RECONSTRUCTIVE

Selective Sentinel Lymph Node Dissection in

Lower Extremity Melanoma
Suzette G. Miranda, M.D.
Brian M. Parrett, M.D.
Rui (Rachel) Li, Ph.D.
Grant Lee, M.D.
Tiffany Chang, M.D.
Niloofar Fadaki, M.D.
Servando Cardona-Huerta,
M.D., Ph.D.
James E. Cleaver, Ph.D.
Mohammed Kashani-Sabet,
M.D.
Stanley P. Leong, M.D.
San Francisco, Calif.
Background: There is debate as to whether deep inguinal lymph nodes should
be removed with the superficial or femoral lymph nodes during sentinel lymph
node biopsy for lower extremity melanoma, when both superficial and deep
inguinal lymph nodes are identified by preoperative lymphoscintigraphy. This
study evaluated the lymphatic drainage patterns in lower extremity melanoma
to determine whether certain patterns could be used to limit the level of node
removal and define the extent of dissection.
Methods: A retrospective outcomes review was performed of lower extrem-
ity melanoma patients with excision and sentinel lymph node biopsy from
1995 to 2010. Outcomes included location of sentinel lymph node drainage
basins, sentinel lymph nodepositivity, and disease-free and overall survival,
with drainage patterns compared between above- and below-knee melanomas.
Results: Of 499 patients with lower extremity melanoma having sentinel lymph
node biopsy, 356 had below-the-knee and 143 had above-the-knee melanoma.
For below-knee melanoma, the node-positivity rate was 23 percent for superfi-
cial inguinal, 0 percent for deep inguinal, and 50 percent for popliteal basins.
For above-knee melanoma, the positivity rate was 21 percent for superficial
inguinal, 33 percent for deep inguinal basins, and 0 percent for popliteal
basins. Importantly, no patients with a negative superficial inguinal sentinel
lymph node had a positive deep inguinal sentinel lymph node on final patho-
logic evaluation.
Conclusions: A difference was noted in patterns of sentinel lymph node
drainage from lower extremity melanoma below and above the knee. Biopsy
for deep inguinal basins may be deferred if there is simultaneous drainage
to the superficial inguinal basin by preoperative lymphoscintigraphy. (Plast.
Reconstr. Surg. 137: 1031, 2016.)
CLINICAL QUESTION/LEVEL OF EVIDENCE: Risk, II.

M
orton et al. published the results of the
first major prospective trial that advocated
the role of selective sentinel lymph node
biopsy in cutaneous melanoma in 1992.1 This
method of staging primary melanoma has become
the standard of care.14 Identification of sentinel
lymph nodes using isosulfan blue dye (Lympha-
zurin; Hirsch Industries, Inc., Richmond, Va.) has
From The Buncke Clinic, California Pacific Medical Center;
the Departments of Surgery and Dermatology, University of
California, San Francisco; Medivation Biostatistics; and
the Center for Melanoma Research & Treatment, California
Pacific Medical Center & Research Institute.
Received for publication May 6, 2015; accepted November
2, 2015.
Presented at the 93rd Annual Meeting of the American As-
sociation of Plastic Surgeons, in Miami, Florida, April 5
through 8, 2014.
Copyright 2016 by the American Society of Plastic Surgeons
DOI: 10.1097/01.prs.0000479990.65243.eb
evolved to include intraoperative gamma probe
guided detection, with an increased identification
rate of sentinel lymph nodes to 96 to 99 percent.57
Over the past decade, there has been debate
as to which nodes (superficial versus deep ingui-
nal) are sentinel lymph nodes and which sentinel
lymph nodes should be removed during sentinel
lymph node biopsy for lower extremity mela-
noma. Under the lymphatic spread theory, there
is an orderly progression of cancer cells to first-
echelon nodes.8,9 Therefore, it would appear rea-
sonable to remove only the first-echelon nodes,
as they are the true sentinel lymph nodes. It is
known that most nodes on a direct lymphatic
drainage pathway are located in the superficial
groin from the lower extremity. In addition to
Disclosure: The authors have no financial interest
to declare in relation to the content of this article.

www.PRSJournal.com 1031
Copyright 2016 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.

the superficial inguinal nodal basin, the deep
inguinal basin (which includes pelvic iliac and
obturator nodes) and popliteal nodal basins have
also been removed during sentinel lymph node
biopsy.1015 Whereas evidence exists that suggests
removing more than two sentinel lymph nodes
does not provide additional information during
sentinel lymph node biopsy,10 others have argued
for removing all blue nodes or nodes with radio-
activity greater than 10 percent of background to
reduce the false-negative rate.11,12
The Multicenter Selective Lymphadenectomy
Trial-I validated the prognostic significance of
sentinel lymph node biopsy, with a 5-year mela-
noma survival rate of 72 percent for sentinel
lymph nodepositive patients compared with
90 percent survival for sentinel lymph nodenega-
tive patients.13 However, what has not been clearly
defined is the need for excising the deep ingui-
nal sentinel lymph nodes in addition to removing
superficial sentinel lymph nodes when preopera-
tive lymphoscintigraphy shows increased radioac-
tivity of lymph nodes in both basins.
Our study was aimed at evaluating lymphatic
drainage patterns in lower extremity melanoma to
determine whether identification of certain drain-
age patterns could be used to limit the removal
of deep inguinal sentinel lymph nodes removed
to adequately stage patients with lower extremity
melanoma. The aim was to identify the positivity
of sentinel lymph nodes and whether there was
any clinical advantage to deep inguinal sentinel
lymph node biopsy versus superficial inguinal sen-
tinel lymph node biopsy alone. Furthermore, the
goal was to use these data to help refine the extent
of completion node dissection in sentinel lymph
nodepositive patients.
PATIENTS AND METHODS
Institutional review board approval was
obtained, and the tumor registry at University
of California, San Francisco and the California
Pacific Medical Center was queried to identify
all patients with lower extremity melanoma who
underwent sentinel lymph node biopsy from 1995
to 2010. Patients who underwent sentinel lymph
node biopsy had a lower extremity melanoma that
was confirmed on biopsy to be greater than or
equal to 1mm or had a thinner melanoma with
adverse features consistent with indications for
sentinel lymph node biopsy.14 The lymphoscinti-
graphic images and report, operative note, and
pathology report were scrutinized and required
from each patient to be included in this study. Any
1032
Copyright 2016 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
Plastic and Reconstructive Surgery March 2016
patient with a missing report was excluded from
the study (14 patients in our study).
The sentinel lymph node biopsy protocol
called for either a single day for both lymphos-
cintigraphy and the operation or lymphoscintig-
raphy during the afternoon before the operation.
Patients received an intradermal injection of fil-
tered technetium-99m sulfur colloid around the
tumor or the biopsy site. Static and dynamic images
were taken with a gamma camera system. Sentinel
lymph nodes were defined as the first lymph node
in lymph node bed to receive lymphatic drain-
age from the tumor. These were identified and
marked by the nuclear medicine physician. From
the nuclear medicine report, the injection dosage,
number of basins involved, number of channels,
and nodal counts for each basin were recorded.
The surgeon and nuclear medicine physician
reviewed the lymphoscintigram before incision.
For those patients who received blue dye, isosul-
fan blue was injected intradermally before the
procedure around the primary melanoma site. An
incision was made over the area of greatest activity
as detected by the handheld gamma probe (Neo-
probe 2000; Neoprobe Corp., Dublin, Ohio). The
incision was carried down through the subcuta-
neous fat, and the superficial fascia was incised.
Using the handheld gamma probe, any sentinel
lymph nodes that were assessed greater than or
equal to 10 percent of the radioactive count of
the hottest sentinel lymph node were removed
by one of three senior surgical oncologists. The
gamma probe was used to search the resection
bed to make sure that there was no residual ele-
vated radioactivity. Further exploration was car-
ried out if the resection bed count remained high.
With some cases, the blue dyestained lymphatics
would be seen and this would confirm the finding
of the radioisotope activity with resultant removal
of the sentinel lymph node. In general, the sen-
tinel lymph node was identified using a gamma
probe, blue dye, or both. No frozen sections were
taken intraoperatively. Nodes were examined by
permanent sections for hematoxylin and eosin
evaluation and immunohistochemical staining
for melanoma-specific markers. Any indurated or
enlarged lymph nodes by deep palpation would
also be removed. The primary melanoma site was
excised after the sentinel lymph node procedure.14
If the popliteal sentinel lymph node was
found, usually above the popliteal crease, a lon-
gitudinal incision of approximately 3 cm would
be made over the marking with the hot spot. The
superficial fascia would be incised and the sentinel
lymph node would be localized with a Neoprobe
 Volume 137, Number 3 Sentinel Lymph Node Dissection

and removed from the adjacent fatty tissue. Occa-
sionally, the sentinel node would be found deeper
adjacent to the neurovasculature and it would be
dissected carefully from the nerve and the vessels.
Outcomes assessed were (1) whether sentinel
lymph nodes drained into the deep, superficial,
or popliteal basins (or a combination of any)
and (2) the sentinel lymph node status of lower
extremity melanoma above and below the knee.
The percentage of drainage into each location,
the rate of sentinel lymph node positivity, and
5-year disease-free and overall survival were deter-
mined. Survival was compared between sentinel
lymph nodepositive and sentinel lymph node
negative patients with above- and below-knee pri-
mary melanomas.
Disease-free survival was calculated from time
of sentinel lymph node biopsy to the first recur-
rence of the patients primary melanoma (local,
regional, and distant) or death as a result of mela-
noma. Overall survival was calculated as the inter-
val between sentinel lymph node biopsy and death
from any cause. Survival curves between groups
were generated using the Kaplan-Meier nonpara-
metric method and compared by log-rank test.
Fishers exact test was performed to determine
whether the proportion of a categorical factor in
binary/ordinal scale (e.g., sentinel lymph node
positivity) differed significantly between lower
extremity melanoma above and below the knee.
Values of p < 0.05 were considered significant. Sta-
tistical analyses were performed with STATA Ver-
sion 10 (StataCorp, College Station, Texas).
RESULTS
From 1995 to 2010, 499 patients underwent
sentinel lymph node biopsy for lower extrem-
ity melanoma. One hundred forty-three patients
had melanoma above the knee and 356 had
melanoma below the knee. Table 1 shows the
different characteristics of melanoma below and
above the knee. The average age of patients was
49 years for those with melanoma above the knee
and 56 years for those with melanoma below the
knee (p < 0.001). Patients with melanoma above
the knee had significantly thicker primary mela-
nomas compared with patients with below-knee
melanoma (2.47mm versus 1.95mm; p = 0.018).
Table2 demonstrates the patients with lower
extremity melanoma below and above the knee
and further categorizes each location to illustrate
whether sentinel lymph nodes drained into only
superficial inguinal, deep inguinal, or popliteal

Table 1. Characteristics of Melanoma above and below the Knee

Frequency of Melanoma
Characteristics Above-Knee (%) Below-Knee (%) p
No. of patients 143 356
Mean age at SLN dissection SD, yr 49 15.4 56 16.9 <0.001
Sex 0.756
Female 95 230
Male 48 126
Histology <0.001
SSM 25 57
NM 16 20
ALM 0 98
MM-NOC 52 75
Desmoplastic 1 6
Unknown 49 100
Breslow thickness SD, mm 1.95 0.109 2.47 0.135 0.018
Ulceration 0.075
Yes 36 105
No 71 182
Clark level 0.338
I, II, and III 37 83
IV and V 84 231
Mean mitosis rate SD, mm2 4.66 3.371 4.23 4.953 0.564
Regression status
Yes 9 20
No. of SLNs removed 0.370
<3 68 152
3 75 203
No. of positive SLNs 1.000
<3 26 66
3 4 9
SLN, sentinel lymph node; SSM, superficial spreading melanoma; NM, nodular melanoma; ALM, acral lentiginous melanoma; MM, malignant
melanoma; NOC, not otherwise classified.

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Copyright 2016 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
 Plastic and Reconstructive Surgery March 2016

Table 2. Sentinel Lymph Node Drainage and Number with below-knee melanoma (0.8 percent) had sen-
of Positive Sentinel Lymph Node in Each Basin tinel lymph node drainage into the deep inguinal
No. of
basin seen on lymphoscintigraphynone of the
Primary Melanoma Site and No. of SLN-Positive patients had positive sentinel lymph nodes seen
SLN Nodal Basin Patients (%) Patients (%) on pathologic evaluation after dissection.
Below the knee 356 The flowchart demonstrated in Figure1 illus-
Superficial inguinal 271 (76) 63 (23) trates that there was also simultaneous drainage
Deep inguinal 3 (0.8) 0 (0)
Popliteal 2 (0.5) 1 (50) seen to both superficial and deep inguinal basins
Deep and superficial 60 (17) 7 (12) on lymphoscintigraphy in 86 patients. Twenty-
Popliteal and superficial 12 (3) 4 (33) seven patients had primary melanoma above the
Popliteal, superficial, and
deep 9 (2) 1 (11) knee, and 59 patients had their primary melanoma
Above the knee 143 below the knee. Of these 86 patients, 74 patients
Superficial inguinal 113 (79) 24 (21) had negative superficial sentinel lymph nodes on
Deep inguinal 3 (2) 1 (33)
Popliteal 0 (0) 0 (0) pathologic assessment after dissection. If the super-
Deep and superficial 27 (19) 5 (18) ficial inguinal sentinel lymph nodes were negative,
SLN, sentinel lymph node. there were never any patients with positive deep
inguinal sentinel lymph nodes. Twelve patients had
basins. Lymph nodes in 113 patients (79 per- positive superficial inguinal and/or deep inguinal
cent) with melanoma above the knee drained sentinel lymph nodesnine were positive in only
into superficial inguinal basins and, of those, the superficial inguinal basin and three had posi-
24 patients (21 percent) had positive sentinel tive sentinel lymph nodes in both the superficial
lymph nodes. Three above-knee melanoma and deep inguinal sentinel lymph nodes.
patients (2 percent) had deep inguinal drainage Figures2 and 3 show the Kaplan-Meier curves
on lymphoscintigraphy and one patient (33 per- confirming that patients with positive sentinel
cent) had a positive sentinel lymph node. Lymph lymph nodes have a significantly reduced disease-
nodes in 271 patients (76 percent) with mela- free survival and overall survival compared with
noma below the knee drained into the superficial patients with negative sentinel lymph nodes.
inguinal basin, of which 63 patients (23 percent) As expected, patients who underwent deep
had sentinel lymph node positivity. Three patients inguinal and superficial inguinal sentinel lymph

Fig. 1. Lower extremity melanoma patients with simultaneous drainage into superficial and deep
inguinal basins on lymphoscintigraphy. SLN, sentinel lymph node; pts, patients.

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Copyright 2016 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
 Volume 137, Number 3 Sentinel Lymph Node Dissection

Fig. 2. Kaplan-Meier curve. Disease-free survival of sentinel lymph nodepositive versus nega-
tive lower extremity melanoma patients. SLN, sentinel lymph node.

Fig. 3. Kaplan-Meier curve. Overall survival of sentinel lymph nodepositive versus negative
lower extremity melanoma patients. SLN, sentinel lymph node.

node biopsy had a significant difference (p < 0.001) DISCUSSION

in time of operation compared with only superfi-
cial inguinal sentinel lymph node biopsy, with an
average of 41.5 minutes versus 82.5 minutes, as
shown in Table3.
One hundred six patients had a positive sen-
tinel lymph node and 34 of those patients had
additional positive nodes found on completion
dissection. Twenty-nine patients had nodes in the
superficial basin, two in the deep basin and three
in both.
Sentinel lymph node biopsy has replaced
radical regional lymph node dissection as a stag-
ing procedure, with less morbidity. The sentinel
lymph node procedure is 95 to 98 percent accu-
rate in staging the regional node basin and iden-
tifies the 15 to 20 percent of patients with nodal
metastasis who require a completion lymph node
dissection.15
When sentinel nodes are positive, it has been
reported that up to 20 percent of patients were

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 Plastic and Reconstructive Surgery March 2016

Table 3. Average Time in Minutes of Sentinel Lymph Node Biopsy for Superficial and Deep Inguinal Basins*
Basin Above the Knee Below the Knee Average
Superficial inguinal SLN biopsy, min 41 42 41.5
Superficial inguinal and deep inguinal SLN
biopsy, min 79 86 82.5
SLN, sentinel lymph node.
*p < 0.001 between average time in minutes for superficial inguinal SLN biopsy vs. superficial and deep inguinal SLN biopsy.

found to have additional involved nodes on
completion nodal dissection, whereas sentinel
lymph nodenegative patients require no further
surgery.1623 Some authors have examined the
approach of tailoring the extent of a completion
groin dissection to the site that most likely con-
tains metastases based on lymphoscintigraphy.24
In the study by van Der Ploeg et al.,24 images were
used to determine the location of the second-ech-
elon node, which they defined as the lymph node
laying on a direct lymphatic pathway from the sen-
tinel node. The location of the second-echelon
node(s) guided the extent of the groin dissection.
A superficial dissection was performed if the sec-
ond-echelon nodes were depicted in the femoro-
inguinal area; if second-echelon nodes were in the
iliac-obturator area, an external iliac and obtura-
tor fossa dissection was performed as well.
In Table 2, patterns of sentinel lymph node
drainage and sentinel lymph nodepositivity from
melanoma below and above the knee are shown.
Some primary tumors drained into more than
one basin. When there was simultaneous senti-
nel lymph node drainage seen in both superficial
and deep inguinal basins (Fig.2), there was never
any positive deep inguinal nodes when superficial
inguinal nodes were negative. Thus, there appears
to be no benefit in performing a deep inguinal
sentinel lymph node biopsy when preoperative
lymphoscintigraphy shows drainage to both the
superficial and deep inguinal basins. This would
reduce the operating and anesthesia time and the
morbidity associated with increased operative time
and surgery.25 Likely postoperative pain and per-
haps lymphedema of the lower extremity would
also be reduced. Our finding is consistent with a
recent review of the literature, with no reports of
deep inguinal sentinel lymph nodes being posi-
tive for primary melanoma below the knee with
concurrent negative superficial inguinal sentinel
lymph nodes.26 Because some patients had posi-
tive deep inguinal sentinel lymph nodes when the

Fig. 4. Proposed algorithm for patients undergoing lymphoscintigraphy in lower extremity

melanoma. SLN, sentinel lymph node; F/U, follow-up.

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Copyright 2016 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
 Volume 137, Number 3 Sentinel Lymph Node Dissection
superficial inguinal sentinel lymph nodes were
positive, we propose an algorithm for dealing with
lower extremity melanoma patients (Fig.4). When
preoperative lymphoscintigraphy shows drainage
to the superficial inguinal basin or to both basins,
patients should undergo a superficial inguinal
sentinel lymph node biopsy only. If the superficial
inguinal sentinel lymph node is positive, a comple-
tion combined ilioinguinal (superficial and deep)
node dissection should be performed.
Completion lymph node dissection is usu-
ally performed for positive sentinel lymph nodes.
However, there is debate as to the management of
patients with a sentinel lymph node containing only
one tumor focus. Specifically, the Multicenter Selec-
tive Lymphadenectomy Trial showed that 88 percent
of patients who have a single tumor focus will have
no additional nodal metastasis when the comple-
tion lymph node dissection specimen is examined
by hematoxylin and eosin staining.15,27,28 The debate
is ongoing regarding whether completion lymph
node dissection versus sentinel lymph node biopsy
plus watchful follow-up is the proper approach for
this group of patients. The number of patients as
reported in this study is not large but is only from
a single institution. Thus, this is a reasonable num-
ber of 499 patients with lower extremity melanoma.
To validate the data as reported in this study, we are
considering working with other melanoma centers.
CONCLUSIONS
There is evidence that sentinel lymph node
biopsy for deep inguinal basins should be deferred
if there is simultaneous drainage to the superficial
basin. If sentinel lymph nodes from the superfi-
cial basin are positive in patients with simultane-
ous drainage, a completion combined ilioinguinal
lymph node dissection should be performed.
Stanley P. L. Leong, M.D.
Department of Surgery
University of California,
San Francisco School of Medicine
2340 Clay Street, 2nd Floor
San Francisco, Calif. 94115
leongsx@sutterhealth.org
acknowledgments
James E. Cleaver, Ph.D., is supported by a gift
from the Tumori Foundation courtesy of Devron Char,
M.D. (California Pacific Medical Center & Research
Institute). Servando Cardona-Huerta, M.D., Ph.D., is
a visiting professor supported by a scholarship from the
Consorcio de Universidades Mexicanas and the Univer-
sidad Autonoma de Nuevo Leon, Mexico. The authors
Copyright 2016 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
appreciate all the support and hard work that Suresh
Thummala, M.D., spent in helping to organize this
article.
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