Abstract

The feasibility of photoacoustic microscopy (PAM) for evaluation of angiogenesis inhibitor was investigated on a chick embryo model in vivo. Different concentrations of the angiogenesis inhibitor, Sunitinib, were applied to the chorioallantoic membrane (CAM) of the chick embryos. Imaging of microvasculature in embryo CAMs was acquired using a laser-scanning PAM system; while the optical microscopy (OM) capturing the microvascular images of the same set of CAMs for comparison served as a gold standard for validating the results from PAM. The microvascular density as a function of applied Sunitinib concentration has been quantified in both PAM and OM images. The results from these two modalities have a good agreement, suggesting that PAM could provide an unbiased quantification of microvascular density for objective evaluation of anti-angiogenesis medication. In comparison with conventional OM which enables only two-dimensional enface imaging, PAM is capable of three-dimensional analysis of microvessels, including not only morphology but also functions, as demonstrated in part by the imaging result on a canine bladder model. The emerging PAM technique shows promise to be used in clinical and preclinical settings for comprehensive and objective evaluation of anti-angiogenesis medications.

© 2013 Optical Society of America

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2013 (2)

S.-L. Chen, Z. Xie, L. J. Guo, X. Wang, “A fiber-optic system for dual-modality photoacoustic microscopy and confocal fluorescence microscopy using miniature components,” Photoacoustics 1(2), 30–35 (2013).
[CrossRef]

E. M. Strohm, E. S. L. Berndl, M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustics,” Biophys. J. 105(1), 59–67 (2013).
[CrossRef] [PubMed]

2012 (3)

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

C. Zhang, K. Maslov, J. Yao, L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[CrossRef] [PubMed]

S.-L. Chen, Z. Xie, T. Ling, L. J. Guo, X. Wei, X. Wang, “Miniaturized all-optical photoacoustic microscopy based on microelectromechanical systems mirror scanning,” Opt. Lett. 37(20), 4263–4265 (2012).
[CrossRef] [PubMed]

2011 (3)

S.-L. Chen, Z. Xie, P. L. Carson, X. Wang, L. J. Guo, “In vivo flow speed measurement of capillaries by photoacoustic correlation spectroscopy,” Opt. Lett. 36(20), 4017–4019 (2011).
[CrossRef] [PubMed]

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Z. Xie, S.-L. Chen, T. Ling, L. J. Guo, P. L. Carson, X. Wang, “Pure optical photoacoustic microscopy,” Opt. Express 19(10), 9027–9034 (2011).
[CrossRef] [PubMed]

2010 (2)

I. Goze, A. Cetin, A. Goze, “Investigation of effects of essential oils of Origanum minutiflorum O Schwarz PH Davis and Cyclotrichium niveum (Labiatae) plants on angiogenesis in shell-less chick embryo culture,” Afr. J. Biotechnol. 9, 2156–2160 (2010).

H. C. Yalcin, A. Shekhar, A. A. Rane, J. T. Butcher, “An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications,” J. Vis. Exp. 44(44), 2154 (2010).
[PubMed]

2009 (2)

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[CrossRef] [PubMed]

2008 (5)

L. V. Wang, “Tutorial on photoacoustic microscopy and computed tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

K. Maslov, H. F. Zhang, S. Hu, L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

D. Ribatti, “Chick embryo chorioallantoic membrane as a useful tool to study angiogenesis,” Int Rev Cell Mol Biol 270, 181–224 (2008).
[CrossRef] [PubMed]

A. M. Cimpean, D. Ribatti, M. Raica, “The chick embryo chorioallantoic membrane as a model to study tumor metastasis,” Angiogenesis 11(4), 311–319 (2008).
[CrossRef] [PubMed]

C. N. Doukas, I. Maglogiannis, A. A. Chatziioannou, “Computer-supported angiogenesis quantification using image analysis and statistical averaging,” IEEE Trans. Inf. Technol. Biomed. 12(5), 650–657 (2008).
[CrossRef] [PubMed]

2007 (3)

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

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

R. K. Wang, S. L. Jacques, Z. Ma, S. Hurst, S. R. Hanson, A. Gruber, “Three dimensional optical angiography,” Opt. Express 15(7), 4083–4097 (2007).
[CrossRef] [PubMed]

2006 (2)

S. Makita, Y. Hong, M. Yamanari, T. Yatagai, Y. Yasuno, “Optical coherence angiography,” Opt. Express 14(17), 7821–7840 (2006).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

2004 (2)

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

C. Peifer, G. Dannhardt, “A novel quantitative chick embryo assay as an angiogenesis model using digital image analysis,” Anticancer Res. 24(3a), 1545–1551 (2004).
[PubMed]

2000 (1)

A. W. Griffioen, G. Molema, “Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation,” Pharmacol. Rev. 52(2), 237–268 (2000).
[PubMed]

1999 (1)

H. Pairleitner, H. Steiner, G. Hasenoehrl, A. Staudach, “Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization,” Ultrasound Obstet. Gynecol. 14(2), 139–143 (1999).
[CrossRef] [PubMed]

1997 (2)

J. A. Izatt, M. D. Kulkarni, S. Yazdanfar, J. K. Barton, A. J. Welch, “In vivo bidirectional color Doppler flow imaging of picoliter blood volumes using optical coherence tomography,” Opt. Lett. 22(18), 1439–1441 (1997).
[CrossRef] [PubMed]

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

1972 (1)

J. Folkman, “Anti-angiogenesis: new concept for therapy of solid tumors,” Ann. Surg. 175(3), 409–416 (1972).
[CrossRef] [PubMed]

Alitalo, K.

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

Allred, E.

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

Alminaite, A.

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

Antonaci, S.

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

Arbeit, J. M.

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Ballini, J.-P.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

Barton, J. K.

Bauman, G.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Berndl, E. S. L.

E. M. Strohm, E. S. L. Berndl, M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustics,” Biophys. J. 105(1), 59–67 (2013).
[CrossRef] [PubMed]

Butcher, J. T.

H. C. Yalcin, A. Shekhar, A. A. Rane, J. T. Butcher, “An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications,” J. Vis. Exp. 44(44), 2154 (2010).
[PubMed]

Bygrave, M.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Carson, P. L.

Cetin, A.

I. Goze, A. Cetin, A. Goze, “Investigation of effects of essential oils of Origanum minutiflorum O Schwarz PH Davis and Cyclotrichium niveum (Labiatae) plants on angiogenesis in shell-less chick embryo culture,” Afr. J. Biotechnol. 9, 2156–2160 (2010).

Chatziioannou, A. A.

C. N. Doukas, I. Maglogiannis, A. A. Chatziioannou, “Computer-supported angiogenesis quantification using image analysis and statistical averaging,” IEEE Trans. Inf. Technol. Biomed. 12(5), 650–657 (2008).
[CrossRef] [PubMed]

Chen, S.-L.

Chin, J. L.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Cimpean, A. M.

A. M. Cimpean, D. Ribatti, M. Raica, “The chick embryo chorioallantoic membrane as a model to study tumor metastasis,” Angiogenesis 11(4), 311–319 (2008).
[CrossRef] [PubMed]

Connors, S.

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

Dannhardt, G.

C. Peifer, G. Dannhardt, “A novel quantitative chick embryo assay as an angiogenesis model using digital image analysis,” Anticancer Res. 24(3a), 1545–1551 (2004).
[PubMed]

Doukas, C. N.

C. N. Doukas, I. Maglogiannis, A. A. Chatziioannou, “Computer-supported angiogenesis quantification using image analysis and statistical averaging,” IEEE Trans. Inf. Technol. Biomed. 12(5), 650–657 (2008).
[CrossRef] [PubMed]

Drangova, M.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Dunmore-Buyze, J.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Fenster, A.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Folkman, J.

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

J. Folkman, “Anti-angiogenesis: new concept for therapy of solid tumors,” Ann. Surg. 175(3), 409–416 (1972).
[CrossRef] [PubMed]

Fransvea, E.

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

Giannelli, G.

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

Goze, A.

I. Goze, A. Cetin, A. Goze, “Investigation of effects of essential oils of Origanum minutiflorum O Schwarz PH Davis and Cyclotrichium niveum (Labiatae) plants on angiogenesis in shell-less chick embryo culture,” Afr. J. Biotechnol. 9, 2156–2160 (2010).

Goze, I.

I. Goze, A. Cetin, A. Goze, “Investigation of effects of essential oils of Origanum minutiflorum O Schwarz PH Davis and Cyclotrichium niveum (Labiatae) plants on angiogenesis in shell-less chick embryo culture,” Afr. J. Biotechnol. 9, 2156–2160 (2010).

Greenberg, N. M.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Griffioen, A. W.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

A. W. Griffioen, G. Molema, “Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation,” Pharmacol. Rev. 52(2), 237–268 (2000).
[PubMed]

Gruber, A.

Guo, L. J.

Hanson, S. R.

Hasenoehrl, G.

H. Pairleitner, H. Steiner, G. Hasenoehrl, A. Staudach, “Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization,” Ultrasound Obstet. Gynecol. 14(2), 139–143 (1999).
[CrossRef] [PubMed]

Holdsworth, D. W.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Hong, Y.

Hu, S.

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

K. Maslov, H. F. Zhang, S. Hu, L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

Hurst, S.

Ilmonen, M.

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

Izatt, J. A.

Izawa, J. I.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Jacques, S. L.

Jiang, H.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Kolios, M. C.

E. M. Strohm, E. S. L. Berndl, M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustics,” Biophys. J. 105(1), 59–67 (2013).
[CrossRef] [PubMed]

Kovalski, J. R.

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Kulkarni, M. D.

Lacefield, J. C.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Lavezzari, G.

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

Ling, T.

Lovisa, B.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

Ma, Z.

Maglogiannis, I.

C. N. Doukas, I. Maglogiannis, A. A. Chatziioannou, “Computer-supported angiogenesis quantification using image analysis and statistical averaging,” IEEE Trans. Inf. Technol. Biomed. 12(5), 650–657 (2008).
[CrossRef] [PubMed]

Makita, S.

Maslov, K.

C. Zhang, K. Maslov, J. Yao, L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[CrossRef] [PubMed]

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

K. Maslov, H. F. Zhang, S. Hu, L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

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

H. F. Zhang, K. Maslov, G. Stoica, L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Mazzocca, A.

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

Molema, G.

A. W. Griffioen, G. Molema, “Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation,” Pharmacol. Rev. 52(2), 237–268 (2000).
[PubMed]

Moussa, M.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Nowak-Sliwinska, P.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

Oladipupo, S. S.

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Ozerdem, U.

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

Pairleitner, H.

H. Pairleitner, H. Steiner, G. Hasenoehrl, A. Staudach, “Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization,” Ultrasound Obstet. Gynecol. 14(2), 139–143 (1999).
[CrossRef] [PubMed]

Peifer, C.

C. Peifer, G. Dannhardt, “A novel quantitative chick embryo assay as an angiogenesis model using digital image analysis,” Anticancer Res. 24(3a), 1545–1551 (2004).
[PubMed]

Perez-Atayde, A. R.

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

Raica, M.

A. M. Cimpean, D. Ribatti, M. Raica, “The chick embryo chorioallantoic membrane as a model to study tumor metastasis,” Angiogenesis 11(4), 311–319 (2008).
[CrossRef] [PubMed]

Rajantie, I.

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

Rane, A. A.

H. C. Yalcin, A. Shekhar, A. A. Rane, J. T. Butcher, “An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications,” J. Vis. Exp. 44(44), 2154 (2010).
[PubMed]

Ribatti, D.

D. Ribatti, “Chick embryo chorioallantoic membrane as a useful tool to study angiogenesis,” Int Rev Cell Mol Biol 270, 181–224 (2008).
[CrossRef] [PubMed]

A. M. Cimpean, D. Ribatti, M. Raica, “The chick embryo chorioallantoic membrane as a model to study tumor metastasis,” Angiogenesis 11(4), 311–319 (2008).
[CrossRef] [PubMed]

Sallan, S. E.

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

Salven, P.

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

Santeford, A. C.

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Shekhar, A.

H. C. Yalcin, A. Shekhar, A. A. Rane, J. T. Butcher, “An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications,” J. Vis. Exp. 44(44), 2154 (2010).
[PubMed]

Shohet, R. V.

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Staudach, A.

H. Pairleitner, H. Steiner, G. Hasenoehrl, A. Staudach, “Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization,” Ultrasound Obstet. Gynecol. 14(2), 139–143 (1999).
[CrossRef] [PubMed]

Steiner, H.

H. Pairleitner, H. Steiner, G. Hasenoehrl, A. Staudach, “Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization,” Ultrasound Obstet. Gynecol. 14(2), 139–143 (1999).
[CrossRef] [PubMed]

Stoica, G.

H. F. Zhang, K. Maslov, G. Stoica, L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Strohm, E. M.

E. M. Strohm, E. S. L. Berndl, M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustics,” Biophys. J. 105(1), 59–67 (2013).
[CrossRef] [PubMed]

Tedrow, U.

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

Valiyeva, F.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

van Beijnum, J. R.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

van den Bergh, H.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

Wang, L. V.

C. Zhang, K. Maslov, J. Yao, L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[CrossRef] [PubMed]

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[CrossRef] [PubMed]

K. Maslov, H. F. Zhang, S. Hu, L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

L. V. Wang, “Tutorial on photoacoustic microscopy and computed tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

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

H. F. Zhang, K. Maslov, G. Stoica, L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Wang, R. K.

Wang, X.

Wei, X.

Weiss, A.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

Welch, A. J.

Winter, S. F.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Wong, T. J.

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

Xie, Z.

Xuan, J. W.

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Yalcin, H. C.

H. C. Yalcin, A. Shekhar, A. A. Rane, J. T. Butcher, “An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications,” J. Vis. Exp. 44(44), 2154 (2010).
[PubMed]

Yamanari, M.

Yao, J.

C. Zhang, K. Maslov, J. Yao, L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[CrossRef] [PubMed]

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Yasuno, Y.

Yatagai, T.

Yazdanfar, S.

Zhang, C.

C. Zhang, K. Maslov, J. Yao, L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[CrossRef] [PubMed]

Zhang, H. F.

K. Maslov, H. F. Zhang, S. Hu, L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

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

H. F. Zhang, K. Maslov, G. Stoica, L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Afr. J. Biotechnol. (1)

I. Goze, A. Cetin, A. Goze, “Investigation of effects of essential oils of Origanum minutiflorum O Schwarz PH Davis and Cyclotrichium niveum (Labiatae) plants on angiogenesis in shell-less chick embryo culture,” Afr. J. Biotechnol. 9, 2156–2160 (2010).

Am. J. Pathol. (1)

A. R. Perez-Atayde, S. E. Sallan, U. Tedrow, S. Connors, E. Allred, J. Folkman, “Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia,” Am. J. Pathol. 150(3), 815–821 (1997).
[PubMed]

Angiogenesis (1)

A. M. Cimpean, D. Ribatti, M. Raica, “The chick embryo chorioallantoic membrane as a model to study tumor metastasis,” Angiogenesis 11(4), 311–319 (2008).
[CrossRef] [PubMed]

Ann. Surg. (1)

J. Folkman, “Anti-angiogenesis: new concept for therapy of solid tumors,” Ann. Surg. 175(3), 409–416 (1972).
[CrossRef] [PubMed]

Anticancer Res. (1)

C. Peifer, G. Dannhardt, “A novel quantitative chick embryo assay as an angiogenesis model using digital image analysis,” Anticancer Res. 24(3a), 1545–1551 (2004).
[PubMed]

Biophys. J. (1)

E. M. Strohm, E. S. L. Berndl, M. C. Kolios, “Probing red blood cell morphology using high-frequency photoacoustics,” Biophys. J. 105(1), 59–67 (2013).
[CrossRef] [PubMed]

Blood (2)

I. Rajantie, M. Ilmonen, A. Alminaite, U. Ozerdem, K. Alitalo, P. Salven, “Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells,” Blood 104(7), 2084–2086 (2004).
[CrossRef] [PubMed]

S. S. Oladipupo, S. Hu, A. C. Santeford, J. Yao, J. R. Kovalski, R. V. Shohet, K. Maslov, L. V. Wang, J. M. Arbeit, “Conditional HIF-1 induction produces multistage neovascularization with stage-specific sensitivity to VEGFR inhibitors and myeloid cell independence,” Blood 117(15), 4142–4153 (2011).
[CrossRef] [PubMed]

Cancer Res. (1)

J. W. Xuan, M. Bygrave, H. Jiang, F. Valiyeva, J. Dunmore-Buyze, D. W. Holdsworth, J. I. Izawa, G. Bauman, M. Moussa, S. F. Winter, N. M. Greenberg, J. L. Chin, M. Drangova, A. Fenster, J. C. Lacefield, “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Res. 67(6), 2830–2839 (2007).
[CrossRef] [PubMed]

Hepatology (1)

A. Mazzocca, E. Fransvea, G. Lavezzari, S. Antonaci, G. Giannelli, “Inhibition of transforming growth factor beta receptor I kinase blocks hepatocellular carcinoma growth through neo-angiogenesis regulation,” Hepatology 50(4), 1140–1151 (2009).
[CrossRef] [PubMed]

IEEE J. Sel. Top. Quantum Electron. (1)

L. V. Wang, “Tutorial on photoacoustic microscopy and computed tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

IEEE Trans. Inf. Technol. Biomed. (1)

C. N. Doukas, I. Maglogiannis, A. A. Chatziioannou, “Computer-supported angiogenesis quantification using image analysis and statistical averaging,” IEEE Trans. Inf. Technol. Biomed. 12(5), 650–657 (2008).
[CrossRef] [PubMed]

Int Rev Cell Mol Biol (1)

D. Ribatti, “Chick embryo chorioallantoic membrane as a useful tool to study angiogenesis,” Int Rev Cell Mol Biol 270, 181–224 (2008).
[CrossRef] [PubMed]

J. Biomed. Opt. (1)

C. Zhang, K. Maslov, J. Yao, L. V. Wang, “In vivo photoacoustic microscopy with 7.6-µm axial resolution using a commercial 125-MHz ultrasonic transducer,” J. Biomed. Opt. 17(11), 116016 (2012).
[CrossRef] [PubMed]

J. Cell. Mol. Med. (1)

P. Nowak-Sliwinska, A. Weiss, J. R. van Beijnum, T. J. Wong, J.-P. Ballini, B. Lovisa, H. van den Bergh, A. W. Griffioen, “Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion,” J. Cell. Mol. Med. 16(7), 1553–1562 (2012).
[CrossRef] [PubMed]

J. Vis. Exp. (1)

H. C. Yalcin, A. Shekhar, A. A. Rane, J. T. Butcher, “An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications,” J. Vis. Exp. 44(44), 2154 (2010).
[PubMed]

Nat. Biotechnol. (1)

H. F. Zhang, K. Maslov, G. Stoica, L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

Nat. Photonics (1)

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[CrossRef] [PubMed]

Nat. Protoc. (1)

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

Opt. Express (3)

Opt. Lett. (4)

Pharmacol. Rev. (1)

A. W. Griffioen, G. Molema, “Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation,” Pharmacol. Rev. 52(2), 237–268 (2000).
[PubMed]

Photoacoustics (1)

S.-L. Chen, Z. Xie, L. J. Guo, X. Wang, “A fiber-optic system for dual-modality photoacoustic microscopy and confocal fluorescence microscopy using miniature components,” Photoacoustics 1(2), 30–35 (2013).
[CrossRef]

Ultrasound Obstet. Gynecol. (1)

H. Pairleitner, H. Steiner, G. Hasenoehrl, A. Staudach, “Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization,” Ultrasound Obstet. Gynecol. 14(2), 139–143 (1999).
[CrossRef] [PubMed]

Other (1)

V. J. Srinivasan, A. C. Chan, and E. Y. Lam, “Doppler OCT and OCT angiography for in vivo imaging of vascular physiology,” Chapter 2 in Selected Topics in Optical Coherence Tomography, book edited by Gangjun Liu (2012).

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Figures (6)

Fig. 1
Fig. 1

Chick embryos are treated by angiogenesis inhibitor, Sunitinib, with different concentrations. From left to right: the 0.9% NaCl as a control solution, and Sunitinib at 300, 100, and 30 µM.

Fig. 2
Fig. 2

3D PAM of canine bladder, demonstrating the excellent capability of PAM in mapping the spatially distributed microvasculatures in biological samples. (a) The MAP images on the XY plane. (b) and (c) 2D cuts of 3D PAM image along the lines indicated in (a), where the left and right columns are for the images before (Grayscale) and after processing (Black/white). (d) The shortest A-line photoacoustic signal and its Hilbert transform. (e) The depth-encoded MAP image. Images (a)-(c) and (e) share the same scale bar shown in the bottom.

Fig. 3
Fig. 3

Co-registered PAM and OM images taken from a chick embryo CAM. (a) The images taken on EDD 5. (b) The images taken on EDD 6 which was one day after the embryo was treated with 100-μM Sunitinib. The vasculature patterns in PAM are in good agreement with the counterpart OM image.

Fig. 4
Fig. 4

Representative PAM images of CAM on EDD 6 when the chick embryos were treated with 10 µl of Sunitinib at different concentrations for a period of 24 hours. The SNRs of PAM images from left to right are 24, 23, 23, and 25 dB, respectively.

Fig. 5
Fig. 5

Conversion of PAM images from grayscale to black/white by using 36 sub-images and C = 0.2. (a) The example result from specimens with high vessel density (treated with Sunitinib at 30 µM). (b) The example results from specimens with low vessel density (treated with Sunitinib at 300 µM). The SNRs of PAM images before image processing are 24 dB and 26 dB in (a) and (b), respectively.

Fig. 6
Fig. 6

Statistical results of vessel density in chick embryo CAM vs. applied drug concentration quantified by PAM (solid line) and OM (dashed line), respectively. The two curves are shifted a little along the x-axis to avoid the overlap of the error bars. The inset shows the normalized curves for better comparison.

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