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ENDOCRINE SURGERY
branch of the superior thyroid artery is also
isolated with identification of the external
branch of the superior laryngeal nerve. The
superior parathyroid gland is dissected from
the thyroid lobe. The inferior pole vessels are
isolated with preservation of the inferior parathyroid gland. Then the dissection is performed
medially to separate the thyroid lobe from the
sternothyroid muscle up to the isthmus. The
endoscopic dissection is finished with the
removal of the three trocars. All vessels are
ligated and divided with harmonic scalpel
through the skin incision. The thyroid lobe is
extracted and the isthmus divided with harmonic scalpel. There is no traction on the RLN
during this step. Only the platysma is sutured
and the skin is closed by skin sealant [22–25].
Central Approach: Miccoli Technique
With this technique, the patient is also in supine
position without neck hyperextension. A 15-mm
horizontal incision is performed 2 cm above the
sternal notch. After dissection of the subcutaneous
fat and platysma, the cervical linea alba is divided
longitudinally for 3 cm. A small retractor is used to
retract the strap muscles and another one for the
thyroid lobe, which is gently dissected from the
strap muscles. The two retractors maintain the
operative space, and a 308 5-mm endoscope is
inserted. Dissection of the thyrotracheal groove is
completed by 2-mm instruments inserted also
through the single skin incision. The middle vein
is ligated by 3-mm vascular clips to avoid electrocautery. The upper pedicle is then exposed with
downward retraction of the thyroid. The upper
vessels are selectively ligated by clips and cut
after identification of the external branch of the
superior laryngeal nerve in most cases. Inferior
vessels are also clipped and cut. After lifting up
the thyroid lobe, the fascia is opened. Small vessels
are closed by clips and the RLN and the parathyroid glands are dissected from the thyroid. Endoscope and the retractors can then be removed. The
thyroid lobe is gently extracted and remaining
vessels and Berry’s ligament are ligated and cut.
The laryngeal nerve is checked before division of
the isthmus. After control of hemostasis, the linea
alba and platysma are sutured with reabsorbable
suture. The skin is closed by skin sealant or subcuticular suture [23, 25].
References
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of training and vocal-cord paralysis in benign thyroid
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2. Udelsman R. Experience counts. Ann Surg. 2004;240:26–7.
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296–303.
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TECHNIQUE OF THYROIDECTOMY
18. Gagner M. Endoscopic subtotal parathyroidectomy in
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13
Lymph Node Dissection in Thyroid Cancer
Henning Dralle and Andreas Machens
Introduction
In locally advanced thyroid cancer confined to
the neck, lymph node surgery pursues curative
intentions but is also performed for the prevention of complications. These complication may
arise from the invasion of local structures, such
as recurrent laryngeal nerve, compromising
quality of life, or trachea and esophagus, which
may be life-threatening [1]. The tumor biology
of thyroid cancer is mainly determined by the
respective tumor type (papillary, follicular, lowdifferentiated, undifferentiated, and medullary)
and the extent of disease (intrathyroidal growth
versus extrathyroidal extension; locoregional
versus distant metastases). To complicate the
matter further, clinical outcome is also influenced by a host of proliferative factors.
Surgery is the single most important, potentially curative treatment modality not only for
the primary tumor but also for locoregional
node metastases. Radioiodine treatment in differentiated thyroid cancer and external beam
radiation in locally advanced differentiated or
undifferentiated thyroid cancer may complement but not replace surgery. For distant metastases, surgical intervention is rarely indicated,
and if so, only as one component of a multimodal approach [2–5]. Such rare instances
include solitary and localized distant metastases, which can be removed safely with acceptable surgical morbidity.
Because thyroid cancer is uncommon and
often takes a chronic course over decades,
management recommendations [6–8] are exclusively derived from single-center or multiinstitutional experience [9, 10]. Mimicking
clinical reality [11, 12], there is only one intervention but no head-to-head comparison of
different types of treatment which would facilitate evidence-based decisions tailored to the
needs of individual patients. This weak evidence
base is a frequent source of disagreement. There
is no consensus about the indication for, and
extent of, lymph node dissection (LND)
(routine versus therapeutic; selective versus
compartment-oriented). As a result, recommendations are based on indirect inferences,
personal experience, or just eminence instead
of evidence [13].
Locoregional Lymph Nodes:
Surgical Anatomy and
Classification Systems
The prognostic relevance of lymph node metastases has remained controversial in solid cancers, especially in thyroid cancer. As in most
types of solid cancer, including thyroid cancer,
the frequency of locoregional lymph node
metastases increases with tumor size [14].
There is also evidence of a direct relationship
between the number of locoregional node
J.G.H. Hubbard et al. (eds.), Endocrine Surgery, Springer Specialist Surgery Series,
DOI 10.1007/978-1-84628-881-4_13, Ó Springer-Verlag London Limited 2009
173
174
ENDOCRINE SURGERY
metastases and the frequency of distant metastases, which is not understood fully. Distant
metastasis, the strongest indicator of cancerspecific death, sometimes occurs in the absence
of lymph node metastases [15, 16]. Several
issues regarding the pathobiology and clinical
implications of lymphatic spread in thyroid
cancer remain unsettled. These areas of uncertainty concern the incidence and prognostic
importance of skip metastases [17] and the anatomical boundaries between the ‘‘locoregional’’
and the ‘‘distant’’ type of lymph node metastases
[18]. Disregarding tumor biology, the current
concepts of surgical anatomy and classification
systems rest wholly on the histopathological
involvement of locoregional nodes in surgical
specimens.
In solid cancer, removal of locoregional
lymph node metastases can result in cure. The
ability of closely reflecting lymphatic spread is
the key requirement for any classification system of locoregional lymph nodes. Specifically
devised for thyroid cancer, the compartment
classification seems to meet this requirement
better than any other classification system,
which are more specific for head and neck
tumors. This classification system defines
three neck compartments and one mediastinal
compartment which contain all the respective
locoregional nodes embedded in fibrofatty tissue. [19–25]. Representing the first echelon of
locoregional node metastasis, the central neck
compartment can be conceived clinically as the
‘‘epicenter’’ of lymphatic spread in thyroid cancer. Thecentral neck compartment is separated
from the lateral neck compartments by the
medial border of the common carotid artery
[22, 26], and from the upper mediastinal
(infrabrachiocephalic) compartment through
a virtual line drawn through the origin of the
right and left common carotid arteries from the
aortic arch. Anatomically, the mediastinal
compartment comprises only those nodes
located below this virtual line. To remove all
mediastinal nodes falling under this anatomical definition, a transsternal approach is
always required. Less well defined are the
external lateral borders of the lateral neck and
mediastinal compartments. There are no fasciae or major vessels to serve as anatomical
landmarks between lateral cervical and nuchal
nodes, or between upper mediastinal and middle mediastinal nodes.
Unfortunately, no standard classification of
locoregional lymph nodes exists for thyroid
cancer. At least four competing staging systems
are in use (Fig. 13.1):
1. The American Academy of Otolaryngology –
Head and Neck Surgery Dissection Classifi-
cation [26, 27] describing six different levels
in the central (level Ia, Ib, and VI) and lateral
(IIb, IIa, III, IV, Va, Vb) neck, but excluding
the infrabrachiocephalic upper
mediastinum;
2. The Japanese Society of Thyroid Surgery
Classification [25] describing seven lymph
node groups in the central (I–IV) and lateral
(V–VII) neck, but excluding the infrabra-
chiocephalic upper mediastinum;
3. The International Union Against Cancer
(UICC) classification [28] describing eight
lymph node groups in the central [1, 2, 8]
and lateral [2–7] neck, but also excluding the
upper mediastinum; and
4. The Compartment Classification [22–24, 29,
30] describing four locoregional compart-
ments in the neck (C1, C2, C3) and upper
mediastinum (C4).
From a practical point of view, all four classification systems have limitations and are
incompatible with one another. The compartment classification is the most straightforward
classification system because it (i) uses the
major arterial structures in the neck and mediastinum as anatomical landmarks; (ii) affords
differentiation by side; and (iii) includes the
upper mediastinum.
The number of lymph nodes removed from
the respective regions depends not only on the
extent of node metastasis and the surgical technique of LND but also on the diligence with
which the histopathological analysis is carried
out. On average, the central neck compartment
harbors 10 nodes (five nodes on either side), the
lateral neck compartments 20 nodes each, and
the mediastinal compartment 10 nodes (five
nodes on either side) [30, 31]. Although the
UICC classification uses the number of positive
nodes as a prognostic marker for many solid
cancers, including breast carcinoma [28], the
UICC classification for thyroid cancer does not
capture this important piece of information.
Recent literature reports suggest that the presence of more than 10 lymph node metastases is
linked to a worse outcome in patients with
175
LYMPH NODE DISSECTION IN THYROID CANCER
ab
cd
Fig. 13.1. Classification systems of locoregional lymph nodes and lymph node groups.(A) American Academy of
Otolaryngology – Head and Neck Surgery (ACOLHNS): (I) submental (IA) and submandibular (IB); II, upper jugular (IIA, IIB); (III)
middle jugular; (IV) lower jugular; (V) posterior triangle (VA, VB); (VI) anterior (reprinted from Robbins KT, Clayman G, Levine PA,
Medina J, Sessions R, Shaha A, Som P, Wolf GT and the Committee for Head and Neck Surgery and Oncology, American Academy of
Otolaryngology-Head and Neck Surgery. Neck dissection classification update. Arch Otolaryngol Head Neck Surg 2002; 128: Fig. 1,
p. 752). (B) Japanese Society of Thyroid Surgery (JSTS): (I) prelaryngeal; (II) pretracheal; (III) paratracheal; (IV) paraglandular; (V)
deep upper cervical; (VI) deep lower cervical; (VII) deep lateral cervical (reprinted from Surgery, vol. 131, Qubain SW, Nakano S, Baba
M, Takao S, Aikou T. Distribution of lymph node micrometastasis in pN0 well-differentiated thyroid carcinoma, pp. 249–56,
copyright 2002, with permission from Elsevier). (C) International Union Against Cancer (UICC): (1) submental; (2) submandibular; (3)
cranial jugular; (4) medial jugular; (5) caudal jugular; (6) dorsal cervical along accessory nerve; (7) supraclavicular; (8) prelaryngeal and
paratracheal (reprinted with permission from Wittekind Ch. Greene FL, Henson DE, Hutter RVP, Sobin LH. TNM Supplement. 3rd ed.
Wiley-Liss New York, 2003, Fig 2a, p. 27). (D) Compartment Classification of Thyroid Locoregional Nodes (CC): (1) cervicocentral right
(1a) and left (1b); (2) cervicolateral right; (3) cervicolateral left; (4) upper mediastinal right (4a) and left (4b).
176
ENDOCRINE SURGERY
papillary and medullary thyroid carcinoma
(MTC) [32–34]. For follicular, poorly differentiated, and undifferentiated carcinoma, there
are no pertinent data.
Indications for Lymph Node
Dissection
Lymph node dissection is performed with
curative (elective or prophylactic versus therapeutic) or palliative intent. Its clinical importance is commensurate with the intensity of
lymphatic tumor dissemination, which is
higher in papillary thyroid cancer (PTC) and
MTC than in other thyroid cancers. Because of
the chronic course of the disease and the threat
of invasion of the neck from extranodal tumor
growth [35], palliative LND has a prominent
role within the treatment concept for PTC and
MTC.
With increasing resolution, imaging has
increased in importance, laying out a roadmap
of positive locoregional nodes, not only in
recurrent but also in primary thyroid cancer.
Advances in cervical ultrasonography, such as
the development of high-resolution imaging
systems and the Doppler power mode, have
improved the detection of suspect nodes
based on a combination of anatomical and
functional parameters. These substantial
improvements in imaging have had major
repercussions on the concept of stage-oriented
surgery, enabling a more tailored approach in
planning LND to the extent of lymph node
metastases. In recurrent thyroid cancer, this
progress has enhanced the effectiveness of
reoperations in the neck [36–44]. The new
technology of fluoro-deoxyglucose (FDG)PET fusion has further refined the localization
of residual tumor and improved the projection
of outcome in radioiodine-negative differentiated [45–49] and MTC [50, 51]. A recent
study on 400 thyroid cancer patients found a
negative correlation between FDG avidity and
cancer-specific survival [49]. As a consequence
of these developments, invasive localizing
techniques for occult thyroid cancer, such as
selective venous catheterization, have largely
been abandoned [52, 53].
Papillary Thyroid Carcinoma
When one considers the recent results of large
single-center studies and systematic evidence-based analyses, there is no doubt that
a clinical diagnosis of node metastases reflects
more aggressive tumor biology in papillary
thyroid carcinoma (PTC) [54, 55] with a
higher risk of locoregional and distant recurrence [15, 33, 56–59]. While therapeutic LND
is unanimously accepted, there is still an
ongoing debate regarding the clinical relevanceofoccultnodemetastasesandtheneed
for routine (i.e., prophylactic) LND of the
central [43, 59, 60–62] and lateral [39, 40, 41,
63] neck compartments.
For papillary microcarcinoma, where lymph
node metastases do occur, there are no data to
support the use of routine central or lateral node
dissection [39, 43, 60, 62] (Table 13.1). For gross
PTC (>10 mm in diameter), conversely, there is
mounting evidence that routine central node dissection should be performed as a minimum [34,
61, 66]. Central LND has been connected to higher
rates of transient and sometimes permanent
hypoparathyroidism and recurrent laryngeal
nerve palsy [61, 62, 64–67]. This risk of surgical
morbidity, which is quite low in experienced
hands, must be balanced with the high recurrence
rates after total thyroidectomy alone, and the
much higher complication rates after completion
central neck dissection. All in all, these data argue
in favor of routine central node dissection for PTC
measuring >10 mm in diameter.
Lateral cervical and, even more, transsternal
mediastinal node dissection are a different
matter, not only because the potential for surgical morbidity is much higher, but also cosmetically because the skin incision needs to
be significantly enlarged to gain full exposure
[22, 68, 69]. During total thyroidectomy for
PTC, regardless of the need for central LND,
the lateral compartments are not routinely
exposed. Therefore, it seems prudent to restrict
routine lateral neck dissection to those tumors
with risk factors of lymphatic spread, such as
large primary tumors and those with massive
extrathyroidalextension[58].InPTC,transsternal LND is rarely indicated in the infrabrachiocephalic upper mediastinum, but clearly
is required for confirmed node metastases
[22, 70].
177
LYMPH NODE DISSECTION IN THYROID CANCER
Table 13.1. Involvement of central and lateral compartments in PTC 10 mm versus >10 mm
Maximum primary tumor diameter
10 mm >10 mm
Central Lateral Central Lateral
Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral
First surgery (%)
(n = 31)
Reoperative surgery (%)
(n = 101)
Source: Adapted from Machens A, Hinze R, Thomusch O, Dralle H. Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J
Surg. 2002;26:22–28. Reprinted with kind permission of Springer Science and Business Media.
Lateral node metastases located contralateral in relation to the primary tumor are a
well-known event in head and neck cancer
[71] but are quite rare in well-differentiated
PTC (Table 13.1). Some PTC variants, such as
the diffuse sclerosing variant, may coincide
14 7 29 0 41 18 29 6
195 5– 3818 2510
there is no indication for routine LND in FTC.
Thesamesurgicalstrategyappliestothe
oxyphilic (‘‘Hu¨rthle cell’’) variant of FTC
because the rates of lymph node and distant
metastasis are similar to those for nonoxy-
philic FTC [84].
with Hashimoto’s thyroiditis and often reveal
involvement of both thyroid lobes and lateral
node metastases in both the right and left neck
[72–76]. When lateral lymph node metastases
are detected in the contralateral neck of pre-
Poorly Differentiated Thyroid
Carcinoma
viously untreated patients, routine dissection
of the central and both lateral neck compartmentsisjustified.
The 6th edition of the WHO classification of
thyroid malignancies, which appeared in 2002
[85], reclassified thyroid carcinomas with lim-
ited evidence of follicular cell origin as poorly
Follicular Thyroid Carcinoma
differentiated thyroid carcinomas (PDTCs).
Both morphologically and biologically, these
Survival following well-differentiated follicular thyroid cancer is mainly determined by the
presence of distant metastases [77–82]. Distant metastases are found in some 20% of
patients, as opposed to some 6% in PTC [16].
With the growth of the primary tumor, lymph
node metastases occur more frequently. The
sizethresholdforlymphnodemetastasesis
higher in follicular thyroid carcinoma (FTC)
(>20 mm) than inPTC (<10mm) [16]. In FTC,
but not PTC, node metastases are associated
with distant metastases, carrying a much
worse prognosis [15]. Because of this fact,
most authors found no evidence that node
metastases in FTC have an independent
adverse effect on survival [83]. Unlike therapeutic LND for preemption of extranodal
growth and subsequent invasion of the neck,
poorly differentiated tumors take an intermedi-
ate position between differentiated and undif-
ferentiated (anaplastic) thyroid carcinomas
(UTCs) [86–92].
Lymph node metastases and distant
metastases occur more frequently (45–65%)
[89, 91] in poorly differentiated than in
well-differentiated thyroid carcinoma. [86,
91]. In one study [89], up to 70% of distant
metastases concentrated radioiodine. Established prognostic factors include primary
tumor size, extrathyroidal extension, and
distant metastases but not lymph node
metastases [86, 89, 91].
By definition, PDTC may originate from FTC
or PTC. Except for large extrathyroidal PDTC,
the preliminary data do not support routine
LND.
178
ENDOCRINE SURGERY
Undifferentiated (Anaplastic)
Thyroid Carcinoma
Extrathyroidal extension with tracheal invasion
and rapid progression to tracheal obstruction
with a high prevalence of distant metastasis are
the hallmarks of UTC. Despite being quite common (30–40%) [93], lymph node metastases are
not a key component of surgical treatment
unless the completeness of the resection hinges
on the removal of these nodes [94–98]. There is
no consensus whether complete resection prolongs survival in UTC [99]. Because of this fact,
extensive surgery with special emphasis on the
preservation of organ function, supported by
adjuvant external radiotherapy, with or without
adjuvant chemotherapy, constitutes the current
treatment of choice for UTC [93, 94, 96, 97,
100–104]. LND is one means of achieving local
control, without having a measurable effect on
survival.
Medullary Thyroid Carcinoma
Medullary thyroid carcinoma, or C-cell carcinoma, is a unique tumor entity within the spectrum of thyroid cancer. Originating from neural
crest cells, it differs in many ways from other
thyroid cancers. Unlike follicular cell-derived
thyroid cancers, MTC cells are unable to express
the sodium/iodine symporter and hence do not
concentrate iodine. As a tribute to their neuroendocrine heritage, MTC cells synthesize
and secrete various hormonal peptides, including calcitonin and carcinoembryonic antigen
(CEA), which can be used as tumor markers.
By the time of diagnosis, up to 20% of patients
have developed distant metastases [105]. Even
with extensive LND, only 60% of node-negative
and 10% of node-positive patients are cured
[105]. Despite these facts, overall survival rates
in MTC are remarkably good and do not differ
much from those seen in differentiated thyroid
cancer [106]: 89% at 5 years [107] and 75–85%
at 10 years [108, 109]. Far from being a homogeneous entity, MTC encompasses a wide range
of tumors from rather indolent [110] to highly
aggressive [1, 111]. Because calcitonin-secreting
C-cells are highly sensitive to external stimulation, calcitonin levels are very useful for early
MTC screening but tend to fluctuate on repeated
measurements. For long-term monitoring of
advanced disease, serum CEA levels may be
more useful because they tend to be more stable
[105, 112, 113].
Lymph node metastases have a prominent
role in MTC [105, 114, 115]. Owing to their
high prevalence, enlarged nodes may be the
first clinical evidence of disease. As early as
1968, just 7 years after MTC was recognized as
a separate tumor entity, Woolner et al. [116]
described the prognostic importance of lymph
node metastases in 77 MTC patients: Nodenegative patients had a life expectancy similar
to the general population whereas node-positive
patients had a 10-year survival rate of just 42%.
Second only to distant metastases, lymph node
metastases are a measure of systemic disease.
Furthermore, lymph node metastases can give
rise to locoregional recurrence, necessitating
the removal of all positive nodes.
Incorporating recent evidence and drawing
on personal experience, the indication for, and
the extent of, lymph node surgery can be summarized as follows:
1. Lymph node metastases may occur with pri-
mary tumors as small as 5 mm. The surgical
window of cure between the development of
lymph node metastases and distant metas-
tases can be quite narrow because distant
metastases have been found with 10 mm
small primary tumors [105]. These data
underscore the need to detect MTC early on
before they have grown larger than 10 mm.
2. Central and lateral node metastases on the
same side of the neck are found equally often
(Table 13.2) [14, 117]. Nevertheless, lympha-
tic spread is a gradual process which is
dependent on the number of positive nodes:
with one to three positive central nodes,
involvement of the ipsilateral lateral neck
increased from 10 to 77%, reaching 98%
with four or more positive central nodes
[118]. These data suggest that, at the very
least, both the central neck compartment
and the lateral neck compartment on the
side of the primary tumor should be dis-
sected when a single positive node is identi-
fied in the central neck.
3. The risk of lateral node metastases in the
contralateral neck and the mediastinum
increases with the size of the primary tumor
[117, 119], with multifocal tumor growth in
the thyroid gland [120], and with the number
Table 13.2. Involvement of central, lateral, and mediastinal compartments in MTC 10 mm versus >10 mm
Maximum primary tumor diameter
10 mm >10 mm
Central Lateral Central Lateral
Ipsilateral Contralateral Ipsilateral Contralateral Mediastinal Ipsilateral Contralateral Ipsilateral Contralateral Mediastinal
LYMPH NODE DISSECTION IN THYROID CANCER
179
First surgery (%)
14 3 11 0 0 46 39 58 33 27
(n = 68)
Reoperative surgery (%)
56 19 50 19 0 60 31 49 22 23
(n =93)
Source: Adapted from Machens A, Hinze R, Thomusch O, Dralle H. Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg. 2002;26:22–28. Reprinted with kind permission of
Springer Science and Business Media.