Lymph Node Dissection
in Papillary Thyroid Carcinoma
Tracy-Ann S. Moo, MD, and Thomas J. Fahey III, MD
The management of papillary thyroid carcinoma continues to evolve. Although the debate
over the extent of thyroidectomy has largely faded, the role of elective neck dissection in
the surgical management of papillary thyroid cancer has become a topic of contention. The
current standard of care for patients with papillary thyroid cancer includes total thyroidectomy and a therapeutic lymph node dissection for patients presenting with clinically evident
nodal disease. However, many surgeons advocate prophylactic central neck lymph node
dissections in patients who present with no clinical or radiographic evidence of lymph node
involvement. Proponents of prophylactic central compartment neck dissection argue that
the incidence of central neck metastases is high and the sensitivity of preoperative
ultrasound is low. Furthermore, central neck dissection advocates argue that clearing the
central neck at the initial operation improves staging accuracy, assists in deciding on
postoperative radioactive iodine treatment, and potentially avoids a higher-risk reoperative
central neck dissection. Selective lateral neck dissections, as well as modified radical neck
dissections, are accepted as necessary therapy in patients with clinically or radiographically positive lateral compartment disease. An essential component of any discussion on
the extent of lymphadenectomy is whether patients derive any additional benefit from
having a lymphadenectomy with total thyroidectomy and whether this can be done without
significantly increasing the morbidity of the operation. Here we discuss the surgical options
for approaching lymphadenectomy in patients presenting with papillary thyroid carcinoma.
Semin Nucl Med 41:84-88 © 2011 Elsevier Inc. All rights reserved.
P
apillary thyroid cancer accounts for approximately 90%
of thyroid malignancies and continues to have an excellent prognosis, despite increasing in incidence during the
past decade.1 However, lymph node metastases are common
and have been reported in up to 90% of patients with papillary thyroid carcinoma.2,3 Many patients will present with
subclinical nodal disease that is not detectable by ultrasonography or physical examination, and the sensitivity of preoperative ultrasound for central neck lymph node metastases is
reported as low as 10%.4 In the past, it was believed that there
was no prognostic significance to lymph node involvement.
However, more recent evidence demonstrates that the presence of lymph node metastases are associated with an increased risk of locoregional recurrence, and in older patients
may be associated with a greater risk of death from thyroid
cancer.3,5-7 As such, the necessity for and extent of lymph
node dissection have emerged as a controversial topic.
New York Presbyterian Hospital, Cornell, New York, NY.
Address reprint requests to Tracy-Ann Moo, MD, Weill Cornell Medical
College, 525 East 68th Street F-2024, New York, NY 10065. E-mail:
[email protected].
84
0001-2998/11/$-see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1053/j.semnuclmed.2010.10.003
It is widely accepted that current surgical therapy for papillary thyroid carcinoma should include total thyroidectomy
and therapeutic central neck dissection (CND) in those patients who present with clinically evident positive lymph
nodes (Fig. 1). In these cases the level VI lymph nodes are
removed. The dissection is carried out from the hyoid bone
superiorly to the suprasternal notch inferiorly and is bordered laterally by the carotid sheaths and dorsally by the
prevertebral fascia. This generally encompasses the area of
initial spread of metastases through draining lymphatic channels of the thyroid. There have been reports of skip metastases—that is direct metastases to the lateral neck— however,
this is probably rare and usually associated with carcinomas
arising in the superior poles.8 Prophylactic dissections of the
central neck—that is routine CND in patients without clinically evident signs of nodal disease by physical examination
or preoperative imaging—is more controversial because
CND is not without morbidity. Within this compartment lie
the parathyroid glands and the recurrent laryngeal nerves,
and the added dissection potentially increases the possibility
of hypoparathyroidism or recurrent nerve injury when performing a total thyroidectomy with CND vs. thyroidectomy
alone.9,10
LN dissection in papillary thyroid carcinoma
85
currence rate of 33%, and the authors found that the greatest
rates of recurrence were among those patients who had had a
berry-picking approach to cervical lymphadenectomy. In addition, we now know that routine CND can be performed
safely with low rates of permanent hypoparathyroidism as
well as recurrent laryngeal nerve injury.12,16 Although the
authors of previous studies quoted high rates of hypoparathyroidism as well as recurrent laryngeal nerve injury, more
recent data has demonstrated that central neck lymph node
dissections can be done with minimal morbidity. Grant et al
examined a series of 420 patients with papillary thyroid carcinoma who underwent thyroidectomy with CND and reported a 1.2% incidence of hypoparathyroidism and only 1
case of recurrent laryngeal nerve injury.10,12
Prophylactic Central
Neck Lymph Node Dissection
Figure 1 Central neck lymph node dissection area.
The surgical management of papillary thyroid carcinoma
now focuses on the prevention of locoregional recurrence as
well as on long-term survival. Proponents of prophylactic
central compartment dissection argue that in addition to potentially avoiding the morbidity of a reoperation, prophylactic dissections provide more accurate staging which facilitates
decisions regarding postoperative radioactive iodine treatment, as well as long term follow-up with thyroglobulin levels. Recent American Thyroid Association guidelines advocate the consideration of prophylactic central neck lymph
node dissection in patients with papillary thyroid carcinoma
and more so in patients with T3 or T4 primary lesions.11
Therapeutic Central
Neck Lymph Node Dissection
In patients who present with clinically evident disease, the
standard of care is to perform a therapeutic neck dissection,
which entails the systematic removal of the lymph nodes in
the central compartment (level VI). It is thought that this
reduces rates of lymph node recurrence as it has been shown
that a large number of nodal recurrences occur in the central
neck.12,13 It is widely accepted that a “berry-picking” approach to clinically positive lymph nodes is not an acceptable
approach and results in high rates of locoregional recurrence.14,15 Davidson et al,15 in a review of one institution’s
experience, examined 183 patients treated for papillary thyroid carcinoma with thyroidectomy and various methods of
lymphadenectomy. In this study population there was a re-
Although there are no prospective randomized controlled
studies demonstrating the efficacy of prophylactic central
neck lymph node dissection, in many centers it is performed
routinely. The rationale is that it reduces the morbidity associated with a potential reoperation, reduces the risk of central
neck lymph node recurrence, provides more accurate information for staging, and facilitates postoperative radioactive
iodine administration as well as long term follow-up. At the
heart of the controversy is the fact that central neck lymph
node metastases are common in papillary thyroid cancer. In
tumors that are ⬎1 cm, central neck lymph node metastases
are found in 40 to almost 90% of cases. Even in papillary
microcarcinoma the rate of lymph node metastases has been
reported in 25%-45% of cases.17,18 Bonnet et al19 recently
examined the importance of the status of the central neck
lymph nodes to postoperative management, even in small
PTC. Bonnet retrospectively reviewed 115 patients with papillary thyroid carcinoma and a tumor size ⬍2 cm without
ultrasonographic evidence of lymph node metastases preoperatively who underwent prophylactic CND. Information
provided by knowing the pathologic stage of the central neck
lymph nodes changed the staging for 30% of patients initially
staged as T1N0, and ultimately modified the indication for
radioactive iodine ablation in these patients.
Opponents of prophylactic CND argue that the presence of
positive lymph nodes does not affect prognosis and survival
in papillary thyroid carcinoma.20-22 For example, Shaha et
al21 performed a retrospective review of 810 patients looking
at prognostic factors, and found that while female sex, young
age, extracapsular extension and low grade histology were
favorable prognosticators, the presence of positive lymph
nodes had no effect on prognosis. Although the authors of
many older studies demonstrated that survival was not affected by the presence of metastatic lymph nodes, nodal disease has been associated with a significantly increased recurrence in more recent studies. Hughes et al23 performed a
matched-pair analysis of 100 patients with previously untreated papillary thyroid carcinoma with and without lymph
node involvement. In this study he looked at the significance
86
of nodal disease in patients with otherwise equivalent prognostic factors and found that while there was no difference in
survival, patients with nodal involvement did have a higher
rate of recurrence, and in patients over 45 years this difference was statistically significant. Additional studies also support the findings of Hughes, et al that lymph node metastasis
increases the rate of locoregional recurrence.5,6,15,24 Furthermore, recent evidence from examination of a large database
indicates that lymph node metastasis can be associated with a
negative impact on survival. Lundgren, et al performed a
nested-case control study and looked at 5123 patients diagnosed with differentiated thyroid cancer. The authors report
that patients with lymph node metastases had a significantly
higher mortality than those without.6
There is also emerging evidence that prophylactic CND
may lead to reduced central neck recurrence. Grant et al12
reviewed 420 patients who had undergone an “optimized”
surgical approach to papillary thyroid carcinoma. These patients all had preoperative ultrasounds to specifically assess
for central and lateral compartment lymph node involvement
and then underwent bilateral thyroidectomy, routine central
neck lymph node dissection and selective lateral neck dissection (compartments III, IV, and V) in those patients with
positive lymph nodes detected by ultrasonography or palpation preoperatively. The authors report a locoregional recurrence rate of only 5% in the previously operated field. Similarly, data from our own institution corroborates these
findings. We performed a retrospective review of 81 patients
presenting with papillary thyroid cancer without clinical evidence of nodal disease. Thirty-seven of these patients underwent thyroidectomy alone whereas 45 underwent thyroidectomy with prophylactic lymph node dissection. Our results
demonstrated a 4.4% locoregional recurrence rate in patients
who had a prophylactic CND compared with 16.7% recurrence rate for patients undergoing thyroidectomy alone.16
These data, however, have yet to be supported by prospective
trials.
Operative morbidity is a major concern in proposing more
widespread adoption of routine prophylactic neck dissection. Though in experienced hands CND has low rates of
both permanent hypoparathyroidism and permanent recurrent laryngeal nerve injury, there are clearly higher rates of
temporary hypoparathyroidism and recurrent laryngeal
nerve injury. In our experience with patients undergoing
total thyroidectomy with prophylactic CND vs. total thyroidectomy alone, there was a significantly higher rate of temporary hypoparathyroidism in those patients who had CND,
31% versus 5% (P ⫽ 0.001; Fig. 2). Because most thyroid
surgery in the United States is performed by surgeons who do
fewer than 10 thyroidectomies per year,25 there is considerable concern that in the hands of less-experienced surgeons,
the incidence of permanent hypoparathyroidism or injury to
the recurrent laryngeal nerves would increase substantially.
Nevertheless, proponents of prophylactic CND point to the
greater risks of hypoparathyroidism and recurrent laryngeal
nerve injury in reoperative central neck surgery as a justification for attempting to clear central neck disease at the initial operation.26-28
T.-A.S. Moo and T.J. Fahey
Figure 2 Complication rates in patients undergoing total thyroidectomy with and without CND.
In an effort to minimize the potential morbidity of a CND,
there have been studies looking into the efficacy of a CND
carried out only on the side of the tumor. Data from our
institution and others demonstrate that tumors ⬍1 cm rarely
metastasize to the contralateral central neck lymph nodes.
We performed a prospective study of central neck lymph
dissection in 116 patients. In patients with tumors ⬍1 cm
compared with those with tumors ⬎1 cm, there was 0%
versus 31% (P ⫽ 0.02) incidence of bilateral lymph node
metastasis.18 In the subset of patients with tumors ⬍1 cm, an
ipsilateral CND may be a viable alternative and should provide the additional information gained from staging the central neck lymph nodes, while at the same time reducing the
additional risk of CND.
Selective Lateral
Neck and Modified
Radical Neck Dissection
A selective lateral neck dissection includes the lymph nodes
of levels III, IV, and V. However, this dissection usually does
not extend posterior to the sternocleidomastoid muscle and
to the border of the trapezius. It is generally agreed that this
should be performed in the presence of clinically apparent
disease and in conjunction with a central compartment dissection (Fig. 3). Patients who present with clinically positive
lateral lymph nodes by examination or ultrasound are also
likely to have central compartment disease. Pereira, et al
found that patients with positive lateral neck lymph nodes
had at least 6 positive central neck nodes at lymphadenectomy.29 There appears to be no role for prophylactic lateral
neck dissections as the lateral compartment is not usually
entered during thyroidectomy and can be operated on without greater morbidity if necessary in the future. Vergez et al
retrospectively looked at 90 patients who had undergone
prophylactic central and lateral neck dissection at the time of
thyroidectomy to determine pattern of lymph node involvement. They found that 62/90 patients who had lateral neck
dissection had no lymph node involvement, and all patients
with positive lateral neck lymph nodes also had positive cen-
LN dissection in papillary thyroid carcinoma
Figure 3 Approach to lymph node dissection in papillary thyroid
carcinoma. PTC, papillary thyroid carcinoma; LNM, lymph node
metastasis; CND, central neck dissection; MRND, modified radical
neck dissection. (Color version of figure is available online.)
87
sound. Therapeutic CNDs are preformed routinely with minimal morbidity in the hands of experienced surgeons. Although
there is a current paucity of data demonstrating a clear decrease
in recurrence for prophylactic CND, it should be considered in
all patients presenting for treatment of papillary thyroid carcinoma. Perhaps an ipsilateral CND may be sufficient in patients
with papillary microcarcinomas. The addition of central neck
dissection to thyroidectomy is beneficial for achieving completeness of disease resection and can provide important information
regarding tumor staging, thus facilitating postoperative management and long-term follow up. Selective lateral neck dissection
and modified radical neck dissections should be performed
when there is clinical evidence of nodal disease in the lateral
neck compartments.
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positive lymph nodes in the lateral neck is quite high.30
Modified radical neck dissection usually includes a dissection of lymph nodes in compartments II through V. In contrast to a radical neck dissection, the sternocleidomastoid
muscle, spinal accessory nerve and internal jugular vein are
preserved. Even so, the morbidity of this operation is high,
with rates of shoulder dysfunction secondary to spinal accessory nerve injury reported in up to 30%.31 Although some
centers advocate full modified radical neck dissection when
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Future controversy is likely to revolve around the use of
lateral compartment neck dissections in patients with subclinical lymph node metastases in the lateral neck. This population of patients is likely to increase in size as preoperative
lateral neck ultrasonography becomes more widely employed in the initial evaluation of patients with papillary thyroid cancer.
Conclusions
Decisions regarding lymphadenectomy in papillary thyroid
carcinoma remain controversial. This is especially the case in
patients presenting with no clinical evidence for lymph node
metastases by physical examination or preoperative ultra-
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