TI-RADS classification of thyroid nodules based on a score modified

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Original
TI-RADS classification of thyroid nodules based on a score modified according to ultrasound criteria for malignancy
TI-RADS classification of thyroid nodules based on
a score modified according to ultrasound criteria
for malignancy
J. Fernández Sánchez *
Radiology and Nuclear Medicine, Robert-Bosch-Krankenhaus, University Hospital, Tübingen University, Stuttgart, Germany
Abstract
Objective: The classification system of the thyroid nodules (TN) TI-RADS (Thyroid Imaging Reporting and Data System)
proposed by Horvath et al. in 2009 is rarely used. The aim of this study was to evaluate a score modified according to
ultrasound (US) criteria for malignancy in order to obtain a better application of this classification in daily practice.
Materials and methods: 3650 TNs were classified according to a score of potential malignancy. US criteria for suspected
malignancy were defined according to published studies and guidelines from various medical international societies.
Each criterion was assigned a point for the final score of malignant probability of the TN. If suspected cervical lymph
nodes were detected, a point was added.
Results: The score in all benign (TI-RADS 2) or probably benign (TI-RADS 3) thyroid nodules was zero. In the TI-RADS
3 group only 2.2% of the TNs were malignant. The scores of TI-RADS 4a, 4b and 4c were one, two and three to four
points, respectively. The malignancy rates were 9.5%, 48% and 85%, respectively. TI-RADS 5 TN had a score of five or
more points with a malignancy of 100% in this study.
Conclusion: A TI-RADS classification based on a score according to the number of suspicious US criteria defined for
malignancy can be applied in daily practice.
© 2014 Sociedad Argentina de Radiología. Published by Elsevier Spain, S.L.U. All rights reserved.
Keywords
Thyroid nodule; TI-RADS; Ultrasound; Thyroid scintigraphy
Introduction
Materials and methods
Thyroid nodules (TNs) may show highly diverse ultrasound
patterns1,2, which often impairs an accurate classification
regarding malignancy. For this reason, in 2009 Horvath et
al3 proposed an evaluation system for TNs called TI-RADS
(Thyroid Imaging Reporting and Data System), similar to the
Breast Imaging Reporting and Data System (BI-RADS)4,5. In
2011, Kwak et al6, complemented this classification adding
one subtype.
However, both systems are difficult to apply. Even if the TIRADS classification is quoted in the medical literature, it is
rarely used in daily practice, perhaps because of some uncertainty on the part of the various specialists that use such
classification.
The aim of this study was to evaluate an easy-to-use TI-RADS
classification based on a modified score according to the US
criteria for malignancy present in each case.
We reviewed the 7960 thyroid ultrasound scans performed
between 2003 and 2013 and stored on the Picture Archiving
and Communication System/Radiology Information System
(PACS/RIS). The scans had been performed, or reviewed prior
to reporting (if performed by a resident physician), by specialists with 5 to 30 years’ experience in thyroid ultrasound. The
US examination of a detected TN consisted in an evaluation
of its echogenicity, internal content (presence of cystic lesions
and/or calcifications), margins, shape and vascular pattern.
Based on studies and guidelines from various national and
international medical societies of different specialties7-16, ultrasound criteria for suspected malignancy were established
(table 1). Each criterion was assigned a point, and an additional point was added when one or more cervical lymph
nodes suspicious for malignancy were detected. Thus, a final
score of malignant probability of a TN was obtained.
138
Rev. Argent. Radiol. 2014;78(3): 138-148
J. Fernández Sánchez
Table 1: Sonographically suspicious criteria for malignancy.
Each criterion is assigned a point in the final score. If suspicious cervical lymph nodes are detected, an additional point
is added to the score for categorizing nodules on TI-RADS
classification.
• Hypoechogenicity
• Microcalcifications
• Partially cystic nodule with eccentric location of the fluid
portion and lobulation of the solid component
• Irregular margins
• Perinodular thyroid parenchyma invasion
• Taller-than-wide shape
• Intranodular vascularity
For TI-RADS assessment, we selected from the PACS imaging archiving system appropriately documented TNs (sagittal
and axial ultrasound images of TNs, obtained by conventional --B mode-- imaging and by color Doppler for the evaluation of perfusion) of which fine needle aspiration (FNA) had
been performed and/or which had been scanned by thyroid
scintigraphy and/or elastosonography and/or other imaging
method (magnetic resonance imaging [MRI], positron emission tomography – computed tomography [PET/CT]) and/or
which had undergone histological assessment after surgery
and/or which had at least a one-year clinical follow-up with
ultrasound scans.
As this was primarily a retrospective study, no approval was
requested from the Ethics Committee.
The statistical analysis was based on the calculation of predictive values of the TI-RADS classification categories.
Results
Of the 7960 thyroid ultrasound scans evaluated, one or several TNs were detected in 6127 and no focal lesions were detected in 1833. Of the latter (n = 1833), 1454 cases showed
diffuse abnormality of the thyroid parenchyma, either due
to Hashimoto’s thyroiditis or to thyroid autoimmune disease
(Grave-Basedow disease), while the remaining 379 patients
with no focal lesion had a normal sized gland, with an ultrasound pattern that was hyperechogenic (in regard to muscle)
and homogeneous, and with normal vascularity on color
Doppler. These normal ultrasound scans of the thyroid, with
an incidence of 4.7% in our series (379/7960 cases) were
classified as TI-RADS 1, similar to BI-RADS classification of the
breast (BI-RADS 1 = normal breast)4,5
Of the 6127 patients with one or several TNs, 1148 met the
study requirements. Of all TNs, 3650 were appropriately documented and had been evaluated by the reference diagnostic
methods. Therefore, they were used for the evaluation of TIRADS classification in this study.
Of these 3650 TNs, 1302 (35.6%) showed benign sonographic features: 73/1302 simple cysts2,17, 104/1302 TNs
with a central cyst (type 1, according to Kim et al classification
for partially cystic TNs)16, 56/1302 TNs with non-interrupted
homogeneous peripheral calcification18 and 1069/1302
spongiform TNs2, 19,20. Based on their ultrasound pattern
and the absence of ultrasound criteria for malignancy, these
TNs had a score of zero. Furthermore, additional tests (FNA [n
= 88] and/or histological examination after surgery [n = 132]
and/or thyroid scintigraphy [n = 585] and/or elastosonography [n = 95] and/or MRI/PET/CT [n = 12] and/or clinical and
sonographic follow-up of at least one year [n = 554] did not
reveal malignancy. Thus, these 1302 TNs were classified as
TI-RADS 2.
The remaining 2194 TNs (60.1%) of the total of 3650 TNs
with no ultrasound criteria for malignancy (score of zero)
appeared as: hyperechoic with or without small cystic abnormalities (527/2194); and solid with peripheral vascularity
and a mixed pattern of hypo, iso or hyperechoic spots and/or
small cystic changes and/or macrocalcifications (1667/2194).
Only 48 (2.2% of 2194) were malignant (histologically confirmed after surgery). In the remaining 2146, additional tests
(FNA [n = 177) and/or histological examination after surgery
[n = 569] and/or thyroid scintigraphy [n = 687] and/or elastosonograhy [n = 128] and/or MRI/PET/CT [n = 18] and/or clinical and ultrasound follow-up of at least one year [n = 843]
did not reveal malignancy. This type of TN was classified as
TI-RADS 3 (i.e., low probability of malignancy).
In turn, 154/3650 TNs (4.2%) were assigned one or more
points of potential malignancy (table 2). One-hundred and
five of those TNs had a score of 1 and 10 of them were malignant (10/105; 9.5%). In 12 of 25 TNs with a score of 2, thyroid carcinoma was histologically detected (12/25; 48%) and
in the case of TNs with a score of 3-4, malignancy increased
up to 85% (12/14).
With the aim of unifying terminology and considering the
malignancy rates published by Horvath et al3 and Kwak et
al6, thyroid nodules were classified as TI-RADS 4a when they
had a score of 1 (malignancy below 10%), as TI-RADS 4b
when they had a score of 2 (malignancy 10-50%) and as TIRADS 4c when they had a score of 3-4 (malignancy 50-85%).
In the remaining 120 TNs with a score of 4, no carcinoma was
detected by the reference methods.
TNs with a score of 5 or higher were classified as TI-RADS 5
(probably malignant, similar to the BI-RADS system). In our
study, these TNs were histologically diagnosed as differentiated thyroid carcinoma (10/10; 100%). Histologically, thyroid
139
Table 2: Nodules with a score of 1 or higher in relation to
histologically proven malignancy following surgery.
Score according Cases (n)
to the number of
sonographically
suspicious criteria
for malignancy
Malignancy
1
2
3-4
5 or higher
10/105 (9.5%)
12/25 (48%)
12/14 (85%)
10/10 (100%)
105
25
14
10
Table 3: TI-RADS classification of thyroid nodules based on
a scoring system according to ultrasound criteria for malignancy.
TI-RADS 1: Normal thyroid gland. No focal lesion.
TI-RADS 2: Benign nodules. Noticeably benign pattern
(0% risk of malignancy)
Score of zero
TI-RADS 3: Probably benign nodules (<5% risk of malignancy)
Score of zero
TI-RADS 4:
• 4a – Undetermined nodules (5-10% risk of malignancy)
Score of 1.
• 4b – Suspicious nodules (10-50% risk of malignancy)
Score of 2.
• 4c – Highly suspicious nodules (50-85% risk of malignancy)
Score of 3-4
TI-RADS 5: Probably malignant nodules (>85% risk of malignancy)
Score of 5 or higher
TI-RADS 6: Biopsy-proven malignancy
carcinomas were papillary (n = 25), follicular (n = 15), oxyphilic (n = 2) or medullary (n = 2).
In 3/6127 cases thyroid papillary carcinoma was diagnosed
prior to ultrasound examination due to surgical excision of
metastatic cervical adenopathy. As in BI-RADS classification,
these cases were classified as TI-RADS 6.
Table 3 summarizes findings in the scoring system and the
corresponding category according to TI-RADS classification,
while table 4 shows the positive predictive value of TI-RADS
categories in this study.
140
Table 4: Positive predictive value of TI-RADS classification
stages.
TI-RADS Category
PV +
T2/T30%
T4a9.5%
T4b48%
T4c85%
T5100%
PV+: positive predictive value
Discussion
TNs are common. The prevalence of TNs in autopsies ranges
between 8.2 and 64.6%21,22, while detection by ultrasound
has increased from 19% to 68% with the technological development of ultrasound equipment23-25. However, TNs continue
to be difficult to evaluate and this is why there are a large
number of medical guidelines. So much so that, according to
a research literature review conducted on PubMed/Medline for
the preparation of this manuscript, only in the (approximately)
last 10 years, over 250 articles have been published, including
studies, recommendations by medical societies and reviews on
guidelines for the detection of TNs, 9,11,13,14,26-35.
TNs show different ultrasound patterns, with a hypo, iso or
hyperechoic structure which, in turn, may be associated not
only with cystic changes of variable shape and size, but also
with macro and/or microcalcifications. In addition, the margins and shape of TNs may be different.
This diversity (much larger than that of focal lesions in other
organs or glands, such as the liver or breast) poses serious
difficulties for a proper classification.
With the aim of solving this problem, in 2009, Horvath et al3
proposed a classification known as TI-RADS (similar to the system used for breast lesions, BI-RADS)4,5 and later Kwak et al6
added a subtype (4c). However, not all the ultrasound features
of nodules proposed by Horvath et at can be applied with certainty in daily practice6, and as regards Kwak et al, they did not
use TN perfusion on color Doppler within their classification.
Thus, our study also assessed the presence of suspicious cervical lymph nodes (differentiating them from Kwak classification
as regards the evaluation criteria for scoring).
Though quoted in the medical literature, TI-RADS classification is hardly used in daily practice. This may be due,
in the first place, to an unawareness of this system by the
wide range of specialists performing thyroid ultrasound scans
Figure 1 TI-RADS 1: normal thyroid gland.
Figure 2 TI-RADS 2: simple thyroid cyst.
Figure 3 TI-RADS 2: solid nodule with central cyst.
Figure 4 TI-RADS 2: nodule with homogeneous peripheral
calcification.
(from family or primary physicians to internists, endocrinologists, surgeons, radiologists and nuclear medicine specialists),
but it may also be attributed to some uncertainty on the part
of the professional performing the US scan (who may be
afraid of misclassifying a TN) or to his/her convenience (as
for some professionals it is easier to report, for example, a
“nodular goiter” or an “enlarged thyroid gland with an hy-
poechoic nodule”, even if this report is not of great help for
the ordering physician).
From this perspective, we propose a TI-RADS classification
based on a scoring system in which each ultrasound abnormality suspicious for malignancy is assigned a score. If one
or more cervical lymph nodes suspicious for malignancy are
detected, an additional point is added (table 1).
141
Figure 5 TI-RADS 2: spongiform nodule.
Figure 6 TI-RADS 3: hyperechoic nodule.
Figure 7 TI-RADS 3: slightly hyperechoic nodule with small
cysts and peripheral vascularity
Figure 8 The nodule on Figure 7 corresponds to a toxic adenoma on thyroid scintigraphy with 99mTC-sodium pertechnetate.
In this study, 4.7% of thyroid ultrasound scans did not show
focal lesion and the thyroid gland showed a hyperechoic, homogeneous and normal ultrasound pattern with no changes
in vascularity. These cases constituted category 1 in TI-RADS
classification (fig. 1), while 35.6% of TNs with well-defined
criteria for benignity (simple cyst, solid nodule with central
cyst, nodule with homogeneous peripheral calcification and
spongiform nodule), with benignity being confirmed by various methods (figs. 2-5), were classified as TI-RADS 2.
Only 2.2% of TNs with peripheral vascularity and hyperechoic
(with or without cystic changes) or diverse US pattern (hypo,
iso or hyperechoic, with cystic changes and/or macrocalcifica-
142
Figure 9 TI-RADS 3: several nodules in the same gland with a
similar ultrasound pattern: hyper or isoechoic nodules, with
small cystic changes and small hypoechoic spots, as well as
microcalcifications (arrow) and peripheral perfusion. In the
thyroid scintigraphy (lower row on the right) TNs appear as
toxic adenomas in a patient with hyperthyroidism.
Figure 10 Patient with nodular goiter. In a hyperechoic nodule
with small cysts, consistent with TI-RADS 3, a small papillary
thyroid carcinoma (pT1b) was histologically detected after
surgery.
Figure 11 TI-RADS4a: markedly hypoechoic nodule, of normal
shape and abnormal vascularity. Score of 1.
Figure 12 TI-RADS 4b: nodule with microcalcifications and
poorly defined irregular margins. Score of 2.
143
Figure 13 TI-RADS 4b: nodule with two sonographically suspicious criteria for malignancy: hypoechogenicity and internal
vascularity.
Figure 14 TI-RADS 4c: nodule with microcalcifications, irregular borders and taller than wide shape (greater in its anteroposterior diameter than in its transverse diameter). Score of 3.
Figure 15 TI-RADS 4c: hypoechoic nodule of irregular margins
with a taller than wide shape. Score of 3.
Figure 16 TI-RADS 5: hypoechogenic nodule with microcalcifications and poorly defined margins, with perinodular tissue invasion (arrow). Taller than wide shape. Presence of a
cervical lymph node suspicious for malignancy (see: Fig. 17).
Overall score of 6.
144
Figure 17 TI-RADS 5: suspicious hypoechoic lymph node, with
round shape and abnormal vascularity. Overall score of 6 for
the nodule of fig. 16.
tions) proved to be malignant. These TNs with a score of 1
and probably benign US findings are classified as TI-RADS 3
(fig. 6) (probability of malignancy < 5%) according to Horvath et al3 and Kwak et al6. In this respect, it should be noted
that many of the TI-RAD 3 nodules are functioning or toxic
thyroid adenomas (figs. 7-9) and that malignancy within this
category is not only a rare occurrence, but also a generally
unexpected histological finding following nodular goiter surgery (fig. 10). In our study, 9.5% of TNs meeting one criterion
for malignancy were diagnosed as thyroid carcinoma.
TNs with a score of 1 were assigned category 4a in TI-RADS
classification (fig. 11), while TNs with a score of 2 were classified as TI-RADS 4b (figs. 12 and 13). In the latter case, the
incidence of malignancy increased up to 48%. In turn, TNs
with a score of 3 or 4 showed an increased incidence of thyroid carcinoma of up to 85%, and were therefore included
within TI-RADS 4c (figs. 14 and 15). In this category, Kwak et
al6 report a probability of malignancy of 50-95%.
Finally, TNs with a score of 5 or higher were classified as TIRADS 5 (figs. 16 and 17). In our study, all TNs with these
ultrasound features proved to be malignant, but Horvath et
al3 and Kwak et al6 report for this category a probability of
malignancy of 85-99%.
The TI-RADS classification based on the scoring system is
shown in table 3. The advantage of this method is that it is
more practical and easy to apply. The first step in the US classification of TNs consists in evaluating the potential presence
of criteria for suspected malignancy. When their presence is
detected, points must be added to the score as appropriate.
Thus, if a TN has a score of 0, it is either definitely benign (TIRADS 2) with the aforementioned US patterns (simple cyst,
solid nodule with central cyst, nodule with homogeneous
peripheral calcification and spongiform nodule) or probably benign (TI-RADS 3). As from a score of 1, TNs begin to
have, depending on the final score, from an undetermined
categorization to a high probability of malignancy. For TNs
classified as TI-RADS 4a, management will depend on the patient’s general clinical condition. In the event of an incidental
finding in a patient with a medical history that suggests no
risk of developing thyroid carcinoma (for example, no family
history of thyroid carcinoma, no exposure to previous radiation to the neck for malignancies, etc.), an ultrasound scan is
enough for TNs less than 1 cm in size, while nodules larger
than 1 cm should be examined by thyroid scintigraphy using
99mTC-sodium pertechnetate to evaluate their uptake36,37.
The possible protocol-based management of TI-RADS 4a,
with an additional evaluation by FNA, depends on medical
history, clinical examination and ultrasound and scintigraphy
findings (further prospective studies would be required). On
the contrary, TNs classified as TI-RADS 4b and 4c should always undergo FNA, except if contraindicated or in the event
of high risk. Based on the results of this study, TI-RADS 5 nodules invariably require histological examination after surgery.
Limitations to this study include the lack of cytological or histological confirmation for all cases. However, those performing ultrasound diagnosis of TNs in daily practice are aware of the impossibility of performing FNA or surgery in all nodules. This is also
impracticable in clinical trials for ethical reasons. In fact, owing to
technological advances in ultrasound imaging and to the implementation of new techniques (such as color Doppler or elastography) and other diagnostic methods (e.g., scintigraphy or PET/CT),
it has been possible to reduce the number of these interventions.
Even if some thyroid carcinomas have slow progression, when
further diagnostic methods show signs of benignity in medical practice, this is considered to be enough, because the
likelihood that they may become malignant is low. For this
reason, despite the unavailability of cytological or histological
confirmation for all 3650 nodules, benignity as defined by
those methods was considered to be valid. Furthermore, in
966 TI-RADS 2 and 3 cases, FNA or surgery was effectively
performed, and in all cases of TI-RADS 3, 4a, 4b, 4c and 5
malignancy, histological confirmation was performed.
TI-RADS is a merely sonographic classification. The final evaluation and therapeutic decision-making in the presence of a
TN cannot be limited to the results of a thyroid ultrasound.
In addition to the standard laboratory tests for the evaluation
of thyroid function, measurement of thyroglobulin, calcitonin
and diverse anti-thyroid antibodies is also important, as well as
the thyroid scintigraphy using 99mTC-sodium pertechnetate.
145
Conclusion
A TI-RADS classification of TNs based on a score according
to the most relevant sonographically suspicious criteria for
malignancy can be better and more easily applied in daily
practice. Based on the criteria for malignancy and the score
assigned in this study, the probability of malignancy for TNs
with a score of 1 is 10%, while for those with a score of 2 is
almost 50% and for those that have been assigned a score of
3 or 4, the probability of malignancy is 85%. All TNs with a
score of 5 or higher are malignant.
A TI-RADS classification based on the scoring system described above should allow for and lead to unification of terminology and codes for TN classification among all physicians
who evaluate the results of a thyroid ultrasound (whether
they are primary physicians, endocrinologists, radiologists or
specialists in nuclear medicine).
Conflicts of interest
The author declares no conflicts of interest.
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TI-RADS classification of thyroid nodules based on a score modified

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