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Int Surg 2010;95:142-146
Lymph Node Surgery in Papillary
Thyroid Carcinoma
Derya Karakoc \ Arif Ozdemir
1 Lecturer
2
2
of General Surgery, and Professor of General Surgery, Department of General Surgery, Hacettepe
University Medical School, Ankara, Turkey
Papillary thyroid carcinoma is the most common type of thyroid cancer, and cervical
lymph node metastasis of the disease is high. Lymph node surgery of the papillary
thyroid carcinoma is controversial because of the good prognosis of the disease.
Although controversy continues on prophylactic lymph node dissection, therapeutic
lymph node dissection is recommended in all guidelines for patients who have known
lymph node metastases.
Key words: Papillary thyroid carcinoma- Lymph node- Surgery
P type of thyroid cancer. It represents 75% of all
detectable lymph node metastasis occurs in around
4
15% to 30% of cases. Occult lymph node metastasis
entiated
sis in clinically node-negative patients is 50%,5 and
apillary thyroid carcinoma is the most common
thyroid malignancies and more than 90% of differ­
1
thyroid cancers.
An increase in the
is reportedly as high as 90%. Lymph node metasta­
incidence of papillary thyroid carcinoma during
2
lymph node metastasis in papillary thyroid micro­
Management of the papillary thyroid carcinoma is
carcinoma 10 mm or less in diameter, occurs at 15%
6 s
to 50%. -
past decades has increased interest in the disease.
controversial because of the lack of prospective
carcinoma, which is defined as papillary thyroid
randomized studies and the excellent prognosis of
the disease. The cause-specific 10-year survival rate
for papillary thyroid carcinoma is 95%.3 Despite
slow tumor growth and a good prognosis, the major
challange involves controlling locoregional recur­
rence. This is why lymph node surgery is considered
important in the treatment of papillary thyroid
carcinoma.
The incidence of cervical lymph node metastasis
is high in papillary thyroid carcinoma. Clinically
Effects of Lymph Node Metastases on
Recurrence and Survival
Patients
who
have
lymph
node
metastases
at
presentation have a higher incidence of recurrent
disease in the cervical region.9 The presence of
metastatic nodes at the time of initial examination is
associated with a 10-fold increase in the risk of
1°
developing a nodal recurrence.
Cervical recur-
Reprint requests: Derya Karakoc, MD, Hacettepe Universitesi Tip Fakultesi, Gene! Cerrahi AD 06100, Sihhiye, Ankara, Turkey.
Tel.: +9 0 312 305 1676, +9 0 532 562 5747; Fax: +9 0 312 385 4983; E-mail: Derykarakoc@yahoo.com
142
Int Surg 2010;95
KARAKOC
LYMPH NODE SURGERY IN PAPILLARY THYROID CARCINOMA
renee is seen in 20% of patients with low-risk
reported in the literature. In most cases, retropha­
papillary thyroid carcinoma and in 60% of those
ryngeal metastasis is associated with other cervical
the tumor, male gender, and older age are among
normal pattern of lymph flow secondary to these
with high-risk diseaseY Extrathyroidal extension of
the factors that contribute to recurrence of the
disease
in
the
presence
of
nodal
metastases.12
Residual metastatic lymph nodes that remain after
initial therapy
are the most
subsequent recurrence.13•14
common cause of
It remains controversial whether the presence of
lymph node metastases, either overt or occult, has
an impact on prognosis. Traditionally, it has been
suggested that the presence of regional metastases
has no effect on survival.15•16 However, studies have
reported
that
lymph
node
metastases
decrease
survival, and this is even prominent among elderly
patients.17•18
the
estimated
lymphatic
drainage of
thyroid carcinoma is central cervical compartment
metastasis followed by lateral cervical compartment
metastasis. However, the metastatic pathways may
be unpredictable, and skip metastasis may occur.
For papillary thyroid carcinoma, central nodal
metastasis was found to be 76%, lateral nodal
the
Age, sex, tumor size, and histopathologic properties
of the tumor are among the most studied parameters
predicting lymph node involvement of the papillary
thyroid carcinoma.
Although age younger than
20 years and older than 45 years, male gender, and
increasing tumor size are proposed to predict lymph
node metastasis, absence of the tumor capsule and
perithyroidal extension are believed to be more
clinicopathologic
primary tumor size.2° For papillary thyroid micro­
carcinoma, central and lateral nodal metastases were
found in 64% and 45%, respectively, with a 5% skip
American Joint Comittee on Cancer and the Amer­
Neck Surgery25:
metastasis may be seen in 30% of patients.
Level III:
For central lymph node metastasis, pretracheal
frequent
paratracheal lymph node metastasis, and for lateral
than
upper
level
ones.
Level IV:
Tumor
position of the metastatic spread. Tumors in the
the spinal accessory nerve.
Lymph nodes that are located lateral to
the spinal accessory nerve.
Lymph nodes that are located between
the levels of the hyoid bone and the
This level is the
middle jugular region.
Lymph nodes that are located between
the level of the cricoid cartilage and the
clavicle.
position within the thyroid gland may affect the
isthmus, middle, and lower parts of the gland
Lymph nodes that are located medial to
cricoid cartilage.
than
lymph node metastasis, mid-lower level nodes are
Lymph nodes that are located above the
level of the hyoid bone to the base of
region.
Level IIA:
metastasis rate.5 Contralateral central lymph node
19%. Bilateral lymph node
Submental and submandibular lymph
nodes.
the skull. This level is the upper jugular
Level liB:
frequent
be
ican Academy of Otolaryngology and Head and
was found to be increased with an increase in
more
to
The most widely used cervical lymph node classi­
lateral compartments, and contralateral involvement
is
found
fication system is based on recommendations by the
Level II:
was found to occur at 7%.19 Contralateral metastasis
metastasis
is
Surgical Anatomy of Cervical Lymph
rates were reportedly 13% and 3% for central and
metastasis is 5% to
parameter
Node Compartments
Level I:
more
of
Predictive Factors for Lymph Node Metastases
metastasis was found to be 65%, and skip metastasis
node
alteration
other metastases?1•22
no
The thyroid gland is located in the central neck, and
lymph
representing
predictive of lymph node metastasis.24
lymphatic drainage follows venous drainage of the
so
likely
important. 23 For papillary thyroid microcarcinoma,
Pattern of Lymph Node Metastases
gland,
metastases,
This
is
the
lower jugular
region.
Level V:
Lymph nodes that are located in the
metastasize most often to the central nodes, and
posterior triangle. This level also in­
often to the ipsilateral lateral nodes.
Lymph nodes that are located in the
tumors in other parts of the gland metastasize most
Retropharyngeal nodes represent a rare site of
nodal metastasis in thyroid cancer. Few cases are
Int Surg 2010;95
cludes the supraclavicular lymph nodes.
Level VI:
central area, posterior and inferior to
the thyroid gland and adjacent to the
143
KARAKOC
LYMPH NODE SURGERY IN PAPILLARY THYROID CARCINOMA
trachea and esophagus. This compart­
ment includes the pretracheal nodes,
paratracheal nodes, precricoid
node
Berry Picking: In this procedure, only suspicious
enlarged lymph nodes are removed. This
and
procedure has lost its popularity.
(Delphian), perithyroidal nodes, and
lymph nodes along the recurrent laryn­
geal nerve.
Level
VII:
These are
the superior mediastinal
lymph nodes.
Central Compartment: Includes level VI lymph
nodes.
Lateral Compartment: Includes level II to level IV
lymph nodes.
tried for papillary thyroid cancer.26 Methylene blue,
isosulfan blue, patent blue, or radiocolloid may be
�
sentinel lymph node biopsy can guide com art­
lymph nodes in the neck. During the procedure, the
sternocleidomastoid muscle,
the internal jugular
vein, and the spinal acceessory nerve are removed.
This procedure was first described in 1906; later it
was modified because of the unwanted cosmetic
results and shoulder dysfunction caused by sacrifice
of the spinal accessory nerve.
Mod ified Radical Neck Dissection: Is also called
functional neck dissection. In this procedure, the
sternocleidomastoid muscle, internal jugular vein,
carotid artery, vagus, phrenic and spinal accessory
submandibular
salivary glands
are
preserved to decrease the morbidity of the radical
neck dissection.
Type I:
Preservation of the spinal accessory nerve.
Type II:
Preservation of the spinal accessory nerve
and internal jugular vein.
Type III:
Sentinel lymph node biopsy, which is used fre­
quently for breast cancer and melanoma, has been
ment-oriented cervical lymph node dissection?
Radical Neck Dissection: Includes the removal of all
and
Sentinel Lymph Node Biopsy: The sentinel lymph node
is defined as the first lymph node draining a tumor.
used to perform the procedure. When positive,
Types of Cervical Lymph Node Dissection
nerves,
Newer surgical approaches
Preservation of the spinal accessory nerve,
internal jugular vein, and sternocleido­
mastoid muscle.
Selective Neck Dissection: Preserves some lymph
node groups. The procedure has 2 subgroups for the
treatment of papillary thyroid carcinoma.
Central Compartment Lymph Node Dissection: In this
procedure, the lymph nodes and the soft tissues in
level VI are removed. During the procedure, the
recurrent laryngeal nerve is preserved.
Lateral Compartment Lymph Node Dissection: In this
procedure, the lymph nodes and the soft tissues
from the lateral wall of the carotid sheath to the
trapezius muscle and from the subclavian vein
inferiorly to the hypoglossal nerve superiorly are
excised. During the procedure, levels IIA, III, IV, and
V are removed. In patients with obvious metastatic
Video-Assisted Cervical Lymph Node Dissection: This
technique has been proposed for better cosmetic
outcorne?8 However, experience with this proce­
dure is very limited, and the oncologic outcome is
controversial. New data are needed for long-term
results of this procedure.
Surgical Strategy
Prophylactic lymph node dissection
Prophylactic lymph node dissection is dissection of
the cervical lymph nodes with no evidence of lymph
node metastasis. The role of prophylactic lymph
node dissection in the management of papillary
thyroid carcinoma is highly controversial because
the effect of lymphatic metastasis on survival is
controversial, and potential surgical complications
are not few.
Prophylactic lymph node dissection may not be
preferred because the nodal recurrence rate may not
be different between the lymph node dissection and
no-dissection groups.5•29 On the other hand, pro­
phylactic central cervical lymph node dissection is
advised by the European Thyroid Association, the
British
Thyroid
Association,
and
the
American
Thyroid Association.30•31 One potential benefit of
routine central cervical lymph node dissection may
be the accurate staging of the tumor, which may
guide subsequent treatment and follow-up. The
procedure may decrease the recurrence of papillary
thyroid carcinoma, improve disease-specific surviv­
al, and significantly reduce levels of serum thyro­
globulin, increasing the rate of athyroglobulinemia.32
However, it should be remembered that the rate of
permanent hypothyroidism and unintentional per­
manent nerve injury is higher when cervical lymph
disease at level VI, levels VI and VII can also be
node dissection is performed with total thyroidecto­
removed.
my than with total thyroidectomy alone.32
144
Int Surg 2010;95
KARAKOC
LYMPH NODE SURGERY IN PAPILLARY THYROID CARCINOMA
In
the
process
of
surgical
decision
making,
3.
Hay 10, Thompson GB, Grant CS, Bergstralh EL Dvorak CE,
possible benefits should always be weighed against
Gorman CA et al. Papillary thyroid carcinoma managed at the
potential morbidity. Because survival is favorable
Mayo Clinic during six decades
for papillary thyroid carcinoma, local recurrence is
in initial therapy and long term outcome in
considered an important parafY1eter for long-term
tively treated patients. World J Surg
follow-up.
The
impact
of
central
compartment
4.
recurrence differs from that of the lateral compart­
ment.
Reoperation
for recurrence
temporal trends
2444
consecu­
2002;26(8):879-885
Shaha AR, Shah JP, Loree TR. Patterns of nodal and distant
metastasis based on histologic varieties in differentiated
in the lateral
compartment can be performed more easily than
(1940-1999):
carcinoma of the thyroid. Am J Surg
5.
1996;172(6):692-694
Wada N, Duh QY, Sugino K, Iwasaki H, Kameyama K,
that for recurrence in the central compartment,
Mimura T et al. Lymph node metastasis from
where more critical structures are located. Reoper­
thyroid microcarcinomas: frequency, pattern of occurrence
ation in the central neck compartment for recurrent
and recurrence, and optimal strategy for neck dissection. Ann
papillary thyroid carcinoma may increase the risk of
hypoparathyroidism and unintentional nerve inj ury
259
papillary
Surg 2003;237(3):399--407
6.
Schonberger L Marienhagen L Agha A, Rozeboom S,
when compared with total thyroidectomy with or
32
without cervical lymph node dissection. Therefore,
Bachmeier E, Schlitt H et al. Papillary microcarcinoma and
because metastases in the central compartment are
46(4):115-120
very common, and given that surgery for recurrence
papillary cancer of the thyroid
7.
in the central compartment may be a complicated
Prophylactic
indicated
for
lymph
node
papillary
dissection
thyroid
may
Sakorafas GH, Giotakis L Stafyla V. Papillary thyroid
Ito Y, Tomoda C, Uruno T, Takamura Y, Miya A, Kobayashi K
et
al.
Clinical significance of metastasis to the central
compartment from papillary microcarcinoma of the thyroid.
microcarcinoma
World J Surg 2006;30(10):91-99
9.
extension, and is greater than 5 mm. Sentinel lymph
Cognetti OM, Pribitkin EA, Keane WB. Management of the
neck in differentiated thyroid cancer. Surg Oneal Clin N Am
node biopsy may also be used for these patients.
Prophylactic lateral neck dissection is not recom­
2007;
2005;31(6):423--438
8.
be
when the disease is multifocal, has extrathyroidal
1cm. Nuklearmedizin
microcarcinoma: a surgical perspective. Cancer Treat Rev
procedure, prophylactic central cervical lymph node
dissection during the initial thyroid surgery may be
27
a logical surgical option.
:5
2008;17(1):157-173
10.
McConahey WM, Hay 10, Woolner LB, van Heerden JA,
mended for patients with papillary thyroid carcinoma.
Taylor WF. Papillary thyroid cancer treated at the mayo
Therapeutic lymph node dissection
findings, therapy, and outcome. Mayo Clin Proc
clinic,
Therapeutic lymph node dissection is dissection of
1946
through
1970:
initial manifestations, pathologic
1986;61(12):
978-996
11.
Cady B, Rossi R. An expanded view of the risk-group
the cervical lymph nodes when cervical lymph node
definition in differentiated thyroid carcinoma. Surgery
metastasis is suspected or shown intraoperatively or
104(6):947-953
preoperatively by clinical or radiologic examination.
12.
Performance of a therapeutic cervical lymph node
Hughes CJ, Shaha AR, Shah JP, Loree TR. Impact of lymph
node metastasis in differentiated carcinoma of the thyroid: a
dissection is based on the fact that regional disease
control is necessary to prevent morbidity from local
1988;
matched-pair analysis. Head Neck
13.
1996;18(2):127-132
Chow SM, Law SC, Chan JK, Au SK, Yau S, Lau WH.
tumor growth, to maintain quality of life, and to
Papillary microcarcinoma of the thyroid: prognostic signifi­
maximize disease-free and possibly overall survival.
cance of lymph node metastasis and multifocality. Cancer
This concept is well accepted in the treatment of
papillary thyroid carcinoma. Compartment-oriented
2003;98(1):31--40
14.
Pereira JA, Jimeno L Miquel L Iglesias M, Munne A, Sancho JJ
lymph node dissections are recommended in all
et al.
guidelines for patients with known lymph node
7
metastases ?
dissection for papillary thyroid carcinoma. Surgery
Mazzaferri EL, Jhiang SM. Long-term impact of initial
surgical and medical therapy on papillary and follicular
References
2.
2005;
138(6):1095-1100
15.
1. Gosnell JE, Clark OH. Surgical approaches to thyroid tumors.
Nodal yield, morbidity, and recurrence after central neck
thyroid cancer. Am J Med
16.
1994;97(5):418-428
Leboulleux S, Rubino C, Baudin E, Caillou B, Hartl OM,
Endocrinol Metab Clin North Am 2008;37(2):437--455
Bidart JM et a/. Prognostic factors for persistent or recurrent
Sosa JA, Udelsman R. Papillary thyroid cancer. Surg Clin
disease of papillary thyroid carcinoma with neck lymph node
North Am 2006;15(3):585-601
metastases and I or tumor extension beyond the thyroid
Int Surg 2010;95
145
LYMPH NODE SURGERY IN PAPILLARY THYROID CARCINOMA
KARAKOC
capsule at initial diagnosis. J Clin Endocrinol Metab 2005;90
25. Robbins KT, Clayman G, Levine PA, Medina J, Sessions R,
Shaha A et al. Neck dissection classification update: revisions
(10):5723-5729
The
proposed by the American Head and Neck Society and the
implication of lymph node metastasis on survival in patients
American Academy of Otolaryngology and Head and Neck
17. Podnos YD,
Smith D, Wagman LD, Ellenhorn JD.
with well-differentiated thyroid cancer. Am Surg 2005;71(9):
731-734
18. Zaydfudim V, Feurer ID, Griffin MR, Phay JE. The impact of
lymph
Surgery. Arch Otolaryngol Head Neck Surg 2002;128(7):751-758
26. Dzodic R.
node
involvement
on
survival
in
papillary and follicular thyroid carcinoma.
patients
with
Surgery 2008;
144(6):1070-1077
Sentinel lymph node biopsy may be used to
support the decision to perform
modified
radical neck
dissection in differentiated thyroid carcinoma. World J Surg
2006;30(5):841-846
27. Sakorafas GH, Sampanis D, Safioleas M. Cervical lymph node
19. Wada N, Masuda K, Nakayama H, Suganuma N, Matsuzu K,
dissection in papillary thyroid cancer: current trends, persist­
Hirakawa S et al. Clinical outcomes in older or younger
ing controversies, and unclarified uncertainties. Surg Oneal
patients with papillary thyroid carcinoma: impact of lymph­
adenopathy and patient age. Eur J Surg Oneal 2008;34(2):
202-207
20. Machens A, Hinze R, Thomusch 0, Dralle H. Pattern of nodal
metastasis for primary and reoperative thyroid cancer. World J
Surg 2002;26(1):22-28
2009 May 15 (Epub ahead of print)
28. Miccoli P, Materazzi G, Berti P. Minimally invasive video­
assisted lateral lymphadenectomy: a proposal. Surg Endosc
2008;22(4):1131-1134
29. Roh JL, Park JY, Park CI. Total thyroidectomy plus neck
dissection
in
differentiated
papillary
thyroid
carcinoma
21. Otsuki N, Nishikawa T, Iwae S, Saito M, Mohri M, Nibu K.
patients: pattern of nodal metastasis, morbidity, recurrence,
Retropharyngeal node metastasis from papillary thyroid
and postoperative levels of serum parathyroid hormone. Ann
carcinoma. Head Neck 2007;29(5):508-511
Surg 2007;245(4):604--{)10
22. Ort S, Goldenberg D. Management of regional metastases in
30. Pacini F, Schlumberger M, Dralle H, Ilisea R, Smith Y,
well differentiated thyroid cancer. Otolaryngol Clin North Am
Viersinga V. European consensus for the management of
2008;41(6):1207-1218
23. Mirallie E, Sagan C, Hamy A, Paineau J, Kahn X, Le Neel JC
patients with differentiated thyroid carcinoma of the follicular
epithelium. Eur J Endocrinol 2006;154(6):787-803
et al. Predictive factors for node involvement in papillary
31. Grubbs EG, Rich TA, Li G, Sturgis EM, Younes MN, Myers JN
thyroid carcinoma: univariate and multivariate analyses. Eur J
et al. Recent advances in thyroid cancer. Curr Probl Surg
Cancer 1999;35(3):420-423
2008;45(3):156-250
24. Roh JL, Kim JM, Park CI. Central cervical node metastases from
32. White ML, Gauger PG, Doherty GM. Central lymph node
papillary thyroid microcarcinoma: pattern and factors predic­
dissection in diffrentiated thyroid carcinoma. World J Surg
tive of nodal metastasis. Ann Surg Oneal 2008;15(9):2482-2486
2007;31(5):895-904
146
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