Abstract

The lymphatic system provides an initial route for cancer cell dissemination in many cancers including melanoma. However, it is largely unknown how the lymphatic system changes during tumor progression due in part to the lack of imaging techniques currently available. In this study, we non-invasively imaged changes of lymphatic function and drainage patterns using near-infrared fluorescence (NIRF) imaging. Dynamic NIRF imaging following intradermal injection of indocyanine green (ICG) was conducted in C57BL/6 mice prior to inoculation of B16F10 murine melanoma cells to the dorsal aspect of the left hindpaw for baseline data or directly to the popliteal lymph node (PLN) and until 21 days post-implantation (p.i.). A series of acquired fluorescent images were quantified to measure lymphatic contractile function. Computed tomography (CT) was also performed to measure the volume of tumor-draining lymph nodes (LNs). We observed significant reduction of lymphatic contractility from 7 days p.i. until 21 days p.i.. Altered lymphatic drainage patterns were also detected at 21 days p.i. in mice with tumor in the paw and at 11 days p.i. in mice with tumor in the PLN, due to lymphatic obstruction of normal lymphatic drainages caused by extensive tumor invasion of draining LNs. Since lymphatic function and architecture were progressively altered during tumor growth and metastasis, non-invasive NIRF imaging may provide a new method to stage disease. In addition, this novel technique can be used as a diagnostic method to non-invasively assess lymphatic response as mechanism of therapeutic action.

© 2013 OSA

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    [CrossRef] [PubMed]
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2012 (5)

A. Alitalo and M. Detmar, “Interaction of tumor cells and lymphatic vessels in cancer progression,” Oncogene31(42), 4499–4508 (2012).
[CrossRef] [PubMed]

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

E. M. Sevick-Muraca, “Translation of near-infrared fluorescence imaging technologies: emerging clinical applications,” Annu. Rev. Med.63(1), 217–231 (2012).
[CrossRef] [PubMed]

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

J. C. Rasmussen, S. Kwon, E. M. Sevick-Muraca, and J. N. Cormier, “The role of lymphatics in cancer as assessed by near-infrared fluorescence imaging,” Ann. Biomed. Eng.40(2), 408–421 (2012).
[CrossRef] [PubMed]

2011 (3)

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

S. Kwon and E. M. Sevick-Muraca, “Mouse phenotyping with near-infrared fluorescence lymphatic imaging,” Biomed. Opt. Express2(6), 1403–1411 (2011).
[CrossRef] [PubMed]

2010 (3)

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods360(1-2), 167–172 (2010).
[CrossRef] [PubMed]

2009 (3)

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

R. C. Ji, “Lymph node lymphangiogenesis: a new concept for modulating tumor metastasis and inflammatory process,” Histol. Histopathol.24(3), 377–384 (2009).
[PubMed]

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
[CrossRef] [PubMed]

2008 (2)

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

M. Rinderknecht and M. Detmar, “Tumor lymphangiogenesis and melanoma metastasis,” J. Cell. Physiol.216(2), 347–354 (2008).
[CrossRef] [PubMed]

2007 (4)

R. F. Uren, R. Howman-Giles, D. K. Chung, and J. F. Thompson, “Metastatic occlusion of a lymphatic collecting vessel in a patient with cutaneous melanoma and clinically normal lymph nodes,” Clin. Nucl. Med.32(4), 312–313 (2007).
[CrossRef] [PubMed]

M. I. Harrell, B. M. Iritani, and A. Ruddell, “Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis,” Am. J. Pathol.170(2), 774–786 (2007).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Noninvasive quantitative imaging of lymph function in mice,” Lymphat. Res. Biol.5(4), 219–232 (2007).
[CrossRef] [PubMed]

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

2006 (3)

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

2005 (3)

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

2004 (1)

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

2003 (3)

M. Streit and M. Detmar, “Angiogenesis, lymphangiogenesis, and melanoma metastasis,” Oncogene22(20), 3172–3179 (2003).
[CrossRef] [PubMed]

R. F. Uren, R. Howman-Giles, and J. F. Thompson, “Patterns of lymphatic drainage from the skin in patients with melanoma,” J. Nucl. Med.44(4), 570–582 (2003).
[PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

2002 (3)

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

J. E. Gershenwald and I. J. Fidler, “Cancer. Targeting lymphatic metastasis,” Science296(5574), 1811–1812 (2002).
[CrossRef] [PubMed]

2001 (3)

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

K. Nakaya, R. Mizuno, and T. Ohhashi, “B16-BL6 melanoma cells release inhibitory factor(s) of active pump activity in isolated lymph vessels,” Am. J. Physiol. Cell Physiol.281(6), C1812–C1818 (2001).
[PubMed]

1991 (1)

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Achen, M. G.

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

Adams, K. E.

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Alitalo, A.

A. Alitalo and M. Detmar, “Interaction of tumor cells and lymphatic vessels in cancer progression,” Oncogene31(42), 4499–4508 (2012).
[CrossRef] [PubMed]

Alitalo, K.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Baldwin, M. E.

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

Berghuis, B.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Berman, C.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Bertoncini, J.

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Blanchard, D. K.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Bonefas, E.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Brown, L. F.

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Bruch, M.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Cassella, M.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

Chan, W.

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

Chen, J.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Chen, Y. L.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Chiang, S. B.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Chung, D. K.

R. F. Uren, R. Howman-Giles, D. K. Chung, and J. F. Thompson, “Metastatic occlusion of a lymphatic collecting vessel in a patient with cutaneous melanoma and clinically normal lymph nodes,” Clin. Nucl. Med.32(4), 312–313 (2007).
[CrossRef] [PubMed]

Claffey, K.

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Clark, R.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Colpaert, C. G.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

Cormier, J. N.

J. C. Rasmussen, S. Kwon, E. M. Sevick-Muraca, and J. N. Cormier, “The role of lymphatics in cancer as assessed by near-infrared fluorescence imaging,” Ann. Biomed. Eng.40(2), 408–421 (2012).
[CrossRef] [PubMed]

Covington, K. R.

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

Cox, C.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Cruse, C. W.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Dadras, S. S.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Derzsi, S.

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

Detmar, M.

A. Alitalo and M. Detmar, “Interaction of tumor cells and lymphatic vessels in cancer progression,” Oncogene31(42), 4499–4508 (2012).
[CrossRef] [PubMed]

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

M. Rinderknecht and M. Detmar, “Tumor lymphangiogenesis and melanoma metastasis,” J. Cell. Physiol.216(2), 347–354 (2008).
[CrossRef] [PubMed]

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

M. Streit and M. Detmar, “Angiogenesis, lymphangiogenesis, and melanoma metastasis,” Oncogene22(20), 3172–3179 (2003).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

di Tomaso, E.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Dirix, L. Y.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

Ditlev, J.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Elledge, R.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Ellwanger, U.

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Espinosa, C.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Fidler, I. J.

J. E. Gershenwald and I. J. Fidler, “Cancer. Targeting lymphatic metastasis,” Science296(5574), 1811–1812 (2002).
[CrossRef] [PubMed]

Fife, C. E.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

Fisher, R. E.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Fukumura, D.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Furuya, M.

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

Garbe, C.

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Gershenwald, J. E.

J. E. Gershenwald and I. J. Fidler, “Cancer. Targeting lymphatic metastasis,” Science296(5574), 1811–1812 (2002).
[CrossRef] [PubMed]

Gonzalez, M.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Guilliod, R.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

Hagendoorn, J.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Hamberg, L. M.

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

Harding, T. C.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Harrell, M. I.

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

M. I. Harrell, B. M. Iritani, and A. Ruddell, “Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis,” Am. J. Pathol.170(2), 774–786 (2007).
[CrossRef] [PubMed]

Hauschild, A.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Hawighorst, T.

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

He, Y.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

Hirakawa, S.

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Horenblas, S.

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
[CrossRef] [PubMed]

Hoshida, T.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Houston, J. P.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Howman-Giles, R.

R. F. Uren, R. Howman-Giles, D. K. Chung, and J. F. Thompson, “Metastatic occlusion of a lymphatic collecting vessel in a patient with cutaneous melanoma and clinically normal lymph nodes,” Clin. Nucl. Med.32(4), 312–313 (2007).
[CrossRef] [PubMed]

R. F. Uren, R. Howman-Giles, and J. F. Thompson, “Patterns of lymphatic drainage from the skin in patients with melanoma,” J. Nucl. Med.44(4), 570–582 (2003).
[PubMed]

Hudson, E.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Inaba, K.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Iritani, B. M.

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

M. I. Harrell, B. M. Iritani, and A. Ruddell, “Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis,” Am. J. Pathol.170(2), 774–786 (2007).
[CrossRef] [PubMed]

Isaka, N.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Jackson, D. G.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Jahnke, K.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Jain, R. K.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Janes, L.

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Ji, R. C.

R. C. Ji, “Lymph node lymphangiogenesis: a new concept for modulating tumor metastasis and inflammatory process,” Histol. Histopathol.24(3), 377–384 (2009).
[PubMed]

Jooss, K.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Jussila, L.

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

Kajiya, K.

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

Karpanen, T.

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

Kawada, K.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

King, P. D.

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

Kirschbaum, S. B.

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

Kloos, B.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

Kodama, S.

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

Koprivnikar, K.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Kort, E. J.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Koshikawa, K.

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

Kozaki, K.

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

Kunstfeld, R.

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

Kwon, S.

J. C. Rasmussen, S. Kwon, E. M. Sevick-Muraca, and J. N. Cormier, “The role of lymphatics in cancer as assessed by near-infrared fluorescence imaging,” Ann. Biomed. Eng.40(2), 408–421 (2012).
[CrossRef] [PubMed]

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Mouse phenotyping with near-infrared fluorescence lymphatic imaging,” Biomed. Opt. Express2(6), 1403–1411 (2011).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods360(1-2), 167–172 (2010).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

S. Kwon and E. M. Sevick-Muraca, “Noninvasive quantitative imaging of lymph function in mice,” Lymphat. Res. Biol.5(4), 219–232 (2007).
[CrossRef] [PubMed]

Lalani, A. S.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Lam, T. K.

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

Lange-Asschenfeldt, B.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Lapinski, P. E.

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

Leijte, J. A.

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
[CrossRef] [PubMed]

Leroux, J. C.

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

Lin, J.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Luan, B.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Lubeck, B. A.

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

Luciani, P.

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

Manabe, T.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Marshall, M. V.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Maus, E. A.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

Mawad, M. E.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Mihm, M. C.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Minato, N.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Mizuno, R.

K. Nakaya, R. Mizuno, and T. Ohhashi, “B16-BL6 melanoma cells release inhibitory factor(s) of active pump activity in isolated lymph vessels,” Am. J. Physiol. Cell Physiol.281(6), C1812–C1818 (2001).
[PubMed]

Mumprecht, V.

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

Muzikansky, A.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Nakaya, K.

K. Nakaya, R. Mizuno, and T. Ohhashi, “B16-BL6 melanoma cells release inhibitory factor(s) of active pump activity in isolated lymph vessels,” Am. J. Physiol. Cell Physiol.281(6), C1812–C1818 (2001).
[PubMed]

Nguyen, L.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Nieweg, O. E.

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
[CrossRef] [PubMed]

Norman, J.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Ohhashi, T.

K. Nakaya, R. Mizuno, and T. Ohhashi, “B16-BL6 melanoma cells release inhibitory factor(s) of active pump activity in isolated lymph vessels,” Am. J. Physiol. Cell Physiol.281(6), C1812–C1818 (2001).
[PubMed]

Oshima, M.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Padera, T. P.

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Paul, T.

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
[CrossRef] [PubMed]

Persaud, K.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

Petillo, D.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Pham, H. Q.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Podgrabinska, S.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

Prevo, R.

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Proulx, S. T.

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

Pytowski, B.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Qian, C. N.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Quinn, M. J.

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

Rasmussen, J. C.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

J. C. Rasmussen, S. Kwon, E. M. Sevick-Muraca, and J. N. Cormier, “The role of lymphatics in cancer as assessed by near-infrared fluorescence imaging,” Ann. Biomed. Eng.40(2), 408–421 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Reintgen, D.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Resau, J. H.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Riccardi, L.

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Rinderknecht, M.

S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
[CrossRef] [PubMed]

M. Rinderknecht and M. Detmar, “Tumor lymphangiogenesis and melanoma metastasis,” J. Cell. Physiol.216(2), 347–354 (2008).
[CrossRef] [PubMed]

Roberts, N.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

Ruddell, A.

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

M. I. Harrell, B. M. Iritani, and A. Ruddell, “Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis,” Am. J. Pathol.170(2), 774–786 (2007).
[CrossRef] [PubMed]

Saba, H.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Sakashita, H.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Sampath, L.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Schirner, M.

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

Scolyer, R. A.

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

Sevick-Muraca, E.

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

Sevick-Muraca, E. M.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

E. M. Sevick-Muraca, “Translation of near-infrared fluorescence imaging technologies: emerging clinical applications,” Annu. Rev. Med.63(1), 217–231 (2012).
[CrossRef] [PubMed]

J. C. Rasmussen, S. Kwon, E. M. Sevick-Muraca, and J. N. Cormier, “The role of lymphatics in cancer as assessed by near-infrared fluorescence imaging,” Ann. Biomed. Eng.40(2), 408–421 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Mouse phenotyping with near-infrared fluorescence lymphatic imaging,” Biomed. Opt. Express2(6), 1403–1411 (2011).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods360(1-2), 167–172 (2010).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Noninvasive quantitative imaging of lymph function in mice,” Lymphat. Res. Biol.5(4), 219–232 (2007).
[CrossRef] [PubMed]

Shannon, K. F.

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

Sharma, R.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Skobe, M.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Smith, L. A.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

Sonoshita, M.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Srinivasan, R. S.

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

Stacker, S. A.

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

Streit, M.

M. Streit and M. Detmar, “Angiogenesis, lymphangiogenesis, and melanoma metastasis,” Oncogene22(20), 3172–3179 (2003).
[CrossRef] [PubMed]

Takabayashi, A.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Takahashi, T.

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

Taketo, M. M.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Tan, I. C.

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

Teh, B. T.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Thompson, J. F.

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

R. F. Uren, R. Howman-Giles, D. K. Chung, and J. F. Thompson, “Metastatic occlusion of a lymphatic collecting vessel in a patient with cutaneous melanoma and clinically normal lymph nodes,” Clin. Nucl. Med.32(4), 312–313 (2007).
[CrossRef] [PubMed]

R. F. Uren, R. Howman-Giles, and J. F. Thompson, “Patterns of lymphatic drainage from the skin in patients with melanoma,” J. Nucl. Med.44(4), 570–582 (2003).
[PubMed]

Tsarfaty, G.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Tsarfaty, I.

C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
[CrossRef] [PubMed]

Tu, G. H.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Uren, R. F.

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
[CrossRef] [PubMed]

R. F. Uren, R. Howman-Giles, D. K. Chung, and J. F. Thompson, “Metastatic occlusion of a lymphatic collecting vessel in a patient with cutaneous melanoma and clinically normal lymph nodes,” Clin. Nucl. Med.32(4), 312–313 (2007).
[CrossRef] [PubMed]

R. F. Uren, R. Howman-Giles, and J. F. Thompson, “Patterns of lymphatic drainage from the skin in patients with melanoma,” J. Nucl. Med.44(4), 570–582 (2003).
[PubMed]

Valdés Olmos, R. A.

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
[CrossRef] [PubMed]

van Dam, P.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

van Dam, P. J.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

Van den Eynden, G. G.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

van der Ploeg, I. M.

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
[CrossRef] [PubMed]

Van Marck, E. A.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

Vandenberghe, M. K.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

VanRoey, M. J.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Velasco, P.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Vermeulen, P. B.

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
[CrossRef] [PubMed]

Vora, A.

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Wells, K.

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
[CrossRef] [PubMed]

Wendt, J. A.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
[CrossRef] [PubMed]

Wilkinson, J. E.

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

Wolf, G. L.

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

Wu, W. W.

J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

Wu, Y.

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

Yamaoka, Y.

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
[CrossRef] [PubMed]

Yla-Herttuala, S.

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
[CrossRef] [PubMed]

Am. J. Pathol. (3)

M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar, “Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma,” Am. J. Pathol.159(3), 893–903 (2001).
[CrossRef] [PubMed]

M. I. Harrell, B. M. Iritani, and A. Ruddell, “Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis,” Am. J. Pathol.170(2), 774–786 (2007).
[CrossRef] [PubMed]

S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival,” Am. J. Pathol.162(6), 1951–1960 (2003).
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Am. J. Physiol. Cell Physiol. (1)

K. Nakaya, R. Mizuno, and T. Ohhashi, “B16-BL6 melanoma cells release inhibitory factor(s) of active pump activity in isolated lymph vessels,” Am. J. Physiol. Cell Physiol.281(6), C1812–C1818 (2001).
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Am. J. Surg. (1)

J. Norman, C. W. Cruse, C. Espinosa, C. Cox, C. Berman, R. Clark, H. Saba, K. Wells, and D. Reintgen, “Redefinition of cutaneous lymphatic drainage with the use of lymphoscintigraphy for malignant melanoma,” Am. J. Surg.162(5), 432–437 (1991).
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Ann. Biomed. Eng. (1)

J. C. Rasmussen, S. Kwon, E. M. Sevick-Muraca, and J. N. Cormier, “The role of lymphatics in cancer as assessed by near-infrared fluorescence imaging,” Ann. Biomed. Eng.40(2), 408–421 (2012).
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Annu. Rev. Med. (1)

E. M. Sevick-Muraca, “Translation of near-infrared fluorescence imaging technologies: emerging clinical applications,” Annu. Rev. Med.63(1), 217–231 (2012).
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Arch. Phys. Med. Rehabil. (1)

I. C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Med. Rehabil.92(5), 756–764, e1 (2011).
[CrossRef] [PubMed]

Biomed. Opt. Express (1)

Cancer Res. (6)

K. Kawada, M. Sonoshita, H. Sakashita, A. Takabayashi, Y. Yamaoka, T. Manabe, K. Inaba, N. Minato, M. Oshima, and M. M. Taketo, “Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes,” Cancer Res.64(11), 4010–4017 (2004).
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S. T. Proulx, P. Luciani, S. Derzsi, M. Rinderknecht, V. Mumprecht, J. C. Leroux, and M. Detmar, “Quantitative imaging of lymphatic function with liposomal indocyanine green,” Cancer Res.70(18), 7053–7062 (2010).
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C. N. Qian, B. Berghuis, G. Tsarfaty, M. Bruch, E. J. Kort, J. Ditlev, I. Tsarfaty, E. Hudson, D. G. Jackson, D. Petillo, J. Chen, J. H. Resau, and B. T. Teh, “Preparing the ‘soil’: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells,” Cancer Res.66(21), 10365–10376 (2006).
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J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo, and K. Jooss, “Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor,” Cancer Res.65(15), 6901–6909 (2005).
[CrossRef] [PubMed]

N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe, “Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2,” Cancer Res.66(5), 2650–2657 (2006).
[CrossRef] [PubMed]

T. Hoshida, N. Isaka, J. Hagendoorn, E. di Tomaso, Y. L. Chen, B. Pytowski, D. Fukumura, T. P. Padera, and R. K. Jain, “Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications,” Cancer Res.66(16), 8065–8075 (2006).
[CrossRef] [PubMed]

Clin. Cancer Res. (1)

G. G. Van den Eynden, M. K. Vandenberghe, P. J. van Dam, C. G. Colpaert, P. van Dam, L. Y. Dirix, P. B. Vermeulen, and E. A. Van Marck, “Increased sentinel lymph node lymphangiogenesis is associated with nonsentinel axillary lymph node involvement in breast cancer patients with a positive sentinel node,” Clin. Cancer Res.13(18), 5391–5397 (2007).
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Clin. Nucl. Med. (1)

R. F. Uren, R. Howman-Giles, D. K. Chung, and J. F. Thompson, “Metastatic occlusion of a lymphatic collecting vessel in a patient with cutaneous melanoma and clinically normal lymph nodes,” Clin. Nucl. Med.32(4), 312–313 (2007).
[CrossRef] [PubMed]

Head Neck (1)

E. A. Maus, I. C. Tan, J. C. Rasmussen, M. V. Marshall, C. E. Fife, L. A. Smith, R. Guilliod, and E. M. Sevick-Muraca, “Near-infrared fluorescence imaging of lymphatics in head and neck lymphedema,” Head Neck34(3), 448–453 (2012).
[CrossRef] [PubMed]

Histol. Histopathol. (1)

R. C. Ji, “Lymph node lymphangiogenesis: a new concept for modulating tumor metastasis and inflammatory process,” Histol. Histopathol.24(3), 377–384 (2009).
[PubMed]

J. Cell. Physiol. (1)

M. Rinderknecht and M. Detmar, “Tumor lymphangiogenesis and melanoma metastasis,” J. Cell. Physiol.216(2), 347–354 (2008).
[CrossRef] [PubMed]

J. Clin. Invest. (1)

P. E. Lapinski, S. Kwon, B. A. Lubeck, J. E. Wilkinson, R. S. Srinivasan, E. Sevick-Muraca, and P. D. King, “RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice,” J. Clin. Invest.122(2), 733–747 (2012).
[CrossRef] [PubMed]

J. Exp. Med. (1)

S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar, “VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis,” J. Exp. Med.201(7), 1089–1099 (2005).
[CrossRef] [PubMed]

J. Immunol. Methods (1)

S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods360(1-2), 167–172 (2010).
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J. Natl. Cancer Inst. (1)

Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo, “Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling,” J. Natl. Cancer Inst.94(11), 819–825 (2002).
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J. Nucl. Med. (2)

J. A. Leijte, I. M. van der Ploeg, R. A. Valdés Olmos, O. E. Nieweg, and S. Horenblas, “Visualization of tumor blockage and rerouting of lymphatic drainage in penile cancer patients by use of SPECT/CT,” J. Nucl. Med.50(3), 364–367 (2009).
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R. F. Uren, R. Howman-Giles, and J. F. Thompson, “Patterns of lymphatic drainage from the skin in patients with melanoma,” J. Nucl. Med.44(4), 570–582 (2003).
[PubMed]

Lymphat. Res. Biol. (1)

S. Kwon and E. M. Sevick-Muraca, “Noninvasive quantitative imaging of lymph function in mice,” Lymphat. Res. Biol.5(4), 219–232 (2007).
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Melanoma Res. (1)

T. K. Lam, R. F. Uren, R. A. Scolyer, M. J. Quinn, K. F. Shannon, and J. F. Thompson, “False-negative sentinel node biopsy because of obstruction of lymphatics by metastatic melanoma: the value of ultrasound in conjunction with preoperative lymphoscintigraphy,” Melanoma Res.19(2), 94–99 (2009).
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Mod. Pathol. (1)

S. S. Dadras, B. Lange-Asschenfeldt, P. Velasco, L. Nguyen, A. Vora, A. Muzikansky, K. Jahnke, A. Hauschild, S. Hirakawa, M. C. Mihm, and M. Detmar, “Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes,” Mod. Pathol.18(9), 1232–1242 (2005).
[CrossRef] [PubMed]

Nat. Med. (1)

M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey, and M. Detmar, “Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis,” Nat. Med.7(2), 192–198 (2001).
[CrossRef] [PubMed]

Nat. Rev. Cancer (1)

S. A. Stacker, M. G. Achen, L. Jussila, M. E. Baldwin, and K. Alitalo, “Lymphangiogenesis and cancer metastasis,” Nat. Rev. Cancer2(8), 573–583 (2002).
[CrossRef] [PubMed]

Neoplasia (1)

A. Ruddell, M. I. Harrell, M. Furuya, S. B. Kirschbaum, and B. M. Iritani, “B lymphocytes promote lymphogenous metastasis of lymphoma and melanoma,” Neoplasia13(8), 748–757 (2011).
[PubMed]

Oncogene (2)

M. Streit and M. Detmar, “Angiogenesis, lymphangiogenesis, and melanoma metastasis,” Oncogene22(20), 3172–3179 (2003).
[CrossRef] [PubMed]

A. Alitalo and M. Detmar, “Interaction of tumor cells and lymphatic vessels in cancer progression,” Oncogene31(42), 4499–4508 (2012).
[CrossRef] [PubMed]

Radiology (1)

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology246(3), 734–741 (2008).
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Science (1)

J. E. Gershenwald and I. J. Fidler, “Cancer. Targeting lymphatic metastasis,” Science296(5574), 1811–1812 (2002).
[CrossRef] [PubMed]

Transl. Oncol. (1)

J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl. Oncol.3(6), 362–372 (2010).
[PubMed]

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Figures (7)

Fig. 1
Fig. 1

Representative NIRF images in the ventral, right, and left view of a mouse prior to and 7, 14, and 21 days after inoculation of murine B16F10 cells in the left hindpaw. An arrowhead indicates altered lymphatic drainage. Arrows, ICG injection site. Asterisk, PLN. Broken arrow, IsLN.

Fig. 2
Fig. 2

Magnified fluorescent images showing lymphatic vessel dilation in the dorsal aspect of the left paw of a mouse at 7, 14, and 21 days p.i. (tumor periphery denoted by red dotted circles) as compared to contralateral right foot. Scale, 1 mm.

Fig. 3
Fig. 3

Immunohistochemical stain for LYVE-1 (brown) showing dilated lymphatic vessels in the peritumoral region on the left foot (B) as compared to the contralateral region on the right foot (A). Computer-assisted image analysis shows a comparable number of lymphatic vessels per area in tumor and contralateral regions (C), but a significant increase of relative area occupied by lymphatics in tumor as compared to control right foot (D). n = 7 mice. Scale, 50 µm. * p < 0.05 vs. control.

Fig. 4
Fig. 4

Fluorescent images of a mouse prior to (A) and 21 days p.i. (B) showing additional lymphatic drainage to the ILN, mainly due to tumor blockage of normal lymphatic drainage to the PLN. Arrow, ICG injection site. Double arrow, PLN. Arrowhead, ILN. The insets show magnified fluorescent images of the rectangles of Figs. 4A and 4B. In Fig. 4B, the injection site was covered to prevent image oversaturation. Scale, 1 mm. An intravital color image (C) after a skin incision above the PLN shows the melanoma-filled PLN. Asterisk, PLN. Color (D) and fluorescent (E) images of dissected PLNs and ILNs on the tumor and contralateral sides of a mouse. Note that the melanoma-filled PLN as indicated by an asterisk in Fig. 4D has low ICG fluorescence as compared to the left ILN due to rerouting of normal lymphatic drainage to the left ILN. Scale, 1 mm. H&E images (x10 objective) confirm extensive PLN metastasis (F) and no metastasis in contralateral PLN (G). Scale, 100 µm.

Fig. 5
Fig. 5

Representative CT images (A) of a mouse prior to and at 7, 14, and 21 days p.i. showing a gradually enlarged tumor-draining PLN as shown in red dotted circles. The primary tumor volume on the left paw (B) is significantly increased at 21 days p.i. as compared to that at 14 days p.i.. * p < 0.05 vs. days 7. The volume of tumor-draining PLNs at 21 days p.i. (C) is significantly larger than that in contralateral PLNs. * p < 0.05 vs. contralateral right PLN.

Fig. 6
Fig. 6

Significant reduction of lymphatic contractile function in an afferent popliteal lymphatic vessel during tumor growth and LN metastasis (A) was observed, whereas lymphatic contraction frequency in an efferent popliteal lymphatic vessel was not changed (B). n = 12 mice. * p < 0.05 vs. baseline.

Fig. 7
Fig. 7

Representative fluorescent images of a mouse prior (A, D, E) to and at 4 (B, F, G) and 11 days p.i. (C, H, I). Scale, 1 mm. Magnified fluorescent images (D, E, F, G, H, I) of two rectangles in A, B, and C showed changes of lymphatic drainage during tumor growth in the PLN. Altered lymphatic drainage to the ILN was observed at 11 days P.I. as indicated by an arrowhead (J). The injection site was covered with black paper to prevent camera saturation. Fluorescent image of dissected ILN and PLN (K). Scale, 1 mm.

Tables (1)

Tables Icon

Table 1 Metastatic Frequency of B16F10 to PLNs and the Status of Altered Lymphatic Drainage Pattern*

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