10-Year experience regarding the reliability and morbidity of radio guided lymph node biopsy in penile cancer patients and the associated radiation exposure of medical staff in this procedure
Lützen et al. BMC Urology
10-Year experience regarding the reliability and morbidity of radio guided lymph node biopsy in penile cancer patients and the associated radiation exposure of medical staff in this procedure
Ulf Lützen 0 1
Carsten Maik Naumann 0 3
Jens Dischinger 2
Marlies Marx 1
René Baumann 4
Yi Zhao 1
Michael Jüptner 1
Daniar Osmonov 3
Katrin Bothe 3
Klaus-Peter Jünemann 3
Maaz Zuhayra 1
0 Equal contributors
1 Department of Nuclear medicine, Molecular Imaging Diagnostics and Therapy, University Hospital Schleswig Holstein , Campus Kiel, Kiel , Germany
2 Northern German Seminar for Radiation Protection gGmbH at the Christian-Albrechts-University Kiel , Kiel , Germany
3 Department of Urology and Pediatric Urology, University Hospital Schleswig Holstein , Campus Kiel, Kiel , Germany
4 Department of Radio Oncology, University Hospital Schleswig Holstein , Campus Kiel, Kiel , Germany
Background: The guidelines of the European Association of Urologists (EAU), of the German Society of Nuclear Medicine (DGN), and the European Society for Medical Oncology (ESMO) recommend sentinel lymph node biopsy (SLNB) for lymph node staging in penile cancer with non-palpable inguinal lymph nodes as one diagnostic method. Despite this, the method is neither widely nor regularly applied in Germany - the same applies to many other countries, which may be due to insecurity in dealing with open radioactive tracers. This study aims to assess the reliability and morbidity of this method, as well as the associated radioactive burden for clinical staff. Methods: Between 2006 and 2016, 34 patients with an invasive penile carcinoma and inconspicuous inguinal lymph node status underwent SLNB in 57 groins after application of a radiotracer (Tc-99 m nanocolloid). We collected the results prospectively. The reliability of the method was assessed by determining the false-negative rate. In addition, we evaluated complication rates and determined the radioactive burden for the clinical staff both pre- and intraoperatively. Results: SLNB was performed in 34 patients with penile cancer with non-palpable inguinal lymph nodes in 57 groins. In two patients inguinal lymph node metastases were detected by means of SLNB. In one patient recurrent inguinal lymph node disease was found after negative SLNB in both groins. Thus, the false negative rate was 3.13 % per patient (1/32 patients) and 3.51 % per groin (2/57 groins). The morbidity rate was 2.94 % per patient (1/34 patients) and 1.75 % per groin (1/57 groins). Radiation exposure for the clinical staff during this procedure was low at a maximum of ca. four μSV per intervention. Conclusions: SLNB is a reliable method with low morbidity that is associated with a low radiation burden for clinical staff. Due to the enhanced methodological and logistic demands, this intervention should be performed in specialized centres and in an interdisciplinary approach.
Penile carcinoma; Sentinel lymph nodes; Lymph node staging; Tc 99 m-nanocolloid; Radiation exposure; Sentinel lymph node biopsy; SPECT/CT
Application of Tc-99 m-labelled nanocolloid for
preand intraoperative imaging of the sentinel lymph
nodes (SLN) is a fully established standard method in
malignant melanoma and breast cancer, both in
Germany and internationally, and it is rooted firmly
in the national and international guidelines of expert
For penile cancer, the European Association of
Urologists (EAU), the German German Society of Nuclear
Medicine (DGN), and the European Society for Medical
Oncology (ESMO) also recommend sentinel lymph node
biopsy (SLNB) in invasive primary tumours with a
moderate degree of differentiation and non-palpable inguinal
lymph nodes [
]. The former EAU categorization of
the penile carcinoma as high-risk, intermediate-risk and
low-risk is no longer in use [
In some few countries like the United Kingdom and
the Netherlands, SLNB using open radioactive nuclides
is an established and widely used procedure for penile
cancer. In other countries like Germany, this procedure
is neither regularly nor widely used. Despite the fact that
urologists frequently deal with ionizing radiation from
other sources, there is a lack of familiarity with the
technique and the high methodological demands of
SLNprocedures, therefor this could be one reason. A further
cause could lie in former publications stating unreliability
of the method of up to 15 % [
The aim of this prospective study is to establish both
the reliability and the morbidity associated with SLNB
after radio-labelling of sentinel lymph nodes with Tc-99
m nanocolloid. In addition, we aim to determine and
assess the radiation burden for clinical staff resulting
from the application of this method, and to compare it
to similar procedures in other tumour entities.
Being a university-based cancer center, we treat all types
of penile cancer, as well as other tumour entities in an
interdisciplinary team. Out of all patients who suffer
from an invasive penile carcinoma and were assigned to
our center by regional and national physicians, only
those with non-palpable inguinal lymph nodes – this
being the only pre-selection criterion – were included in
this study in the period 2006 to 2016. During this
period, 34 patients with an inconspicuous inguinal
lymph node status in 57 groins were included in this
study. 23 patients showed non-palpable inguinal lymph
nodes bilaterally, 11 patients only unilaterally. The latter
patients presented palpable inguinal lymph nodes in the
contra lateral groin in the physical examination. All
groins without palpable inguinal lymph nodes
underwent SLNB with Tc-99-labelled nanocolloid, regardless
of the palpation status in the contra lateral groin. The
applied tracer was a pure gamma emitter with a half-life
of six hours and energy of 141 keV.
All patients included in this study underwent initial
preoperative physical screening, including palpation and
additional ultrasound examination of the inguinal region.
Preoperative cross-section images via magnetic resonance
imaging (MRI) and computer tomography (CT) of the
pelvic region, including the inguinal region, were not
The median age of the patients was 63.5 (34–84) years.
The details of the malignant disease, the tumour
characteristics as well as the SLN diagnostic results and the
results of the follow-up are presented in Table 1.
Nuclear medical imaging of SLN was done following
a-two-day protocol [
]. On the preoperative day, the
patients received an intradermal peritumoural injection
of the radio tracer under local anesthesia (Fig. 1). We
applied an overall activity of 150 MBq, Tc-99 m-labelled
nanocolloid. We performed lymphatic drainage
scintigraphies in several projections (at least four): at the
earliest on the injection day at least one hour p. i., − or, in
the case of lacking or retarded lymphatic drainage, on
the morning before the surgical intervention. For
indirect body contouring, the emission measurements for
generation of planar images were performed additionally
by means of a Co-57 planar source (Fig. 2). Image
acquisition was done with a twin head gamma camera
(Siemens, ECAM and Symbia T).
In addition we performed single-photon-emission
computed tomography/computed tomography (SPECT/
CT) of the lower abdomen, the pelvic abdomen and the
inguinal region with a twin head SPECT/CT-hybrid
camera (Siemens, Symbia T and Symbia Intevo). CT-data
were acquired in a so-called low-dose technique. The
scans of the functional imaging were fused with the
coregistered CT-scans (Fig. 3). In this context,
morphological imaging enabled attenuation correction of the
emission data on the one hand, as well as easier
anatomical allocation of the radio-marked lymph nodes,
thus facilitating better surgical planning, on the other.
Subsequent to the imaging process, we identified and
marked the SLN by means of a Co-57 pen as well as a
felt-tip pen on the skin surface. In addition we
performed a perilesional intradermal injection of patent
blue immediately before the surgical intervention.
Intraoperatively, the SLN were identified both visually, via the
blue hue accrued in the lymph nodes, as well as by
measuring the radioactivity by means of a gamma probe.
In the case of preoperative non-visualization of radioactive
labeled lymph nodes in scintigraphy the day before
surgery, an intraoperative exploration, augmented by the
gamma probe, was done the following day. All detectable
radioactive-labeled, blue stained as well as clinically
suspicious lymph nodes that were not detected by preoperative
physical examination (e.g. due to obesity) were removed
as recommended [
Each enrolled patient of this study received a
prophylactic antibiotic therapy as a single shot application of
cephalosporin prior to surgery. Incisions of approximately four
cm were made for extirpation of the lymph nodes,
following the relaxed skin tension lines. All patients were
provided with drains at the end of surgery. The drains were
left until the flow-rate was equal or smaller than 20 ml per
24 h. The mean respectively median operation time was
130.3 min respectively 120 min. On average, 3.2 lymph
nodes (median 2/range 1–11) per patient were resected.
Neither compression bondages nor stockings were
applied. The mean, respectively median length of the
postoperative hospitalization was 5.6, respectively 5.0 days.
Histopathological examination of the entire SLNs was
done in 100 micrometer (μm) sections under additional
hematoxylin-eosin staining. In case there was evidence of
positive SLNs with malignant tumour cells, we performed
a radical lymphadenectomy (LAE) in a two-stage surgical
intervention in the affected inguinal region and if
necessary a systemic cytotoxic therapy. In our cohort, inguinal
LAE was necessary in two cases. In one case, chronic
lymphedema of the lower extremity resulted. In the
other case, there were no unexpected events in terms
Three different urologists performed the
SLNBprocedures. Preoperatively, also three different nuclear
medicine physicians performed the applications of the
radioactive tracer. Morbidity and disease-free survival
(DFS) after SLNB was evaluated during clinical
outpatient follow-up examinations.
As a reference standard, a negative groin was defined
as a histologically negative SLN status and uneventful
follow-up without nodal recurrence. A positive groin
was defined as a histologically positive SLN status or
lymph node recurrence during the follow-up period.
Based on this definition, we compared SLNB to the
reference standard of follow-up examinations. Follow-up
was done in the same way in all histologically negative
SLN-patients i.e. by physical examination, including
inguinal node palpation of the groins in three-monthly
intervals for the first two years, every four months in
year three and in six-monthly intervals in the fourth and
fifth year after diagnosis.
For assessment of the radiation exposure of the
involved medical staff in this procedure, we performed
both pre- and intraoperative measurements. To this end,
we applied a dose rate meter (Berthold, LB123 and
Berthold, TOL F) to measure the dose rate (DR) and
the time needed for each procedural step. Using these
two measured parameters we calculated the effective
dose and the hand dose of the involved staff. As a control
we used an additional digital personal dosimeter
(Polimaster, PM1621MA) for determination of the
effective dose of the surgeon. During the measurements, the
digital personal dosimeter was placed in the breast pocket
of the surgeons’ shirt. Prior to radiation measurements
during the SLN-procedures, the background radiation in
all rooms was determined and subtracted. In view of the
fact that the lower detection limit of the
thermoluminescence ring dosimeter (TLD) of fingers is >100 μSv, we
abstained from using TLD finger rings during pre- and
intraoperative measurements. TLD is only of limited use
due to the low applied activity and the required pre- and
intraoperative times during the procedure, and it is
inferior to measurement via sensitive dose rate meters. The
assessment comprises the following: preoperatively, the
identification of dose values for the staff from nuclear
medicine, and intraoperatively, that for anesthetists,
surgical staff and the surgeon, taking into account the required
time span, the distance to the radiation source, and the
intensity of applied activity.
Prior to the procedure, all patients were duly informed
about the details of the measures and gave their written
informed consent for this guideline-conform procedure.
In addition, the study was approved by the Ethics
Committee of Kiel University (AK D 426/07).
Reliability and morbidity
In two patients, metastatic disease in the SLN was
proven by means of SLNB with subsequent histological
examination (Table 1). There were no false-positive
results. In one patient, bilateral recurrence of inguinal
lymph node metastases was diagnosed four months after
histologically negative SLNB. After clinical suspicion of
the inguinal lymph node recurrence a bilateral inguinal
LAE was conducted. The mean resp. median
diseasefree survival of patients with a negative SLN result was
52.26 resp. 51 (4–109) months. One patient died from
the consequences of a stroke ca. five months after the
intervention. A further patient died from the
consequences of a renal cell carcinoma ca. twelve months
after treatment of penile carcinoma. All other patients
were examined as part of the regular follow-up.
The current data, which covers a period of ten years,
shows a false-negative rate of 3.13 % in relation to the
number of patients (1/32 patients) and 3.51 % in relation
to number of investigated groins (2/57 groins).
Assessment of morbidity after SLNB alone showed one case of
a prolonged inguinal lymphorrhea, which disappeared
spontaneously by leaving the intraoperatively placed
drain. SLNB-associated morbidity was thus calculated
as 2.94 % per patient (1/34 patients) and 1.75 % per groin
The patient who had a false-negative SLNB result
during follow-up had a rather unusual clinical course
and deserves special attention. In this patient, SLNB was
performed during a secondary resection, i. e. after
resection of the primary tumour ex domo with an unclear
resection status. Despite a unilaterally unsuccessful
visualization of a radio-labelled SLN, we performed
follow-up investigations on the basis of the T1 stadium
diagnosed ex domo and the G1 differentiation as well as
a R0 resection according to the guidelines. Unfortunately
in this case tumour specimens were not available for our
pathologists for re-evaluation.
During a sonographic follow-up examination four
months after surgery, we found a bilateral lymph node
recurrence, which was successfully resolved by surgical
intervention as mentioned above. The patient has been
disease-free during further follow-up.
Based on cross-counting (Table 2) and chi-square test
we calculated for SLNB a sensitivity of 66.67 % and a
specificity of 100.00 %, with a 95 % confidence interval
(CI) of 9.5 to 99.2 % (sensitivity) respectively of 88.8 to
100.0 % (specificity).
Radiation exposure of involved staff
Table 3 shows the pre- and intraoperatively measured
mean DR of the applied radioactivity at various distances
to the radiation source.
In consideration of the measured exposure time of
45 min with a mean distance of 30 cm to the patient
prior to resection of the primary tumour, and a exposure
time of 120 min after resection of the primary tumour, we
calculated a mean effective dose for the surgeon of ca. four
μSv per patient (2.2 μSv/h × 0.75 h + 1.1 μSv/h × 2 h),
based on the measured mean dose rate values presented
in Table 2. The mean effective dose for the surgeon as
controlled by the digital dosimeter is ca. 4.06 μSv for the
entire surgical intervention. The values thus concur
closely with the estimated values.
Table 2 Cross-table of the results of SLNB and follow-up and of
Results of SLNB and follow-up (n)
Histo. positive Histo. negative
true positive false positive
all true findings all false findings all findings
3 31 34
The mean hand dose of the surgeon is calculated to be
ca. 18 μSv per patient (20 μSv/h × 0.75 h + 1.5 μSv/h ×
The surgical staff can keep a distance of at least 50 cm
to the patient resp. the surgical area during the entire
procedure. In the worst case, this can result in a mean
effective dose of 0.98 μSv per patient (0.5 μSv/h × 0.75 h +
0.3 μSv/h × 2 h) for these persons. The hand dose is
Table 4 shows a summary of the mean pre- and
intraoperative radiation exposure for the clinical staff as has
been measured or estimated above for penile carcinoma
SLNB, in comparison with the mean dose values that
apply in malignant melanoma or breast cancer SLNB
Reliability and morbidity
The indication for an LAE in penile carcinomas has
been under controversial discussion for many years,
especially with respect to clinically and sonographically
inconspicuous inguinal lymph nodes [
]. The degree of
metastatic spread and the respective appropriate
therapeutic management have a significant impact on patient
survival. Classic inguinal LAE is associated with a
substantial morbidity rate of up to 87.5 % according to the
literature (e. g. wound healing problems, generation of
seroma or lymphorrhea, etc.) [
Only 20 to 25 % of patients with clinically negative
inguinal lymph node status harbour occult metastases.
By reverse logic, this means that ca. 75 to 80 % of
patients with clinically inconspicuous inguinal lymph
nodes undergo the increased of morbidity risk going
through this surgical intervention in vain. A tentative
watchful waiting approach, however, involves a high risk
of tumour-related mortality. Results from the literature
show that resection of metachronous, clinically evident
metastases during follow-up procedures significantly
diminishes the long-term survival chances of these
patients, compared to immediate resection of occult
metastases, from 84 to 35 % [
]. Thus we did not
choose the tentative approach in the patients included in
Alternative, non-invasive functional and morphological
imaging procedures such as positron-emission
tomography/computed tomography (PET/CT) or MRI and CT
alone do not have sufficient sensitivity in patients with
clinically inconspicuous inguinal lymph node status
Effective Dose E [μSv] Organ-dose of the
hands Hhands [μSv]
]; they are not seen as useful and have thus not
been used as obligatory imaging tools in this study.
EAU guidelines recommend performance of SLNB in
penile carcinomas with a tumour stadium ≥ T1G2 and
non-palpable inguinal lymph nodes (cN0) [
SLNlabelling with radioactive tracers is not available, the
guidelines alternatively recommend a fine needle
aspiration biopsy (FNAB) of the inguinal lymph nodes with
subsequent cytopathological examination.
Regarding FNAB, however, the low sensitivity of only
39 % in penile cancer has to be taken into consideration
]. A further alternative is to base the treatment
strategy on individual risk factors [
]. A decision in favor or
against inguinal SLNB based on risk factors like tumour
stage and/or tumour differentiation for metastatic risk
assessment involves substantial uncertainties. All
patients with proven or clinically evident invasive penile
cancer without palpable inguinal lymph nodes
underwent SLNB. In case of uncertainty concerning the
invasiveness of the tumor, we performed preoperative
radioactive lymph node labeling including scintigraphy.
SLNB was only performed if rapid frozen section during
surgery showed at least a T1-carcinoma. However, the
reliability of histopathological tumour grading based
solely on rapid frozen section is unclear and has not
been described in literature yet. Even paraffin-embedded
specimens show a high degree of inter-observer
variability among pathologists with respect to tumour staging
and tissue differentiation [
]. Taking these facts into
account, we accepted a possible over
diagnosis/-treatment in a very low number of patients with
T1G1tumours by SLNB. As mentioned before, the remarkable
thing was that the only relapse due to a false-negative
SLNB-procedure was proven in a patient with a
T1G1disease, who had undergone primary surgery ex domo.
For this reason, we performed SLNB in each invasive
carcinoma of this entity.
The results from our study show that SLNB after
radio-labelling with Tc 99 m-nanocolloid is a reliable
method for lymph node-diagnostics.
The false-negative rate of 3.13 % in relation to the
number of patients (1/32 patients) and 3.51 % in relation
to number of investigated groins (2/57 groins) is
comparable to that of the results of the Dutch workgroup
around Leitje et al. [
], but significantly better than the
results of the Swedish workgroup around Kirrander et
], whose false-negative rate was 15 % in a study
published in 2012. In the aforementioned Dutch study
the false-negative rate was seven percent [
]. In the
study by Leitje et al. the results are based on the number
of the examined inguinal regions and have not been
calculated per patient as in our study. The Dutch study
observes that the metastases rate of ten percent is
comparatively low, which implies the question whether the
high logistic and methodic demands of SLNB with
radioactive nuclides can be justified.
Compared to other studies e.g. Lam et al. [
Kroon et al. [
] who report rates of 28 respectively 22 %
of histologically positive lymph nodes under employment
of SLNB, our rate of metastatic disease is lower. The
reason might be that the patients enrolled in the study of
Lam et al. had a significantly higher risk of metastatic
disease, as can be seen in the lower number of T1-tumours
(42 %) compared to our study (56 %). More importantly,
the study of Lam et al. included a higher rate of
G3tumours (53 %). In our study the G3-tumour rate is only
18 %. Moreover, the study by Kroon et al. included only
patients with T2- and T3-tumours, while T1-tumours
were not taken into account, in contrast to our study.
These facts and the criteria leading to the low number of
primarily positive lymph nodes using the SLNB-procedure
might be responsible for our statistical results of
sensitivity, specificity, and the 95 % CI. Although our study
includes a large patient cohort compared to other German
studies, the number is rather small by international
]. It is well possible that higher rates of metastases
are found in larger patient cohorts in the future.
The following consideration shows the clinical
implication of radio-labelled SLNB: in the current study, we
were able to prove a negative nodal status by SLNB with
sufficiently long follow-up periods in 31 patients.
Based on the now obsolete risk classification stated in
the 2004 EAU-guidelines [
], 19 high-risk patients
would have undergone obligatory LAE and further 13
intermediate-risk patients would have been candidates
for a facultative classic inguinal LAE without any further
diagnostic gain. In this context it has to be mentioned
that the patient who had a bilateral inguinal lymph node
recurrence after negative SLNB was a low-risk patient
(T1G1/Table 1) and was diagnosed and underwent R0
resection ex domo where SLNB was not indicated.
Unfortunately, tumor specimens were not available for
reevaluation by our pathologist.
Based only on the SLNB result, we were able to
spare these patients the severe morbidity associated
with classic inguinal LAE while guarding diagnostic
safety. As a consequence we were able to reduce
morbidity in our patient cohort to 2.94 % per patient
(1/34 patients) and 1.75 % per groin (1/57 groins) by
In view of the results of our study, especially the case
of the patient who underwent ex domo surgery of the
primary tumour, the question arises whether SLNB after
application of radioactive lymphogenic tracers can also
be safely applied as a secondary intervention, i.e. after
resection of the primary tumour.
Graafland et al. [
] performed a metachronous SLNB
in 40 patients after earlier resection of the primary
tumour. The reported results of a two-stage procedure
are comparable to those of primary SLNB.
Our results cannot be used to confirm the findings by
Graafland et al. as we encountered lymph node
recurrence after a false-negative SLN-procedure four months
after secondary SLNB during follow-up. In the currently
described patient collective after primary SLNB the
false-negative rate is zero percent.
Risks and benefits of SLNB and classic inguinal LAE
As mentioned the morbidity of a classic inguinal LAE is
as high as 87.5 % [
]. Due to the fact that lymph
node metastases can only be proven in ca. 20 to 25 % of
patients with clinically non-palpable inguinal lymph
nodes , this treatment later reveals itself to have been
unnecessary in 75 to 80 % of these patients.
As already stated, the Dutch workgroup around
Horenblas, like some other workgroups, reported false
negative rates of approximately 15 % during the early
implementation phase of the SLNB-procedure [
Data from an analysis by Neto et al. require a critical
view . These comprise studies examining the results of
SLNB including patients with palpable inguinal lymph
nodes. SLNB is not recommended by the expert society
guidelines in patients with palpable inguinal lymph nodes
due to its high unreliability [
]. In our study, we could
show excellent reliability of SLNB, with a false negative
rate of only 3.51 % (2/57) per groin respectively 3.13 %
(1/32) per patient. Like us, Lam and coworkers report
a false negative rate of 5 % (in relation to the groins)
respectively 6 % (in relation to the patients) in a cohort of
264 patients. The faulty procedures occurred mainly
during the implementation of the method [
the false negative rates of classic inguinal LAE for staging,
no data in the literature are available yet.
One of the limitations of SLNB might be that tumour
cells can lead to obstruction or occlusion of the
lymphatic drainage pathways and can either cause a complete
blockage or a rerouting of the radio tracer [
aspect can lead to restraints of SLNB. The risk of a
relevant modification of lymphatic and thus tracer drainage
depends on the metastatic load in the lymphatic
pathways and in the lymph nodes. The risk of lymph node
metastases in patients with palpable lymph nodes is
about 50 % and therefore much higher than in those
with an inconspicuous inguinal lymph node status during
palpation of the groins (20 to 25 %). For this reason,
expert society guidelines do not recommend SLNB in
patients with palpable inguinal lymph nodes, as has been
mentioned before .
The validity of clinical groin palpation within the
physical examination is influenced by the physical
constitution of the patient on one hand, and by the experience
of the examiner on the other. In our study, one patient
developed a bilateral lymph node recurrence four
months after histologically negative SLNB. The
assessment of the inguinal lymph node status was impeded by
corpulence. Obesity is capable of veiling otherwise
palpable and potentially tumour-infested lymph nodes, thus
wrongly leading to the conclusion that the patient is
eligible for SLNB, which presents another limitation of
this staging procedure. This risk of misjudgment could
be minimized by preoperative sonography of the groins,
as a supplement to clinical palpation.
As mentioned, a further possible source of errors in
the application of this procedure is associated with the
two-stage approach of SLNB after surgical removal of
primary tumour. While Graafland et al. [
uniform results in 40 cases of a metachronously performed
SLNB, we believe that surgery-related modifications of
the tracer drainage, e.g. through scar formation or edema,
might be a reason for the false-negative SLNB in one
patient of this study.
Radiation exposure of the involved staff
German radiation protection laws prescribe that any
indication for the application of ionizing radiation, also
that of open radioactive nuclides, is mandatorily bound
to a medical indication identified by a physician with the
necessary expertise [
]. Thus the resulting benefit of
this procedure for the patient outweighs the potential
risk of ionizing radiation.
Based on the specifications of the German radiation
protection commission (Strahlenschutzkommission, SSK),
we have calculated an effective dose of 0.5 to 1.5
Millisievert (mSv) in patients undergoing the SLN procedure
according to a so-called two-day protocol under application
of the above-described tracer with an activity of 150 MBq
]. Our dosimetric calculations fit to the data from
the literature. Application of an additional low-dose
CT in the pelvic region leads to an additional
effective dose of 1–2 mSv [
]. We were able to confirm
this by our calculations (CT Expo Version 2.4/2015/
G. Stamm, H. D. Nagel).
According to our measurements and calculations, the
effective dose for the nuclear-medical staff of 0.5 μSv
(nuclear medicine technologists) resp. 1.5 μSv (nuclear
medicine physicians) is relatively low, which is owed to
the fact that preoperative application of the tracer,
despite its high radioactive load of 150 MBq, requires little
time, and thus makes the exposure time much shorter
than the intraoperative exposure. The effective dose
values for the nuclear medical staff are comparable to
those occurring during application of this kind of
procedure in other tumour entities like breast cancer
or malignant melanoma.
Compared to other procedures in nuclear medicine,
sentinel lymph node diagnostics with radioactive tracers
is associated with a relatively low radiation burden for
the nuclear medical staff.
Physicians and technologists in nuclear medicine are
allowed to be exposed to radiation by profession and are
as such allocated to at least Category B with a maximum
effective dosage of 6 mSv (6000 μSv)/a and a maximum
hand dosage of 150 mSv (150000 μSv)/a. If the nuclear
medicine physician was to only perform this kind of
procedure, up to 4000 procedures per year would be
eligible. If the nuclear medicine expert was allocated to
category A of professional radiation exposure, maximum
eligible effective dose would even be 20 mSv/a with a
maximum hand dose of 500 mSv/a [
In this tumour entity, organ-preserving surgical
resection of the primary tumour can be technically
demanding and time-consuming. Thus the surgeon is the person
with the highest effective dose exposure as shown by our
pre- and intraoperative measurements (maximum of ca.
four μSv per patient).
Compared to other tumour entities, the effective dose
for the surgeon of penile carcinoma is higher (Table 3).
This is due to the fact that more time is required in
penile cancer surgery, − i.e. for the preparation of the
primary tumour and subsequent functional
reconstruction of the urethra -, compared to resection of malignant
melanoma in unproblematic localizations or
mastocarcinoma resection including the SLN; this considered, the
radiation exposure time in penile cancer is longer.
Surgical staff including urologists is not classified as
“radiation-exposed by profession” and is eligible for
exposure up to a maximum effective dose of 1 mSv (1000
μSv)/a and a maximum hand dose of 50 mSv (50000
]. The effective dose for surgical staff
measured by us amounts to ca. 1.0 μSv per patient (Table 3).
Based on these results, this means that the surgical staff
could perform ca. 1000 SLN interventions per year
without exceeding the threshold value of German radiation
protection regulations, while the surgeon could perform
ca. 250 interventions per year [
] In addition, it has
to be taken into account that penile carcinomas both in
Europe and in the U.S. are much more rare than for
example breast cancer or malignant melanoma . While
the effective dose for the surgeon per patient is thus
higher than in the other mentioned entities, the overall
dose remains relatively low and far below the threshold
of the radiation protection laws.
Our calculations and measurements as well as the data
in the literature on staff radiation exposure [
shown that both the staff in nuclear medicine and the
surgical staff can be expected to undergo only very
limited radiation exposure, which is well within the legal
boundaries. A tentative attitude towards SLNB with
radioactive lymph node labelling cannot be justified on
the basis of radiation protection aspects. Worries and
fears on this score are unfounded. For more
transparency, surgeons in Germany who perform SLNB with
radioactive labelling have been obliged since 2011 to
complete a 6 h–training in radiation protection [
Regardless of this, the procedure has high methodical
demands and requires an experienced and
interdisciplinary team consisting of a specialist in nuclear medicine,
an urologist and a pathologist. This method could be
facilitated through multidisciplinary centres or by
collaborative clinical setups.
SLNB with SLN-labelling via Tc-99 m nanocolloids in
penile cancer is a valuable diagnostic method associated
with low morbidity rates. It offers a high degree of
reliability, especially when performed during surgical
resection of the primary tumour. The method has high
methodological and logistical demands as it among other
things requires an interdisciplinary team. In due
consideration of radiation protection laws, the resulting radiation
exposure for clinical staff during the SLN- procedure is
low, and a tentative attitude towards this approach is not
We thank Mrs. Almut Kalz for proofreading and editing the article,
Mr. Bernhard Egeler for the technical support and Dr. Imme Haubitz for her
advice and her expertise in statistical issues.
There is no funding in connection with this study.
MZ: Data analysis, Manuscript editing. CMN: Statistical analysis, Manuscript
editing. JD: Acquisition of data. RB: Acquisition of data. MM: Acquisition of
data. YZ: Statistical analysis. MJ: Statistical analysis. DO: contributed to
conception. KB: contributed to conception. KPJ: Protocol development. UL:
Protocol development, Manuscript writing. All authors read and approved
the final manuscript.
All authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
In this study, we obtained the patient-informed consent of the involved
patients before starting; the study was additionally approved by the Ethics
Committee of Kiel University (Az. D426/07).
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