Surgical Science, 2011, 2, 57-61
doi:10.4236/ss.2011.22012 Published Online April 2011 (http://www.SciRP.org/journal/ss)
Sentinel Lymph Node Biopsy as Guidance for Lateral Neck
Dissection in Patients with Papillary Thyroid Carcinoma
Yoshifumi Ikeda
Department of Surgery, Teiky o Uni versi t y School of Medi cine, 2-11-1 Kaga, Itabashi-ku, Tokyo 173-8605, Japan
Received January 11, 2011; revised January 20, 2011; accepted Ja n u ary 27, 2011
Abstract
Introduction: The surgical management of lateral lymph nodes in differentiated thyroid carcinoma is contro-
versies. Therefore, we analyzed whether sentinel lymph nodes (SLN) biopsy of the first draining nodes in the
jugulo-carotid chain is an accurate technique to select patients with true-positive but nonpalpable lymph
nodes for selective lateral node dissection. Materials and Methods: From January 2009 to December 2009,
12 patients with solitary papillary carcinoma measuring 2 cm by ultrasonography were included in this study.
After the thyroid gland was exposed to avoid injuring the lateral thyroid lymphatic connection, approxi-
mately 0.2 ml of 5mg/ml indocyanine green was injected into the parenchyma of upper and lower thyroid
gland. Some stained lymph nodes in the jugulo-carotid chain could be identified following the stained lym-
phatic duct and dissected as the SLN. After that, thyroidectomy with modified neck dissection was per-
formed. Results: The mean tumor size was 22.1 ± 4.6 mm. Identification and biopsy of stained SLN in the
ipsilateral jugulo-carotid chain was successful in all 12 cases. In 6 cases, histopathological analysis of SLNs
revealed metastases of the papillary thyroid carcinoma. Among them, 2 cases had additional metastatic
lymph nodes in the ipsilateral compartment. Of the 6 patients who had negative lymph node metastasis
(LNM) in SLNs, all patients had negative LNM in the ipsilateral compartment. Conclusions: The method
may be helpful in the detection of true-positive but nonpalpable lymph nodes and may support a decision to
perform a selective lateral node dissection in patients with papillary thyroid carcinoma.
Keywords: Sentinel Lymph Node, Thyroid Carcinoma, Lateral Neck Dissection
1. Introduction
Well differentiated papillary thyroid carcinoma has a
high propensity to spread to regional lymph nodes and
lymph node metastases are frequently occurred in pa-
tients with clinically negative lymph nodes [1]. Since
lymph node metastasis has not been considered progno s-
tic poor survival, prophylactic lymph node dissection is
controversial [2]. There is wide consensus on an anato-
mosurgical subdivision of potentially involved lymph
nodes in four compartments; central, ipsilateral, conta-
lateral, and mediastinal [4]. The central and ipsilateral
compartments are two representative compartments to
which papillary carcinoma can metastasize. The central
compartment can be dissected via the same surgical inci-
sion used for thyroidectomy. Furthermore, a second sur-
gery for recurrence to the central nodes increases the risk
of complications such as recurrent nerve paralysis and
parathyroid dysfunction [5,6]. Therefore, routine central
node dissection is recommended at the initial surgery
regardless of whether the dissection is therapeutic or
prophylactic. In contrast, the lateral compartment dissec-
tion, regarded as the second region to which papillary
carcinoma metastasizes, is less accessible because wound
extension and a wide range of tissue peeling are neces-
sary for lateral node dissection, and postoperative com-
plaints of patients such as pain, limitation of neck
movement, edema, and sensory abnormality increase.
Therefore, lateral node dissection should be performed
for patients with papillary carcinoma demonstrating me-
tastasis in the lateral compartment. Although preopera-
tive radiological investigations such as ultrasonography
(US), enhanced computed tomography (CT), and mag-
netic resonance imaging (MRI) were improved, its diag-
nostic accuracy is far from perfect.
The concept of sen tinel lymp h nodes (SLN) as the first

58 Y. IKEDA
node(s) to receive drainage from a tumor was introduced
by Ramon Cabanas [7] and later well established in skin
melanoma [8] and breast cancer. [9,10] Controversies in
the surgical management of lymph nodes in differenti-
ated thyroid carcinoma, have led some authors to pro-
pose that SLN should be sampled in patients with thyroid
carcinoma to support the decision whether to perform
lymph node dissection or not. The technique is feasible
and safe and may be used to select patients with true
positive lymph nodes fo r selective lymph nod e dissection.
[11-17]
In previous studies, the stained lymphatic channels in
the central compartment were traced and followed up to
the first blue-stained lymph node, which was defined as
the SLN. However, central and lateral compartment each
has its own lymphatic vessels. We analyzed whether
SLN biopsy of the first draining node(s) in the jugulo-
carotid chain is an accurate technique to select patients
with true-positive but nonpalpable lymph nodes for se-
lective lateral node dissection.
2. Materials and Methods
2.1. Patients
From January 2009 to December 2009, 12 patients with
well differentiated papillary thyroid carcinoma under-
went SLN biopsy in the lower jugulo-carotid chain. Pre-
operatively, all patients had clinical ex amination for sus-
picious thyroid tumors, US of the neck, fine needle aspi-
ration biopsy, CT of the neck, chest X-ray, and blood
tests of thyroid hormones, thyrotrophin (TSH), serum
thyroglobulin, and anti-th yroglobu lin antibody lev els. No
patient had a history of neck surgery for head and neck
cancers. Patients with solitary papillary carcinoma mea-
suring 2 cm by US without massive extrathyroid exten-
sion (corresponding T4 or pT4), clinically apparent
lymph node in lateral component or distant metastasis at
diagnosis were included in this study. The study was
approved by the Institutional Review Board of our insti-
tution, and written informed consent sheet was obtained
from each patient.
2.2. Surgical Procedure and Detection of SLN
Under general anesthesia, the patient is placed in a su-
pine position with the neck extended. A transversal skin
incision was made on the anterior border of the sterno-
cleidomastoid muscle of the tumor side, 3 cm above the
sternal notch. The superior and inferior skin flaps devel-
oped and the strap muscles were separated from the
sternocleidomastoid muscle. The sternohyoid muscle
was separated from the sternothyroid muscle. After di-
viding the sternohyoid and sternothyroid muscle, the
sternohyoid muscle was retracted medially and the ster-
nothyroid muscle was retracted laterally. Then the thy-
roid gland could be exposed to avoid injuring the lateral
thyroid lymphatic connection. By using a 27-gauge nee-
dle, approximately 0.2 ml of 5mg/ml indocyanine green
was injected into the parenchyma of upper and lower
thyroid gland. Care was taken not to stain any surround-
ing tissue with the indocyanine green. After 5 minutes,
connective tissue between the sternothyroid and sterno-
cleidomastoid muscles was sharply divided and the ca-
rotid artery and the internal jugular vein were exposed.
During this procedure, we could usually find a stained
lymphatic duct cross the carotid artery. Some stained
lymph nodes in the jugulo-carotid chain could be identi-
fied following the stained lymphatic duct. The first
stained lymph node was defined as the SLN. After that,
the lateral neck dissection was continued above and be-
yond the omohyoid muscle, around the internal jugular
vein, extending from the carotid artery to the trapezoid
muscle and total thyroid lobectomy and dissection of the
central neck compartment were performed (Figure 1). All
dissected nodes were examined by conventional (hema-
toxylin eosin) histopathological examination. Postopera-
tively, thyroid-stimulating hormone suppression thyrox-
ine therapy was administered to all patients. All patients
were followed regularly by clinical and US examination,
whole-body radioiodine scanning, and serum thyroglobu-
lin measurements.
2.3. Data Analysis
Pathologic specimens were st ai ned wi t h hematoxyl i n and
30 40
Figure 1. Macroscopic appearance of resected specimen
(lymph node was separated from each compartment): (red
circle) central compartment, (blue circle) lateral compart-
ment, (black circle) sentinel lymph nodes in lateral com-
partment.

Y. IKEDA
59
eosin and were observed under light microscopy. Results
of permanent pathology were considered the standard of
reference. Sensitivity, specificity, accuracy, and positive
and negative predictive values of the SLN biopsies were
calculated. Values were expressed as the mean ± stan-
dard deviation. Postsurgical morbidity information on the
patients was obtained from follow-up clinical and labo-
ratory data.
3. Results
The median age at diagnosis was 53 years (range 32–65),
and there were 9 women and 3 men. The mean tumor
size was 22.1 ± 4.6mm. Of the 12 patients, 8 (67%) had
pathological lymph node metastasis (LNM). LNM in the
central neck compartment and ipsilateral compartment
was found in 8 patients and 6, respectively. The average
number of lymph nodes dissection in ipsilateral and cen-
tral compartment was 11.4 ± 4.1 and 4.6 ± 4.0, respec-
tively.
Identification and biopsy of stained SLN in the ipsi-
lateral jugulo-carotid chain was successful in all 12 cases.
The identification rate (IR) of SLN was 100%. The av-
erage number of SLNs per draining area was 2.0 ± 0.7.
In 6 cases, histopathological analysis of SLNs re-
vealed metastases of the papillary thyroid carcinoma.
Among them, 2 cases had additional metastatic lymph
nodes in the ipsilateral compartment. Of the 6 patients
who had negative LNM in SLNs, all patients had nega-
tive LNM in the ipsilateral compartment. We found the
IR of 100% (12 out of 12), with specificity of 100% (6
out of 6) and sensitivity of 100% (6 out of 6). Negative
predictive va lue was 100% (6 out of 6), and pos itive pre-
dictive value was 100% (6 out of 6), while overall accu-
racy of the method was 100% (12 out of 12) (Table 1).
4. Discussion
The cervical chain nodes are distributed within the ante-
rior and lateral areas of the neck, mainly alongside the
various jugular veins. Most of them form part of the deep
lateral cervical chain which runs along the lateral side of
Table 1. Sentinel lymph node biopsy for evaluating lateral
lymph node metastasis.
SLN
LNM positiveSLN LNM negative Total
Lateral
LNM positive 6 0 6
Lateral
LNM negative 0 6 6
Total 6 6 12
SLN: sentinel lymph no d e, LNM: lymph node me t astasis.
the internal jugular vein located deep within the sterno-
cleidomastoid muscle, and which drains directly into the
jugular lymphatic trunk. Other nodes, however, join to
form alternative pathways such as the posterior cervical
accessory chain, the superficial external jugular chain,
and two anterior cervical chains known as the superficial
anterior jugular chain and the deep prelaryngo-tracheal
chain. In the lower part of the neck, a paratracheal recur-
rent chain is also present [18]. These cervical chain
nodes are independent lymph node compartment. The
lymphatic drainage of the thyroid gland is chiefly by
vessels that accompany the arterial blood supply. The
superior lymphatic channels drain the cranial border of
the isthmus, much of the medial surface of the lobes, and
the ventral and dorsal surfaces of the upper part of the
lobes. The inferior channels drain the major portion of
the isthmus and the lower portions of the lobes. The up-
per channels empty into the upper deep cervical nodes,
and the lower ones empty into the lower deep cervical
nodes including the supraclaviculars and into pretracheal
and prelaryngeal n odes. An ad ditional drainage, from the
middle of each lobe, passes directly laterally to enter the
deep cervical nodes. Therefore, regional lymph node
metastases such as the central and ipsilateral compart-
ments in which lymph node metastases were occurred
have different lymphatic channels from the thyroid
gland.
Although some papers [19,20] described that the node
status of the central compartment in papillary thyroid
carcinoma was moderately predictive of that of lateral
compartment, 20% to 45% patients with the absence of
positive central nodes had positive nodes in the ipsilat-
eral neck compartment. Moreover, skip metastasis leap-
ing the central lymph node compartment has also been
reported in papillary thyroid carcinoma [21-23]. There-
fore, lateral compartment has its own lymphatic vessels
and the first metastatic node(s) named SLNs.
SLN biopsy have emerged as a promising minimally
invasive surgical technique to detect metastatic nodes in
patients with melanoma and breast, colon, esophageal,
gastric, lung, head and neck, and thyroid cancers. Kele-
men et al. [11] first applied the concept of SLN in 17
thyroid malignancies using patent blue dye. The IR was
88.2%, due to two retrosternal localized SLN, and false-
negative cases constitu ted 8%. Fukui and colleagu es [12]
analyzed the methylene blue staining of SLN in 22 pa-
tients with papillary thyroid carcinoma. IR was 95.5%,
with 14.3% false-negative investigations. Catarci and
coworkers [13] performed a combined technique of SLN
mapping in 6 cases of papillary thyroid carcinoma. The
overall IR using vital dye (patent blue V), preoperative
lymphoscintigraphy (99mTc-labeled colloidal albumin),
and intraoperative hand-held gamma probe detection was

60 Y. IKEDA
100%, while IR was 66%, 50%, and 83% for each of th e
methods respectively. In a recent study, Roh et al. [24]
showed that SLNs were identified in 46 of 50 patients
(92%). Of these, 14 SLNs were positive and 32 SLNs
were negative on intraoperative frozen sections. One
patient had a positive SLN in the jug ular region and sub-
sequently underwent modified radical neck dissection.
Final pathologic examination revealed that 18 patients
(36%), including 4 who had negative SLNs, had central
lymph node metastasis. Thus, the sensitivity, specificity,
accuracy, and positive and negative predictive values of
SLN biopsy were 77.8%, 100%, 92%, 100%, and 88.9%,
respectively. Temporary and permanent hypocalcemia
developed in 19 patients and 1 patient, respectively.
There were no di rect c omplications of SL N s ampling.
Overall, the previous studies have shown that stained
SLNs were found in the central or lateral neck compart-
ments, or both, and SLN biopsy has the potential to iden-
tify which patients might be most likely to benefit from
central neck dissection at the time of initial surgery [2 4].
Since central neck dissection did not increase permanent
morbidity and revealed a significant rate of non-clinically
evident node metastases, central neck dissection should
be routinely combined with thyroidectomy in papillary
thyroid carcinoma [25].
Taking into consideration the central and ipsilateral
compartments have different lymphatic channels from
the thyroid gland and its own SLN and central neck dis-
section was routinely performed in our hospital, our
study was designed to trace the stained nodes in the ju-
gulo-carotid chain to identify which patients might be
most likely to ben efit from lateral neck dissection in cas-
es of papillary thyroid carcinoma.
In our study we used total of 0.4 ml of 5 mg/ml indo-
cyanine green injected into the parenchyma of upper and
lower thyroid gland for intraoperative lymphatic map-
ping. After 5 minutes, the whole thyroid lobe in which
indocyanine green injected dyed well. Although the ma-
jority of lymphatic channels an d lymph nodes were dyed
blue in central compartment, several lymphatic channels
were identified in lateral compartment. The SLNs in lat-
eral compartment were identified following a stained
lymphatic channel. Although the sample size was small
in our study, IR was 100 %, with specificity of 100% and
sensitivity of 100%. Negativ e pred ictive value was 100 %,
and positive predictive value was 100%. Moreover, 4 in
6 cases with metastasis to the lateral compartment, the
SLN is the only positive nod e.
Our report suggest that SLN biopsy of lateral com-
partment in patients who have papillary thyroid carci-
noma without suspected lymphadenopathy can identify
occult metastases early and can avoid the morbidity as-
sociated with routine and unnecessary lymph node dis-
section. However, additional studies are needed that in-
clude diagnostic sensitivity in frozen section, larger pa-
tient samples, a control group and longer follow-up.
5. Conclusions
Our results imply that SLN biopsy in the lower jugulo-
carotid chain using indocyanine green mapping is a fea-
sible, safe, and accurate method of estimating lymph
node status in the lateral neck compartment. The method
may be helpful in the detection of true-positive but non-
palpable lymph nodes and may support a decision to
perform a selective lateral node dissection in patients
with papillary thyroid carcinoma.
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