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european urology supplements 8 (2009) 470–477
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Consequences of Missed Nodes during Retroperitoneal Lymph
Node Dissection and How to Avoid Them
Giorgio Pizzocaro *, Andrea Guarneri
University of Milan, S. Giuseppe Hospital, Urologic Clinic 2nd, Milan, Italy
Article info
Abstract
Keywords:
Retroperitoneal lymph node
dissection (RPLND)
Missed nodes
Templates
Prospective nerve sparing
Context: Today, the role of urologic surgery in the management of nonseminomatous germ cell tumours (NSGCT) of the testis is limited to
orchiectomy and post-chemotherapy surgery for residual disease. Retroperitoneal lymph node dissection (RPLND) in low stage disease is considered an optional staging procedure and templates have been
introduced to avoid the risk of postoperative loss of antegrade ejaculation. Furthermore, patients with positive nodes are given adjuvant
chemotherapy.
Objective: To determine how best to develop templates that help
surgeons to avoid missed nodes at RPLND maintaining antegrade
ejaculation.
Evidence acquisition: Only through a thorough understanding of the
lymphatic drainage of the testis can we hope to avoid missed nodes
during RPLND. This paper looks at the history of research in this area of
functional anatomy as well as at the current work on the management of
RPLN metastases in nonseminomatous germ cell tumours (NSGCT).
Evidence synthesis: Templates that have been constructed to guide open
or laparoscopic RPLND are fit for nerve sparing but are not able to avoid
occasional missed nodes at RPLND. Critical evaluation of current templates suggests to extent RPLND templates to further zones. The consequence is that more extended templates can compromise antegrade
ejaculation, which can be secured by prospective nerve sparing technique.
Furthermore, RPLND alone will cure 70% of pathological stage IIA patients.
Conclusions: Landing zones for retroperitoneal lymph node metastases
are too scattered to design a restricted template that will allow both
radical RPLND and an easy nerve-sparing technique to maintain antegrade ejaculation. We also have to bear in mind that chemotherapy is not
a panacea for missed or recurrent nodal metastases: radical surgery does
have curative potential and prospective nerve-sparing is safer than
templates.
# 2009 European Association of Urology. Published by Elsevier B.V. All rights reserved.
* Corresponding author. Tel. +39 02 70105700/+39 335 6167380; Fax: +39 02 93660296.
E-mail address: pizzocaro@iol.it (G. Pizzocaro).
1569-9056/$ – see front matter # 2009 European Association of Urology. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.eursup.2009.01.008
european urology supplements 8 (2009) 470–477
1.
471
Introduction
Theoretically, there are several consequences of
missed nodes during retroperitoneal lymph node
dissection (RPLND). Retroperitoneal relapse can occur
if at least one missed node contains vital cancer, and
late recognition of relapse can result if the tumour
does not yield any serum tumour marker rise. If the
missed node was the only pathologic node in that
patient, he will be discharged from the hospital as
pathologic stage I. The disease will progress with
time, and an easy case may become a difficult one.
Repeat RPLND is not an easy operation, and not all
germ cell tumour metastases are curable with
chemotherapy.
2.
Evidence acquisition
2.1.
Lymphatic drainage of the testis
To avoid missed nodes at RPLND, it is imperative to
know the lymphatic drainage of the testis. Lymphatic drainage from the testis to the retroperitoneal
nodes was well known more than a century ago. The
French surgeon Cune´o gave an accurate description
of retroperitoneal nodes (Fig. 1) in 1901 at the Societe´
de Anatomi in Paris, France [1]. He divided superficial nodes (those lateral and anterior to the great
vessels) from deep nodes (those behind the great
vessels): ‘‘The para-aortic nodes are on both sides of
aorta: They drain the lymph from the common iliac
nodes and from kidneys and testis (or ovary). Right
para-aortic nodes are all around inferior vena cava.
Pre-aortic nodes drain the lymph from para aortic
nodes and from lymphatics around the mesenteric
and celiac arteries. Deep retro-aortic nodes receive
the lymph from para-aortic and pre-aortic nodes
and drain into the Pecquet’s cisterna chyli, which
continues upward with the thoracic duct’’ (Fig. 1).
Contemporarily, he and other surgeons [2–4] introduced RPLND en bloc with the spermatic cord and
the cancerous testis. Nevertheless, testicular cancer
has remained an anecdotal disease since World War
II, when >1000 testicular cancers were studied at the
Washington Armed Forces Institute of Pathology [5].
So far, the natural history of testicular tumours was
widely understood, and Mallis and Patton [6] moved
the field of transperitoneal RPLND for nonseminomatous germ cell tumours (NSGCT).
In 1963, Bursch and Sayegh [7] reported their
studies on the visualisation of human testicular
lymphatics, combining pedal and funicular lymphangiography. These studies revealed primary zones of
spread not shown on pedal lymphangiography.
Fig. 1 – Artistic drainage of retroperitoneal lymph nodes by
Cune´o, 1901 [1].
Chiappa et al [8] and Wahlqvist et al [9] confirmed
and added to these observations. Consequently,
surgeons started to study the distribution of retroperitoneal lymph node metastases.
2.2.
Distribution of retroperitoneal lymph node
metastases
2.2.1.
Memorial Sloan-Kettering Cancer Center [10]
In 1974, Ray et al [10] reported the distribution of
retroperitoneal lymph node metastases in 122 out of
321 ‘‘explored’’ NSGCT of the testis. For the right
testis, the paracaval, precaval, interaortocaval, preaortic, right common iliac, and right external iliac
nodes represented the ipsilateral distribution. The
contralateral distribution (left testis) was attributed
to the para-aortic, preaortic, left common iliac, and
left external iliac nodes. Experience with anomalies
such as horseshoe kidney, retroaortic left renal vein,
and left cardinal vein suggested that such malformations did not materially influence the distribution of
the retroperitoneal lymphatic drainage of the testis.
In the earlier years, extended bilateral RPLND was
performed from ureter to ureter and from renal
pedicles to bifurcation of the aorta, including
dissection of the common iliac and proximal onethird of the external iliac vessels. Overall, 61 patients
on each side had radically resected RPLND metastases: On the right side, 18 patients had metastases
in a solitary node and 43 had multiple nodal
metastases. On the left side, 17 patients had a
solitary metastasis and 44 had multiple metastases.
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The conclusions were that the lymphatic drainage from the right testis is to interaortocaval,
precaval, preaortic, paracaval, right common iliac,
and right external iliac nodes. The lymphatic
drainage from the left testis is to the para-aortic,
preaortic, left common iliac, and left external iliac
nodes, in that order. With right-sided tumours, the
metastases were to the ipsilateral nodes in 85% of
cases, to both ipsilateral and contralateral nodes in
13% of cases, and to contralateral nodes only in
1 case. With left-sided tumours, the ipsilateral nodes
alone were involved in 80% of cases and both
ipsilateral and contralateral nodes were involved in
20% of cases.
2.2.2.
Indiana University [11]
Eight years later, Donohue et al [11] studied the
distribution of nodal metastases in nonseminomatous testis cancer, with particular interest in the
suprahilar zone. The distribution of nodal metastases in 104 consecutive pathologic stage II NSGCT
patients was analysed and segregated into 11
anatomic zones of spread: (1) right paracaval, (2)
right precaval, (3) interaortocaval, (4) left preaortic,
(5) left para-aortic, (6) right suprahilar, (7) left
suprahilar, (8) right iliac, (9) left iliac, (10) interiliac,
and (11) gonadal veins. All patients underwent full
bilateral dissection from ureter to ureter and from
diaphragmatic crura down to aortic bifurcation and
iliac arteries. Tumour deposits in these 11 nodal
zones were correlated with the side of the primary
tumour (right vs left) and the extent of retroperitoneal metastases: B1, B2, B3 (IIA, IIB, IIC).
Lymphatic drainage from the right testis involved
interaortocaval, precaval, and preaortic zones, in
that order. In no case of early stage disease (B1) was
there any suprahilar nodal involvement; however,
with more extensive disease, suprahilar nodes were
found in up to 33% of the cases. Lymphatic drainage
from the left testis revealed a marked predilection
for the left para-aortic and preaortic zones in early
stage disease and extension to the interaortocaval
zone in stage B2 disease. The involvement of only
three suprahilar nodes was noted in early stage (B1)
disease. Again, with advanced B2 disease, suprahilar
nodes were involved much more frequently.
Gonadal veins were involved with tumour in 14%
of cases on the right side and in 17% of cases on the
left. The iliac areas were involved rarely in early
stage disease, and contralateral iliacs were not
involved except for one case, right to left. No
contralateral tumour was seen in early stage disease
with the primary site in the left testis, and only one
tumour was seen in late-stage disease. Conversely, if
the tumour originated in the right testis, contral-
ateral involvement did occur in early stage disease
and more often in late-stage disease. Suprahilar
metastases are extremely rare in early stage disease,
and crossover of metastases is clearly prevalent
from right side to left.
2.2.3.
Testicular Tumour Study Group
The third fundamental paper on distribution of
retroperitoneal lymph node metastases in NSGCT
came from a multicentre German cooperative study
[12], demonstrating that big studies can be performed outside high-volume centres. The aim of the
study was to identify the localisation of retroperitoneal lymph node metastases in pathologic
stage II NSGCT of the testis to obtain both a safe
template for RPLND and to preserve antegrade
ejaculation.
The study included 214 consecutive patients with
pathologically documented retroperitoneal metastases, excluding those with metastases >5 cm.
Patients were divided into three groups: group 1
consisted of solitary metastasis; group 2 consisted of
2–5 metastatic nodes with none >2 cm (B1); and
group 3 consisted of >5 metastases between 2 and
5 cm (stage B2). Results were evaluated according to
metastatic groups and laterality, comparing patients
with only one metastatic node to patients with
stage-B1 or B2 disease. Also in this study, the
crossover of metastases was not seen in patients
with only one metastatic node. In contrast, in
patients with multiple metastases, the crossover
from right to left was more frequent (15%) than the
crossover left to right (5%), which was observed only
in pathologic stage B2 case. This study confirmed
the results of the two preceding studies, with the
exception that no one confirmed Ray et al’s [10]
observation of a contralateral solitary metastasis.
2.2.4.
Conclusions
These three studies confirm that in pathologic stage
IIA disease, the crossover left to right is rare, while
the reverse—right to left—is more common.
Furthermore, looking at anatomy and distribution
of metastases, it is also clear that testicular
lymphatics do not follow only the vein, as it was
believed. The fact that on the right side metastases
are more frequent in the interaortocaval region and
on the left side they are preferentially distributed
between the superior para-aortal region and the
renal vein demonstrates that testicular lymphatics
follow at a large both vein and artery.
Furthermore, the nodes behind the great vessels
[1] have never been mentioned in these three
studies. Recently, it has been reported in three
papers [13–15] that the major site of nodal recur-
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rences is retrocaval: All these cases had advanced
disease, and if the lumbar veins are not divided,
retrocaval metastases will be missed. We need to
bear clearly in mind that the inferior vena cava (IVC)
is surrounded by the whole package of right paraaortic nodes [1]. The same situation exists on the
opposite side when there is the left cardinal vein
instead of the IVC. In this situation, anatomy is
overturned. It is a matter of fact that the terms
interaortocaval, precaval, laterocaval, and retrocaval
may be confusing: All of these nodes are right
para-aortic nodes.
2.3.
Full and modified templates for retroperitoneal lymph
node dissection
Table 2 – Distribution of retroperitoneal lymph node
metastasis in patients with only one metastatic node
(sum of template in Ray et al [10] and Weissbach and
Boedefeld [12])
Anatomical sites
Table 1 – Distribution of retroperitoneal lymph node
metastases in pathologic stage IIA disease (sum of
templates in Donohue et al [11] and Weissbach and
Boedefeld [12])
Anatomic sites
Right side
(92 patients)
Paracaval
Precaval
Interaortocaval
Preaortic
Para-aortic
21
37
55
12
6
(23%)
(40%)
(60%)
(13%)
(6.5%)
Right iliac
Common
External
Left iliac
Hilar/suprahilar
8
1*
3
2*
(9%)
(1%)*
(3%)
(2%)*
*
Refers to Weissbach and Boedefeld [12] only.
Left side
(75 patients)
– –
2* (2.7%)*
8 (11 %)
24 (32 %)
67 (89 %)
–
–
3
3
–
–
(4%)
(4%)
Left side
(55 patients)
Paracaval
Precaval
Interaortocaval
Preaortic
Para-aortic
7y (13%)y
13 (24%)
24 (44%)
3 (5.5%)
––
–
1y (2 %)y
1y (2 %)y
4y (7 %)y
48 (87%)
Right iliac
Common
External
Left iliac
Hilar/suprahilar
5 (9%)
1z (2%)z
––
1y (2%)y
–
–
1z (2%)z
–
y
These three studies [10–12] should allow us to define
the landing zones and to design templates to avoid
unnecessary extended RPLND in early stage disease.
No retroperitoneal zone was disease free in pathologic stages IIB and IIC [11,12]. Adding up Donohue
et al’s [11] and Weissbach and Boedefeld’s [12]
reports, right-sided stage IIA tumours had all zones
involved by metastases, while three zones on the
left sided (precaval and contralateral iliac) were
tumour free (Table 1). Considering patients with
only one metastatic node [10,12], the distribution of
retroperitoneal metastases was unilateral only on
the right side, while contralateral metastases (precaval and interaortocaval) were found in two cases
of left-sided tumours (Table 2).
Recently, Eggener et al [16] reported on 191
consecutive patients with pathologic stage II NSGCT
out of 364 patients with clinical stage I disease and
136 patients with clinical stage IIA disease who
underwent RPLND at Memorial Sloan-Kettering
Cancer Centre (MSKCC) between 1989 and 2004.
Right side
(54 patients)
z
Refers to Weissbach and Boedefeld’s findings only [12].
Refers to Ray et al’s findings only [10].
Teratoma alone was present in 17 of these 191
patients (9%) and in combination with other histologies in other 26 patients (14%).
Pathologic stage following RPLND was pN1 in 91
patients (47%), pN2 in 97 patients (51%), and pN3 in
only 3 patients (2%). Cure with surgery alone was
achieved in 90% of pathologic stage I patients and in
70% of pathologic stage IIA patients. Patients with
pathologic stage IIB or IIC disease received adjuvant
chemotherapy.
The aim of the study was to define the incidence
of missed nodes outside five modified RPLND
templates, three described for open surgery [10–12]
and two for laparoscopic surgery [17,18]. Extratemplate disease ranged from 3% to 23%, including 23%
of patients with chemoresistant teratomatous elements. For the right-side templates, inclusion of
para-aortic, preaortic, and right common iliac zones
would have decreased the incidence of extratemplate
disease to 2%. For the left-side template, inclusion of
the interaortacaval, precaval, paracaval, and left
common iliac zones would have decreased the
incidence of extratemplate disease to 3%. In other
words, for the right side only left iliac nodes could be
omitted; for the left side, only the right iliac nodes
could be omitted. Hilar/suprahilar nodes were not
considered in this study.
How can we introduce these data into clinical
practice? Solitary lymph node metastases cannot be
predicted, but early stage lymph node metastases
are usually found in about 30% of clinical stage I
disease and in about 60% of cases in clinical stage IIA
disease [16]. Today, RPLND is an option for both
clinical stage I and clinical stage IIA disease [19].
Surveillance is favoured in low-risk stage I disease
(metastases in 14–22% of cases), and chemotherapy
is favoured both in high-risk (vascular invasion)
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clinical stage I patients (metastases in 48%) and in all
clinical IIA cases (metastases in 60% of cases).
Post-RPLND loss of antegrade ejaculation has
been nearly ‘‘demonized’’ for years, and very few
words have been spent to explain the mechanism of
loss of antegrade ejaculation and how it can be
elegantly avoided. The nerve-sparing technique was
introduced by Jewett et al in 1988 [20]: T12–L3 fibres
coming from both right and left sympathetic chains
converge on both sides of the aorta to form a plexus
around the origin of the inferior mesenteric artery.
This superior plexus passes over the aortic bifurcation to slide down and reach the inferior hypogastric
plexus and the pelvic plexus. The sympathetic fibres
are responsible for the closure of the bladder neck
during orgasm to avoid antegrade ejaculation
(emission is supported by pelvic nerves S2–S3). All
sympathetic structures are recognisable and, when
they are not adherent to retroperitoneal metastases,
they can be identified and prospectively preserved
(Fig. 2).
Additionally, template dissections can preserve
ejaculation, with unilateral RPLND for clinical [21] or
intraoperative [22] stage I disease or with modified
RPLND templates to avoid contralateral nerves. In
particular, it has been demonstrated that by
preserving only the contralateral L3 fibre at the
level of the inferior mesenteric artery antegrade,
ejaculation is usually maintained [23] (Fig. 3).
Furthermore, imipramine chloride (a drug used to
close the bladder neck for enuresis) helps antegrade
Fig. 3 – Bilateral modified template with nerve sparing of
contralateral L3 for a right tumour.
emission. The difference between prospective
nerve-sparing RPLND and template dissection is
that the prospective RPLND allows a full bilateral
dissection (Fig. 2), while modified template RPLND
avoids contralateral dissection and can miss nodes
around the preserved nerves.
Weissbach and Boedefeld [12] proposed modified
unilateral templates for clinical stage I NSGCT to
obtain preservation of antegrade ejaculation sparing
the contralateral sympathetic nerves. The templates
included the right side, paracaval, precaval, interaortocaval upper preaortic (above the level of the
inferior mesenteric artery), and common iliac nodes;
on the left side was the para-aortic nodes and upper
preaortic nodes. It was a good template to avoid loss
of antegrade ejaculation but not so good to avoid
missed nodes. According to the distribution of
lymph node metastases, it is clear that even in the
case of a solitary metastasis on the right side
(Table 2), an occasional patient may have metastatic
disease. Weissbach and Boedefeld’s templates have
been proposed for clinical stage I disease [12], but
they fit only for the great majority, not the totality, of
patients.
2.4.
Fig. 2 – Bilateral nerve sparing following bilateral
retroperitoneal lymph node dissection.
Laparoscopic retroperitoneal lymph node dissection
Laparoscopic RPLND (L.RPLND) has become a routine
approach for pathologic staging of clinical stage I
NSGCT of the testis in several centres. L.RPLND is
typically performed unilaterally on a modified flank
position, and lymph node dissection usually follows
european urology supplements 8 (2009) 470–477
the boundaries described by Weissbach and Boedefeld [12]. As L.RPLND was considered a staging
procedure, patients with positive nodes are regularly
given two courses of adjuvant chemotherapy [24–26].
Recently, Steiner et al introduced the bilateral
nerve-sparing L.RPLND technique [27], and Rassweiler et al produced an excellent review paper
comparing L.RPLND to open RPLND (O.RPLND) [28].
Nevertheless, it is impossible to evaluate the
curative potential of L.RPLND, as pathologic stage
II patients are typically given two courses of
adjuvant chemotherapy. When I started to perform
L.RPLND in clinical stage I patients, I decided not to
give adjuvant chemotherapy to N+ patients, as it
was done on open surgery [29], but the first two
patients with positive nodes developed liver metastases in a few months [30]. Nevertheless, in the
Rassweiler et al review [28], of 140 patients with
positive nodes (25%) who were to receive adjuvant
chemotherapy, 14 did not. Only two of these patients
relapsed, but not in the liver. Also, in the German
Testicular Cancer Study Group [31], only 2 out of 10
N+ patients who did not want to receive adjuvant
chemotherapy relapsed.
Tumour seeding after L.RPLND has been sporadically reported, and in a large review paper, only
one case was reported out of 479 L.RPLND cases [32].
L.RPLND seems to be feasible. Also, bilateral laparoscopic nerve-sparing RPLND is technically feasible
[33], and even obese patients can undergo successful
L.RPLND [34].
The weak point of L.RPLND seems to be recurrences outside templates [16,24,26,28,35,36], usually
following original or modified Weissbach-Boedefeld
templates [12]. This is a template deficiency, but it is
also the responsibility of the surgeon to trust
templates in the presence of metastatic disease at
surgery. This topic has been deeply studied in
Innsbruck [25,27,37,38]. The researchers first studied
whether primary metastatic spread could be behind
the lumbar vessels when positive nodes were
exclusively ventral to the great vessels in early
stage disease, while metastases behind the lumbar
vessels were found only in 3 out of 25 patients with
multiple metastases [37]. Also, none of the pathologic stage I patients who relapsed after L.RPLND
had developed any relapse behind the great lumbar
vessels [25]. They also found retrocaval recurrence
only in postchemotherapy L.RPLND [38], as was
reported by others [13–15].
2.5.
Postchemotherapy surgery
In this era of surveillance in good-risk stage I disease
and of primary chemotherapy in all other cases
475
[19,39,40], the recognised role for surgery is postchemotherapy removal of residual disease after
primary chemotherapy. The aim of this surgery is to
avoid early and late relapses. In two recent and
important reports [41,42], viable cancer was present
in 12% of patients, mature teratoma in 37% and
fibrosis necrosis in 51% of patients in two cumulative series of 684 cases.
In the European study [41], patients were selected
for modified template resection or radical template
resection on the basis of the prechemotherapy
location and size of the residual mass. Radical
resection was performed in all cases of contralateral
spread, interaortocaval location, or tumour diameter >5 cm; a modified template resection was
performed if the prechemotherapy location of the
residual mass corresponded to the primary landing
zone and the residual mass was 5 cm. Ejaculation
was preserved in 85% of patients who underwent a
modified template and in 25% of patients who
underwent full bilateral resection. After a median
follow-up of 39 mo, only eight (5%) patients recurred,
three after modified RPLND and five after full
template. All patients underwent salvage surgery:
Four had teratoma, and three had vital cancer.
Another six patients developed systemic disease.
In the American study [42], 210 patients (40%) had
teratoma, and 59 patients (11%) had viable cancer.
The median follow-up for survivors was 45 mo.
Their results were evaluated according to four
different templates: Weissbach and Boedefeld [12],
Indiana [11], Ray et al [10], and Johns Hopkins
University [18]. The incidence of retroperitoneal
extratemplate disease ranged from 7% (Ray et al) to
32% (Weissbach and Boedefeld). Furthermore, a
German study group realized that postchemotherapy FDG-PET is unable to give a clear benefit in the
prediction of tumour viability in residual masses
[43].
3.
Evidence synthesis
The studies on the distribution of retroperitoneal
metastases in NSGCT of the testis were intended to
help surgeons to avoid both missed nodes at RPLND
and unnecessary extended dissections. Ray et al [10],
Donohue et al [11], and Weissbach and Boedefeld
[12] correctly analysed the distribution of both single
RPLND metastases [10,12] and pathologic stages IIA,
IIB, and IIC [11,12]. Excellent laparoscopic surgeons
in Innsbruck found the correct surgical approach to
L.RPLND [17] and contemporarily applied the Weissbach-Boedefeld template to L.RPLND for clinical
stage I NSGCT [17]. The problem arose when the
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template dissection became an easy guide to nervesparing RPLND instead of the more difficult and
demanding prospective nerve-sparing RPLND first
described by Jewett et al [20]. Maintaining antegrade
ejaculation seemed to become the priority goal at
staging RPLND, nearly to the extent of forgetting that
approximately 30% of clinical stage I patients do
have metastatic nodes and that approximately 50%
of these metastatic nodes are pathologic stage IIB
disease [13].
Of course, surgical planning has to be changed
during staging RPLND whenever evidence of metastasis occurs. The staging template has to cover
pathologic stage IIA disease, which is mainly
diagnosed at definitive pathologic examination.
According to Table 1 and the Steiner at al paper
[13], a security template for left-sided clinical stage 1
NSGCT should include at least interaorta and left
iliac nodes besides para-aortic and preaortic nodes.
A theoretical 5% relapse risk remains for precaval
and hilar/suprahilar nodes. A security template for
right-sided tumours should include all anatomic
sites. Including upper para-aortic nodes at least, the
risk for the right side will decrease to 4.5%. Only a
prospective nerve sparing surgery will allow both
radical RPLND and maintenance of antegrade
ejaculation.
4.
Conclusions
The only conclusion is that landing zones for
retroperitoneal lymph node metastases are too
scattered to design a restricted template that will
allow radical RPLND and an easy nerve-sparing
technique to maintain antegrade ejaculation. If a
restricted template is used, missed nodes are to be
expected, and extratemplate metastases are not the
fault of the template but a responsibility of the
surgeon. We have also to bear clearly in mind that
chemotherapy is not a panacea for missed or
recurrent nodal metastases (memento teratoma)
and that prospective nerve-sparing surgery is not
only technically demanding but is also safer than
templates.
Conflicts of interest
The authors have nothing to disclose.
Funding support
None.
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