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L. Zarifmahmoudi et al.
bronchoscopy guidance. Time to wait after intraoperative injection does not need to be very long and
10–15 min is enough for successful SLN detection.
The radiotracer should be injected carefully to
not penetrate the airways as leakage into the airways can make intraoperative SLN mapping and
biopsy diffi cult (Tiffet et al. reported four detection failures due to airway injection in their
study) [ 12 ]. Figure 20.2 shows planar lymphos-
cintigraphy images with radiotracer leakage into
the airways. This does not seem to be of concern
in preoperative injections as radiotracer would
wash away the airways with time [ 56 , 57 ].
20.2.3 Dose and Volume
of the Injected Radiotracer
The dose of the radiotracer is highly dependent on
the time of injection in relation to the surgery. For
intraoperative injection usually 1–2 mCi divided
into four aliquots is used, and for preoperative
injection, 6–8 mCi divided into four aliquots [ 58 ].
Volume of injection is totally 1–1.5 mL which is
divided into four samples for injection.
20.2.4 Role of Preoperative
Lymphoscintigraphy
and SPECT/CT
The prerequisite of preoperative lymphoscintigraphy imaging is preoperative CT- or
bronchoscopy- guided injection of the radiotracer.
There is not enough information in the literature
regarding preoperative lymphoscintigraphy and
SPECT/CT. However few reports showed that
preoperative imaging especially SPECT/CT can
identify the location of SLNs before surgery
which can guide the surgeons intraoperatively.
Fig. 20.2 Planar lymphoscintigraphy images of an
NSCLC patient. Note airway leakage of the radiotracer on
the early image (5 min image) which disappeared on the
delayed images and the sentinel lymph node which is
apparent on the 6 h image (Reproduced with permission
10.1067/mtc.2002.124496 ) )
(
20 Radioguided Sentinel Lymph Node Mapping and Biopsy in Non-small Cell Lung Cancer (NSCLC)
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325
Unusual location of the SLNs can also be easily
identifi ed which otherwise would be neglected
by the surgeons. By better preoperative localization, SPECT/CT fi ndings may decrease operating
time, decrease patient morbidity, and improve the
accuracy of pathological examination. Injection
problems such as leakage of the radiotracer into
the airways and pleural space could also be
identifi ed readily by SPECT/CT imaging [ 59 ,
60 ]. Figures 20.3 , 20.4 , 20.5 , and 20.6 show
examples of SPECT/CT fi ndings in NSCLC SLN
mapping and biopsy.
However, compared to the other solid tumors
such as genitourinary cancers, breast cancer,
and melanoma, the utility of SPECT/CT in
NSCLC SLN mapping and biopsy seems to be
limited. In the Abele et al. study, SLNs were
identifi ed only in 50 % of the patients on
SPECT/CT imaging [ 60 ]. Another study by
Nomori et al. showed that SPECT/CT could
identify SLNs in the hila especially in segmental and lobar lymph node areas, but not in the
mediastinum. This can be an advantage for
SPECT/CT imaging as intraoperative SLN
localization by gamma probes can be hard in
the hilar and segmental areas [ 61 ] (Figure 20.7 ).
Figure 20.6 shows an example of a patient with
hilar SLN on SPECT/CT images.
Fig. 20.3 Transverse and sagittal fused SPECT/CT images of an NSCLC in the LUL. A is a sentinel lymph node in the
left suprahilar area and B is the injection site (Reproduced with permission (
Fig. 20.4 Transverse and coronal fused SPECT/CT images of an NSCLC in the RUL . A is a sentinel lymph node in the
gastrohepatic area (Reproduced with permission (
10.1007/s12149-014-0821-1 ) )
10.1007/s12149-014-0821-1 ) )
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L. Zarifmahmoudi et al.
Fig. 20.5 Coronal and sagittal fused SPECT/CT images of an NSCLC in the RLL. Diffuse activity in the pleural space
is due to radiotracer pleural space leakage (Reproduced with permission (
10.1007/s12149-014-0821-1 ) )
Fig. 20.6 Transverse and coronal fused SPECT/CT images of an NSCLC in the LUL. Note airway leakage of the
radiotracer into the left mainstem bronchus (Reproduced with permission (
20.3 Alternative Approaches
to SLN Mapping and
Biopsy in NSCLC
20.3.1 Blue Dyes
SLN mapping and biopsy using a dye-only
method is not as successful as other solid tumors.
A systematic review by Taghizadeh Kermani
et al. showed only 64.4 % which is pretty low as
compared to the radiotracer method [ 4 ].
Lower detection rate by dye alone is related to
black discoloration of the mediastinal lymph
10.1007/s12149-014-0821-1 ) )
nodes in most patients (anthracosis) which makes
it diffi cult to fi nd dye-stained SLNs in the mediastinum [ 58 ]. Among the dye methods, indocya-
nine green had the worst detection rate as
indocyanine green (although bright under fl uorescent light) is not readily visible by the unaided
eye [ 32 ].
Due to possible occurrence of some allergic
and nonallergic complications including hypersensitivity (even anaphylactic) reaction in the
form of pulmonary edema, blue discoloration of
the skin or body fl uids, and skin necrosis [ 62 , 63 ]
and very low detection rate by dye techniques,
20 Radioguided Sentinel Lymph Node Mapping and Biopsy in Non-small Cell Lung Cancer (NSCLC)
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327
a
b
Fig. 20.7 Fused SPECT/CT images in an NSCLC of the
LUL. ( a ) is the injection site and ( b ) is a segmental
sentinel lymph node ( white arrow ) (Reproduced with per-
mission (
10.1016/j.jtcvs.2007.02.013 ) )
Despite being a promising alternative to the
conventional radiotracers, PET tracers are limited by their cost.
20.3.3 Magnetic Particles
Ferumoxides (a colloidal superparamagnetic
iron oxide of nonstoichiometric magnetite),
which are used as a contrasting agent for MRI,
have been recently applied for SLN mapping
and biopsy in NSCLC patients. The magnetic
particles are injected peri- tumorally and the
magnetic force within SLNs is detected by
handheld magnetometer [ 19 , 64 ]. Intraoperative
application of mentioned magnetic particle for
SLN mapping and biopsy of NSCLC patients
resulted in the detection, accuracy, sensitivity,
and false-negative rates of 81.6 %, 96.8 %,
85.7 %, and 14.3 %, respectively [ 19 ]. Similar
outcomes have been obtained by using ferucarbotran (clinically approved superparamagnetic
iron oxide) for SLN mapping and biopsy of
patients with NSCLC [ 21 ].
It is suggested that applying magnetic particles for SLN mapping and biopsy is associated
with high sensitivity, detection rate, and accuracy
without any radiation burden to the patients and
surgical staff. Larger studies are still needed to
validate the abovementioned fi ndings.
using blue dye (alone or in combination) in
NSCLC SLN mapping and biopsy is not justifi ed.
20.3.2 PET Radiotracers
Thus far, only one group reported application
of PET radiotracers for SLN mapping and biopsy
in NSCLC. Eo et al. used Ga-68-labeled mannosylated human serum albumin (Ga-68-MSA)
for SLN mapping and biopsy in NSCLC
(Figure 20.8 ). They enrolled 34 patients of clini-
cally stage I NSCLC. The radiotracer was
injected peri-tumorally under CT guidance 1–3 h
before surgery, and PET imaging was started
15–30 min postinjection. They had 100 % detection rate and no false-negative results [ 50 ].
20.3.4 Fluorescent Dyes
Near-infrared (NIR) fl uorescent lymphatic imaging is a novel method for SLN mapping and
biopsy in solid tumors and also has been used for
SLN mapping and biopsy in NSCLC.
Although indocyanine green (ICG) was diffi cult to visualize using regular room light with
the unaided eye because it was masked by the
black appearance of the SLNs, its ability of
absorbing infrared rays (as an NIR lymphatic
fl uorophore) during in vivo binding with serum
proteins appeared to be advantageous for SLN
mapping and biopsy of NSCLC.
The clinical effi cacy of this new technique
for NSCLC has been investigated by several
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68
Ga-MSA PET
Fusion
18
F-FDG PET
Fig. 20.8 Sentinel lymph node imaging by 68Ga-MSA
PET/CT. Black arrow shows the injection site, and red
arrow shows the sentinel node activity. Yellow arrow
research groups. In 2012, Yamashita et al.
reported the results of fl uorescent imaging for
SLN mapping and biopsy in 61 NSCLC patients
with 80.3 % detection rate and 2.1 % false-negative rate [
65 ]. Ichinose et al. also reported
excellent results by NIR imaging in 12 patients
with 91.6 % detection rate and no false-negative
case [ 25 ]. However, Matsuoka et al. showed less
satisfactory results on 12 NSCLC patients with
66.6 % detection rate [ 27 ].
The advantages of this new technique over
radioisotopes are lower radioactivity exposure
and no shine-through effect. The technique may
also reveal deeply located SLNs in the lung
parenchyma or mediastinal fat tissue; however
identifi cation of SLNs should begin as soon as
possible because dye may pass through to the
non-SLNs as time passes [ 65 ].
CT
shows tumor activity (Reproduced with permission
10.1245/s10434-014-3986-x ) )
(
Further studies are needed to increase the
validity of ICG fl uorescence imaging-guided
lung surgery and to be used for SLN mapping and
biopsy in NSCLC. Dose, imaging time and
method, and many other variables should be optimized before routine clinical imaging [ 46 ].
20.3.5 Carbon Nanoparticles
Suspension
In a single report, Jiang-Peng et al. studied the
effi cacy of carbon nanoparticles for SLN mapping and biopsy in 15 NSCLC patients with
73.3 % detection rate and 85.7 % sensitivity [ 10 ].
However, carbon nanoparticles do not seem to be
a viable alternative for radiotracers as they share
the same shortcoming as the blue dyes.
20 Radioguided Sentinel Lymph Node Mapping and Biopsy in Non-small Cell Lung Cancer (NSCLC)
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a
b
c
329
Fig. 20.9 ( a ) NSCLC after exposure of the lung and injection of the tracer in the peri-tumoral area. ( b ) Resected tumor
and harvested lymph nodes. ( c ) Tumoral bed after resection of the tumor and lymph node dissection
20.4 Intraoperative Detection
and Resection of SLNs
well with very high surgical detection rate [
Preoperative CT- or bronchoscopy- guided radio-
58 ].
tracer injection can provide the opportunity for
For intraoperative SLN detection, an acoustic
gamma detection probe is used to guide the surgeons to the location of SLNs.
As mentioned above, the success rate (surgical detection rate) for radiotracer-guided SLN
biopsy in NSCLC is high and comparable to
other solid tumors such as breast cancer and
melanoma. Pooled surgical detection rate was
highest for studies using radiotracer intraoperatively and peri-tumorally: 95.3 % [89.9–97.9 %]
[ 4 , 58 ].
Acoustic gamma detection probes are very
reliable for SLN localization in NSCLC; even
laparoscopic gamma detection probes for videoassisted thoracoscopic surgery (VATS) work very
preoperative lymphoscintigraphy and SPECT/CT
which can guide the surgeons to the correct position of the intrathoracic SLNs. However, intraoperative injection also works well as shown by
multiple studies. Figure
20.9 shows intraopera-
tive SLN mapping and biopsy in an NSCLC.
However, detection of SLNs near the injection
site can be very hard due to obscured uptake in the
nearby SLNs. Learning curve effect also can be a
problem in utilizing acoustic gamma detection
probes. Thus far, two studies have reported possible learning curve effect when performing SLN
mapping and biopsy in NSCLC patients using
radiotracers and fl uorescent imaging [ 14 , 65 ]. This
learning curve effect can compromise the perfor-
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mance of the thoracic surgeon early on in the process of gaining experience with this technique.
20.4.1 Role of Portable Gamma
Cameras and 3D Systems
(fhSPECT)
Thus far, no study has reported the application of
intraoperating portable gamma cameras and freehand SPECT devices for SLN mapping and biopsy
in NSCLC. Due to the complex anatomy of the
thorax, these novel technologies could potentially
be of real help in NSCLC, and this future studies
should be considered using these devices.
Conclusion
SLN mapping and biopsy is an accurate
method for mediastinal lymph node staging in
NSCLC patients. Successful SLN mapping
and biopsy needs careful selection of patients
(only cN0 patients without history of chemotherapy) and proper administration route of
the radiotracer (peri-tumoral injection is preferred over intra-tumoral injection). Alternative
methods, such as magnetic particles and fl uorescent dyes, seem to be very promising and
need further validation studies in the future.
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