Abstract

Fluorescent contrast agents are widely employed in biomedical research. While many studies have reported deep tissue imaging of fluorescent moieties using either fluorescence-based or absorption-based (optoacoustic) imaging systems, no systematic comparison has been performed regarding the actual performance of these imaging modalities in detecting deep-seated fluorescent agents. Herein, an integrated imager combining epi-fluorescence and volumetric optoacoustic imaging capabilities has been employed in order to evaluate image degradation with depth for several commonly-used near-infrared dyes in both modes. We performed controlled experiments in tissue-mimicking phantoms containing deeply embedded targets filled with different concentrations of Alexa Fluor 700, Alexa Fluor 750, indocyanine green (ICG) and IRDye 800CW. The results are further corroborated by multi-modal imaging of ICG through mouse tissues in vivo. It is shown that optoacoustics consistently provides better sensitivity in differentiating fluorescent targets located at depths beyond 2 mm in turbid tissues, as quantified by evaluating image contrast, signal to noise ratio and spatial resolution performance.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (10)

S. J. Sahl, S. W. Hell, and S. Jakobs, “Fluorescence nanoscopy in cell biology,” Nat. Rev. Mol. Cell Biol. 18(11), 685–701 (2017).
[Crossref] [PubMed]

J. B. Grimm, A. K. Muthusamy, Y. Liang, T. A. Brown, W. C. Lemon, R. Patel, R. Lu, J. J. Macklin, P. J. Keller, N. Ji, and L. D. Lavis, “A general method to fine-tune fluorophores for live-cell and in vivo imaging,” Nat. Methods 14(10), 987–994 (2017).
[Crossref] [PubMed]

X. L. Deán-Ben, S. Gottschalk, B. Mc Larney, S. Shoham, and D. Razansky, “Advanced optoacoustic methods for multiscale imaging of in vivo dynamics,” Chem. Soc. Rev. 46(8), 2158–2198 (2017).
[Crossref] [PubMed]

F. J. O. Landa, X. L. Deán-Ben, R. Sroka, and D. Razansky, “Volumetric Optoacoustic Temperature Mapping in Photothermal Therapy,” Sci. Rep. 7(1), 9695 (2017).
[Crossref] [PubMed]

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

P. W. Wright, L. M. Brier, A. Q. Bauer, G. A. Baxter, A. W. Kraft, M. D. Reisman, A. R. Bice, A. Z. Snyder, J. M. Lee, and J. P. Culver, “Functional connectivity structure of cortical calcium dynamics in anesthetized and awake mice,” PLoS One 12(10), e0185759 (2017).
[Crossref] [PubMed]

M. R. Tomaszewski, I. Q. Gonzalez, J. P. O’Connor, O. Abeyakoon, G. J. Parker, K. J. Williams, F. J. Gilbert, and S. E. Bohndiek, “Oxygen Enhanced Optoacoustic Tomography (OE-OT) Reveals Vascular Dynamics in Murine Models of Prostate Cancer,” Theranostics 7(11), 2900–2913 (2017).
[Crossref] [PubMed]

M. T. Berninger, P. Mohajerani, M. Wildgruber, N. Beziere, M. A. Kimm, X. Ma, B. Haller, M. J. Fleming, S. Vogt, M. Anton, A. B. Imhoff, V. Ntziachristos, R. Meier, and T. D. Henning, “Detection of intramyocardially injected DiR-labeled mesenchymal stem cells by optical and optoacoustic tomography,” Photoacoustics 6, 37–47 (2017).
[Crossref] [PubMed]

X. L. Deán-Ben, S. Gottschalk, G. Sela, S. Shoham, and D. Razansky, “Functional optoacoustic neuro-tomography of calcium fluxes in adult zebrafish brain in vivo,” Opt. Lett. 42(5), 959–962 (2017).
[Crossref] [PubMed]

Z. Chen, X. L. Deán-Ben, S. Gottschalk, and D. Razansky, “Hybrid system for in vivo epifluorescence and 4D optoacoustic imaging,” Opt. Lett. 42(22), 4577–4580 (2017).
[Crossref] [PubMed]

2016 (3)

V. Ermolayev, X. L. Dean-Ben, S. Mandal, V. Ntziachristos, and D. Razansky, “Simultaneous visualization of tumour oxygenation, neovascularization and contrast agent perfusion by real-time three-dimensional optoacoustic tomography,” Eur. Radiol. 26(6), 1843–1851 (2016).
[Crossref] [PubMed]

P. J. Cranfill, B. R. Sell, M. A. Baird, J. R. Allen, Z. Lavagnino, H. M. de Gruiter, G. J. Kremers, M. W. Davidson, A. Ustione, and D. W. Piston, “Quantitative assessment of fluorescent proteins,” Nat. Methods 13(7), 557–562 (2016).
[Crossref] [PubMed]

M. Seeger, A. Karlas, D. Soliman, J. Pelisek, and V. Ntziachristos, “Multimodal optoacoustic and multiphoton microscopy of human carotid atheroma,” Photoacoustics 4(3), 102–111 (2016).
[Crossref] [PubMed]

2015 (7)

O. S. Wolfbeis, “An overview of nanoparticles commonly used in fluorescent bioimaging,” Chem. Soc. Rev. 44(14), 4743–4768 (2015).
[Crossref] [PubMed]

W. Jahr, B. Schmid, C. Schmied, F. O. Fahrbach, and J. Huisken, “Hyperspectral light sheet microscopy,” Nat. Commun. 6(1), 7990 (2015).
[Crossref] [PubMed]

R. Cao, J. P. Kilroy, B. Ning, T. Wang, J. A. Hossack, and S. Hu, “Multispectral photoacoustic microscopy based on an optical-acoustic objective,” Photoacoustics 3(2), 55–59 (2015).
[Crossref] [PubMed]

C. J. H. Ho, G. Balasundaram, W. Driessen, R. McLaren, C. L. Wong, U. S. Dinish, A. B. E. Attia, V. Ntziachristos, and M. Olivo, “Multifunctional Photosensitizer-Based Contrast Agents for Photoacoustic Imaging,” Sci. Rep. 4(1), 5342 (2015).
[Crossref] [PubMed]

I. Stoffels, S. Morscher, I. Helfrich, U. Hillen, J. Leyh, N. C. Burton, T. C. Sardella, J. Claussen, T. D. Poeppel, H. S. Bachmann, A. Roesch, K. Griewank, D. Schadendorf, M. Gunzer, and J. Klode, “Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging,” Sci. Transl. Med. 7(317), 317ra199 (2015).
[Crossref] [PubMed]

P. Subochev, A. Orlova, M. Shirmanova, A. Postnikova, and I. Turchin, “Simultaneous photoacoustic and optically mediated ultrasound microscopy: an in vivo study,” Biomed. Opt. Express 6(2), 631–638 (2015).
[Crossref] [PubMed]

X. L. Deán-Ben, A. C. Stiel, Y. Jiang, V. Ntziachristos, G. G. Westmeyer, and D. Razansky, “Light fluence normalization in turbid tissues via temporally unmixed multispectral optoacoustic tomography,” Opt. Lett. 40(20), 4691–4694 (2015).
[Crossref] [PubMed]

2014 (7)

P. W. Winter, A. G. York, D. D. Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

L. Xi, G. Zhou, N. Gao, L. Yang, D. A. Gonzalo, S. J. Hughes, and H. Jiang, “Photoacoustic and fluorescence image-guided surgery using a multifunctional targeted nanoprobe,” Ann. Surg. Oncol. 21(5), 1602–1609 (2014).
[Crossref] [PubMed]

Y. Yamada and S. Okawa, “Diffuse optical tomography: Present status and its future,” Opt. Rev. 21(3), 185–205 (2014).
[Crossref]

A. T. Eggebrecht, S. L. Ferradal, A. Robichaux-Viehoever, M. S. Hassanpour, H. Dehghani, A. Z. Snyder, T. Hershey, and J. P. Culver, “Mapping distributed brain function and networks with diffuse optical tomography,” Nat. Photonics 8(6), 448–454 (2014).
[Crossref] [PubMed]

B. Rao, F. Soto, D. Kerschensteiner, and L. V. Wang, “Integrated photoacoustic, confocal, and two-photon microscope,” J. Biomed. Opt. 19(3), 036002 (2014).
[Crossref] [PubMed]

Z. Guo, S. Park, J. Yoon, and I. Shin, “Recent progress in the development of near-infrared fluorescent probes for bioimaging applications,” Chem. Soc. Rev. 43(1), 16–29 (2014).
[Crossref] [PubMed]

2013 (8)

D. M. Shcherbakova and V. V. Verkhusha, “Near-infrared fluorescent proteins for multicolor in vivo imaging,” Nat. Methods 10(8), 751–754 (2013).
[Crossref] [PubMed]

A. M. Winkler, K. Maslov, and L. V. Wang, “Noise-equivalent sensitivity of photoacoustics,” J. Biomed. Opt. 18(9), 097003 (2013).
[Crossref] [PubMed]

I. Kosik and J. J. L. Carson, “Combined 3D photoacoustic and 2D fluorescence imaging of indocyanine green contrast agent flow,” Proc. SPIE 8581, 858143 (2013).
[Crossref]

X. L. Deán-Ben and D. Razansky, “Functional optoacoustic human angiography with handheld video rate three dimensional scanner,” Photoacoustics 1(3-4), 68–73 (2013).
[Crossref] [PubMed]

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

X. L. Deán-Ben, A. Ozbek, and D. Razansky, “Volumetric real-time tracking of peripheral human vasculature with GPU-accelerated three-dimensional optoacoustic tomography,” IEEE Trans. Med. Imaging 32(11), 2050–2055 (2013).
[Crossref] [PubMed]

Z. Qin, D. J. Hall, M. A. Liss, C. K. Hoh, C. J. Kane, A. M. Wallace, and D. R. Vera, “Optimization via specific fluorescence brightness of a receptor-targeted probe for optical imaging and positron emission tomography of sentinel lymph nodes,” J. Biomed. Opt. 18(10), 101315 (2013).
[Crossref] [PubMed]

Y. Wang, J. Xia, and L. V. Wang, “Deep-tissue photoacoustic tomography of Förster resonance energy transfer,” J. Biomed. Opt. 18(10), 101316 (2013).
[Crossref] [PubMed]

2012 (3)

P. Shao, W. Shi, P. Hajireza, and R. J. Zemp, “Integrated micro-endoscopy system for simultaneous fluorescence and optical-resolution photoacoustic imaging,” J. Biomed. Opt. 17(7), 0760241 (2012).
[Crossref] [PubMed]

A. Ale, V. Ermolayev, E. Herzog, C. Cohrs, M. H. de Angelis, and V. Ntziachristos, “FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography,” Nat. Methods 9(6), 615–620 (2012).
[Crossref] [PubMed]

D. J. Webb and C. M. Brown, “Epi-Fluorescence Microscopy,” Methods Mol. Biol. 931, 29–59 (2012).
[Crossref] [PubMed]

2011 (3)

S. M. van den Wildenberg, B. Prevo, and E. J. Peterman, “A brief introduction to single-molecule fluorescence methods,” Methods Mol. Biol. 783, 81–99 (2011).
[Crossref] [PubMed]

F. Stuker, J. Ripoll, and M. Rudin, “Fluorescence Molecular Tomography: Principles and Potential for Pharmaceutical Research,” Pharmaceutics 3(4), 229–274 (2011).
[Crossref] [PubMed]

X. L. Deán-Ben, D. Razansky, and V. Ntziachristos, “The effects of acoustic attenuation in optoacoustic signals,” Phys. Med. Biol. 56(18), 6129–6148 (2011).
[Crossref] [PubMed]

2010 (1)

2008 (1)

G. Marriott, S. Mao, T. Sakata, J. Ran, D. K. Jackson, C. Petchprayoon, T. J. Gomez, E. Warp, O. Tulyathan, H. L. Aaron, E. Y. Isacoff, and Y. Yan, “Optical lock-in detection imaging microscopy for contrast-enhanced imaging in living cells,” Proc. Natl. Acad. Sci. U.S.A. 105(46), 17789–17794 (2008).
[Crossref] [PubMed]

2007 (2)

E. M. C. Hillman and A. Moore, “All-optical anatomical co-registration for molecular imaging of small animals using dynamic contrast,” Nat. Photonics 1(9), 526–530 (2007).
[Crossref] [PubMed]

D. Razansky and V. Ntziachristos, “Hybrid photoacoustic fluorescence molecular tomography using finite-element-based inversion,” Med. Phys. 34(11), 4293–4301 (2007).
[Crossref] [PubMed]

2004 (1)

B. Yuan, N. Chen, and Q. Zhu, “Emission and absorption properties of indocyanine green in Intralipid solution,” J. Biomed. Opt. 9(3), 497–503 (2004).
[Crossref] [PubMed]

Aaron, H. L.

G. Marriott, S. Mao, T. Sakata, J. Ran, D. K. Jackson, C. Petchprayoon, T. J. Gomez, E. Warp, O. Tulyathan, H. L. Aaron, E. Y. Isacoff, and Y. Yan, “Optical lock-in detection imaging microscopy for contrast-enhanced imaging in living cells,” Proc. Natl. Acad. Sci. U.S.A. 105(46), 17789–17794 (2008).
[Crossref] [PubMed]

Abeyakoon, O.

M. R. Tomaszewski, I. Q. Gonzalez, J. P. O’Connor, O. Abeyakoon, G. J. Parker, K. J. Williams, F. J. Gilbert, and S. E. Bohndiek, “Oxygen Enhanced Optoacoustic Tomography (OE-OT) Reveals Vascular Dynamics in Murine Models of Prostate Cancer,” Theranostics 7(11), 2900–2913 (2017).
[Crossref] [PubMed]

Achorn, O. B.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Ale, A.

A. Ale, V. Ermolayev, E. Herzog, C. Cohrs, M. H. de Angelis, and V. Ntziachristos, “FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography,” Nat. Methods 9(6), 615–620 (2012).
[Crossref] [PubMed]

Allen, J. R.

P. J. Cranfill, B. R. Sell, M. A. Baird, J. R. Allen, Z. Lavagnino, H. M. de Gruiter, G. J. Kremers, M. W. Davidson, A. Ustione, and D. W. Piston, “Quantitative assessment of fluorescent proteins,” Nat. Methods 13(7), 557–562 (2016).
[Crossref] [PubMed]

Andreasson, K. I.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Antaris, A. L.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Anton, M.

M. T. Berninger, P. Mohajerani, M. Wildgruber, N. Beziere, M. A. Kimm, X. Ma, B. Haller, M. J. Fleming, S. Vogt, M. Anton, A. B. Imhoff, V. Ntziachristos, R. Meier, and T. D. Henning, “Detection of intramyocardially injected DiR-labeled mesenchymal stem cells by optical and optoacoustic tomography,” Photoacoustics 6, 37–47 (2017).
[Crossref] [PubMed]

Atochin, D. N.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Attia, A. B. E.

C. J. H. Ho, G. Balasundaram, W. Driessen, R. McLaren, C. L. Wong, U. S. Dinish, A. B. E. Attia, V. Ntziachristos, and M. Olivo, “Multifunctional Photosensitizer-Based Contrast Agents for Photoacoustic Imaging,” Sci. Rep. 4(1), 5342 (2015).
[Crossref] [PubMed]

Bachmann, H. S.

I. Stoffels, S. Morscher, I. Helfrich, U. Hillen, J. Leyh, N. C. Burton, T. C. Sardella, J. Claussen, T. D. Poeppel, H. S. Bachmann, A. Roesch, K. Griewank, D. Schadendorf, M. Gunzer, and J. Klode, “Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging,” Sci. Transl. Med. 7(317), 317ra199 (2015).
[Crossref] [PubMed]

Baird, M. A.

P. J. Cranfill, B. R. Sell, M. A. Baird, J. R. Allen, Z. Lavagnino, H. M. de Gruiter, G. J. Kremers, M. W. Davidson, A. Ustione, and D. W. Piston, “Quantitative assessment of fluorescent proteins,” Nat. Methods 13(7), 557–562 (2016).
[Crossref] [PubMed]

Balasundaram, G.

C. J. H. Ho, G. Balasundaram, W. Driessen, R. McLaren, C. L. Wong, U. S. Dinish, A. B. E. Attia, V. Ntziachristos, and M. Olivo, “Multifunctional Photosensitizer-Based Contrast Agents for Photoacoustic Imaging,” Sci. Rep. 4(1), 5342 (2015).
[Crossref] [PubMed]

Bartelt, A.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Bauer, A. Q.

P. W. Wright, L. M. Brier, A. Q. Bauer, G. A. Baxter, A. W. Kraft, M. D. Reisman, A. R. Bice, A. Z. Snyder, J. M. Lee, and J. P. Culver, “Functional connectivity structure of cortical calcium dynamics in anesthetized and awake mice,” PLoS One 12(10), e0185759 (2017).
[Crossref] [PubMed]

Bawendi, M. G.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Baxter, G. A.

P. W. Wright, L. M. Brier, A. Q. Bauer, G. A. Baxter, A. W. Kraft, M. D. Reisman, A. R. Bice, A. Z. Snyder, J. M. Lee, and J. P. Culver, “Functional connectivity structure of cortical calcium dynamics in anesthetized and awake mice,” PLoS One 12(10), e0185759 (2017).
[Crossref] [PubMed]

Berninger, M. T.

M. T. Berninger, P. Mohajerani, M. Wildgruber, N. Beziere, M. A. Kimm, X. Ma, B. Haller, M. J. Fleming, S. Vogt, M. Anton, A. B. Imhoff, V. Ntziachristos, R. Meier, and T. D. Henning, “Detection of intramyocardially injected DiR-labeled mesenchymal stem cells by optical and optoacoustic tomography,” Photoacoustics 6, 37–47 (2017).
[Crossref] [PubMed]

Beziere, N.

M. T. Berninger, P. Mohajerani, M. Wildgruber, N. Beziere, M. A. Kimm, X. Ma, B. Haller, M. J. Fleming, S. Vogt, M. Anton, A. B. Imhoff, V. Ntziachristos, R. Meier, and T. D. Henning, “Detection of intramyocardially injected DiR-labeled mesenchymal stem cells by optical and optoacoustic tomography,” Photoacoustics 6, 37–47 (2017).
[Crossref] [PubMed]

Bice, A. R.

P. W. Wright, L. M. Brier, A. Q. Bauer, G. A. Baxter, A. W. Kraft, M. D. Reisman, A. R. Bice, A. Z. Snyder, J. M. Lee, and J. P. Culver, “Functional connectivity structure of cortical calcium dynamics in anesthetized and awake mice,” PLoS One 12(10), e0185759 (2017).
[Crossref] [PubMed]

Bischof, T. S.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Bohndiek, S. E.

M. R. Tomaszewski, I. Q. Gonzalez, J. P. O’Connor, O. Abeyakoon, G. J. Parker, K. J. Williams, F. J. Gilbert, and S. E. Bohndiek, “Oxygen Enhanced Optoacoustic Tomography (OE-OT) Reveals Vascular Dynamics in Murine Models of Prostate Cancer,” Theranostics 7(11), 2900–2913 (2017).
[Crossref] [PubMed]

Brier, L. M.

P. W. Wright, L. M. Brier, A. Q. Bauer, G. A. Baxter, A. W. Kraft, M. D. Reisman, A. R. Bice, A. Z. Snyder, J. M. Lee, and J. P. Culver, “Functional connectivity structure of cortical calcium dynamics in anesthetized and awake mice,” PLoS One 12(10), e0185759 (2017).
[Crossref] [PubMed]

Brown, C. M.

D. J. Webb and C. M. Brown, “Epi-Fluorescence Microscopy,” Methods Mol. Biol. 931, 29–59 (2012).
[Crossref] [PubMed]

Brown, T. A.

J. B. Grimm, A. K. Muthusamy, Y. Liang, T. A. Brown, W. C. Lemon, R. Patel, R. Lu, J. J. Macklin, P. J. Keller, N. Ji, and L. D. Lavis, “A general method to fine-tune fluorophores for live-cell and in vivo imaging,” Nat. Methods 14(10), 987–994 (2017).
[Crossref] [PubMed]

Bruns, O. T.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Burton, N. C.

I. Stoffels, S. Morscher, I. Helfrich, U. Hillen, J. Leyh, N. C. Burton, T. C. Sardella, J. Claussen, T. D. Poeppel, H. S. Bachmann, A. Roesch, K. Griewank, D. Schadendorf, M. Gunzer, and J. Klode, “Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging,” Sci. Transl. Med. 7(317), 317ra199 (2015).
[Crossref] [PubMed]

Cao, R.

R. Cao, J. P. Kilroy, B. Ning, T. Wang, J. A. Hossack, and S. Hu, “Multispectral photoacoustic microscopy based on an optical-acoustic objective,” Photoacoustics 3(2), 55–59 (2015).
[Crossref] [PubMed]

Carr, J. A.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Carson, J. J. L.

I. Kosik and J. J. L. Carson, “Combined 3D photoacoustic and 2D fluorescence imaging of indocyanine green contrast agent flow,” Proc. SPIE 8581, 858143 (2013).
[Crossref]

Chang, J.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Chen, C.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Chen, N.

B. Yuan, N. Chen, and Q. Zhu, “Emission and absorption properties of indocyanine green in Intralipid solution,” J. Biomed. Opt. 9(3), 497–503 (2004).
[Crossref] [PubMed]

Chen, O.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Chen, Z.

Chitnis, A.

Christensen, R.

Claussen, J.

I. Stoffels, S. Morscher, I. Helfrich, U. Hillen, J. Leyh, N. C. Burton, T. C. Sardella, J. Claussen, T. D. Poeppel, H. S. Bachmann, A. Roesch, K. Griewank, D. Schadendorf, M. Gunzer, and J. Klode, “Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging,” Sci. Transl. Med. 7(317), 317ra199 (2015).
[Crossref] [PubMed]

Cohrs, C.

A. Ale, V. Ermolayev, E. Herzog, C. Cohrs, M. H. de Angelis, and V. Ntziachristos, “FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography,” Nat. Methods 9(6), 615–620 (2012).
[Crossref] [PubMed]

Coropceanu, I.

O. T. Bruns, T. S. Bischof, D. K. Harris, D. Franke, Y. Shi, L. Riedemann, A. Bartelt, F. B. Jaworski, J. A. Carr, C. J. Rowlands, M. W. B. Wilson, O. Chen, H. Wei, G. W. Hwang, D. M. Montana, I. Coropceanu, O. B. Achorn, J. Kloepper, J. Heeren, P. T. C. So, D. Fukumura, K. F. Jensen, R. K. Jain, and M. G. Bawendi, “Next-generationin vivooptical imaging with short-wave infrared quantum dots,” Nat Biomed Eng 1(4), 56 (2017).
[Crossref] [PubMed]

Cranfill, P. J.

P. J. Cranfill, B. R. Sell, M. A. Baird, J. R. Allen, Z. Lavagnino, H. M. de Gruiter, G. J. Kremers, M. W. Davidson, A. Ustione, and D. W. Piston, “Quantitative assessment of fluorescent proteins,” Nat. Methods 13(7), 557–562 (2016).
[Crossref] [PubMed]

Culver, J. P.

P. W. Wright, L. M. Brier, A. Q. Bauer, G. A. Baxter, A. W. Kraft, M. D. Reisman, A. R. Bice, A. Z. Snyder, J. M. Lee, and J. P. Culver, “Functional connectivity structure of cortical calcium dynamics in anesthetized and awake mice,” PLoS One 12(10), e0185759 (2017).
[Crossref] [PubMed]

A. T. Eggebrecht, S. L. Ferradal, A. Robichaux-Viehoever, M. S. Hassanpour, H. Dehghani, A. Z. Snyder, T. Hershey, and J. P. Culver, “Mapping distributed brain function and networks with diffuse optical tomography,” Nat. Photonics 8(6), 448–454 (2014).
[Crossref] [PubMed]

Dai, H.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Davidson, M. W.

P. J. Cranfill, B. R. Sell, M. A. Baird, J. R. Allen, Z. Lavagnino, H. M. de Gruiter, G. J. Kremers, M. W. Davidson, A. Ustione, and D. W. Piston, “Quantitative assessment of fluorescent proteins,” Nat. Methods 13(7), 557–562 (2016).
[Crossref] [PubMed]

de Angelis, M. H.

A. Ale, V. Ermolayev, E. Herzog, C. Cohrs, M. H. de Angelis, and V. Ntziachristos, “FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography,” Nat. Methods 9(6), 615–620 (2012).
[Crossref] [PubMed]

de Gruiter, H. M.

P. J. Cranfill, B. R. Sell, M. A. Baird, J. R. Allen, Z. Lavagnino, H. M. de Gruiter, G. J. Kremers, M. W. Davidson, A. Ustione, and D. W. Piston, “Quantitative assessment of fluorescent proteins,” Nat. Methods 13(7), 557–562 (2016).
[Crossref] [PubMed]

Dean-Ben, X. L.

V. Ermolayev, X. L. Dean-Ben, S. Mandal, V. Ntziachristos, and D. Razansky, “Simultaneous visualization of tumour oxygenation, neovascularization and contrast agent perfusion by real-time three-dimensional optoacoustic tomography,” Eur. Radiol. 26(6), 1843–1851 (2016).
[Crossref] [PubMed]

Deán-Ben, X. L.

Z. Chen, X. L. Deán-Ben, S. Gottschalk, and D. Razansky, “Hybrid system for in vivo epifluorescence and 4D optoacoustic imaging,” Opt. Lett. 42(22), 4577–4580 (2017).
[Crossref] [PubMed]

X. L. Deán-Ben, S. Gottschalk, G. Sela, S. Shoham, and D. Razansky, “Functional optoacoustic neuro-tomography of calcium fluxes in adult zebrafish brain in vivo,” Opt. Lett. 42(5), 959–962 (2017).
[Crossref] [PubMed]

X. L. Deán-Ben, S. Gottschalk, B. Mc Larney, S. Shoham, and D. Razansky, “Advanced optoacoustic methods for multiscale imaging of in vivo dynamics,” Chem. Soc. Rev. 46(8), 2158–2198 (2017).
[Crossref] [PubMed]

F. J. O. Landa, X. L. Deán-Ben, R. Sroka, and D. Razansky, “Volumetric Optoacoustic Temperature Mapping in Photothermal Therapy,” Sci. Rep. 7(1), 9695 (2017).
[Crossref] [PubMed]

X. L. Deán-Ben, A. C. Stiel, Y. Jiang, V. Ntziachristos, G. G. Westmeyer, and D. Razansky, “Light fluence normalization in turbid tissues via temporally unmixed multispectral optoacoustic tomography,” Opt. Lett. 40(20), 4691–4694 (2015).
[Crossref] [PubMed]

X. L. Deán-Ben and D. Razansky, “Functional optoacoustic human angiography with handheld video rate three dimensional scanner,” Photoacoustics 1(3-4), 68–73 (2013).
[Crossref] [PubMed]

X. L. Deán-Ben, A. Ozbek, and D. Razansky, “Volumetric real-time tracking of peripheral human vasculature with GPU-accelerated three-dimensional optoacoustic tomography,” IEEE Trans. Med. Imaging 32(11), 2050–2055 (2013).
[Crossref] [PubMed]

X. L. Deán-Ben, D. Razansky, and V. Ntziachristos, “The effects of acoustic attenuation in optoacoustic signals,” Phys. Med. Biol. 56(18), 6129–6148 (2011).
[Crossref] [PubMed]

Dehghani, H.

A. T. Eggebrecht, S. L. Ferradal, A. Robichaux-Viehoever, M. S. Hassanpour, H. Dehghani, A. Z. Snyder, T. Hershey, and J. P. Culver, “Mapping distributed brain function and networks with diffuse optical tomography,” Nat. Photonics 8(6), 448–454 (2014).
[Crossref] [PubMed]

Diao, S.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref] [PubMed]

Dinish, U. S.

C. J. H. Ho, G. Balasundaram, W. Driessen, R. McLaren, C. L. Wong, U. S. Dinish, A. B. E. Attia, V. Ntziachristos, and M. Olivo, “Multifunctional Photosensitizer-Based Contrast Agents for Photoacoustic Imaging,” Sci. Rep. 4(1), 5342 (2015).
[Crossref] [PubMed]

Driessen, W.

C. J. H. Ho, G. Balasundaram, W. Driessen, R. McLaren, C. L. Wong, U. S. Dinish, A. B. E. Attia, V. Ntziachristos, and M. Olivo, “Multifunctional Photosensitizer-Based Contrast Agents for Photoacoustic Imaging,” Sci. Rep. 4(1), 5342 (2015).
[Crossref] [PubMed]

Eggebrecht, A. T.

A. T. Eggebrecht, S. L. Ferradal, A. Robichaux-Viehoever, M. S. Hassanpour, H. Dehghani, A. Z. Snyder, T. Hershey, and J. P. Culver, “Mapping distributed brain function and networks with diffuse optical tomography,” Nat. Photonics 8(6), 448–454 (2014).
[Crossref] [PubMed]

Ermolayev, V.

V. Ermolayev, X. L. Dean-Ben, S. Mandal, V. Ntziachristos, and D. Razansky, “Simultaneous visualization of tumour oxygenation, neovascularization and contrast agent perfusion by real-time three-dimensional optoacoustic tomography,” Eur. Radiol. 26(6), 1843–1851 (2016).
[Crossref] [PubMed]

A. Ale, V. Ermolayev, E. Herzog, C. Cohrs, M. H. de Angelis, and V. Ntziachristos, “FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography,” Nat. Methods 9(6), 615–620 (2012).
[Crossref] [PubMed]

Fahrbach, F. O.

W. Jahr, B. Schmid, C. Schmied, F. O. Fahrbach, and J. Huisken, “Hyperspectral light sheet microscopy,” Nat. Commun. 6(1), 7990 (2015).
[Crossref] [PubMed]

Ferradal, S. L.

A. T. Eggebrecht, S. L. Ferradal, A. Robichaux-Viehoever, M. S. Hassanpour, H. Dehghani, A. Z. Snyder, T. Hershey, and J. P. Culver, “Mapping distributed brain function and networks with diffuse optical tomography,” Nat. Photonics 8(6), 448–454 (2014).
[Crossref] [PubMed]

Fleming, M. J.

M. T. Berninger, P. Mohajerani, M. Wildgruber, N. Beziere, M. A. Kimm, X. Ma, B. Haller, M. J. Fleming, S. Vogt, M. Anton, A. B. Imhoff, V. Ntziachristos, R. Meier, and T. D. Henning, “Detection of intramyocardially injected DiR-labeled mesenchymal stem cells by optical and optoacoustic tomography,” Photoacoustics 6, 37–47 (2017).
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Franke, D.

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F. J. O. Landa, X. L. Deán-Ben, R. Sroka, and D. Razansky, “Volumetric Optoacoustic Temperature Mapping in Photothermal Therapy,” Sci. Rep. 7(1), 9695 (2017).
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Stoffels, I.

I. Stoffels, S. Morscher, I. Helfrich, U. Hillen, J. Leyh, N. C. Burton, T. C. Sardella, J. Claussen, T. D. Poeppel, H. S. Bachmann, A. Roesch, K. Griewank, D. Schadendorf, M. Gunzer, and J. Klode, “Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging,” Sci. Transl. Med. 7(317), 317ra199 (2015).
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L. Xi, G. Zhou, N. Gao, L. Yang, D. A. Gonzalo, S. J. Hughes, and H. Jiang, “Photoacoustic and fluorescence image-guided surgery using a multifunctional targeted nanoprobe,” Ann. Surg. Oncol. 21(5), 1602–1609 (2014).
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Biomed. Opt. Express (1)

Chem. Soc. Rev. (3)

X. L. Deán-Ben, S. Gottschalk, B. Mc Larney, S. Shoham, and D. Razansky, “Advanced optoacoustic methods for multiscale imaging of in vivo dynamics,” Chem. Soc. Rev. 46(8), 2158–2198 (2017).
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Eur. Radiol. (1)

V. Ermolayev, X. L. Dean-Ben, S. Mandal, V. Ntziachristos, and D. Razansky, “Simultaneous visualization of tumour oxygenation, neovascularization and contrast agent perfusion by real-time three-dimensional optoacoustic tomography,” Eur. Radiol. 26(6), 1843–1851 (2016).
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IEEE Trans. Med. Imaging (1)

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J. Biomed. Opt. (6)

Z. Qin, D. J. Hall, M. A. Liss, C. K. Hoh, C. J. Kane, A. M. Wallace, and D. R. Vera, “Optimization via specific fluorescence brightness of a receptor-targeted probe for optical imaging and positron emission tomography of sentinel lymph nodes,” J. Biomed. Opt. 18(10), 101315 (2013).
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B. Yuan, N. Chen, and Q. Zhu, “Emission and absorption properties of indocyanine green in Intralipid solution,” J. Biomed. Opt. 9(3), 497–503 (2004).
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A. M. Winkler, K. Maslov, and L. V. Wang, “Noise-equivalent sensitivity of photoacoustics,” J. Biomed. Opt. 18(9), 097003 (2013).
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B. Rao, F. Soto, D. Kerschensteiner, and L. V. Wang, “Integrated photoacoustic, confocal, and two-photon microscope,” J. Biomed. Opt. 19(3), 036002 (2014).
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Y. Wang, J. Xia, and L. V. Wang, “Deep-tissue photoacoustic tomography of Förster resonance energy transfer,” J. Biomed. Opt. 18(10), 101316 (2013).
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Nat Biomed Eng (1)

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Nat. Methods (4)

D. M. Shcherbakova and V. V. Verkhusha, “Near-infrared fluorescent proteins for multicolor in vivo imaging,” Nat. Methods 10(8), 751–754 (2013).
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Y. Yamada and S. Okawa, “Diffuse optical tomography: Present status and its future,” Opt. Rev. 21(3), 185–205 (2014).
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F. Stuker, J. Ripoll, and M. Rudin, “Fluorescence Molecular Tomography: Principles and Potential for Pharmaceutical Research,” Pharmaceutics 3(4), 229–274 (2011).
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Photoacoustics (4)

X. L. Deán-Ben and D. Razansky, “Functional optoacoustic human angiography with handheld video rate three dimensional scanner,” Photoacoustics 1(3-4), 68–73 (2013).
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F. J. O. Landa, X. L. Deán-Ben, R. Sroka, and D. Razansky, “Volumetric Optoacoustic Temperature Mapping in Photothermal Therapy,” Sci. Rep. 7(1), 9695 (2017).
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Figures (4)

Fig. 1
Fig. 1 Lay-out of the hybrid fluorescence-optoacoustic experimental set-up used for the sensitivity comparison. (a) Three-dimensional lay-out of the set-up; (b) Cross sectional view of (a). Tank 1 was filled with a tissue mimicking medium. Tank 2 was filled with distilled water to couple the acoustic signal from the tubing to the transducer array. During the experiment, only the water tank was translated up and down to change the depth of the tubing within the tissue-mimicking medium.
Fig. 2
Fig. 2 Experimental imaging results for the ICG-filled tubing. (a) Fluorescence images captured at different target depths with ICG concentration of 10 μg/ml and 50 μg/ml. Note that each image is normalized to its own maximum value to optimize the contrast. (b) The corresponding optoacoustic single slice images extracted from the reconstructed volumetric image data. Both fluorescence and optoacoustic images were averaged over 1 s acquisitions. (c) Plot of image contrast which was calculated based on the ROIs shown in (a) and (b). (d) FWHM of the tubing diameter extracted from the images in (a) and (b).
Fig. 3
Fig. 3 Image performance comparison for Alexa Fluor 700, Alexa Fluor 750 and IRDye 800CW fluorescent dyes. The left column shows the comparison of image contrast and the right column shows the corresponding FWHM of the tubing extracted from the images. The image contrast was calculated according to the ROIs shown in Figs. 2(a) and 2(b).
Fig. 4
Fig. 4 In vivo mouse imaging results. (a) Photograph of the experiment with the tubing placed under the mouse leg. The red box shows the imaged region. (b) Fluorescence image of the tubing containing ICG at 20 μg/ml concentration. (c) Zoom-in fluorescence image from a smaller ROI indicated by the dashed box in (b). (d) The corresponding maximum intensity projection (MIP) of the 3D optoacoustic image acquired from the same area as in (b). (e) Single slice optoacoustic image of the tubing. (f) SNR plots of fluorescence and optoacoustic image intensity for the ROIs shown in (b). The standard deviation of the noise was calculated in ROI5 containing only water.

Tables (1)

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Table 1 Dye information of ICG [28, 29], AF700 [30], AF750 [30], and IRDye 800CW [31, 35].

Equations (1)

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C=( I sig I bg )/( I sig + I bg ),

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