Abstract

Murine hindlimb ischemia is a useful model for investigation of the mechanisms of peripheral arterial disease and for understanding the role of endothelial cells and generic factors affecting vascular regeneration or angiogenesis. To date, important research with these models has explored tissue reperfusion following ischemia with Laser Doppler methods, methods which provide information about superficial (~mm) vascular regeneration. In this work, we employ diffuse correlation spectroscopy (DCS) and diffuse optical spectroscopy (DOS) in mice after hindlimb ischemia. We hypothesize that vascular re-growth is not uniform in tissue, and therefore, since diffuse optical methods are capable of probing deep tissues, that the diffuse optics approach will provide a more complete picture of the angiogenesis process throughout the whole depth profile of the limb. Besides increased depth penetration, the combined measurements of DCS and DOS enable all-optical, noninvasive, longitudinal monitoring of tissue perfusion and oxygenation that reveals the interplay between these hemodynamic parameters during angiogenesis. Control mice were found to reestablish 90% of perfusion and oxygen consumption during this period, but oxygen saturation in the limb only partially recovered to about 30% of its initial value. The vascular recovery of mice with endothelial cell-specific deletion of HIF-2α was found to be significantly impaired relative to control mice, indicating that HIF-2α is important for endothelial cell functions in angiogenesis. Comparison of DOS/DCS measurements to parallel measurements in the murine models using Laser Doppler Flowmetry reveal differences in the reperfusion achieved by superficial versus deep tissue during neoangiogenesis; findings from histological analysis of blood vessel development were further correlated with these differences. In general, the combination of DCS and DOS enables experimenters to obtain useful information about oxygenation, metabolism, and perfusion throughout the limb. The results establish diffuse optics as a practical noninvasive method to evaluate the role of transcription factors, such as the endothelial cell-specific HIF-2α, in genetic ally modified mice.

© 2010 OSA

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2010 (3)

T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73(7), 076701 (2010).
[CrossRef]

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

2009 (4)

C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
[CrossRef] [PubMed]

N. Skuli, L. Liu, A. Runge, T. Wang, L. Yuan, S. Patel, L. Iruela-Arispe, M. C. Simon, and B. Keith, “Endothelial deletion of hypoxia-inducible factor-2  (HIF-2 ) alters vascular function and tumor angiogenesis,” Blood 114(2), 469–477 (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]

W. Schaper, “Collateral circulation: past and present,” Basic Res. Cardiol. 104(1), 5–21 (2009).
[CrossRef] [PubMed]

2008 (2)

2007 (6)

B. Zhou, M. C. Poon, W. T. Pu, and Z. C. Han, “Therapeutic neovascularization for peripheral arterial diseases: advances and perspectives,” Histol. Histopathol. 22(6), 677–686 (2007).
[PubMed]

M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
[CrossRef] [PubMed]

S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
[CrossRef] [PubMed]

H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
[CrossRef] [PubMed]

H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
[CrossRef] [PubMed]

G. Q. Yu, T. F. Floyd, T. Durduran, C. Zhou, J. J. Wang, J. A. Detre, and A. G. Yodh, “Validation of diffuse correlation spectroscopy for muscle blood flow with concurrent arterial spin labeled perfusion MRI,” Opt. Express 15(3), 1064–1075 (2007).
[CrossRef] [PubMed]

2006 (2)

M. M. Hickey and M. C. Simon, “Regulation of angiogenesis by hypoxia and hypoxia-inducible factors,” Curr. Top. Dev. Biol. 76, 217–257 (2006).
[CrossRef] [PubMed]

M. Heil, I. Eitenmüller, T. Schmitz-Rixen, and W. Schaper, “Arteriogenesis versus angiogenesis: similarities and differences,” J. Cell. Mol. Med. 10(1), 45–55 (2006).
[CrossRef] [PubMed]

2005 (3)

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]

P. Carmeliet, “Angiogenesis in life, disease and medicine,” Nature 438(7070), 932–936 (2005).
[CrossRef] [PubMed]

A. Matsumoto, S. Matsumoto, A. L. Sowers, J. W. Koscielniak, N. J. Trigg, P. Kuppusamy, J. B. Mitchell, S. Subramanian, M. C. Krishna, and K. I. Matsumoto, “Absolute oxygen tension (pO(2)) in murine fatty and muscle tissue as determined by EPR,” Magn. Reson. Med. 54(6), 1530–1535 (2005).
[CrossRef] [PubMed]

2004 (2)

H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
[CrossRef] [PubMed]

K. L. Covello and M. C. Simon, “HIFs, hypoxia, and vascular development,” Curr. Top. Dev. Biol. 62, 37–54 (2004).
[CrossRef] [PubMed]

2003 (2)

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[CrossRef] [PubMed]

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48(15), 2405–2418 (2003).
[CrossRef] [PubMed]

2002 (4)

D. A. Boas, J. P. Culver, J. J. Stott, and A. K. Dunn, “Three dimensional Monte Carlo code for photon migration through complex heterogeneous media including the adult human head,” Opt. Express 10(3), 159–170 (2002).
[PubMed]

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).
[CrossRef] [PubMed]

K. R. Forrester, C. Stewart, J. Tulip, C. Leonard, and R. C. Bray, “Comparison of laser speckle and laser Doppler perfusion imaging: measurement in human skin and rabbit articular tissue,” Med. Biol. Eng. Comput. 40(6), 687–697 (2002).
[CrossRef] [PubMed]

M. Solonenko, R. Cheung, T. M. Busch, A. Kachur, G. M. Griffin, T. Vulcan, T. C. Zhu, H. W. Wang, S. M. Hahn, and A. G. Yodh, “In vivo reflectance measurement of optical properties, blood oxygenation and motexafin lutetium uptake in canine large bowels, kidneys and prostates,” Phys. Med. Biol. 47(6), 857–873 (2002).
[PubMed]

2001 (3)

E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
[CrossRef] [PubMed]

I. E. Hoefer, N. van Royen, I. R. Buschmann, J. J. Piek, and W. Schaper, “Time course of arteriogenesis following femoral artery occlusion in the rabbit,” Cardiovasc. Res. 49(3), 609–617 (2001).
[CrossRef] [PubMed]

J. Mayhew, D. Johnston, J. Martindale, M. Jones, J. Berwick, and Y. Zheng, “Increased oxygen consumption following activation of brain: theoretical footnotes using spectroscopic data from barrel cortex,” Neuroimage 13(6), 975–987 (2001).
[CrossRef] [PubMed]

2000 (1)

P. Carmeliet, “Mechanisms of angiogenesis and arteriogenesis,” Nat. Med. 6(4), 389–395 (2000).
[CrossRef] [PubMed]

1998 (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).
[PubMed]

1997 (2)

H. Tian, S. L. McKnight, and D. W. Russell, “Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells,” Genes Dev. 11(1), 72–82 (1997).
[CrossRef] [PubMed]

D. A. Boas and A. G. Yodh, “Spatially varying dynamical properties of turbid media probed with diffusing temporal light correlation,” J. Opt. Soc. Am. A 14(1), 192–215 (1997).
[CrossRef]

1995 (2)

D. A. Boas, L. E. Campbell, and A. G. Yodh, “Scattering and imaging with diffusing temporal field correlations,” Phys. Rev. Lett. 75(9), 1855–1858 (1995).
[CrossRef] [PubMed]

G. L. Wang and G. L. Semenza, “Purification and characterization of hypoxia-inducible factor 1,” J. Biol. Chem. 270(3), 1230–1237 (1995).
[CrossRef] [PubMed]

1993 (1)

V. E. Papaioannou and J. G. Fox, “Efficacy of tribromoethanol anesthesia in mice,” Lab. Anim. Sci. 43(2), 189–192 (1993).
[PubMed]

1992 (1)

S. R. Arridge, M. Cope, and D. T. Delpy, “The theoretical basis for the determination of optical pathlengths in tissue: temporal and frequency analysis,” Phys. Med. Biol. 37(7), 1531–1560 (1992).
[CrossRef] [PubMed]

1979 (1)

S. Takatani and M. D. Graham, “Theoretical analysis of diffuse reflectance from a two-layer tissue model,” IEEE Trans. Biomed. Eng. 26(12), 656–664 (1979).
[CrossRef] [PubMed]

1965 (1)

J. A. Nelder and R. Mead, “A simplex method for function minimization,” Comput. J. 7, 308–313 (1965).

1964 (1)

L. H. Gray and J. M. Steadman, “Determination of the oxyhaemoglobin dissociation curves for mouse and rat blood,” J. Physiol. 175, 161–171 (1964).
[PubMed]

1958 (1)

K. Schmidt-Neilsen and J. L. Larimer, “Oxygen dissociation curves of mammalian blood in relation to body size,” Am. J. Physiol. 195(2), 424–428 (1958).
[PubMed]

Acevedo, V. D.

S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
[CrossRef] [PubMed]

Arridge, S. R.

S. R. Arridge, M. Cope, and D. T. Delpy, “The theoretical basis for the determination of optical pathlengths in tissue: temporal and frequency analysis,” Phys. Med. Biol. 37(7), 1531–1560 (1992).
[CrossRef] [PubMed]

Baker, W. B.

T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73(7), 076701 (2010).
[CrossRef]

Bertout, J. A.

J. A. Bertout, S. A. Patel, and M. C. Simon, “The impact of O2 availability on human cancer,” Nat. Rev. Cancer 8(12), 967–975 (2008).
[CrossRef] [PubMed]

Berwick, J.

J. Mayhew, D. Johnston, J. Martindale, M. Jones, J. Berwick, and Y. Zheng, “Increased oxygen consumption following activation of brain: theoretical footnotes using spectroscopic data from barrel cortex,” Neuroimage 13(6), 975–987 (2001).
[CrossRef] [PubMed]

Bherer, L.

Boas, D. A.

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48(15), 2405–2418 (2003).
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D. A. Boas, J. P. Culver, J. J. Stott, and A. K. Dunn, “Three dimensional Monte Carlo code for photon migration through complex heterogeneous media including the adult human head,” Opt. Express 10(3), 159–170 (2002).
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D. A. Boas, L. E. Campbell, and A. G. Yodh, “Scattering and imaging with diffusing temporal field correlations,” Phys. Rev. Lett. 75(9), 1855–1858 (1995).
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Boengler, K.

E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
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K. R. Forrester, C. Stewart, J. Tulip, C. Leonard, and R. C. Bray, “Comparison of laser speckle and laser Doppler perfusion imaging: measurement in human skin and rabbit articular tissue,” Med. Biol. Eng. Comput. 40(6), 687–697 (2002).
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T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
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M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
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H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
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H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
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M. Solonenko, R. Cheung, T. M. Busch, A. Kachur, G. M. Griffin, T. Vulcan, T. C. Zhu, H. W. Wang, S. M. Hahn, and A. G. Yodh, “In vivo reflectance measurement of optical properties, blood oxygenation and motexafin lutetium uptake in canine large bowels, kidneys and prostates,” Phys. Med. Biol. 47(6), 857–873 (2002).
[PubMed]

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H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
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E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
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D. A. Boas, L. E. Campbell, and A. G. Yodh, “Scattering and imaging with diffusing temporal field correlations,” Phys. Rev. Lett. 75(9), 1855–1858 (1995).
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M. Solonenko, R. Cheung, T. M. Busch, A. Kachur, G. M. Griffin, T. Vulcan, T. C. Zhu, H. W. Wang, S. M. Hahn, and A. G. Yodh, “In vivo reflectance measurement of optical properties, blood oxygenation and motexafin lutetium uptake in canine large bowels, kidneys and prostates,” Phys. Med. Biol. 47(6), 857–873 (2002).
[PubMed]

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T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73(7), 076701 (2010).
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M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
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S. R. Arridge, M. Cope, and D. T. Delpy, “The theoretical basis for the determination of optical pathlengths in tissue: temporal and frequency analysis,” Phys. Med. Biol. 37(7), 1531–1560 (1992).
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D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48(15), 2405–2418 (2003).
[CrossRef] [PubMed]

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[CrossRef] [PubMed]

D. A. Boas, J. P. Culver, J. J. Stott, and A. K. Dunn, “Three dimensional Monte Carlo code for photon migration through complex heterogeneous media including the adult human head,” Opt. Express 10(3), 159–170 (2002).
[PubMed]

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E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
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S. R. Arridge, M. Cope, and D. T. Delpy, “The theoretical basis for the determination of optical pathlengths in tissue: temporal and frequency analysis,” Phys. Med. Biol. 37(7), 1531–1560 (1992).
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Detre, J. A.

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

G. Q. Yu, T. F. Floyd, T. Durduran, C. Zhou, J. J. Wang, J. A. Detre, and A. G. Yodh, “Validation of diffuse correlation spectroscopy for muscle blood flow with concurrent arterial spin labeled perfusion MRI,” Opt. Express 15(3), 1064–1075 (2007).
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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).
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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]

Dunn, A. K.

Durduran, T.

T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73(7), 076701 (2010).
[CrossRef]

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
[CrossRef] [PubMed]

G. Q. Yu, T. F. Floyd, T. Durduran, C. Zhou, J. J. Wang, J. A. Detre, and A. G. Yodh, “Validation of diffuse correlation spectroscopy for muscle blood flow with concurrent arterial spin labeled perfusion MRI,” Opt. Express 15(3), 1064–1075 (2007).
[CrossRef] [PubMed]

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[CrossRef] [PubMed]

Durning, S. M.

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

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M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
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M. Heil, I. Eitenmüller, T. Schmitz-Rixen, and W. Schaper, “Arteriogenesis versus angiogenesis: similarities and differences,” J. Cell. Mol. Med. 10(1), 45–55 (2006).
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Emanuele, M. J.

H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
[CrossRef] [PubMed]

Eucker, S. A.

C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
[CrossRef] [PubMed]

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H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
[CrossRef] [PubMed]

Fernandez, B.

E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
[CrossRef] [PubMed]

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H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
[CrossRef] [PubMed]

Floyd, T. F.

Forrester, K. R.

K. R. Forrester, C. Stewart, J. Tulip, C. Leonard, and R. C. Bray, “Comparison of laser speckle and laser Doppler perfusion imaging: measurement in human skin and rabbit articular tissue,” Med. Biol. Eng. Comput. 40(6), 687–697 (2002).
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M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
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S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
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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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Friess, S. H.

C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
[CrossRef] [PubMed]

Furuya, D.

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[CrossRef] [PubMed]

Gagnon, L.

Gangula, R. D.

S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
[CrossRef] [PubMed]

Gaynor, J. W.

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

Glatstein, E.

H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
[CrossRef] [PubMed]

H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
[CrossRef] [PubMed]

H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
[CrossRef] [PubMed]

Grady, M. S.

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
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[PubMed]

Greenberg, J. H.

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[CrossRef] [PubMed]

Greenberg, N. M.

S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
[CrossRef] [PubMed]

Griffin, G. M.

M. Solonenko, R. Cheung, T. M. Busch, A. Kachur, G. M. Griffin, T. Vulcan, T. C. Zhu, H. W. Wang, S. M. Hahn, and A. G. Yodh, “In vivo reflectance measurement of optical properties, blood oxygenation and motexafin lutetium uptake in canine large bowels, kidneys and prostates,” Phys. Med. Biol. 47(6), 857–873 (2002).
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T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
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E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
[CrossRef] [PubMed]

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D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48(15), 2405–2418 (2003).
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B. Zhou, M. C. Poon, W. T. Pu, and Z. C. Han, “Therapeutic neovascularization for peripheral arterial diseases: advances and perspectives,” Histol. Histopathol. 22(6), 677–686 (2007).
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B. Zhou, M. C. Poon, W. T. Pu, and Z. C. Han, “Therapeutic neovascularization for peripheral arterial diseases: advances and perspectives,” Histol. Histopathol. 22(6), 677–686 (2007).
[PubMed]

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T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
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H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
[CrossRef] [PubMed]

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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
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C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
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H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
[CrossRef] [PubMed]

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D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48(15), 2405–2418 (2003).
[CrossRef] [PubMed]

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N. Skuli, L. Liu, A. Runge, T. Wang, L. Yuan, S. Patel, L. Iruela-Arispe, M. C. Simon, and B. Keith, “Endothelial deletion of hypoxia-inducible factor-2  (HIF-2 ) alters vascular function and tumor angiogenesis,” Blood 114(2), 469–477 (2009).
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H. Tian, S. L. McKnight, and D. W. Russell, “Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells,” Genes Dev. 11(1), 72–82 (1997).
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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
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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).
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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]

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[CrossRef] [PubMed]

I. E. Hoefer, N. van Royen, I. R. Buschmann, J. J. Piek, and W. Schaper, “Time course of arteriogenesis following femoral artery occlusion in the rabbit,” Cardiovasc. Res. 49(3), 609–617 (2001).
[CrossRef] [PubMed]

E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
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M. Heil, I. Eitenmüller, T. Schmitz-Rixen, and W. Schaper, “Arteriogenesis versus angiogenesis: similarities and differences,” J. Cell. Mol. Med. 10(1), 45–55 (2006).
[CrossRef] [PubMed]

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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).
[CrossRef] [PubMed]

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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
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G. L. Wang and G. L. Semenza, “Purification and characterization of hypoxia-inducible factor 1,” J. Biol. Chem. 270(3), 1230–1237 (1995).
[CrossRef] [PubMed]

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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
[CrossRef] [PubMed]

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H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
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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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N. Skuli, L. Liu, A. Runge, T. Wang, L. Yuan, S. Patel, L. Iruela-Arispe, M. C. Simon, and B. Keith, “Endothelial deletion of hypoxia-inducible factor-2  (HIF-2 ) alters vascular function and tumor angiogenesis,” Blood 114(2), 469–477 (2009).
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J. A. Bertout, S. A. Patel, and M. C. Simon, “The impact of O2 availability on human cancer,” Nat. Rev. Cancer 8(12), 967–975 (2008).
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N. Skuli, L. Liu, A. Runge, T. Wang, L. Yuan, S. Patel, L. Iruela-Arispe, M. C. Simon, and B. Keith, “Endothelial deletion of hypoxia-inducible factor-2  (HIF-2 ) alters vascular function and tumor angiogenesis,” Blood 114(2), 469–477 (2009).
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S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
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D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48(15), 2405–2418 (2003).
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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
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A. Matsumoto, S. Matsumoto, A. L. Sowers, J. W. Koscielniak, N. J. Trigg, P. Kuppusamy, J. B. Mitchell, S. Subramanian, M. C. Krishna, and K. I. Matsumoto, “Absolute oxygen tension (pO(2)) in murine fatty and muscle tissue as determined by EPR,” Magn. Reson. Med. 54(6), 1530–1535 (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).
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A. Matsumoto, S. Matsumoto, A. L. Sowers, J. W. Koscielniak, N. J. Trigg, P. Kuppusamy, J. B. Mitchell, S. Subramanian, M. C. Krishna, and K. I. Matsumoto, “Absolute oxygen tension (pO(2)) in murine fatty and muscle tissue as determined by EPR,” Magn. Reson. Med. 54(6), 1530–1535 (2005).
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K. R. Forrester, C. Stewart, J. Tulip, C. Leonard, and R. C. Bray, “Comparison of laser speckle and laser Doppler perfusion imaging: measurement in human skin and rabbit articular tissue,” Med. Biol. Eng. Comput. 40(6), 687–697 (2002).
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E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
[CrossRef] [PubMed]

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E. Deindl, I. Buschmann, I. E. Hoefer, T. Podzuweit, K. Boengler, S. Vogel, N. van Royen, B. Fernandez, and W. Schaper, “Role of ischemia and of hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit,” Circ. Res. 89(9), 779–786 (2001).
[CrossRef] [PubMed]

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M. Solonenko, R. Cheung, T. M. Busch, A. Kachur, G. M. Griffin, T. Vulcan, T. C. Zhu, H. W. Wang, S. M. Hahn, and A. G. Yodh, “In vivo reflectance measurement of optical properties, blood oxygenation and motexafin lutetium uptake in canine large bowels, kidneys and prostates,” Phys. Med. Biol. 47(6), 857–873 (2002).
[PubMed]

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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]

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).
[CrossRef] [PubMed]

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G. L. Wang and G. L. Semenza, “Purification and characterization of hypoxia-inducible factor 1,” J. Biol. Chem. 270(3), 1230–1237 (1995).
[CrossRef] [PubMed]

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H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
[CrossRef] [PubMed]

H. W. Wang, M. E. Putt, M. J. Emanuele, D. B. Shin, E. Glatstein, A. G. Yodh, and T. M. Busch, “Treatment-induced changes in tumor oxygenation predict photodynamic therapy outcome,” Cancer Res. 64(20), 7553–7561 (2004).
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M. Solonenko, R. Cheung, T. M. Busch, A. Kachur, G. M. Griffin, T. Vulcan, T. C. Zhu, H. W. Wang, S. M. Hahn, and A. G. Yodh, “In vivo reflectance measurement of optical properties, blood oxygenation and motexafin lutetium uptake in canine large bowels, kidneys and prostates,” Phys. Med. Biol. 47(6), 857–873 (2002).
[PubMed]

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H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
[CrossRef] [PubMed]

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T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
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N. Skuli, L. Liu, A. Runge, T. Wang, L. Yuan, S. Patel, L. Iruela-Arispe, M. C. Simon, and B. Keith, “Endothelial deletion of hypoxia-inducible factor-2  (HIF-2 ) alters vascular function and tumor angiogenesis,” Blood 114(2), 469–477 (2009).
[CrossRef] [PubMed]

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M. Bosch-Marce, H. Okuyama, J. B. Wesley, K. Sarkar, H. Kimura, Y. V. Liu, H. Zhang, M. Strazza, S. Rey, L. Savino, Y. F. Zhou, K. R. McDonald, Y. Na, S. Vandiver, A. Rabi, Y. Shaked, R. Kerbel, T. Lavallee, and G. L. Semenza, “Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia,” Circ. Res. 101(12), 1310–1318 (2007).
[CrossRef] [PubMed]

Wileyto, E. P.

H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
[CrossRef] [PubMed]

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S. F. Winter, V. D. Acevedo, R. D. Gangula, K. W. Freeman, D. M. Spencer, and N. M. Greenberg, “Conditional activation of FGFR1 in the prostate epithelium induces angiogenesis with concomitant differential regulation of Ang-1 and Ang-2,” Oncogene 26(34), 4897–4907 (2007).
[CrossRef] [PubMed]

Witzenbichler, B.

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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M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
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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]

Yodh, A.

H.-W. Wang, E. Rickter, M. Yuan, E. P. Wileyto, E. Glatstein, A. Yodh, and T. M. Busch*, “Effect of Photosensitizer Dose on Fluence Rate Responses to Photodynamic Therapy,” Photochem. Photobiol. 83(5), 1040–1048 (2007).
[CrossRef] [PubMed]

Yodh, A. G.

T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73(7), 076701 (2010).
[CrossRef]

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
[CrossRef] [PubMed]

H. W. Wang, J. C. Finlay, K. Lee, T. C. Zhu, M. E. Putt, E. Glatstein, C. J. Koch, S. M. Evans, S. M. Hahn, T. M. Busch, and A. G. Yodh, “Quantitative comparison of tissue oxygen and motexafin lutetium uptake by ex vivo and noninvasive in vivo techniques in patients with intraperitoneal carcinomatosis,” J. Biomed. Opt. 12(3), 034023 (2007).
[CrossRef] [PubMed]

G. Q. Yu, T. F. Floyd, T. Durduran, C. Zhou, J. J. Wang, J. A. Detre, and A. G. Yodh, “Validation of diffuse correlation spectroscopy for muscle blood flow with concurrent arterial spin labeled perfusion MRI,” Opt. Express 15(3), 1064–1075 (2007).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

Yu, G.

T. Durduran, C. Zhou, E. M. Buckley, M. N. Kim, G. Yu, R. Choe, J. W. Gaynor, T. L. Spray, S. M. Durning, S. E. Mason, L. M. Montenegro, S. C. Nicolson, R. A. Zimmerman, M. E. Putt, J. J. Wang, J. H. Greenberg, J. A. Detre, A. G. Yodh, and D. J. Licht, “Optical measurement of cerebral hemodynamics and oxygen metabolism in neonates with congenital heart defects,” J. Biomed. Opt. 15(3), 037004 (2010).
[CrossRef] [PubMed]

M. N. Kim, T. Durduran, S. Frangos, B. L. Edlow, E. M. Buckley, H. E. Moss, C. Zhou, G. Yu, R. Choe, E. Maloney-Wilensky, R. L. Wolf, M. S. Grady, J. H. Greenberg, J. M. Levine, A. G. Yodh, J. A. Detre, and W. A. Kofke, “Noninvasive measurement of cerebral blood flow and blood oxygenation using near-infrared and diffuse correlation spectroscopies in critically brain-injured adults,” Neurocrit. Care 12(2), 173–180 (2010).
[CrossRef] [PubMed]

C. Zhou, S. A. Eucker, T. Durduran, G. Yu, J. Ralston, S. H. Friess, R. N. Ichord, S. S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14(3), 034015 (2009).
[CrossRef] [PubMed]

Yu, G. Q.

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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Figures (6)

Fig. 1
Fig. 1

Schematic diagram showing the position of the optical probe on the mouse hindlimb. The design of the probe is shown in the right side for both DOS (top) and DCS (bottom).

Fig. 2
Fig. 2

Median perfusion ratio calculated from all the survival mice, separated by mice genotype. Data were collected at (a) 5 mm and (b) 10 mm source-detector separations with DCS, and (c) with LDF. Error bars represent the standard error across the animals, and the stars are the time points with statistical difference between the two mice genotypes (ANOVA, p < 0.05).

Fig. 3
Fig. 3

(a) Absolute scattering coefficient at 785 nm, (b) tissue oxygen saturation and (c) THC in the limb calculated from all the survival mice, separated by mice genotype, for both the non-occluded and occluded hindlimbs. Error bars represent the standard error across the animals, and the stars denote the time points with statistical difference between the two mice genotypes (ANOVA, p < 0.05).

Fig. 4
Fig. 4

Representative field in the adductor muscle showing Rhodamine-labeled vessels/capillaries in the non-occluded and the occluded limb from control and KO mice, obtained 28 days after femoral artery ligation.

Fig. 5
Fig. 5

(a) Vessel/capillary density and vascular area in an adductor muscle specimen from a control mouse 28 days after femoral artery ligation. Vasculature was visualized using a Rhodamine Lectin staining. Images were taken at the most superficial part (labeled superficial) of the muscle, immediately under the skin, and approximately 4 mm into the muscle (labeled deep). (b) Quantification of superficial and deep vascular area for both the non-occluded and occluded limbs in control mice. (c) Comparison of the perfusion ratios obtained via DCS (10 mm source-detector separations) to LDF measured perfusion ratios. The plot on the left contains data from pre- and post-surgery, while the one in the right shows data from the follow-up measurements. The gray line indicates a unity slope for Perfusion RatioDCS/Perfusion RatioLDF, while the red line shows the best linear fit to the data.

Fig. 6
Fig. 6

Metabolic rate of oxygen consumption ratio in the limb for all the time points measured, and separated by mice genotype. Error bars represent the standard error across all the animals, and the stars denote the time points with statistical difference between the two mice genotypes (ANOVA, p < 0.05).

Tables (1)

Tables Icon

Table 1 Perfusion Ratio calculated by three different approaches from DCS data from control mice, separated by source-detector separation. Uncertainty of the values denotes the standard error across all animals

Equations (6)

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

Φ ( r , t ) = v 4 π D m ( e k 0 . r + , m r + , m e k 0 . r , m r . m ) ,
μ s ' ( λ ) = A λ b  and  μ a ( λ ) = i ε i ( λ ) c i .
G 1 ( τ ) = 3 μ s ' 4 π m ( e K ( τ ) r + , m r + , m e K ( τ ) r , m r . m ) ,
g 2 ( r , t , τ ) = 1 + β | g 1 ( r , t , τ ) | 2 .
O E F = S a O 2 S t O 2 γ S a O 2 ,
M R O 2 ( o c ) M R O 2 ( n o ) = B F I ( o c ) B F I ( n o ) c H b ( o c ) / c H b ( n o ) T H C ( o c ) / T H C ( n o ) ,

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