Functional recovery of fluid drainage precedes lymphangiogenesis in acute murine foreleg lymphedema

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 11, 2012, Pages

  Mendez, Uziel ^a   Brown, Emily M ^a   Ongstad, Emily L ^a   Slis, Justin R ^a   Goldman, Jeremy ^a  

^a Michigan Technological University   (United States)

Author keywords

Axillary lymph node dissection; Interstitial flow; Lymphedema; Vascular endothelial growth factor receptor 3

Indexed keywords

INDOCYANINE GREEN; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3; VASCULOTROPIN RECEPTOR 3 NEUTRALIZING ANTIBODY;

ACUTE FORELEG LYMPHEDEMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXILLARY LYMPH NODE; AXILLARY LYMPH NODE EXTIRPATION; CONTROLLED STUDY; FEMALE; INTERSTITIAL FLUID; LYMPH NODE DISSECTION; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHATIC DRAINAGE; LYMPHEDEMA; LYMPHOGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES; DRAINAGE; EXTRACELLULAR FLUID; FEMALE; FORELIMB; LYMPH NODE EXCISION; LYMPHANGIOGENESIS; LYMPHEDEMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MODELS, ANIMAL; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOVERY OF FUNCTION;

EID: 84861786725     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01159.2011     Document Type: Article

References (35)

1. Avraham T, Clavin NW, Daluvoy SV, Fernandes J, Soares MS, Corderio AP, Mehrara BJ. Fibrosis is a key inhibitor of lymphatic regneration. Plast Reconstr Surg 124: 438-450, 2009.
2. Avraham T, Daluvoy S, Zampell J, Yan A, Haviv YS, Rockson SG, Mehrara BJ. Blockade of transforming growth factor-β1 accelerates lymphatic regeneration during wound repair. Am J Pathol 177: 3202- 3214, 2010.
3. Bates DO. An interstitial hypothesis for breast cancer related lymphoedema. Pathophyseology 17: 289-294, 2010.
4. Bates DO, Levick JR, Mortimer PS. Starling pressures in the human arm and their alteration in postmastectomy oedema. J Physiol 477: 355-363, 1994.
5. Bates DO, Levick JR, Mortimer PS. Subcutaneous interstitial fluid pressure and arm volume in lymphoedema. Int J Microcirc Clin Exp 11: 359-373, 1992.
6. Cheung L, Han J, Beilhack A, Joshi S, Wilburn P, Dua A, An A, Rockson SG. An experimental model for the study of lymphedema and its response to therapeutic lymphangiogenesis. Biodrugs 20: 363-370, 2006.
7. Clarke D, Martinez A, Cox RS. Analysis of cosmetic results and complications in patients with stage-I and stage-Ii breast-cancer treated by biopsy and irradiation. Int J Radiat Oncol 9: 1807-1813, 1983.
8. Clavin NW, Avraham T, Fernandez J, Daluvoy SV, Soares MA, Chaudhry A, Mehrara BJ. TGF-β1 is a negative regulator of lymphatic regeneration during wound repair. Am J Physiol Heart Circ Physiol 295: H2113-H2127, 2008.
9. Goldman J, Conley KA, Raehl A, Bondy DM, Pytowski B, Swartz MA, Rutkowksi JM, Jaroch DB, Ongstad EL. Regulation of lymphatic capillary regeneration by interstitial flow in skin. Am J Physiol Heart Circ Physiol 292: H2176-H2183, 2007.
10. Goldman J, Rutkowski JM, Shields JD, Pasquier MC, Cui Y, Schmokel HG, Willey S, Hicklin DJ, Pytowski B, Swartz MA. Cooperative and redundant roles of VEGFR-2 and VEGFR-3 signaling in adult lymphangiogenesis. FASEB J 21: 1003-1012, 2007.
11. Guyton AC, Scheel K, Murphree D. Interstitial fluid pressure. 3. Its effect on resistance to tissue fluid mobility. Circ Res 19: 412-419, 1966.
12. Ikomi F, Kawai Y, Nakayama J, Ogiwara N, Sasaki K, Mizuno R, Ohhashi T. Critical roles of VEGF-C-VEGF receptor 3 in reconnection of the collecting lymph vessels in mice. Microcirculation 15: 1-13, 2008.
13. Jin da P, An A, Liu J, Nakamura K, Rockson SG. Therapeutic responses to exogenous VEGF-C administration in experimental lymphedema: immunohistochemical and molecular characterization. Lymphat Res Biol 7: 47-57, 2009.
14. Kissin MW, Querci della Rovere G, Easton D, Westbury G. Risk of lymphoedema following the treatment of breast cancer. Br J Surg 73: 580-584, 1986.
15. Mortimer PS. The pathophysiology of lymphedema. Cancer 83: 2798-2802, 1998.
16. Mortimer PS, Bates DO, Brassington HD, Stanton AWB, Strachan DP, Levick JR. The prevalence of arm oedema following treatment for breast cancer. Qjm-Mon J Assoc Phys 89: 377-380, 1996.
17. Ogata F, Azuma R, Kikuchi M, Koshima I, Morimoto Y. Novel lymphography using indocyanine green dye for near-infrared fluorescence labeling. Ann Plast Surg 58: 652-655, 2007.
18. Ogata F, Narushima M, Mihara M, Azuma R, Morimoto Y, Koshima I. Intraoperative lymphography using indocyanine green dye for near-infrared fluorescence labeling in lymphedema. Ann Plast Surg 59: 180-184, 2007.
19. Ongstad EL, Bouta EM, Roberts JE, Uzarski JS, Gibbs SE, Sabel MS, Cimmino VM, Roberts MA, Goldman J. Lymphangiogenesis-independent resolution of experimental edema. Am J Physiol Heart Circ Physiol 299: H46-H54, 2010.
20. Pytowski B, Goldman J, Persaud K, Wu Y, Witte L, Hicklin DJ, Skobe M, Boardman KC, Swartz MA. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst 97: 14-21, 2005.
21. Rutkowski JM, Markhus CE, Gyenge CC, Alitalo K, Wiig H, Swartz MA. Dermal collagen and lipid deposition correlate with tissue swelling and hydraulic conductivity in murine primary lymphedema. Am J Pathol 176: 1122-1129, 2010.
22. Sevick-Muraca EM, Sharma R, Rasmussen JC, Marshall MV, Wendt JA, Pham HQ, Bonefas E, Houston JP, Sampath L, Adams KE, Blanchard DK, Fisher RE, Chiang SB, Elledge R, Mawad ME. Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study. Radiology 246: 734-741, 2008.
23. Sharma R, Wang W, Rasmussen JC, Joshi A, Houston JP, Adams KE, Cameron A, Ke S, Kwon S, Mawad ME, Sevick-Muraca EM. Quantitative imaging of lymph function. Am J Physic! Heart Circ Physic! 292: H3109-H3118, 2007.
24. Stanton AW, Modi S, Mellor RH, Levick JR, Mortimer PS. Recent advances in breast cancer-related lymphedema of the arm: lymphatic pump failure and predisposing factors. Lymphat Res Biol7: 29-45, 2009.
25. Starling EH. On the absorption of fluids from the connective tissue spaces. J Physiol 19: 312-326, 1896.
26. Suami H, Pan WR, Taylor GI. The lymphatics of the skin filled by a dermal backflow: an observation in a scarred cadaver leg. Lymphology 40: 122-126, 2007.
27. Szuba A, Pyszel A, Jedrzejuk D, Janczak D, Andrzejak R. Presence of functional axillary lymph nodes and lymph drainage within arms in women with and without breast cancer-related lymphedema. Lymphology 40: 81-86, 2007.
28. Szuba A, Skobe M, Karkkainen MJ, Shin WS, Beynet DP, Rockson NB, Dakhil N, Spilman S, Goris ML, Strauss HW, Quertermous T, Alitalo K, Rockson SG. Therapeutic lymphangiogenesis with human recombinant VEGF-C. FASEB J 16: 1985-1987, 2002.
29. Tammela T, Saaristo A, Holopainen T, Lyytikka J, Kotronen A, Pitkonen M, Abo-Ramadan U, Yla-Herttuala S, Petrova TV, Alitalo K. Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat Med 13: 1458-1466, 2007.
30. Unno N, Inuzuka K, Suzuki M, Yamamoto N, Sagara D, Nishiyama M, Konno H. Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema. J Vasc Surg 45: 1016-1021, 2007.
31. Uzarski J, Drelles MB, Gibbs SE, Ongstad EL, Goral JC, McKeown KK, Raehl AM, Roberts MA, Pytowski B, Smith MR, Goldman J. The resolution of lytnphedema by interstitial flow in the mouse tail skin. Am J Physiol Heart Circ Physiol 294: H1326-H1334, 2008.
32. Warren AG, Slavin SA. Scar lymphedema-fact or fiction? Ann Plas Surg 59: 41-45, 2007.
33. Yan A, Avraham T, Zampell JC, Aschen SZ, Mehrara BJ. Mechanisms of lymphatic regeneration after tissue transfer. PLos One 6: e17201, 2011.
34. Yoon YS, Murayama T, Gravereaux E, Tkebuchava T, Silver M, Curry C, Wecker A, Kirchmair R, Hu CS, Kearney M, Ashare A, Jackson DG, Kubo H, Isner JM, Losordo DW. VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema. J Clin Invest 111: 717-725, 2003.
35. Zampell JC, Yan A, Avraham T, Andrade V, Malliaris S, Aschen S, Rockson SG, Mehrara BJ. Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema. Am J Physiol Cell Physiol 300: C1107-C1121, 2011.