Abstract

Many vasculature-related diseases affecting skeletal muscle function have been studied in mouse models. Noninvasive quantification of muscle blood flow responses during postocclusive reactive hyperemia (PORH) is often used to evaluate vascular function in human skeletal muscles. However, blood flow measurements during PORH in small skeletal muscles of mice are rare due to the lack of appropriate technologies coupled with the challenge of measurement setup resulting from the lack of large enough test sites. In this study, we explored adapting diffuse correlation spectroscopy (DCS) for noninvasive measurement of the relative changes of blood flow (rBF) in mouse thigh muscles during PORH. A small fiber-optic probe was designed and glued on the mouse thigh to reduce the motion artifact induced by the occlusion procedure. Arterial occlusion was created by tying a polyvinyl chloride (PVC) tube around the mouse thigh while the muscle rBF was continuously monitored by DCS to ensure the success of the occlusion. After 5 min, the occlusion was rapidly released by severing the PVC tube using a cautery pen. Typical rBF responses during PORH were observed in all mice (n=7), which are consistent with those observed by arterial-spin-labeled magnetic resonance imaging (ASL-MRI) as reported in the literature. On average, rBF values from DCS during occlusion were lower than 10% (3.1±2.2%) of the baseline values (assigning 100%), indicating the success of arterial occlusion in all mice. Peak values of rBF during PORH measured by the DCS (357.6±36.3%) and ASL-MRI (387.5±150.0%) were also similar whereas the values of time-to-peak (the time duration from the end of occlusion to the peak rBF) were quite different (112.6±35.0s versus 48.0±27.0s). Simultaneous measurements by these two techniques are needed to identify the factors that may cause such discrepancy. This study highlights the utility of DCS technology to quantitatively evaluate tissue blood flow responses during PORH in mouse skeletal muscles. DCS holds promise as valuable tool to assess blood flow regulation in mouse models with a variety of vascular diseases (e.g., hypercholesterolemia, diabetes, peripheral artery disease).

© 2013 Optical Society of America

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    [CrossRef]

2012 (5)

M. Roustit and J. L. Cracowski, “Non-invasive assessment of skin microvascular function in humans: an insight into methods,” Microcirculation 19, 47–64 (2012).
[CrossRef]

K. Gurley, Y. Shang, and G. Yu, “Noninvasive optical quantification of absolute blood flow, blood oxygenation, and oxygen consumption rate in exercising skeletal muscle,” J. Biomed. Opt. 17, 075010 (2012).
[CrossRef]

N. Munk, B. Symons, Y. Shang, R. Cheng, and G. Yu, “Noninvasively measuring the hemodynamic effects of massage on skeletal muscle: a novel hybrid near-infrared diffuse optical instrument,” J. Bodywave Mov. Ther. 16, 22–28 (2012).
[CrossRef]

R. Cheng, Y. Shang, D. Hayes, S. P. Saha, and G. Yu, “Noninvasive optical evaluation of spontaneous low frequency oscillations in cerebral hemodynamics,” NeuroImage 62, 1445–1454 (2012).
[CrossRef]

Y. Shang, K. Gurley, B. Symons, D. Long, R. Srikuea, L. J. Crofford, C. A. Peterson, and G. Yu, “Noninvasive optical characterization of muscle blood flow, oxygenation, and metabolism in women with fibromyalgia,” Arthritis Res. Ther. 14, R236 (2012).
[CrossRef]

2011 (5)

G. Yu, Y. Shang, Y. Zhao, R. Cheng, L. Dong, and S. P. Saha, “Intraoperative evaluation of revascularization effect on ischemic muscle hemodynamics using near-infrared diffuse optical spectroscopies,” J. Biomed. Opt. 16, 027004 (2011).
[CrossRef]

D. Irwin, L. Dong, Y. Shang, R. Cheng, M. Kudrimoti, S. D. Stevens, and G. Yu, “Influences of tissue absorption and scattering on diffuse correlation spectroscopy blood flow measurements,” Biomed. Opt. Express 2, 1969–1985 (2011).
[CrossRef]

Y. Shang, L. Chen, M. Toborek, and G. Yu, “Diffuse optical monitoring of repeated cerebral ischemia in mice,” Opt. Express 19, 20301–20315 (2011).
[CrossRef]

A. J. Rufaihah, N. F. Huang, S. Jame, J. C. Lee, H. N. Nguyen, B. Byers, A. De, J. Okogbaa, M. Rollins, R. Reijo-Pera, S. S. Gambhir, and J. P. Cooke, “Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease,” Arterioscler. Thromb. Vasc. Biol. 31, E72–E79 (2011).
[CrossRef]

C. Baligand, C. Wary, J. C. Menard, E. Giacomini, J. Y. Hogrel, and P. G. Carlier, “Measuring perfusion and bioenergetics simultaneously in mouse skeletal muscle: a multiparametric functional-NMR approach,” NMR Biomed. 24, 281–290 (2011).
[CrossRef]

2010 (4)

N. Roche-Labarbe, S. A. Carp, A. Surova, M. Patel, D. A. Boas, P. E. Grant, and M. A. Franceschini, “Noninvasive optical measures of CBV, StO(2), CBF index, and rCMRO(2) in human premature neonates’ brains in the first six weeks of life,” Hum. Brain Mapp. 31, 341–352 (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, 173–180 (2010).
[CrossRef]

Y. Shang, T. B. Symons, T. Durduran, A. G. Yodh, and G. Yu, “Effects of muscle fiber motion on diffuse correlation spectroscopy blood flow measurements during exercise,” Biomed. Opt. Express 1, 500–511 (2010).
[CrossRef]

R. C. Mesquita, N. Skuli, M. N. Kim, J. M. Liang, S. Schenkel, A. J. Majmundar, M. C. Simon, and A. G. Yodh, “Hemodynamic and metabolic diffuse optical monitoring in a mouse model of hindlimb ischemia,” Biomed. Opt. Express 1, 1173–1187 (2010).
[CrossRef]

2009 (3)

2008 (2)

D. Bertoldi, P. Loureiro de Sousa, Y. Fromes, C. Wary, and P. G. Carlier, “Quantitative, dynamic and noninvasive determination of skeletal muscle perfusion in mouse leg by NMR arterial spin-labeled imaging,” Magn. Reson. Imaging 26, 1259–1265 (2008).
[CrossRef]

J. Li, M. Ninck, L. Koban, T. Elbert, J. Kissler, and T. Gisler, “Transient functional blood flow change in the human brain measured noninvasively by diffusing-wave spectroscopy,” Opt. Lett. 33, 2233–2235 (2008).
[CrossRef]

2007 (2)

G. Yu, T. 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, 1064–1075 (2007).
[CrossRef]

A. L. Huang, A. E. Silver, E. Shvenke, D. W. Schopfer, E. Jahangir, M. A. Titas, A. Shpilman, J. O. Menzoian, M. T. Watkins, J. D. Raffetto, G. Gibbons, J. Woodson, P. M. Shaw, M. Dhadly, R. T. Eberhardt, J. F. Keaney, N. Gokce, and J. A. Vita, “Predictive value of reactive hyperemia for cardiovascular events in patients with peripheral arterial disease undergoing vascular surgery,” Arterioscler. Thromb. Vasc. Biol. 27, 2113–2119 (2007).
[CrossRef]

2006 (2)

E. T. Petersen, I. Zimine, Y. C. L. Ho, and X. Golay, “Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques,” Br. J. Radiol. 79, 688–701 (2006).
[CrossRef]

P. G. Carlier, D. Bertoldi, C. Baligand, C. Wary, and Y. Fromes, “Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy,” NMR Biomed. 19, 954–967 (2006).
[CrossRef]

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, 520–526 (2005).
[CrossRef]

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11, 3543–3552 (2005).
[CrossRef]

G. Yu, T. Durduran, G. Lech, C. Zhou, B. Chance, E. R. Mohler, and A. G. Yodh, “Time-dependent blood flow and oxygenation in human skeletal muscles measured with noninvasive near-infrared diffuse optical spectroscopies,” J. Biomed. Opt. 10, 024027 (2005).
[CrossRef]

2004 (1)

Z. Guo, W. Su, H. Pang, and M. Gong, “COX-2 up-regulation and vascular smooth muscle contractile hyperreactivity in spontaneous diabetic db/db mice,” Diabetes 54, 190 (2004).

2001 (2)

C. Emanueli, A. Minasi, A. Zacheo, J. Chao, L. Chao, M. B. Salis, S. Straino, M. G. Tozzi, R. Smith, L. Gaspa, G. Bianchini, F. Stillo, M. C. Capogrossi, and P. Madeddu, “Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia,” Circulation 103, 125–132 (2001).
[CrossRef]

C. Cheung, J. P. Culver, K. Takahashi, J. H. Greenberg, and A. G. Yodh, “In vivo cerebrovascular measurement combining diffuse near-infrared absorption and correlation spectroscopies,” Phys. Med. Biol. 46, 2053–2065 (2001).
[CrossRef]

2000 (1)

F. W. Prinzen and J. B. Bassingthwaighte, “Blood flow distributions by microsphere deposition methods,” Cardiovasc. Res. 45, 13–21 (2000).
[CrossRef]

1999 (1)

A. E. Caballero, S. Arora, R. Saouaf, S. C. Lim, P. Smakowski, J. Y. Park, G. L. King, F. W. LoGerfo, E. S. Horton, and A. Veves, “Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes,” Diabetes 48, 1856–1862 (1999).
[CrossRef]

1997 (1)

1995 (2)

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

J. H. Krege, J. B. Hodgin, J. R. Hagaman, and O. Smithies, “A noninvasive computerized tail-cuff system for measuring blood pressure in mice,” Hypertension 25, 1111–1115 (1995).
[CrossRef]

1994 (1)

1988 (1)

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing-wave spectroscopy,” Phys. Rev. Lett. 60, 1134–1137 (1988).
[CrossRef]

1987 (1)

G. Maret and P. E. Wolf, “Multiple light scattering from disordered media. The effect of Brownian motion of scatterers,” Z. Phys. B 65, 409–413 (1987).
[CrossRef]

1985 (1)

M. H. Criqui, A. Fronek, E. Barrettconnor, M. R. Klauber, S. Gabriel, and D. Goodman, “The prevalence of peripheral arterial-disease in a defined population,” Circulation 71, 510–515 (1985).
[CrossRef]

1981 (1)

J. H. Lombard and B. R. Duling, “Multiple mechanisms of reactive hyperemia in arterioles of the hamster-cheek pouch,” Am. J. Physiol. 241, H748–H755 (1981).

1973 (1)

A. Fronek, K. Johansen, R. B. Dilley, and E. F. Bernstein, “Ultrasonographically monitored postocclusive reactive hyperemia in the diagnosis of peripheral arterial occlusive disease,” Circulation 48, 149–152 (1973).
[CrossRef]

Arger, P. H.

Arora, S.

A. E. Caballero, S. Arora, R. Saouaf, S. C. Lim, P. Smakowski, J. Y. Park, G. L. King, F. W. LoGerfo, E. S. Horton, and A. Veves, “Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes,” Diabetes 48, 1856–1862 (1999).
[CrossRef]

Baligand, C.

C. Baligand, C. Wary, J. C. Menard, E. Giacomini, J. Y. Hogrel, and P. G. Carlier, “Measuring perfusion and bioenergetics simultaneously in mouse skeletal muscle: a multiparametric functional-NMR approach,” NMR Biomed. 24, 281–290 (2011).
[CrossRef]

P. G. Carlier, D. Bertoldi, C. Baligand, C. Wary, and Y. Fromes, “Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy,” NMR Biomed. 19, 954–967 (2006).
[CrossRef]

Barrettconnor, E.

M. H. Criqui, A. Fronek, E. Barrettconnor, M. R. Klauber, S. Gabriel, and D. Goodman, “The prevalence of peripheral arterial-disease in a defined population,” Circulation 71, 510–515 (1985).
[CrossRef]

Bassingthwaighte, J. B.

F. W. Prinzen and J. B. Bassingthwaighte, “Blood flow distributions by microsphere deposition methods,” Cardiovasc. Res. 45, 13–21 (2000).
[CrossRef]

Bernstein, E. F.

A. Fronek, K. Johansen, R. B. Dilley, and E. F. Bernstein, “Ultrasonographically monitored postocclusive reactive hyperemia in the diagnosis of peripheral arterial occlusive disease,” Circulation 48, 149–152 (1973).
[CrossRef]

Bertoldi, D.

D. Bertoldi, P. Loureiro de Sousa, Y. Fromes, C. Wary, and P. G. Carlier, “Quantitative, dynamic and noninvasive determination of skeletal muscle perfusion in mouse leg by NMR arterial spin-labeled imaging,” Magn. Reson. Imaging 26, 1259–1265 (2008).
[CrossRef]

P. G. Carlier, D. Bertoldi, C. Baligand, C. Wary, and Y. Fromes, “Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy,” NMR Biomed. 19, 954–967 (2006).
[CrossRef]

Bianchini, G.

C. Emanueli, A. Minasi, A. Zacheo, J. Chao, L. Chao, M. B. Salis, S. Straino, M. G. Tozzi, R. Smith, L. Gaspa, G. Bianchini, F. Stillo, M. C. Capogrossi, and P. Madeddu, “Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia,” Circulation 103, 125–132 (2001).
[CrossRef]

Boas, D. A.

N. Roche-Labarbe, S. A. Carp, A. Surova, M. Patel, D. A. Boas, P. E. Grant, and M. A. Franceschini, “Noninvasive optical measures of CBV, StO(2), CBF index, and rCMRO(2) in human premature neonates’ brains in the first six weeks of life,” Hum. Brain Mapp. 31, 341–352 (2010).
[CrossRef]

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, 192–215 (1997).
[CrossRef]

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

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, 520–526 (2005).
[CrossRef]

Buckley, E. M.

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C. Baligand, C. Wary, J. C. Menard, E. Giacomini, J. Y. Hogrel, and P. G. Carlier, “Measuring perfusion and bioenergetics simultaneously in mouse skeletal muscle: a multiparametric functional-NMR approach,” NMR Biomed. 24, 281–290 (2011).
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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, 173–180 (2010).
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E. M. Buckley, N. M. Cook, T. Durduran, M. N. Kim, C. Zhou, R. Choe, G. Yu, S. Shultz, C. M. Sehgal, D. J. Licht, P. H. Arger, M. E. Putt, H. Hurt, and A. G. Yodh, “Cerebral hemodynamics in preterm infants during positional intervention measured with diffuse correlation spectroscopy and transcranial Doppler ultrasound,” Opt. Express 17, 12571–12581 (2009).
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Cooke, J. P.

A. J. Rufaihah, N. F. Huang, S. Jame, J. C. Lee, H. N. Nguyen, B. Byers, A. De, J. Okogbaa, M. Rollins, R. Reijo-Pera, S. S. Gambhir, and J. P. Cooke, “Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease,” Arterioscler. Thromb. Vasc. Biol. 31, E72–E79 (2011).
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Y. Shang, K. Gurley, B. Symons, D. Long, R. Srikuea, L. J. Crofford, C. A. Peterson, and G. Yu, “Noninvasive optical characterization of muscle blood flow, oxygenation, and metabolism in women with fibromyalgia,” Arthritis Res. Ther. 14, R236 (2012).
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C. Cheung, J. P. Culver, K. Takahashi, J. H. Greenberg, and A. G. Yodh, “In vivo cerebrovascular measurement combining diffuse near-infrared absorption and correlation spectroscopies,” Phys. Med. Biol. 46, 2053–2065 (2001).
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[CrossRef]

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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, 173–180 (2010).
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G. Yu, T. 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, 1064–1075 (2007).
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Y. Shang, T. B. Symons, T. Durduran, A. G. Yodh, and G. Yu, “Effects of muscle fiber motion on diffuse correlation spectroscopy blood flow measurements during exercise,” Biomed. Opt. Express 1, 500–511 (2010).
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C. Zhou, S. Eucker, T. Durduran, G. Yu, J. Ralston, S. Friess, R. Ichor, S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14, 034015 (2009).
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E. M. Buckley, N. M. Cook, T. Durduran, M. N. Kim, C. Zhou, R. Choe, G. Yu, S. Shultz, C. M. Sehgal, D. J. Licht, P. H. Arger, M. E. Putt, H. Hurt, and A. G. Yodh, “Cerebral hemodynamics in preterm infants during positional intervention measured with diffuse correlation spectroscopy and transcranial Doppler ultrasound,” Opt. Express 17, 12571–12581 (2009).
[CrossRef]

G. Yu, T. 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, 1064–1075 (2007).
[CrossRef]

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11, 3543–3552 (2005).
[CrossRef]

G. Yu, T. Durduran, G. Lech, C. Zhou, B. Chance, E. R. Mohler, and A. G. Yodh, “Time-dependent blood flow and oxygenation in human skeletal muscles measured with noninvasive near-infrared diffuse optical spectroscopies,” J. Biomed. Opt. 10, 024027 (2005).
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[CrossRef]

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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, 173–180 (2010).
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Emanueli, C.

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

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N. Roche-Labarbe, S. A. Carp, A. Surova, M. Patel, D. A. Boas, P. E. Grant, and M. A. Franceschini, “Noninvasive optical measures of CBV, StO(2), CBF index, and rCMRO(2) in human premature neonates’ brains in the first six weeks of life,” Hum. Brain Mapp. 31, 341–352 (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, 173–180 (2010).
[CrossRef]

Friess, S.

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

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D. Bertoldi, P. Loureiro de Sousa, Y. Fromes, C. Wary, and P. G. Carlier, “Quantitative, dynamic and noninvasive determination of skeletal muscle perfusion in mouse leg by NMR arterial spin-labeled imaging,” Magn. Reson. Imaging 26, 1259–1265 (2008).
[CrossRef]

P. G. Carlier, D. Bertoldi, C. Baligand, C. Wary, and Y. Fromes, “Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy,” NMR Biomed. 19, 954–967 (2006).
[CrossRef]

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M. H. Criqui, A. Fronek, E. Barrettconnor, M. R. Klauber, S. Gabriel, and D. Goodman, “The prevalence of peripheral arterial-disease in a defined population,” Circulation 71, 510–515 (1985).
[CrossRef]

A. Fronek, K. Johansen, R. B. Dilley, and E. F. Bernstein, “Ultrasonographically monitored postocclusive reactive hyperemia in the diagnosis of peripheral arterial occlusive disease,” Circulation 48, 149–152 (1973).
[CrossRef]

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M. H. Criqui, A. Fronek, E. Barrettconnor, M. R. Klauber, S. Gabriel, and D. Goodman, “The prevalence of peripheral arterial-disease in a defined population,” Circulation 71, 510–515 (1985).
[CrossRef]

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A. J. Rufaihah, N. F. Huang, S. Jame, J. C. Lee, H. N. Nguyen, B. Byers, A. De, J. Okogbaa, M. Rollins, R. Reijo-Pera, S. S. Gambhir, and J. P. Cooke, “Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease,” Arterioscler. Thromb. Vasc. Biol. 31, E72–E79 (2011).
[CrossRef]

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C. Emanueli, A. Minasi, A. Zacheo, J. Chao, L. Chao, M. B. Salis, S. Straino, M. G. Tozzi, R. Smith, L. Gaspa, G. Bianchini, F. Stillo, M. C. Capogrossi, and P. Madeddu, “Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia,” Circulation 103, 125–132 (2001).
[CrossRef]

Giacomini, E.

C. Baligand, C. Wary, J. C. Menard, E. Giacomini, J. Y. Hogrel, and P. G. Carlier, “Measuring perfusion and bioenergetics simultaneously in mouse skeletal muscle: a multiparametric functional-NMR approach,” NMR Biomed. 24, 281–290 (2011).
[CrossRef]

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A. L. Huang, A. E. Silver, E. Shvenke, D. W. Schopfer, E. Jahangir, M. A. Titas, A. Shpilman, J. O. Menzoian, M. T. Watkins, J. D. Raffetto, G. Gibbons, J. Woodson, P. M. Shaw, M. Dhadly, R. T. Eberhardt, J. F. Keaney, N. Gokce, and J. A. Vita, “Predictive value of reactive hyperemia for cardiovascular events in patients with peripheral arterial disease undergoing vascular surgery,” Arterioscler. Thromb. Vasc. Biol. 27, 2113–2119 (2007).
[CrossRef]

Gisler, T.

Glatstein, E.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11, 3543–3552 (2005).
[CrossRef]

Gokce, N.

A. L. Huang, A. E. Silver, E. Shvenke, D. W. Schopfer, E. Jahangir, M. A. Titas, A. Shpilman, J. O. Menzoian, M. T. Watkins, J. D. Raffetto, G. Gibbons, J. Woodson, P. M. Shaw, M. Dhadly, R. T. Eberhardt, J. F. Keaney, N. Gokce, and J. A. Vita, “Predictive value of reactive hyperemia for cardiovascular events in patients with peripheral arterial disease undergoing vascular surgery,” Arterioscler. Thromb. Vasc. Biol. 27, 2113–2119 (2007).
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M. H. Criqui, A. Fronek, E. Barrettconnor, M. R. Klauber, S. Gabriel, and D. Goodman, “The prevalence of peripheral arterial-disease in a defined population,” Circulation 71, 510–515 (1985).
[CrossRef]

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, 173–180 (2010).
[CrossRef]

Grant, P. E.

N. Roche-Labarbe, S. A. Carp, A. Surova, M. Patel, D. A. Boas, P. E. Grant, and M. A. Franceschini, “Noninvasive optical measures of CBV, StO(2), CBF index, and rCMRO(2) in human premature neonates’ brains in the first six weeks of life,” Hum. Brain Mapp. 31, 341–352 (2010).
[CrossRef]

Gratton, E.

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, 173–180 (2010).
[CrossRef]

C. Cheung, J. P. Culver, K. Takahashi, J. H. Greenberg, and A. G. Yodh, “In vivo cerebrovascular measurement combining diffuse near-infrared absorption and correlation spectroscopies,” Phys. Med. Biol. 46, 2053–2065 (2001).
[CrossRef]

Guo, Z.

Z. Guo, W. Su, H. Pang, and M. Gong, “COX-2 up-regulation and vascular smooth muscle contractile hyperreactivity in spontaneous diabetic db/db mice,” Diabetes 54, 190 (2004).

Gurley, K.

Y. Shang, K. Gurley, B. Symons, D. Long, R. Srikuea, L. J. Crofford, C. A. Peterson, and G. Yu, “Noninvasive optical characterization of muscle blood flow, oxygenation, and metabolism in women with fibromyalgia,” Arthritis Res. Ther. 14, R236 (2012).
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K. Gurley, Y. Shang, and G. Yu, “Noninvasive optical quantification of absolute blood flow, blood oxygenation, and oxygen consumption rate in exercising skeletal muscle,” J. Biomed. Opt. 17, 075010 (2012).
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R. Cheng, Y. Shang, D. Hayes, S. P. Saha, and G. Yu, “Noninvasive optical evaluation of spontaneous low frequency oscillations in cerebral hemodynamics,” NeuroImage 62, 1445–1454 (2012).
[CrossRef]

Heil, 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, 520–526 (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, 520–526 (2005).
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D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing-wave spectroscopy,” Phys. Rev. Lett. 60, 1134–1137 (1988).
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G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11, 3543–3552 (2005).
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G. Yu, Y. Shang, Y. Zhao, R. Cheng, L. Dong, and S. P. Saha, “Intraoperative evaluation of revascularization effect on ischemic muscle hemodynamics using near-infrared diffuse optical spectroscopies,” J. Biomed. Opt. 16, 027004 (2011).
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C. Zhou, S. Eucker, T. Durduran, G. Yu, J. Ralston, S. Friess, R. Ichor, S. Margulies, and A. G. Yodh, “Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury,” J. Biomed. Opt. 14, 034015 (2009).
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Figures (6)

Fig. 1.
Fig. 1.

(a) Animal experimental setup and (b) DCS device. The mouse was anesthetized with 1% isoflurane through inhaling and secured on a heated pad by taping the limbs. A fiber-optic probe was glued on the mouse right thigh. A surgical cautery was used to burn/cut the PVC tube. The fiber-optic probe with source and detector fibers were connected to the DCS device.

Fig. 2.
Fig. 2.

Small DCS fiber-optic probe consisted of a rectangular foam pad (a), to confine the source and detector fibers (b) at a distance of 6 mm (c).

Fig. 3.
Fig. 3.

Schematic showing the arterial occlusive procedure. (a) The fiber-optic probe was glued on the mouse right thigh for monitoring muscle rBF throughout the experimental procedure. The PVC tube was loosely wrapped between the hip and glued probe at rest. (b) The tying force on the tube was increased to occlude the artery for 5 min. (c) A surgical cautery was used to burn the tube and release the occlusion.

Fig. 4.
Fig. 4.

Typical blood flow response during POHR in one mouse. Two vertical solid gray lines indicate the beginning and ending of the arterial occlusion, respectively. The dot inside the red circle represents the peak rBF during PORH. The time duration from the occlusion release to the peak rBF is defined as time-to-peak.

Fig. 5.
Fig. 5.

Individual rBF responses during PORH. All time-course data are aligned at Time 0 when the arterial occlusion was released.

Fig. 6.
Fig. 6.

Average rBF responses and variations (depicted as standard deviation bars) during PORH for n=7 mice. All time-course data are aligned at Time 0 when the arterial occlusion was released.

Tables (1)

Tables Icon

Table 1. Comparison of Blood Flow Responses During PORH Measured by DCS and ASL-MRI

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