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Important surgical concepts and techniques in inguinal lymph node

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Article  in  Current Opinion in Urology · February 2019

DOI: 10.1097/MOU.0000000000000591

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REVIEW

CURRENT
OPINION Important surgical concepts and techniques
in inguinal lymph node dissection
Juan Chipollini a, Jenny Garcia-Castaneda a, Alfredo Harb-De la Rosa a,
Salim Cheriyan b, Mounsif Azizi b, and Philippe E. Spiess b

Purpose of review
Penile cancer is a rare disease with significant physical and psychosocial morbidity. It has a propensity to
spread to the inguinal lymph nodes where it can progress to the pelvis and beyond. Here, we present a
contemporary review on the surgical management of the lymph nodes.
Recent findings
Appropriate management of the lymph nodes is critical, and has been shown to impact survival for these
patients. Those with lower stage disease can achieve cure with inguinal lymph node dissection (ILND),
whereas a multidisciplinary approach is required in those with more extensive disease. Tertiary referral
center should be strongly considered. Advances in surgical techniques have allowed for improved
outcomes and lower morbidity postoperatively. Modified ILND can be safely performed for those with
nonpalpable nodes, whereas diagnostic sentinel node biopsy is a good alternative in centers of
experience. Minimally invasive ILND has recently gained popularity with favorable results at short-term
follow-up. For those with more advanced disease, the literature remains scarce with no high-level evidence
as of yet.
Summary
Early upfront surgery appears the best way to approach men with early involvement of the inguinal lymph
nodes, whereas systemic therapy is typically reserved for higher volume disease. Clinical trial enrollment
continues to be a priority to garner more evidence-based recommendations for this aggressive malignancy.
Keywords
complications, inguinal lymph node dissection, penile cancer, techniques

INTRODUCTION the surgical management of the inguinal lymph

Penile cancer (PeCa) is rare in industrialized nations
with an incidence of approximately one per 100 000
men [1]. The most common histology is a squamous
cell carcinoma arising from the glans or prepuce in
more than 80% of cases [2]. A complete and thor-
ough assessment of the inguinal region is critical
given that the most important predictor of survival
is involvement of the lymph nodes [3–5]. Even for
patients with clinically negative groins (cN0), the
risk of micrometastases approaches 25% [4]. Hence,
inguinal lymph node dissection (ILND) is an essen-
tial component in the management of PeCa
patients, especially for those with lymph node posi-
tive disease in which performance of ILND has been
&&
shown to significantly impact survival [6 ,7].
Traditionally, ILND has carried significant
patient morbidity. Various modifications and tech-
niques have been described in the literature in order
to improve postoperative outcomes. Herein, we
review important considerations and strategies for
nodes and highlight techniques and concepts to
minimize postoperative complications while pre-
serving oncological efficacy of a historically
morbid operation.
CLINICAL EVALUATION
Often, patients will present with a palpable and
visible mass on the penis which may be associated
with pain, urinary obstruction, bleeding or even foul
a
Division of Urology, Department of Surgery, the University of Arizona
College of Medicine, Tucson, Arizona and bDepartment of Genitourinary
Oncology, Moffitt Cancer Center, Tampa, Florida, USA
Correspondence to Juan Chipollini, MD, Division of Urology, Department
of Surgery, the University of Arizona College of Medicine, 1501 N.
Campbell Ave, PO Box 245077, Tucson, AZ 85724-5077, USA.
Tel: +1 479 966 6651; e-mail: jchipollini@surgery.arizona.edu
Curr Opin Urol 2019, 29:286–292
DOI:10.1097/MOU.0000000000000591

www.co-urology.com Volume 29  Number 3  May 2019

Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.


KEY POINTS
 ILND has a survival benefit for men with PeCa.
 Surgical modifications involving less dissection
techniques have improved postoperative outcomes
after ILND.
 Prompt recognition and treatment of complications can
limit long-term disability.
 Prospective studies continue to be needed in the
surgical management of PeCa.
odor which may delay diagnosis when first seen in
the community setting. A clinical examination for
lymph node involvement should assess for palpabil-
ity, size and number of inguinal masses, laterality,
mobility or any degree of fixation. Imaging with
computer tomography (CT) or MRI is another
option for those with difficult physical examination
because of obesity or previous inguinal surgery. PET/
CT imaging with 18F-fluorodeoxyglucose has been
performed to help diagnostic work-up although its
accuracy is better when palpable inguinal adenop-
athy is present and risk of harboring lymph node
metastases (LNMs) is significantly increased to 50–
60% [8].
Consideration of the primary tumor is the main
determinant for lymphatic staging. There are well-
established factors for LNM, in particular: primary
tumor stage, degree of differentiation, perineural
invasion and the presence of lymphovascular inva-
sion which have been shown as strong predictors for
metastatic disease [9,10]. Other prognostic markers
such as p53, Ki-67 and epithelial cadherin have been
evaluated in univariable and multivariable analyses
although not externally validated to this date [11–
13]. Given the low incidence of PeCa, which limits
patient enrollment in prospective studies, contro-
versies on the optimal management of the lymph
nodes continue to this day.
PROPHYLACTIC VERSUS DELAYED
INGUINAL LYMPH NODE DISSECTION
For cN0 patients, early lymphadenectomy has been
shown to have superior oncologic outcomes versus
awaiting for nodal disease to occur [7,14]. Even a
delay of up to 3 months can negatively impact
recurrence in both lymph node negative and posi-
tive cases [15]. For those with pathological N0 dis-
ease, 100% disease-specific survival has been
reported at short-term follow-up [16]. Even the
removal of micrometastatic disease can significantly
improve survival as opposed to watchful waiting for
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Inguinal lymph node dissection Chipollini et al.
nodal disease to occur [7,17]. Thus, both European
Association of Urology and National Comprehen-
sive Cancer Network guidelines recommend inva-
sive lymph node staging for any cN0 patient with
primary tumor features at risk of micrometastases,
that is: pT1 with the presence of lymphovascular
invasion, perineural invasion and/or poor differen-
tiation (pT1b) or any tumor pT2 and above [4,18].
For patients with clinically positive groins
(cNþ), a thorough ILND can still be beneficial while
curing a select few with nodal metastatic disease
[16,19]. For that reason, it is no longer recom-
mended to await the traditional 3–6 weeks of anti-
biotics treatment for patients presenting with
palpable disease. For atypical presentation or when
in need for systemic therapy, a fine needle aspiration
with cytology can be performed when in need of
histologic confirmation of disease [20]. In select
patients with symptomatic inguinal LNM, upfront
ILND may be considered if deemed to be resectable
with consideration for adjuvant therapy. Current
guidelines recommend a multimodal approach for
those with bulky disease consisting of neoadjuvant
chemotherapy followed by surgical resection,
although the timing of systemic therapies continues
to be controversial.
To help answer some of these controversies, the
Internal Penile Advanced Cancer Trial (InPACT)
(NCT02305654) has recently opened. This is a large,
multinational collaboration with plans to accrue 400
cNþ patients over a 5-year period to be randomized
into three arms: upfront ILND, neoadjuvant chemo-
therapy or neoadjuvant chemoradiotherapy; the latter
two followed by surgery. The trial will undoubtedly
provide valuable prospective data and answer some
important questions in the optimal timing of surgery
and its integration with systemic therapy.
MODIFIED VERSUS RADICAL INGUINAL
LYMPH NODE DISSECTION
ILND has traditionally been known as a technically
demanding procedure with high complication rates.
Methods to minimize complications have included
limiting dissection techniques. In 1988, Catalona
[21] introduced the modified LND by reducing dis-
section lateral to the femoral vessels and caudal to
the fossa ovalis while preserving the saphenous
veins. Over time, other modifications have added
a shorter incision and avoidance of Sartorius muscle
transposition [22]. Although this dissection is
appealing for cN0 patients in which the risks of
surgery may outweigh the benefits, a radical ILND
is still recommended in the presence of inguinal
disease. Figure 1 displays the differences in extent
of dissection between the two procedures.
www.co-urology.com 287
Special commentary
FIGURE 1. Limits of dissection of standard versus modified ILND.
DYNAMIC SENTINEL NODE BIOPSY
The consistency of the penile lymphatic drainage to
a group of nodes located superomedial to the
sapheno-femoral junction was the foundation to
the concept of sentinel node biopsy (SNB) in PeCa.
Initial series describing this approach resulted in no
evidence of metastases when the SNB was negative
[23]. However, detection of metastases in the senti-
nel node remains an indication for complete super-
ficial and deep inguinal dissection.
Subsequent reports on SNB documented a rather
high false negative rate reaching up to 50% with
standard dissections and 25% with extended dissec-
tions. Authors concluded that false negative biopsies
were the result of variation in the anatomic location of
the sentinel lymph node [24–27]. As a result, biopsies
targeting a specific anatomic location are no longer
recommended given the considerable unreliability.
Dynamic sentinel node biopsy (DSNB), on the
other hand, consists of a minimally invasive proce-
dure that allows to determine the precise location of
the sentinel node. The method includes preoperative
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usage of lymphoscintigraphy to identify the sentinel
lymph nodes, patent blue dye injection and intraop-
erative guidance with a g-probe to visualize lymphatic
drainage [28]. There are still, however, complications
associated with this procedure including infection,
seroma and wound edge necrosis as described in a
large study with complication rate of 4.7% [29].
In recent years, a meta-analysis looking at new
techniques using radiocolloid-based DSNB has shown
promising results. Nonetheless, this procedure should
still be performed in specialized centers [30]. In sum-
mary, DSNB has acceptable sensitivity when per-
formed at high-volume centers using a standardized
protocol [31]. Therefore, its utility and applicability
should be limited to centers with experienced sur-
geons and nuclear medicine specialists.
MINIMALLY INVASIVE INGUINAL LYMPH
NODE DISSECTION
Given the high complication rates with the open
approach, minimally invasive and robotic techniques
Volume 29  Number 3  May 2019

have been implemented with the aim of decreasing
complications. The indications for the minimally
invasive techniques are the same as for open sur-
gery. Initial experiences for laparoscopic ILND were
first described for melanoma [32]. Urologists
adopted this approach for the management of
penile tumors with Bishoff et al. [33] first reporting
this approach. The robotic platform has since been
adapted and several reports demonstrate significant
improvements in morbidity while maintaining
oncologic equivalency [34].
Several advantages are achieved with the robotic
approach when compared to the standard laparo-
scopic approach including increased magnification,
ergonomic platform and three-dimensional vision
that allows for greater precision and dexterity [35].
However, prospective studies comparing these tech-
niques head-to-head are currently lacking.
To date, both laparoscopic and robotic
approaches for ILND have rendered similar results
as far as node counts when compared to open ILND.
Therefore, we conclude that minimally invasive
approaches are promising but still require further
validation with larger sample sizes and longer fol-
low-up in order to determine its efficacy and com-
plication rates when compared to open approaches
and/or DSNB.
OPEN SURGICAL TECHNIQUES
The most common types of incisions reported in the
literature have been the horizontal versus ‘S’ or ‘T’-
type incisions, although the former has been the
most commonly used by centers of excellence
FIGURE 2. Anatomical zones in inguinal node dissection.
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Inguinal lymph node dissection Chipollini et al.
because of its lower risk of skin necrosis [19,22].
There is little reported on the ideal number of lymph
nodes removed at the time of ILND although a
registry study reported a lymph node yield more
than 15 to be an independent predictor of survival
[36]. Nonetheless, a good understanding of the sur-
gical anatomy is necessary and referral to centers
with experience with this surgery is recommended.
Patients are placed in the frog-leg position and
prophylactic antibiotic coverage is given within
30 min prior to incision along with readministration
at one or two half-lives [37]. Cefazolin is typically
enough to provide adequate coverage but culture-
specific antibiotics should be given preoperatively in
cases of active infections. A 10-cm parallel incision
below the inguinal ligament is usually enough to gain
exposure to the superficial inguinal nodes. The skin
flaps should not be too thin and should keep a good
amount of subcutaneous tissues above Camper’s fas-
cia to keep vascularization of the flaps and minimize
risks of wound ischemia and dehiscence [38,39]. Skin
hooks can also be used to handle the flaps with
minimal disturbance of subcutaneous tissues.
Careful ligation is necessary to decrease the risk
of leaks and seroma. Metallic clips should be used
throughout the dissection to control perforating
blood vessels and lymphatic channels. Self-sustain-
ing retractors can be used to maintain exposure to
the surgical field. All nodes above the fascia lata are
considered the superficial inguinal lymph nodes
and are typically divided into five zones in relation
to the femoral vessels (Fig. 2) [22,40]. In our experi-
ence, the majority of the lymph nodes will be found
in the central and medial zones. In obese patients, it
www.co-urology.com 289
Special commentary
may be easy to overlook the superior medial zone
nodal tissue if a prominent suprapubic fat pad
is present.
Dissection should be carried to the level of the
external oblique fascia and external ring, and pro-
ceed superiorly to the edge of the skin flaps as well as
distally to the edge of the template. Intraoperative
frozen section has been shown to have diagnostic
value in determining the need to proceed to a radical
dissection [41]. It may be time-saving to proceed to
the contralateral dissection while awaiting frozen
section results. To harvest the deep nodes, the fascia
lata is entered at the level of the fossa ovalis. The
deep nodes are typically no more than 3–5 lymph
nodes contained within the femoral sheath. The
node of Cloquet is the most proximal and consid-
ered the margin between the inguinal and pelvic
lymph nodes.
If a deep dissection is required, a Sartorius trans-
position is performed for coverage of the femoral
vessels. Closure with skin staplers should be ade-
quate. Postoperative closed suction drainage within
the inguinal wound is also recommended and
removed once outputs are less than 30–50 ml per
24 h period [39]. For larger defects, tissue flaps using
gracilis, anterolateral thigh, internal oblique, tensor
fascia lata and rectus abdominis have been described
in small retrospective series although not without
their own complications and should be done in
centers with adequate experience with these recon-
structive techniques [22,42].
POSTOPERATIVE CARE
It is unclear whether a period of rest is necessary
after ILND although advisable 48–72 h if a myocu-
taneous flap is used [39]. Although some advocate
keeping patients on antibiotics in the postoperative
period or until drains come out, differences in
wound infections remain uncertain. Compressive
devices have been studied in other cancer types
for lymphedema reduction although no studies
Table 1. Contemporary reports of postoperative morbidity after inguinal lymph node dissection
First author Year Country Number of patients
Gopman et al. [44] 2015 United States,
Netherlands,
China, Germany
Koifman et al. [43] 2013 Brazil
Stuiver et al. [45] 2013 Netherlands
Yao et al. [46] 2010 China
Spiess et al. [39] 2008 United States
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have been performed specifically for PeCa patients.
At the minimum, sequential compressive devices
may help with early lymphedema and decreased
the risk of thromboembolic complications. Periop-
erative low-dose heparin can also be used, although
it might increase lymphatic leakage [38].
PREVENTION AND MANAGEMENT OF
COMPLICATIONS
Currently, the majority of the ILND-related compli-
cations are secondary to infections, wound healing
and lymphedema, with the latter two shown to be
decreasing over time [39,43]. With hopes of decreas-
ing complications, trends in operative management
have resulted in more limited dissection techniques
especially for those with cN0 disease at the time of
surgery. Surgical morbidity remains a significant
concern for those requiring more extensive dissec-
tions and some of these complications can result in
long-term disability. Table 1 [44,43,45,46,39] con-
tains a list of common complications from contem-
porary series of patients after prophylactic or
therapeutic ILND.
LYMPHOCELE AND LYMPHEDEMA
Traditionally, the rate of lymphocele and lymph-
edema has ranged between 9 and 16% and 16 and
50%, respectively; in older series of patients [47–49].
Preservation of the saphenous vein with adoption of
modified ILND has significant reduced these two
complications. During dissection, careful lymphatic
control can be obtained with meticulous ligation of
channels. Data on fibrin glue and other sealants
have been conflicting in other disease sites, so there
are no recommendations for these products in PeCa
as of yet. Leaving closed suction drains until drain-
age is 30–50 ml or less per day is preferred. By doing
so, fluid accumulation can be prevented and result
in early adhesions between skin flaps and underly-
ing fascia and muscle [50]. Patients can leave the
Complication rate Most common complications
327 55.4% Infection, seroma, dehiscence,
lymphocele, necrosis,
scrotal edema
170 10.3% Lymphedema, seroma
163 58% Infection, seroma, necrosis
75 24.7% Infection, necrosis, lymphedema,
seroma, lymphocele
43 49% Lymphedema, wound
dehiscence, infection
Volume 29  Number 3  May 2019

hospital with drains and monitor the outputs daily
until eventual drain removal. Use of fitted compres-
sion stockings during ambulation is preferred until
6 months after surgery when patients can be reas-
sessed without these devices, and early referral to a
lymphedema specialist if chronic lymphedema
develops [39,50].
WOUND INFECTION
Patients should be covered with prophylactic anti-
biotics at the time of surgery. Patients with active
infection should undergo culture-specific treatment
prior to ILND in order to prevent sepsis. Microorgan-
isms isolated from septic wounds have included
gram-negative rods, Staphylococcus species, diphthe-
roids and Peptostreptococcus. Hence, broad-spectrum
antibiotics (e.g. ampicillin/gentamycin or ampicil-
lin/ciprofloxacin) may decrease the risk of wound
infection [38]. As the drains may provide an avenue
for bacterial migration into the ILND wound, keeping
patients on prophylactic antibiotics has been recom-
mended until the drains can be removed [39,50].
FLAP NECROSIS AND DEHISCENCE
Keeping the skin flaps well vascularized by dissect-
ing beneath Scarpa’s fascia is recommended. Avoid-
ance of T and S incisions is encouraged [22,39,51].
Intravenous fluorescein injection and observation
of the skin flaps under ultraviolet light to evaluate
vascularization has been reported with moderate
success in preventing wound dehiscence [52]. If
there is excessive tension during closure, reconstruc-
tion with myocutaneous flaps can be used. For
prophylactic dissections or smaller defects, a Sarto-
rious muscle flap is typically sufficient. For larger
defects, the rectus femoris flap has been utilized
with acceptable wound healing [53]. Inguinal recon-
struction should be considered early, along with
plastic surgery consultation, if expecting a large
defect or previously radiated field. When skin edges
cannot be approximated, the margins can be
sutured to the underlying muscle and the remaining
tissues covered with a split-thickness skin graft [38].
For wounds that fail to heal, vacuum-assisted clo-
sure has been reported to be superior to standard
wound care in a small series of PeCa patients [54]. A
prospective study is underway evaluating the value
of prophylactic vacuum therapy in wound compli-
cations after ILND [55].
MISCELLANEOUS COMPLICATIONS
Neuropraxia and nerve injury are rare after ILND
and likely because of excess traction or thermal
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Inguinal lymph node dissection Chipollini et al.
injury, so gentle wound retraction and careful cau-
tery should be used to avoid nerve injury. To mini-
mize the risk of deep venous thrombosis (DVT),
early ambulation and sequential compression devi-
ces can further decrease the risk of DVT [50]. Peri-
operative low-molecular weight heparin can be used
in the postoperative setting when a period of immo-
bilization is expected but its role in PeCa is not
yet clear.
CONCLUSION
For patients with PeCa, a thorough and meticulous
lymphadenectomy can offer a chance for cure.
Performance of ILND should not be deterred for
fear of complications and referral to a center of
experience cannot be overemphasized. Limited
dissection techniques have improved periopera-
tive outcomes. Careful planning and prompt treat-
ment of complications can help improve
morbidity and quality of life of affected patients,
and may result in fewer delays of further adjuvant
therapy. Prospective studies and continued collab-
oration is needed to advance evidence-based rec-
ommendations.
Acknowledgements
None.
Financial support and sponsorship
None.
Conflicts of interest
There are no conflicts of interest.
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Volume 29  Number 3  May 2019