Abstract

The longitudinal effect of an anti-vascular endothelial growth factor receptor 2 (VEGFR-2) antibody (DC 101) therapy on a xenografted renal cell carcinoma (RCC) mouse model was monitored using hybrid diffuse optics. Two groups of immunosuppressed male nude mice (seven treated, seven controls) were measured. Tumor microvascular blood flow, total hemoglobin concentration and blood oxygenation were investigated as potential biomarkers for the monitoring of the therapy effect twice a week and were related to the final treatment outcome. These hemodynamic biomarkers have shown a clear differentiation between two groups by day four. Moreover, we have observed that pre-treatment values and early changes in hemodynamics are highly correlated with the therapeutic outcome demonstrating the potential of diffuse optics to predict the therapy response at an early time point.

© 2017 Optical Society of America

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  88. L. Dong, M. Kudrimoti, D. Irwin, L. Chen, S. Kumar, Y. Shang, C. Huang, E. L. Johnson, S. D. Stevens, B. J. Shelton, and G. Yu, “Diffuse optical measurements of Head Neck tumor hemodynamics for early prediction of chemoradiation therapy outcomes,” J. Biomed. Opt. 21(8), 085004 (2016).
    [Crossref]
  89. G. Yu, T. Durduran, C. Zhou, T. C. Zhu, J. C. Finlay, T. M. Busch, S. B. Malkowicz, S. M. Hahn, and A. G. Yodh, “Real-time in situ monitoring of human prostate photodynamic therapy with diffuse light,” Photochem. Photobiol. 82(5), 1279–1284 (2007).
    [Crossref]
  90. H. W. Wechsel, K. H. Bichler, G. Feil, W. Loeser, S. Lahme, and E. Petri, “Renal cell carcinoma: relevance of angiogenetic factors,” Anticancer Res. 19(2C), 1537–1540 (1999).
    [PubMed]
  91. J. Jacobsen, K. Grankvist, T. Rasmuson, A. Bergh, G. Landberg, and B. Ljungberg, “Expression of vascular endothelial growth factor protein in human renal cell carcinoma,” BJU Int. 93(3), 297–302 (2004).
    [Crossref] [PubMed]
  92. R. K. Jain, “Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy,” Science 307(5706), 58–62 (2005).
    [Crossref] [PubMed]
  93. J. Johansson, M. Mireles, J. Morales, P. Farzam, M. Martínez, O. Casanovas, and T. Durduran, “Scanning, non-contact, hybrid broadband diffuse optical spectroscopy and diffuse correlation spectroscopy system,” Biomedical Opt. Express 7(2), 481 (2016).
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2016 (9)

I. Duran, J. Lambea, P. Maroto, J. L. González-Larriba, L. Flores, S. Granados-Principal, M. Graupera, B. Sáez, A. Vivancos, and O. Casanovas, “Resistance to Targeted Therapies in Renal Cancer: The Importance of Changing the Mechanism of Action,” Target. Oncol. 12, 19–35 (2016).
[Crossref] [PubMed]

C. Errico, B. F. Osmanski, S. Pezet, O. Couture, Z. Lenkei, and M. Tanter, “Transcranial functional ultrasound imaging of the brain using microbubble-enhanced ultrasensitive Doppler,” NeuroImage 124, 752–761 (2016).
[Crossref]

F. Martelli, T. Binzoni, A. Pifferi, L. Spinelli, A. Farina, and A. Torricelli, “There’s plenty of light at the bottom: statistics of photon penetration depth in random media,” Sci. Rep. 6(1), 27057 (2016).
[Crossref]

G. Jiménez-Valerio, M. Martínez-Lozano, N. Bassani, A. Vidal, M. Ochoa-de Olza, C. Suárez, X. García-del Muro, J. Carles, F. Viñals, M. Graupera, S. Indraccolo, and O. Casanovas, “Resistance to Antiangiogenic Therapies by Metabolic Symbiosis in Renal Cell Carcinoma PDX Models and Patients,” Cell Reports 15(6), 1134–1143 (2016).
[Crossref] [PubMed]

D. Boas, S. Sakadžic, J. Selb, P. Farzam, M. Franceschini, and S. Carp, “Establishing the diffuse correlation spectroscopy signal relationship with blood flow,” Neurophotonics 3(3), 031412 (2016).
[Crossref] [PubMed]

D. Rohrbach, H. Salem, M. Aksahin, and U. Sunar, “Photodynamic Therapy-Induced Microvascular Changes in a Nonmelanoma Skin Cancer Model Assessed by Photoacoustic Microscopy and Diffuse Correlation Spectroscopy,” Photonics 3(3), 48 (2016).
[Crossref]

L. Dong, M. Kudrimoti, D. Irwin, L. Chen, S. Kumar, Y. Shang, C. Huang, E. L. Johnson, S. D. Stevens, B. J. Shelton, and G. Yu, “Diffuse optical measurements of Head Neck tumor hemodynamics for early prediction of chemoradiation therapy outcomes,” J. Biomed. Opt. 21(8), 085004 (2016).
[Crossref]

G. Ramirez, A. Proctor, K. Jung, T. Wu, S. Han, R. Adams, J. Ren, D. Byun, K. Madden, E. Brown, T. Foster, P. Farzam, T. Durduran, and R. Choe, “Chemotherapeutic drug-specific alteration of microvascular blood flow in murine breast cancer as measured by diffuse correlation spectroscopy,” Biomedical Opt. Express 7(9), 3610 (2016).
[Crossref]

J. Johansson, M. Mireles, J. Morales, P. Farzam, M. Martínez, O. Casanovas, and T. Durduran, “Scanning, non-contact, hybrid broadband diffuse optical spectroscopy and diffuse correlation spectroscopy system,” Biomedical Opt. Express 7(2), 481 (2016).
[Crossref]

2015 (2)

T. M. Bydlon, R. Nachabé, N. Ramanujam, H. J. C. M. Sterenborg, and B. H. W. Hendriks, “Chromophore based analyses of steady-state diffuse reflectance spectroscopy: current status and perspectives for clinical adoption,” J. Biophotonics 8(1–2), 9–24 (2015).
[Crossref]

S. H. Chung, M. D. Feldman, D. Martinez, H. Kim, M. E. Putt, D. R. Busch, J. Tchou, B. J. Czerniecki, M. D. Schnall, M. A. Rosen, A. DeMichele, A. G. Yodh, and R. Choe, “Macroscopic optical physiological parameters correlate with microscopic proliferation and vessel area breast cancer signatures,” Breast Cancer Res. : BCR 17(1), 72 (2015).
[Crossref] [PubMed]

2014 (6)

M. Tanter and M. Fink, “Ultrafast imaging in biomedical ultrasound,” IEEE Trans. Ultrason., Ferroelect., Freq. Control 61(1), 102–119 (2014).
[Crossref]

J. Allen and K. Howell, “Microvascular imaging: techniques and opportunities for clinical physiological measurements,” Physiol. Meas. 35(7), R91–R141 (2014).
[Crossref] [PubMed]

C. Fontanella, E. Ongaro, S. Bolzonello, M. Guardascione, G. Fasola, and G. Aprile, “Clinical advances in the development of novel VEGFR2 inhibitors,” Ann. Transl. Med. 2(12), 123 (2014).

M. Braunagel, A. Graser, M. Reiser, and M. Notohamiprodjo, “The role of functional imaging in the era of targeted therapy of renal cell carcinoma,” World J. Urol. 32(1), 47–58 (2014).
[Crossref]

L. Moserle, G. Jiménez-Valerio, and O. Casanovas, “Antiangiogenic therapies: going beyond their limits,” Cancer Discov. 4(1), 31–41 (2014).
[Crossref]

R. Choe, M. E. Putt, P. M. Carlile, T. Durduran, J. M. Giammarco, D. R. Busch, K. W. Jung, B. J. Czerniecki, J. Tchou, M. D. Feldman, C. Mies, M. A. Rosen, M. D. Schnall, A. DeMichele, and A. G. Yodh, “Optically measured microvascular blood flow contrast of malignant breast tumors,” PLoS ONE 9(6), e99683 (2014).
[Crossref] [PubMed]

2013 (2)

D. R. Busch, R. Choe, T. Durduran, and A. G. Yodh, “Towards non-invasive characterization of breast cancer and cancer metabolism with diffuse optics,” PET clinics 8(3), 345–365 (2013).
[Crossref]

D. R. Busch, R. Choe, M. a. Rosen, W. Guo, T. Durduran, M. D. Feldman, C. Mies, B. J. Czerniecki, J. Tchou, A. Demichele, M. D. Schnall, and A. G. Yodh, “Optical malignancy parameters for monitoring progression of breast cancer neoadjuvant chemotherapy,” Biomedical Opt. Express 4(1), 105–121 (2013).
[Crossref]

2012 (5)

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

S. Ueda, D. Roblyer, A. Cerussi, A. Durkin, A. Leproux, Y. Santoro, S. Xu, T. D. O’Sullivan, D. Hsiang, R. Mehta, J. Butler, and B. J. Tromberg, “Baseline tumor oxygen saturation correlates with a pathologic complete response in breast cancer patients undergoing neoadjuvant chemotherapy,” Cancer Res. 72(17), 4318–4328 (2012).
[Crossref] [PubMed]

G. Yu, “Near-infrared diffuse correlation spectroscopy in cancer diagnosis and therapy monitoring,” J. Biomed. Opt. 17(1), 010901 (2012).
[Crossref] [PubMed]

T. M. Baran, J. D. Wilson, S. Mitra, J. L. Yao, E. M. Messing, D. L. Waldman, and T. H. Foster, “Optical property measurements establish the feasibility of photodynamic therapy as a minimally invasive intervention for tumors of the kidney,” J. Biomed. Opt. 17(9), 0980021 (2012).
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R. C. Mesquita, S. W. Han, J. Miller, S. S. Schenkel, A. Pole, T. V. Esipova, S. a. Vinogradov, M. E. Putt, A. G. Yodh, and T. M. Busch, “Tumor blood flow differs between mouse strains: Consequences for vasoresponse to photodynamic therapy,” PLoS ONE 7(5), 1–10 (2012).
[Crossref]

2011 (6)

J. H. Pinthus, K. F. Whelan, D. Gallino, J. P. Lu, and N. Rothschild, “Metabolic features of clear-cell renal cell carcinoma: Mechanisms and clinical implications,” Can. Urol. Assoc. J. 5(4), 274–282 (2011).
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D. Whitaker-Menezes, U. E. Martinez-Outschoorn, N. Flomenberg, R. Birbe, A. K. Witkiewicz, A. Howell, S. Pavlides, A. Tsirigos, A. Ertel, R. G. Pestell, P. Broda, C. Minetti, M. P. Lisanti, and F. Sotgia, “Hyperactivation of oxidative mitochondrial metabolism in epithelial Cancer Cells in situ,” Cell Cycle 10(23), 4047–4064 (2011).
[Crossref] [PubMed]

R. C. Mesquita, T. Durduran, G. Yu, E. M. Buckley, M. N. Kim, C. Zhou, R. Choe, U. Sunar, and A. G. Yodh, “Direct measurement of tissue blood flow and metabolism with diffuse optics,” Philos. Trans. A Math. Phys. Eng. Sci. 369(1955), 4390–4406 (2011).
[Crossref] [PubMed]

D. Zhang, E.-m. E. Hedlund, S. Lim, F. Chen, Y. Zhang, B. Sun, and Y. Cao, “Antiangiogenic agents significantly improve survival in tumor-bearing mice by increasing tolerance to chemotherapy-induced toxicity,” Proc. Natl. Acad. Sci. U.S.A. 108(10), 4117–4122 (2011).
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D. Roblyer, S. Ueda, A. Cerussi, W. Tanamai, A. Durkin, R. Mehta, D. Hsiang, J. a. Butler, C. McLaren, W.-P. Chen, and B. Tromberg, “Optical imaging of breast cancer oxyhemoglobin flare correlates with neoadjuvant chemotherapy response one day after starting treatment,” Proc. Natl. Acad. Sci. U.S.A. 108(35), 14626–31 (2011).
[Crossref] [PubMed]

C. Coppin, C. Kollmannsberger, L. Le, F. Porzsolt, and T. J. Wilt, “Targeted therapy for advanced renal cell cancer (RCC): a Cochrane systematic review of published randomised trials,” BJU Int. 108(10), 1556–1563 (2011).
[Crossref] [PubMed]

2010 (2)

T. L. Becker, A. D. Paquette, K. R. Keymel, B. W. Henderson, and U. Sunar, “Monitoring blood flow responses during topical ALA-PDT,” Biomedical Opt. Express 2(1), 123–130 (2010).
[Crossref]

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] [PubMed]

2009 (6)

M. Pàez-Ribes, E. Allen, J. Hudock, T. Takeda, H. Okuyama, F. Viñals, M. Inoue, G. Bergers, D. Hanahan, and O. Casanovas, “Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis,” Cancer Cell 15(3), 220–231 (2009).
[Crossref] [PubMed]

K. Vishwanath, D. Klein, K. Chang, T. Schroeder, M. W. Dewhirst, and N. Ramanujam, “Quantitative optical spectroscopy can identify long-term local tumor control in irradiated murine Head Neck xenografts,” J. Biomed. Opt. 14(5), 054051 (2009).
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R. K. Jain, D. G. Duda, C. G. Willett, D. V. Sahani, A. X. Zhu, J. S. Loeffler, T. T. Batchelor, and A. G. Sorensen, “Biomarkers of response and resistance to antiangiogenic therapy,” Nat. Rev. Clin. Oncol. 6(6), 327–338 (2009).
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M. Draijer, E. Hondebrink, T. van Leeuwen, and W. Steenbergen, “Review of laser speckle contrast techniques for visualizing tissue perfusion,” Lasers Med. Sci. 24(4), 639–651 (2009).
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H. P. Eikesdal and R. Kalluri, “Drug resistance associated with antiangiogenesis therapy,” Semin. Cancer Biol. 19(5), 310–317 (2009).
[Crossref] [PubMed]

H.-W. Wang, J.-K. Jiang, C.-H. Lin, J.-K. Lin, G.-J. Huang, and J.-S. Yu, “Diffuse reflectance spectroscopy detects increased hemoglobin concentration and decreased oxygenation during colon carcinogenesis from normal to malignant tumors,” Opt. Express 17(4), 2805–2817 (2009).
[Crossref] [PubMed]

2008 (5)

S. L. Jacques and B. W. Pogue, “Tutorial on diffuse light transport,” J. Biomed. Opt. 13(4), 041302 (2008).
[Crossref] [PubMed]

G. Bergers and D. Hanahan, “Modes of resistance to anti-angiogenic therapy,” Nat. Rev. Cancer 8(8), 592–603 (2008).
[Crossref] [PubMed]

L. M. Ellis and D. J. Hicklin, “VEGF-targeted therapy: mechanisms of anti-tumour activity,” Nat. Rev. Cancer 8(8), 579–591 (2008).
[Crossref] [PubMed]

C. Sessa, A. Guibal, G. Del Conte, and C. Rüegg, “Biomarkers of angiogenesis for the development of antiangiogenic therapies in oncology: tools or decorations?” Nat. Clin. Pract. Oncol. 5(7), 378–391 (2008).
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Y. Xue, P. Religa, R. Cao, A. J. Hansen, F. Lucchini, B. Jones, Y. Wu, Z. Zhu, B. Pytowski, Y. Liang, W. Zhong, P. Vezzoni, B. Rozell, and Y. Cao, “Anti-VEGF agents confer survival advantages to tumor-bearing mice by improving cancer-associated systemic syndrome,” Proc. Natl. Acad. Sci. U.S.A. 105(47), 18513–18518 (2008).
[Crossref] [PubMed]

2007 (11)

H. Youssoufian, D. J. Hicklin, and E. K. Rowinsky, “Review: Monoclonal antibodies to the vascular endothelial growth factor receptor-2 in cancer therapy,” Clin. Cancer Res. 13(18), 5544–5548 (2007).
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K. Garber, “Personal mouse colonies give hope for pancreatic cancer patients,” J. Natl. Cancer Inst. 99(2), 105–107 (2007).
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V. R. Kondepati, H. M. Heise, and J. Backhaus, “Recent applications of near-infrared spectroscopy in cancer diagnosis and therapy,” Anal. Bioanal. Chem. 390(1), 125 (2007).
[Crossref] [PubMed]

J. a. Sosman, I. Puzanov, and M. B. Atkins, “Opportunities and obstacles to combination targeted therapy in renal cell cancer,” Clin. Cancer Res. 13(2 Pt 2), 764s–769s (2007).
[Crossref] [PubMed]

J. Folkman, “Angiogenesis: an organizing principle for drug discovery?” Nat. Rev. Drug Discov. 6(4), 273–286 (2007).
[Crossref] [PubMed]

P. Vaupel and A. Mayer, “Hypoxia in cancer: significance and impact on clinical outcome,” Cancer Metastasis Rev. 26(2), 225–239 (2007).
[Crossref] [PubMed]

A. Cerussi, D. Hsiang, N. Shah, R. Mehta, A. Durkin, J. Butler, and B. J. Tromberg, “Predicting response to breast cancer neoadjuvant chemotherapy using diffuse optical spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 104(10), 4014–4019 (2007).
[Crossref] [PubMed]

C. Zhou, R. Choe, N. Shah, T. Durduran, G. Yu, A. Durkin, D. Hsiang, R. Mehta, J. Butler, A. Cerussi, B. J. Tromberg, and A. G. Yodh, “Diffuse optical monitoring of blood flow and oxygenation in human breast cancer during early stages of neoadjuvant chemotherapy,” J. Biomed. Opt. 12(5), 051903 (2007).
[Crossref] [PubMed]

S. Kopetz, C. Jimenez, S.-M. Tu, and P. Sharma, “Pulmonary arteriovenous fistula in a patient with renal cell carcinoma,” The Eur. Respir. J. 29(4), 813–815 (2007).
[Crossref] [PubMed]

G. Yu, T. Durduran, C. Zhou, T. C. Zhu, J. C. Finlay, T. M. Busch, S. B. Malkowicz, S. M. Hahn, and A. G. Yodh, “Real-time in situ monitoring of human prostate photodynamic therapy with diffuse light,” Photochem. Photobiol. 82(5), 1279–1284 (2007).
[Crossref]

U. Sunar, S. Makonnen, C. Zhou, T. Durduran, G. Yu, H.-W. Wang, W. M. Lee, and A. G. Yodh, “Hemodynamic responses to antivascular therapy and ionizing radiation assessed by diffuse optical spectroscopies,” Opt. Express 15(23), 15507–15516 (2007).
[Crossref] [PubMed]

2006 (1)

U. Sunar, H. Quon, T. Durduran, J. Zhang, J. Du, C. Zhou, G. Yu, R. Choe, A. Kilger, R. Lustig, L. Loevner, S. Nioka, B. Chance, and A. G. Yodh, “Noninvasive diffuse optical measurement of blood flow and blood oxygenation for monitoring radiation therapy in patients with Head Neck tumors: a pilot study,” J. Biomed. Opt. 11(6), 064021 (2006).
[Crossref]

2005 (5)

B. J. Tromberg, A. Cerussi, N. Shah, M. Compton, A. Durkin, D. Hsiang, J. Butler, and R. Mehta, “Imaging in breast cancer: diffuse optics in breast cancer: detecting tumors in pre-menopausal women and monitoring neoadjuvant chemotherapy,” Breast Cancer Res. 7(6), 279–285 (2005).
[Crossref]

W. K. Rathmell, T. M. Wright, and B. I. Rini, “Molecularly targeted therapy in renal cell carcinoma,” Expert Rev. Anticancer Ther. 5(6), 1031–1040 (2005).
[Crossref] [PubMed]

O. Casanovas, D. J. Hicklin, G. Bergers, and D. Hanahan, “Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors,” Cancer Cell 8(4), 299–309 (2005).
[Crossref] [PubMed]

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(9), 3543–3552 (2005).
[Crossref] [PubMed]

R. K. Jain, “Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy,” Science 307(5706), 58–62 (2005).
[Crossref] [PubMed]

2004 (2)

J. Jacobsen, K. Grankvist, T. Rasmuson, A. Bergh, G. Landberg, and B. Ljungberg, “Expression of vascular endothelial growth factor protein in human renal cell carcinoma,” BJU Int. 93(3), 297–302 (2004).
[Crossref] [PubMed]

R. T. Tong, Y. Boucher, S. V. Kozin, F. Winkler, D. J. Hicklin, and R. K. Jain, “Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors,” Cancer Res. 64(11), 3731–3736 (2004).
[Crossref] [PubMed]

2003 (2)

C. Menon, G. M. Polin, I. Prabakaran, A. Hsi, C. Cheung, J. P. Culver, J. F. Pingpank, C. S. Sehgal, A. G. Yodh, and D. G. Buerk, and Others, “An integrated approach to measuring tumor oxygen status using human melanoma xenografts as a model,” Cancer Res. 63(21), 7232–7240 (2003).
[PubMed]

N. Ferrara, H.-P. Gerber, and J. LeCouter, “The biology of VEGF and its receptors,” Nat. Med. 9(6), 669–676 (2003).
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2002 (4)

L. Hlatky, P. Hahnfeldt, and J. Folkman, “Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn’t tell us,” J. Natl. Cancer Inst. 94(12), 883–893 (2002).
[Crossref] [PubMed]

D. E. Goertz, J. L. Yu, R. S. Kerbel, P. N. Burns, and F. S. Foster, “High-frequency Doppler ultrasound monitors the effects of antivascular therapy on tumor blood flow,” Cancer Res. 62(22), 6371–6375 (2002).
[PubMed]

C. J. Bruns, M. Shrader, M. T. Harbison, C. Portera, C. C. Solorzano, K.-W. Jauch, D. J. Hicklin, R. Radinsky, and L. M. Ellis, “Effect of the vascular endothelial growth factor receptor-2 antibody DC101 plus gemcitabine on growth, metastasis and angiogenesis of human pancreatic cancer growing orthotopically in nude mice,” Int. J. Cancer. 102(2), 101–108 (2002).
[Crossref] [PubMed]

H. Simonnet, N. Alazard, K. Pfeiffer, C. Gallou, C. Béroud, J. Demont, R. Bouvier, H. Schägger, and C. Godinot, “Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma,” Carcinogenesis 23(5), 759–768 (2002).
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2001 (3)

M. S. Gee, H. M. Saunders, J. C. Lee, J. F. Sanzo, W. T. Jenkins, S. M. Evans, G. Trinchieri, C. M. Sehgal, M. D. Feldman, and W. M. Lee, “Doppler ultrasound imaging detects changes in tumor perfusion during antivascular therapy associated with vascular anatomic alterations,” Cancer Res. 61(7), 2974–2982 (2001).
[PubMed]

J. D. Briers, “Laser Doppler, speckle and related techniques for blood perfusion mapping and imaging,” Physiol. Meas. 22(4), R35–R66 (2001).
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R. S. Kerbel, J. Yu, J. Tran, S. Man, A. Viloria-Petit, G. Klement, B. L. Coomber, and J. Rak, “Possible mechanisms of acquired resistance to anti-angiogenic drugs: Implications for the use of combination therapy approaches,” Cancer Metastasis Rev. 20(1), 79–86 (2001).
[Crossref]

2000 (2)

G. Klement, S. Baruchel, J. Rak, S. Man, K. Clark, D. J. Hicklin, P. Bohlen, and R. S. Kerbel, “Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity,” The J. Clin. Invest. 105(8), R15–R24 (2000).
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P. Carmeliet and R. K. Jain, “Angiogenesis in cancer and other diseases,” Nature 407(6801), 249–257 (2000).
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1999 (4)

G. Capellá, L. Farré, A. Villanueva, G. Reyes, C. García, G. Tarafa, and F. Lluís, “Orthotopic models of human pancreatic cancer,” Ann. N.Y. Acad. Sci. 880(93), 103–109 (1999).
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E. L. Hull, D. L. Conover, and T. H. Foster, “Carbogen-induced changes in rat mammary tumour oxygenation reported by near infrared spectroscopy,” Br. J. Cancer 79(11–12), 1709–1716 (1999).
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M. Prewett, J. Huber, Y. Li, A. Santiago, W. O’Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, P. Bohlen, and D. J. Hicklin, “Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors,” Cancer Res. 59(20), 5209–5218 (1999).
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H. W. Wechsel, K. H. Bichler, G. Feil, W. Loeser, S. Lahme, and E. Petri, “Renal cell carcinoma: relevance of angiogenetic factors,” Anticancer Res. 19(2C), 1537–1540 (1999).
[PubMed]

1998 (2)

L. Witte, D. J. Hicklin, Z. Zhu, B. Pytowski, H. Kotanides, P. Rockwell, and P. Böhlen, “Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy,” Cancer Metastasis Rev. 17(2), 155–161 (1998).
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L. Witte, D. J. Hicklin, Z. Zhu, B. Pytowski, H. Kotanides, P. Rockwell, and P. Böhlen, “Monoclonal antibodies targeting the vegf receptor-2 (flk1/kdr) as an anti-angiogenic therapeutic strategy,” Cancer Metastasis Rev. 17(2), 155–161 (1998).
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1997 (2)

R. A. Weersink, J. E. Hayward, K. R. Diamond, and M. S. Patterson, “Accuracy of Noninvasive In Vivo Measurements of Photosensitizer Uptake Based on a Diffusion Model of Reflectance Spectroscopy,” Photochem. Photobiol. 66(3), 326–335 (1997).
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M. G. Nichols, E. L. Hull, and T. H. Foster, “Design and testing of a white-light, steady-state diffuse reflectance spectrometer for determination of optical properties of highly scattering systems,” Appl. Opt. 36(1), 93–104 (1997).
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1996 (1)

G. Reyes, A. Villanueva, C. García, F. J. Sancho, J. Piulats, F. Lluís, and G. Capellá, “Orthotopic xenografts of human pancreatic carcinomas acquire genetic aberrations during dissemination in nude mice,” Cancer Res. 56(24), 5713–5719 (1996).
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1995 (2)

D. Boas, L. Campbell, and A. Yodh, “Scattering and Imaging with Diffusing Temporal Field Correlations,” Phys. Rev. Lett. 75(9), 1855–1858 (1995).
[Crossref] [PubMed]

J. Folkman, “Angiogenesis in cancer, vascular, rheumatoid and other disease,” Nat. Med. 1(1), 27–30 (1995).
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1994 (1)

A. Takahashi, H. Sasaki, S. J. Kim, K. Tobisu, T. Kakizoe, T. Tsukamoto, Y. Kumamoto, T. Sugimura, and M. Terada, “Markedly increased amounts of messenger RNAs for vascular endothelial growth factor and placenta growth factor in renal cell carcinoma associated with angiogenesis,” Cancer Res. 54(15), 4233–4237 (1994).
[PubMed]

1993 (2)

H. B. Stone, J. M. Brown, T. L. Phillips, and R. M. Sutherland, “Oxygen in human tumors: correlations between methods of measurement and response to therapy. Summary of a workshop held November 19–20, 1992, at the National Cancer Institute, Bethesda, Maryland,” Radiat. Res. 136(3), 422–434 (1993).
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Figures (6)

Fig. 1
Fig. 1 (A) The schematic of hand-held DOS/DCS probe and the way it is applied on the tumor. The probe schematic only contains the location of the fibers that have been used in this study. The probe is designed to be self-calibrating, featuring a miniaturized semicircle scheme for assessing the source-detector coupling coefficients. There is a DOS source in one end of diameter and also a self-calibration source in the center of semicircle. The DOS detectors are located on the circumference of this semicircle that makes them equidistant from the calibration source. (B) An anesthetized nude mouse with a renal tumor and the optical probes (control and main) on top of the shoulder muscle and tumors with a photograph of the main probe tip on the top. Since the illuminated light to different fibers was not homogeneous they have different brightness and visibility. The smaller dots (seven locations) correspond to single mode fibers (DCS detector fibers). Not all the sources and detectors of the main probe are used in this study.
Fig. 2
Fig. 2 The results of histologies retrieved from the extracted tumor after sacrificing the animal. T1–T7 correspond to values of seven treated animals and C1–C7 corresponds to the control animals. (A) Microvessel density (MVD) in the extracted tumor measured by CD31 staining. Tumors of treated mice have lower MVD in comparison to control group (P = 0.002). (B) The extracted tumor weight of treated and control group. The extracted tumors from the treated animals are lighter than control ones (P = 0.034). (C) The percentage of tumor necrotic area. There is no statistically significant difference in the tumor percent necrotic area of treated and control group (P = 0.8). Symbol ⊛ indicates statistically significant difference between two groups (treated and control).
Fig. 3
Fig. 3 The optically measured pretreatment (day zero) hemodynamic properties of the RCC tumor in comparison with the control muscle. From left to right: (A) The higher than healthy shoulder muscle value (P< 10−4). (B) The total hemoglobin concentration in the tumor is lower than the healthy shoulder muscle (P = 8×10−4). (C) Blood oxygen saturation of the RCC in the tumor is higher than healthy shoulder muscle (P< 10−4). Symbol ⊛ indicates statistically significant difference between two locations (tumor and muscle).
Fig. 4
Fig. 4 The measured blood flow index versus total hemoglobin concentration measured over the course treatment on all mice. The red starts and green circles indicate measured values from treated and control animals respectively. In both control and treated group the measured total hemoglobin concentration and blood flow index have positive correlation.
Fig. 5
Fig. 5 Daily changes of tumor size and optically measured hemodynamic parameters during the first 18 days, which corresponds to the period when no mouse had been sacrificed, for groups of seven treated (T1–T7) in left column and seven control animals (C1–C7) in right column. Each marker and error bar represent the value corresponding to average and standard deviation of measurement over all tumor locations on a specific mouse. The solid line is a fitted LOESS curve and the gray lines are the 95% confidence intervals. (A, B) represent tumor sizes measured by palpation, (C, D) blood flow index, (E, F), total hemoglobin concentration, and (G, H) Oxygen saturation.
Fig. 6
Fig. 6 The correlation between early changes of optically measured blood flow and the extracted tumor weight. (A) Correlation between drop in BFI after the first session of therapy (day four) and the extracted tumor weight. (B) The correlation between maximum BFI drop in the first week of therapy and the extracted tumor weight.

Tables (1)

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Table 1 Median and inter-quartile range pre-treatment (day zero) values of optically measured parameters on RCC tumors and the control muscle are shown. Furthermore, the median and inter-quartile range of variability of measured parameters in different locations is also shown to give an impression of the variability over probe re-locations at a given time point. Symbol ⊛ indicates a statistically significant difference between two tissue types (tumor and muscle)

Equations (1)

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G 1 ( ρ , τ ) = 3 μ s 4 π [ exp ( K ( τ ) r 1 ) r 1 exp ( K ( τ ) r b ) r b ] .

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