A chronic and latent lymphatic insufficiency follows recovery from acute lymphedema in the rat foreleg

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 9, 2012, Pages

  Mendez, Uziel ^a   Stroup, Emily M ^a   Lynch, Laura L ^a   Waller, Anna B ^a   Goldman, Jeremy ^a  

^a Michigan Technological University   (United States)

Author keywords

Axillary lymph node dissection; Inflammation; Lymphangiogenesis; Lymphatic drainage; Oxazolone; Secondary lymphedema

Indexed keywords

INDOCYANINE GREEN; OXAZOLONE;

ANIMAL EXPERIMENT; ARM; ARTICLE; AXILLARY LYMPH NODE EXTIRPATION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EXPOSURE; FEMALE; FLUID TRANSPORT; FORELEG; INDOCYANINE GREEN ANGIOGRAPHY; INDOCYANINE GREEN LYMPHOGRAPHY; INFLAMMATION; INTERSTITIAL FLUID; LEG; LEG EDEMA; LEG SWELLING; LYMPH NODE DISSECTION; LYMPHATIC DRAINAGE; LYMPHATIC SYSTEM; LYMPHATIC SYSTEM DISEASE; LYMPHEDEMA; LYMPHOGRAPHY; NONHUMAN; PRIORITY JOURNAL; RAT; SKINFOLD THICKNESS; SURGICAL TECHNIQUE;

ACUTE DISEASE; ANIMALS; FEMALE; FORELIMB; INFLAMMATION; LYMPH NODE EXCISION; LYMPHATIC SYSTEM; LYMPHEDEMA; LYMPHOGRAPHY; MODELS, ANIMAL; OXAZOLONE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84868356626     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00522.2012     Document Type: Article

References (46)

1. Akl TJ, Nagai T, Cote GL, Gashev AA. Mesenteric lymph flow in adult and aged rats. Am J Physiol Heart Circ Physiol 301: H1828-H1840, 2011.
2. Avraham T, Clavin NW, Daluvoy SV, Fernandes J, Soares MS, Corderio AP, Mehrara BJ. fibrosis is a key inhibitor of lymphatic regneration. Plastic Reconstr Surg 124: 438-450, 2009.
3. Avraham T, Daluvoy S, Zampell J, Yan A, Haviv YS, Rockson SG, Mehrara BJ. Blockade of transforming growth factor-beta1 accelerates lymphatic regeneration during wound repair. Am J Pathol 177: 3202-3214, 2010.
4. Bates DO. An interstitial hypothesis for breast cancer related lymphoedema. Pathophysiology 17: 289-294, 2010.
5. 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.
6. 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.
7. Guo RL, Zhou Q, Proulx ST, Wood R, Ji RC, Ritchlin CT, Pytowski B, Zhu ZP, Wang YJ, Schwarz EM, Xing LP. Inhibition of lymphangiogenesis and lymphatic drainage via vascular endothelial growth factor receptor 3 blockade increases the severity of inflammation in a mouse model of chronic inflammatory arthritis. Arthritis Rheum 60: 2666-2676, 2009.
8. Halsted WS. The swelling of the arm after operation for cancer of the breast, elephantiasis chirurgica, its causes and prevention. Bull Johns Hopkins Hosp 32: 309-313, 1921.
9. He CF, Young AJ, West CA, Su M, Konerding MA, Mentzer SJ. Stimulation of regional lymphatic and blood flow by epicutaneous oxazolone. J Appl Physiol 93: 966-973, 2002.
10. Huggenberger R, Siddiqui SS, Brander D, Ullmann S, Zimmermann K, Antsiferova M, Werner S, Alitalo K, Detmar M. An important role of lymphatic vessel activation in limiting acute inflammation. Blood 117: 4667-4678, 2011.
11. Huggenberger R, Ullmann S, Proulx ST, Pytowski B, Alitalo K, Detmar M. Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J Exp Med 207: 2255-2269, 2010.
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: 591-603, 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. Kaplan DH, Igyarto BZ, Gaspari AA. Early immune events in the induction of allergic contact dermatitis. Nat Rev Immunol 12: 114-124, 2012.
15. Kaplan DH, Kissenpfennig A, Clausen BE. Insights into Langerhans cell function from Langerhans cell ablation models. Eur J Immunol 38: 2369-2376, 2008.
16. 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.
17. Liao S, Cheng G, Conner DA, Huang YH, Kucherlapati RS, Munn LL, Ruddle NH, Jain RK, Fukumura D, Padera TP. Impaired lymphatic contraction associated with immunosuppression. Proc Natl Acad Sci USA 108: 18784-18789, 2011.
18. Mak SS, Yeo W, Lee YM, Tse SM, Ho FP, Zee B, Chan E. Risk factors for the initiation and aggravation of lymphoedema after axillary lymph node dissection for breast cancer. Hong Kong Med J 15: 8-12, 2009.
19. Mendez U, Brown EM, Ongstad EL, Slis JR, Goldman J. Functional recovery of fluid drainage precedes lymphangiogenesis in acute murine foreleg lymphedema. Am J Physiol Heart Circ Physiol 302: H2250-H2256, 2012.
20. Mortimer PS. The pathophysiology of lymphedema. Cancer 83: 2798-2802, 1998.
21. 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.
22. Nakamura K, Radhakrishnan K, Wong YM, Rockson SG. Antiinflammatory pharmacotherapy with ketoprofen ameliorates experimental lymphatic vascular insufficiency in mice. Plos One 4: e8380, 2009.
23. 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.
24. Ogata F, Narushima M, Mihara M, Azuma R, Morimoto Y, Koshima I. Intraoperative lymphography using indocyanine green dye for nearinfrared fluorescence labeling in lymphedema. Ann Plast Surg 59: 180-184, 2007.
25. Olszewski W. On the pathomechanism of development of postsurgical lymphedema. Lymphology 6: 35-51, 1973.
26. 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.
27. Pain SJ, Barber RW, Solanki CK, Ballinger JR, Britton TB, Mortimer PS, Purushotham AD, Peters AM. Short-term effects of axillary lymph node clearance surgery on lymphatic physiology of the arm in breast cancer. J Appl Physiol 99: 2345-2351, 2005.
28. Saint-Mezard P, Berard F, Dubois B, Kaiserlian D, Nicolas JF. The role of CD4+ and CD8+ T cells in contact hypersensitivity and allergic contact dermatitis. Eur J Dermatol 14: 131-138, 2004.
29. Sakorafas GH, Peros G, Cataliotti L, Vlastos G. Lymphedema following axillary lymph node dissection for breast cancer. Surg Oncol 15: 153-165, 2006.
30. Saul ME, Thomas PA, Dosen PJ, Isbister GK, O'Leary MA, Whyte IM, McFadden SA, van Helden DF. A pharmacological approach to first aid treatment for snakebite. Nat Med 17: 809-811, 2011.
31. 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.
32. 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 Physiol Heart Circ Physiol 292: H3109-H3118, 2007.
33. Stanton AW, Modi S, Bennett Britton TM, Purushotham AD, Peters AM, Levick JR, Mortimer PS. Lymphatic drainage in the muscle and subcutis of the arm after breast cancer treatment. Breast Cancer Res Treat 117: 549-557, 2009.
34. 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 Biol 7: 29-45, 2009.
35. 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.
36. Sugaya M, Kuwano Y, Suga H, Miyagaki T, Ohmatsu H, Kadono T, Okochi H, Blauvelt A, Tamaki K, Sato S. Lymphatic dysfunction impairs antigen-specific immunization, but augments tissue swelling following contact with allergens. J Invest Dermatol 132: 667-676, 2012.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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 lymphedema by interstitial flow in the mouse tail skin. Am J Physiol Heart Circ Physiol 294: H1326-H1334, 2008.
42. Warren AG, Slavin SA. Scar lymphedema: fact or fiction? Ann Plas Surg 59: 41-45, 2007.
43. Weiler M, Kassis T, Dixon JB. Sensitivity analysis of near-infrared functional lymphatic imaging. J Biomed Opt 17: 066019, 2012.
44. 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.
45. Zampell JC, Elhadad S, Avraham T, Weitman E, Aschen S, Yan A, Mehrara BJ. Toll-like receptor deficiency worsens inflammation and lymphedema after lymphatic injury. Am J Physiol Cell Physiol 302: C709-C719, 2012.
46. Zampell JC, Yan A, Avraham T, Daluvoy S, Weitman ES, Mehrara BJ. HIF-1alpha coordinates lymphangiogenesis during wound healing and in response to inflammation. FASEB J 26: 1027-1039, 2012.