Abstract

Secondary lymphedema is an acquired lymphatic disorder, which occurs because of damage to the lymphatic system from surgery and/or radiation therapy for cancer treatment. However, it remains unknown how post-nodal collecting lymphatic vessels (CLVs) draining to the surgical wound area change in response to lymphadenectomy. We investigated functional and architectural changes of inguinal-to-axillary internodal CLVs (ICLVs) in mice after a single axillary LN (ALN) dissection using near-infrared fluorescence imaging. Our data showed no lymph flow in the ICLVs draining from the inguinal LN (ILN) at 2 days post-surgery. External compression enabled visualization of a small segment of contractile fluorescent ICLVs, but not all the way to the axillary region. At day 6, abnormal lymphatic drainage patterns, including lateral and retrograde lymph flow via vessels branching off the ICLVs were observed, which started to disappear beginning 9 days after surgery. The administration of vascular endothelial growth factor (VEGF)-C into the wound increased resolution of altered lymphatic drainage. Lymphatic drainage from the base of the tail to the ILN did not significantly change over time. These results demonstrate that lymph flow in the CLVs is dramatically affected by a LN dissection and long-term interruption of lymph flow might cause CLV dysfunction and thus contribute to chronic lymphatic disorders.

© 2016 Optical Society of America

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  32. H. Hoshi, K. Kamiya, H. Aijima, K. Yoshida, and E. Endo, “Histological observations on rat popliteal lymph nodes after blockage of their afferent lymphatics,” Arch. Histol. Jpn. 48(2), 135–148 (1985).
    [Crossref] [PubMed]
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    [PubMed]

2015 (2)

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

T. Kodama, Y. Hatakeyama, S. Kato, and S. Mori, “Visualization of fluid drainage pathways in lymphatic vessels and lymph nodes using a mouse model to test a lymphatic drug delivery system,” Biomed. Opt. Express 6(1), 124–134 (2015).
[Crossref] [PubMed]

2014 (4)

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

S. Kwon, G. D. Agollah, G. Wu, and E. M. Sevick-Muraca, “Spatio-temporal changes of lymphatic contractility and drainage patterns following lymphadenectomy in mice,” PLoS One 9(8), e106034 (2014).
[Crossref] [PubMed]

E. M. Sevick-Muraca, S. Kwon, and J. C. Rasmussen, “Emerging lymphatic imaging technologies for mouse and man,” J. Clin. Invest. 124(3), 905–914 (2014).
[Crossref] [PubMed]

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[Crossref] [PubMed]

2013 (5)

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]

K. S. Blum, S. T. Proulx, P. Luciani, J. C. Leroux, and M. Detmar, “Dynamics of lymphatic regeneration and flow patterns after lymph node dissection,” Breast Cancer Res. Treat. 139(1), 81–86 (2013).
[Crossref] [PubMed]

M. Hofmann, R. Pflanzer, N. N. Zoller, A. Bernd, R. Kaufmann, D. Thaci, J. Bereiter-Hahn, S. Hirohata, and S. Kippenberger, “Vascular endothelial growth factor C-induced lymphangiogenesis decreases tumor interstitial fluid pressure and tumor,” Transl. Oncol. 6(4), 398–404 (2013).
[Crossref] [PubMed]

E. Bazigou and T. Makinen, “Flow control in our vessels: vascular valves make sure there is no way back,” Cell. Mol. Life Sci. 70(6), 1055–1066 (2013).
[Crossref] [PubMed]

M. A. Hall, H. Robinson, W. Chan, and E. M. Sevick-Muraca, “Detection of lymphangiogenesis by near-infrared fluorescence imaging and responses to VEGF-C during healing in a mouse full-dermis thickness wound model,” Wound Repair Regen. 21(4), 604–615 (2013).
[Crossref] [PubMed]

2012 (7)

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

J. C. Zampell, A. Yan, S. Elhadad, T. Avraham, E. Weitman, and B. J. Mehrara, “CD4(+) cells regulate fibrosis and lymphangiogenesis in response to lymphatic fluid stasis,” PLoS One 7(11), e49940 (2012).
[Crossref] [PubMed]

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[Crossref] [PubMed]

S. Kwon, C. Davies-Venn, and E. M. Sevick-Muraca, “In vivo dynamic imaging of intestinal motions using diet-related autofluorescence,” Neurogastroenterol. Motil. 24(5), 494–497 (2012).
[Crossref] [PubMed]

U. Mendez, E. M. Brown, E. L. Ongstad, J. R. Slis, and J. Goldman, “Functional recovery of fluid drainage precedes lymphangiogenesis in acute murine foreleg lymphedema,” Am. J. Physiol. Heart Circ. Physiol. 302(11), H2250–H2256 (2012).
[Crossref] [PubMed]

U. Mendez, E. M. Stroup, L. L. Lynch, A. B. Waller, and J. Goldman, “A chronic and latent lymphatic insufficiency follows recovery from acute lymphedema in the rat foreleg,” Am. J. Physiol. Heart Circ. Physiol. 303(9), H1107–H1113 (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]

2011 (3)

J. C. Zampell, A. Yan, T. Avraham, V. Andrade, S. Malliaris, S. Aschen, S. G. Rockson, and B. J. Mehrara, “Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema,” Am. J. Physiol. Cell Physiol. 300(5), C1107–C1121 (2011).
[Crossref] [PubMed]

K. Alitalo, “The lymphatic vasculature in disease,” Nat. Med. 17(11), 1371–1380 (2011).
[Crossref] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Mouse phenotyping with near-infrared fluorescence lymphatic imaging,” Biomed. Opt. Express 2(6), 1403–1411 (2011).
[Crossref] [PubMed]

2010 (2)

Y. Wang and G. Oliver, “Current views on the function of the lymphatic vasculature in health and disease,” Genes Dev. 24(19), 2115–2126 (2010).
[Crossref] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods 360(1-2), 167–172 (2010).
[Crossref] [PubMed]

2007 (3)

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]

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

2003 (1)

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

2002 (2)

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

2001 (1)

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

1991 (1)

R. E. Mebius, P. R. Streeter, J. Brevé, A. M. Duijvestijn, and G. Kraal, “The influence of afferent lymphatic vessel interruption on vascular addressin expression,” J. Cell Biol. 115(1), 85–95 (1991).
[Crossref] [PubMed]

1985 (1)

H. Hoshi, K. Kamiya, H. Aijima, K. Yoshida, and E. Endo, “Histological observations on rat popliteal lymph nodes after blockage of their afferent lymphatics,” Arch. Histol. Jpn. 48(2), 135–148 (1985).
[Crossref] [PubMed]

1983 (1)

J. H. Wolfe, D. Rutt, and J. B. Kinmonth, “Lymphatic obstruction and lymph node changes--a study of the rabbit popliteal node,” Lymphology 16(1), 19–26 (1983).
[PubMed]

1982 (1)

G. Steinmann, E. Földi, M. Földi, P. Rácz, and K. Lennert, “Morphologic findings in lymph nodes after occlusion of their efferent lymphatic vessels and veins,” Lab. Invest. 47(1), 43–50 (1982).
[PubMed]

Abo-Ramadan, U.

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

Achen, M. G.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Agollah, G. D.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[Crossref] [PubMed]

S. Kwon, G. D. Agollah, G. Wu, and E. M. Sevick-Muraca, “Spatio-temporal changes of lymphatic contractility and drainage patterns following lymphadenectomy in mice,” PLoS One 9(8), e106034 (2014).
[Crossref] [PubMed]

Aijima, H.

H. Hoshi, K. Kamiya, H. Aijima, K. Yoshida, and E. Endo, “Histological observations on rat popliteal lymph nodes after blockage of their afferent lymphatics,” Arch. Histol. Jpn. 48(2), 135–148 (1985).
[Crossref] [PubMed]

Aldrich, M. B.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[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]

Alitalo, K.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

K. Alitalo, “The lymphatic vasculature in disease,” Nat. Med. 17(11), 1371–1380 (2011).
[Crossref] [PubMed]

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

Andrade, V.

J. C. Zampell, A. Yan, T. Avraham, V. Andrade, S. Malliaris, S. Aschen, S. G. Rockson, and B. J. Mehrara, “Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema,” Am. J. Physiol. Cell Physiol. 300(5), C1107–C1121 (2011).
[Crossref] [PubMed]

Antila, S.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

Araki, J.

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[Crossref] [PubMed]

Ardipradja, K.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Aschen, S.

J. C. Zampell, A. Yan, T. Avraham, V. Andrade, S. Malliaris, S. Aschen, S. G. Rockson, and B. J. Mehrara, “Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema,” Am. J. Physiol. Cell Physiol. 300(5), C1107–C1121 (2011).
[Crossref] [PubMed]

Ashare, A.

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

Aspelund, A.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

Avraham, T.

J. C. Zampell, A. Yan, S. Elhadad, T. Avraham, E. Weitman, and B. J. Mehrara, “CD4(+) cells regulate fibrosis and lymphangiogenesis in response to lymphatic fluid stasis,” PLoS One 7(11), e49940 (2012).
[Crossref] [PubMed]

J. C. Zampell, A. Yan, T. Avraham, V. Andrade, S. Malliaris, S. Aschen, S. G. Rockson, and B. J. Mehrara, “Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema,” Am. J. Physiol. Cell Physiol. 300(5), C1107–C1121 (2011).
[Crossref] [PubMed]

Baldwin, M. E.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Bass, S. S.

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

Bazigou, E.

E. Bazigou and T. Makinen, “Flow control in our vessels: vascular valves make sure there is no way back,” Cell. Mol. Life Sci. 70(6), 1055–1066 (2013).
[Crossref] [PubMed]

Bereiter-Hahn, J.

M. Hofmann, R. Pflanzer, N. N. Zoller, A. Bernd, R. Kaufmann, D. Thaci, J. Bereiter-Hahn, S. Hirohata, and S. Kippenberger, “Vascular endothelial growth factor C-induced lymphangiogenesis decreases tumor interstitial fluid pressure and tumor,” Transl. Oncol. 6(4), 398–404 (2013).
[Crossref] [PubMed]

Berman, C.

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

Bernd, A.

M. Hofmann, R. Pflanzer, N. N. Zoller, A. Bernd, R. Kaufmann, D. Thaci, J. Bereiter-Hahn, S. Hirohata, and S. Kippenberger, “Vascular endothelial growth factor C-induced lymphangiogenesis decreases tumor interstitial fluid pressure and tumor,” Transl. Oncol. 6(4), 398–404 (2013).
[Crossref] [PubMed]

Beynet, D. P.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Blum, K. S.

K. S. Blum, S. T. Proulx, P. Luciani, J. C. Leroux, and M. Detmar, “Dynamics of lymphatic regeneration and flow patterns after lymph node dissection,” Breast Cancer Res. Treat. 139(1), 81–86 (2013).
[Crossref] [PubMed]

Bouvet, M.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Brevé, J.

R. E. Mebius, P. R. Streeter, J. Brevé, A. M. Duijvestijn, and G. Kraal, “The influence of afferent lymphatic vessel interruption on vascular addressin expression,” J. Cell Biol. 115(1), 85–95 (1991).
[Crossref] [PubMed]

Brown, E. M.

U. Mendez, E. M. Brown, E. L. Ongstad, J. R. Slis, and J. Goldman, “Functional recovery of fluid drainage precedes lymphangiogenesis in acute murine foreleg lymphedema,” Am. J. Physiol. Heart Circ. Physiol. 302(11), H2250–H2256 (2012).
[Crossref] [PubMed]

Bueler, H.

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

Burrows, 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]

Caesar, C.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Chai, M. G.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Chan, W.

M. A. Hall, H. Robinson, W. Chan, and E. M. Sevick-Muraca, “Detection of lymphangiogenesis by near-infrared fluorescence imaging and responses to VEGF-C during healing in a mouse full-dermis thickness wound model,” Wound Repair Regen. 21(4), 604–615 (2013).
[Crossref] [PubMed]

Chang, J.

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

Cox, C. E.

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

Curry, C.

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

Dakhil, N.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Darne, C.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[Crossref] [PubMed]

Davies, P. F.

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

Davies-Venn, C.

S. Kwon, C. Davies-Venn, and E. M. Sevick-Muraca, “In vivo dynamic imaging of intestinal motions using diet-related autofluorescence,” Neurogastroenterol. Motil. 24(5), 494–497 (2012).
[Crossref] [PubMed]

Detmar, M.

K. S. Blum, S. T. Proulx, P. Luciani, J. C. Leroux, and M. Detmar, “Dynamics of lymphatic regeneration and flow patterns after lymph node dissection,” Breast Cancer Res. Treat. 139(1), 81–86 (2013).
[Crossref] [PubMed]

Duijvestijn, A. M.

R. E. Mebius, P. R. Streeter, J. Brevé, A. M. Duijvestijn, and G. Kraal, “The influence of afferent lymphatic vessel interruption on vascular addressin expression,” J. Cell Biol. 115(1), 85–95 (1991).
[Crossref] [PubMed]

Dupont, E.

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

Elhadad, S.

J. C. Zampell, A. Yan, S. Elhadad, T. Avraham, E. Weitman, and B. J. Mehrara, “CD4(+) cells regulate fibrosis and lymphangiogenesis in response to lymphatic fluid stasis,” PLoS One 7(11), e49940 (2012).
[Crossref] [PubMed]

Endo, E.

H. Hoshi, K. Kamiya, H. Aijima, K. Yoshida, and E. Endo, “Histological observations on rat popliteal lymph nodes after blockage of their afferent lymphatics,” Arch. Histol. Jpn. 48(2), 135–148 (1985).
[Crossref] [PubMed]

Enholm, B.

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

Farnsworth, R. H.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Fife, C. E.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[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]

Földi, E.

G. Steinmann, E. Földi, M. Földi, P. Rácz, and K. Lennert, “Morphologic findings in lymph nodes after occlusion of their efferent lymphatic vessels and veins,” Lab. Invest. 47(1), 43–50 (1982).
[PubMed]

Földi, M.

G. Steinmann, E. Földi, M. Földi, P. Rácz, and K. Lennert, “Morphologic findings in lymph nodes after occlusion of their efferent lymphatic vessels and veins,” Lab. Invest. 47(1), 43–50 (1982).
[PubMed]

Fox, S. B.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Francois, M.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

Fu, J.

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

Goldman, J.

U. Mendez, E. M. Brown, E. L. Ongstad, J. R. Slis, and J. Goldman, “Functional recovery of fluid drainage precedes lymphangiogenesis in acute murine foreleg lymphedema,” Am. J. Physiol. Heart Circ. Physiol. 302(11), H2250–H2256 (2012).
[Crossref] [PubMed]

U. Mendez, E. M. Stroup, L. L. Lynch, A. B. Waller, and J. Goldman, “A chronic and latent lymphatic insufficiency follows recovery from acute lymphedema in the rat foreleg,” Am. J. Physiol. Heart Circ. Physiol. 303(9), H1107–H1113 (2012).
[Crossref] [PubMed]

Gonzalez-Garay, M. L.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[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]

Goris, M. L.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Gravereaux, E.

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

Guilliod, R.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[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]

Hall, M. A.

M. A. Hall, H. Robinson, W. Chan, and E. M. Sevick-Muraca, “Detection of lymphangiogenesis by near-infrared fluorescence imaging and responses to VEGF-C during healing in a mouse full-dermis thickness wound model,” Wound Repair Regen. 21(4), 604–615 (2013).
[Crossref] [PubMed]

Hara, H.

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[Crossref] [PubMed]

Harris, N. C.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Hatakeyama, Y.

Hayashi, K.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Hayashi, Y.

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[Crossref] [PubMed]

Hess, P. R.

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

Hirohata, S.

M. Hofmann, R. Pflanzer, N. N. Zoller, A. Bernd, R. Kaufmann, D. Thaci, J. Bereiter-Hahn, S. Hirohata, and S. Kippenberger, “Vascular endothelial growth factor C-induced lymphangiogenesis decreases tumor interstitial fluid pressure and tumor,” Transl. Oncol. 6(4), 398–404 (2013).
[Crossref] [PubMed]

Hoffman, R. M.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Hofmann, M.

M. Hofmann, R. Pflanzer, N. N. Zoller, A. Bernd, R. Kaufmann, D. Thaci, J. Bereiter-Hahn, S. Hirohata, and S. Kippenberger, “Vascular endothelial growth factor C-induced lymphangiogenesis decreases tumor interstitial fluid pressure and tumor,” Transl. Oncol. 6(4), 398–404 (2013).
[Crossref] [PubMed]

Holopainen, T.

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

Hoshi, H.

H. Hoshi, K. Kamiya, H. Aijima, K. Yoshida, and E. Endo, “Histological observations on rat popliteal lymph nodes after blockage of their afferent lymphatics,” Arch. Histol. Jpn. 48(2), 135–148 (1985).
[Crossref] [PubMed]

Hu, C. S.

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K. S. Blum, S. T. Proulx, P. Luciani, J. C. Leroux, and M. Detmar, “Dynamics of lymphatic regeneration and flow patterns after lymph node dissection,” Breast Cancer Res. Treat. 139(1), 81–86 (2013).
[Crossref] [PubMed]

Quertermous, T.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Rácz, P.

G. Steinmann, E. Földi, M. Földi, P. Rácz, and K. Lennert, “Morphologic findings in lymph nodes after occlusion of their efferent lymphatic vessels and veins,” Lab. Invest. 47(1), 43–50 (1982).
[PubMed]

Rasmussen, J. C.

E. M. Sevick-Muraca, S. Kwon, and J. C. Rasmussen, “Emerging lymphatic imaging technologies for mouse and man,” J. Clin. Invest. 124(3), 905–914 (2014).
[Crossref] [PubMed]

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[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]

Reintgen, D. S.

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

Robinson, H.

M. A. Hall, H. Robinson, W. Chan, and E. M. Sevick-Muraca, “Detection of lymphangiogenesis by near-infrared fluorescence imaging and responses to VEGF-C during healing in a mouse full-dermis thickness wound model,” Wound Repair Regen. 21(4), 604–615 (2013).
[Crossref] [PubMed]

Rockson, N. B.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Rockson, S. G.

J. C. Zampell, A. Yan, T. Avraham, V. Andrade, S. Malliaris, S. Aschen, S. G. Rockson, and B. J. Mehrara, “Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema,” Am. J. Physiol. Cell Physiol. 300(5), C1107–C1121 (2011).
[Crossref] [PubMed]

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Roufail, S.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Rupasinghe, T. W.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Rutt, D.

J. H. Wolfe, D. Rutt, and J. B. Kinmonth, “Lymphatic obstruction and lymph node changes--a study of the rabbit popliteal node,” Lymphology 16(1), 19–26 (1983).
[PubMed]

Saaristo, A.

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

Saharinen, P.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

Salud, C. J.

S. S. Bass, C. E. Cox, C. J. Salud, G. H. Lyman, C. McCann, E. Dupont, C. Berman, and D. S. Reintgen, “The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer,” J. Am. Coll. Surg. 192(1), 9–16 (2001).
[Crossref] [PubMed]

Sawamoto, N.

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[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.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[Crossref] [PubMed]

S. Kwon, G. D. Agollah, G. Wu, and E. M. Sevick-Muraca, “Spatio-temporal changes of lymphatic contractility and drainage patterns following lymphadenectomy in mice,” PLoS One 9(8), e106034 (2014).
[Crossref] [PubMed]

E. M. Sevick-Muraca, S. Kwon, and J. C. Rasmussen, “Emerging lymphatic imaging technologies for mouse and man,” J. Clin. Invest. 124(3), 905–914 (2014).
[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]

M. A. Hall, H. Robinson, W. Chan, and E. M. Sevick-Muraca, “Detection of lymphangiogenesis by near-infrared fluorescence imaging and responses to VEGF-C during healing in a mouse full-dermis thickness wound model,” Wound Repair Regen. 21(4), 604–615 (2013).
[Crossref] [PubMed]

S. Kwon, C. Davies-Venn, and E. M. Sevick-Muraca, “In vivo dynamic imaging of intestinal motions using diet-related autofluorescence,” Neurogastroenterol. Motil. 24(5), 494–497 (2012).
[Crossref] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Mouse phenotyping with near-infrared fluorescence lymphatic imaging,” Biomed. Opt. Express 2(6), 1403–1411 (2011).
[Crossref] [PubMed]

S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods 360(1-2), 167–172 (2010).
[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]

Shayan, R.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Shin, W. S.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Silver, M.

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

Skobe, M.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Slis, J. R.

U. Mendez, E. M. Brown, E. L. Ongstad, J. R. Slis, and J. Goldman, “Functional recovery of fluid drainage precedes lymphangiogenesis in acute murine foreleg lymphedema,” Am. J. Physiol. Heart Circ. Physiol. 302(11), H2250–H2256 (2012).
[Crossref] [PubMed]

Sloan, E. K.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Spilman, S.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[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.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Stanczuk, L.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

Steinmann, G.

G. Steinmann, E. Földi, M. Földi, P. Rácz, and K. Lennert, “Morphologic findings in lymph nodes after occlusion of their efferent lymphatic vessels and veins,” Lab. Invest. 47(1), 43–50 (1982).
[PubMed]

Strauss, H. W.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Streeter, P. R.

R. E. Mebius, P. R. Streeter, J. Brevé, A. M. Duijvestijn, and G. Kraal, “The influence of afferent lymphatic vessel interruption on vascular addressin expression,” J. Cell Biol. 115(1), 85–95 (1991).
[Crossref] [PubMed]

Stroup, E. M.

U. Mendez, E. M. Stroup, L. L. Lynch, A. B. Waller, and J. Goldman, “A chronic and latent lymphatic insufficiency follows recovery from acute lymphedema in the rat foreleg,” Am. J. Physiol. Heart Circ. Physiol. 303(9), H1107–H1113 (2012).
[Crossref] [PubMed]

Sweet, D. T.

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

Szuba, A.

A. Szuba, M. Skobe, M. J. Karkkainen, W. S. Shin, D. P. Beynet, N. B. Rockson, N. Dakhil, S. Spilman, M. L. Goris, H. W. Strauss, T. Quertermous, K. Alitalo, and S. G. Rockson, “Therapeutic lymphangiogenesis with human recombinant VEGF-C,” FASEB J. 16(14), 1985–1987 (2002).
[PubMed]

Tammela, T.

A. Aspelund, T. Tammela, S. Antila, H. Nurmi, V. M. Leppänen, G. Zarkada, L. Stanczuk, M. Francois, T. Mäkinen, P. Saharinen, I. Immonen, and K. Alitalo, “The Schlemm’s canal is a VEGF-C/VEGFR-3-responsive lymphatic-like vessel,” J. Clin. Invest. 124(9), 3975–3986 (2014).
[Crossref] [PubMed]

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

Tan, I. C.

G. D. Agollah, M. L. Gonzalez-Garay, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, C. Darne, C. E. Fife, R. Guilliod, E. A. Maus, P. D. King, and E. M. Sevick-Muraca, “Evidence for SH2 domain-containing 5′-inositol phosphatase-2 (SHIP2) contributing to a lymphatic dysfunction,” PLoS One 9(11), e112548 (2014).
[Crossref] [PubMed]

Thaci, D.

M. Hofmann, R. Pflanzer, N. N. Zoller, A. Bernd, R. Kaufmann, D. Thaci, J. Bereiter-Hahn, S. Hirohata, and S. Kippenberger, “Vascular endothelial growth factor C-induced lymphangiogenesis decreases tumor interstitial fluid pressure and tumor,” Transl. Oncol. 6(4), 398–404 (2013).
[Crossref] [PubMed]

Tkebuchava, T.

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

Todokoro, T.

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[Crossref] [PubMed]

Tomita, K.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Tsuchiya, H.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Tull, D. L.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Veikkola, T.

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
[Crossref] [PubMed]

Waller, A. B.

U. Mendez, E. M. Stroup, L. L. Lynch, A. B. Waller, and J. Goldman, “A chronic and latent lymphatic insufficiency follows recovery from acute lymphedema in the rat foreleg,” Am. J. Physiol. Heart Circ. Physiol. 303(9), H1107–H1113 (2012).
[Crossref] [PubMed]

Wang, Y.

Y. Wang and G. Oliver, “Current views on the function of the lymphatic vasculature in health and disease,” Genes Dev. 24(19), 2115–2126 (2010).
[Crossref] [PubMed]

Wecker, A.

Y. S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C. S. Hu, M. Kearney, A. Ashare, D. G. Jackson, H. Kubo, J. M. Isner, and D. W. Losordo, “VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema,” J. Clin. Invest. 111(5), 717–725 (2003).
[Crossref] [PubMed]

Weitman, E.

J. C. Zampell, A. Yan, S. Elhadad, T. Avraham, E. Weitman, and B. J. Mehrara, “CD4(+) cells regulate fibrosis and lymphangiogenesis in response to lymphatic fluid stasis,” PLoS One 7(11), e49940 (2012).
[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]

Williams, S. P.

T. Karnezis, R. Shayan, C. Caesar, S. Roufail, N. C. Harris, K. Ardipradja, Y. F. Zhang, S. P. Williams, R. H. Farnsworth, M. G. Chai, T. W. Rupasinghe, D. L. Tull, M. E. Baldwin, E. K. Sloan, S. B. Fox, M. G. Achen, and S. A. Stacker, “VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium,” Cancer Cell 21(2), 181–195 (2012).
[Crossref] [PubMed]

Wolfe, J. H.

J. H. Wolfe, D. Rutt, and J. B. Kinmonth, “Lymphatic obstruction and lymph node changes--a study of the rabbit popliteal node,” Lymphology 16(1), 19–26 (1983).
[PubMed]

Wu, G.

S. Kwon, G. D. Agollah, G. Wu, and E. M. Sevick-Muraca, “Spatio-temporal changes of lymphatic contractility and drainage patterns following lymphadenectomy in mice,” PLoS One 9(8), e106034 (2014).
[Crossref] [PubMed]

Xia, L.

D. T. Sweet, J. M. Jiménez, J. Chang, P. R. Hess, P. Mericko-Ishizuka, J. Fu, L. Xia, P. F. Davies, and M. L. Kahn, “Lymph flow regulates collecting lymphatic vessel maturation in vivo,” J. Clin. Invest. 125(8), 2995–3007 (2015).
[Crossref] [PubMed]

Yamamoto, N.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Yamamoto, T.

M. Mihara, H. Hara, Y. Hayashi, M. Narushima, T. Yamamoto, T. Todokoro, T. Iida, N. Sawamoto, J. Araki, K. Kikuchi, N. Murai, T. Okitsu, I. Kisu, and I. Koshima, “Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy,” PLoS One 7(7), e41126 (2012).
[Crossref] [PubMed]

Yamauchi, K.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref] [PubMed]

Yan, A.

J. C. Zampell, A. Yan, S. Elhadad, T. Avraham, E. Weitman, and B. J. Mehrara, “CD4(+) cells regulate fibrosis and lymphangiogenesis in response to lymphatic fluid stasis,” PLoS One 7(11), e49940 (2012).
[Crossref] [PubMed]

J. C. Zampell, A. Yan, T. Avraham, V. Andrade, S. Malliaris, S. Aschen, S. G. Rockson, and B. J. Mehrara, “Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema,” Am. J. Physiol. Cell Physiol. 300(5), C1107–C1121 (2011).
[Crossref] [PubMed]

Ylä-Herttuala, S.

T. Tammela, A. Saaristo, T. Holopainen, J. Lyytikkä, A. Kotronen, M. Pitkonen, U. Abo-Ramadan, S. Ylä-Herttuala, T. V. Petrova, and K. Alitalo, “Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation,” Nat. Med. 13(12), 1458–1466 (2007).
[Crossref] [PubMed]

A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Ylä-Herttuala, and K. Alitalo, “Lymphangiogenic gene therapy with minimal blood vascular side effects,” J. Exp. Med. 196(6), 719–730 (2002).
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Yoon, Y. S.

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Supplementary Material (4)

NameDescription
» Visualization 1: MOV (914 KB)      NIR fluorescent image sequences from dynamic imaging show aberrant lymphatic drainage at day 6 post-lymphadenectomy.
» Visualization 2: MOV (912 KB)      NIR fluorescent image sequences from dynamic imaging show pulsatile activity through a side branch of internodal collecting lymphatic vessels at day 9 post-lymphadenectomy.
» Visualization 3: MOV (916 KB)      NIR fluorescent image sequences from dynamic imaging show another example of aberrant lymphatic drainage at day 6 post-lymphadenectomy.
» Visualization 4: MOV (855 KB)      NIR fluorescent image sequences from dynamic imaging show lymph flow in the segment of the collecting lymphatic vessels during compression in mice at day 2 post-lymphadenectomy.

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Figures (10)

Fig. 1
Fig. 1 Representative stereoscopic color images 5 mins after i.d. injection of EBD to the paw showing (A) the superficial left BLN filled with blue dye and (B) the deep ALN after skin incision. Arrow, BLN. Double arrow, ALN. Scale, 5 mm. Wrist thickness (C) and arm area (D) in mice (n = 6) were measured and the operated side was normalized to the contralateral right side.
Fig. 2
Fig. 2 A. Schematic of lymphatic drainage pathways from the base of the tail to the ILN and to the ALN after injection of ICG as well as from the paw to the BLN and to the ALN after injection of Alexa-680-BSA. The deeply located ALN and vessels are dotted. Arrow heads indicate flow direction. B. White light, NIR and FR fluorescent, and overlay images in mice prior to and 2, 6, 9, and 13 days after surgical removal of the left ALN. NIRF and FRF images were acquired 10 mins and 3 mins after i.d. injection of ICG or Alexa680-BSA, respectively. Double arrow, ICG injection site. Arrow, Alexa680-BSA injection site. Closed arrow head, ILN. Open arrow head, BLN, Open arrow, internodal collecting lymphatic vessels. Asterisk, abnormal lymphatic drainage patterns on the paw. Pound sign, FRF from the gut (See Visualization 1 and Visualization 2).
Fig. 3
Fig. 3 White light, NIR and FR fluorescent, and overlay images in mice prior to and 2, 6, and 37 days after surgical removal of the left ALN. NIRF and FRF images were acquired 10 mins and 3 mins after i.d. injection of ICG or Alexa680, respectively. Double arrow, ICG injection site. Double open arrow, backflow. Arrow, Alexa680-BSA injection site. Closed arrow head, ILN. Open arrow head, BLN, Open arrow, right ALN. Asterisk, abnormal lymphatic drainage patterns on the paw. Inset at Day 37, overlay of NIR and FR fluorescent images of an excised BLN in the bottom row at Day 37. Scale, 1mm, (see Visualization 3).
Fig. 4
Fig. 4 A. White light and NIR fluorescent images in mice prior to and 2 and 6 days after axillary lymphadenectomy. At 2 days post-surgery, NIR fluorescent images were acquired before and after external compression to the ILN (n = 4). Double arrow, ICG injection site. Closed arrow head, ILN. Open arrow head, BLN, Open arrow, internodal collecting lymphatic vessels. B. The fluorescent intensity profiles as a function of time in mice after selecting a ROI in the collecting lymphatic vessels before and after compression for one min, (see Visualization 4).
Fig. 5
Fig. 5 A. White light and fluorescent images in the left lateral side of mice prior to and 1, 2, 6, and 24 hrs after ALN removal, following i.d. injection of ICG to the base of the tail. Double arrow, ICG injection site. Arrow head, ILN. Inset, magnified image of the white rectangle region. Scale, 1 mm. B. The fluorescent intensities in the axillary region in mice (white) before and up to 24 hrs after axillary lymphadenectomy and mice with no surgery (grey). * p < 0.05 vs. non-surgery mice (n = 7/group). C. The lymphatic contraction frequency in the internodal collecting lymphatic vessels before and 10 mins after surgery. D. Representative image demonstrating lymphatic vessel contraction (before, black; after, red). * p < 0.05.
Fig. 6
Fig. 6 Intravital color images after direct injection of EBD into the ILN (A, B) and H&E images (C, D) in mice with (A) or without axillary lymphadenectomy (B). Scale, 5 mm. Inset, magnified image of the white dotted rectangle region. Arrow, branching off lymphatic vessels. Arrow head, backflow of EBD. Scale, 500 µm. Quantification of collecting lymphatic vessel area (n = 7/group) at Day 2 (E) and Day 6 (F). * p < 0.05.
Fig. 7
Fig. 7 Representative stereoscopic color images immediately after i.d. injection of EBD into the ILN, showing backflow of EBD-laden lymph in mice at 2 days post-surgery (A) as compared to control mice (B). Scale, 5 mm. Inset, magnified image of the white dotted rectangle region. Scale, 100 µm.
Fig. 8
Fig. 8 A. Intravital images of dissected left and right ILNs 2 and 6 days after axillary lymphadenectomy. B. The quantification of weight of the ILNs (n = 5/group). C. H&E and zoomed in images of left and right ILNs at 2 and 6 days post-surgery. Arrow, phagocytes containing erythrocytes (erythrophagocytosis).
Fig. 9
Fig. 9 (A) White light and NIR fluorescent images of right side of mice prior to and 2 and 6 days after surgical removal of the left ALN. Double arrow, ICG injection site. Arrow head, ILN. Open arrow, internodal collecting lymphatic vessels. Arrow head, ILN. Open arrow, internodal collecting lymphatic vessels. Double arrows, ICG injection site. (B) Quantification of lymphatic contractile function in the collecting lymphatic vessel in the contralateral right side of mice (n = 3) prior to and 2 and 6 days after left axillary lymphadenectomy.
Fig. 10
Fig. 10 NIR fluorescent images of VEGF-C (n = 11) or PBS (n = 5) treated mice prior to and 2, 6, and 10 days after surgical removal of the left ALN. Double arrow, ICG injection site. Arrow head, ILN. Open arrow, internodal collecting lymphatic vessels. Asterisk, aberrant lymphatic drainage to the contralateral ALN. Double arrows, ICG injection site.

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