Modified Technique of Radical Inguinal Lymphadenectomy For Penile Carcinoma: Morbidity and Outcome

tapraid4/jur-juro/jur-juro/jur99909/jur8189d09z ROYERL S1 5/5/10 12:09 Art: 6208
Modified Technique of Radical Inguinal Lymphadenectomy for

Penile Carcinoma: Morbidity and Outcome
Kai Yao,* Hua Tu,* Yong-Hong Li, Zi-Ke Qin, Zhuo-Wei Liu, Fang-Jian Zhou
and Hui Han
From the Department of Urology, Cancer Center, Sun Yat-Sen University and State Key Laboratory of Oncology in Southern China,
Guangzhou, P. R. China
Purpose: Classic radical inguinal lymphadenectomy is associated with significant morbidity. Modified inguinal lymphadenectomy has been used to decrease
the complication rate but it may compromise the oncological effect and depends
on the use of intraoperative frozen sections, which may be inaccurate. We modified the technique of radical inguinal lymphadenectomy to decrease postoperative complications without compromising oncological effectiveness.
Materials and Methods: We performed 150 modified radical inguinal dissections
in 75 patients with penile carcinoma from February 1999 to September 2008.
Patients underwent modified radical inguinal dissection characterized by an
S-shaped incision, precisely separating layers using an anatomical landmark and
preserving the fascia lata. The boundaries of dissection are the same as those of
radical inguinal lymphadenectomy. Survival and morbidity data were retrospectively analyzed, and survival probabilities were calculated.
Results: Followup ranged from 12 to 113 months. Overall 3-year survival was
92%, and for N0, N1, N2 and N3 disease it was 100%, 100%, 85% and 57.1%,
respectively. A total of 37 complications occurred including wound infection
(1.4%), skin necrosis (4.7%), lymphedema (13.9%), seroma (2.0%), lymphocele
(2.0%) and deep venous thrombosis (0.7%).
Conclusions: Morbidity related to groin dissection in patients with penile carcinoma can be decreased and oncological effectiveness can be preserved using this
modified inguinal dissection technique.
Key Words: lymph node excision, lymph nodes, penile neoplasms, morbidity
IN patients with penile cancer lymph
node metastasis is the most important variable affecting survival.1 The
radical inguinal LAD described by
Daseler et al is considered the most
extensive approach to groin dissection
for penile carcinoma.2 However, this
procedure is associated with high
morbidity.1,3 To reduce morbidity Catalona proposed a modified inguinal
LAD in which the lateral and caudal
dimensions of the dissection were decreased.4 The modified inguinal LAD
is associated with less morbidity than
radical inguinal LAD.5,6 However, reducing the field of dissection in the

modified inguinal LAD increased the
potential for false-negative histopathological results and, thus, compromised the oncological effectiveness of
the procedure. The high false-negative rate of 15% described by Lopes et
al should be considered in light of recent findings concerning lymphatic
drainage to the lateral superior Daselers zone, which is not dissected in
this approach.7,8 In addition, the modified inguinal LAD must be extended
0022-5347/10/1842-0001/0
THE JOURNAL OF UROLOGY
2010 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION
Vol. 184, 000, August 2010

Printed in U.S.A.
DOI:10.1016/j.juro.2010.03.140
Dochead: Adult Urology
AND
RESEARCH, INC.
Abbreviations
and Acronyms
FA femoral artery
FNAC fine needle aspiration
cytology
FV femoral vein
LAD lymphadenectomy
SV saphenous vein
Submitted for publication November 9, 2009.
Nothing to disclose.
* Equal study contribution.
Correspondence: Department of Urology,
Sun Yat-sen University Cancer Center and
State Key Laboratory of Oncology in Southern
China, Guangzhou 510060, P.R. China (telephone: 86-20-8734-3309; FAX: 86-20-87343656; e-mail: hanhui1967@sina.com or zhoufj@
mail.sysu.edu.cn).
Editors Note: This article is the

of 5 published in this issue
for which category 1 CME credits
can be earned. Instructions for
obtaining credits are given with
the questions on pages and
.
www.jurology.com

2
MODIFIED RADICAL INGUINAL LYMPHADENECTOMY FOR PENILE CARCINOMA
to a radical inguinal LAD if positive nodes are

present on frozen section, which may be inaccurate
for the diagnosis of lymph node involvement and
may simultaneously increase hospital costs. Thus,
we modified the technique based on the boundaries
of the radical dissection to ensure the radical oncological effect while reducing morbidity.
In addition, the majority of patients with penile
cancer in China are of low socioeconomic class without adequate access to health care, which makes
regular followup examination difficult. If regional
lymph node metastasis is missed initially, cases that
could have been cured via LAD can rarely be salvaged with delayed therapeutic dissection.9,10 In addition, the hospital readmission cost is an economic
burden for these patients. Faced with this difficult
situation we amputate the penis simultaneously
with bilateral inguinal LAD in most cases to assure
adequate treatment. We do not perform dynamic
sentinel node biopsy and ultrasound guided FNAC.
The technique of dynamic sentinel node biopsy has
been extensively studied in only a few specialized
centers where a reduced false-negative rate of 4.8%
was recently reported.11 Ultrasound guided FNAC
can detect lymph node metastases with a sensitivity
of 93% and specificity of 91% in cases with palpable
lymph nodes. However, the sensitivity is low when
assessing lymph node status in patients with cN0
disease.12,13 Ultrasound guided FNAC is useful only
if positive because negative findings cannot rule out
malignancy. The mortality rate from such missed
cases is between 4% and 44%.14 In this retrospective
study we report morbidity and outcomes of a modified radical inguinal LAD technique for 75 patients
with penile cancer performed at our center since
1999.
MATERIALS AND METHODS
Operative Indications
Treatment protocols were discussed with the patient and
the importance of rigorous followup was emphasized. Considering that a surveillance program was unsuitable for
them, most of the patients consented to inguinal LAD, of
whom 75 underwent modified radical inguinal LAD. Of
the 75 patients 15 were referred from other hospitals after
treatment of the primary lesion and required only lymphadenectomy. The other patients underwent simultaneous
penectomy and lymphadenectomy. Adjuvant radiation
therapy was given in cases of pN2 and pN3 disease. All
procedures were performed by 2 surgeons (FJZ and HH).
Treatment
The boundaries of dissection were the apex of the femoral
triangle distally, the sartorius muscle laterally, the adductor longus muscle medially and the inguinal ligament
superiorly. The floor of the dissection was above the fascia
lata. A 12 cm, S-shaped incision was made beginning 2 cm
medial to the anterior superior iliac spine. The incision
proceeded distally through the middle of the groin crease,
then vertically along the surface projection of the FA, and
ended 3.5 cm inferior and medial to the fossa ovalis (fig. 1).
The skin was incised until a white, semihyaline membranous layer of fibrous tissue was identified (fig. 2, a). The
skin flaps were separated in this plane and left covered by
the superficial layer of Campers fascia (fig. 2, b). Next the
tissues between the superficial layer of Campers fascia
and fascia lata were dissected, including the superficial
inguinal lymphatic tissues (fig. 2, c). All subcutaneous
lymphatics were ligated at the periphery of the dissection.
The SV was preserved (fig. 3, a). The cribriform fascia
near the femoral canal was divided, and the deep inguinal
lymph nodes, lying in the fossa ovalis medial to the FV,
were dissected from the inguinal ligament to distal to the
fossa ovalis (fig. 3, b). The posterior and lateral aspects of
the femoral vessels and femoral nerve were not cleared.
The fascia lata was preserved completely (fig. 3, c) and
sutured to the subcutaneous tissue (fig. 3, d). In this
technique the transposition of the sartorius muscle is
eliminated. A suction drainage was placed subcutaneously
and maintained until drainage was less than 10 ml daily
for 2 consecutive days.
F1
F2
F3
Patients
Between February 1999 and September 2008 a total of 115
Chinese patients were treated for penile carcinoma. Mean
patient age was 51.5 years (range 19 to 79). Clinical staging consisted of primary tumor evaluation, inguinal palpation to assess the presence or absence of identifiable
lymph nodes, and computerized tomography of the chest,
abdomen and pelvis. All cases were M0 disease. Radical
inguinal LAD was performed in 9 patients and modified
inguinal LAD was performed in 7, while 20 only consented
to treatment of the primary lesion. Fixed inguinal lymph
nodes were present in 2 patients who were treated with
only systemic chemotherapy. Patients lost to followup
were excluded from the analysis and 2 of these were in the
modified radical inguinal LAD group. Thus, a total of 75
patients were included in this study, and had disease
classified according to the 2002 TNM classification as
cN0 27 (36%), cN118 (24%) and cN230 (40%).
C
O
L
O
R
Figure 1. a, S-shaped incision markings. SCIA, superficial circumflex iliac artery. SEPA, superficial external pudendal artery.
SEA, superficial epigastric artery. ASIS, anterior superior iliac
spine. PTPB, pubic tubercle of pubic bone. b, S-shaped surgical
incision.

C
O
L
O
R
C
O
L
O
R
Figure 2. a, skin was incised until white, semihyaline membranous layer of fibrous tissue was identified. b, arrows indicate white,
semihyaline, membranate layer of fibrous tissue. Skin flaps were separated in plane. c, tissues between superficial layer of Campers
fascia and fascia lata were dissected. 1, skin and subcutaneous tissue. 2, superfascial layer of Campers fascia. 3, anatomical landmark.
4, deep layer of Campers fascia. 5, fascia lata. 6, muscle of thigh.
Data Collection and Followup

Data on survival and complications were obtained from
medical charts, outpatient clinic records and when necessary through contact with the patients family. All pathological examinations were performed by 3 pathologists.
Complications were classified as major or minor. Major

complications included lymphedema interfering with ambulation and deep venous thrombosis. Minor complications included lymphedema (include leg and scrotal) that
did not interfere with ambulation and resolved within 1
C
O
L
O
R
C
O
L
O
R
Figure 3. a, SV was preserved. b, cribriform fascia near femoral canal was divided. OF, oval fossa. II, inguinal ligament. SC, spermatic
cord. c, fascia lata was preserved completely. 1, adductor longus muscles. 2, sartorius muscle. 3, fossa ovalis. 4, fascia lata. d, fascia
lata was sutured to subcutaneous tissue.

4
Table 1. Summary of surgical outcome, followup and survival data

Lymph Node Stage
Overall
No. pts
No. pathological grade:
G1
G2
G3
No. tumor stage:
T1
T2
T3
T4
No. recurrence:
Penis
Scrotum
Groin
Pelvis
Liver
% Disease-free survival:
1-Yr
2-Yr
3-Yr
% Overall survival:
1-Yr
2-Yr
3-Yr
pN0
pN1
75
36
12
39
28
8
24
12
0
6
4
2
8
8 (1*)
4 (2*)
1
4 (1*)
2 (2*)
38.5
57.1
100
28
29
12
6
9
2
2
0
3
2
18
14
2
2
1
1
0
0
0
0
5
6
1
0
2
1
1
0
0
0
5
8
6 (2*)
1 (1*)
3
0
1*
0
1*
1*
0
1
3 (1*)
3 (2*)
3
0
0
0
2*
1*
35.7
51.7
83.3
66.7
90.7
88.0
88.0
97.2
97.2
97.2
96.0
93.3
92.0
100
100
100
20
91.7
83.3
83.3
100
100
100
pN2
pN3
7
Node Pos Rate (%)

52.0
90.0
85.0
85.0
57.1
57.1
57.1
95.0
90.0
85.0
71.4
57.1
57.1
* Number dead of carcinoma of the penis.
month, seroma or lymphocele formation not requiring aspiration, wound infection without sepsis and minimal skin
necrosis requiring no therapy. All the patients were advised to follow up every 3 to 6 months in the first 2 years
and then once yearly. Statistical analysis was performed
with SPSS (v15.0) and the Kaplan-Meier technique was
used to evaluate survival probabilities.
RESULTS
T1
Surgical Outcomes
In this population of 75 patients 150 modified radical inguinal dissections were performed and the
data are presented in table 1. The average number
of lymph nodes obtained was 12.6 per side with an
average of 2.1 deep lymph nodes per side. There
were 12, 20 and 7 patients with stage pN1, pN2 and
pN3 disease, respectively. Of the 48 patients with
palpable lymph nodes 30 (62.5%) had positive nodes
on subsequent histological examination. In the 27
patients with nonpalpable nodes on clinical examination 9 (33.3%) had positive nodal disease.
Followup and Survival
Median followup was 51 months (range 12 to 113).
At followup 69 patients survived and 6 died of the
disease. There were 9 recurrences observed during
followup. Mean time to recurrence after LAD was 9
months (range 3 to 15) and there was no inguinal
recurrence in this series. The locations of recurrence
are presented in table 1. The 3-year disease-free

survival for N0, N1, N2 and N3 disease was 97.2%,
83.3%, 85.0% and 57.1%, respectively. The 3-year
overall survival for N0, N1, N2 and N3 disease was
100%, 100%, 85% and 57.1%, respectively.
Morbidity
A total of 37 complications occurred and are presented in table 2. There were 129 dissections with no
complications (86%) and 15 with 1 or 2 minor complications (10%). The most common complication
was lymphedema (13.9%) but it was minor in most
cases. Skin edge necrosis was minor, without wound
dehiscence in 7 dissections and required no treatment. There were minor groin complications in 31
cases (20.7%), and 6 major complications were observed including 5 cases of lymphedema and 1 of
deep venous thrombosis.
Table 2. Complications of modified LAD
No. (%)
Minor:
Skin necrosis
Lymphedema
Seroma
Infection
Lymphocele
Major:
Lymphedema
Deep venous thrombosis
7 (4.7)
16 (10.6)
3 (2.0)
2 (1.4)
3 (2.0)
5 (3.3)
1 (0.7)
T2

DISCUSSION
T3
Several of the techniques we adopted such as

preserving the SV and leaving the sartorius muscle
in place were proposed by Catalona, and used in the
modified inguinal LAD.4 Subsequently Jacobellis
proposed the concept of a modified radical inguinal
LAD in which the 2 previously mentioned techniques were also adopted, while the whole area described by Daseler et al was dissected.2,17 These
techniques have been demonstrated as effective in
decreasing morbidity.15,22,23 In addition to these 2
modifications we describe several other modifications of surgical technique for preventing complications.
We adopted the use of an S-shaped incision. Compared to a conventional S-shaped incision for ilioinguinal dissection our S-shaped incision was shorter
and more oblique, thus providing satisfactory exposure without placing excessive tension on the flaps.
Histological examination revealed that Campers
fascia of the groin was divided into superficial and
deep layers by a denser band of connective tissue.
Anatomical studies revealed that the skin of the
groin is supplied by 2 arterial plexuses, that is the
subdermal plexus deep to the skin and the deep
fascial plexus. Large branches from the perforator
formed a deep fascial plexus in the deep adipofascial
layer, which communicates with the subdermal
plexus by sending small ascending branches.24 Further oblique branches arose from the perforator
which do not contribute to the fascial plexus and
instead travel directly toward the skin to form part
of the subdermal plexus.24,25 After removal the deep
adipofascial layer, the fascial plexus and the oblique
vessels supplying the subdermal plexus are damaged. The blood supply to the skin flap is provided by
the perforators in adjacent vascular territories at
the margins of the flap by communicating with the
subdermal plexus. The blood supply of skin flaps in
the inguinal region arises from the superficial
Although radical inguinal LAD has proven therapeutic value, the associated high morbidity limits its
use. The modified inguinal LAD is associated with
lower morbidity. However, the oncological effect is
unreliable.7,8,15 With these considerations we modified the radical inguinal LAD to reduce the associated morbidity yet maintain the therapeutic effectiveness.
Adequate dissection boundaries are essential for
attaining excellent disease control. In our series all
recurrence was outside the inguinal region. The
overall 3-year survival in our series was 92% with
84.6% survival for node positive disease. In a recent
series 100 cases of penile cancer were managed according to the European Association of Urology
guidelines, with an overall cancer 3-year survival
rate of 92% and 81% for node positive disease, outcomes similar to ours.16 We believe this satisfactory
long-term survival is due to the radical boundaries
of dissection. Moreover node count is an important
surrogate marker for the quality of lymph node dissection. In our series the average number of lymph
nodes was 12.6 per side with 2.1 deep lymph nodes,
which is comparable with the number reported in
previous studies.17,18
Moreover the morbidity in our series was decreased to a level comparable to that of the modified
inguinal LAD, and was significantly lower than that
of radical inguinal LAD (table 3).4 6,15,19 23 Compared with most studies of radical inguinal LAD,
infection, skin necrosis, seroma and lymphocele
rates were lower in our series while the rate of
lymphedema was comparable. Thus, we considered
that the decreased complication rate in our study is
related to the S-shaped incision, dissection in definite anatomical planes, preservation of the greater
SV, complete preservation of the fascia lata and
leaving the sartorius muscle in place.
Table 3. Reported morbidity of modified and radical inguinal LAD
References
Modified groups:
Catalona4
Parra20
Coblentz and Theodorescu21
Bevan-Thomas et al5
Bouchot et al6
dAncona et al15
Standard groups:
Ravi19
Ayyappan et al18
Bevan-Thomas et al5
Bouchot et al6
Nelson et al22
dAncona et al15
Spiess et al23
Present series
No. LAD
% Infection
% Skin Necrosis
% Lymphedema
% Seroma
% Lymphocele
12
24
22
66
118
42
0
0
4.5
9.1
0.8
0
8.3
0
4.5
4.5
2.5
0
100
8.3
36.4
21.2
3.4
0
0
0
0
12.1
2.5
26.3
8.3
4.2
22.7
0
0
10.5
405
135
40
58
80
8
86
150
16.3
70
15
6.9
7.5
0
9
1.4
62
36
12.5
12
10
37.5
11
4.7
26.7
57
25
22.4
15
37.5
17
13.9
6.9
12
7.5
13.8
0
37.5
0
2.0
9
87
5
5.2
15
12.5
2
2.0

6
branches of the inferior epigastric, external pudendal and circumflex iliac arteries, which run parallel
to the inguinal ligament. In theory the S-shaped
skin incision minimally damages these arteries and
subsequently preserves the blood supply of the adjacent vascular territories of the skin flap. Moreover
tension on the skin sutures is reduced, which potentially results in better healing. Although the Sshaped incision has been reported to be associated
with a significant rate of skin flap necrosis, in our
study the rate of skin flap necrosis was comparable
to that of other incisions.4,10
In addition, we identified a white, semihyaline,
membranous layer of fibrous tissue between the 2
layers of Campers fascia, an anatomical landmark
that locates the correct cleavage plane to dissect the
skin flaps. Jacobellis pointed out that dissecting the
skin flaps in the correct plane is critical in decreasing the complication rate.17 However, the method of
identifying the correct cleavage plane remains unclear. Campers fascia of the groin region is composed of 2 layers. The subdermal plexus is primarily
distributed in the superficial layer and the superficial lymph nodes only reside in the deep layer. The
correct dissection plane is between the 2 layers.
Guided by the layer of white fibrous tissue as a
landmark, dissection of the skin flaps causes minimal disruption of blood vessels and the superficial
lymphatic tissue can be completely removed. The
occurrence of skin necrosis (4.7%) and wound dehiscence was low in our series. If the skin flap is too
thin the subdermal plexus will be damaged and the
arterial supply will be disrupted, leading to ischemia and skin necrosis. The idea that skin flaps
should be preserved deep to Scarpas fascia or left
thicker has been frequently mentioned. Actually
Scarpas fascia is fused to the fascia lata of the thigh
1 cm below the inguinal ligament. A thicker skin
flap inevitably contains tissue of the deep layer of
Campers fascia, which may harbor metastatic nodes
and result in recurrence. In addition, residual tissue

will lose most of its blood supply after dissection,
which can lead to fat necrosis or infection.
Finally the fascia lata was preserved completely.
The deep inguinal nodes originate directly from the
superficial lymphatic tissue and are always situated
within the opening of the fossa ovalis.26 There are no
lymph nodes distal to the lower margin of the fossa
ovalis and lateral to the femoral vessels beneath the
fascia lata.27 In addition, the cribriform fascia is a
derivative of thickened connective tissue filling the
fossa ovalis and its embryological origin is different
from that of the fascia lata. With preservation of
the fascia lata we can protect the capillaries beneath
the fascia lata, and decrease the chances of seroma
and lymphocele formation. In addition, the femoral
vessels may be covered by the fascia lata, eliminating the need for transposition of the sartorius muscle. A study that adopted the technique of preservation of fascia for groin dissection in the treatment of
vulvar carcinoma reported oncological effectiveness
while decreasing the complication rate.28 In our
cases the reliability of this procedure was further
validated by the absence of regional recurrence and
lower morbidity.
There are some limitations to this study including
its retrospective nature and the lack of randomized
trials to evaluate this technique. In addition, we
offered this operation to patients with clinically
node negative status due to socioeconomic factors,
which may have influenced the results.
CONCLUSIONS
Our modified surgical technique of radical LAD,
characterized by an S-shaped incision, precise separation of layers using a membranate anatomical
landmark and preservation of the fascia lata, decreases groin dissection related complications without jeopardizing oncological effectiveness.
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2. Daseler EH, Anson BJ and Reimann AF: Radical

excision of the inguinal and iliac lymph glands;
study based upon 450 anatomical dissections and
upon supportive clinical observations. Surg Gynecol Obstet 1948; 87: 679.
5. Bevan-Thomas R, Slaton JW and Pettaway CA:

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3. David SS and Kenneth WA: Surgery of penile and

urethral carcinoma. In: Campbell-Walsh Urology,
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Novick et al: Philadelphia: Elsevier 2007; pp
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inguinal lymphadenectomy for invasive penile
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and results. J Urol 2003; 169: 1349.
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tapraid4/jur-juro/jur-juro/jur99909/jur8189d09z ROYERL S1 5/5/10 12:09 Art: 6208