Abstract

Hyperspectral imaging of hemoglobin (Hb) saturation and first-pass fluorescence imaging of blood transit time were combined to analyze the oxygenation of and blood flow through microvessel networks. The combination imaging technique was demonstrated in a mouse dorsal window chamber model of a growing Caki-2 human renal cell carcinoma over time. Data from Hb saturation and blood supply time maps show the formation of arteriovenous malformations and shunting of blood directly from arteries to the tumor core and into veins in the periphery of the tumor. Images and data analysis show these malformations result in an oxygenated environment ideal for a tumor to proliferate.

© 2013 Optical Society of America

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References

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  1. P. Carmeliet, J. Intern. Med. 255, 538 (2004).
    [Crossref]
  2. S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
    [Crossref]
  3. M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
    [Crossref]
  4. K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
    [Crossref]
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    [Crossref]
  6. A. D. Bangham, M. M. Standish, and J. C. Watkens, J. Mol. Biol. 13, 238 (1965).
    [Crossref]
  7. S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
    [Crossref]

2010 (2)

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
[Crossref]

2009 (1)

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

2008 (1)

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

2005 (1)

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

2004 (1)

P. Carmeliet, J. Intern. Med. 255, 538 (2004).
[Crossref]

1965 (1)

A. D. Bangham, M. M. Standish, and J. C. Watkens, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Bangham, A. D.

A. D. Bangham, M. M. Standish, and J. C. Watkens, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Brurberg, K. G.

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Cao, Y.

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

Carmeliet, P.

P. Carmeliet, J. Intern. Med. 255, 538 (2004).
[Crossref]

Choe, S.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Coll, J. L.

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

Dedeugd, C.

M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
[Crossref]

Dewhirst, M. W.

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

Donovan, O.

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

Dufort, S.

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

Gaustad, J. V.

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Graff, B. A.

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Gulati, G.

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Josserand, V.

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

Lee, Y. J.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Moeller, B. J.

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

Oh, S.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Oh, S. P.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Oye, K. S.

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Park, S. O.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Raizada, M. K.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Rofstad, E. K.

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Sancey, L.

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

Siemann, D. W.

M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
[Crossref]

Sorg, B. S.

M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
[Crossref]

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

Standish, M. M.

A. D. Bangham, M. M. Standish, and J. C. Watkens, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Walter, G.

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Wankhede, M.

M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
[Crossref]

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

Watkens, J. C.

A. D. Bangham, M. M. Standish, and J. C. Watkens, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Wenk, C.

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

Biochim. Biophys. Acta (1)

S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J. L. Coll, Biochim. Biophys. Acta 1798, 2266 (2010).
[Crossref]

J. Biomed. Opt. (1)

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, J. Biomed. Opt. 10, 044004 (2005).
[Crossref]

J. Clin. Invest. (1)

S. O. Park, M. Wankhede, Y. J. Lee, S. Choe, S. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, J. Clin. Invest. 119, 3487 (2009).
[Crossref]

J. Intern. Med. (1)

P. Carmeliet, J. Intern. Med. 255, 538 (2004).
[Crossref]

J. Mol. Biol. (1)

A. D. Bangham, M. M. Standish, and J. C. Watkens, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Microvasc. Res. (1)

K. S. Oye, G. Gulati, B. A. Graff, J. V. Gaustad, K. G. Brurberg, and E. K. Rofstad, Microvasc. Res. 75, 179(2008).
[Crossref]

Oncol. Rep. (1)

M. Wankhede, C. Dedeugd, D. W. Siemann, and B. S. Sorg, Oncol. Rep. 23, 685 (2010).
[Crossref]

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Figures (2)

Fig. 1.
Fig. 1. Analysis of a Caki-2 tumor over 4 days. (a) Bright-field images. The supplying artery (SA) and draining vein (DV) of interest are indicated. (b) Full Hb saturation and (c) BST maps with magnified region of interest indicate the development of AV malformations. Venous branches carrying blood from systemic flow [arrowhead symbol in lower left of (b)] and shunted tumor blood flow [arrow symbol in lower left of (b)] are indicated.

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Fig. 2.
Fig. 2. (a) ROIs chosen for comparison of BST and Hb saturation. (b) Hb saturation versus BST over time (mean ± standard deviation) for ROIs seen in (a). (c) Comparison of mean values of BST and Hb saturation for ROIs 6, 7, and 8 over time (mean ± standard deviation).

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