Abstract

Current imaging techniques capable of tracking nanoparticles in vivo supply either a large field of view or cellular resolution, but not both. Here, we demonstrate a multimodality imaging platform of optical coherence tomography (OCT) techniques for high resolution, wide field of view in vivo imaging of nanoparticles. This platform includes the first in vivo images of nanoparticle pharmacokinetics acquired with photothermal OCT (PTOCT), along with overlaying images of microvascular and tissue morphology. Gold nanorods (51.8 ± 8.1 nm by 15.2 ± 3.3 nm) were intravenously injected into mice, and their accumulation into mammary tumors was non-invasively imaged in vivo in three dimensions over 24 hours using PTOCT. Spatial frequency analysis of PTOCT images indicated that gold nanorods reached peak distribution throughout the tumors by 16 hours, and remained well-dispersed up to 24 hours post-injection. In contrast, the overall accumulation of gold nanorods within the tumors peaked around 16 hours post-injection. The accumulation of gold nanorods within the tumors was validated post-mortem with multiphoton microscopy. This shows the utility of PTOCT as part of a powerful multimodality imaging platform for the development of nanomedicines and drug delivery technologies.

© 2014 Optical Society of America

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2013

2012

J. M. Tucker-Schwartz, T. Hong, D. C. Colvin, Y. Q. Xu, and M. C. Skala, “Dual-modality photothermal optical coherence tomography and magnetic-resonance imaging of carbon nanotubes,” Opt. Lett.37(5), 872–874 (2012).
[CrossRef] [PubMed]

H. M. Subhash, H. Xie, J. W. Smith, and O. J. T. McCarty, “Optical detection of indocyanine green encapsulated biocompatible poly (lactic-co-glycolic) acid nanoparticles with photothermal optical coherence tomography,” Opt. Lett.37(5), 981–983 (2012).
[CrossRef] [PubMed]

C. Pache, N. L. Bocchio, A. Bouwens, M. Villiger, C. Berclaz, J. Goulley, M. I. Gibson, C. Santschi, and T. Lasser, “Fast three-dimensional imaging of gold nanoparticles in living cells with photothermal optical lock-in Optical Coherence Microscopy,” Opt. Express20(19), 21385–21399 (2012).
[CrossRef] [PubMed]

G. J. Liu, A. J. Lin, B. J. Tromberg, and Z. P. Chen, “A comparison of Doppler optical coherence tomography methods,” Biomed. Opt. Express3(10), 2669–2680 (2012).
[CrossRef] [PubMed]

J. M. Tucker-Schwartz, T. A. Meyer, C. A. Patil, C. L. Duvall, and M. C. Skala, “In vivo photothermal optical coherence tomography of gold nanorod contrast agents,” Biomed. Opt. Express3(11), 2881–2895 (2012).
[CrossRef] [PubMed]

A. A. Manzoor, L. H. Lindner, C. D. Landon, J. Y. Park, A. J. Simnick, M. R. Dreher, S. Das, G. Hanna, W. Park, A. Chilkoti, G. A. Koning, T. L. M. ten Hagen, D. Needham, and M. W. Dewhirst, “Overcoming Limitations in Nanoparticle Drug Delivery: Triggered, Intravascular Release to Improve Drug Penetration into Tumors,” Cancer Res.72(21), 5566–5575 (2012).
[CrossRef] [PubMed]

2011

G. Y. Guan, R. Reif, Z. H. Huang, and R. K. K. Wang, “Depth profiling of photothermal compound concentrations using phase sensitive optical coherence tomography,” J. Biomed. Opt.16(12), 126003 (2011).
[CrossRef] [PubMed]

Y. Jung, R. Reif, Y. G. Zeng, and R. K. Wang, “Three-Dimensional High-Resolution Imaging of Gold Nanorods Uptake in Sentinel Lymph Nodes,” Nano Lett.11(7), 2938–2943 (2011).
[CrossRef] [PubMed]

A. S. Thakor, J. Jokerst, C. Zavaleta, T. F. Massoud, and S. S. Gambhir, “Gold Nanoparticles: A Revival in Precious Metal Administration to Patients,” Nano Lett.11(10), 4029–4036 (2011).
[CrossRef] [PubMed]

Y. S. Chen, W. Frey, S. Kim, P. Kruizinga, K. Homan, and S. Emelianov, “Silica-Coated Gold Nanorods as Photoacoustic Signal Nanoamplifiers,” Nano Lett.11(2), 348–354 (2011).
[CrossRef] [PubMed]

J. Fang, H. Nakamura, and H. Maeda, “The EPR effect: Unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect,” Adv. Drug Deliv. Rev.63(3), 136–151 (2011).
[CrossRef] [PubMed]

2010

S. K. Libutti, G. F. Paciotti, A. A. Byrnes, H. R. Alexander, W. E. Gannon, M. Walker, G. D. Seidel, N. Yuldasheva, and L. Tamarkin, “Phase I and pharmacokinetic studies of CYT-6091, a novel PEGylated colloidal gold-rhTNF nanomedicine,” Clin. Cancer Res.16(24), 6139–6149 (2010).
[CrossRef] [PubMed]

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]

R. John, R. Rezaeipoor, S. G. Adie, E. J. Chaney, A. L. Oldenburg, M. Marjanovic, J. P. Haldar, B. P. Sutton, and S. A. Boppart, “In vivo magnetomotive optical molecular imaging using targeted magnetic nanoprobes,” Proc. Natl. Acad. Sci. U.S.A.107(18), 8085–8090 (2010).
[CrossRef] [PubMed]

D. Jacob, R. L. Shelton, and B. E. Applegate, “Fourier domain pump-probe optical coherence tomography imaging of Melanin,” Opt. Express18(12), 12399–12410 (2010).
[CrossRef] [PubMed]

A. S. Paranjape, R. Kuranov, S. Baranov, L. L. Ma, J. W. Villard, T. Y. Wang, K. V. Sokolov, M. D. Feldman, K. P. Johnston, and T. E. Milner, “Depth resolved photothermal OCT detection of macrophages in tissue using nanorose,” Biomed. Opt. Express1(1), 2–16 (2010).
[CrossRef] [PubMed]

S. Moon, S. W. Lee, and Z. P. Chen, “Reference spectrum extraction and fixed-pattern noise removal in optical coherence tomography,” Opt. Express18(24), 24395–24404 (2010).
[CrossRef] [PubMed]

2009

A. L. Oldenburg, M. N. Hansen, T. S. Ralston, A. Wei, and S. A. Boppart, “Imaging gold nanorods in excised human breast carcinoma by spectroscopic optical coherence tomography,” J. Mater. Chem.19(35), 6407–6411 (2009).
[CrossRef] [PubMed]

S. D. Perrault, C. Walkey, T. Jennings, H. C. Fischer, and W. C. W. Chan, “Mediating Tumor Targeting Efficiency of Nanoparticles Through Design,” Nano Lett.9(5), 1909–1915 (2009).
[CrossRef] [PubMed]

J. A. Schwartz, A. M. Shetty, R. E. Price, R. J. Stafford, J. C. Wang, R. K. Uthamanthil, K. Pham, R. J. McNichols, C. L. Coleman, and J. D. Payne, “Feasibility Study of Particle-Assisted Laser Ablation of Brain Tumors in Orthotopic Canine Model,” Cancer Res.69(4), 1659–1667 (2009).
[CrossRef] [PubMed]

G. von Maltzahn, J. H. Park, A. Agrawal, N. K. Bandaru, S. K. Das, M. J. Sailor, and S. N. Bhatia, “Computationally Guided Photothermal Tumor Therapy Using Long-Circulating Gold Nanorod Antennas,” Cancer Res.69(9), 3892–3900 (2009).
[CrossRef] [PubMed]

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
[CrossRef] [PubMed]

C. L. Zavaleta, B. R. Smith, I. Walton, W. Doering, G. Davis, B. Shojaei, M. J. Natan, and S. S. Gambhir, “Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A.106(32), 13511–13516 (2009).
[CrossRef] [PubMed]

L. Tong, Q. S. Wei, A. Wei, and J. X. Cheng, “Gold Nanorods as Contrast Agents for Biological Imaging: Optical Properties, Surface Conjugation and Photothermal Effects,” Photochem. Photobiol.85(1), 21–32 (2009).
[CrossRef] [PubMed]

Y. Akiyama, T. Mori, Y. Katayama, and T. Niidome, “The effects of PEG grafting level and injection dose on gold nanorod biodistribution in the tumor-bearing mice,” J. Control. Release139(1), 81–84 (2009).
[CrossRef] [PubMed]

2008

X. M. Qian, X. H. Peng, D. O. Ansari, Q. Yin-Goen, G. Z. Chen, D. M. Shin, L. Yang, A. N. Young, M. D. Wang, and S. M. Nie, “In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags,” Nat. Biotechnol.26(1), 83–90 (2008).
[CrossRef] [PubMed]

W. H. De Jong, W. I. Hagens, P. Krystek, M. C. Burger, A. J. A. M. Sips, and R. E. Geertsma, “Particle size-dependent organ distribution of gold nanoparticles after intravenous administration,” Biomaterials29(12), 1912–1919 (2008).
[CrossRef] [PubMed]

D. C. Adler, S. W. Huang, R. Huber, and J. G. Fujimoto, “Photothermal detection of gold nanoparticles using phase-sensitive optical coherence tomography,” Opt. Express16(7), 4376–4393 (2008).
[CrossRef] [PubMed]

A. Mariampillai, B. A. Standish, E. H. Moriyama, M. Khurana, N. R. Munce, M. K. K. Leung, J. Jiang, A. Cable, B. C. Wilson, I. A. Vitkin, and V. X. D. Yang, “Speckle variance detection of microvasculature using swept-source optical coherence tomography,” Opt. Lett.33(13), 1530–1532 (2008).
[CrossRef] [PubMed]

M. C. Skala, M. J. Crow, A. Wax, and J. A. Izatt, “Photothermal Optical Coherence Tomography of Epidermal Growth Factor Receptor in Live Cells Using Immunotargeted Gold Nanospheres,” Nano Lett.8(10), 3461–3467 (2008).
[CrossRef] [PubMed]

2007

H. S. Choi, W. Liu, P. Misra, E. Tanaka, J. P. Zimmer, B. Itty Ipe, M. G. Bawendi, and J. V. Frangioni, “Renal clearance of quantum dots,” Nat. Biotechnol.25(10), 1165–1170 (2007).
[CrossRef] [PubMed]

T. Akkin, C. Joo, and J. F. de Boer, “Depth-resolved measurement of transient structural changes during action potential propagation,” Biophys. J.93(4), 1347–1353 (2007).
[CrossRef] [PubMed]

A. M. Gobin, M. H. Lee, N. J. Halas, W. D. James, R. A. Drezek, and J. L. West, “Near-infrared resonant nanoshells for combined optical imaging and photothermal cancer therapy,” Nano Lett.7(7), 1929–1934 (2007).
[CrossRef] [PubMed]

A. Agarwal, S. W. Huang, M. O’Donnell, K. C. Day, M. Day, N. Kotov, and S. Ashkenazi, “Targeted gold nanorod contrast agent for prostate cancer detection by photoacoustic imaging,” J. Appl. Phys.102(6), 064701 (2007).
[CrossRef]

A. K. Oyelere, P. C. Chen, X. H. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjug. Chem.18(5), 1490–1497 (2007).
[CrossRef] [PubMed]

N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett.7(4), 941–945 (2007).
[CrossRef] [PubMed]

2006

J. F. Hainfeld, D. N. Slatkin, T. M. Focella, and H. M. Smilowitz, “Gold nanoparticles: a new X-ray contrast agent,” Br. J. Radiol.79(939), 248–253 (2006).
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A. Agarwal, S. W. Huang, M. O’Donnell, K. C. Day, M. Day, N. Kotov, and S. Ashkenazi, “Targeted gold nanorod contrast agent for prostate cancer detection by photoacoustic imaging,” J. Appl. Phys.102(6), 064701 (2007).
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S. W. Jones, R. A. Roberts, G. R. Robbins, J. L. Perry, M. P. Kai, K. Chen, T. Bo, M. E. Napier, J. P. Y. Ting, J. M. Desimone, and J. E. Bear, “Nanoparticle clearance is governed by Th1/Th2 immunity and strain background,” J. Clin. Invest.123(7), 3061–3073 (2013).
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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).
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A. K. Oyelere, P. C. Chen, X. H. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjug. Chem.18(5), 1490–1497 (2007).
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S. D. Perrault, C. Walkey, T. Jennings, H. C. Fischer, and W. C. W. Chan, “Mediating Tumor Targeting Efficiency of Nanoparticles Through Design,” Nano Lett.9(5), 1909–1915 (2009).
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J. F. Hainfeld, D. N. Slatkin, T. M. Focella, and H. M. Smilowitz, “Gold nanoparticles: a new X-ray contrast agent,” Br. J. Radiol.79(939), 248–253 (2006).
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Y. S. Chen, W. Frey, S. Kim, P. Kruizinga, K. Homan, and S. Emelianov, “Silica-Coated Gold Nanorods as Photoacoustic Signal Nanoamplifiers,” Nano Lett.11(2), 348–354 (2011).
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J. G. Fujimoto, “Optical coherence tomography for ultrahigh resolution in vivo imaging,” Nat. Biotechnol.21(11), 1361–1367 (2003).
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B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
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Y. Jung, R. Reif, Y. G. Zeng, and R. K. Wang, “Three-Dimensional High-Resolution Imaging of Gold Nanorods Uptake in Sentinel Lymph Nodes,” Nano Lett.11(7), 2938–2943 (2011).
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G. Y. Guan, R. Reif, Z. H. Huang, and R. K. K. Wang, “Depth profiling of photothermal compound concentrations using phase sensitive optical coherence tomography,” J. Biomed. Opt.16(12), 126003 (2011).
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Wang, T. Y.

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M. C. Skala, M. J. Crow, A. Wax, and J. A. Izatt, “Photothermal Optical Coherence Tomography of Epidermal Growth Factor Receptor in Live Cells Using Immunotargeted Gold Nanospheres,” Nano Lett.8(10), 3461–3467 (2008).
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L. Tong, Q. S. Wei, A. Wei, and J. X. Cheng, “Gold Nanorods as Contrast Agents for Biological Imaging: Optical Properties, Surface Conjugation and Photothermal Effects,” Photochem. Photobiol.85(1), 21–32 (2009).
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L. Tong, Q. S. Wei, A. Wei, and J. X. Cheng, “Gold Nanorods as Contrast Agents for Biological Imaging: Optical Properties, Surface Conjugation and Photothermal Effects,” Photochem. Photobiol.85(1), 21–32 (2009).
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X. M. Qian, X. H. Peng, D. O. Ansari, Q. Yin-Goen, G. Z. Chen, D. M. Shin, L. Yang, A. N. Young, M. D. Wang, and S. M. Nie, “In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags,” Nat. Biotechnol.26(1), 83–90 (2008).
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X. M. Qian, X. H. Peng, D. O. Ansari, Q. Yin-Goen, G. Z. Chen, D. M. Shin, L. Yang, A. N. Young, M. D. Wang, and S. M. Nie, “In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags,” Nat. Biotechnol.26(1), 83–90 (2008).
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X. M. Qian, X. H. Peng, D. O. Ansari, Q. Yin-Goen, G. Z. Chen, D. M. Shin, L. Yang, A. N. Young, M. D. Wang, and S. M. Nie, “In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags,” Nat. Biotechnol.26(1), 83–90 (2008).
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Yuan, F.

M. R. Dreher, W. G. Liu, C. R. Michelich, M. W. Dewhirst, F. Yuan, and A. Chilkoti, “Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers,” J. Natl. Cancer Inst.98(5), 335–344 (2006).
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S. K. Hobbs, W. L. Monsky, F. Yuan, W. G. Roberts, L. Griffith, V. P. Torchilin, and R. K. Jain, “Regulation of transport pathways in tumor vessels: Role of tumor type and microenvironment,” Proc. Natl. Acad. Sci. U.S.A.95(8), 4607–4612 (1998).
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S. K. Libutti, G. F. Paciotti, A. A. Byrnes, H. R. Alexander, W. E. Gannon, M. Walker, G. D. Seidel, N. Yuldasheva, and L. Tamarkin, “Phase I and pharmacokinetic studies of CYT-6091, a novel PEGylated colloidal gold-rhTNF nanomedicine,” Clin. Cancer Res.16(24), 6139–6149 (2010).
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Zavaleta, C.

A. S. Thakor, J. Jokerst, C. Zavaleta, T. F. Massoud, and S. S. Gambhir, “Gold Nanoparticles: A Revival in Precious Metal Administration to Patients,” Nano Lett.11(10), 4029–4036 (2011).
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Zavaleta, C. L.

C. L. Zavaleta, B. R. Smith, I. Walton, W. Doering, G. Davis, B. Shojaei, M. J. Natan, and S. S. Gambhir, “Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A.106(32), 13511–13516 (2009).
[CrossRef] [PubMed]

Zeng, Y. G.

Y. Jung, R. Reif, Y. G. Zeng, and R. K. Wang, “Three-Dimensional High-Resolution Imaging of Gold Nanorods Uptake in Sentinel Lymph Nodes,” Nano Lett.11(7), 2938–2943 (2011).
[CrossRef] [PubMed]

Zimmer, J. P.

H. S. Choi, W. Liu, P. Misra, E. Tanaka, J. P. Zimmer, B. Itty Ipe, M. G. Bawendi, and J. V. Frangioni, “Renal clearance of quantum dots,” Nat. Biotechnol.25(10), 1165–1170 (2007).
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Adv. Drug Deliv. Rev.

J. Fang, H. Nakamura, and H. Maeda, “The EPR effect: Unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect,” Adv. Drug Deliv. Rev.63(3), 136–151 (2011).
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Bioconjug. Chem.

A. K. Oyelere, P. C. Chen, X. H. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjug. Chem.18(5), 1490–1497 (2007).
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Biomaterials

W. H. De Jong, W. I. Hagens, P. Krystek, M. C. Burger, A. J. A. M. Sips, and R. E. Geertsma, “Particle size-dependent organ distribution of gold nanoparticles after intravenous administration,” Biomaterials29(12), 1912–1919 (2008).
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Biomed. Opt. Express

Biophys. J.

T. Akkin, C. Joo, and J. F. de Boer, “Depth-resolved measurement of transient structural changes during action potential propagation,” Biophys. J.93(4), 1347–1353 (2007).
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Br. J. Radiol.

J. F. Hainfeld, D. N. Slatkin, T. M. Focella, and H. M. Smilowitz, “Gold nanoparticles: a new X-ray contrast agent,” Br. J. Radiol.79(939), 248–253 (2006).
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Cancer Res.

J. A. Schwartz, A. M. Shetty, R. E. Price, R. J. Stafford, J. C. Wang, R. K. Uthamanthil, K. Pham, R. J. McNichols, C. L. Coleman, and J. D. Payne, “Feasibility Study of Particle-Assisted Laser Ablation of Brain Tumors in Orthotopic Canine Model,” Cancer Res.69(4), 1659–1667 (2009).
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G. von Maltzahn, J. H. Park, A. Agrawal, N. K. Bandaru, S. K. Das, M. J. Sailor, and S. N. Bhatia, “Computationally Guided Photothermal Tumor Therapy Using Long-Circulating Gold Nanorod Antennas,” Cancer Res.69(9), 3892–3900 (2009).
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A. A. Manzoor, L. H. Lindner, C. D. Landon, J. Y. Park, A. J. Simnick, M. R. Dreher, S. Das, G. Hanna, W. Park, A. Chilkoti, G. A. Koning, T. L. M. ten Hagen, D. Needham, and M. W. Dewhirst, “Overcoming Limitations in Nanoparticle Drug Delivery: Triggered, Intravascular Release to Improve Drug Penetration into Tumors,” Cancer Res.72(21), 5566–5575 (2012).
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Clin. Cancer Res.

S. K. Libutti, G. F. Paciotti, A. A. Byrnes, H. R. Alexander, W. E. Gannon, M. Walker, G. D. Seidel, N. Yuldasheva, and L. Tamarkin, “Phase I and pharmacokinetic studies of CYT-6091, a novel PEGylated colloidal gold-rhTNF nanomedicine,” Clin. Cancer Res.16(24), 6139–6149 (2010).
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Drug Discov. Today

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Invest. Ophthalmol. Vis. Sci.

M. D. Wojtkowski, T. H. Ko, J. G. Fujimoto, T. Bajraszewski, I. Gorczynska, P. Targowski, A. Kowalczyk, J. S. Schuman, and J. S. Duker, “Ultrahigh speed, ultrahigh resolution optical coherence tomography using spectral domain detection,” Invest. Ophthalmol. Vis. Sci.45, U50 (2004).

J. Appl. Phys.

A. Agarwal, S. W. Huang, M. O’Donnell, K. C. Day, M. Day, N. Kotov, and S. Ashkenazi, “Targeted gold nanorod contrast agent for prostate cancer detection by photoacoustic imaging,” J. Appl. Phys.102(6), 064701 (2007).
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J. Biomed. Opt.

G. Y. Guan, R. Reif, Z. H. Huang, and R. K. K. Wang, “Depth profiling of photothermal compound concentrations using phase sensitive optical coherence tomography,” J. Biomed. Opt.16(12), 126003 (2011).
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J. Clin. Invest.

S. W. Jones, R. A. Roberts, G. R. Robbins, J. L. Perry, M. P. Kai, K. Chen, T. Bo, M. E. Napier, J. P. Y. Ting, J. M. Desimone, and J. E. Bear, “Nanoparticle clearance is governed by Th1/Th2 immunity and strain background,” J. Clin. Invest.123(7), 3061–3073 (2013).
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J. Mater. Chem.

A. L. Oldenburg, M. N. Hansen, T. S. Ralston, A. Wei, and S. A. Boppart, “Imaging gold nanorods in excised human breast carcinoma by spectroscopic optical coherence tomography,” J. Mater. Chem.19(35), 6407–6411 (2009).
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J. Natl. Cancer Inst.

M. R. Dreher, W. G. Liu, C. R. Michelich, M. W. Dewhirst, F. Yuan, and A. Chilkoti, “Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers,” J. Natl. Cancer Inst.98(5), 335–344 (2006).
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C. J. Murphy, T. K. Sau, A. M. Gole, C. J. Orendorff, J. X. Gao, L. Gou, S. E. Hunyadi, and T. Li, “Anisotropic metal nanoparticles: Synthesis, assembly, and optical applications,” J. Phys. Chem. B109(29), 13857–13870 (2005).
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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).
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N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett.7(4), 941–945 (2007).
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A. M. Gobin, M. H. Lee, N. J. Halas, W. D. James, R. A. Drezek, and J. L. West, “Near-infrared resonant nanoshells for combined optical imaging and photothermal cancer therapy,” Nano Lett.7(7), 1929–1934 (2007).
[CrossRef] [PubMed]

A. S. Thakor, J. Jokerst, C. Zavaleta, T. F. Massoud, and S. S. Gambhir, “Gold Nanoparticles: A Revival in Precious Metal Administration to Patients,” Nano Lett.11(10), 4029–4036 (2011).
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M. C. Skala, M. J. Crow, A. Wax, and J. A. Izatt, “Photothermal Optical Coherence Tomography of Epidermal Growth Factor Receptor in Live Cells Using Immunotargeted Gold Nanospheres,” Nano Lett.8(10), 3461–3467 (2008).
[CrossRef] [PubMed]

Y. Jung, R. Reif, Y. G. Zeng, and R. K. Wang, “Three-Dimensional High-Resolution Imaging of Gold Nanorods Uptake in Sentinel Lymph Nodes,” Nano Lett.11(7), 2938–2943 (2011).
[CrossRef] [PubMed]

Nat. Biotechnol.

J. G. Fujimoto, “Optical coherence tomography for ultrahigh resolution in vivo imaging,” Nat. Biotechnol.21(11), 1361–1367 (2003).
[CrossRef] [PubMed]

H. S. Choi, W. Liu, P. Misra, E. Tanaka, J. P. Zimmer, B. Itty Ipe, M. G. Bawendi, and J. V. Frangioni, “Renal clearance of quantum dots,” Nat. Biotechnol.25(10), 1165–1170 (2007).
[CrossRef] [PubMed]

X. M. Qian, X. H. Peng, D. O. Ansari, Q. Yin-Goen, G. Z. Chen, D. M. Shin, L. Yang, A. N. Young, M. D. Wang, and S. M. Nie, “In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags,” Nat. Biotechnol.26(1), 83–90 (2008).
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Nat. Med.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
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Opt. Express

Opt. Lett.

Photochem. Photobiol.

L. Tong, Q. S. Wei, A. Wei, and J. X. Cheng, “Gold Nanorods as Contrast Agents for Biological Imaging: Optical Properties, Surface Conjugation and Photothermal Effects,” Photochem. Photobiol.85(1), 21–32 (2009).
[CrossRef] [PubMed]

Proc. Natl. Acad. Sci. U.S.A.

R. John, R. Rezaeipoor, S. G. Adie, E. J. Chaney, A. L. Oldenburg, M. Marjanovic, J. P. Haldar, B. P. Sutton, and S. A. Boppart, “In vivo magnetomotive optical molecular imaging using targeted magnetic nanoprobes,” Proc. Natl. Acad. Sci. U.S.A.107(18), 8085–8090 (2010).
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S. K. Hobbs, W. L. Monsky, F. Yuan, W. G. Roberts, L. Griffith, V. P. Torchilin, and R. K. Jain, “Regulation of transport pathways in tumor vessels: Role of tumor type and microenvironment,” Proc. Natl. Acad. Sci. U.S.A.95(8), 4607–4612 (1998).
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C. L. Zavaleta, B. R. Smith, I. Walton, W. Doering, G. Davis, B. Shojaei, M. J. Natan, and S. S. Gambhir, “Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy,” Proc. Natl. Acad. Sci. U.S.A.106(32), 13511–13516 (2009).
[CrossRef] [PubMed]

Science

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical Coherence Tomography,” Science254(5035), 1178–1181 (1991).
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Other

Arnida, M. M. Janat-Amsbury, A. Ray, C. M. Peterson, and H. Ghandehari, “Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages,” European journal of pharmaceutics and biopharmaceutics: official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e. V 77, 417-423 (2011).

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Figures (7)

Fig. 1
Fig. 1

Contrast agents and PTOCT imaging instrumentation. (a) Extinction spectrum of AuNR samples with an absorption peak of approximately 740 nm, with a representative TEM (inset, scale bar = 100 nm). (b) A fiber-based PTOCT system was constructed for imaging. The titanium sapphire laser was amplitude modulated and used as a photothermal heating source. Mice with dorsal skinfold window chambers containing mammary tumors were intravenously injected with AuNRs into the tail vein and imaged with PTOCT over time. SLD: Superluminescent diode; PC: Polarization controllers; 50/50: Fiber coupler

Fig. 2
Fig. 2

PTOCT signal analysis. (a) AuNRs (dark yellow, top) in optically scattering tissue (bright yellow, top) are identified by the OCT imaging beam (black dashed line, top) by their photothermal heat release signature after absorption of an amplitude-modulated heating beam (red dashed structure, top). Oscillations in heat release from AuNRs cause oscillations in optical path length and thus the phase of the OCT interference pattern over time (bottom). (b) For each PTOCT B-scan, a complex-valued 3D data set is constructed as a function of depth (z), space (x), and time (t) (top left). The temporal derivative of the phase (Φ) of this 3D data set is taken, followed by a temporal Fourier transform (top left). A peak in this Fourier-transformed data at 500 Hz (the amplitude-modulation frequency of the photothermal beam, green-dashed circle) reveals the presence of AuNRs (top right). This analysis is repeated at all spatial positions to reconstruct the 2D cross-sectional PTOCT image, which localizes AuNRs (green pixels, bottom right). The magnitude of the depth-resolved data set provides the traditional OCT structural image (bottom left). Bottom panels show representative OCT and PTOCT images of a solid agarose phantom with AuNRs spatially confined to the left capillary tube (scale bar = 1 mm).

Fig. 3
Fig. 3

Representative in vivo PTOCT image volumes. (a) 3D rendering of mouse 4T1 tumor 16 hours after AuNR injection via the tail vein, with OCT of tissue structure (gray channel), SVOCT of vessel morphology (red channel), and PTOCT of AuNRs (green channel). (b) An angled slice through the 3D volume reveals depth-resolved anatomy, vessel morphology, and AuNR distribution. (c) Removing the structural information reveals the underlying vessels (red) and AuNR distribution (green) in three dimensions. (d) After averaging over the depth dimension, co-registered 2D en face projections of tissue morphology, vessel morphology, and AuNR distribution are visible in the tumor tissue (scale bar = 1 mm).

Fig. 4
Fig. 4

PTOCT signals increase in vivo after AuNR injection. En face projection images of tissue morphology (OCT, gray), vessel morphology (SVOCT, red), and AuNR distribution (PTOCT, green) in a mouse tumor pre-injection, and 2 hours, 16 hours, and 24 hours after injection of either 1X PBS (top) or AuNRs (bottom) in 1X PBS (scale bar = 1 mm). The PTOCT signal appears only after injection of AuNRs. White arrows point to regions of positive PTOCT signal 2 hours after injection.

Fig. 5
Fig. 5

In vivo temporal and spatial tracking of AuNR uptake in tumors using PTOCT. En face PTOCT projection images from all mice 16 hours after injection of either (a) PBS (n = 2) or (b) AuNRs (n = 4) (scale bar = 1 mm). (c) Mean PTOCT signal at each imaging time-point for the two mice injected with PBS and the four mice injected with AuNRs (“preinj” = pre-injection). (d) Mean ± standard error PTOCT signal for all mice injected with either PBS (n = 2) or AuNRs (n = 4). *p<0.05.

Fig. 6
Fig. 6

Spatial frequency content analysis of in vivo PTOCT images reveals an increase in low spatial frequencies over time. (a) PTOCT en face images (top) and accompanying 2D spatial Fourier transforms (bottom) from a representative mouse tumor 2 hours, 16 hours, and 24 hours after injection of AuNRs (scale bar = 1 mm). The red circle highlights the cutoff between high (outside the ring) and low (inside the ring) spatial frequencies. (b) Percent of image energy due to low spatial frequencies over time for four mice injected with AuNRs. (c) Mean ± standard error of the image energy due to low and high spatial frequencies for mice injected with AuNRs (n = 4) over time. *p < 0.05.

Fig. 7
Fig. 7

Validation of AuNR uptake into tumor tissue. Representative 20X multiphoton image of tumor tissue 24 hours after tail vein injection of (a) 1X PBS or (b) AuNRs, imaged ex vivo (scale bar = 100 µm). (b) Mean ± standard error of the multiphoton signal across all ex vivo images from mice injected with either PBS (n = 4 images) or AuNRs (n = 8 images). *p < 0.05

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