Abstract

Subcutaneously implanted experimental tumors in mice are commonly used in cancer research. Despite their superficial location, they remain a challenge to image non-invasively at sufficient spatial resolution for microvascular studies. Here we evaluate the capabilities of optical coherence tomography (OCT) angiography for imaging such tumors directly through the murine skin in-vivo. Data sets were collected from mouse tumors derived from fibrosarcoma cells genetically engineered to express only single splice variant isoforms of vascular endothelial growth factor A (VEGF); either VEGF120 or VEGF188 (fs120 and fs188 tumors respectively). Measured vessel diameter was found to be significantly (p<0.001) higher for fs120 tumors (60.7 ± 4.9μm) compared to fs188 tumors (45.0 ± 4.0μm). The fs120 tumors also displayed significantly higher vessel tortuosity, fractal dimension and density. The ability to differentiate between tumor types with OCT suggests that the visible abnormal vasculature is representative of the tumor microcirculation, providing a robust, non-invasive method for observing the longitudinal dynamics of the subcutaneous tumor microcirculation.

© 2017 Optical Society of America

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2017 (1)

D. W. Wei, A. J. Deegan, and R. K. Wang, “Automatic motion correction for in vivo human skin optical coherence tomography angiography through combined rigid and nonrigid registration,” J. Biomed. Opt. 22(6), 066013 (2017).
[Crossref] [PubMed]

2016 (2)

A. Chekkoury, A. Nunes, J. Gateau, P. Symvoulidis, A. Feuchtinger, N. Beziere, S. V. Ovsepian, A. Walch, and V. Ntziachristos, “High-Resolution Multispectral Optoacoustic Tomography of the Vascularization and Constitutive Hypoxemia of Cancerous Tumors,” Neoplasia 18(8), 459–467 (2016).
[Crossref] [PubMed]

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

2015 (1)

2014 (2)

N. M. Biel, J. A. Lee, B. S. Sorg, and D. W. Siemann, “Limitations of the dorsal skinfold window chamber model in evaluating anti-angiogenic therapy during early phase of angiogenesis,” Vasc Cell 6(1), 17 (2014).
[Crossref] [PubMed]

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

2012 (1)

K. Jurczyszyn, B. J. Osiecka, and P. Ziółkowski, “The Use of Fractal Dimension Analysis in Estimation of Blood Vessels Shape in Transplantable Mammary Adenocarcinoma in Wistar Rats after Photodynamic Therapy Combined with Cysteine Protease Inhibitors,” Comput. Math. Methods Med. 2012, 1–6 (2012).
[Crossref]

2011 (5)

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).

K. Calabro, A. Curtis, J.-R. Galarneau, T. Krucker, and I. J. Bigio, “Gender variations in the optical properties of skin in murine animal models,” J. Biomed. Opt. 16(1), 011008 (2011).
[Crossref] [PubMed]

P. Carmeliet and R. K. Jain, “Molecular mechanisms and clinical applications of angiogenesis,” Nature 473(7347), 298–307 (2011).
[Crossref] [PubMed]

D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell 144(5), 646–674 (2011).
[Crossref] [PubMed]

S. Goel, D. G. Duda, L. Xu, L. L. Munn, Y. Boucher, D. Fukumura, and R. K. Jain, “Normalization of the Vasculature for Treatment of Cancer and Other Diseases,” Physiol. Rev. 91(3), 1071–1121 (2011).
[Crossref] [PubMed]

2010 (1)

2009 (1)

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)

B. Nico, V. Benagiano, D. Mangieri, N. Maruotti, A. Vacca, and D. Ribatti, “Evaluation of microvascular density in tumors: pro and contra,” Histol. Histopathol. 23(5), 601–607 (2008).
[PubMed]

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
[Crossref] [PubMed]

2005 (2)

T. Jeswani and A. R. Padhani, “Imaging tumour angiogenesis,” Cancer Imaging 5(1), 131–138 (2005).
[Crossref] [PubMed]

C. O. S. Sorzano, P. Thévenaz, and M. Unser, “Elastic Registration of Biological Images Using Vector-Spline Regularization,” IEEE Trans. Biomed. Eng. 52(4), 652–663 (2005).
[Crossref] [PubMed]

2004 (1)

F. Kiessling, S. Greschus, M. P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M. M. Mueller, N. E. Fusenig, H. Traupe, and W. Semmler, “Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis,” Nat. Med. 10(10), 1133–1138 (2004).
[Crossref] [PubMed]

2003 (1)

C. Fink, F. Kiessling, M. Bock, M. P. Lichy, B. Misselwitz, P. Peschke, N. E. Fusenig, R. Grobholz, and S. Delorme, “High-resolution three-dimensional MR angiography of rodent tumors: Morphologic characterization of intratumoral vasculature,” J. Magn. Reson. Imaging 18(1), 59–65 (2003).
[Crossref] [PubMed]

2001 (1)

H. Kämpfer, J. Pfeilschifter, and S. Frank, “Expressional regulation of angiopoietin-1 and -2 and the tie-1 and -2 receptor tyrosine kinases during cutaneous wound healing: a comparative study of normal and impaired repair,” Lab. Invest. 81(3), 361–373 (2001).
[Crossref] [PubMed]

1996 (1)

J. Xiong, A. Kurz, D. I. Sessler, O. Plattner, R. Christensen, M. Dechert, and T. Ikeda, “Isoflurane produces marked and nonlinear decreases in the vasoconstriction and shivering thresholds,” Anesthesiology 85(2), 240–245 (1996).
[Crossref] [PubMed]

1993 (1)

H. A. Lehr, M. Leunig, M. D. Menger, D. Nolte, and K. Messmer, “Dorsal skinfold chamber technique for intravital microscopy in nude mice,” Am. J. Pathol. 143(4), 1055–1062 (1993).
[PubMed]

1992 (1)

D. I. Sessler, J. McGuire, J. Hynson, A. Moayeri, and T. Heier, “Thermoregulatory vasoconstriction during isoflurane anesthesia minimally decreases cutaneous heat loss,” Anesthesiology 76(5), 670–675 (1992).
[Crossref] [PubMed]

1984 (1)

L. S. Hansen, J. E. Coggle, J. Wells, and M. W. Charles, “The influence of the hair cycle on the thickness of mouse skin,” Anat. Rec. 210(4), 569–573 (1984).
[Crossref] [PubMed]

1979 (1)

N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst. Man Cybern. 9(1), 62–66 (1979).
[Crossref]

1963 (1)

M. P. Wiedeman, “Dimensions of blood vessels from distributing artery to collecting vein,” Circ. Res. 12(4), 375–378 (1963).
[Crossref] [PubMed]

Akerman, S.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Baran, U.

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

Barber, P. R.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Benagiano, V.

B. Nico, V. Benagiano, D. Mangieri, N. Maruotti, A. Vacca, and D. Ribatti, “Evaluation of microvascular density in tumors: pro and contra,” Histol. Histopathol. 23(5), 601–607 (2008).
[PubMed]

Beziere, N.

A. Chekkoury, A. Nunes, J. Gateau, P. Symvoulidis, A. Feuchtinger, N. Beziere, S. V. Ovsepian, A. Walch, and V. Ntziachristos, “High-Resolution Multispectral Optoacoustic Tomography of the Vascularization and Constitutive Hypoxemia of Cancerous Tumors,” Neoplasia 18(8), 459–467 (2016).
[Crossref] [PubMed]

Biel, N. M.

N. M. Biel, J. A. Lee, B. S. Sorg, and D. W. Siemann, “Limitations of the dorsal skinfold window chamber model in evaluating anti-angiogenic therapy during early phase of angiogenesis,” Vasc Cell 6(1), 17 (2014).
[Crossref] [PubMed]

Bigio, I. J.

K. Calabro, A. Curtis, J.-R. Galarneau, T. Krucker, and I. J. Bigio, “Gender variations in the optical properties of skin in murine animal models,” J. Biomed. Opt. 16(1), 011008 (2011).
[Crossref] [PubMed]

Björndahl, M. A.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Bock, M.

F. Kiessling, S. Greschus, M. P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M. M. Mueller, N. E. Fusenig, H. Traupe, and W. Semmler, “Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis,” Nat. Med. 10(10), 1133–1138 (2004).
[Crossref] [PubMed]

C. Fink, F. Kiessling, M. Bock, M. P. Lichy, B. Misselwitz, P. Peschke, N. E. Fusenig, R. Grobholz, and S. Delorme, “High-resolution three-dimensional MR angiography of rodent tumors: Morphologic characterization of intratumoral vasculature,” J. Magn. Reson. Imaging 18(1), 59–65 (2003).
[Crossref] [PubMed]

Boucher, Y.

S. Goel, D. G. Duda, L. Xu, L. L. Munn, Y. Boucher, D. Fukumura, and R. K. Jain, “Normalization of the Vasculature for Treatment of Cancer and Other Diseases,” Physiol. Rev. 91(3), 1071–1121 (2011).
[Crossref] [PubMed]

Bouma, B. E.

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]

Calabro, K.

K. Calabro, A. Curtis, J.-R. Galarneau, T. Krucker, and I. J. Bigio, “Gender variations in the optical properties of skin in murine animal models,” J. Biomed. Opt. 16(1), 011008 (2011).
[Crossref] [PubMed]

Carmeliet, P.

P. Carmeliet and R. K. Jain, “Molecular mechanisms and clinical applications of angiogenesis,” Nature 473(7347), 298–307 (2011).
[Crossref] [PubMed]

Charles, M. W.

L. S. Hansen, J. E. Coggle, J. Wells, and M. W. Charles, “The influence of the hair cycle on the thickness of mouse skin,” Anat. Rec. 210(4), 569–573 (1984).
[Crossref] [PubMed]

Chekkoury, A.

A. Chekkoury, A. Nunes, J. Gateau, P. Symvoulidis, A. Feuchtinger, N. Beziere, S. V. Ovsepian, A. Walch, and V. Ntziachristos, “High-Resolution Multispectral Optoacoustic Tomography of the Vascularization and Constitutive Hypoxemia of Cancerous Tumors,” Neoplasia 18(8), 459–467 (2016).
[Crossref] [PubMed]

Christensen, R.

J. Xiong, A. Kurz, D. I. Sessler, O. Plattner, R. Christensen, M. Dechert, and T. Ikeda, “Isoflurane produces marked and nonlinear decreases in the vasoconstriction and shivering thresholds,” Anesthesiology 85(2), 240–245 (1996).
[Crossref] [PubMed]

Coggle, J. E.

L. S. Hansen, J. E. Coggle, J. Wells, and M. W. Charles, “The influence of the hair cycle on the thickness of mouse skin,” Anat. Rec. 210(4), 569–573 (1984).
[Crossref] [PubMed]

Coralli-Foxon, C.

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

Cross, N. A.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Curtis, A.

K. Calabro, A. Curtis, J.-R. Galarneau, T. Krucker, and I. J. Bigio, “Gender variations in the optical properties of skin in murine animal models,” J. Biomed. Opt. 16(1), 011008 (2011).
[Crossref] [PubMed]

Dachs, G. U.

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

Davis, W. O.

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

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K. Calabro, A. Curtis, J.-R. Galarneau, T. Krucker, and I. J. Bigio, “Gender variations in the optical properties of skin in murine animal models,” J. Biomed. Opt. 16(1), 011008 (2011).
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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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H. A. Lehr, M. Leunig, M. D. Menger, D. Nolte, and K. Messmer, “Dorsal skinfold chamber technique for intravital microscopy in nude mice,” Am. J. Pathol. 143(4), 1055–1062 (1993).
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D. I. Sessler, J. McGuire, J. Hynson, A. Moayeri, and T. Heier, “Thermoregulatory vasoconstriction during isoflurane anesthesia minimally decreases cutaneous heat loss,” Anesthesiology 76(5), 670–675 (1992).
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T. Jeswani and A. R. Padhani, “Imaging tumour angiogenesis,” Cancer Imaging 5(1), 131–138 (2005).
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G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
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H. Kämpfer, J. Pfeilschifter, and S. Frank, “Expressional regulation of angiopoietin-1 and -2 and the tie-1 and -2 receptor tyrosine kinases during cutaneous wound healing: a comparative study of normal and impaired repair,” Lab. Invest. 81(3), 361–373 (2001).
[Crossref] [PubMed]

Plattner, O.

J. Xiong, A. Kurz, D. I. Sessler, O. Plattner, R. Christensen, M. Dechert, and T. Ikeda, “Isoflurane produces marked and nonlinear decreases in the vasoconstriction and shivering thresholds,” Anesthesiology 85(2), 240–245 (1996).
[Crossref] [PubMed]

Prise, V. E.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Qi, X.

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

Qin, W.

Reyes-Aldasoro, C. C.

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Ribatti, D.

B. Nico, V. Benagiano, D. Mangieri, N. Maruotti, A. Vacca, and D. Ribatti, “Evaluation of microvascular density in tumors: pro and contra,” Histol. Histopathol. 23(5), 601–607 (2008).
[PubMed]

Ruhrberg, C.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Semmler, W.

F. Kiessling, S. Greschus, M. P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M. M. Mueller, N. E. Fusenig, H. Traupe, and W. Semmler, “Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis,” Nat. Med. 10(10), 1133–1138 (2004).
[Crossref] [PubMed]

Sessler, D. I.

J. Xiong, A. Kurz, D. I. Sessler, O. Plattner, R. Christensen, M. Dechert, and T. Ikeda, “Isoflurane produces marked and nonlinear decreases in the vasoconstriction and shivering thresholds,” Anesthesiology 85(2), 240–245 (1996).
[Crossref] [PubMed]

D. I. Sessler, J. McGuire, J. Hynson, A. Moayeri, and T. Heier, “Thermoregulatory vasoconstriction during isoflurane anesthesia minimally decreases cutaneous heat loss,” Anesthesiology 76(5), 670–675 (1992).
[Crossref] [PubMed]

Shima, D. T.

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Siemann, D. W.

N. M. Biel, J. A. Lee, B. S. Sorg, and D. W. Siemann, “Limitations of the dorsal skinfold window chamber model in evaluating anti-angiogenic therapy during early phase of angiogenesis,” Vasc Cell 6(1), 17 (2014).
[Crossref] [PubMed]

Sorg, B. S.

N. M. Biel, J. A. Lee, B. S. Sorg, and D. W. Siemann, “Limitations of the dorsal skinfold window chamber model in evaluating anti-angiogenic therapy during early phase of angiogenesis,” Vasc Cell 6(1), 17 (2014).
[Crossref] [PubMed]

Sorzano, C. O. S.

C. O. S. Sorzano, P. Thévenaz, and M. Unser, “Elastic Registration of Biological Images Using Vector-Spline Regularization,” IEEE Trans. Biomed. Eng. 52(4), 652–663 (2005).
[Crossref] [PubMed]

Standish, B. A.

Steele, A. J.

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

Stylianopoulos, T.

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]

Symvoulidis, P.

A. Chekkoury, A. Nunes, J. Gateau, P. Symvoulidis, A. Feuchtinger, N. Beziere, S. V. Ovsepian, A. Walch, and V. Ntziachristos, “High-Resolution Multispectral Optoacoustic Tomography of the Vascularization and Constitutive Hypoxemia of Cancerous Tumors,” Neoplasia 18(8), 459–467 (2016).
[Crossref] [PubMed]

Tearney, G. J.

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]

Thévenaz, P.

C. O. S. Sorzano, P. Thévenaz, and M. Unser, “Elastic Registration of Biological Images Using Vector-Spline Regularization,” IEEE Trans. Biomed. Eng. 52(4), 652–663 (2005).
[Crossref] [PubMed]

Thurman, S. T.

Tozer, G. M.

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Traupe, H.

F. Kiessling, S. Greschus, M. P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M. M. Mueller, N. E. Fusenig, H. Traupe, and W. Semmler, “Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis,” Nat. Med. 10(10), 1133–1138 (2004).
[Crossref] [PubMed]

Tyrrell, J. 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).
[Crossref] [PubMed]

Unser, M.

C. O. S. Sorzano, P. Thévenaz, and M. Unser, “Elastic Registration of Biological Images Using Vector-Spline Regularization,” IEEE Trans. Biomed. Eng. 52(4), 652–663 (2005).
[Crossref] [PubMed]

Vacca, A.

B. Nico, V. Benagiano, D. Mangieri, N. Maruotti, A. Vacca, and D. Ribatti, “Evaluation of microvascular density in tumors: pro and contra,” Histol. Histopathol. 23(5), 601–607 (2008).
[PubMed]

Vakoc, B. J.

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]

Vitkin, A.

Vosseler, S.

F. Kiessling, S. Greschus, M. P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M. M. Mueller, N. E. Fusenig, H. Traupe, and W. Semmler, “Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis,” Nat. Med. 10(10), 1133–1138 (2004).
[Crossref] [PubMed]

Walch, A.

A. Chekkoury, A. Nunes, J. Gateau, P. Symvoulidis, A. Feuchtinger, N. Beziere, S. V. Ovsepian, A. Walch, and V. Ntziachristos, “High-Resolution Multispectral Optoacoustic Tomography of the Vascularization and Constitutive Hypoxemia of Cancerous Tumors,” Neoplasia 18(8), 459–467 (2016).
[Crossref] [PubMed]

Wang, J.

Wang, R. K.

D. W. Wei, A. J. Deegan, and R. K. Wang, “Automatic motion correction for in vivo human skin optical coherence tomography angiography through combined rigid and nonrigid registration,” J. Biomed. Opt. 22(6), 066013 (2017).
[Crossref] [PubMed]

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

Z. Zhi, W. Qin, J. Wang, W. Wei, and R. K. Wang, “4D optical coherence tomography-based micro-angiography achieved by 1.6-MHz FDML swept source,” Opt. Lett. 40(8), 1779–1782 (2015).
[Crossref] [PubMed]

Wei, D. W.

D. W. Wei, A. J. Deegan, and R. K. Wang, “Automatic motion correction for in vivo human skin optical coherence tomography angiography through combined rigid and nonrigid registration,” J. Biomed. Opt. 22(6), 066013 (2017).
[Crossref] [PubMed]

Wei, W.

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

Z. Zhi, W. Qin, J. Wang, W. Wei, and R. K. Wang, “4D optical coherence tomography-based micro-angiography achieved by 1.6-MHz FDML swept source,” Opt. Lett. 40(8), 1779–1782 (2015).
[Crossref] [PubMed]

Weinberg, R. A.

D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell 144(5), 646–674 (2011).
[Crossref] [PubMed]

Wells, J.

L. S. Hansen, J. E. Coggle, J. Wells, and M. W. Charles, “The influence of the hair cycle on the thickness of mouse skin,” Anat. Rec. 210(4), 569–573 (1984).
[Crossref] [PubMed]

Wiedeman, M. P.

M. P. Wiedeman, “Dimensions of blood vessels from distributing artery to collecting vein,” Circ. Res. 12(4), 375–378 (1963).
[Crossref] [PubMed]

Wilson, B. C.

Xiong, J.

J. Xiong, A. Kurz, D. I. Sessler, O. Plattner, R. Christensen, M. Dechert, and T. Ikeda, “Isoflurane produces marked and nonlinear decreases in the vasoconstriction and shivering thresholds,” Anesthesiology 85(2), 240–245 (1996).
[Crossref] [PubMed]

Xu, J.

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

Xu, L.

S. Goel, D. G. Duda, L. Xu, L. L. Munn, Y. Boucher, D. Fukumura, and R. K. Jain, “Normalization of the Vasculature for Treatment of Cancer and Other Diseases,” Physiol. Rev. 91(3), 1071–1121 (2011).
[Crossref] [PubMed]

Yang, V. X.

Zhi, Z.

Ziólkowski, P.

K. Jurczyszyn, B. J. Osiecka, and P. Ziółkowski, “The Use of Fractal Dimension Analysis in Estimation of Blood Vessels Shape in Transplantable Mammary Adenocarcinoma in Wistar Rats after Photodynamic Therapy Combined with Cysteine Protease Inhibitors,” Comput. Math. Methods Med. 2012, 1–6 (2012).
[Crossref]

Am. J. Pathol. (1)

H. A. Lehr, M. Leunig, M. D. Menger, D. Nolte, and K. Messmer, “Dorsal skinfold chamber technique for intravital microscopy in nude mice,” Am. J. Pathol. 143(4), 1055–1062 (1993).
[PubMed]

Anat. Rec. (1)

L. S. Hansen, J. E. Coggle, J. Wells, and M. W. Charles, “The influence of the hair cycle on the thickness of mouse skin,” Anat. Rec. 210(4), 569–573 (1984).
[Crossref] [PubMed]

Anesthesiology (2)

J. Xiong, A. Kurz, D. I. Sessler, O. Plattner, R. Christensen, M. Dechert, and T. Ikeda, “Isoflurane produces marked and nonlinear decreases in the vasoconstriction and shivering thresholds,” Anesthesiology 85(2), 240–245 (1996).
[Crossref] [PubMed]

D. I. Sessler, J. McGuire, J. Hynson, A. Moayeri, and T. Heier, “Thermoregulatory vasoconstriction during isoflurane anesthesia minimally decreases cutaneous heat loss,” Anesthesiology 76(5), 670–675 (1992).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Cancer Imaging (1)

T. Jeswani and A. R. Padhani, “Imaging tumour angiogenesis,” Cancer Imaging 5(1), 131–138 (2005).
[Crossref] [PubMed]

Cancer Res. (1)

G. M. Tozer, S. Akerman, N. A. Cross, P. R. Barber, M. A. Björndahl, O. Greco, S. Harris, S. A. Hill, D. J. Honess, C. R. Ireson, K. L. Pettyjohn, V. E. Prise, C. C. Reyes-Aldasoro, C. Ruhrberg, D. T. Shima, and C. Kanthou, “Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform-producing tumors,” Cancer Res. 68(7), 2301–2311 (2008).
[Crossref] [PubMed]

Cell (1)

D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell 144(5), 646–674 (2011).
[Crossref] [PubMed]

Circ. Res. (1)

M. P. Wiedeman, “Dimensions of blood vessels from distributing artery to collecting vein,” Circ. Res. 12(4), 375–378 (1963).
[Crossref] [PubMed]

Comput. Math. Methods Med. (1)

K. Jurczyszyn, B. J. Osiecka, and P. Ziółkowski, “The Use of Fractal Dimension Analysis in Estimation of Blood Vessels Shape in Transplantable Mammary Adenocarcinoma in Wistar Rats after Photodynamic Therapy Combined with Cysteine Protease Inhibitors,” Comput. Math. Methods Med. 2012, 1–6 (2012).
[Crossref]

Histol. Histopathol. (1)

B. Nico, V. Benagiano, D. Mangieri, N. Maruotti, A. Vacca, and D. Ribatti, “Evaluation of microvascular density in tumors: pro and contra,” Histol. Histopathol. 23(5), 601–607 (2008).
[PubMed]

IEEE Trans. Biomed. Eng. (1)

C. O. S. Sorzano, P. Thévenaz, and M. Unser, “Elastic Registration of Biological Images Using Vector-Spline Regularization,” IEEE Trans. Biomed. Eng. 52(4), 652–663 (2005).
[Crossref] [PubMed]

IEEE Trans. Syst. Man Cybern. (1)

N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst. Man Cybern. 9(1), 62–66 (1979).
[Crossref]

J. Biomed. Opt. (2)

D. W. Wei, A. J. Deegan, and R. K. Wang, “Automatic motion correction for in vivo human skin optical coherence tomography angiography through combined rigid and nonrigid registration,” J. Biomed. Opt. 22(6), 066013 (2017).
[Crossref] [PubMed]

K. Calabro, A. Curtis, J.-R. Galarneau, T. Krucker, and I. J. Bigio, “Gender variations in the optical properties of skin in murine animal models,” J. Biomed. Opt. 16(1), 011008 (2011).
[Crossref] [PubMed]

J. Magn. Reson. Imaging (1)

C. Fink, F. Kiessling, M. Bock, M. P. Lichy, B. Misselwitz, P. Peschke, N. E. Fusenig, R. Grobholz, and S. Delorme, “High-resolution three-dimensional MR angiography of rodent tumors: Morphologic characterization of intratumoral vasculature,” J. Magn. Reson. Imaging 18(1), 59–65 (2003).
[Crossref] [PubMed]

Lab. Invest. (1)

H. Kämpfer, J. Pfeilschifter, and S. Frank, “Expressional regulation of angiopoietin-1 and -2 and the tie-1 and -2 receptor tyrosine kinases during cutaneous wound healing: a comparative study of normal and impaired repair,” Lab. Invest. 81(3), 361–373 (2001).
[Crossref] [PubMed]

Nat. Med. (2)

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]

F. Kiessling, S. Greschus, M. P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M. M. Mueller, N. E. Fusenig, H. Traupe, and W. Semmler, “Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis,” Nat. Med. 10(10), 1133–1138 (2004).
[Crossref] [PubMed]

Nature (1)

P. Carmeliet and R. K. Jain, “Molecular mechanisms and clinical applications of angiogenesis,” Nature 473(7347), 298–307 (2011).
[Crossref] [PubMed]

Neoplasia (1)

A. Chekkoury, A. Nunes, J. Gateau, P. Symvoulidis, A. Feuchtinger, N. Beziere, S. V. Ovsepian, A. Walch, and V. Ntziachristos, “High-Resolution Multispectral Optoacoustic Tomography of the Vascularization and Constitutive Hypoxemia of Cancerous Tumors,” Neoplasia 18(8), 459–467 (2016).
[Crossref] [PubMed]

Opt. Eng. (1)

U. Baran, W. Wei, J. Xu, X. Qi, W. O. Davis, and R. K. Wang, “Video-rate volumetric optical coherence tomography-based microangiography,” Opt. Eng. 55(4), 040503 (2016).
[Crossref]

Opt. Lett. (3)

Physiol. Rev. (1)

S. Goel, D. G. Duda, L. Xu, L. L. Munn, Y. Boucher, D. Fukumura, and R. K. Jain, “Normalization of the Vasculature for Treatment of Cancer and Other Diseases,” Physiol. Rev. 91(3), 1071–1121 (2011).
[Crossref] [PubMed]

PLoS One (1)

C. Kanthou, G. U. Dachs, D. V. Lefley, A. J. Steele, C. Coralli-Foxon, S. Harris, O. Greco, S. A. Dos Santos, C. C. Reyes-Aldasoro, W. R. English, and G. M. Tozer, “Tumour Cells Expressing Single VEGF Isoforms Display Distinct Growth, Survival and Migration Characteristics,” PLoS One 9(8), e104015 (2014).
[Crossref] [PubMed]

Vasc Cell (1)

N. M. Biel, J. A. Lee, B. S. Sorg, and D. W. Siemann, “Limitations of the dorsal skinfold window chamber model in evaluating anti-angiogenic therapy during early phase of angiogenesis,” Vasc Cell 6(1), 17 (2014).
[Crossref] [PubMed]

Other (4)

W. R. English, S. J. Lunt, M. Fisher, D. V. Lefley, M. Dhingra, Y.-C. Lee, K. Bingham, J. E. Hurrell, S. K. Lyons, C. Kanthou, and G. M. Tozer, “Differential Expression of VEGFA Isoforms Regulates Metastasis and Response to Anti-VEGFA Therapy in Sarcoma,” Cancer Res., p. canres.0255.2016, (2017).

A. Puaux, L. C. Ong, Y. Jin, I. Teh, M. Hong, P. K. H. Chow, X. Golay, and J. Abastado, “A Comparison of Imaging Techniques to Monitor Tumor Growth and Cancer Progression in Living Animals,” vol. 2011, (2011).

R. A. Byers, G. Tozer, N. J. Brown, and S. J. Matcher, “High-resolution label-free vascular imaging using a commercial, clinically approved dermatological OCT scanner,” in SPIE BiOS, (2016).

A. F. Frangi, W. J. Niessen, K. L. Vincken, and M. A. Viergever, “Multiscale vessel enhancement filtering,” vol. 1496, pp. 130–137, (1998).

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Figures (10)

Fig. 1
Fig. 1 Experimental setup within a plastic chamber which was heated to 32°C internal temperature. A) Rodent facemask for administration of isoflurane gaseous anesthesia. B) CD-1 Nude mouse. C) Plastic standoff which gently contacts the skin around the subcutaneous tumor. D) The OCT imaging probe (Vivosight). E) Feedback controlled heated mat. F) Rectal temperature probe (Feeds back to the heated mat). G) Mobile clamp for repositioning of the OCT imaging probe.
Fig. 2
Fig. 2 En-face svOCT images of an fs188 tumor before (Left) and after (Right) wavelet/FFT filtering was performed using a Daubechies wavelet to a decomposition level of 5. The colors correspond to the depth of the detected vessels, red vessels are 0-300μm and green vessels are 300-600μm beneath the skin surface.
Fig. 3
Fig. 3 Processing steps for the quantification of svOCT data. A) En-face svOCT image captured from a subcutaneous fs-120 tumor 17 days post-implantation. Dashed box shows zoomed section from B-G. B) Zoomed section of the en-face svOCT image. C) The result of the hessian-based filtering algorithm. D) The result of B*C, improved vascular contrast against the background. E) Binary threshold in green overlaid on the original image. F) Skeleton in blue overlaid on the original image. G) Map of vessel diameter calculated using the binary threshold and the skeleton data from E and F.
Fig. 4
Fig. 4 A selection of 6x6mm en-face svOCT images. A-D) Images of baseline murine skin vasculature without the presence of a tumor. E-L) Images of established subcutaneous tumor vasculature, each image is of a separate tumor captured once the largest tumor diameter exceeded 10mm. Middle row (E-H) shows tumors expressing only the VEGF120 isoform (fs120) and bottom row (I-L) shows tumors expressing only the VEGF188 isoform (fs188). All images were captured from different animals. The colors correspond to the depth of the detected vessels, red vessels are 0-400μm and green vessels are 400-800μm beneath the skin surface. E-L) Number of days post-implantation > 14 days.
Fig. 5
Fig. 5 Top and middle rows) Depth encoded short-term longitudinal svOCT images of both an fs120 and an fs188 tumor over a period of 5 days. Images have been elastically registered together using UnwarpJ [23] such that the same vessels align on subsequent frames. Bottom row) 4x4mm (Zoomed) en-face svOCT images showing long-term longitudinal vascular progression from pre- tumor implantation to 15-days post- tumor implantation. Each separate row represents longitudinal data that was captured from one unique animal. The colors correspond to the depth of the detected vessels, red vessels are 0-400μm and green vessels are 400-800μm beneath the skin surface. The white number in the lower left corner of each image corresponds to the number of days post-tumor implantation that the image was captured.
Fig. 6
Fig. 6 Line plots showing the variation in measured vessel length per square mm as a function of time within subcutaneous tumors expressing either the VEGF120 isoform (blue) or the VEGF188 isoform (red). The standard deviation in the measured mean vessel length for each animal is calculated as a function of time, and represents how much variance is visible within the measurement. The average of these standard deviations across all four fs120 mice (1.4mm−1) is higher than those in the fs188 cohort (0.4mm−1), however this result does not reach statistical significance (p = 0.063).
Fig. 7
Fig. 7 Comparing the depth penetration of OCT against histological sections of murine rear-dorsum skin. A) H&E stained section of healthy skin. B) OCT B-scan of healthy skin (Different animal to A). C) H&E stained section of the skin above an fs120 tumor, showing the lack of the muscular layer. D) OCT B-scan of the skin above an fs120 tumor (Same animal as C). E) H&E stained section of skin with an fs188 tumor visible beneath the muscular (panniculus carnosus) layer of the skin. F) OCT B-scan of the skin above an fs188 tumor (Same animal as E).
Fig. 8
Fig. 8 Variation in the thickness of the hypodermis (fat) layer within healthy skin compared to that of the skin encapsulating ~12mm diameter fs188 and fs120 tumors. The fatty layer is significantly thicker in healthy skin than both fs188 and fs120 skin, furthermore this layer is also significantly thicker in fs188 skin than fs120 skin. A thicker fat layer appears to correlate with an increase in the number of hair follicles present, reducing the depth penetration of the OCT imaging beam. (columns, mean; bars, standard deviation; crosses, datapoints). All groups contain n = 7 samples, significance calculated using a one-way ANOVA followed by a Tukey-Kramer HSD test.
Fig. 9
Fig. 9 CD31 immunohistochemistry demonstrating the presence of endothelial cells lining the vessels within the rear-dorsum skin of CD1 nude mice. A-C) H&E stained serial sections of healthy, fs120 and fs188 skin respectively. D-F) CD31 immunostained serial sections of healthy, fs120 and fs188 skin respectively. Endothelial cells are stained in brown. Red arrows represent the largest visible vessel lumen. Red boxes represent the zoomed sections from G-I. G-I) Zoomed view of vessels within the hypodermis of the CD31 stained sections. The fs120 tumor shown here was excised 14 days post-implantation and is a different tumor to the one shown in Fig. 9. The fs188 tumor shown here was excised 20 days post-implantation, and is the same tumor shown in Fig. 9.
Fig. 10
Fig. 10 The variation in quantitative vessel parameters between fs120 tumors (n = 9) and fs188 tumors (n = 8) at the study endpoint. Columns: The average value of each respective quantitative parameter across the entire fs120 or fs188 group. (bars, standard deviation). Statistical significance calculated using an independent two-sample t-test between the fs120 and fs188 data sets.

Equations (1)

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SV(x,y,z)=median((I(x,y,z,n) 1 k n=1 k I(x,y,z,n) ) 2 )

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