Abstract

Liver fibrosis is a major cause for increasing mortality worldwide. Preclinical research using animal models is required for the discovery of new anti-fibrotic therapies, but currently relies on endpoint liver histology. In this study, we investigated a cost-effective and portable photoacoustic/ultrasound (PA/US) imaging system as a potential non-invasive alternative. Fibrosis was induced in mice using CCl4 followed by liver imaging and histological analysis. Imaging showed significantly increased PA features with higher frequency signals in fibrotic livers versus healthy livers. This corresponds to more heterogeneous liver structure resulting from collagen deposition and angiogenesis. Importantly, PA response and its frequency were highly correlated with histological parameters. These results demonstrate the preclinical feasibility of the PA imaging approach and applicability of dual PA/US system.

© 2016 Optical Society of America

Full Article  |  PDF Article
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References

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    [Crossref]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]

2016 (3)

L. J. Rich and M. Seshadri, “Photoacoustic monitoring of tumor and normal tissue response to radiation,” Sci. Rep. 6, 21237 (2016).
[Crossref] [PubMed]

J. Tang, J. E. Coleman, X. Dai, and H. Jiang, “Wearable 3-D Photoacoustic Tomography for Functional Brain Imaging in Behaving Rats,” Sci. Rep. 6, 25470 (2016).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

2015 (4)

S. Y. Nam, E. Chung, L. J. Suggs, and S. Y. Emelianov, “Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct,” Tissue Eng. Part C Methods 21(6), 557–566 (2015).
[Crossref] [PubMed]

X. L. Deán-Ben, S. J. Ford, and D. Razansky, “High-frame rate four dimensional optoacoustic tomography enables visualization of cardiovascular dynamics and mouse heart perfusion,” Sci. Rep. 5, 10133 (2015).

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

2014 (4)

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

K. Daoudi, P. J. van den Berg, O. Rabot, A. Kohl, S. Tisserand, P. Brands, and W. Steenbergen, “Handheld probe integrating laser diode and ultrasound transducer array for ultrasound/photoacoustic dual modality imaging,” Opt. Express 22(21), 26365–26374 (2014).
[Crossref] [PubMed]

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

2013 (1)

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

2012 (2)

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Z. Guo, Z. Xu, and L. V. Wang, “Dependence of photoacoustic speckles on boundary roughness,” J. Biomed. Opt. 17(4), 046009 (2012).
[Crossref] [PubMed]

2011 (1)

V. Hernandez-Gea and S. L. Friedman, “Pathogenesis of liver fibrosis,” Annu. Rev. Pathol. 6(1), 425–456 (2011).
[Crossref] [PubMed]

2009 (1)

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

2008 (5)

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

S. L. Friedman, “Hepatic fibrosis -- overview,” Toxicology 254(3), 120–129 (2008).
[Crossref] [PubMed]

D. Schuppan and N. H. Afdhal, “Liver cirrhosis,” Lancet 371(9615), 838–851 (2008).
[Crossref] [PubMed]

S. L. Friedman, “Mechanisms of hepatic fibrogenesis,” Gastroenterology 134(6), 1655–1669 (2008).
[Crossref] [PubMed]

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[Crossref] [PubMed]

2007 (1)

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

2005 (1)

2003 (1)

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

2002 (1)

1991 (1)

G. J. Diebold, T. Sun, and M. I. Khan, “Photoacoustic monopole radiation in one, two, and three dimensions,” Phys. Rev. Lett. 67(24), 3384–3387 (1991).
[Crossref] [PubMed]

Afdhal, N. H.

D. Schuppan and N. H. Afdhal, “Liver cirrhosis,” Lancet 371(9615), 838–851 (2008).
[Crossref] [PubMed]

Aichler, M.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Ashida, H.

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

Beziere, N.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Bohndiek, S. E.

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Brands, P.

Brands, P. J.

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

Burton, N. C.

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Caldwell, S. H.

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

Carson, P. L.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Chamberland, D. L.

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[Crossref] [PubMed]

Chung, E.

S. Y. Nam, E. Chung, L. J. Suggs, and S. Y. Emelianov, “Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct,” Tissue Eng. Part C Methods 21(6), 557–566 (2015).
[Crossref] [PubMed]

Coleman, J. E.

J. Tang, J. E. Coleman, X. Dai, and H. Jiang, “Wearable 3-D Photoacoustic Tomography for Functional Brain Imaging in Behaving Rats,” Sci. Rep. 6, 25470 (2016).
[Crossref] [PubMed]

Dai, X.

J. Tang, J. E. Coleman, X. Dai, and H. Jiang, “Wearable 3-D Photoacoustic Tomography for Functional Brain Imaging in Behaving Rats,” Sci. Rep. 6, 25470 (2016).
[Crossref] [PubMed]

Daoudi, K.

de Mul, F. F. M.

Deán-Ben, X. L.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

X. L. Deán-Ben, S. J. Ford, and D. Razansky, “High-frame rate four dimensional optoacoustic tomography enables visualization of cardiovascular dynamics and mouse heart perfusion,” Sci. Rep. 5, 10133 (2015).

Deng, C. X.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

Deyo, D. J.

Diebold, G. J.

G. J. Diebold, T. Sun, and M. I. Khan, “Photoacoustic monopole radiation in one, two, and three dimensions,” Phys. Rev. Lett. 67(24), 3384–3387 (1991).
[Crossref] [PubMed]

Emelianov, S. Y.

S. Y. Nam, E. Chung, L. J. Suggs, and S. Y. Emelianov, “Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct,” Tissue Eng. Part C Methods 21(6), 557–566 (2015).
[Crossref] [PubMed]

Esenaliev, R. O.

Fehm, T. F.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

Ford, S. J.

X. L. Deán-Ben, S. J. Ford, and D. Razansky, “High-frame rate four dimensional optoacoustic tomography enables visualization of cardiovascular dynamics and mouse heart perfusion,” Sci. Rep. 5, 10133 (2015).

Fowlkes, J. B.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

Frenz, M.

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

Friedman, S. L.

V. Hernandez-Gea and S. L. Friedman, “Pathogenesis of liver fibrosis,” Annu. Rev. Pathol. 6(1), 425–456 (2011).
[Crossref] [PubMed]

S. L. Friedman, “Hepatic fibrosis -- overview,” Toxicology 254(3), 120–129 (2008).
[Crossref] [PubMed]

S. L. Friedman, “Mechanisms of hepatic fibrogenesis,” Gastroenterology 134(6), 1655–1669 (2008).
[Crossref] [PubMed]

Gambhir, S. S.

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Gertsch, A.

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

Goodman, Z. D.

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

Gorelikov, I.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Gottschalk, S.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

Guo, Z.

Z. Guo, Z. Xu, and L. V. Wang, “Dependence of photoacoustic speckles on boundary roughness,” J. Biomed. Opt. 17(4), 046009 (2012).
[Crossref] [PubMed]

Hernandez-Gea, V.

V. Hernandez-Gea and S. L. Friedman, “Pathogenesis of liver fibrosis,” Annu. Rev. Pathol. 6(1), 425–456 (2011).
[Crossref] [PubMed]

Hori, S.

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Jaeger, M.

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

Jiang, H.

J. Tang, J. E. Coleman, X. Dai, and H. Jiang, “Wearable 3-D Photoacoustic Tomography for Functional Brain Imaging in Behaving Rats,” Sci. Rep. 6, 25470 (2016).
[Crossref] [PubMed]

Jokerst, J. V.

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Joshi, B.

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Kawauchi, S.

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

Khan, M. I.

G. J. Diebold, T. Sun, and M. I. Khan, “Photoacoustic monopole radiation in one, two, and three dimensions,” Phys. Rev. Lett. 67(24), 3384–3387 (1991).
[Crossref] [PubMed]

Kimm, M.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Kitz, M.

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

Kohl, A.

Kolios, M. C.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Kolkman, R. G.

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

Kolkman, R. G. M.

Kosanke, Y.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Ku, G.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Larin, K. V.

Larina, I. V.

Licha, K.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Lin, J. D.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Liu, X.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

Machtaler, S.

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Matsuura, N.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Meier, R.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Meng, Z. X.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Morscher, S.

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Motamedi, M.

Nam, S. Y.

S. Y. Nam, E. Chung, L. J. Suggs, and S. Y. Emelianov, “Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct,” Tissue Eng. Part C Methods 21(6), 557–566 (2015).
[Crossref] [PubMed]

Nelson, R. C.

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

Ntziachristos, V.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Nunes, A.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Pang, Y.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Prough, D. S.

Rabot, O.

Razansky, D.

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

X. L. Deán-Ben, S. J. Ford, and D. Razansky, “High-frame rate four dimensional optoacoustic tomography enables visualization of cardiovascular dynamics and mouse heart perfusion,” Sci. Rep. 5, 10133 (2015).

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Rich, L. J.

L. J. Rich and M. Seshadri, “Photoacoustic monitoring of tumor and normal tissue response to radiation,” Sci. Rep. 6, 21237 (2016).
[Crossref] [PubMed]

Rockey, D. C.

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

Roessler, B. J.

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[Crossref] [PubMed]

Rummeny, E. J.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Saitoh, D.

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

Sasportas, L. S.

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Sato, S.

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

Schüpbach, S.

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

Schuppan, D.

D. Schuppan and N. H. Afdhal, “Liver cirrhosis,” Lancet 371(9615), 838–851 (2008).
[Crossref] [PubMed]

Seshadri, M.

L. J. Rich and M. Seshadri, “Photoacoustic monitoring of tumor and normal tissue response to radiation,” Sci. Rep. 6, 21237 (2016).
[Crossref] [PubMed]

Siphanto, R. I.

Smith, A. D.

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

Steenbergen, W.

Stoica, G.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Strohm, E. M.

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Suggs, L. J.

S. Y. Nam, E. Chung, L. J. Suggs, and S. Y. Emelianov, “Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct,” Tissue Eng. Part C Methods 21(6), 557–566 (2015).
[Crossref] [PubMed]

Sun, T.

G. J. Diebold, T. Sun, and M. I. Khan, “Photoacoustic monopole radiation in one, two, and three dimensions,” Phys. Rev. Lett. 67(24), 3384–3387 (1991).
[Crossref] [PubMed]

Tang, J.

J. Tang, J. E. Coleman, X. Dai, and H. Jiang, “Wearable 3-D Photoacoustic Tomography for Functional Brain Imaging in Behaving Rats,” Sci. Rep. 6, 25470 (2016).
[Crossref] [PubMed]

Tao, C.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

Taruttis, A.

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Terakawa, M.

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

Thumma, K. K.

Tisserand, S.

Tsunoi, Y.

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

van Adrichem, L. N. A.

van den Berg, P. J.

van Leeuwen, T. G.

van Neck, J. W.

von Schacky, C.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Walch, A.

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Wang, L. V.

Z. Guo, Z. Xu, and L. V. Wang, “Dependence of photoacoustic speckles on boundary roughness,” J. Biomed. Opt. 17(4), 046009 (2012).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Wang, X.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Xie, X.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Xu, G.

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Xu, Z.

Z. Guo, Z. Xu, and L. V. Wang, “Dependence of photoacoustic speckles on boundary roughness,” J. Biomed. Opt. 17(4), 046009 (2012).
[Crossref] [PubMed]

Yuan, J.

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Annu. Rev. Pathol. (1)

V. Hernandez-Gea and S. L. Friedman, “Pathogenesis of liver fibrosis,” Annu. Rev. Pathol. 6(1), 425–456 (2011).
[Crossref] [PubMed]

Appl. Opt. (1)

Arthritis Rheumatol. (1)

N. Beziere, C. von Schacky, Y. Kosanke, M. Kimm, A. Nunes, K. Licha, M. Aichler, A. Walch, E. J. Rummeny, V. Ntziachristos, and R. Meier, “Optoacoustic imaging and staging of inflammation in a murine model of arthritis,” Arthritis Rheumatol. 66(8), 2071–2078 (2014).
[Crossref] [PubMed]

Burns (1)

Y. Tsunoi, S. Sato, S. Kawauchi, H. Ashida, D. Saitoh, and M. Terakawa, “In vivo photoacoustic molecular imaging of the distribution of serum albumin in rat burned skin,” Burns 39(7), 1403–1408 (2013).
[Crossref] [PubMed]

Gastroenterology (1)

S. L. Friedman, “Mechanisms of hepatic fibrogenesis,” Gastroenterology 134(6), 1655–1669 (2008).
[Crossref] [PubMed]

Hepatology (1)

D. C. Rockey, S. H. Caldwell, Z. D. Goodman, R. C. Nelson, A. D. Smith, and American Association for the Study of Liver Diseases, “Liver biopsy,” Hepatology 49(3), 1017–1044 (2009).
[Crossref] [PubMed]

Inverse Probl. (1)

M. Jaeger, S. Schüpbach, A. Gertsch, M. Kitz, and M. Frenz, “Fourier reconstruction in optoacoustic imaging using truncated regularized inverse k-space interpolation,” Inverse Probl. 23(6), S51–S63 (2007).
[Crossref]

J. Biomed. Opt. (3)

Z. Guo, Z. Xu, and L. V. Wang, “Dependence of photoacoustic speckles on boundary roughness,” J. Biomed. Opt. 17(4), 046009 (2012).
[Crossref] [PubMed]

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

D. L. Chamberland, X. Wang, and B. J. Roessler, “Photoacoustic tomography of carrageenan-induced arthritis in a rat model,” J. Biomed. Opt. 13(1), 011005 (2008).
[Crossref] [PubMed]

J. Cereb. Blood Flow Metab. (1)

S. Gottschalk, T. F. Fehm, X. L. Deán-Ben, and D. Razansky, “Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography,” J. Cereb. Blood Flow Metab. 35(4), 531–535 (2015).
[Crossref] [PubMed]

J. Nucl. Med. (1)

S. E. Bohndiek, L. S. Sasportas, S. Machtaler, J. V. Jokerst, S. Hori, and S. S. Gambhir, “Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib,” J. Nucl. Med. 56(12), 1942–1947 (2015).
[Crossref] [PubMed]

Lancet (1)

D. Schuppan and N. H. Afdhal, “Liver cirrhosis,” Lancet 371(9615), 838–851 (2008).
[Crossref] [PubMed]

Nat. Biotechnol. (1)

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Opt. Express (2)

Phys. Med. Biol. (1)

E. M. Strohm, I. Gorelikov, N. Matsuura, and M. C. Kolios, “Modeling photoacoustic spectral features of micron-sized particles,” Phys. Med. Biol. 59(19), 5795–5810 (2014).
[Crossref] [PubMed]

Phys. Rev. Lett. (1)

G. J. Diebold, T. Sun, and M. I. Khan, “Photoacoustic monopole radiation in one, two, and three dimensions,” Phys. Rev. Lett. 67(24), 3384–3387 (1991).
[Crossref] [PubMed]

PLoS One (1)

A. Taruttis, S. Morscher, N. C. Burton, D. Razansky, and V. Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs,” PLoS One 7(1), e30491 (2012).
[Crossref] [PubMed]

Radiology (1)

G. Xu, Z. X. Meng, J. D. Lin, J. Yuan, P. L. Carson, B. Joshi, and X. Wang, “The functional pitch of an organ: quantification of tissue texture with photoacoustic spectrum analysis,” Radiology 271(1), 248–254 (2014).
[Crossref] [PubMed]

Sci. Rep. (4)

G. Xu, Z. X. Meng, J. D. Lin, C. X. Deng, P. L. Carson, J. B. Fowlkes, C. Tao, X. Liu, and X. Wang, “High resolution Physio-chemical Tissue Analysis: Towards Non-invasive In Vivo Biopsy,” Sci. Rep. 6, 16937 (2016).
[Crossref] [PubMed]

X. L. Deán-Ben, S. J. Ford, and D. Razansky, “High-frame rate four dimensional optoacoustic tomography enables visualization of cardiovascular dynamics and mouse heart perfusion,” Sci. Rep. 5, 10133 (2015).

L. J. Rich and M. Seshadri, “Photoacoustic monitoring of tumor and normal tissue response to radiation,” Sci. Rep. 6, 21237 (2016).
[Crossref] [PubMed]

J. Tang, J. E. Coleman, X. Dai, and H. Jiang, “Wearable 3-D Photoacoustic Tomography for Functional Brain Imaging in Behaving Rats,” Sci. Rep. 6, 25470 (2016).
[Crossref] [PubMed]

Tissue Eng. Part C Methods (1)

S. Y. Nam, E. Chung, L. J. Suggs, and S. Y. Emelianov, “Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct,” Tissue Eng. Part C Methods 21(6), 557–566 (2015).
[Crossref] [PubMed]

Toxicology (1)

S. L. Friedman, “Hepatic fibrosis -- overview,” Toxicology 254(3), 120–129 (2008).
[Crossref] [PubMed]

Supplementary Material (2)

NameDescription
» Visualization 1: MP4 (398 KB)      3D photoacoustic visualization (control liver)
» Visualization 2: MP4 (533 KB)      3D photoacoustic visualization (control liver)

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Figures (6)

Fig. 1
Fig. 1 Experimental setup: (a) experimental setups for CCl4-induced liver fibrosis mouse model. CCl4 was administered to mice for 6 weeks to induce liver fibrosis. Control mice are healthy mice that received olive oil. (b) bimodal photoacoustic and ultrasound hand held imaging probe, (c) photoacoustic and ultrasound imaging setup and (d) experimental imaging setup, and scanning plane and direction in mice.
Fig. 2
Fig. 2 Non-invasive photoacoustic (PA) imaging and quantitation in control and CCl4-induced liver fibrosis mouse models. (a) Representative PA/US overlay scanned images of liver from healthy (control) mice (n = 5) and CCl4-treated fibrotic mice (n = 6). The confined blue lines denote the region of interest (ROI) registered during PA imaging and quantitation for the PA images. (b) Cross-view representation of the 3-dimensional volumetric reconstruction of PA imaging in the control livers and fibrotic mouse livers based on the ROI as shown in overlay images (see online Visualization 1 and Visualization 2). (c) The graph depicts the number of PA pixels (calculated in ROI within scanned livers, detailed in methods) in control livers and 6 weeks fibrotic livers. Each symbol represents an individual mouse. Data represent mean ± SEM. ***p<0.001 denotes statistical significance.
Fig. 3
Fig. 3 Photoacoustic frequency analysis. (a) Example of a control PA spectrum versus the spectrum of a fibrotic liver. Notice the difference in spectral content, especially the shift in the spectral peak from 0.5 MHz (control, n = 5) towards 1.5 MHz (fibrotic, n = 6). (b) Contrast in PA spectral amplitude between 1.5 MHz and 0.5 MHz as quantified in a heterogeneity index. In (b), each circle represents an individual mouse. ***p<0.0001 denotes statistical significance.
Fig. 4
Fig. 4 Histological analysis of fibrotic parameters in control and CCl4-induced liver fibrosis mouse model. Representative photomicrographs of (a) Collagen I and (c) CD31 from healthy (control, n = 5), and 6 weeks (n = 6) CCl4-treated fibrotic mice. Quantitative histological analysis of (b) Collagen I and (d) CD31 immuno-histochemical stainings were performed in livers of the individual groups. Each symbol represents an individual mouse. Data represent mean ± SEM. *p<0.05, ***p<0.001 denotes statistical significance.
Fig. 5
Fig. 5 Correlative analysis of number of photoacoustic pixels (PA) and heterogeneity index (HI) with histological parameters. Panels a and b depict correlations between PA pixels and % intensity of Collagen I and CD31 staining respectively. In addition, panel c shows the correlation between collagen I and CD31. Panels d and e show the correlation between the heterogeneity index (HI) and collagen I and CD31 staining respectively. Finally, panel f depicts the correlation between number of PA pixels and HI. Correlations were assessed using Pearson's correlative analysis. The dot plots for all the correlations were generated using the GraphPad Prism software. ‘R2’ denotes Pearson correlation coefficient and ‘p’ denotes statistical significance.
Fig. 6
Fig. 6 Absorption measurements for collagen I. (a) Absorption spectra measured using a Shimadzu UV-2501 spectrophotometer of collagen I / PBS solution in cuvettes. The concentrations were taken as per the average of collagen I concentration in typical fibrotic livers. (b) Plotting of the absorption at 808 nm for the range of concentrations shows proper linear behavior. Assuming 2% of the liver shows collagen scarring and that the total amount of collagen I is concentrated only in these scars, then the approximate absorption coefficient within scars is (0.025 / cm) / 2% = 5 / cm. This is of the same order as the absorption of hemoglobin in functioning blood vessels.

Tables (1)

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Table 1 Antibodies used for the immunohistochemistry

Equations (1)

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HI= | Y( 1.5 MHz ) || Y( 0.5 MHz ) | | Y( 1.5 MHz ) |+| Y( 0.5 MHz ) | ,

Metrics