Journal of Surgical Oncology

The Use of Supraclavicular Free Flap With Vascularized Lymph Node Transfer for Treatment of Lymphedema: A Prospective Study of 100 Consecutive Cases ANDRES A. MARDONADO, MD, PhD, RU CHEN, MD, AND DAVID W. CHANG,

MD, FACS*

Section of Plastic and Reconstructive Surgery, Department of Surgery, University of Chicago Medical Center, Chicago, Illinois

Background and Objectives: Vascularized lymph node transfer (VLNT) is gaining popularity for treatment of lymphedema. The purpose of this study was to evaluate the flap and the donor site morbidity of the supraclavicular (SC) VLNT. Methods: A review of a prospective database was performed for patients who had undergone SC VLNT to treat upper or lower extremity lymphedema. Flap and donor site complications were registered for each patient. A detailed technical surgical approach is explained. Results: One hundred consecutive patients with lower or upper extremity lymphedema underwent SC VLNT (84% from the right side) with a mean of 11-months follow-up (range 3–19 months). There were no flap loss but three flaps (3%) required re-exploration due to venous congestion of the skin paddle. Two patients had local infection and three patients developed chyle leak (3%) at the donor site but resolved spontaneously. No donor site secondary lymphedema was noted. Conclusions: This is the largest prospective series of SC free flap VLNT for treatment of lymphedema. Low flap and donor site morbidity makes this flap an appealing source of lymph node transfer for lymphedema treatment.

J. Surg. Oncol.

ß 2016 Wiley Periodicals, Inc.

KEY WORDS: supraclavicular flap; lymph node transfer; lymphedema; free flap

INTRODUCTION Vascularized lymph node transfer (VLNT) has recently gained significant popularity for treatment of lymphedema [1]. The superficial groin, axilla, and submental regions have all been described as useful sources for vascularized lymph nodes. The most dreaded complication of harvesting lymph nodes from groin and axilla is the risk of secondary donor site lymphedema [2,3]. Meanwhile, submental lymph node transfer leads to unsightly visible donor-site scar and the potential for injury to the marginal mandibular nerve [4]. In a search for a better source of vascularized lymph nodes for transfer to treat lymphedema, the use of free supraclavicular flap with its deep cervical lymph nodes was previously published by the senior author [5]. The advantages include lower risk of secondary lymphedema and less conspicuous scar with minimal donor site complications.

Historical and Anatomical Review of Supraclavicular Flap The supraclavicular flap was initially described by Kazanjian and Converse as “in charretera” or acromial flap in 1949 [6]. Its clinical use was reported by Mathes and Wilson in the 1970s [7,8]. The introduction of the highly reliable pectoralis major myocutaneous flap made the supraclavicular flap a second line flap of choice until Pallua et al., in the 1990s, described the refinement of this flap, increasing its reliability and leading to its recent resurgence for head and neck reconstruction [9,10]. The supraclavicular flap has been used mainly as a pedicle flap to cover defects over the sternum, neck, trachea, retroauricular area, cheek, and oral cavity, and is considered a very reliable flap [11–13]. Supraclavicular flap complications have been discussed by Nthumba et al. [14]. They reviewed 349 pedicled supraclavicular flaps in patients from 14 different studies. The complication rate for flap failures was 1.4% (5), partial necrosis 6.9% (24), with overall complication rate of 8.3% (29 flaps), including wound dehiscence, infection, and hypertrophic scars [15].

ß 2016 Wiley Periodicals, Inc.

The blood supply of supraclavicular flap is based on the supraclavicular artery (SCA) (1.0–1.5 mm) and vein (1.0–1.5 mm). Cadaver dissections have shown that the SCA arises 3–4 cm from the origin of the transverse cervical artery, found in the triangle between the dorsal edge of the sternocleidomastoid muscle, the external jugular vein, and the medial part of the clavicle [10]. Moreover, the SCA runs along two accompanying veins; one or two veins may drain into the transverse cervical vein, and the other may drain into the external jugular vein [16]. When harvested as a free lymph node transfer without the skin component, the blood supply comes from branches of transverse cervical artery and vein. Innervation is supplied by the cervical nerves (C3–C4). Branches of the supraclavicular nerve were found to emerge from the deep fascia at a separate location from the vascular pedicle with the major nerve root exiting underneath the sternocleidomastoid muscle near the midpoint of the muscle belly [17]. Other important nerves present in this area are the phrenic nerve and the vagus nerve (lateral and medial to internal jugular, respectively). The lymph nodes in the supraclavicular area belong to the Vb level according to the American Academy of Otolaryngology-Head and Neck Surgery modification of the system of assigning levels for cervical lymph nodes. The main lymphatic drainage of this group of lymph nodes comes from breast, lung, esophagus, and thyroid [18]. Efferent lymphatics (typically 2–3) form the SC trunk, which enters the

Conflicts of interest: Nothing to declare. *Correspondence to: David W. Chang, MD, FACS, Section of Plastic and Reconstructive Surgery, University of Chicago, 5841 S. Maryland Avenue, MC 6035, Chicago, IL 60637. Fax: 773-702-1634. E-mail: [email protected] Received 6 June 2016; Accepted 27 June 2016 DOI 10.1002/jso.24351 Published online in Wiley Online Library (wileyonlinelibrary.com).

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subclavian venous angle either directly, or via the thoracic duct (or the right lymphatic duct) [19]. In this paper, we evaluated a prospectively collected data of 100 consecutive patients who underwent vascularized lymph node transfers harvested from the supraclavicular region for the treatment of upper or lower extremity lymphedema. The questions we wanted to address included: is the flap reliable? What are possible donor site complications? Specifically, what is the risk of causing secondary lymphedema?

MATERIALS AND METHODS This prospective study was approved by our Institutional Review Board. One hundred consecutive patients with extremity lymphedema were enrolled in the study and underwent supraclavicular lymph node (SCLN) transfer at our institution between September 2013 and December 2015. Age, sex, body mass index (BMI), location, lymphedema etiology, duration of lymphedema, indocyanine green (ICGN) and clinical stage, preoperative lymphedema life impact scale (LLIS), flap and donor site complications were registered for each patient. Clinical stage was based on the 2013 consensus classification by the International Society of Lymphology [20], and the ICGN stage was based on the classification previously described by the senior author [21–24].

Surgical Approach Right side was the preferred site for harvesting of supraclavicular lymph node transfer to avoid thoracic duct on the left side. Left side was used only if the patient presented with right arm lymphedema. The flap can be harvested with a skin paddle or without the skin depending on the soft tissue requirement of the recipient site. SCLN are found in the triangle formed by sternocleidomastoid (SCM) muscle medially, the clavicle inferiorly, and the external jugular vein laterally (Fig. 1). The incision is performed from the lateral border of the SCM muscle, 1 cm above the clavicle and about 5 cm toward the external jugular vein. The first structure found is platysma muscle. Under the platysma muscle, one or two branches of supraclavicular nerves will be encountered and sometimes need to be cut to facilitate the dissection. If needed, nerve endings are hemoclipped and allowed to fall deep into the donor site to avoid painful neuroma. The lateral border of SCM is retracted after opening the platysma. When the skin paddle is harvested, external jugular vein (EJV) or its branches are often included to facilitate venous drainage of the flap. The omohyoid muscle is then encountered and divided. Dissection proceeds carefully along the lateral border of the internal

Fig. 1. Preoperative marks for supraclavicular flap dissection. Journal of Surgical Oncology

jugular vein (IJV). Meticulous hemostasis is essential. All lymphatic ducts are carefully preserved or ligated. The transverse cervical vessels are found deep below the omohyoid muscle (Fig. 2). Occasionally, the transverse cervical artery can be very small and it needs to be followed to the thyrocervical trunk where the size gets larger. The surrounding fat with visible lymph nodes are dissected above the anterior scalene muscle. Lymphatic channels can be viewed during the dissection. Clipping one side and leaving the flap side of the channel open is important in order to avoid donor site lymphorrhea and to allow theoretical growth factors and lymphangiogenesis regeneration on the recipient side. A caution must be made to ensure that thoracic duct or major lymphatic duct is not damaged inadvertently (Fig. 3). If a major lymphatic duct must be ligated to facilitate the harvesting of the lymph nodes, it should be re-implanted to a branch of the vein under the microscope. Phrenic nerve will be visible on top of the scalene muscle and needs to be preserved. The donor site is closed with subdermal and intracuticular sutures. A drain is placed until the output falls below 30 cc over 24 hr for 2 consecutive days. The flap is monitored for 72 hr using an implantable doppler placed distal to the arterial anastomoses if buried or clinically if skin paddle is included. The patient is usually discharged on the third day.

RESULTS One hundred patients underwent SCLNT for treatment of extremity lymphedema with a mean of 11-months follow-up (range 3–19 months). Of 100 flaps, 84 were harvested without the skin paddle and 16 with the skin paddle. The average age of the patients was 55 years (range 24–81 years). The average duration of lymphedema was 8.2 years (range 1–62 years); 90% of the patients were female; average BMI was 27 (range 20–48); 78% had secondary lymphedema and 22% had primary lymphedema; 58% of the patients had stage I clinical lymphedema, the rest having stage II; the mean ICGN stage was 3.1 (range 1–4); the average preoperative volume differential for lymphedematous extremities of patients compared with their unaffected contralateral extremity was 26% (range 2–73%). 84% of SCLN were transferred from the right side; the recipient side was 16% right axilla, 34% left axilla, 20% right groin, and 30% left groin.

Flap Complications There was no flap loss. Three flaps (3%) required reexploration, one of them with skin island. Reexploration was performed immediately after the acute loss of signal from the implantable Doppler in two cases, with both flaps being saved. In the third case, reexploration was performed 6 hr after signal was lost on the skin paddle. The anastomoses

Supraclavicular Lymph Node Transfer

Fig. 4.

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A typical donor site scar.

successfully. There were minimum paresthesia complaints without dysesthesia during the first month, particularly over the more caudal skin below the scar. No secondary donor site lymphedema was noted (Fig. 5).

DISCUSSION

Two patients developed donor site infection. One of them was successfully treated with oral antibiotics, and the second one required intraoperative wash, drain, and intravenous antibiotics. Both donor site patients healed 1 month after surgery. Chyle leak developed in three patients (3%). All resolved spontaneous with medium chain diet and drain suction. All scars healed well and were noted to be aesthetically pleasing by most patients (Fig. 4). One patient presented with a lymphocele 1 year following the surgery. It was removed in OR

This is the first large study of using a supraclavicular free flap as donor site for lymph node transfer in upper and lower extremity lymphedema patients. In our practice, flap reliability, inconspicuous scar, and low risk for donor site morbidity including secondary lymphedema, make the supraclavicular our first option for LNT when there is no need for a combined large soft tissue reconstruction. However, safe harvesting of this flap requires full knowledge of the anatomy, complete understanding of potential donor site morbidity and meticulous attention to surgical technique. First, there is a significant anatomic variation of arterial and venous supply in this region, both in terms of the location and the size. The surgeon must be able to adjust the approach accordingly to ensure blood supplies to the lymph nodes are preserved during the dissection. Furthermore, there are many important structures in the region including carotid artery, internal jugular vein, phrenic nerve, and thoracic duct. A meticulous surgical approach is required to avoid damaging any key structures and also to prevent devastating complications. The main complication that we all are concerned when harvesting vascularized lymph nodes are causing secondary donor site lymphedema. Vignes et al. [25–27] recently detailed 38% of patients developing complications on the groin donor site, most frequently leading to iatrogenic ipsilateral limb lymphedema. Thus, for groin and axillary lymph

Fig. 3. Donor site after supraclavicular lymph node transfer. Preserved lymphatic vessel can be seen medially. Phrenic nerve running over the scalene muscle is seen.

Fig. 5.

Fig. 2.

Supraclavicular lymph node flap after dissection.

were open but the skin paddle remained congested, and the skin component of the flap required debridement.

Donor Site Complications

Journal of Surgical Oncology

Complications.

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nodes, most of us use reverse mapping techniques to help avoid damaging the sentinel nodes in that region. The supraclavicular lymph nodes mainly drain breast, lung, esophagus, and thyroid. There has been one anecdotal communication to the senior author that upper limb lymphatic drainage to the supraclavicular area has been seen on an injection study. There has been one case-report of donor-site arm lymphedema following SC flap of a same case by two different groups of authors [28,29]. It is uncertain what type of approach was used in this particular case, but when the photo of the case is carefully seen, the donor site scar appears very different than ours in terms of the location as well as the extent of the deformity. Another donor site for LNT is the submental area, popularized by Cheng et al. [4]. Although it shares with the SC LNT the advantage of low risk of donor site lymphedema, harvesting from the submental region results in a visible donor site scar and potential injury to the marginal mandibular nerve. We hereby present a first large prospective study using the SC LNT for upper and lower extremities. Although there is not a perfect donor site for LNT, our results have been very encouraging in terms of low flap and donor site morbidity.

CONCLUSION Based on our experience, with careful understanding of the anatomy and meticulous surgical dissection, supraclavicular vascularized lymph node transfer can be performed safely with minimal flap and donor-site morbidity.

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11. Pallua N, E Demir: Postburn head and neck reconstruction in children with the fasciocutaneous supraclavicular artery island flap. Ann Plast Surg 2008;60:276–282. 12. Chiu ES, Liu PH, Friedlander PL: Supraclavicular artery island flap for head and neck oncologic reconstruction: Indications, complications, and outcomes. Plast Reconstr Surg 2009;124: 115–123. 13. Pallua N, Wolter TP: Defect classification and reconstruction algorithm for patients with tracheostomy using the tunneled supraclavicular artery island flap. Langenbecks Arch Surg 2010;395:1115–1119. 14. Nthumba PM: The supraclavicular artery flap: A versatile flap for neck and orofacial reconstruction. J Oral Maxillofac Surg 2012;70: 1997–2004. 15. Rashid M, Zia-Ul-Islam M, Sarwar SUR, et al.: The “expansile” supraclavicular artery flap for release of postburn neck contractures. J Plast Reconstr Aesthet Surg 2006;59: 1094–1101. 16. Vinh VQ, Van Anh T, Ogawa R, et al.: Anatomical and clinical studies of the supraclavicular flap: Analysis of 103 flaps used to reconstruct neck scar contractures. Plast Reconstr Surg 2009;123: 1471–1480. 17. Sands TT, Martin JB, Simms E, et al.: Supraclavicular artery island flap innervation: Anatomical studies and clinical implications. J Plast Reconstr Aesthet Surg 2012;65:68–71. 18. Shah JP, Patel SG, Singh B, editors: Head and neck surgery and oncology. Philadelphia: Elsevier Health Sciences; 2012. 19. F€oldi M, F€oldi E, editors: Foldi’s textbook of lymphology for physicians and lymphedema therapists. Munich: Elsevier, Urban & Fischer Verlag; 2006. 20. International Society of Lymphology: The diagnosis and treatment of peripheral lymphedema: 2013 Consensus Document of the International Society of Lymphology. Lymphology 2013;1:1–11. 21. Suami H, Chang DW, Yamada K, et al.: Use of indocyanine green fluorescent lymphography for evaluating dynamic lymphatic status. Plast Reconstr Surg 2011;127:74–76. 22. Chang DW, Suami H, Skoracki R: A prospective analysis of 100 consecutive lymphovenous bypass cases for treatment of extremity lymphedema. Plast Reconstr Surg 2013;132:1305–1314. 23. Chang DW: Lymphaticovenular bypass for lymphedema management in breast cancer patients: A prospective study. Plast Reconstr Surg 2010;126:752–758. 24. Patel KM, Lin CY, Cheng MH: A prospective evaluation of lymphedema-specific quality-of-life outcomes following vascularized lymph node transfer. Ann Surg Oncol 2014;22:1–7. 25. Patel KM, Chu S-Y, Huang JJ, et al.: Preplanning vascularized lymph node transfer with duplex ultrasonography: An evaluation of 3 donor sites. Plast Reconstr Surg 2014;2:193. 26. Gomez Martın C, Murillo C, Maldonado AA, et al.: Double autologous lymph node transplantation (ALNT) at the level of the knee and inguinal region for advanced lymphoedema of the lower limb (elephantiasis). J Plast Reconstr Aesthet Surg 2014;67: 267–270. 27. Vignes S, Blanchard M, Yannoutsos A, et al.: Complications of autologous lymph-node transplantation for limb lymphoedema. Eur J Vasc Endovasc Surg 2013;45:516–520. 28. 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;135:939–940. 29. Lee M, McClure E, Reinertsen E, et al.: Lymphedema of the upper extremity following supraclavicular lymph node harvest. Plast Reconstr Surg 2015;135:1079–1082.

SYNOPSIS The purpose of this study was to evaluate the flap and the donor site morbidity of the supraclavicular (SC) VLNT. This is the largest prospective series of SC free flap VLNT for treatment of lymphedema. Low flap and donor site morbidity makes this flap an appealing source of lymph node transfer for lymphedema treatment. Journal of Surgical Oncology

The use of supraclavicular free flap with vascularized lymph node transfer for treatment of lymphedema: A prospective study of 100 consecutive cases.

Vascularized lymph node transfer (VLNT) is gaining popularity for treatment of lymphedema. The purpose of this study was to evaluate the flap and the ...
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