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Sentinel Node Evaluation in Prostate Cancer
Willem Meinhardt *
Netherlands Cancer Institute/Antoni van Leeuwenhoek Hospital, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
Article info
Abstract
Keywords:
Lymph nodes
Lymphadenectomy
Prostate cancer
Radioguided surgery
Sentinel node
Objectives: Provide an overview of the use of the sentinel node (SN) technique in
prostate carcinoma. The relevance of nodal staging in the several stages of prostate
carcinoma, technical aspects of the SN technique, indications, and lessons learned
from it are discussed.
Introduction: The lymph node status is relevant in all M0 tumour stages. In early
prostate cancer the changes of nodal involvement are so low that invasive diagnostics are superfluous. However, the definition of this early stage is narrowing
since the results of extensive node dissection have shown that previously assumed
low-risk patients may harbour positive lymph nodes. On the other hand, in locally
advanced cases, if the decision for external-beam radiation on the lymph node
basins in combination with radiation of the prostate and 3 yr of hormonal therapy
has been made, a lymph node dissection seems superfluous.
Methods: SN dissection may be performed in open surgery or as a laparoscopic
technique. A radioactive tracer is injected into the prostate and on g-camera imaging
it is decided which lymph nodes are the possible first landing zones for the prostate
tumour. During the radioguided surgery, the excision of the SNs, a handheld g probe
is used to identify the radioactive nodes. On introducing the method in a clinic, it is
important to do a conformal extensive pelvic lymph node dissection as well to
ensure that logistics and the performance are reliable.
Results: SN dissection is as reliable as a diagnostic tool as extended pelvic lymph
node dissection. Because it may show cancer-bearing nodes outside of the region of
the extended lymph node dissection, such as the presacral area, it may on occasion
be even more sensitive.
Discussion: The SN technique is likely to have fewer complications compared to the
extended lymph node dissection. On the other hand, an extended lymph node dissection may still be indicated when the SN procedure yields only a few positive lymph
nodes and definite cure is still the aim. Weighing the advantages and disadvantages of
the laparoscopic versus the open SN technique is not different than in any other
procedure. In the near future, sophisticated imaging techniques will identify nodes
that are suspicious for micrometastases. This will make minimal invasive methods to
confirm the nodal status not superfluous, but more in demand.
Conclusion: When the nodal stage is important for treatment decisions, only
extended dissections or the SN method will provide accurate staging. The SN
procedure is less invasive and will avoid an extensive node dissection in the majority
of cases.
# 2007 European Association of Urology and European Board of Urology.
Published by Elsevier B.V. All rights reserved.
* Tel. +031 (0) 205129111; Fax: +031 (0) 205122554.
E-mail address: [email protected].
1871-2592/$ – see front matter # 2007 European Association of Urology and European Board of Urology. doi:10.1016/j.eeus.2007.07.003
Published by Elsevier B.V. All rights reserved.
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eau-ebu update series 5 (2007) 223–231
1.
Introduction
1.1.
Brief history
Even 30 yr ago studies showed that prostate
carcinoma lymph node metastases have their first
landing zones in lymph node areas around the
internal iliac artery, obturator fossa, external iliac
artery, common iliac artery, and presciatic and
presacral areas [1]. However, this was the era of
rather late diagnosis and most men with positive
nodes had involvement of more than one area.
When diagnostic methods improved, the attention
shifted towards risk assessment and defining a
group of patients in whom a node dissection could
be avoided [2].
For patients who were candidates for perineal
prostatectomy or external-beam radiation, a strong
case was made for laparoscopic lymphadenectomy.
After the introduction of laparoscopic pelvic node
dissection for prostate carcinoma, studies comparing minilaparotomy with laparoscopic resection
were done. The number of nodes excised in these
studies and the limitations of the laparoscopic
technique in the early days have somehow made
a pelvic node dissection synonymous with clearing
the obturator fossa only in many urologic practises
[3,4]. More recently, publications of urologists who
documented their practice of extended lymph node
dissection have caused reasons for concern [5,6].
Dissection of only the obturator fossa misses, in
some series, up to 75% of the clinically occult
metastasis [7].
The sentinel node (SN) concept was first developed by Cabanas and applied to patients with penile
carcinoma. With lymphangiography studies he
assessed the location of the first lymph node from
the lymphatics of the penis. Excision of only this
node on both sides was believed to give sufficient
proof of lymph node involvement [8]. The SN
procedure is a diagnostic procedure. In case of
penile carcinoma it was used as a tool to decide if a
complete lymphadenectomy was indicated or not.
Unfortunately, the method was not reliable enough.
Morton described the dynamic SN procedure. By
injecting a dye and a radioactive tracer in or near the
tumour, the spread of the tracer could be followed
on a g camera and the first landing zones could be
visualised. With a handheld probe these nodes may
then be identified during surgery [9]. The method
proved to be of great use in patients with breast
carcinoma and those with melanoma [10,11].
The benefit for the patients was great because
many could be spared a regional lymphadenectomy
and the disfiguring arm oedema that sometimes
follows. In urology the dynamic SN procedure was
pioneered by Horenblas on men with penile cancer,
and it developed into a very reliable diagnostic
method [12].
The success in penile carcinoma may be attributed
to several factors. The tumour as injection site is
easily accessible. The first landing zone, the groin, is a
superficial area, so the SN procedure is a minor
operation. But most of all, the squamous cell
carcinoma of the penis never skips the lymph nodes
of the groin. Metastases elsewhere without a positive
lymph node in the groin are not seen, unless there is a
sarcomatoid component in the tumour [13].
Unfortunately, these factors are not present in
other urologic cancers. So a lymphadenectomy is still
considered the standard diagnostic procedure for
bladder and prostate carcinoma by many urologists.
Wawroschek showed the feasibility of the SN
procedure in patients with prostate carcinoma [14].
1.2.
Indications for assessment of the nodal status
The risk assessment of the likelihood of nodal
involvement and the practice to refrain from lymph
node dissection in the lower risk groups is in doubt
since the publication of incidence figures of node
involvement in the low-risk groups with extended
lymph node dissection [5,6]. The group of patients in
whom a node dissection can be omitted safely is
probably more limited than generally agreed in
recent years. Prostatectomy patients may have a
survival benefit from complete node dissection
[7,15]. In patients with a low nodal metastatic load
this may be simply due to the removal of all tumour.
There is also the statistical effect on survival in the
pN0 and in the pN+ groups by better allocation of
patients with micrometastases. For patients with
two or more nodes it might be mainly a prolongation
of their progression-free survival. (For a detailed
discussion, see Dhar et al [16].)
According to other experts, adjuvant hormonal
treatment is indicated in node-positive prostatectomy patients; N1 patients will then have almost the
same 10-yr cancer-specific survival as N0 patients,
but N2 and N3 patients will still do worse [17].
Another development that makes accurate staging important is the use of radiotherapy in
appropriate candidates. Since the introduction of
conformal radiotherapy, it is possible and profitable
to give very high doses to the prostate. However,
when the lymph node basins are to be radiated as
well, the radiation dose safely given to the prostate
is restricted. To make this type of treatment decision
a reliable assessment of the nodal involvement is
mandatory.
eau-ebu update series 5 (2007) 223–231
A study on outcomes of radiotherapy suggests
that patients will not benefit from adjuvant hormonal therapy in T1/T2, Gleason score < 7 if they have a
proven pN0 [18]. Three years of hormonal treatment
may be avoided in these patients by a reliable nodal
status assessment.
1.3.
Prognostic significance of the nodal status
Prostate-specific antigen (PSA), clinical tumour
stage, and Gleason sum score are already powerful
prognosticators. Several nomograms are available to
combine them and make reliable predictions of the
possibility for definite cure [19,20]. However, accuracy is 70–80% [21]. This may not appeal to the
patient as a tool to make major treatment decisions.
Thus, in many patients with an apparently organconfined cancer additional diagnostics are still
desirable. In a population-based study of men with
prostate carcinoma with pN+, M0, the majority on
conservative treatment, the cancer-specific survival
rate was 72% at 5 yr and the median survival was 8 yr
[22]. In this study, Gleason sum score tended to
make a difference in survival, but T category, PSA
level, or treatment did not affect the outcome.
In a cohort of patients treated with external-beam
radiation, the prognosis of N+ patients was much
worse [23]. The risk of dying of prostate cancer at
10 yr was 17% for N0 patients and 57% for N+
patients. A significant difference in survival was not
found between the N1, N2, and N3 patients, despite
225
extensive lymphadenectomy in the N1 and N2
patients. However, in this old series, the radiation
dose would be considered low these days. Studer did
find differences in tumour-specific survival between
patients with one, two, and more than two affected
nodes. After meticulous lymph node dissection and
prostatectomy, but without adjuvant therapy, the
median survival in patients with more than two
positive nodes was reached at 6 yr, but patients with
only micrometastasis had a 10-yr disease-specific
survival of 80% [14].
2.
Methods
Before surgery a radionuclide is injected in two to six portions
into the peripheral zone of the prostate, guided by transrectal
ultrasound. Injection in both lobes is important because each
prostate lobe drains mainly into the ipsilateral group of pelvic
lymph nodes [24]. The peripheral zone is the target; its
drainage pattern is not different from the other zones [25].
Several carriers of the radionuclide (99mTc) are in use.
Comparisons for prostate cancer have not been done as yet
(for a discussion, see Beri and Janetschek [26]) After 15 min,
scintigraphy is performed on the g camera and repeated after
2 and 4 h, to distinguish a ductectasy of a lymph vessel from a
real node and to decide which lymph nodes are first echelon
and which nodes are second echelon. After 4 h the pattern
does not change significantly [27]. Single-photon emission
computed tomography/computed tomography (SPECT/CT) is
an asset, providing additional anatomic information and,
according to some authors, increasing the yield of SNs [28]
(Fig. 1). Surgery is performed 5–20 h after injection. A g probe
Fig. 1 – Single-proton emission computed tomography/computed tomography shows anatomic details of the location of the
sentinel node and so facilitates the intraoperative detection (picture by R.A. Valdés Olmos, Netherlands Cancer Institute).
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eau-ebu update series 5 (2007) 223–231
is used in the radioguided surgery to locate the active nodes in
vivo and after excision is used ex vivo to confirm the node’s
activity and to separate it from adjacent fatty tissue or other
nodes, and finally to check the operation field for residual
activity.
When the method is introduced in a practice, a confirmatory extended node dissection is highly recommended in the
beginning, to get the logistics right and to make sure the
method is properly performed [29]. This is necessary because
several choices must be made in terms of equipment,
materials, and methods. Communication between the nuclear
medicine department and the performing urologist must meet
high standards, because hygienic rules of radiography need to
be applied and decisions on the location of first-echelon nodes
must be discussed.
3.
Results
3.1.
Validation
The pioneers of the SN dissection for prostate cancer
have performed an additional extended lymph node
dissection so they could show the reliability of this
method [14]. The false-negative rate is very low
when compared to the gold standard, the extended
pelvic lymph node dissection; in the largest series
only two negative SNs were found in 207 patients
with positive nodes [30].
Additional evidence of the reliability of the
laparoscopic SN method is found in the fact that
the diagnostic yield is twice as high compared to old
pelvic node dissection series and identical to
modern series of open extended pelvic lymph node
dissection [26].
3.2.
Anatomic considerations
SN research will answer the question which nodes
are affected first of all. Careful documentation of
extensive lymph node resection series will answer
the question in which tumour stages excision of all
tumour-bearing nodes is necessary to cure the
patient and which areas must be covered. To
describe the location of SNs and to communicate
the extent of an extended resection, agreement
must be reached on the nomenclature. Unfortunately, the literature seems to lack generally
agreed-on definitions of the boundaries of the
lymph node-bearing areas in the pelvic region.
Surgical atlases give a rather vague description and
leave room for interpretation. An example is shown
in Fig. 2, where two acknowledged authorities seem
to place the obturator lymph node area in different
places [6,31].
As the anatomic regions are defined currently, it
does not necessarily mean that the whole of that
Fig. 2 – Two acknowledged authorities seem to place the
obturator lymph node area in different places. This
illustrates the need for unequivocal definitions of the
involved anatomic sites [6,30]. (a) Extend of lymph node
dissection performed; (1) external iliac, (2) obturator fossa
(3) internal iliac (hypogastric). (b) The field of dissection:
Region 1, paracaval; Region 2, interaortocaval; Region 3,
paraaortic; Regions 4 & 5, common iliac; Regions 6 & 7,
external iliac; Region 8, intercommon iliac (presacral);
Regions 9 & 10, obturator; Regions 11 & 12, internal iliac.
particular area is relevant for the specific aim to find
affected lymph nodes. Indeed, the SNs were found to
cluster around the bifurcation of the internal and
external iliac artery, thus involving parts of the
obturator fossa, the external iliac, the internal iliac,
and communal iliac regions [27] (Fig. 3). This notion
that not the whole of these regions may be relevant
has been expressed before: ‘‘in a high proportion of
patients a SN was located along the initial centimetres of the hypogastric artery’’ [32].
The distribution of positive lymph nodes as
reported in various SN series are shown in
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Fig. 3 – Positive sentinel nodes (SNs) cluster around the iliac
bifurcation and are not scattered throughout the several
anatomic sites [27]. The right side is the location of the SNs
that contained prostate cancer; on the left side are the
negative SNs.
Table 1. Often more than one region is involved, so
this is a calculation from the original publications
[33–35]. The obturator fossa, together with the
internal and external iliac regions, accounts for
91% of the tumour-positive sentinel lymph nodes.
This agrees nicely with the definition of an extended
lymph node dissection as proposed by Burkhard and
Studer [36].
So the obturator fossa, the external iliac, the
internal iliac, common iliac, the presciatic, and the
presacral areas are all known to harbour nodes that
might be the first landing zones of prostate
carcinoma. The clearance of all these regions is a
major undertaking (Fig. 4). For most urologists this is
only justified when this manoeuvre makes the
difference for definite cure. Until new imaging
techniques can guide us, the borders of the extended
node dissection will necessarily be arbitrary.
3.3.
Complications
In a previous issue of the European Association of
Urology update series it was argued from the
Fig. 4 – An extensive node dissection, involving the
presacral area and the para-aortic nodes up to the inferior
mesenteric artery is a rather large operation. Most authors
define their extended lymphadenectomy template smaller
(picture by the audiovisual department, Netherlands
Cancer Institute).
literature that an extended pelvic node dissection
has a complication rate not different from the
limited dissection [37].
However, since then several papers have documented a higher complication rate. Briganti et al in
their paper on 963 patients report a complication
rate of 19.8% for an extended open lymph node
dissection, more than twice what they report for
dissection of fewer than 10 nodes [38]. Clark and
coworkers did a limited dissection on one side and
an extended dissection on the other side on the
same patients and found three times as many
complications on the extended side [39]. The
majority of complications were related to the
development of lymphoceles.
In our own experience we did not see an increase
in complications when we performed extended
pelvic lymphadenectomy in (open) cystectomies,
but in our laparoscopic diagnostic extended dissections we experienced an unacceptable complication
rate of 23% [27].
Table 1 – Distribution of positive lymph nodes as reported in various sentinel node series
Weckermann et al [33]
Obturator fossa
Internal iliac
External iliac
Common iliac
Presacral
Other
Presacral or other
24%
38%
27%
—
—
—
10%
Jeschke et al [34]
32%
29%
40%
0%
0%
—
—
Often more than one region is involved, so calculations are from the original publications [33–35].
Corvin et al [35]
43%
20%
12%
13%
12%
—
—
Mean
32%
29%
30
—
—
—
—
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Beri and Janetschek reported a 35.3% rate of
procedure-related complications from the laparoscopic extended lymph node dissections, whereas
for the laparoscopic SN procedure they found only
an 0.8% rate of complications [26].
3.4.
Contraindications
Patients with a history of transurethral resection of
the prostate (TURP) had a 20% chance of an
undetectable SN in one series [33]. Recent acute
prostatitis (eg, after prostate biopsies) is a contraindication for the intraprostatic application of the SN
tracer [34].
4.
Discussion
Especially authors from the United States and
Australia challenge the need for anything more
than a limited lymph node dissection in combination with a retropubic prostatectomy. Their main
arguments are the additional costs, the complications involved, and the low yield in their experience
(3.2% for Clark et al [39] and 2.4% for Garret et al [40]).
The great difference with the European findings of
much higher incidence figures of nodal involvement
is not yet fully explained.
4.1.
Advantages of the SN procedure compared to an
extended node dissection
prostatectomy, the extended lymphadenectomy
does not increase the number of complications in
high-volume series [5,36].
When the SN procedure reveals a minor lymph
node involvement and cure is still the aim, an
additional extended lymphadenectomy is needed
[30].
4.3.
If a laparoscopic prostatectomy is performed, the
combination with a laparoscopic SN procedure is
the logical combination. The open and the laparoscopic SN procedures have the same diagnostic
yield, but comparisons are not made [26]. The
advantages and disadvantages of a laparoscopic
procedure compared to an open procedure are the
same as in any procedure. Especially patients
opting for an external-beam radiation treatment
have much to gain by a laparoscopic procedure
[35].
4.4.
Future developments
4.4.1.
Treatment strategies
As in other cancers, treatment strategies will be
developed with (neo) adjuvant drugs other than
hormones. The evaluation of the necessary studies
will be more effective with stratification for the
nodal status.
4.4.2.
An SN dissection involves less dissection and may
have a lower complication rate [26]. In 5–10%
positive lymph nodes may be found outside of the
extended lymphadenectomy area (Table 1). In SN
techniques the nodes are presented one by one and
often will be scrutinised with immunohistochemistry techniques in addition to routine microscopy
[41]. This will improve the diagnostic accuracy.
Especially when the patient is to undergo externalbeam radiation treatment or a perineal prostatectomy, this less invasive procedure has its merits.
When the laparoscopic SN techniques develop into a
widely available technique with a low complication
rate, the discussion on the sense or not of assessment of the nodal status in low-risk groups may be
settled in the future.
Open or laparoscopic?
Imaging techniques
Recent developments in imaging techniques will
enable us to identify lymph nodes that are very
suspicious of harbouring micrometastases. (This is
a node with a tumour of <2 mm diameter [42].)
Aspiration biopsy is rather likely to be false
negative in such a case. This will make a confirmatory excision of such a lymph node mandatory (and preferably in the least invasive way).
Positron emission tomography/CT (PET/CT) will not
reveal micrometastases with the present technique
[43].
4.4.3.
Innovations
Innovations, such as the handheld g camera, to be
used during the SN operation, will make the
(laparoscopic) excision of a SN easier and even
more reliable.
4.2.
Disadvantages of the SN procedure compared to an
extended node dissection
4.4.4.
It is a technically demanding procedure, especially
the laparoscopic SN procedure. It involves high-tech
equipment and skills. Combined with a retropubic
Innovative imaging techniques will point to lymph
nodes suspicious of harbouring micrometastases.
When aspiration biopsy is negative, a minimal
invasive excision technique, preferably image-
Future perspectives
eau-ebu update series 5 (2007) 223–231
guided, will be sensitive enough to confirm this
suspicion or will prove that the patient is node
negative. The necessary extent of the node dissection with curative intent will be based on imaging
techniques. When the situation is judged to be
beyond definite cure, adjuvant treatment decisions
will be based, among other relevant information
such as molecular tumour characteristics, on the
nodal status and not on a best guess according to
nomograms.
[13]
[14]
[15]
Conflicts of interest
[16]
The authors have nothing to disclose.
[17]
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CME questions
Please visit www.eu-acme.org/europeanurology
to answer these CME questions on-line. The CME
credits will then be attributed automatically.
1. In prostate carcinoma, lymph nodes outside of
the obturator fossa
A. Are as often involved as the nodes inside of the
fossa.
B. Are second-echelon nodes.
C. If positive, indicate an urgent need for hormonal treatment.
D. Are recognised as relevant only since the last
decade.
2. The presence of prostate cancer in multiple
lymph nodes in cM0 patients,
A. Indicates death within 5 yr.
B. Makes immediate hormonal treatment mandatory.
C. Makes an extended lymph node dissection
mandatory.
D. Is of more prognostic significance than initial
serum prostate-specific antigen value.
3. The presence or absence of microscopic lymph
node metastases in prostate carcinoma
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A. Can be detected with the sentinel node
procedure.
B. Can be detected with the sentinel node procedure and with a computed tomography scan.
C. Can only be detected with a 3-Tesla magnetic
resonance imaging scan.
D. Can be detected with the sentinel node
procedure, as well as with magnetic resonance imaging, as well as with a positron
emission tomography scan.
4. The dynamic sentinel lymph node dissection is
preferable to an extended lymph node dissection
because
A. It is easier to perform.
B. It is more accurate.
C. There is level A evidence it causes fewer
complications.
D. Not true, it depends on the clinical context.
5. The dynamic sentinel node technique
A. Is scientifically speaking interesting, but of
little practical use.
B. Always needs to be followed by an extended
lymphadenectomy.
C. Makes an extended lymphadenectomy unnecessary in the majority of patients.
D. Was invented by Cabanas.
eau-ebu update series 5 (2007) 223–231
6. The extended lymph node dissection, according
to most authors, involves:
A. Obturator fossa, external iliac nodes, internal
iliac nodes, presciatic nodes, presacral nodes,
and the common iliac nodes.
231
B. Obturator fossa, external iliac nodes, internal
iliac nodes.
C. Obturator fossa, external iliac nodes, internal
iliac nodes, presciatic nodes.
D. Obturator fossa, external iliac nodes.