Abstract

As part of a proof-of-concept study for future delivery of targeted near-infrared fluorescent (NIRF) tracers, we sought to assess the delivery of micrograms of indocyanine green to all the axillary lymph nodes following intraparenchymal breast injections and intradermal arm injections in 20 subjects with advanced breast carcinoma and undergoing complete axillary lymph node dissection. Lymphatic vessels and nodes were assessed in vivo. Ex vivo images demonstrated that 87% of excised lymph nodes, including 81% of tumor-positive lymph nodes, were fluorescent. Future clinical studies using microdose amounts of tumor-targeting NIRF contrast agents may demonstrate improved surgical intervention with reduced morbidity.

© 2013 Optical Society of America

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2013

C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
[CrossRef] [PubMed]

J. Wu, R. Ma, H. Cao, Z. Wang, C. Jing, Y. Sun, Y. Zhang, Z. Yang, R. M. Hoffman, and J. Tang, “Intraoperative imaging of metastatic lymph nodes using a fluorophore-conjugated antibody in a her2/neu-expressing orthotopic breast cancer mouse model,” Anticancer Res.33(2), 419–424 (2013).
[PubMed]

B. E. Schaafsma, F. P. Verbeek, D. D. Rietbergen, B. van der Hiel, J. R. van der Vorst, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, F. W. van Leeuwen, and A. L. Vahrmeijer, “Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer,” Br. J. Surg.100(8), 1037–1044 (2013).
[CrossRef] [PubMed]

T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
[CrossRef] [PubMed]

E. M. Sevick-Muraca and B. Zhu, “The need for performance standards in clinical translation and adoption of fluorescence molecular imaging,” Med. Phys.40(4), 040402 (2013).
[CrossRef] [PubMed]

2012

B. Zhu, I.-C. Tan, J. C. Rasmussen, and E. M. Sevick-Muraca, “Validating the sensitivity and performance of near-infrared fluorescence imaging and tomography devices using a novel solid phantom and measurement approach,” Technol. Cancer Res. Treat.11(1), 95–104 (2012).
[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]

M. Takeuchi, T. Sugie, K. Abdelazeem, H. Kato, N. Shinkura, M. Takada, H. Yamashiro, T. Ueno, and M. Toi, “Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer,” Breast J.18(6), 535–541 (2012).
[CrossRef] [PubMed]

G. C. Wishart, S. W. Loh, L. Jones, and J. R. Benson, “A feasibility study (icg-10) of indocyanine green (icg) fluorescence mapping for sentinel lymph node detection in early breast cancer,” Eur. J. Surg. Oncol.38(8), 651–656 (2012).
[CrossRef] [PubMed]

A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

J. R. van der Vorst, B. E. Schaafsma, F. P. Verbeek, M. Hutteman, J. S. Mieog, C. W. Lowik, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients,” Ann. Surg. Oncol.19(13), 4104–4111 (2012).
[CrossRef] [PubMed]

F. Wu, M. Tamhane, and M. E. Morris, “Pharmacokinetics, lymph node uptake, and mechanistic pk model of near-infrared dye-labeled bevacizumab after iv and sc administration in mice,” AAPS J.14(2), 252–261 (2012).
[CrossRef] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
[CrossRef] [PubMed]

M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
[CrossRef] [PubMed]

N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
[CrossRef] [PubMed]

J. W. Han, Y. J. Seo, J. E. Choi, S. H. Kang, Y. K. Bae, and S. J. Lee, “The efficacy of arm node preserving surgery using axillary reverse mapping for preventing lymphedema in patients with breast cancer,” J. Breast Cancer15(1), 91–97 (2012).
[CrossRef] [PubMed]

2010

I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
[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]

2009

J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol.20(1), 74–82 (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]

D. Murawa, C. Hirche, S. Dresel, and M. Hünerbein, “Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence,” Br. J. Surg.96(11), 1289–1294 (2009).
[CrossRef] [PubMed]

T. B. Britton, C. K. Solanki, S. E. Pinder, P. S. Mortimer, A. M. Peters, and A. D. Purushotham, “Lymphatic drainage pathways of the breast and the upper limb,” Nucl. Med. Commun.30(6), 427–430 (2009).
[CrossRef] [PubMed]

J. E. Choi, Y. S. Jeon, S. H. Kang, and S. J. Lee, “Preservation of lymphatic drainage of arm during axillary procedure in breast cancer patients,” J. Breast Cancer12(3), 179–185 (2009).
[CrossRef]

R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
[CrossRef] [PubMed]

C. Boneti, S. Korourian, Z. Diaz, C. Santiago, S. Mumford, L. Adkins, and V. S. Klimberg, “Scientific impact award: Axillary reverse mapping (arm) to identify and protect lymphatics draining the arm during axillary lymphadenectomy,” Am. J. Surg.198(4), 482–487 (2009).
[CrossRef] [PubMed]

J. A. P. Leijte, I. M. C. 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

S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
[CrossRef] [PubMed]

S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
[CrossRef] [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]

L. Sampath, W. Wang, and E. M. Sevick-Muraca, “Near infrared fluorescent optical imaging for nodal staging,” J. Biomed. Opt.13(4), 041312 (2008).
[CrossRef] [PubMed]

E. M. Sevick-Muraca and J. C. Rasmussen, “Molecular imaging with optics: Primer and case for near-infrared fluorescence techniques in personalized medicine,” J. Biomed. Opt.13(4), 041303 (2008).
[CrossRef] [PubMed]

T. Karpanen and K. Alitalo, “Molecular biology and pathology of lymphangiogenesis,” Annu. Rev. Pathol.3(1), 367–397 (2008).
[CrossRef] [PubMed]

2007

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]

M. Thompson, S. Korourian, R. Henry-Tillman, L. Adkins, S. Mumford, K. C. Westbrook, and V. S. Klimberg, “Axillary reverse mapping (arm): A new concept to identify and enhance lymphatic preservation,” Ann. Surg. Oncol.14(6), 1890–1895 (2007).
[CrossRef] [PubMed]

2006

S. Hirakawa, L. F. Brown, S. Kodama, K. Paavonen, K. Alitalo, and M. Detmar, “Vegf-c-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites,” Blood109(3), 1010–1017 (2006).
[CrossRef] [PubMed]

2005

K. Alitalo, T. Tammela, and T. V. Petrova, “Lymphangiogenesis in development and human disease,” Nature438(7070), 946–953 (2005).
[CrossRef] [PubMed]

T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer12(3), 211–215 (2005).
[CrossRef] [PubMed]

2001

J. A. Petrek, R. T. Senie, M. Peters, and P. P. Rosen, “Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis,” Cancer92(6), 1368–1377 (2001).
[CrossRef] [PubMed]

1976

M. L. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, “Light-absorbing properties, stability, and spectral stabilization of indocyanine green,” J. Appl. Physiol.40(4), 575–583 (1976).
[PubMed]

Abdelazeem, K.

M. Takeuchi, T. Sugie, K. Abdelazeem, H. Kato, N. Shinkura, M. Takada, H. Yamashiro, T. Ueno, and M. Toi, “Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer,” Breast J.18(6), 535–541 (2012).
[CrossRef] [PubMed]

Abrahams, D.

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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).
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C. Boneti, S. Korourian, Z. Diaz, C. Santiago, S. Mumford, L. Adkins, and V. S. Klimberg, “Scientific impact award: Axillary reverse mapping (arm) to identify and protect lymphatics draining the arm during axillary lymphadenectomy,” Am. J. Surg.198(4), 482–487 (2009).
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M. Thompson, S. Korourian, R. Henry-Tillman, L. Adkins, S. Mumford, K. C. Westbrook, and V. S. Klimberg, “Axillary reverse mapping (arm): A new concept to identify and enhance lymphatic preservation,” Ann. Surg. Oncol.14(6), 1890–1895 (2007).
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P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
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K. Alitalo, T. Tammela, and T. V. Petrova, “Lymphangiogenesis in development and human disease,” Nature438(7070), 946–953 (2005).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
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M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
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I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
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J. W. Han, Y. J. Seo, J. E. Choi, S. H. Kang, Y. K. Bae, and S. J. Lee, “The efficacy of arm node preserving surgery using axillary reverse mapping for preventing lymphedema in patients with breast cancer,” J. Breast Cancer15(1), 91–97 (2012).
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C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
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G. C. Wishart, S. W. Loh, L. Jones, and J. R. Benson, “A feasibility study (icg-10) of indocyanine green (icg) fluorescence mapping for sentinel lymph node detection in early breast cancer,” Eur. J. Surg. Oncol.38(8), 651–656 (2012).
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R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
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N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
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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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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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C. Boneti, S. Korourian, Z. Diaz, C. Santiago, S. Mumford, L. Adkins, and V. S. Klimberg, “Scientific impact award: Axillary reverse mapping (arm) to identify and protect lymphatics draining the arm during axillary lymphadenectomy,” Am. J. Surg.198(4), 482–487 (2009).
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T. B. Britton, C. K. Solanki, S. E. Pinder, P. S. Mortimer, A. M. Peters, and A. D. Purushotham, “Lymphatic drainage pathways of the breast and the upper limb,” Nucl. Med. Commun.30(6), 427–430 (2009).
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S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
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S. Hirakawa, L. F. Brown, S. Kodama, K. Paavonen, K. Alitalo, and M. Detmar, “Vegf-c-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites,” Blood109(3), 1010–1017 (2006).
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N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
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P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
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J. Wu, R. Ma, H. Cao, Z. Wang, C. Jing, Y. Sun, Y. Zhang, Z. Yang, R. M. Hoffman, and J. Tang, “Intraoperative imaging of metastatic lymph nodes using a fluorophore-conjugated antibody in a her2/neu-expressing orthotopic breast cancer mouse model,” Anticancer Res.33(2), 419–424 (2013).
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N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
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R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
[CrossRef] [PubMed]

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M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
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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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J. W. Han, Y. J. Seo, J. E. Choi, S. H. Kang, Y. K. Bae, and S. J. Lee, “The efficacy of arm node preserving surgery using axillary reverse mapping for preventing lymphedema in patients with breast cancer,” J. Breast Cancer15(1), 91–97 (2012).
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J. E. Choi, Y. S. Jeon, S. H. Kang, and S. J. Lee, “Preservation of lymphatic drainage of arm during axillary procedure in breast cancer patients,” J. Breast Cancer12(3), 179–185 (2009).
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R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
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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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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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C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
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C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
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S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
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S. Hirakawa, L. F. Brown, S. Kodama, K. Paavonen, K. Alitalo, and M. Detmar, “Vegf-c-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites,” Blood109(3), 1010–1017 (2006).
[CrossRef] [PubMed]

Diaz, Z.

C. Boneti, S. Korourian, Z. Diaz, C. Santiago, S. Mumford, L. Adkins, and V. S. Klimberg, “Scientific impact award: Axillary reverse mapping (arm) to identify and protect lymphatics draining the arm during axillary lymphadenectomy,” Am. J. Surg.198(4), 482–487 (2009).
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D. Murawa, C. Hirche, S. Dresel, and M. Hünerbein, “Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence,” Br. J. Surg.96(11), 1289–1294 (2009).
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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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N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
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P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
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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).
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J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol.20(1), 74–82 (2009).
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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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A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
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Gillies, R. J.

N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
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S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
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P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
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N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
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Guilliod, R.

P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
[CrossRef] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
[CrossRef] [PubMed]

Han, J. W.

J. W. Han, Y. J. Seo, J. E. Choi, S. H. Kang, Y. K. Bae, and S. J. Lee, “The efficacy of arm node preserving surgery using axillary reverse mapping for preventing lymphedema in patients with breast cancer,” J. Breast Cancer15(1), 91–97 (2012).
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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).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
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Hattori, A.

A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

Heath, C. H.

C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
[CrossRef] [PubMed]

Henry-Tillman, R.

M. Thompson, S. Korourian, R. Henry-Tillman, L. Adkins, S. Mumford, K. C. Westbrook, and V. S. Klimberg, “Axillary reverse mapping (arm): A new concept to identify and enhance lymphatic preservation,” Ann. Surg. Oncol.14(6), 1890–1895 (2007).
[CrossRef] [PubMed]

Hirakawa, S.

S. Hirakawa, L. F. Brown, S. Kodama, K. Paavonen, K. Alitalo, and M. Detmar, “Vegf-c-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites,” Blood109(3), 1010–1017 (2006).
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A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

Hirche, C.

D. Murawa, C. Hirche, S. Dresel, and M. Hünerbein, “Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence,” Br. J. Surg.96(11), 1289–1294 (2009).
[CrossRef] [PubMed]

Hoffman, R. M.

J. Wu, R. Ma, H. Cao, Z. Wang, C. Jing, Y. Sun, Y. Zhang, Z. Yang, R. M. Hoffman, and J. Tang, “Intraoperative imaging of metastatic lymph nodes using a fluorophore-conjugated antibody in a her2/neu-expressing orthotopic breast cancer mouse model,” Anticancer Res.33(2), 419–424 (2013).
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Horenblas, S.

J. A. P. Leijte, I. M. C. 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]

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]

Huang, C. C.

C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
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D. Murawa, C. Hirche, S. Dresel, and M. Hünerbein, “Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence,” Br. J. Surg.96(11), 1289–1294 (2009).
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Hunt, K. K.

I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
[PubMed]

Hurley, K. E.

S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
[CrossRef] [PubMed]

Hutteman, M.

J. R. van der Vorst, B. E. Schaafsma, F. P. Verbeek, M. Hutteman, J. S. Mieog, C. W. Lowik, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients,” Ann. Surg. Oncol.19(13), 4104–4111 (2012).
[CrossRef] [PubMed]

Ikeda, T.

T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

Inomoto, T.

T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer12(3), 211–215 (2005).
[CrossRef] [PubMed]

Inoue, H.

A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
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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).
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J. E. Choi, Y. S. Jeon, S. H. Kang, and S. J. Lee, “Preservation of lymphatic drainage of arm during axillary procedure in breast cancer patients,” J. Breast Cancer12(3), 179–185 (2009).
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R. C. Ji, “Lymph node lymphangiogenesis: A new concept for modulating tumor metastasis and inflammatory process,” Histol. Histopathol.24(3), 377–384 (2009).
[PubMed]

Jing, C.

J. Wu, R. Ma, H. Cao, Z. Wang, C. Jing, Y. Sun, Y. Zhang, Z. Yang, R. M. Hoffman, and J. Tang, “Intraoperative imaging of metastatic lymph nodes using a fluorophore-conjugated antibody in a her2/neu-expressing orthotopic breast cancer mouse model,” Anticancer Res.33(2), 419–424 (2013).
[PubMed]

Jones, L.

G. C. Wishart, S. W. Loh, L. Jones, and J. R. Benson, “A feasibility study (icg-10) of indocyanine green (icg) fluorescence mapping for sentinel lymph node detection in early breast cancer,” Eur. J. Surg. Oncol.38(8), 651–656 (2012).
[CrossRef] [PubMed]

Kallan, M. J.

S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
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A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
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Kang, S. H.

J. W. Han, Y. J. Seo, J. E. Choi, S. H. Kang, Y. K. Bae, and S. J. Lee, “The efficacy of arm node preserving surgery using axillary reverse mapping for preventing lymphedema in patients with breast cancer,” J. Breast Cancer15(1), 91–97 (2012).
[CrossRef] [PubMed]

J. E. Choi, Y. S. Jeon, S. H. Kang, and S. J. Lee, “Preservation of lymphatic drainage of arm during axillary procedure in breast cancer patients,” J. Breast Cancer12(3), 179–185 (2009).
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T. Karpanen and K. Alitalo, “Molecular biology and pathology of lymphangiogenesis,” Annu. Rev. Pathol.3(1), 367–397 (2008).
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M. Takeuchi, T. Sugie, K. Abdelazeem, H. Kato, N. Shinkura, M. Takada, H. Yamashiro, T. Ueno, and M. Toi, “Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer,” Breast J.18(6), 535–541 (2012).
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A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

King, P. D.

P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
[CrossRef] [PubMed]

Kinoshita, J.

A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

Kinoshita, T.

T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

Kitai, T.

T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer12(3), 211–215 (2005).
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Klimberg, V. S.

C. Boneti, S. Korourian, Z. Diaz, C. Santiago, S. Mumford, L. Adkins, and V. S. Klimberg, “Scientific impact award: Axillary reverse mapping (arm) to identify and protect lymphatics draining the arm during axillary lymphadenectomy,” Am. J. Surg.198(4), 482–487 (2009).
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M. Thompson, S. Korourian, R. Henry-Tillman, L. Adkins, S. Mumford, K. C. Westbrook, and V. S. Klimberg, “Axillary reverse mapping (arm): A new concept to identify and enhance lymphatic preservation,” Ann. Surg. Oncol.14(6), 1890–1895 (2007).
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S. Hirakawa, L. F. Brown, S. Kodama, K. Paavonen, K. Alitalo, and M. Detmar, “Vegf-c-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites,” Blood109(3), 1010–1017 (2006).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
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Korourian, S.

C. Boneti, S. Korourian, Z. Diaz, C. Santiago, S. Mumford, L. Adkins, and V. S. Klimberg, “Scientific impact award: Axillary reverse mapping (arm) to identify and protect lymphatics draining the arm during axillary lymphadenectomy,” Am. J. Surg.198(4), 482–487 (2009).
[CrossRef] [PubMed]

M. Thompson, S. Korourian, R. Henry-Tillman, L. Adkins, S. Mumford, K. C. Westbrook, and V. S. Klimberg, “Axillary reverse mapping (arm): A new concept to identify and enhance lymphatic preservation,” Ann. Surg. Oncol.14(6), 1890–1895 (2007).
[CrossRef] [PubMed]

Krishnamurthy, S.

I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
[PubMed]

Kuerer, H. M.

I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
[PubMed]

Kwant, G.

M. L. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, “Light-absorbing properties, stability, and spectral stabilization of indocyanine green,” J. Appl. Physiol.40(4), 575–583 (1976).
[PubMed]

Kwon, S.

P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
[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]

M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
[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]

Lachance, P.-A.

M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
[CrossRef] [PubMed]

Landsman, M. L.

M. L. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, “Light-absorbing properties, stability, and spectral stabilization of indocyanine green,” J. Appl. Physiol.40(4), 575–583 (1976).
[PubMed]

Lapinski, P. E.

P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
[CrossRef] [PubMed]

Lee, S. J.

J. W. Han, Y. J. Seo, J. E. Choi, S. H. Kang, Y. K. Bae, and S. J. Lee, “The efficacy of arm node preserving surgery using axillary reverse mapping for preventing lymphedema in patients with breast cancer,” J. Breast Cancer15(1), 91–97 (2012).
[CrossRef] [PubMed]

J. E. Choi, Y. S. Jeon, S. H. Kang, and S. J. Lee, “Preservation of lymphatic drainage of arm during axillary procedure in breast cancer patients,” J. Breast Cancer12(3), 179–185 (2009).
[CrossRef]

Leijte, J. A. P.

J. A. P. Leijte, I. M. C. 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]

Liefers, G. J.

B. E. Schaafsma, F. P. Verbeek, D. D. Rietbergen, B. van der Hiel, J. R. van der Vorst, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, F. W. van Leeuwen, and A. L. Vahrmeijer, “Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer,” Br. J. Surg.100(8), 1037–1044 (2013).
[CrossRef] [PubMed]

J. R. van der Vorst, B. E. Schaafsma, F. P. Verbeek, M. Hutteman, J. S. Mieog, C. W. Lowik, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients,” Ann. Surg. Oncol.19(13), 4104–4111 (2012).
[CrossRef] [PubMed]

Lloyd, M. C.

N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
[CrossRef] [PubMed]

Localio, A. R.

S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
[CrossRef] [PubMed]

Loh, S. W.

G. C. Wishart, S. W. Loh, L. Jones, and J. R. Benson, “A feasibility study (icg-10) of indocyanine green (icg) fluorescence mapping for sentinel lymph node detection in early breast cancer,” Eur. J. Surg. Oncol.38(8), 651–656 (2012).
[CrossRef] [PubMed]

Lopez, A. S.

N. K. Tafreshi, M. M. Bui, K. Bishop, M. C. Lloyd, S. A. Enkemann, A. S. Lopez, D. Abrahams, B. W. Carter, J. Vagner, S. R. Grobmyer, R. J. Gillies, and D. L. Morse, “Noninvasive detection of breast cancer lymph node metastasis using carbonic anhydrases ix and xii targeted imaging probes,” Clin. Cancer Res.18(1), 207–219 (2012).
[CrossRef] [PubMed]

Lowik, C. W.

J. R. van der Vorst, B. E. Schaafsma, F. P. Verbeek, M. Hutteman, J. S. Mieog, C. W. Lowik, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients,” Ann. Surg. Oncol.19(13), 4104–4111 (2012).
[CrossRef] [PubMed]

Ma, R.

J. Wu, R. Ma, H. Cao, Z. Wang, C. Jing, Y. Sun, Y. Zhang, Z. Yang, R. M. Hoffman, and J. Tang, “Intraoperative imaging of metastatic lymph nodes using a fluorophore-conjugated antibody in a her2/neu-expressing orthotopic breast cancer mouse model,” Anticancer Res.33(2), 419–424 (2013).
[PubMed]

Maggiorotto, F.

R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
[CrossRef] [PubMed]

Marshall, M. V.

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]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol.20(1), 74–82 (2009).
[CrossRef] [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.

P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
[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]

McLaughlin, S. A.

S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
[CrossRef] [PubMed]

Meric-Bernstam, F.

I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
[PubMed]

Mieog, J. S.

J. R. van der Vorst, B. E. Schaafsma, F. P. Verbeek, M. Hutteman, J. S. Mieog, C. W. Lowik, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients,” Ann. Surg. Oncol.19(13), 4104–4111 (2012).
[CrossRef] [PubMed]

Miller, L. T.

S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
[CrossRef] [PubMed]

Mininanni, P.

R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
[CrossRef] [PubMed]

Mittendorf, E. A.

I. Bedrosian, G. V. Babiera, E. A. Mittendorf, H. M. Kuerer, L. Pantoja, K. K. Hunt, S. Krishnamurthy, and F. Meric-Bernstam, “A phase i study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients,” Cancer116(11), 2543–2548 (2010).
[PubMed]

Miwa, M.

T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer12(3), 211–215 (2005).
[CrossRef] [PubMed]

Miyamoto, R.

A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

Mook, G. A.

M. L. Landsman, G. Kwant, G. A. Mook, and W. G. Zijlstra, “Light-absorbing properties, stability, and spectral stabilization of indocyanine green,” J. Appl. Physiol.40(4), 575–583 (1976).
[PubMed]

Morris, K. T.

S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
[CrossRef] [PubMed]

Morris, M. E.

F. Wu, M. Tamhane, and M. E. Morris, “Pharmacokinetics, lymph node uptake, and mechanistic pk model of near-infrared dye-labeled bevacizumab after iv and sc administration in mice,” AAPS J.14(2), 252–261 (2012).
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A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
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J. A. Petrek, R. T. Senie, M. Peters, and P. P. Rosen, “Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis,” Cancer92(6), 1368–1377 (2001).
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Petrek, J. A.

J. A. Petrek, R. T. Senie, M. Peters, and P. P. Rosen, “Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis,” Cancer92(6), 1368–1377 (2001).
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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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T. B. Britton, C. K. Solanki, S. E. Pinder, P. S. Mortimer, A. M. Peters, and A. D. Purushotham, “Lymphatic drainage pathways of the breast and the upper limb,” Nucl. Med. Commun.30(6), 427–430 (2009).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
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S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
[CrossRef] [PubMed]

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M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
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T. B. Britton, C. K. Solanki, S. E. Pinder, P. S. Mortimer, A. M. Peters, and A. D. Purushotham, “Lymphatic drainage pathways of the breast and the upper limb,” Nucl. Med. Commun.30(6), 427–430 (2009).
[CrossRef] [PubMed]

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M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
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P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
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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]

B. Zhu, I.-C. Tan, J. C. Rasmussen, and E. M. Sevick-Muraca, “Validating the sensitivity and performance of near-infrared fluorescence imaging and tomography devices using a novel solid phantom and measurement approach,” Technol. Cancer Res. Treat.11(1), 95–104 (2012).
[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]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol.20(1), 74–82 (2009).
[CrossRef] [PubMed]

E. M. Sevick-Muraca and J. C. Rasmussen, “Molecular imaging with optics: Primer and case for near-infrared fluorescence techniques in personalized medicine,” J. Biomed. Opt.13(4), 041303 (2008).
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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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S. A. McLaughlin, M. J. Wright, K. T. Morris, G. L. Giron, M. R. Sampson, J. P. Brockway, K. E. Hurley, E. R. Riedel, and K. J. Van Zee, “Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: Objective measurements,” J. Clin. Oncol.26(32), 5213–5219 (2008).
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B. E. Schaafsma, F. P. Verbeek, D. D. Rietbergen, B. van der Hiel, J. R. van der Vorst, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, F. W. van Leeuwen, and A. L. Vahrmeijer, “Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer,” Br. J. Surg.100(8), 1037–1044 (2013).
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M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (2012).
[CrossRef] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
[CrossRef] [PubMed]

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J. A. Petrek, R. T. Senie, M. Peters, and P. P. Rosen, “Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis,” Cancer92(6), 1368–1377 (2001).
[CrossRef] [PubMed]

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C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
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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).
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[CrossRef] [PubMed]

L. Sampath, W. Wang, and E. M. Sevick-Muraca, “Near infrared fluorescent optical imaging for nodal staging,” J. Biomed. Opt.13(4), 041312 (2008).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

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B. E. Schaafsma, F. P. Verbeek, D. D. Rietbergen, B. van der Hiel, J. R. van der Vorst, G. J. Liefers, J. V. Frangioni, C. J. van de Velde, F. W. van Leeuwen, and A. L. Vahrmeijer, “Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer,” Br. J. Surg.100(8), 1037–1044 (2013).
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J. A. Petrek, R. T. Senie, M. Peters, and P. P. Rosen, “Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis,” Cancer92(6), 1368–1377 (2001).
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E. M. Sevick-Muraca and B. Zhu, “The need for performance standards in clinical translation and adoption of fluorescence molecular imaging,” Med. Phys.40(4), 040402 (2013).
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P. E. Burrows, M. L. Gonzalez-Garay, J. C. Rasmussen, M. B. Aldrich, R. Guilliod, E. A. Maus, C. E. Fife, S. Kwon, P. E. Lapinski, P. D. King, and E. M. Sevick-Muraca, “Lymphatic abnormalities are associated with rasa1 gene mutations in mouse and man,” Proc. Natl. Acad. Sci. U.S.A.110(21), 8621–8626 (2013).
[CrossRef] [PubMed]

B. Zhu, I.-C. Tan, J. C. Rasmussen, and E. M. Sevick-Muraca, “Validating the sensitivity and performance of near-infrared fluorescence imaging and tomography devices using a novel solid phantom and measurement approach,” Technol. Cancer Res. Treat.11(1), 95–104 (2012).
[PubMed]

M. A. Hall, K. L. Pinkston, N. Wilganowski, H. Robinson, P. Ghosh, A. Azhdarinia, K. Vazquez-Arreguin, A. M. Kolonin, B. R. Harvey, and E. M. Sevick-Muraca, “Comparison of mabs targeting epithelial cell adhesion molecule for the detection of prostate cancer lymph node metastases with multimodal contrast agents: Quantitative small-animal pet/ct and nirf,” J. Nucl. Med.53(9), 1427–1437 (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]

M. A. Hall, S. Kwon, H. Robinson, P.-A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate72(2), 129–146 (2012).
[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]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol.20(1), 74–82 (2009).
[CrossRef] [PubMed]

E. M. Sevick-Muraca and J. C. Rasmussen, “Molecular imaging with optics: Primer and case for near-infrared fluorescence techniques in personalized medicine,” J. Biomed. Opt.13(4), 041303 (2008).
[CrossRef] [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]

L. Sampath, W. Wang, and E. M. Sevick-Muraca, “Near infrared fluorescent optical imaging for nodal staging,” J. Biomed. Opt.13(4), 041312 (2008).
[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).
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T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer12(3), 211–215 (2005).
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T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

Shimizu, T.

A. Hirano, M. Kamimura, K. Ogura, N. Kim, A. Hattori, Y. Setoguchi, F. Okubo, H. Inoue, R. Miyamoto, J. Kinoshita, M. Fujibayashi, and T. Shimizu, “A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients,” Ann. Surg. Oncol.19(13), 4112–4116 (2012).
[CrossRef] [PubMed]

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M. Takeuchi, T. Sugie, K. Abdelazeem, H. Kato, N. Shinkura, M. Takada, H. Yamashiro, T. Ueno, and M. Toi, “Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer,” Breast J.18(6), 535–541 (2012).
[CrossRef] [PubMed]

Simoes Torpey, H. A.

S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
[CrossRef] [PubMed]

Sismondi, P.

R. Ponzone, N. T. Cont, F. Maggiorotto, E. Cassina, P. Mininanni, N. Biglia, and P. Sismondi, “Extensive nodal disease may impair axillary reverse mapping in patients with breast cancer,” J. Clin. Oncol.27(33), 5547–5551 (2009).
[CrossRef] [PubMed]

Smith, L. A.

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]

Solanki, C. K.

T. B. Britton, C. K. Solanki, S. E. Pinder, P. S. Mortimer, A. M. Peters, and A. D. Purushotham, “Lymphatic drainage pathways of the breast and the upper limb,” Nucl. Med. Commun.30(6), 427–430 (2009).
[CrossRef] [PubMed]

Solin, L. J.

S. A. Norman, A. R. Localio, S. L. Potashnik, H. A. Simoes Torpey, M. J. Kallan, A. L. Weber, L. T. Miller, A. Demichele, and L. J. Solin, “Lymphedema in breast cancer survivors: Incidence, degree, time course, treatment, and symptoms,” J. Clin. Oncol.27(3), 390–397 (2008).
[CrossRef] [PubMed]

Sugie, T.

T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

M. Takeuchi, T. Sugie, K. Abdelazeem, H. Kato, N. Shinkura, M. Takada, H. Yamashiro, T. Ueno, and M. Toi, “Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer,” Breast J.18(6), 535–541 (2012).
[CrossRef] [PubMed]

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J. Wu, R. Ma, H. Cao, Z. Wang, C. Jing, Y. Sun, Y. Zhang, Z. Yang, R. M. Hoffman, and J. Tang, “Intraoperative imaging of metastatic lymph nodes using a fluorophore-conjugated antibody in a her2/neu-expressing orthotopic breast cancer mouse model,” Anticancer Res.33(2), 419–424 (2013).
[PubMed]

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T. Sugie, T. Sawada, N. Tagaya, T. Kinoshita, K. Yamagami, H. Suwa, T. Ikeda, K. Yoshimura, M. Niimi, A. Shimizu, and M. Toi, “Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer,” Ann. Surg. Oncol.20(7), 2213–2218 (2013).
[CrossRef] [PubMed]

Sweeny, L.

C. H. Heath, N. L. Deep, L. N. Beck, K. E. Day, L. Sweeny, K. R. Zinn, C. C. Huang, and E. L. Rosenthal, “Use of panitumumab-irdye800 to image cutaneous head and neck cancer in mice,” Otolaryngol. Head Neck Surg.148(6), 982–990 (2013).
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Supplementary Material (1)

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Figures (6)

Fig. 1
Fig. 1

Typical injection sites in the arm and diseased breast. The solid arrows indicate the location of seven intradermal injections administered in the arm, while the dashed arrows indicate a subareolar injection and four intraparenchymal injections administered in the quadrants of the breast.

Fig. 2
Fig. 2

Image of (a) the intraoperative imaging system used to assess lymphatic drainage of the arm and breast in the operating suite and (b) the ex vivo imaging system to assess the fluorescent status of the excised lymph nodes in the pathology suite.

Fig. 3
Fig. 3

(a) Image montage of lymphatic vasculature in the arm, axilla, and breast of subject (B20). While most of the lymphatics are linear and well-defined, atypical tortuous lymphatics are noted in the arm (inset box) and the drainage areas from the areola towards both the sternum and the axilla. (b) Image of axillary lymph nodes (subject B20). (c) Network of lymphatic capillaries in the upper outer quadrant of the breast in subject B01. The surgical markings are also visible as dark lines. (d) Image of lymphatic drainage towards a possible internal mammary lymph node near the sternum (subject B13). (e) Intraoperative image of fluorescent lymph nodes in the exposed axilla of subject B11. The fluorescence image is overlaid on a white light image for improved anatomical reference. Injection sites in (a), (b) and (d) are covered by round bandages.

Fig. 4
Fig. 4

(a) Color image and (b) near-infrared fluorescence image in pseudo color images of resected lymph nodes on the imaging grid (subject B19). (c) and (f) Color images of resected lymph nodes (subjects B19 and B08 respectively), (d) and (g) near-infrared fluorescence images, and (e) and (h) images of the corresponding slides from pathology. The presence of two distinct nodes in the elongated tissue sample in (c) are clearly seen in (d) and (e), and the locations of the NIRF signals also correspond well with the presence of the nodal tissues in the other stained slices (e) and (h). Note, due to pathologic processing, the scale, orientation, and cross section of the specimens in (e) and (h) are not necessarily the same as their corresponding color and NIRF images.

Fig. 5
Fig. 5

(a) Image of the multi-welled phantom containing 0 to 1.0 nM Qdot 800 fluorophore. (b) Image of the typical fluorescence image detected across all the gains. (c) Fluorescence intensity profile of a line drawn across the center of the wells shown in (b). The minimum detectable signal was determined by calculating the SNR between the 0.4 nM and the 0 nM wells.

Fig. 6
Fig. 6

Plot of the minimum detectable signal-to-noise ratio as a function of the gain for the ex vivo imager (EMCCD, dots) and the intraoperative imager (intensified CCD, circles).

Tables (2)

Tables Icon

Table 1 Demographics of female breast cancer subjects enrolled in the study.

Tables Icon

Table 2 Summary of specimen status for each subject.

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