Advances in treatment of lymphedema with supraclavicular vascularized lymph node transfer_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

PAN Wenjie ¹ ,  DENG Chengliang ^1,2

1. Department of Burns and Plastic Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi Guizhou, 563003, P. R. China;
2. Collaborative Innovation Center of Tissue Repair and Regenerative Medicine, Zunyi Guizhou, 563003, P. R. China;

Corresponding author：

DENG Chengliang, Email: cheliadeng@sina.com

Keywords：

Lymphedema; supraclavicular lymph node; vascularized lymph node transfer

DOI：

10.7507/1002-1892.202302104

Video：

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Objective To review the research progress of supraclavicular vascularized lymph node transfer (VLNT). Methods The research literature related to supraclavicular VLNT at home and abroad in recent years was extensively reviewed, and the anatomy of supraclavicular lymph nodes, clinical applications, and complications of supraclavicular VLNT were summarized. Results The supraclavicular lymph nodes are anatomically constant, located in the posterior cervical triangle zone, and the blood supply comes mainly from the transverse cervical artery. There are individual differences in the number of supraclavicular lymph nodes, and preoperative ultrasonography is helpful to clarify the number of lymph nodes. Clinical studies have shown that supraclavicular VLNT can relieve limb swelling, reduce the incidence of infection, and improve quality of life in patients with lymphedema. And the effectiveness of supraclavicular VLNT can be improved by combined with lymphovenous anastomosis, resection procedures, and liposuction. Conclusion There are a large number of supraclavicular lymph nodes, with abundant blood supply. It has been proven to be effective for any period of lymphedema, and the combined treatment is more effective. The more clinical studies are needed to clarify the effectiveness of supraclavicular VLNT alone or in combination, as well as the surgical approach and timing of the combined treatment.

Citation： PAN Wenjie, DENG Chengliang. Advances in treatment of lymphedema with supraclavicular vascularized lymph node transfer. Chinese Journal of Reparative and Reconstructive Surgery, 2023, 37(6): 736-741. doi: 10.7507/1002-1892.202302104 Copy

1.	Schulze H, Nacke M, Gutenbrunner C, et al. Worldwide assessment of healthcare personnel dealing with lymphoedema. Health Econ Rev, 2018, 8(1): 10. doi: 10.1186/s13561-018-0194-6.
2.	Rockson SG, Karaca-Mandic P, Skoracki R, et al. Clinical evaluation of a novel wearable compression technology in the treatment of lymphedema, an open-label controlled study. Lymphat Res Biol, 2022, 20(2): 125-132.
3.	Thompson B, Gaitatzis K, Janse de Jonge X, et al. Manual lymphatic drainage treatment for lymphedema: a systematic review of the literature. J Cancer Surviv, 2021, 15(2): 244-258.
4.	de Sire A, Losco L, Lippi L, et al. Surgical treatment and rehabilitation strategies for upper and lower extremity lymphedema: A comprehensive review. Medicina (Kaunas), 2022, 58(7): 954. doi: 10.3390/medicina58070954.
5.	Di Taranto G, Bolletta A, Chen SH, et al. A prospective study on combined lymphedema surgery: Gastroepiploic vascularized lymph nodes transfer and lymphaticovenous anastomosis followed by suction lipectomy. Microsurgery, 2021, 41(1): 34-43.
6.	Bobrek K, Nabavizadeh R, Nabavizadeh B, et al. How to care and minimize the sequelae of lower extremity lymphedema. Semin Oncol Nurs, 2022, 38(3): 151270. doi: 10.1016/j.soncn.2022.151270.
7.	Gallagher KK, Lopez M, Iles K, et al. Surgical approach to lymphedema reduction. Curr Oncol Rep, 2020, 22(10): 97. doi: 10.1007/s11912-020-00961-4.
8.	Chang DW, Dayan J, Greene AK, et al. Surgical treatment of lymphedema: a systematic review and meta-analysis of controlled trials. Results of a consensus conference. Plast Reconstr Surg, 2021, 147(4): 975-993.
9.	Winters H, Tielemans HJP, Paulus V, et al. A systematic review and meta-analysis of vascularized lymph node transfer for breast cancer-related lymphedema. J Vasc Surg Venous Lymphat Disord, 2022, 10(3): 786-795.
10.	Li Y, Dong R, Li Z, et al. Intra-abdominal vascularized lymph node transfer for treatment of lymphedema: A systematic literature review and meta-analysis. Microsurgery, 2021, 41(8): 802-815.
11.	Clodius L, Smith PJ, Bruna J, et al. The lymphatics of the groin flap. Ann Plast Surg, 1982, 9(6): 447-458.
12.	Althubaiti GA, Crosby MA, Chang DW. Vascularized supraclavicular lymph node transfer for lower extremity lymphedema treatment. Plast Reconstr Surg, 2013, 131(1): 133e-135e.
13.	Robbins KT, Shaha AR, Medina JE, et al. Consensus statement on the classification and terminology of neck dissection. Arch Otolaryngol Head Neck Surg, 2008, 134(5): 536-538.
14.	Ooi AS, Chang DW. 5-step harvest of supraclavicular lymph nodes as vascularized free tissue transfer for treatment of lymphedema. J Surg Oncol, 2017, 115(1): 63-67.
15.	Steinbacher J, Tinhofer IE, Meng S, et al. The surgical anatomy of the supraclavicular lymph node flap: A basis for the free vascularized lymph node transfer. J Surg Oncol, 2017, 115(1): 60-62.
16.	Sapountzis S, Singhal D, Rashid A, et al. Lymph node flap based on the right transverse cervical artery as a donor site for lymph node transfer. Ann Plast Surg, 2014, 73(4): 398-401.
17.	Huelke DF. A study of the transverse cervical and dorsal scapular arteries. Anat Rec, 1958, 132(3): 233-245.
18.	Kwiecien GJ, Gharb BB, Tadisina KK, et al. Quantity of lymph nodes in the vascularized lymph node transfer influences its lymphaticovenous drainage. J Reconstr Microsurg, 2018, 34(1): 41-46.
19.	Gerety PA, Pannucci CJ, Basta MN, et al. Lymph node content of supraclavicular and thoracodorsal-based axillary flaps for vascularized lymph node transfer. J Vasc Surg Venous Lymphat Disord, 2016, 4(1): 80-87.
20.	Liu HL, Chung JC. The lymph node content of supraclavicular lymph node flap: a histological study on fresh human specimens. Lymphat Res Biol, 2019, 17(5): 537-542.
21.	Akita S, Mitsukawa N, Kuriyama M, et al. Comparison of vascularized supraclavicular lymph node transfer and lymphaticovenular anastomosis for advanced stage lower extremity lymphedema. Ann Plast Surg, 2015, 74(5): 573-579.
22.	李平, 何波, 杨羿, 等. 血管化锁骨上窝淋巴结皮瓣移植治疗肢体淋巴水肿近期疗效. 中华显微外科杂志, 2017, 40(3): 218-221.
23.	Maldonado AA, Chen R, Chang DW. The use of supraclavicular free flap with vascularized lymph node transfer for treatment of lymphedema: A prospective study of 100 consecutive cases. J Surg Oncol, 2017, 115(1): 68-71.
24.	Ciudad P, Agko M, Perez Coca JJ, et al. Comparison of long-term clinical outcomes among different vascularized lymph node transfers: 6-year experience of a single center’s approach to the treatment of lymphedema. J Surg Oncol, 2017, 116(6): 671-682.
25.	Visconti G, Tartaglione G, Bartoletti R, et al. Compartimental harvesting of dual lymph node flap from the right supraclavicular area for the treatment of lower extremity lymphedema: A case series. J Plast Reconstr Aesthet Surg, 2019, 72(2): 211-215.
26.	Ciudad P, Huayllani MT, Forte AJ, et al. Vascularized lymph node transfer for the treatment of posttraumatic lower extremity lymphedema: a preliminary report. Indian J Plast Surg, 2022, 55(1): 97-101.
27.	Visconti G, Constantinescu T, Chen PY, et al. The venous lymph node flap: concepts, experimental evidence, and potential clinical implications. J Reconstr Microsurg, 2016, 32(8): 625-631.
28.	Visconti G, Constantinescu T, Araki J, et al. The venous lymph node flap for the treatment of peripheral lymphedema: Preliminary evidence. Microsurgery, 2017, 37(1): 86-87.
29.	Kadletz-Wanke L, Oberndorfer F, Grabner E, et al. Evaluation of the external jugular vein overlying the sternocleidomastoid muscle as venous lymph-node flap. J Clin Med, 2022, 11(7): 1812. doi: 10.3390/jcm11071812.
30.	Visconti G, Constantinescu T, Chen HC. The venous lymph-node flap. Microsurgery, 2016, 36(6): 527-528.
31.	Fillon M. Combined physiologic and excisional therapies improve cancer-related lymphedema outcomes. CA Cancer J Clin, 2018, 68(4): 237-239.
32.	Hayashi A, Visconti G, Yamamoto T, et al. Intraoperative imaging of lymphatic vessel using ultra high-frequency ultrasound. J Plast Reconstr Aesthet Surg, 2018, 71(5): 778-780.
33.	van Heumen S, Riksen JJM, Bramer WM, et al. Imaging of the lymphatic vessels for surgical planning: A systematic review. Ann Surg Oncol, 2023, 30(1): 462-479.
34.	Sapountzis S, Ciudad P, Lim SY, et al. Modified Charles procedure and lymph node flap transfer for advanced lower extremity lymphedema. Microsurgery, 2014, 34(6): 439-447.
35.	Chilgar RM, Khade S, Chen HC, et al. Surgical treatment of advanced lymphatic filariasis of lower extremity combining vascularized lymph node transfer and excisional procedures. Lymphat Res Biol, 2019, 17(6): 637-646.
36.	Ciudad P, Agko M, Huang TCT, et al. Comprehensive multimodal surgical treatment of end-stage lower extremity lymphedema with toe management: The combined Charles’, Homan’s, and vascularized lymph node transfer (CHAHOVA) procedures. J Surg Oncol, 2019, 119(4): 430-438.
37.	Nicoli F, Constantinides J, Ciudad P, et al. Free lymph node flap transfer and laser-assisted liposuction: a combined technique for the treatment of moderate upper limb lymphedema. Lasers Med Sci, 2015, 30(4): 1377-1385.
38.	魏苗苗, 吴祥奎, 吴必华, 等. 手动负压抽吸联合血管化淋巴结移植治疗继发性下肢淋巴水肿的疗效分析. 组织工程与重建外科, 2022, 18(1): 14-18.
39.	Masia J, Pons G, Nardulli ML. Combined surgical treatment in breast cancer-related lymphedema. J Reconstr Microsurg, 2016, 32(1): 16-27.
40.	Qiu SS, Chen HY, Cheng MH. Vascularized lymph node flap transfer and lymphovenous anastomosis for klippel-trenaunay syndrome with congenital lymphedema. Plast Reconstr Surg Glob Open, 2014, 2(6): e167. doi: 10.1097/gox.0000000000000099.
41.	Cheng MH, Tee R, Chen C, et al. Simultaneous ipsilateral vascularized lymph node transplantation and contralateral lymphovenous anastomosis in bilateral extremity lymphedema with different severities. Ann Surg Oncol, 2020, 27(13): 5267-5276.
42.	Chung JH, Hwang YJ, Park SH, et al. Preliminary outcomes of combined surgical approach for lower extremity lymphedema: supraclavicular lymph node transfer and lymphaticovenular anastomosis. J Plast Surg Hand Surg, 2022, 56(5): 261-269.
43.	Garza RM, Beederman M, Chang DW. Physical and functional outcomes of simultaneous vascularized lymph node transplant and lymphovenous Bypass in the treatment of lymphedema. Plast Reconstr Surg, 2022, 150(1): 169-180.
44.	Yamamoto T, Yoshimatsu H, Yamamoto N. Complete lymph flow reconstruction: A free vascularized lymph node true perforator flap transfer with efferent lymphaticolymphatic anastomosis. J Plast Reconstr Aesthet Surg, 2016, 69(9): 1227-1233.
45.	Akita S, Yamaji Y, Tokumoto H, et al. Improvement of the efficacy of vascularized lymph node transfer for lower-extremity lymphedema via a prefabricated lympho-venous shunt through lymphaticovenular anastomosis between the efferent lymphatic vessel and small vein in the elevated vascularized lymph node. Microsurgery, 2018, 38(3): 270-277.
46.	Massey MF, Gupta DK. The incidence of donor-site morbidity after transverse cervical artery vascularized lymph node transfers: the need for a lymphatic surgery national registry. Plast Reconstr Surg, 2015, 135(5): 939e-940e.
47.	Lee M, McClure E, Reinertsen E, et al. Lymphedema of the upper extremity following supraclavicular lymph node harvest. Plast Reconstr Surg, 2015, 135(6): 1079e-1082e.
48.	Seong IH, Park JW, Woo KJ. No-fat diet for treatment of donor site chyle leakage in vascularized supraclavicular lymph node transfer. Arch Craniofac Surg, 2020, 21(6): 376-379.
49.	Teven CM, Hunter CL, Chang DW. Management of high-output chyle leak after harvesting of vascularized supraclavicular lymph nodes. Plast Reconstr Surg, 2019, 143(4): 1251-1256.

1. Schulze H, Nacke M, Gutenbrunner C, et al. Worldwide assessment of healthcare personnel dealing with lymphoedema. Health Econ Rev, 2018, 8(1): 10. doi: 10.1186/s13561-018-0194-6.
2. Rockson SG, Karaca-Mandic P, Skoracki R, et al. Clinical evaluation of a novel wearable compression technology in the treatment of lymphedema, an open-label controlled study. Lymphat Res Biol, 2022, 20(2): 125-132.
3. Thompson B, Gaitatzis K, Janse de Jonge X, et al. Manual lymphatic drainage treatment for lymphedema: a systematic review of the literature. J Cancer Surviv, 2021, 15(2): 244-258.
4. de Sire A, Losco L, Lippi L, et al. Surgical treatment and rehabilitation strategies for upper and lower extremity lymphedema: A comprehensive review. Medicina (Kaunas), 2022, 58(7): 954. doi: 10.3390/medicina58070954.
5. Di Taranto G, Bolletta A, Chen SH, et al. A prospective study on combined lymphedema surgery: Gastroepiploic vascularized lymph nodes transfer and lymphaticovenous anastomosis followed by suction lipectomy. Microsurgery, 2021, 41(1): 34-43.
6. Bobrek K, Nabavizadeh R, Nabavizadeh B, et al. How to care and minimize the sequelae of lower extremity lymphedema. Semin Oncol Nurs, 2022, 38(3): 151270. doi: 10.1016/j.soncn.2022.151270.
7. Gallagher KK, Lopez M, Iles K, et al. Surgical approach to lymphedema reduction. Curr Oncol Rep, 2020, 22(10): 97. doi: 10.1007/s11912-020-00961-4.
8. Chang DW, Dayan J, Greene AK, et al. Surgical treatment of lymphedema: a systematic review and meta-analysis of controlled trials. Results of a consensus conference. Plast Reconstr Surg, 2021, 147(4): 975-993.
9. Winters H, Tielemans HJP, Paulus V, et al. A systematic review and meta-analysis of vascularized lymph node transfer for breast cancer-related lymphedema. J Vasc Surg Venous Lymphat Disord, 2022, 10(3): 786-795.
10. Li Y, Dong R, Li Z, et al. Intra-abdominal vascularized lymph node transfer for treatment of lymphedema: A systematic literature review and meta-analysis. Microsurgery, 2021, 41(8): 802-815.
11. Clodius L, Smith PJ, Bruna J, et al. The lymphatics of the groin flap. Ann Plast Surg, 1982, 9(6): 447-458.
12. Althubaiti GA, Crosby MA, Chang DW. Vascularized supraclavicular lymph node transfer for lower extremity lymphedema treatment. Plast Reconstr Surg, 2013, 131(1): 133e-135e.
13. Robbins KT, Shaha AR, Medina JE, et al. Consensus statement on the classification and terminology of neck dissection. Arch Otolaryngol Head Neck Surg, 2008, 134(5): 536-538.
14. Ooi AS, Chang DW. 5-step harvest of supraclavicular lymph nodes as vascularized free tissue transfer for treatment of lymphedema. J Surg Oncol, 2017, 115(1): 63-67.
15. Steinbacher J, Tinhofer IE, Meng S, et al. The surgical anatomy of the supraclavicular lymph node flap: A basis for the free vascularized lymph node transfer. J Surg Oncol, 2017, 115(1): 60-62.
16. Sapountzis S, Singhal D, Rashid A, et al. Lymph node flap based on the right transverse cervical artery as a donor site for lymph node transfer. Ann Plast Surg, 2014, 73(4): 398-401.
17. Huelke DF. A study of the transverse cervical and dorsal scapular arteries. Anat Rec, 1958, 132(3): 233-245.
18. Kwiecien GJ, Gharb BB, Tadisina KK, et al. Quantity of lymph nodes in the vascularized lymph node transfer influences its lymphaticovenous drainage. J Reconstr Microsurg, 2018, 34(1): 41-46.
19. Gerety PA, Pannucci CJ, Basta MN, et al. Lymph node content of supraclavicular and thoracodorsal-based axillary flaps for vascularized lymph node transfer. J Vasc Surg Venous Lymphat Disord, 2016, 4(1): 80-87.
20. Liu HL, Chung JC. The lymph node content of supraclavicular lymph node flap: a histological study on fresh human specimens. Lymphat Res Biol, 2019, 17(5): 537-542.
21. Akita S, Mitsukawa N, Kuriyama M, et al. Comparison of vascularized supraclavicular lymph node transfer and lymphaticovenular anastomosis for advanced stage lower extremity lymphedema. Ann Plast Surg, 2015, 74(5): 573-579.
22. 李平, 何波, 杨羿, 等. 血管化锁骨上窝淋巴结皮瓣移植治疗肢体淋巴水肿近期疗效. 中华显微外科杂志, 2017, 40(3): 218-221.
23. Maldonado AA, Chen R, Chang DW. The use of supraclavicular free flap with vascularized lymph node transfer for treatment of lymphedema: A prospective study of 100 consecutive cases. J Surg Oncol, 2017, 115(1): 68-71.
24. Ciudad P, Agko M, Perez Coca JJ, et al. Comparison of long-term clinical outcomes among different vascularized lymph node transfers: 6-year experience of a single center’s approach to the treatment of lymphedema. J Surg Oncol, 2017, 116(6): 671-682.
25. Visconti G, Tartaglione G, Bartoletti R, et al. Compartimental harvesting of dual lymph node flap from the right supraclavicular area for the treatment of lower extremity lymphedema: A case series. J Plast Reconstr Aesthet Surg, 2019, 72(2): 211-215.
26. Ciudad P, Huayllani MT, Forte AJ, et al. Vascularized lymph node transfer for the treatment of posttraumatic lower extremity lymphedema: a preliminary report. Indian J Plast Surg, 2022, 55(1): 97-101.
27. Visconti G, Constantinescu T, Chen PY, et al. The venous lymph node flap: concepts, experimental evidence, and potential clinical implications. J Reconstr Microsurg, 2016, 32(8): 625-631.
28. Visconti G, Constantinescu T, Araki J, et al. The venous lymph node flap for the treatment of peripheral lymphedema: Preliminary evidence. Microsurgery, 2017, 37(1): 86-87.
29. Kadletz-Wanke L, Oberndorfer F, Grabner E, et al. Evaluation of the external jugular vein overlying the sternocleidomastoid muscle as venous lymph-node flap. J Clin Med, 2022, 11(7): 1812. doi: 10.3390/jcm11071812.
30. Visconti G, Constantinescu T, Chen HC. The venous lymph-node flap. Microsurgery, 2016, 36(6): 527-528.
31. Fillon M. Combined physiologic and excisional therapies improve cancer-related lymphedema outcomes. CA Cancer J Clin, 2018, 68(4): 237-239.
32. Hayashi A, Visconti G, Yamamoto T, et al. Intraoperative imaging of lymphatic vessel using ultra high-frequency ultrasound. J Plast Reconstr Aesthet Surg, 2018, 71(5): 778-780.
33. van Heumen S, Riksen JJM, Bramer WM, et al. Imaging of the lymphatic vessels for surgical planning: A systematic review. Ann Surg Oncol, 2023, 30(1): 462-479.
34. Sapountzis S, Ciudad P, Lim SY, et al. Modified Charles procedure and lymph node flap transfer for advanced lower extremity lymphedema. Microsurgery, 2014, 34(6): 439-447.
35. Chilgar RM, Khade S, Chen HC, et al. Surgical treatment of advanced lymphatic filariasis of lower extremity combining vascularized lymph node transfer and excisional procedures. Lymphat Res Biol, 2019, 17(6): 637-646.
36. Ciudad P, Agko M, Huang TCT, et al. Comprehensive multimodal surgical treatment of end-stage lower extremity lymphedema with toe management: The combined Charles’, Homan’s, and vascularized lymph node transfer (CHAHOVA) procedures. J Surg Oncol, 2019, 119(4): 430-438.
37. Nicoli F, Constantinides J, Ciudad P, et al. Free lymph node flap transfer and laser-assisted liposuction: a combined technique for the treatment of moderate upper limb lymphedema. Lasers Med Sci, 2015, 30(4): 1377-1385.
38. 魏苗苗, 吴祥奎, 吴必华, 等. 手动负压抽吸联合血管化淋巴结移植治疗继发性下肢淋巴水肿的疗效分析. 组织工程与重建外科, 2022, 18(1): 14-18.
39. Masia J, Pons G, Nardulli ML. Combined surgical treatment in breast cancer-related lymphedema. J Reconstr Microsurg, 2016, 32(1): 16-27.
40. Qiu SS, Chen HY, Cheng MH. Vascularized lymph node flap transfer and lymphovenous anastomosis for klippel-trenaunay syndrome with congenital lymphedema. Plast Reconstr Surg Glob Open, 2014, 2(6): e167. doi: 10.1097/gox.0000000000000099.
41. Cheng MH, Tee R, Chen C, et al. Simultaneous ipsilateral vascularized lymph node transplantation and contralateral lymphovenous anastomosis in bilateral extremity lymphedema with different severities. Ann Surg Oncol, 2020, 27(13): 5267-5276.
42. Chung JH, Hwang YJ, Park SH, et al. Preliminary outcomes of combined surgical approach for lower extremity lymphedema: supraclavicular lymph node transfer and lymphaticovenular anastomosis. J Plast Surg Hand Surg, 2022, 56(5): 261-269.
43. Garza RM, Beederman M, Chang DW. Physical and functional outcomes of simultaneous vascularized lymph node transplant and lymphovenous Bypass in the treatment of lymphedema. Plast Reconstr Surg, 2022, 150(1): 169-180.
44. Yamamoto T, Yoshimatsu H, Yamamoto N. Complete lymph flow reconstruction: A free vascularized lymph node true perforator flap transfer with efferent lymphaticolymphatic anastomosis. J Plast Reconstr Aesthet Surg, 2016, 69(9): 1227-1233.
45. Akita S, Yamaji Y, Tokumoto H, et al. Improvement of the efficacy of vascularized lymph node transfer for lower-extremity lymphedema via a prefabricated lympho-venous shunt through lymphaticovenular anastomosis between the efferent lymphatic vessel and small vein in the elevated vascularized lymph node. Microsurgery, 2018, 38(3): 270-277.
46. Massey MF, Gupta DK. The incidence of donor-site morbidity after transverse cervical artery vascularized lymph node transfers: the need for a lymphatic surgery national registry. Plast Reconstr Surg, 2015, 135(5): 939e-940e.
47. Lee M, McClure E, Reinertsen E, et al. Lymphedema of the upper extremity following supraclavicular lymph node harvest. Plast Reconstr Surg, 2015, 135(6): 1079e-1082e.
48. Seong IH, Park JW, Woo KJ. No-fat diet for treatment of donor site chyle leakage in vascularized supraclavicular lymph node transfer. Arch Craniofac Surg, 2020, 21(6): 376-379.
49. Teven CM, Hunter CL, Chang DW. Management of high-output chyle leak after harvesting of vascularized supraclavicular lymph nodes. Plast Reconstr Surg, 2019, 143(4): 1251-1256.

Chinese Journal of Reparative and Reconstructive Surgery

Advances in treatment of lymphedema with supraclavicular vascularized lymph node transfer

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