Invest Clin 64(2): 173 - 183, 2023 https://doi.org/10.54817/IC.v64n2a04
Corresponding author: Qinghong Qu. Department of Ultrasound Imaging, The First
People’s Hospital of Wenling,
Wenling, Zhejiang, China. Phone: +86013758658813. Email: quqinghongh@163.com
The sonographic features of preoperative
ultrasonography of metastatic tumors
of thyroid cancer confirmed by surgical
pathology.
Lingling Ruan1, Qingxin Zhang2 and Qinghong Qu
1Department of Ultrasound Imaging, The First People’s Hospital of Wenling, Wenling,
Zhejiang, China.
2Department of Critical Medicine, The First People’s Hospital of Wenling, Wenling,
Zhejiang, China.
Keywords: surgical pathology; thyroid cancer; metastatic lesions; ultrasonography;
sonographic features.
Abstract. This study aimed to analyze the sonographic features of metastatic
tumors
in patients with thyroid cancer that underwent preoperative ultrasonogra-
phy. One hundred and three thyroid cancer patients whose metastases were con-
firmed by surgical pathology in The First People’s Hospital of Wenling from January
2020 to
December 2021 were enrolled. All patients received preoperative ultra-
sound
examinations, and the sonographic features were analyzed. Ultrasound ex-
amination
showed 83.50% of cervical lymph node metastasis (CLNM), 24.27% of
soft tissue
invasion (STI), 3.88% of distant organ metastasis (DOM), 8.74% of CLNM
+ STI, 0.97% of CLNM + DOM, and 0.97% of CLNM + STI+DOM. Unilateral CLNM
accounted for 72.09%, while bilateral CLNM accounted for 27.91%. The mean long
diameter of metastatic lymph nodes was (1.83±0.63) cm, and the mean short di-
ameter
was (1.03±0.42) cm. Metastases to zone II, III, IV, V, VI, and VII accounted
for 8.14%, 48.84%, 23.26%, 4.65%, 11.63%, and 3.49%, respectively. The L/T ratio
of lymph nodes in 65 cases was lower than 2; 45 of 70 solid metastases exhibited
solid
hyperechoic, 15 multifocal hyperechoic, seven unifocal hyperechoic, and three
diffusely distributed solid hyperechoic images. There were 25 patients with STI that
experienced invasion of the thyroid capsule, ten patients experienced the invasion
of the cervical fatty muscles, two patients had invasion of the trachea, and one pa-
tient
had invasion of the thyroid cartilage. Of the four patients with DOM, one had
parotid
metastasis, one had submandibular metastasis, one had axillary metastasis,
and one
had uterine metastasis. The most common metastatic sites of thyroid can-
cer are
cervical lymph nodes. However, there were also metastases in the soft tissues
and
distant organs. The ultrasonography exhibited typical sonographic features. An
adequate familiarity with these sonographic features can aid in detecting suspicious
metastases in time, which is crucial to the clinical diagnosis, treatment, and prog-
nostic
assessment.
174 Ruan et al.
Investigación Clínica 64(2): 2023
Características ecográficas de la ultrasonografía preoperatoria
de tumores metastásicos de cáncer de tiroides confirmados
por patología quirúrgica.
Invest Clin 2023; 64 (2): 173 – 183
Palabras clave: patología quirúrgica; cáncer de tiroides; lesiones metastásicas;
ultrasonografía; Características ecográficas.
Resumen. Este estudio tuvo como objetivo analizar las características
ecográficas de
tumores metastásicos en pacientes con cáncer de tiroides
que se sometieron a una
ultrasonografía preoperatoria. Se inscribieron 103
pacientes con cáncer de tiroides
cuyas metástasis fueron confirmadas por
patología quirúrgica en el primer Hospital
Popular de Wenling desde enero
de 2020 hasta diciembre de 2021. Todos los
pacientes recibieron un examen
de ultrasonido preoperatorio y se analizaron sus características ecográficas.
El examen de ultrasonido mostró 83,50% de metástasis de
ganglios linfáticos
cervicales (CLNM), 24,27% de invasión de tejidos blandos (ITS), 3,88% de me-
tástasis de órganos distantes (DOM), 8,74% de CLNM + ITS, 0,97% de
CLNM
+ DOM y 0,97% de CLNM + STI + DOM. La CLNM unilateral representó
un
72,09%, mientras que la CLNM bilateral representó el 27,91%. El diámetro
largo medio de los ganglios linfáticos metastásicos fue 1,83 ± 0,63 cm, y el
diámetro corto
medio fue 1,03 ± 0,42 cm. La metástasis a las Zonas II, III,
IV, V, VI y VII representan 8,14%, 48,84%, 23,26%, 4,65%, 11,63% y 3,49%,
respectivamente. La
relación L/T del ganglio linfático en 65 casos fue inferior
a 2. Cuarenta y cinco de 70 metástasis sólidas exhibieron hiperecoico sólido,
15 hiperecoico multifocal, 7 hiperecoico unifocal y 3 hiperecoico sólido dis-
tribuido difusamente. Hubo 25 pacientes con ITS experimentados por inva-
sión de la cápsula tiroidea, 10 pacientes
experimentaron invasión de los mús-
culos grasos cervicales, 2 pacientes con invasión
de la tráquea y 1 paciente con
invasión del cartílago tiroideo. De los 4 pacientes con
DOM, 1 tenía metástasis
parótidas, 1 tenía metástasis submandibulares, 1 tenía
metástasis axilares y 1
tenía metástasis uterina. Los sitios metastásicos más comunes
de cáncer de ti-
roides son los ganglios linfáticos cervicales. También hay metástasis en
los teji-
dos blandos y los órganos distantes. La ultrasonografía exhibió características
ecográficas típicas. La familiaridad adecuada con las características ecográficas
puede
ayudar a detectar metástasis sospechosas a tiempo, lo cual es clave para
el diagnóstico
clínico, el tratamiento y la evaluación pronóstica.
Received: 11-11-2022 Accepted: 28-12-2022
INTRODUCTION
The thyroid is a vital hormone gland
that critically impacts the body’s metabo-
lism. Thyroid cancer refers to malignant tu-
mors originating from the thyroid 1. Regar-
ding pathological types, papillary thyroid
carcinoma has the highest incidence
and a
higher degree of differentiation than other
types. However, it is less malignant,
resul-
ting in a relatively better prognosis. Patients
can survive longer, while local and
distant
Preoperative ultrasonography of metastatic thyroid cancer 175
Vol. 64(2): 173 - 183, 2023
metastases primarily invade the lymph no-
des 2. Evidence on metastasis of papillary
thyroid carcinoma found that the inciden-
ce of CLNM surpassed 80% 3. Another study
found that more than 60% of patients with
medullary thyroid
carcinoma already have
lymph node metastases in the neck when re-
ceiving surgery. In comparison, about 80%
of undifferentiated thyroid carcinomas will
induce lymph
node metastases 4.
Since thyroid cancer does not present
specifically in its early stage, most patients
see a doctor due to neck lumps and pal-
pable nodules. Some patients even have
swellings that have been present for years
upon consultation 5,6. Once local invasion
or
distant metastases occurs, the probability
of postoperative recurrence is
significantly
higher, severely increasing the risk of pa-
tient death 7. Metastasis of thyroid can-
cer is widely recognized as an independent
factor affecting prognosis 8. Thus, early
clinical detection of metastases in patients
with thyroid cancer can guide
physicians to
formulate a comprehensive treatment plan
and determine the efficacy as well as patient
prognosis by observing the metastatic le-
sions.
Ultrasound, as the most common
imaging method, has shown good value
in
clinical applications with simple ope-
ration and accurate results As diagnosis
and
treatment technologies advance, the
performance of ultrasound instruments is
gradually improved, and high-frequency ul-
trasound can not only show the internal
structure of the lesion but also visualize
the blood flow of the lesion site, which can
guide the clinical judgment of the nature
of the lesion 9,10. Most studies have explored
ultrasound’s role in examining thyroid can-
cer 11,12. However, there is a lack of research
on its effectiveness in the diagnosis of
metastatic thyroid cancer. This study was
conducted to investigate the value of the
preoperative implementation of ultrasound
in
103 patients with pathologically confir-
med metastatic thyroid cancer.
MATERIALS AND METHODS
Baseline data
One hundred and three thyroid cancer
patients whose metastases were confirmed
by surgical pathology in The First People’s
Hospital of Wenling from January 2020 to
December 2021 were enrolled, including 45
males and 58 females, with patient ages
ran-
ging from 22 to 71 years, with an average
age of 51.16±10.38 years. All patients
had
pathologically confirmed metastasis after
surgery and underwent preoperative
ultra-
sonography. All patients were aware of the
study procedures and voluntarily
signed the
study consent form. This study got ethical
approval from our hospital.
Methods
SONOLINE, a color Doppler ultrasound
diagnostic instrument (Type:
MylabClassC),
was used for examination with a probe fre-
quency set from 7.0 to 12.0 MHz. During the
examination, the patient lay in a supine po-
sition with the head
slightly tilted back, and
the shoulder and neck were elevated with soft
pillows to
ensure complete exposure of the
examined area. The parameter settings of the
color
Doppler diagnostic instrument were tu-
ned, and the patient’s position was adjusted
to
ensure the most satisfactory ultrasound
images. For patients diagnosed with metas-
tatic
thyroid cancer on ultrasonography, the
type and location of the metastasis were
re-
corded, and its characteristics, such as long
and short diameters, morphology, borders,
fusion, internal echogenicity, calcification,
cystic changes, and blood flow signals were
recorded. Metastases were typed according
to the metastatic patterns,
including Type I:
CLNM, Type II: STI, and Type III: DOM. The
subdivision of the
lymph nodes was comple-
ted according to the neck dissection classifi-
cation 13,14 (Fig. 1) and endorsed by the rele-
vant organizations and committees. If there
were
metastatic lymph nodes in a zone that
were present for more than one month, the
largest of these lymph nodes was examined.
176 Ruan et al.
Investigación Clínica 64(2): 2023
Outcome Measurements
The metastases of 103 patients with
thyroid cancer were analyzed. The
ultra-
sound features of metastatic lymph nodes,
including location, number, size,
morpho-
logy, and internal echogenicity, were analy-
zed. The ultrasound features of soft tissue
invasion and distant organ metastases were
also analyzed.
Statistical Methods
All data were analyzed using SPSS
23.0. Count data [n (%)] were tested by χ2.
ANOVA with post hoc F test was per-
formed for multi-point comparisons.
Mea-
surement data were indicated by mean ±
standard deviations, p<0.05 was conside-
red statistically significant.
RESULTS
Overall thyroid cancer metastasis
Among the 103 patients with thyroid
cancer, there were 86 cases (83.50%) of
CLNM, 25 cases (24.27%) of STI, and 4 ca-
ses (3.88%) of DOM revealed by preope-
rative ultrasonography. There were nine
patients with CLMN and STI, accounting
for 8.74%, and one patient presented with
CLMN and DOM, accounting
for 0.97%.
Some of the ultrasound findings are shown
in Fig. 2 and Fig. 3.
The ultrasound features of CLNM
Preoperative ultrasonography showed
86 patients with CLNM, of which 62 ca-
ses
were unilateral CLNM, accounting for
72.09%, and 24 cases were bilateral CLNM,
accounting for 27.91%. The long diame-
ter of metastatic lymph nodes in these 86
patients ranged from 0.6-2.9 cm, with a
mean long diameter of 1.83±0.63 cm, and
short diameter ranged from 0.3-1.7 cm, with
a mean short diameter of 1.03±0.42 cm.
In terms of location, there were seven
cases in zone II, accounting for 8.14%; 42
cases in zone III, accounting for 48.84%; 20
cases in zone IV, accounting for 23.26%;
four
cases in zone V, accounting for 4.65%; 10
cases in zone VI, accounting for 11.63%,
three cases in zone VII, accounting for
3.49%, and no metastasis in zone I. Morpho-
logically, 65 of the 86 patients with CLNM
had a lymph node L/T ratio <2
and showed
a round-like or round shape.
Regarding internal echogenicity, 66 ca-
ses of CLNM showed no medullary
manifes-
tations. Punctate hyperechogenicity could
be observed within the lymph nodes in 43
patients, and the pathological examination
showed microcalcified colloid.
Coarse calci-
fication could be observed within the lymph
nodes in three patients, and
the metastatic
lymph nodes in six patients with patho-
logically confirmed papillary
thyroid cancer
showed internal cystic necrosis with partial
or complete cystic changes.
Fig. 1. Image of levels and sublevels of the neck
(Modified image from Robbins et al. 14).
Preoperative ultrasonography of metastatic thyroid cancer 177
Vol. 64(2): 173 - 183, 2023
The sonograms of metastatic lymph
node cystic changes showed mostly
hete-
rogeneous thickness separation, some with
wall nodules or with punctate hyperechoge-
nicity, and larger wall nodules showed the
presence of blood flow signal
within them.
Seventy cases developed solid metastases,
including 45 cases of solid
hypoechogenici-
ty, 15 cases of multifocal hyperechogenicity,
seven cases of unifocal
hyperechogenicity,
and three cases of diffusely distributed so-
lid hyperechogenicity
(Table 1).
Ultrasound features of soft tissue invasion
Cervical soft tissue invasion occurred
in 25 cases, manifesting as the invasion of
the thyroid peritoneum in all patients, in-
vasion of the fatty muscles in 10 patients,
invasion of the trachea in two cases, and in-
vasion of the thyroid cartilage in one case.
Ultrasonography showed capsule disruption,
no clear line of demarcation between the
pri-
mary lesion and the soft tissues, hete-
rogeneous echogenicity, and calcification
(Table 2). Some of the ultrasound findings
are shown in Fig. 4.
Ultrasound features of distant organ
metastases
Distant organ metastases occurred in
four cases, including one case, with uterine
metastasis, in which the ultrasonography
showed a solid mass with septa. One case
presented with parotid metastasis and
showed as a solitary and solid hypoechoic
nodule in the parotid gland with clear bor-
ders, sharp margins, and posterior acoustic
enhancement, very close to mixed tumors
of the salivary gland. One case presented
with axillary metastasis, and ultrasonogra-
phy showed axillary lymph nodes with a L/T
ratio of <2 and no medullary type. Fina-
lly, one case presented metastasis in the
submandibular gland, and ultrasonography
showed a solid, hypoechoic nodule with
coarse margins (Table 3). Some of the ultra-
sound findings are shown in Fig. 5.
Fig. 2. Morphology of thyroid metastases. (A)
shows an enlarged lymph node in the
right
cervical region III, partly with intense
echogenicity, clear borders, full shape,
in-
distinct corticomedullary demarcation,
and absence of the lymphatic hilum; (B)
shows an enlarged lymph node in the right
cervical region VI; (C) shows the right axi-
llary metastasis.
178 Ruan et al.
Investigación Clínica 64(2): 2023
Fig. 3. Internal echo image of the thyroid gland. (A) shows an enlarged lymph node in
the right cervical re-
gion IV; (B) shows a left cervical enlarged lymph node with clear
borders, indistinct corticomedullary
demarcation, and multiple intense echogenic foci.
Table 1
The ultrasound features of cervical lymph node metastasis from thyroid cancer
%p
Preoperative ultrasonography of metastatic thyroid cancer 179
Vol. 64(2): 173 - 183, 2023
Table 2
The ultrasound features of soft tissue invasion
Ultrasound sonographic features Number of cases %
Invasion of the thyroid capsule 25 100.00
Invasion of the fatty muscles 10 40.00
Invasion of trachea 2 8.00
Invasion of the thyroid cartilage 1 4.00
Note: χ2 test was used.
Fig. 4. Cervical soft tissue invasion. The hypoechoic mass in the subcutaneous soft tissue of the left neck has a
clear
border, irregular shape, and uneven edge; CDFI: no evident blood flow signal was observed.
Table 3
The ultrasound features of distant organ metastases
Ultrasound sonographic features Number of cases %
Uterine metastasis 1 25.00
Parotid metastases 1 25.00
Axillary metastasis 1 25.00
Submandibular metastases 1 25.00
Note: χ2 test was used.
DISCUSSION
The types of metastasis in patients
with thyroid cancer include cervical lymph
node metastasis, soft tissue invasion, and
distant organ metastasis, and the inciden-
ce
of cervical lymph node metastasis is the
highest 15. Clinical data showed that half of
the patients with thyroid cancer had deve-
loped regional lymph node metastasis upon
consultation, with the highest incidence of
ipsilateral and middle CLNM, which
con-
tains bilateral CLNM and supraclavicular
lymph node metastasis 16. A small
fraction
of patients developed lymph node metasta-
sis when the primary tumor was tiny, which
180 Ruan et al.
Investigación Clínica 64(2): 2023
Fig. 5. Distant metastases. Figure A: left side; Figure B: right side. Hypoechoic masses were observed in both
parotid glands, with clear borders, uneven
edges, partially angular and irregular shapes, and no
evident internal blood flow signal.
was the first symptom of metastatic lymph
node enlargement in some patients
17.
Lymph node metastasis was predomi-
nantly unilateral. Unilateral metastasis
ac-
counted for 72.09% of this study’s 86 pa-
tients with thyroid cancer. Statistics
showed
that lymph node metastases were mostly in
the middle and lower of the neck,
being ap-
proximately 68% of all neck lymph nodes 18.
Studies have shown that lymph
node enlar-
gement could be detected in only 30% of
patients with papillary thyroid
cancer un-
dergoing physical examination. Pathological
examination revealed that over
80% of pa-
tients have lymph node metastasis, indi-
cating some underdiagnosis of lymph node
metastasis by ultrasound 19. It was found
that thyroid cancer patients with
CLNM ex-
perience higher recurrence rates, mortality,
and worse prognosis than
patients without
CLNM 20. Early examination is required for
the detection of lymph
node metastasis in
patients with thyroid cancer. Comprehensive
observation of lymph
node in terms of mor-
phology, borders, internal echogenicity and
other features was performed. The following
reliable features of lymph node metastasis
were
summarized in this study with referen-
ce to ultrasound findings. Solid hyperechoic
or hypoechoic nodules, cystic changes, and
gravel-like calcifications were found, with
zones III, IV, and VI being the metastatic
areas with the highest incidence rate.
Stu-
dies have shown that ultrasound showed an
accuracy of >75% in the diagnosis of CLNM
in patients with thyroid cancer 21. Studies
have proposed that thyroid cancer
first me-
tastasized to zone VI lymph nodes, showing
the highest rate of metastasis 22. A study
analyzed patients with papillary thyroid
cancer treated with systemic lymph
node
dissection. It showed that over 80% of pa-
tients had multi-divisional metastases,
with
the highest rates in Zone III, Zone IV, Zone
II, and Zone V. However, there were
no cases
of metastasis to Zone I 23, which is consis-
tent with the results of this study, demons-
trating that the rate of metastasis from the
highest to the lowest occurred in
Zone III,
Zone IV, Zone VI, Zone II, Zone V, and Zone
VII. There were no patients
with metastasis
to Zone I. However, in clinical practice,
the missed rate of lymph
node metastases
was highest in zone VI, and the diagnos-
tic rate by ultrasound for metastatic lymph
nodes in this region was low. However, typi-
cal features could be
obtained since other
primary head and neck tumors basically do
not metastasize to
this region 24. It can
be concluded from the above analysis that
Preoperative ultrasonography of metastatic thyroid cancer 181
Vol. 64(2): 173 - 183, 2023
clinical physicians
should pay attention to
zones III, IV and VI of the neck to reduce
missed diagnoses
and ensure the diagnostic
accuracy.
Invasion of the surrounding soft tis-
sues and organs is also one metastatic rou-
te of thyroid cancer, primarily affecting the
thyroid capsule, the fatty muscles, the tra-
cheal
ring, the thyroid cartilage, and the
larynx 25. In this study, 25 patients develo-
ped soft tissue invasion involving the thyroid
capsule, ten patients developed invasion of
the
fatty muscles. Two patients had invasion
of the trachea, and one patient had invasion
of the thyroid cartilage. If the primary
lesion is in close proximity to the thyroid
capsule, there is a higher risk of CLNM and
also the invasion of adjacent soft tissues,
in
which aggressive surgical treatment and
complete clearance of regional lymph
no-
des on the lateral side of the neck are
required 26. Although papillary thyroid
car-
cinoma showed a slight malignant transfor-
mation, it can develop distant
metastases,
with bone, brain, and lung more likely in-
volved. The limitations of ultrasonography
result in a low detection rate in these si-
tes by ultrasonography 27. Previous evidence
showed that distant metastases from papi-
llary thyroid cancer
occurred in the breast,
axilla, orbit, and pancreas, and ultrasonogra-
phy was performed
based on patient history
28. In this study, distant organ metastases
occurred in four cases of thyroid cancer
(parotid gland, submandibular gland, axilla)
and one case in
the uterus.
In conclusion, the most common me-
tastatic site of thyroid cancer is the cervical
lymph nodes. The soft tissues and distant
organs were also involved. There are typical
sonographic features in ultrasonography,
and adequate familiarity with the
sonogra-
phic features can help to diagnose suspi-
cious metastases in a timely manner, which
is crucial for clinical diagnosis, treatment,
and prognostic assessment.
However, there
are shortcomings in the present study, as
shown by the small sample
size and the lack
of sufficient representativeness of the obtai-
ned results, as well as the
lack of differentia-
tion of thyroid cancer types for the analysis
of metastases, which
need to be improved in
future studies.
Funding
This research did not receive any spe-
cific grant from funding agencies in the pu-
blic, commercial, or not-for-profit sectors.
Conflict of Interests
The authors declared no conflict of in-
terest.
Author’s ORCID numbers
• Lingling Ruan:
0000-0002-4402-7323
• Qingxin Zhang:
0000-0002-1748-2005
• Qinghong Qu:
0000-0002-9261-5592
Participation in development and writing
of the paper
Concept and design: QQ and LR. Acqui-
sition of data, literature review, and refine-
ment of manuscript: All authors. Analysis
and interpretation of data: LR and QZ. Ma-
nuscript writing: LR. Review of final manus-
cript: QQ.
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