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14 Radioguided Surgery of Thyroid Carcinoma Recurrences
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postoperative patient imaging, (2) ultrasonography, and (3) gamma probe detection using the
three-sigma criteria for threshold determination.
The approach was feasible and allowed for successful resection of recurrent thyroid cancer
tissue.
Recently, Francis et al. [ 67 ] reported on 13
patients with recurrent well-differentiated thyroid
cancer. The patients were divided into two groups,
iodine-positive vs iodine-negative (9 and 4
patients, respectively), in whom 18 F-FDG- directed
surgery was performed. This study confi rmed the
feasibility of the technique and former results.
In summary, PET-guided surgery is feasible
and detects the preoperatively found FDG-avid
lesions (Fig. 14.1 ), but it is also challenging owing
to the high energy (511 keV) of the photons emitted by 18 F-FDG. Up to now no PET tracers (e.g.,
124
I) other than 18 F-FDG have been evaluated for
radioguided surgery of recurrent DTC.
14.3.2.3 Intralesional Injection
99m
Tc-Labeled Colloids
of
The technique of intraoperative radioguided
occult lesion localization (ROLL), developed for
use in non-palpable breast cancer, has been transferred to locoregional recurrent thyroid cancer.
Its feasibility was fi rst described in two patients
with non-palpable thyroid lymph node metastases after previous operation on the neck compartment for treatment of PTC and medullary thyroid
cancer, respectively [ 69 ].
The intralesional injection of
99m
Tc-labeled
colloids provides an alternative to intraoperative
ultrasound examination, wire-guided excision, or
intraoperative ultrasound-guided dye injection.
The method has mainly been investigated for
excision of recurrent non-palpable lymph node
metastases.
In 2010 Erbil et al. reported on a further 46
patients with recurrent or persistent PTC detected
by elevated thyroglobulin level, positive radioiodine whole-body scan, or PET and confi rmed by
fi ne-needle aspiration cytology and fi ne-needle
aspiration thyroglobulin measurement [ 70 ]
(Table 14.3 ). Under ultrasound guidance, 20 MBq
99m
of
Tc- labeled rhenium colloid was injected
directly into the pathologic node. Most other
99m
groups reporting on this topic used
Tc-macroaggregated albumin (MAA) [ 71 – 73 , 75 ]. In order
to prove successful injection, Erbil et al. performed preoperative scintigraphy 30 min and
12 h after injection [ 70 ]. Additional preoperative
SPECT/CT may be used as a road map and to
speed up the identifi cation of radiolabeled tissue
[ 77 ]. For intraoperative lesion detection, Erbil
et al. measured the activity counts 3 times for
20 s each and calculated a mean count rate. The
background count rate was derived from a measurement over the normal adjacent tissue.
Besides radioguided lymph node dissection,
the feasibility of intralesional injection has also
been investigated for perioperative identifi cation
of residual thyroid tissue and parathyroid adenoma using a very small amount (7.4 MBq) of
99m
Tc-MAA, injected 90 min prior to surgery.
Terzioglu et al. showed that despite the low
injected activity, measurement over 10 s is suffi cient [ 71 ]. An advantage of this protocol is the
reduction of radiation exposure to surgeons. Both
colloid tracers allowed the dedicated intraoperative detection of preoperatively assessed suspicious lesions, even in patients with extensive scar
tissue. Recently, Giles et al. published the results
of the fi rst randomized study using low-dose
99m
Tc-MAA injection [ 75 ]. Patients with non-
palpable lymph node metastatic disease were
randomized to radioguided lesion localization or
intraoperative ultrasound localization (IOUS).
Both approaches had a high rate of safe and successful excision of recurrent lymph nodes in
patients with PTC. Radioguided surgery may be
preferred by surgeons unskilled in IOUS because
it is very easy to perform.
For radioguided lesion localization, the radioiodine avidity of the tumor lesions is not relevant.
In 2013 Borso et al. [
sional injection of
74 ] described the intrale-
99m
Tc-MAA in patients with
iodine-negative DTC. In 12 out of 35 cases, a
minimally invasive excision could be performed,
whereas the other patients underwent an additional modifi ed radical neck dissection. Ninetyfi ve percent of the marked lesions could be easily
detected during surgery by use of a gamma probe.
Detection of the remaining three lesions was also
possible, but was hindered by tracer leakage.
218
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C. Bluemel et al.
Table 14.3 Surgery guided by
Tukenmez et al. (2007) [
Erbil et al. (2010) [
Terzioglu et al. (2010) [
Martino et al. (2010) [
Ilgan et al. (2010) [
Borso et al. (2013) [
Bellotti et al. (2013) [
Giles et al. (2014) [
Jung et al. (2014) [
99m
TIGMA
albumin, LNM lymph node metastases
a
Not reported in the available abstract
Tc-macroaggregated human serum albumin and indocyanine green,
70 ] 46
72 ] 20
73 ] 8
74 ] 32
13 ] 22
75 ] 20
76 ] 7
99m
Tc-labeled colloids (characteristics of trials)
No. of patients Radiopharmaceutical Injected activity Lesions
69 ] 2
71 ] 21
99m
Tc-rhenium colloid 20 MBq LNM
99m
Tc-rhenium colloid 20 MBq LNM
99m
Tc-MAA 7.4 MBq LNM, thyroid tissue,
99m
Tc-MAA 14.8 MBq LNM
99m
Tc-MAA 7.4–14.8 MBq Local recurrence and
99m
Tc-MAA 7.4 MBq a
99m
Tc-MAA 20 MBq LNM
99m
Tc-MAA 7.4 MBq LNM
99m
Tc-TIGMA 0.1 ml of TIGMA Not specifi ed
Recurrence rates were similar in both groups
(33 % for ROLL vs 40 % for additional neck
dissection).
In the same year Bellotti et al. [ 78 ] reported
on 22 patients with recurrent DTC in whom a
gamma probe was used for intraoperative lesion
detection and a small-fi eld gamma camera for
intraoperative imaging. All included patients had
undergone radical surgery including central and/
or lateral neck dissection for primary treatment
and suffered from locoregional lymph node
recurrences of PTC in the follow-up. Recurrent
disease was detected by thyroglobulin measurement, ultrasound, radioiodine whole-body scan,
and fi ne-needle aspiration cytology. In a 1-day
protocol, 20 MBq of
99m
Tc-MAA (0.2 ml) was
directly injected into the suspicious lesions
under ultrasound guidance before surgery.
Thirty-nine pathologic nodes were injected and
61 nodes removed, including 22 additional nodes
not injected by radiotracer. Of these additional
lymph nodes, seven (31.8 %) were metastatic.
Similarly, Erbil et al. and Giles et al. reported
metastatic disease in 32–40 % of additionally
resected nodes [ 70 , 75 ]. Bellotti et al. avoided
preoperative imaging because intraoperative
images of the cervical region were acquired with
the gamma camera. After imaging, the thyroid
bed was explored using the acoustic gamma
probe, enabling lesion localization. Complete
excision was proven by measuring the count rate
parathyroid adenoma
lateral compartment
99m
Tc - MAA
99m
Tc-marcoaggregated
of the lesions and the surgical bed after resection
on the one hand and by intraoperative imaging
on the other. Bellotti et al. demonstrated that this
technique is feasible without complications and
does not prolong the operation signifi cantly.
Intraoperative imaging allowed for a minimally
invasive approach and fast lesion localization
and was of additional value if lesion detection
with the gamma probe was diffi cult [
78 ].
Recently, a radiofl uorescence approach com-
bining
99m
Tc-MAA with indocyanine green
(TIGMA) was reported in seven patients with a
recurrent DTC [ 76 ]. The maximum excitation
light wavelength of indocyanine green is 780 nm
and the highest emission light wavelength,
800 nm, generating a low background signal as
this light is not absorbed by tissue and is invisible
to human eye [
79 ]. Jung et al. reported that pre-
operative hybrid tracer preparation required
about 20 min. Under ultrasound guidance, 0.1 ml
of the mixture was injected. For intraoperative
imaging, a near-infrared fl uorescence (NIRF)
camera was necessary in addition to a gamma
probe. Prior to incision, a scan with the gamma
probe was performed and confi rmed by use of the
NIRF camera, enabling NIRF observation in real
time. The fl uorescence could be easily detected at
a depth of 3.25 mm and the hybrid tracer was
retained at the injection site without spreading to
adjacent tissue, resulting in better imaging than
was possible with indocyanine green alone. The
14 Radioguided Surgery of Thyroid Carcinoma Recurrences
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219
authors reported that TIGMA is safe (low toxicity) and facilitates the detection of recurrent
lesions. However, fl uorescence imaging requires
further surgical equipment (NIRF camera) and
may be infl uenced by surgical lights.
It has to be kept in mind that the intralesional
injection of a radiotracer has one major limitation: the technique is only suitable in lesions
which can be localized by ultrasound. This may
be the reason for the unexpected lymph node
metastasis at non-injected nodes [ 75 ] and the
appearance of suspicious nodes during follow-up
[ 34 , 74 ]. Therefore, radioguided resection may
be combined with compartment-oriented lymph
node dissection [ 75 ].
14.4 Medullary Thyroid Cancer
Sporadic or hereditary medullary thyroid cancer
(MTC) is a rare disease and only 3–10 % of thyroid
cancers are of medullary origin [ 80 , 81 ]. However,
this thyroid cancer has a recurrence rate of up to
50 % [ 80 ], and resection seems to be the only
promising treatment option for achievement of
locoregional disease control in patients with recurrent disease. For detection of recurrent disease,
besides calcitonin and CEA measurement or ultrasonography, use of various radiotracers has been
described, e.g.,
99m
Tc-MIBI, 18 F- l - dihydroxyphenylalanine
(DOPA), and 68 Ga-labeled somatostatin analogs
[
82 ]. The value of radioguided surgery in facilitat-
ing tumor detection has been investigated, but not
for all available radiotracers.
99m
Tc-(V)-DMSA, thallium-201,
Adams et al. investigated 35 patients with previously operated MTC and suspicion for recurrence due to elevated calcitonin levels [
86 , 87 ].
These patients underwent CT scanning and diagnostic double-nuclide scintigraphy. First 180 or
222 MBq
lowed by 500 MBq
111
In-DTPA octreotide was injected, fol-
99m
Tc-(V)-DMSA. Image
acquisition was performed 4 and 24 h later for
111
In-DTPA octreotide and 6 h later for
99m
Tc-(V)DMSA imaging including whole-body scintigraphy and SPECT. In the fi rst study (n = 10),
double-nuclide scintigraphy revealed 20 of 30
suspicious lesions, while radiologic imaging (CT
and sonography) revealed 15 of the lesions.
Intraoperative use of a gamma probe detected all
lesions, but three lesions proved false positive,
showing lymphadenitis on histopathology [ 86 ]. In
the second study (n = 25), the sensitivity of preoperative CT,
99m
and
111
In-DTPA-octreoitide scintigraphy,
Tc-(V)-DMSA was 32 %, 34 %, and 65 %,
respectively [ 87 ]. For radioguided surgery the
tracer with the highest detection rate was reinjected preoperatively. During surgery, a tumor-tonon-tumor count ratio of 2:1 was considered
positive. Detection rates were compared with preoperative imaging and intraoperative palpation.
The smallest detected metastasis within the entire
cohort was a lymph node with a diameter of
5 mm. The sensitivity of radioguided surgery was
superior to that of surgical palpation (97 % vs
65 %) [ 87 ], and radioguided surgery allowed
detection of 30 % more lesions compared with
preoperative conventional imaging [
88 ].
14.4.2 Radioimmunoguided Surgery
14.4.1
99m
Tc-(V)-DMSA-Guided
Surgery
99m
Tc-(V)-DMSA scintigraphy is a diagnostic
tool for detection of recurrent medullary cancer,
99m
but
Tc-(V)-DMSA is no longer commercially
available. The reported sensitivity of this imaging
method varies and it has reduced sensitivity for
bone metastases [ 83 – 85 ]. The variation in detec-
tion rate may be attributable to the use of different commercial kits and their instability [ 82 ].
123
131
I-,
I-, and
111
In-labeled monoclonal antibodies have been investigated for imaging of MTC
[ 89 – 91 ]. Only three reports are available on
radioimmunoguided surgery in MTC [ 92 – 94 ].
In 1993, Peltier et al. [ 94 ] described two-step
radioimmunotargeting in patients with recurrent
MTC and performed radioguided surgery in fi ve
patients. This group injected a bispecifi c antibody
(anti-CEA monoclonal IgG coupled with anti-InDTPA monoclonal IgG) and
111
In-labeled DTPA
dimer (diDTPA-TL). The procedure of tumor
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C. Bluemel et al.
radioimmunotargeting consisted of two steps: fi rst
1 mg/10 kg of body weight non- radiolabeled specifi c antibody was injected intravenously over
20 min. Four days later 1 nmol/10 kg
111
In-labeled
diDTPA-TL was injected. Preoperative scintigraphy including SPECT was performed after 5 and
24 h. In three of the fi ve patients who underwent
surgery, intraoperative use of the gamma probe
detected suspicious lesions not identifi ed by the surgeon. Two further studies confi rmed the feasibility
of this technique [ 92 , 93 ]. De Labriolle-Vaylet et al.
pointed out the additional value of the technique
compared with physical examination and conventional imaging. In their cohort of 13 patients, 22 of
34 metastases would have been missed using the
latter methods. Radioimmunoguided surgery had
an accuracy of 86 % (sensitivity 75 %, specifi city
90 %). The limitations of this promising technique
are the time delay and the availability of competing
radiolabeled compounds.
14.4.3
123
123
I- MIBG-Guided Surgery
Iodine-123-labeled MIBG can be used for diagnostic purposes in patients with MTC. However,
there has been only one published case in which
123
I-MIBG guided surgery was used in MTC.
Shimotake et al. reported on a MEN2B 14-yearold girl suffering from recurrent MTC in whom
reoperation on the cervical and upper mediastinal
regions was hampered by fi brotic scar tissue due
to four previous neck operations. Twenty-four
hours after injection of 100 MBq
123
I-MIBG, successful tumor resection in the cervical region and
upper mediastinum was possible without side
effects. However, because many recurrent MTCs
are not MIBG avid, somatostatin receptor scintigraphy imaging may have greater potential.
radiolabeled somatostatin analogs. As long ago
as 1995, Wangberg et al. investigated ten patients
with residual MTC using
111
In-DTPA-octreotideguided surgery [ 95 ]. Injection of the radiotracer
(140–300 MBq) was performed 24–168 h prior to
surgery. Eight of the ten patients had positive
lesions on preoperative scintigraphy performed
24 h after injection. At surgery, in situ measurements of macroscopically identifi ed tumors were
false negative in 4 out of 37 lesions.
In summary, MTC is rare and therefore only a
limited number of reports are available on
radioguided surgery in patients with recurrent
disease. However, the results are promising and
further studies are necessary to investigate new
tracers (e.g., 68 Ga-labeled somatostatin analogs)
and the ROLL concept.
14.5 Outlook
Currently the experience gained in the application of radioguided surgery techniques in residual
or recurrent (differentiated) thyroid cancer is still
limited. Despite promising results in this challenging setting, radioguided approaches have not
yet become established in daily clinical routine
or in guidelines. One reason may be the existence
of multiple competing tracers, which may hamper selection of the “optimal” tracer. Furthermore,
no studies exist on very novel tracers like
68 Ga-labeled somatostatin analogs in MTC. In
future studies the role of intraoperative imaging
needs to be investigated, and evaluation of
radioguided surgery for non-locoregional metastases would also be of interest.
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Medullary thyroid cancer often expresses somatostatin receptors, which can be visualized with
somatostatin receptor scintigraphy. Radioguided
surgery has also been investigated using
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Part VII
https://t.me/med1917
Clinical Application: Urogenital Tract
Radioguided Sentinel Lymph Node
https://t.me/med1917
Biopsy and Lymphatic Mapping
in Urogenital Malignancies
Henk G. van der Poel , Joost A. P. Leijte ,
and Simon Horenblas
1 5
Contents
15.1 Introduction 228
15.2 Penile Cancer 228
15.2.1 Preoperative Visualization of Lymphatic
Drainage 229
15.2.2 Intraoperative SLN Detection Using
Gamma Tracing 230
15.2.3 Optical Tracers and SLN
Detection in Penile Cancer 230
15.2.4 Clinical Outcome 231
15.3 Prostate Cancer 231
15.3.1 Preoperative Imaging 232
15.3.2 Intraoperative Detection 232
15.3.3 Outcome 234
15.4 Bladder Cancer 234
15.5 Testis and Renal Cancer 234
15.6 Summary 241
References 241
H. G. van der Poel () • J. A. P. Leijte • S. Horenblas
Department of Urology , Netherlands Cancer Institute ,
Amsterdam , NL , USA
h.vd.poel@nki.nl
e-mail:
Abstract
Radioguided sentinel lymph node (SLN)
detection is applied in the management of several urogenital malignancies. International
guidelines recommend SLN detection in men
with penile cancer and increased risk of nodal
metastases. For several other urogenital malignancies, SLN detection is considered experimental: prostate cancer, testicular cancer,
bladder cancer, and renal cancer. Largest
series are published on prostate cancer management. No randomized studies are available
for review. Although SLN detection was
shown to provide detection of nodal metastases outside standard nodal dissection templates in prostate and bladder cancer, the lack
of standard methodology and defi nitions of
SLN may explain why SLN detection is still
considered experimental. Only few studies
discuss the use of SLN detection in renal and
testicular cancer. With improved intraoperative imaging modalities, better anatomical
localization of SLN in particular in the retroperitoneum is feasible. This may boost the
design of appropriately designed prospective
comparative trials to study the oncological
benefi t of SLN detection in urogenital
malignancies.
© Springer International Publishing Switzerland 2016
K. Herrmann et al. (eds.), Radioguided Surgery: Current Applications and Innovative
Directions in Clinical Practice, DOI 10.1007/978-3-319-26051-8_15
227
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