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 We reviewed the 7960 thyroid ultrasound scans performed patterns1,2, which often impairs an accurate classification between 2003 and 2013 and stored on the Picture Archiving regarding malignancy. For this reason, in 2009 Horvath et and Communication System/Radiology Information System al3 proposed an evaluation system for TNs called TI-RADS (PACS/RIS). The scans had been performed, or reviewed prior (Thyroid Imaging Reporting and Data System), similar to the to reporting (if performed by a resident physician), by special- Breast Imaging Reporting and Data System (BI-RADS)4,5. In ists with 5 to 30 years’ experience in thyroid ultrasound. The 2011, Kwak et al6, complemented this classification adding US examination of a detected TN consisted in an evaluation one subtype. of its echogenicity, internal content (presence of cystic lesions However, both systems are difficult to apply. Even if the TI- and/or calcifications), margins, shape and vascular pattern. RADS classification is quoted in the medical literature, it is Based on studies and guidelines from various national and rarely used in daily practice, perhaps because of some un- international medical societies of different specialties7-16, ul- certainty on the part of the various specialists that use such trasound criteria for suspected malignancy were established classification. (table 1). Each criterion was assigned a point, and an ad- The aim of this study was to evaluate an easy-to-use TI-RADS ditional point was added when one or more cervical lymph classification based on a modified score according to the US nodes suspicious for malignancy were detected. Thus, a final criteria for malignancy present in each case. score of malignant probability of a TN was obtained.

138 Rev. Argent. Radiol. 2014;78(3): 138-148 TI-RADS classification of thyroid nodules based on a score modified according to ultrasound criteria for malignancy J. Fernández Sánchez

Table 1: Sonographically suspicious criteria for malignancy. study requirements. Of all TNs, 3650 were appropriately doc- Each criterion is assigned a point in the final score. If suspi- umented and had been evaluated by the reference diagnostic cious cervical lymph nodes are detected, an additional point methods. Therefore, they were used for the evaluation of TI- is added to the score for categorizing nodules on TI-RADS RADS classification in this study. classification. Of these 3650 TNs, 1302 (35.6%) showed benign sono- graphic features: 73/1302 simple cysts2,17, 104/1302 TNs • Hypoechogenicity with a central cyst (type 1, according to Kim et al classification • Microcalcifications for partially cystic TNs)16, 56/1302 TNs with non-interrupted • Partially cystic nodule with eccentric location of the fluid homogeneous peripheral calcification18 and 1069/1302 portion and lobulation of the solid component spongiform TNs2, 19,20. Based on their ultrasound pattern • Irregular margins and the absence of ultrasound criteria for malignancy, these • Perinodular thyroid parenchyma invasion TNs had a score of zero. Furthermore, additional tests (FNA [n • Taller-than-wide shape = 88] and/or histological examination after surgery [n = 132] • Intranodular vascularity and/or thyroid scintigraphy [n = 585] and/or elastosonogra- phy [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 For TI-RADS assessment, we selected from the PACS imag- TI-RADS 2. ing archiving system appropriately documented TNs (sagittal The remaining 2194 TNs (60.1%) of the total of 3650 TNs and axial ultrasound images of TNs, obtained by convention- with no ultrasound criteria for malignancy (score of zero) al --B mode-- imaging and by color Doppler for the evalua- appeared as: hyperechoic with or without small cystic ab- tion of perfusion) of which fine needle aspiration (FNA) had normalities (527/2194); and solid with peripheral vascularity been performed and/or which had been scanned by thyroid and a mixed pattern of hypo, iso or hyperechoic spots and/or scintigraphy and/or elastosonography and/or other imaging small cystic changes and/or macrocalcifications (1667/2194). method (magnetic resonance imaging [MRI], positron emis- Only 48 (2.2% of 2194) were malignant (histologically con- sion tomography – computed tomography [PET/CT]) and/or firmed after surgery). In the remaining 2146, additional tests which had undergone histological assessment after surgery (FNA [n = 177) and/or histological examination after surgery and/or which had at least a one-year clinical follow-up with [n = 569] and/or thyroid scintigraphy [n = 687] and/or elasto- ultrasound scans. sonograhy [n = 128] and/or MRI/PET/CT [n = 18] and/or clini- As this was primarily a retrospective study, no approval was cal and ultrasound follow-up of at least one year [n = 843] requested from the Ethics Committee. did not reveal malignancy. This type of TN was classified as The statistical analysis was based on the calculation of predic- TI-RADS 3 (i.e., low probability of malignancy). tive values of the TI-RADS classification categories. 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 ma- Results lignant (10/105; 9.5%). In 12 of 25 TNs with a score of 2, thy- roid carcinoma was histologically detected (12/25; 48%) and Of the 7960 thyroid ultrasound scans evaluated, one or sev- in the case of TNs with a score of 3-4, malignancy increased eral TNs were detected in 6127 and no focal lesions were de- up to 85% (12/14). tected in 1833. Of the latter (n = 1833), 1454 cases showed With the aim of unifying terminology and considering the diffuse abnormality of the thyroid parenchyma, either due malignancy rates published by Horvath et al3 and Kwak et to Hashimoto’s thyroiditis or to thyroid autoimmune disease al6, thyroid nodules were classified as TI-RADS 4a when they (Grave-Basedow disease), while the remaining 379 patients had a score of 1 (malignancy below 10%), as TI-RADS 4b with no focal lesion had a normal sized gland, with an ultra- when they had a score of 2 (malignancy 10-50%) and as TI- sound pattern that was hyperechogenic (in regard to muscle) RADS 4c when they had a score of 3-4 (malignancy 50-85%). and homogeneous, and with normal vascularity on color In the remaining 120 TNs with a score of 4, no carcinoma was Doppler. These normal ultrasound scans of the thyroid, with detected by the reference methods. an incidence of 4.7% in our series (379/7960 cases) were TNs with a score of 5 or higher were classified as TI-RADS 5 classified as TI-RADS 1, similar to BI-RADS classification of the (probably malignant, similar to the BI-RADS system). In our breast (BI-RADS 1 = normal breast)4,5 study, these TNs were histologically diagnosed as differenti- Of the 6127 patients with one or several TNs, 1148 met the ated thyroid carcinoma (10/10; 100%). Histologically, thyroid

Rev. Argent. Radiol. 2014;78(3): 138-148 139 TI-RADS classification of thyroid nodules based on a score modified according to ultrasound criteria for malignancy

Table 2: Nodules with a score of 1 or higher in relation to Table 4: Positive predictive value of TI-RADS classification histologically proven malignancy following surgery. stages.

Score according Cases (n) Malignancy TI-RADS Category PV + to the number of sonographically T2/T3 0% suspicious criteria T4a 9.5% for malignancy T4b 48% T4c 85% 1 105 10/105 (9.5%) T5 100% 2 25 12/25 (48%) 3-4 14 12/14 (85%) PV+: positive predictive value 5 or higher 10 10/10 (100%)

Table 3: TI-RADS classification of thyroid nodules based on Discussion a scoring system according to ultrasound criteria for malig- nancy. TNs are common. The prevalence of TNs in autopsies ranges between 8.2 and 64.6%21,22, while detection by ultrasound TI-RADS 1: Normal thyroid gland. No focal lesion. has increased from 19% to 68% with the technological devel- TI-RADS 2: Benign nodules. Noticeably benign pattern opment of ultrasound equipment23-25. However, TNs continue (0% risk of malignancy) to be difficult to evaluate and this is why there are a large Score of zero number of medical guidelines. So much so that, according to TI-RADS 3: Probably benign nodules (<5% risk of malig- a research literature review conducted on PubMed/Medline for nancy) the preparation of this manuscript, only in the (approximately) Score of zero last 10 years, over 250 articles have been published, including TI-RADS 4: studies, recommendations by medical societies and reviews on • 4a – Undetermined nodules (5-10% risk of malignancy) guidelines for the detection of TNs, 9,11,13,14,26-35. Score of 1. TNs show different ultrasound patterns, with a hypo, iso or • 4b – Suspicious nodules (10-50% risk of malignancy) hyperechoic structure which, in turn, may be associated not Score of 2. only with cystic changes of variable shape and size, but also • 4c – Highly suspicious nodules (50-85% risk of malignancy) with macro and/or microcalcifications. In addition, the mar- Score of 3-4 gins and shape of TNs may be different. TI-RADS 5: Probably malignant nodules (>85% risk of ma- This diversity (much larger than that of focal lesions in other lignancy) organs or glands, such as the liver or breast) poses serious Score of 5 or higher difficulties for a proper classification. TI-RADS 6: Biopsy-proven malignancy With the aim of solving this problem, in 2009, Horvath et al3 proposed a classification known as TI-RADS (similar to the sys- tem used for breast lesions, BI-RADS)4,5 and later Kwak et al6 carcinomas were papillary (n = 25), follicular (n = 15), oxy- added a subtype (4c). However, not all the ultrasound features philic (n = 2) or medullary (n = 2). of nodules proposed by Horvath et at can be applied with cer- In 3/6127 cases thyroid papillary carcinoma was diagnosed tainty in daily practice6, and as regards Kwak et al, they did not prior to ultrasound examination due to surgical excision of use TN perfusion on color Doppler within their classification. metastatic cervical adenopathy. As in BI-RADS classification, Thus, our study also assessed the presence of suspicious cervi- these cases were classified as TI-RADS 6. cal lymph nodes (differentiating them from Kwak classification Table 3 summarizes findings in the scoring system and the as regards the evaluation criteria for scoring). corresponding category according to TI-RADS classification, Though quoted in the medical literature, TI-RADS classi- while table 4 shows the positive predictive value of TI-RADS fication is hardly used in daily practice. This may be due, categories in this study. in the first place, to an unawareness of this system by the wide range of specialists performing thyroid ultrasound scans

140 Rev. Argent. Radiol. 2014;78(3): 138-148 TI-RADS classification of thyroid nodules based on a score modified according to ultrasound criteria for malignancy J. Fernández Sánchez

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, endocrinolo- poechoic nodule”, even if this report is not of great help for gists, surgeons, radiologists and nuclear medicine specialists), the ordering physician). but it may also be attributed to some uncertainty on the part From this perspective, we propose a TI-RADS classification of the professional performing the US scan (who may be based on a scoring system in which each ultrasound abnor- afraid of misclassifying a TN) or to his/her convenience (as mality suspicious for malignancy is assigned a score. If one for some professionals it is easier to report, for example, a or more cervical lymph nodes suspicious for malignancy are “nodular goiter” or an “enlarged thyroid gland with an hy- detected, an additional point is added (table 1).

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Figure 5 TI-RADS 2: spongiform nodule. Figure 6 TI-RADS 3: hyperechoic nodule.

Figure 7 TI-RADS 3: slightly hyperechoic nodule with small Figure 8 The nodule on Figure 7 corresponds to a toxic adeno- cysts and peripheral vascularity ma on thyroid scintigraphy with 99mTC-sodium pertechnetate.

In this study, 4.7% of thyroid ultrasound scans did not show cyst, nodule with homogeneous peripheral calcification and focal lesion and the thyroid gland showed a hyperechoic, ho- spongiform nodule), with benignity being confirmed by vari- mogeneous and normal ultrasound pattern with no changes ous methods (figs. 2-5), were classified as TI-RADS 2. in vascularity. These cases constituted category 1 in TI-RADS Only 2.2% of TNs with peripheral vascularity and hyperechoic classification (fig. 1), while 35.6% of TNs with well-defined (with or without cystic changes) or diverse US pattern (hypo, criteria for benignity (simple cyst, solid nodule with central iso or hyperechoic, with cystic changes and/or macrocalcifica-

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Figure 9 TI-RADS 3: several nodules in the same gland with a Figure 10 Patient with nodular goiter. In a hyperechoic nodule similar ultrasound pattern: hyper or isoechoic nodules, with with small cysts, consistent with TI-RADS 3, a small papillary small cystic changes and small hypoechoic spots, as well as thyroid carcinoma (pT1b) was histologically detected after microcalcifications (arrow) and peripheral perfusion. In the surgery. thyroid scintigraphy (lower row on the right) TNs appear as toxic adenomas in a patient with hyperthyroidism.

Figure 11 TI-RADS4a: markedly hypoechoic nodule, of normal Figure 12 TI-RADS 4b: nodule with microcalcifications and shape and abnormal vascularity. Score of 1. poorly defined irregular margins. Score of 2.

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Figure 13 TI-RADS 4b: nodule with two sonographically suspi- Figure 14 TI-RADS 4c: nodule with microcalcifications, irregu- cious criteria for malignancy: hypoechogenicity and internal lar borders and taller than wide shape (greater in its antero- vascularity. posterior diameter than in its transverse diameter). Score of 3.

Figure 15 TI-RADS 4c: hypoechoic nodule of irregular margins Figure 16 TI-RADS 5: hypoechogenic nodule with microcal- with a taller than wide shape. Score of 3. cifications and poorly defined margins, with perinodular tis- sue invasion (arrow). Taller than wide shape. Presence of a cervical lymph node suspicious for malignancy (see: Fig. 17). Overall score of 6.

144 Rev. Argent. Radiol. 2014;78(3): 138-148 TI-RADS classification of thyroid nodules based on a score modified according to ultrasound criteria for malignancy J. Fernández Sánchez

detected, points must be added to the score as appropriate. Thus, if a TN has a score of 0, it is either definitely benign (TI- RADS 2) with the aforementioned US patterns (simple cyst, solid nodule with central cyst, nodule with homogeneous peripheral calcification and spongiform nodule) or prob- ably 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 pa- tient’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 radia- tion 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 Figure 17 TI-RADS 5: suspicious hypoechoic lymph node, with findings (further prospective studies would be required). On round shape and abnormal vascularity. Overall score of 6 for the nodule of fig. 16. the contrary, TNs classified as TI-RADS 4b and 4c should al- ways undergo FNA, except if contraindicated or in the event tions) proved to be malignant. These TNs with a score of 1 of high risk. Based on the results of this study, TI-RADS 5 nod- and probably benign US findings are classified as TI-RADS 3 ules invariably require histological examination after surgery. (fig. 6) (probability of malignancy < 5%) according to Hor- Limitations to this study include the lack of cytological or histologi- vath et al3 and Kwak et al6. In this respect, it should be noted cal confirmation for all cases. However, those performing ultra- that many of the TI-RAD 3 nodules are functioning or toxic sound diagnosis of TNs in daily practice are aware of the impos- thyroid adenomas (figs. 7-9) and that malignancy within this sibility of performing FNA or surgery in all nodules. This is also category is not only a rare occurrence, but also a generally impracticable in clinical trials for ethical reasons. In fact, owing to unexpected histological finding following nodular goiter sur- technological advances in ultrasound imaging and to the imple- gery (fig. 10). In our study, 9.5% of TNs meeting one criterion mentation of new techniques (such as color Doppler or elastogra- for malignancy were diagnosed as thyroid carcinoma. phy) and other diagnostic methods (e.g., scintigraphy or PET/CT), TNs with a score of 1 were assigned category 4a in TI-RADS it has been possible to reduce the number of these interventions. classification (fig. 11), while TNs with a score of 2 were clas- Even if some thyroid carcinomas have slow progression, when sified as TI-RADS 4b (figs. 12 and 13). In the latter case, the further diagnostic methods show signs of benignity in medi- incidence of malignancy increased up to 48%. In turn, TNs cal practice, this is considered to be enough, because the with a score of 3 or 4 showed an increased incidence of thy- likelihood that they may become malignant is low. For this roid carcinoma of up to 85%, and were therefore included reason, despite the unavailability of cytological or histological within TI-RADS 4c (figs. 14 and 15). In this category, Kwak et confirmation for all 3650 nodules, benignity as defined by al6 report a probability of malignancy of 50-95%. those methods was considered to be valid. Furthermore, in Finally, TNs with a score of 5 or higher were classified as TI- 966 TI-RADS 2 and 3 cases, FNA or surgery was effectively RADS 5 (figs. 16 and 17). In our study, all TNs with these performed, and in all cases of TI-RADS 3, 4a, 4b, 4c and 5 ultrasound features proved to be malignant, but Horvath et malignancy, histological confirmation was performed. al3 and Kwak et al6 report for this category a probability of TI-RADS is a merely sonographic classification. The final evalu- malignancy of 85-99%. ation and therapeutic decision-making in the presence of a The TI-RADS classification based on the scoring system is TN cannot be limited to the results of a thyroid ultrasound. shown in table 3. The advantage of this method is that it is In addition to the standard laboratory tests for the evaluation more practical and easy to apply. The first step in the US clas- of thyroid function, measurement of thyroglobulin, calcitonin sification of TNs consists in evaluating the potential presence and diverse anti-thyroid antibodies is also important, as well as of criteria for suspected malignancy. When their presence is the thyroid scintigraphy using 99mTC-sodium pertechnetate.

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