Abstract

Optical-resolution photoacoustic microscopy (OR-PAM) of oxygen saturation (sO2) offers high-resolution functional information on living tissue. Limited by the availability of high-speed multi-wavelength lasers, most OR-PAM systems use wavelengths around 532nm. Blood has high absorption coefficients in this spectrum, which may cause absorption saturation and induce systematic errors in sO2 imaging. Here, we present nonlinear OR-PAM that compensates for the absorption saturation in sO2 imaging. We model the absorption saturation at different absorption coefficients and ultrasonic bandwidths. To compensate for the absorption saturation, we develop an OR-PAM system with three optical wavelengths and implement a nonlinear algorithm to compute sO2. Phantom experiments on bovine blood validate that the nonlinear OR-PAM can improve the sO2 accuracy by up to 0.13 for fully oxygenated blood. In vivo sO2 imaging has been conducted in the mouse ear. The nonlinear sO2 results agree with the normal physiological values. These results show that the absorption saturation effect can be compensated for in nonlinear OR-PAM, which improves the accuracy of functional photoacoustic imaging.

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

Full Article  |  PDF Article
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2018 (4)

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
[Crossref] [PubMed]

T. J. Allen, O. Ogunlade, E. Zhang, and P. C. Beard, “Large area laser scanning optical resolution photoacoustic microscopy using a fibre optic sensor,” Biomed. Opt. Express 9(2), 650–660 (2018).
[Crossref] [PubMed]

P. H. Reza, K. Bell, W. Shi, J. Shapiro, and R. J. Zemp, “Deep non-contact photoacoustic initial pressure imaging,” Optica 5(7), 814 (2018).
[Crossref]

2017 (4)

Y. Liang, L. Jin, B.-O. Guan, and L. Wang, “2 MHz multi-wavelength pulsed laser for functional photoacoustic microscopy,” Opt. Lett. 42(7), 1452–1455 (2017).
[Crossref] [PubMed]

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
[Crossref] [PubMed]

L. Xu, S. Alam, Q. Kang, D. P. Shepherd, and D. J. Richardson, “Raman-shifted wavelength-selectable pulsed fiber laser with high repetition rate and high pulse energy in the visible,” Opt. Express 25(1), 351–356 (2017).
[Crossref] [PubMed]

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for In Vivo Small-animal Blood Vasculature Imaging,” J. Vis. Exp. 124(124), e55810 (2017).
[Crossref] [PubMed]

2016 (4)

A. Hussain, W. Petersen, J. Staley, E. Hondebrink, and W. Steenbergen, “Quantitative blood oxygen saturation imaging using combined photoacoustics and acousto-optics,” Opt. Lett. 41(8), 1720–1723 (2016).
[Crossref] [PubMed]

T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
[Crossref] [PubMed]

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[Crossref] [PubMed]

S. Huang, P. K. Upputuri, H. Liu, M. Pramanik, and M. Wang, “A dual-functional benzobisthiadiazole derivative as an effective theranostic agent for near-infrared photoacoustic imaging and photothermal therapy,” J. Mater. Chem. B Mater. Biol. Med. 4(9), 1696–1703 (2016).
[Crossref]

2015 (4)

G. Diot, A. Dima, and V. Ntziachristos, “Multispectral opto-acoustic tomography of exercised muscle oxygenation,” Opt. Lett. 40(7), 1496–1499 (2015).
[Crossref] [PubMed]

P. K. Upputuri, K. Sivasubramanian, C. S. K. Mark, and M. Pramanik, “Recent developments in vascular imaging techniques in tissue engineering and regenerative medicine,” BioMed Res. Int. 2015, 783983 (2015).
[Crossref] [PubMed]

R. Hochuli, P. C. Beard, and B. Cox, “Effect of wavelength selection on the accuracy of blood oxygen saturation estimates obtained from photoacoustic images,” Proc. SPIE 9323, 93231V (2015).
[Crossref]

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

2014 (3)

2013 (4)

S. Hu and L. V. Wang, “Optical-resolution photoacoustic microscopy: auscultation of biological systems at the cellular level,” Biophys. J. 105(4), 841–847 (2013).
[Crossref] [PubMed]

P. Hajireza, A. Forbrich, and R. J. Zemp, “Multifocus optical-resolution photoacoustic microscopy using stimulated Raman scattering and chromatic aberration,” Opt. Lett. 38(15), 2711–2713 (2013).
[Crossref] [PubMed]

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

J. Yao and L. V. Wang, “Photoacoustic microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

2012 (1)

Y. Jiang, A. Forbrich, T. Harrison, and R. J. Zemp, “Blood oxygen flux estimation with a combined photoacoustic and high-frequency ultrasound microscopy system: a phantom study,” J. Biomed. Opt. 17(3), 036012 (2012).
[Crossref] [PubMed]

2011 (2)

J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
[Crossref] [PubMed]

L. Wang, K. Maslov, J. Yao, B. Rao, and L. V. Wang, “Fast voice-coil scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 36(2), 139–141 (2011).
[Crossref] [PubMed]

2010 (3)

J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
[Crossref] [PubMed]

C. Kim, C. Favazza, and L. V. Wang, “In Vivo Photoacoustic Tomography of Chemicals: High-Resolution Functional and Molecular Optical Imaging at New Depths,” Chem. Rev. 110(5), 2756–2782 (2010).
[Crossref] [PubMed]

Z. Guo, S. Hu, and L. V. Wang, “Calibration-free absolute quantification of optical absorption coefficients using acoustic spectra in 3D photoacoustic microscopy of biological tissue,” Opt. Lett. 35(12), 2067–2069 (2010).
[Crossref] [PubMed]

2008 (1)

M. Nitzan and H. Taitelbaum, “The measurement of oxygen saturation in arterial and venous blood,” IEEE Instrum. Meas. Mag. 11(3), 9–15 (2008).
[Crossref]

2007 (4)

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

K. Maslov, H. F. Zhang, and L. V. Wang, “Effects of wavelength-dependent fluence attenuation on the noninvasive photoacoustic imaging of hemoglobin oxygen saturation in subcutaneous vasculaturein vivo,” Inverse Probl. 23(6), S113–S122 (2007).
[Crossref]

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[Crossref]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
[Crossref] [PubMed]

2000 (1)

K. Briely-Sabo and A. Bjornerud, “Accurate de-oxygenation of ex vivo whole blood using sodium Dithionite,” in Proc. Intl. Sot. Mag. Reson. Med 8, 2025 (2000).

1984 (1)

K. D. Vandegriff and J. S. Olson, “The kinetics of O2 release by human red blood cells in the presence of external sodium dithionite,” J. Biol. Chem. 259(20), 12609–12618 (1984).
[PubMed]

1962 (1)

R. J. Hill and W. Konigsberg, “The structure of human hemoglobin. IV. The chymotryptic digestion of the alpha chain of human hemoglobin,” J. Biol. Chem. 237(10), 3151–3156 (1962).
[PubMed]

Alam, S.

Allen, T. J.

Beard, P.

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Beard, P. C.

T. J. Allen, O. Ogunlade, E. Zhang, and P. C. Beard, “Large area laser scanning optical resolution photoacoustic microscopy using a fibre optic sensor,” Biomed. Opt. Express 9(2), 650–660 (2018).
[Crossref] [PubMed]

R. Hochuli, P. C. Beard, and B. Cox, “Effect of wavelength selection on the accuracy of blood oxygen saturation estimates obtained from photoacoustic images,” Proc. SPIE 9323, 93231V (2015).
[Crossref]

Bell, K.

Bian, L.

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

Bjornerud, A.

K. Briely-Sabo and A. Bjornerud, “Accurate de-oxygenation of ex vivo whole blood using sodium Dithionite,” in Proc. Intl. Sot. Mag. Reson. Med 8, 2025 (2000).

Briely-Sabo, K.

K. Briely-Sabo and A. Bjornerud, “Accurate de-oxygenation of ex vivo whole blood using sodium Dithionite,” in Proc. Intl. Sot. Mag. Reson. Med 8, 2025 (2000).

Cao, R.

T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
[Crossref] [PubMed]

Chen, R.

T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
[Crossref] [PubMed]

J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
[Crossref] [PubMed]

Chen, X.

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

Cox, B.

R. Hochuli, P. C. Beard, and B. Cox, “Effect of wavelength selection on the accuracy of blood oxygen saturation estimates obtained from photoacoustic images,” Proc. SPIE 9323, 93231V (2015).
[Crossref]

Deán-Ben, X. L.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
[Crossref] [PubMed]

Delpy, D.

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Dima, A.

Diot, G.

Elwell, C.

J. Laufer, D. Delpy, C. Elwell, and P. Beard, “Quantitative spatially resolved measurement of tissue chromophore concentrations using photoacoustic spectroscopy: application to the measurement of blood oxygenation and haemoglobin concentration,” Phys. Med. Biol. 52(1), 141–168 (2007).
[Crossref] [PubMed]

Estrada, H.

J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
[Crossref] [PubMed]

Favazza, C.

C. Kim, C. Favazza, and L. V. Wang, “In Vivo Photoacoustic Tomography of Chemicals: High-Resolution Functional and Molecular Optical Imaging at New Depths,” Chem. Rev. 110(5), 2756–2782 (2010).
[Crossref] [PubMed]

Fehm, T. F.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
[Crossref] [PubMed]

Forbrich, A.

Gottschalk, S.

J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
[Crossref] [PubMed]

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
[Crossref] [PubMed]

Guan, B.-O.

Guo, Z.

Hajireza, P.

Harrison, T.

Y. Jiang, A. Forbrich, T. Harrison, and R. J. Zemp, “Blood oxygen flux estimation with a combined photoacoustic and high-frequency ultrasound microscopy system: a phantom study,” J. Biomed. Opt. 17(3), 036012 (2012).
[Crossref] [PubMed]

Heinmiller, A.

R. J. Paproski, A. Heinmiller, K. Wachowicz, and R. J. Zemp, “Multi-wavelength photoacoustic imaging of inducible tyrosinase reporter gene expression in xenograft tumors,” Sci. Rep. 4(1), 5329 (2014).
[Crossref] [PubMed]

Hill, R. J.

R. J. Hill and W. Konigsberg, “The structure of human hemoglobin. IV. The chymotryptic digestion of the alpha chain of human hemoglobin,” J. Biol. Chem. 237(10), 3151–3156 (1962).
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S. Hu and L. V. Wang, “Optical-resolution photoacoustic microscopy: auscultation of biological systems at the cellular level,” Biophys. J. 105(4), 841–847 (2013).
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Kang, Q.

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Konigsberg, W.

R. J. Hill and W. Konigsberg, “The structure of human hemoglobin. IV. The chymotryptic digestion of the alpha chain of human hemoglobin,” J. Biol. Chem. 237(10), 3151–3156 (1962).
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J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
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C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
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S. Huang, P. K. Upputuri, H. Liu, M. Pramanik, and M. Wang, “A dual-functional benzobisthiadiazole derivative as an effective theranostic agent for near-infrared photoacoustic imaging and photothermal therapy,” J. Mater. Chem. B Mater. Biol. Med. 4(9), 1696–1703 (2016).
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J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
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P. K. Upputuri, K. Sivasubramanian, C. S. K. Mark, and M. Pramanik, “Recent developments in vascular imaging techniques in tissue engineering and regenerative medicine,” BioMed Res. Int. 2015, 783983 (2015).
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Maslov, K.

L. Wang, K. Maslov, and L. V. Wang, “Single-cell label-free photoacoustic flowoxigraphy in vivo,” Proc. Natl. Acad. Sci. U.S.A. 110(15), 5759–5764 (2013).
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L. Wang, K. Maslov, J. Yao, B. Rao, and L. V. Wang, “Fast voice-coil scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 36(2), 139–141 (2011).
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K. Maslov, H. F. Zhang, and L. V. Wang, “Effects of wavelength-dependent fluence attenuation on the noninvasive photoacoustic imaging of hemoglobin oxygen saturation in subcutaneous vasculaturein vivo,” Inverse Probl. 23(6), S113–S122 (2007).
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H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
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H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
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Maslov, K. I.

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
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J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
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T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
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M. Nitzan and H. Taitelbaum, “The measurement of oxygen saturation in arterial and venous blood,” IEEE Instrum. Meas. Mag. 11(3), 9–15 (2008).
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Olson, J. S.

K. D. Vandegriff and J. S. Olson, “The kinetics of O2 release by human red blood cells in the presence of external sodium dithionite,” J. Biol. Chem. 259(20), 12609–12618 (1984).
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Paproski, R. J.

R. J. Paproski, A. Heinmiller, K. Wachowicz, and R. J. Zemp, “Multi-wavelength photoacoustic imaging of inducible tyrosinase reporter gene expression in xenograft tumors,” Sci. Rep. 4(1), 5329 (2014).
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Petersen, W.

Pramanik, M.

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for In Vivo Small-animal Blood Vasculature Imaging,” J. Vis. Exp. 124(124), e55810 (2017).
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S. Huang, P. K. Upputuri, H. Liu, M. Pramanik, and M. Wang, “A dual-functional benzobisthiadiazole derivative as an effective theranostic agent for near-infrared photoacoustic imaging and photothermal therapy,” J. Mater. Chem. B Mater. Biol. Med. 4(9), 1696–1703 (2016).
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P. K. Upputuri, K. Sivasubramanian, C. S. K. Mark, and M. Pramanik, “Recent developments in vascular imaging techniques in tissue engineering and regenerative medicine,” BioMed Res. Int. 2015, 783983 (2015).
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C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
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Razansky, D.

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S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
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J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
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Richardson, D. J.

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J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
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Sharma, A.

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for In Vivo Small-animal Blood Vasculature Imaging,” J. Vis. Exp. 124(124), e55810 (2017).
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Shi, W.

Shung, K. K.

J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
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Sivaramakrishnan, M.

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
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Sivasubramanian, K.

P. K. Upputuri, K. Sivasubramanian, C. S. K. Mark, and M. Pramanik, “Recent developments in vascular imaging techniques in tissue engineering and regenerative medicine,” BioMed Res. Int. 2015, 783983 (2015).
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Staley, J.

Steenbergen, W.

Stoica, G.

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
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T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
[Crossref] [PubMed]

Taitelbaum, H.

M. Nitzan and H. Taitelbaum, “The measurement of oxygen saturation in arterial and venous blood,” IEEE Instrum. Meas. Mag. 11(3), 9–15 (2008).
[Crossref]

Tsytsarev, V.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
[Crossref] [PubMed]

Upputuri, P. K.

S. Huang, P. K. Upputuri, H. Liu, M. Pramanik, and M. Wang, “A dual-functional benzobisthiadiazole derivative as an effective theranostic agent for near-infrared photoacoustic imaging and photothermal therapy,” J. Mater. Chem. B Mater. Biol. Med. 4(9), 1696–1703 (2016).
[Crossref]

P. K. Upputuri, K. Sivasubramanian, C. S. K. Mark, and M. Pramanik, “Recent developments in vascular imaging techniques in tissue engineering and regenerative medicine,” BioMed Res. Int. 2015, 783983 (2015).
[Crossref] [PubMed]

Vandegriff, K. D.

K. D. Vandegriff and J. S. Olson, “The kinetics of O2 release by human red blood cells in the presence of external sodium dithionite,” J. Biol. Chem. 259(20), 12609–12618 (1984).
[PubMed]

Wachowicz, K.

R. J. Paproski, A. Heinmiller, K. Wachowicz, and R. J. Zemp, “Multi-wavelength photoacoustic imaging of inducible tyrosinase reporter gene expression in xenograft tumors,” Sci. Rep. 4(1), 5329 (2014).
[Crossref] [PubMed]

Wang, J.

J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
[Crossref] [PubMed]

Wang, L.

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

Y. Liang, L. Jin, B.-O. Guan, and L. Wang, “2 MHz multi-wavelength pulsed laser for functional photoacoustic microscopy,” Opt. Lett. 42(7), 1452–1455 (2017).
[Crossref] [PubMed]

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

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

L. Wang, K. Maslov, J. Yao, B. Rao, and L. V. Wang, “Fast voice-coil scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 36(2), 139–141 (2011).
[Crossref] [PubMed]

Wang, L. V.

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[Crossref] [PubMed]

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

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

S. Hu and L. V. Wang, “Optical-resolution photoacoustic microscopy: auscultation of biological systems at the cellular level,” Biophys. J. 105(4), 841–847 (2013).
[Crossref] [PubMed]

J. Yao and L. V. Wang, “Photoacoustic microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
[Crossref] [PubMed]

L. Wang, K. Maslov, J. Yao, B. Rao, and L. V. Wang, “Fast voice-coil scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 36(2), 139–141 (2011).
[Crossref] [PubMed]

Z. Guo, S. Hu, and L. V. Wang, “Calibration-free absolute quantification of optical absorption coefficients using acoustic spectra in 3D photoacoustic microscopy of biological tissue,” Opt. Lett. 35(12), 2067–2069 (2010).
[Crossref] [PubMed]

J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
[Crossref] [PubMed]

C. Kim, C. Favazza, and L. V. Wang, “In Vivo Photoacoustic Tomography of Chemicals: High-Resolution Functional and Molecular Optical Imaging at New Depths,” Chem. Rev. 110(5), 2756–2782 (2010).
[Crossref] [PubMed]

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[Crossref]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
[Crossref] [PubMed]

K. Maslov, H. F. Zhang, and L. V. Wang, “Effects of wavelength-dependent fluence attenuation on the noninvasive photoacoustic imaging of hemoglobin oxygen saturation in subcutaneous vasculaturein vivo,” Inverse Probl. 23(6), S113–S122 (2007).
[Crossref]

Wang, M.

S. Huang, P. K. Upputuri, H. Liu, M. Pramanik, and M. Wang, “A dual-functional benzobisthiadiazole derivative as an effective theranostic agent for near-infrared photoacoustic imaging and photothermal therapy,” J. Mater. Chem. B Mater. Biol. Med. 4(9), 1696–1703 (2016).
[Crossref]

Wang, T.

T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
[Crossref] [PubMed]

Wen, G.

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

Wissmeyer, G.

J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
[Crossref] [PubMed]

Wong, S. H. D.

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

Wong, T. T. W.

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

Xia, Y.

J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
[Crossref] [PubMed]

Xu, L.

Yang, B.

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
[Crossref] [PubMed]

Yang, J.-M.

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

Yao, J.

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[Crossref] [PubMed]

J. Yao, L. Wang, J.-M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C.-H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12(5), 407–410 (2015).
[Crossref] [PubMed]

J. Yao and L. V. Wang, “Photoacoustic microscopy,” Laser Photonics Rev. 7(5), 758–778 (2013).
[Crossref] [PubMed]

J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
[Crossref] [PubMed]

L. Wang, K. Maslov, J. Yao, B. Rao, and L. V. Wang, “Fast voice-coil scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 36(2), 139–141 (2011).
[Crossref] [PubMed]

Yin, C.

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P. H. Reza, K. Bell, W. Shi, J. Shapiro, and R. J. Zemp, “Deep non-contact photoacoustic initial pressure imaging,” Optica 5(7), 814 (2018).
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R. J. Paproski, A. Heinmiller, K. Wachowicz, and R. J. Zemp, “Multi-wavelength photoacoustic imaging of inducible tyrosinase reporter gene expression in xenograft tumors,” Sci. Rep. 4(1), 5329 (2014).
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P. Hajireza, A. Forbrich, and R. J. Zemp, “Multifocus optical-resolution photoacoustic microscopy using stimulated Raman scattering and chromatic aberration,” Opt. Lett. 38(15), 2711–2713 (2013).
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Y. Jiang, A. Forbrich, T. Harrison, and R. J. Zemp, “Blood oxygen flux estimation with a combined photoacoustic and high-frequency ultrasound microscopy system: a phantom study,” J. Biomed. Opt. 17(3), 036012 (2012).
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J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
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H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
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C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
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J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
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T. Wang, N. Sun, R. Cao, B. Ning, R. Chen, Q. Zhou, and S. Hu, “Multiparametric photoacoustic microscopy of the mouse brain with 300-kHz A-line rate,” Neurophotonics 3(4), 045006 (2016).
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J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
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ACS Nano (1)

C. Yin, G. Wen, C. Liu, B. Yang, S. Lin, J. Huang, P. Zhao, S. H. D. Wong, K. Zhang, X. Chen, G. Li, X. Jiang, J. Huang, K. Pu, L. Wang, and L. Bian, “Organic Semiconducting Polymer Nanoparticles for Photoacoustic Labeling and Tracking of Stem Cells in the Second Near-Infrared Window,” ACS Nano 12(12), 12201–12211 (2018).
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Appl. Opt. (1)

Appl. Phys. Lett. (1)

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
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P. K. Upputuri, K. Sivasubramanian, C. S. K. Mark, and M. Pramanik, “Recent developments in vascular imaging techniques in tissue engineering and regenerative medicine,” BioMed Res. Int. 2015, 783983 (2015).
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S. Hu and L. V. Wang, “Optical-resolution photoacoustic microscopy: auscultation of biological systems at the cellular level,” Biophys. J. 105(4), 841–847 (2013).
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C. Kim, C. Favazza, and L. V. Wang, “In Vivo Photoacoustic Tomography of Chemicals: High-Resolution Functional and Molecular Optical Imaging at New Depths,” Chem. Rev. 110(5), 2756–2782 (2010).
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K. Maslov, H. F. Zhang, and L. V. Wang, “Effects of wavelength-dependent fluence attenuation on the noninvasive photoacoustic imaging of hemoglobin oxygen saturation in subcutaneous vasculaturein vivo,” Inverse Probl. 23(6), S113–S122 (2007).
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J. Wang, T. Liu, S. Jiao, R. Chen, Q. Zhou, K. K. Shung, L. V. Wang, and H. F. Zhang, “Saturation effect in functional photoacoustic imaging,” J. Biomed. Opt. 15(2), 021317 (2010).
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Y. Jiang, A. Forbrich, T. Harrison, and R. J. Zemp, “Blood oxygen flux estimation with a combined photoacoustic and high-frequency ultrasound microscopy system: a phantom study,” J. Biomed. Opt. 17(3), 036012 (2012).
[Crossref] [PubMed]

J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
[Crossref] [PubMed]

J. Biophotonics (1)

J. Rebling, H. Estrada, S. Gottschalk, G. Sela, M. Zwack, G. Wissmeyer, V. Ntziachristos, and D. Razansky, “Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks,” J. Biophotonics 11(9), e201800057 (2018).
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S. Huang, P. K. Upputuri, H. Liu, M. Pramanik, and M. Wang, “A dual-functional benzobisthiadiazole derivative as an effective theranostic agent for near-infrared photoacoustic imaging and photothermal therapy,” J. Mater. Chem. B Mater. Biol. Med. 4(9), 1696–1703 (2016).
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Nat. Protoc. (1)

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
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S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, V. Tsytsarev, and D. Razansky, “Correlation between volumetric oxygenation responses and electrophysiology identifies deep thalamocortical activity during epileptic seizures,” Neurophotonics 4(1), 011007 (2017).
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R. J. Paproski, A. Heinmiller, K. Wachowicz, and R. J. Zemp, “Multi-wavelength photoacoustic imaging of inducible tyrosinase reporter gene expression in xenograft tumors,” Sci. Rep. 4(1), 5329 (2014).
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Figures (3)

Fig. 1
Fig. 1 Schematic diagram of OR-PAM system with a three-wavelength pulsed laser. BS: beam splitter R/T: 90/10, DM1&DM2: dichroic mirror 550 nm short-pass, HWP1-3: half-wave plate, LPF: 540 nm long-pass filter, PBS: polarization beam splitter, SM fiber 1-2: single-mode fiber, UST: ultrasonic transducer, VNDF: variable neutral density filter.
Fig. 2
Fig. 2 (a) Spectrum of the three-wavelength stimulated-Raman-scattering laser. (b) Absorption saturation effect with different axial resolutions and absorption coefficients. (c) Impact of absorption saturation effect on sO2 accuracy using linear method. The nonlinear sO2 results is the same as the set values. The tilted dashed line represents an ideal case that the linear sO2 results are unbiased. (d) In vitro sO2 measurement of bovine blood samples using both linear and nonlinear models. Sample size = 5.
Fig. 3
Fig. 3 (a) In vivo imaging of the total hemoglobin concentration in the mouse ear. (b) Close-up of the blue dashed box in (a). (c) Comparison of the linear and nonlinear sO2 values in three artery-vein pairs as labeled in the white dashed boxes in (d) and (e). Error bars are standard derivations. (d) Linear sO2 image of the mouse ear. (e) Nonlinear sO2 image of the mouse ear.

Equations (5)

Equations on this page are rendered with MathJax. Learn more.

PA=kΓηF[1exp( μ a Δz)],
PA=kΓηF μ a Δz,
PA=kΓηF[1exp(r(s O 2 ε oxy +(1s O 2 ) ε de ) C HbT Δz)].
P A 1i P A 2i = 1exp[ u i (s O 2_i ε 1 oxy +(1s O 2_i ) ε 1 de )] 1exp[ u i (s O 2_i ε 2 oxy +(1s O 2_i ) ε 2 de )] ,
P A 3i P A 2i = 1exp[ u i (s O 2_i ε 3 oxy +(1s O 2_i ) ε 3 de )] 1exp[ u i (s O 2_i ε 2 oxy +(1s O 2_i ) ε 2 de )] ,