Lymphoedema Following Regional Lymph Node Surgery for Breast Cancer
Authors:
P. Vrtělová 1; O. Coufal 1,2; V. Fait 1,2; L. Gabrielová 1; O. Zapletal 1
Authors‘ workplace:
Klinika operační onkologie, Masarykův onkologický ústav, Brno
1; Lékařská fakulta MU, Brno
2
Published in:
Klin Onkol 2017; 30(1): 34-40
Category:
Review
doi:
https://doi.org/10.14735/amko201734
Overview
Background:
The treatment of breast cancer is based on the multimodal principle and surgery of regional lymph nodes is an inseparable part of this. Indication criteria are changing constantly folowing advances in other modalities. It is necessary to consider not only the diagnostic or therapeutic benefit but also to take into account adverse effects. Previous studies have demonstrated that axillary dissection (ALND) is burdened by a high frequency of chronic lymphoedema of the arm or chest wall; however, a considerable percentage of patients may also suffer from lymphoedema after sentinel lymph node biopsy (SLNB).
Aim:
This paper focuses on the pathophysiology of lymphoedema, its potential predictive factors, and its complications. Furthermore, it presents an overview of published studies comparing the incidences of lymphoedema after current axillary surgery for breast cancer together with current trends designed to radically reduce the number of these operations. It also briefly refers to the possibilities of implementing preventive or therapeutic operations for lymphoedema.
Conclusions:
Both ALND and SLNB are burdened by a clinically significant risk of lymphoedema. This risk is more serious after ALND. In the medium term, approximately 7–59% of operated patients suffer from lymphoedema. The incidence of lymphoedema after SLNB, considered a very gentle method, is also not negligible (0–14%). As the number of patients surviving breast cancer treatment continues to increase, monitoring the undesirable effects of axillary surgery over the long term will become more important. The results of published studies support research into treatment methods that have the potential to reduce the radicality of axillary surgery while preserving or improving total medical effectiveness.
Key words:
breast neoplasms – sentinel lymph node biopsy – axillary dissection – adverse effects – breast cancer lymphedema
This work was supported by the grants MEYS – NPS I – LO1413 and MH CZ – DRO (MMCI, 00209- 805).
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE recommendation for biomedical papers.
Submitted:
7. 11. 2016
Accepted:
5. 12. 2016
Sources
1. Krag DN, Weaver DL, Alex JC et al. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 1993; 2 (6): 335–339.
2. Giuliano AE, Kirgan DM, Guenther JM et al. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220 (3): 391–398.
3. Giuliano AE, Hunt KK, Ballman KV et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 2011; 305 (6): 569–575. doi: 10.1001/jama.2011.90.
4. Galimberti V, Cole BF, Zurrida S et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial. Lancet Oncol 2013; 14 (4): 297–305. doi: 10.1016/S1470-2045 (13) 70035-4.
5. Boughey JC, Suman VJ, Mittendorf EA et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA 2013; 310 (14): 1455–1461. doi: 10.1001/jama.2013.278932.
6. Kuehn T, Bauerfeind I, Fehm T et al. Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol 2013; 14 (7): 609–618. doi: 10.1016/S1470-2045 (13) 70166-9.
7. Donker M, van Tienhoven G, Straver ME et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol 2014; 15 (12): 1303–1310. doi: 10.1016/S1470-2045 (14) 70460-7.
8. Gentilini O, Veronesi U. Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: sentinel node versus observation after axillary UltraSouND). Breast 2012; 21 (5): 678–681. doi: 10.1016/j.breast.2012.06.013.
9. DiSipio T, Rye S, Newman B et al. Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol 2013; 14 (6): 500–515. doi: 10.1016/S1470-2045 (13) 70076-7.
10. Soares EW, Nagai HM, Bredt LC et al. Morbidity after conventional dissection of axillary lymph nodes in breast cancer patients. World J Surg Oncol 2014; 12: 67. doi: 10.1186/1477-7819-12-67.
11. Křížová H, Wald M, Barkmanová J. Lymfoscintigrafie u pacientek s nekončetinovým lymfedémem po disekci axily a radioterapii. Klin Onkol 2006; 19 (5): 252–254.
12. Degnim AC, Miller J, Hoskin TL et al. A prospective study of breast lymphedema: frequency, symptoms, and quality of life. Breast Cancer Res Treat 2012; 134 (3): 915–922. doi: 10.1007/s10549-012-2004-x.
13. Verbelen H, Gebruers N, Eeckhout FM et al. Shoulder and arm morbidity in sentinel node-negative breast cancer patients: a systematic review. Breast Cancer Res Treat 2014; 144 (1): 21–31. doi: 10.1007/s10549-014-2846-5.
14. Benda K. Lymfedém končetin v ordinaci praktického lékaře. Med Pro Praxi 2006; 6: 276–279.
15. Mayrovitz HN. The standard of care for lymphedema: current concepts and physiological considerations. Lymphat Res Biol 2009; 7 (2): 101–108. doi: 10.1089/lrb.2009.0006.
16. Chen C, Crooks S, Keeley V et al. BLS clinical definitions. Sevenoaks: British Lymphology Society: 2001.
17. Granzow JW, Soderberg JM, Kaji AH et al. Review of current surgical treatments for lymphedema. Ann Surg Oncol 2014; 21 (4): 1195–1201. doi: 10.1245/s10434-014-3518-8.
18. Narushima M, Mihara M, Yamamoto Y et al. The intravascular stenting method for treatment of extremity lymphedema with multi-configuration lymphaticovenous anastomoses. Plast Reconstr Surg 2010; 125 (3): 935–943. doi: 10.1097/PRS.0b013e3181cb64da.
19. International Society of Lymphology. The diagnosis and treatment of peripheral lymphedema: 2013 Consensus Document of the International Society of Lymphology. Lymphology 2013; 46 (1): 1–11.
20. Masmoudi A, Maaloul I, Turki H et al. Erysipelas after breast cancer treatment (26 cases). Dermatol Online J 2005; 11 (3): 12.
21. Pereira de Godoy JM, Azoubel LM, Guerreiro Godoy M de F. Erysipelas and lymphangitis in patients undergoing lymphedema treatment after breast-cancer therapy. Acta Dermatovenerol Alp Pannonica Adriat 2009; 18 (2): 63–65.
22. Park SI, Yang EJ, Kim DK et al. Prevalence and epidemiological factors involved in cellulitis in Korean patients with lymphedema. Ann Rehabil Med 2016; 40 (2): 326–333.
23. Hughes LL, Styblo TM, Thoms WW et al. Cellulitis of the breast as a complication of breast-conserving surgery and irradiation. Am J Clin Oncol 1997; 20 (4): 338–341.
24. Ruocco V, Schwartz RA, Ruocco E. Lymphedema: an immunologically vulnerable site for development of neoplasms. J Am Acad Dermatol 2002; 47 (1): 124–127.
25. Stewart FW, Treves N. Lymphangiosarcoma in postmastectomy lymphedema; a report of six cases in elephantiasis chirurgica. Cancer 1948; 1 (1): 64–81.
26. Sharma A, Schwartz RA. Stewart-Treves syndrome: pathogenesis and management. J Am Acad Dermatol 2012; 67 (6): 1342–1348. doi: 10.1016/j.jaad.2012.04.028.
27. Lee R, Saardi KM, Schwartz RA. Lymphedema-related angiogenic tumors and other malignancies. Clin Dermatol 2014; 32 (5): 616–620. doi: 10.1016/j.clindermatol.2014.04.008.
28. Schrenk P, Rieger R, Shamiyeh A et al. Morbidity following sentinel lymph node biopsy versus axillary lymph node dissection for patients with breast carcinoma. Cancer 2000; 88 (3): 608–614.
29. Sener SF, Winchester DJ, Martz CH et al. Lymphedema after sentinel lymphadenectomy for breast carcinoma. Cancer 2001; 92 (4): 748–752.
30. Burak WE, Hollenbeck ST, Zervos EE et al. Sentinel lymph node biopsy results in less postoperative morbidity compared with axillary lymph node dissection for breast cancer. Am J Surg 2002; 183 (1): 23–27.
31. Haid A, Kuehn T, Konstantiniuk P et al. Shoulder-arm morbidity following axillary dissection and sentinel node only biopsy for breast cancer. Eur J Surg Oncol 2002; 28 (7): 705–710.
32. Temple LK, Baron R, Cody HS 3rd et al. Sensory morbidity after sentinel lymph node biopsy and axillary dissection: a prospective study of 233 women. Ann Surg Oncol 2002; 9 (7): 654–662.
33. Swenson KK, Nissen MJ, Ceronsky C et al. Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol 2002; 9 (8): 745–753.
34. Veronesi U, Paganelli G, Viale G et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 2003; 349 (6): 546–553.
35. Peintinger F, Reitsamer R, Stranzl H et al. Comparison of quality of life and arm complaints after axillary lymph node dissection vs sentinel lymph node biopsy in breast cancer patients. Br J Cancer 2003; 89 (4): 648–652.
36. Rietman JS, Dijkstra PU, Geertzen JH et al. Treatment-related upper limb morbidity 1 year after sentinel lymph node biopsy or axillary lymph node dissection for stage I or II breast cancer. Ann Surg Oncol 2004; 11 (11): 1018–1024.
37. Rietman JS, Geertzen JH, Hoekstra HJ et al. Long term treatment related upper limb morbidity and quality of life after sentinel lymph node biopsy for stage I or II breast cancer. Eur J Surg Oncol 2006; 32 (2): 148–152.
38. Barranger E, Dubernard G, Fleurence J et al. Subjective morbidity and quality of life after sentinel node biopsy and axillary lymph node dissection for breast cancer. J Surg Oncol 2005; 92 (1): 17–22.
39. Purushotham AD, Upponi S, Klevesath MB et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol 2005; 23 (19): 4312–4321.
40. Rönkä R, von Smitten K, Tasmuth T et al. One-year morbidity after sentinel node biopsy and breast surgery. Breast 2005; 14 (1): 28–36.
41. Mansel RE, Fallowfield L, Kissin M et al. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst 2006; 98 (9): 599–609.
42. Langer I, Guller U, Berclaz G et al. Morbidity of sentinel lymph node biopsy (SLN) alone versus SLN and completion axillary lymph node dissection after breast cancer surgery: a prospective Swiss multicenter study on 659 patients. Ann Surg 2007; 245 (3): 452–461.
43. Lucci A, McCall LM, Beitsch PD et al. Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011. J Clin Oncol 2007; 25 (24): 3657–3663.
44. Husted Madsen A, Haugaard K, Soerensen J et al. Arm morbidity following sentinel lymph node biopsy or axillary lymph node dissection: a study from the Danish Breast Cancer Cooperative Group. Breast 2008; 17 (2): 138–147.
45. Del Bianco P, Zavagno G, Burelli P et al. Morbidity comparison of sentinel lymph node biopsy versus conventional axillary lymph node dissection for breast cancer patients: results of the sentinella-GIVOM Italian randomised clinical trial. Eur J Surg Oncol 2008; 34 (5): 508–513.
46. McLaughlin SA, Wright MJ, Morris KT et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 2008; 26 (32): 5213–5219. doi: 10.1200/JCO.2008.16.3725.
47. McLaughlin SA, Wright MJ, Morris KT et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: patient perceptions and precautionary behaviors. J Clin Oncol 2008; 26 (32): 5220–5226. doi: 10.1200/JCO.2008.16.3766.
48. Gill G, SNAC Trial Group of the Royal Australasian College of Surgeons (RACS) and NHMRC Clinical Trials Centre. Sentinel-lymph-node-based management or routine axillary clearance? One-year outcomes of sentinel node biopsy versus axillary clearance (SNAC): a randomized controlled surgical trial. Ann Surg Oncol 2009; 16 (2): 266–275. doi: 10.1245/s10434-008-0229-z.
49. Helms G, Kühn T, Moser L et al. Shoulder-arm morbidity in patients with sentinel node biopsy and complete axillary dissection – data from a prospective randomised trial. Eur J Surg Oncol 2009; 35 (7): 696–701. doi: 10.1016/j.ejso.2008.06.013.
50. Kootstra JJ, Hoekstra-Weebers JE, Rietman JS et al. A longitudinal comparison of arm morbidity in stage I–II breast cancer patients treated with sentinel lymph node biopsy, sentinel lymph node biopsy followed by completion lymph node dissection, or axillary lymph node dissection. Ann Surg Oncol 2010; 17 (9): 2384–2394. doi: 10.1245/s10434-010-0981-8.
51. Ashikaga T, Krag DN, Land SR et al. Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection. J Surg Oncol 2010; 102 (2): 111–118. doi: 10.1002/jso.21535.
52. Kootstra JJ, Dijkstra PU, Rietman H et al. A longitudinal study of shoulder and arm morbidity in breast cancer survivors 7 years after sentinel lymph node biopsy or axillary lymph node dissection. Breast Cancer Res Treat 2013; 139 (1): 125–134. doi: 10.1007/s10549-013-2509-y.
53. Sagen A, Kaaresen R, Sandvik L et al. Upper limb physical function and adverse effects after breast cancer surgery: a prospective 2.5-year follow-up study and preoperative measures. Arch Phys Med Rehabil 2014; 95 (5): 875–881. doi: 10.1016/j.apmr.2013.12. 015.
54. Armer JM, Stewart BR. A comparison of four diagnostic criteria for lymphedema in a post-breast cancer population. Lymphat Res Biol 2005; 3 (4): 208–217.
55. Gerber LH. A review of measures of lymphedema. Cancer 1998; 83 (12 Suppl American): 2803–2804.
56. Karges JR, Mark BE, Stikeleather SJ et al. Concurrent validity of upper-extremity volume estimates: comparison of calculated volume derived from girth measurements and water displacement volume. Phys Ther 2003; 83 (2): 134–145.
57. Taylor R, Jayasinghe UW, Koelmeyer L et al. Reliability and validity of arm volume measurements for assessment of lymphedema. Phys Ther 2006; 86 (2): 205–214.
58. Cornish BH, Chapman M, Hirst C et al. Early diagnosis of lymphedema using multiple frequency bioimpedance. Lymphology 2001; 34 (1): 2–11.
59. Czerniec SA, Ward LC, Refshauge KM et al. Assessment of breast cancer-related arm lymphedema – comparison of physical measurement methods and self-report. Cancer Invest 2010; 28 (1): 54–62. doi: 10.3109/07357900902918494.
60. Ramos SM, O‘Donnell LS, Knight G. Edema volume, not timing, is the key to success in lymphedema treatment. Am J Surg 1999; 178 (4): 311–315.
61. Pain SJ, Purushotham AD. Lymphoedema following surgery for breast cancer. Br J Surg 2000; 87 (9): 1128–1141.
62. Rockson SG, Miller LT, Senie R et al. American Cancer Society Lymphedema workshop. Workgroup III: diag- nosis and management of lymphedema. Cancer 1998; 83 (12 Suppl American): 2882–2885.
63. Petrek JA, Senie RT, Peters M et al. Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 2001; 92 (6): 1368–1377.
64. Tsai RJ, Dennis LK, Lynch CF et al. The risk of developing arm lymphedema among breast cancer survivors: a meta-analysis of treatment factors. Ann Surg Oncol 2009; 16 (7): 1959–1972. doi: 10.1245/s10434-009- 0452-2.
65. Vieira RA, da Costa AM, de Souza JL et al. Risk factors for arm lymphedema in a cohort of breast cancer patients followed up for 10 years. Breast Care (Basel) 2016; 11 (1): 45–50. doi: 10.1159/000442489.
66. Schijven MP, Vingerhoets AJ, Rutten HJ et al. Comparison of morbidity between axillary lymph node dissection and sentinel node biopsy. Eur J Surg Oncol 2003; 29 (4): 341–350.
67. Crane-Okada R, Wascher RA, Elashoff D et al. Long-term morbidity of sentinel node biopsy versus complete axillary dissection for unilateral breast cancer. Ann Surg Oncol 2008; 15 (7): 1996–2005. doi: 10.1245/s10434-008-9909-y.
68. Helyer LK, Varnic M, Le LW et al. Obesity is a risk factor for developing postoperative lymphedema in breast cancer patients. Breast J 2010; 16 (1): 48–54. doi: 10.1111/j.1524-4741.2009.00855.x.
69. Paskett ED, Dean JA, Oliveri JM et al. Cancer-related lymphedema risk factors, diagnosis, treatment, and impact: a review. J Clin Oncol 2012; 30 (30): 3726–3733. doi: 10.1200/JCO.2012.41.8574.
70. Földi E, Földi M. Lymfostatické nemoci. In: Földi M, Földi E (eds). Lymfologie. 7th ed. Praha: Grada 2014: 189–280.
71. Pain SJ, Barber RW, Solanki CK et al. Short-term effects of axillary lymph node clearance surgery on lymphatic physiology of the arm in breast cancer. J Appl Physiol 2005; 99 (6): 2345–2351.
72. Casley-Smith JR, Morgan RG, Piller NB. Treatment of lymphedema of the arms and legs with 5,6-benzo-[alpha]-pyrone. N Engl J Med 1993; 329 (16): 1158–1163.
73. Yue T, Zhuang D, Zhou P et al. A prospective study to assess the feasibility of axillary reverse mapping and evaluate Its effect on preventinglymphedema in breast cancer patients. Clin Breast Cancer 2015; 15 (4): 301–306. doi: 10.1016/j.clbc.2015.01.010.
74. Han C, Yang B, Zuo WS et al. The feasibility and oncological safety of axillary reverse mapping in patients with breast cancer: A systematic review and meta-analysis of prospective studies. PLoS One 2016; 11 (2): e0150285. doi: 10.1371/journal.pone.0150285.
75. Bedrosian I, Babiera GV, Mittendorf EA et al. A phase I study to assess the feasibility and oncologic safety of axillary reverse mapping in breast cancer patients. Cancer 2010; 116 (11): 2543–2548. doi: 10.1002/cncr.25096.
76. Pavlista D, Eliska O. Relationship between the lymphatic drainage of the breast and the upper extremity: a postmortem study. Ann Surg Oncol 2012; 19 (11): 3410–3415. doi: 10.1245/s10434-012-2363-x.
77. Boccardo F, Casabona F, De Cian F et al. Lymphedema microsurgical preventive healing approach: a new technique for primary prevention of arm lymphedema after mastectomy. Ann Surg Oncol 2009; 16 (3): 703–708. doi: 10.1245/s10434-008-0270-y.
78. Yamashita K, Shimizu K. Endoscopic video-assisted breast surgery: procedures and short-term results. J Nippon Med Sch 2006; 73 (4): 193–202.
79. Luo C, Guo W, Yang J et al. Comparison of mastoscopic and conventional axillary lymph node dissection in breast cancer: long-term results from a randomized, multicenter trial. Mayo Clin Proc 2012; 87 (12): 1153–1161. doi: 10.1016/j.mayocp.2012.07.022.
80. Hussein O, El-Nahhas W, El-Saed A et al. Video-assisted axillary surgery for cancer: non-randomized comparison with conventional techniques. Breast 2007; 16 (5): 513–519.
81. Aponte-Rueda ME, Saade Cárdenas RA, Saade Aure MJ. Endoscopic axillary dissection: a systematic review of the literature. Breast 2009; 18 (3): 150–158. doi: 10.1016/j.breast.2009.05.001.
82. Coufal O, Fait V. Rehabilitační péče o pacientky s karcinomem prsu. In: Coufal O, Fait V (eds). Chirurgická léčba karcinomu prsu. Praha: Grada Publishing 2011: 389–396.
83. Vítová, V, Vítová H, Hrubá D. Péče o komplikovaný lymfedém provázející specifické malignity žen – vybrané kazuistiky. Interní Med 2011; 13 (5): 214–218.
84. Chang DW. Lymphaticovenular bypass for lymphedema management in breast cancer patients: a prospective study. Plast Reconstr Surg 2010; 126 (3): 752–758. doi: 10.1097/PRS.0b013e3181e5f6a9.
85. Damstra RJ, Voesten HG, van Schelven WD et al. Lymphatic venous anastomosis (LVA) for treatment of secondary arm lymphedema: a prospective study of 11 LVA procedures in 10 patients with breast cancer related lymphedema and a critical review of the literature. Breast Cancer Res Treat 2009; 113 (2): 199–206.
86. Lin CH, Ali R, Chen SC et al. Vascularized groin lymph node transfer using the wrist as a recipient site for management of postmastectomy upper extremity lymphedema. Plast Reconstr Surg 2009; 123 (4): 1265–1275. doi: 10.1097/PRS.0b013e31819e6529.
87. Gharb BB, Rampazzo A, Spanio di Spilimbergo S et al. Vascularized lymph node transfer based on the hilar perforators improves the outcome in upper limb lymphedema. Ann Plast Surg 2011; 67 (6): 589–593. doi: 10.1097/SAP.0b013e3181f88e8a.
88. Becker C, Assouad J, Riquet M et al. Postmastectomy lymphedema: long-term results following microsurgical lymph node transplantation. Ann Surg 2006; 243 (3): 313–315.
89. Damstra RJ, Voesten HG, Klinkert P et al. Circumferential suction-assisted lipectomy for lymphoedema after surgery for breast cancer. Br J Surg 2009; 96 (8): 859–864. doi: 10.1002/bjs.6658.
90. Schaverien MV, Munro KJ, Baker PA et al. Liposuction for chronic lymphoedema of the upper limb: 5 years of experience. J Plast Reconstr Aesthet Surg 2012; 65 (7): 935–942. doi: 10.1016/j.bjps.2012.01.021.
91. Cormier JN, Rourke L, Crosby M et al. The surgical treatment of lymphedema: a systematic review of the contemporary literature (2004–2010). Ann Surg Oncol 2012; 19 (2): 642–651. doi: 10.1245/s10434-011-2017-4.
92. van der Walt JC, Perks TJ, Zeeman BJ et al. Modified Charles procedure using negative pressure dressings for primary lymphedema: a functional assessment. Ann Plast Surg 2009; 62 (6): 669–675.
93. Baker A, Kim H, Sempleh JL et al. Experimental assessment of pro-lymphangiogenic growth factors in the treatment of post-surgical lymphedema following lymphadenectomy. Breast Cancer Res 2010; 12 (5): R70.
94. Visuri MT, Honkonen KM, Hartiala P et al. VEGF-C and VEGF-C156S in the pro-lymphangiogenic growth factor therapy of lymphedema: a large animal study. Angiogenesis 2015; 18 (3): 313–326. doi: 10.1007/s10456-015-9469-2.
95. Yan A, Avraham T, Zampell JC et al. Adipose-derived stem cells promote lymphangiogenesis in response to VEGF-C stimulation or TGF-β1 inhibition. Future Oncol 2011; 7 (12): 1457–1473. doi: 10.2217/fon.11.121.
96. Kanapathy M, Kalaskar D, Mosahebi A et al. Development of a tissue-engineered lymphatic graft using nanocomposite polymer for the treatment of secondary lymphedema. Artif Organs 2016; 40 (3): E1–E11. doi: 10.1111/aor.12604.
Labels
Paediatric clinical oncology Surgery Clinical oncologyArticle was published in
Clinical Oncology
2017 Issue 1
Most read in this issue
- Lymphoedema Following Regional Lymph Node Surgery for Breast Cancer
- Epithelial-mesenchymal Transition in Tumor Tissue and Its Role for Metastatic Spread of Cancer
- Daratumumab – Hope for Myeloma Patients, a Challenge for Clinical Laboratories
- Options of Chemotherapy in the Treatment of Prostate Cancer