Abstract

Longitudinal monitoring techniques for preclinical models of vascular remodeling are critical to the development of new therapies for pathological conditions such as ischemia and cancer. In models of skeletal muscle ischemia in particular, there is a lack of quantitative, non-invasive and long term assessment of vessel morphology. Here, we have applied speckle variance optical coherence tomography (OCT) methods to quantitatively assess vascular remodeling and growth in a mouse model of peripheral arterial disease. This approach was validated on two different mouse strains known to have disparate rates and abilities of recovering following induction of hind limb ischemia. These results establish the potential for speckle variance OCT as a tool for quantitative, preclinical screening of pro- and anti-angiogenic therapies.

© 2014 Optical Society of America

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2014 (3)

L. V. Wang and L. Gao, “Photoacoustic microscopy and computed tomography: from bench to bedside,” Annu. Rev. Biomed. Eng. 16(1), 155–185 (2014).
[Crossref] [PubMed]

K. M. Poole, C. A. Patil, C. E. Nelson, D. R. McCormack, M. C. Madonna, C. L. Duvall, and M. C. Skala, “Longitudinal study of arteriogenesis with swept source optical coherence tomography and hyperspectral imaging,” Proc. SPIE 8934, 89341Z (2014).
[Crossref]

R. Reif, U. Baran, and R. K. Wang, “Motion artifact and background noise suppression on optical microangiography frames using a naïve Bayes mask,” Appl. Opt. 53(19), 4164–4171 (2014).
[Crossref] [PubMed]

2013 (6)

G. Liu and R. Wang, “Stripe motion artifact suppression in phase-resolved OCT blood flow images of the human eye based on the frequency rejection filter,” Chin. Opt. Lett. 11(3), 031701 (2013).
[Crossref]

H. C. Hendargo, R. Estrada, S. J. Chiu, C. Tomasi, S. Farsiu, and J. A. Izatt, “Automated non-rigid registration and mosaicing for robust imaging of distinct retinal capillary beds using speckle variance optical coherence tomography,” Biomed. Opt. Express 4(6), 803–821 (2013).
[Crossref] [PubMed]

S. Yousefi, J. Qin, Z. Zhi, and R. K. Wang, “Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters,” J. Biomed. Opt. 18(8), 086004 (2013).
[Crossref] [PubMed]

B. Davoudi, M. Morrison, K. Bizheva, V. X. Yang, R. Dinniwell, W. Levin, and I. A. Vitkin, “Optical coherence tomography platform for microvascular imaging and quantification: initial experience in late oral radiation toxicity patients,” J. Biomed. Opt. 18(7), 076008 (2013).
[Crossref] [PubMed]

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
[Crossref] [PubMed]

K. M. Poole, J. M. Tucker-Schwartz, W. W. Sit, A. J. Walsh, C. L. Duvall, and M. C. Skala, “Quantitative optical imaging of vascular response in vivo in a model of peripheral arterial disease,” Am. J. Physiol. Heart Circ. Physiol. 305(8), H1168–H1180 (2013).
[Crossref] [PubMed]

2012 (9)

A. Rege, N. V. Thakor, K. Rhie, and A. P. Pathak, “In vivo laser speckle imaging reveals microvascular remodeling and hemodynamic changes during wound healing angiogenesis,” Angiogenesis 15(1), 87–98 (2012).
[Crossref] [PubMed]

M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Longitudinal Imaging of Heart Development With Optical Coherence Tomography,” IEEE J Sel. Top. Quantum Electron. 18(3), 1166–1175 (2012).
[Crossref]

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
[Crossref] [PubMed]

R. Reif, J. Qin, L. An, Z. Zhi, S. Dziennis, and R. Wang, “Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system,” Int. J. Biomed. Imaging 2012, 509783 (2012).
[Crossref] [PubMed]

N. Landázuri, G. Joseph, R. E. Guldberg, and W. R. Taylor, “Growth and regression of vasculature in healthy and diabetic mice after hindlimb ischemia,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 303(1), R48–R56 (2012).
[Crossref] [PubMed]

J. Qin, R. Reif, Z. Zhi, S. Dziennis, and R. Wang, “Hemodynamic and morphological vasculature response to a burn monitored using a combined dual-wavelength laser speckle and optical microangiography imaging system,” Biomed. Opt. Express 3(3), 455–466 (2012).
[Crossref] [PubMed]

M. F. Kraus, B. Potsaid, M. A. Mayer, R. Bock, B. Baumann, J. J. Liu, J. Hornegger, and J. G. Fujimoto, “Motion correction in optical coherence tomography volumes on a per A-scan basis using orthogonal scan patterns,” Biomed. Opt. Express 3(6), 1182–1199 (2012).
[Crossref] [PubMed]

L. Conroy, R. S. DaCosta, and I. A. Vitkin, “Quantifying tissue microvasculature with speckle variance optical coherence tomography,” Opt. Lett. 37(15), 3180–3182 (2012).
[Crossref] [PubMed]

S. Zotter, M. Pircher, T. Torzicky, B. Baumann, H. Yoshida, F. Hirose, P. Roberts, M. Ritter, C. Schütze, E. Götzinger, W. Trasischker, C. Vass, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Large-field high-speed polarization sensitive spectral domain OCT and its applications in ophthalmology,” Biomed. Opt. Express 3(11), 2720–2732 (2012).
[Crossref] [PubMed]

2011 (9)

Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express 2(3), 579–591 (2011).
[Crossref] [PubMed]

T. Schmoll, A. S. Singh, C. Blatter, S. Schriefl, C. Ahlers, U. Schmidt-Erfurth, and R. A. Leitgeb, “Imaging of the parafoveal capillary network and its integrity analysis using fractal dimension,” Biomed. Opt. Express 2(5), 1159–1168 (2011).
[Crossref] [PubMed]

J. Enfield, E. Jonathan, and M. Leahy, “In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT),” Biomed. Opt. Express 2(5), 1184–1193 (2011).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
[Crossref] [PubMed]

M. E. Seaman, S. M. Peirce, and K. Kelly, “Rapid analysis of vessel elements (RAVE): a tool for studying physiologic, pathologic and tumor angiogenesis,” PLoS ONE 6(6), e20807 (2011).
[Crossref] [PubMed]

S. Yousefi, Z. Zhi, and R. K. Wang, “Eigendecomposition-based clutter filtering technique for optical micro-angiography,” IEEE Trans. Biomed. Eng. 58(8), 2316–2323 (2011).
[Crossref] [PubMed]

S. M. Weis and D. A. Cheresh, “Tumor angiogenesis: molecular pathways and therapeutic targets,” Nat. Med. 17(11), 1359–1370 (2011).
[Crossref] [PubMed]

Y. Jia, J. Qin, Z. Zhi, and R. K. Wang, “Ultrahigh sensitive optical microangiography reveals depth-resolved microcirculation and its longitudinal response to prolonged ischemic event within skeletal muscles in mice,” J. Biomed. Opt. 16(8), 086004 (2011).
[Crossref] [PubMed]

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
[Crossref] [PubMed]

2010 (5)

S. Rey and G. L. Semenza, “Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling,” Cardiovasc. Res. 86(2), 236–242 (2010).
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D. Chalothorn and J. E. Faber, “Strain-dependent variation in collateral circulatory function in mouse hindlimb,” Physiol. Genomics 42(3), 469–479 (2010).
[Crossref] [PubMed]

M. C. Skala, A. Fontanella, L. Lan, J. A. Izatt, and M. W. Dewhirst, “Longitudinal optical imaging of tumor metabolism and hemodynamics,” J. Biomed. Opt. 15(1), 011112 (2010).
[Crossref] [PubMed]

V. J. Srinivasan, J. Y. Jiang, M. A. Yaseen, H. Radhakrishnan, W. Wu, S. Barry, A. E. Cable, and D. A. Boas, “Rapid volumetric angiography of cortical microvasculature with optical coherence tomography,” Opt. Lett. 35(1), 43–45 (2010).
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A. Mariampillai, M. K. Leung, M. Jarvi, B. A. Standish, K. Lee, B. C. Wilson, A. Vitkin, and V. X. Yang, “Optimized speckle variance OCT imaging of microvasculature,” Opt. Lett. 35(8), 1257–1259 (2010).
[Crossref] [PubMed]

2009 (7)

M. C. Skala, A. Fontanella, H. Hendargo, M. W. Dewhirst, and J. A. Izatt, “Combined hyperspectral and spectral domain optical coherence tomography microscope for noninvasive hemodynamic imaging,” Opt. Lett. 34(3), 289–291 (2009).
[Crossref] [PubMed]

T. Schmoll, C. Kolbitsch, and R. A. Leitgeb, “Ultra-high-speed volumetric tomography of human retinal blood flow,” Opt. Express 17(5), 4166–4176 (2009).
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K. Lee, D. Z. Qian, S. Rey, H. Wei, J. O. Liu, and G. L. Semenza, “Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells,” Proc. Natl. Acad. Sci. U.S.A. 106(7), 2353–2358 (2009).
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R. Gupta, J. Tongers, and D. W. Losordo, “Human studies of angiogenic gene therapy,” Circ. Res. 105(8), 724–736 (2009).
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I. Kumar, C. A. Staton, S. S. Cross, M. W. Reed, and N. J. Brown, “Angiogenesis, vascular endothelial growth factor and its receptors in human surgical wounds,” Br. J. Surg. 96(12), 1484–1491 (2009).
[Crossref] [PubMed]

A. Limbourg, T. Korff, L. C. Napp, W. Schaper, H. Drexler, and F. P. Limbourg, “Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia,” Nat. Protoc. 4(12), 1737–1748 (2009).
[Crossref] [PubMed]

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
[Crossref] [PubMed]

2008 (3)

C. Jacoby, Y. C. Böring, A. Beck, A. Zernecke, V. Aurich, C. Weber, J. Schrader, and U. Flögel, “Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: a 9.4T study,” J. Magn. Reson. Imaging 28(3), 637–645 (2008).
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W. Drexler and J. G. Fujimoto, “State-of-the-art retinal optical coherence tomography,” Prog. Retin. Eye Res. 27(1), 45–88 (2008).
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A. Mariampillai, B. A. Standish, E. H. Moriyama, M. Khurana, N. R. Munce, M. K. Leung, J. Jiang, A. Cable, B. C. Wilson, I. A. Vitkin, and V. X. Yang, “Speckle variance detection of microvasculature using swept-source optical coherence tomography,” Opt. Lett. 33(13), 1530–1532 (2008).
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2007 (2)

B. A. Standish, V. X. D. Yang, N. R. Munce, L. M. Wong Kee Song, G. Gardiner, A. Lin, Y. I. Mao, A. Vitkin, N. E. Marcon, and B. C. Wilson, “Doppler optical coherence tomography monitoring of microvascular tissue response during photodynamic therapy in an animal model of Barrett’s esophagus,” Gastrointest. Endosc. 66(2), 326–333 (2007).
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C. L. Duvall, D. Weiss, S. T. Robinson, F. M. Alameddine, R. E. Guldberg, and W. R. Taylor, “The role of osteopontin in recovery from hind limb ischemia,” Arterioscler. Thromb. Vasc. Biol. 28(2), 290–295 (2007).
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2006 (2)

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
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S. Zbinden, L. C. Clavijo, B. Kantor, H. Morsli, G. A. Cortes, J. A. Andrews, G. J. Jang, M. S. Burnett, and S. E. Epstein, “Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials,” Am. J. Physiol. Heart Circ. Physiol. 292(4), H1891–H1897 (2006).
[Crossref] [PubMed]

2005 (3)

U. Schmidt-Erfurth, R. A. Leitgeb, S. Michels, B. Povazay, S. Sacu, B. Hermann, C. Ahlers, H. Sattmann, C. Scholda, A. F. Fercher, and W. Drexler, “Three-dimensional ultrahigh-resolution optical coherence tomography of macular diseases,” Invest. Ophthalmol. Vis. Sci. 46(9), 3393–3402 (2005).
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A. Helisch, S. Wagner, N. Khan, M. Drinane, S. Wolfram, M. Heil, T. Ziegelhoeffer, U. Brandt, J. D. Pearlman, H. M. Swartz, and W. Schaper, “Impact of mouse strain differences in innate hindlimb collateral vasculature,” Arterioscler. Thromb. Vasc. Biol. 26(3), 520–526 (2005).
[Crossref] [PubMed]

A. Unterhuber, B. Povazay, B. Hermann, H. Sattmann, A. Chavez-Pirson, and W. Drexler, “In vivo retinal optical coherence tomography at 1040 nm - enhanced penetration into the choroid,” Opt. Express 13(9), 3252–3258 (2005).
[Crossref] [PubMed]

2004 (1)

C. L. Duvall, W. R. Taylor, D. Weiss, and R. E. Guldberg, “Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury,” Am. J. Physiol. Heart Circ. Physiol. 287(1), H302–H310 (2004).
[Crossref] [PubMed]

2003 (3)

R. Cao, E. Bråkenhielm, R. Pawliuk, D. Wariaro, M. J. Post, E. Wahlberg, P. Leboulch, and Y. Cao, “Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2,” Nat. Med. 9(5), 604–613 (2003).
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D. E. Goertz, J. L. Yu, R. S. Kerbel, P. N. Burns, and F. S. Foster, “High-frequency 3-D color-flow imaging of the microcirculation,” Ultrasound Med. Biol. 29(1), 39–51 (2003).
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J. G. Fujimoto, “Optical coherence tomography for ultrahigh resolution in vivo imaging,” Nat. Biotechnol. 21(11), 1361–1367 (2003).
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2002 (1)

D. Scholz, T. Ziegelhoeffer, A. Helisch, S. Wagner, C. Friedrich, T. Podzuweit, and W. Schaper, “Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice,” J. Mol. Cell. Cardiol. 34(7), 775–787 (2002).
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2001 (2)

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
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A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
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2000 (3)

1999 (1)

M. Prewett, J. Huber, Y. Li, A. Santiago, W. O’Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, P. Bohlen, and D. J. Hicklin, “Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors,” Cancer Res. 59(20), 5209–5218 (1999).
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1998 (2)

A. F. Frangi, W. J. Niessen, K. L. Vincken, and M. A. Viergever, “Multiscale vessel enhancement filtering,” Lect. Notes Comput. Sci. 1496, 130–137 (1998).
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T. Couffinhal, M. Silver, L. P. Zheng, M. Kearney, B. Witzenbichler, and J. M. Isner, “Mouse model of angiogenesis,” Am. J. Pathol. 152(6), 1667–1679 (1998).
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1997 (2)

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G. H. Gibbons and V. J. Dzau, “The emerging concept of vascular remodeling,” N. Engl. J. Med. 330(20), 1431–1438 (1994).
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Ahlers, C.

T. Schmoll, A. S. Singh, C. Blatter, S. Schriefl, C. Ahlers, U. Schmidt-Erfurth, and R. A. Leitgeb, “Imaging of the parafoveal capillary network and its integrity analysis using fractal dimension,” Biomed. Opt. Express 2(5), 1159–1168 (2011).
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U. Schmidt-Erfurth, R. A. Leitgeb, S. Michels, B. Povazay, S. Sacu, B. Hermann, C. Ahlers, H. Sattmann, C. Scholda, A. F. Fercher, and W. Drexler, “Three-dimensional ultrahigh-resolution optical coherence tomography of macular diseases,” Invest. Ophthalmol. Vis. Sci. 46(9), 3393–3402 (2005).
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Alameddine, F. M.

C. L. Duvall, D. Weiss, S. T. Robinson, F. M. Alameddine, R. E. Guldberg, and W. R. Taylor, “The role of osteopontin in recovery from hind limb ischemia,” Arterioscler. Thromb. Vasc. Biol. 28(2), 290–295 (2007).
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An, L.

R. Reif, J. Qin, L. An, Z. Zhi, S. Dziennis, and R. Wang, “Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system,” Int. J. Biomed. Imaging 2012, 509783 (2012).
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Andrews, J. A.

S. Zbinden, L. C. Clavijo, B. Kantor, H. Morsli, G. A. Cortes, J. A. Andrews, G. J. Jang, M. S. Burnett, and S. E. Epstein, “Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials,” Am. J. Physiol. Heart Circ. Physiol. 292(4), H1891–H1897 (2006).
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Aurich, V.

C. Jacoby, Y. C. Böring, A. Beck, A. Zernecke, V. Aurich, C. Weber, J. Schrader, and U. Flögel, “Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: a 9.4T study,” J. Magn. Reson. Imaging 28(3), 637–645 (2008).
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Barry, S.

Bartlett, L. A.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
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Barton, J. K.

Baumann, B.

Beck, A.

C. Jacoby, Y. C. Böring, A. Beck, A. Zernecke, V. Aurich, C. Weber, J. Schrader, and U. Flögel, “Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: a 9.4T study,” J. Magn. Reson. Imaging 28(3), 637–645 (2008).
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Bizheva, K.

B. Davoudi, M. Morrison, K. Bizheva, V. X. Yang, R. Dinniwell, W. Levin, and I. A. Vitkin, “Optical coherence tomography platform for microvascular imaging and quantification: initial experience in late oral radiation toxicity patients,” J. Biomed. Opt. 18(7), 076008 (2013).
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Blatter, C.

Boas, D. A.

Bock, R.

Bohlen, P.

M. Prewett, J. Huber, Y. Li, A. Santiago, W. O’Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, P. Bohlen, and D. J. Hicklin, “Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors,” Cancer Res. 59(20), 5209–5218 (1999).
[PubMed]

Bolay, H.

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
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Böring, Y. C.

C. Jacoby, Y. C. Böring, A. Beck, A. Zernecke, V. Aurich, C. Weber, J. Schrader, and U. Flögel, “Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: a 9.4T study,” J. Magn. Reson. Imaging 28(3), 637–645 (2008).
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Bouma, B. E.

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
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B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
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Bråkenhielm, E.

R. Cao, E. Bråkenhielm, R. Pawliuk, D. Wariaro, M. J. Post, E. Wahlberg, P. Leboulch, and Y. Cao, “Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2,” Nat. Med. 9(5), 604–613 (2003).
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Brandt, U.

A. Helisch, S. Wagner, N. Khan, M. Drinane, S. Wolfram, M. Heil, T. Ziegelhoeffer, U. Brandt, J. D. Pearlman, H. M. Swartz, and W. Schaper, “Impact of mouse strain differences in innate hindlimb collateral vasculature,” Arterioscler. Thromb. Vasc. Biol. 26(3), 520–526 (2005).
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Brown, E. B.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
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Brown, N. J.

I. Kumar, C. A. Staton, S. S. Cross, M. W. Reed, and N. J. Brown, “Angiogenesis, vascular endothelial growth factor and its receptors in human surgical wounds,” Br. J. Surg. 96(12), 1484–1491 (2009).
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Burnett, M. S.

S. Zbinden, L. C. Clavijo, B. Kantor, H. Morsli, G. A. Cortes, J. A. Andrews, G. J. Jang, M. S. Burnett, and S. E. Epstein, “Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials,” Am. J. Physiol. Heart Circ. Physiol. 292(4), H1891–H1897 (2006).
[Crossref] [PubMed]

Burns, P. N.

D. E. Goertz, J. L. Yu, R. S. Kerbel, P. N. Burns, and F. S. Foster, “High-frequency 3-D color-flow imaging of the microcirculation,” Ultrasound Med. Biol. 29(1), 39–51 (2003).
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Cable, A.

Cable, A. E.

Cadotte, D. W.

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
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Campbell, R. B.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
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Cao, R.

R. Cao, E. Bråkenhielm, R. Pawliuk, D. Wariaro, M. J. Post, E. Wahlberg, P. Leboulch, and Y. Cao, “Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2,” Nat. Med. 9(5), 604–613 (2003).
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Cao, Y.

R. Cao, E. Bråkenhielm, R. Pawliuk, D. Wariaro, M. J. Post, E. Wahlberg, P. Leboulch, and Y. Cao, “Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2,” Nat. Med. 9(5), 604–613 (2003).
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Carmeliet, P.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
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P. Carmeliet and R. K. Jain, “Angiogenesis in cancer and other diseases,” Nature 407(6801), 249–257 (2000).
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Cepurna, W.

Chalothorn, D.

D. Chalothorn and J. E. Faber, “Strain-dependent variation in collateral circulatory function in mouse hindlimb,” Physiol. Genomics 42(3), 469–479 (2010).
[Crossref] [PubMed]

Chavez-Pirson, A.

Chen, Z.

Cheresh, D. A.

S. M. Weis and D. A. Cheresh, “Tumor angiogenesis: molecular pathways and therapeutic targets,” Nat. Med. 17(11), 1359–1370 (2011).
[Crossref] [PubMed]

Chiu, S. J.

Clavijo, L. C.

S. Zbinden, L. C. Clavijo, B. Kantor, H. Morsli, G. A. Cortes, J. A. Andrews, G. J. Jang, M. S. Burnett, and S. E. Epstein, “Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials,” Am. J. Physiol. Heart Circ. Physiol. 292(4), H1891–H1897 (2006).
[Crossref] [PubMed]

Conroy, L.

Cortes, G. A.

S. Zbinden, L. C. Clavijo, B. Kantor, H. Morsli, G. A. Cortes, J. A. Andrews, G. J. Jang, M. S. Burnett, and S. E. Epstein, “Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials,” Am. J. Physiol. Heart Circ. Physiol. 292(4), H1891–H1897 (2006).
[Crossref] [PubMed]

Couffinhal, T.

T. Couffinhal, M. Silver, L. P. Zheng, M. Kearney, B. Witzenbichler, and J. M. Isner, “Mouse model of angiogenesis,” Am. J. Pathol. 152(6), 1667–1679 (1998).
[PubMed]

Cross, S. S.

I. Kumar, C. A. Staton, S. S. Cross, M. W. Reed, and N. J. Brown, “Angiogenesis, vascular endothelial growth factor and its receptors in human surgical wounds,” Br. J. Surg. 96(12), 1484–1491 (2009).
[Crossref] [PubMed]

DaCosta, R. S.

Davoudi, B.

B. Davoudi, M. Morrison, K. Bizheva, V. X. Yang, R. Dinniwell, W. Levin, and I. A. Vitkin, “Optical coherence tomography platform for microvascular imaging and quantification: initial experience in late oral radiation toxicity patients,” J. Biomed. Opt. 18(7), 076008 (2013).
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de Boer, J. F.

Dewhirst, M. W.

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
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M. C. Skala, A. Fontanella, L. Lan, J. A. Izatt, and M. W. Dewhirst, “Longitudinal optical imaging of tumor metabolism and hemodynamics,” J. Biomed. Opt. 15(1), 011112 (2010).
[Crossref] [PubMed]

M. C. Skala, A. Fontanella, H. Hendargo, M. W. Dewhirst, and J. A. Izatt, “Combined hyperspectral and spectral domain optical coherence tomography microscope for noninvasive hemodynamic imaging,” Opt. Lett. 34(3), 289–291 (2009).
[Crossref] [PubMed]

Dinniwell, R.

B. Davoudi, M. Morrison, K. Bizheva, V. X. Yang, R. Dinniwell, W. Levin, and I. A. Vitkin, “Optical coherence tomography platform for microvascular imaging and quantification: initial experience in late oral radiation toxicity patients,” J. Biomed. Opt. 18(7), 076008 (2013).
[Crossref] [PubMed]

Drexler, H.

A. Limbourg, T. Korff, L. C. Napp, W. Schaper, H. Drexler, and F. P. Limbourg, “Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia,” Nat. Protoc. 4(12), 1737–1748 (2009).
[Crossref] [PubMed]

Drexler, W.

W. Drexler and J. G. Fujimoto, “State-of-the-art retinal optical coherence tomography,” Prog. Retin. Eye Res. 27(1), 45–88 (2008).
[Crossref] [PubMed]

U. Schmidt-Erfurth, R. A. Leitgeb, S. Michels, B. Povazay, S. Sacu, B. Hermann, C. Ahlers, H. Sattmann, C. Scholda, A. F. Fercher, and W. Drexler, “Three-dimensional ultrahigh-resolution optical coherence tomography of macular diseases,” Invest. Ophthalmol. Vis. Sci. 46(9), 3393–3402 (2005).
[Crossref] [PubMed]

A. Unterhuber, B. Povazay, B. Hermann, H. Sattmann, A. Chavez-Pirson, and W. Drexler, “In vivo retinal optical coherence tomography at 1040 nm - enhanced penetration into the choroid,” Opt. Express 13(9), 3252–3258 (2005).
[Crossref] [PubMed]

Drinane, M.

A. Helisch, S. Wagner, N. Khan, M. Drinane, S. Wolfram, M. Heil, T. Ziegelhoeffer, U. Brandt, J. D. Pearlman, H. M. Swartz, and W. Schaper, “Impact of mouse strain differences in innate hindlimb collateral vasculature,” Arterioscler. Thromb. Vasc. Biol. 26(3), 520–526 (2005).
[Crossref] [PubMed]

Dunn, A. K.

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
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K. M. Poole, C. A. Patil, C. E. Nelson, D. R. McCormack, M. C. Madonna, C. L. Duvall, and M. C. Skala, “Longitudinal study of arteriogenesis with swept source optical coherence tomography and hyperspectral imaging,” Proc. SPIE 8934, 89341Z (2014).
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K. M. Poole, J. M. Tucker-Schwartz, W. W. Sit, A. J. Walsh, C. L. Duvall, and M. C. Skala, “Quantitative optical imaging of vascular response in vivo in a model of peripheral arterial disease,” Am. J. Physiol. Heart Circ. Physiol. 305(8), H1168–H1180 (2013).
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C. L. Duvall, D. Weiss, S. T. Robinson, F. M. Alameddine, R. E. Guldberg, and W. R. Taylor, “The role of osteopontin in recovery from hind limb ischemia,” Arterioscler. Thromb. Vasc. Biol. 28(2), 290–295 (2007).
[Crossref] [PubMed]

C. L. Duvall, W. R. Taylor, D. Weiss, and R. E. Guldberg, “Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury,” Am. J. Physiol. Heart Circ. Physiol. 287(1), H302–H310 (2004).
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[Crossref] [PubMed]

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L. V. Wang and L. Gao, “Photoacoustic microscopy and computed tomography: from bench to bedside,” Annu. Rev. Biomed. Eng. 16(1), 155–185 (2014).
[Crossref] [PubMed]

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

Wang, R. K.

R. Reif, U. Baran, and R. K. Wang, “Motion artifact and background noise suppression on optical microangiography frames using a naïve Bayes mask,” Appl. Opt. 53(19), 4164–4171 (2014).
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S. Yousefi, J. Qin, Z. Zhi, and R. K. Wang, “Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters,” J. Biomed. Opt. 18(8), 086004 (2013).
[Crossref] [PubMed]

S. Yousefi, Z. Zhi, and R. K. Wang, “Eigendecomposition-based clutter filtering technique for optical micro-angiography,” IEEE Trans. Biomed. Eng. 58(8), 2316–2323 (2011).
[Crossref] [PubMed]

Y. Jia, J. Qin, Z. Zhi, and R. K. Wang, “Ultrahigh sensitive optical microangiography reveals depth-resolved microcirculation and its longitudinal response to prolonged ischemic event within skeletal muscles in mice,” J. Biomed. Opt. 16(8), 086004 (2011).
[Crossref] [PubMed]

Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express 2(3), 579–591 (2011).
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Wariaro, D.

R. Cao, E. Bråkenhielm, R. Pawliuk, D. Wariaro, M. J. Post, E. Wahlberg, P. Leboulch, and Y. Cao, “Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2,” Nat. Med. 9(5), 604–613 (2003).
[Crossref] [PubMed]

Watanabe, M.

M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Longitudinal Imaging of Heart Development With Optical Coherence Tomography,” IEEE J Sel. Top. Quantum Electron. 18(3), 1166–1175 (2012).
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C. Jacoby, Y. C. Böring, A. Beck, A. Zernecke, V. Aurich, C. Weber, J. Schrader, and U. Flögel, “Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: a 9.4T study,” J. Magn. Reson. Imaging 28(3), 637–645 (2008).
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S. M. Weis and D. A. Cheresh, “Tumor angiogenesis: molecular pathways and therapeutic targets,” Nat. Med. 17(11), 1359–1370 (2011).
[Crossref] [PubMed]

Weiss, D.

C. L. Duvall, D. Weiss, S. T. Robinson, F. M. Alameddine, R. E. Guldberg, and W. R. Taylor, “The role of osteopontin in recovery from hind limb ischemia,” Arterioscler. Thromb. Vasc. Biol. 28(2), 290–295 (2007).
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C. L. Duvall, W. R. Taylor, D. Weiss, and R. E. Guldberg, “Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury,” Am. J. Physiol. Heart Circ. Physiol. 287(1), H302–H310 (2004).
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M. Prewett, J. Huber, Y. Li, A. Santiago, W. O’Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, P. Bohlen, and D. J. Hicklin, “Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors,” Cancer Res. 59(20), 5209–5218 (1999).
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B. A. Standish, V. X. D. Yang, N. R. Munce, L. M. Wong Kee Song, G. Gardiner, A. Lin, Y. I. Mao, A. Vitkin, N. E. Marcon, and B. C. Wilson, “Doppler optical coherence tomography monitoring of microvascular tissue response during photodynamic therapy in an animal model of Barrett’s esophagus,” Gastrointest. Endosc. 66(2), 326–333 (2007).
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Xiang, S.

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E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
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Yang, V. X.

B. Davoudi, M. Morrison, K. Bizheva, V. X. Yang, R. Dinniwell, W. Levin, and I. A. Vitkin, “Optical coherence tomography platform for microvascular imaging and quantification: initial experience in late oral radiation toxicity patients,” J. Biomed. Opt. 18(7), 076008 (2013).
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M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
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A. Mariampillai, M. K. Leung, M. Jarvi, B. A. Standish, K. Lee, B. C. Wilson, A. Vitkin, and V. X. Yang, “Optimized speckle variance OCT imaging of microvasculature,” Opt. Lett. 35(8), 1257–1259 (2010).
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S. Yousefi, J. Qin, Z. Zhi, and R. K. Wang, “Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters,” J. Biomed. Opt. 18(8), 086004 (2013).
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S. Yousefi, Z. Zhi, and R. K. Wang, “Eigendecomposition-based clutter filtering technique for optical micro-angiography,” IEEE Trans. Biomed. Eng. 58(8), 2316–2323 (2011).
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H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
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T. Couffinhal, M. Silver, L. P. Zheng, M. Kearney, B. Witzenbichler, and J. M. Isner, “Mouse model of angiogenesis,” Am. J. Pathol. 152(6), 1667–1679 (1998).
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S. Yousefi, J. Qin, Z. Zhi, and R. K. Wang, “Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters,” J. Biomed. Opt. 18(8), 086004 (2013).
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R. Reif, J. Qin, L. An, Z. Zhi, S. Dziennis, and R. Wang, “Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system,” Int. J. Biomed. Imaging 2012, 509783 (2012).
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J. Qin, R. Reif, Z. Zhi, S. Dziennis, and R. Wang, “Hemodynamic and morphological vasculature response to a burn monitored using a combined dual-wavelength laser speckle and optical microangiography imaging system,” Biomed. Opt. Express 3(3), 455–466 (2012).
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Y. Jia, J. Qin, Z. Zhi, and R. K. Wang, “Ultrahigh sensitive optical microangiography reveals depth-resolved microcirculation and its longitudinal response to prolonged ischemic event within skeletal muscles in mice,” J. Biomed. Opt. 16(8), 086004 (2011).
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Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express 2(3), 579–591 (2011).
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S. Yousefi, Z. Zhi, and R. K. Wang, “Eigendecomposition-based clutter filtering technique for optical micro-angiography,” IEEE Trans. Biomed. Eng. 58(8), 2316–2323 (2011).
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A. Helisch, S. Wagner, N. Khan, M. Drinane, S. Wolfram, M. Heil, T. Ziegelhoeffer, U. Brandt, J. D. Pearlman, H. M. Swartz, and W. Schaper, “Impact of mouse strain differences in innate hindlimb collateral vasculature,” Arterioscler. Thromb. Vasc. Biol. 26(3), 520–526 (2005).
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D. Scholz, T. Ziegelhoeffer, A. Helisch, S. Wagner, C. Friedrich, T. Podzuweit, and W. Schaper, “Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice,” J. Mol. Cell. Cardiol. 34(7), 775–787 (2002).
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Am. J. Pathol. (1)

T. Couffinhal, M. Silver, L. P. Zheng, M. Kearney, B. Witzenbichler, and J. M. Isner, “Mouse model of angiogenesis,” Am. J. Pathol. 152(6), 1667–1679 (1998).
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C. L. Duvall, W. R. Taylor, D. Weiss, and R. E. Guldberg, “Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury,” Am. J. Physiol. Heart Circ. Physiol. 287(1), H302–H310 (2004).
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K. M. Poole, J. M. Tucker-Schwartz, W. W. Sit, A. J. Walsh, C. L. Duvall, and M. C. Skala, “Quantitative optical imaging of vascular response in vivo in a model of peripheral arterial disease,” Am. J. Physiol. Heart Circ. Physiol. 305(8), H1168–H1180 (2013).
[Crossref] [PubMed]

S. Zbinden, L. C. Clavijo, B. Kantor, H. Morsli, G. A. Cortes, J. A. Andrews, G. J. Jang, M. S. Burnett, and S. E. Epstein, “Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials,” Am. J. Physiol. Heart Circ. Physiol. 292(4), H1891–H1897 (2006).
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Am. J. Physiol. Regul. Integr. Comp. Physiol. (1)

N. Landázuri, G. Joseph, R. E. Guldberg, and W. R. Taylor, “Growth and regression of vasculature in healthy and diabetic mice after hindlimb ischemia,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 303(1), R48–R56 (2012).
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Angiogenesis (1)

A. Rege, N. V. Thakor, K. Rhie, and A. P. Pathak, “In vivo laser speckle imaging reveals microvascular remodeling and hemodynamic changes during wound healing angiogenesis,” Angiogenesis 15(1), 87–98 (2012).
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Annu. Rev. Biomed. Eng. (1)

L. V. Wang and L. Gao, “Photoacoustic microscopy and computed tomography: from bench to bedside,” Annu. Rev. Biomed. Eng. 16(1), 155–185 (2014).
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Appl. Opt. (1)

Arterioscler. Thromb. Vasc. Biol. (2)

A. Helisch, S. Wagner, N. Khan, M. Drinane, S. Wolfram, M. Heil, T. Ziegelhoeffer, U. Brandt, J. D. Pearlman, H. M. Swartz, and W. Schaper, “Impact of mouse strain differences in innate hindlimb collateral vasculature,” Arterioscler. Thromb. Vasc. Biol. 26(3), 520–526 (2005).
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C. L. Duvall, D. Weiss, S. T. Robinson, F. M. Alameddine, R. E. Guldberg, and W. R. Taylor, “The role of osteopontin in recovery from hind limb ischemia,” Arterioscler. Thromb. Vasc. Biol. 28(2), 290–295 (2007).
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Biomed. Opt. Express (8)

J. Qin, R. Reif, Z. Zhi, S. Dziennis, and R. Wang, “Hemodynamic and morphological vasculature response to a burn monitored using a combined dual-wavelength laser speckle and optical microangiography imaging system,” Biomed. Opt. Express 3(3), 455–466 (2012).
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H. C. Hendargo, R. Estrada, S. J. Chiu, C. Tomasi, S. Farsiu, and J. A. Izatt, “Automated non-rigid registration and mosaicing for robust imaging of distinct retinal capillary beds using speckle variance optical coherence tomography,” Biomed. Opt. Express 4(6), 803–821 (2013).
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M. F. Kraus, B. Potsaid, M. A. Mayer, R. Bock, B. Baumann, J. J. Liu, J. Hornegger, and J. G. Fujimoto, “Motion correction in optical coherence tomography volumes on a per A-scan basis using orthogonal scan patterns,” Biomed. Opt. Express 3(6), 1182–1199 (2012).
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T. Schmoll, A. S. Singh, C. Blatter, S. Schriefl, C. Ahlers, U. Schmidt-Erfurth, and R. A. Leitgeb, “Imaging of the parafoveal capillary network and its integrity analysis using fractal dimension,” Biomed. Opt. Express 2(5), 1159–1168 (2011).
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Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express 2(3), 579–591 (2011).
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D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
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S. Zotter, M. Pircher, T. Torzicky, B. Baumann, H. Yoshida, F. Hirose, P. Roberts, M. Ritter, C. Schütze, E. Götzinger, W. Trasischker, C. Vass, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Large-field high-speed polarization sensitive spectral domain OCT and its applications in ophthalmology,” Biomed. Opt. Express 3(11), 2720–2732 (2012).
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J. Enfield, E. Jonathan, and M. Leahy, “In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT),” Biomed. Opt. Express 2(5), 1184–1193 (2011).
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Br. J. Surg. (1)

I. Kumar, C. A. Staton, S. S. Cross, M. W. Reed, and N. J. Brown, “Angiogenesis, vascular endothelial growth factor and its receptors in human surgical wounds,” Br. J. Surg. 96(12), 1484–1491 (2009).
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Cancer Res. (1)

M. Prewett, J. Huber, Y. Li, A. Santiago, W. O’Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, P. Bohlen, and D. J. Hicklin, “Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors,” Cancer Res. 59(20), 5209–5218 (1999).
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S. Rey and G. L. Semenza, “Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling,” Cardiovasc. Res. 86(2), 236–242 (2010).
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Cell (1)

D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell 100(1), 57–70 (2000).
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Chin. Opt. Lett. (1)

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Gastrointest. Endosc. (1)

B. A. Standish, V. X. D. Yang, N. R. Munce, L. M. Wong Kee Song, G. Gardiner, A. Lin, Y. I. Mao, A. Vitkin, N. E. Marcon, and B. C. Wilson, “Doppler optical coherence tomography monitoring of microvascular tissue response during photodynamic therapy in an animal model of Barrett’s esophagus,” Gastrointest. Endosc. 66(2), 326–333 (2007).
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IEEE J Sel. Top. Quantum Electron. (1)

M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Longitudinal Imaging of Heart Development With Optical Coherence Tomography,” IEEE J Sel. Top. Quantum Electron. 18(3), 1166–1175 (2012).
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IEEE Trans. Biomed. Eng. (1)

S. Yousefi, Z. Zhi, and R. K. Wang, “Eigendecomposition-based clutter filtering technique for optical micro-angiography,” IEEE Trans. Biomed. Eng. 58(8), 2316–2323 (2011).
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Int. J. Biomed. Imaging (1)

R. Reif, J. Qin, L. An, Z. Zhi, S. Dziennis, and R. Wang, “Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system,” Int. J. Biomed. Imaging 2012, 509783 (2012).
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Invest. Ophthalmol. Vis. Sci. (1)

U. Schmidt-Erfurth, R. A. Leitgeb, S. Michels, B. Povazay, S. Sacu, B. Hermann, C. Ahlers, H. Sattmann, C. Scholda, A. F. Fercher, and W. Drexler, “Three-dimensional ultrahigh-resolution optical coherence tomography of macular diseases,” Invest. Ophthalmol. Vis. Sci. 46(9), 3393–3402 (2005).
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J. Biomed. Opt. (5)

B. Davoudi, M. Morrison, K. Bizheva, V. X. Yang, R. Dinniwell, W. Levin, and I. A. Vitkin, “Optical coherence tomography platform for microvascular imaging and quantification: initial experience in late oral radiation toxicity patients,” J. Biomed. Opt. 18(7), 076008 (2013).
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M. C. Skala, A. Fontanella, L. Lan, J. A. Izatt, and M. W. Dewhirst, “Longitudinal optical imaging of tumor metabolism and hemodynamics,” J. Biomed. Opt. 15(1), 011112 (2010).
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Y. Jia, J. Qin, Z. Zhi, and R. K. Wang, “Ultrahigh sensitive optical microangiography reveals depth-resolved microcirculation and its longitudinal response to prolonged ischemic event within skeletal muscles in mice,” J. Biomed. Opt. 16(8), 086004 (2011).
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M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
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S. Yousefi, J. Qin, Z. Zhi, and R. K. Wang, “Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters,” J. Biomed. Opt. 18(8), 086004 (2013).
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J. Magn. Reson. Imaging (1)

C. Jacoby, Y. C. Böring, A. Beck, A. Zernecke, V. Aurich, C. Weber, J. Schrader, and U. Flögel, “Dynamic changes in murine vessel geometry assessed by high-resolution magnetic resonance angiography: a 9.4T study,” J. Magn. Reson. Imaging 28(3), 637–645 (2008).
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J. Mol. Cell. Cardiol. (1)

D. Scholz, T. Ziegelhoeffer, A. Helisch, S. Wagner, C. Friedrich, T. Podzuweit, and W. Schaper, “Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice,” J. Mol. Cell. Cardiol. 34(7), 775–787 (2002).
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H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
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J. G. Fujimoto, “Optical coherence tomography for ultrahigh resolution in vivo imaging,” Nat. Biotechnol. 21(11), 1361–1367 (2003).
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Nat. Med. (4)

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
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E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
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S. M. Weis and D. A. Cheresh, “Tumor angiogenesis: molecular pathways and therapeutic targets,” Nat. Med. 17(11), 1359–1370 (2011).
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R. Cao, E. Bråkenhielm, R. Pawliuk, D. Wariaro, M. J. Post, E. Wahlberg, P. Leboulch, and Y. Cao, “Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2,” Nat. Med. 9(5), 604–613 (2003).
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Nat. Protoc. (2)

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Figures (5)

Fig. 1
Fig. 1 The hind limb ischemia model is depicted in (A) with vessel ligation points and the imaging area of interest in the adductor muscle region. A schematic of the swept-source OCT system with a 1060 nm center wavelength, 100 kHz sweep-rate source (Axsun) is shown in (B). Lateral and axial resolution are 16 μm and 6.5 μm in air, respectively. FBG – fiber Bragg grating. BD – balanced detector. AI/AO – Analog input/analog output. VA – variable attenuator. DM – dispersion matching cube. M – mirror. SL – scan lens. GP – galvo pair.
Fig. 2
Fig. 2 Flow chart of image processing procedures for speckle variance images of the vasculature. Speckle variance [33] was computed over eight repeated B-scans collected at each spatial position in the volume, and the tissue was segmented using the corresponding structural image. The resulting speckle variance B-scans were then median filtered, de-shadowed [54], and projected in the depth dimension. B-scans with a high average speckle variance signal due to bulk motion artifacts were identified and replaced with the average of the nearest bulk motion-free B-scans, and a corrected average intensity projection was computed. The projected image was then Hessian filtered [5557] to derive a vessel mask from which quantitative morphology metrics were extracted.
Fig. 3
Fig. 3 Representative speckle variance OCT images of the adductor muscle from each mouse strain, including the contralateral control limb (far left) and the ischemic limb imaged non-invasively over a time-course. Images are shown for both Balb/c (top row) and FVB (bottom row) mice. The last imaging time point was day 19 for Balb/c mice and day 21 for FVB mice.
Fig. 4
Fig. 4 Vascular morphology metrics were quantified from speckle variance OCT projection images for Balb/c (n = 4) and FVB (n = 3) mice. FVB mice showed increased (A) vessel area density and (B) vessel length fraction at day 7 and subsequent time points post-surgery in the ischemic adductor region relative to Balb/c mice (*p<0.05 between strains). Balb/c mice also showed a decrease in both parameters between days 7 and 19 (p<0.05), while vessel area density and length fraction increased for FVB mice between days 3 and 7 and days 3 and 14, respectively (p<0.05). (C) Significant differences in the length of vasculature within a given range of vessel diameters were also detected (*p<0.05 for indicated range of diameters). The last imaging time point was day 19 for Balb/c mice and day 21 for FVB mice.
Fig. 5
Fig. 5 Representative structural OCT images from the adductor muscle region, including the contralateral control limb (left) and the ischemic limb imaged non-invasively over a time-course. A change in tissue structure beneath the skin is observed in the ischemic limb, presumably due to inflammation. Scale bar is 1 mm.

Tables (1)

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Table 1 Quantitative morphology metrics extracted from speckle variance OCT projection images

Metrics