Journal of Plastic, Reconstructive & Aesthetic Surgery (2015) 68, 419e427
Lymphatic anatomy of the inguinal region in aid of vascularized lymph node flap harvesting* Mario F. Scaglioni, Hiroo Suami* Department of Plastic and Reconstructive Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA Received 27 June 2014; accepted 31 October 2014
KEYWORDS Vascularized lymph node transfer; Lymphatic system; Lymphedema; Sentinel lymph node; Indocyanine green fluorescence lymphography; Inguinal lymph nodes
Summary Background: Vascularized lymph node transfer (VLNT) has shown promise as a treatment for breast cancererelated lymphedema, a common and debilitating condition among breast cancer survivors. In VLNT, the most popular lymph node flap donor site is the inguinal region; however, concerns about the possibility of iatrogenic lymphedema hamper the widespread adoption of VLNT. A better understanding of the anatomy of the lymphatic system in the inguinal region is essential to preserving lymph drainage in the leg and avoiding iatrogenic lymphedema. Methods: Five human cadaver hind-quarter specimens were used for this study. First, the specimens were scanned with indocyanine green fluorescence lymphography to map the lymphatic vessels. A dual injection technique using different radiocontrast media was then applied to delineate arteries and lymphatic vessels on radiographs. Finally, radiological analysis and meticulous dissection were used to investigate relationships between the arteries and lymphatic vessels. Results: By chasing the lymphatic vessels retrogradely from their corresponding lymph nodes, we were able to divide the superficial inguinal lymph nodes into three subgroups: the abdominal, medial thigh, and lateral thigh nodes. We found no connections between the superficial and deep lymphatic system in the inguinal region. The dominant lymph nodes draining the leg were in the lower part of the inguinal triangle, and their efferent lymphatic vessels ran medial to the common femoral artery.
* Presented in part at the 3rd International Symposium on Lymphedema Surgical Treatment, Barcelona, Spain, March 5, 2014; Presented in part at the 10th Australasian Lymphology Association Conference, Auckland, New Zealand, from April 3e5, 2014. * Corresponding author. Department of Plastic Surgery, Unit 1488, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd. Houston, TX 77030, USA. Tel.: þ1 713 794 1247; fax: þ1 713 794 5492. E-mail address: [email protected] (H. Suami).
http://dx.doi.org/10.1016/j.bjps.2014.10.047 1748-6815/ª 2014 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
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M.F. Scaglioni, H. Suami Conclusions: Preserving the sentinel nodes of the lower leg in the medial thigh and their efferent lymphatic vessels is crucial to avoid iatrogenic lymphedema in limbs with donor sites for VLNT. ª 2014 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
Introduction Lymphedema is a chronic, progressive, debilitating condition, affecting up to 250 million people worldwide. In developed countries, cancer treatments are the major cause of lymphedema.1e4 Breast cancererelated lymphedema (BCRL) is a well-known common issue among breast cancer survivors; axillary lymph node dissection (Odds ratio (OR) 1.3e6.7), chemotherapy (OR 1.6e2.0), and irradiation (OR 1.7e3.8) increase its risk.5 The standard treatment for lymphedema is decongestive therapy consisting of exercise, compression garment use, skin care, and manual lymph drainage. However, lymphedema that is resistant to the standard treatment requires surgery, which is a challenging task. Although several surgical modalities for addressing lymphedema have been introduced, none offers a definitive cure. Vascularized lymph node transfer (VLNT) has been gaining popularity as a prospective promising option for the surgical treatment of lymphedema since Becker et al. reported its outcomes for patients with BCRL.6 In VLNT, free flaps that includes lymph nodes are transferred to the regions where lymph nodes have been removed for cancer treatment7,8 or to the distal parts of lymphedematous limbs9,10 to restore lymphatic drainage. Donor sites for VLNT have included the inguinal,6e10 lateral thoracic,11 submental,12 and supraclavicular regions.13 The most popular VLNT donor site in patients with BCRL is the inguinal region because its lymph node flap can be combined with abdominal flaps to simultaneously accomplish delayed autologous breast reconstruction and VLNT.6,7 One major concern regarding the harvest of inguinal lymph nodes for VLNT is the possibility of causing iatrogenic lymphedema in the donor limb. Becker et al. stressed that the superficial inguinal lymph nodes located along the superficial circumflex iliac vein drain lymph fluid mainly from the abdominal wall and that their procurement did not impair lymph drainage of the lower limb.11 Viitanen et al. used circumferential measurement and quantitative lymphoscintigraphy to assess lymphatic function in the donor lower extremities and found that although no patients developed symptoms of postoperative lymphedema, lymphatic transport function was often impaired in the donor limb.14 Pons et al. reported a case of irreversible iatrogenic lymphedema associated with VLNT and advised surgeons to take precautions to prevent iatrogenic lymphedema.15 Current knowledge about the anatomy of the lymphatic system is largely based on anatomy atlases depicting lymphatic vessels that were detected using mercury injection method.16e18 Detailed anatomic knowledge of the
lymphatic system is crucial to avoid donor site lymphedema following flap harvest for VLNT. Some studies have already provided useful anatomic information about the inguinal lymph nodes targeted for VLNT: Dayan et al. used magnetic resonance angiography to identify the number of inguinal lymph nodes and their location relative to anatomical landmarks,19 and Zhang et al. performed a similar study using computed tomography angiography.20 However, no studies have described the lymphatic vessels that connect nodes or the direction of lymphatic drainage, two important factors that must be considered to preserve lower extremity lymph drainage. To demonstrate the lymphatic system radiographically, Kinmonth developed a lymphangiography technique that included cannulation directly into the lymphatic vessel at the dorsal foot and injection of contrast medium into the vessel to demonstrate
Figure 1 Lymphangiogram of the normal right lower extremity. Sentinel lymph nodes of the lower leg (black arrows) and their efferent lymphatic vessels (white arrows) are shown.
Lymphatic anatomy of the inguinal region
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radiographic image of the lymphatic system.21 The lymphangiography images clearly demonstrated the sentinel lymph nodes of the lower leg and their efferent lymphatic vessels, which are the main tracts that must be preserved during VLNT (Figure 1). In the present anatomic study, we used our original microinjection technique akin to Kinmonth’s in a cadaver model to 1) investigate the relationship between the lymphatic system in the abdomen and that in the lower extremity, 2) track the course of the sentinel lymph nodes’ efferent lymphatic vessels in the lower extremity, and 3) elucidate the relationship between the lymphatic system and arteries in the inguinal region in order to secure blood supply to the vascularized lymph node flap.
Materials and methods Indocyanine green fluorescence lymphography study Five hind-quarter specimens from three fresh female cadavers of moderate size without scars were selected for the study. The cadavers were obtained from the Willed Body Program of the Department of Neurobiology and Anatomy at The University of Texas Medical School at Houston. Before two cadavers were separated into parts for frozen storage, 0.3 ml of indocyanine green (ICG) (IC-Green; Akorn, Inc., Lake Forest, IL, USA) was injected into the dermis at multiple locations in the toe webs, edge of the foot, and lateral thigh and in abdominal regions along a horizontal line at the umbilical level and along the sagittal midline. To facilitate the uptake and dispersal of ICG into the lymphatic system, we massaged the body by hand for 20 min beginning at the injection sites and continuing towards the inguinal regions. The body was then scanned using an ICG fluorescence lymphography system (Photodynamic Eye; Hamamatsu K.K., Hamamatsu, Japan), which detects the near-infrared radiation from the ICG compound to demonstrate anatomical structures up to 12 mm below the surface of the skin. Using the images displayed on a monitor as a guide, we used a marker to map the lymphatic pathways on the skin (Figure 2; see also Video, Supplemental Digital Content 1, which shows ICG lymphography of the cadaver lower limb). Supplementary data related to this article can be found online at http://dx.doi.org/10.1016/j.bjps.2014.10.047. After lymphatic mapping was complete, the body was eviscerated using a frontal midline incision from the sternal notch to the pubic symphysis. The hind-quarter specimen was separated using a horizontal incision at the umbilical level, and the spinal bone, pubic symphysis, and sacral bone were cut along the sagittal midline using an electric reciprocating saw. The specimens were kept in frozen storage until the second injection procedure was performed.
Dual injection technique To demonstrate the lymphatics and arteries simultaneously and to discriminate between them, we used a modified
Figure 2 Indocyanine green lymphangiography (left) and tracing of the lymphatic vessels (right).
version of a radiographic microinjection technique Suami et al. developed to visualize the lymphatic system in a cadaver model.22,23 First, we inserted a 16- or 18-French urinary catheter into the external iliac artery and injected approximately 300 ml of a radio-opaque mixture of 30% zinc oxide (Fisher Scientific, Pittsburgh, PA), 20% latex rubber (Carolina Biological Supply Company, Burlington, NC), and 50% water. The pink latex rubber solidified inside arterial lumen within half a day. Second, we cut the skin around the ankle joint using the ICG lymphographyebased lymphatic maps as a guide and identified the lymphatic vessels by inflating them with 3% hydrogen peroxide. We then injected a radio-opaque mixture of 30% barium sulfate (Fisher Scientific, Pittsburgh, PA), 70% 3% hydrogen peroxide, and a few drops of acrylic dye (Liquitex Artist Color Materials, Piscataway, NJ); Prussian blue, deep violet, and phthalocyanine green, into each lymphatic vessel. We also identified the lymphatic vessels in the lateral thigh and lower abdominal regions and injected them with the barium sulfate mixture. Because barium sulfate (injected into the lymphatics) and zinc oxide (injected into the arteries) have different radiocontrast intensities,24 we were able to distinguish between lymphatic vessels and arteries on radiographs. We chased each afferent lymphatic vessel injected with barium sulfate using meticulous dissection under microscopy (Discovery V8; Carl Zeiss, Inc., Thornwood, NY) until the vessel reached the first-tier (sentinel) lymph node. Because the barium sulfate mixture perfused no further than a regional lymph node, we injected 0.3e0.5 ml of 3% hydrogen peroxide into the subcapsular space of the lymph
422 node to inflate and identify the efferent lymphatic vessels. We repeated this lymphatic microinjection procedure to fill the efferent lymphatic vessels until the injected mixture reached the intrapelvic region beyond the inguinal ligament. Lymph nodes were delineated radiographically by tagging them with round brass tabs. Valvular structures inside the lumen of the lymphatic vessels that regulate lymphatic flow unidirectionally were assessed to determine the direction of lymphatic drainage. The lymphatic vessels’ course and their relationship to the inguinal lymph nodes were recorded using digital photography (PowerShot G12, Cannon USA, Inc., Melville, NY), and their flow directions were noted.
Radiological analysis After completing the dual injection procedures in the arteries and lymphatic vessels, we radiographed the hindquarter specimen using an FCR Go portable x-ray system (Fujifilm Medical Systems USA Inc., Stamford, CT) (Figure 3). Skin and soft tissue in the front thigh and intrapelvic regions were separated from the femoral and pelvic bones using mid-lateral and mid-medial incisions. The dissected specimen was spread on a plastic board and radiographed. Montages of the radiographic images were created on a desktop computer, and graphic software (Adobe Photoshop CS6, Adobe Systems Inc., San Jose, CA) was used to trace the arteries and lymphatic vessels and indicate their flow directions (Figures 4 and 6).
Figure 3 A radiograph of the right hind-quarter specimen after completion of the dual injection technique. Lymph nodes with brass tabs (white), lymphatic vessels (black), and the femoral artery (red) are shown in a radiograph.
M.F. Scaglioni, H. Suami
Results ICG fluorescence lymphography images of cadavers that had been injected with ICG and massaged showed clearly delineated shiny linear structures running axially and proximally in the lower leg. Subsequent dissection confirmed that these shiny linear structures were lymphcollecting vessels running through the subcutaneous fat. Uptake of ICG into the lymphatic vessels was highly selective, and ICG fluorescence lymphography demonstrated no other vascular structures. We could track the lymphatic vessels until just below the knee, but they were no longer visible above the knee. Although the ICG injected around the foot could delineate the lymphatic vessels in a manner similar to that of imaging studies in live humans, the ICG injected at the lateral thigh and lower abdominal regions remained at the injection site and did not demonstrate any structures. Mapping the lymphatic vessels reduced the time required to search for them and thus facilitated the process of injecting the radio-opaque mixture. The different radiocontrast intensities of the two radiopaque formulas (zinc oxide and barium sulfate) enabled us to discriminate between lymphatic vessels and arteries on radiographs (Figures 3 and 4). The lymphatics and arteries were also distinguished by their branching patterns; arteries have a dendritic and tapering pattern, whereas lymphatic have a linear and uniform pattern. Tagged metal tabs were used to delineate the locations of the inguinal lymph nodes on radiographs (Figures 3 and 4). Barium sulfate and zinc oxide are less toxic than lead oxide, which we previously used as contrast media for cadaver injection studies. Barium sulfate, which can be stained any color, helped to distinguish lymphatic vessels from surrounding yellow fat tissue (Figure 5). Our novel dual injection technique could also demonstrate arterial blood supply to the lymph nodes (Figure 5, bottom). Radiographs and photographs revealed that the lymphatic vessels originating from the lower leg converged in the medial thigh and ran towards the inguinal region. These lymphatic vessels formed a medial bundle running parallel with the great saphenous vein and were consistently found to connect to 2 or 3 sentinel lymph nodes located in the distal part of the inguinal triangle (lymph nodes A, B, and C in Figures 5 and 6). The two most distal lymph nodes (A and B) were considered to be the dominant lymph nodes draining the lower leg, and they were consistently located on both sides of the great saphenous vein (Figure 5). These sentinel nodes’ efferent lymphatic vessels did not connect to any lymph nodes within the inguinal triangle, ran straight into the pelvis, and always ran first along the medial side of the common femoral artery and then along the external iliac artery. The lymphatic vessels in the lateral thigh region were sparse. These vessels did not connect to the two dominant lymph nodes but did connect to the lymph nodes located at the lateral part of the inguinal triangle. The lymphatic vessels in the lower abdominal area were identified 5e10 cm below the boundary at which the specimen was excised from the cadaver. These vessels converged unidirectionally towards the first-tier lymph node located in the upper part in the inguinal triangle
Lymphatic anatomy of the inguinal region
423 (SCIA) (Figures 4 and 6, left) and were located close to the SCIA. However, in the absence of the SCIA in one specimen, these lymph nodes were supplied by the superficial inferior epigastric artery (SIEA) (Figures 5 and 6, right) and were located in its vicinity. The abdominal lymph nodes at the medial side (nodes G and H in Figure 6, left; node F in Figure 6, right) received their blood supply from anonymous branches from the common femoral artery. The superficial lymphatic vessel, which ran along the short saphenous vein in the calf region, connected to the popliteal lymph nodes in the popliteal fossa. The efferent lymphatic vessel of the popliteal nodes ran deep and along the deep femoral artery posteriorly. In the inguinal region, the vessel ran posterior to the common femoral artery and did not connect to either the superficial lymphatic vessels or lymph nodes (Figure 6, right). However, the vessel did connect to an intrapelvic lymph node above the inguinal ligament.
Discussion
Figure 4 A vascularized groin lymph node flap (lateral (*) and medial side (**)) dissected from a right hind-quarter specimen; a view of the undersurface of the flap (top), a radiograph of the flap (middle), and tracing of the radiograph (bottom) are shown. The artery (red) is the superficial circumflex iliac artery.
(node F in Figure 6, left; node E in Figure 6, right). The efferent lymphatic vessels of the first-tier node ran medially. Two to four lymph nodes situated superficial to the Scarpa’s fascia were aligned in parallel below the inguinal ligament. The efferent lymphatic vessels of the upper medial node ran deep, passed below the inguinal ligament, and approached the efferent lymphatic vessels of the dominant lymph node medially. The lymph nodes in the abdominal group received their blood supply from the superficial circumflex iliac artery
Anatomical atlases made by Mascagni (Figure 7)17 and Sappey18 both depict two lymph nodes located in the distal part of the inguinal triangle that connect to lymphatic vessels from the medial thigh. Kinmonth’s lymphangiography technique demonstrated two similar lymph nodes (Figure 1). These lymph nodes may be the dominant lymph nodes draining the lower leg that we identified in the present study. In previous studies, our group investigated the lymphatic system in the upper extremity in a cadaver model26,27 and consistently found one or two dominant lymph nodes at the lateral axillary region. We presume that the anatomic structure of the upper extremity is similar to that of the lower extremity and that, like the upper extremity, the lower extremity has two or three dominant nodes. Recognition of the sentinel lymph nodes of the lower leg potentially has clinical importance regarding the use of sentinel node biopsy for skin cancer in the lower leg and the avoidance of iatrogenic lymphedema following VLNT. Ours is the first study to use ICG imaging to map lymphatics in a fresh cadaver (Figure 2). These images were similar to the ICG lymphography images of lymphatic vessels in normal lower extremities.25 We knew from previous studies that an intradermal injection of the dye into the finger webs sometimes demonstrates the lymphatic vessels in frozen and thawed cadaver specimens, however, the injected dye traveled only several centimeters in the lymphatic lumen in the frozen specimens.26 In the present study, our use of fresh, non-frozen cadavers for the ICG imaging studies may explain why the ICG traveled the long distance from the foot to below the knee. Although the injected ICG could demonstrate the lymphatic vessels in the lower leg, it did not demonstrate them in the abdominal and lateral thigh regions, which were different from the ICG imaging in clinical settings. Although we are unable to account for the difference in ICG activity between the foot and the abdominal and lateral thigh regions we speculate that the lymphatic system in the terminal area of the body may have an anatomic structure that enables it to capture foreign material more effectively.
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Figure 5 Photographs of the right inguinal area after dissection (right side is distal). Lymphatic vessels in the medial thigh (blue) and in the abdomen (green); lymph nodes (A to F); the superficial inferior epigastric artery (SEA); and the great saphenous vein (SV) are shown. Arrows indicate the arterial supply to the lymph nodes.
M.F. Scaglioni, H. Suami On the basis of findings from cadaver studies,26,28 animal experiments,29,30 historical reviews,24,25,31 and clinical diagnostic imaging studies,32e34 the senior author proposed the concept of “lymphosomes” to describe territories of the superficial lymphatic system and their corresponding lymph nodes. In the present study, the superficial lymph nodes in the inguinal region could be divided into three subgroups based on the connecting lymphatic vessels: the abdominal group, the lateral thigh group, and the medial thigh group (Figure 8). Each group of lymph nodes was color-coded, and their corresponding lymphatic vessels were also colorcoded retrogradely from the node, thereby delineating them as lymphosomes. Although the lymphatic system has minor differences among individuals and between sides of the body, we could successfully approximate a general pattern of the superficial lymphatic drainage. We expect that the lymphosome concept will increase our understanding of the lymphatic system and enable us to define suitable lymph node donor sites for VLNT. According to our findings, the abdominal lymph node group could be targeted for VLNT, whereas the medial thigh lymph node group must be preserved (Figure 9).
Figure 6 Mapping arteries and lymphatic vessels demonstrated on radiographs in two specimens. Purple indicates efferent lymphatic vessels of the leg sentinel nodes (AeC); blue, deep lymphatic vessels; green, superficial lymphatic vessels; and red, arteries. The “*” indicates the superficial circumflex iliac artery; “**” indicates the superficial inferior epigastric artery. The black arrowheads indicate directions of lymph flow.
Lymphatic anatomy of the inguinal region
Figure 7 Mascagni’s diagram depicts the leg sentinel nodes (arrows). (From Mascagni P. Vasorum Lymphaticorum Corporis Humani Historia et Ichnographia. Siena: Pazzini Carli; 1787.)
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Figure 9 Schematic diagram of lymphatic drainage in the inguinal region. Lymph drains from the leg via the sentinel nodes (yellow) and their efferent lymphatic vessels (purple), and surgeons should avoid disturbing these nodes and vessels during VLNT. Lymph drains from the abdominal (orange), lateral thigh (green), and deep lymphatics (blue) are shown.
Our cadaver dissection results showed that the inguinal lymph nodes, which were responsible for abdominal lymphatic drainage, are located along the lower edge of the inguinal ligament and supplied by the SCIA or SIEA and anonymous branches from the common femoral artery. Several groups have reported various surgical approaches to harvesting a lymph node flap for VLNT from the inguinal region.6,7,9e11,14,19 Our findings concur with those of previous reports describing how to harvest a VLNT flap without impairing the lymph drainage pathways in the lower extremity. However, there is little information about the importance of preserving the leg sentinel lymph nodes and their efferent lymphatic vessels. Other authors have described using reverse lymphatic mapping techniques in the upper extremity, in which dye is injected into the medial upper arm to stain the arm sentinel lymph nodes.34,35 We suggest applying the same reverse mapping technique to preserve leg lymphatic drainage following VLNT. The better understanding of the lymphatic system anatomy that such a technique would provide would hopefully contribute to safer VLNTs in patients with BCRL.
Conclusion Figure 8 Lymphosomes in the inguinal region: the abdominal (orange), lateral thigh (green), and medial thigh (yellow) groups are shown.
We developed a dual injection technique that uses two different contrast media (barium sulfate and zinc oxide) to
426 radiographically demonstrate the arteries, lymphatic vessels, and lymph nodes simultaneously in a cadaver model. The superficial inguinal lymph nodes can be divided into three subgroups: the abdominal, medial thigh, and lateral thigh groups. The abdominal group can be targeted for VLNT. The sentinel nodes in the medial thigh group are the dominant nodes draining the lower leg. Our anatomic study suggests that these nodes and their efferent lymphatic vessels must be preserved to retain lymphatic drainage of the lower extremity following VLNT.
Financial disclosure The authors have no sources of financial or other support and no financial or professional relationships that may pose a competing interest.
Ethical approval N/A.
Acknowledgments This study was supported in part by the Kyte Research and Education Fund, and by the Sister Institutional Network Fund 35640 at MD Anderson. The authors thank Rony Avristcher, M.D., Department of Interventional Radiology, The University of Texas MD Anderson Cancer Center for providing his advices.
References 1. Kissin MW, Querci della Rovere G, Easton D, Westbury G. Risk of lymphoedema following the treatment of breast cancer. Br J Surg 1986;73:580e4. 2. Armer J, Fu MR, Wainstock JM, Zagar E, Jacobs LK. Lymphedema following breast cancer treatment, including sentinel lymph node biopsy. Lymphology 2004;37:73e91. 3. Vignes S, Arrault M, Dupuy A. Factors associated with increased breast cancer-related lymphedema volume. Acta Oncol 2007; 46:1138e42. 4. 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;26:5213e9. 5. DiSipio T, Rye S, Hayes S. Incidence of unilateral arm lymphedema after breast cancer: a systematic review and metaanalysis. Lancet Oncol 2013;14:500e15. 6. Becker C, Assouad J, Riquet M, Hidden G. Postmastectomy lymphedema: long-term results following microsurgical lymph node transplantation. Ann Surg 2006;243:313e5. 7. Saaristo AM, Niemi TS, Viitanen TP, Tervala TV, Hartiala P, Suominen EA. Microvascular breast reconstruction and lymph node transfer for postmastectomy lymphedema patients. Ann Surg 2012;255:468e73. 8. Vignes S, Blanchard M, Yannoutsos A, Arrault M. Complications of autologous lymph-node, transplantation for limb lymphoedema. Eur J Vasc Endovasc Surg 2013;45:516e20. 9. 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;123:1265e75.
M.F. Scaglioni, H. Suami 10. Cheng MH, Chen SC, Henry SL, Tan BK, Lin MC, Huang JJ. Vascularized groin lymph node flap transfer for postmastectomy upper limb lymphedema: flap anatomy, recipient sites, and outcomes. Plast Reconstr Surg 2013;131:1286e98. 11. Becker C, Vasile JV, Levine JL, et al. Microlympahtic surgery for the treatment of iatrogenic lymphedema. Clin Plast Surg 2012;39:385e98. 12. Cheng MH, Huang JJ, Nguyen DH, et al. A novel approach to the treatment of lower extremity lymphedema by transferring a vascularized submental lymph node flap to the ankle. Gynecol Oncol 2012;126:93e8. 13. Sapountzis S, Singhal D, Rashid A, Ciudad P, Meo D, Chen HC. Lymph node flap based on the right transverse cervical artery as a donor site for lymph node transfer. Ann Plast Surg 2014; 73:398e401. 14. Viitanen TP, Ma ¨ki MT, Seppa ¨nen MP, Suominen EA, Saaristo AM. Donor-site lymphatic function after microvascular lymph node transfer. Plast Reconstr Surg 2012;130:1246e53. 15. Nuck A. Adenographia Curiosa et Uteri Foeminei Anatome Nova. Lyon: Betavorum, P. van der Aa; 1692. 16. Mascagni P. Vasorum lymphaticorum corporis humani historia et ichnographia. Sienna: Pazzini Carli; 1787. 17. Sappey MPC. Anatomie, Physiologie, Pathologie des Vaisseaux Lymphatiques Consideres Chez L’homme et les Vertebres. Paris: A. Delahaye and E. Lecrosnier; 1874. 18. Pons G, Masia J, Loschi P, Nardulli ML, Duch J. A case of donorsite lymphoedema after lymph node-superficial circumflex iliac artery perforator flap transfer. J Plast Reconstr Aesthet Surg 2014;67:119e23. 19. Dayan JH, Dayan E, Kagen A, et al. The use of magnetic resonance angiography in vascularized groin lymph node transfer: an anatomic study. J Reconstr Microsurg 2014;30: 41e5. 20. Zhang H, Chen W, Mu L, et al. The distribution of lymph nodes and their nutrient vessels in the groin region: an anatomic study for design of the lymph node flap. Microsurgery 2014;34: 558e61. 21. Kinmonth JB. The lymphatics: diseases, lymphography, and surgery. London, UK: Edward Arnold; 1972. 22. Suami H, Taylor GI, Pan WR. A new radiographic cadaver injection technique for investigating the lymphatic system. Plast Reconstr Surg 2005;115:2007e13. 23. Suami H, Taylor GI, O’Neill J, Pan WR. Refinements of the radiographic cadaver injection technique for investigating minute lymphatic vessels. Plast Reconstr Surg 2007;120:61e7. 24. Yamazaki S, Suami H, Imanishi N, et al. Three-dimensional demonstration of the lymphatic system in the lower extremities with multi-detector-row computed tomography: a study in a cadaver model. Clin Anat 2013;26:258e66. 25. 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: 1305e14. 26. Suami H, Taylor GI, Pan WR. The lymphatic territories of the upper limb: anatomical study and clinical implications. Plast Reconstr Surg 2007;119:1813e22. 27. Suami H, Pan WR, Taylor GI. Changes in the lymph structure of the upper limb after axillary dissection: radiographic and anatomical study in a human cadaver. Plast Reconstr Surg 2007;120:982e91. 28. Suami H, O’Neill JK, Pan WR, Taylor GI. Superficial lymphatic system of the upper torso: preliminary radiographic results in human cadavers. Plast Reconstr Surg 2008;121:1231e9. 29. Suami H, Shin D, Chang DW. Mapping of lymphosomes in the canine forelimb: comparative anatomy between canines and humans. Plast Reconstr Surg 2012:129612e20. 30. Bartels P. Das lymphgefasssystem. Jena, Germany: Verlag von Gustav Fischer; 1909.
Lymphatic anatomy of the inguinal region 31. Jossifow GM. Das Lymphgefasssystem des Menschen. Jena, Germany: Verlag von Gustav Fischer; 1930. 32. Reynolds HM, Dunbar PR, Uren RF, et al. Three-dimensional visualisation of lymphatic drainage patterns in patients with cutaneous melanoma. Lancet Oncol 2007;8:806e12. 33. Reynolds HM, Walker CG, Dunbar PR, et al. Functional anatomy of the lymphatics draining the skin: a detailed statistical analysis. J Anat 2010;216:344e55.
427 34. Thompson M, Korourian S, Henry-Tillman R, et al. Axillary reverse mapping (ARM): a new concept to identify and enhance lymphatic preservation. Ann Surg Oncol 2007;14:1890e5. 35. Boneti C, Korourian S, Bland K, et al. Axillary reverse mapping: mapping and preserving arm lymphatics may be important in preventing lymphedema during sentinel lymph node biopsy. J Am Coll Surg 2008;206:1038e42. discussion 1042e1044.
Lymphatic anatomy of the inguinal region in aid of vascularized lymph node flap harvesting* Mario F. Scaglioni, Hiroo Suami* Department of Plastic and Reconstructive Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA Received 27 June 2014; accepted 31 October 2014
KEYWORDS Vascularized lymph node transfer; Lymphatic system; Lymphedema; Sentinel lymph node; Indocyanine green fluorescence lymphography; Inguinal lymph nodes
Summary Background: Vascularized lymph node transfer (VLNT) has shown promise as a treatment for breast cancererelated lymphedema, a common and debilitating condition among breast cancer survivors. In VLNT, the most popular lymph node flap donor site is the inguinal region; however, concerns about the possibility of iatrogenic lymphedema hamper the widespread adoption of VLNT. A better understanding of the anatomy of the lymphatic system in the inguinal region is essential to preserving lymph drainage in the leg and avoiding iatrogenic lymphedema. Methods: Five human cadaver hind-quarter specimens were used for this study. First, the specimens were scanned with indocyanine green fluorescence lymphography to map the lymphatic vessels. A dual injection technique using different radiocontrast media was then applied to delineate arteries and lymphatic vessels on radiographs. Finally, radiological analysis and meticulous dissection were used to investigate relationships between the arteries and lymphatic vessels. Results: By chasing the lymphatic vessels retrogradely from their corresponding lymph nodes, we were able to divide the superficial inguinal lymph nodes into three subgroups: the abdominal, medial thigh, and lateral thigh nodes. We found no connections between the superficial and deep lymphatic system in the inguinal region. The dominant lymph nodes draining the leg were in the lower part of the inguinal triangle, and their efferent lymphatic vessels ran medial to the common femoral artery.
* Presented in part at the 3rd International Symposium on Lymphedema Surgical Treatment, Barcelona, Spain, March 5, 2014; Presented in part at the 10th Australasian Lymphology Association Conference, Auckland, New Zealand, from April 3e5, 2014. * Corresponding author. Department of Plastic Surgery, Unit 1488, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd. Houston, TX 77030, USA. Tel.: þ1 713 794 1247; fax: þ1 713 794 5492. E-mail address: [email protected] (H. Suami).
http://dx.doi.org/10.1016/j.bjps.2014.10.047 1748-6815/ª 2014 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
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M.F. Scaglioni, H. Suami Conclusions: Preserving the sentinel nodes of the lower leg in the medial thigh and their efferent lymphatic vessels is crucial to avoid iatrogenic lymphedema in limbs with donor sites for VLNT. ª 2014 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
Introduction Lymphedema is a chronic, progressive, debilitating condition, affecting up to 250 million people worldwide. In developed countries, cancer treatments are the major cause of lymphedema.1e4 Breast cancererelated lymphedema (BCRL) is a well-known common issue among breast cancer survivors; axillary lymph node dissection (Odds ratio (OR) 1.3e6.7), chemotherapy (OR 1.6e2.0), and irradiation (OR 1.7e3.8) increase its risk.5 The standard treatment for lymphedema is decongestive therapy consisting of exercise, compression garment use, skin care, and manual lymph drainage. However, lymphedema that is resistant to the standard treatment requires surgery, which is a challenging task. Although several surgical modalities for addressing lymphedema have been introduced, none offers a definitive cure. Vascularized lymph node transfer (VLNT) has been gaining popularity as a prospective promising option for the surgical treatment of lymphedema since Becker et al. reported its outcomes for patients with BCRL.6 In VLNT, free flaps that includes lymph nodes are transferred to the regions where lymph nodes have been removed for cancer treatment7,8 or to the distal parts of lymphedematous limbs9,10 to restore lymphatic drainage. Donor sites for VLNT have included the inguinal,6e10 lateral thoracic,11 submental,12 and supraclavicular regions.13 The most popular VLNT donor site in patients with BCRL is the inguinal region because its lymph node flap can be combined with abdominal flaps to simultaneously accomplish delayed autologous breast reconstruction and VLNT.6,7 One major concern regarding the harvest of inguinal lymph nodes for VLNT is the possibility of causing iatrogenic lymphedema in the donor limb. Becker et al. stressed that the superficial inguinal lymph nodes located along the superficial circumflex iliac vein drain lymph fluid mainly from the abdominal wall and that their procurement did not impair lymph drainage of the lower limb.11 Viitanen et al. used circumferential measurement and quantitative lymphoscintigraphy to assess lymphatic function in the donor lower extremities and found that although no patients developed symptoms of postoperative lymphedema, lymphatic transport function was often impaired in the donor limb.14 Pons et al. reported a case of irreversible iatrogenic lymphedema associated with VLNT and advised surgeons to take precautions to prevent iatrogenic lymphedema.15 Current knowledge about the anatomy of the lymphatic system is largely based on anatomy atlases depicting lymphatic vessels that were detected using mercury injection method.16e18 Detailed anatomic knowledge of the
lymphatic system is crucial to avoid donor site lymphedema following flap harvest for VLNT. Some studies have already provided useful anatomic information about the inguinal lymph nodes targeted for VLNT: Dayan et al. used magnetic resonance angiography to identify the number of inguinal lymph nodes and their location relative to anatomical landmarks,19 and Zhang et al. performed a similar study using computed tomography angiography.20 However, no studies have described the lymphatic vessels that connect nodes or the direction of lymphatic drainage, two important factors that must be considered to preserve lower extremity lymph drainage. To demonstrate the lymphatic system radiographically, Kinmonth developed a lymphangiography technique that included cannulation directly into the lymphatic vessel at the dorsal foot and injection of contrast medium into the vessel to demonstrate
Figure 1 Lymphangiogram of the normal right lower extremity. Sentinel lymph nodes of the lower leg (black arrows) and their efferent lymphatic vessels (white arrows) are shown.
Lymphatic anatomy of the inguinal region
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radiographic image of the lymphatic system.21 The lymphangiography images clearly demonstrated the sentinel lymph nodes of the lower leg and their efferent lymphatic vessels, which are the main tracts that must be preserved during VLNT (Figure 1). In the present anatomic study, we used our original microinjection technique akin to Kinmonth’s in a cadaver model to 1) investigate the relationship between the lymphatic system in the abdomen and that in the lower extremity, 2) track the course of the sentinel lymph nodes’ efferent lymphatic vessels in the lower extremity, and 3) elucidate the relationship between the lymphatic system and arteries in the inguinal region in order to secure blood supply to the vascularized lymph node flap.
Materials and methods Indocyanine green fluorescence lymphography study Five hind-quarter specimens from three fresh female cadavers of moderate size without scars were selected for the study. The cadavers were obtained from the Willed Body Program of the Department of Neurobiology and Anatomy at The University of Texas Medical School at Houston. Before two cadavers were separated into parts for frozen storage, 0.3 ml of indocyanine green (ICG) (IC-Green; Akorn, Inc., Lake Forest, IL, USA) was injected into the dermis at multiple locations in the toe webs, edge of the foot, and lateral thigh and in abdominal regions along a horizontal line at the umbilical level and along the sagittal midline. To facilitate the uptake and dispersal of ICG into the lymphatic system, we massaged the body by hand for 20 min beginning at the injection sites and continuing towards the inguinal regions. The body was then scanned using an ICG fluorescence lymphography system (Photodynamic Eye; Hamamatsu K.K., Hamamatsu, Japan), which detects the near-infrared radiation from the ICG compound to demonstrate anatomical structures up to 12 mm below the surface of the skin. Using the images displayed on a monitor as a guide, we used a marker to map the lymphatic pathways on the skin (Figure 2; see also Video, Supplemental Digital Content 1, which shows ICG lymphography of the cadaver lower limb). Supplementary data related to this article can be found online at http://dx.doi.org/10.1016/j.bjps.2014.10.047. After lymphatic mapping was complete, the body was eviscerated using a frontal midline incision from the sternal notch to the pubic symphysis. The hind-quarter specimen was separated using a horizontal incision at the umbilical level, and the spinal bone, pubic symphysis, and sacral bone were cut along the sagittal midline using an electric reciprocating saw. The specimens were kept in frozen storage until the second injection procedure was performed.
Dual injection technique To demonstrate the lymphatics and arteries simultaneously and to discriminate between them, we used a modified
Figure 2 Indocyanine green lymphangiography (left) and tracing of the lymphatic vessels (right).
version of a radiographic microinjection technique Suami et al. developed to visualize the lymphatic system in a cadaver model.22,23 First, we inserted a 16- or 18-French urinary catheter into the external iliac artery and injected approximately 300 ml of a radio-opaque mixture of 30% zinc oxide (Fisher Scientific, Pittsburgh, PA), 20% latex rubber (Carolina Biological Supply Company, Burlington, NC), and 50% water. The pink latex rubber solidified inside arterial lumen within half a day. Second, we cut the skin around the ankle joint using the ICG lymphographyebased lymphatic maps as a guide and identified the lymphatic vessels by inflating them with 3% hydrogen peroxide. We then injected a radio-opaque mixture of 30% barium sulfate (Fisher Scientific, Pittsburgh, PA), 70% 3% hydrogen peroxide, and a few drops of acrylic dye (Liquitex Artist Color Materials, Piscataway, NJ); Prussian blue, deep violet, and phthalocyanine green, into each lymphatic vessel. We also identified the lymphatic vessels in the lateral thigh and lower abdominal regions and injected them with the barium sulfate mixture. Because barium sulfate (injected into the lymphatics) and zinc oxide (injected into the arteries) have different radiocontrast intensities,24 we were able to distinguish between lymphatic vessels and arteries on radiographs. We chased each afferent lymphatic vessel injected with barium sulfate using meticulous dissection under microscopy (Discovery V8; Carl Zeiss, Inc., Thornwood, NY) until the vessel reached the first-tier (sentinel) lymph node. Because the barium sulfate mixture perfused no further than a regional lymph node, we injected 0.3e0.5 ml of 3% hydrogen peroxide into the subcapsular space of the lymph
422 node to inflate and identify the efferent lymphatic vessels. We repeated this lymphatic microinjection procedure to fill the efferent lymphatic vessels until the injected mixture reached the intrapelvic region beyond the inguinal ligament. Lymph nodes were delineated radiographically by tagging them with round brass tabs. Valvular structures inside the lumen of the lymphatic vessels that regulate lymphatic flow unidirectionally were assessed to determine the direction of lymphatic drainage. The lymphatic vessels’ course and their relationship to the inguinal lymph nodes were recorded using digital photography (PowerShot G12, Cannon USA, Inc., Melville, NY), and their flow directions were noted.
Radiological analysis After completing the dual injection procedures in the arteries and lymphatic vessels, we radiographed the hindquarter specimen using an FCR Go portable x-ray system (Fujifilm Medical Systems USA Inc., Stamford, CT) (Figure 3). Skin and soft tissue in the front thigh and intrapelvic regions were separated from the femoral and pelvic bones using mid-lateral and mid-medial incisions. The dissected specimen was spread on a plastic board and radiographed. Montages of the radiographic images were created on a desktop computer, and graphic software (Adobe Photoshop CS6, Adobe Systems Inc., San Jose, CA) was used to trace the arteries and lymphatic vessels and indicate their flow directions (Figures 4 and 6).
Figure 3 A radiograph of the right hind-quarter specimen after completion of the dual injection technique. Lymph nodes with brass tabs (white), lymphatic vessels (black), and the femoral artery (red) are shown in a radiograph.
M.F. Scaglioni, H. Suami
Results ICG fluorescence lymphography images of cadavers that had been injected with ICG and massaged showed clearly delineated shiny linear structures running axially and proximally in the lower leg. Subsequent dissection confirmed that these shiny linear structures were lymphcollecting vessels running through the subcutaneous fat. Uptake of ICG into the lymphatic vessels was highly selective, and ICG fluorescence lymphography demonstrated no other vascular structures. We could track the lymphatic vessels until just below the knee, but they were no longer visible above the knee. Although the ICG injected around the foot could delineate the lymphatic vessels in a manner similar to that of imaging studies in live humans, the ICG injected at the lateral thigh and lower abdominal regions remained at the injection site and did not demonstrate any structures. Mapping the lymphatic vessels reduced the time required to search for them and thus facilitated the process of injecting the radio-opaque mixture. The different radiocontrast intensities of the two radiopaque formulas (zinc oxide and barium sulfate) enabled us to discriminate between lymphatic vessels and arteries on radiographs (Figures 3 and 4). The lymphatics and arteries were also distinguished by their branching patterns; arteries have a dendritic and tapering pattern, whereas lymphatic have a linear and uniform pattern. Tagged metal tabs were used to delineate the locations of the inguinal lymph nodes on radiographs (Figures 3 and 4). Barium sulfate and zinc oxide are less toxic than lead oxide, which we previously used as contrast media for cadaver injection studies. Barium sulfate, which can be stained any color, helped to distinguish lymphatic vessels from surrounding yellow fat tissue (Figure 5). Our novel dual injection technique could also demonstrate arterial blood supply to the lymph nodes (Figure 5, bottom). Radiographs and photographs revealed that the lymphatic vessels originating from the lower leg converged in the medial thigh and ran towards the inguinal region. These lymphatic vessels formed a medial bundle running parallel with the great saphenous vein and were consistently found to connect to 2 or 3 sentinel lymph nodes located in the distal part of the inguinal triangle (lymph nodes A, B, and C in Figures 5 and 6). The two most distal lymph nodes (A and B) were considered to be the dominant lymph nodes draining the lower leg, and they were consistently located on both sides of the great saphenous vein (Figure 5). These sentinel nodes’ efferent lymphatic vessels did not connect to any lymph nodes within the inguinal triangle, ran straight into the pelvis, and always ran first along the medial side of the common femoral artery and then along the external iliac artery. The lymphatic vessels in the lateral thigh region were sparse. These vessels did not connect to the two dominant lymph nodes but did connect to the lymph nodes located at the lateral part of the inguinal triangle. The lymphatic vessels in the lower abdominal area were identified 5e10 cm below the boundary at which the specimen was excised from the cadaver. These vessels converged unidirectionally towards the first-tier lymph node located in the upper part in the inguinal triangle
Lymphatic anatomy of the inguinal region
423 (SCIA) (Figures 4 and 6, left) and were located close to the SCIA. However, in the absence of the SCIA in one specimen, these lymph nodes were supplied by the superficial inferior epigastric artery (SIEA) (Figures 5 and 6, right) and were located in its vicinity. The abdominal lymph nodes at the medial side (nodes G and H in Figure 6, left; node F in Figure 6, right) received their blood supply from anonymous branches from the common femoral artery. The superficial lymphatic vessel, which ran along the short saphenous vein in the calf region, connected to the popliteal lymph nodes in the popliteal fossa. The efferent lymphatic vessel of the popliteal nodes ran deep and along the deep femoral artery posteriorly. In the inguinal region, the vessel ran posterior to the common femoral artery and did not connect to either the superficial lymphatic vessels or lymph nodes (Figure 6, right). However, the vessel did connect to an intrapelvic lymph node above the inguinal ligament.
Discussion
Figure 4 A vascularized groin lymph node flap (lateral (*) and medial side (**)) dissected from a right hind-quarter specimen; a view of the undersurface of the flap (top), a radiograph of the flap (middle), and tracing of the radiograph (bottom) are shown. The artery (red) is the superficial circumflex iliac artery.
(node F in Figure 6, left; node E in Figure 6, right). The efferent lymphatic vessels of the first-tier node ran medially. Two to four lymph nodes situated superficial to the Scarpa’s fascia were aligned in parallel below the inguinal ligament. The efferent lymphatic vessels of the upper medial node ran deep, passed below the inguinal ligament, and approached the efferent lymphatic vessels of the dominant lymph node medially. The lymph nodes in the abdominal group received their blood supply from the superficial circumflex iliac artery
Anatomical atlases made by Mascagni (Figure 7)17 and Sappey18 both depict two lymph nodes located in the distal part of the inguinal triangle that connect to lymphatic vessels from the medial thigh. Kinmonth’s lymphangiography technique demonstrated two similar lymph nodes (Figure 1). These lymph nodes may be the dominant lymph nodes draining the lower leg that we identified in the present study. In previous studies, our group investigated the lymphatic system in the upper extremity in a cadaver model26,27 and consistently found one or two dominant lymph nodes at the lateral axillary region. We presume that the anatomic structure of the upper extremity is similar to that of the lower extremity and that, like the upper extremity, the lower extremity has two or three dominant nodes. Recognition of the sentinel lymph nodes of the lower leg potentially has clinical importance regarding the use of sentinel node biopsy for skin cancer in the lower leg and the avoidance of iatrogenic lymphedema following VLNT. Ours is the first study to use ICG imaging to map lymphatics in a fresh cadaver (Figure 2). These images were similar to the ICG lymphography images of lymphatic vessels in normal lower extremities.25 We knew from previous studies that an intradermal injection of the dye into the finger webs sometimes demonstrates the lymphatic vessels in frozen and thawed cadaver specimens, however, the injected dye traveled only several centimeters in the lymphatic lumen in the frozen specimens.26 In the present study, our use of fresh, non-frozen cadavers for the ICG imaging studies may explain why the ICG traveled the long distance from the foot to below the knee. Although the injected ICG could demonstrate the lymphatic vessels in the lower leg, it did not demonstrate them in the abdominal and lateral thigh regions, which were different from the ICG imaging in clinical settings. Although we are unable to account for the difference in ICG activity between the foot and the abdominal and lateral thigh regions we speculate that the lymphatic system in the terminal area of the body may have an anatomic structure that enables it to capture foreign material more effectively.
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Figure 5 Photographs of the right inguinal area after dissection (right side is distal). Lymphatic vessels in the medial thigh (blue) and in the abdomen (green); lymph nodes (A to F); the superficial inferior epigastric artery (SEA); and the great saphenous vein (SV) are shown. Arrows indicate the arterial supply to the lymph nodes.
M.F. Scaglioni, H. Suami On the basis of findings from cadaver studies,26,28 animal experiments,29,30 historical reviews,24,25,31 and clinical diagnostic imaging studies,32e34 the senior author proposed the concept of “lymphosomes” to describe territories of the superficial lymphatic system and their corresponding lymph nodes. In the present study, the superficial lymph nodes in the inguinal region could be divided into three subgroups based on the connecting lymphatic vessels: the abdominal group, the lateral thigh group, and the medial thigh group (Figure 8). Each group of lymph nodes was color-coded, and their corresponding lymphatic vessels were also colorcoded retrogradely from the node, thereby delineating them as lymphosomes. Although the lymphatic system has minor differences among individuals and between sides of the body, we could successfully approximate a general pattern of the superficial lymphatic drainage. We expect that the lymphosome concept will increase our understanding of the lymphatic system and enable us to define suitable lymph node donor sites for VLNT. According to our findings, the abdominal lymph node group could be targeted for VLNT, whereas the medial thigh lymph node group must be preserved (Figure 9).
Figure 6 Mapping arteries and lymphatic vessels demonstrated on radiographs in two specimens. Purple indicates efferent lymphatic vessels of the leg sentinel nodes (AeC); blue, deep lymphatic vessels; green, superficial lymphatic vessels; and red, arteries. The “*” indicates the superficial circumflex iliac artery; “**” indicates the superficial inferior epigastric artery. The black arrowheads indicate directions of lymph flow.
Lymphatic anatomy of the inguinal region
Figure 7 Mascagni’s diagram depicts the leg sentinel nodes (arrows). (From Mascagni P. Vasorum Lymphaticorum Corporis Humani Historia et Ichnographia. Siena: Pazzini Carli; 1787.)
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Figure 9 Schematic diagram of lymphatic drainage in the inguinal region. Lymph drains from the leg via the sentinel nodes (yellow) and their efferent lymphatic vessels (purple), and surgeons should avoid disturbing these nodes and vessels during VLNT. Lymph drains from the abdominal (orange), lateral thigh (green), and deep lymphatics (blue) are shown.
Our cadaver dissection results showed that the inguinal lymph nodes, which were responsible for abdominal lymphatic drainage, are located along the lower edge of the inguinal ligament and supplied by the SCIA or SIEA and anonymous branches from the common femoral artery. Several groups have reported various surgical approaches to harvesting a lymph node flap for VLNT from the inguinal region.6,7,9e11,14,19 Our findings concur with those of previous reports describing how to harvest a VLNT flap without impairing the lymph drainage pathways in the lower extremity. However, there is little information about the importance of preserving the leg sentinel lymph nodes and their efferent lymphatic vessels. Other authors have described using reverse lymphatic mapping techniques in the upper extremity, in which dye is injected into the medial upper arm to stain the arm sentinel lymph nodes.34,35 We suggest applying the same reverse mapping technique to preserve leg lymphatic drainage following VLNT. The better understanding of the lymphatic system anatomy that such a technique would provide would hopefully contribute to safer VLNTs in patients with BCRL.
Conclusion Figure 8 Lymphosomes in the inguinal region: the abdominal (orange), lateral thigh (green), and medial thigh (yellow) groups are shown.
We developed a dual injection technique that uses two different contrast media (barium sulfate and zinc oxide) to
426 radiographically demonstrate the arteries, lymphatic vessels, and lymph nodes simultaneously in a cadaver model. The superficial inguinal lymph nodes can be divided into three subgroups: the abdominal, medial thigh, and lateral thigh groups. The abdominal group can be targeted for VLNT. The sentinel nodes in the medial thigh group are the dominant nodes draining the lower leg. Our anatomic study suggests that these nodes and their efferent lymphatic vessels must be preserved to retain lymphatic drainage of the lower extremity following VLNT.
Financial disclosure The authors have no sources of financial or other support and no financial or professional relationships that may pose a competing interest.
Ethical approval N/A.
Acknowledgments This study was supported in part by the Kyte Research and Education Fund, and by the Sister Institutional Network Fund 35640 at MD Anderson. The authors thank Rony Avristcher, M.D., Department of Interventional Radiology, The University of Texas MD Anderson Cancer Center for providing his advices.
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