Abstract

In this study, we in vivo examined injury progression after intracerebral haemorrhage (ICH) induced by collagenase in mice using cross-sectional photoacoustic tomography (csPAT). csPAT displayed high resolution with high sensitivity for ICH detection. The PAT images obtained showed high correlation with conventional histologic images. Quantitative analysis of the hematoma areas detected by csPAT showed high consistency with the neurologic deficit score (NDS). By utilizing the dual-wavelength method, the development of the hemoglobin area was monitored. Our results indicated that noninvasive csPAT can be used to track the dynamic progression of post-ICH, and to evaluate therapeutic interventions in preclinical ICH models.

© 2017 Optical Society of America

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2017 (5)

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

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[PubMed]

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

D. Wu, J. Yang, G. Zhang, and H. Jiang, “Noninvasive in vivo monitoring of collagenase induced intracerebral hemorrhage by photoacoustic tomography,” Biomed. Opt. Express 8(4), 2276–2286 (2017).
[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).
[PubMed]

2016 (3)

L. Xi and H. Jiang, “Integrated photoacoustic and diffuse optical tomography system for imaging of human finger joints in vivo,” J. Biophotonics 9(3), 213–217 (2016).
[PubMed]

I. Olefir, E. Mercep, N. C. Burton, S. V. Ovsepian, and V. Ntziachristos, “Hybrid multispectral optoacoustic and ultrasound tomography for morphological and physiological brain imaging,” J. Biomed. Opt. 21(8), 86005 (2016).
[PubMed]

D. Wu and J. Zhang, “In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI,” Neuroimage 125, 84–93 (2016).
[PubMed]

2015 (3)

O. I. Alomair, I. M. Brereton, M. T. Smith, G. J. Galloway, and N. D. Kurniawan, “In vivo high angular resolution diffusion-weighted imaging of mouse brain at 16.4 Tesla,” PLoS One 10(6), e0130133 (2015).
[PubMed]

L. Xi and H. Jiang, “High resolution three-dimensional photoacoustic imaging of human finger joints in vivo,” Appl. Phys. Lett. 107, 063701 (2015).

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

2014 (5)

C. Darne, Y. Lu, and E. M. Sevick-Muraca, “Small animal fluorescence and bioluminescence tomography: a review of approaches, algorithms and technology update,” Phys. Med. Biol. 59(1), R1–R64 (2014).
[PubMed]

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

W. Zhu, Y. Gao, C. F. Chang, J. R. Wan, S. S. Zhu, and J. Wang, “Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase,” PLoS One 9(5), e97423 (2014).
[PubMed]

X. L. Deán-Ben and D. Razansky, “Adding fifth dimension to optoacoustic imaging: volumetric time-resolved spectrally enriched tomography,” Light Sci. Appl. 3, e137 (2014).

2013 (5)

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

M. M. McDowell, C. P. Kellner, S. M. Barton, C. B. Mikell, E. S. Sussman, S. G. Heuts, and E. S. Connolly, “The role of advanced neuroimaging in intracerebral hemorrhage,” Neurosurg. Focus 34(4), E2 (2013).
[PubMed]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

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

2012 (2)

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

M. Li, R. M. Akhavan-Sharif, R. M. Friedlander, R. Du, and R. Thiex, “What sequences on high-field MR best depict temporal resolution of experimental ICH and edema formation in mice?” J. Biomed. Biotechnol. 2012, 961461 (2012).
[PubMed]

2011 (2)

A. Ng and J. Swanevelder, “Resolution in ultrasound imaging,” Continuing Education in Anaesthesia, Critical Care Pain 11, 186–192 (2011).

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[PubMed]

2010 (3)

V. Ntziachristos, “Going deeper than microscopy: the optical imaging frontier in biology,” Nat. Methods 7(8), 603–614 (2010).
[PubMed]

J. Wang, “Preclinical and clinical research on inflammation after intracerebral hemorrhage,” Prog. Neurobiol. 92(4), 463–477 (2010).
[PubMed]

C. J. van Asch, M. J. Luitse, G. J. Rinkel, I. van der Tweel, A. Algra, and C. J. Klijn, “Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis,” Lancet Neurol. 9(2), 167–176 (2010).
[PubMed]

2009 (1)

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

2008 (1)

C. L. MacLellan, G. Silasi, C. C. Poon, C. L. Edmundson, R. Buist, J. Peeling, and F. Colbourne, “Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion,” J. Cereb. Blood Flow Metab. 28(3), 516–525 (2008).
[PubMed]

2007 (2)

J. Wang and S. Doré, “Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage,” Brain 130(Pt 6), 1643–1652 (2007).
[PubMed]

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

2006 (1)

G. Xi, R. F. Keep, and J. T. Hoff, “Mechanisms of brain injury after intracerebral haemorrhage,” Lancet Neurol. 5(1), 53–63 (2006).
[PubMed]

2005 (1)

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1 Pt 2), 016706 (2005).
[PubMed]

1991 (1)

L. A. Hayman, K. H. Taber, J. J. Ford, and R. N. Bryan, “Mechanisms of MR signal alteration by acute intracerebral blood: old concepts and new theories,” AJNR Am. J. Neuroradiol. 12(5), 899–907 (1991).
[PubMed]

Akhavan-Sharif, R. M.

M. Li, R. M. Akhavan-Sharif, R. M. Friedlander, R. Du, and R. Thiex, “What sequences on high-field MR best depict temporal resolution of experimental ICH and edema formation in mice?” J. Biomed. Biotechnol. 2012, 961461 (2012).
[PubMed]

Algra, A.

C. J. van Asch, M. J. Luitse, G. J. Rinkel, I. van der Tweel, A. Algra, and C. J. Klijn, “Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis,” Lancet Neurol. 9(2), 167–176 (2010).
[PubMed]

Alomair, O. I.

O. I. Alomair, I. M. Brereton, M. T. Smith, G. J. Galloway, and N. D. Kurniawan, “In vivo high angular resolution diffusion-weighted imaging of mouse brain at 16.4 Tesla,” PLoS One 10(6), e0130133 (2015).
[PubMed]

Al-Shahi Salman, R.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Babacan, S. D.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Bamberg, E.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Barton, S. M.

M. M. McDowell, C. P. Kellner, S. M. Barton, C. B. Mikell, E. S. Sussman, S. G. Heuts, and E. S. Connolly, “The role of advanced neuroimaging in intracerebral hemorrhage,” Neurosurg. Focus 34(4), E2 (2013).
[PubMed]

Beard, P.

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[PubMed]

Bednar, B.

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Beer, R.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Beziere, N.

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Brauner, M.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Brereton, I. M.

O. I. Alomair, I. M. Brereton, M. T. Smith, G. J. Galloway, and N. D. Kurniawan, “In vivo high angular resolution diffusion-weighted imaging of mouse brain at 16.4 Tesla,” PLoS One 10(6), e0130133 (2015).
[PubMed]

Bryan, R. N.

L. A. Hayman, K. H. Taber, J. J. Ford, and R. N. Bryan, “Mechanisms of MR signal alteration by acute intracerebral blood: old concepts and new theories,” AJNR Am. J. Neuroradiol. 12(5), 899–907 (1991).
[PubMed]

Buist, R.

C. L. MacLellan, G. Silasi, C. C. Poon, C. L. Edmundson, R. Buist, J. Peeling, and F. Colbourne, “Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion,” J. Cereb. Blood Flow Metab. 28(3), 516–525 (2008).
[PubMed]

Burton, N. C.

I. Olefir, E. Mercep, N. C. Burton, S. V. Ovsepian, and V. Ntziachristos, “Hybrid multispectral optoacoustic and ultrasound tomography for morphological and physiological brain imaging,” J. Biomed. Opt. 21(8), 86005 (2016).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Campbell, A.

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

Carhuapoma, J. R.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Carney, P. R.

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

Carney, P. S.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Chang, C. F.

W. Zhu, Y. Gao, C. F. Chang, J. R. Wan, S. S. Zhu, and J. Wang, “Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase,” PLoS One 9(5), e97423 (2014).
[PubMed]

Chen, W.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Chopp, M.

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Christensen, H.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Clark, C. G.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

Claussen, J.

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Colbourne, F.

C. L. MacLellan, G. Silasi, C. C. Poon, C. L. Edmundson, R. Buist, J. Peeling, and F. Colbourne, “Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion,” J. Cereb. Blood Flow Metab. 28(3), 516–525 (2008).
[PubMed]

Connolly, E. S.

M. M. McDowell, C. P. Kellner, S. M. Barton, C. B. Mikell, E. S. Sussman, S. G. Heuts, and E. S. Connolly, “The role of advanced neuroimaging in intracerebral hemorrhage,” Neurosurg. Focus 34(4), E2 (2013).
[PubMed]

Cordonnier, C.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Csiba, L.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Darne, C.

C. Darne, Y. Lu, and E. M. Sevick-Muraca, “Small animal fluorescence and bioluminescence tomography: a review of approaches, algorithms and technology update,” Phys. Med. Biol. 59(1), R1–R64 (2014).
[PubMed]

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).
[PubMed]

X. L. Deán-Ben and D. Razansky, “Adding fifth dimension to optoacoustic imaging: volumetric time-resolved spectrally enriched tomography,” Light Sci. Appl. 3, e137 (2014).

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

Deisseroth, K.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Doré, S.

J. Wang and S. Doré, “Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage,” Brain 130(Pt 6), 1643–1652 (2007).
[PubMed]

Driessen, W. H.

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Du, R.

M. Li, R. M. Akhavan-Sharif, R. M. Friedlander, R. Du, and R. Thiex, “What sequences on high-field MR best depict temporal resolution of experimental ICH and edema formation in mice?” J. Biomed. Biotechnol. 2012, 961461 (2012).
[PubMed]

Duris, K.

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

Edmundson, C. L.

C. L. MacLellan, G. Silasi, C. C. Poon, C. L. Edmundson, R. Buist, J. Peeling, and F. Colbourne, “Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion,” J. Cereb. Blood Flow Metab. 28(3), 516–525 (2008).
[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).
[PubMed]

Ford, J. J.

L. A. Hayman, K. H. Taber, J. J. Ford, and R. N. Bryan, “Mechanisms of MR signal alteration by acute intracerebral blood: old concepts and new theories,” AJNR Am. J. Neuroradiol. 12(5), 899–907 (1991).
[PubMed]

Forsting, M.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Friedlander, R. M.

M. Li, R. M. Akhavan-Sharif, R. M. Friedlander, R. Du, and R. Thiex, “What sequences on high-field MR best depict temporal resolution of experimental ICH and edema formation in mice?” J. Biomed. Biotechnol. 2012, 961461 (2012).
[PubMed]

Galloway, G. J.

O. I. Alomair, I. M. Brereton, M. T. Smith, G. J. Galloway, and N. D. Kurniawan, “In vivo high angular resolution diffusion-weighted imaging of mouse brain at 16.4 Tesla,” PLoS One 10(6), e0130133 (2015).
[PubMed]

Gao, C.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Gao, Y.

W. Zhu, Y. Gao, C. F. Chang, J. R. Wan, S. S. Zhu, and J. Wang, “Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase,” PLoS One 9(5), e97423 (2014).
[PubMed]

Goddard, L. L.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Gottschalk, A.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Gottschalk, S.

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).
[PubMed]

Han, X.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Han, Y.

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Harnof, S.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Hayman, L. A.

L. A. Hayman, K. H. Taber, J. J. Ford, and R. N. Bryan, “Mechanisms of MR signal alteration by acute intracerebral blood: old concepts and new theories,” AJNR Am. J. Neuroradiol. 12(5), 899–907 (1991).
[PubMed]

Heuts, S. G.

M. M. McDowell, C. P. Kellner, S. M. Barton, C. B. Mikell, E. S. Sussman, S. G. Heuts, and E. S. Connolly, “The role of advanced neuroimaging in intracerebral hemorrhage,” Neurosurg. Focus 34(4), E2 (2013).
[PubMed]

Hoff, J. T.

G. Xi, R. F. Keep, and J. T. Hoff, “Mechanisms of brain injury after intracerebral haemorrhage,” Lancet Neurol. 5(1), 53–63 (2006).
[PubMed]

Horton, N. G.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

Hou, Z.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Huang, H.

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

Jetzfellner, T.

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Jiang, H.

D. Wu, J. Yang, G. Zhang, and H. Jiang, “Noninvasive in vivo monitoring of collagenase induced intracerebral hemorrhage by photoacoustic tomography,” Biomed. Opt. Express 8(4), 2276–2286 (2017).
[PubMed]

J. Yang, D. Wu, Y. Tang, and H. Jiang, “Photoacoustic microscopy of electronic acupuncture (EA) effect in small animals,” J. Biophotonics 10(2), 217–223 (2017).
[PubMed]

L. Xi and H. Jiang, “Integrated photoacoustic and diffuse optical tomography system for imaging of human finger joints in vivo,” J. Biophotonics 9(3), 213–217 (2016).
[PubMed]

L. Xi and H. Jiang, “High resolution three-dimensional photoacoustic imaging of human finger joints in vivo,” Appl. Phys. Lett. 107, 063701 (2015).

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

Karki, K.

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Kay, K.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Keep, R. F.

G. Xi, R. F. Keep, and J. T. Hoff, “Mechanisms of brain injury after intracerebral haemorrhage,” Lancet Neurol. 5(1), 53–63 (2006).
[PubMed]

Kellner, C. P.

M. M. McDowell, C. P. Kellner, S. M. Barton, C. B. Mikell, E. S. Sussman, S. G. Heuts, and E. S. Connolly, “The role of advanced neuroimaging in intracerebral hemorrhage,” Neurosurg. Focus 34(4), E2 (2013).
[PubMed]

Kim, T.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Klijn, C. J.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

C. J. van Asch, M. J. Luitse, G. J. Rinkel, I. van der Tweel, A. Algra, and C. J. Klijn, “Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis,” Lancet Neurol. 9(2), 167–176 (2010).
[PubMed]

Knight, R. A.

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Kobat, D.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

Krafft, P. R.

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

Krieger, D.

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Kurniawan, N. D.

O. I. Alomair, I. M. Brereton, M. T. Smith, G. J. Galloway, and N. D. Kurniawan, “In vivo high angular resolution diffusion-weighted imaging of mouse brain at 16.4 Tesla,” PLoS One 10(6), e0130133 (2015).
[PubMed]

Lan, X.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Ledbetter, K. A.

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Lekic, T.

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

Li, L.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Li, M.

M. Li, R. M. Akhavan-Sharif, R. M. Friedlander, R. Du, and R. Thiex, “What sequences on high-field MR best depict temporal resolution of experimental ICH and edema formation in mice?” J. Biomed. Biotechnol. 2012, 961461 (2012).
[PubMed]

Li, Q.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Liewald, J. F.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Lin, L.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Lu, Y.

C. Darne, Y. Lu, and E. M. Sevick-Muraca, “Small animal fluorescence and bioluminescence tomography: a review of approaches, algorithms and technology update,” Phys. Med. Biol. 59(1), R1–R64 (2014).
[PubMed]

Luitse, M. J.

C. J. van Asch, M. J. Luitse, G. J. Rinkel, I. van der Tweel, A. Algra, and C. J. Klijn, “Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis,” Lancet Neurol. 9(2), 167–176 (2010).
[PubMed]

Ma, C.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

MacLellan, C. L.

C. L. MacLellan, G. Silasi, C. C. Poon, C. L. Edmundson, R. Buist, J. Peeling, and F. Colbourne, “Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion,” J. Cereb. Blood Flow Metab. 28(3), 516–525 (2008).
[PubMed]

Maslov, K.

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Wang, L.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Wang, L. P.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Wang, L. V.

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1 Pt 2), 016706 (2005).
[PubMed]

Wang, W.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Wang, Z.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Watzke, N.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Wise, F. W.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

Wood, P. G.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Wu, D.

D. Wu, J. Yang, G. Zhang, and H. Jiang, “Noninvasive in vivo monitoring of collagenase induced intracerebral hemorrhage by photoacoustic tomography,” Biomed. Opt. Express 8(4), 2276–2286 (2017).
[PubMed]

J. Yang, D. Wu, Y. Tang, and H. Jiang, “Photoacoustic microscopy of electronic acupuncture (EA) effect in small animals,” J. Biophotonics 10(2), 217–223 (2017).
[PubMed]

D. Wu and J. Zhang, “In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI,” Neuroimage 125, 84–93 (2016).
[PubMed]

Xi, G.

G. Xi, R. F. Keep, and J. T. Hoff, “Mechanisms of brain injury after intracerebral haemorrhage,” Lancet Neurol. 5(1), 53–63 (2006).
[PubMed]

Xi, L.

L. Xi and H. Jiang, “Integrated photoacoustic and diffuse optical tomography system for imaging of human finger joints in vivo,” J. Biophotonics 9(3), 213–217 (2016).
[PubMed]

L. Xi and H. Jiang, “High resolution three-dimensional photoacoustic imaging of human finger joints in vivo,” Appl. Phys. Lett. 107, 063701 (2015).

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

Xu, C.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

Xu, M.

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1 Pt 2), 016706 (2005).
[PubMed]

Yang, D.

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Yang, J.

D. Wu, J. Yang, G. Zhang, and H. Jiang, “Noninvasive in vivo monitoring of collagenase induced intracerebral hemorrhage by photoacoustic tomography,” Biomed. Opt. Express 8(4), 2276–2286 (2017).
[PubMed]

J. Yang, D. Wu, Y. Tang, and H. Jiang, “Photoacoustic microscopy of electronic acupuncture (EA) effect in small animals,” J. Biophotonics 10(2), 217–223 (2017).
[PubMed]

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Yao, J.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Zhang, F.

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Zhang, G.

Zhang, J.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

D. Wu and J. Zhang, “In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI,” Neuroimage 125, 84–93 (2016).
[PubMed]

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

Zhang, J. H.

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

Zhang, R.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Zhang, T.

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

Zhao, X.

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Zhou, J.

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

Zhou, R.

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

Zhu, L.

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Zhu, S. S.

W. Zhu, Y. Gao, C. F. Chang, J. R. Wan, S. S. Zhu, and J. Wang, “Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase,” PLoS One 9(5), e97423 (2014).
[PubMed]

Zhu, W.

W. Zhu, Y. Gao, C. F. Chang, J. R. Wan, S. S. Zhu, and J. Wang, “Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase,” PLoS One 9(5), e97423 (2014).
[PubMed]

AJNR Am. J. Neuroradiol. (1)

L. A. Hayman, K. H. Taber, J. J. Ford, and R. N. Bryan, “Mechanisms of MR signal alteration by acute intracerebral blood: old concepts and new theories,” AJNR Am. J. Neuroradiol. 12(5), 899–907 (1991).
[PubMed]

Appl. Phys. Lett. (1)

L. Xi and H. Jiang, “High resolution three-dimensional photoacoustic imaging of human finger joints in vivo,” Appl. Phys. Lett. 107, 063701 (2015).

Biomed. Opt. Express (1)

Brain (1)

J. Wang and S. Doré, “Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage,” Brain 130(Pt 6), 1643–1652 (2007).
[PubMed]

Continuing Education in Anaesthesia, Critical Care Pain (1)

A. Ng and J. Swanevelder, “Resolution in ultrasound imaging,” Continuing Education in Anaesthesia, Critical Care Pain 11, 186–192 (2011).

Int. J. Stroke (1)

T. Steiner, R. Al-Shahi Salman, R. Beer, H. Christensen, C. Cordonnier, L. Csiba, M. Forsting, S. Harnof, C. J. Klijn, D. Krieger, A. D. Mendelow, C. Molina, J. Montaner, K. Overgaard, J. Petersson, R. O. Roine, E. Schmutzhard, K. Schwerdtfeger, C. Stapf, T. Tatlisumak, B. M. Thomas, D. Toni, A. Unterberg, and M. Wagner, “European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage,” Int. J. Stroke 9(7), 840–855 (2014).
[PubMed]

Interface Focus (1)

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[PubMed]

J. Biomed. Biotechnol. (1)

M. Li, R. M. Akhavan-Sharif, R. M. Friedlander, R. Du, and R. Thiex, “What sequences on high-field MR best depict temporal resolution of experimental ICH and edema formation in mice?” J. Biomed. Biotechnol. 2012, 961461 (2012).
[PubMed]

J. Biomed. Opt. (1)

I. Olefir, E. Mercep, N. C. Burton, S. V. Ovsepian, and V. Ntziachristos, “Hybrid multispectral optoacoustic and ultrasound tomography for morphological and physiological brain imaging,” J. Biomed. Opt. 21(8), 86005 (2016).
[PubMed]

J. Biophotonics (2)

J. Yang, D. Wu, Y. Tang, and H. Jiang, “Photoacoustic microscopy of electronic acupuncture (EA) effect in small animals,” J. Biophotonics 10(2), 217–223 (2017).
[PubMed]

L. Xi and H. Jiang, “Integrated photoacoustic and diffuse optical tomography system for imaging of human finger joints in vivo,” J. Biophotonics 9(3), 213–217 (2016).
[PubMed]

J. Cereb. Blood Flow Metab. (2)

C. L. MacLellan, G. Silasi, C. C. Poon, C. L. Edmundson, R. Buist, J. Peeling, and F. Colbourne, “Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion,” J. Cereb. Blood Flow Metab. 28(3), 516–525 (2008).
[PubMed]

J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. R. Carney, and H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awake-moving rats,” J. Cereb. Blood Flow Metab. 35(8), 1224–1232 (2015).
[PubMed]

J. Vis. Exp. (1)

P. R. Krafft, W. B. Rolland, K. Duris, T. Lekic, A. Campbell, J. Tang, and J. H. Zhang, “Modeling Intracerebral Hemorrhage in Mice: Injection of Autologous Blood or Bacterial Collagenase,” J. Vis. Exp. 67(67), e4289 (2012).
[PubMed]

Lancet Neurol. (2)

G. Xi, R. F. Keep, and J. T. Hoff, “Mechanisms of brain injury after intracerebral haemorrhage,” Lancet Neurol. 5(1), 53–63 (2006).
[PubMed]

C. J. van Asch, M. J. Luitse, G. J. Rinkel, I. van der Tweel, A. Algra, and C. J. Klijn, “Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis,” Lancet Neurol. 9(2), 167–176 (2010).
[PubMed]

Light Sci. Appl. (1)

X. L. Deán-Ben and D. Razansky, “Adding fifth dimension to optoacoustic imaging: volumetric time-resolved spectrally enriched tomography,” Light Sci. Appl. 3, e137 (2014).

Nat. Methods (1)

V. Ntziachristos, “Going deeper than microscopy: the optical imaging frontier in biology,” Nat. Methods 7(8), 603–614 (2010).
[PubMed]

Nat. Photonics (2)

T. Kim, R. Zhou, M. Mir, S. D. Babacan, P. S. Carney, L. L. Goddard, and G. Popescu, “White-light diffraction tomography of unlabelled live cells,” Nat. Photonics 8, 256–263 (2014).

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[PubMed]

Nature (1)

F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, and K. Deisseroth, “Multimodal fast optical interrogation of neural circuitry,” Nature 446(7136), 633–639 (2007).
[PubMed]

Nature Biomedical Engineering (1)

L. Li, L. Zhu, C. Ma, L. Lin, J. Yao, L. Wang, K. Maslov, R. Zhang, W. Chen, and J. Shi, “Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution,” Nature Biomedical Engineering 1, 0071 (2017).

Neuroimage (3)

D. Wu and J. Zhang, “In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI,” Neuroimage 125, 84–93 (2016).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

N. C. Burton, M. Patel, S. Morscher, W. H. Driessen, J. Claussen, N. Beziere, T. Jetzfellner, A. Taruttis, D. Razansky, B. Bednar, and V. Ntziachristos, “Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization,” Neuroimage 65, 522–528 (2013).
[PubMed]

Neurophotonics (1)

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).
[PubMed]

Neurosurg. Focus (1)

M. M. McDowell, C. P. Kellner, S. M. Barton, C. B. Mikell, E. S. Sussman, S. G. Heuts, and E. S. Connolly, “The role of advanced neuroimaging in intracerebral hemorrhage,” Neurosurg. Focus 34(4), E2 (2013).
[PubMed]

Photoacoustics (1)

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

Phys. Med. Biol. (1)

C. Darne, Y. Lu, and E. M. Sevick-Muraca, “Small animal fluorescence and bioluminescence tomography: a review of approaches, algorithms and technology update,” Phys. Med. Biol. 59(1), R1–R64 (2014).
[PubMed]

Phys. Rev. E Stat. Nonlin. Soft Matter Phys. (1)

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1 Pt 2), 016706 (2005).
[PubMed]

PLoS One (2)

W. Zhu, Y. Gao, C. F. Chang, J. R. Wan, S. S. Zhu, and J. Wang, “Mouse models of intracerebral hemorrhage in ventricle, cortex, and hippocampus by injections of autologous blood or collagenase,” PLoS One 9(5), e97423 (2014).
[PubMed]

O. I. Alomair, I. M. Brereton, M. T. Smith, G. J. Galloway, and N. D. Kurniawan, “In vivo high angular resolution diffusion-weighted imaging of mouse brain at 16.4 Tesla,” PLoS One 10(6), e0130133 (2015).
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Prog. Neurobiol. (1)

J. Wang, “Preclinical and clinical research on inflammation after intracerebral hemorrhage,” Prog. Neurobiol. 92(4), 463–477 (2010).
[PubMed]

Sci. Rep. (1)

J. Yang, Q. Li, Z. Wang, C. Qi, X. Han, X. Lan, J. Wan, W. Wang, X. Zhao, Z. Hou, C. Gao, J. R. Carhuapoma, S. Mori, J. Zhang, and J. Wang, “Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice,” Sci. Rep. 7, 40358 (2017).
[PubMed]

Stroke (1)

K. Karki, R. A. Knight, Y. Han, D. Yang, J. Zhang, K. A. Ledbetter, M. Chopp, and D. M. Seyfried, “Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage,” Stroke 40(10), 3384–3389 (2009).
[PubMed]

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G. Paxinos and C. Watson, The rat brain in stereotaxic coordinates, (Academic Press, 1998).

B. R. Masters and L. V. Wang, Photoacoustic Imaging and Spectroscopy (CRC Press, 2009).

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Figures (7)

Fig. 1
Fig. 1 Modeling ICH in mice. (a) The simplified schematic of a coronal brain section 0.2 mm anterior of bregma illustrates the proposed location of collagenase injection. LV: lateral ventricle, CPu: caudate-putamen, cc: corpus callosum. (b) Representative photograph of a coronal brain section, obtained on day 3 after injection of collagenase.
Fig. 2
Fig. 2 Experimental configuration of photoacoustic imaging system. (a) The panorama of imaging system. OPO: Optical Parametric Oscillator, PD: Photodiode, BS: Beam Splitter, AH: Animal Holder, TR: Transducer, OF: Optical Fiber. RC: resin chamber (b) Close-up view of the resin chamber. Line-shaped light was delivered to the imaging object at horizontal plane, and the focused transducer was set exactly at the same horizontal plane to obtain the highest sensitivity of ultrasound detection.
Fig. 3
Fig. 3 Phantom testing. (a) Reconstructed image of the carbon fibers. (b) Lateral profile of the selected carbon fiber. (c) The geometry of 2 suture lines. (d) Image at position 1(z = 0mm), only one suture line was observed here. (e) Image at position 2(z = −0.5mm), two suture line were observed here (f) Image at position 3(z = −1mm), one suture line was observed.
Fig. 4
Fig. 4 Three typical coronal slices of a mouse brain. (a) Three slices of PAT images. CPu: caudate-putamen, cc: corpus callosum TH: thalamus, HY: hypothalamus. HP: hippocampus (b) Histology images of the corresponding PAT slices.
Fig. 5
Fig. 5 Development of the haemorrhagic lesion over time assessed by PAT in comparison with the histology. (a) Representative PAT images show the haemorrhagic lesion (red outline) on 1, 3, 7, and 28 days after ICH. (b) Corresponding frozen brain slices (unstained) on 1, 3, 7, and 28 days after ICH. Different cohorts of animals were used for PAT scans and for histology. (c, d, e) Quantitative analysis shows that the time-dependent changes in ratio of total lesion area to the contralateral hemisphere area were similar when assessed by PAT and histology. (PAT: n = 3 at each time point; Histology: n = 3 at each time point. CL: contralateral hemisphere)
Fig. 6
Fig. 6 Development of the haemorrhagic area using two wavelengths. (a) Representative oxy-signal images on day 1, 3, 7, and 28 days after ICH. (b) Representative deoxy-signal images on day 1, 3, 7, and 28 days after ICH. (c) Corresponding frozen brain slices (unstained) on 1, 3, 7, and 28 days after ICH. (d, e) Quantitative analysis shows the time-dependent changes in ratio of HVR in CPu to the contralateral hemisphere area. (CL = contralateral;*P<0.05 vs day1;one-way ANOVA).
Fig. 7
Fig. 7 Neurologic deficit score (NDS) correlates with brain region area changes assessed by PAT. (a) Major structures in the ICH brain in PA image (white line indicated the cortex thickness). (b) Quantitative analysis of PA image showed that the ratio of ipsilateral striatum to contralateral hemisphere area increased significantly at day 1 and day 3, then progressively decreased at days 7 and 28 (CL: contralateral hemisphere). (c)The cortex thickness also decreased significantly after ICH then increased at day 28 (d) Neurologic deficit progressively decreased from day 1 to day 28 after ICH (n = 6 mice). (e) Scatter plot shows positive correlation between lesion area on PAT and NDS (n = 3 mice).

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H( x, λ m )=Φ( x )[ ε HbR ( λ m ) C HbR ( x )+ ε Hb O 2 ( λ m ) C Hb O 2 ( x ) ].

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