Abstract

We present a dual modality functional optical coherence tomography and photoacoustic microscopy (OCT-PAM) system. The photoacoustic modality employs an akinetic optical sensor with a large imaging window. This imaging window enables direct reflection mode operation, and a seamless integration of optical coherence tomography (OCT) as a second imaging modality. Functional extensions to the OCT-PAM system include Doppler OCT (DOCT) and spectroscopic PAM (sPAM). This functional and non-invasive imaging system is applied to image zebrafish larvae, demonstrating its capability to extract both morphological and hemodynamic parameters in vivo in small animals, which are essential and critical in preclinical imaging for physiological, pathophysiological and drug response studies.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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    [Crossref]

2019 (3)

C. Liu, J. Liao, L. Chen, J. Chen, R. Ding, X. Gong, C. Cui, Z. Pang, W. Zheng, and L. Song, “The integrated high-resolution reflection-mode photoacoustic and fluorescence confocal microscopy,” Photoacoustics 14, 12–18 (2019).
[Crossref]

L. Ruzicka, D. Howe, S. Ramachandran, S. Toro, C. Van Slyke, Y. Bradford, A. Eagle, D. Fashena, K. Frazer, P. Kalita, P. Mani, R. Martin, S. Moxon, H. Paddock, C. Pich, K. Schaper, X. Shao, A. Singer, and M. Westerfield, “The Zebrafish Information Network: new support for non-coding genes, richer Gene Ontology annotations and the Alliance of Genome Resources,” Nucleic Acids Res. 47(D1), D867–D873 (2019).
[Crossref]

Y. Chang, Y. Hu, Z. Chen, and D. Xing, “Co-impulse multispectral photoacoustic microscopy and optical coherence tomography system using a single supercontinuum laser,” Opt. Lett. 44(18), 4459–4462 (2019).
[Crossref]

2018 (5)

M. Li, Y. Tang, and J. Yao, “Photoacoustic tomography of blood oxygenation: A mini review,” Photoacoustics 10, 65–73 (2018).
[Crossref]

W. Zhang, Y. Li, V. P. Nguyen, Z. Huang, Z. Liu, X. Wang, and Y. M. Paulus, “High-resolution, in vivo multimodal photoacoustic microscopy, optical coherence tomography, and fluorescence microscopy imaging of rabbit retinal neovascularization,” Light: Sci. Appl. 7(1), 103 (2018).
[Crossref]

M. J. Moore, S. El-Rass, Y. Xiao, Y. Wang, X.-Y. Wen, and M. C. Kolios, “Simultaneous ultra-high frequency photoacoustic microscopy and photoacoustic radiometry of zebrafish larvae in vivo,” Photoacoustics 12, 14–21 (2018).
[Crossref]

M. J. Moore, E. M. Strohm, and M. C. Kolios, “Triplex micron-resolution acoustic, photoacoustic, and optical transmission microscopy via photoacoustic radiometry,” Opt. Express 26(17), 22315–22326 (2018).
[Crossref]

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

2017 (2)

2016 (6)

S. Manohar and D. Razansky, “Photoacoustics: a historical review,” Adv. Opt. Photonics 8(4), 586–617 (2016).
[Crossref]

S. Preisser, W. Rohringer, M. Liu, C. Kollmann, S. Zotter, B. Fischer, and W. Drexler, “All-optical highly sensitive akinetic sensor for ultrasound detection and photoacoustic imaging,” Biomed. Opt. Express 7(10), 4171–4186 (2016).
[Crossref]

Z. Chen, S. Yang, and D. Xing, “Optically integrated trimodality imaging system: combined all-optical photoacoustic microscopy, optical coherence tomography, and fluorescence imaging,” Opt. Lett. 41(7), 1636–1639 (2016).
[Crossref]

R. Haindl, W. Trasischker, A. Wartak, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Total retinal blood flow measurement by three beam Doppler optical coherence tomography,” Biomed. Opt. Express 7(2), 287–301 (2016).
[Crossref]

T. R. Djukic, S. Karthik, I. Saveljic, V. Djonov, and N. Filipovic, “Modeling the Behavior of Red Blood Cells within the Caudal Vein Plexus of Zebrafish,” Front. Physiol. 7, 455 (2016).
[Crossref]

K. Pekkan, B. Chang, F. Uslu, K. Mani, C.-Y. Chen, and R. Holzman, “Characterization of zebrafish larvae suction feeding flow using μPIV and optical coherence tomography,” Exp. Fluids 57(7), 112 (2016).
[Crossref]

2015 (5)

R. Haindl, W. Trasischker, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Three-beam Doppler optical coherence tomography using a facet prism telescope and MEMS mirror for improved transversal resolution,” J. Mod. Opt. 62(21), 1781–1788 (2015).
[Crossref]

D. Soliman, G. J. Tserevelakis, M. Omar, and V. Ntziachristos, “Combining microscopy with mesoscopy using optical and optoacoustic label-free modes,” Sci. Rep. 5(1), 12902 (2015).
[Crossref]

W. Song, Q. Wei, W. Liu, T. Liu, J. Yi, N. Sheibani, A. A. Fawzi, R. A. Linsenmeier, S. Jiao, and H. F. Zhang, “A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography,” Sci. Rep. 4(1), 6525 (2015).
[Crossref]

X. Liu, T. Liu, R. Wen, Y. Li, C. A. Puliafito, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy for in vivo multimodal retinal imaging,” Opt. Lett. 40(7), 1370–1373 (2015).
[Crossref]

Z. Chen, S. Yang, Y. Wang, and D. Xing, “All-optically integrated photo-acoustic microscopy and optical coherence tomography based on a single Michelson detector,” Opt. Lett. 40(12), 2838–2841 (2015).
[Crossref]

2014 (2)

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]

J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafish–on the move towards ophthalmological research,” Eye 28(4), 367–380 (2014).
[Crossref]

2013 (1)

L. Wang, K. Maslov, and L. V. Wang, “Single-cell label-free photoacoustic flowoxigraphy in vivo,” Proc. Natl. Acad. Sci. 110(15), 5759–5764 (2013).
[Crossref]

2012 (5)

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. S. Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS One 7(8), e44018 (2012).
[Crossref]

G. Gestri, B. A. Link, and S. C. F. Neuhauss, “The visual system of zebrafish and its use to model human ocular diseases,” Dev. Neurobiol. 72(3), 302–327 (2012).
[Crossref]

J. J. Ganis, N. Hsia, E. Trompouki, J. L. de Jong, A. DiBiase, J. S. Lambert, Z. Jia, P. J. Sabo, M. Weaver, R. Sandstrom, J. A. Stamatoyannopoulos, Y. Zhou, and L. I. Zon, “Zebrafish globin switching occurs in two developmental stages and is controlled by the LCR,” Dev. Biol. (Amsterdam, Neth.) 366(2), 185–194 (2012).
[Crossref]

X. Zhang, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy: accomplishing optical coherence tomography and photoacoustic microscopy with a single light source,” J. Biomed. Opt. 17(3), 030502 (2012).
[Crossref]

S. Ye, R. Yang, J. Xiong, K. K. Shung, Q. Zhou, C. Li, and Q. Ren, “Label-free imaging of zebrafish larvae in vivo by photoacoustic microscopy,” Biomed. Opt. Express 3(2), 360–365 (2012).
[Crossref]

2011 (2)

S. Kim, Y.-S. Chen, G. P. Luke, and S. Y. Emelianov, “In vivo three-dimensional spectroscopic photoacoustic imaging for monitoring nanoparticle delivery,” Biomed. Opt. Express 2(9), 2540–2550 (2011).
[Crossref]

K. Divakar Rao, P. Upadhyaya, M. Sharma, and P. K. Gupta, “Noninvasive Imaging of Ethanol-Induced Developmental Defects in Zebrafish Embryos Using Optical Coherence Tomography,” Birth Defects Res., Part B 95(1), 7–11 (2011).
[Crossref]

2010 (1)

A. R. Migliaccio, “Erythroblast enucleation,” Haematologica 95(12), 1985–1988 (2010).
[Crossref]

2009 (2)

E. W. Stein, K. Maslov, and L. V. Wang, “Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy,” J. Biomed. Opt. 14(2), 020502 (2009).
[Crossref]

S. S. Kitambi, K. J. McCulloch, R. T. Peterson, and J. J. Malicki, “Small molecule screen for compounds that affect vascular development in the zebrafish retina,” Mech. Dev. 126(5-6), 464–477 (2009).
[Crossref]

2008 (6)

D. Carradice and G. J. Lieschke, “Zebrafish in hematology: sushi or science?” Blood 111(7), 3331–3342 (2008).
[Crossref]

S. Jiao and M. Ruggeri, “Polarization effect on the depth resolution of optical coherence tomography,” J. Biomed. Opt. 13(6), 060503 (2008).
[Crossref]

D. Baldessari and M. Mione, “How to create the vascular tree? (Latest) help from the zebrafish,” Pharmacol. Ther. 118(2), 206–230 (2008).
[Crossref]

A. Szkulmowska, M. Szkulmowski, A. Kowalczyk, and M. Wojtkowski, “Phase-resolved Doppler optical coherence tomography–limitations and improvements,” Opt. Lett. 33(13), 1425–1427 (2008).
[Crossref]

L. Kagemann, H. Ishikawa, J. Zou, P. Charukamnoetkanok, G. Wollstein, K. A. Townsend, M. L. Gabriele, N. Bahary, X. Wei, J. G. Fujimoto, and J. S. Schuman, “Repeated, noninvasive, high resolution spectral domain optical coherence tomography imaging of zebrafish embryos,” Mol. Vis. 14, 2157–2170 (2008).

N. V. Iftimia, D. X. Hammer, R. D. Ferguson, M. Mujat, D. Vu, and A. A. Ferrante, “Dual-beam Fourier domain optical Doppler tomography of zebrafish,” Opt. Express 16(18), 13624–13636 (2008).
[Crossref]

2007 (2)

L. R. Manning, J. E. Russell, J. C. Padovan, B. T. Chait, A. Popowicz, R. S. Manning, and J. M. Manning, “Human embryonic, fetal, and adult hemoglobins have different subunit interface strengths. Correlation with lifespan in the red cell,” Protein Sci. 16(8), 1641–1658 (2007).
[Crossref]

G. Kari, U. Rodeck, and A. P. Dicker, “Zebrafish: An Emerging Model System for Human Disease and Drug Discovery,” Clin. Pharmacol. Ther. (Hoboken, NJ, U. S.) 82(1), 70–80 (2007).
[Crossref]

2006 (1)

A. L. Rubinstein, “Zebrafish assays for drug toxicity screening,” Expert Opin. Drug Metab. Toxicol. 2(2), 231–240 (2006).
[Crossref]

2005 (2)

S. Rieger, R. P. Kulkarni, D. Darcy, S. E. Fraser, and R. W. Köster, “Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos,” Dev. Dyn. 234(3), 670–681 (2005).
[Crossref]

S. Grillitsch, N. Medgyesy, T. Schwerte, and B. Pelster, “The influence of environmental PO2 on hemoglobin oxygen saturation in developing zebrafish Danio rerio,” J. Exp. Biol. 208(2), 309–316 (2005).
[Crossref]

2003 (1)

T. Schwerte, D. Uberbacher, and B. Pelster, “Non-invasive imaging of blood cell concentration and blood distribution in zebrafish Danio rerio incubated in hypoxic conditions in vivo,” J. Exp. Biol. 206(8), 1299–1307 (2003).
[Crossref]

2001 (1)

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The Vascular Anatomy of the Developing Zebrafish: An Atlas of Embryonic and Early Larval Development,” Dev. Biol. (Amsterdam, Neth.) 230(2), 278–301 (2001).
[Crossref]

2000 (1)

B. L. Roman and B. M. Weinstein, “Building the vertebrate vasculature: research is going swimmingly,” BioEssays 22(10), 882–893 (2000).
[Crossref]

1998 (1)

H. W. Detrich, M. Westerfield, and L. I. Zon, “Overview of the Zebrafish system,” Methods Cell Biol. 59, 3–10 (1998).
[Crossref]

1997 (1)

1996 (2)

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Brand, F. J. van Eeden, M. Furutani-Seiki, M. Granato, M. Hammerschmidt, C. P. Heisenberg, Y. J. Jiang, D. A. Kane, M. C. Mullins, and C. Nusslein-Volhard, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

B. Pelster and W. W. Burggren, “Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio),” Circ. Res. 79(2), 358–362 (1996).
[Crossref]

1995 (2)

B. M. Weinstein, D. L. Stemple, W. Driever, and M. C. Fishman, “gridlock, a localized heritable vascular patterning defect in the zebrafish,” Nat. Med. 1(11), 1143–1147 (1995).
[Crossref]

X. J. Wang, T. E. Milner, and J. S. Nelson, “Characterization of fluid flow velocity by optical Doppler tomography,” Opt. Lett. 20(11), 1337–1339 (1995).
[Crossref]

1991 (1)

A. Fercher, C. Hitzenberger, and M. Juchem, “Measurement of Intraocular Optical Distances Using Partially Coherent Laser Light,” J. Mod. Opt. 38(7), 1327–1333 (1991).
[Crossref]

1986 (1)

K. Wada, T. Masujima, H. Yoshida, T. Murakami, N. Yata, and H. Imai, “Application of Photoacoustic Microscopy to Analysis of Biological Components in Tissue Sections,” Chem. Pharm. Bull. 34(4), 1688–1693 (1986).
[Crossref]

1981 (1)

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
[Crossref]

1975 (1)

H. J. Atkinson, “The functional significance of the haemoglobin in a marine nematode, Enoplus brevis (Bastian),” J. Exp. Biol. 62, 1–9 (1975).

Allio, G.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Andreana, M.

Atkinson, H. J.

H. J. Atkinson, “The functional significance of the haemoglobin in a marine nematode, Enoplus brevis (Bastian),” J. Exp. Biol. 62, 1–9 (1975).

Azevedo, A. S.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Bahary, N.

L. Kagemann, H. Ishikawa, J. Zou, P. Charukamnoetkanok, G. Wollstein, K. A. Townsend, M. L. Gabriele, N. Bahary, X. Wei, J. G. Fujimoto, and J. S. Schuman, “Repeated, noninvasive, high resolution spectral domain optical coherence tomography imaging of zebrafish embryos,” Mol. Vis. 14, 2157–2170 (2008).

Bahram, S.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Baldessari, D.

D. Baldessari and M. Mione, “How to create the vascular tree? (Latest) help from the zebrafish,” Pharmacol. Ther. 118(2), 206–230 (2008).
[Crossref]

Baumann, B.

R. Haindl, W. Trasischker, A. Wartak, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Total retinal blood flow measurement by three beam Doppler optical coherence tomography,” Biomed. Opt. Express 7(2), 287–301 (2016).
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R. Haindl, W. Trasischker, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Three-beam Doppler optical coherence tomography using a facet prism telescope and MEMS mirror for improved transversal resolution,” J. Mod. Opt. 62(21), 1781–1788 (2015).
[Crossref]

Bradford, Y.

L. Ruzicka, D. Howe, S. Ramachandran, S. Toro, C. Van Slyke, Y. Bradford, A. Eagle, D. Fashena, K. Frazer, P. Kalita, P. Mani, R. Martin, S. Moxon, H. Paddock, C. Pich, K. Schaper, X. Shao, A. Singer, and M. Westerfield, “The Zebrafish Information Network: new support for non-coding genes, richer Gene Ontology annotations and the Alliance of Genome Resources,” Nucleic Acids Res. 47(D1), D867–D873 (2019).
[Crossref]

Brand, M.

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Brand, F. J. van Eeden, M. Furutani-Seiki, M. Granato, M. Hammerschmidt, C. P. Heisenberg, Y. J. Jiang, D. A. Kane, M. C. Mullins, and C. Nusslein-Volhard, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

Brownlie, A.

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Brand, F. J. van Eeden, M. Furutani-Seiki, M. Granato, M. Hammerschmidt, C. P. Heisenberg, Y. J. Jiang, D. A. Kane, M. C. Mullins, and C. Nusslein-Volhard, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

Burggren, W. W.

B. Pelster and W. W. Burggren, “Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio),” Circ. Res. 79(2), 358–362 (1996).
[Crossref]

Carapito, R.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Carradice, D.

D. Carradice and G. J. Lieschke, “Zebrafish in hematology: sushi or science?” Blood 111(7), 3331–3342 (2008).
[Crossref]

Chabannes, V.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Chait, B. T.

L. R. Manning, J. E. Russell, J. C. Padovan, B. T. Chait, A. Popowicz, R. S. Manning, and J. M. Manning, “Human embryonic, fetal, and adult hemoglobins have different subunit interface strengths. Correlation with lifespan in the red cell,” Protein Sci. 16(8), 1641–1658 (2007).
[Crossref]

Chang, B.

K. Pekkan, B. Chang, F. Uslu, K. Mani, C.-Y. Chen, and R. Holzman, “Characterization of zebrafish larvae suction feeding flow using μPIV and optical coherence tomography,” Exp. Fluids 57(7), 112 (2016).
[Crossref]

Chang, W.

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,” (1991).

Chang, Y.

Charukamnoetkanok, P.

L. Kagemann, H. Ishikawa, J. Zou, P. Charukamnoetkanok, G. Wollstein, K. A. Townsend, M. L. Gabriele, N. Bahary, X. Wei, J. G. Fujimoto, and J. S. Schuman, “Repeated, noninvasive, high resolution spectral domain optical coherence tomography imaging of zebrafish embryos,” Mol. Vis. 14, 2157–2170 (2008).

Chen, C.-Y.

K. Pekkan, B. Chang, F. Uslu, K. Mani, C.-Y. Chen, and R. Holzman, “Characterization of zebrafish larvae suction feeding flow using μPIV and optical coherence tomography,” Exp. Fluids 57(7), 112 (2016).
[Crossref]

Chen, J.

C. Liu, J. Liao, L. Chen, J. Chen, R. Ding, X. Gong, C. Cui, Z. Pang, W. Zheng, and L. Song, “The integrated high-resolution reflection-mode photoacoustic and fluorescence confocal microscopy,” Photoacoustics 14, 12–18 (2019).
[Crossref]

Chen, L.

C. Liu, J. Liao, L. Chen, J. Chen, R. Ding, X. Gong, C. Cui, Z. Pang, W. Zheng, and L. Song, “The integrated high-resolution reflection-mode photoacoustic and fluorescence confocal microscopy,” Photoacoustics 14, 12–18 (2019).
[Crossref]

Chen, Q.

Chen, Y.-S.

Chen, Z.

Chhetri, J.

J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafish–on the move towards ophthalmological research,” Eye 28(4), 367–380 (2014).
[Crossref]

Croix, C. M. S.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. S. Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS One 7(8), e44018 (2012).
[Crossref]

Cui, C.

C. Liu, J. Liao, L. Chen, J. Chen, R. Ding, X. Gong, C. Cui, Z. Pang, W. Zheng, and L. Song, “The integrated high-resolution reflection-mode photoacoustic and fluorescence confocal microscopy,” Photoacoustics 14, 12–18 (2019).
[Crossref]

Darcy, D.

S. Rieger, R. P. Kulkarni, D. Darcy, S. E. Fraser, and R. W. Köster, “Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos,” Dev. Dyn. 234(3), 670–681 (2005).
[Crossref]

Dave, D.

de Jong, J. L.

J. J. Ganis, N. Hsia, E. Trompouki, J. L. de Jong, A. DiBiase, J. S. Lambert, Z. Jia, P. J. Sabo, M. Weaver, R. Sandstrom, J. A. Stamatoyannopoulos, Y. Zhou, and L. I. Zon, “Zebrafish globin switching occurs in two developmental stages and is controlled by the LCR,” Dev. Biol. (Amsterdam, Neth.) 366(2), 185–194 (2012).
[Crossref]

Detrich, H. W.

H. W. Detrich, M. Westerfield, and L. I. Zon, “Overview of the Zebrafish system,” Methods Cell Biol. 59, 3–10 (1998).
[Crossref]

DiBiase, A.

J. J. Ganis, N. Hsia, E. Trompouki, J. L. de Jong, A. DiBiase, J. S. Lambert, Z. Jia, P. J. Sabo, M. Weaver, R. Sandstrom, J. A. Stamatoyannopoulos, Y. Zhou, and L. I. Zon, “Zebrafish globin switching occurs in two developmental stages and is controlled by the LCR,” Dev. Biol. (Amsterdam, Neth.) 366(2), 185–194 (2012).
[Crossref]

Dicker, A. P.

G. Kari, U. Rodeck, and A. P. Dicker, “Zebrafish: An Emerging Model System for Human Disease and Drug Discovery,” Clin. Pharmacol. Ther. (Hoboken, NJ, U. S.) 82(1), 70–80 (2007).
[Crossref]

Ding, R.

C. Liu, J. Liao, L. Chen, J. Chen, R. Ding, X. Gong, C. Cui, Z. Pang, W. Zheng, and L. Song, “The integrated high-resolution reflection-mode photoacoustic and fluorescence confocal microscopy,” Photoacoustics 14, 12–18 (2019).
[Crossref]

Distel, M.

Divakar Rao, K.

K. Divakar Rao, P. Upadhyaya, M. Sharma, and P. K. Gupta, “Noninvasive Imaging of Ethanol-Induced Developmental Defects in Zebrafish Embryos Using Optical Coherence Tomography,” Birth Defects Res., Part B 95(1), 7–11 (2011).
[Crossref]

Djonov, V.

T. R. Djukic, S. Karthik, I. Saveljic, V. Djonov, and N. Filipovic, “Modeling the Behavior of Red Blood Cells within the Caudal Vein Plexus of Zebrafish,” Front. Physiol. 7, 455 (2016).
[Crossref]

Djukic, T. R.

T. R. Djukic, S. Karthik, I. Saveljic, V. Djonov, and N. Filipovic, “Modeling the Behavior of Red Blood Cells within the Caudal Vein Plexus of Zebrafish,” Front. Physiol. 7, 455 (2016).
[Crossref]

Dollé, G.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Dower, N.

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
[Crossref]

Drexler, W.

Driever, W.

B. M. Weinstein, D. L. Stemple, W. Driever, and M. C. Fishman, “gridlock, a localized heritable vascular patterning defect in the zebrafish,” Nat. Med. 1(11), 1143–1147 (1995).
[Crossref]

Eagle, A.

L. Ruzicka, D. Howe, S. Ramachandran, S. Toro, C. Van Slyke, Y. Bradford, A. Eagle, D. Fashena, K. Frazer, P. Kalita, P. Mani, R. Martin, S. Moxon, H. Paddock, C. Pich, K. Schaper, X. Shao, A. Singer, and M. Westerfield, “The Zebrafish Information Network: new support for non-coding genes, richer Gene Ontology annotations and the Alliance of Genome Resources,” Nucleic Acids Res. 47(D1), D867–D873 (2019).
[Crossref]

El-Rass, S.

M. J. Moore, S. El-Rass, Y. Xiao, Y. Wang, X.-Y. Wen, and M. C. Kolios, “Simultaneous ultra-high frequency photoacoustic microscopy and photoacoustic radiometry of zebrafish larvae in vivo,” Photoacoustics 12, 14–21 (2018).
[Crossref]

Emelianov, S. Y.

Fashena, D.

L. Ruzicka, D. Howe, S. Ramachandran, S. Toro, C. Van Slyke, Y. Bradford, A. Eagle, D. Fashena, K. Frazer, P. Kalita, P. Mani, R. Martin, S. Moxon, H. Paddock, C. Pich, K. Schaper, X. Shao, A. Singer, and M. Westerfield, “The Zebrafish Information Network: new support for non-coding genes, richer Gene Ontology annotations and the Alliance of Genome Resources,” Nucleic Acids Res. 47(D1), D867–D873 (2019).
[Crossref]

Fawzi, A. A.

W. Song, Q. Wei, W. Liu, T. Liu, J. Yi, N. Sheibani, A. A. Fawzi, R. A. Linsenmeier, S. Jiao, and H. F. Zhang, “A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography,” Sci. Rep. 4(1), 6525 (2015).
[Crossref]

Fekonja, N.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Fercher, A.

A. Fercher, C. Hitzenberger, and M. Juchem, “Measurement of Intraocular Optical Distances Using Partially Coherent Laser Light,” J. Mod. Opt. 38(7), 1327–1333 (1991).
[Crossref]

Ferguson, R. D.

Ferrante, A. A.

Fiehler, J.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Filipovic, N.

T. R. Djukic, S. Karthik, I. Saveljic, V. Djonov, and N. Filipovic, “Modeling the Behavior of Red Blood Cells within the Caudal Vein Plexus of Zebrafish,” Front. Physiol. 7, 455 (2016).
[Crossref]

Fischer, B.

Fishman, M. C.

B. M. Weinstein, D. L. Stemple, W. Driever, and M. C. Fishman, “gridlock, a localized heritable vascular patterning defect in the zebrafish,” Nat. Med. 1(11), 1143–1147 (1995).
[Crossref]

Flotte, T.

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,” (1991).

Follain, G.

G. Follain, N. Osmani, A. S. Azevedo, G. Allio, L. Mercier, M. A. Karreman, G. Solecki, M. J. Garcia Leòn, O. Lefebvre, N. Fekonja, C. Hille, V. Chabannes, G. Dollé, T. Metivet, F. D. Hovsepian, C. Prudhomme, A. Pichot, N. Paul, R. Carapito, S. Bahram, B. Ruthensteiner, A. Kemmling, S. Siemonsen, T. Schneider, J. Fiehler, M. Glatzel, F. Winkler, Y. Schwab, K. Pantel, S. Harlepp, and J. G. Goetz, “Hemodynamic Forces Tune the Arrest, Adhesion, and Extravasation of Circulating Tumor Cells,” Dev. Cell 45(1), 33–52.e12 (2018).
[Crossref]

Fraser, S. E.

S. Rieger, R. P. Kulkarni, D. Darcy, S. E. Fraser, and R. W. Köster, “Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos,” Dev. Dyn. 234(3), 670–681 (2005).
[Crossref]

Frazer, K.

L. Ruzicka, D. Howe, S. Ramachandran, S. Toro, C. Van Slyke, Y. Bradford, A. Eagle, D. Fashena, K. Frazer, P. Kalita, P. Mani, R. Martin, S. Moxon, H. Paddock, C. Pich, K. Schaper, X. Shao, A. Singer, and M. Westerfield, “The Zebrafish Information Network: new support for non-coding genes, richer Gene Ontology annotations and the Alliance of Genome Resources,” Nucleic Acids Res. 47(D1), D867–D873 (2019).
[Crossref]

Fujimoto, J. G.

L. Kagemann, H. Ishikawa, J. Zou, P. Charukamnoetkanok, G. Wollstein, K. A. Townsend, M. L. Gabriele, N. Bahary, X. Wei, J. G. Fujimoto, and J. S. Schuman, “Repeated, noninvasive, high resolution spectral domain optical coherence tomography imaging of zebrafish embryos,” Mol. Vis. 14, 2157–2170 (2008).

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,” (1991).

Furutani-Seiki, M.

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Brand, F. J. van Eeden, M. Furutani-Seiki, M. Granato, M. Hammerschmidt, C. P. Heisenberg, Y. J. Jiang, D. A. Kane, M. C. Mullins, and C. Nusslein-Volhard, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

Gabriele, M. L.

L. Kagemann, H. Ishikawa, J. Zou, P. Charukamnoetkanok, G. Wollstein, K. A. Townsend, M. L. Gabriele, N. Bahary, X. Wei, J. G. Fujimoto, and J. S. Schuman, “Repeated, noninvasive, high resolution spectral domain optical coherence tomography imaging of zebrafish embryos,” Mol. Vis. 14, 2157–2170 (2008).

Ganis, J. J.

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Biomed. Opt. Express (5)

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Figures (8)

Fig. 1.
Fig. 1. (a) Functional OCT-PAM system. (b) Absolute velocity extraction principle for zebrafish body and eye. (c) 3-D printed zebrafish larva mount. (d) Zebrafish larva in recovery position mounted in the indentation of the zebrafish mount.
Fig. 2.
Fig. 2. Normalized hemoglobin absorption coefficients for human and adult zebrafish blood.
Fig. 3.
Fig. 3. Depth sectioned OCT average intensity en face projections (slab size 120 µm). The uppermost slice starts with the focus at the position of the eye (a) continuing depth increments through the body (b)-(d) to the tail in (e), spanning a total depth of 600 µm. Blue triangle: eye; blue square: yolk sac; blue arrow: myotomes; ochre: pigment cells; yellow: ear with two otoliths; magenta: notochord; green: spinal cord; brown: internal organs; ME: Myelencephalon; HB: hindbrain; MB: midbrain; PG: pineal gland; SB: swim bladder.
Fig. 4.
Fig. 4. OCT-PAM image of a zebrafish larva. (a) OCT average intensity projection, (b) PAM maximum amplitude projection, (c) multimodal OCT-PAM. The 50 kHz 532 nm pump laser was used to acquire the PAM image. DA: dorsal aorta; CV: caudal vein; DLAV: dorsal longitudinal anastomotic vessel; SB: swim bladder; YS: yolk sac; ISV: intersegmental vessel.
Fig. 5.
Fig. 5. Comparison between OCT, DOCT and histology. (a) OCT B-scan at the position of the brown vertical line in Fig. 4(a). (b) Histology, transverse image from a 5 dpf zebrafish larva at a similar anterior-posterior position [51]. (c) Phase difference image from a. Color bar indicates phase in rad. (d) Velocity profile of the DA, (e) CV, and (f) velocity profiles of the DA at different timepoints after Doppler angle correction. Color bar indicates velocity in mm/s. Magenta ellipse: notochord; green ellipse: spinal cord; yellow ellipse: lateral line; red ellipse: dorsal aorta; purple ellipse: caudal vein; blue arrows: myotomes (segmental muscles).
Fig. 6.
Fig. 6. Longitudinal DOCT blood velocity evaluation in the DA. 10 Hz sample frequency, 30 samples. red values: local peak velocities, green values: local minimum velocities, magenta curve section: velocity evaluation for the data illustrated in Fig. 5(f).
Fig. 7.
Fig. 7. Histology [52] and DOCT side by side comparison (transverse cut). Blue bars: region of interest for OCT imaging; green arrows: retinal layers; 1: ganglion cell layer; 2: inner plexiform layer; 3: inner nuclear layer; 4: outer nuclear layer; green ellipse: retinal pigmented epithelium; blue triangle: HYA. Color bar for phase difference overlay: $\pm$ 2 rad.
Fig. 8.
Fig. 8. Oxygenation map of a zebrafish larval tail. The image is acquired after spectral unmixing using the absorption coefficients of human (a) and zebrafish blood (b), respectively.

Tables (2)

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Table 1. System specifications

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Table 2. Quantitative DOCT evaluation.

Equations (3)

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v = v a x i a l c o s ( α ) and F = v π d 2 4
P ( λ i , x , y ) = Φ ( λ ) ( ϵ H b R ( λ i ) C H b R ( x , y ) + ϵ H b O 2 ( λ i ) C H b O 2 ( x , y ) ) ,
s O 2 ( x , y ) = C H b O 2 ( x , y ) C H b O 2 ( x , y ) + C H b R ( x , y ) 100 %