances the development of test methods and numerical models as tools for assessment of nanoparticle damage and its implications, and highlights the importance of considering GNR damage in development of PAI products, even for exposures well below laser safety limits.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (3)

P. Li, Y. Wu, D. Li, X. Su, C. Luo, Y. Wang, J. Hu, G. Li, H. Jiang, and W. Zhang, “Seed-Mediated Synthesis of Tunable-Aspect-Ratio Gold Nanorods for Near-Infrared Photoacoustic Imaging,” Nanoscale Res. Lett. 13(1), 313 (2018).
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A. M. Wilson, J. Mazzaferri, É. Bergeron, S. Patskovsky, P. Marcoux-Valiquette, S. Costantino, P. Sapieha, and M. Meunier, “In Vivo Laser-Mediated Retinal Ganglion Cell Optoporation Using KV1.1 Conjugated Gold Nanoparticles,” Nano Lett. 18(11), 6981–6988 (2018).
[Crossref] [PubMed]

2017 (3)

C. Paviolo and P. R. Stoddart, “Gold Nanoparticles for Modulating Neuronal Behavior,” Nanomaterials (Basel) 7(4), 92 (2017).
[Crossref] [PubMed]

D. A. Nedosekin, T. Fahmi, Z. A. Nima, J. Nolan, C. Cai, M. Sarimollaoglu, E. Dervishi, A. Basnakian, A. S. Biris, and V. P. Zharov, “Photoacoustic in vitro flow cytometry for nanomaterial research,” Photoacoustics 6, 16–25 (2017).
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[Crossref] [PubMed]

2016 (7)

W. C. Vogt, C. Jia, K. A. Wear, B. S. Garra, and T. Joshua Pfefer, “Biologically relevant photoacoustic imaging phantoms with tunable optical and acoustic properties,” J. Biomed. Opt. 21(10), 101405 (2016).
[Crossref] [PubMed]

Y. Du, Q. Jiang, N. Beziere, L. Song, Q. Zhang, D. Peng, C. Chi, X. Yang, H. Guo, G. Diot, V. Ntziachristos, B. Ding, and J. Tian, “DNA-Nanostructure-Gold-Nanorod Hybrids for Enhanced In Vivo Optoacoustic Imaging and Photothermal Therapy,” Adv. Mater. 28(45), 10000–10007 (2016).
[Crossref] [PubMed]

C. J. DeSantis, D. Huang, H. Zhang, N. J. Hogan, H. Zhao, Y. Zhang, A. Manjavacas, Y. Zhang, W.-S. Chang, P. Nordlander, S. Link, and N. J. Halas, “Laser-Induced Spectral Hole-Burning through a Broadband Distribution of Au Nanorods,” J. Phys. Chem. C 120(37), 20518–20524 (2016).
[Crossref]

Y. Wang and L. Guo, “Nanomaterial-Enabled Neural Stimulation,” Front. Neurosci. 10(69), 69 (2016).
[PubMed]

L. Gentemann, S. Kalies, M. Coffee, H. Meyer, T. Ripken, A. Heisterkamp, R. Zweigerdt, and D. Heinemann, “Modulation of cardiomyocyte activity using pulsed laser irradiated gold nanoparticles,” Biomed. Opt. Express 8(1), 177–192 (2016).
[Crossref] [PubMed]

R. Xiong, S. K. Samal, J. Demeester, and et al.., “Laser-assisted photoporation: fundamentals, technological advances and applications,” Advances in Physics: X 1(4), 596–620 (2016).

E. Y. Lukianova-Hleb, Y.-S. Kim, I. Belatsarkouski, A. M. Gillenwater, B. E. O’Neill, and D. O. Lapotko, “Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles,” Nat. Nanotechnol. 11(6), 525–532 (2016).
[Crossref] [PubMed]

2015 (3)

M. Lakshman and A. Needles, “Screening and quantification of the tumor microenvironment with micro-ultrasound and photoacoustic imaging,” Nat. Methods 12(4), 372 (2015).
[Crossref]

J. Zhong, L. Wen, S. Yang, L. Xiang, Q. Chen, and D. Xing, “Imaging-guided high-efficient photoacoustic tumor therapy with targeting gold nanorods,” Nanomedicine (Lond.) 11(6), 1499–1509 (2015).
[Crossref] [PubMed]

W. Li and X. Chen, “Gold nanoparticles for photoacoustic imaging,” Nanomedicine (Lond.) 10(2), 299–320 (2015).
[Crossref] [PubMed]

2014 (3)

L. Cavigli, M. de Angelis, F. Ratto, P. Matteini, F. Rossi, S. Centi, F. Fusi, and R. Pini, “Size Affects the Stability of the Photoacoustic Conversion of Gold Nanorods,” J. Phys. Chem. C 118(29), 16140–16146 (2014).
[Crossref]

T. Gould, Q. Wang, and T. J. Pfefer, “Optical-thermal light-tissue interactions during photoacoustic breast imaging,” Biomed. Opt. Express 5(3), 832–847 (2014).
[Crossref] [PubMed]

G. B. Braun, T. Friman, H.-B. Pang, A. Pallaoro, T. Hurtado de Mendoza, A.-M. A. Willmore, V. R. Kotamraju, A. P. Mann, Z.-G. She, K. N. Sugahara, N. O. Reich, T. Teesalu, and E. Ruoslahti, “Etchable plasmonic nanoparticle probes to image and quantify cellular internalization,” Nat. Mater. 13(9), 904–911 (2014).
[Crossref] [PubMed]

2013 (1)

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref] [PubMed]

2012 (3)

B. T. Cox, J. G. Laufer, P. C. Beard, and S. R. Arridge, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17, 061202 (2012).

J. V. Jokerst, A. J. Cole, D. Van de Sompel, and S. S. Gambhir, “Gold nanorods for ovarian cancer detection with photoacoustic imaging and resection guidance via Raman imaging in living mice,” ACS Nano 6(11), 10366–10377 (2012).
[Crossref] [PubMed]

E. Herzog, A. Taruttis, N. Beziere, A. A. Lutich, D. Razansky, and V. Ntziachristos, “Optical imaging of cancer heterogeneity with multispectral optoacoustic tomography,” Radiology 263(2), 461–468 (2012).
[Crossref] [PubMed]

2011 (2)

S. Walt, S. C. Colbert, and G. Varoquaux, “The NumPy Array: A Structure for Efficient Numerical Computation,” Comput. Sci. Eng. 13(2), 22–30 (2011).
[Crossref]

M. J. Crow, K. Seekell, J. H. Ostrander, and A. Wax, “Monitoring of receptor dimerization using plasmonic coupling of gold nanoparticles,” ACS Nano 5(11), 8532–8540 (2011).
[Crossref] [PubMed]

2010 (5)

J. Park, A. Estrada, J. A. Schwartz, P. Diagaradjane, S. Krishnan, A. K. Dunn, and J. W. Tunnell, “Intra-organ biodistribution of gold nanoparticles using intrinsic two-photon-induced photoluminescence,” Lasers Surg. Med. 42(7), 630–639 (2010).
[Crossref] [PubMed]

H. Cui and X. Yang, “In vivo imaging and treatment of solid tumor using integrated photoacoustic imaging and high intensity focused ultrasound system,” Med. Phys. 37(9), 4777–4781 (2010).
[Crossref] [PubMed]

A. Taruttis, E. Herzog, D. Razansky, and V. Ntziachristos, “Real-time imaging of cardiovascular dynamics and circulating gold nanorods with multispectral optoacoustic tomography,” Opt. Express 18(19), 19592–19602 (2010).
[Crossref] [PubMed]

L.-C. Chen, C.-W. Wei, J. S. Souris, S.-H. Cheng, C.-T. Chen, C.-S. Yang, P.-C. Li, and L.-W. Lo, “Enhanced photoacoustic stability of gold nanorods by silica matrix confinement,” J. Biomed. Opt. 15(1), 016010 (2010).
[Crossref] [PubMed]

Y.-S. Chen, W. Frey, S. Kim, K. Homan, P. Kruizinga, K. Sokolov, and S. Emelianov, “Enhanced thermal stability of silica-coated gold nanorods for photoacoustic imaging and image-guided therapy,” Opt. Express 18(9), 8867–8878 (2010).
[Crossref] [PubMed]

2009 (2)

C. L. Didychuk, P. Ephrat, A. Chamson-Reig, S. L. Jacques, and J. J. L. Carson, “Depth of photothermal conversion of gold nanorods embedded in a tissue-like phantom,” Nanotechnology 20(19), 195102 (2009).
[Crossref] [PubMed]

E. C. Cho, J. Xie, P. A. Wurm, and Y. Xia, “Understanding the role of surface charges in cellular adsorption versus internalization by selectively removing gold nanoparticles on the cell surface with a I2/KI etchant,” Nano Lett. 9(3), 1080–1084 (2009).
[Crossref] [PubMed]

2008 (2)

2007 (1)

J. D. Hunter, “Matplotlib: A 2D Graphics Environment,” Comput. Sci. Eng. 9(3), 90–95 (2007).
[Crossref]

2006 (1)

2000 (2)

S. Link, C. Burda, B. Nikoobakht, and M. A. El-Sayed, “Laser-Induced Shape Changes of Colloidal Gold Nanorods Using Femtosecond and Nanosecond Laser Pulses,” J. Phys. Chem. B 104(26), 6152–6163 (2000).
[Crossref]

S. Link, Z. L. Wang, and M. A. El-Sayed, “How Does a Gold Nanorod Melt?” J. Phys. Chem. B 104(33), 7867–7870 (2000).
[Crossref]

1999 (1)

S.-S. Chang, C.-W. Shih, C.-D. Chen, W.-C. Lai, and C. R. C. Wang, “The Shape Transition of Gold Nanorods,” Langmuir 15(3), 701–709 (1999).
[Crossref]

1995 (1)

L. Wang, S. L. Jacques, and L. Zheng, “MCML--Monte Carlo modeling of light transport in multi-layered tissues,” Comput. Methods Programs Biomed. 47(2), 131–146 (1995).
[Crossref] [PubMed]

1991 (1)

Arridge, S. R.

B. T. Cox, J. G. Laufer, P. C. Beard, and S. R. Arridge, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17, 061202 (2012).

Basnakian, A.

D. A. Nedosekin, T. Fahmi, Z. A. Nima, J. Nolan, C. Cai, M. Sarimollaoglu, E. Dervishi, A. Basnakian, A. S. Biris, and V. P. Zharov, “Photoacoustic in vitro flow cytometry for nanomaterial research,” Photoacoustics 6, 16–25 (2017).
[Crossref] [PubMed]

Beard, P. C.

B. T. Cox, J. G. Laufer, P. C. Beard, and S. R. Arridge, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt. 17, 061202 (2012).

Belatsarkouski, I.

E. Y. Lukianova-Hleb, Y.-S. Kim, I. Belatsarkouski, A. M. Gillenwater, B. E. O’Neill, and D. O. Lapotko, “Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles,” Nat. Nanotechnol. 11(6), 525–532 (2016).
[Crossref] [PubMed]

Bergeron, É.

A. M. Wilson, J. Mazzaferri, É. Bergeron, S. Patskovsky, P. Marcoux-Valiquette, S. Costantino, P. Sapieha, and M. Meunier, “In Vivo Laser-Mediated Retinal Ganglion Cell Optoporation Using KV1.1 Conjugated Gold Nanoparticles,” Nano Lett. 18(11), 6981–6988 (2018).
[Crossref] [PubMed]

Beziere, N.

Y. Du, Q. Jiang, N. Beziere, L. Song, Q. Zhang, D. Peng, C. Chi, X. Yang, H. Guo, G. Diot, V. Ntziachristos, B. Ding, and J. Tian, “DNA-Nanostructure-Gold-Nanorod Hybrids for Enhanced In Vivo Optoacoustic Imaging and Photothermal Therapy,” Adv. Mater. 28(45), 10000–10007 (2016).
[Crossref] [PubMed]

E. Herzog, A. Taruttis, N. Beziere, A. A. Lutich, D. Razansky, and V. Ntziachristos, “Optical imaging of cancer heterogeneity with multispectral optoacoustic tomography,” Radiology 263(2), 461–468 (2012).
[Crossref] [PubMed]

Biris, A. S.

D. A. Nedosekin, T. Fahmi, Z. A. Nima, J. Nolan, C. Cai, M. Sarimollaoglu, E. Dervishi, A. Basnakian, A. S. Biris, and V. P. Zharov, “Photoacoustic in vitro flow cytometry for nanomaterial research,” Photoacoustics 6, 16–25 (2017).
[Crossref] [PubMed]

Braun, G. B.

G. B. Braun, T. Friman, H.-B. Pang, A. Pallaoro, T. Hurtado de Mendoza, A.-M. A. Willmore, V. R. Kotamraju, A. P. Mann, Z.-G. She, K. N. Sugahara, N. O. Reich, T. Teesalu, and E. Ruoslahti, “Etchable plasmonic nanoparticle probes to image and quantify cellular internalization,” Nat. Mater. 13(9), 904–911 (2014).
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E. C. Cho, J. Xie, P. A. Wurm, and Y. Xia, “Understanding the role of surface charges in cellular adsorption versus internalization by selectively removing gold nanoparticles on the cell surface with a I2/KI etchant,” Nano Lett. 9(3), 1080–1084 (2009).
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Figures (9)

Fig. 1
Fig. 1 Schematic of the photoacoustic imaging (left) and nanorod exposure (right) experimental setups (not to scale).
Fig. 2
Fig. 2 TEM micrographs of the 800-nm resonant nanorods at the indicated radiant exposures. All scale bars are 200 nm.
Fig. 3
Fig. 3 Absorbance spectra of the 800-nm resonant nanorods at different radiant exposures (a), and plasmon peak position as a function of radiant exposure (b). The stock, 5 mJ/cm2, and 10 mJ/cm2 spectra in (a) are overlapped, indicating that nanorod shape is stable at these exposure levels. The 10, 50 and 90% lines in (b) correspond to 13.8 ± 0.7, 23 ± 1, and 40 ± 2 mJ/cm2, respectively.
Fig. 4
Fig. 4 (a) Photoacoustic spectra of the nanorod samples after exposure at 5.0 ± 0.5 mJ/cm2 (left axis, colored lines) compared to spectrophotometric data from the stock sample (right axis, dashed black line). (b) Exposure at 10.0 ± 0.9 mJ/cm2. (c) Exposure at 20 ± 2 mJ/cm2. (d) Exposure at 30 ± 1 mJ/cm2.
Fig. 5
Fig. 5 Calculated fluence (F) map using the optical properties of 1% Intralipid at 800 nm with a normal incidence Gaussian beam (1.25 cm diameter), normalized to the incident radiant exposure (H0). Values greater than zero indicate fluence exceeding the incident radiant exposure.
Fig. 6
Fig. 6 Contour plot of photoacoustic spectra collected from a 5-mm deep tube while scanning along its length in 3-mm steps.
Fig. 7
Fig. 7 (a) Photoacoustic spectra collected from an undamaged (33 mm) and damaged (15 mm) location along the tube length. (b) Photoacoustic images of the tube at an undamaged (33 mm) and damaged (15 mm) location, collected at 800 nm.
Fig. 8
Fig. 8 (a) Photoacoustic signal from the different tubes with 800 nm irradiation at ~20 mJ/cm2 radiant exposure over 1000 pulses. Inset: expanded view of photoacoustic signal over the first 10 pulses. (b) Resultant photoacoustic spectra after irradiation.
Fig. 9
Fig. 9 Photoacoustic peak position acquired from the 4-mm deep tube after irradiation at the specified radiant exposures. The 10, 50, and 90% lines correspond to 3.7 ± 0.2, 8.3 ± 0.5, and 19 ± 1 mJ/cm2, respectively.

Tables (3)

Tables Icon

Table 1 Estimated fluence (mJ/cm2) at each tube depth and radiant exposure using the Monte Carlo simulation data at 800 nm excitation. (*) indicates fluence above the 10% threshold from the dose-response curve in Fig. 3(b) where spectral changes are expected to occur.

Tables Icon

Table 2 Calculated SBR and CNR from the images in Fig. 8(b).

Tables Icon

Table 3 Radiant exposure levels and estimated fluence obtained from the dose-response curve in Fig. 9. These values are compared to those obtained from the cuvette-based spectrophotometric method (Fig. 3(b)).

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