Ultrasonography Classification of the American Thyroid Association for Predicting Malignancy in Thyroid Nodules >1cm with Indeterminate Cytology: A Prospective Study

Abstract

The objective of this prospective study was to evaluate the ultrasonography classification of the American Thyroid Association (ATA) for predicting malignancy in thyroid nodules >1 cm with indication for fine-needle aspiration (FNA) whose cytology was indeterminate. Additionally, the combination of the ATA classification with Doppler analysis was evaluated. All patients with thyroid nodules >1 cm were eligible. Each nodule was assigned to one of the ATA categories. Exclusively or predominantly intranodular vascularity was considered suspicious. One hundred and thirty-seven patients with 143 nodules underwent FNA and those with indeterminate cytology (Bethesda category III or IV) were selected. All patients were referred for surgery. Among the 143 nodules evaluated, 92 were benign, 33 were malignant, 13 were noninvasive follicular thyroid neoplasms with papillary-like nuclear features (NIFTP), and 5 were tumors of uncertain malignant potential (TUMP). The rate of malignancy, including NIFTP and TUMP in this definition, was 80%, 42.8%, 13%, 10%, and 23% for nodules with a high suspicion, intermediate suspicion, low suspicion, very low suspicion, and undefined ultrasonographic pattern, respectively. Considering NIFPT and TUMP as benign, these rates were 72%, 22.4%, 4.3%, 0%, and 15.4%, respectively. The addition of Doppler analysis did not significantly improve the prediction of malignancy obtained with the ATA classification alone. The results of this prospective study show the usefulness of the ATA ultrasonographic classification for predicting malignancy specifically in thyroid nodules >1 cm with indeterminate cytology. The ATA category of the nodule should influence the decision for follow-up, molecular tests, or surgery.

Key words

thyroid nodule - indeterminate cytology - ultrasonography - American Thyroid Association - Doppler - malignancy

• References

• 1 Bongiovanni M, Spitale A, Faquin WC, Mazzucchelli L, Baloch ZW. The Bethesda System for Reporting Thyroid Cytopathology: A meta-analysis. Acta Cytol 2012; 56: 333-339
• 2 Cibas ES, Ali SZ. The 2017 Bethesda System for Reporting Thyroid Cytopathology. Thyroid 2017; 27: 1341-1346
• 3 Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid 2016; 26: 1-133
• 4 Nikiforov YE, Carty SE, Chiosea SI, Coyne C, Duvvuri U, Ferris RL, Gooding WE, LeBeau SO, Ohori NP, Seethala RR, Tublin ME, Yip L, Nikiforova MN. Impact of the Multi-Gene ThyroSeq Next-Generation Sequencing Assay on Cancer Diagnosis in Thyroid Nodules with Atypia of Undetermined Significance/Follicular Lesion of Undetermined Significance Cytology. Thyroid 2015; 25: 1217-1223
• 5 Russ G, Bonnema SJ, Erdogan MF, Durante C, Ngu R, Leenhardt L. European Thyroid Association Guidelines for Ultrasound Malignancy Risk Stratification of Thyroid Nodules in Adults: The EU-TIRADS. Eur Thyroid J 2017; 6: 225-237
• 6 Trimboli P, Fulciniti F, Zilioli V, Ceriani L, Giovanella L. Accuracy of international ultrasound risk stratification systems in thyroid lesions cytologically classified as indeterminate. Diagn Cytopathol 2017; 45: 113-117
• 7 Grani G, Lamartina L, Ascoli V, Bosco D, Nardi F, D'Ambrosio F, Rubini A, Giacomelli L, Biffoni M, Filetti S, Durante C, Cantisani V. Ultrasonography scoring systems can rule out malignancy in cytologically indeterminate thyroid nodules. Endocrine 2017; 57: 256-261
• 8 Lee JH, Han K, Kim EK, Moon HJ, Yoon JH, Park VY, Kwak JY. Risk Stratification of Thyroid Nodules With Atypia of Undetermined Significance/Follicular Lesion of Undetermined Significance (AUS/FLUS) Cytology Using Ultrasonography Patterns Defined by the 2015 ATA Guidelines. Ann Otol Rhinol Laryngol 2017; 126: 625-633
• 9 Tang AL, Falciglia M, Yang H, Mark JR, Steward DL. Validation of American Thyroid Association Ultrasound Risk Assessment of Thyroid Nodules Selected for Ultrasound Fine-Needle Aspiration. Thyroid 2017; 27: 1077-1082
• 10 Bardet S, Ciappuccini R, Pellot-Barakat C, Monpeyssen H, Michels JJ, Tissier F, Blanchard D, Menegaux F, de Raucourt D, Lefort M, Reznik Y, Rouxel A, Heutte N, Brenac F, Leconte A, Buffet C, Clarisse B, Leenhardt L. Shear Wave Elastography in Thyroid Nodules with Indeterminate Cytology: Results of a Prospective Bicentric Study. Thyroid 2017; 27: 1441-1449
• 11 Seethala RR, Baloch ZW, Barletta JA, Khanafshar E, Mete O, Sadow PM, LiVolsi VA, Nikiforov YE, Tallini G, Thompson LD. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a review for pathologists. Mod Pathol. 2018; 31: 39-55
• 12 Iared W, Shigueoka DC, Cristófoli JC, Andriolo R, Atallah AN, Ajzen SA, Valente O. Use of color Doppler ultrasonography for the prediction of malignancy in follicular thyroid neoplasms: systematic review and meta-analysis. J Ultrasound Med. 2010; 29: 419-425
• 13 Rosario PW, Ward LS, Carvalho GA, Graf H, Maciel RM, Maciel LM, Maia AL, Vaisman M. Sociedade Brasileira de Endocrinologia e Metabologia. Thyroid nodules and differentiated thyroid cancer: Update on the Brazilian consensus. Arq Bras Endocrinol Metabol 2013; 57: 240-264
• 14 Use of Neck Ultrasound to Guide Needle Aspiration Decision-Making. 2014 ATA Guidelines on Thyroid Nodules and Differentiated Thyroid Cancer - Highlights, Consensus, and Controversies. ICE/Endo 2014
• 15 Cibas ES, Ali SZ. The Bethesda System for Reporting Thyroid Cytopathology. Thyroid 2009; 19: 1159-1165
• 16 Rosario PW, da Silva AL, Nunes MS, Ribeiro Borges MA, Mourão GF, Calsolari MR. Risk of malignancy in 1502 solid thyroid nodules>1 cm using the new ultrasonographic classification of the American Thyroid Association. Endocrine 2016; 56: 442-445
• 17 Frates MC, Benson CB, Doubilet PM, Cibas ES, Marqusee E. Can color Doppler sonography aid in the prediction of malignancy of thyroid nodules?. J Ultrasound Med 2003; 22: 127-131
• 18 De Nicola H, Szejnfeld J, Logullo AF, Wolosker AM, Souza LR, Chiferi Jr V. Flow pattern and vascular resistive index as predictors of malignancy risk in thyroid follicular neoplasms. J Ultrasound Med 2005; 24: 897-904
• 19 Rosario PW, Silva AL, Borges MA, Calsolari MR. Is Doppler ultrasound of additional value to gray-scale ultrasound in differentiating malignant and benign thyroid nodules?. Arch Endocrinol Metab 2015; 59: 79-83
• 20 Williams ED. Guest Editorial: Two Proposals Regarding the Terminology of Thyroid Tumors. Int J Surg Pathol 2000; 8: 181-183
• 21 Rosario PW, Mourão GF, Nunes MB, Nunes MS, Calsolari MR. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Endocr Relat Cancer 2016; 23: 893-897
• 22 Yoon JH, Lee HS, Kim EK, Moon HJ, Kwak JY. Malignancy Risk Stratification of Thyroid Nodules: Comparison between the Thyroid Imaging Reporting and Data System and the 2014 American Thyroid Association Management Guidelines. Radiology 2016; 278: 917-924