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Original Article |

Lymphatic Drainage to the Popliteal Basin in Distal Lower Extremity Malignant Melanoma FREE

Tehillah S. Menes, MD; Jacob Schachter, MD; Adam P. Steinmetz, MD; Ruth Hardoff, MD, DSc; Haim Gutman, MD
[+] Author Affiliations

From the Departments of Surgery B (Drs Menes and Gutman) and Nuclear Medicine (Drs Steinmetz and Hardoff) and Institute of Oncology (Dr Schachter), Rabin Medical Center, Beilinson Campus, Petah Tiqva, and Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel.


Arch Surg. 2004;139(9):1002-1006. doi:10.1001/archsurg.139.9.1002.
Text Size: A A A
Published online

Hypotheses  Melanoma of the distal lower extremity may drain to the popliteal basin. Drainage pathways and retrieval of the popliteal sentinel nodes may affect patient outcome.

Design  Retrospective analysis of popliteal involvement in patients with stage IB or higher melanoma, operated on from August 1, 1993, to July 31, 2003.

Setting  Tertiary referral, university-affiliated medical center.

Patients  One hundred six melanoma patients who underwent combined lymphoscintigraphy and blue dye–guided sentinel node biopsy, radical popliteal dissection, or both.

Main Outcome Measures  Incidence and patterns of drainage to popliteal nodes; effect on staging and outcome.

Results  Lymphoscintigraphy (n = 8) and physical examination (n = 2) identified 10 cases (9%) of draining to the popliteal basin, with concurrent drainage to the groin. Three distinct drainage patterns were identified, with different popliteal node locations. Seven of 8 popliteal sentinel nodes were retrieved, 1 of which was metastatic with no groin metastasis. Two patients had synchronous palpable popliteal and groin metastases and underwent radical groin and popliteal dissection. All 3 patients with popliteal metastases relapsed early with synchronous systemic and in-transit disease. One of 7 patients with negative sentinel nodes is alive with in-transit disease; all others are disease free.

Conclusions  According to this series, the popliteal basin is the site of first drainage in about 9% of patients, with concurrent drainage to the groin. The 3 distinct patterns of drainage to the popliteal region and the presence of isolated popliteal metastases may affect the surgical treatment. Therefore, drainage to popliteal sentinel nodes and the pattern of this drainage should be noted in all distal lower extremity melanomas.

Figures in this Article

Metastatic disease of the regional lymph nodes is the most important predictor of outcome in malignant melanoma.1 The use of lymphoscintigraphy, intraoperative lymphatic mapping, and sentinel node biopsy for the detection of micrometastases in the regional lymph nodes has made it possible to delineate lymphatic pathways in individual patients. Lymphoscintigraphy can also detect aberrantly located and in-transit sentinel nodes, even in the extremities, where drainage of lesions is considered to be more predictable than in the head and neck and trunk.2 This is important because the rate of metastasis to in-transit nodes is similar to that to conventional locations.1

We reviewed our experience with drainage to the popliteal nodes in patients with malignant melanomas of the distal extremities, with a focus on the lymphatic pathways, rate of drainage, metastasis to the popliteal basin, and clinical course. We sought to identify the most prevalent pattern of drainage to the popliteal region from melanoma sites on the distal lower extremity.

Of the 476 patients with stage IB or higher melanoma who underwent surgery in our unit between August 1, 1993, and July 31, 2003, performed or supervised by a single surgical oncologist (H.G.), 149 had a primary lesion in the lower extremity. The 106 patients with a lesion at the knee or distally constituted the study group for the present analysis. All data were entered prospectively into our departmental database.

Since 1994, all patients with melanoma and negative findings on systemic workup who fall into 1 of the 4 categories established by the Melanoma and Soft Tissue Tumor Board of Rabin Medical Center3 have been offered sentinel node biopsy with preoperative lymphoscintigraphy. Briefly, 2 to 3 mCi of technetium 99m–labeled nanocolloid (Nanocoll; Nycomed Amersham Sorin Srl, Milan, Italy) was injected intradermally in 4 to 6 sites around the biopsy scar or the primary lesion (0.1 mL per injection). An SP-6 rectangular gamma camera equipped with a high-resolution collimator (Elscint Ltd, Haifa, Israel) was used to obtain dynamic and static images with the patient in the supine position and upright with 90° flexed knee (lateral view). The projected location of the sentinel node was marked on the skin. All patients also underwent intraoperative lymphatic mapping with patent blue V dye (Laboratoire Guerbet, Aulnay-Sous-Bois, France). A handheld gamma probe (Neoprobe 1000 or 2000; Neoprobe Corporation, Dublin, Ohio) was used beginning in 1999. Sentinel nodes were serially sectioned, stained with standard hematoxylin-eosin, and, if negative, stained with S100 and HMB-45. The popliteal fossa was explored and radically dissected, as applicable, with the patient in the face-down position. A transverse skin incision through the natural popliteal skin crease was used, without skin flaps, for popliteal node retrieval. The common peroneal and tibial nerves were identified and isolated, and the popliteal vessels were located. There were no surgical complications from the popliteal procedure in this series, except for one failure to find the sentinel node. Patients found to have an involved sentinel node or a clinically apparent metastatic lymph node, without evidence of systemic disease, underwent radical dissection of the lymph node basin. Radical popliteal lymph node dissection was performed as described by Karakousis and Wabnitz.4

The patients ranged in age from 27 to 84 years (median age, 55 years); 68 (64%) were female. At presentation, the lesion was located on the leg in 61 patients, the ankle or Achilles region in 4, and the foot in 41 (including 16 on the toes and 6 on the heel). The mean ± SD melanoma thickness was 2.9 ± 2.3 mm (median, 2.3 mm; range, 0-13 mm). On histologic study, the lesion was identified as acral lentiginous in 24 patients (23%), nodular in 24 (23%), unclassified in 23 (22%), superficial spreading in 20 (19%), lentigo maligna in 2 (2%), and desmoplastic in 2 (2%); the histologic type was not specified in 11 patients (10%). Ulceration was noted in 32 patients (30%).

Ten patients (9%) had drainage to the popliteal nodes (Table 1); metastases were palpable in 2 at presentation. The primary lesions in this subgroup were located on the calf (n = 3), Achilles tendon (n = 1), heel (n = 3), lateral aspect of the dorsum of the foot (n = 2), and base of the fifth toenail (n = 1) (Figure 1). All had concomitant drainage to the groin, evident clinically or by lymphoscintigraphy. The lymphoscintigraphic images in the 8 patients without palpable nodes identified at least 3 distinct patterns of lymphatic drainage to the popliteal basin (Figure 2). In pattern 1, the popliteal nodes were in-transit or interval nodes, located subcutaneously. In patterns 2 and 3, the popliteal nodes were first-order sentinel nodes, located subfascially, close to the popliteal vessels. The groin nodes were first- or second-order sentinel nodes. The drainage pattern could be definitely categorized in 5 of the 8 lymphoscintigraphies as pattern 1 (n = 2), pattern 2 (n = 2), and pattern 3 (n = 1); in 1 additional case, there was a modified pattern 3 with a crossover at the ankle level.

Table Graphic Jump LocationTable 1. Characteristics of Patients With Malignant Melanoma of the Distal Lower Extremity Draining to Popliteal Nodes
Place holder to copy figure label and caption
Figure 1.

Location of primary lesions draining to the popliteal basin in the present series.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Patterns of drainage to the popliteal basin by retrospective review of lymphoscintigraphic images. MM indicates primary melanoma; P, popliteal sentinel node; and G, groin sentinel node.

Graphic Jump Location

In 7 of the 8 patients, the popliteal sentinel node was identified intraoperatively; the remaining patient had had preoperative uptake in the popliteal region, but the sentinel node was not detected. Metastasis was detected in 1 patient (2 positive sentinel nodes) by immunohistochemical analysis; this patient's groin sentinel node was metastasis free. Two patients had synchronous palpable popliteal and groin metastases and underwent radical groin and popliteal dissection.

All 3 patients with popliteal involvement relapsed a short time after surgery with systemic and in-transit metastases; all 3 subsequently died. Of the remaining 7 patients, the 5 without popliteal involvement and the patient with an unidentified sentinel node were disease free 12 months after surgery, and 1 patient is alive with in-transit disease.

Although lymphatic drainage varies for all anatomic locations, it seems to be more predictable in the lower extremity.2 Traditionally, 2 main drainage routes were recognized for the distal lower extremity: the major route, which originates at the medial aspect of the foot and runs parallel to the course of the greater saphenous vein, draining into the inguinal nodes, and the minor route, which originates at the lateral aspect of the foot and follows the small saphenous vein, draining into the popliteal nodes.5 However, the introduction of lymphoscintigraphy for sentinel node procedures has brought the conventional anatomic pathways into question, while revealing new ones.6 As shown in Figure 3, there are superficial (subcutaneous) and deeper (subfascial) lymphatic channels reaching the popliteal fossa. Patterns 2 and 3 (Figure 2) involve the deeper route, and the sentinel nodes would be expected to be located close to the popliteal vessels, whereas in pattern 1, the sentinel node should be located subcutaneously, superficial to the fascia in the popliteal region. Therefore, if pattern 1 is demonstrated preoperatively, there is no need to open the deep fascia or search at the level of the popliteal vessels. To our knowledge, this differentiation has not been reported before.

Place holder to copy figure label and caption
Figure 3.

Pathways of drainage to the popliteal basin (original artwork based on Kiss and Szentagothai7).

Graphic Jump Location

In the present study, the fifth toe, the lateral aspect of the sole, the heel, the Achilles tendon area, and the calf were shown to drain to the popliteal fossa, which fits well with the classic anatomic descriptions. Our review of the literature indicated that lesions on the anterior part of the leg and on the dorsum of the foot may drain into the popliteal nodes as well (Table 2).8,9 This is perhaps due to distal interconnections between the 2 main lymphatic routes, as noted in one of our lymphoscintigraphies (modified pattern 3, results not shown).

Table Graphic Jump LocationTable 2. Literature Review of Drainage to Popliteal Nodes From Primary Melanoma of the Distal Lower Extremity

Drainage to the popliteal basin was present in a significant percentage (>9%) of our patients with malignant melanoma of the distal lower extremity. Most of them were identified during the last 2 years of this study, so the actual rate of popliteal basin drainage may have been higher. The reported prevalence ranges from 1% to 20%1,2,1015 with lymphoscintigraphy alone or combined with blue dye and a handheld gamma probe. This wide range can hardly be explained by demographic differences. We suspect that the rate of detection of drainage to the popliteal nodes may depend on the awareness, persistence, and technique with which it is sought. Uren et al16 found that, after changing their imaging protocol, the rate of drainage to the popliteal nodes increased from 2.3% to 16%. It is our practice to perform lymphoscintigraphy on all patients with melanoma, with attention to the lymphatic channels and to the interval basins. Based on the present series and the findings of others,16 a search for the popliteal sentinel nodes is mandatory, and lymphoscintigraphy should be applied routinely in all primary locations, with a 10-minute acquisition over every node field that can drain the site. These locations should also be investigated intraoperatively with a handheld gamma probe.16 In addition to the standard anteroposterior and oblique views, lateral views of the popliteal region (with the patient standing up and the knee joint flexed) may be helpful. Placing the patient facedown during surgery, even for sentinel node biopsy alone, yielded the best exposure of the whole basin. The medial approach to popliteal exploration with the patient lying supine, commonly practiced by vascular surgeons, requires extensive dissection. This is probably unnecessary for lymph node sampling, may cause difficulty in identification of the nerves, and may disrupt the thin lymphatic channels leading to the nodes. Insufficient attention to detail, the relative unfamiliarity of many surgeons with the popliteal fossa and patterns of drainage to it, the low rate of popliteal involvement, and the tendency to simplify intraoperative positioning of the patient and shorten the surgical procedure may lead to underdetection of popliteal sentinel nodes.

We believe that our series reveals new observations. Whenever there is lymphatic drainage to the popliteal fossa, it is accompanied by drainage to the groin. However, the popliteal nodes may be metastatic in the absence of a detectable groin metastasis. There are at least 3 distinct patterns of drainage to the popliteal fossa, and the individual pattern may have an effect on the anatomic location of the nodes and on the presence of first- or second-order sentinel node involvement. We urge clinicians and investigators to pay attention to these features in cases of distal lower limb melanoma.

It has been shown that the rate of metastases in sentinel nodes in unconventional locations is similar to that in conventional locations, demonstrating the importance of examining the in-transit sentinel nodes.1,8 This claim is supported by the present study, in which we identified a 30% (3/10) rate of metastatically involved popliteal nodes. The popliteal area should, therefore, always be examined when the primary lesion involves the distal lower extremity.

In conclusion, examination of the popliteal sentinel nodes for metastases is an important part of the staging and treatment of malignant melanoma of the distal lower extremity. Drainage to these nodes is not rare and should be sought. The individual pattern of drainage should be noted, as it may affect the surgical procedure. When radioactivity is found in the popliteal basin, these nodes should be retrieved, and if metastatic disease is found, radical popliteal dissection is the standard of care.

Correspondence: Haim Gutman, MD, Department of Surgery B, Rabin Medical Center, Beilinson Campus, Petah Tiqva 49100, Israel (hgutman@post.tau.ac.il).

Accepted for publication December 9, 2003.

We thank Gloria Ginzach and Hanni Penn for their editorial and secretarial assistance. We also thank Aharon Shimoni for his cooperation and nuclear medicine technical expertise.

McMasters  KMChao  CWong  SL  et al.  Interval sentinel nodes in melanoma. Arch Surg. 2002;137543- 549
PubMed Link to Article
Statius Muller  MGHennipman  FAvan Leeuwen  PAMPijpers  RVuylsteke  RJCLMMeijer  S Unpredictability of lymphatic drainage patterns in melanoma patients. Eur J Nucl Med. 2002;29255- 261
Link to Article
Schachter  JLaish  AMekhmandarov  S  et al.  Standard and nonstandard applications of sentinel node–guided melanoma surgery. World J Surg. 2000;24491- 495
PubMed Link to Article
Karakousis  CPWabnitz  RC Popliteal lymph-node dissection. Atlas of Operations for Soft Tissue Tumors. New York, NY McGraw-Hill Book Co1998;459- 466
Uhara  HSaida  TWatanabe  TTakizawa  Y Lymphangitis of the foot demonstrating lymphatic drainage pathways from the sole. J Am Acad Dermatol. 2002;47502- 504
PubMed Link to Article
Thompson  JFUren  RFShaw  HM  et al.  Location of sentinel nodes in patients with cutaneous melanoma: new insights into lymphatic anatomy. J Am Coll Surg. 1999;189195- 206
PubMed Link to Article
Kiss  FSzentagothai  I Systema nervosum, angiologia, organa sensum. Atlas Anatomiae Corporis Humani. Budapest, Hungary Octogesima Prima, Medicina Konyvkiado1984;200- 202
Roozendaal  GKde Vries  JDHvan Poll  D  et al.  Sentinel nodes outside lymph node basins in patients with melanoma. Br J Surg. 2001;88305- 308
PubMed Link to Article
Thompson  JFHunt  JACuljak  GUren  RFHowman-Giles  RHarman  CR Popliteal lymph node metastasis from primary cutaneous melanoma. Eur J Surg Oncol. 2000;26172- 176
PubMed Link to Article
Lieber  KAStandiford  SBKuvshinoff  BWOta  DM Surgical management of aberrant sentinel lymph node drainage in cutaneous melanoma. Surgery. 1998;124757- 762
PubMed Link to Article
Uren  RFHowman-Giles  RThompson  JF Patterns of lymphatic drainage from the skin in patients with melanoma. J Nucl Med. 2003;44570- 582
PubMed
Leong  SPLAchtem  TAHabib  FA  et al.  Discordancy between clinical predictions vs lymphoscintigraphic and intraoperative mapping of sentinel lymph node drainage of primary melanoma. Arch Dermatol. 1999;1351472- 1476
PubMed Link to Article
Morris  KTStevens  JSPommier  RFFletcher  WSVetto  JT Usefulness of preoperative lymphoscintigraphy for the identification of sentinel lymph nodes in melanoma. Am J Surg. 2001;181423- 426
PubMed Link to Article
Sumner III  WERoss  MIMansfield  PF  et al.  Implications of lymphatic drainage to unusual sentinel lymph node sites in patients with primary cutaneous melanoma. Cancer. 2002;95354- 360
PubMed Link to Article
Georgeu  GAEl-Muttardi  NMercer  DM Malignant melanoma metastasis to the sentinel node in the popliteal fossa. Br J Plast Surg. 2002;55443- 445
PubMed Link to Article
Uren  RFHowman-Giles  RBThompson  JF Failure to detect drainage to the popliteal and epitrochlear lymph nodes on cutaneous lymphoscintigraphy in melanoma patients [letter]. J Nucl Med. 1998;392195
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

Location of primary lesions draining to the popliteal basin in the present series.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Patterns of drainage to the popliteal basin by retrospective review of lymphoscintigraphic images. MM indicates primary melanoma; P, popliteal sentinel node; and G, groin sentinel node.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Pathways of drainage to the popliteal basin (original artwork based on Kiss and Szentagothai7).

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Characteristics of Patients With Malignant Melanoma of the Distal Lower Extremity Draining to Popliteal Nodes
Table Graphic Jump LocationTable 2. Literature Review of Drainage to Popliteal Nodes From Primary Melanoma of the Distal Lower Extremity

References

McMasters  KMChao  CWong  SL  et al.  Interval sentinel nodes in melanoma. Arch Surg. 2002;137543- 549
PubMed Link to Article
Statius Muller  MGHennipman  FAvan Leeuwen  PAMPijpers  RVuylsteke  RJCLMMeijer  S Unpredictability of lymphatic drainage patterns in melanoma patients. Eur J Nucl Med. 2002;29255- 261
Link to Article
Schachter  JLaish  AMekhmandarov  S  et al.  Standard and nonstandard applications of sentinel node–guided melanoma surgery. World J Surg. 2000;24491- 495
PubMed Link to Article
Karakousis  CPWabnitz  RC Popliteal lymph-node dissection. Atlas of Operations for Soft Tissue Tumors. New York, NY McGraw-Hill Book Co1998;459- 466
Uhara  HSaida  TWatanabe  TTakizawa  Y Lymphangitis of the foot demonstrating lymphatic drainage pathways from the sole. J Am Acad Dermatol. 2002;47502- 504
PubMed Link to Article
Thompson  JFUren  RFShaw  HM  et al.  Location of sentinel nodes in patients with cutaneous melanoma: new insights into lymphatic anatomy. J Am Coll Surg. 1999;189195- 206
PubMed Link to Article
Kiss  FSzentagothai  I Systema nervosum, angiologia, organa sensum. Atlas Anatomiae Corporis Humani. Budapest, Hungary Octogesima Prima, Medicina Konyvkiado1984;200- 202
Roozendaal  GKde Vries  JDHvan Poll  D  et al.  Sentinel nodes outside lymph node basins in patients with melanoma. Br J Surg. 2001;88305- 308
PubMed Link to Article
Thompson  JFHunt  JACuljak  GUren  RFHowman-Giles  RHarman  CR Popliteal lymph node metastasis from primary cutaneous melanoma. Eur J Surg Oncol. 2000;26172- 176
PubMed Link to Article
Lieber  KAStandiford  SBKuvshinoff  BWOta  DM Surgical management of aberrant sentinel lymph node drainage in cutaneous melanoma. Surgery. 1998;124757- 762
PubMed Link to Article
Uren  RFHowman-Giles  RThompson  JF Patterns of lymphatic drainage from the skin in patients with melanoma. J Nucl Med. 2003;44570- 582
PubMed
Leong  SPLAchtem  TAHabib  FA  et al.  Discordancy between clinical predictions vs lymphoscintigraphic and intraoperative mapping of sentinel lymph node drainage of primary melanoma. Arch Dermatol. 1999;1351472- 1476
PubMed Link to Article
Morris  KTStevens  JSPommier  RFFletcher  WSVetto  JT Usefulness of preoperative lymphoscintigraphy for the identification of sentinel lymph nodes in melanoma. Am J Surg. 2001;181423- 426
PubMed Link to Article
Sumner III  WERoss  MIMansfield  PF  et al.  Implications of lymphatic drainage to unusual sentinel lymph node sites in patients with primary cutaneous melanoma. Cancer. 2002;95354- 360
PubMed Link to Article
Georgeu  GAEl-Muttardi  NMercer  DM Malignant melanoma metastasis to the sentinel node in the popliteal fossa. Br J Plast Surg. 2002;55443- 445
PubMed Link to Article
Uren  RFHowman-Giles  RBThompson  JF Failure to detect drainage to the popliteal and epitrochlear lymph nodes on cutaneous lymphoscintigraphy in melanoma patients [letter]. J Nucl Med. 1998;392195
PubMed

Correspondence

CME


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